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LATIN AMERICAN JOURNAL OF AQUATIC RESEARCH

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Escuela de Ciencias del Mar
Pontificia Universidad Catlica de Valparaso
Valparaso, Chile
lajar@ucv.cl

ASSOCIATE EDITORS

Patricio Arana Jos Angel Alvarez Perez


Escuela de Ciencias del Mar Centro de Cincias Tecnolgicas, da Terra e do Mar
Pontifcia Universidad Catlica de Valparaso, Universidade do Vale do Itajai
Valparaso, Chile Itajai, Santa Catarina, Brasil
Walter Helbling Nelson Silva
Estacin de Fotobiologa Playa Unin Escuela de Ciencias del Mar
Rawson, Chubut, Argentina Pontificia Universidad Catlica de Valparaso
Valparaso, Chile
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Departamento de Ciencias Bsicas Ingo Wehrtmann
Universidad de Los Lagos Escuela de Biologa
Osorno, Chile Universidad de Costa Rica
San Jos, Costa Rica
EDITORIAL COMMITTEE

Juan Carlos Castilla Fernando L. Diehl


Facultad de Ciencias Biolgicas Asociacin Brasilea de Oceanografa
Pontificia Universidad Catlica de Chile Centro Balneario Cambori, Brasil
Santiago, Chile
Rubn Escribano
Enrique Dupr Departamento de Oceanografa
Departamento de Biologa Marina Universidad de Concepcin
Universidad Catlica del Norte Concepcin, Chile
Coquimbo, Chile
Michel E. Hendrickx
Pierre Fren Unidad Acadmica de Mazatln
Institut de Recherche Halieutique Universidad Nacional Autnoma de Mxico
Mditerranenne et Tropicale Mazatln, Sinaloa, Mxico
Ste Cedex, Francia
Oscar Pizarro
Carlos Moreno Departamento de Geofsica
Instituto de Ecologa Universidad de Concepcin
Universidad Austral de Chile Concepcin, Chile
Campus Isla Teja, Valdivia, Chile
Ricardo Prego
Guido Plaza Departamento de Biogeoqumica Marina
Escuela de Ciencias del Mar Institutode Investigaciones Marinas
Pontificia Universidad Catlica de Valparaso Vigo, Espaa
Valparaso, Chile

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LATIN AMERICAN JOURNAL OF AQUATIC RESEARCH
Lat. Am. J. Aquat. Res., 39(2) 2011

CONTENTS

Research Articles

Joseph Selvin, Aseer Manilal, Suganthan Sujith, George Seghal Kiran & Aron Premnath Lipton
Efficacy of marine green alga Ulva fasciata extract on the management of shrimp bacterial diseases. Eficacia del extrac-
to del alga marina verde Ulva fasciata sobre el manejo de las enfermedades bacterianas en camarones197-204

Luciano N. Padovani, Mara D. Vias & Marcelo Pjaro


Importance of the Ro de la Plata estuarine front (southwestern Atlantic Ocean) in the feeding ecology of Argentine
anchovy, Engraulis anchoita (Clupeiformes, Clupeidae). Importancia del frente estuarial del Ro de la Plata (Ocano Atln-
tico sudoccidental) en la ecologa trfica de la anchota argentina, Engraulis anchoita (Clupeiformes, Clupei-
dae)......205-213

Susana Mara Velurtas, Ana Cristina Daz, Anala Vernica Fernndez-Gimenez & Jorge Lino Fenucci
Influence of dietary starch and cellulose levels on the metabolic profile and apparent digestibility in penaeoid shrimp.
Influencia del nivel de almidn y celulosa en la dieta sobre el perfil metablico y digestibilidad aparente en camarones penaeoi-
deos..214-224

Ral Prez-Gonzlez
Catch composition of the spiny lobster Panulirus gracilis (Decapoda: Palinuridae) off the western coast of Mexico.
Composicin de la captura de la langosta espinosa Panulirus gracilis (Decapoda: Palinuridae) en la costa oeste de Mxi-
co.........225-235

Mauricio F. Landaeta, Claudia A. Bustos, Pamela Palacios-Fuentes, Pablo Rojas & Fernando Balbontn
Distribucin del ictioplancton en la Patagonia austral de Chile: potenciales efectos del deshielo de Campos de Hielo
Sur. Ichthyoplankton distribution in South Patagonia, Chile: potential effects of ice melting from the Southern Ice Field...236-249

Jess Rodrguez-Romero, Laura del Carmen Lpez-Gonzlez, Felipe Galvn-Magaa, Francisco J. Snchez-Gutirrez, Roxana
B. Inohuye-Rivera & Juan C. Prez-Urbiola
Seasonal changes in a fish assemblage associated with mangroves in a coastal lagoon of Baja California Sur, Mexico.
Cambios estacionales de la comunidad de peces asociada a zonas de manglar en una laguna costera de Baja California Sur,
Mxico ....250-260

Douglas Fernando Peir, Paulo Ricardo Pezzuto & Fernando Luis Mantelatto
Relative growth and sexual dimorphism of Austinixa aidae (Brachyura: Pinnotheridae): a symbiont of the ghost shrimp
Callichirus major from the southwestern Atlantic. Crecimiento relativo y dimorfismo sexual en Austinixa aidae (Barchyura:
Pinnotheridae): un simbionte del camarn fantasma Callichirus major del Atlntico sudoccidental ...261-270

Joan Sebastin Salas-Leiva & Enrique Dupr


Cryopreservation of the microalgae Chaetoceros calcitrans (Paulsen): analysis of the effect of DMSO temperature and
light regime during different equilibrium periods. Criopreservacin de las microalgas Chaetoceros calcitrans (Paulsen):
anlisis del efecto de la temperatura de DMSO y rgimen de luz durante diferentes perodos de equil-
brio.......271-279

Paulina Soto, Hernn Gaete & Mara Eliana Hidalgo


Assessment of catalase activity, lipid peroxidation, chlorophyll-a, and growth rate in the freshwater green algae Pseu-
dokirchneriella subcapitata exposed to copper and zinc. Evaluacin de la actividad de la catalasa, peroxidacin lipdica,
clorofila-a y tasa de crecimiento en la alga verde de agua dulce Pseudokirchneriella subcapitata expuesta a cobre y
zinc. .....280-285

www.scielo.cl/imar.htm www.lajar.cl
Luis Fernando Payn, Andrs Felipe Navia, Efran A. Rubio & Paola Andrea Meja-Falla
Biologa de la raya guitarra Rhinobatos leucorhynchus (Gnther, 1867) (Rajiformes: Rhinobatidae) en el Pacfico co-
lombiano. Biology of the guitar ray Rhinobatos leucorhynchus (Gnther, 1867) (Rajiformes: Rhinobatidae) in the Colombian
Pacific...................................................................................................................................................................................286-296

Alfredo C. Barretto, Margarita B. Sez, Mara R. Rico & Andrs J. Jaureguizar


Age determination, validation, and growth of Brazilian flathead (Percophis brasiliensis) from the southwest Atlantic
coastal waters (34-41S). Determinacin de edad, validacin y crecimiento del pez palo (Percophis brasiliensis) de
aguas costeras del Atlntico sudoccidental (34-41S) ......297-305

Santiago Andrs Echaniz & Alicia Mara Vignatti


Seasonal variation and influence of turbidity and salinity on the zooplankton of a saline lake in central Argentina. Va-
riacin estacional e influencia de la turbidez y la salinidad sobre el zooplancton de un lago salino de la regin central de Argen-
tina........................................................................................................................................................................................306-315

Rodrigo Wiff, Juan Carlos Quiroz, Vilma Ojeda & Mauricio A. Barrientos
Estimacin de mortalidad natural e incertidumbre para congrio dorado (Genypterus blacodes Schneider, 1801) en la
zona sur-austral de Chile. Estimation of natural mortality and uncertainty in pink cusk-eel (Genypterus blacodes Schneider,
1801) in southern Chile.....316-326

Christopher Concha, Emilio Figueroa & Federico M. Winkler


Asociacin entre la tasa de autofecundacin y la frecuencia de larvas malformadas en poblaciones cultivadas del os-
tin del norte Argopecten purpuratus (Lamarck, 1819). Association between self-fertilization rates and the frequency of mal-
formed larvae in farmed populations of the northern scallop Argopecten purpuratus (Lamarck, 1819)..327-337

Andrea Ubilla & Ivn Valdebenito


Use of antioxidants on rainbow trout Oncorhynchus mykiss (Walbaum, 1792) sperm diluent: effects on motility and
fertilizing capability. Uso de antioxidantes en el diluyente espermtico para trucha arcoiris Oncorhynchus mykiss (Walbaum,
1792): efecto en la motilidad y capacidad fecundante.........................................................................338-343

Mara Alejandra Romero, Silvana Dans, Ral Gonzlez, Guillermo Svendsen, Nstor Garca & Enrique Crespo
Solapamiento trfico entre el lobo marino de un pelo Otaria flavescens y la pesquera de arrastre demersal del golfo
San Matas-Patagonia, Argentina. Trophic overlap between South American sea lion Otaria flavescens and trawl demersal
fishery in San Matas gulf-Patagonia, Argentina...344-358

Viviana Bravo, Sergio Palma & Nelson Silva


Seasonal and vertical distribution of medusae in Aysn region, southern Chile. Distribucin estacional y vertical de me-
dusas en la regin de Aysn, sur de Chile.359-377

Short Communications

Mauricio Ibarra & Patricio M. Arana


Crecimiento del camarn excavador Parastacus pugnax (Poeppig, 1835) determinado mediante tcnica de marcaje.
Growth of burrowing crayfish Parastacus pugnax (Poeppig, 1835) determined by marking technique......378-384

Subramanian Bragadeeswaran, Sangappellai Thangaraj, Kolandhasamy Prabhu & Solaman Raj Sophia Rani
Antifouling activity by sea anemone (Heteractis magnifica and H. aurora) extracts against marine biofilm bacteria. Ac-
tividades anti-incrustantes de las extractos de las anmonas marinas Heteractis magnifica y H. aurora frente a biofilm de
bacterias marinas........................385-389

Miguel Avendao & Marcela Cantillnez


Reestablecimiento de Choromytilus chorus (Molina, 1782) (Bivalvia: Mytilidae) en el norte de Chile. Reestablishment of
Choromytilus chorus (Molina, 1782) (Bivalvia: Mytilidae) in northern Chile.....390-396

www.scielo.cl/imar.htm www.lajar.cl
Lat. Am. J. Aquat. Res., 39(2): 197-204, 2011 Efficacy of marine green alga Ulva fasciata 197
DOI: 10.3856/vol39-issue2-fulltext-1

Research Article

Efficacy of marine green alga Ulva fasciata extract on the management of


shrimp bacterial diseases

Joseph Selvin1, Aseer Manilal2, Suganthan Sujith3, George Seghal Kiran4 & Aron Premnath Lipton5
1-4
Department of Microbiology, Bharathidasan University
Tiruchirappalli 620 024, India
5
Centre for Marine Science and Technology, M.S. University
Rajakkamankalam Kanyakumari District, India

ABSTRACT. Secondary metabolites of the green algae, Ulva fasciata, were tested to determine the efficacy
of controlling shrimp bacterial pathogens. Exploratory experiments indicated that an intermediate dose
(1 g kg-1 of shrimp) of Ulva in the diet was highly effective at controlling bacterial pathogens of shrimp, as
compared to lower (500 mg kg-1) and higher (1.5 g kg-1) doses. The pilot experiments evaluated the percent of
relative protection afforded shrimps treated with Ulva diet and faced with various concentrations of bacterial
pathogen. The survival of shrimps treated with Ulva diet was significant (P < 0.01). The present findings
indicate that the green U. fasciata may be an excellent source for developing a potent medicated feed for
shrimp disease management.
Keywords: Penaeus monodon, bacterial diseases, Vibrio, shell disease, proactive management, Ulva fasciata.

Eficacia del extracto del alga marina verde Ulva fasciata sobre el manejo de las
enfermedades bacterianas en camarones

RESUMEN. Metabolites secundario de algas verdes Ulva fasciata fue probado para determinar la eficacia de
controlar el camarn pathogens bacterial. Las conclusiones de experimentos exploratorios indicaron que la
dosis mediana (1 g kg-1 de camarn) de dieta Ulva era sumamente eficaz en el control de pathogens bacterial
de camarn cuando comparado al ms abajo (500 mg kg-1) y ms alto (1,5 g kg-1) dosis. En los experimentos
pilotos, la proteccin de pariente de por ciento de camarones trat con la dieta Ulva y desafi con varias
concentraciones de bacterial patgeno fueron evaluados. La supervivencia de camarones trat con la dieta
Ulva era significativo (P < 0,01). Basado en las conclusiones presentes, podra ser deducido que U. verde
fasciata puede ser una fuente excelente para desarrollar la comida potente medicinal para la direccin de
enfermedad de camarn.
Palabras clave: Penaeus monodon, enfermedades bacteriales, Vibrio, enfermedad de cscara, direccin
proactiva, Ulva fasciata.
___________________
Corresponding author: Aseer Manilal (aseermanilal@gmail.com)

INTRODUCTION (Karunasagar et al., 1997; Selvin & Lipton 2003a;


Manilal et al., 2010b). Vibrio species are considered to
Bacterial disease outbreaks particularly vibriosis and be members of the normal bacterial flora of shrimp
black shell disease impose a significant constraint on and the culture environment (Jiravanichpaisal et al.,
the sustainable production of shrimp (Bachere et al., 1994; Otta et al., 1999). Often acting as opportunistic
1995; Verschuere et al., 2000; Selvin et al., 2005; pathogens or secondary invaders, they may cause total
Manilal et al., 2010b). In Asia, among the pathogenic mortality of reared shrimps (Lightner, 1988; Nash et
Vibrio group, 11 species were reported from the al., 1992).
shrimp culture systems (Lavilla-Pitogo, 1995). V. Although few reports evidenced the efficacy of
alginolyticus and V. harveyi poses a serious disease algae-based products in shrimp health management
problem in cultured black tiger shrimp in India (Furusawa et al., 1991; Yamasaki et al., 1997), the
198 Lat. Am. J. Aquat. Res.

role of marine natural product in shrimp disease extracts were filtered and concentrated to recover the
management has been realized recently (Selvin & excess solvents in another distillation system. The
Lipton, 2003, 2004; Selvin et al. 2004b; Huang et al., concentrated extract (about 100 mL) was again filtered
2006; Manilal et al., 2009). It was found that marine through a Whatman N1 filter paper fitted with a
secondary metabolites are promising resources for the
development of eco-friendly management practices for Buchner funnel using suction pressure.
shrimp diseases (Selvin & Lipton, 2003; Selvin et al., Finally, it was reduced to thick oily natured crude
2004, 2004b; Manilal et al., 2009, 2009a). Moreover, extract in a rotary vacuum evaporator (Yamato) at
secondary metabolites of green algae Ulva fasciata 40C, collected in airtight plastic vials and stored in
elicited the non-specific defense factors of shrimp the refrigerator for further activity studies.
against pathogenic invaders (Selvin, 2002; Selvin et
al., 2004b). In addition, medicated feed formulated Determination of median lethal dose (MLD) of
with polysaccharides isolated from the Indian green algal extract
algae, Acrosiphonia orientalis were found to be
Primary exploratory (dose selecting) experiments were
effective in control of White Spot Syndrome Virus
(Manilal et al., 2009). Recently, Huang et al. (2006) conducted with broad range of the test compounds.
envisages the effect of Sargassum fusiforme Chosen concentrations such as: 100, 1000 and 2000
polysaccharide extracts on vibriosis resistance and mg kg-1 shrimp of U. fasciata extract were prepared in
immune activity of the shrimp, Fenneropenaeus 5% EtOH in normal saline to ensure complete
chinensis. solubility. Ten shrimps (abw = 8.5 g) per group
(triplicates) were injected intra-muscularly with 0.1
Southwest coast of India is a unique marine habitat
mL of appropriate dose or 5% EtOH in normal saline
infested with diverse variety of seaweeds. The
(control). The immediate reflexes and mortality were
biological activity of seaweeds from the southwest observed every hour for the first 6 h and every 24 h
coast of India (Kollam coast) is already reported for 7 days. Based on the exploratory experiments,
(Manilal et al., 2009, 2009a, 2009b, 2010, 2010a, narrow ranges were administered to the experimental
2011, 2011a). In this background, the present study shrimp to determine the median lethal dose (LD50).
aims to establish the effect of algal-based medicated
feed on the survival of experimentally infected Preparation of medicated diet
shrimps. Top-coated medicated feed was prepared with
appropriate quantity of Ulva extract on the surface of
the feed at a rate of 3.2% of the shrimp body weight
MATERIALS AND METHODS
daily. To prepare the medicated feed, 30, 60 and 80 g
of Ulva extract was incorporated in medicated diet.
Collection of marine algae The shrimp were fed with a commercially formulated
The mature plants of Ulva fasciata was handpicked shrimp feed with the following proximate
from the intertidal and subtidal habitat of the Kollam composition: 35.6% crude protein, 3.5% lipids, 5.9%
(0854'N, 7638'E) area located on the southwestern fibre, 45.7% nitrogen-free extract and 11.21% ash.
coast of India. The collection was performed during Commercial pellet shrimp grower feed No. 1 (C.P.
the period from June 2007 to August 2007 when algal feeds, Cochin) was used for preparing medicated feed
biomass remains dominant. Live and healthy plants for the experiments on leaching of Ulva extract in the
water. The extract was dissolved in 50 mL of 4%
were harvested manually and washed thoroughly in
gelatin water and sprayed on 1 kg of pellet feed using
running water. Cleaned plant materials were shade
a TLC sprayer. The sprayed medicated feed was dried
dried under an air jet to prevent photolysis and thermal in a hot air oven at 40C.
degradation. The completely dried material was
weighed and ground coarsely in a mechanical grinder Pathogenicity and LD50 value of shrimp pathogens
(Manilal et al., 2010).
Initially, the slant culture of shrimp pathogens (V.
fischeri, V. alginolyticus, V. harveyi and Aeromonas
Extraction of algae
sp.) was activated and 1 mL of 18 h culture was
For extraction, 500 g of finely powdered algal material inoculated in 25 mL nutrient broth. This was kept
was refluxed three times in a 5 L capacity round overnight at 30 2C in a shaker at 180 5 rpm. An
bottom flask in a water bath at 65C for about 6 h 18 h shake culture was centrifuged at 4800 x g for 15
using dichloromethane: methanol (1:1) as a binary min at 40C (Eppendorf). Cell pellets were washed
azeotropic solvent (Manilal et al., 2009b). The twice with normal saline (NS), re-suspended and
Efficacy of marine green alga Ulva fasciata 199

serially diluted in NS and enumerated using a Petroff- cfu/shrimp) challenge dose and higher challenge dose
Hausser counting chamber by plating on nutrient agar (107 to 108 cfu/shrimp) of single culture of bacterial
supplemented with 2% NaCl (Himedia). This was also pathogens such as V. fischeri, V. harveyi, V. algino-
plated on nutrient agar to get the colony forming units lyticus and Aeromonas sp., and combined culture of
(cfu) values. The black tiger shrimp Penaeus monodon pathogen (V. harveyi, 5 x 105 + V. alginolyticus, 5 x
post-larvae (PL-20) obtained from the Matsyafed 105 = 106 cfu/shrimp) and transferred to the 100 L
hatchery, Kollam and were reared in a 1000 L fiber glass aquaria. They were observed for a period of 15
reinforced plastic tanks provided with constant days for mortality and external clinical symptoms
aeration and 50% daily water exchange. They were (Austin & Austin, 1989). The Ulva diet was continued
reared at optimum hydrological conditions such as after challenge for 15 days. Parallel control shrimps
salinity (35 ppt), temperature (30 2C) and pH (7.8). (10 numbers) received 0.1 mL normal saline only. The
Healthy juveniles (average body weight = 5.4 2.2 g) mortality/infectivity percentages were estimated
were segregated and maintained at 20 shrimps/tank in according to Sung et al. (1994). The Percent Relative
200 L high-density plastic (HDP) tanks before starting Protection (PRP) was determined by the following
the experiment. The challenged shrimps were expression:
maintained at 10 shrimps/tanks in glass aquaria.
Shrimps were intramuscularly injected with 0.1 mL of % of mortality (treated)
PRP = 1- x 100
bacterial inoculums using a 1 mL tuberculin syringe at % of mortality (control)
ventral side between the second and third segment.
Preliminary examinations revealed that challenge dose To determine if significant differences existed
of 103 colony forming unit (cfu) per shrimp could not between the treated and control shrimps, all results
kill the injected shrimp (Manilal et al., 2010b). were analyzed using ANOVA. The significant
Therefore the concentrations of 105 to 108 cfu of the differences were indicated at P < 0.01.
appropriate single (V. fischeri, V. alginolyticus, V.
harveyi and Aeromonas sp.) and combined culture (V. RESULTS
alginolyticus + V. harveyi) of bacteria per shrimp were
used. Parallel control groups received 0.1 mL of The Median Lethal Dose (MLD) of Ulva extract in P.
normal saline (NS) only. Ten shrimps were used for monodon was determined to be 1120 mg kg-1 shrimp.
each inoculation level. The mortality and reflexes of During the preliminary experiment, the infection
the shrimps were observed for every 15 min in the (pathogenicity range) was obtained at a higher dose of
first hour of post-inoculation and every 1 h until the 108 cfu/shrimp after 5 days of inoculation with
6th h (Manilal et al., 2010b). Subsequent monitoring luminescent V. fischeri type culture. The LD50 values
was done every 12 h for a period of seven days of bacterial pathogens were ranged as 2.8 x 107
(Tendencia & Dureza, 1997). The appropriate cfu/shrimp for V. fischeri and 106 cfu/shrimp for V.
harveyi, V. alginolyticus and Aeromonas sp. The
concentration of pathogens (105 to 108 cfu), which
external clinical symptoms were characterized as
causes mortality within 24 h or within 7 days, was
shell necrosis and black spots on the shell,
considered as LD50 whereas which causes infection or
necrotised chelate legs, anorexia, feeble movement
abnormalities was considered as ID50 (Infectivity and mortality.
Dose) (Manilal et al., 2010b). The LD50 dose was
calculated by the probit method, after Wardlaw The effect of different algal extracts in the survival
of experimentally infected shrimp is presented in
(1985).
Table 1. The shrimp fed with the dose rate of 500-mg
kg-1 shrimp had the lowest protection against bacterial
Effect of different dose of algal extracts in the
infection. At this dose, the shrimp challenged with V.
survival of experimentally infected shrimps
fischeri produced infection in 60% of challenged
The shrimps with an average body weight of 5.6 1.8 shrimp, whereas the shrimp challenged with V.
g range were reared in the circular high density plastic harveyi and V. alginolyticus caused infection to the
(HDP) tanks at a stocking density of 60 individuals extent of 80%. The experimental group, fed with
per 600 L of seawater. They were fed with Ulva diet median (1 g kg-1 shrimp) and higher (1.5 g kg-1
(1 g kg-1 shrimp) in three equal installments at a rate shrimp) doses of medicated feed exhibited more or
of 3.2% of their body weight for a period of 15 days. less similar level of protection. At these treatment
On the 16th day, three duplicate groups each of treated levels, no mortality was noticed in the shrimps
shrimps (10 numbers/group) were grouped in to three challenged with V. harveyi and Aeromonas sp.
and intramuscularly injected with LD50 (106 whereas V. fischeri and V. alginolyticus caused 20%
200 Lat. Am. J. Aquat. Res.

Table 1. Efficacy of Ulva diet on protection and survival of experimentally infected Penaeus monodon.
Tabla 1. Eficacia de Ulva dieta sobre la proteccin y la supervivencia experimentalmente se infectan Penaeus monodon.

Percentage of infection within 15 days*


Medicated feed dose rate (g kg-1)
V. fischeri V. alginolyticus V. harveyi Aeromonas sp.

0.5 60 80 80 40
1.0 20 20 0 0
1.5 10 20 10 0

*100% mortality was observed in the control treatments

infection. The infected shrimps showed external enhanced virulence obtained by the pathogenic
clinical symptoms such as shell necrosis and black isolates passed through the host, prior to the in
spots on the shell. Subsequent symptoms such as captivity control experiments. The treated group
necrotised chelate legs, anorexia, feeble movement challenged with higher dose (107 to 108 cfu/shrimp) of
were culminated in mortality, particularly in control bacterial inoculum had low survival. The survival rate
and lower treatments. Based on these findings, it could of Ulva treated shrimp was 100% against the infection
be envisaged that shrimp fed with 1 g kg-1 will provide caused by the shrimp bacterial pathogens. Selvin et al.
high protection compared to other doses. (2004b) reported that inhibition of bacterial
The survival rate of treated and control shrimp propagation was a possible mechanism by which Ulva
against various bacterial pathogens is depicted in medication provided protection from infection.
Figures 1 to 4. The shrimps challenged with Shrimp disease management using Ulva diet was
potentiated pathogen produced more infection or proven to be an effective eco-friendly management
mortality in the treated group than those caused by the strategy for sustainable shrimp farming (Selvin, 2002;
LD50 value of individual pathogen. In the case of V. Selvin & Lipton, 2003). Ulva diet was found to be a
fischeri, the LD50 did not cause mortality in the treated potent immunomodulator and therefore it was
group while all the control shrimp died (Fig. 1). Ulva considered as a proactive drug (Selvin et al., 2004b).
diet elicited significant survival (60 in terms of PRP) As per our earlier finding, 88% of viable V. fischeri
against the lethal dose (108 cfu/shrimp) of V. fischeri. cells were cleared-off from the haemolymph within 1
However 20% infection was observed among the h in the Ulva treated group. These findings suggest the
surviving shrimp of Ulva fed group (Table 2). The quick production of bactericidins in the haemolymph
Ulva diet elicited complete protection (100% survival) of Ulva treated group. The rapid bacterial clearance
against the infection of V. harveyi and V. rate of shrimp haemocytes was stimulated by Ulva
alginolyticus. The inoculation of a higher dose (107 treatment. Therefore it was conjectured that
cfu/shrimp) of Aeromonas sp. caused 40% infection in bacteridins found in shrimp plasma might be inducibly
the Ulva treated group (Table 2). It was found that the released from haemocytes by Ulva medication.
Ulva diet produced a higher level of protection (80% Recently Huang et al. (2006) reported the effect of
survival) against the infection caused by the combined seaweed Sargassum fusiforme polysaccharide extracts
pathogens. Invariably, the survival of treated shrimp on vibriosis resistance and immune activity of the
against the bacterial infection was significant at P < treated shrimp. Literature also evidenced the in vivo
0.01 level (Table 2). antiviral (WSSV) potency of seaweed-based
medicated feed in Penaeus monodon (Manilal et al.,
DISCUSSION 2009). Satoh et al. (1987) investigated the effect of
Ulva on susceptibility of infectious disease in red sea
Based on the findings, shrimp fed with Ulva-based bream Pagrus major fed with 5% Ulva pertusa meal
medicated feed at a dose rate of 1 g kg-1 could supplementation diet. The Ulva meal increased the
effectively control the bacterial pathogens challenged resistance against infection caused by Pasteurella
in this study. Invariably the shrimp treated and piscicida. A spray-dried preparation of micro-algae
challenged subsequently with the LD50 of appropriate Tetraselmis suecica was reported to control a variety
bacteria gave higher survival than the control group. of fish pathogens such as A. salmonicida,
In the control group, early high mortality was Staphylococcus liquifaciens, V. anguillarum, V.
observed than the actual LD50. It may be due to the salmonicida and V. ruckeri (Austin & Day, 1990).
Efficacy of marine green alga Ulva fasciata 201

Control inoculated with 10E+8 cfu/shrimp

Control inoculated with 10E+7 cfu/shrimp

Treated inoculated with 10E+7 cfu/shrimp

Treated inoculated with 10E+8 cfu/shrimp

Figure 1. Survival of shrimp fed with and without Ulva incorporated medicated diet following challenge with V. fischeri.
Figura 1. Supervivencia de camarones alimentados con y sin Ulva incorporada como dieta medicinal para combatir el
Vibrio fischeri.

Control inoculated with 10E+6 cfu/shrimp of


V. harveyi

Ulva inoculated with 10E+6 cfu/shrimp of


V. harveyi

Ulva inoculated with 10E+6 cfu/shrimp of


V. alginolyticus

Control inoculated with 10E+6 cfu/shrimp of


V. alginolyticus

Figure 2. Survival of shrimp fed with and without Ulva incorporated diet following challenge with Vibrio sp.
Figura 2. Supervivencia de camarones alimentados con y sin Ulva incorporada a dietas para combatir el Vibrio sp.

Control inoculated with 10E+7 cfu/shrimp

Control inoculated with 10E+6 cfu/shrimp

Treated inoculated with 10E+7 cfu/shrimp

Treated inoculated with 10E+6 cfu/shrimp

Figure 3. Survival of shrimp fed with and without Ulva incorporated medicated diet following challenge with Aeromonas
sp.
Figura 3. Supervivencia de camarones alimentados con y sin Ulva incorporada a dietas medicinales para combatir
Aeromonas sp.
202 Lat. Am. J. Aquat. Res.

Control inoculated with 10E+7 cfu/shrimp

Ulva inoculated with 10E+7 cfu/shrimp

Figure 4. Survival of shrimp fed with and without Ulva diet following combined pathogenic challenge (V. harveyi and V.
alginolyticus).
Figura 4. Supervivencia de camarones alimentados con y sin Ulva en dietas para combatir en forma combinada (V.
harveyi y V. alginolyticus).

Table 2. Efficacy of Ulva diet (1000 mg kg-1) on the percent relative protection (PRP) of Penaeus monodon against
bacterial infections.
Tabla 2. Eficacia de la dieta de Ulva (1000 mg kg-1) sobre el porcentaje de proteccin relativa de Penaeus monodon
contra las infecciones bacterianas.

Dose Cumulative Mortality within % shell necrosis in the


Bacterial pathogens PRP
(cfu/shrimp) 15 days (%)*(Treated n = 20) treated shrimp (n = 20)
V. fischeri 108 40 60 20
107 0 100 0
V. harveyi 106 0 100 0
V. alginolyticus 106 0 100 0
Aeromonas sp. 107 0 100 40
106 0 100 0
Combined pathogen 106 20 80 0
i. V. harveyi, 5 x 105
ii. V. alginolyticus 5 x 105
*Based on the cumulative mortality the calculated survival rate was significant at P < 0.01.
100% mortality was observed in the control treatments, except Aeromonas sp. which was 80%

Based on the present study, therapeutic formulation form an excellent source for developing potent
(Ulva diet) can be easily prepared with crude extract. formulations as a package of proactive management
Therefore purification strategies and consequent practice for sustainable shrimp farming.
synthetic analogue development process need not be
undertaken. As the extract was prepared from the
dried material, such source material can easily be ACKNOWLEDGEMENTS
stored for 12 months. To sustain the host-defense
system and relative protection against pathogenic The author Aseer Manilal is gratefully acknowledged
invaders, the Ulva medication can be used as a Council of Scientific and Industrial Research (CSIR),
prophylactic agent for the entire culture period at low New Delhi for providing Senior Research Fellowship.
cost. Based on the present findings, it could be This work is funded by Department of Biotechnology,
inferred that the secondary metabolites of U. fasciata New Delhi (BT/PR8064/AAQ/03/290/2006).
Efficacy of marine green alga Ulva fasciata 203

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Lat. Am. J. Aquat. Res., 39(2): 205-213, 2011 Anchovy feeding in an estuarine front, Argentine 205
DOI: 10.3856/vol39-issue2-fulltext-2

Research Article

Importance of the Ro de la Plata estuarine front (southwestern Atlantic Ocean)


in the feeding ecology of Argentine anchovy, Engraulis anchoita
(Clupeiformes, Clupeidae)

Luciano N. Padovani1,2,3, Mara D. Vias1,2,3 & Marcelo Pjaro1


1
Instituto Nacional de Investigacin y Desarrollo Pesquero, P.O. Box 175, B7602HSA
Mar del Plata, Argentina
2
Consejo Nacional de Investigaciones Cientficas y Tcnicas, P.O. Box 175, B7602HSA, Argentina
3
Universidad Nacional de Mar del Plata, P.O. Box 175, B7602HSA, Argentina

ABSTRACT. The feeding of Engraulis anchoita was studied in the coastal reproductive habitat of the
northern population during the spawning period. Stomach contents of anchovy adults and plankton samples
taken during a research cruise were examined. The highest stomach fullness values were found in the Rio de la
Plata estuary, particularly at stations close to the surface salinity front. Copepods, particularly those < 1 mm
total length, represented by Paracalanus spp. and Oithona spp., were the most abundant prey. The dominance
of small copepods in the Argentine anchovy diet is noted for the first time. Ecological implications of this fact
are discussed. Other abundant preys were appendicularians, cladocerans, and fish eggs. The species
composition of the zooplankton samples coincided roughly with that found in the stomach contents. However,
selective feeding was observed on preys > 1 mm total length. This might be explained by a low gill rakers
efficiency of adult anchovies to retain small prey. In the Rio de la Plata front, both the reported large
biomasses of zooplankton and the observed intense anchovy feeding revealed the ecological significance of
this front, especially when compared with the contiguous poor in food coastal areas.
Keywords: Engraulis anchoita, feeding, stomach content, estuarine front, copepods, southwestern Atlantic,
Argentina.

Importancia del frente estuarial del Ro de la Plata (Ocano Atlntico sudoccidental)


en la ecologa trfica de la anchota argentina, Engraulis anchoita
(Clupeiformes, Clupeidae)

RESUMEN. Se estudi la alimentacin de la poblacin nortea de Engraulis anchoita en el hbitat


reproductivo costero durante su periodo de desove. Se analizaron los contenidos estomacales de adultos de
anchota y muestras de zooplancton tomados durante un crucero de investigacin. Los mayores valores de
replecin estomacal se encontraron en el estuario del Ro de la Plata, particularmente en estaciones cercanas al
frente salino de superficie. Los coppodos fueron las presas ms abundantes, particularmente especmenes < 1
mm de longitud total, representados por Paracalanus spp. y Oithona spp. Este dominio de pequeos
coppodos en la dieta de la anchota argentina se destaca por primera vez. Se discutieron las implicancias
ecolgicas de este hecho. Otras presas abundantes fueron: apendicularias, cladceros y huevos de peces. La
composicin de especies en las muestras de zooplancton coincidi a grandes rasgos con las encontradas en los
contenidos estomacales. Sin embargo, se observ seleccin sobre presas > 1 mm de longitud total. Esto se
puede explicar por la baja eficiencia del aparato branquial de anchotas adultas para retener pequeas presas.
En el frente del Ro de la Plata, las altas biomasas de zooplancton reportadas y la intensa alimentacin
observada, evidencian su significancia ecolgica, especialmente cuando se compara con aguas costeras
adyacentes pobres en alimento.
Palabras clave: Engraulis anchoita, alimentacin, contenido estomacal, frente estuarial, coppodos, Atlntico
sudoccidental, Argentina.
___________________
Corresponding author: Luciano Padovani (lucianopadovani@inidep.edu.ar)
206 Lat. Am. J. Aquat. Res.

INTRODUCTION potential anchovy feeding area into the CRH. This is


not surprising since other estuarine fronts in the world
Engraulis anchoita is the most abundant and wide- have been related to important anchovy spawning and
spread pelagic fish in the southwest Atlantic. It plays a feeding grounds (Palomera, 1992; Motos et al., 1996;
key role in the pelagic ecosystem of the Argentine Peebles, 2002). However, previous studies in the CRH
Sea, being an important component in the diet of have not been addressed to this question. Moreover,
commercial species such as hake, squid and mackerel the characterization of anchovy diet (e.g. taxonomic
(Angelescu, 1982). Two distinct populations are rec- identification and quantification of ingested prey
ognized south of 34S: the northern stock, between 34 items) was inaccurate in these studies, especially re-
and 41S; and the Patagonian stock between 41 and garding small prey.
48S (Hansen et al., 1984). The northern stock, object
In this work, anchovy stomach contents were
of this study, performs seasonal migrations between
analysed in order to assess differences in the feeding
coastal and shelf waters. In spring and early summer
activity between RdP front and the rest of the CRH.
the schools migrate into the coastal reproductive habi-
Characterization of anchovy diet in the CRH was
tat (hereafter CRH) off the Buenos Aires Province (<
carried out and prey composition in stomach contents
50 m depth), where massive spawning takes place
was compared with the prey availability in the field.
(Snchez & Ciechomski, 1995). Larvae and juveniles
remain in coastal waters during their growing period.
After spawning, in summer and early autumn, schools MATERIALS AND METHODS
disperse into outer shelf waters to feed, accumulating
Study site
a large amount of energy for the next reproductive
cycle (Angelescu, 1982; Hansen & Madirolas, 1996). Subantarctic coastal waters of the Buenos Aires
Province (< 50 m depth) are vertically homogeneous
E. anchoita adults are opportunistic predators on
all over the year because they are mixed by winds and
meso and macrozooplankton. They exhibit, like other
tides. They are poorer in nitrate and less productive
engraulids, two different feeding mechanisms: filtra-
than subantarctic shelf waters (> 50 m depth) which
tion for smaller prey, and capture or biting for larger
are stratified during the warmer season. Both are
ones (Leong & OConnell, 1969; Angelescu, 1982).
separated by a semi-permanent temperature front
Previous studies indicate that anchovy feeding in (Carreto et al., 1995). North of 38S the coastal waters
the CRH was negligible when compared with the in- are modified by the RdP estuary (Fig. 1). This
tense feeding occurring in shelf waters (Angelescu & estuarine front shows a high primary productivity,
Anganuzzi, 1981; Angelescu, 1982; Schwingel & driven by the nutrient input from the river and by the
Castello, 1994; Capitanio et al., 1997; Pjaro, 2002). vertical stability of the water column (Carreto et al.,
In the former, individuals feed almost exclusively on 1986). It is characterized by a salt wedge structure and
small zooplankters (e.g. small copepods species, ap- strong horizontal salinity gradients. More saline and
pendicularians and cladocerans) while in shelf waters dense marine waters penetrate into the estuary on the
large zooplankters constitute their food (e.g. Calanidae bottom, whereas more dilute and less dense river
copepods, euphausiids and hyperiid amphipods). This waters flows toward the sea at the surface (Guerrero et
feeding pattern seems to reflect the food availability al., 1997). The estuarine dynamics and the strong
found in zooplankton studies with lower biomass in pycnoclines of the salt wedge would favor the
the CRH than in shelf waters (Pjaro, 2002; Vias et accumulation and retention of plankton (Acha et al.,
al., 2002; Marrari et al., 2004). However, in northern 2008).
sector of the CRH high zooplankton biomasses have
been reported (Vias et al., 2002; Marrari et al., Sample collection, treatment and data analysis
2004). This sector is strongly influenced by the Rio de The material used in this study was obtained on board
la Plata (RdP), the second most important river of the R/V Oca Balda on a cruise performed in coastal
South America. Its estuarine front plays a central role areas of the Buenos Aires Province between 34 and
in the biological production, and zooplankton aggrega- 41S (Fig. 1). The sampling period (16 October-2
tions are a recurrent feature in this area probably be- November 2004) was coincident with the peak of
cause of retention and accumulation process (Madi- anchovy spawning in the study area (Snchez &
rolas et al., 1997; Acha et al., 2008). Ciechomski, 1995).
The presence of zooplankton aggregations together Oceanographic data were obtained in 70 stations
with the fact that high densities of anchovy schools with a CTD system (Kiel Multisonde Compact Sys-
occur frequently in RdP front (Hansen & Madirolas, tem, ME Meerestechnik Elektronic, Kiel, Germany).
1996; Martos et al., 2005) suggest that this may be a The salinity CTD data were calibrated by salinometer
Anchovy feeding in an estuarine front, Argentine 207

Zooplankton samples (n = 13) were collected with


a 200 m meshed 61 cm diameter Bongo net, using
oblique tows in the whole water column (Fig. 1). The
samples were fixed in 4% formaldehyde.
In the laboratory, both zooplankton and stomach
content samples were sub-sampled into aliquots in
order to quantify the zooplankters. The individuals
were identified to the lowest possible taxonomic level
and their total length (TL) was measured. They were
placed in three size classes, < 1 and 1-2 mm TL for the
mesozooplankton and > 2 mm TL for the macrozoo-
plankton.
Anchovy feeding selectivity in relation to food
availability was calculated as the alpha selectivity
index (i) of Chesson (1978), using the formula:

Figure 1. Study area and location of the sampling where; ri = the percentage of food item i in the stom-
stations. (X) trawls, (O) zooplankton. Dashed line ach content; pi = the percentage of the same item in
divides northern and southern sectors of study area zooplankton; n = the total number of food items as-
(38S). sessed.
Figura 1. rea de estudio y ubicacin de las estaciones
de muestreo. (X) lances de pesca, (O) zooplancton. La RESULTS
lnea de guiones divide los sectores norte y sur del rea
de estudio (38S). Hydrography
Surface salinity values in the study area were ranged
measurements of discrete water samples. Surface sa- between 19.5 and 33.9 (Fig. 2). The lowest values
linity distribution was drawn to locate the RdP estua- corresponded to the RdP estuary. The isohaline of 30,
rine front. considered the boundary of estuarine waters (Guer-
rero, 1998), showed a south-eastward extension indi-
Anchovies were collected using a Nichimo midwa-
cating a river discharge in this direction whose influ-
ter trawl net with a 10 mm mesh size and immediately
ence reaches 3750S. A well-defined frontal zone was
fixed in 10% formaldehyde. Stomach contents of 240
observed with highest salinity gradients south of Sam-
adult fishes of both sexes (110 to 194 mm total length)
borombn Bay. In the rest of the study area, out of the
randomly selected from sixteen trawl stations (n = 15
river influence, the salinity values were above 33.
per trawl) were examined (Fig. 1). Tows were per-
formed both during the day and night (Table 1). Each Feeding index
stomach was weighed with and without food content Mean Stomach Fullness Index (mSFI) of anchovy in
in order to determine the weight of the ingested prey, the CRH showed a well-defined pattern with the four
expressed as the difference between both weights. To highest values located in RdP frontal area (Fig. 2).
assess the feeding activity, mean Stomach Fullness
Index (mSFI) was calculated for each trawl as the This highest values were observed in specimens
ratio between ingested prey and whole animal collected from trawl stations close to the surface salin-
weights. According to Angelescu (1982), this index ity front, (away from the 30 isohaline): station N4
indicates the stage of satiety and ranges from empty (mSFI: 2.49), N5 (mSFI: 2.01), N7 (mSFI: 1.34) and
stomach (< 0.5% of anchovy total weight) to full N8 (mSFI: 1.33). Some individuals reached SFI val-
ues about 6, which mean a full stomach. In the re-
stomach (> 6% of anchovy total weight).
maining stations, the mSFI were smaller than 1.00
Anchovies and stomachs were weighed using a indicating empty or partially empty stomachs.
digital balance to nearest 0.01 g. No correction was
applied to the weight values for fixation effect on the Prey composition
individuals. The dilated stomachs found empty for The total bulk of anchovy diet was made up of zoo-
regurgitation during trawling, were discarded. plankton (Table 1). Mesozooplankton < 1 mm TL fol
208 Lat. Am. J. Aquat. Res.

Calanoida copepodites) and to a lesser extent by


appendicularians. Anchovy eggs and unidentified fish
eggs were less numerous. The least abundant
macrozooplankton > 2 mm was dominated by decapod
larvae and the Calanoides carinatus copepod.
From the application of the feeding selectivity
index to different prey size classes, high selectivity
was observed for mesozooplankton 1-2 mm TL and
macrozooplankton > 2 mm TL at the expense of
mesozooplankton < 1 mm (Fig. 3a). Furthermore,
unidentified fish eggs showed high index in the
northern sector of the study area (north of 38S) while
the appendicularians were in the southern part (south
of 38S) (Fig. 3b); what happened due to the high
number of specimens found in stomach from stations
4 and 12 for unidentified fish eggs and appendicu-
larians respectively (Table 1).
Figure 2. Mean Stomach Fullness Index (mSFI) of
Engraulis anchoita adults at each trawling position in DISCUSSION
relationship with surface salinity distribution. Isohaline
30 is shown thicker. High feeding activity was detected in anchovies
Figura 2. ndice de Replecin Estomacal promedio from the proximity of RdP surface salinity front, in
(IREp) de adultos de Engraulis anchoita para cada lance contrast with a lower activity recorded in the rest of
de pesca en relacin con la distribucin de salinidad the CRH. Moreover, it is worth mentioning that during
superficial. La isohalina de 30 se muestra engrosada. the cruise high anchovy biomasses were recorded in

lowed by the 1-2 mm TL fraction were dominant.


Copepods were the most important group reaching
almost 50% of prey items (PI). Other important groups
were appendicularians (22.1% PI), cladocerans
(14.7% PI), represented by Evadne nordmanni and
Podon spp., and fish eggs (12.6% PI), including
unidentified fish eggs and anchovy eggs. To a lesser
extent veliger stages of lamellibranchs, unidentified
nauplii, decapod larvae and amphipods were found.
The more abundant copepods in stomachs
belonged to the < 1 mm TL fraction (Paracalanus spp.
+ Calanoida copepodites and Oithona spp.). Copepods
size class 1-2 mm TL (Ctenocalanus vanus,
Clausocalanus brevipes, Centropages brachiatus +
Calanoida copepodites) was less abundant and
individuals > 2 mm TL (Calanoides carinatus) were
fairly rare.

Zooplankton composition and food selectivity


Mesozooplankton < 1 mm TL fraction was the most
abundant in study area (Table 2). Copepods
(Paracalanus spp. + Calanoida copepodites and Figure 3. Feeding selectivity index values according to
Oithona spp.) constituted the bulk of this fraction Chesson (1978). a) prey size classes; b) main anchovy
followed by cladocerans (Evadne nordmanni and prey items (north and south of 38S).
Podon spp). The 1-2 mm TL size class was Figura 3. Valores del ndice de selectividad de Chesson
represented by copepods (Ctenocalanus vanus, (1978). a) por clases de tamao de presa; b) por
Clausocalanus brevipes, Centropages brachiatus + principales tems presa (al norte y sur de 38S).
Table 1. Stomach contents of Engraulis anchoita adults in its coastal reproductive habitat (CRH). Average number of specimens of each prey item from each trawl is
indicated. (n: number of anchovies examined). * Ctenocalanus vanus, Clausocalanus brevipes, Centropages brachiatus and Calanoida copepodites.
Tabla 1. Contenido estomacal de adultos de Engraulis anchoita en su hbitat reproductivo costero (HRC). Se indica el nmero promedio de especimenes de cada tem presa
para cada lance. (n: nmero de anchotas analizadas) * Ctenocalanus vanus, Clausocalanus brevipes, Centropages brachiatus y copepoditos de Calanoida.

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16
Trawl Total
(n=15) (n=15) (n=15) (n=15) (n=15) (n=15) (n=15) (n=15) (n=15) (n=15) (n=15) (n=15) (n=15) (n=15) (n=15) (n=15)
Time 10:57 10:35 20:14 23:55 8:34 20:51 22:53 20:44 0:27 16:35 16:16 18:47 10:19 20:57 10:40 18:08
Mesozooplankton (< 1 mm) 49.50 242.71 108.75 199.24 1259.24 112.03 179.29 87.65 143.16 55.22 136.33 1020.11 61.50 1813.81 87.89 606.67 6163.08
Copepods 44.05 206.43 99.75 159.41 1083.24 29.92 149.18 53.62 80.77 45.11 81.66 805.91 38.83 775.16 86.82 536.33 4276.20
Euterpina acutifrons 13.85 0.89 2.01 1.06 14.26 0 5.92 0 0.83 0.91 3.19 0.07 0.67 0 0 1.12 44.80
Oithona spp. 8.50 92.38 19.71 117.03 733.14 12.91 48.70 29.68 38.78 9.94 29.23 155.20 6.17 422.77 68.67 71.86 1864.66
Paracalanus spp. +
Calanoida copepodites 21.70 113.15 78.03 41.31 335.84 17.02 94.56 23.94 41.16 34.26 49.24 650.63 32.00 352.40 18.15 463.35 2366.73
Unidentified nauplii 0 1.89 0.33 10.17 0 0.22 1.33 0.33 1.33 0.56 0.50 0 0.50 0 0 0 17.16
Cladocerans 0.95 28.20 1.67 27.33 120.33 78.67 14.78 30.72 50.33 7.17 52.83 214.20 21.50 1038.64 1.07 70.33 1758.72
Evadne nordmanni 0 17.00 0.56 16.17 65.89 55.83 4.83 11.79 37.51 2.33 13.54 180.93 0.35 531.89 0 9.07 947.69
Podon spp. 0.95 11.20 1.11 11.16 54.44 22.84 9.95 18.93 12.82 4.84 39.29 33.27 21.15 506.75 1.07 61.26 811.03
Veliger stages of
Lamellibranchs 4.50 6.20 7.00 2.33 55.67 3.22 14.00 2.97 10.72 2.39 1.33 0 0.67 0 0 0 111.00
Mesozooplankton (1-2 mm) 3.50 133.74 24.85 1202.98 253.76 31.30 141.41 93.40 51.34 35.53 36.29 3114.25 19.00 280.82 26.64 46.98 5495.77
Copepods* 2.05 7.99 20.51 9.65 77.76 1.41 35.07 27.96 11.90 3.80 16.12 980.58 3.00 131.33 0.71 33.31 1363.16
Fish eggs 0.50 2.73 2.33 1192.17 24.67 10.11 7.11 43.05 5.94 0.33 19.17 0 15.67 142.82 24.60 7.33 1498.54
Anchovy eggs 0 1.93 0.67 132.33 24.67 10.11 7.11 41.76 5.94 0.33 19.17 0 15.33 142.82 17.46 7.33 426.97
Unidentified fish eggs 0.50 0.8 1.66 1059.84 0 0 0 1.29 0 0 0 0 0.34 0 7.14 0 1071.57
Appendicularians 0.95 123.01 2.00 1.17 151.33 19.78 99.22 22.39 33.50 31.39 1.00 2133.67 0.33 6.67 1.33 6.33 2634.07
Anchovy feeding in an estuarine front, Argentine

Macrozooplankton (> 2 mm) 0 0 1 1.55 0 0 3 235 0 0 1 20 0 9 0 1 272.42


Copepods 0 0 0.40 0.21 0 0 2.96 234.00 0 0 0.93 20.37 0 2.59 0 0.22 261.69
Calanoides carinatus 0 0 0.40 0.21 0 0 2.96 234.00 0 0 0.93 20.37 0 2.59 0 0.22 261.69
Decapod larvae 0 0.47 0.33 1.33 0 0.33 0.22 0.44 0 0 0 0 0 6.67 0 0.80 10.60
Amphipods 0 0 0 0 0 0 0 0.07 0.07 0 0 0 0 0 0 0 0.13

Total 53.00 376.92 134.33 1403.77 1513.00 143.66 323.88 415.56 194.56 90.74 173.54 4154.73 80.50 2103.88 114.53 654.67 11931.28

Copepods (%) 86.98 56.89 89.83 12.06 76.73 21.81 57.80 75.94 47.63 53.90 56.88 43.49 51.97 43.21 76.43 87.05 49.46
Appendicularians (%) 1.79 32.64 1.49 0.08 10.00 13.77 30.63 5.39 17.22 34.59 0.58 51.36 0.41 0.32 1.16 0.97 22.08
Cladocerans (%) 1.79 7.48 1.24 1.95 7.95 54.76 4.56 7.39 25.87 7.90 30.44 5.16 26.71 49.37 0.93 10.74 14.74
Fish eggs (%) 0.94 0.73 1.74 84.93 1.63 7.04 2.20 10.36 3.06 0.37 11.04 0 19.46 6.79 21.48 1.12 12.56
209
210 Lat. Am. J. Aquat. Res.

Table 2. Taxonomic composition and abundance (ind m-3) of zooplankton in coastal reproductive habitat (CRH) of
anchovy. (SD: standard deviation). *Ctenocalanus vanus, Clausocalanus brevipes, Centropages brachiatus and
Calanoida copepodites.
Tabla 2. Composicin taxonmica y abundancia (ind m-3) de zooplancton en el hbitat reproductivo costero (HRC) de la
anchota (SD: desviacin estndar). *Ctenocalanus vanus, Clausocalanus brevipes, Centropages brachiatus and
Calanoida copepodites.

Taxa Mean SD Abundance range


Mesozooplankton < 1 mm 988.92 1233.54 134.23 - 4546.16
Copepods 736.61 1164.65 61.13 - 4408.57
Euterpina acutifrons 10.38 34.42 0 - 124.77
Oithona spp. 156.10 154.92 13.37 - 518.67
Paracalanus spp. + Calanoida copepodites 570.13 1107.14 46.98 - 4173.52
Unidentified nauplii 27.20 68.94 0 - 254.44
Cladocerans 212.08 324.92 2.44 - 1206.41
Evadne nordmanni 130.83 235.38 0 - 820.55
Podon spp. 81.25 115.03 0 - 385.86
Veliger stages of Lamellibranchs 13.03 22.74 0 - 74.52
Mesozooplankton 1-2 mm 144.42 116.86 25.84 - 396.03
Copepods* 76.92 86.97 3.25 - 286.64
Fish eggs 9.88 11.50 0 - 33.76
Anchovy eggs 9.59 11.05 0 - 31.93
Unidentified fish eggs 0.29 0.56 0 - 1.83
Appendicularians 57.63 87.41 0 - 327.77
Macrozooplankton > 2 mm 7.81 13.36 0.58 - 50.31
Copepods 1.52 2.83 0 - 10.7
Calanoides carinatus 1.52 2.83 0 - 10.7
Decapod larvae 1.97 5.69 0 - 20.80
Amphipods 0.04 0.09 0 - 0.27
Chaetognaths 3.30 4.91 0 - 16.88
Pteropods 0.97 3.39 0 - 12.23

this area (Hansen, 2004), which agrees with the cited observed in E. anchoita and several other anchovy
preference of this species for salinity frontal regions species (Angelescu, 1982; Tudela & Palomera, 1997;
(Martos et al., 2005). Pjaro, 2002).
Although the low number of samples does not In this study, most of items ingested by anchovies
allow to be conclusive, these results support the belonged to < 1 mm and 1-2 mm TL mesozooplankton
hypotheses that this area could be a preferred site of fractions. According to Angelescu (1982), these prey
intense food intake by anchovy within less productive size (< 2 mm) would correspond to a filtration feeding
coastal waters. mechanism in argentine anchovy. The prey spectrum
The different time of the day when samples were found is in accordance with the taxonomic groups
collected might reduce the significance of this finding, mentioned by other authors in the CRH where the
taking into account that a diel feeding cycle has been copepods were the main prey of anchovy followed by
described for E. anchoita (Angelescu, 1982). appendicularians and cladocerans (Capitanio et al.,
However, this cycle was observed mainly in shelf 1997; Mianzan et al., 2001; Pjaro et al., 2007).
waters where two periods of feeding activity at sunset However, the large incidence of small copepods (<
and sunrise were reported. On the contrary, in the 1 mm TL) in Argentine anchovy diet is highlighted in
CRH this pattern was weak probably due to lower this work because they were, for the first time,
food availability. Under these conditions of limited accurately identified and quantified. These results
food availability an extended feeding period has been agree with those frequently reported for European
Anchovy feeding in an estuarine front, Argentine 211

anchovy (Tudela & Palomera, 1997; Plounevez & eggs and larvae, due to the fact that greatest amounts
Champalbert, 1999, 2000; Borme et al., 2009). of large zooplankton also mean higher amounts of
The main small copepod species found in stomach potential predators. According to this, the strategy of
content were Paracalanus spp., Oithona spp. and the fishes could consist in feeding in shelf waters,
copepodite stages of Calanoida. It is known that these which is dominated by high concentrations of large
copepods form dense aggregations associated with zooplankton, and subsequently migrate into the CRH
saline discontinuities of the estuarine front (Vias et where dominant small zooplankton is suitable for
al., 2002; Marrari et al., 2004). feeding larvae (Pjaro, 2002).
Small copepods are important links in marine food The present findings, although based on few
webs, acting not only as major grazers of small samples, would suggest that in RdP front, the above
phytoplankton but also preying upon heterotrophic mentioned strategy should be revised since intense
protists which are components of the microbial loop feeding occurs in this sector of the CRH. The
(Turner, 2004). Thus, they might play a significant coincidence of both feeding and spawning grounds
role in the energy transfer to anchovy by an alternative could have important implications. It might be
pathway to the traditional herbivorous food web of expected an increased reproductive potential of E.
shelf waters: spring diatom bloom-herbivorous anchoita in the estuarine front as it was reported for
calanoid copepods-fish. other anchovy species spawning in food rich areas
The species composition and relative abundance (Peebles et al., 1996). Further studies are required to
observed in zooplankton samples coincided roughly confirm this observation.
with the stomach contents. However, despite of the
large abundance of small copepods in anchovy diet, a ACKNOWLEDGEMENTS
clear selectivity for prey greater than 1 mm TL was
observed in this work. This might be explained by a The authors are indebted to Dr. Jorge Hansen,
decrease in retention efficiency of small prey by the Director of the Anchovy Project of INIDEP, and the
filtering apparatus of larger fishes. In fact, an increase Oceanography Laboratory of INIDEP for providing
in gill-raker spacing with anchovy size has been the environmental data. This study was partially
previously shown (Angelescu, 1981). funded by CONICET-PIP5009; PICT 15227-03 and
Intensive predation on patches of unidentified fish UNMdP 15/E269.
eggs and appendicularians was observed in two
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Received: 15 June 2010; Accepted: 13 April 2011


Lat. Am. J. Aquat. Res., 39(2): 214-224, 2011 Lat. Am. J. Aquat. Res. 214
DOI: 10.3856/vol39-issue2-fulltext-3

Research Article

Influence of dietary starch and cellulose levels on the metabolic profile and
apparent digestibility in penaeoid shrimp

Susana Mara Velurtas3, Ana Cristina Daz2,3, Anala Vernica Fernndez-Gimenez1,3


& Jorge Lino Fenucci1,3
1
Consejo Nacional de Investigaciones Cientficas y Tcnicas
2
Comisin de Investigaciones Cientficas
3
Departamento de Ciencias Marinas, Facultad de Ciencias Exactas y Naturales
Universidad Nacional de Mar del Plata, Funes 3350, B7602AYL, Mar del Plata, Argentina

ABSTRACT. The present study compared the effect of different starch/cellulose ratios (30/0, 20/10, 10/20,
0/30) on the metabolic response and apparent digestibility in two species of penaeoids: Artemesia longinaris
and Pleoticus muelleri. Adult animals were used in order to obtain sufficient quantities of haemolymph and
faecal material for analysis. No significant differences were found in levels of plasma metabolites in P.
muelleri, but in A. longinaris, a significant increase was observed in glucose, total protein, and cholesterol in
correlation with increased dietary starch. The apparent digestibility coefficients decreased from 83.7% to
51.2% (A. longinaris) and from 71.9% to 7.6% (P. muelleri) as the dietary starch levels increased. The ratio of
amylase activity to protease activity (A/P ratio) declined in A. longinaris when the percentage of dietary starch
increased. In contrast, the A/P ratio for P. muelleri increased with higher starch concentrations. These results
demonstrated a close relationship between the feeding habits and digestive physiology of the two species
studied; they also suggest a more herbivorous behavior for A. longinaris and more omnivorous habits for P.
muelleri.
Keywords: Artemesia longinaris, Pleoticus muelleri, apparent digestibility, carbohydrate metabolism,
cellulose, starch, haemolymph, Argentina.

Influencia del nivel de almidn y celulosa en la dieta sobre el perfil metablico y


digestibilidad aparente en camarones penaeoideos

RESUMEN. En el presente estudio se compar el efecto de diferentes concentraciones de almidn/celulosa


(30/0; 20/10; 10/20; 0/30) sobre la respuesta metablica y la digestibilidad aparente en dos especies de
peneidos, Artemesia longinaris y Pleoticus muelleri. Se utilizaron animales adultos a fin de obtener cantidades
suficientes de hemolinfa y heces para los anlisis. No hubo diferencias significativas en los niveles de
metabolitos plasmticos en P. muelleri, en cambio en A. longinaris se observ un incremento significativo de
la glucosa, protenas totales y colesterol en relacin con el aumento del almidn en la dieta. Los coeficientes
de digestibilidad aparente disminuyeron de 83,7% a 51,2% (A. longinaris) y de 71,9% a 7,6% (P. muelleri) a
medida que los porcentajes de almidn en la dieta aumentaron. El cociente entre la actividad de amilasa y
proteasa (A/P) se redujo en A. longinaris con los mayores porcentajes de almidn dietario; por el contrario, el
cociente A/P en P. muelleri aument cuando la concentracin fue ms alta. Estos resultados demostraron que
existe una estrecha relacin entre los hbitos alimentarios y la fisiologa digestiva de las dos especies
estudiadas; sugiriendo un comportamiento ms herbvoro para A. longinaris y ms omnvoro para P. muelleri.
Palabras clave: Artemesia longinaris, Pleoticus muelleri, digestibilidad aparente, metabolismo de
carbohidratos, celulosa, almidn, hemolinfa, Argentina.

___________________
Corresponding author: Ana Cristina Daz (acdiaz@mdp.edu.ar)
215 Influence of dietary cellulose level in penaeoid shrimp

INTRODUCTION levels can only be properly interpreted if the


nutritional state of the shrimp is carefully controlled.
The major achievements in crustacean nutrition The present study was designed to compare the
include the identification of a protein sparing effect of dietary effect of different ratio starch/cellulose on
dietary carbohydrates and lipids, leading to selected physiological, metabolic, and hematological
considerably lower protein requirements than those responses and the apparent digestibility in two species
originally suggested. The proteins are the higher of penaoids (Artemesia longinaris and Pleoticus
reserve substrate in shrimp, which can be converted to muelleri). Both species present seasonal and yearly
carbohydrates following the gluconeogenic pathway fluctuations in catches; it is therefore important to
(Campbell, 1991). The carbohydrates are not essential establish the feasibility of culturing them on
for crustaceans; shrimp appear to be able to utilize commercial basis to keep a continue supply of these
complex carbohydrates better than simple ones such as species to the market. The Aquaculture group from the
glucose, which is quickly absorbed and released into University of Mar del Plata has been working with
the haemolymph, resulting in a physiologically both species, but mainly with P. muelleri, on different
abnormal elevation of plasma glucose levels (New, aspects of the biology, nutrition, maturation, massive
1976, 1990; Shiau & Peng, 1992). Starch is nowadays larval culture, and growth out in ponds. Some studies
the typical carbohydrate in formulated feeds for have demonstrated good survival and growth under
crustaceans; it is well hydrolyzed by shrimp such as culture conditions (Fenucci et al., 1983, 1990;
Fenneropenaeus indicus and Litopenaeus vannamei Petriella et al., 1984; Daz et al., 1996), and
but poorly hydrolyzed by lobsters (Verri et al., 2001). determined the nutritional requirements (Fernndez-
The rate of nutrient absorption depends on the rate Gimenez & Fenucci, 2002; Romanos-Mangialardo &
at which nutrients come into contact with the Fenucci, 2002) as well as gonadal maturation in
absorptive epithelium. Dietary fibers, such as captivity (Daz et al., 1997, 2001; Daz & Fenucci,
cellulose, are associated with the delay in stomach 2004), and characterized the digestive proteinases in
emptying and contribute to the efficient utilization of relation to the molting cycle (Fernndez-Gimenez et
dietary protein (Gomez Daz & Nakagawa, 1990). al., 2002).
Determination of digestibility can be used to select
ingredients that optimize the nutritional value and
reduce costs of formulated feeds. Among the methods MATERIALS AND METHODS
employed in feed digestibility studies in crustaceans,
the use of chromic oxide as an inert indicator is Feed and feeding trials
recommended with procedural steps to insure Artemesia longinaris and Pleoticus muelleri were
accuracy (Fenucci et al., 1980, 2009; Lee & obtained from a commercial fisherman in the coastal
Lawrence, 1997; Divakaran et al., 2002). waters of Mar del Plata, Argentina (38S). Large adult
The carbohydrates are incorporated in aquaculture animals were used in these experiments to obtain
feeds to reduce costs and for their binding properties sufficient quantities of faecal material for the analysis
during feed manufacturing. Waste management has of feed digestibility. All individuals were kept in 150
become a prime concern for shrimp farming in many L glass aquaria with continuous aeration during four
countries. It is generally accepted that a better weeks. Filtered seawater (to 5m) was exchanged at a
understanding of feed utilization by the shrimp is rate of 50% per day. Shrimp were exposed to constant
essential to reduce environmental pollution through conditions of photoperiod (11 h light-13 h dark),
both ammonia excretion and feces egestion; temperature (18C), pH 7, and salinity (31 ppt). The
carbohydrate utilization can be achieved and ammonium concentration never exceeded 0.2 mg L-1.
consequently lead to a decrease in the amount of All groups were fed ad libitum once a day (09:30 h).
nitrogen waste. Formulated feeds were tested in triplicate groups for
Haemolymph is the prime component involved in both species, each A. longinaris group consisted of 6
the defense mechanism of crustaceans; several shrimp (2.7 0.9 g mean weight) and P. muelleri
metabolic variables of haemolymph, such as proteins, groups had 4 shrimp (9.7 2.0 g mean weight),
glucose, and cholesterol have been proposed to randomly chosen.
monitor the effect of environmental conditions on wild The treatments consisted of four dry formulated
and cultured shrimp (Hall & Van Ham, 1998; Snchez feed prepared to contain different ratios
et al., 2001; Pascual et al., 2003). Fluctuations in starch/cellulose (30/0; 20/10; 10/20; 0/30), with 0.5%
biochemical variables are also associated with the chromic oxide as an inert indicator (to calculate the
physiological response to stress, but these variables apparent protein digestibility coefficients). Formu-
Lat. Am. J. Aquat. Res. 216

lations were made according to the chemical diagnosis (Wiener Laboratories SAIC, Argentina),
composition results of the by-products meal in order according to the manufacturers protocols and
to obtain isoproteic and isolipidic diets. The chemical quantified in a Metrolab 1600DR (Wienerlab
composition of the formulated feeds was confirmed Instrument). The extracts were analyzed in triplicate.
through proximate analysis (Table 1) according to
AOAC (1997). All ingredients, from a local feed Enzyme assays
manufacturer, were mixed and cold pelleted (< 50C) The amount of soluble protein in the homogenized
by extrusion (Fenucci & Zein-Eldin, 1976) and were midgut glands used for enzyme analysis was
oven-dried for 24 h at 50C. determined by the Bradford method (1976). Albumin
from chicken egg white (Sigma) was used as the
Apparent digestibility standard.
After a 7-day period of adjustment to the new Total proteinase determination was performed with
conditions and diets was beginning of fecal collection. 1% azocasein in 50 mM Tris-HCl, pH 7.5 as substrate.
To determine the apparent digestibility for crude Triplicates of 5 L of enzyme extracts were mixed
protein, before each feeding, feces were collected with 0.5 mL of buffer and 0.5 mL of substrate
during two weeks by siphoning and rinsed with solution. The reaction mixtures were incubated for 10
distilled water to eliminate the excess of salts. The min at 25C. Proteolysis was stopped by adding 0.5 ml
fecal material from each tank was pooled and frozen at of 20% trichloroacetic acid TCA, and the mixture was
-20C for analysis. centrifuged in Eppendorf tubes for 5 min at 14 000 g.
Proximate analyses of faecal samples were carried The supernatants were separated from the undigested
out using AOAC methods (1997). The chromic oxide substrate and the absorbance at 366 nm was recorded
levels were measured with a spectrophotometer (540 for the released dye (Garca-Carreo, 1992).
nm) (Shimadzu UV-2102 PC, UV-visible Scanning Total -amylase activity was determined using
Spectrophotometer). The apparent digestibility commercial kits for medical diagnosis (Wiener
coefficient (ADC) was estimated according to Fenucci Laboratories SAIC, Argentina), according to the
et al. (1980): ADC (% protein digestibility) = 100 - manufacturers protocols and quantified in a Metrolab
(Ia/Ib . IIb/IIa . 100) where: Ia = %Cr2O3 feed; Ib = % 1600DR (Wienerlab Instrument).
Cr2O3 feces; IIa = % protein food; IIb = % protein feces.
Total cellulase activity was determined according
to Martnez et al. (1999) modified method. A solution
Sampling and analyses of metabolic variables
of crystalline cellulose was prepared in substrate
At the end of the experiments (four weeks), shrimp buffer sodium acetate 0.05 M; pH 5. A 24 mL volume
were anaesthetized in ice water for approximately 5 of this substrate solution was then mixed with 1 mL of
min, then the haemolymph was extracted and midgut midgut gland extract, incubated with gentle agitation,
gland was removed. All shrimp used in the analysis for 2 h at 30C. The reaction mixture was centrifuged,
were in the intermolt stage (Petriella, 1984; Daz & 2 ml of supernatant was separated and added 0.1 mL
Petriella, 1990). Samples collected from eight starch solution (100 mg mL-1) and 2 mL of 3.5-
individuals (n = 8) of each treatment group were dinitrosalicilic acid. Then, the extract was incubated
analyzed separately. for 5 min at 100C and the absorbance was recorded at
Approximately 200-300 L of haemolymph were 490 nm. The extracts were analyzed in triplicate.
extracted from the arthrodial membrane of the fifth
pereiopod of each organism; using a 1 mL syringe Statistical Analysis
rinsed with a 10% cooled anticoagulant solution of One-way ANOVA and Duncans multiple
sodium citrate. The haemolymph was centrifuged at comparisons of means were preformed to compare the
800 g for 5 min, and plasma transferred into a new data obtained. Homogeneity of variances was verified
tube and stored at -20C for further analysis. with Cochrans test. An arcsine transformation was
Midgut glands were carefully dissected and applied before processing percentages data. Protein
immediately frozen at -20C and homogenized in digestibility among different treatments was evaluated
chilled distilled water and centrifuged for 30 min through regression analyses. A correlation coefficient
(10,000 g at 4C), the upper aqueous phase was stored was used to describe the fit of the data on the
at -20C. regression line. ANCOVA was used to test differences
Glucose, total protein and cholesterol concen- among regression lines. To find out the relationships
trations in plasma and supernatants from homogenate among different ratio starch/cellulose in the diet and
were measured using commercial kits for medical metabolic variables, Pearson's rank correlation
217 Influence of dietary cellulose level in penaeoid shrimp

Table 1. Ingredient composition of formulated feeds.


Tabla 1. Composicin de las dietas formuladas.

Ingredient Formulated feed (g 100 g-1 dry feed)


D1 D2 D3 D4
a
Fish meal 48 48 48 48
Soybean mealb 15.5 15.5 15.5 15.5
Manioc starchc 30 20 10 0
Cellulose microcrystallined 0 10 20 30
Fish oil 2 2 2 2
Lecithin 0.5 0.5 0.5 0.5
Cholesterol 0.5 0.5 0.5 0.5
Vitamin supplemente 0.5 0.5 0.5 0.5
Mineralsf 0.5 0.5 0.5 0.5
Fish soluble 1 1 1 1
Chromic oxide 0.5 0.5 0.5 0.5
Na alginate 1 1 1 1
Proximate composition (% dry matter)
Dry matter 99.3 97.6 98.2 99.2
Crude protein 37.9 38.2 38.2 37.8
Total lipid 12.4 13.2 12.0 12.7
Ash 11.0 11.6 10.8 10.2
a
Agustinier S.A. Mar del Plata, Argentina. bMelrico S.A. Argentina.
c
Molinos Chacabuco, Argentina. d Merck, Germany.
e
Vitamin premix (mg kg-1 of premix): cholecalciferol 35; thiamin 163;
rivoflavin 156; pyridoxine 213; calcium pantothenate 250; biotin 250; niacin
500; folic acid 25; B12 HCL 20; ascorbic acid Rovimix STAY C 781;
menadione 34; inositol 300; choline chloride 200; a-tocopherol acetate 1750;
vitamin A acetate 180 (Roche, Argentina).
f
Mineral premix: calcium 1,000 mg; magnesium 500 mg; potassium 99 mg;
zinc 30 mg; 10 mg; iron 10 mg; copper 2 mg; iodine 150 g; selenium 200
g; chromium 200 g; molybdenum 500 g (Twin Laboratories, Inc. USA).

coefficient was done. A probability level of 0.05 was concentration of metabolites was different in both
used to assess significance in all measured parameters. species. The highest level of cholesterol was observed
(Sokal & Rohlf, 1995). in A. longinaris fed with D1 (30/0, starch/cellulose),
whereas concentrations of glucose and total protein
were not significantly different. In contrast, in P.
RESULTS
muelleri glucose was significantly higher in shrimp
fed with D1 than in those fed with diet containing
Metabolic variables
lower starch levels.
Mean values of metabolic variables for each species
are shown in Figure 1. There were no significant Enzyme assays
differences in levels of plasma metabolites in P. Soluble protein content of the midgut gland was 15.3
muelleri when shrimp were fed with different ratio 1.68 mg mL-1 in A. longinaris and 17.3 2.30 mg
starch/cellulose. Significant variations were observed mL-1 in P. muelleri. No significant differences were
in the metabolic variables of A. longinaris, a observed in proteinase and -amylase activity in
significant increase in glucose, total protein, and midgut gland extracts from the four dietary groups in
cholesterol was noted in correlation with the increase both species (Table 2). No specific cellulase activity
in starch. was observed in the midgut gland extracts.
The analysis of the midgut gland from shrimp fed The ratio of amylase activity to protease activity
with different levels of starch/cellulose showed that (A/P ratio) decreased in A. longinaris when the
Lat. Am. J. Aquat. Res. 218

Figure 1. Metabolic variables in haemolymph and midgut gland of A. longinaris and P. muelleri fed with different ratio
starch/cellulose in the diet. Error bars indicate standard deviation. Different letters indicate statistical differences (P <
0.05).
Figura 1. Variables metablicas en hemolinfa y hepatopncreas de A. longinaris y P. muelleri alimentados con diferentes
niveles de almidn/celulosa en la dieta. La barra indica la desviacin estndar. Letras distintas indican diferencias
estadsticas significativas (P < 0,05).

percentage of dietary starch increased. In contrast, the the cellulose rate, except glucose in haemolymph for
A/P ratio for P. muelleri increased when starch A. longinaris (Table 3) and glucose in midgut gland
concentration was high (Fig. 2). for P. muelleri (Table 4). Metabolic variables were
correlated with each other.
Apparent Digestibility
The apparent protein digestibility coefficients
decreased from 83.7% to 51.2% in A. longinaris) and DISCUSSION
from 71.9% to 7.6% in P. muelleri with the increase in
dietary cellulose levels, and was significantly different Dietary nutritional requirements of two species of
among treatments. In vivo apparent protein penaeoids were investigated on the basis of their
digestibility was related to dietary cellulose contents haemolymph metabolic contents and the apparent
as shown by the regression analysis (y = 0.095x2 - digestibility analysis to determine which the dietary
4,2647x + 88,671; R2 = 0.7198 for A. longinaris, and y components that were better assimilated are. The
= 97,476 e-0, 0829x, R2 = 0.724 for P. muelleri) (Fig. 3). penaeoids shrimp do not present a dietary glucose
requirement since this compound can come from the
Pearsons Correlation gluconeogenesis from the amino acids. Nevertheless,
Pearson correlation coefficients showed that all these organisms own a complete enzymatic structure
variables exhibited a greater degree of correlation with for the digestion of proteins and polysaccharides, such
219 Influence of dietary cellulose level in penaeoid shrimp

Table 2. Specific enzyme levels ( SEM) recorded from midgut gland at four levels of dietary starch/cellulose in A.
longinaris and P. muelleri.
Tabla 2. Niveles enzimticos ( ESM) especficos registrados en hepatopncreas de A. longinaris y P. muelleri alimenta-
dos con cuatro niveles dietarios de almidn/celulosa.

Protease Amylase
Formulated feed
A. longinaris P. muelleri A. longinaris P. muelleri
a a a
D1 0.11 0.007 0.25 0.117 2.06 0.007 3.78 0.410a
D2 0.11 0.056a 0.24 0.009a 2.30 0.007a 2.99 0.183a
D3 0.09 0.011a 0.32 0.019a 2.56 0.084a 2.20 0.128a
D4 0.05 0.024b 0.47 0.066a 2.56 0.275a 3.69 0.134a
Specific protease activity expressed as Abs/mg protein/min. Specific amylase activity
expressed as mg starch hydrolyzed/mg protein/min. Different superscripts are significantly
different, P < 0.05.

Figure 2. The effect of dietary starch levels on ratio of Figure 3. Apparent protein digestibility at four levels of
amylase specific activity to protease specific activity on dietary starch/cellulose in A. longinaris and P. muelleri.
polynomial regression analysis in A. longinaris and P. Values are means of three observations. Error bars
muelleri (y = 0.051x2 2.602x + 50.80, R = 0.969 for A. indicate standard deviation.
longinaris, and y = 0.009x2 + 0.001x + 7.387, R = 0.867 Figura 3. Digestibilidad aparente de protenas con cuatro
for P. muelleri). niveles de almidn/celulosa en la dieta de A. longinaris y
Figura 2. Regresin polinomial del efecto de los niveles P. muelleri. Los valores representan la media de tres
de almidn en la dieta sobre el cociente entre la actividad observaciones. La barra indica la desviacin estndar.
especfica de amilasa y la de proteasa en A. longinaris y
P. muelleri (y = 0,051x2 2,602x + 50,80; R = 0,969
para A. longinaris; y = 0,009x2 + 0,001x + 7,387; R = bonds, which are (1-4). The inclusion of starch in
0,867 para P. muelleri). the shrimps diet represents the greater source of
energy. The incorporation of cellulose was used to
as starch, glycogen, laminarin, and chitin that are compensate the amount of carbohydrates added to the
natural components of their diet. (Tacon, 1990). The experimental diet or to increase stomach emptying
starch is a straight-chain consisting of glucose (Shiau, 1997).
molecules linked together by (1-4) bonds, The type of food is a dominant factor affecting
conformed by two units amylose and amylopectin. shrimp haemolymph metabolites (Pascual et al.,
The starches rich in amylose are poorly digestible 2003). Baseline levels of the haemolymph metabolites
because -amylase cannot hydrolyze the amylase, in were obtained by Rosas et al. (2002) in Litopenaeus
contrast, the starch rich in amylopectin is relatively vannamei to be used as reference parameters. Glucose
well digested (Gaxiola et al., 2006). The cellulose is is the major component of circulating carbohydrates in
also a polymer of glucose but it differs in its glycoside crustaceans, but its concentration varies markedly
Lat. Am. J. Aquat. Res. 220

Table 3. Correlation matrix of metabolic variables and cellulose in feed for Artemesia longinaris.
Tabla 3. Matriz de correlacin de las variables metablicas y el nivel de celulosa en la dieta para Artemesia longinaris.

C GH PH ChH GMG PMG ChMG APD


C 1
GH -0.983 1
PH -0.919* 0.901* 1
ChH -0.941* 0.928* 0.998 1
GMG -0.432* 0.445* 0.042* 0.106* 1
PMG -0.865* 0.941* 0.749* 0.785* 0.524* 1
ChMG -0.866* 0.940* 0.842* 0.865* 0.313* 0.973 1
APD -0.874* 0.889* 0.983 0.980 -0.014* 0.786* 0.893* 1
*P < 0.05. C-Cellulose feed; GH -Glucose Haemolymph; PH- Total Protein Haemolymph; ChH -
Cholesterol Haemolymph; GMG -Glucose Midgut Gland; PMG -Total Protein Midgut Gland; ChMG -
Cholesterol Midgut Gland; APD - Apparent Protein Digestibility

Table 4. Correlation matrix of metabolic variables and cellulose in feed for Pleoticus muelleri.
Tabla 4. Matriz de correlacin de las variables metablicas y el nivel de celulosa en la dieta para Pleoticus muelleri.

C GH PH ChH GMG PMG ChMG APD


C 1
GH -0.775* 1
PH -0.866* 0.871* 1
ChH -0.445* 0.751* 0.346* 1
GMG -0.954 0.913* 0.868* 0.674* 1
PMG 0.245* -0.536* -0.753* -0.960 -0.478* 1
ChMG -0.252* -0.340* -0.232* -0.138* 0.063* 0.025* 1
APD -0.947* 0.620* 0.661* 0.471* 0.886* -0.346* 0.515* 1
*P < 0.05. C-Cellulose feed; GH -Glucose Haemolymph; PH - Total Protein Haemolymph; ChH
-Cholesterol Haemolymph; GMG -Glucose Midgut Gland; PMG -Total Protein Midgut Gland;
ChMG - Cholesterol Midgut Gland; APD -Apparent Protein Digestibility

among the species (Chang & OConnor, 1983). From the entire set of metabolites studied in A.
Increases in haemolymph glucose are also associated longinaris plasma, glucose, total protein, and
with the physiological response to stress in shrimp, but cholesterol were the most affected by the increase of
levels can only be properly interpreted if the starch in diet. But in P. muelleri there were no
nutritional state of the shrimp is carefully controlled significant variations under the same conditions.
(Hall & Van Ham, 1998). Furthermore, the glucose in In P. muelleri, cholesterol in midgut gland showed
haemolymph is an indicator of the carbohydrates slight fluctuations, however in A. longinaris,
metabolism and the level of this nutrient in the diet. In significant differences were observed among dietary
the present study, the glucose levels were similar to treatments (Fig. 1). The shrimps midgut gland is
considered the main storage organ, mainly
those reported in juvenile L. setiferus, L. vannamei
accumulating lipids, and to a lesser degree, glycogen.
and L. stylirostris (Rosas et al., 2000). In A.
It has been proposed in crustaceans, that cholesterol is
longinaris, the glucose in haemolymph was no conserved due to their role as structural component of
correlated with cellulose level in the diet (Table 3); cell membranes, and is also an essential nutrient for
shrimp could activate its compensation mechanism crustaceans since they are incapable of de novo
that allowed the recovery of haemolymph metabolites synthesis of the steroid ring (Rabid et al., 1999). The
to maintain the homeostasis. This mechanism could dependence of haemolymph cholesterol on dietary
involve the use of reserves stored in digestive gland, lipids levels is related to the ability of shrimp to store
such as demonstrated in other species (Pascual et al., and synthesize lipids. Mourente & Rodrguez (1991)
2003). and Teshima (1998) showed that because of the
221 Influence of dietary cellulose level in penaeoid shrimp

limited space in shrimps digestive gland, lipids must synthesis from the transamination pathway, and its
be processed rapidly and delivered into the posterior storing (Rosas et al., 2001). The values of
haemolymph, where they are transported to the proteins in haemolymph and digestibility for the
different tissues to be metabolized. With regards to P. different treatments in P. muelleri did not adjust to a
muelleri, this species will be using cholesterol of the same pattern. Whereas digestibility was greater in D1
diet quicker than A. longinaris. Probably for that and D2, there were no differences in the circulating
reason it is observed higher levels of cholesterol in A. proteins. From the analysis of the proteins data it can
longinaris haemolymph and midgut gland and in P. be postulated that P. muelleri employs these absorbed
muelleri only in the haemolymph. As all supplied diets proteins for muscular development or growth.
had the same cholesterol level, it was evident that P. Penaeid shrimp adapt quite well to changes in diet
muelleri presented a greater requirement of this composition by the induction of digestive enzymes
nutrient, which was demonstrated by a smaller level of synthesized and secreted in midgut gland. These
reserve. P. muelleri would be more carnivorous and enzymes hydrolyze a variety of substrates and various
require cholesterol from animal sources. This is in factors are involved in their regulation, including diet
agreement with the results of digestibility, which (Gamboa-Delgado et al., 2003). Therefore, the
decreased with increasing cellulose inclusion digestive enzyme profile can be used to illustrate the
Borrer & Lawrence (1989) observed that the level capacity of shrimp to exploit diet in order to meet
of dietary cellulose affected apparent protein nutritional requirements. Carnivorous species
digestibility in Farfantepenaeus aztecus, by lowering generally have a wide range of proteolytic enzyme at
digestibility values as cellulose levels increased. A high concentrations, which is consistent with their
similar result was observed in Macrobrachium ability to hydrolyze high levels of dietary protein
rosenbergii (Gonzlez-Pea et al., 2002). On the other (Johnston & Yellowlees, 1998). However, omnivores
hand, in L. vannamei the protein digestibility did not and herbivores have a wide range and higher
change with the different levels of cellulose (Borrer & concentration of carbohydrases, consistent with their
Lawrence, 1989; Guo et al., 2006). It was evident that ability to hydrolyze plant and animal dietary
A. longinaris fed with diets poor in cellulose content carbohydrate (Wigglesworth & Griffith, 1994). The
(D1 and D2) assimilated better the nutrients than P. decline in the ratio of amylase to protease observed in
muelleri and this fact was reflected by an increase of A. longinaris in our study, confirms that carbohydrate
circulating metabolites and the apparent digestibility digestion and its utilization change with the increase
(Fig. 3). In both species, the digestibility values in dietary starch levels. In contrast, in P. muelleri the
decreased from D1 to D4, nevertheless the values of A/P ratio was correlated with dietary starch level. This
apparent digestibility in A. longinaris were higher than shift in relative importance of carbohydrate and
in P muelleri. This fact would be related to the rate of protein highlights the strategy outlined above,
nutrient absorption that depends on the time at which whereby carbohydrate energy reserves are used
nutrients come into contact with the absorptive initially, while protein becomes important once
epithelium. According to other authors, the relative carbohydrate reserves are depleted.
influence of dietary fiber on the movement of In the current study, there was no cellulase activity
nutrients along the gastrointestinal tract affects in the midgut gland of both species. It is now clear
nutrient absorption (Shiau, 1997). So, it is possible that cellulases are produced endogenously in a number
that the dietary fiber with high viscosity reduces the of invertebrate taxa that includes crustaceans; genes
interaction between the enzymes and substrates, for cellulose enzymes (-glucosidase and endo--1,4-
reducing absorption rates. The binding capability of glucanase) are present in the genome of crayfish
the dietary fiber is another possible factor that can (Cherax sp.) (Linton et al., 2006). However, in
reduce the availability of nutrients (Gonzlez-Pea et penaeoid species cellulose digestion has not been
al., 2002). unequivocally demonstrated (Shiau, 1997). More
The proteins are essential nutrients for the suitable substrates and assays for the determination of
penaeoids shrimps because they are basic for growth, cellulase activity are required to clarify matters.
the regulation of the internal osmotic pressure, the Although the bibliography indicates that both
gluconeogenesis and the immune system (Rosas et al., species studied in this work present a similar
2002). Therefore variations of this nutrient in nourishing regime (Boschi, 1989; Gavio & Boschi,
haemolymph can be used as good indicator of general 2004), studies in culture conditions showed that both
physiological state. The increment in haemolymph species have a 92% apparent digestibility of proteins
proteins observed in A. longinaris feed D1 and D2 with diets having fish meal as the main ingredient;
(high levels starch) could be related with amino acids when this ingredient is replaced by soybean meal, the
Lat. Am. J. Aquat. Res. 222

digestibility is 83% for A. longinaris and 47.7% for P. Daz, A.C. & J.L. Fenucci. 2004. Effect of artificial
muelleri (Fenucci et al., 2009). This difference in nutrition on the induction of precocious maturation in
digestibility can be related to the more carnivorous Pleoticus muelleri Bate (Crustacea, Penaeoidea).
behavior of the latter species. The present study shows Aquac. Res., 35: 1166-1171.
that apparent protein digestibility was influenced by Daz, A.C. & A.M. Petriella. 1990. Moult staging in the
the levels of dietary starch and cellulose in both shrimp, Pleoticus muelleri Bate. J. Aquac. Tropics, 5:
species; increasing cellulose levels caused significant 181-189.
reduction in protein digestibility. The inclusion of Daz, A.C., A.V. Fernndez-Gimenez, N.S. Harn & J.L.
starch as source of carbohydrates in the diet seems to Fenucci. 2001. Reproductive performance of male
be more suitable than cellulose. Argentine red shrimp Pleoticus muelleri Bate
(Decapoda, Penaeoidea) in culture conditions. J.
ACKNOWLEDGEMENTS World Aquac. Soc., 32(2): 236-242.
Divakaran, S., L. Obaldo & I.P. Forster. 2002. Note on
This research was funded by a grant PIP. N112- the methods for determination of chromic oxide in
200801-02585 from CONICET (Consejo Nacional de shrimp feeds. J. Agric. Food Chem., 50: 464-46.
Investigaciones Cientficas y Tcnicas) Argentina. Fenucci, J.L., M.I. Mller & J.H. Magnaterra. 1990.
Special thanks to Dra. Liliana Sousa by the revision of Factibilidad de cra del langostino (Pleoticus
the English language of the manuscript. The authors muelleri). Frente Martimo, 7(B): 103-108.
also thanks anonymous reviewers and editor for Fenucci, J.L., Z. Zein-Eldin & A.L. Lawrence. 1980. The
critically reviewing the manuscript. nutritional response of two penaeid species to various
levels of squid meal in a prepared feed. Proc. World
Aquac. Soc., 11: 403-409.
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Received: 7 July 2010; Accepted: 19 April 2011


Lat. Am. J. Aquat. Res., 39(2): 225-235, 2011 Population structure of Panulirus gracilis 225
DOI: 10.3856/vol39-issue2-fulltext-4

Research Article

Catch composition of the spiny lobster Panulirus gracilis (Decapoda: Palinuridae)


off the western coast of Mexico

Ral Prez-Gonzlez
Universidad Autnoma de Sinaloa, Facultad de Ciencias del Mar
P.O. Box 610, Mazatln, Sinaloa, Mxico

ABSTRACT. The lobster fishery in the Gulf of California and the south-central region of the western coast of
Mexico consists of small-scale artisanal activity supported by Panulirus gracilis and P. inflatus, with an
annual average catch of 132 ton. The present study analyzes the landing composition of this fishery and the
population structure of P. gracilis. Carapace lengths (CL) for this species ranged from 35 to 125 mm, and the
most frequent sizes were between 60 and 85 mm. The size distribution was approximately normal. This
implies that the fishery is composed of several size classes, with annual recruitment to the fishing areas. For
the 1989-1990 and 1990-1991 fishing seasons, the mean monthly sizes of males were between 70.18 11.74
and 81.11 6.76 mm CL, whereas females averaged from 73.60 8.95 to 80.28 7.53 mm CL. Power-law
relationships between carapace length (CL in mm) and total weight (TW in g) were determined, resulting in
the following equations: PT = 0.0021 CL2.7689 for males and PT = 0.0009 CL3.0038 for females. During certain
periods of the year, males dominated the catch; however, the overall annual male:female ratio was near 1:1.
Keywords: population structure, spiny lobster, Panulirus gracilis, Gulf of California, Mexico.

Composicin de la captura de la langosta espinosa Panulirus gracilis


(Decapoda: Palinuridae) en la costa oeste de Mxico

RESUMEN. La pesquera de langosta en el golfo de California y en el centro-sur de la costa occidental de


Mxico es una actividad artesanal a pequea escala y es sostenida por Panulirus gracilis y P. inflatus, con una
captura promedio anual de 132 ton. En este estudio se analiza la composicin de los desembarques de esta
pesquera y la estructura de la poblacin de P. gracilis. El intervalo de talla de esta especie fue de 35 a 125
mm de longitud del cefalotrax (LC) y el ms frecuente se encontr entre 60 y 85 mm. La distribucin de
tallas fue aproximadamente normal. Esto implica que la pesquera est compuesta por varias clases de tallas,
con un reclutamiento anual a las reas de pesca. La talla media mensual de machos fue entre 70,18 11,74 y
81,11 6,76 mm LC y en hembras de 73,60 8,95 a 80,28 7,53 mm LC, durante las temporadas de pesca
1989-1990 y 1990-1991. Se determin la relacin entre la LC (en mm) y el peso total (PT, en g), obtenindose
las siguientes ecuaciones: PT = 0.0021 LC2.7689 en machos y PT = 0.0009LC3.0038 en hembras. Durante ciertos
perodos del ao los machos son dominantes en las capturas, pero la proporcin machos:hembras durante todo
el ao es cercana a 1:1.
Palabras clave: estructura poblacional, langosta, Panulirus gracilis, golfo de California, Mxico.
___________________
Corresponding author: Ral Prez-Gonzlez (raulp@ola.icmyl.unam.mx)

INTRODUCTION The annual landings of these species were estimated at


approximately 500-650 t during the 15-year period
On the Mexican coast of the Pacific Ocean and Gulf from 1990-2005. This production includes the catches
of California, Panulirus gracilis and P. inflatus are of these species obtained in Baja California (A. Vega-
locally important fishery resources and their Velzquez, pers. comm.).
harvesting is exclusively a small-scale artisanal Traditionally, P. gracilis and P. inflatus were
activity, developed mainly on the continental shelf. captured in traps and sometimes by divers (Prez-
226 Lat. Am. J. Aquat. Res.

Gonzlez et al., 2002a). A major change in the Lobsters caught with tangle nets from depths of
exploitation strategy of these species took place during approximately 0.5-35 m were sampled at random
the 1980s and early 1990s with the progressive every month from September, 1989 to November,
introduction of tangle nets, which have almost totally 1991.
replaced other fishing methods. These tangle nets To determine the relationships among total length
(called chinchorros langosteros in the region) (TL), carapace length (CL), total weight (TW) and
usually have stretched meshes of 101.6 and 114.3 mm, carapace width (CW), regression equations for TL vs
lengths between 75.0 and 200.0 m and a height CL, TW vs CW and CW vs CL were calculated from
between 0.9 and 1.8 m. In general, the nets are left in sample of whole male and female P. gracilis caught in
the water for 24 h (one fishing day). A longer set time the same study area. The TL was measured from
leads to better catches of spiny lobster, as they are between the rostral horns to the posterior end of the
attracted by fishes, crustaceans, mollusks and other
telson with a modified ichthyometer ( 1 mm). CL and
invertebrates caught in the nets (Olabarra, 1999;
CW were measured with a vernier caliper ( 0.01
Plascencia-Gonzlez & Van der Heiden, 2002; Prez-
mm), with the former being measured along the mid-
Gonzlez, 2006; Prez-Gonzlez et al., 2002b, 2006).
dorsal line, from the transverse ridge between the
Panulirus gracilis (called gera, verde, arenera or postorbital spines to the posterior edge of the
playera spiny lobster) is distributed along the coastline carapace, and the latter at the greatest width of the
of the eastern Pacific from Baja California, Mexico, to carapace. TW was measured with a field balance ( 1
Paita, Peru and the Galapagos Islands (Holthuis, 1991; g).
Hendrickx, 1995). P. inflatus is endemic to Mexico, Additionally, to obtain CL and TW to the nearest
but P. gracilis is also fished in Panama (Butler & mm and g, respectively, selected individuals were
Pease, 1965), on the continental coast of Ecuador transported to the laboratory each month to be
(Loesch & Lpez, 1966; Bez, 1983), and in the measured with a digital caliper ( 0.1 mm) and
Galapagos Islands (Holthuis & Loesch, 1967). Most weighed on an electronic balance ( 0.01 g). These
studies on the two spiny lobsters coexisting along the data were used to estimate the parameters of the
western coast of Mexico have considered them both; relationship between TW and CL by a linear
only a few have been performed on the latter species regression analysis of the log-transformed data:
specifically.
TW= aCLb Ln (CL) + Ln(a)
The catch composition, population structure, sex
ratio, and fishery characteristics of both species have where a and b are constants.
been described on the Mexican Pacific (Weinborn,
Data were grouped into 5-mm class intervals, weighed
1977; Briones et al., 1981; Jurez-Carrillo et al.,
for each landing and compiled into annual
2006) and Gulf of California coasts (Prez-Gonzlez
distributions. The size distribution and sex ratio were
et al., 1992a, 1992b; Valadez-Manzano et al., 2003;
obtained from the pooled sample (catch obtained by
Arzola-Gonzlez et al., 2007). Here we report these
accompanying fishermen in the field plus commercial
characteristics for P. gracilis off the western coast of
landings).
Mexico in the lower part of the Gulf of California.
RESULTS
MATERIALS AND METHODS
From September, 1989 to November, 1991, a total of
Commercial lobster fishing on the western coast of the 13,834 spiny lobster were caught, of which 5,799
Gulf of California occurs in the south, primarily at the (41.92%) belonged to the species P. gracilis and 8,035
state of Sinaloa. Therefore, the study area in this (58.08%) to P. inflatus. The observed relative
region was located from the north of Punta Piaxtla to proportions of these lobster species showed an
the south in Mazatlan Bay, between 2310-2348N inversion during the study period (Fig. 2). P. inflatus
and 10624-10654W (Fig. 1). The coast presents predominated from September 1989 to September
extensive sand beaches with some gravel-sand 1990, whereas P. gracilis was more abundant from
patches, while large areas offshore are rocky or October 1990 to November 1991, except in February
covered with gravel-sand. and October of 1991.
The target species was determined according to the Morphometric relationships
catalogues of Holthuis (1991) and Hendrickx (1995) TL vs CL and CW vs CL exhibited linear
catches were weighed monthly. To determine the relationships, while TW vs CW was potential, and
population structure of P. gracilis, catches were their equations appear in Table 1. The determination
sampled by accompanying fishermen in the field. coefficient (R2) values were high.
Population structure of Panulirus gracilis 227

Figure 1. Map of the study area in the lower part of the Gulf of California, western coast of Mexico.
Figura 1. Mapa del rea de estudio en la parte baja del golfo de California, costa occidental de Mxico.

TW-CL relationship
Data from 279 specimens (159 males; size range 42-
92 mm CL, weight range 60-580 g, and 120 females;
size range 48-86 mm CL, weight range 100-580 g),
were used to determine the relationship between TW
and CL (Fig. 3). The relationships between carapace
length (CL in mm) and total weight (TW in g) were as
follows: for males, TW = 0.0021 CL2.7689; for females,
TW = 0.0009 CL3.0038. The male relationship was
allometric (b 3, P < 0.05), whereas for females it
was isometric (b = 3, P > 0.05).

Size distribution
Figure 2. Panulirus inflatus and P. gracilis landings The size of the landed P. gracilis individuals
between September 1989 and November 1991 in the ranged from 40 to 120 mm CL in 1990, with most of
lower part of the Gulf of California, Mexico. the individuals sized from 65 to 90 mm CL; the mode
Figura 2. Capturas de Panulirus inflatus and P. gracilis was 75 mm CL (Fig. 4). In 1991, the specimens
desembarcadas entre septiembre de 1989 y noviembre de ranged from 35 to 125 mm CL, with most of the
1991 en la parte baja del golfo de California, Mxico. individuals sized from 60 to 85 mm CL; the mode was
228 Lat. Am. J. Aquat. Res.

Table 1. Regression equations for the relationships between total length (TL) and carapace length (CL), total weight
(TW) and CL and carapace width (CW) and CL estimated for both sexes of Panulirus gracilis in the lower part of the
Gulf of California, Mexico.
Tabla 1. Ecuaciones de las relaciones entre la longitud total (TL) y longitud del cefalotrax (CL), peso total (TW) y CL, y
ancho del cefalotrax (CW) y CL estimadas tanto para ambos sexos como separados de Panulirus gracilis en la parte baja
del golfo de California, Mxico.

Relationship Equation R2 n
Males + females
TL vs CL TL = 2.5027 CL + 16.036 0.898 271
TW vs CW TW = 0.0017 CW 2.973 0.886 271
CW vs CL CW = 0.7458 CL + 4.271 0.930 271
Males
TL vs CL TL = 2.3714 CL + 22.037 0.898 159
TW vs CW TW = 0.002 CW 2.9241 0.890 159
CW vs CL CW = 0.7403 CL + 4.4196 0.930 159
Females
TL vs CL TL = 2.8109 CL + 0.0933 0.949 112
TW vs CW TW = 0.0012 CW 3.0784 0.896 112
CW vs CL CW = 0.7616 CL + 3.57 0.934 112

75 mm CL (Fig. 5). No change in the modal size


classes was found between the 1989-1990 and the
1990-1991 fishing seasons.
The sample mean and standard deviation were
analyzed for the 1989-1990 and 1990-1991 fishing
seasons. The monthly mean size, standard deviation
and size range of the sample, as a whole and by sex,
are presented in Table 2; the corresponding weight
data are given in Table 3. In the 1989-1990 fishing
season, the monthly mean sizes and weights of males
were between 70.18 11.74 and 81.11 6.76 mm CL
and 317.28 142.59 and 427.73 98.61 g TW,
respectively, and for females they were between 75.06
6.51 and 80.28 7.53 mm CL and 371.86 90.15
and 437.76 109.91 g TW. For the 1990-1991 fishing
season, the monthly mean sizes and weights of males
were between 71.09 11.31 and 79.30 6.99 mm CL
and 300.61 150.38 and 417.33 105.71 g TW,
respectively, and for females, they were between
73.60 8.95 and 77.23 6.62 mm CL and 355.00
124.12 and 431.67 136.05 g TW.
Sex ratio
Figure 3. Relationship between carapace length and total A total of 5,799 P. gracilis lobsters were examined.
weight in the spiny lobster Panulirus gracilis from the Of these, 56.4% were males (3,272) and 43.6% were
lower part of the Gulf of California, Mexico. females (2,527). The overall sex ratio (M:F) was
Figura 3. Relacin entre la longitud del cefalotrax y el 1:1.3. However, the sex ratio varied monthly (Fig. 6).
peso total en la langosta espinosa Panulirus gracilis en la The catch rates of male lobsters were consistently
parte baja del golfo de California, Mxico. higher in summer and autumn than those of females,
Population structure of Panulirus gracilis 229

Figure 4. Size-frequency distributions of Panulirus Figure 5. Size-frequency distributions of Panulirus


gracilis for a) both sexes, b) males and c) females by 5- gracilis for a) both sexes, b) males and c) females by 5-
mm-CL size classes during 1990 in the lower part of the mm-CL size classes during 1991 in the lower part of the
Gulf of California, Mexico. Gulf of California, Mexico.
Figura 4. Frecuencia de tallas (intervalo cada 5 mm de Figura 5. Frecuencia de tallas (intervalo cada 5 mm de
LC) de a) machos+hembras, b) machos y c) hembras de LC) de a) machos+hembras, b) machos y c) hembras de
Panulirus gracilis durante 1990 en la parte baja del golfo Panulirus gracilis durante 1991 en la parte baja del golfo
de California, Mxico. de California, Mxico.

Figure 6. Percentage of males and females of Panu-


lirus gracilis in monthly samples from September
1989 to November 1991 in the lower part of the Gulf
of California, Mexico.
Figura 6. Porcentajes mensuales de machos y
hembras de Panulirus gracilis entre septiembre de
1989 y noviembre de 1991 en la parte baja del golfo
de California, Mxico.
230 Lat. Am. J. Aquat. Res.

Table 2. Monthly mean size, standard deviation and size range whole and by sex of the carapace length (CL, in mm) of
Panulirus gracilis, during 1989-1990 and 1990-1991 fishing seasons in the lower part of the Gulf of California, Mexico.
Tabla 2. Nmero de hembras y machos de Panulirus gracilis e intervalos de talla, medias y desviacin estndar mensua-
les de la longitud del cefalotrax (CL, en mm), durante las temporadas de pesca 1989-1990 y 1990-1991 en la parte baja
del golfo de California, Mxico.

Season 1989-1990
Total Males Females
Month n CL n Range CL n Range CL
X SD CL (mm) X SD CL (mm) X SD
Sep 132 76.38 5.48 100 64.8-99.1 75.90 4.88 32 64.1-93.8 77.86 6.91
Oct 143 77.19 5.96 105 65.8-87.1 76.06 4.86 38 63.1-94.2 80.28 7.53
Nov 158 76.96 7.60 93 60.6-113.1 76.69 6.71 65 61.2-98.6 77.35 8.76
Dec 174 77.68 7.76 90 53.1-101.8 79.06 7.88 84 57.5-93.9 76.19 7.38
Jan 142 79.39 6.52 72 68.0-93.2 80.14 6.21 70 63.5-96.0 78.62 6.78
Feb 125 78.69 7.56 66 62.7-98.2 81.11 6.76 59 63.1-95.5 75.98 7.54
Mar 178 76.03 8.75 67 47.6-109.7 77.64 11.44 111 56.0-95.0 75.06 6.51
Apr 267 78.17 7.53 87 55.8-109.3 80.31 9.16 180 65.2-96.3 77.14 6.37
May 272 75.17 10.25 69 39.2-95.3 70.18 11.74 203 47.0-100.0 76.87 9.11

Season 1990-1991

Total Males Females


Month n CL n Range CL n Range CL
X SD CL (mm) X SD CL (mm) X SD
Sep 47 76.46 7.94 34 61.3-96.9 76.73 7.78 13 60.2-88.1 75.76 8.63
Oct 168 78.22 8.26 99 43.9-106.3 79.12 7.75 69 56.9-102.6 76.93 8.84
Nov 153 76.98 5.17 98 68.9-90.1 77.43 4.35 55 67.6-98.4 76.18 6.35
Jan 261 75.70 7.86 146 49.0-98.8 76.11 8.70 115 60.5-101.4 75.19 6.65
Feb 237 76.25 7.87 108 52.6-107.4 75.95 8.40 129 51.3-100.6 76.49 7.43
Mar 278 77.93 6.80 94 66.4-104.6 79.30 6.99 184 67.1-96.1 77.23 6.62
Apr 176 74.82 8.43 32 46.8-107.0 71.38 13.64 144 51.1-94.1 75.59 6.59
May 190 72.96 9.65 49 53.5-107.7 71.09 11.31 141 53.4-100.3 73.60 8.95

which were more abundant in spring; however, the water, whereas the nets were deployed offshore over
overall sex ratio exhibited a significantly equal gravel-sandy bottoms at depths between 8.0 and 25-
distribution (1:1, P > 0.05) during the winter months. 35.0 m (the habitat of P. gracilis) in periods of strong
ocean swells, coinciding with the observations
DISCUSSION recorded by Prez-Gonzlez et al. (1992a).
The periodic inversion in the proportions of P.
Catch composition gracilis and P. inflatus in commercial catches has
Nets are the main fishing method used in the study previously been observed along the Mexican Pacific
area and are deployed in rocky and gravel-sandy areas. coast (Briones-Fourzn & Lozano-lvarez, 1992;
Prez-Gonzlez et al. (2002a) indicated that the Valadez-Manzano et al., 2003; Arzola-Gonzlez et al.,
periodically inverse proportions of P. gracilis and P.
2007). Tangle nets and SCUBA diving are the fishing
inflatus observed in commercial catches during the
methods utilized in the south of this region of the
fishing season or annually is due to their different
behaviors and the meteorological conditions related to Pacific Ocean and are associated with the different
the habitat occupied by each species. In this study, we proportions of these species obtained in the
observed that the fishermen set their nets close to the commercial catches. Briones-Fourzn & Lozano-
coast over rocky bottoms, the preferred habitat of P. lvarez (1992) and Valadez-Manzano et al. (2003)
inflatus (0.5-8.0 m depth), during periods of calm suggested that this pattern is related to the habitats of
Population structure of Panulirus gracilis 231

Table 3. Monthly mean size, standard deviation and size range whole and by sex of the total weight (W, in g), Panulirus
gracilis, during 1989-1990 and 1990-1991 fishing seasons in the lower part of the Gulf of California, Mexico.
Tabla 3. Nmero de hembras y machos de Panulirus gracilis e intervalos de talla, medias y desviaciones estndar
mensuales del peso total (W, en g), durante las temporadas de pesca 1989-1990 y 1990-1991 en la parte baja del golfo de
California, Mxico.

Fishing season 1989-1990


Total Males Females
Month n W n Range W n Range W
X SD W (g) X SD W (g) X SD
Sep 132 355.0 85.1 100 205-780 338.2 73.8 32 220-630 407.4 97.3
Oct 143 369.7 87.3 105 230-590 345.1 61.8 38 230-695 437.8 109.9
Nov 158 377.4 115.1 93 175-1075 361.7 102.5 65 230-795 399.9 128.6
Dec 168 395.3 114.3 90 195-755 394.2 104.5 78 165-700 396.6 125.3
Jan 142 405.5 102.7 72 220-630 402.4 94.3 70 200-790 408.6 111.4
Feb 125 410.4 106.0 66 205-655 427.7 98.6 59 220-695 391.0 111.4
Mar 178 378.2 116.5 67 84-960 388.7 150.7 111 135-720 371.9 90.2
Apr 267 414.3 113.4 87 150-960 426.4 139.2 180 230-735 408.4 98.5
May 272 396.6 139.8 69 47-730 317.3 142.6 203 105-840 423.6 128.5

Fishing season 1990-1991


Total Males Females
Month n W n Range W n Range W
X SD W (g) X SD W (g) X SD

Sep 46 413.5 119.5 34 200-780 407.1 114.6 12 205-650 431.7 136.1


Oct 168 421.4 123.2 99 75-850 417.3 105.7 69 175-975 427.1 145.3
Nov 153 390.9 75.1 98 280-550 388.1 62.6 55 270-725 396.0 93.7
Jan 261 365.1 106.2 146 105-730 360.3 111.6 115 195-860 371.1 99.0
Feb 237 377.8 112.4 108 110-850 360.9 110.5 129 120-770 391.9 112.5
Mar 278 400.7 104.6 94 240-870 401.9 110.9 184 270-725 400.2 101.5
Apr 176 364.5 110.7 32 90-870 318.1 171.3 144 100-640 374.8 89.7
May 190 341.0 133.1 49 130-860 300.6 150.4 141 140-790 355.0 124.1

each species. These authors indicated that fishermen Size distribution


deployed their nets on the type of bottom where P. The modal size of P. gracilis landed in this study (75
gracilis is more abundant to select for this species, mm CL) during the 1989-1990 and 1990-1991 fishing
whereas divers prefer rocky bottoms, where visibility seasons was smaller than that reported by Salazar-
is better, thus obtaining larger proportions of P. Navarro (2000) (85 mm CL) but similar to that
inflatus. recorded by Prez-Gonzlez et al. (1992a) and Flores-
Additionally, Prez-Gonzlez et al. (2002b) Campaa et al. (1993). However, the mean size found
reported that the abundance of P. gracilis and P. contrasts with other studies performed in study area or
inflatus varies as a function of depth. In the study area in adjacent zones. For example, during the 1977
(see Fig. 1), the bottoms are rocky between 0.5 and fishing season, the mean sizes were higher than the
10-15 m and gravel-sandy from 12-15 to 35-40 m. minimum legal size (MLS) of 82.0 mm CL, with the
Therefore, P. inflatus is found inshore (0.5-15 m catchable stock in the range of 75.0-110 mm CL
depth), whereas the abundance of the P. gracilis (Wiedfeldt, 1997), whereas, beginning in the early
increases with depth. The two species coexist in a 1980s, the mean sizes have been lower that the MLS.
similar proportion at depths between eight to Prez-Gonzlez (1986), Quintero-Montoya (1999) and
approximately 18 m. Valadez-Manzano et al. (2003) recorded mean sizes of
232 Lat. Am. J. Aquat. Res.

72.0 < 70 and 70 mm CL during the 1983-1984, 1996- more catchable than smaller males (e.g., Tremblay &
1997/1997-1998 and 2001-2002 fishing seasons, Smith, 2001; Ziegler et al., 2002).
respectively. The seasonal disparity in the sex ratio of P. gracilis
Prez-Gonzlez et al. (2002a) reported that, as a has been associated with the differential male and
consequence of the high fishing mortality in sublegal female movements associated with their reproductive
sizes, the stock-turnover rate has increased, with an activity, which occurs in summer and autumn (Prez-
equivalent decrease in the age at first maturity and an Gonzlez et al., 1992b; Briones-Fourzn & Lozano-
increase in mean fecundity, suggesting a low rate of lvarez, 1992; Arzola-Gonzlez et al., 2007). This
compliance with fishery regulations due to a lack of timing of the main reproductive period in P. gracilis is
strict enforcement. Fishing pressure on sublegal sizes evidenced by the higher abundance of larvae
of the spiny lobsters P. gracilis and P. inflatus, phyllosoma found in the study area from June to
including a high proportion of immature individuals, October (Muoz-Garca et al., 2000, 2004), as well as
has increased since the early 1990s. Similarly, in the by the observations of a higher value of the
present study, we observed that ovigerous females gonadosomatic index and the most females with
were also being captured. mature gonads during these months (Puga-Lpez,
2004).
Yallonardo et al. (2002) did not find changes in the
size frequency in the spiny lobster P. guttatus between The catch rates of male lobsters were higher during
1986-1988 and 1998-99, suggesting that fishing the reproductive period (summer and autumn) than
pressure on this resource had not yet been increased to those of females, which were more abundant during
the point that it negatively affected the size structure spring (the nonreproductive period). After mating and
of the population. Montgomery (1995) and Padilla- oviposition, the bulk of the female population is
Ramos & Briones-Fourzn (1997) indicated that the expected to migrate to deeper waters during egg
fishing locality and/or pattern of movement of lobsters development and to return to inshore areas prior to egg
along the shore could be additional factors influencing hatching. This suggests that P. gracilis females are
the size composition of the catch and should be taken less catchable than males during their reproductive
into account when analyzing the mean monthly size of period because the bulk of the female population
the catch. probably migrates to deeper waters and/or presents
decreased activity. This pattern of movement of the
Sex ratio females toward deeper waters has been observed in P.
argus in the northern Caribbean and Bahamas
As found in the present study, a P. gracilis sex ratio
(Herrnkind, 1980, 1985; Kanciruk, 1980), south of
close to unity has been reported by Weinborn (1977);
Florida (Gregory & Labisky, 1986), on the continental
Briones et al. (1981); Prez-Gonzlez et al. (1992b);
shelf of the Quintana Roo, Mexico (Lozano-lvarez et
Flores-Campaa et al. (1993) and Salazar-Navarro
al., 1991), and in the northwest islands of the Cape
(2000). However, Arzola-Gonzlez et al. (2007) found
Verde Archipelago (east-central Atlantic) (Freitas &
that the sex ratio favored males over females in the
Castro, 2005); it has also been observed in P. ornatus
1995 (2.6:1), 1996 (1.6:1) and 1997 (2.4:1) fishing
in the Gulf of Papua (Bell et al., 1987, Pitcher et al.,
seasons.
1992), in P. guttatus on the Caribbean coast of Mexico
MacDiarmid & Sainte-Marie (2006) suggested that (Padilla-Ramos & Briones-Fourzn, 1997), and in
many fisheries appear to have the potential to alter Palinurus elephas in the western region of the
population sex ratio and sexual size dimorphism, and Mediterranean Sea (Goi et al., 2001).
they noted a number of factors that could result in sex-
biased exploitation. For example, one sex may be Panulirus inflatus presents similar patterns of
more vulnerable to capture due to its greater spatial reproductive activity and male and female movements
and/or temporal exposure to fishing gear. Goi et al. related to mating, oviposition, egg development and
(2001) reported that the scarcity of males in February egg hatching (Prez-Gonzlez et al., 1992b, Briones-
may indicate a substantial sex segregation of the Fourzn & Lozano-lvarez, 1992; Arzola-Gonzlez et
Palinurus elephas population at this time, but the al., 2007). This species coexists with P. gracilis along
presence of recent postmolt males in the samples also the Mexican Pacific coast and in the lower part of the
suggested reduced activity and, thus, catchability, Gulf of California.
related to ecdysis. A decrease of approximately 70% Kanciruk (1980) indicated that differences between
in catchability has been estimated for late-postmolt male and female movements appear to cause these
Panulirus argus (Lipcius & Herrnkind, 1982) and P. unbalanced sex ratios in a number of other spiny
cygnus (Morgan, 1974). In several species, males are lobster species. Maturing adults of most well-studied
more catchable than females, and larger males are palinurid species exhibit either an incremental
Population structure of Panulirus gracilis 233

ontogenetic migration that culminates in mating and northeast coast of Queensland. Aust. J. Mar.
spawning in distinct adult habitats or seasonal inshore- Freshwat. Res., 38: 197-210.
offshore movements for mating or foraging (Butler et Briones-Fourzn, P. 1991. Consideraciones para el
al., 2006). manejo de Panulirus guttatus (Latreille) en Quintana
There are other factors that could result in sex- Roo, Mxico. In: P. Briones-Fourzn (ed.). Memorias
biased exploitation. For example, the male-skewed sex del Taller Regional sobre Manejo de la Pesquera de
ratio observed for P. guttatus (Losada-Tosteson et al., Langostas. Universidad Nacional Autnoma de
2001) has been associated with the method of capture Mxico/Secretara de Pesca, Mxico, pp. 81-89.
(traps vs handpicking, Briones-Fourzn, 1991), lower
Briones-Fourzn, P. & G. Contreras-Ortiz. 1999.
catchability (Evans & Lockwood, 1994), differential
male and female movements associated with their Reproduction of the spiny lobster, Panulirus guttatus
reproductive activity (Briones-Fourzn & Contreras- (Decapoda: Palinuridae), on the Caribbean coast of
Ortiz, 1999), and lower abundance due to differential Mexico. J. Crust. Biol., 19: 171-179.
mortality (Evans et al., 1995; Sharp et al., 1997). Briones-Fourzn, P. & E. Lozano-lvarez. 1992. Aspects
Furthermore, Losada-Tosteson et al. (2001) indicated of the reproduction of Panulirus inflatus (Bouvier)
that the evolutionary mechanics of skewed sex ratios and P. gracilis Streets (Decapoda: Palinuridae) from
in P. guttatus, if they exist, require further study. the Pacific coast of the Mexico. J. Crust. Biol., 12(1):
Thus, obtaining information on the quantity and 41-50.
size composition of individuals harvested and changes Briones, P., E. Lozano, A. Martnez & A.S. Cortes. 1981.
in the abundance of species is fundamental for the Aspectos generales de la biologa y pesca de las
effective management of fishery resources. Such data langostas en Zihuatanejo, Gro., Mxico (Crustacea:
provide knowledge about the impact of harvesting on Palinuridae). An. Inst. Cienc. Mar Limnol., Univ.
the population and on the temporal and spatial Nac. Autn. Mxico, 8(1): 79-102.
distributions of individuals of different sizes
(Montgomery, 1995). For this reason, periodic Butler, J.A. & N.L. Pease. 1965. Spiny lobster
evaluations of the lobster fishery should be conducted explorations in the Pacific and Caribbean waters of
to improve monitoring of the status of this fishery on the Republic of Panama. U.S. Fish and Wildlife
the Mexican Pacific and Gulf of California coasts. Serv., Special Scient. Rep. Fish., 505: 1-26.
Butler, M.J., R.S. Steneck & W.F. Herrnkind. 2006.
Juvenile and adult ecology. In: B.F. Phillips (ed.).
ACKNOWLEDGEMENTS
Lobster: biology, management, aquaculture and
The author thanks Luis M. Valadez and Martn I. fisheries. Blackwell Publishing, Ames, Iowa, pp. 263-
Borrego for their help in field (sampling) activities. 309.
Commercial samples were obtained from catches of Evans, C.R. & A.P.M. Lockwood. 1994. Population field
the Sociedades Cooperativas Punta Tiburn and studies of the guinea chick lobster Panulirus guttatus
Jos Mara Canizalez. This project was supported by (Latreille) at Bermuda: abundance, catchability, and
the Secretara de Educacin Pblica, Mxico. behaviour. J. Shellfish Res., 13: 393-415.
Evans, C.R., A.P.M. Lockwood, A.J. Evans & E. Free.
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Received: 27 May 2008; Accepted: 25 April 2011


Lat. Am. J. Aquat. Res., 39(2): 236-249, 2011 Lat. Am. J. Aquat. Res. 236
DOI: 10.3856/vol39-issue2-fulltext-5

Research Article

Distribucin del ictioplancton en la Patagonia austral de Chile: potenciales efectos


del deshielo de Campos de Hielo Sur

Mauricio F. Landaeta1,, Claudia A. Bustos2, Pamela Palacios-Fuentes1, Pablo Rojas3 &


Fernando Balbontn1
1
Facultad de Ciencias del Mar y de Recursos Naturales, Universidad de Valparaso
P.O. Box 580, Reaca, Via del Mar, Chile
2
Programa Doctorado en Acuicultura, Universidad Catlica del Norte, P.O. Box 117, Coquimbo, Chile
3
Divisin de Investigacin en Acuicultura, Centro de Maricultura Hueihue
Instituto de Fomento Pesquero, Ancud, Chile

RESUMEN. Durante octubre-noviembre de 2009 se realiz un crucero oceanogrfico entre 50 y 53S de


Chile austral, en las cercanas del glaciar Campos de Hielo Sur. Las estaciones cercanas al glaciar presentaron
baja temperatura (1-3C) y salinidad (< 25), y alta estabilidad (frecuencia de Brunt-Visl N > 0,1 ciclos s-1).
Los principales taxa del ictioplancton fueron huevos y larvas de sardina fueguina Sprattus fuegensis, pez hacha
Maurolicus parvipinnis, Macrouridae y merluza austral Merluccius australis. El desove principal de S.
fuegensis (~ 8000 huevos 10 m-2) ocurri en zonas mezcladas de la plataforma continental adyacente, mientras
que el desove de M. parvipinnis ocurri en canales intermedios asociado a valores intermedios de estabilidad
(N~0,06 ciclos s-1). Se observ una nula o baja abundancia de huevos y larvas de peces en las cercanas del
glaciar, y la abundancia de huevos de M. parvipinnis estuvo relacionada positivamente con la temperatura y
salinidad de la columna de agua y negativamente con la estabilidad de la columna de agua. Adems, hubo una
relacin negativa entre la densidad del agua de mar y el dimetro de los huevos de S. fuegensis. La relacin
entre deshielo e ictioplancton podra tener consecuencias en el transporte advectivo y mortalidad masiva de
huevos y larvas de peces y el acople pelgico-bentnico en la Patagonia austral de Chile. Como el cambio
climtico global ha incrementado los deshielos de glaciares en latitudes altas, y el aumento del ingreso de
aguas de baja temperatura y salinidad podra tener consecuencias en el ictioplancton de la Patagonia chilena.
Palabras clave: estratificacin, distribucin, ictioplancton, Campo de Hielo Sur, sur de Chile.

Ichthyoplankton distribution in South Patagonia, Chile: potential effects of ice


melting from the Southern Ice Field

ABSTRACT. In October-November 2009, an oceanographic survey was carried out between 50 and 53S off
southern Chile, near the Southern Ice Field. The stations near the glacier showed low temperatures (1-3C) and
salinity (< 25), and high stability (Brunt-Visl frequency N > 0.1 cycles s-1). Main ichthyoplankton taxa
were eggs and larvae of southern sprat Sprattus fuegensis, lightfish Maurolicus parvipinnis, Macrouridae, and
southern hake Merluccius australis. The main spawning area of S. fuegensis (~8000 eggs 10 m-2) occurred in
mixed zones of the adjacent continental shelf, whereas the spawning of M. parvipinnis occurred in
intermediate channels associated with medium stability values (N~0.06 cycles s-1). Fish egg and larval
abundances were null or scarce near the glacier, and the abundance of M. parvipinnis eggs was positively
related to the temperature and salinity of the water column, and negatively related to water column stability.
Moreover, a negative relationship was observed between seawater density and the diameter of S. fuegensis
eggs. The relation between ice melting and ichthyoplankton may have consequences for advective transport
and mass mortality of fish eggs and larvae, as well as pelagic-benthic coupling in the Chilean South Patagonia.
Global climate change has increased glacier ice melting at high latitudes, and the increased entry of colder,
less saline waters in coastal areas may have consequences for the ichthyoplankton in the Chilean Patagonia.
Keywords: stratification, distribution, ichthyoplankton, Southern Ice Field, southern Chile.

___________________
Corresponding author: Mauricio F. Landaeta (mauricio.landaeta@uv.cl)
237 Deshielos y distribucin de ictioplancton en la Patagonia, Chile

INTRODUCCIN Castro, 2006b), recientemente, se ha detectado que en


zonas donde ocurren deshielos (i.e., baja temperatura
La zona sur austral de Chile (4130S-56S) se y salinidad), tanto la diversidad como la abundancia
caracteriza por presentar una geometra costera de huevos y larvas de peces es baja (Bustos et al.,
compleja, caracterizada por fiordos, islas, canales y 2010).
archipilagos, con una longitud de 1600 km y un rea Los deshielos de glaciares pueden causar
superficial de aproximadamente 240.000 km2 (Palma mortalidad masiva de zooplancton, particularmente
& Silva, 2004). A lo largo de esta zona tambin hay durante verano, con estimaciones de biomasa muerta
numerosos aportes de agua dulce, provenientes de de 0,17 gC m-2 (Wslawski & Legezyska, 1998). Los
descargas de ros de rgimen pluvial, nival y mixto mecanismos que generan mortalidad asociados a una
(Dvila et al., 2002), de lluvias (2000-5000 mm ao-1, fuente de agua dulce se deben a la incapacidad del
Strub et al., 1998) y deshielos de glaciares, que zooplancton de evadir el agua de baja salinidad por la
generan una capa superficial de agua de baja densidad mezcla turbulenta y morir por estrs osmtico
con una fuerte picnoclina a aproximadamente 20-30 m (Kaartvedt & Aksnes, 1992; Eiane & Daase, 2002).
de profundidad y una capa profunda de mayor Por lo tanto, es posible hipotetizar que la distribucin
densidad. Como consecuencia de esto, el sistema se espacial y la abundancia de estados tempranos de
comporta como un estuario, con una capa superficial peces para aquellas especies que usan esta rea como
de mayor velocidad que se mueve hacia fuera de la zona de desove y crianza larval temprana podran ser
costa y una capa profunda que ingresa al sistema con afectados por los deshielos de Campo de Hielo Sur en
menor velocidad (Silva et al., 1997). la zona austral de Chile (50-53S). El objetivo del
Este sistema estuarino presenta fuertes variaciones presente trabajo es establecer la distribucin espacial
estacionales en la incidencia de radiacin solar que del ictioplancton en la zona de influencia del glaciar
afectan significativamente la variabilidad de la Campos de Hielo Sur durante la poca de primavera
biomasa fitoplanctnica y la produccin primaria en la austral, relacionar la abundancia con variables
capa de mezcla (Iriarte et al., 2007), produciendo ambientales y sugerir posibles consecuencias del
cambios en la estructura del ecosistema desde una incremento del deshielo producto del cambio
clsica trama trfica pelgica en primavera a una climtico global en la Patagonia Chilena.
trama microbiana en invierno (Gonzlez et al., 2010).
Acoplado al aumento de fitoplancton coincide una
mayor actividad reproductiva en primavera de MATERIALES Y MTODOS
crustceos decpodos (Mujica & Medina, 2000;
Mujica & Nava, 2010) y peces marinos (Landaeta & Durante octubre y noviembre de 2009 se realiz un
Castro, 2006a; Landaeta et al., 2009), cuando se crucero oceanogrfico entre 5006S y 5245S a
presenta mayor oferta alimenticia y menor cantidad de bordo del buque cientfico AGOR Vidal Gormaz (Fig.
predadores gelatinosos (p.e., Chaetognatha, Sagitta 1), que comprendi el muestreo de 40 estaciones. En
spp., Eukrohnia hamata, Villenas et al., 2009). cada una de ellas se midieron las variables
hidrogrficas de la columna de agua con un CTD
Por otra parte, a lo largo de Chile austral ocurren
Seabird SB-19 desde la superficie hasta 500 m de
cambios en los aportes de agua dulce, que generan dos
profundidad o hasta 10 m por sobre el fondo. El
zonas de muy baja salinidad cerca de 44-46S (por
zooplancton fue capturado mediante lances doble
aportes de ros de alto caudal) y alrededor de 52-53S
oblicuos con una red Tucker trawl (1 m2 de boca,
(por efecto de deshielos, Dvila et al., 2002) y que no
mallas de 300 m de apertura), con sistema de dos
slo incrementan la estabilidad de la columna de agua,
redes y flujmetro para estimar el volumen filtrado de
sino que aumentan los gradientes verticales y
cada red. Una vez a bordo, las redes fueron lavadas y
horizontales de densidad. De esta forma ocurre
agregacin de partculas en estas zonas frontales, las muestras de los lances de bajada (p.e., 0-200 m)
desde parches de alimento planctnico (Landaeta & fueron preservadas en formalina al 4% tamponeada
Castro, 2006b) hasta macroalgas flotando a la deriva con borato de sodio, y las muestras de los lances de
(i.e., Macrocystis pyrifera y Durvillaea antarctica, subida (p.e., 200-0 m) fueron fijados con etanol al
Hinojosa et al., 2010). Aunque se han postulado 75%, para anlisis de otolitos (no incluidos). Los
relaciones positivas significativas entre la abundancia volmenes filtrados variaron entre 22,74 y 897,20 m3
de estados tempranos de peces y la estabilidad en la lance-1 (promedio desviacin estndar, 221,94
zona norte de la Patagonia Chilena (Bustos et al., 150,94 m3 lance-1).
2007, 2008a, 2008b), que podran tener consecuencias En laboratorio, se separaron los huevos y larvas de
positivas para la alimentacin larval (Landaeta & peces de las muestras preservadas en formalina. El
Lat. Am. J. Aquat. Res. 238

Figura 1. Zona de estudio, indicando la posicin de las estaciones de muestreo y transectas.


Figure 1. Study area, showing location of sampling stations and transects.

ictioplancton fue identificado hasta el nivel Con la informacin del CTD, se calcul como
taxonmico ms bajo posible basado en las estimador de la estabilidad de la columna de agua para
descripciones de Ciechomski (1971); Moser (1996); cada una de las estaciones oceanogrficas, la
Balbontn et al. (2004); Uribe & Balbontn (2005); frecuencia de Brunt-Visl (N = [(g/) x (/z)]1/2),
Bustos & Landaeta (2005) y Landaeta et al. (2008). donde g es la gravedad (9,8 m s-2), es la densidad del
Los huevos fueron contados y separados en tres agua de mar, y z es la profundidad, que es la
estados: (a) estado I, sin embrin, (b) estado II, con frecuencia a la cual oscilar una partcula desplazada
embrin temprano y (c) estado III, pre-eclosin. Se verticalmente dentro de un ambiente estticamente
tomaron aleatoriamente huevos de sardina fueguina estable.
Sprattus fuegensis para medir su dimetro. Se Se realizaron regresiones lineales simples por
realizaron tres medidas de dimetro de cada huevo - mnimos cuadrados entre las variables ambientales
independiente de su estado de desarrollo- bajo una (temperatura, salinidad, estabilidad), el dimetro de
lupa estereomicroscpica Olympus SZ-61 con cmara los huevos de S. fuegensis y la abundancia
digital Moticam 2000 (2.0M Pxel), usando el estandarizada de huevos y larvas de algunos taxa
software Motic Images Plus 2.0 y se calcul el seleccionadas, calculando el 95% de intervalo de
promedio de las tres mediciones de tamao de cada confianza de los modelos lineales. Los valores de
huevo. Se comprob la normalidad de los datos de temperatura y salinidad correspondieron al promedio
tamao de los huevos con una prueba de Shapiro- de los datos recolectados por el CTD en la columna de
Wilks. La abundancia de huevos y larvas de peces fue agua muestreada por la red. El valor de estabilidad
estandarizada en individuos por 10 m2 (ind 10 m-2). corresponde al valor mximo obtenido en la columna
239 Deshielos y distribucin de ictioplancton en la Patagonia, Chile

de agua de cada una de las estaciones oceanogrficas. Para el rea y periodo de estudio hubo una relacin
Los valores de abundancia del ictioplancton y significativa entre la temperatura promedio de la
frecuencia de Brunt-Visl fueron transformados con columna de agua muestreada y el valor mximo
logaritmo en base 10. estimado de la frecuencia de Brunt-Visl (F = 15,88;
Para investigar la relacin entre las variables g.l. 1, 33; P < 0,001), al igual que con la salinidad (F =
oceanogrficas con la abundancia del ictioplancton se 6,72; g.l. 1, 33; P = 0,014). Es decir, las zonas que
utiliz el Anlisis de Componentes Principales (ACP) presentaron baja temperatura y baja salinidad (i.e.,
(Jongmann et al., 1995). Este anlisis permite zonas de deshielo) fueron altamente estables, y por
identificar un mnimo de componentes funcionales tanto, N es un buen estimador del efecto de deshielo
(variables oceanogrficas) que pueden explicar la en la zona de estudio.
distribucin de las variables dependientes (huevos y
larvas de peces). Adicionalmente, se utiliz la prueba Composicin y distribucin del ictioplancton
de correlacin R de Spearman (Hays, 1981) para Durante el crucero oceanogrfico realizado en
investigar la relacin entre las diferentes variables primavera de 2009 se recolect un total de 5511
oceanogrficas con la abundancia de larvas y huevos huevos y 676 larvas de peces, correspondientes a 22 y
de las diferentes taxa.
19 taxa, respectivamente (Tablas 2 y 3). Los huevos
de sardina fueguina Sprattus fuegensis y el pez hacha
RESULTADOS Maurolicus parvipinnis fueron los ms importantes
durante el periodo de estudio, con 64,6 y 28,1% de
Caractersticas hidrolgicas y estabilidad de la dominancia, respectivamente. Otros taxa importantes
columna de agua en el rea de estudio fueron los huevos de merluza
Las condiciones hidrolgicas de la columna de agua austral Merluccius australis, pejerrata (familia
en la zona de estudio estuvieron influidas por los Macrouridae) y lenguado austral (Hippoglossina sp.,
deshielos del glaciar Campos de Hielo Sur (CHS) probablemente H. mystacium) (Tabla 2). Entre las
(Tabla 1, Figs. 2 y 3). Se detectaron bajas larvas de peces, los taxa ms importantes fueron M.
temperaturas (1,4C) y bajas salinidades (14,62) en las parvipinnis, S. fuegensis, Bathylagichthys parini,
cercanas al glaciar, generando aguas de baja densidad Macrouridae, Sebastes oculatus y M. australis (Tabla
del agua (t = 11,47 kg m-3) y alta estabilidad de la 3). Cabe destacar la recoleccin por primera vez en
columna de agua (0,16 ciclos s-1) (Tabla 1). aguas chilenas de una postlarva de 12,4 mm de
Espacialmente, se observ que en el seno Europa Psychrolutes marmoratus (Psychrolutidae), carac-
ocurri una inversin trmica entre 5 a 20 m de terizada por un cuerpo globoso, fuertemente pig-
profundidad, con aguas de baja temperatura (1-3C) y mentado, con presencia de estructuras espinosas en la
baja salinidad (< 25) provenientes de deshielos de zona frontal de la cabeza, supraocular y dorsalmente a
CHS, y un gradiente horizontal de densidad entre seno la altura de la insercin de la aleta pectoral1.
Europa y canal Concepcin. Esto provoc una Los huevos recientemente desovados (estado I) de
columna de agua altamente estratificada y estable en S. fuegensis fueron recolectados a lo largo del canal
los primeros 40 m de la columna de agua del seno Concepcin y en la plataforma continental adyacente,
Europa, con valores de frecuencia de Brunt-Visl a lo largo del estero Las Montaas (que no tiene
mayores a 0,1 ciclos s-1 (Fig. 2). En cambio, en la boca conectividad con CHS) y en el golfo Almirante Montt
del canal Concepcin y en la plataforma continental (Fig. 4). Los huevos ms desarrollados y las larvas se
adyacente, se detectaron valores de temperatura > 8C, recolectaron en estas mismas reas, destacando las
salinidad > 31 y una columna de agua altamente mayores abundancias (~8000 huevos 10 m-2) sobre la
mezclada (N < 0,025 ciclos s-1) (Fig. 2). plataforma continental y su ausencia en las estaciones
En el golfo Almirante Montt, con cierta influencia ms cercanas al glaciar. Se detectaron bajas
de CHS, se detectaron aguas de baja temperatura abundancias (< 100 ind 10 m-2) de huevos y larvas en
(~7C), salinidad (< 25), densidad (< 20 kg m-3) y las cercanas del Estrecho de Magallanes (Fig. 4). Un
mayor estabilidad (N > 0,025 ciclos s-1) (Fig. 3). Se patrn totalmente diferente present la distribucin
observ que el Paso M. Vicua, una morrena que espacial de los estados tempranos del pez hacha M.
reduce la profundidad mxima a ~55 m, impidi la parvipinnis. En general, los canales (Concepcin,
intrusin de aguas de origen ocenico (> 8C, > 31, > Sarmiento, Unin, Smyth) fueron utilizados como
24 kg m-3) al interior del golfo Almirante Montt.
Adems, a lo largo de los canales Smyth y Unin (Fig.
1
1), la picnoclina y la mayor estabilidad se encontraron http://ictioplanctonenchile.blogspot.com/2010/05/postlarva-
aproximadamente a 50 m de profundidad (Fig. 3). de-psychrolutidae.html
Lat. Am. J. Aquat. Res. 240

Tabla 1. Resumen de las condiciones hidrogrficas presentes durante el crucero CIMAR 15 en octubre-noviembre de
2009.
Table 1. Summary of hydrographic conditions found during the cruise CIMAR 15 in October-November 2009.

Temperatura (C) Salinidad t (kg m-3) Brunt-Visl (ciclos s-1)


Mnimo 1,428 14,626 11,479 0
Mximo 9,472 33,484 26,073 0,165
Promedio 8,260 31,586 24,549 0,012
Desviacin estndar 0,861 3,148 2,386 0,013
Mediana 8,595 33,017 25,595 0,007

Figura 2. Secciones verticales de condiciones oceanogrficas de la transecta con lnea continua indicada en la Figura 1.
Los puntos indican los datos extrados de los lances de CTD.
Figure 2. Vertical sections of oceanographic conditions of continuos line transect showed in Figure 1. Dots correspond to
data from CTD casts.

zonas de desove (Fig. 5), con abundancias totales de (n = 127), con distribucin normal de los dimetros
los huevos entre 40 y 897 huevos 10 m-2 (Tabla 2), y (prueba de Shapiro-Wilks, W = 0,992, P = 0,719)
con una distribucin espacial similar de las larvas. La (Fig. 6a). Los huevos de mayor tamao (> 1,25 mm)
abundancia fluctu entre 3 y 293 larvas 10 m-2 (Tabla fueron recolectados en aguas de menor temperatura (<
3). No obstante, en las estaciones ms cercanas al 7C) y salinidad (< 21), producto de los deshielos, que
glaciar no se detectaron huevos de esta especie y se generaron aguas de baja densidad (t = 16-17 kg m-3,
recolectaron bajas densidades (0-13 ind 10 m-2) de Fig. 6b). De hecho, el dimetro de los huevos de S.
larvas de M. parvipinnis (Fig. 5). fuegensis tuvo una relacin negativa y significativa (P
Aguas de deshielo y su relacin con el ictioplancton < 0,001) con la densidad del agua de mar (Fig. 6b).
Los huevos de sardina fueguina presentaron un rango De los otros componentes del ictioplancton, slo la
amplio de tamaos, variando entre 0,922 y 1,361 mm abundancia de los huevos del pez hacha Maurolicus
241 Deshielos y distribucin de ictioplancton en la Patagonia, Chile

Figura 3. Secciones verticales de condiciones oceanogrficas de la transecta con lnea segmentada indicada en la Figura
1. Los puntos indican los datos extrados de los lances de CTD.
Figure 3. Vertical sections of oceanographic conditions of dotted line transect showed in Figure 1. Dots correspond to
data from CTD casts.

Tabla 2. Composicin y abundancia (ind 10 m-2) de huevos de peces capturados durante primavera de 2009. DE:
desviacin estndar. Dominancia es el porcentaje de abundancia del taxon con respecto a la abundancia total. Ocurrencia
es el porcentaje de estaciones oceanogrficas con presencia positiva del taxon con respecto al total de estaciones
muestreadas.
Table 2. Composition and abundance (ind 10 m-2) of fish eggs collected in spring 2009. DE: standard deviation.
Dominance is the percentage of taxon abundance in relation to the whole abundance. Occurrence is the percentage of
oceanographic stations with positive presence of taxon respective to total sampled stations.

Taxa Media DE Mediana Dominancia Ocurrencia Rango de abundancia


(%) (%)
Sprattus fueguensis 946,60 2613,10 21,54 64,60 45,00 2,23 - 8163,38
Maurolicus parvipinnis 246,70 267,90 126,85 28,06 75,00 8,34 - 897,03
Merluccius australis 63,07 165,89 11,94 3,35 35,00 2,23 - 634,81
Normanichthys crockeri 15,87 - 15,87 0,06 2,50 15,87
Genypterus blacodes 7,47 0,51 7,54 0,08 7,50 6,93 - 7,94
Macroronus magellanicus 6,47 1,80 6,47 0,05 5,00 5,19 - 7,75
Lampanyctodes hectoris 4,46 - 4,46 0,02 2,50 4,46
Prolatilus jugularis 3,11 - 3,11 0,01 2,50 3,11
Hippoglossina sp. 25,98 22,56 24,02 0,30 7,50 4,46 - 49,45
Macrouridae 26,18 36,77 12,01 1,29 32,50 3,40 - 118,83
Pinguipedidae 6,18 - 6,18 0,02 2,50 6,18
Huevos no identificados 21,12 45,38 11,84 2,16 67,50 2,22 - 243,84
Lat. Am. J. Aquat. Res. 242

Tabla 3. Composicin y abundancia (ind 10 m-2) de larvas de peces capturadas durante primavera de 2009. DE:
desviacin estndar. Dominancia es el porcentaje de abundancia del taxon con respecto a la abundancia total. Ocurrencia
es el porcentaje de estaciones oceanogrficas con presencia positiva del taxn con respecto al total de estaciones
muestreadas.
Table 3. Composition and abundance (ind 10 m-2) of fish larvae collected in spring 2009. DE: standard deviation.
Dominance is the percentage of taxon abundance in relation to the whole abundance. Occurrence is the percentage of
oceanographic stations with positive presence of taxon respective to total sampled stations.

Taxa Media DE Mediana Dominancia Ocurrencia Rango de abundancia


(%) (%)
Sprattus fuegensis 54,61 70,19 23,39 18,09 42,50 3,77 - 249,40
Bathylagichthys parini 53,91 75,41 15,09 17,86 42,50 5,68 - 222,79
Maurolicus parvipinnis 66,06 69,59 44,56 42,47 82,50 3,11 - 293,72
Merluccius australis 17,75 19,28 9,21 4,15 30,00 5,19 - 73,35
Macruronus magellanicus 24,02 - 24,02 0,47 2,50 24,02
Macrouridae 23,38 25,55 12,01 5,01 27,50 3,11 - 89,12
Genypterus blacodes 19,78 13,48 19,11 1,54 10,00 7,52 - 33,36
Cataetyx messieri 9,85 2,13 9,85 0,38 5,00 8,34 - 11,35
Sebastes oculatus 15,63 16,92 11,78 4,87 40,00 4,97 - 74,18
Helicolenus lenguerichi 3,11 - 3,11 0,06 2,50 3,11
Agonopsis chiloensis 3,11 - 3,11 0,06 2,50 3,11
Leptonotus blainvilleanus 10,16 - 10,16 0,20 2,50 10,16
Psychrolutes marmoratus 3,78 - 3,78 0,07 2,50 3,78
Notothenia sp. 1 9,49 5,43 9,33 0,92 12,50 3,78 - 17,03
Notothenia sp. 2 8,85 0,90 8,89 0,52 7,50 7,94 - 9,73
Seriolella caerulea 7,56 6,29 7,56 0,29 5,00 3,11 - 12,01
Sp. A 6,18 - 6,18 0,12 2,50 6,18
Sp. B 5,32 0,50 5,32 0,21 5,00 4,97 - 5,68
Sp. C 6,93 - 6,93 0,14 2,50 6,93
No identificado 16,45 13,20 14,14 2,57 20,00 5,29 - 44,28

parvipinnis se relacion significativamente con las por el 63% de las estaciones se asoci positivamente
variables ambientales de la columna de agua (Fig. 7). con valores intermedios de estabilidad vertical (~ 0,06
Se encontr una reduccin significativa de la ciclos s-1) de la columna de agua. Una importante
abundancia de sus huevos en zonas con menor proporcin de la abundancia total del ictioplancton
temperatura (relacin positiva, Fig. 7a, P = 0,0060), (34% huevos; 51% larvas) se concentr en este grupo.
menor salinidad (relacin positiva, Fig. 7b, P = Un segundo conjunto, compuesto por diez estaciones
0,0007) y mayor estabilidad de la columna de agua (25%) se asoci negativamente con valores de
(relacin negativa, Fig. 7c, P = 0,0063), correspon- temperatura del mar cercanos a 7C. A diferencia del
dientes a las estaciones cercanas a CHS. grupo anterior, ste congreg la mayor abundancia de
Los dos primeros componentes principales (ACP) huevos de peces (66%) y, a un 47% del total de larvas
explicaron el 70% de la varianza. La contribucin de de peces. Finalmente, el tercer grupo compuesto por
las estaciones con mayor abundancia de ictioplancton cuatro estaciones (10%) se asoci positivamente con
con las variables oceanogrficas de los dos primeros valores de densidad del mar cercanos a 23 kg m-3. Esta
componentes fue utilizada para realizar asociaciones agrupacin slo represent a un 2% de la abundancia
estadsticas entre ambos tipos de variables. Se total de larvas y, menos del 1% de la abundancia total
detectaron tres tipos de asociaciones entre las de huevos de peces (Fig. 8).
diferentes estaciones de muestreo y las variables El anlisis de correlacin R de Spearman realizado
oceanogrficas (Fig. 8). El primer grupo compuesto con las larvas de peces, mostr relaciones positivas
243 Deshielos y distribucin de ictioplancton en la Patagonia, Chile

Figura 4. Distribucin espacial de huevos por estado de desarrollo y larvas de sardina fueguina Sprattus fuegensis durante
primavera de 2009. Abundancia estandarizada a ind 10 m-2.
Figura 4. Spatial distribution of eggs by developmental stage and larval southern sprat Sprattus fuegensis during austral
spring 2009. Standardised abundance in ind 10 m-2.

estadsticamente significativas con un bajo coeficiente estadios tempranos de B. parini (Bathylagidae)


de correlacin (r = ~ 0,4) entre los estadios tempranos mostraron relaciones positivas significativas con la
de M. parvipinnis y las condiciones hidrolgicas de la frecuencia de Brunt-Visl. Finalmente, el total de
columna de agua (Tabla 4). Las larvas de Seriolella larvas de peces mostr relaciones positivas
caerulea (cojinoba del sur) presentaron relaciones significativas con un bajo coeficiente de correlacin (r
positivas significativas con la salinidad y densidad de = ~0,4) slo con valores de temperatura, salinidad y
la columna de agua. Cabe destacar que solo los densidad (Tabla 4).
Lat. Am. J. Aquat. Res. 244

Figura 5. Distribucin espacial de huevos por estado de desarrollo y larvas de pez hacha Maurolicus parvipinnis durante
primavera de 2009. Abundancia estandarizada en ind 10 m-2.
Figura 5. Spatial distribution of eggs by developmental stage and larval lightfish Maurolicus parvipinnis during austral
spring 2009. Standardised abundance in ind 10 m-2.

Para los huevos de peces, el anlisis de correlacin significativas con las variables fsicas, al igual que el
mostr relaciones positivas significativas entre los total de huevos colectados en el ara de estudio (Tabla
huevos de Hippoglossina sp. y M. parvipinnis con 4).
valores de temperatura, salinidad y densidad de la
DISCUSIN
columna de agua. Los huevos de merluza austral (M.
australis) mostraron relaciones positivas con un bajo El anlisis del ictioplancton presente en la zona sur
coeficiente de correlacin (r = ~0,3) con los valores de austral de Chile cercana a uno de los glaciares ms
salinidad y densidad. Los huevos de peces de la grandes del Hemisferio Sur, permiti establecer que
familia Macrouridae mostraron relaciones positivas en primavera de 2009 las aguas de baja temperatura y
245 Deshielos y distribucin de ictioplancton en la Patagonia, Chile

Figura 6. a) Histograma de tamao de huevos (mm) de


sardina fueguina Sprattus fuegensis. b) Regresin lineal
entre dimetro (mm) de huevos de S. fuegensis y t (kg
m-3). Las lneas punteadas corresponden al intervalo de
confianza del 95%.
Figure 6. a) Histogram of southern sprat Sprattus
fuegensis egg size (mm). b) Linear regression between S.
fuegensis egg diameter (mm) and t (kg m-3). Dotted
lines correspond to 95% confidence level.

salinidad, y alta estabilidad provenientes de los


deshielos del glaciar afectan significativamente la
composicin y distribucin espacial de los estados
tempranos de peces marinos, el tamao de los huevos Figura 7. Regresiones lineales entre el logaritmo de la
de sardina fueguina S. fuegensis y la abundancia de abundancia de huevos del pez hacha Maurolicus
huevos de pez hacha M. parvipinnis. parvipinnis y a) temperatura (C), b) salinidad y c) el
Tanto los anlisis multivariados como el anlisis logaritmo de la frecuencia de Brunt-Visl (ciclos s-1).
individual de distribucin espacial de los taxa Las lneas punteadas corresponden al intervalo de
mostraron que el ictioplancton se concentr en las confianza del 95%.
estaciones oceanogrficas con valores intermedios de Figure 7. Linear regressions between logaritm of lighfish
estabilidad (~0,06 ciclos s-1), y que hubo ausencia o Maurolicus parvipinnis egg abundance and a) tempe-
una baja abundancia de huevos y larvas en las zonas rature (C), b) salinity and c) logaritm of Brunt-Visl
cercanas al glaciar Campo de Hielo Sur. Los valores frequency (cycles s-1). Dotted lines correspond to 95%
de los datos ambientales (temperatura y salinidad) confidence level.
Lat. Am. J. Aquat. Res. 246

El aporte de aguas fras, de baja salinidad (i.e., de


baja densidad) producto del deshielo del glaciar puede
afectar la salinidad superficial de la columna de agua
hasta 50 m de profundidad y hasta 75 km mar afuera,
generando una anomala positiva en salinidad cerca de
la costa entre 48 y 53S, e incrementa la circulacin
estuarina del sistema (Dvila et al., 2002),
transportando el zooplancton presente en la capa de
mezcla hacia los canales intermedios, ya sea en forma
pasiva o activamente en estados larvales ms
desarrollados, como se ha planteado para larvas de
cabrilla Sebastes oculatus (Landaeta & Castro,
2006b). Por otro lado, durante primavera en la zona
austral de Chile dominan vientos con direccin norte,
por lo que el transporte de Ekman resultante es hacia
el este, desacelerando la adveccin superficial fuera de
los canales (Dvila et al., 2002). Ambos mecanismos
fsicos podran explicar parcialmente el aparente
movimiento de los huevos de sardina fueguina desde
Figura 8. Proyeccin de las variables fsicas con la la plataforma continental hacia canal Concepcin (Fig.
abundancia del ictioplancton mediante el anlisis de 4) o la mantencin de huevos y larvas de M.
componentes principales (ACP) en Chile austral durante parvipinnis dentro de los canales muestreados (Fig. 5).
primavera de 2009. Si el desove ocurre subsuperficialmente (p.e., bajo 50
Figure 8. Projection of physical variables and m de profundidad), como lo realiza M. parvipinnis en
ichthyoplankton abundance in the Principal Component Chile central (Landaeta & Castro, 2002), el transporte
Analysis (PCA) in southern Chile during austral spring neto sera hacia el interior de los canales,
2009. incrementando los tiempos de residencia de los
estados tempranos en la zona de estudio. En el
presente caso, es difcil establecer la posicin vertical
utilizados en los anlisis de regresin correspondieron del desove, ya que los muestreos fueron integrados, y
a promedios de la columna de agua muestreada por la M. parvipinnis ha mostrado una amplia variabilidad en
red de plancton, por lo que los efectos directos de sus tcticas reproductivas en sistemas de fiordos
intrusiones de aguas de baja salinidad y temperatura (Bustos et al., 2008b, 2011; Landaeta et al., 2009).
estn suavizados por los valores ambientales de aguas En cuanto a composicin del ictioplancton, sta fue
ms profundas, y por lo tanto es esperable que la similar a la encontrada previamente durante la
interaccin de las aguas superficiales con el primavera austral en otros cruceros para la zona de
ictioplancton haya sido subestimada. No obstante, las estudio. Durante fines de la dcada de 1990, se
relaciones fueron significativas. recolectaron altas densidades de larvas de merluza de
La zona austral de Chile se caracteriza por amplios cola Macruronus magellanicus, pero sus abundancias
rangos de valores de estratificacin vertical (N) de la se redujeron considerablemente despus del 2008
columna de agua, entre 0,0003 y 0,539 ciclos s-1 en la (Bernal & Balbontn, 2003; Bustos et al., 2011). Otros
Patagonia norte (Bustos et al., 2008a) y entre 0,013 y componentes del ictioplancton, como las larvas de M.
0,296 ciclos s-1 en la Patagonia sur (Bustos et al., parvipinnis, S. fuegensis y Sebastes oculatus
2011), indicando una alta variabilidad espacial en las mantuvieron su importancia relativa en ambos
condiciones ambientales. En la Patagonia norte se han periodos de tiempo (Bustos et al., 2011).
observado relaciones positivas entre la estratificacin El tamao de los huevos de S. fuegensis present
vertical y la abundancia de huevos y larvas de peces, un rango ms amplio que el descrito previamente por
mientras que en la Patagonia sur se han detectado Ciechomski (1971) para aguas argentinas (1,017-1,030
relaciones negativas con el ictioplancton (Bustos et mm). Adems, se observ que los huevos de mayor
al., 2008a, 2011). Esto sugiere que hay mecanismos tamao (> 1,25 mm) se recolectaron en reas de baja
diferentes que generan la estratificacin vertical (p.e., salinidad y densidad. La salinidad donde ocurre el
pluviosidad versus deshielo) y que a su vez producen desove puede afectar varias propiedades de los huevos
diferentes respuestas en los estados tempranos de los de peces, incluyendo el dimetro y la flotabilidad
peces marinos. neutra (Kucera et al., 2002). Los huevos desovados en
247 Deshielos y distribucin de ictioplancton en la Patagonia, Chile

Tabla 4. Coeficientes de correlacin R de Spearman entre huevos y larvas de peces con valores promedio de temperatura
(Temp), salinidad (Sal), densidad (t) y Frecuencia Brunt-Visl (Frec. B-V) en Chile austral. *P < 0,05.
Table 4. Spearman R correlation coefficients between fish eggs and larvae with mean values of temperatura (Temp),
salinity (Sal), density (t) and Brunt-Visl frequency (Frec. B-V) in southern Chile. *P < 0.05.

LARVAS HUEVOS
Taxa Temp Sal t Frec. B-V Taxa Temp Sal Dens Frec. B-V
A. chiloensis -0,0347 0,2707 0,2707 -0,2013 G. blacodes 0,1739 0,1323 0,1241 -0,1097
B. parini 0,0784 -0,0705 -0,0696 0,3363* Hippoglossina sp. 0,3449* 0,4321* 0,4321* -0,2294
C. messieri -0,2393 -0,1578 -0,1578 0,0579 L. hectoris 0,2568 0,2291 0,2291 -0,0624
G. blacodes -0,0752 -0,2136 -0,2136 0,1098 M. magellanicus 0,0531 0,0430 0,0430 -0,0221
H. lenguerichi -0,0347 0,2707 0,2707 -0,2013 M. parvipinnis 0,5960* 0,5310* 0,5291* -0,1234
L. blainvilleanus 0,0347 -0,0347 -0,0208 0,2013 M. australis 0,1265 0,3710* 0,3856* -0,0857
M. magellanicus 0,2291 0,2568 0,2568 -0,1457 N. crockeri -0,1735 -0,2013 -0,2013 -0,1041
M. parvipinnis 0,4720* 0,3534* 0,3492* -0,1651 P. jugularis -0,0347 0,2707 0,2707 -0,2013
M. australis 0,1942 0,2308 0,2382 0,1971 S. fuegensis -0,0232 0,2157 0,2260 -0,1379
S. oculatus 0,2921 0,2300 0,2241 0,0439 Macrouridae 0,3668* 0,3377* 0,3497* 0,0557
S. caerulea -0,1160 0,2359* 0,2483* -0,1323 Pinguipedidae 0,1041 0,2429 0,2429 -0,1735
S. fuegensis -0,0641 -0,1134 -0,1134 -0,0168 Sp. A 0,2291 0,2568 0,2568 -0,1457
Nothotenia sp. 1 0,1439 0,3775 0,3775 -0,2475 Sp. B 0,0976 0,0584 0,0584 0,1287
Macrouridae -0,0763 -0,1319 -0,1319 0,1735 Sp. C 0,1180 0,0763 0,0763 0,1041
Nothotenia sp. 2 0,0322 0,2169 0,2216 -0,2570 Sp. D 0,2568 0,2291 0,2291 -0,0624
P. marmoratus -0,1324 0,0688 0,0797 -0,1452 Sp. E -0,0902 0,0208 0,0347 0,2152
Sp. A 0,1041 0,2429 0,2429 -0,1735 Sp. F 0,0134 0,1928 0,2025 0,0228
Sp. B -0,1715 0,0748 0,0942 -0,0390 Sp. G 0,1874 0,1319 0,1319 -0,0347
Sp. C 0,0208 0,0069 0,0069 0,0763 Sp. I 0,0782 0,2439 0,2504 -0,1089
Sp. No identif. 0,0634 0,0264 0,0201 -0,0588 Sp. K -0,0624 -0,0624 -0,0624 0,0485
Total larvas 0,4058* 0,4289* 0,4307* -0,0923 Sp. L -0,0208 0,0485 0,0485 0,0069
Sp. M 0,1225 0,1048 0,1134 0,0394
Total huevos 0,4628* 0,6111* 0,6207* -0,1444

reas de baja salinidad tienen mayor contenido de explicada por las consecuencias fisiolgicas que
agua, y Thorsen et al. (1996) sugieren que estos generan aguas de baja densidad en el zooplancton.
huevos presentan mayor contenido de aminocidos Durante la poca de deshielo (primavera y verano) se
libres en su interior, que actan como efectores incrementa el aporte de agua dulce al sistema, que
osmticos incrementando el contenido de agua del aumenta la mezcla turbulenta en la capa de mezcla.
huevo durante la hidratacin. Sin embargo, un mayor Adicionalmente, procesos de vientos locales de fuerte
dimetro de los huevos asociados a zonas de baja
intensidad a lo largo de fiordos y canales puede
salinidad no est correlacionado con un mayor tamao
de eclosin larval (Kucera et al., 2002). Entonces, el reducir la circulacin estuarina y atrapar plancton en
mayor dimetro de los huevos de S. fuegensis en zonas zonas cercanas a deshielos (Eiane & Daase, 2002).
de baja salinidad (o cercana a los deshielos del glaciar) Aunque los zooplancteres intentan evadir esta zona de
eventualmente no generara ventajas adaptativas a las baja salinidad a travs de migraciones verticales, la
larvas recin eclosionadas (i.e., mayor tamao de mezcla turbulenta puede reducir sus capacidades
eclosin) y por lo tanto, no incrementara las natatorias, produciendo stress osmtico (Kaartvedt &
probabilidades de sobrevivencia en un rea de alto Aksnes, 1992) y muerte masiva (~1000 ind m-2, Eiane
stress ambiental. & Daase, 2002), lo que parcialmente podra explicar la
La ausencia y escasa abundancia de algunos taxa ausencia o escasa abundancia de ictioplancton en
en las zonas ms cercanas al glaciar puede ser zonas cercanas a Campos de Hielo Sur.
Lat. Am. J. Aquat. Res. 248

Las mortalidades masivas de zoo e ictioplancton AGRADECIMIENTOS


producto de los deshielos de glaciares generan como
consecuencia un acople pelgico-bentnico. El Los autores agradecen a Mara Ins Muoz y la
zooplancton muerto (biomasa entre 0,01 y 2,8 g peso tripulacin del Vidal Gormaz por la toma de las
hmedo m-2, 0,03-0,17 gC m-2, Wslawski & muestras de plancton, a Carolina Rojas, quien apoy
Legezyska, 1998) sirve como importante entrada de en la separacin del ictioplancton y a los tres
materia orgnica a excavadores bentnicos carnvoros; evaluadores annimos. Este trabajo fue financiado por
por ejemplo, en fiordos rticos la liberacin de el proyecto CIMAR C15F 09-03 adjudicado a C.
juveniles de anfpodos excavadores Onisimicus Bustos y el proyecto Fondecyt 11090020 adjudicado a
caricus est sincronizada con el mximo de M. Landaeta. Durante el desarrollo del trabajo, C.
mortalidad de zooplancton en la poca de deshielos Bustos fue financiada por una beca doctoral de
(Nygrd et al., 2009). CONICYT.
Los deshielos incrementan tambin la turbidez de
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Received: 24 June 2010; Accepted: 27 April 2011


Lat. Am. J. Aquat. Res., 39(2): 250-260, 2011 Lat. Am. J. Aquat. Res. 250
DOI: 10.3856/vol39-issue2-fulltext-6

Research Article

Seasonal changes in a fish assemblage associated with mangroves in a coastal


lagoon of Baja California Sur, Mexico

Jess Rodrguez-Romero1, Laura del Carmen Lpez-Gonzlez2, Felipe Galvn-Magaa3


Francisco J. Snchez-Gutirrez3, Roxana B. Inohuye-Rivera1 & Juan C. Prez-Urbiola1
1
Centro de Investigaciones Biolgicas del Noroeste, P.O. Box 128, La Paz, B.C.S. 23000, Mxico
2
Instituto Nacional de la Pesca, Pitgoras 1320, Col. Santa Cruz Atoyac, Mxico, D.F. 03310, Mxico
3
Centro Interdisciplinario de Ciencias Marinas, Av. Instituto Politcnico Nacional s/n
P.O. Box 592, La Paz, B.C.S. 23000, Mxico

ABSTRACT. The fish assemblage in a coastal lagoon with mangroves known as Rancho Bueno was
determined and associated with environmental parameters. We used an experimental otter trawl net to catch
the fish, and 62 fish species were identified from 48 genera and 30 families. The most abundant species were:
Etropus crossotus, Eucinostomus gracilis, Paralabrax maculatofasciatus, Sphoeroides annulatus, and
Eucinostomus dowii. The water temperature changed seasonally, being warm from July through December and
cold from January through June. We found more fish species during the warm season than during the cold
season. The southern area of the coastal lagoon had the highest diversity and species richness. The small size
of the fishes registered confirms the ecological role of coastal lagoons as nursery areas that offer protection
and feeding to commercially important fish near Baha Magdalena, Mexico.
Keywords: soft-bottom fish assemblage, environmental parameters, mangrove, Rancho Bueno, Baja
California Sur, Mexico.

Cambios estacionales de la comunidad de peces asociada a zonas de manglar en una


laguna costera de Baja California Sur, Mxico

RESUMEN. Se determin la estructura de peces asociada a factores ambientales en una laguna costera con
manglar denominada Rancho Bueno. Se utiliz una red de arrastre experimental para la captura y se
identificaron 62 especies de peces de 48 gneros y 30 familias. Las especies ms importantes fueron Etropus
crossotus, Eucinostomus gracilis, Paralabrax maculatofasciatus, Sphoeroides annulatus y Eucinostomus
dowii. La temperatura del agua vari estacionalmente, siendo clida de julio a diciembre y fra de enero a
junio. Se registr un mayor nmero de especies de peces durante la poca clida comparada con la poca fra.
La zona sur de la laguna costera present una mayor diversidad y riqueza especfica. El menor tamao de los
peces registrados, confirma el papel ecolgico de las lagunas costeras, consideradas como reas de crianza las
cuales proporcionan proteccin y alimentacin a los peces de importancia comercial cerca de Baha
Magdalena, Mxico.
Palabras clave: comunidad de peces de fondos suaves, parmetros ambientales, manglar, Rancho Bueno,
Baja California Sur, Mxico.

___________________
Corresponding author: Jess Rodrguez-Romero (jrodri04@cibnor.mx)

INTRODUCTION the tropical North Equatorial Current (Galvn-Magaa


et al., 2000; Bizzarro, 2008); this is a zone with
The western coast of the Baja California Peninsula is transitional marine conditions influenced by
influenced by the temperate California Current and by upwellings, which contribute to high primary
251 Fish assemblage in a coastal lagoon from Mxico

productivity almost year round. It is a biologically total number of individuals. The Shannon-Wiener
active center (BAC), where many marine fish from diversity index (H') was calculated as follows: H' =
different trophic levels are found (Lluch-Belda, 2000). (ni / N) log (ni / N), where: ni is the number of
The study area named Rancho Bueno is a coastal individuals of species i and N is the total individuals
lagoon located at the southern area of the Baha of all species in the sample. The evenness index
Magdalena-Almejas lagoon complex, which is an (Pielou, 1966) was calculated as follows: E = H' / ln
important fishing area, mainly for artisanal fisheries (S), where H' is the Shannon index and S is the
(Ramrez & Gutirrez, 1987; Bizzarro et al., 2007; number of species. The dominance or Biological
Bizzarro, 2008) and sardine (Robinson, 2000). Value Index (BVI) (Sanders, 1960) was calculated as
i
In spite of this high natural productivity, there are follows: BVI = j Puij, where i is the species, j is the
few published data on fish species taxonomy, sample locality, and Puij is the point level of species i
abundance and diversity from this important fishing at locality j.
area (Galvn-Magaa et al., 2000; Rodrguez-Romero
et al., 2008, 2009). Also is poor known the relation A Principal Components Analysis (PCA) by
between the fish assemblages and environmental season and locations were used, including
parameters in this area, or how these parameters environmental and ecological data.
determine the seasonal or spatial changes in the fish
structure. The objective of our study is to know the RESULTS
influence of environmental parameters in the seasonal
and spatial changes of the fish assemblages in a The Rancho Bueno coastal lagoon was divided into
shallow coastal lagoon in the western coast of Baja three zones: North (locations 1, 2, 3, 4), Central (5, 6,
California peninsula. 7), and South (8, 9, 10) (Fig. 1). The warm season
went from July to December 1993, with average water
MATERIALS AND METHODS temperatures ranging from 22.6 to 27.9C; whereas
the cold season went from January through June 1994,
Study area with average temperatures ranging from 18.8 to
The coastal lagoon of Rancho Bueno is located 22.0C. The temperature increased from north to south
between 241730-242045N, and 1112030- in the coastal lagoon, averaging 21.0C at location 1
1112740W. It is 10.9 km long and 1.2 km wide. (North) and 25.1C at location 10 (South). Salinity
The depth is shallow, from 1 to 6 m, with ~95% of its changed little during the year, ranging from 34.6 to
perimeter bordered by mangrove (Rhyzophora 35.5 psu. Spatial variations in salinity were small,
mangle, Laguncularia racemosa and Avicennia ranging from 34.3 psu at location 1 to 36.6 psu at
germinans). The bottom includes sand, silt and clay, location 10 (Tables 1 and 2).
and some stony areas (Mendoza & Lechuga, 1995). The depths and substrate types are shown in Table
From October 1993 through September 1994, we 2. The Northern Zone (locations 1 to 4), had sandy
did twelve surveys at ten locations. One tow was bottoms and greater depths than the Southern Zone
carried out at each location using an experimental (locations 8 to 10), which had higher salinity and
otter trawl net of 6.0 m length and 4.0 m wide with shallow depths.
doors of 0.60 x 0.40 m and 3.15 cm mesh size. The We captured 3,082 fish, all juveniles, with a total
bottom temperature, salinity, water depth, and bottom weight of 102.04 kg, belonging to 62 species in 48
type were recorded. Specimens were fixed in 10% genera and 30 families. The most important families
formaldehyde solution for later identification using were: Haemulidae (ten species); Lutjanidae, Gerreidae
specific keys for each fish species. and Paralichthyidae (five species each), Serranidae
Using the weight data of each species, ecological (four species), and Sciaenidae and Urolophidae (three
indexes were calculated. The relative abundance (RA) species each). The most common species were:
and relative weight (RW) were calculated as follows: Etropus crossotus (688 specimens), Eucinostomus
RA(%) = (n / N) * (100) and RW(%) = (w / W) * (100), gracilis (544), Paralabrax maculatofasciatus (253),
where n is the number of species captured, N is the Sphoeroides annulatus (242), Eucinostomus dowii
total number of specimens, w is the weight of each (229), Orthopristis reddingi (133) and Diapterus
species, and W is the weight of all specimens. peruvianus (108).
The species richness index (D) proposed by Locations 9, 10 and 5 had the highest numbers of
Margalef (1969) was calculated as follows: D = (S fish. The months with highest organism numbers
1) / ln N, where S is the number of species and N is the were: September 1994 (937 fish from 32 species)
Lat. Am. J. Aquat. Res. 252

Figure 1. Study area and sampling locations Rancho Bueno coastal lagoon in southern Baha Magdalena, Baja California
Sur, Mexico.
Figura 1. rea de estudio y localidades de muestreo en la laguna costera de Rancho Bueno ubicada al sur de Baha
Magdalena, Baja California Sur, Mxico.

Table 1. Average water temperature and salinity during The fish species better represented by relative
1993-1994 in Rancho Bueno, Mexico. abundance, in order of importance, were: E. crossotus,
Tabla 1. Temperatura y salinidad promedio durante E. gracilis, P. maculatofasciatus, S. annulatus, E.
1993-1994 en Rancho Bueno, Mxico. dowii, O. reddingi and D. peruvianus, composing
71.3% of the specimens and over 35% of the total
relative weight (Fig. 2). On each sampling, E.
Average Average crossotus and E. gracilis had the highest relative
Month
Temperature (C) Salinity (psu) abundance (22.3 and 17.6%); while P.
Oct. 27.6 34.8 maculatofasciatus had the highest relative weight
Nov. 25.2 35.0 (11.2%). It is important to mention that of 62 fish
Dec. 22.6 34.7 species, 38 (61.29%) are of commercial importance
Jan. 22.0 35.0
(species marked with an asterisk in Table 4).
Feb. 19.9 35.5 The highest seasonal and spatial species richness
according to species abundance occurred in October
Mar. 20.5 34.9
(3.9); whereas the lowest richness occurred in April
Apr. 18.8 35.0 (0.4). The lowest value was from the northern zone
May 18.9 35.2 during the cold months; whereas the highest value was
Jun. 21.0 35.5 from the southern zone during the period September
Jul. 22.7 35.0 through January.
Aug. 25.7 35.1 The diversity index ranged from 0.4 to 3.6 (bits
ind-1), with the minimum value at location 7 in April;
Sep. 27.9 35.0
whereas the maximum diversity was found at location
10 in October (both in the southern zone). Locations 1
and October 1993 (469 fish from 36 species). Six of to 4 in the northern zone had lower diversity than
the 62 species were found at all locations: E. locations 7 to 10 in the southern zone, which also had
crossotus, P. maculatofasciatus, Paralichthys cali- the highest diversity.
fornicus, S. annulatus, Symphurus atramentatus and The lowest evenness occurred in the cold season
Synodus lucioceps. (values below 0.6.); the minimum value (0.25) was at
253 Fish assemblage in a coastal lagoon from Mexico

Table 2. Characteristics of Rancho Bueno coastal lagoon, Mexico sampling sites.


Tabla 2. Descripcin de las localidades de muestreo en la laguna costera Rancho Bueno, Mxico.

Tow depth Temperature Salinity


Zone Site Substrate type
(m) (C) (psu)
North 1 Sand 2.9 21.04 34.36
2 Sand 2.5 21.17 34.10
3 Sand 3.6 21.26 34.13
4 Sand 3.5 21.34 34.44
Central 5 Sand-silt 2.1 21.59 34.61
6 Sand-silt 2.0 22.73 34.96
7 Sand-silt 2.2 24.17 35.40
South 8 Silt 1.4 24.24 35.87
9 Silt 1.8 24.63 36.12
10 Silt 1.6 25.07 36.58

Using PCA, we detected two main groups of fish


(Fig. 4). In the first group were six species: P.
californica, O. cantharinus, U. halleri, S. ovale, E.
crossotus and P. maculatofasciatus, which were
associated to northern locations (1, 2, 3 and 4) in the
coastal lagoon, with higher biomass in deep locations
and close to the entrance to the open ocean.
The other group included 11 fish species at
locations 5 to 10, which are in the center and south
area, with lower biomass but higher organism
numbers and evenness, associated to shallow waters
with higher water temperature and salinity.
The seasonal PCA (Fig. 5) recorded two periods,
associated to cold waters during January-June (winter-
spring), and a warm period from July to December
(summer-fall). In this last period the diversity, species
Figure 2. Relative abundance and weight of dominant number, and organism abundance showed the highest
fish species at Rancho Bueno coastal lagoon. affinity with 12 dominant fish species, including P.
Figura 2. Abundancia relativa y biomasa de las especies maculatofaciatus, Sphoeiroides annulatus, Lutjanus
dominantes de peces en la laguna costera de Rancho argentiventris, Hoplopagrus guntheri, Calamus
Bueno. brachysomus, Balistes polylepis and others. During
the cold period, with highest biomass and salinity, the
most common species were: P. californicus, U.
location 4 in May, followed by location 7 in April
halleri, E. crossotus, A. mazatlanus, O. cantharinus
(0.39). The highest evenness (1.0) in some locations
and S. lucioceps.
was recorded in November, December, February, and
August. In general, the cold season had lower
DISCUSSION
evenness than the warm season (0.72 to 0.77). In table
3 are shown the monthly values of ecological indexes.
The topographic and hydrographic characteristics of
The fish species of highest importance according to the coastal lagoon of Rancho Bueno, provide optimal
the Biological Value Index were: E. crossotus, E. conditions as a nursery, feeding, and reproduction area
gracilis, S. annulatus, P. maculatofasciatus and E. for many fish species that are important as commercial
dowii, with index values of 94, 64, 62, 60 and 48, species. This ecosystem has high primary productivity
respectively (Fig. 3).The monthly analyses of this that promotes species richness. Mendoza & Lechuga
index are shown in Table 4. (1995), found higher accumulated organic matter in
Table 3. Monthly values of ecological indices by zone and sampling site. D: Species richness (Margalef, 1969), H: Diversity (Shannon-Wiener), E: Evenness (Pielou,
1966).
Tabla 3. Valores mensuales de los ndices ecolgicos por zona y localidades de muestreo. D: Riqueza de especies (Margalef, 1969), H: Diversidad (Shannon- Wiener), E:
Uniformidad (Pielou, 1966).

October November December January February March


Location
D. H' E D H' E D H' E D H' E D H' E D H' E
North 1 2.06 1.97 0.62 1.86 1.92 0.96 1.52 2.07 0.89 1.23 1.29 0.55
2 2.64 2.03 0.59 1.86 1.92 0.96 2.4 2.5 0.97 0.91 0.92 0.92 1.37 1.66 0.83
3 2 2.22 0.79 0.91 0.92 0.92 1.82 1.58 1 1.21 1.73 0.86
4 2.32 2.38 0.72 1.82 1.58 1 2.41 2.63 0.94 1.94 2.24 0.8 0.72 1 1 1.37 1.45 0.72
Central 5 2.72 2.8 0.88 0.72 0.81 0.81 2.59 2.82 0.89 1.64 2.01 0.78 0.56 0.92 0.92
6 2.34 2.62 0.93 0.62 0.97 0.97 1.12 1.46 0.92 1.21 1.42 0.71 1.24 1.52 0.96 1.2 1.77 0.76
7 0.87 0.86 0.43 1.44 1 1 1.5 1.72 0.66 1.44 1.55 0.77 2.12 2.13 0.71 0.72 0.67 0.42
South 8 2 1.78 0.59 2.16 2 1 2.73 2.41 0.73 2.16 2.53 0.9 1.82 2.36 0.79
9 2.72 2.11 0.55 3.47 3.29 0.8 1.64 1.65 0.55 1.44 1.5 0.95 2.23 2.25 0.97 1.62 1.87 0.72
10 3.96 3.62 0.85 0.91 1.33 0.66 2.32 1.82 0.53 3.44 2.99 0.75 2.06 2.24 0.96 1.94 2.29 0.72
Lat. Am. J. Aquat. Res.

April May June July August September


Location
D H' E D H' E D H' E D H' E D H' E D H' E
North 1 0.91 0.92 0.92 0.96 1.41 0.89 1.56 2.2 0.95 1.44 1.5 0.95
2 0.62 0.72 0.72 1.01 1.62 0.7 1.67 1.92 0.96 0.62 0.72 0.72
3 1 1.19 0.6 1.59 1.53 0.54 0.69 0.61 0.39 1.11 1.72 0.86 1.86 2.42 0.81
4 1.41 1.26 0.54 0.58 0.4 0.25 1.7 1.33 0.44 0.91 0.99 0.62 1.23 1.8 0.7
Central 5 1.12 1.46 0.92 1.31 1.38 0.53 3.07 2.82 0.68
6 0.94 1.06 0.53 2.4 2.11 0.67 1 1.32 0.66 0.91 0.92 0.92 0.91 0.92 0.92 3.55 3.26 0.77
7 0.39 0.39 0.39 0.91 0.92 0.92 0.91 0.99 0.62 1.24 1.37 0.86 2.93 3.3 0.83
South 8 0.62 0.97 0.97 0.91 0.92 0.92 3.34 2.91 0.76 1.12 1.46 0.92 1.44 1 1 2.4 3.04 0.88
9 2.39 2.26 0.65 1.86 1.97 0.66 2.09 2.3 0.89 2.01 2.52 0.98 2.39 2.86 0.75
10 1.69 2.31 0.82 1.44 1.5 0.95 1.8 1.94 0.69 1.61 2.05 0.88 1.03 1.15 0.72
254
255 Fish assemblage in a coastal lagoon from Mexico

analysis showed that the main fish species (E.


crossotus, P. maculatofasciatus and S. annulatus)
represented over 70% of the total relative abundance
and almost 37% of the relative biomass. This indicates
that, in spite of being the most numerous species, their
small size affects their biomass. The southern
locations from the Rancho Bueno lagoon had the
highest relative abundance, almost 40%.
The highest species richness values occurred
during the warm months, and the lowest values during
the cold months. Gutirrez-Snchez et al. (2007)
reported in Bahia Magdalena, Mexico, the highest
values of species richness between February and July,
Figure 3. Biological Value Index of the most common as a consequence of the mix of fish species with
fish species at coastal lagoon of Rancho Bueno, Mexico. different zoogeographic affinities. In Baha
Figura 3. ndice de valor biolgico de las especies de Concepcin (Gulf of California), Rodrguez-Romero
peces ms importantes de la laguna costera de Rancho et al. (1998) found the highest species richness in
Bueno, Mxico. September and the lowest in February. The species
richness in the southern Bahia Concepcion was also
influenced by the muddy substrate, because locations
the southern area, which also we found higher fish
with several habitat types increase the species richness
abundance.
(Krebs, 1978; Blaber, 1985; Rodrguez-Romero et al.,
The number of fish species and marine organisms 1994), because there are prey from different habitats
was higher in the southern area of Rancho Bueno, which are consumed by fishes. We found the highest
where average water temperature was higher and the diversity during the warm months, with the highest
bottom was muddy. In contrast to northern locations, value (3.6 bits ind-1) in October and the lowest in
the southern locations had fewer fish species and April (0.4), which agrees with the diversity changes
organisms, with sandy bottoms and lower water associated to sampling location, fishing method, fish
temperatures. In months with low temperatures, the dynamics, biology of each fish species, feeding
number of fish species and other organisms was low. relationships, and environmental conditions
During February, we found fewer fish (55) belonging (Margalef, 1974).
to 15 families; whereas during warmer months, mainly The Rancho Bueno coastal lagoon could be
September, we found 937 fish belonging to 19 considered as a mature fish community, considering
families. The main species were: P. maculato- the high diversity found with little disturbance (Odum,
fasciatus, S. annulatus, E. dowii, O. reddingi and D. 1972). The locations in the southern area are
peruvianus. Of these species, E. crossotus, P. apparently uniform, because they are in the most
maculatofasciatus and S. annulatus were common protected area; however, these shallow areas are
during the sampling period. associated with high changes in water temperature and
The fish species found in our study have been salinity, and with the highest diversity and evenness.
reported for the Baha Magdalena-Almejas lagoon Seasonal changes in diversity are associated with
complex (Torres-Orozco & Castro-Aguirre, 1992; De changes in water temperature, which also affect the
La Cruz-Agero et al., 1994; Galvn-Magaa et al., presence of fish, diversity and abundance (Rodrguez-
2000). The importance of our results is the high Romero et al., 1998, 2005). De La Cruz (2004)
number of fish species found, and mostly were studied fish assemblages in four mangroves areas
juveniles (62), which confirm that Rancho Bueno is close to Baha de La Paz (Gulf of California), he
used as a nursery and feeding area by fish species with found the highest values of abundance and diversity
commercial importance. during the warm months and the lowest during cold
The coastal lagoon of Rancho Bueno had a high months; whereas Acevedo (1997) in Laguna Ojo de
number of fish species comparing with other locations Liebre (western coast of Baja California) registered
in Baja California Sur. Rodrguez et al., 1998 and that locations in the north coastal lagoon had the
Gutirrez-Snchez et al. (2007) also found a high highest water temperatures and the highest fish
number of fish species; however De La Cruz (2004) diversity. Also Horn & Allen (1985), found that fish
found only 25 fish species in four estuarine areas from communities in bays and estuaries in southern
Baha de la Paz. The abundance and relative biomass California, are influenced by oceanic waters and had
Lat. Am. J. Aquat. Res. 256

Table 4. Biological Value Index of fish species found at Rancho Bueno, Mexico. Species with (*) have commercial
importance.
Tabla 4. ndice de Valor Biolgico de las especies de peces registradas en Rancho Bueno, Mxico. Las especies marcadas
con asterisco (*) tienen importancia comercial.

1993 1994
Species
Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep
Achirus mazatlanus 25 12 7 35 8 39 18 32 13 24 9 26
Arius platypogon* 5
Balistes polylepis* 27 21 22 17 10 8 6 11
Bothus constellatus 32 9 9 9 9 9 5
Calamus brachysomus* 29 13 22 21 24
Caranx caninus* 2 6
Centropomus medius* 9
Chaetodipterus zonatus* 7 7 9
Chaetodon humeralis 15
Cyclopsetta panamensis* 8 10 18 5 15
Cynoscion parvipinnis* 14 9
Dactylagnus mundus 7 8 9
Diapterus peruvianus* 9 14 8 6 14 29
Diodon holocanthus 8 8 7
Diodon hystrix 7 7 14
Diplectrum pacificum* 13 6
Epinephelus analogus* 15 5 7
Etropus crossotus 62 34 77 65 40 87 40 70 78 77 47 39
Eucinostomus dowii* 21 20 15 7 19 19 16 10 34
Eucinostomus gracilis* 65 19 66 16 20 8 45
Eugerres axillaris* 10
Fistularia commersonii 7
Gerres cinereus* 10
Gymnura marmorata* 7 10 9 20 8 9 1
Haemulon steindachneri* 7 15 3
Haemulopsis leuciscus* 12 7 15 9 15 3
Haemulopsis nitidus* 3
Hippocampus ingens 4 10 13 15
Hoplopagrus guntheri* 10 7 18
Hypsoblennius gentilis 8 8 9 17
Hypsopsetta guttulata* 7
Lutjanus aratus* 10 10 7
Lutjanus argentiventris* 8 15 16 14 9 17 29
Lutjanus colorado* 4
Lutjanus novemfasciatus* 5
Menticirrhus undulatus* 10
Microlepidotus inornatus* 4
Micropogonias ectenes* 9 6
Orthopristis cantharinus* 8 10
Orthopristis reddingi* 22 4 18 7 9 30
Paralabrax maculatofasciatus* 72 14 81 70 16 16 14 16 52 19 47 22
Paralabrax nebulifer* 9
Paralichthys californicus* 45 9 9 19 16 5 15 23 15 7 35
Paralichthys woolmani* 38 9 26 8
257 Fish assemblage in a coastal lagoon from Mexico

1993 1994
Species
Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep
Pleuronichthys ritteri 8 9
Pomadasys bayanus* 4 20
Pomadasys macracanthus 2 6 7
Pomadasys panamensis* 6 4
Prionotus ruscarius 11 9 8 22 6 5 5
Pseudupeneus grandisquamis 12 19 5 12 7 5
Scarus perrico* 7
Scorpaena russula 8 6 1
Sphoeroides angusticeps 4 1
Sphoeroides annulatus* 24 32 40 24 10 36 17 34 40 26 27 53
Syacium ovale 42 7 9
Symphurus atramentatus 4 28 4 6 31 21 27 14
Symphurus fasciolaris 18
Synodus lucioceps 2 63 38 25 55 9 26 24 9 12
Urobatis halleri 6 10 8 4 19 17 22 10 9 8
Urobatis maculatus 8
Urotrygon asterias 7 12 9
Xenistius californiensis 2

Figure 4. Spatial Principal Component Analyses associated with water temperature, salinity, depth, substrate (grain type)
total abundance, biomass, fish dominant species and sampling locations (1 to 10).
Figura 4. Anlisis espacial de componentes principales asociado a la temperatura del agua, salinidad, profundidad,
substrato, abundancia total, biomasa, especies de peces dominantes y localidades de muestreo (1 a 10).
Lat. Am. J. Aquat. Res. 258

Figure 5. Monthly Principal Component Analyses associated with water temperature, salinity, biomass, number of fish
species (SPP), diversity, total abundance. JF: January-February, MA: March-April, MJ: May-June, JA: July-August, SO:
September-October, NO: November-December.
Figura 5. Anlisis mensual de componentes principales asociado a temperatura del agua, salinidad, biomasa, numero de
especies de peces, diversidad, abundancia total. JF: enero-febrero. MA: marzo-abril, MJ: mayo-junio, JA: julio-agosto,
SO: septiembre-octubre, NO: noviembre-diciembre.

seasonal changes in abundance and diversity. The temperate zone affinity or were widely distributed,
biological value index showed that E. crossotus, E. such as P. californicus, Orthopristis cantharinus, E.
gracilis, S. annulatus, P. maculatofasciatus and E. crossotus, Sciacium ovale and Urobatis halleri.
dowii were the most important fish species in the In the southern area, we found high abundance and
Rancho Bueno coastal lagoon. Their dominance might diversity, with more fish of small size (mostly
be attributed to their high occurrence during all juveniles). Juveniles were common in protected areas
sampling. associated to mangroves. The most common species
In the upper Gulf of California, Prez-Mellado & were: E. dowii, B. polylepis, H. guntheri, Sphoeroides
Findley (1985) found that E. crossotus and annulatus, E. gracilis, Lutjanus argentiventris,
Citharichthys spp. were the most abundant species in Syacium ovale, Diapterus peruvianus and O. reddingi,
the shrimp trawl by-catch, followed by Diplectrum which are from temperate-tropical habitats or are
pacificum and Scorpaena sonorae; whereas widely distributed (Robertson & Allen, 2002). Baja
Rodrguez-Romero et al. (1998) in Baha Concepcin California Sur is a biogeographically transition zone
(central Gulf of California) found that P. (Castro-Aguirre & Torres-Orozco, 1993), where
maculatofasciatus, E. crossotus, Urobatis halleri and tropical, sub-tropical, and temperate fish coexist.
Sphoeroides lispus were the most important fish Changes in spatial and seasonal fish composition are
species. associated to fluctuating environmental conditions in
Our PCA and cluster analysis indicated that two this transition zone. Galvn-Magaa et al. (2000)
groups characterized the fish assemblage in the confirmed that northwestern Mexico is one of the
Rancho Bueno coastal lagoon. In the northern area most diverse areas in terms of tropical, temperate and
with deeper water, the highest biomass was tropical-temperate transition marine species.
represented by few fish species with high importance; The west coast of Baja California Sur is a tropical-
larger fish were more frequent and these species had temperate transition zone, where seasonal gradients
259 Fish assemblage in a coastal lagoon from Mexico

are influenced by the cold California Current and the Blaber, S.J. 1985. The ecology of fishes of estuaries and
Eastern Pacific Equatorial Current (Bizzarro, 2008). lagoons of the Indopacific with particular reference to
The water temperature changes, substrate type, and Southeast Africa, Chap. 12. In: A. Yez-Arancibia
feeding habitats were the most influential (ed.). Fish community ecology in estuaries and
environmental elements affecting the fish assemblages coastal lagoons: towards and ecosystem integration.
in this area. The monthly PCA also indicated two Universidad Nacional Autnoma de Mxico, pp. 247-
distinct periods, dominated by water temperature: 266.
winter-spring and summer-autumn (Fig. 6). The water Castro-Aguirre, J.L. & R. Torres-Orozco. 1993. Conside-
temperature, habitat type and primary productivity are raciones acerca del origen de la ictiofauna de Baha
important for ecosystem productivity (Mendoza- Magdalena-Almejas, un sistema lagunar de la costa
Salgado & Lechuga-Devze, 1995). occidental de Baja California Sur, Mxico. An. Esc.
In conclusion, the Rancho Bueno coastal lagoon Nac. Cienc. Biol., 38: 67-73.
supports nursery and feeding areas for juvenile fish De la Cruz-Agero, J., F. Galvn-Magaa, L.A. Abitia-
with high commercial importance, such as snappers, Crdenas, J. Rodrguez-Romero & F.J. Gutirrez-
groupers, mojarras and flatfishes. Also is a Snchez. 1994. Lista sistemtica de los peces marinos
reproduction area for many commercial fish species de Baha Magdalena, Baja California Sur. Cienc.
from temperate and tropical affinities. We found Mar., 20: 17-31.
seasonal changes in the fish assemblages of this De la Cruz, S.J.A. 2004. Caracterizacin ctica de la
coastal lagoon based on changes in water temperature, composicin, diversidad y abundancia en cuatro
substrate type and depth. The highest species richness esteros de La Baha de La Paz, B.C.S., Mxico.
and diversity were found during the warmer months, Bachelor Thesis. Universidad Autnoma de Baja
and the highest number of organisms was found in the California Sur, La Paz, B.C.S., 57 pp.
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muddy bottoms included Sargassum spp. and Crdenas & J. Rodrguez- Romero. 2000. The
mangrove roots; whereas the northern area had few distribution and affinities of the shore fishes of Baja
fish species, the bottom was sandy and had low water California Sur lagoons. In: M. Munawar, S.G.
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ACKNOWLEDGEMENTS monograph series. Backhuys Publishers, Leiden, pp.
383-398.
We thank Mario Cota-Castro and Juan Jos Ramrez Gutirrez-Snchez, F.J., F. Galvn-Magaa, L.A. Abitia-
for helping with sampling. Financial support was Crdenas & J. Rodrguez-Romero. 2007. Peces
provided by the Centro de Investigaciones Biolgicas demersales de Baha Magdalena. In: R.R. Funes, J.
del Noroeste project Estructura y funcin de Gmez & R. Palomares (eds.). Estudios ecolgicos en
comunidades de peces en el Estero de Rancho Bueno, Baha Magdalena. Gobierno del Estado. de Baja
B.C.S. Mexico. FGM and FJGS thank the Instituto California del Sur. SeTur. De B.C.S., Fondo para la
Politcnico Nacional (COFAA and EDI fellowships). proteccin de los recursos marinos de B.C.S.,
We thank Laura Sampson for editing the English CICIMAR-IPN, pp. 241-250.
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Horn, M.H. & L.G. Allen. 1985. Fish community
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Received: 12 July 2010; Accepted: 29 April 2011


Lat. Am. J. Aquat. Res., 39(2): 261-270, 2011 Relative growth of symbiotic crab Austinixa aidae 261
DOI: 10.3856/vol39-issue2-fulltext-7

Research Article

Relative growth and sexual dimorphism of Austinixa aidae (Brachyura:


Pinnotheridae): a symbiont of the ghost shrimp Callichirus major from the
southwestern Atlantic

Douglas Fernando Peir1, Paulo Ricardo Pezzuto2 & Fernando Luis Mantelatto1
1
Laboratory of Bioecology and Crustacean Systematics, Department of Biology, FFCLRP
University of So Paulo, Postgraduate Program in Comparative Biology
Avenida Bandeirantes 3900, CEP 14040-901, Ribeiro Preto, SP, Brazil
2
Universidade do Vale do Itaja, Centro de Cincias Tecnolgicas da Terra e do Mar
Rua Uruguai, 458, CEP 88302-202, Itaja, SC, Brazil

ABSTRACT. Species of the family Pinnotheridae constitute an ideal group for morphometric studies due to
their complex morphological adaptations. These adaptations respond to the selective pressure of a symbiotic
life style. This study describes the relative growth and morphometric features of the symbiotic pea crab
Austinixa aidae (associated with the ghost shrimp Callichirus major), from the sandy beaches in the southwest
Atlantic, Brazil. Significant differences were detected in the biometric proportions, particularly the chelar
propodus length and carapace width, of each sex. These dimensions were also related to the size at which the
individuals reached morphological sexual maturity (5.1 mm of carapace width for both sexes). Males and
females were 2.4 times wider than long, which corresponds to the principal adaptation developed by Austinixa
species to live in cryptic environments. Moreover, juveniles were proportionally more rounded. The changes
in the biometric proportions of carapace length and width of A. aidae were more pronounced in males and
females, adaptations that facilitate roaming within the galleries of their hosts.
Keywords: pinnotherid crabs, traditional morphometry, size-at-maturity, sexual dimorphism, southwestern Atlantic.

Crecimiento relativo y dimorfismo sexual en Austinixa aidae (Barchyura:


Pinnotheridae): un simbionte del camarn fantasma Callichirus major
del Atlntico sudoccidental

RESUMEN. Las especies de la familia Pinnotheridae constituyen un grupo ideal para la realizacin de
estudios morfomtricos, debido a sus complejas adaptaciones morfolgicas. Estas adaptaciones son respuesta a
la presin de seleccin debida a su vida simbionte. En este estudio se describi el crecimiento relativo y las
caractersticas morfomtricas del cangrejo simbionte Austinixa aidae (asociado con el camarn fantasma
Callichirus major), de una playa de arena del Atlntico suroeste de Brasil. Se determinaron diferencias
significativas en las proporciones biomtricas de cada sexo, entre la longitud del propodio y ancho del
caparazn. Estas dimensiones estuvieron relacionadas tambin con la talla en que los individuos muestran
cambios morfolgicos en su madurez sexual (5.1 mm de ancho del caparazn en ambos sexos). Los machos y
hembras fueron 2,4 veces ms anchos que largos, lo que corresponde a la adaptacin principal que las especies
del gnero Austinixa, han desarrollado para vivir en ambientes crpticos. Adems, los juveniles fueron
proporcionalmente ms redondeados. Los cambios en las proporciones biomtricas de longitud y ancho del
caparazn de A. aidae, fueron ms pronunciados en machos y hembras, adaptaciones que facilitan el
desplazamiento al interior de las galeras construidas por sus hospederos.
Palabras clave: cangrejos pinnothridos, morfometra tradicional, talla de madurez, dimorfismo sexual,
Atlntico sudoccidental.

___________________
Corresponding author: Fernando Luis Mantelatto (flmantel@usp.br)
262 Lat. Am. J. Aquat. Res.

INTRODUCTION MATERIALS AND METHODS

Pea crabs of the family Pinnotheridae De Haan, 1833 Sampling was carried out bimonthly during daytime at
constitute a promising group for morphometric studies low tide (in an area of approximately 400 m length
because of their complex morphological adaptations to and 30 m width), from May 2005 to September 2006
symbiotic life style. Over 300 species of this family in the intertidal zone of Perequ-au Beach, Ubatuba,
display symbiotic relationships (both facultative and northern coast of State of So Paulo, Brazil
obligated) with a wide variety of bivalves, gastropods, (232459.99S, 450317.13W), a semi-protected
polychaetes, crustaceans, echinoderms, echiurids, and dissipative beach composed by fine sand. Crabs
brachiopods, balanoglossids and ascidians (Schmitt et were collected with commercial yabby pumps,
al., 1973; Harrison & Hanley, 2005; Ng et al., 2008). developed by Rodrigues (1966) and similar to the one
These symbioses are an intriguing system and, described by Manning (1975), from Callichirus major
galleries, separated from the sand by a 1 mm mesh
consequently, almost all the morphological features of
sieve, frozen, and analyzed in laboratory.
these crabs are strongly adapted in order to achieve a
successful relationship. Their adaptation to this variety Crabs were sexed by revising the shape of the
of hosts likely accounts for their diversity, and this can pleopods. Males have a pair of long, thin pleopods on
consequently drive towards a confused state of the ventral surface of the first abdominal somite and a
pair of short pleopods on the second abdominal somite
systematics in some members of the group (Palacios-
(together they compose the gonopods); females have
Theil et al., 2009).
four pairs of short pleopods from the second to the
Among representatives of this family, the fifth abdominal somites (Narchi, 1973). Specimens
polyphyletic pinnotherid crab genus Austinixa Heard with undifferentiated or not developed pleopods and
& Manning, 1997 (sensu Palacios-Theil et al., 2009) is gonopore were considered/named juveniles (no
less diverse than other members of the Pinnotheridae, identified as males or females). The following
and comprise currently eight described species (Ng et measurements were taken under a stereomicroscope
al., 2008). The enlargement of carapace, the third pair with the aid of a drawing tube (0.1 mm precision):
of pereopods, and a conspicuous lobe on the outer carapace width (CW), carapace length (CL), abdomen
margin of the basal segment on the exopod of the third width (AW) (between fourth and fifth abdominal
maxilliped are the main synapomorphies with the tagma), height (HQ) and length (LQ) of cheliped
Pinnixa complex (in which Austinixa was included) propods (left and right), and the gonopod length (GN)
(Heard & Manning, 1997; Campos, 2006). These (from the shaft to tip). The wet weight (WW) was
morphological modifications presumably facilitate measured, after the samples were drained by paper
lateral movement within the microhabitats (narrow towel, with an electronic analytical balance (0.0001 g
precision), to assess changes in weight related to
tubes and burrows) occupied by these crabs (Zmarzly,
sexual maturity.
1992; McDermott, 2006).
The carapace width was used as independent
As far as we know, only three studies have been
variable, because it represents the crabs body size. To
devoted exclusively to understand the relative growth assess the chelae dimorphism (heterochely), the
(allometry) in Austinixa: Alves & Pezzuto (1999), Mann-Whitney Rank Sum Test (due the non-
Alves et al. (2005) and Valena-Silva et al. (2008), all normality of the data) was applied to compare
on Austinixa patagoniensis (Rathbum, 1918). For differences in mean values of HQ and LQ, in both
Austinixa aidae (Righi, 1967), no studies have been chelipeds. The same test was applied to compare
published. differences on sizes of males and females.
Likewise the lifestyle, the allometry of pea crabs Relative growth was quantitatively described by
varies considerably, and some body character- fitting the allometric equation (Y = aXb) for each body
ristics/features are poorly understood for species of dimension against the independent variable (CW) by
Austinixa. Taking into account the lack of descriptions least-squares regression analysis (Hartnoll, 1974,
on the allometry, the aim of this study was to describe 1978). Inflection (transition) points corresponding to
the relative growth and body features of the symbiotic changes in the allometry pattern during the growth
crab A. aidae [associated with the thalassinid ghost were first identified by eye on dispersion graphs. They
shrimp Callichirus major (Say, 1818)], from a sandy were then iteratively searched by a specific routine of
beach in the southwest Atlantic. We also estimated the the software Regrans (Pezzuto, 1993); the routine
size at maturity and the existence of sexual seeks the CW value where the data could be split into
dimorphism in this population. two subsets resulting in the lowest combined residual
Relative growth of symbiotic crab Austinixa aidae 263

sum of squares. An Overall Test for Coincidental relative growth. This analysis revealed differences in
Regressions (Zar, 1996, p. 368) was conducted to growth rates of a few body structures in both males
check the validity of the transition point. It and females (Table 1).
compares the difference between the global sum of The carapace length of males, females, and
squares (calculated from a single model fitted to the juveniles showed negative allometric growth (b < 1),
data), and the pooled residual sum of squares (i.e. of with no transition points (Fig. 1a, Table 1). The same
the subsets located to the left and right sides of the pattern was also found for the abdomen width of
transition point) (Zar, 1996). If a significant difference males (Fig. 1b). On the other hand, the female
was found, the ANCOVA ( = 0.05) was used to test abdomen width exhibited two transition points at 5.1
the difference between intercepts and slopes of the and 7.2 mm CW. Below 5.1 mm and between 5.1 and
two regressions, corresponding then to the pre and 7.2 mm, growth was positive allometric, and from 7.2
post-pubertal phases of growth (Zar, 1996). On the mm growth was isometric. For juveniles, growth was
analysis of the allometric growth, constant (b) gives positive allometric, without transition points.
information about the increase of one biometric
Because no statistical differences were found
dimension in relation to another; isometric growth was
between the HQ and HL of both left and right chelar
considered when b was = 1, negative allometric
propodus (P = 0.931 and P = 0.942 for total of
growth with b < 1, and positive allometry with b > 1
individuals; males P = 0.897 and P = 0.772; females P
(Hartnoll, 1982). When involved different units, like
= 0.982 and P = 0.822; and juveniles P = 0.513 and P
the CW and the WW, the value of isometry assume b
= 0.577, respectively), only the measurements of the
= 3 (Valenti, 1984; Biagi & Mantelatto, 2006).
left chelar propodus were used in the relative growth
The sexual dimorphism in Decapoda occurs by analysis.
differences in relative growth between males and
females, which in initial stages are not clear. There are The maximum height of the chelar propodus of
body structures that present strong and consistent males and females (Fig. 1c) showed positive
patterns of variations in allometry associated to allometric growth, with no transition points. For
maturation, for example the cheliped of males and the juveniles, growth showed negative allometry, with no
abdomen of females in Brachyura (Hartnoll, 1978, transition points.
1982). These structures are related to reproductive The maximum length of the male chelar propodus
activities of both sexes, and are associated to showed positive allometric growth, with a break in the
dimorphism in mature stages. The body dimension dispersion data and an inflection at 5.1 mm CW (Fig.
related to maturation and reproductive activity 1d). For females, growth was positive allometric,
increase in major rates than the carapace (positive while for juveniles, growth was isometric, both with
allometric growth) (Hartnoll, 1982). no significant transition points.
Maximum and minimum sizes of males and
The wet weight of males showed positive
females were verified, as well as the minimum size of
allometric growth up to 5.7 mm CW, and after this
ovigerous females and the length of their reproductive
size, growth changed to negative allometric. In
period, which was identified by the percentage of
ovigerous females in relation to the total number of females, growth was positive allometric up to the
females caught bimonthly (Alves et al., 2005). transition point at 5.4 mm CW, changing to isometric
in larger sizes. For juveniles, growth was described by
The normality of data-set was evaluated before to a single, positive allometric equation (Fig. 1e).
the use of parametric tests. The statistical analysis
were conducted by using Sigma-Stat 2.03 and The gonopods showed isometric growth up to 3.0
Regrans (Pezzuto, 1993), according to Zar (1996) (P < mm (CW), and after that the growth was negative
0.05 significance). All material was preserved in allometric (Fig. 1f).
ethanol 80% and deposited in the Crustacean
Collection of the Departamento de Biologia, Body features, maturity and sexual dimorphism
Faculdade de Filosofia, Cincias e Letras de Ribeiro The CW of male crabs varied between 2.0 and 10.1
Preto, Universidade de So Paulo, (CCDB/FF mm (mean 5.8 2.2 mm CW), and females between
CLRP/USP) under the catalogue # 2102. 2.5 and 10.5 mm (mean 6.1 2.0 mm CW). No
significant differences in CW between the sexes were
RESULTS detected (P = 0.154).
The CW of males was, on average, 2.4 0.4
Relative growth (standard deviation) times the CL; for females and
In total, 246 males (42.2%), 263 females (45.1%) and juveniles, the means were 2.4 0.3 and 1.9 0.3,
74 juveniles (12.7%) of A. aidae were analyzed for respectively. Smaller individuals had, therefore, a
264 Lat. Am. J. Aquat. Res.

Table 1. Austinixa aidae. Regressions for body dimensions: carapace length (CL), abdomen width (AW), height of left
cheliped propodus (HQ), length of left cheliped propodus (LQ), wet weight (WW), and gonopod length (GL) versus the
carapace width (CW), separately for males, females and juveniles. Sample number (n), equation for total data (Total)
when no transition points are present, correlation coefficient (r), allometric level (a), positive (+), negative (-), isometric
(=), allometric growth constant (b). All measurements are in mm. All correlations were significant (P < 0.05).
Tabla 1. Austinixa aidae. Anlisis de regresin entre diferentes dimensiones corporales: Longitud del caparazn (CL),
ancho del abdomen (AW), altura del propodio del quelpodo izquierdo (HQ), longitud del propodio del quelpodo
izquierdo (LQ), peso hmedo (WW), longitud del gonoporo (GL) versus el ancho del caparazn (CW), anlisis separado
para machos, hembras y juveniles. Nmero de individuos (n), ecuacin de regresin (Total) cuando no estn presentes
puntos de transicin, coeficiente (r), alometria (a), positivo (+), negativo (-), isometra (=), constante de crecimiento
alometrico (b). Todas las medidas son en mm. Todas la correlaciones fueron significativas (P < 0,05).

Dimension Sex n Segment Y = aXb r a b


0.711
Males 246 Total CL = 0.671CW 0.967 - 0.711
CL Females 263 Total CL = 0.628CW0.764 0.956 - 0.764
Juveniles 74 Total CL = 0.743CW0.627 0.861 - 0.627
Males 244 Total AW = 0.303CW0.884 0.985 - 0.884
Females 97 < 5.1 AW = 0.139CW1.692 0.889 + 1.692
AW 164 5.1 < CW < 7.2 AW = 0.143CW1.783 0.715 + 1.783
> 7.2 AW = 0.597CW1.097 0.731 = 1.097
Juveniles 70 Total AW = 0.228CW1.197 0.916 + 1.197
Males 238 Total HQ = 0.096CW1.379 0.974 + 1.379
HQ Females 252 Total HQ = 0.114CW1.193 0.965 + 1.193
Juveniles 69 Total HQ = 0.156CW0.854 0.847 - 0.854
Males 102 < 5.1 LQ = 0.243CW1.197 0.949 + 1.197
136 > 5.1 LQ = 0.195CW1.312 0.949 + 1.312
LQ
Females 255 Total LQ = 0.275CW1.084 0.989 + 1.084
Juveniles 69 Total LQ = 0.308CW0.978 0.922 = 0.978
Males 108 < 5.7 WW = 0.00002CW4.557 0.808 + 4.557
110 > 5.7 WW = 0.0003CW2.834 0.957 - 2.834
WW Females 135 < 5.4 WW = 0.0001CW3.646 0.796 + 3.646
90 > 5.4 WW = 0.0002CW3.133 0.961 = 3.133
Juveniles 70 Total WW = 0.000008CW5.000 0.601 + 5.000
GL Males 31 < 3.0 GL = 0.134CW1.629 0.637 = 1.629
209 > 3.0 GL = 0.362CW0.876 0.974 - 0.876

slightly more rounded body than males and females, the frequency of this sexual category were also
whose carapaces become progressively narrower with identified. These features led us to characterize the
size. reproductive period as seasonal continuous.
As identified by dispersion points and values
obtained by the regression function between LQ and DISCUSSION
CW, males attain sexual maturity at 5.1 mm CW (Fig.
1d, Table 1). In females, sexual maturity also occurs Relative growth
from 5.1 mm CW, as indicated by the AW/CW The carapace length of males and females did not
relationship (Fig. 1b, Table 1). This value corresponds show significant changes in the allometric pattern
also to the smallest ovigerous females observed during during the growth. Only a few differences, for both
the study period. The ovigerous females occurred on sexes, were detected in the CL vs CW relationship.
almost all sampled months and seasonal increases in This pattern can be observed in many species of
Relative growth of symbiotic crab Austinixa aidae 265

Figure 1. Austinixa aidae. Relationships between width (CW) and: a) carapace length (CL), b) abdomen width (AW), c)
height of left cheliped propodus (HQ), d), length of left cheliped propodus (LQ), e) wet weight (WW), f) gonopod length
(GL). The arrows show the transition points (white arrows for females; black arrows for males).
Figura 1. Austinixa aidae. Representacin de diferentes relaciones biomtricas entre las variables dependientes a)
longitud del caparazn (CL), b) ancho del abdomen (AW), c) altura del propodio del quelpodo izquierdo (HQ), d)
longitud del propodio del quelpodo izquierdo (LQ), e) peso hmedo (WW), f) longitud del gonopodo (GL) versus ancho
del caparazn (CW) como variable independiente. Las flechas indican los puntos de transicin (flechas blancas para
hembras y negras para machos).
266 Lat. Am. J. Aquat. Res.

Brachyura (Hartnoll, 1982; Alves et al., 2005), occidentalis Rathbun, 1893, among others (see
including A. patagoniensis (Alves & Pezzuto, 1999; Zmarzly, 1992). The relationships involving the
Alves et al., 2005; Valena-Silva et al., 2008). In chelae indicate a smaller investment in the growth of
contrast, the abdomen allometry is one of the best this structure in females, probably due to absence of
dimensions to evidence sexual dimorphism in fights for territory, burrow construction or courting
brachyuran crabs (Hartnoll, 1974). The enlargement of behaviour, allowing females to allocate energy to the
the female abdomen is more evident in sexually somatic growth.
mature individuals (Hartnoll, 1982). In Pinnotheridae, The dimensions of the left and right chelar
the discontinuity in the relative growth of abdomen is propodus (HQ and LQ) of A. aidae represent reliably
related to the sexual maturity of females (Pohle & the size of these structures when compared with each
Telford, 1982; Bell, 1988; Alves & Pezzuto, 1999; other, considering that both sides do not differ in size,
Alves et al., 2005), probably related to pleopodial shape, and probably function. The same was observed
incubation mechanism. In the present study, a in A. patagoniensis in two different localities (Alves &
transition stage in female abdomen growth was Pezzuto, 1999; Alves et al., 2005). This similarity
apparent at 5.1 mm CW, which is probably the size at between both sides differs from the frequently pattern
the puberty molt. This estimate of maturity size observed in Brachyura with many levels of
coincided with the size of the smallest ovigerous heterochely (Hartnoll, 1982). The shape and size of
females captured (5.1 mm CW). In addition, another chelipeds are important parameters for brachyuran
transition point at 7.2 mm (CW) reflects the end of the lifestyles, since these structures are used in
increase in abdomen growth. As observed in the reproductive and agonistic interactions, as well as in
present study, the relative growth rate of the abdomen feeding (Negreiros-Fransozo & Fransozo, 2003). In
has a tendency to decrease as soon as it attains the mature individuals of A. aidae, the chelipeds are
functional size (Hartnoll, 1978). This occurs because strong with the palm quadrangular in males, and
any disproportionate increase in abdomen width could rectangular with convex edges in females (Melo,
reduce the efficiency of egg incubation, and creates 1996).
difficulties for the crabs locomotion (Hartnoll, 1982),
The wet weight of males showed a break in the
especially for pinnotherids which live associated with
continuity of dispersion points at 5.7 mm CW, which
hosts and are sometimes limited in terms of
may reflect the weight at sexual maturity, occurring
locomotion because of the small internal space
0.6 mm after the relationships involving the chelae. In
available. In addition, the pattern of sexual
females, a discontinuity of this relationship occurred
dimorphism in body size herein observed for A. aidae
at 5.4 mm CW, which is also related to the estimated
represents one of some other lines of reasoning that
size at sexual maturity. Although these results
argues in against the idea of social monogamy in this
corroborate the estimated sizes at maturity, they
species, which is polygynandrous (Peir et al.,
should be treated with caution because weight can be
submitted). In this sense, this topic need more work
strongly influenced not only by body size but also by
and to be experimentally explored in the future.
the nutritional state of individuals and the time of
In males it is possible to identify an interval in the year, which add variability to the data. The juveniles
dispersion points at 5.1 mm CW in the relationship did not show transition points in weight, probably
involving the maximum length of the cheliped because of limitations in the accuracy of the
propodus, which is related to the acquisition of sexual measurements and/or low variation in this dimension
maturity. The meaning of full chelar development during this life stage.
occurring only with maturity is related to economy of
Carapace size of male and female A. aidae was
resources, reducing the waste of energy on increase of
very similar. This pattern between both sexes appears
these structures causes during the initial instars
to be common among the members of this genus (A.
(Hartnoll, 1982). patagoniensis - Alves & Pezzuto, 1998; Alves et al.,
Females did not show noticeable changes of 2005; Valena-Silva et al., 2008; A. gorei -
allometry in the chelae, although the relationships McDermott, 2006), which may be related to the small
showed positive allometry. Some species of size attained by the specimens. However, some
Pinnotheridae have sexually dimorphic chelae, e.g.: differences in this size pattern were detected; for
Austinixa behreae (Manning & Felder, 1989), instance, females of A. aidae attained a slightly larger
Austinixa chacei (Wass, 1955), A. patagoniensis size (10.5 mm CW) than males (10.1 mm CW), which
(Rathbun, 1918), (see Manning & Felder, 1989), may indicate sexual differences in growth. Females
Pinnixa faba (Dana, 1851), Pinnixa littoralis Holmes, being larger than males is not a common pattern in
1894, Pinnixa minuscula Zmarzly, 1992, Pinnixa brachyurans, and differs from that found for
Relative growth of symbiotic crab Austinixa aidae 267

Table 2. Austinixa aidae. Maximum size of males and females, minimum size of ovigerous females and the known
reproductive periods of species of the genus Austinixa. All measures refer to carapace width (mm).
Tabla 2. Austinixa aidae. Tamao mximo de machos y hembras y tamao mnimo de hembras ovgeras y los periodos
reproductivos de especies del gnero Austinixa. Todas las medidas estn referidas al ancho del caparazn (mm).

Locality Maximum size Minimum size of Reproductive


Species References
(Latitude) Males Females ovigerous females period

Austinixa Balnerio Seasonal


11.5 11.5 8.0 Alves & Pezzuto (1998)
patagoniensis Cassino (3213S) (October to March)
Austinixa Balnerio
13.6 13.1 7.9 Continuous Alves et al. (2005)
patagoniensis Cambori (2659S)
Austinixa Ubatumirim Beach
9.5 9.4 6.7 No data available Valena-Silva et al. (2008)
patagoniensis (2320S)
Perequ-au Beach Present study; Peir &
Austinixa aidae 10.1 10.5 5.1 Seasonal continuous
(2324S) Mantelatto (2011)

A. patagoniensis in Brazil (Valena-Silva et al., 2008) combination with differences in food limitations and
(Table 2). The larger size attained by the females temperature between the two areas. Obviously, the
allows us to hypothesize that 1) they have a faster lack of information available on the size of specimens
growth rate than males, and 2) this may be along the species geographical distribution does not
advantageous because the larger size may be related to at present allow a comparative analysis. Reproduction
high reproductive potential and incubation of more is outside the scope of this paper, but it is important to
eggs. The physical space available for egg attachment highlight the possible influence of latitude on
is a limiting factor in decapods (Reid & Corey, 1991; reproductive period. Ubatuba is subtropical and a
Hines, 1982), and for associated pinnotherid crabs biogeographical boundary, where the geographical
there are still many questions to be answered, e.g., the distributions of many tropical species end and those of
reproductive features (fecundity, reproductive output), temperate and subantarctic species begin (Costa et al.,
and which aspects of the reproductive biology are 2000). This situation explains the continuous presence
adaptable to locally occurring environmental factors. of egg-bearing females of A. aidae in Ubatuba, in
Comparing the maximum size of A. aidae with contrast to the seasonal reproduction in the
other Austinixa species, A. aidae is slightly smaller southernmost population of A. patagoniensis (Table
than A. patagoniensis and larger than A. gorei, A. 2). The differences in minimum size attained by
cristata, A. behreae, and A. chacei (see Manning & ovigerous females for the different regions (Table 2)
Felder, 1989; Alves & Pezzuto, 1998; McDermott, also corroborate our hypothesis. The underlying
2006), which probably is related to differences in local reasons for these differences need to be investigated in
dynamics and hosts where the species live, and the future, in order to clarify these patterns.
including availability of resources in the environment,
effects of predation, and influence of latitude as well. Body features, maturity, and sexual dimorphism
These small size differences among the species and The carapace width of differentiated males and
sexes may be related to latitudinal variation. In terms females of A. aidae was, on average, 2.4 times the
of carapace size, the members of A. patagoniensis length, which corresponds to the principal adaptations
from the southernmost regions (32o and 26oS) are of Austinixa species to live in cryptic environments.
larger than at Ubatuba (23S) (Alves & Pezzuto, 1999; On the other hand the unsexed juveniles were
Alves et al., 2005). The pattern of mean size of the proportionally more rounded. This feature, is shared
specimens, with southern crabs reaching larger sizes, among species of Pinnixa and Austinixa, and has been
agrees with that proposed by Abele (1982), who suggested by various authors (Zmarzly, 1992; Heard
postulated that the size of crustaceans decreases with & Manning, 1997; McDermott, 2006) to represent an
decreasing latitude. According to Mantelatto et al. adaptation to the symbiotic lifestyle of these crabs,
(2010), the explanations for this size difference may which inhabit callianassid galleries and polychaete
be related to 1) less-stressful social and energy- tubes. The wider and slimmer (anterior-posterior)
demanding activities in the southern population, and body facilitates the locomotion inside the burrows
2) the possibility that this profile is acting in constructed by its hosts. The complexity of host use
268 Lat. Am. J. Aquat. Res.

pattern can be influenced by several factors that have suggestions, and to anonymous reviewers for their
not been evaluated by us as fitness payoffs to hosts suggestions and contributions toward the improvement
and their symbionts, spatial patterning or density of of this paper. The support of the Postgraduate Program
the host population, and the ability of symbionts to in Comparative Biology of FFCLRP/USP, and of the
recognize suitable hosts and to initiate and maintain Centro de Biologia Marinha (CEBIMar/USP) during
the symbiotic relationship (see Grove & Woodin, the collections are also acknowledged. We also thank
1996, for review). Dra. Janet Reid (JWR Associates) for revision on
In agreement with the recognized role of the English and Luis M. Pardo and Patricio Hernez for
cheliped and abdomen in reproductive functions in Spanish revision. All data collection was conducted
Brachyura (Hartnoll, 1982; Alves et al., 2005), and the according current applicable state and federal laws of
importance for determination of morphological Brazil.
maturation, the probable size of maturity for A. aidae
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Received: 15 June 2010; Accepted: 09 May 2011


Cryopreservation of the microalgae Chaetoceros calcitrans
Lat. Am. J. Aquat. Res., 39(2): 271-279, 2011 271
DOI: 10.3856/vol39-issue2-fulltext-8

Research Article

Cryopreservation of the microalgae Chaetoceros calcitrans (Paulsen):


analysis of the effect of DMSO temperature and light regime during different
equilibrium periods

Joan Sebastin Salas-Leiva1 & Enrique Dupr1


1
Universidad Catlica del Norte, Facultad de Ciencias del Mar
P.O. Box 117, Coquimbo, Chile

ABSTRACT. We evaluated the effect of three variables (cryoprotectant temperature, light regime, and time of
exposure to the cryoprotectant) throughout the equilibrium period during cryopreservation on the viability of
the microalga Chaetoceros calcitrans (Paulsen). For this, the cryoprotectant dimethyl sulfoxide (DMSO) at
5% (v/v) was added at three different temperatures (4, 10, and 25C) before placing the microalgae in
cryobiological straws for freezing. Once inside the cryobiological straws, the microalgal-cryoprotectant
suspensions were subjected to the following light regimes for 15 or 45 min: complete light, complete darkness,
light/darkness, and darkness/light. Suspensions were then frozen under controlled conditions and stored in
liquid nitrogen. The viability index proposed by Caavate & Lubian (1995b) was used to measure microalgal
viability after cryopreservation. Results indicated that it is necessary to use a cryoprotectant to ensure the
viable cryopreservation of C. calcitrans. Statistical analyses showed that the temperature of the DMSO
influenced the viability of cryopreserved microalgae and that there was no synergistic effect between the other
variables studied. The viabilities obtained with DMSO at 25C, 10C, and 4C were 34.9%, 27.8%, and 20.6%,
respectively.
Keywords: cryopreservation, diatoms, DMSO, temperature, light, equilibrium period.

Criopreservacin de las microalgas Chaetoceros calcitrans (Paulsen): anlisis del


efecto de la temperatura de DMSO y rgimen de luz durante diferentes
perodos de equilibrio

RESUMEN. Se evalu el efecto de tres variables la temperatura del crioprotector, el rgimen de luz y el
tiempo de exposicin al crioprotector durante el perodo de equilibrio en el proceso de criopreservacin
sobre la viabilidad de la microalga Chaetoceros calcitrans (Paulsen). Para ello se utiliz, el crioprotector
dimetilsulfxido (DMSO) al 5% (v/v), el cual fue adicionado a tres temperaturas diferentes (4, 10 y 25C)
antes de que las microalgas fueran introducidas dentro de pajuelas criobiolgicas para su congelacin. Una vez
dentro de las pajuelas, las suspensiones de microalgas con crioprotector se sometieron durante 15 o 45 min a
luz completa, oscuridad completa, luz/oscuridad y oscuridad/luz. Luego se congelaron de manera controlada y
se almacenaron en nitrgeno lquido. La viabilidad de las microalgas posterior a la criopreservacin fue
medida a travs del ndice de viabilidad propuesto por Caavate & Lubian (1995b). Los resultados indicaron
que es necesario el uso de criprotector para la criopreservacin viable de C. calcitrans. El anlisis estadstico
demostr que la temperatura del DMSO influye sobre la viabilidad de la microalga criopreservada y que no
existe efecto sinrgico entre las dems variables de estudio. Las viabilidades alcanzadas usando DMSO a
25C, 10C y 4C fueron de 34,9%, 27,8% y 20,6% respectivamente.
Palabras clave: criopreservacin, diatomea, DMSO, temperatura, luz, periodo de equilibrio.
___________________
Corresponding author: Joan Sebastin Salas-Leiva (jsalasleiva@gmail.com)

INTRODUCTION cultures. For example, species such as Chaetoceros


calcitrans offers high content of fat acids (EPA),
Microalgae used in aquaculture offer main nutritional antioxidants e immune system stimulants substances
requirements to vertebrate and invertebrate aqua- (vitamin C and B2), and its small size (2.5 to 6 m of
272 Lat. Am. J. Aquat. Res.

diameter) makes it strongly appropriated to feed (< 10%) and short equilibrium periods (< 30 min) at
mollusks, echinoderms, crustaceans and some low temperatures (0-10C) increase post-thawing
zooplankton like Artemia (Brown et al., 1997, 1999; viability (Tzovenis et al., 2004; Day, 2007). Other
Becker, 2004; Krichnavarruk et al., 2005; Khoi et al., studies suggest that high viability can be obtained with
2006). concentrations of approximately 20% CPA,
The intensive production of microalgae for feeding equilibrium periods between 30-45 min (or longer)
purposes, often face problems caused by loss of stock and temperatures of approximately 20C (Caavate &
cultures or nutritive quality of these microorganisms Lubian, 1994, 1995b, 1997a, 1997b; Poncet & Vern,
(Caavate & Lubian, 1995a; Day & Brand, 2005; 2003; Mitbavkar & Chandrashekar, 2006; Gwo et al.,
Mitbavkar & Chandrashekar, 2006; Gwo et al., 2005). 2005). These contrasting results have not only been
For that reason, aquaculture facilities always look reported in microalgae, but also in other
microorganisms (Hublek, 2003; Wu et al., 2008).
for strains of microalgae from subcultures or
Another important aspect during the equilibrium
cryopreserved collections with biochemical profiles
period is the chemical and osmotic stress induced by
suitable for feeding commercial species (Caavate &
the addition of CPAs. Under stressed conditions, the
Lubian, 1995b; Cordero & Voltolina, 1997; Day &
light irradiation of cells can damage the
Harding, 2007).
photosynthetic systems (photosystem II). This damage
Cryopreservation allows the viable storage of cells can be lethal, depending on the amount of time cells
or tissues over long periods of time at extremely low are exposed to stress, even if it is to low-light
temperatures (-196C), keeping them in a state of irradiation (Yordanov & Velikova, 2000; Murata et
suspended animation in which biological activity al., 2007).
practically stops (Saks, 1978). The main advantages of
Several microalgae species have been
microalgal cryopreservation are the immediate
cryopreserved with different methodologies obtaining
availability of strains for culture, low costs of
viabilities up to 100% (Caavate & Lubian, 1994,
maintenance of strains, optimal use of space and
1995a , 1995b). In the case of species of the genera
materials, and avoidance of genetic drift that could
Chaetoceros, Chaetoceros gracilis (Caavate &
occur through serial transfer when cultures are
Lubian, 1995b, 1997a) and Chaetoceros sp. (Cordero
maintained long-term (Kuwano et al., 2004). Despite
& Voltolina, 1997) have shown viabilities after
the importance of cryopreservation, its application to
cryopreservation lower than 40%. For the species
microalgae should be studied to better understand the
Chaetoceros muelleri, cryopreservation has been
degrees of susceptibility and sensitivity of these
successfully reported using DMSO 10% and 15%,
organisms to cryopreservation, such as: type of strain
however, there are not quantitative reports of viability
and the effect of cell size, shape, growth and rate (Rhodes et al., 2006).
phase, freezing and thawing rate, storage temperature
and duration, among others, that affect post-freezing On the basis of the information mentioned above,
viability (Mortain-Bertrand et al., 1996; Taylor & this study aims to analyze the effect of the DMSO
Fletcher, 1999; Rhodes et al., 2006; Day & Harding, temperature, time of exposition to this cryoprotectant
2007). and light regimen during the equilibrium period on the
post-cryopreservation viability of C. calcitrans.
Cryopreservation involves three stages:
equilibrium, freezing and thawing. To protect cells
throughout the process, cryoprotectant agents (CPAs) MATERIALS AND METHODS
are added before freezing (Fuller, 2004; Dumont et al.,
2006). During the equilibrium period, the microalgae- Culture of Chaetoceros calcitrans
cryoprotectant suspension is maintained for a A strain of C. calcitrans was obtained from the
predefined time to allow exchange between laboratory of Universidad Catlica del Norte at
intracellular solutes and the cryoprotectant solution. Coquimbo, Chile. Two flasks of 250 mL were used to
Three important variables are related to the use of establish two 120 mL cultures using Guillard &
CPAs: concentration, temperature and time of Ryther (1962) medium enriched with silicate (30
exposure, and there are different methods of handling Na2SiO3.9H2O). Cultures non axenic but free of
them reported in literature. For example, tests with protozoan and bacteria (genera Vibrio) were
DMSO concentrations ranging from 1 to 32%, maintained at 20C, under continuous irradiation at 65
equilibrium periods lasting from 10 to 240 min and mol photons m-2 s-1 provided with cold light lamps
temperatures ranging between 4 and 23C (Panis et (Philips TL-TRS 40W/54). One culture was labeled as
al., 1990), have indicated that low CPA concentrations t and the other, as d. Both t and d cultures were
Cryopreservation of the microalgae Chaetoceros calcitrans 273

harvested on the 5th day. The t culture was carried to All tests were carried out using a CryoLogic CL-
intermediate culture with a volume of 1400 mL under 3300 freezing system and the CryoGenesis V5
the conditions of culture media, temperature, and software. The temperature of the straws was
irradiation (same conditions above mentioned). The d diminished starting at treatment temperatures (4, 10,
culture, was used to estimate a growth curve using and 25C) down to -4C, using a cooling rate of 3C
different initial densities. Seven cultures of 120 mL min-1. This temperature was held for 1 min and
were inoculated with approximately 95000 (d1), continuing with the freezing at the same cooling rate
360000 (d2), 865000 (d3), 970000 (d4), 1310000 (d5), down to -60C (held for 10 min). Finally, the straws
1585000 (d6) and 2565000 (d7) cells per mL-1. were placed in liquid nitrogen (-196C) and stored
Growth according to initial and final densities was until evaluation.
analyzed based on a function of potential correlation Samples were thawed using a water bath at 25C
with the equation Y= aXb (Caavate & Lubian, for 2 min and the content of the straws was distributed
1995b). in 1.5 mL Eppendorf tubes. Culture medium was
The t culture was used to perform cryopreservation added step-by-step to a 0.1 mL aliquot of microalgae-
tests. To begin treatments, the intermediate t culture cryoprotectant solution of each treatment in tubes.
was harvested on the 6th day and placed in 50 mL Each tube was used to carry out a 10 mL culture under
tubes, which were then centrifuged at 2500 rpm for 10 the same growth conditions described previously. Cell
min. The microalgal pellet obtained was resuspended density was measured every day from the inoculation
and distributed into three 50 mL tubes to carry out all day until day 5 using a Neubauer counting chamber
treatments (each tube was considered a replicate of the under a phase-contrast photon microscope (Nikon
entire experiment and also was used to make its own Optiphot).
control).
Evaluation of growth and viabilities
Cryopreservation procedures Culture growth curves were estimated using
To apply treatments, 0.30 mL microalgal concentrate exponential correlation. Specific growth () of C.
from intermediate t culture were placed in 1.5 mL calcitrans was calculated using the following
Eppendorf tubes. The stock solution of the equation:
cryoprotectant dimethyl sulfoxide (DMSO) was
(day-1) = [Ln(Cf/Ci)]/(tf- ti) (1)
prepared at 10% (v/v) with autoclaved and micro
filtered seawater and it was added at a ratio of 1:1 where Ci is the initial cell concentration; Cf, the final
(microalgae:cryoprotectant) to each sample at three cell concentration; and t, the time of culture in days.
temperatures (4, 10, and 25C). Final cryoprotectant Specific growth () was calculated after the adaptation
concentration was 5% (v/v). At each temperature, the phase. Growth curves were illustrated for each
microalgae-cryoprotectant suspensions were intro- treatment according to Affan et al. (2007).
duced into 0.5 mL straws (IMV France) and sealed The viability index (V) proposed by Caavate &
with polyvinyl alcohol (Sigma). The equilibrium Lubian (1995b) was used to estimate post-
period lasted 15 or 45 min while the straws were cryopreservation viability:
exposed to four light regimes: complete light,
V = [(C0/Ci)x(C5/(aC0b)] x 100 (2)
complete darkness, light/darkness and darkness/light.
Light and darkness in the latter two regimes were where C0 is the inoculation density (day 0); C5, final
distributed equally as follows: for the 15 min period, density for day 5 of culture; Ci, maximum initial
straws with microalgae were exposed to 7.5 min light density (dilution 1:100 prior to cryopreservation); a
and 7.5 min darkness and vice versa; for the 45 min and b, are regression coefficients obtained for 5 days
period, straws were exposed to 22.5 min light and 22.5 in relation to C0 in the d cultures.
min darkness and viceversa (Table 1). Light
The term aC 0 b is equivalent to the expression
irradiation in each treatment was the same mentioned
in culture conditions. aX b in a potential equation.
To compare the effect of cryopreservation with and The experiment corresponded to a completely
without DMSO, additional tests were carried out at randomized factorial design that generated 24
temperatures of 4, 10, and 25C and with 15 min of treatments (Table 1), each with three replicates. Three
equilibrium period under complete light. All straws non-cryopreserved controls and d cultures were
were filled as described before but sterilized available throughout the process. Viability indexes (V)
microfiltered seawater was added instead of the were calculated for each replicate and were compared
cryoprotectant. using a factorial ANOVA, followed by Duncans
274 Lat. Am. J. Aquat. Res.

Table 1. Light regime, temperature, and time of exposure of microalgae to DMSO during the equilibrium period for the
different treatments (T).
Tabla 1. Rgimen de luz, temperatura y tiempo de exposicin de las microalgas durante el tiempo de equilibrio para los
diferentes tratamientos (T).

Light regime Complete light Complete darkness Light/darkness Darkness/light


Time of exposure DMSO temperature (C)
(min) 4 10 25 4 10 25 4 10 25 4 10 25
15 T1 T9 T17 T2 T10 T18 T3 T11 T19 T4 T12 T20
45 T5 T13 T21 T6 T14 T22 T7 T15 T23 T8 T16 T24

multiple range tests. All statistical analyses were Specific growth ( day-1) was higher in cultures of
performed with a 95% confidence level ( = 0.05) cryopreserved cells than in non-cryopreserved cells
using Statsoft statistics software version 7 (Statsoft, (controls). Growth curves of treatments, as well as,
UK). specific growth rates were similar to those reported for
d cultures. The highest specific growth rates in
RESULTS cryopreserved treatments were reached with the
treatment with the lowest cell densities (treatments 17,
Non-cryopreserved cultures (controls) 15, and 13) and conversely, low specific growth rates
Cell growth was similar in controls of all replicates were reached with treatments with higher cell
and there were no significant differences among them densities (treatments 22, 23, and 18) (Table 2). Of the
(P > 0.05). Growth curves showed correlation treatments with DMSO at 4 and 10C, 93.75%
coefficients ranging between 0.86 and 0.89. Average presented average growth rates above 1 ( day-1),
initial density and on the fifth day were 2.0 x 106 cells whereas only 50% of the treatments with DMSO at
mL-1 and 3.5 x 106 cells mL-1respectively. Controls 25C exceeded that same growth rate. Controls
and d cultures showed similar growth tendencies (Y = presented a growth rate of 0.11 day-1.
aebx). The specific growth rate was faster in cultures
Estimation and comparison of viability
obtained from inoculations with low cell density mL-1
(Table 2). The correlation aXb for d cultures indicated The average initial concentration (Ci) before
an inverse relationship between initial and final cryopreservation was of 2.0 x 106 cells mL-1. The
inoculation densities (Y = 1 x 106 X-0.072; R2 = 0.8325). viability of C. calcitrans in all cases was higher than
12.2% (treatment 15) and did not exceed 34.9%
Cryopreservation of Chaetoceros calcitrans (treatment 22) (Table 2, Fig. 2). A factorial ANOVA
was performed to identify those variables that most
Post-cryopreservation cultures
influence the viability of cryopreserved C. calcitrans.
All cryopreservation tests without DMSO at 4, 10 and Data (proportion of viability) presented a normal
25C, resulted in complete cell death on day 2 of frequency distribution according to the Kolmogorov-
culture post-cryopreservation. In those treatments Smirnov test (P > 0.05), and variance homogeneity
using DMSO, different percentages of viability were was verified according to Levenes test (P > 0.05).
observed after thawing (day 5). Hypotheses of the statistical model and their
Initial culture densities of post-cryopreservation interactions were compared by parametric statistical
treatments at time of inoculation (C0) ranged between analysis, which indicated that only the temperature of
3.1 x 105-7.7 x 105 cells mL-1, and densities on day 5 DMSO had a significant effect (P < 0.05) on the
of culture (C5) varied between approximately 2.5 x viability of cryopreserved C. calcitrans (Table 3).
106-3.7 x 106 cells mL-1. Growth curves of the 24 Duncan multiple range analysis, performed after the
treatments exposed to cryopreservation exhibited an factorial ANOVA, revealed significant differences
adaptation phase within the first two days of culture. between the temperatures of 4 and 25C and between
High cell death and low densities were observed on 10 and 25C (P < 0.05), whereas there were no
day 2 in all cultures. From day 3 on, evidence of an significant differences between the temperatures of 4
exponential growth phase was determined from a high and 10C. Although analyses indicated that the light
cell growth rate (Fig.1). regimen had no statistically significant effect, average
Cryopreservation of the microalgae Chaetoceros calcitrans 275

Table 2. Growth rates ( day-1) and viabilities indexes of Chaetoceros calcitrans. Controls, d cultures and treatments.
Tabla 2. Tasas de crecimiento ( dia-1) e ndices de viabilidad para Chaetoceros calcitrans. Controles, cultivos d y trata-
mientos.

Treatment day-1 Viability index (%) Treatment day-1 Viability index (%)
Control 0.11 0.04 9 1.16 0.22 21.5 2.72
d1 1.28* 10 1.25 0.49 21.1 12.78
d2 0.83* 11 1.05 0.32 22.9 3.53
d3 0.51* 12 1.30 018 21.5 11.10
d4 0.47* 13 1.41 0.19 14.1 0.89
d5 0.35* 14 1.01 0.35 27.8 17.55
d6 0.28* 15 1.58 0.04 12.2 3.08
d7 0.10* 16 1.10 0.45 19.5 12.54
1 1.10 0.13 19.1 6.90 17 1.67 0.30 16.7 11.57
2 1.28 0.41 15.5 7.64 18 0.75 0.23 31.7 7.71
3 1.20 0.25 18.5 9.89 19 1.03 0.19 29.0 10.60
4 1.15 0.38 20.6 1.94 20 0.88 0.06 23.5 4.73
5 0.88 0.15 19.3 13.75 21 1.09 0.17 14.8 6.53
6 1.16 0.23 15.6 8.44 22 0.70 0.03 34.9 7.82
7 1.03 0.18 16.6 9.25 23 0.77 0.08 32.7 7.84
8 1.09 0.28 16.0 4.96 24 1.04 0.38 21.4 14.43
*single measurements
Data highlighted in bold indicates the highest viabilities.

Figure 1. Growth curves of all treatments exposed to


cryopreservation (numbers to the right indicate
treatments; Ctrl: control).
Figura 1. Curvas de crecimiento de todos los trata-
mientos sometidos a criopreservacin, (Nmeros a la
derecha: indica el tratamiento y Ctrl: control).

viability tended to increase with complete darkness in other species. For example, adaptation phases
and a 15 min of time of exposure. longer than 1 day have been reported for Chaetoceros
muelleri and C. gracilis, Tetraselmis tetrathele and T.
DISCUSSION gracilis, Dunaliella salina and D. tertiolecta, and
Navicula incerta, among others (Caldern & Serpa,
Growth and cryopreservation 2003; Leal et al., 2003; Affan et al., 2007; Moura-
Cell growth of Chaetoceros calcitrans was similar in Junior et al., 2007). The specific growth rates of d
both d and t cultures (prior to cryopreservation). No cultures were higher with low densities of inoculated
adaptation phase was detected in either culture. If it cells as it was expected; since they are conditioned by
did occur, it was very mild, similar to that reported by factors such as nutrient depletion, pH alteration, CO2
Phatarpekar et al. (2000) for the same species; this deficiency, and reduced light penetration, among
could be attributed to faster cellular reproduction than others (Fogg & Than-Tun, 1960).
276 Lat. Am. J. Aquat. Res.

It was only possible to generate viable cell cultures of


C. calcitrans when DMSO was added. Low or no
viability has been reported for the species C. gracilis
(Caavate & Lubian, 1995b), Chaetoceros sp.
(Cordero & Voltolina, 1997), and Nannochloropsis
oculata (Gwo et al., 2005) in the absence of CPA.
Although viabilities up to 69% have been obtained
without using CPA for Tetraselmis chuii,
Nannochloropsis gaditana and Nannochloris atomus
(Caavate & Lubian, 1995b) and, certain
Chlorococcaceae and Cyanobacteria (Day et al.,
2000). Such differential responses to cryopreservation
(with/without cryoprotectant) depend directly on each
species physiological mechanisms to tolerate osmotic
stress induced by below-zero temperatures. In the case
Figure 2. Effect of temperature of DMSO (5%) during of C. calcitrans, its reaction to cryopreservation
the equilibrium period on viability of Chaetoceros without DMSO could be explained by the excessive
calcitrans. dehydration at the intracellular level caused by the
Figura 2. Efecto de la temperatura del DMSO (5%) formation of extracellular ice crystals that promote
durante el perodo de equilibrio sobre la viabilidad de cell death (Tanaka et al., 2001; Day & Harding, 2007).
Chaetoceros calcitrans.

Table 3. Factorial variance analysis (ANOVA) of viability post-cryopreservation of C. calcitrans. SS: sum of squares.
DF: degrees of freedom. SM: square of the mean, and F values and P value.
Tabla 3. Anlisis de Varianza Factorial (ANOVA) de la viabilidad posterior a la criopreservacin de C. calcitrans. SS:
Suma de cuadrados. DF: grados de libertad. SM: Cuadrado de la media, F y P (estadsticos).

Variable SS DF SM F value P value


Temperature (DMSO) 0.079 2 0.039 4.638 0.014
Light regime 0.044 3 0.014 1.735 0.172
Time of exposure 0.003 1 0.003 0.408 0.525
Temperature x light regime 0.094 6 0.015 1.841 0.110
Temperature x time of exposure 0.004 2 0.002 0.290 0.749
Light regime x time of exposure 0.013 3 0.004 0.521 0.669
Temperature x light regime x time of exposure 0.019 6 0.003 0.375 0.891
Error 0.411 48 0.008

Mechanical damage, cannot be discarded because accumulation of free amino acids (mainly proline) and
several organelles could have been destroyed. The DMSP (a DMSO precursor) (Ferrario et al., 2004;
responses to cryopreservation obtained in this study, Mock & Thomas, 2005; Houdan et al., 2005; Ralph et
as well as the results of Cordero and Voltolina (1997) al., 2005).
in Chaetoceros sp., suggest that the presence of CPAs
is necessary for post-freezing cell recovery in Effectiveness of cryopreservation
Chaetoceros microalgae as in other microorganisms. The maximum mean viability reached in this study
DMSO has shown high levels of toxicity in several was 34.9%. In studies conducted by other authors
species (Caavate & Lubian, 1994; Fuller, 2004). (Caavate & Lubian, 1995b, 1997a, 1997b), the
Although in the case of C. calcitras was indispensable viabilities of different non-diatom microalgae treated
to obtain viable cells after criopereservation, which with CPA reached 100%, whereas viabilities for
indicates a natural tolerance to this kind of substances diatoms such as C. gracilis were below 40%, this
in its cytoplasm. Natural tolerance for freezing and suggests that, within the physiological mechanisms of
hiperosmotic substances in other diatoms of this diatoms to respond to osmotic stress, the presence of a
genera, such as Chaetoceros castracanei and species rigid silicon wall seems to play an important role in
from Artic and Antartic, has been attributed to the cryopreservation because it could confer fragility to
Cryopreservation of the microalgae Chaetoceros calcitrans 277

the cryopreserved cell (rupture during freezing or penetrating cryoprotectant and does not require a
thawing). Mortality caused by that fragility could be prolonged equilibrium period to yield good results, as
minimized, in the case of C. calcitrans, by the high compared with slow-penetrating CPAs, such as
surface/volume ratio of this species, which, would glycerol, that need more than 60 min (Karlsson &
help reduce the formation of intracellular ice Toner, 1996; Day et al., 1998; Hublek, 2003; Fuller,
(Mortain-Bertrand et al., 1996). However, this should 2004). The DMSO rate of penetration during the
not be considered a rule for small-sized diatoms equilibrium period depends on cell size and type,
because other factors, such as rate of freezing and differential permeability of cell membranes, and
thawing, also affect microalgae viability, regardless of membrane lipid content. Therefore the lengths of
the inherent conditions of the cells and growth effective equilibrium periods vary from species to
conditions (Ben-Amotz & Gilboa, 1980a, 1980b; species (Salinas-Flores et al., 2008). Norton & Joiner
Caavate & Lubian, 1997a, 1997b; Day et al., 1998). (1968) reported DMSO 7.5% and equilibrium periods
The analysis of the variation of V indicated that the up to 149 min to cruopreserve sporocites of Eimeria
temperature of DMSO during the equilibrium phase is tenella due its low permeable membrane.
the factor that most influences post-freezing viability There are no reports on the effect of using light
of C. calcitrans. The Duncan multiple range test regimens during the equilibrium period similar those
indicated that viability at 4 and 10C is lower than at used in this study. The light regime results did not lead
25C. Based on these results, the optimal temperature to the detection of significant differences in viability;
of DMSO during the equilibrium phase of however, it is interesting to note a pattern of low
cryopreservation of C. calcitrans is 25C. This viabilities seen in those treatments that included
temperature is close to the range mentioned by Taylor complete light. This result could be attributed to
& Fletcher (1999), who recommended using alteration or damage in the electron transport system.
equilibrium temperatures between 18 and 23C, as This has been described for the green algae
well as to that proposed by other authors (Caavate & Chlamydomonas reinhardtii where severe damage was
Lubian, 1995b,1997a, 1997b), who obtained high observed in the electron transport chain when the
viabilities (> 90%) with different microalgae species. algae was exposed to methanol in the presence of light
Studies conducted by Tanaka et al. (2001) also during the equilibrium period. Piasecki et al. (2009)
indicated that temperatures close to 23C facilitate the recommend that these microorganisms be cultured
osmotic exchange of DMSO solution and the cell under very low light or in complete darkness during
during the equilibrium period, because increasing this phase.
temperatures increase molecular movement and Finally, post-cryopreservation cell survival or
kinetic energy of the H2O-DMSO solution; this causes mortality can be mainly attributed to the existence of
DMSO diffusion to proceed faster at 25C with the several levels of genetic variability (Medlini et al.,
appropriate solute concentration than at 4 and 10C. In 2000), which would be responsible for the differential
this study, when DMSO was added at 4 and 10C, response of C. calcitrans cells to osmotic stress and
average V were lower than 20%, contrary to what was post-freezing survival lower than 100% (Fahy, 1986).
found by other authors (Panis et al., 1990; Mortain-
Bertrand et al., 1996; Hublek, 2003) who suggested
that temperatures between 0 and 10C during the ACKNOWLEDGEMENTS
equilibrium period are appropriate for cryopre-
servation because they protect the cells from CPA This study was supported by Fondef Grant D05 I-
toxicity since at physiological temperatures, the 10246. Our sincere appreciation to Dr. Dayana Salas-
cryoprotectant is highly toxic. We suggest that it is Leiva for her assistance in the statistical design of this
more important to ensure the entry of DMSO into the study, the critical reading of the manuscript, and her
cell than to try to minimize its toxicity because the helpful comments. We want to thank to Roberto
freezing/thawing process apparently has a more Garca for his help during the experimental phase of
traumatic effect than that induced by CPA toxicity. this study.
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DOI: 10.3856/vol39-issue2-fulltext-9

Research Article

Assessment of catalase activity, lipid peroxidation, chlorophyll-a, and


growth rate in the freshwater green algae Pseudokirchneriella subcapitata
exposed to copper and zinc

Paulina Soto1, Hernn Gaete1,3 & Mara Eliana Hidalgo2


1
Departamento de Biologa y Ciencias Ambientales
2
Departamento de Qumica y Bioqumica
3
Centro de Investigacin y Gestin de Recursos Naturales (CIGREN), Facultad de Ciencias
Universidad de Valparaso, Valparaso, Chile

ABSTRACT. In this work, the effect of copper and zinc on green alga Pseudokirchneriella subcapitata was
evaluated through catalase activity, lipid peroxidation by TBARS essay, growth rate, and the chlorophyll-a
concentration. Catalase activity increased significantly (P < 0.05) in comparison to the control at 0.1 mg L-1
copper and 0.075 mg L-1 zinc, whereas the damage to the cell membrane expressed as nmols/106cell of
malondialdehyde increased significantly (P < 0.05) at 0.025 mg L-1 copper and 0.1 mg L-1 zinc. On the other
hand, a significant (P < 0.05) decrease in chlorophyll-a concentration was found at 0.075 mg L-1 of both
metals. The results showed that catalase activity, lipid peroxidation, and chlorophyll-a concentration were
more sensitive to metals than the growth rate.
Keywords: toxicity, bioassays, water quality, oxidative damage, Pseudokirchneriella subcapitata, Chile.

Evaluacin de la actividad de la catalasa, peroxidacin lipdica, clorofila-a y tasa de


crecimiento en la alga verde de agua dulce Pseudokirchneriella subcapitata
expuesta a cobre y zinc

RESUMEN. En este trabajo, se evalu el efecto del cobre y zinc en la alga verde Pseudokirchneriella
subcapitata a travs de la actividad catalasa, peroxidacin lipdica por el ensayo TBARS, tasa de crecimiento
y concentracin de clorofila-a. La actividad catalasa aument significativamente (P < 0,05) en comparacin al
control en 0,1 mg L-1 y 0,075 mg L-1 de cobre y zinc respectivamente, mientras que el dao en la membrana
celular expresado en nanomols/106 clulas de malondialdehdo aument significativamente en 0,025 mg L-1 y
0,1 mg L-1 de cobre y zinc respectivamente. Por otra parte, hubo una disminucin significativa (P < 0,05) en la
concentracin de clorofila-a en ambos metales a 0,075 mgL-1. Los resultados mostrados en actividad catalasa,
peroxidacin lipdica y concentracin de clorofila-a son parmetros ms sensibles que la tasa de crecimiento a
los metales.
Palabras clave: toxicidad, bioensayos, calidad de agua, dao oxidativo Pseudokirchneriella subcapitata,
Chile.
___________________
Corresponding author: Hernn Gaete (hernan.gaete@uv.cl)

INTRODUCTION an essential redox-active transition metal, which acts


as a structural element in regulatory proteins, and
Metals such as copper and zinc are released into the participates in electron transport in photosynthesis,
aquatic ecosystems by anthropogenic activities such as mitochondrial respiration, oxidative stress responses,
agricultural, industrial and mining (Yruela, 2005). In cell wall metabolism and hormone signaling (Moreno,
this ecosystems the primary producers play an 2003; Srivastava et al., 2006). Zinc is essential for the
important role in the structure and functioning of stability of cell membranes in the activation of over
aquatic ecosystems. Any negative effect on them will 300 enzymes in the metabolism of proteins and
affect upper trophic levels (Li et al., 2006). Copper is nucleic acids (Cakmak & Marschner, 1988). However,
281 Catalase, lipidperoxidation, chlorophyll-a and growth in P. subcapitata exposed to copper and zinc

in high concentrations these metals can be toxic to The goal of this study is to evaluate the effect of
aquatic organisms (Srivastava et al., 2006). copper and zinc on P. subcapitata, through the activity
The metals, as other environmental factors of catalase, lipidperoxidation by TBARS assay,
(ultraviolet light, extreme temperatures, radiation, growth rate and concentration of chlorophyll-a.
environmental pollution, etc.) induce ROS (reactive
oxygen species) formation inside the cell (Marshall & MATERIALS AND METHODS
Newman, 2002). These ROS are formed under
physiological conditions in manageable proportions, The green alga species Pseudokirchneriella
while maintaining a balance due to the defensive subcapitata, belonging to the order Chlorococcales,
cellular enzymes (Drge, 2003). The breakdown of class Chlorophyceae, was acquired in the Laboratory
this balance is known as oxidative stress, which results of Phycology of University of Concepcin, Chile.
in alterations of the structure-function of organs,
systems, or specialized transport (Ames et al., 1993). Bioassays
The damage caused by oxidative stress in fatty acid The bioassays were carried out according to the
rich structures, such as cell membranes, results in lose Chilean standard NCh2706 (2002). Prior to the
rigidity, integrity and permeability. This process bioassay a nutrient solution consisting of five stock
known as lipidperoxidation, produces carbonylic solutions, which contain: micronutrients, macro-
compounds such as malondialdehyde. Aerobic nutrients, Fe-EDTA, trace elements and NaHCO3 was
organisms have developed antioxidant defence prepared. The algae was inoculated into 500 mL
mechanisms to prevent cell damage by ROS (Finkel & Erlenmeyer flasks in an equal volume for all samples,
Holbrook, 2000; Sohal et al., 2002). The enzyme from culture stock during the exponential phase of
catalase has an active participation in the reactions that growth. Then, they were enriched with the nutrient
reduce the intracellular levels of H2O2 formed from concentration to avoid false negatives, and volumes of
the superoxide radical (De Zwart et al., 1999). copper sulphate pentahydrate (CuSO4.5H2O) and zinc
Although copper can act at many different levels in sulphate heptahydrate (ZnSO4. 7H2O) were added
the cell, one of the most important mechanisms of until a concentration of 0.025, 0.05, 0.075 and 0.1 mg
copper action in green plants is believed to be the L-1 of Cu and Zn respectively. Finally, the flask was
inhibition of electron transfer in the chloroplasts, the adjusted to 300 mL with distilled water. Additionally,
destruction of the chloroplast membrane, and a blank was prepared containing only the inoculum of
inhibition of the photosynthetic pigments formation P. subcapitata, nutrients and water. Each treatment
(Yan & Pan, 2002; Charles et al., 2006). and the blank, in triplicate, was exposed to continuous
The microalga of freshwater Pseudokirchneriella cool white light with a low intensity of 90 10 mol
subcapitata has been used in toxicity bioassays due to m-2 s-1, at 23C 2C and shaken by hand every day.
their sensitivity to chemicals agents. In these tests, the To have a biomass of microalgae that would make the
exposed population rate growth is the response determinations, the exposure time was 15 days. The
variable determinated (NCh2706, 2002). At present, it cell density (n) was determined at the beginning and
is known that the molecular alterations are the first the end of the bioassay counting directly in a
detectable, quantifiable responses, allowing the microscope using a Neubauer Bright Line
evaluation of exposure to agents at sublethal level. hemacytometer.
The biomarker concept is based in that the first level The growth rate (k) expressed as number of cell
of interaction of pollutants with organisms is the duplications was determined from:
molecular-cellular (Huschek & Hansen, 2005). k = 3,322 x log Nn log N0
The studies on oxidative stress caused by metals in tn
microalgae are few, the most are in green plants
(Okamoto et al., 1996; Lee & Shin, 2003; Elisabetta & Where tn is the time elapsed between the start and
Gioacchino, 2004; Mallick, 2004; Li et al., 2006). end of the trial (in days), N0 is the nominal initial cell
The lipidperoxidation`s products determination density and Nn is the density at the end of the test.
(TBARS), together with the evaluation of the catalase
activity are effective methods used to assess oxidative Chlorophyll-a
stress (Scandalios, 1997; Nordberg & Arne, 2001). In To determine the chlorophyll-a concentration, 100 mL
this research is proposed that the molecular response of the sample was filtered and immersed in acetone
is more sensitive than the response at the population (90% V/V) for 20 h in darkness and cold. The
level in P. subcapitata exposed to copper and zinc. absorbance of the solvent was determined at 630, 645
Lat. Am. J. Aquat. Res. 282

and 665 nm in a spectrophotometer (Cecil CE 2000


model 2041). The chlorophyll-a concentration was
calculated through the Richards & Thompson (1952):
mg chl-a m3 = (15, 6 E665 2 E645 0,8 E630) x 10
V
Where E665 is the absorbance at 665 nm, E645 the
absorbance at 645 nm, E630 at 630 nm and V the
volumen sample leaked.

Oxidative stress parameters


A volumen of 200 mL of each treatment was Figure 1. Growth rate of P. subcapitata exposed to
centrifuged and frozen with liquid nitrogen before copper and zinc *: significant difference to the control (P
grinding it with a mortar. Two mL of buffer 50 mM < 0.05)( n:4).
sodium phosphate (pH 7.0) were added to obtain an Figura 1. Tasa de crecimiento de P. subcapitata
approximate volume of 3 mL, 1 mL of which was expuesta a cobre y zinc *: diferencia significativa al
used to measure thiobarbituric acid reactive species control (P < 0,05).
(TBARS) and the remaining 2 mL to determine the
enzymatic activity of catalase (CAT).
trations (Table 1) were observed. The concentration of
chlorophyll-a decreased significantly at copper
Determination of thiobarbituric acid reactive
concentration 0.05 mg L-1 and zinc concentration
species (TBARS)
0.075 mg L-1. However an increase of chlorophyll-a at
Lipidperoxidation was determined using the TBARS 0.025 mg L-1 of copper was observed (Fig. 2). Only
assay: samples were treated with trichloroacetic acid the correlation with zinc was significant (Table 1).
and then with thiobarbituric acid, the complex formed
The catalase activity increased in comparison to
absorbed at 540 nm, the results are expressed in
the control in 0.075 mg L-1 and 0.05 mg L-1 of copper
nanomoles of MDA/106 cells. MDA content was
and zinc, respectively (Fig. 3). Zinc induced the
calculated using the calibration curve of MDA bis
activation of the antioxidant enzyme catalase at lower
dimethylacethal.
concentration than copper. The correlation between
metal concentration and catalase activity was
Catalase activity (CAT)
significant only for zinc (Table 1). There was
The enzymatic activity of catalase was determined, by significant correlation between lipid damage
spectrophotometry following the hydrogen peroxide expressed as malondialdehyde content and catalase
degradation rates for 1 min every 15 sec, at 240 nm activity (Table 1). The lipid damage in the cell
which is accelerated in the presence of enzyme membrane was higher with copper than zinc. The
(Ratkevicius et al., 2003; Contreras et al., 2005; damage was observed in exposure to 0.025 mg L-1
Cargnelutti et al., 2006; Hidalgo et al., 2006). The copper, while for zinc it was observed at 0.1 mg L-1
sample (2 mL) was concentrated by centrifugation at (Fig. 4). In this case, the correlation between damage
3500 rpm for 15 min. A blank (2.9 mL sodium to the cell membrane expressed as nmols/106cell of
phosphate buffer pH 7.0 and 100 mL of supernatant) malondialdehyde was significant to copper and zinc
was used. The results are expressed as U/106 cells (Li (Table 1).
et al., 2006). The results were analyzed through the
analysis of variance Anova and correlation determined DISCUSSION
with the program Systat 5.0. For each treatment three
replicates were considered. Copper was more toxic than zinc in relationship at the
rate growth, chlorophyll-a content and, lipope-
RESULTS roxidation endpoints, wich is similar to what was
reported by Utgikar et al. (2004) in Vibrio fischeri.
The growth rate of P. subcapitata exposed to copper However, copper toxicity was lower than what was
decreased at 0.075 mg L-1, while in the presence of found by Kaneko et al. (2004); these autors reported
zinc no statistically significant differences to the an IC50 at 0.11 mg L-1 of copper in Selenastrum
control was found in the range of concentration tested capricornutum, similar values were reported by
(Fig.1), however correlations with metal concen- Bossuyt & Janseen (2004) in the same species, our
283 Catalase, lipidperoxidation, chlorophyll-a and growth in P. subcapitata exposed to copper and zinc

Table 1. Correlation between measured parameters.


Tabla 1. Correlacin entre los parmetros medidos.

Concentration CatCu CatZn ClofCu ClofZn MdaCu MdaZn


CatCu 0.71
CatZn 0.98* -
ClofCu 0.74 -0.53 -
ClofZn -0.93* - -0.96*
MdaCu 0.92* 0.93* - -0.69
MdaZn 0.81 - 0.78 - -0.88*
Cu -0.88* -0.92* - 0.74 - -0.98*
Zn -0.90* - -0.95* - 0.90* - -0.78
Concentration : metal concentrations; CatCu: catalase activity exposured to copper; CatZn: catalase
activity exposured to zinc; ClofCu: Chlorophyll-a exposured to copper; ClofZn: chlorophyll-a exposure
to zinc; MdaCu: MDA production exposured to copper ; MdaZn : MDA production exposured to
zinc; Cu: growth rate exposured to copper; Zn: growth rate exposured to zinc. *: indicate significant
correlation (P < 0.05).

Figure 2. Chlorophyll-a concentrations in P. subcapitata


exposed to copper and zinc. *: significant difference to
the control (P < 0.05).
Figura 2. Concentracin de clorofila-a en P. subca- Figure 4. Effect of copper and zinc different
pitata expuesta a cobre y zinc. *: Indica signifi- concentrations on MDA production in P. subcapitata. *
cativamente diferente al control (P < 0,05). :Indicate significantly different to the control (P < 0.05).
Figura 4. Efectos del cobre y zinc a diferentes
concentraciones sobre la produccin de MDA en P.
subcapitata. *: Indica significativamente diferente al
control (P < 0,05).

study show that at copper concentration similar the


inhibition on the rate growth was less to twenty
percent. The differences may be due to the chemical
characteristics of test water, such as pH, hardness,
time exposure, concentration and type of chelating
agent in the nutrients used in the these studies. On the
Figure 3. Catalase activity in P. subcapitata exposed to other hand, the differences in the effects of the
copper.and zinc. *: significant difference to the control respective metals could be attributed to the redox
(P < 0.05). potential of the metals. Copper has a greater redox
Figura 3. Actividad catalasa en P. subcapitata expuesta potential that zinc (Cu E = 0.16 and Zn E = -0.76)
a cobre y zinc. *: Indica significativamente diferente al which would lead to an increased oxidant effect at
control (P < 0,05). lower concentrations.
Lat. Am. J. Aquat. Res. 284

A manifestation of the hormesis effect was significantly from 0.5 mg L-1 of copper and 3, 25 mg
expressed under the Cu exposure. The stimulation of L-1 of zinc. The difference with our work can be
chlorophyll-a at the most low concentration of copper explained by the different sensibility between species.
was similar to that founded by Knauer et al. (1997) Similarly, Srivastava et al. (2006) reported a gradual
and Janssen & Heijrick (2003). Whitton (1970) increase in the content MDA and significant
reported that the algae growth may be stimulated by differences to the control in Hydrilla verticillata at the
low metal concentrations and inhibited at high metal highest concentration of copper tested.
concentrations. The parameter chlorophyll-a concen- In conclusion, both metals induce the antioxidant
tration was more sensitive than growth rate. The activity of catalase. Copper induces lipidperoxidation
lowest content of chlorophyll-a in the higher at lower concentrations than zinc. Copper and zinc
concentrations of the metals can be due to the cause adverse effects on the physiology of P.
peroxidation of chloroplast membranes. Metals can subcapitata determined through the content of
destabilize the membrane by oxidation due to free chlorophyll-a. The growth rate was less sensitive to
radicals formation. Copper alters membrane tilacoides the metals that catalase activity, lipidperoxidation and
and causes changes in its composition (De Vos et al., chlorophyl-a content. The molecular parameters can
1991), interference with the photosynthetic system and be more adecuate than growth rate to monitoring the
the a decline in the rate of photosynthesis (Cook et al., effect in microalgae aquatic ecosystems.
1997; Yruela, 2005). Our results differ from those
reported by Bossuyt & Janssen (2004), who found a
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DOI: 10.3856/vol39-issue2-fulltext-10

Research Article

Biologa de la raya guitarra Rhinobatos leucorhynchus (Gnther, 1867)


(Rajiformes: Rhinobatidae) en el Pacfico colombiano

Luis Fernando Payn1, Andrs Felipe Navia1, Efran A. Rubio2 & Paola Andrea Meja-Falla1
1
Fundacin Colombiana para la Investigacin y Conservacin de Tiburones y Rayas, SQUALUS
Carrera 79 N 6-37, Cali, Colombia
2
Universidad del Valle, Departamento de Biologa, Seccin de Biologa Marina
A.A. 25360, Cali, Colombia

RESUMEN. La raya guitarra Rhinobatos leucorhynchus es comnmente capturada como fauna acompaante
en la pesca del camarn de aguas someras del Pacfico colombiano, tanto a nivel industrial como artesanal. A
partir de 286 ejemplares capturados incidentalmente entre 2001 y 2007, se estudiaron diferentes aspectos
biolgicos de esta especie. Las hembras fueron proporcionalmente ms grandes que los machos, aunque el
crecimiento fue similar en ambos sexos (alomtrico). Los embriones no presentaron diferencias sexuales
significativas ni en talla ni en peso. La proporcin sexual en adultos fue 2,4:1 (hembras-machos), mientras que
en embriones esta proporcin fue de 1:1. El 51,5% de machos present claspers desarrollados y calcificados y
el 56,5% de las hembras estaban grvidas, presentando fecundidades entre 1 y 6 embriones, con tallas entre 3
y 19,5 cm, sugiriendo una talla de nacimiento entre 19 y 19,5 cm LT. La talla mediana de madurez de las
hembras fue menor que la de machos (48,48 cm y 51,18 cm LT, respectivamente), y las hembras presentaron
cras a partir de 44 cm LT. Los hbitos alimentarios de esta especie mostraron 30 tems presa, con camarones
de la familia Penaeidae, y especialmente Trachypenaeus sp. como alimento principal. La raya guitarra
present diferencias significativas en la dieta de machos y hembras, y la amplitud de nicho indic que es
especialista en su dieta. Los resultados de este estudio aportan informacin til para plantear medidas de
manejo de R. leucorhynchus, especie que requiere atencin, dado sus caractersticas biolgicas y su
importancia comercial y de consumo.
Palabras clave: batoideos, reproduccin, crecimiento, dieta, ecologa alimentaria.

Biology of the guitar ray Rhinobatos leucorhynchus (Gnther, 1867)


(Rajiformes: Rhinobatidae) in the Colombian Pacific

ABSTRACT. The guitar ray Rhinobatos leucorhynchus is commonly caught as by-catch of industrial and
artisanal shrimp trawling in the shallow waters of the Colombian Pacific. The biological aspects of this species
were studied using 286 animals caught as by-catch between 2001 and 2007. The females were proportionally
larger than males, although growth was similar (allometric) for both sexes. The embryos showed no significant
differences by sex in either size or weight. The adult sex ratio was 2.4:1 (females-males), whereas in embryos
this ratio was 1:1. 51.5% of males, 51.5% had developed, calcified claspers, and 56.5% of females were
pregnant, carrying between 1 and 6 embryos of 3 to 19.5 cm, suggesting a size at birth of 19 to 19.5 cm TL.
The median size at maturity for females was lower than that of males (48.48 cm and 51.18 cm TL,
respectively), and the females had embryos starting at 44 cm TL. The feeding habits of this species showed 30
prey items, with shrimp from the Penaeidae family and especially Trachypenaeus sp. as main food. The diets
of male and female guitar rays differed significantly, and the niche breadth indicated that this species has a
specialist diet. The results of this study provide useful information for proposing management measures for R.
leucorhynchus, a species that requires attention given its biological characteristics and its importance in terms
of commerce and human consumption.
Keywords: batoids, reproduction, growth, diet, feeding ecology.

___________________
Corresponding author: Paola Andrea Meja-Falla (pmejia@squalus.org)
287 Biologa de Rhinobatos leucorhynchus en el Pacfico colombiano

INTRODUCCIN oscura y superficie inferior blanca. Esta especie habita


aguas tropicales costeras y estuarios de fondos suaves
Las rayas de la familia Rhinobatidae, conocidas y arenosos y est distribuida desde el golfo de
mundialmente como rayas guitarra y a nivel local California a las islas Galpagos en Ecuador
como guitarrillas, se agrupan en cuatro gneros, tres (Robertson & Allen, 2008). En el Pacfico colombiano
subgneros y al menos 48 especies, y estn esta especie es capturada regularmente como fauna
distribuidas en todos los mares tropicales y templados, acompaante en faenas de pesca de camarn a nivel
desde aguas costeras y someras a profundidades hasta artesanal e industrial (Navia, 2002; Gmez & Meja-
de 370 m (Compagno, 2005). En el Pacfico Oriental Falla, 2008); y aunque no presenta un alto valor
Tropical (POT) se encuentran los gneros Zapteryx y comercial, su carne es vendida a nivel local y las
Rhinobatos con dos y cinco especies, respectivamente, aletas dorsales de los ejemplares ms grandes son
siendo todas endmicas de esta regin (Robertson & comercializadas (Navia et al., 2008). Aunque no
Allen, 2008). Para el Pacfico colombiano se ha existe una pesca dirigida hacia la especie, su presencia
confirmado la presencia de Z. xyster, R. en hbitats estuarinos cercanos a la costa y aguas
leucorhynchus, R. planiceps, R. prahli, quedando por someras, la hacen vulnerable a la pesca de arrastre
confirmar la presencia de Z. exasperata y R. practicada en estas zonas.
glaucostigmus (Meja-Falla et al., 2007). Navia et al. (2009) plantean que el conocimiento
La familia Rhinobatidae, y en especial el gnero sobre R. leucorhynchus en Colombia se limita a pocos
Rhinobatos, hace parte importante de la captura registros de su distribucin latitudinal y batimtrica
incidental de numerosas pesqueras en el mundo (Navia, 2002; Payn, 2006), un estudio sobre sus
(Stobutzki et al., 2002; Klippel et al., 2005) lo que, relaciones trficas con otras especies simptricas de
junto a otras amenazas como la degradacin de elasmobranquios (Navia et al., 2007) y a un estudio
hbitats y el comercio de sus aletas dorsales (Fowler et preliminar para la determinacin de edad (Soler,
al., 2005), ha llevado a que 37 de las 48 especies estn 2006). Con este trabajo, cuyo objetivo fue estudiar la
incluidas en la Lista Roja de Especies Amenazadas de biologa de la raya guitarra R. leucorhynchus, en
la IUCN, siendo 10 de stas categorizadas como trminos de su crecimiento, reproduccin y
vulnerables o amenazadas y una como crticamente alimentacin, se incrementa el conocimiento sobre sus
amenazada (Rhinobatos horkelli) (IUCN, 2010). caractersticas de historia de vida y se aporta
Numerosos estudios sobre la historia de vida de informacin til para futuras medidas de manejo y
condrictios ubican a estas especies como estrategas k, conservacin de la especie.
exhibiendo bajas tasas de crecimiento, maduracin
sexual tarda, bajas tasas de fecundidad y largos ciclos MATERIALES Y MTODOS
de vida (Holden, 1974). Para el gnero Rhinobatos se
conocen pocos estudios en Amrica. Villavicencio- Entre los aos 2001 y 2007, se capturaron ejemplares
Garayzar (1993) y Mrquez-Faras (2007) describen de R. leucorhynchus en monitoreos a bordo de embar-
que R. productus en el golfo de California alcanza la caciones de pesca industrial de camarn, en la zona
madurez despus de los 50 cm longitud total (LT) central de pesca del Pacfico colombiano (505N,
(machos a los 53 cm y hembras a los 57 cm LT), tiene 7716W-231N, 7835W). Los ejemplares fueron
un largo periodo de gestacin (11 a 12 meses) y una congelados y trasladados al laboratorio para su
fecundidad promedio de cinco cras que nacen a los anlisis. Se registr el peso total (W), longitud total
17,5 cm LT. En Brasil, Lessa et al. (1986) y Texeira (LT) y sexo de cada ejemplar. El estmago y las
(1982) proponen que las especies de Rhinobatos gnadas fueron removidos de la cavidad corporal,
presentan relacin directa entre la talla y la fecundidad identificando, en este ltimo caso y de manera
y diferenciacin sexual por talla. En el Caribe macroscpica, el estado de madurez siguiendo las
colombiano, Grijalba-Bendeck et al. (2008) describen escalas de Martin & Cailliet (1988) y Snelson et al.
la biologa reproductiva de R. percellens sealndola (1988). Las cras encontradas fueron medidas (LT),
como una especie matrotrfica con viviparidad pesadas y sexadas y los huevos fueron contados y
aplacentaria y fecundidad entre 2 y 4 embriones por medidos (dimetro en cm).
ao; y Polo-Silva & Grijalba-Bendeck (2008) la Las relaciones entre W (g) y LT (cm) fueron
ubican como un depredador con dieta preferencial de estimadas para machos y hembras (en embriones y en
crustceos. individuos libres) siguiendo el modelo W = a x LTb,
R. leucorhynchus (Gnther, 1886) presenta dorso donde a y b son constantes. El tipo de desarrollo fue
de coloracin gris oscuro, algunas veces con manchas definido a partir de la pendiente de la relacin de los
plidas, hocico muy plido, translcido, sin punta logaritmos de LT y W mediante una prueba t-Student,
Lat. Am. J. Aquat. Res. 288

probando si es isomtrico (b = 3) o alomtrico (b 3) RESULTADOS


(Pauly, 1983). La similitud de esta relacin entre
machos y hembras fue evaluada mediante la Crecimiento
comparacin de los coeficientes de determinacin de Las hembras se capturaron en tallas entre 20,0 y 76,0
cada sexo (Zar, 1999). cm LT (59,21 10,56) y los machos entre 22,5 y 64,3
La proporcin de sexos fue determinada para cm LT (49,12 9,86), encontrando dimorfismo sexual
adultos y embriones usando una prueba de Chi- en la longitud total (nH = 201, nM = 85, g.l. = 2,81, t =
cuadrado con los valores observados y esperados (0,5) 7,43; P < 0,001). Sin embargo, ambos sexos
de machos y hembras. La longitud de primera presentaron un crecimiento similar, siendo alomtrico
madurez de machos fue determinada por el cambio de en ambos casos (bHembras= 3,24, bMachos= 3,30,
pendiente en la relacin de la longitud del clasper en tc-Hembras= 2,976, tc-Machos= 2,207; P < 0,05) y ligera,
funcin de la LT. Se evalu la existencia de
ms no significativamente, menor en las hembras (P =
dependencia de la fecundidad con la talla de la madre,
0,729) (Fig. 1).
a partir de la relacin de la LT con el nmero de
huevos y el nmero de cras. La talla mediana de Las cras (n = 101) se encontraron en diversos
madurez se estim para ambos sexos con una funcin estadios de crecimiento intrauterino, con tallas entre
logstica de la forma PLi=1/(1+e-b(Li+L50)), donde PLi es 3,0 y 19,5 cm LT (12,53 5,10) y pesos entre 0,2 y
la proporcin de individuos maduros en el intervalo de 24,2 g (9,19 8,22). Las diferencias sexuales en tallas
tallas Li, b es la pendiente y L50 es la talla a la cual el y pesos de las cras no fueron significativas (Tabla 1)
50% de los individuos estn maduros; este modelo fue y su desarrollo a nivel intrauterino fue similar entre
fijado usando regresin no lineal de mnimos machos y hembras, presentando ambos sexos una
cuadrados (Haddon, 2001). relacin longitud total-peso casi idntica (P > 0,05)
Los contenidos estomacales fueron identificados al (Fig. 2).
nivel taxonmico ms bajo posible y cada grupo de
presas fue contado y pesado con 0,01 g de precisin. Proporcin de sexos
Para determinar si el tamao de la muestra fue
Se analiz un total de 286 individuos adultos (201
suficiente para describir con precisin la dieta se us
hembras y 85 machos), hallando una proporcin de
la medida de diversidad trfica acumulada o curva de
acumulacin de especies (Ferry & Cailliet, 1996); para sexos dominada por hembras de 2,4:1 (2c = 47,05; g.l.
reducir el sesgo del orden de las muestras, se = 1; P < 0,001). Por su parte, los embriones cuyo sexo
realizaron 50 aleatorizaciones y para verificar la pudo ser determinado (35 hembras y 46 machos)
confiabilidad de la curva obtenida, se utilizaron los presentaron una proporcin sexual de 1:1 (2c = 1,49;
estimadores de riqueza de especies Chao e ICE g.l. = 1; P < 0,001), mostrando similitud en el aporte
(Colwell, 2005). La contribucin de cada tem de de ambos sexos a la poblacin.
presa a la dieta fue estimada usando tres ndices
numricos discutidos y revisados por Hyslop (1980) y
Corts (1997). El valor obtenido del ndice de
Importancia Relativa (IIR) se estandariz a porcentaje
(%IIR) para facilitar la comparacin entre tipos de
presas de una misma especie y entre dietas de
diferentes especies (Corts, 1997). Para probar la
independencia entre las categoras de alimento y sexo
se realizaron tablas de contingencia (columnas x filas)
(Zar, 1999), con contenidos estomacales agrupados en
siete categoras grandes y expresados como ocurrencia
(Corts, 1997). Anlisis de cambios ontognicos no
fueron realizados, dado el escaso nmero de
estmagos de individuos juveniles. Para determinar la
especializacin en la dieta se us la amplitud de nicho,
siguiendo la medida estandarizada de Levins (Ba)
(Krebs, 1999) y aplicando el %IIR (transformado a
proporcin) de las diferentes presas identificadas; este Figura 1. Relacin entre la longitud total y el peso total
ndice vara en un rango de 0 a 1, donde valores de machos y hembras de R. leucorhynchus.
cercanos a 0 indican una dieta especializada y Figure 1. Relationship between the total length and total
cercanos a 1 expresan dieta generalista (Krebs, 1999). weight of males and females of R. leucorhynchus.
289 Biologa de Rhinobatos leucorhynchus en el Pacfico colombiano

Tabla 1. Valores de la media y desviacin estndar de la longitud total (cm) y peso (g) de las cras de R. leucorhynchus,
indicando los valores de la prueba t entre sexos.
Table 1. Mean and standard deviation values of the total length (cm) and weight (g) of embryos of R. leucorhynchus,
indicating the t-test values between sexes.

Hembras (n = 35) Machos (n = 46) Valor t g.l. P


Longitud total 12,76 4.92 14,40 4.33 -1,562 79 0,122
Peso total 9,70 8.89 11,76 7.72 -0,983 79 0,329

que estaban maduros. La relacin entre la longitud


total (LT) y la longitud del clasper mostr un
crecimiento rpido entre los 42 y 50 cm LT, con punto
de inflexin en 47 cm (Fig. 4); el macho ms pequeo
con indicios de madurez fue de 42 cm LT,
correspondientes a los 62,1% de la longitud asinttica
calculada para machos en este estudio (67,68 cm LT).
La mayora de las hembras capturadas (86,0%)
estaban maduras, de las cuales el 56,5% present cras
en sus teros (estado 4) y el 26,3% huevos en sus
ovarios pero no cras (estado 3). La talla mnima de
madurez se registr a 44 cm LT, correspondiente al
55,0% de la longitud asinttica calculada para
hembras en este estudio (80,0 cm LT).
Figura 2. Relacin entre la longitud total y el peso total La talla mediana de madurez de las hembras fue de
en embriones de R. leucorhynchus. 48,5 cm LT, mientras que la de machos fue mayor
(51,2 cm LT) (Fig. 5). Estas tallas corresponden al
Figure 2. Relationship between the total length and total
60,6% y al 75,6% de las longitudes asintticas
weight of embryos of R. leucorhynchus.
calculadas en el estudio, respectivamente.

Fecundidad
Rhinobatos leucorhynchus mostr funcionalidad en
sus dos ovarios, con fecundidad ovrica entre 1 y 16
huevos (5,61 2,87) que variaron entre 0,4 y 3,4 cm
de dimetro (1,86 0,64; n = 183). La fecundidad
uterina vari de 1 a 6 (3,45 1,15) con mayor
frecuencia (moda) en 4 embriones. Los resultados
encontrados sugieren que la fecundidad (ovrica y
uterina) de la raya guitarra es dependiente de la talla
materna, donde las hembras ms grandes presentaron
mayor cantidad de huevos y embriones (Fig. 3). El
tamao de cras y huevos mostr una relacin directa
durante la etapa de gestacin, observndose que a
medida que los embriones crecen, los huevos tambin
lo hacen. Finalmente, embriones con tallas cercanas a
19 cm LT, presentaron un desarrollo casi completo y
un saco vitelino muy pequeo. Figura 3. Relacin entre la longitud total de la madre
con el nmero de cras y huevos, indicando dependencia
Estados de madurez para hembras y machos de la fecundidad con la talla materna.
Al evaluar el estado de madurez de los machos se Figure 3. Relationship between the total length of
encontr que el 51,5% present los claspers females and the number of their embryos and eggs,
completamente desarrollados y calcificados indicando indicating dependence of fecundity with maternal length.
Lat. Am. J. Aquat. Res. 290

Figura 4. Relacin entre la longitud total y la longitud Figura 6. Curva de acumulacin de especies para la dieta
del clasper de machos de R. leucorhynchus. de Rhinobatos leucorhynchus y sus respectivos esti-
Figure 4. Relationship between the total length and madores.
clasper length of R. leucorhynchus males. Figure 6. Species accumulation curve for the Rhinobatos
leucorhynchus diet and its respective estimates.

peso, seguidos por crustceos, camarones no


identificados y peces (Fig. 7). La amplitud de nicho
calculada para R. leucorhynchus fue de 0,06,
indicando que es especialista en su dieta, con las dos
presas principales mencionadas.
Se encontr diferencia significativa entre la dieta
(agrupada) de machos y hembras de R. leucorhynchus
(2 = 13,288; g.l. = 6; P = 0,038), existiendo diferencia
en el mayor nmero de presas identificadas en las
hembras (7) y en el mayor consumo de peces. Por su
parte, los machos consumen menos presas (5), pero en
mayor proporcin crustceos y estomatpodos.

Figura 5. Ojivas de madurez sexual en machos y DISCUSIN


hembras de R. leucorhynchus.
Figure 5. Sexual maturity ogives for males and females Los ejemplares de raya guitarra colectados en el rea
of R. leucorhynchus. de estudio presentaron mayores tallas que las
reportadas por McEachran & di Sciara (1995) (62,5
Dieta cm LT) y por Robertson & Allen (2008) (63 cm LT)
Se analizaron los contenidos estomacales de 211 para el Pacfico Oriental Tropical, siendo esta
ejemplares (147 hembras y 64 machos) donde se diferencia mayor en hembras (76,0 cm LT) que en
encontraron 30 tems presa y un coeficiente de machos (64,3 cm LT). Aunque la relacin entre
vacuidad de 18,0%. La curva de acumulacin de longitud total y peso no mostr diferencias
presas y sus respectivos estimadores indicaron que la significativas entre hembras y machos, estos ltimos
muestra fue suficiente para la descripcin de la dieta son ligeramente ms pequeos que las hembras y
de la especie, cubriendo ms del 91,7 % del total de presentan un menor peso corporal en tallas similares.
presas esperadas para una muestra de este tamao Diferencias similares aunque significativas, han sido
(Fig. 6). De todas las presas identificadas, los reportadas para R. horkelli (Texeira, 1982), R.
camarones, especialmente Trachypenaeus sp. fueron productus (Villavicencio-Garayzar, 1995) y R.
los de mayor importancia en la dieta de la especie cemiculus (Seck et al., 2004). A nivel embrionario, las
(%IIR = 52,0) (Tabla. 2). La dieta de R. leucorhynchus curvas de la relacin longitud total-peso de machos y
es heterognea, con dos tems presa (Trachypenaeus hembras fueron casi idnticas, presentando ambos
sp. y Penaeidae) dominantes en nmero, ocurrencia y sexos un crecimiento similar. De esta forma, ambos
291 Biologa de Rhinobatos leucorhynchus en el Pacfico colombiano

Tabla 2. Valores de porcentaje de ocurrencia (%O), porcentaje en nmero (%N), porcentaje en peso (%W), ndice de
importancia relativa (IIR) y porcentaje de ndice de importancia relativa (%IIR) de las presas consumidas por Rhinobatos
leucorhynchus.
Table 2. Values of frequency of occurrence (%O), percentage by number (% N), percentage by weight (%W), index of
relative importance (IIR) and percentage of the index of relative importance (%IIR) of prey consumed by Rhinobatos
leucorhynchus.

Presa %O %N %W IIR %IIR


Trachypenaeus sp. 28,44 33,43 21,30 1556,32 51,98
Penaeidae 18,96 18,81 24,93 829,20 27,69
Crustceos 9,95 12,45 5,72 180,75 6,04
Camarones 8,06 11,29 5,87 138,22 4,62
Peces 9,95 3,62 10,13 136,80 4,57
Porichthys margaritatus 3,79 1,59 9,72 42,90 1,43
Callinectes sp. 4,27 1,88 5,14 29,96 1,00
Portunidae 5,21 2,32 1,84 21,68 0,72
Sicyonia sp. 3,32 1,45 1,57 10,01 0,33
Cangrejos 3,32 1,74 0,89 8,71 0,29
Stomatopoda 1,42 0,43 5,60 8,57 0,29
Batrachoididae 3,32 1,16 0,64 5,96 0.20
Squillidae 2,84 1,30 0,28 4,50 0,15
Raninoides benedicti 2,37 0,87 0,91 4,22 0,14
Trachypenaeus byrdi 1,90 0,87 0,73 3,04 0,10
Squilla sp. 1,42 1,16 0,63 2,55 0,09
Callinectes toxotes 1,90 0,58 0,61 2,25 0,08
Portunus sp. 1,90 1,01 0,09 2,09 0,07
Trachypenaeus brevisuturae 0,95 0,29 1,09 1,31 0,04
Trachypenaeus fuscina 0.95 0,43 0,68 106 0,04
Anomura 1,42 0,43 0,09 0,74 0,02
Processa sp. 1,42 0,43 0,08 0,73 0,02
Sicyonia disdorsalis 0,95 0,29 0,30 0,56 0,02
Meiosquilla swetti 0,95 0,43 0,13 0,53 0,02
Brachyura 0,95 0,43 0,10 0,51 0,02
Squilla parva 0,47 0,43 0,51 0,45 0,01
Solenoceridae 0,47 0,29 0,15 0,21 0,01
Solenocera agassizzi 0,47 0,14 0,23 0,18 0,01
Donacidae 0,47 0,29 0,03 0,15 0,00
Leucosiidae 0,47 0,14 0,03 0,08 0,00
TOTAL 122,27 100,00 100,00 2994,22 100,00

sexos presentan crecimientos similares durante su 2008). Adicionalmente, la muestra colectada para este
desarrollo (tanto intrauterino como externo), pero estudio no present individuos juveniles y la mayora
presiones intrnsecas a las hembras (p.e. su viviparidad de las hembras y machos estaban maduros; as, se
aplacentaria) provocan ligeros cambios, siendo ms puede sugerir que la zona donde se realizan los
marcada esta diferencia en la talla mxima alcanzada arrastres de camarn industrial, presenta una alta
por ambos sexos. actividad reproductiva, con segregacin por tallas y
La proporcin de sexos mostr diferencias sexos. Sin embargo, considerando la proporcin
significativas siendo 2,4:1 favorable para las hembras, sexual encontrada en embriones (1:1), se propone que
estableciendo una posible segregacin por sexos, tal el aporte a la poblacin de hembras y machos es
como se ha planteado para varias especies de rayas similar, pero luego del parto y durante el desarrollo de
(p.e. Braccini & Chiaramonte, 2002; Ebert et al., los individuos, se inicia un proceso de segregacin
Lat. Am. J. Aquat. Res. 292

nacimiento entre estos valores (19,0 y 19,5 cm LT).


Esta talla es similar a la reportada por Villavicencio-
Garayzar (1993) y Downton-Hoffmann (2001) para R.
productus en el Pacfico Mexicano, pero es menor a lo
registrado por Abdel-Aziz et al. (1993), Capap et al.
(1997, 1999) e Ismen et al. (2007) para R. rhinobatos
en el Mediterrneo y el Atlntico este tropical.
La falta de datos a lo largo del ao no permiti
definir el ciclo reproductivo de la especie. Sin
embargo, la frecuencia de tallas de los embriones
permite considerar que cerca del mes de agosto, las
hembras pueden empezar a parir sus cras, tal como ha
sido reportado para R. hynnicephalus en aguas
japonesas (Kume et al., 2009).
La relacin directa entre el tamao de los huevos y
de los embriones, puede indicar que, simultneamente
al desarrollo embrionario se presenta el desarrollo
ovrico. Esto sugiere que, una vez los embriones son
expulsados, las hembras pueden recomenzar el ciclo
reproductivo. Esta posible estrategia reproductiva se
Figura 7. Representacin grfica del ndice de ajusta a la descrita para otras especies del mismo
importancia relativa (IIR) de las presas consumidas por gnero como R. horkelli, R. annulatus, R. productus y
R. leucorhynchus, indicando aquellas de mayor R. cemiculus en las que para un mismo periodo de
importancia. tiempo, de manera simultnea al desarrollo
Figure 7. Graphic representation of the relative embrionario crecen los ovocitos de la siguiente
importance index (IIR) of prey consumed by R. progenie, los cuales son fecundados en los das
leucorhynchus, indicating those of greatest importance. siguientes a la expulsin de los neonatos
(Villavicencio-Garayzar, 1995; Valadou et al., 2006;
espacial en tallas y sexos. Se han encontrado Kume et al., 2009). Esto explica adems la presencia
resultados similares en proporcin de embriones en R. de embriones en etapas iniciales (3 cm LT) y finales
productus, R. hynnicephalus y R. rhinobatos (19 cm LT) del desarrollo embrionario en un mismo
(Villavicencio-Garayzar, 1993, 1995; Webin & mes (p.e. agosto).
Shuyuan, 1993; Cek et al., 2009). Ms del 90% de las hembras estaban maduras, por
La fecundidad uterina de R. leucorhynchus (entre 1 lo que se infiere que el periodo entre junio y
y 6 embriones) es menor a la de otras especies de la septiembre es poca reproductiva para la raya guitarra.
misma familia, como R. productus (2-10) (Downton- Aunque no se encontraron machos con semen, ms del
Hoffmann, 2001; Mrquez-Faras, 2007) y Zapteryx 60% estaban maduros, basado en la longitud, el grado
brevirostris (Abilhoa et al., 2007), pero ms alta que de calcificacin y rotacin de los claspers tal como
la de R. cemiculus (2-4) (Valadou et al., 2006). As plantean Joung & Chen (1995). En cortes histolgicos
mismo, la dependencia de la fecundidad con la talla realizados a machos maduros de la especie (Payn,
materna encontrada en la especie, ya ha sido registrada 2006), se observ que las clulas reproductivas
en otras especies de Rhinobatos como R. horkelli, R. presentaban diferentes estados de madurez, mostrando
annulatus, R. productus y R. hynnicephalus (Lessa et porcentajes similares entre clulas maduras
al., 1986; Villavicencio-Garayzar, 1993; Webin & (espermatozoides) y clulas inmaduras (esperma-
Shuyuan, 1993; Mrquez-Faras, 2007; Kume et al., togonias y espermtidas). De acuerdo con la poca
2009). reproductiva en la cual fueron tomadas las muestras,
Los embriones con tallas cercanas a los 19 cm LT, se pueden sugerir dos posibilidades, que los machos
presentaron un desarrollo casi completo y un saco ya se hubieran apareado y por lo tanto habran
vitelino muy pequeo; as, y considerando que la descargado todo el semen, o por otra parte, que
menor talla conocida para un organismo de vida libre estuvieran en una etapa previa al apareamiento en la
es de 19 cm LT (Gmez & Meja-Falla, 2008) y el cual sus conductos se estuvieran cargando.
embrin intrauterino ms grande encontrado en este La talla mediana de madurez sexual de hembras
estudio fue de 19,5 cm LT, se considera la talla de fue de 48,5 cm LT y de machos de 51,2 cm LT,
293 Biologa de Rhinobatos leucorhynchus en el Pacfico colombiano

mientras que la talla promedio de captura fue de 59,2 especialmente a cambios en las estructuras dentales
y 49,1 cm LT, respectivamente, por lo tanto, se infiere entre los sexos.
que la mayora de los individuos capturados ya han La ausencia de ejemplares juveniles en la muestra
tenido la oportunidad de reproducirse anteriormente. sugiere una separacin espacial entre los diferentes
La talla mnima de madurez es similar para ambos estados ontognicos, por lo cual los neonatos y
sexos (42 y 44 cm LT, para machos y hembras, juveniles no ocurren en los mismos sitios de captura
respectivamente). Sin embargo, dado que las hembras de los adultos, y s lo hacen probablemente en zonas
alcanzan mayores tallas, el porcentaje en que alcanzan ms cercanas a la costa. Los estados tempranos
esa talla si difiere entre machos y hembras (62,1% y tienden a concentrarse en sectores poco profundos de
55,0%, respectivamente), y al igual que lo reportado gran productividad y abundante alimento, como por
por Kume et al. (2009), las hembras alcanzan la talla ejemplo, aguas someras, planicies submareales
de madurez en tallas ms grandes que los machos. costeras y estuarios (Bass, 1978; Castro, 1987).
La curva de acumulacin de presas construida para
R. leucorhynchus indic que el tamao de muestra fue AGRADECIMIENTOS
adecuado para hacer una descripcin de su dieta en el
rea de estudio. Esta especie es especialista en su dieta Los autores agradecen a los pescadores artesanales e
consumiendo mayoritariamente camarones, en industriales de Buenaventura que aportaron las
especial de la familia Penaeidae y del gnero muestras para efectuar este trabajo; a Don Agustn
Trachypenaeus. Estos resultados concuerdan con lo Martnez, por facilitar los embarques en el barco
reportado para otras especies del gnero en frica, el camaronero Arraijn; a Henry Lpez por facilitar el
Mediterrneo, California y Brasil (Caverivier & trabajo de muestras en el Puerto; a la Universidad del
Rabarison-Andriamirado, 1997; Goitein et al., 1998; Valle y la Fundacin SQUALUS por el apoyo
Shibuya et al., 2005; Basusta et al., 2007; Ismen et al., logstico; a IdeaWild por la donacin de equipos para
2007). Aparentemente R. leucorhynchus, al igual que trabajo de campo y de laboratorio, a los miembros de
las otras especies de su gnero, no est adaptada para la Fundacin SQUALUS Jos Sergio Hleap y
perseguir activamente peces de media agua (Talent,
Alexnder Tobn por el apoyo a bordo, y a Juliana
1982). Por el contrario, extrae su alimento de los
Lpez por el apoyo en el anlisis de muestras en
fondos areno-fangosos donde habita, llevando a que su
campo y en laboratorio.
alimentacin est basada principalmente en
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Received: 29 July 2010; Accepted: 16 May 2011 Education, India, 718 pp.
Lat. Am. J. Aquat. Res., 39(2): 297-305, 2011 Age and growth of brazilian flathead 297
DOI: 10.3856/vol39-issue2-fulltext-11

Research Article

Age determination, validation, and growth of Brazilian flathead


(Percophis brasiliensis) from the southwest Atlantic coastal waters (34-41S)

Alfredo C. Barretto1, Margarita B. Sez2, Mara R. Rico2 & Andrs J. Jaureguizar2,3


1
Departamento de Biodiversidad y Biologa Experimental, Facultad de Ciencias Exactas y Naturales
Universidad de Buenos Aires (UBA), Ciudad Universitaria Pabelln 2, 1428, Buenos Aires, Argentina
2
Instituto Nacional de Investigacin y Desarrollo Pesquero (INIDEP)
P.O. Box 175, 7600 Mar del Plata, Argentina
3
Comisin de Investigaciones Cientficas de la Provincia de Buenos Aires
Calle 526 entre 10 y 11, 1900 La Plata, Argentina

ABSTRACT. The age and growth parameters of Brazilian flathead, Percophis brasiliensis, from the
southwest Atlantic coastal waters (34-41S) were determined for samples collected in spring (n = 853; years
1998 and 2000) and winter (n = 596; year 2004), whereas age was validated through the edge analysis of
otoliths collected in 2007 (n = 1367 otoliths). The indices of precision APE, V, and D were used to test the
reproducibility, between agers, of the ages determined from 845 otoliths. Maximum determined ages were 19
years for males and 15 years for females. One opaque and one translucent band are laid down per year, in the
sagittal otolith. According to the APE (0.668%), V (1.121%), and D (0.647%) indices, the age determination
was consistent. Von Bertalanffys growth parameters [males: spring (L = 58.1 cm, k = 0.26 year-1, t0 = -2.02
years), winter (L = 58.7 cm, k = 0.21 year-1, t0 = -2.90 years); females: spring (L = 65.2 cm, k = 0.29 year-1,
t0 = -1.15 years), winter (L = 63.5 cm, k = 0.26 year-1, t0 = -2.01 years)] were significantly different between
sexes and seasons. From the first year of life, females grow faster and reach greater lengths than males of the
same age due, probably, to an asynchronism in the sexual maturity.
Keywords: Brazilian flathead, Percophis brasiliensis, age determination, otolith, validation, growth, south-
west Atlantic.

Determinacin de edad, validacin y crecimiento del pez palo


(Percophis brasiliensis) de aguas costeras del Atlntico sudoccidental (34-41S)

RESUMEN. Se determin la edad y los parmetros de crecimiento del pez palo, Percophis brasiliensis, de
aguas costeras del Atlntico sudoccidental (34-41S) en muestras obtenidas durante primavera (n = 853; aos
1998 y 2000) e invierno (n = 596; ao 2004), mientras que la edad fue validada mediante anlisis del tipo de
borde de otolitos colectados durante 2007 (n = 1367 otoliths). Los ndices de precisin APE, V, y D fueron
usados para probar la reproducibilidad, entre lectores, de las edades determinadas a partir de 845 otolitos. Las
edades mximas determinadas fueron 19 aos para machos y 15 aos para hembras. Una banda opaca y una
translcida se depositan anualmente en el otolito sagitta. Los ndices APE (0,668%), V (1,121%) y D
(0,647%) indican que la determinacin de la edad fue consistente. Los parmetros de crecimiento de Von
Bertalanffy [machos: primavera (L = 58,1 cm, k = 0,26 ao-1, t0 = -2,02 aos); invierno (L = 58,7 cm, k =
0,21 ao-1, t0 = -2,90 aos). hembras: primavera (L = 65,2 cm, k = 0,29 ao-1, t0 = -1,15 aos); invierno
(L = 63,5 cm, k = 0,26 ao-1, t0 = -2,01 aos)] fueron significativamente diferentes entre sexos y estaciones. A
partir del primer ao de vida, las hembras crecen ms rpido y alcanzan mayores longitudes que los machos de
la misma edad debido, probablemente, a un asincronismo en la madurez sexual.
Palabras clave: pez palo, Percophis brasiliensis, determinacin de edad, otolito, validacin, crecimiento,
Atlntico sudoccidental.

___________________
Corresponding author: Andres J. Jaureguizar (ajj@inidep.edu.ar)
298 Lat. Am. J. Aquat. Res.

INTRODUCTION flathead, associated to its reproduction activity in the


salinity front located within the southwest Atlantic
The Brazilian flathead Percophis brasiliensis (Quoy & coastal water (34-41S) (Macchi & Acha, 1998;
Gaimard) is a demersal fish species (Olivier et al., Militelli & Macchi, 2001), could allow differences in
1968) that inhabits southwest Atlantic coastal waters. the estimated growth parameters. Detect, therefore,
Its distribution extends from 23S (Rio de Janeiro, these differences is important at the time of using age-
Brazil) to 47S (north of Santa Cruz Province, length keys for transforming length data in age data.
Argentina) (Gosztonyi, 1981; Cousseau & Perrotta, This study represents the first attempt to validate
2004). In the southern area of its distribution (34- Brazilian flatheads age determination and to estimate
41S), it is one of the most important species caught the growth parameter of each sex by season.
by the coastal commercial fishery (Lasta et al., 1999;
Carozza et al., 2001; Fernndez-Aroz et al., 2004).
Despite the importance of this species and the MATERIALS AND METHODS
increasing captures that have been detected during the
last years (Rico & Perrotta, 2009), few studies have Age determination
been focused to obtain relevant biological information Samples were collected from southwest Atlantic costal
for its fisheries management. There are information waters (34-41S) by bottom trawling in waters from 7
about feeding (San Romn, 1972; Bergonzi, 1997), to 50 m depth (Fig. 1), during INIDEP cruises carried
growth (Tomo, 1969; San Romn, 1974; Perrotta & out in spring (1998, 2000) and winter (2004). Age was
Fernndez-Gimnez, 1996), distribution (Fernndez- determined to 1449 specimens, 853 in spring (439
Gimnez, 1995; Rico & Perrotta, 2006) and males, 414 females) and 596 in winter (251 males, 345
reproduction (Macchi & Acha, 1998; Militelli, 1999; females). Of each specimen total length (TL) and sex
Militelli & Macchi, 2001; Rodrgues et al., 2007). For (by macroscopic examination of the gonads) were
successful fisheries management is very important to recorded, while sagittal otoliths were removed from
evaluate the fish population state. Studies on age the fish and stored dry in paper envelopes for age
determination and growth parameters estimation, determination. Randomly, one sagittal otolith from the
amongst others, are fundamental to knowledge of pair was embedded in opaque epoxy resin and
population dynamics (Sparre & Venema, 1995; Cotter sectioned transversely through the core with a micro-
et al., 2004; Dulvy et al., 2004; Begg et al., 2005). cutter (Maruto MC-201) obtaining thus thin transverse
The age and growth parameters of Brazilian sections of 0.5 mm in thickness. The opaque bands of
flathead have been determined through the counting of these sections were counted by two independent
the otolith rings (Tomo, 1969; San Romn, 1974; readers under incident and transmitted light using a
Perrotta & Fernndez-Gimnez, 1996). However, stereomicroscope at 40X magnification. Age was
none of these authors reported the growth parameters determined to the nearest lower without knowledge of
of each sex nor validated the determined ages. In the length and sex of the specimen. If the two
marine teleost fishes it is assumed that growth independent readings differed, then the otolith was
increments are laid down annually on hard parts, such considered unreadable. We used the average percent
as scales or otoliths, and the age is determined by error (APE), the coefficient of variation (V) and the
counting the rings that are present in these hard index of precision (D) (Beamish & Fournier, 1981;
structures (Jones, 1992; Campana & Thorrold, 2001). Chang 1982) to test the reproducibility between agers
Errors in the assignment of age may contribute to of the ageing process, from 845 otoliths (620 spring,
overexploitation of a stock or species, often through 225 winter).
underestimating true age and producing optimistic Age validation
estimates of growth and mortality rates. Consequently, The validation of the annual formation of opaque
validation of age readings is a requirement for manage bands was established by examining the monthly
stocks, particularly for those being assessed by means proportions of opaque or translucent edges (Dannevig,
of age-structured models (Campana, 2001; Begg et al., 1933) throughout a year. Monthly samples (1367
2005). otoliths) from commercial fisheries in the same area,
Therefore, the aims of this study were determine from January to December 2007, were use to validate
the age of males and females of Brazilian flathead, the age.
validate it, obtain the growth parameters of each sex
(in spring and winter) and compare it statistically Growth
(between sexes, in each season; and between season, The Von Bertalanffy growth model (1938) was fitted,
for each sex). The seasonal migration of Brazilian in each season, to observed length-at-age data of
Age and growth of brazilian flathead 299

Figure 1. Study area showing their bathymetry (m) and the location of the sampling stations during spring () and winter
().
Figura 1. rea de estudio indicando la batimetra y localizacin de las estaciones de muestreo durante primavera () e
invierno ().

males and females by nonlinear regression TL = L (1 RESULTS


e k(t t0); where TL is the total length (cm) at
age t (years), L the mean maximum total length Age determination
(cm), k a growth rate parameter (year-1) and t0 the Of the 1467 otoliths that were examined, 1449 were
theoretical age (years) at zero length. The likelihood considered readable (98.8% of coincidence between
ratio test (LRT) was used to estimate the growth readers). The average percent error (APE = 0.668%),
parameters (L, k, t0) and to compare the growth the coefficient of variation (V = 1.121%) and the
curves (Aubone & Whler, 2000). The approximate index of precision (D = 0.647) indicate that the
growth parameter values required by LRT were determination of age was consistent. All the spring
obtained following Gulland & Holts methodology otoliths sections showed opaque bands at the edge,
whereas the 99.2% of the winter otoliths showed a
(1959) for L [male (spring = 57.6 cm, winter 63.5
translucent one. The first band next to the core was not
cm), female (spring = 63.3 cm, winter 62.1 cm)] and
as well defined as the others and in the 95.4% of the
von Bertalanffys methodology (1934) for k [males
otoliths it was opaque. In some cases this band was
(spring = 0.28 year-1, winter = 0.21 year-1), female very much thicker (or very much thinner) than the
(spring = 0.43 year-1; winter = 0.29 year-1)] and t0 second opaque band, in other cases was composed of
[males (spring = -1.93 years; winter = -1.54 years), 1 to 3 opaque bands separated by much thinner
female (spring = -0.04 years, winter = 1.79 years)] translucent bands, or was less visible than the other
(Sparre & Venema, 1995). These approximate values opaque bands, or was present on one side of the
were also used to evaluate the goodness of fit of sulcus. This band was only considered if it was
different growth models through the Quasi-Newton present inside the sulcus.
Method (QNM) of the Statistica 6 Program. QNM The age and length ranges of each considered
was also used to estimate the goodness of fit of the group of Brazilian flathead specimens were: males
selected growth model to the observed length-at-age [spring (0-14 years), (24-61 cm); winter (0-19 years),
data. All statistical inferences were based considering (26-63 cm)], females [spring (0-14 years), (20-67 cm);
an alpha error level of 5% ( = 0.05). winter (0-15 years), (23-73 cm)]. Both sexes showed,
300 Lat. Am. J. Aquat. Res.

in each season, unimodal age frequency distributions:


males showed a modal value of 2 years in both
seasons, whereas spring modal value of females (2
years) was smaller than the one of winter (4 years)
(Fig. 2).

Age validation
The monthly proportions of the sagittal otoliths edge
types showed that the opaque-band formation begins
in September and it remains present at the otolith edge
until February; from this month on, the translucent
band begins to lay down and it is present at the
otoliths edge until September, when the opaque-band Figure 3. Monthly frequency of the opaque and
formation begins (Fig. 3). This beginning of the translucent edges in the sagitta otolith of Percophis
opaque band formation is earlier in males than in brasiliensis males () and females () during 2007 and
females. These results show that, annually, one the monthly sample size by sex. Transverse section of a
opaque and one translucent band are deposited at the sagitta, at core level, of a 5 years old specimen collected
edge of the sagittal otoliths and, therefore, one opaque in winter.
plus one translucent band represents 1 year of the Figura 3. Frecuencia mensual de bordes opacos y
fishs life. translucidos en otolitos sagitta de Percophis brasiliensis
por sexo: machos () y hembras () durante el ao 2007 y
Growth tamaos mustrales mensuales por sexo. Seccin
transversal de un sagitta, a nivel del ncleo, de un
The von Bertalanffy growth model showed a good fit
espcimen de 5 aos de edad colectado en invierno.
to the observed length-at-age data (Table 1): females
are larger than males of the same age from the first
year of life (Figs. 4a y 4b). At this age, both sexes Females grow faster and attain larger sizes than the
attain 50% of its maximum total length. Comparison males [L (P < 0.01), k (P < 0.1), t0 (P < 0.01), in
of growth parameters for both seasons showed spring; and L (P < 0.01), k (P < 0.05), t0 (P < 0.1), in
significant differences between sexes (LRT, P < 0.01). winter] (Figs. 4a-4b; Table 1). The difference between
ks of both sexes was marginally significant in spring
(P = 0.06).
Furthermore, significant differences in the
estimated growth parameters of each sex were
detected between seasons (LRT, P < 0.05 for males
and P < 0.01 for females) (Figs. 4c-4d). The males
showed marginally significant differences in k (P =
0.077) and t0 (P = 0.056), but did not differ in L (P >
0.5); whereas the females showed significant
differences in L (P < 0.01) and t0 (P < 0.01), but did
not differ in k (P > 0.05).

DISCUSSION

The high coincidence percentage among the two


independent readers as well as the values of the
precision indices indicate that the sagitta otolith of
Brazilian flathead is easy to read, as happens with
most of sagitta otoliths of template waters marine
fishes (Panella, 1974; Ricker, 1979; Sparre &
Figure 2. Age frequency distributions of males (a) and Venema, 1995). In spite of this, there were doubts
females (b) during spring () and winter (). about considering or not the first opaque band next to
Figura 2. Distribuciones de frecuencia de edades de the core because it was not as well defined as the
machos (a) y hembras (b) durante primavera () e others. Peres & Haimovici (2004), studying chernias
invierno (). Polyprion americanus (Bloch & Schneider) otoliths,
Age and growth of brazilian flathead 301

Table 1. Von Bertalanffys growth parameters (L, k, t0) of Percophis brasiliensis, determination coefficient (r2)
estimated through LRT and QNM respectively, and sample size (n).
Tabla 1. Parmetros de crecimiento de von Bertalanffy (L, k, t0) de Percophis brasiliensis, coeficiente de determinacin
(r2) estimado mediante de LRT y QNM respectivamente, y tamao muestral (n).

Males Females
Parameter
Spring Winter Spring Winter
L (cm) 58.1 58.7 65.2 63.5
k (year-1) 0.26 0.21 0.29 0.26
t0 (years) -2.02 -2.90 -1.15 -2.01
n 439 251 414 345
r2 0.82 0.66 0.84 0.67

Figure 4. Growth curves of both sexes ( males and females) of Percophis brasiliensis in a same season, a) spring and
b) winter, and of each sex c) males and d) females by season ( spring and winter). Observed mean total length-at-age
and fitted von Bertalanffy growth model (dash line, predicted total length values for ages out of observed range). Sample
sizes (n) of each comparison were: a) ( 439 and 414), b) ( 251 and 345), c) ( 439 and 251) and d) ( 414 and
345).
Figura 4. Curvas de crecimiento de ambos sexos ( machos y hembras) de Percophis brasiliensis en una misma
estacin, a) primavera y b) invierno), de cada sexo c) machos y d) hembras por estacin ( primavera y invierno).
Longitud total media por edad observada y modelo de crecimiento de von Bertalanffy ajustado (lnea discontinua, valores
de longitud totales predichos para edades fuera del rango observado). Tamaos muestrales (n) para cada comparacin: a)
( 439 y 414), b) ( 251 y 345), c) ( 439 y 251) y d) ( 414 y 345).

considered it as a false band, and named it central years, San Romn (1974); 12 years, Perrotta &
area. However, the age determinations made to the Fernndez-Gimnez (1996)].
nearest inferior age are not modified by considering or It was verified that only one opaque and one
not this band. Future studies must be done to verify if translucent band are laid down annually in the sagittal
this first opaque band is true or not. The maximum otoliths of Brazilian flathead, which appear between
ages observed in this study (19 years for males and 15 September-February and during the rest of the year,
for females) were higher than maximum ages respectively. This result is consistent with previous
registered for the species [6 years, Tomo (1969); 7 studies for other coastal species at the region e.g.
302 Lat. Am. J. Aquat. Res.

Micropogonias furnieri (Desmarest) (Cotrina, 1998), old specimens (age from which maximum total length
Cynoscion guatucupa (Cuvier) (Castelli-Vieira & seems to be reached) and of the greater longevity of
Haimovici, 1993; Lpez-Cazorla, 2000) and Pogonias them. In the case of k, differences could be
cromis (Linnaeus) (Urteaga & Perrotta, 2001). The consequence of the greater number of < 3 years old
opaque-band (fast growth) formation period coincides, specimens and of its younger ages. The age and
partially, with Brazilian flatheads reproductive growth determinations done indicate that Brazilian
period. Males reproductive period (August-April) is flathead is a relatively long-lived, low-growing
wider than the females (October-April) (Rodrgues,
species; as most of the demersal species of the South
2009). This difference could be responsible of the
Atlantic coastal water (34-41S) (Lasta et al., 2000),
earlier onset of males opaque-band formation.
like M. furnieri (Agemax = 39 years; kmax 0.20
The Von Bertalanffy growth model acceptably year-1; Carozza et al., 2004), C. guatucupa (Agemax =
described (r2 0.7) Brazilian flatheads growth, as 23 years; kmax 0.40 year-1; Ruarte et al., 2004),
generally occurs when this model is fitted to length-at- Pagrus pagrus (Linnaeus) (Agemax = 16 years; kmax
age data of adult specimens (Jones, 1992; Sparre & 0.15 year-1; Cotrina & Carozza, 2000) and P. cromis
Venema, 1995). The estimated L (`s: 58.1 and 58.7 (Agemax = 41 years; kmax 0.18 year-1; Urteaga &
cm; s: 65.2 and 63.5 cm) values were lower than the Perrotta, 2001).
values estimated previously by Tomo (1969) [L =
Brazilian flathead showed differential growth from
86.94 cm (pooled sexes); L = 84.70 cm (females)], by
the first year of life (Figs. 4a-4b); in coincidence with
San Romn (1974) [L = 86.2 cm (pooled sexes)], and
San Romn (1974) females are larger than males of
by Perrotta & Fernndez Gimnez (1996) [L = 68.39 the same age. Considering the age determinations
cm (pooled sexes; northern study area); L = 70.78 cm done in this study and the length-at-maturity reported
(pooled sexes; southern study area)] (Tables 1 and 2). by Militelli (1999), males first sexual maturity occurs
On the other hand, the estimated k values (`s: 0.26 when they are 1 years old (TL50% = 29.24 cm), while
and 0.21 year-1; s: 0.29 and 0.26 year-1) were higher in females this happens when they are 2 years old
than those estimated by San Romn (1974) [k = 0.170 (TL50% = 38.71 cm). This asynchronism in the sexual
year-1 (pooled sexes)] and by Perrotta & Fernndez- maturity could explain the differential growth
Gimnez (1996) [k = 0.186 year-1 (pooled sexes; developed for each sex because, from this event, the
northern study area); k = 0.145 year-1 (pooled sexes; growth rate decreases markedly (Brett, 1979). The
southern study area)]; were also higher than those earlier onset of males sexual maturity could be
estimated by Tomo (1969) [k = 0.210 year-1 (pooled responsible for both the earlier decrease of their
sexes); k = 0.220 year-1 (females)], with the exception growth rate and, consequently, the lower total length
of the males k value of winter (k = 0.210 year-1) reached because, after this event, they ought to
which was similar to those values estimated by the channel surplus energy not only into growth, like
latter author (Tables 1 and 2). females do up to 2 years old, but also into reproduc-
The lower L values estimated in this study could tion. This sexual dimorphism in growth, with females
be a consequence of the greater number of > 9 years larger than males of the same age, is common in some

Table 2. Percophis brasiliensiss growth parameters (L, k, and t0) obtained, from von Bertalanffys model, by previous
studies in the southwest Atlantic coastal water (34-41S).
Tabla 2. Parmetros de crecimiento de Percophis brasiliensis obtenidos (L, k, and t0), a partir del modelo de von
Bertalanffy, por estudios previos en aguas costeras del Atlntico sudoccidental (34-41S).

Sample L k t0
Reference Sex
Area Season Type (cm) (year-1) (years)

Perrotta & Fernndez-Gimenz (1996) Northern Winter Research 68.39 0.186 -1.956
SACS
Perrotta & Fernndez-Gimnez (1996) Southern Winter Research 70.78 0.145 -2.858
SACS
San Romn (1974) Inside All year Commercial 86.20 0.170 0.270
SACS round
Tomo (1969) Inside Not Commercial 86.94 0.210 0.160
SACS available
Tomo (1969) Inside Not Commercial 84.70 0.220 0.035
SACS available
Age and growth of brazilian flathead 303

coastal species that inhabit the South Atlantic coastal directions in innovation and implementation. Mar.
water (34-41S), like M. furnieri (Carozza et al., Freshw. Res., 56: 477-483.
2004) and C. guatucupa (Ruarte et al., 2004). Bergonzi, C. 1997. Interrelaciones trficas de algunas
Finally, differences in the growth parameters of especies de peces del rea costera de la provincia de
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Received: 27 May 2010; Accepted: 22 May 2011


Lat. Am. J. Aquat. Res., 39(2): 306-315, 2011 Lat. Am. J. Aquat. Res. 306
DOI: 10.3856/vol39-issue2-fulltext-12

Research Article

Seasonal variation and influence of turbidity and salinity on the zooplankton of a


saline lake in central Argentina

Santiago Andrs Echaniz1 & Alicia Mara Vignatti1


1
Facultad de Ciencias Exactas y Naturales, Universidad Nacional de La Pampa
Avenida Uruguay 151, 6300 Santa Rosa, Provincia de La Pampa, Repblica Argentina

ABSTRACT. The limnology of saline water bodies at other latitudes is fairly well known, but in Argentina
such studies have only recently begun. The applicability of many conclusions regarding the functioning of
these environments around the world is limited due to the scant ecological knowledge of some endemic
species recorded in the assemblages of Argentine lakes. The aims of this work were to determine the effects of
salinity and inorganic turbidity on the taxonomic composition, abundance, and zooplankton biomass in a
shallow, hypereutrophic, mesosaline lake in the north of La Pampa province characterized by seasonality,
variations in level and salinity, and the lack of macrophytes and fishes, and to compare it with other shallow
lakes of the province. We found important differences with other saline lakes: the species richness was lower;
the mean abundance of zooplankton was between four and six times higher; and rotifers, which were not
affected by salinity or the concentration of inorganic suspended solids, were numerically predominant.
Crustaceans, on the other hand, were negatively affected by these environmental factors. Biomass was two-
fold higher than that recorded in the same period in two shallow lakes of Pampa, with similar nutrient
concentrations but lower salinities.
Keywords: saline lakes, inorganic turbidity, zooplankton biomass, Boeckella poopoensis, Argentina.

Variacin estacional e influencia de la turbidez y la salinidad sobre el zooplancton


de un lago salino de la regin central de Argentina

RESUMEN. La limnologa de los cuerpos de agua salinos de otras latitudes es bastante conocida, pero en
Argentina se ha comenzado a estudiar recientemente. Muchas conclusiones sobre el funcionamiento de estos
ambientes a nivel mundial son de aplicacin restringida debido a que las asociaciones registradas en los lagos
argentinos tienen algunas especies endmicas, cuyo conocimiento ecolgico es escaso. Los objetivos de este
trabajo fueron determinar los efectos de la salinidad y la turbidez inorgnica sobre la composicin taxonmica,
abundancia y biomasa zooplanctnica en un lago somero mesosalino hipereutrfico del norte de La Pampa,
caracterizado por su temporalidad, variaciones del nivel y salinidad, carencia de macrfitas y peces, y
compararlo con otros lagos someros de la provincia. Se encontraron importantes diferencias con otros lagos
salinos, la riqueza especfica fue menor, la abundancia media del zooplancton fue entre 4 a 6 veces superior y
el predominio numrico fue de los rotferos, que no fueron afectados por la salinidad o la concentracin de
slidos suspendidos inorgnicos, a diferencia de los crustceos, que fueron afectados negativamente por estos
factores ambientales. La biomasa fue dos veces ms elevada que la registrada en el mismo perodo en dos
lagos someros pampeanos con parecida concentracin de nutrientes pero con salinidades menores.
Palabras clave: lagos salinos, turbidez inorgnica, biomasa zooplanctnica, Boeckella poopoensis, Argentina.

___________________
Corresponding author: Santiago Echaniz (sechaniz@cpenet.com.ar)

INTRODUCTION 1986). They are widely distributed in the world and


are abundant in arheic and endorheic basins of arid
Saline water bodies can be defined as those with and semiarid regions (Williams, 2002). They are
salinities equal to or higher than 3 g L-1 (Hammer, highly influenced by the human activities carried out
307 Zooplankton of a turbid saline lake of Argentina

in their basins, which cause changes in their Forest (Cabrera, 1976). Has a surface of 62.8 ha and a
characteristics, with the consequent loss of maximum depth of 2.6 m.
biodiversity (Velasco et al., 2006). The mean annual precipitations of the region are
The limnology of water bodies in other latitudes is around 700 mm (Casagrande et al., 2006), with a
relatively well-known, whereas, in Argentina, there maximum in summer, but the potential evapotrans-
are only a few reports on the saline lakes of Buenos piration is about 800 mm year-1 (Roberto et al., 1994).
Aires (Olivier, 1955; Ringuelet, 1968, 1972) and The lake is fed by rainfalls and, to a lesser extent, by
Santa Fe provinces (Jos de Paggi & Paggi, 1998), the phreatic waters. It is an arheic water body, which loses
northwest (Locascio de Mitrovich et al., 2005; water by evaporation or infiltration and suffers large
Villagra de Gamundi et al., 2008) and Crdoba level fluctuations. The land of its basin is used for
province (Bucher, 2006). Therefore, the information agriculture and extensive cattle breeding. It has a
on their taxonomic composition, abundance and regular shape, its bottom sediments consists mainly of
zooplankton biomass and its variation is still scarce. sands, and there is absence of macrophytes and ichtyc
We have thus recently started studies on the fauna.
ecology and zooplankton of saline lakes of La Pampa
province, in the semiarid center of Argentina (Echaniz Field and laboratory work
et al., 2005, 2006; Vignatti et al., 2007). However, in Samples were collected monthly from December 2005
those works, we determined mainly the population until December 2006, except in August, in the three
density but not the biomass in relation with stations located along the longest axis of the lake.
environmental parameters. Water temperature, dissolved oxygen concentration
Many of the conclusions on the functioning of (oximeter Lutron OD 5510), water transparency
saline lakes are applicable for the shallow lakes of La (Secchi disc), and pH (digital pH meter Cornning PS
Pampa, but little is known on the ecology of the 15) were determined in each station. Water samples
assemblages recorded in the central region of were taken and kept refrigerated until their analysis in
Argentina, where some species, especially the laboratory.
crustaceans, are endemic to the neotropical region Two quantitative zooplankton samples were
(Adamowicz et al., 2004; Echaniz et al., 2005, 2006; collected in each site with a 10-l Schindler-Patalas
Vignatti et al., 2007). trap, with a 0.04 mm mesh size, and one qualitative
The aims of this work were to analyze the sample with a net 22 cm in diameter and a similar
variations in the main limnological parameters and the mesh size. All the samples were anesthetized with
zooplankton of an inorganic turbid shallow lake with CO2 and kept refrigerated until fixation, with the aim
high salinity, located in the north of La Pampa to avoid contractions that may deform the individuals
province, along its annual cycle, and to test the collected.
following hypotheses: i) that the high concentration of Salinity was determined by means of the
dissolved solids affects the taxonomic composition gravimetric method with drying at 104C.
and abundance of the zooplankton community, ii) that Chlorophyll-a concentration was measured by
inorganic turbidity has detrimental effects on the extraction with aqueous acetone and spectropho-
development of zooplankton (Quirs et al., 2002; tometry (spectrophotometer Metrolab 1700) (Arar,
Torremorell et al., 2007), and iii) that at nutrient 1997; APHA, 1999), total nitrogen by means of the
concentrations equal to those of other Pampean water Kjeldahl method, and total phosphorus by digestion
bodies with lower salinity, this lake has a higher with potassium peroxodisulfate in acid medium and
biomass of zooplankton, in agreement with that UV-visible spectrophotometry (APHA, 1999).
reported by Evans et al. (1996) for lakes of Canada. The content of suspended solids was determined
with fiberglass filters (Microclar FFG047WPH), dried
MATERIALS AND METHODS at 103-105C until constant weight and calcined at
550C (EPA, 1993). Macro-and microzooplankton
Study area (Kalff, 2002) were counted under a stereoscopic and a
The Prato shallow lake is located in the north of La conventional optical microscope, in Bogorov and
Pampa province (6415W, 3526S) (Fig. 1), in a Sedgwick-Rafter chambers respectively.
plain region with soft hills and covered with a sand Conventional measurements of the individuals of
layer of variable thickness (Calmels & Casado, 2005), each species sampled were taken with a Carl Zeiss
in the ecotone between the phytogeographical ocular micrometer, and length-dry weight formulae
provinces of the Pampean Plains and the Thorny were used to determine zooplankton biomass (Dumont
Lat. Am. J. Aquat. Res. 308

Figure 1. Location of the Prato shallow lake in the north of La Pampa province, Argentina. a, b and c: sampling sites.
Figura 1. Localizacin de la laguna de Prato en el norte de la provincia de La Pampa, Argentina. a, b y c: sitios de
muestreo.

et al., 1975; Rosen, 1981; McCauley, 1984; Culver et


al., 1985; Kobayashi, 1997).
Non parametric ANOVA Kruskal Wallis test,
Spearmans correlations and principal component
analysis (PCA) (Zar, 1996; Mangeaud, 2004; Prez,
2004) were carried out by means of the PAST
software version 1.94b (Hammer et al., 2001).

RESULTS

Physical and chemical parameters


Figure 2. Monthly variation of maximum depth and
Spatial variations of this parameters were not concentration of total dissolved solids (TDS) in Prato
significant, so we used mean values. The mean shallow lake.
concentration of total dissolved solids in the water was
Figura 2. Variacin mensual de la profundidad mxima
25.3 g L-1, but increased as the level of water y de la concentracin de slidos disueltos totales (TDS)
decreased (Fig. 2 and Table 1), and was characterized en la laguna de Prato.
by the predominance of Cl- and Na+, which were
higher than 49% and 92% of the anions and cations The concentration of organic suspended solids was
respectively. The pH was high (9.02 0.16) and higher during the first four months and was
relatively stable (Table 1). significantly correlated with chlorophyll-a concen-
The water temperature varied seasonally, with a tration (R = 0.65; P = 0.022), whereas that of
maximum of 26.8C in December 2005 and a inorganic suspended solids was more abundant during
the last six months (Fig. 4). We found a significant
minimum of 8.1C in July 2006 (Fig. 3). The
correlation between the concentration of inorganic
concentration of dissolved oxygen was also variable, suspended solids and that of total phosphorus (R =
oscillating between 9.8 mg L-1 in December 2005 and 0.75; P = 0.005).
1.3 mg L-1 in April 2006 (Fig. 3). The concentration of Water transparency was reduced (0.17 m 0.06)
nutrients was high and variable (Table 1). and variable along the year (Fig. 5, Table 1), and was
Chlorophyll-a concentration correlated with water significantly correlated with the concentration of
temperature (R = 0.73; P = 0.0065) and presented a inorganic suspended solids (R = -0.89; P = 0.0001),
maximum in February 2006, but was relatively low but not significantly correlated with that of organic
and stable during the rest of the period studied (Fig. suspended solids (R = 0.02; P = 0.940) or chlorophyll-
4). a concentration (R = 0.40; P = 0.194) (Fig. 8).
309 Zooplankton of a turbid saline lake of Argentina

Table 1. Main physical and chemical parameters registered in Prato shallow lake during the studied period. TP: total
phosforus, TN: total nitrogen.
Tabla 1. Principales parmetros fsico qumicos registrados en la laguna de Prato durante el perodo estudiado. TP:
fsforo total, TN: nitrgeno total.

Mean Min. Max.


Transparency (m) 0.17 0.08 0.31
Salinity (g L-1) 25.34 19.47 36.84
pH 9.02 8.9 9.32
TP (mg L-1) 18.1 11.25 25
TN (mg L-1) 28.62 20.63 35.63
TN:TP 1.58 1.3 2.5
Chlorophill-a (mg m-3) 30.79 9.35 94.79
Dissolved oxigen (mg L-1) 6.3 1.3 9.8
Inorganic suspended solids (mg L-1) 38.03 10 63.2
Organic suspended solids (mg L-1) 37.52 16 78.7

Figure 4. Monthly variation of the concentration of


Figure 3. Monthly variation of water temperature and inorganic and organic suspended solids and chlorophyll-
dissolved oxygen concentration in Prato shallow lake. a in Prato shallow lake.
Figura 3. Variacin mensual de la temperatura del agua Figura 4. Variacin mensual de la concentracin de
y de la concentracin de oxgeno disuelto en la laguna de slidos suspendidos inorgnicos y orgnicos y de
Prato. clorofila-a en la laguna de Prato.

Zooplankton The density of the community presented two peaks


We recorded a total of six species (Table 2). Among during the warmer months (Fig. 6), produced mainly
crustaceans, Moina eugeniae and the calanoid by rotifers (B. dimidiatus in January 2006 and B.
Boeckella poopoensis were constantly present, plicatilis in December 2006). Although their
whereas M. macrocopa and the harpacticoid abundance was very variable and there were months
Cletocamptus deitersi were recorded along four and during which they were not recorded, they presented
nine months respectively. Among rotifers, Brachionus the highest annual mean abundance (Fig. 7, Table 2).
plicatilis was present along 10 months, whereas B. The PCA, whose first two components allowed
dimidiatus along only 2 months (Table 2). Variations explaining more than 60% of the variance, showed
of micro- and macrozooplankton abundance between positive correlations between their abundance, the
sampling sites were not significant. concentrations of organic suspended solids,
The spatial variations of the zooplankton chlorophyll-a and water temperature, but negative
abundance and biomass were not significant, so we correlations between their abundance and salinity and
used mean values. inorganic suspended solids concentrations (Fig. 8).
Lat. Am. J. Aquat. Res. 310

Figure 6. Monthly variation in the total zooplanktonic


abundance in Prato shallow lake. The values are the
mean of the three sampling stations.
Figure 5. Monthly variation of water transparency in Figura 6. Variacin mensual de la abundancia total
Prato shallow lake. zooplanctnica en la laguna de Prato. Los valores
Figura 5. Variacin mensual de la transparencia del agua corresponden al promedio de las tres estaciones de
en la laguna de Prato. muestreo.

Among crustaceans, the most abundant species was


B. poopoensis followed by M. eugeniae (Table 2). B.
poopoensis presented its maximum abundances at the
beginning of the summer, whereas M. eugeniae and
M. macrocopa did so during fall. The PCA showed
positive correlations between crustacean abundance,
chlorophyll-a concentration and water transparency,
but negative ones between crustacean abundance,
salinity and inorganic suspended solids (Fig. 8).
The mean biomass of the zooplankton community
(6614.1 g L-1 4336.9) presented a peak during fall
and a minimum in spring (Fig. 9). In all cases, the Figure 7. Monthly variation in the percent composition
highest contribution was that of crustaceans (Fig. 10), of the zooplanktonic abundance during the studied
among which B. poopoensis represented more than period. The values are the mean of the three sampling
their biomass and salinity and organic suspended solid stations.
concentrations. The contribution of rotifers was Figura 7. Variacin mensual de la composicin
important only in December 2006, when it represented porcentual de la abundancia zooplanctnica durante el
29.5% of the total (Fig. 10) and the PCA also showed perodo estudiado. Los valores corresponden al promedio
a positive correlation with abundance and water de las tres estaciones de muestreo.
temperature (Fig. 8).
DISCUSSION et al., 2005, 2006; Vignatti et al., 2007). This
phenomenon is particularly important because these
The Prato lake is located in the western boundary of lakes are located in a region where the evapo-
the Pampean plain (Cabrera, 1976), and although it transpiration overpasses precipitations (Roberto et al.,
shares characteristics with typical Pampean lakes of 1994). This characteristic was reflected in this lake by
the province of Buenos Aires (Ringuelet, 1968 and the decrease of almost 0.6 m in the water level and an
1972; Torremorell et al., 2007), such as the reduced increase in the concentration of dissolved solids,
depth and the polymixis, it differs from them because which, at the end of the study, was almost twice of the
of its seasonality and great variations in water level initial value, although it was within the mesosaline
and salinity. range (Hammer, 1986).
These fluctuations are typical of most shallow The absence of variations in the spatial distribution
lakes of La Pampa province, which are mainly fed by of physical and chemical parameters and zooplank-
precipitations and lose water by evaporation (Echaniz tonic abundance and biomass of this lake was
311 Zooplankton of a turbid saline lake of Argentina

Figure 8. Results of the Principal Component Analysis (PCA). Rot.: rotifers, Clad.: cladocerans, Cop.: copepods, Ab.:
abundance, Biom.: biomass, TN and TP: total nitrogen and phosphorus concentrations, Inorg. susp. sol.: inorganic
supended solids, Org. susp. sol.: organic suspended solids, Transp.: water transparency, Temp.: water temperature, Chl a:
chlorophyll concentration.
Figura 8. Resultados del Anlisis de Componentes Principales (ACP). Rot.: rotferos, Clad.: cladceros, Cop.:
coppodos, Ab.: abundancia, Biom.: biomasa, TN y TP: concentraciones de nitrgeno y fsforo totales, Inorg. susp. sol.:
slidos suspendidos inorgnicos, Org. susp. sol.: slidos suspendidos orgnicos, Transp.: transparencia del agua, Temp.:
temperatura del agua. Chl a: concentracin de clorofila.

Table 2. List of species recorded, mean, minimum and maximum abundance and biomass and relative frequency of their
appearance in the samples.
Tabla 2. Lista de las especies registradas, abundancia y biomasa medias, mnimas y mximas y frecuencia relativa de
aparicin en las muestras.

Frequency Abundance (ind L-1) Biomass (g L-1)


(%) Mean Min. Max. Mean Min. Max.
Cladocerans
Moina eugeniae Olivier, 195 100 219.1 14 1235.3 1611.4 153 8190.2
Moina macrocopa (Straus, 1820) 33.3 28 0 312.7 185.54 0 2101.1
Copepods
Boeckella poopoensis Marsh, 1906 100 369.7 72.7 737.3 4236.3 512.2 9436
Cletocamptus deitersi (Richard, 1897) 66.7 4.2 0 13.5 4.28 0 17.2
Rotifers
Brachionus plicatilis Mller, 1786 83.3 1330.4 0 11546.7 412 0 3002.1
Brachionus dimidiatus Bryce, 1931 16.7 872.5 0 10467 34.9 0 418.7

probably related to their shallow depth, the shape of tionally low bivalent cations concentrations (Ca++ and
their basin (flat and free from obstacles) and to wind Mg++) (Echaniz et al., 2006).
action, all of which determine their polymictic The lake studied presented some characteristics
condition and the permanent mixture of water. that differentiate it from other environments of La
Another feature shared by most lakes of La Pampa Pampa with similar salinity, in particular, among the
is the predominance of Cl- and Na+, with propor- physical factors, its reduced transparency, which was
Lat. Am. J. Aquat. Res. 312

Figure 9. Monthly variation in total zooplankton Figure 10. Monthly variation in the percent composition
biomass during the studied period. The values are the of zooplankton biomass. The values are the mean of the
mean of the three sampling stations. three sampling stations.
Figura 9. Variacin mensual de la biomasa total del Figura 10. Variacin mensual de la composicin
zooplancton durante el perodo estudiado. Los valores porcentual de la biomasa del zooplancton. Los valores
corresponden al promedio de las tres estaciones de corresponden al promedio de las tres estaciones de
muestreo. muestreo.

almost 10 times lower than that recorded in previous shallow lakes (Markensten & Pierson, 2003; De
studies (Echaniz et al., 2006; Vignatti et al., 2007). Vicente et al., 2006; Borell-Lvstedt & Bengtsson,
This high turbidity was due to the differential 2008), since removal favors the resolubilization of the
predominance of the two fractions of suspended solids nutrients of the internal load (Havens et al., 2007),
along the year. Those of organic origin were higher which, in turn, favors the internal eutrophication of the
during the summer, when the concentration of lake (Smolders et al., 2006). This was probably the
chlorophyll-a was also high, whereas those of case in the lake studied in this work, since the highest
inorganic origin were higher during winter and spring, concentrations of phosphorus were found during the
when more intense winds are present (Cano, 1980). second half of the year, during which stronger winds
Due to the scarce depth of the lake, these winds cause are present (Cano, 1980) and the concentrations of
the removal and resuspension of bottom sediments inorganic suspended solids were highest. In addition,
(Scheffer, 1998; Borell Lvstedt & Bengtsson, 2008). the reduced capacity of phosphorus and nitrogen
In addition, unlike that found in similar lakes of the absorption of the sediments due to the relatively large
province, this situation was favored by the total size of the predominant particles (Kapanen, 2008) and
absence of macrophytes, which make resuspension to the fact that water is lost only by evaporation
more difficult. because the lake is an arheic environment leads to
accumulation processes.
The high concentrations of nutrients, which
allowed us to characterize the lake as hypereutrophic Zooplankton diversity was reduced, a common
(OECD, 1982), were similar to those of other situation in environments with high salinity (Hammer,
environments of La Pampa (Echaniz et al., 2008; 1986; Herbst, 2001; Ivanova & Kazantseva, 2006), but
Echaniz & Vignatti, unpublished data), but, in another feature that differentiates this lake from others
particular, total phosphorus was several times higher of La Pampa is the lower species richness found, since
than those reported by Quirs et al. (2002) and the species richness in other lakes with similar
Sosnovsky & Quirs (2006) for shallow lakes of concentrations of dissolved solids but much higher
Buenos Aires province. This could be due, on one transparency is close to 15 (Echaniz et al., 2006,
hand, to the high impact caused by the dragging of the Vignatti et al., 2007).
feces of animals that feed on its basin, especially As regards the zooplankton found, the species
during storms (Carpenter et al., 1998; Bennett et al., recorded were typical of these ecosystems and were
1999; Bremigan et al., 2008), since cattle can excrete characterized by the presence of autochthonous
between 9 and 16 kg of phosphorus.ind.year-1 (Russell halophilic crustaceans, such as Moina eugeniae, a
et al., 2008). On the other hand, the resuspension of species restricted to saline waters of the central region
sediments by the wind is particularly important in of Argentina (Paggi, 1998; Echaniz et al., 2006), and
313 Zooplankton of a turbid saline lake of Argentina

Boeckella poopoensis, a species that has a very wide financial support of the project and Mr. Hugo Prato
geographical distribution, from the north of Patagonia and his family, owners of the rural establishment in
to the south of Per (Menu-Marque et al., 2000; De which the lake is located.
los Ros, 2005; Locascio de Mitrovich et al., 2005).
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Received: 10 August 2010; Accepted: 22 May 2011


Lat. Am. J. Aquat. Res., 39(2): 316-326, 2011 Lat. Am. J. Aquat. Res. 316
DOI: 10.3856/vol39-issue2-fulltext-13

Research Article

Estimacin de mortalidad natural e incertidumbre para congrio dorado


(Genypterus blacodes Schneider, 1801) en la zona sur-austral de Chile

Rodrigo Wiff1, J.C. Quiroz1, Vilma Ojeda1 & Mauricio A. Barrientos2


1
Divisin de Investigacin Pesquera, Instituto de Fomento Pesquero
Blanco 839, Valparaso, Chile
2
Instituto de Matemticas, Pontificia Universidad Catlica de Valparaso
Blanco Viel 596, Cerro Barn, Valparaso, Chile

RESUMEN. El congrio dorado (Genypterus blacodes) es un pez demersal de gran importancia econmica en
la pesquera multiespecfica y multiflota que opera en la zona sur-austral de Chile (4128-5700S). Desde
principio de los aos noventas se consider para efectos de la evaluacin poblacional la existencia de un nico
stock. Sin embargo, varios antecedentes relacionados con la historia de vida y demografa han conducido a
que, desde el ao 2005, la evaluacin de esta especie se realice bajo dos stocks administrativos, uno en la zona
norte (4128-4700S) y otro en la zona sur (4700-5700S). La separacin de stocks produce una demanda
por actualizacin de parmetros de historia de vida, entre stos la mortalidad natural (M). En este trabajo se
estim M para el congrio dorado mediante mtodos empricos aplicados por zona y sexo. La incertidumbre en
M fue incorporada a travs de remuestreo de Monte Carlo considerando dos fuentes de error, una proveniente
de los parmetros de historia de vida que alimentan los modelos empricos y otra, proveniente de los
coeficientes que los definen. El promedio de M mediante los diferentes mtodos mostr, para una determinada
zona, importantes diferencias entre sexos, como tambin para sexos conjuntos entre zonas de pesca. Los
individuos de la zona norte presentaron mayor M que aquellos provenientes de la zona sur y los coeficientes de
variacin por mtodo son altamente dependientes del tipo de error incorporado. El mtodo de Pauly (1980)
parece ser el ms adecuado para el congrio dorado entregando valores de M para sexos conjuntos de 0,27 ao-1
(IC: 0,13-0,47) en la zona norte y 0,23 ao-1 (IC: 0,11-0,40) en la zona sur.
Palabras clave: Genypterus blacodes, mortalidad natural, pesquera demersal, historias de vida, demografa,
sur de Chile.

Estimation of natural mortality and uncertainty in pink cusk-eel


(Genypterus blacodes Schneider, 1801) in southern Chile
ABSTRACT. Pink cusk-eel (Genypterus blacodes) is a demersal fish of high economic importance for the
multi-species and multi-fleet fishery operating off far-southern Chile (4128-5700S). Since the early 1990s,
the existence of a single stock was assumed for purposes of stock assessments. However, several attributes
related with life history and demography led to the designation, as of 2005, of two administrative stocks of this
species, a northern-austral stock stock (4128-4700S) and a southern-austral stock (4700-5700S). The
division of these stocks has produced a demand for updating life history parameters, including natural
mortality (M). In the present work, we used empirical methods to estimate M for pink cusk-eel by zone and
sex. The uncertainty in M was incorporated through Monte Carlo resampling considering two sources of error:
one from the life history parameters that feed the empirical models and the other from the coefficients that
define them. The average M obtained by the different methods showed important differences between sexes
for a given zone and between combined sexes between the different fishing zones. The M for individuals from
the northern-austral zone was higher than that for those from the southern-austral zone. The coefficients of
variation by method were highly dependent on the type of error incorporated. Paulys (1980) method seems to
be the most appropriate for pink cusk-eel, providing M values for the combined sexes of 0.27 year-1 (IC: 0.13-
0.47) for the northern-austral zone and 0.23 year-1 (IC: 0.11-0.40) for the southern-austral zone.
Keywords: Genypterus blacodes, natural mortality, demersal fishery, life history, demography, southern
Chile.
___________________
Corresponding author: Rodrigo Wiff (rwiff@ifop.cl)
317 Mortalidad natural en congrio dorado, zona sur-austral de Chile

INTRODUCCIN la zona norte (4128S-4700S) y zona sur (4700-


5700S) de la zona sur-austral (Fig. 1), suponiendo la
Las especies que constituyen el gnero Genypterus existencia de dos unidades de stocks. Esta separacin
son peces bento-demersales que habitan el talud y de stocks requiere el anlisis de los parmetros de
plataforma continental en el hemisferio sur. Aunque historias de vidas diferenciados por zonas. En este
seis especies pertenecientes a este gnero podran ser sentido, si bien Wiff et al. (2007) contribuyeron
de inters econmico (Ward & Reilly, 2001), el proporcionando estimaciones de parmetros de creci-
congrio dorado (Genypterus blacodes) es la especie miento de von Bertalanffy por sexo, tanto para la zona
ms importante en trminos de intencionalidad de norte como la zona sur, an existe carencia sobre los
pesca y niveles de captura, conformando importantes valores de mortalidad natural (M) para cada zona con
pesqueras en Australia (Ward et al., 2001), Nueva sus valores de incertidumbre asociados.
Zelandia (Horn, 1993), Argentina (Cordo, 2001) y Las estimaciones disponibles de M para congrio
Chile (Wiff & Quiroz, 2010). dorado han sido realizadas en forma determinista y
Acorde a los registros histricos de capturas empleando mtodos bioanalgicos para la extensin
disponibles, la pesquera de congrio dorado en Chile total de la zona sur-austral (Aguayo et al., 1986; Ojeda
se ha desarrollado entre Talcahuano (3644S) y el sur et al., 1986). En este sentido, estimaciones detalladas
del Cabo de Hornos (5700S); sin embargo, la de M por zonas son altamente deseables para la
principal zona de explotacin est circunscrita a la determinacin de biomasas poblacionales. El principal
zona sur-austral (4128-5700S) (Fig. 1). objetivo de este trabajo es proveer estimaciones de
Actualmente, el congrio dorado es capturado por una mortalidad de congrio dorado por sexo y zona, por
pesquera multiflota constituida por una componente medio de un conjunto de modelos empricos e
industrial de embarcaciones arrastreras y palangreras, incorporado la incertidumbre intrnseca de diferentes
y una segunda componente artesanal de embar- parmetros de historia de vida.
caciones espineleras. Esta pesquera comenz a ser El enfoque de modelacin para la determinacin
monitoreada a principio de los aos setenta, del status del recurso y estrategias de explotacin
registrndose bajas capturas que evidenciaban una actualmente implementado en congrio dorado depende
reducida intencio-nalidad de pesca hacia esta especie. fuertemente de los valores de M (Wiff & Quiroz,
Durante la dcada de los ochenta la flota comenz a 2010). En efecto, M es un parmetro clave en la
dirigir esfuerzo sobre el recurso y ya a principio de los determinacin de la dinmica poblacional y esta tiene
aos noventa, debido a los altos niveles de captura influencia directa sobre los estimados de produccin,
registrados, las autoridades competentes decidieron ya sea en trminos de crecimiento somtico o la razn
declarar al congrio dorado en estado de plena entre la poblacin desovante y la abundancia de
explotacin (Decreto Supremo N 656). reclutas. A pesar de su importancia, M ha sido el
Este estado de explotacin corresponde a una parmetro de historia de vida estimado con menor
disposicin de la Ley General de Pesca y Acuicultura rigurosidad, esto en contraste con otros parmetros de
de Chile, que bsicamente faculta a la administracin historia de vida como fecundidad, madurez y
pesquera al establecimiento de cuotas de captura. En crecimiento (Hewitt & Hoenig, 2005). Idealmente, las
este contexto, desde 1992 esta pesquera se ha tasas de mortalidad natural debiesen ser estimadas a
manejado por medio de cuotas de captura lo que ha travs de mtodos tales como marcaje-recaptura o
llevado a estimar niveles de biomasas. Las anlisis telemtrico (Pollock et al., 2004). Sin
estimaciones de biomasas son obtenidas regularmente embargo, estos mtodos son difciles de implementar
desde modelos de evaluacin de stock, los que han para la poblacin de congrio dorado en Chile, tanto
contemplado el anlisis de poblacin virtual y los por el costo asociado, como los aspectos logsticos
modelos estadsticos de captura a la edad. Hasta el ao relativos a la prospeccin de un rea geogrficamente
2004, la modelacin inclua un nico stock de congrio accidentada como la zona sur-austral. Por otro lado, el
dorado distribuido en la zona sur-austral (Montecinos anlisis de la curva de captura es un mtodo comn
& Canales, 2004). Sin embargo, Wiff et al. (2005) para estimar mortalidad, sin embargo, este mtodo
mostraron diferencias demogrficas como tallas requiere supuestos acerca de la condicin virginal del
medias y proporcin sexual como tambin en la stock que es difcil de cumplir bajo los actuales
funcin de crecimiento al interior de la zona sur- niveles de explotacin de congrio dorado (Wiff &
austral, proponiendo una diferenciacin en las zonas Quiroz, 2010).
de manejo de la pesquera demersal sur-austral (PDA). Una alternativa para estimar M proviene de los
Bajo estos argumentos, desde el ao 2005 se viene mtodos empricos, los cuales bsicamente tratan de
realizando una modelacin poblacional separada para predecir procesos poblacionales complejos en base a
Lat. Am. J. Aquat. Res. 318

Figura 1. Mapa de la zona de estudio indicando las reas de pesca y las principales ciudades.
Figure 1. Map of the study zone indicating fishing areas and the main cities.

otros parmetros de historia de vida o atributos acuerdo a la disponibilidad y calidad de los


demogrficos que son ms fciles de obtener. parmetros de historia de vida. Los mtodos
Particularmente en el caso de M, las relaciones seleccionados fueron (1) Alverson & Carney (1975);
empricas tratan de dar cuenta de la relacin existente (2) Pauly (1980); (3) Frisk et al., (2001); (4) Hoenig
entre sta y otros parmetros de historia de vida. Estas (1983) y (5) Jensen (1996). Los tres primeros mtodos
relaciones han encontrado sustento terico, tanto consideran los parmetros de crecimiento de la
desde el punto de vista evolutivo (Charnov, 1993) funcin de von Bertalanffy en longitud,
como ecolgico (Jensen, 1996). En este trabajo se l(a) = l (1 e-k (a-a0)), donde l es la longitud a edad a,
emplean relaciones empricas para proporcionar un l es la longitud asinttica, k es el coeficiente de
rango plausible de M para congrio dorado crecimiento y a0 es la edad terica cuando l=0. El
incorporando la incertidumbre. mtodo de Hoenig usa la longevidad amax, mientras
que el mtodo de Jensen incorpora la edad de madurez
MATERIALES Y MTODOS a50%, como un indicador de la sobrevivencia (Tabla 1).
Los parmetros de crecimiento y sus errores
Las estimaciones de M se obtuvieron a travs de cinco estndar, separados por zonas de la PDA y sexo
mtodos empricos que fueron seleccionados de fueron obtenidos de Wiff et al. (2007), mientras que
319

Tabla 1. Descripcin de los mtodos aplicados y su coeficiente de variacin (CV). M: mortalidad natural; l y k: parmetros de crecimiento de la ecuacin de von
Bertalanffy, a50%: edad del 50% de madurez, amax longevidad, T: temperatura del ambiente.
Table 1. Applied method description and their coeffcients of variation (CV). M: natural mortality, l y k: growth parameters of the von Bertalanffy equation, a50%: age at
50% of maturity, amax: longevity, T: habitat temperature.

Mtodo Formulacin Coeficientes (CV) Referencia de CV

Alverson & Carney (1975) M = 3k(1 - ) / = 0,62(0,22) Cubillos (2003)


= 0,0066
= 0,2790(0,24)
Pauly (1980) log10=(M) = - - log10(l) + log10 (k) + log10 (T) Pauly (1980)
(T) = 0,6543(0,11)
= 0,4634(0,18)
= 1,1(0,22)
Frisk et al. (2001) M = exp( k + ) Quiroz et al. (2010)
= 0,8(0,62)
Jensen (1996) M = / a50% = 1,65(0,20) *
= 1,44(0,20)
Hoenig (1983) log (M) = - log amax *
= 0,982(0,20)
Mortalidad natural en congrio dorado, zona sur-austral de Chile

(*) CV = 0.2 fue considerado


Lat. Am. J. Aquat. Res. 320

sus respectivas matrices de correlacin fueron corresponden a la mnima y mxima reportada para la
obtenidas de Wiff et al. (2006). Luego, amax es zona sur-austral (Bustos et al., 2007).
estimada como la edad a la cual el 95% de l es La incorporacin del error de coeficiente en el
alcanzado. La longitud al 50% de madurez (l50%) fue mtodo de Pauly (1980) y el de Alverson & Carney
obtenida de Aguayo et al. (2001), quienes reportan (1975), fue realizada a travs de remuestreo de los
(l50% = 82,2 cm (IC95%=80,5-84,2) para hembras y coeficientes de regresin desde una distribucin
(l50% = 70,2 cm (IC95%=66,7-73,8) para machos, normal y con coeficientes de variacin (CV) acorde a
indistintamente de las zonas de pesca. Con estos la Tabla 1. Debido a la falta de informacin
parmetros, a50% fue calculada con los parmetros de relacionada con los estimadores de varianza del
crecimiento especficos para cada sexo y zona. mtodo de Jensen (1996) y el de Hoenig (1983), al
La incertidumbre fue incorporada siguiendo el igual que como lo consideraron Quiroz et al. (2010),
mtodo propuesto por Quiroz et al. (2010). De se asumi que los coeficientes de regresin fueron
acuerdo a estos autores, las estimaciones de M fueron normalmente distribuidos con un CV del 20%.
evaluadas incluyendo dos fuentes independientes de
incertidumbre:
RESULTADOS
(1) Los errores provenientes desde los parmetros
de historia de vida que son usados como valores de En trminos generales, las estimaciones promedio de
entrada en los modelos empricos (de aqu en adelante mortalidad natural (M) entregadas por los mtodos
error de rasgo); para ambas zonas y sexos fueron menores con el
(2) el error intrnseco provenientes desde los mtodo de Pauly (1980), ya sea incorporando
coeficientes que definen las ecuaciones empricas (de nicamente el error de rasgo o adicionando el error de
aqu en adelante error de coeficiente). La coeficiente (Tabla 2). Por el contrario, los mayores
incertidumbre fue incorporada a travs del mtodo niveles de M promedio se obtuvieron por el mtodo de
Monte Carlo, remuestreando 5000 veces los Frisk et al. (2001) y por el mtodo de Jensen (1996).
parmetros de crecimiento, longitud de madurez, Cuando se analiza M a travs de los mtodos,
temperatura promedio del ambiente y los coeficientes incorporando error de rasgo ms error de coeficiente,
de regresin de los mtodos descritos. la media para machos de la zona norte se encuentra
La incertidumbre de los parmetros de crecimiento entre 0,33 y 0,55 ao-1; mientras que para los machos
fue incorporada a travs del remuestreo desde una en la zona sur, la media tiene un rango entre 0,30 y
distribucin normal multivariada que utiliza la matriz 0,49 ao-1. En el caso de las hembras de la zona norte,
de covarianza descrita por los estimadores asintticos la media de M a travs de los mtodos se encuentra
de varianza y correlacin. Definiendo los parmetros entre 0,26 y 0,43 ao-1. En el caso de las hembras de la
de crecimiento como un vector u de longitud n, se zona sur, el rango promedio de M a travs de los
tiene que u = {l , k , a0 } , luego es posible obtener m mtodos result ligeramente inferior que el obtenido
para la zona norte, variando entre 0,24 y 0,38 ao-1.
vectores aleatorios u m* = X = [ x1 ,.., xm ]T desde la Las estimaciones de M promedio para ambos sexos
funcin de distribucin de densidad: incorporando ambas fuentes de error cubri entre 0,26
1 1
y 0,44 ao-1 para individuos de la zona norte y
f ( x1 ,.., xm ) = exp (X u )T 1 (X u ) , (1) medianamente menor, entre 0,23 y 0,34 ao-1, para
(2 ) n /2 2
1/2

individuos de la zona sur-austral. En trminos de


donde es la matriz de varianza-covarianza (n x n) de gnero, los machos presentan una M mayor que en
u, la cual rene las siguientes caractersticas: E(X) = u hembras para una misma zona, adems, es recurrente
tal que, E (X u )(X u )T = donde E es el operador para ambos sexos que en la zona sur se obtengan

menores valores de M (Figs. 2 y 3).
esperanza.
La incorporacin del error de coeficiente produce
Por otro lado, el parmetro a50% fue remuestreado un incremento en el CV de M hasta en ms de 100
desde una distribucin uniforme truncada acorde al veces, esto en comparacin con las estimaciones de M
intervalo del 95% de confianza de la longitud a la que nicamente incorporan error de rasgo. Sin
madurez. Un procedimiento similar fue implementado embargo, la sensibilidad de la incorporacin del error
para introducir la incertidumbre en la temperatura del de coeficiente vari a travs de los mtodos usados.
ambiente utilizada por el mtodo de Pauly (1980), Por ejemplo, para el mtodo de Jensen (1996) y el de
remuestreando desde una distribucin uniforme Pauly (1980), la incorporacin del error de coeficiente
truncada entre 8 y 11C. Estos valores de temperatura hace variar a los estimados de M entre 2 y 10 veces,
321 Mortalidad natural en congrio dorado, zona sur-austral de Chile

Tabla 2. Estimaciones de mortalidad natural en congrio dorado incorporando error de rasgo y error de coeficientes.
Table 2. Natural mortality estimates for pink cusk-eel incorporating trait-error and coefficient-error.

Zona Norte, Pesquera Demersal Sur-Austral


Sexo Error de Rasgo Error de rasgo + error de coeficiente
CV(%) Mediana Media CV(%) Mediana Media
Jensen (1996) Machos 7,04 0,37 0,37 20,90 0,37 0,37
Hembras 2,94 0,28 0,28 19,76 0,28 0,28
Ambos 3,34 0,26 0,26 20,10 0,26 0,26
Pauly (1980) Machos 4,27 0,31 0,31 38,03 0,31 0,33
Hembras 4,23 0,25 0,24 40,55 0,24 0,26
Ambas 4,25 0,25 0,25 40,54 0,25 0,27
Frisk et al. (2001) Machos 0,76 0,47 0,47 63,00 0,47 0,55
Hembras 0,89 0,35 0,35 65,78 0,35 0,43
Ambos 0,66 0,35 0,35 68,62 0,36 0,44
Alverson & Carney (1975) Machos 0,69 0,44 0,44 67,46 0,44 0,51
Hembras 0,81 0,34 0,34 66,39 0,34 0,39
Ambos 0,60 0,34 0,34 63,66 0,34 0,39
Hoenig (1983) Machos 0,65 0,38 0,38 62,28 0,39 0,45
Hembras 0,77 0,28 0,28 67,63 0,28 0,34
Ambos 0,57 0,29 0,29 68,34 0,30 0,35
Zona Sur, Pesquera Demersal Sur-Austral
Jensen (1996) Machos 8,20 0,42 0,42 21,57 0,42 0,42
Hembras 3,07 0,30 0,30 20,27 0,30 0,30
Ambos 3,28 0,29 0,29 20,20 0,29 0,29
Pauly (1980) Machos 4,33 0,28 0,28 39,33 0,27 0,30
Hembras 4,27 0,22 0,22 41,40 0,22 0,24
Ambas 4,27 0,21 0,21 41,68 0,21 0,23
Frisk et al. (2001) Machos 0,85 0,40 0,40 67,29 0,40 0,47
Hembras 0,60 0,31 0,31 69,54 0,31 0,38
Ambos 0,60 0,27 0,27 71,61 0,27 0,34
Alverson & Carney (1975) Machos 0,77 0,39 0,39 63,17 0,39 0,44
Hembras 0,54 0,30 0,30 62,43 0,30 0,35
Ambos 0,54 0,27 0,27 66,51 0,28 0,31
Hoenig (1983) Machos 0,75 0,35 0,35 65,24 0,35 0,42
Hembras 0,52 0,26 0,26 66,61 0,26 0,32
Ambos 0,53 0,24 0,24 72,35 0,24 0,29

mientras que para los restantes mtodos la DISCUSIN


incorporacin del error de coeficiente logra
incrementar los niveles de M entre 79 y 137 veces. Cada uno de los mtodos implementados entregan
Esto indica que, frente la incorporacin de ambas diferente estimaciones de media, mediana y CV. Estas
fuentes de incertidumbre, los intervalos de confianza diferencias son causadas en parte por los parmetros
de M para los mtodos de Frisk et al. (2001); Alverson de historia de vida requeridos para la implementacin
& Carney (1975) y Hoenig (1983) son mayores que de cada mtodo en especfico. Cuando solamente se
aquellos estimados con el mtodo de Jensen (1996) o introduce el error de rasgo, los mtodos que dependen
el de Pauly (1980) (Figs. 2 y 3). de parmetros anexos a los de crecimiento (Pauly,
Cuando se analizan ambas fuentes de 1980; Jensen, 1996), presentan mayor dispersin que
incertidumbre, para todos los mtodos, zonas y sexos, aquellos que dependen completamente del crecimiento
la media fue siempre mayor que la mediana. Esto (Hoenig, 1983; Alverson & Carney, 1975; Frisk et al.
indica que al incorporar error de coeficiente produce 2001). Esto se puede deber a que los parmetros de
una asimetra negativa (kurtosis) en la distribucin de crecimiento de la funcin de von Bertalanffy
M, posiblemente debido a la naturaleza log-normal de reportados por Wiff et al. (2007) presentan un
los coeficientes que definen los mtodos empricos. coeficiente de variacin muy bajo, que a su vez, es
Lat. Am. J. Aquat. Res. 322

Figura 2. Estimaciones de mortalidad natural por sexo en congrio dorado para la zona norte de la pesquera demersal sur-
austral, incorporando error de rasgo y error de coeficiente.
Figure 2. Natural mortality estimates by sexes for pink cusk-eel in the northern-austral zone incorporating trait-error and
coefficient-error.

Figura 3. Estimaciones de mortalidad natural por sexo en congrio dorado para la zona sur de la pesquera demersal sur-
austral, incorporando error de rasgo y error de coeficiente.
Figure 3. Natural mortality estimates by sexes for pink cusk-eel in the southern-austral zone incorporating trait-error and
coefficient-error.
323 Mortalidad natural en congrio dorado, zona sur-austral de Chile

transferido a las estimaciones de M. Por otra parte, la El mtodo de Pauly (1980) depende de dos
incorporacin del error de coeficiente incrementa de parmetros de historia de vida, cuatro coeficientes
forma importante el CV e introduce asimetra en la regresivos y la temperatura del ambiente, sin embargo,
distribucin de M, a travs de las zonas y entre sexos. a pesar del mayor nmero de parmetros y
Este incremento de CV es una consecuencia directa de coeficientes regresivos, este mtodo no entrega el
la incorporacin de una fuente adicional de mayor CV cuando ambas fuentes de error son
incertidumbre, mientras que la asimetra de la incluidas. En efecto, el mtodo de Pauly (1980)
distribucin posiblemente obedece a la estructura muestra el segundo CV ms pequeo despus del
multiplicativa en escala logartmica que es asumida en mtodo del Jensen (1996). Esta aparente contradiccin
los errores de los diferentes coeficientes que describen entre el nmero de parmetros y coeficiente del
los mtodos aplicados. modelo de Pauly (1980) y la magnitud del CV de M,
Debido a que es imposible conocer el valor fue explicado por Quiroz et al. (2010) y atribuido a la
verdadero de M, carece de sentido comparar los alta correlacin existente entre los parmetros de
mtodos en trminos de precisin, no obstante, es crecimiento. Bajo la metodologa propuesta en este
acertado comparar estos mtodos en trminos de la artculo para incorporar incertidumbre, cuando se
sensibilidad de M a los errores en los parmetros de remuestrean parmetros altamente correlacionados, el
historia de vida y en los coeficientes que describen los resultado es la obtencin de menor variacin como es
mtodos empricos. Adems, nuestros resultados M en el caso del modelo de Pauly (1980). Otra
indican que los mtodos utilizados para estimar M no particularidad del mtodo de Pauly (1980) es la
deberan ser comparados utilizando nicamente error incorporacin de la temperatura del hbitat, que en el
de rasgo, sin antes evaluar las consecuencias en las caso de la columna de agua y las profundidades donde
estimaciones de M debido a la incorporacin del error habita el congrio dorado, podran ser consideradas
en los coeficientes. En efecto, usar nicamente el error invariable. Esto es particularmente importante ya que
se conoce que esto puede ser un factor clave en la
de coeficiente puede ser difcil de interpretar cuando
determinacin de M (Brown et al., 2004).
se compara el mejor mtodo en trminos de CV,
debido a que stos son altamente sensibles al nmero La propuesta del mtodo emprico ms adecuado,
de coeficientes y a la forma funcional de sus errores. depende de la calidad de los parmetros que alimentan
De esta forma, la variabilidad en las estimaciones de los mtodos empricos y la naturaleza matemtica de
M est fuertemente asociada a la naturaleza estos. El mtodo de Jensen (1996) podra estar
paramtrica de los mtodos aplicados. Por ejemplo, sesgado para la determinacin de M, debido a que la
los mtodos de Jensen (1996) y Alverson & Carney edad de madurez proviene de la madurez a la longitud
(1975) dependen de un parmetro de historia de vida y reportada por Aguayo et al. (2001) en individuos de
un coeficiente de regresin. En trminos de historia de congrio dorado capturados en toda la extensin
vida, el mtodo de Jensen depende de a50%, mientras geogrfica de la zona sur-austral, sin hacer ningn tipo
que el mtodo de Alverson & Carney (1975) utiliza el de distincin geogrfica en trminos de stock como
parmetro de crecimiento k. Cuando ambos errores fue recomendado por Wiff et al. (2006). Por otro lado,
son incorporados, el mtodo de Jensen (1996) presenta el mtodo de Hoenig (1983) utiliza la longevidad
el menor CV. Debido a que los parmetros de mxima derivada de la talla asinttica, posiblemente
crecimiento y la edad de madurez presentan valores introduciendo un sesgo o un error adicional al
bajos de CV (Aguayo et al., 2001; Wiff et al., 2007), considerar una relacin funcional emprica entre la
los elevados niveles de CV para el mtodo de longevidad y la longitud asinttica. As mismo, el
Alverson & Carney (1975) en comparacin con el mtodo de Frisk et al. (2001) fue inicialmente
mtodo de Jensen (1996), se deben al error de propuesto para elasmobranquios. Sin embargo, Quiroz
coeficiente para cada uno de estos mtodos. Por otra et al. (2010) sealan que especies de elasmobranquios
parte, el mtodo de Hoenig (1983) y el mtodo de y peces telesteos comparten la misma dependencia de
Frisk et al. (2001) tambin dependen de un parmetro M con los parmetros de crecimiento, lo que posibilita
de historia de vida, pero stos requieren dos el empleo de mtodos empricos desarrollados para
coeficientes de regresin. Cuando ambas fuentes de peces telesteos en poblaciones de elamosbranquios y
error son consideradas, estos mtodos muestran viceversa. De todas formas, la no especificidad del
intervalos de confianza ms altos que los obtenidos mtodo de Frisk et al. (2001) exclusivamente para
por los restantes mtodos empricos. Esta es una telesteos podra causar que este mtodo muestre las
consecuencia derivada de la magnitud del error en los mayores estimaciones de M.
coeficientes regresivos de estos mtodos, que en Por ltimo, bajo los argumentos descritos en el
definitiva se propagan a la variabilidad de M. prrafo anterior, se recomienda considerar las
Lat. Am. J. Aquat. Res. 324

estimaciones del mtodo de Pauly (1980) como las mortalidad natural es claramente esencial y la
menos sesgadas para congrio dorado a travs de sexos incorporacin de las diferentes fuentes de
y zonas de pesca. En este contexto, las estimaciones incertidumbre en la evaluacin de stock es, por tanto,
del mtodo de Pauly (1980) que incorporan ambos altamente deseable. Las estimaciones de M y sus
errores (rasgos y coeficientes) sugieren emplear, ya intervalos de confianza, en el caso de congrio dorado,
sea en modelos poblacionales o anlisis de pueden ser incorporadas en los modelos de evaluacin
sobrevivencia, los siguientes valores de M: 0,33 ao-1 de stock y propagadas a las estrategias de manejo. Lo
(IC: 0,17-0,57) para machos zona norte, 0,30 ao-1 ms comn es el anlisis de sensibilidad, donde una
(IC: 0,15-0,52) para machos zona sur, 0,26 ao-1 (IC: evaluacin de stock es realizada repetidamente para
0,13-0,47) hembras zona norte y 0,24 ao-1 (IC: 0,12- varios valores de M obtenidos desde los intervalos de
0,43) hembras zona sur. Mientras que para sexos confianza (Quiroz et al., 2011). Una segunda va es
conjuntos se sugiere utilizar 0,27 ao-1 (IC: 0,13-0,47) utilizar una aproximacin bayesiana configurando una
para la zona norte y 0,23 ao-1 (IC: 0,11-0,40) para la distribucin emprica de M en base a sus intervalos de
confianza y utilizarla como distribuciones a priori
zona sur. Estas estimaciones son similares a las
(McAllister et al., 1994; Patterson, 1999). Finalmente,
reportadas para toda la zona sur-austral por medio de
la incertidumbre de M tambin puede ser incluida en
mtodos empricos, como aquellas estimadas por
modelos estado-espacio, donde el error en M puede ser
Aguayo et al., (1986) con valores de 0,35 ao-1 para incorporado como una de las componentes aleatorias
machos y 0,23 ao-1 para hembras, mientras que Ojeda (error de proceso) que regulan la estocasticidad en la
et al. (1986) calculan valores de 0,28 ao-1 y 0,25 dinmica poblacional (Millar & Meyer, 2000).
ao-1 para machos y hembras respectivamente.
Investigaciones recientes orientadas a explorar la Este estudio evidencia que los estimados de M para
una determinada zona son diferentes entre sexos,
estructura ecosistmica (Arancibia et al., 2003), como
como tambin para sexos conjuntos entre zonas de
tambin, el modelamiento multiespecie para la zona
pesca. Para una zona dada, los machos presentan
sur-austral (Arancibia et al., 2010), han empleado el
mayores estimados de M que las hembras. Cuando se
valor de M = 0,26 ao-1 utilizado en las ms recientes
compara entre zonas, los individuos de la zona norte
evaluaciones de stocks (Wiff & Quiroz, 2010), el que
presentan mayor mortalidad que los provenientes de la
ha sido adoptado de las estimaciones de Aguayo et al.
zona sur. Esto obedece a que los individuos de la zona
(1986) realizadas hace ms de una dcada. Por tanto,
norte para un sexo dado, son ms pequeos a una edad
es fehaciente que la actualizacin de los valores de M
especfica (Wiff et al., 2007), haciendo que k sea
en congrio dorado y su incertidumbre, ya sea por
mayor. A su vez k es directamente proporcional a M
gnero o rea de distribucin, viene a precisar los
(Charnov, 1993), causando que en la zona norte se
resultados de investigaciones que emplean este
obtengan mayores estimados de M que en la zona sur.
parmetro. Las notorias diferencias de las magnitudes de
La tarea de comparar los mtodos empricos, ya mortalidad natural por zona de pesca apoya la
sea por la naturaleza de sus coeficientes o la diferenciacin de stock sugerida por Wiff et al. (2005)
certidumbre en los parmetros de historia de vida, no y entregan elementos para profundizar en el concepto
solamente obedece a la seleccin de un mtodo de stock pesquero del congrio dorado en la zona sur-
consistente con los rasgos demogrficos y dinmica austral. En este contexto, el primer antecedente sobre
poblacional de congrio dorado, sino tambin, por a las la identificacin de unidades de stock en esta especie
consecuencias que conlleva una inadecuada fue realizado por Chong (1993) en base a un anlisis
especificacin de M en los modelos de evaluacin de morfomtrico de los otolitos. El resultado de este
stock. Ultang (1977) explor la sensibilidad de los anlisis mostr que an cuando las variables
resultados del anlisis de poblacin virtual (APV) a un morfomtricas presentan diferencias importantes entre
conjunto de escenarios de variabilidad de M. Los zona norte y sur, existe una importante sobreposicin
resultados fueron concluyentes en indicar que de los grupos etreos que impide considerarlos como
imprecisiones de M en torno a un 50% deben
unidades discretas. Sin embargo, este estudio no fue
ocasionar sesgos del orden de 20% en las estimaciones
concluyente respecto a la determinacin de una o ms
de la mortalidad por pesca. En este mismo sentido,
unidades de stock, sugiriendo la necesidad de
otras investigaciones han mostrado que la variabilidad
incorporar otras tcnicas ms precisas de anlisis.
temporal de M incrementa de forma importante la
variabilidad de los reclutamientos estimados en el El comportamiento de especies pertenecientes al
contexto de un modelo edad-estructurado (Lapointe et gnero Genypterus sugiere una tendencia a conformar
al., 1992; Aanes et al., 2007). En este sentido, evaluar mltiples poblaciones, las que pueden ser
el nivel de sensibilidad de las estimaciones de consideradas administrativamente unidades de stock
325 Mortalidad natural en congrio dorado, zona sur-austral de Chile

independientes. Esta independencia en los stocks ha Diagnstico de las principales pesqueras nacionales
sido confirmada en reas de pesca extranjeras demersales (peces) zona sur austral 1985. Estado de
comparativamente menores que la zona sur-austral. En situacin del recurso. Corporacin de Fomento de la
este contexto, Wiff et al. (2005) reunieron Produccin (AP 86/55). Instituto de Fomento
antecedentes biolgico-pesqueros, como crecimiento, Pesquero, Chile, 143 pp.
tallas medias, proporcin sexual, que avalan la Aguayo, M., I. Pay, R. Cspedes, H. Miranda, V.
existencia de caractersticas demogrficas diferentes Catasti, S. Lillo, P. Glvez, L. Adasme, F. Balbontn
para congrio dorado entre diferentes reas de la zona & R. Bravo. 2001. Dinmica reproductiva de merluza
sur-austral. Posteriormente, Wiff et al. (2007) del sur y congrio dorado. Proyecto FIP 99-15: 114 pp.
presentaron un anlisis detallado de los parmetros de Alverson, D.L. & M.J. Carney. 1975. A graphic review
crecimiento, indicando que existen diferencias of the growth and decay of population cohorts. J.
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En un trabajo ms reciente, Brito et al. (2008) Arancibia, H., S. Neira, V. Christensen, R. Olson, F.
efectuaron un anlisis por medio de redes neuronales y Arregun-Snchez, L. Cubillos, R. Quiones, C.
caracteres morfomtricos sugiriendo diferenciacin Gatica & M. Medina. 2003. Enfoque metodolgico
geogrfica dentro de la zona sur-austral. Estos autores para el anlisis ecosistmico en la administracin de
adems, sealaron que los resultados son concordantes pesqueras de la zona central de Chile. Proyecto FIP
con aquellos encontrados por Chong (1993). 2001-29: 278 pp.
Recientemente, Canales-Aguirre et al. (2010),
emplearon tcnicas de microsatelites para determinar Arancibia, H., S. Neira, M. Barros, C. Gatica, M.J.
la variabilidad gentica y estructura poblacional del Ziga, R. Alarcn & E. Acua. 2010. Formulacin e
congrio dorado en tres subzonas de la zona sur-austral implementacin de un enfoque multiespecfico de
de Chile. Los resultados indicaron que no existe evaluacin de stock en recursos demersales de la zona
diferenciacin gentica a nivel de poblacional para la sur austral. Fase I. Informe Final Proyecto FIP 2008-
23: 301 pp.
zona comprendida entre los 41 y 57S. Sin embargo,
el bajo contraste entre las muestras recopiladas en la Brown, J.H., J.F. Gillooly, A.P. Allen, V.M. Savage &
zona norte y sur, en concomitancia con el bajo poder G.B. West. 2004. Toward a metabolic theory of
estadstico de las pruebas empleadas, dejan ecology. Ecology, 85: 1771-1789.
importantes interrogantes sobre estos resultados y las Brito, C.G., V. Ojeda & L. Rodrguez. 2008. Anlisis
conclusiones sobre la existencia de ms de un stock de morfomtrico de otolitos de congrio dorado
congrio dorado para la zona sur-austral. El presente (Genypterus blacodes) como mecanismo de
trabajo complementa los vacos de conocimiento discriminacin de unidades poblacionales y
respecto a la historia de vida de congrio dorado, y de aplicacin de redes neuronales artificiales en
paso mejora la evaluacin de stock por zonas de estimacin de edad. En: J.C. Gutirrez & E. Yez
administracin en trminos de precisin y sesgo. (eds.). Nuevas aproximaciones metodolgicas para el
anlisis de pesqueras. Servicio de Publicaciones
AGRADECIMIENTOS Universidad de Huelva, Huelva, pp. 73-88.
Bustos, C., F. Balbontn & M. Landaeta. 2007. Spawning
Este trabajo fue financiado por el proyecto of the southern hake Merluccius australis (Pisces:
Investigacin del estatus y evaluacin de estrategias Merlucciidae) in Chilean fjords. Fish. Res., 83: 23-32.
de explotacin en congrio dorado 2011, realizado por
Canales-Aguirre, C.B., S. Ferrada, C.E. Hernndez & R.
el Instituto de Fomento Pesquero. Se desea agradecer
a dos revisores annimos cuyos comentarios Galleguillos. 2010. Population structure and
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Autofecundacin
Lat. Am. J. Aquat. Res., 39(2): 327-337, 2011 y malformacin larval en ostin Argopecten purpuratus 327
DOI: 10.3856/vol39-issue2-fulltext-14

Research Article

Asociacin entre la tasa de autofecundacin y la frecuencia de larvas


malformadas en poblaciones cultivadas del ostin del norte Argopecten
purpuratus (Lamarck, 1819)

Christopher Concha1, Emilio Figueroa1 & Federico M. Winkler1, 2


1
Departamento Biologa Marina, Facultad de Ciencias del Mar, Universidad Catlica del Norte
P.O. Box 117, Coquimbo, Chile
2
Centro de Estudios Avanzados en Zona ridas (CEAZA), Universidad Catlica del Norte
P.O. Box 117, Coquimbo, Chile

RESUMEN. El incremento de la frecuencia de malformaciones y la reduccin de la viabilidad y fecundidad


suelen ser las primeras manifestaciones de la depresin por consanguinidad en animales. El ostin del norte,
Argopecten purpuratus (Lamarck, 1819), es una especie hermafrodita funcional con autofecundacin parcial y
durante la reproduccin artificial puede presentar altos grados de autofecundacin. En este trabajo se analiz la
asociacin de la tasa de autofecundacin con la frecuencia de larvas malformadas y la supervivencia larval. Se
desovaron adultos maduros y se recogieron separadamente los gametos femeninos del 5 pulso de liberacin
en adelante y los masculinos. Los ovocitos fueron fecundados con espermatozoides de otro individuo,
formando familias de hermanos completos. La tasa de autofecundacin se verific por la proporcin de
ovocitos que entra en divisin en una muestra de ellos sin fecundar. La tasa de autofecundacin vari entre
familias de 0 a 100%, con distribucin de frecuencias normal. La proporcin de larvas malformadas se
distribuy al azar entre las familias analizadas, pero se correlacion negativamente, en forma moderada pero
significativa, con la tasa de autofecundacin y la temperatura media del cultivo. Los datos sugieren que la
autofecundacin en las familias de ostiones puede favorecer una mayor homeostasis del desarrollo larval.
Palabras clave: depresin por consanguinidad, pectnidos, hermafroditismo, homeostasis del desarrollo,
Argopecten purpuratus.

Association between self-fertilization rates and the frequency of malformed larvae in


farmed populations of the northern scallop Argopecten purpuratus (Lamarck, 1819)

ABSTRACT. Increased frequencies of malformations and the reduction of viability and fecundity are some of
the first manifestations of inbreeding depression in animals. The northern scallop, Argopecten purpuratus
(Lamarck, 1819), is a functional hermaphrodite species with partial self-fertilization. During artificial
reproduction, this species may present high degrees of self-fertilization. In this work, the association between
the selfing rate and the frequency of larval malformations and survival were analyzed. Mature adults were
spawned, and female and male gametes were collected separately from the fifth or later spawning pulses.
Oocytes were fertilized with sperm from another individual, forming families of complete siblings. Selfing
rates were verified by the proportion of cleaving oocytes in a non-fertilized sample. Self-fertilization ranged
from 0 to 100% among families, with a normal distribution. The proportion of malformed larvae was
distributed randomly among the families analyzed, but was negatively correlated moderately but
significantly with the selfing rate and the mean water temperature of the culture. These results suggest that
self-fertilization in scallop families can favor greater homeostasis of larval development.
Keywords: inbreeding depression, pectinids, hermaphroditism, developmental homeostasis, Argopecten
purpuratus.

___________________
Corresponding author: Federico Winkler (fwinkler@ucn.cl)
328 Lat. Am. J. Aquat. Res.

INTRODUCCIN ambiente controlado (Winkler & Estvez, 2003; Toro


et al., 2009). En A. purpuratus y otros bivalvos, como
La consanguinidad o endogamia es un factor relevante Pecten maximus, Placopecten magellanicus y
en el proceso de cambio de las frecuencias genotpicas Crassostrea gigas, el proceso de desove se inicia
en una poblacin. En muchas especies con cuando los ovocitos pasan de la profase I a la metafase
reproduccin cruzada causa prdida en el valor de I, seguido de la ruptura de la vescula germinal y su
parmetros vinculados con la adecuacin biolgica y liberacin al medio (Widoeati et al., 1995; Dsilets et
la produccin, conocida como depresin por al., 1995; Kyosuka et al., 1997; Martnez et al., 2000).
consanguinidad (Falconer & Mackay, 1996; Lynch & Cuando el ovocito se encuentra en metafase I puede
Walsh, 1998). Este fenmeno ha sido ampliamente ser fecundado por los espermatozoides y, en
informado para especies de plantas y animales pectnidos, al ser evacuados ambos tipos de gametos
(Charlesworth & Charlesworth, 1979, 1987; Lande & por una va comn, es posible la autofecundacin en el
Schemske, 1985, 1987; De Rose & Roff, 1999; tracto genital (Mackie, 1984; Widoeati et al., 1995).
Crnokrak & Roff, 1999; Lens et al., 2000; Wang et As, la autofecundacin durante el desove es
al., 2002), incluido diversas especies de moluscos, considerado un fenmeno comn en pectnidos
donde el incremento de la endogamia suele hermafroditas (Beaumont, 1986; Benninger & Le
manifestarse en una disminucin de las tasas de Pennec, 1991; Ibarra et al., 1995). En cultivos
crecimiento, mayor mortalidad o incremento de artificiales, donde los reproductores son confinados a
frecuencia de malformaciones, entre otros (Beaumont, pequeos volmenes de agua, se presume que la
1986; Evans et al., 2004; Deng et al., 2005; Ibarra et autofecundacin sera mayor que en la naturaleza,
al., 1995; Park et al., 2006; Martnez et al., 2007; pero no hay estimaciones de las tasa de
entre otros). autofecundacin en el medio natural.
La consanguinidad se produce por el cruzamiento El efecto del incremento en la consanguinidad
entre individuos que estn ms emparentados entre s derivado de la autofecundacin ha mostrado
que el promedio de la poblacin (Falconer & Mackay, resultados discrepantes entre estudios en pectnidos.
1996; Martnez & Figueras, 2007), y tiene su mxima Algunos autores han informado evidencias de
expresin en la autofecundacin. Esta es comn en depresin por consanguinidad, con supervivencias o
una gran variedad de plantas hermafroditas crecimientos menores en larvas producidas por
(Charlesworth & Charlesworth, 1979), donde, sin autofecundacin que los controles producidos por
embargo, se han descrito evidencias de adaptaciones fecundacin cruzada (Beaumont, 1986; Ibarra et al.,
que involucran sistemas que promueven la 1995; Martnez et al., 2007; Zheng et al., 2008; Toro
exofecundacin (Charlesworth & Charlesworth, et al., 2009, 2010). Otros, en cambio, no han
1987). En animales, y particularmente en moluscos, encontrado evidencias de ello (Betancourt et al., 1994;
existen diversas especies hermafroditas, como ostras Winkler & Estvez, 2003).
(Murakoshi & Hirata, 1993; Evans et al., 2004), El incremento de las malformaciones durante la
caracoles de tierra (Ruppert & Barnes, 1996), entre etapa de desarrollo es una de las primeras
otros. Sin embargo, muchas de esas especies tambin manifestaciones de la depresin por consaguinidad
exhiben mecanismos que previenen la autote- (Evans et al., 2004; Park et al., 2006). Esto se ha
cundacin, como la alternancia de sexos (Ruppert & observado en larvas de organismos marinos, como
Barnes, 1996; Calvo et al., 1998), mecanismos abalones (Deng et al., 2005; Park et al., 2006), ostras
eficientes de dispersin de gametos, sincronizacin de (Evans et al., 2004; Naciri-Graven et al., 2000) y
desoves e incompatibilidad gamtica, entre otros peces (Lu & Bernatchez, 1999; Wang et al., 2002),
(Knowlton & Jackson, 1993). entre otros. Tericamente, este fenmeno se asocia
En los moluscos pectnidos existe un gran nmero con prdida de homeostasis de desarrollo, es decir, la
de especies hermafroditas funcionales, cuyos capacidad para compensar eficientemente los efectos
miembros poseen una gnada dividida en una porcin adversos del ambiente para desarrollar en forma
masculina y otra femenina (Ruppert & Barnes, 1996; precisa el plan ontogentico contenido en el genoma
Calvo et al., 1998). En varios de ellos se ha informado de los individuos, en un ambiente determinado
la maduracin sincrnica de ambas porciones de la (Waddington, 1953, 1957; Dobzhansky & Wallace,
gnada y desoves simultneos (Guzmn et al., 1998). 1953; Dobzhansky, 1955; Thoday, 1958; Nijhout &
As, en el ostin del norte, Argopecten purpuratus Davidowitz, 2003). As, la mayor frecuencia de
(Lamarck, 1819), se han registrado tasas de malformaciones en una poblacin se vincula con
autofecundacin que varan entre 0 y 100%, con menores niveles de adecuacin biolgica (Evans et al.,
promedios en torno al 10 y 20%, durante desoves en 2004; Deng et al., 2005).
Autofecundacin y malformacin larval en ostin Argopecten purpuratus 329

La presencia de larvas malformadas durante la masculinos, se los retir del recipiente en que estaban,
reproduccin artificial de Argopecten purpuratus ha lavndolos cuidadosamente con agua filtrada y
sido descrita por Avendao et al. (2001), quienes esterilizada con UV, y se los coloc en un recipiente
consideran este factor como un problema en la con agua de mar fresca. Los primeros cinco pulsos de
produccin de semillas de esta especie. Hasta el emisin de ovocitos fueron descartados para prevenir
presente no existe un anlisis de la variacin en la tasa un exceso de autofecundacin. Para ello, luego de
de malformaciones entre poblaciones de ostiones ni emitir cada pulso de gametos, el reproductor fue
una explicacin sobre sus posibles causas. retirado del recipiente, lavado en la forma descrita
Considerando que las malformaciones son una previamente y colocado en un nuevo recipiente con
manifestacin frecuente de la depresin por agua fresca, segn el procedimiento descrito por
consanguinidad, y que durante la reproduccin Winkler & Estvez (2003).
artificial de esta especie se producen grados variables Previo a realizar la fecundacin cruzada, se separ
de autofecundacin, puede presumirse que ambos una muestra de 1 mL de agua desde el recipiente
fenmenos estn conectados. As, en este trabajo se conteniendo los ovocitos, la que se incub a
intenta verificar si la frecuencia de malformaciones en temperatura ambiente (aprox. 16C) por 4 h. Al cabo
las larvas es una consecuencia de la consanguinidad de este tiempo se observ bajo microscopio, para
derivada de la autofecundacin que se produce durante verificar la presencia de zigotos en divisin, productos
la reproduccin artificial. de autofecundacin (Winkler & Estvez, 2003) y se
obtuvieron tres fotos del desove de cada hembra con
MATERIALES Y MTODOS una cmara fotogrfica digital Canon Power Shot A
620 adosada a un microscopio. Se examinaron 70
Se obtuvieron al azar reproductores maduros de una ovocitos/cigotos por hembra desovada, y la tasa de
poblacin de ostiones de cultivo provenientes de autofecundacin se expres como el porcentaje de
captacin natural de baha Tongoy, los que fueron cigotos en divisin sobre el total de ovocitos
trasladados al Laboratorio Central de Cultivos de la analizados.
Universidad Catlica del Norte, Sede Coquimbo. Con El incremento en el coeficiente de consanguinidad
ellos se establecieron 91 familias, por fecundacin (F) para cada familia durante el proceso de
cruzada, y en cada una de ellas se estim la tasa de reproduccin artificial se estim como:
autofecundacin, frecuencia de malformaciones y F = (1 - C)/2
mortalidad. Los experimentos se realizaron entre el 3
donde C es la proporcin de individuos producidos
de julio del 2008 y 14 de enero del 2009.
por exofecundacin en la poblacin (Winkler &
Desove y obtencin de gametos Estvez, 2003). El incremento de consanguinidad
derivado del grado de parentesco entre los individuos
Adultos maduros fueron estimulados para inducir a que se cruzan se consider despreciable para los
desove utilizando la metodologa descrita por Di Salvo efectos de este experimento, dado que los
et al. (1984), recogiendo independientemente los reproductores se obtuvieron al azar de una poblacin
gametos masculinos y femeninos, cada uno de un silvestre (Tongoy) compuesta por ms de 60 millones
grupo diferente de ejemplares. Esta especie de individuos, de los cuales se estima que un 20%
normalmente libera sus gametos en pulsos, inicindose seran adultos (S. Cortez, com. pers.), y los cruces se
el desove con la evacuacin de espermatozoides, hicieron al azar. As, la consanguinidad derivada de
seguido, entre 10 y 20 min despus, por los ovocitos
este factor debera ser, en promedio, la misma que en
(Martnez et al., 2007). El cambio de sexo fue
la poblacin base.
monitoreado por observacin del color del rin. Este
es observable por delante del msculo aductor al La fecundacin se realiz usando una proporcin
separar las valvas del reproductor, y adquiere un color aproximada de 10 espermatozoides por ovocito. Cada
blanco lechoso durante la expulsin de los familia fue dispuesta en un estanque de 200 L
espermatozoides, cambiando a un color rojo independiente, con agua de mar filtrada a 1 y
anaranjado al iniciar la liberacin de ovocitos esterilizada con luz UV. El cultivo larval se realiz a
(Winkler & Estvez, 2003). Los espermatozoides se temperatura ambiente, con recambio completo de agua
recogieron en cubetas con agua filtrada a 1 y cada dos das y aeracin constante a partir de las 48 h.
esterilizada con luz UV, retirando los individuos del Se aliment a diario con 10 L de Isochrysis galbana
recipiente antes de iniciarse el cambio en el tipo de var. tahiti (2,5 x 104 cel mL-1) por estanque. La
gametos liberados. Para la recoleccin de ovocitos se densidad de larvas vari de ~12 larvas mL-1 al inicio
dej que los individuos concluyesen de emitir gametos del cultivo, a ~1 larva mL-1 al final de ste. La
330 Lat. Am. J. Aquat. Res.

temperatura del agua de los estanques fue registrada familias se analizaron con una prueba de Kolmogorov-
tres veces al da (maana, medioda y tarde) con un Smirnov. La proporcin promedio de larvas
termmetro (0,1C). malformadas al inicio y a mediados del cultivo fueron
Durante el cambio de agua las larvas se retuvieron analizadas utilizando una prueba t-Student, para
en un tamiz de 45 m, y de l se colectaron muestras verificar si exista diferencia entre ellos.
de larvas siguiendo la metodologa descrita por Di
Salvo et al. (1984), las que fueron almacenadas en RESULTADOS
tubos Eppendorf de 1,5 mL con formalina al 5% hasta
su anlisis. La supervivencia y la frecuencia de larvas De las 91 familias formadas en siete eventos de
malformadas por familia se evalu al segundo da reproduccin (Tabla 1), slo 20 de ellas (22%)
post-fecundacin, a la mitad y al final del perodo de alcanzaron el estadio de pediveliger, etapa en que se
cultivo. Para compensar eventuales variaciones en las inicia el proceso de fijacin, la cual se alcanz en 20 a
tasas de desarrollo causadas por diferencias en la
22 das de cultivo, dependiendo de la temperatura de
temperatura de cultivo (Ruiz et al., 2008), la segunda
cultivo. Sesenta y dos familias (68%) sobrevivieron
medicin se hizo cuando las larvas alcanzaron las
hasta la etapa media del desarrollo larval. La
251,7 Unidades Trmicas Acumuladas (UTA)
proporcin de larvas vivas promedio por familia
(Brenko & Calabrese, 1969; Uki & Kikuchi, 1984;
Prez, 2002; Gallegos, 2003; Gonzlez, 2003). La mostr una marcada cada a lo largo del cultivo, con
mortalidad se estim por la diferencia en la cantidad una reduccin de aproximadamente el 80% entre la
de larvas entre periodos sucesivos de medicin. Para primera y segunda medicin, y slo el 5% de las
ello se cont bajo lupa el nmero de larvas vivas en larvas de cada familia sobrevivi hasta el final del
una alcuota de 1 mL de la muestra obtenida del tamiz, cultivo (Fig. 1).
y se extrapol al volumen total del estanque. El alto de La tasa de autofecundacin vari de 0% a 100%
las larvas se midi a partir de imgenes digitales entre las familias, con un promedio general de 43%, y
obtenidas con un microscopio de transmisin dotado distribucin normal (P > 0,05). El 19% de las familias
con cmara fotogrfica, y usando el programa Image- no present autofecundacin (F = 0) pero en un 17%
Pro Plus 4.0, calibrado para que las medidas fuesen de ellas todas los cigotos producidos provienen de
registradas en micrmetros. autofecundacin (F = 50%) (Fig. 2). As, el
La presencia de malformaciones se verific incremento de la consanguinidad promedio estimado
mediante observacin bajo microscopio y registro durante el proceso artificial de reproduccin fue de
microfotogrfico de 50 larvas tomadas al azar por 21,5%. La longitud de las larvas al inicio del cultivo
familia, para cada etapa del cultivo definida vari entre 92 y 102 m, con un promedio de 98 3
previamente. Como criterios para definir la m, alcanzando 207 9 m a la edad de fijacin (Fig.
manifestacin de alteraciones en el desarrollo se 3), con una tasa de crecimiento de 4,1 m da-1.
usaron las descripciones de la morfologa normal de
A las 48 h post-desove todas las larvas se
las larvas de A. purpuratus de Bellolio et al. (1994) y
encontraron en estadio de veliger, con una concha de
de las deformaciones informadas por Avendao et al.
(2001). forma semicircular con bordes regulares (Fig. 4a). A
mediados del cultivo esta forma se ha modificado
Anlisis de los datos levemente para adoptar la tpica forma de larva D (Fig.
La asociacin de la frecuencia de larvas malformadas 4c). En algunas larvas se observ una hendidura muy
por familia con el porcentaje de autofecundacin o la marcada en el contorno de la concha, caracterstica
temperatura promedio del agua del cultivo, y la que se registr tanto a inicios (Fig. 4b) como a
relacin entre el porcentaje de autofecundacin y la mediados del cultivo (Fig. 4d). La proporcin de
mortalidad larval en cultivo, se examinaron mediante larvas con esta malformacin vari entre las familias
anlisis de regresin simple (Yi = + Xi). La de 0 a 12% al inicio, y de 0 a 10% mediados del
significancia de los coeficientes de regresin fue cultivo, con promedios de 4 y 3%, respectivamente (P
verificada mediante una prueba t-Student (Sokal & > 0,05). En la ltima medicin todas las larvas
Rolf, 1981). observadas se encontraron en estadio de pedivelger,
La distribucin de frecuencias de larvas con conchas de forma semicircular (Fig. 4e), y no se
malformadas entre familia se compar con una observaron individuos con morfologas alteradas. La
distribucin de Poisson, usando la prueba de Chi- distribucin de frecuencias de larvas malformadas
cuadrado para bondad de ajuste como prueba de entre las familias fue al azar, tanto al inicio como a
hiptesis. Los porcentajes de autofecundacin para las mediados del cultivo (P > 0,05; Fig. 5).
Autofecundacin y malformacin larval en ostin Argopecten purpuratus 331

Tabla 1. Temperatura promedio del agua ( DE) en estanques de cultivo de larvas de Argopecten purpuratus en tres
etapas del cultivo, para siete eventos de reproduccin.
Table 1. Mean water temperature in culturing tanks ( SD) with Argopecten purpuratus larvae at three moments of the
larval life span in seven culture batch.

Temperatura del cultivo (C)


Desove Fecha
Inicio Mediados Final Promedio
1 03/11/2008 17 ( 1,0) 17 ( 0,7) 17 ( 0,8)
2 14/11/2008 17 ( 0,6) 17 ( 0,6)
3 25/11/2008 17 ( 0,7) 18 ( 0,7) 18 ( 0,7)
4 09/12/2008 19 ( 1,0) 20 ( 0,6) 20 ( 0,6) 20 ( 0,7)
5 06/01/2009 19 ( 0,6) 19 ( 0,7) 19 ( 0,6) 19 ( 0,6)
6 07/01/2009 18 ( 0,6) 19 ( 0,8) 19 ( 0,7) 19 ( 0,7)
7 14/01/2009 19 ( 0,6) 19 ( 0,6) 19 ( 0,6)
Promedio 18 ( 0,7) 19 ( 0,1) 19 ( 0,6) 18,7 ( 0,5)

Figura 1. Supervivencia relativa promedio de larvas de Figura 3. Variacin en la longitud promedio de larvas de
A. purpuratus en tres momentos del periodo de cultivo. A. purpuratus a lo largo del perodo de cultivo.
Figure 1. Average relative survivorship of A. purpuratus Figure 3. Variation in the mean shell length of A.
larvae at three moments of the larval culturing period. purpuratus larvae along of the larval cultivation period.

edades (r = 0,426 y 0,359, respectivamente; P < 0,05).


Por su parte, la temperatura media del agua del cultivo
no se asoci significativamente con la frecuencia de
larvas con alteraciones morfolgicas a las 48 h post-
fecundacin (P > 0,05), pero si se observ una
moderada pero significativa asociacin negativa (P <
0,05) entre dichas variables en la medicin realizada a
mediados del cultivo (Fig. 7). En cambio, las tasas de
Figura 2. Incremento de la consanguinidad (F), autofecundacin ni la temperatura media del agua se
estimado por la proporcin de cigotos autofecundados, asociaron con la mortalidad larval (P > 0,05).
en 91 familias de A. purpuratus.
Figure 2. Increment of the inbreeding (F) estimated DISCUSIN
trough the selfing rate, in 91 families of A. purpuratus.
La presencia de una hendidura muy marcada en el
contorno de la concha de las larvas a las 48 h post-
Las familias con tasas ms altas de fecundacin es similar a las alteraciones descritas por
autofecundacin tendieron a tener menor proporcin Avendao et al. (2001). Estas alteraciones persisten al
de larvas malformadas que aquellas con menor menos hasta mediados del periodo de desarrollo
autofecundacin, tanto en las evaluaciones realizadas larval, sugiriendo que ellas no seran letales en esta
a inicios como a mediados del cultivo (Fig. 6), etapa o que pueden generarse durante el crecimiento
aprecindose una moderada pero significativa de las larvas velger. Su ausencia al final del cultivo,
correlacin negativa entre ambas variables en las dos no obstante, parece indicar que estas alteraciones en la
332 Lat. Am. J. Aquat. Res.

Figura 4. Larvas de A. purpuratus. a las 48 h post-


fecundacin: a) normal, b) malformada; a las 251,7
U.T.A. de cultivo: c) normal, d) malformada; e) al final
del cultivo.
Figure 4. Larvae of A. purpuratus: after 48 h Figura 5. Distribucin de frecuencia de familias con
fertilization: a) normal, b) malformed; after 251.7 U.T.A. diferentes nmero de larvas malformadas por muestra: a)
of cultivation; c) normal, d) malformed; e) at the end of al inicio, b) a mediados del periodo de cultivo (251,7
the cultivation period. 8,9 U.T.A.). (N = 50 larvas por familia).
Figure 5. Frequency distribution of families with
different number of malformed larvae per sample: a) at
concha pueden asociarse con mortalidad selectiva the beginning, b) at the middle of the cultivation period
como proponen Avendao et al. (2001). No obstante, (251.7 8.9 U.T.A). (N = 50 larvae for family).
por su baja frecuencia en los cultivos, menor al 12%,
este no parece ser un factor relevante en el xito de la
produccin de juveniles de ostin del norte en 1981; Di Salvo et al., 1984; He et al., 1999), y se
sistemas controlados. puede presumir que al abreviarse ciertas etapas crticas
Las malformaciones morfolgicas se asocian con de la ontogenia se reduce la probabilidad de accidentes
alteraciones aleatorias en el patrn de desarrollo causantes de malformaciones en los procesos de
ontogentico de los organismos (Waddington, 1957), morfognesis. No obstante, como se ha observado en
las que se suponen no heredables y distribuidas al azar Ciona savignyi, temperaturas superiores al ptimo
en la poblacin, fenmeno denominado inestabilidad para el desarrollo embrionario de la especie podran
del desarrollo (ID; Palmer, 1994). Factores favorecer el incremento de la ID (Nomaguchi et al.,
ambientales pueden incidir en la frecuencia y 1997).
magnitud de la ID en las poblaciones (Markow, 1995; La frecuencia de larvas malformadas en A.
Dethlefsen et al., 1996; Jezierska et al., 2000) y la purpuratus se distribuy al azar entre familias, y se
temperatura ha sido descrita como uno de ellos en correlacion negativamente con la tasa de
distintos organismos (Zimmerman & Pechenik, 1991; autofecundacin. Este resultado contradice los
Nomaguchi et al., 1997; Hallare et al., 2005). resultados de estudios previos sobre el efecto de la
Nuestros resultados muestran que el incremento de consanguinidad en especies con reproduccin cruzada,
temperatura, dentro de los rangos estudiados, tendera en las que el incremento en la ID en las progenies
a favorecer una mayor estabilidad de desarrollo en A. suele ser una de las primeras manifestaciones de la
purpuratus. Temperaturas ms altas aumentan las depresin por consanguinidad (Smouse, 1986; Deng et
tasas de desarrollo en moluscos (Barra et al., 2005), y al., 2005; Park et al., 2006). No obstante, en
en particular en pectnidos (Tettelbach & Rhodes, cruzamientos entre especies o poblaciones conespe-
Autofecundacin y malformacin larval en ostin Argopecten purpuratus 333

Figura 7. Asociacin entre la temperatura promedio del


agua de cultivo y la frecuencia de larvas malformadas en
91 familias de A. purpuratus a mediados del periodo de
cultivo.
Figure 7. Association between the average water
temperature and the frequency of malformed larvae in 91
A. purpuratus families at the middle of the cultivation
period.
Figura 6. Asociacin entre el porcentaje de
autofecundacin y frecuencia de larvas malformadas en 1984; Avendao et al., 2001; Winkler & Estvez,
91 familias de A. purpuratus. a) al inicio, b) mediados 2003; Martnez et al., 2007). Durante el desarrollo
(251,7 8,9 U.T.A.) del periodo de cultivo. ontogentico de A. purpuratus, la proporcin de
Figure 6. Association between the self-fertilization individuos generados por autofecundacin dentro de
proportion and the frequency of malformed larvae in 91 familias se reduce significativamente (Toro et al.,
families of A. purpuratus. a) at the beginning, b) the 2009, 2010), as como la homocigosis en loci
middle (251.7 8.9 U.T.A.) of the cultivation period. aloenzimticos (Winkler et al., 2009), indicando la
ocurrencia de fuertes efectos selectivos contra los
cficas genticamente divergentes (subespecies, razas ejemplares con ms alta consanguinidad dentro de la
geogrficas, etc.) tambin se ha observado incremento poblacin. No obstante, si dentro de una poblacin
en las tasas de malformaciones, fenmeno conocido diferentes genotipos multiloci producen fenotipos
como depresin por exogamia (Alibert & Auffray, similarmente adaptados, mientras que otras
2003). En ambos casos el fenmeno se asocia a una combinaciones genotpicas tienen menor adecuacin
reduccin de la homeostasis del desarrollo (HD) de las biolgica relativa, en un escenario de intensa seleccin
progenies respecto de sus parentales, es decir, de natural sobrevivirn y se reproducirn preferentemente
capacidad del genoma para compensar alteraciones los individuos con genotipos que otorguen los mejores
causadas por el ambiente en el plan de desarrollo niveles de coadaptacin genmica, y las progenies
ontogentico contenido en los genes de un organismo producidas por autofecundacin tendrn una mejor
(Wadington, 1957). La base gentica de la prdida de oportunidad de reunir combinaciones allicas
HD se ha vinculado con menores niveles de ventajosas que aquellas producidas por reproduccin
coadaptacin genmica, es decir, de la capacidad del cruzada al azar. La tendencia hacia menores tasas de
genoma de los individuos para actuar malformaciones en larvas de familias con mayores
coordinadamente para producir el fenotipo normal. En niveles de autofecundacin se podra asociar al efecto
el caso de la consanguinidad se atribuye al incremento de la seleccin natural en la generacin parental y la
de la homocigosis y una mayor probabilidad de probabilidad que se reproduzcan en las progenies
expresin de alelos recesivos deletreos al estado algunos de estos genotipos particularmente ventajosos.
homocigoto (Woolf & Markow, 2003). En los cruces La consanguinidad produce desequilibrios de fase
exogmicos, en cambio, se producira por la gamtica entre loci no ligados fsicamente y favorece
incompatibilidad entre ambos genomas parentales para la conformacin de complejos genticos particu-
controlar eficientemente los procesos de morfognesis larmente coadaptados (Endler, 1977, Templeton,
individual (Alibert & Auffray, 2003). 1986), lo que puede contribuir a acentuar este
A. purpuratus es una especie con alta fecundidad, fenmeno.
pero slo una proporcin muy baja de los cigotos Los niveles de autofecundacin observados en este
producidos completa su desarrollo larval, y an menos trabajo variaron ampliamente entre individuos y, en
sobreviven hasta la edad reproductiva (Di Salvo et al., promedio, superan lo informado previamente para esta
334 Lat. Am. J. Aquat. Res.

especie utilizando la misma metodologa de desove y consanguinidad en una especie es particularmente


cuantificacin (Winkler & Estvez, 2003; Toro et al., significativa. Lo que destaca este trabajo, sin embargo,
2009, 2010). En la reproduccin artificial de esta es que en una especie con autofecundacin parcial, los
especie con fines comerciales se suelen recoger efectos negativos de la consanguinidad en algunos
separadamente los gametos de ambos sexos y la rasgos, podran ser balanceados por efectos positivos
fecundacin se realiza usando pools de gametos de en otros.
varios reproductores (Bellolio et al., 1994), o bien se
usan cruces masivos en que un gran nmero de
AGRADECIMIENTOS
reproductores desovan en un estanque y la
fecundacin ocurre espontneamente. En ambos casos,
Los autores agradecen a quienes brindaron su apoyo
los primeros pulsos de liberacin de ovocitos, en los
tcnico en el trabajo, Johanna Tamayo, Janette Aliaga
que la autofecundacin es mayor (Winkler & Estvez,
y Miguel Rivera; a William Faras, Manuel Carmona y
2003), no se descartan. As, es esperable que los
Ricardo Garca por su apoyo en las labores de cultivo
niveles de autofecundacin durante la reproduccin
larval; al Prof. Hctor Flores por las fructferas
artificial de la especie, y por lo tanto de
discusiones y al Biol. Sergio Cortez (SERNAPESCA)
consanguinidad, sean mayores an que los estimados
por la informacin sobre el banco de Tongoy. Trabajo
en este trabajo. En la naturaleza, en cambio, se
parcialmente financiado por el Proyecto INNOVA
presume que las tasas de autofecundacin seran ms
05CR11PPT-18.
bajas que en cultivo (Martnez et al., 2000). Coherente
con este supuesto, los estudios de gentica poblacional
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Received: 27 September 2010; Accepted: 24 May 2011


Lat. Am. J. Aquat. Res., 39(2): 338-343, 2011 Lat. Am. J. Aquat. Res. 338
DOI: 10.3856/vol39-issue2-fulltext-15

Research Article

Use of antioxidants on rainbow trout Oncorhynchus mykiss (Walbaum, 1792)


sperm diluent: effects on motility and fertilizing capability

Andrea Ubilla1 & Ivn Valdebenito1


1
Universidad Catlica de Temuco, Facultad de Recursos Naturales
Escuela de Acuicultura. P.O. Box 15-D, Temuco, Chile

ABSTRACT. The present investigation determined how different antioxidants incorporated into the sperm
diluent for cold storage of semen affected sperm motility and spermatozoan fertility capabilities of the rainbow
trout. For the evaluations, fresh semen (C) and semen that had been stored without diluents (T1) were used as
control groups. The diluents were prepared using a base of UCT diluents (T2), adding grape polyphenol (0.1 g
100 mL-1) (T3), trolox C (0.1 g 100 mL-1) (T4), polyphenol (0.1 g 100 mL-1) plus trolox (0.1 g 100 mL-1) (T5),
and vitamin C (0.018 g 100 mL-1) (T6). The incorporation of antioxidants into sperm diluents prolongs
motility and fertility of rainbow trout semen. The results show that by day two, all of the treatments showed
level 5 sperm motility. After seven days of storage, only T3 and T6 dropped to level 4 sperm motility. The
duration of flagellate activity on this day was maximal for T3 with 36.87 0.51 s and minimal for T6 with
29.78 0.52 s. On day seven, fertility was maintained with no statistically significant differences between the
control and T2 (92.80 0.62%), T3 (83.66 2.52%), T4 (90.46 1.60%), T5 (83.57 2.75%), and T6 (83.57
2.30%). By days 10 and 17 of storage, the fertility of T1 was zero and that of T2 was significantly lower
than the control group. On day 17, the highest percentage of fertilization was 97.38 1.85% for T5 and the
lowest value was 64.69 3.76% for T2. The results allow concluding that the sperm viability of semen stored
with different antioxidants is significantly prolonged.
Keywords: Oncorhynchus mykiss, polyphenol, trolox C, vitamin C, fertilizing capability, sperm motility.

Uso de antioxidantes en el diluyente espermtico para trucha arcoiris Oncorhynchus


mykiss (Walbaum, 1792): efecto en la motilidad y capacidad fecundante

RESUMEN. En la presente investigacin se determin el efecto en la motilidad espermtica y la fertilidad del


espermatozoide de trucha arcoiris, de diferentes antioxidantes incorporados en el diluyente espermtico para el
almacenamiento en fro de semen. Para las evaluaciones se utiliz como control semen fresco (C) y semen
almacenado sin diluir (T1), los diluyentes fueron preparados utilizando como base el diluyente UCT (T2) al
que se le incorpor polifenol de uva (0,1 g 100 mL-1) (T3), trolox C (0,1 g 100 mL-1) (T4), polifenol ms
trolox (0,1 g 100 mL-1 + 0,1 g 100 mL-1), respectivamente (T5) y vitamina C (0,018 g 100 mL-1) (T6). La
incorporacin de antioxidantes en los diluyentes espermticos, prolongan la motilidad y fertilidad del semen
de trucha arcoiris. Los resultados muestran que al da dos todos los tratamientos presentaban un nivel 5 de
motilidad. Despus de 7 das de almacenamiento, slo T3 y T6 bajaron a un nivel 4 de motilidad. La duracin
de la actividad flagelar en este da fue mxima en T3 con 36,87 0,51 s y mnima en T6 con 29,78 0,52 s.
Al da 7 la fertilidad se mantuvo sin diferencias estadsticamente significativas con el control en T2 (92,80
0,62%), T3 (83,66 2,52%), T4 (90,46 1,60%), T5 (83,57 2,75%) y T6 (83,57 2,30%). Los das 10 y 17
de almacenamiento, la fertilidad de T1 fue cero y la de T2 fue significativamente menor al control. Al da 17 el
mayor porcentaje de fecundacin fue de 97,38 1,85% para T5 y el menor valor fue de 64,69 3,76% para
T2. Los resultados permiten concluir que el semen almacenado con distintos antioxidantes prolonga
significativamente la viabilidad espermtica.
Palabras clave: Oncorhynchus mykiss, polifenol, trolox C, vitamina C, capacidad fecundante, motilidad
espermtica.
___________________
Corresponding author: Andrea Ubilla (cubilla@uct.cl)
339 Use of antioxidants in rainbow trout Oncorhynchus mykiss sperm diluents

INTRODUCTION results have been obtained (Ball et al., 2001a), since


the enzymes present in seminal plasma are not always
Sperm extender diluents improve motility and efficient enough to reduce the effects of ORSs
fertilization percentages of cold stored semen (Stoss, (Lamirande et al., 1997; Peeker et al., 1997).
1983; McNiven et al., 1993; Billard, 1990; Snchez & The objective of this present investigation was to
Rubilar, 2001; Valdebenito et al., 2009). These evaluate the effects of the incorporation of three
solutions prevent the oxidization of the plasmatic and antioxidants applied to semen of rainbow trout
mitochondrial membrane, delivering energetic (Oncorhynchus mykiss) during cold storage for 17
substrates and allowing the maintenance of sperma- days.
tozoa at stable pH and osmolarity conditions of the
extracellular mediums (Morisawa & Susuki, 1980;
MATERIALS AND METHODS
Morisawa et al., 1983; Batellier et al., 2001). Gametes
are aerobic cells where oxygen plays an essential role
Gamete recollection and semen storage
for their performance. Oxygen free radicals are
continuously generated in the different metabolic To simulate the conditions of the fish farms, a pool
pathways, and are capable of interacting with different of semen was uses (1 mL per male and six ml total)
biomolecules, causing cell damage. Oxidative stress is with maximum motility was obtained from six adult
a consequence of the unbalance produced between the male rainbow trouts (Oncorhynchus mykiss) that were
production of free radicals and the anti oxidizing at their second spawning from the Quetro S.A. fish
capabilities of an organism, where this can become farm (332332S, 714047W) in the south of
very harmful if there is a high production of oxygen Chile. The semen samples were obtained by
reactive species (ORS) (Saleh et al., 2002; Membrillo abdominal massage, avoiding contamination with
et al., 2003). feces and urine. An initial motility evaluation was
In mammals, sperm motility can become seriously carried out at the same center, according to the
affected by ORSs. At a molecular level they can Snchez-Rodrguez & Billard (1977) scale, that
obstruct the phosphorylation of proteins, preventing considers zero as the minimum and five as the
sperm movement (De Lamirande et al., 1998). maximum score. The selected samples (all with level
Reactive species also exist, that are produced naturally 5) were taken to the Reproduction Laboratory of the
by the cell, these are in low concentrations intervening Universidad Catlica de Temuco (UCT) in sterilized
in processes like capacitation, acrosomic reaction and containers with oxygen, at 4C and in the absence of
the union of the spermatozoa to the pellucid zone light.
(Sharman & Agarwal, 1996; De Lamirande et al.,
1997, 1998; Aitken et al., 2004; Allamaneni et al., Sperm density
2004). Sperm density of the semen (N of spermatozoa/mL),
Antioxidants are molecules that prevent the was determined in four aliquots, by a counting
uncontrolled production of free radical or inhibit their Neubauer chamber using the methodology described
reactions with biological structures (Halliwell & by Oppenheim (1973) for blood cells.
Chirico, 1993). In seminal plasma and in spermatozoa
of teleostei fish there are different types of Sperm count
antioxidants (Liu et al., 1995; Ciereszko et al., 2000; Sperm count was determined in five samples. Semen
Lahnsteiner et al., 2010a), which are important for the was put into five microhematocrit. Then, these were
in vivo maintenance of sperm viability, and that could centrifuged at 10.000 rpm for a 10 min period. Later,
have relevance for the practice of supplementation of by means of a table, the percentage of spermatozoa
the semen storage and cryopre-servation mediums to was determined from the semen samples.
improve the quality of the spermatozoa. Ascorbic acid
(Ciereszko & Dabrowski, 1995; Metwally & Fouad, Sperm diluents
2009) and Uric acid (Ciereszko et al., 1999) are To evaluate the effectiveness of the antioxidants
considered important antioxidants in teleostei semen. polyphenol, trolox C and vitamin C, one part of the
In rainbow trout and carp semen, methionine sulfoxide pool semen was diluted into two parts of diluent (1:2)
reductase and methionine can have antioxidant according to the following treatment group: fresh
functions (Lahnsteiner, 2009). semen control (C) of different male; undiluted stored
Experimentally, to reduce the levels of ORS in semen (T1); semen diluted with UCT medium (UCT
mammals, ascorbic acid and/or catalase have been with KCl to inhibit motility) (T2); T2 + polyphenol
added to sperm extender diluents, where satisfactory (0.1 g 100 mL-1l) (T3); T2 + trolox C (0.1 g 100 mL-1)
Lat. Am. J. Aquat. Res. 340

(T4); T2 + polyphenol (0.1 g 100 mL-1) + trolox C Statistical analysis


(0.1 g 100 mL-1) T5; T2 + vitamin C (0.018 g 100 To establish the level of motility of the semen, the
mL-1) (T6). Osmolarity was determined same day mode of each treatment was used. For the rest of the
using a Micro-Sample Osmometer model Fiske 210 parameters, the average values and standard deviations
and the pH values were measured with a digital were used. Using the statistical software GaphPad
pHmeter model pH 21 and the value that were Prism 5, an ANOVA and Kruskall-Wallis tests were
obtained are indicated in Table 1. applied to identify the existence of statistically
Evaluation of the level and duration of sperm significant differences between the group (P 0.05).
motility of rainbow trout semen with different
sperm diluents RESULTS
Once at the reproduction laboratory, the semen
samples were diluted at a 1:2 ratio with the applied Sperm motility and sperm count
diluents and maintained at 4C in an incubation
The sperm density obtained from the pool of semen
chamber, with permanent agitation and in the absence
of light. was of 16 2,3 x 109 spermatozoa/mL and the average
percentage of the sperm count obtained during the
For sperm activation, an activating solution with
experiment was of 33,2 1,1%. The mode that was
280 mOsmol kg-1 osmolarity and 9.0 pH level,
prepared with NaCl 9% was used. The evaluations registered for motility on day 2 in all of the treatment
were carried out in the reproduction laboratory of the group was level 5. On day 7; T3 and T6 had lowered
UCT at room temperatures (10C), where flagellate to level 4. By day 9; T1 and T2 had level 0 and on day
activity of the spermatozoa was observed through a 17; T3, T4, T5 and T6 maintained level 3 (Fig. 1).
Nikon Eclipse E400 microscope; at 10x to determine The duration of motility observed on day 2 (Fig. 2)
the level of motility, and at 40x to determine the was of 37.07 0.24 s, for T4 and the minimum value
duration (in seconds) of this flagellate activity, of 34.04 0.35 s for T5. On day 17 T1 and T2 did not
considering the moment the spermatozoa initiate present flagellate activity, the highest value was of
linear movement and ending when they begin local
7.08 1.02 s for T5 and the lowest was of 2.34
rotation movements. The evaluation was carried out in
20 aliquots for each treatment. These evaluations were 0.48 s for T3. The differences that were observed
carried out on days 2, 4, 7, 9, 11, 14 and 17 of storage. between both treatment group were statistically
significant.
Fertilizing capabilities
The evaluation of the fertilizing capability was done Fertilizing capabilities
after 7, 10 and 17 days of storage, on a pool of The sperm density that was used for fertilization was
recently extracted fish eggs, from six females during of 1.600.000 spermatozoa/oocyte in all of the
their second spawning, raised at the same fish farm. treatment group. The average fertilization percentages
The eggs were deposited into plastic containers (five on day 7 were 83.15 6.10% for C and 66.42 4.06%
replicas per treatment) with approximately 100 eggs
for T1 (Fig. 3). Treatments T2, T3, T4, T5 and T6 did
each. Coelomic fluid was extracted and fertilization
was carried out by adding 10 L of semen from the not present statistically significant differences. On day
control (C) and T1 group. For diluted semen of group 10, T1 presented 0% of fertilization and T2 presented
T2, T3, T4, T5 and T6, 20 L were used for each 68.02 1.40%. T3, T4, T5 and T6 did not present
replica. statistically significant differences. By day 17, T1 did
Five minutes after fertilization, river water was not present fertilization, and T2 presented 64.69
added to the gametes and semen residues were 3.76%. T3, T4, T5 and T6 did not present statistically
cleaned. Then, hydration of the eggs was carried out significant differences in their fertilizing capability
for 30 min followed by the introduction of the eggs (Fig 3).
into enumerated micro-incubaters and into containers
with an open flow system at 9C, according to the fish DISCUSION
farm protocols.
Determination of fertilizing percentages The results of the present investigation show that the
After 14 days of incubation, the percentage of use of vitamin C, trolox and polyphenol in sperm
fertilization was determined using acetic acid 10%, by diluents for rainbow trout, preserves sperm motility,
depositing 30 random fish eggs and considering those improving significantly the fertilizing capability of
that have observed neural tubes as fertilized eggs. semen and increasing spermatozoa storage times.
341 Use of antioxidants in rainbow trout Oncorhynchus mykiss sperm diluents

Table 1. Osmolarity and pH values for the treatments used in the storage of rainbow trout semen.
Tabla 1. Valores de osmolaridad y pH para los tratamientos utilizados en el almacenamiento de semen de trucha arcoiris.

Treatments Information Osmolarity mOsmol kg-1 pH


C Fresh semen 300 8.0
T1 Undiluted stored semen 300 8.0
T2 Semen diluted with UCT medium 288 8.0
T3 T2 + polyphenol 280 7.5
T4 T2 + trolox 290 7.8
T5 T2 + polyphenol + trolox 288 7.7
T6 T2 + vitamin C 260 7.5

Figure 1. Level of motility (Mode) in rainbow trout Figure 2. Motility (s) of rainbow trout spermatozoa
spermatozoa, submitted to different antioxidant treat- submitted to different antioxidant treatments. The values
ments. Different letters seen a same day indicate that are given as averages SD (n = 20). Different letters
statistically significant differences exist (n = 20). indicate that statistically significant differences exist for
Figura 1. Nivel de motilidad (Moda) en espermatozoides a same day (P < 0.05).
de trucha arcoiris sometidos a diferentes tratamientos con Figura 2. Motilidad (s) en espermatozoides de trucha
antioxidantes. Letras dife-rentes en un mismo da indica arcoiris sometidos a diferentes tratamientos con
diferencias estads-ticamente significativas (n = 20). antioxidantes. Los valores se entregan en promedio SD
(n = 20). Letras diferentes indica que existen diferencias
Sperm motility in all the antioxidant treatment estadsticamente significativas para un mismo da (P <
0,05).
group is considerably improved in T5, which presents
the highest value of 7.08 1.02 s at day 17, this can be
helping to protect the lipid membrane from
explained since the combined use of polyphenol and peroxidation (May, 1999). -tocopherol can act as an
trolox can increase their actions as antioxidants (Ball antioxidant or pro-oxidant, since it inhibits or
et al., 2001b). Polyphenols on their part, act mainly by facilitates lipid peroxidation of the low density
chelating metals and capturing in vitro the ORSs and lipoproteins. The pro-oxidizing activity of -
nitrogen reactive species (NRS) in a more efficient tocopherol is prevented by ascorbate, for which
manner than vitamin C (Larkins, 1999). The same vitamin E can only be effective in combinations with
occurs with the separate use of trolox and vitamin C, vitamin C (Carr et al., 2000). The combination of
this last element is the main antioxidant found in vitamin E, a lipophilic antioxidant, with vitamin C, a
plasma and in the cells, that by donating electrons to hydrophilic antioxidant and/or selenium, desintoxicate
the tocoperoxil radical of the oxidized vitamin E, it the lipids from the peroxides (Schwenke & Behr,
recycles the antioxidant function of -tocopherol, 1998).
Lat. Am. J. Aquat. Res. 342

semen of different teleostei fish for 72 to 120 h with


uric acid and 72 h with methionine.
There is limited information on antioxidant
systems in teleostei fish spermatozoa to be able to
define which antioxidant is the most adequate one for
semen storage. It is because of this, that in this work,
the effect of adding antioxidants that are soluble in
water and lipids, into the sperm diluents is evaluated
to maintain the integrity of the spermatozoa,
protecting the cells and reducing the risk of lipid
peroxidation which would affect sperm motility
(Ciereszco & Dabrowski, 1995).
Due to its positive effects on motility parameters,
fertilizing capabilites, stability and low price, the use
of polyphenol, trolox and vitamin C can be a useful
Figure 3. Fertilizing capabilities of rainbow trout compliment for the storage of salmonid spermatozoa.
spermatozoa submitted to different antioxidant treat-
ments. The values are given as averages SD (n = 15).
Different letters indicate that statistically significant ACKNOWLADGEMENTS
differences exist for a same day (P < 0.05).
Figura 3. Capacidad fecundante en espermatozoides de Financed by the FONDEF D06I1020 Project and
trucha arcoiris sometidos a diferentes tratamientos con collaboration of the Quetro S.A. and Dropco S.A.
antioxidantes. Los valores se entregan en promedio SD companies.
(n = 15). Letras diferentes indica que existen diferencias
estadsticamente significativas en un mismo da (P <
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DOI: 10.3856/vol39-issue2-fulltext-16

Research Article

Solapamiento trfico entre el lobo marino de un pelo Otaria flavescens y la


pesquera de arrastre demersal del golfo San Matas, Patagonia, Argentina

Mara Alejandra Romero1, Silvana Dans2, Ral Gonzlez1, Guillermo Svendsen1


Nstor Garca2 & Enrique Crespo2
1
Instituto Multidisciplinario de Investigacin y Desarrollo de la Patagonia Norte (IDEPA)
CONICET/Universidad Nacional del Comahue, Gemes 1030, 8520
San Antonio Oeste-Ro Negro, Argentina
2
Centro Nacional Patagnico (CENPAT), CONICET/Universidad Nacional de la Patagonia
San Juan Bosco, Boulevard Brown 2915, 9120 Puerto Madryn-Chubut, Argentina

RESUMEN. A nivel internacional, paralelo a la declinacin y al colapso de pesqueras de gran escala, surgi
un inters creciente por el estudio de las interacciones entre mamferos marinos y pesqueras. El golfo San
Matas (Patagonia, Argentina) es considerado un ecosistema pesquero independiente de las aguas de la
Plataforma Continental Argentina, con condiciones oceanogrficas y biolgicas particulares. La condicin de
sistema semi-cerrado podra generar escenarios particulares para la interaccin entre la flota pesquera de
arrastre de fondo y la poblacin de lobos marinos de un pelo Otaria flavescens. En el presente trabajo se
caracteriz la dieta del predador y la composicin de las capturas pesqueras a fin de evaluar el solapamiento
trfico entre ambos componentes. A partir de este anlisis y la comparacin de las tallas de las presas
consumidas, se encontr que la posibilidad de una interaccin competitiva entre la flota pesquera y los lobos
marinos, a partir de la utilizacin de recursos similares, sera baja en el ecosistema del golfo San Matas.
Palabras clave: Otaria flavescens, lobo marino, golfo San Matas, pesquera de arrastre, solapamiento trfico,
Patagonia argentina.

Trophic overlap between the South American sea lion Otaria flavescens and the
demersal trawl fishery in San Matas Gulf, Patagonia, Argentina

ABSTRACT. As world fisheries began to decline and massive collapses were observed, the competition
between marine mammals and fisheries became an issue of growing concern. San Matas Gulf (Patagonia,
Argentina) is considered to be a fishery ecosystem independent of the Argentine Continental Shelf waters,
with particular oceanographic and biological properties. As a semi-enclosed ecosystem, this gulf may generate
particular scenarios for interactions between the demersal trawl fishery fleet and the population of South
American sea lions Otaria flavescens. In this paper, the diet of the top predator and the composition of fishery
catches were characterized in order to assess the trophic overlap between these two components. This analysis
and a comparison of the sizes of prey consumed revealed a low probability of competition for similar
resources between the fishing fleet and the marine mammals in the San Matas Gulf ecosystem.
Keywords: Otaria flavescens, sea lion, San Matas gulf, trawl fishery, trophic overlap, Patagonia, Argentina.
___________________
Corresponding author: Mara Alejandra Romero (aromero@ibmpas.org)

INTRODUCCIN funcionamiento de los ecosistemas (Bowen, 1997;


Pauly et al., 1998a). Durante las ltimas dcadas, se
La dieta y los hbitos alimentarios de una especie ha especulado que los efectos a largo plazo producto
determinan su ubicacin dentro de una red trfica, y de la grave disminucin en la abundancia de muchas
definen su rol ecolgico (Pauly et al., 1998a). En poblaciones de mamferos marinos, como conse-
general, los mamferos marinos estn posicionados cuencia de impactos de origen antrpico (caza,
cerca o en la parte superior de la estructura trfica, y contaminacin de los ambientes, capturas
se considera que pueden tener un rol importante en el incidentales), podran haber afectado de modo
345 Solapamiento trfico lobo marino-pesquera de arrastre, golfo San Matas, Argentina

permanente a los ecosistemas marinos (Parsons, 1992; ndices de solapamiento trfico no miden directamente
Pauly et al., 1998b; Springer et al., 2003). competencia, la similitud en la biologa trfica entre
Por otro lado, paralelo a la profundizacin de la los componentes involucrados puede ser un indicador
crisis pesquera mundial, tambin se ha discutido de potenciales interacciones competitivas.
acerca de los efectos que los mamferos marinos El golfo San Matas es considerado un ecosistema
podran generar sobre la pesca, compitiendo pesquero independiente de las aguas de la Plataforma
directamente por los recursos disponibles (Butterworth Argentina, siendo administrado en forma autnoma
et al., 1988; Bowen, 1997). De forma simple, se por el gobierno de la Provincia de Ro Negro-
pensaba que disminuyendo las poblaciones de Argentina. Desde hace ms de tres dcadas se
mamferos marinos, las capturas pesqueras se desarrolla una pesquera dirigida al complejo de
incrementaran en una proporcin directa a lo especies demersales y demersal-pelgicas. De acuerdo
consumido por los mamferos, ahora disponible para a sus propiedades oceanogrficas y biolgicas, se ha
la pesca (Yodzis, 1998). Esta interpretacin fue sugerido que algunas de las especies forman unidades
utilizada para promover la reduccin en el tamao de demogrficas diferentes a las existentes en la
algunas poblaciones de mamferos marinos (Wickens Plataforma Continental Argentina, como es el caso de
et al., 1992). la merluza comn Merluccius hubbsi, principal
La controversia acerca de este argumento se centr especie blanco de la pesquera (Di Gicomo et al.,
en la pregunta bsica sobre cunto consumen 1993; Sardella & Timi, 2004; Gonzlez et al., 2007).
realmente los mamferos marinos y surgi la Esta condicin de sistema semi-cerrado del golfo San
necesidad de estudiar el rol que cumplen en el Matas podra generar escenarios particulares para la
ecosistema (Yodzis, 2001). Otro debate surgi a partir interaccin entre la flota pesquera de arrastre demersal
del reconocimiento que este simple esquema est que opera en el golfo y algunos predadores tope del
incluido en una red trfica mucho ms compleja de ecosistema.
interacciones que pueden afectar los resultados
A lo largo de la costa del golfo San Matas, se
(Lavigne, 1995), y en la cual los efectos de las
interacciones indirectas propagados a travs de la red asientan durante todo el ao numerosos apostaderos de
trfica pueden ser ms importantes que los efectos lobos marinos de un pelo Otaria flavescens, aunque su
propios de las interacciones directas (Yodzis, 2000). nmero y localizacin exacta pueden variar estacional-
mente (Grandi et al., 2008). Estos apostaderos
El estudio del rol ecolgico de los mamferos
pertenecen a lo que se denomina la unidad funcional
marinos y su grado de interaccin con las pesqueras
del Norte de Patagonia, la cual ha mostrado una
se convirti en foco de inters de muchos estudios
tendencia positiva cercana al 6% anual (Dans et al.,
(Northridge, 1984, 1991; Bowen, 1997; De Master et
2004). Los apostaderos del golfo San Matas son
al., 2001; Koen-Alonso & Yodzis, 2005; Kaschner &
Pauly, 2005; Dillingham et al., 2006; Morissette et al., algunos de los que han registrado las mayores tasas de
2006). Sin embargo, una evaluacin dirigida a estudiar incremento, tanto en el nmero total como en la
la competencia real entre las pesqueras y los produccin de cras. Esta especie puede realizar viajes
mamferos marinos es difcil de realizar, en parte de alimentacin extensos, especialmente los machos.
debido al supuesto subyacente que para que exista Las hembras estaran ms restringidas a alimentarse en
competencia, la remocin de uno de los competidores reas cercanas a la costa y a los lugares de cra (Koen-
debe resultar en un incremento mensurable en la Alonso et al., 2000), con lo cual se espera que preden
disponibilidad de alimento para el otro componente con mayor regularidad dentro de las aguas del golfo.
(Cooke, 2002). Asimismo, el desarrollo de modelos En este contexto, el objetivo de este trabajo fue
suficientemente detallados para demostrar de forma analizar en forma comparativa la dieta del lobo marino
inequvoca la existencia de una interaccin de un pelo y la composicin de las capturas pesqueras
competitiva, est en gran medida, limitado por la de la flota de arrastre demersal. Este anlisis abarc
complejidad de las interacciones trficas en los tanto la comparacin de las especies presa como las
ecosistemas marinos y la dificultad para obtener datos tallas consumidas/capturadas.
fiables de cada uno de los componentes (Yodzis,
2000; Plagnyi & Butterworth, 2002).
MATERIALES Y MTODOS
Consecuentemente, la mayor parte de los esfuerzos
en investigacin han apuntado a estudiar el grado de
solapamiento trfico, es decir, la medida en que las Dieta del lobo marino de un pelo
especies de mamferos marinos y la pesca hacen uso La muestra consisti de un total de 34 estmagos
de los mismos recursos alimenticios. A pesar que los colectados en el golfo San Matas entre 2006 y 2009
Lat. Am. J. Aquat. Res. 346

(Fig. 1). Los estmagos fueron obtenidos a partir de La importancia relativa de las presas en la dieta fue
animales encontrados muertos en la costa y evaluada mediante la frecuencia de ocurrencia (%FO),
provenientes de capturas incidentales (Tabla 1). Las la dominancia numrica o porcentaje en nmero (%N),
capturas fueron realizadas por barcos arrastreros de la dominancia en peso o porcentaje en peso (%W) y el
fondo dirigidos a la captura de merluza comn. ndice de importancia relativa porcentual (%IRI). El
Previo a la necropsia se registr la longitud IRI (Pinkas et al., 1971; Corts, 1997) es una medida
estndar (LS, cm) de los individuos y se revis comnmente utilizada ya que provee un resumen de la
externamente para constatar la presencia de heridas. composicin de la dieta y se obtiene como:
Los estmagos una vez removidos fueron IRIi = (%Wi + %Ni) % FOi (1)
almacenados en bolsas de polietileno en fro (-20C), Los ndices fueron calculados por especie, por
para su posterior anlisis. El tamao corporal de los grupo zoolgico (peces, moluscos y crustceos) y por
individuos vari entre 170 y 220 cm, con una edad grupo ecolgico. Los grupos ecolgicos considerados
entre 2 y 18 aos (Grandi et al., 2009). fueron: pelgico, bentnico y demersal. Este ltimo
Los contenidos estomacales fueron descongelados fue subdividido en demersal-pelgico (presas que
y lavados utilizando tamices secuenciales de tienen un patrn de migracin diario, dispersndose en
diferentes tamaos de malla (de 0,5 a 10 mm). En el la columna de agua durante la noche y permaneciendo
caso de encontrar presas intactas fueron cerca del fondo durante las horas de luz) y demersal-
inmediatamente identificadas, medidas y pesadas. Las bentnico (presas que no realizan migraciones
partes diagnsticas remanentes (otolitos, huesos y verticales).
picos de cefalpodos) fueron recuperadas y Para cuantificar la incertidumbre debida al
almacenadas en etanol 70%. Las presas fueron muestreo, se generaron intervalos de confianza no
identificadas al nivel taxonmico ms bajo posible, paramtricos de 95% para los ndices de porcentaje en
utilizando colecciones de referencia (colecciones nmero (%N) y porcentaje en peso (%W), mediante
depositadas en el CENPAT y en el IDEPA), y una tcnica de remuestreo (bootstrap) (Efron, 1979).
catlogos publicados (Menni et al., 1984; Roper et al., La rutina para ejecutar el bootstrap fue escrita en
1984; Clarke, 1986; Boschi et al., 1992; Gosztonyi & lenguaje de programacin R. Las muestras al azar
Kuba, 1996; Boltovskoy, 1999; Volpedo & fueron extradas con reemplazo, y el procedimiento
Echevarra, 2000; Garca-Godos, 2001). fue repetido 1000 veces.
El nmero total de peces consumidos por individuo
fue determinado a partir del conteo de otolitos, Composicin de las capturas de la flota de arrastre
discriminando en derechos, izquierdos y otolitos no demersal
asignados. El nmero mnimo de otolitos por especie Los datos sobre composicin especfica de las
fue obtenido como la suma del nmero mayor de capturas y distribucin de frecuencias de tallas de las
otolitos identificados (ya sean izquierdos o derechos), especies capturadas fueron obtenidos de los informes
ms la mitad de los otolitos no identificados. El peridicos del Programa de Observadores Pesqueros
nmero de cefalpodos fue estimado a partir del (POP) de la Provincia de Ro Negro. Los observadores
mximo nmero de picos superiores o inferiores son embarcados desde los puertos de San Antonio
encontrados en cada estmago (Pierce & Boyle, Oeste y San Antonio Este, siguiendo un criterio de
1991). seleccin al azar de las embarcaciones. Tpicamente,
La longitud (LT, longitud total de los peces y los viajes de pesca de la flota de arrastre tienen una
LDM, longitud dorsal del manto de los cefalpodos, duracin promedio de 3 a 6 das, realizando entre 2 y
cm) y peso hmedo (g) de las presas al momento de la 5 lances por da de pesca (duracin del lance 2-5 h).
ingestin fue estimado a partir de las piezas duras El esfuerzo de muestreo del POP, en relacin a los
remanentes, utilizando regresiones alomtricas desembarcos anuales de merluza comn y el esfuerzo
(Pineda et al., 1996; Bassoi, 1997; Koen-Alonso et al., de pesca (medido en nmero de lances y horas
2000). A fin de minimizar la subestimacin de los efectivas de pesca), se indica en la Tabla 2.
parmetros, slo los otolitos y picos no daados El muestreo sobre la composicin especfica de las
fueron medidos. Cuando en los estmagos se capturas consisti en la recoleccin de una muestra al
encontraron piezas digeridas o destruidas, las medidas azar de la captura (al menos 6 cajones de 40 kg cada
de estos elementos fueron asignadas a partir de una uno), previo a la seleccin y descarte por parte de la
muestra al azar de las piezas enteras y no digeridas de tripulacin. Posteriormente, la muestra fue clasificada
cada especie, encontradas dentro del mismo estmago y cuantificada por especie. Los observadores
(Koen-Alonso et al., 1998). repitieron esta rutina en uno/dos lance/s de pesca por
347 Solapamiento trfico lobo marino-pesquera de arrastre, golfo San Matas, Argentina

Figura 1. rea de estudio. Los crculos indican los lugares de varamientos o capturas incidentales de lobo marino de un
pelo Otaria flavescens.
Figure 1. Area of study. The circles indicate South American sea lion Otaria flavescens sampling sites.

Tabla 1. Resumen de las muestras de lobo marino de un pelo Otaria flavescens consideradas para el estudio de dieta. En
parntesis se indica el nmero de estmagos vacos.
Table 1. Summary of samples of South American sea lion Otaria flavescens considered for the study of the diet. The
number of empty stomachs is shown in parenthesis.

Machos Hembras
Muerto en la costa Captura incidental Muerto en la costa Captura incidental
2006 3 (2) 1 1 0
2007 2 (1) 7 10 (3) 0
2008* 3 1 1 (1) 3
2009 0 0 1 (1) 0
* se captur incidentalmente un animal de sexo indeterminado

da. El conjunto de datos disponible para caracterizar porcentaje en peso e importancia relativa (%IRI) no
la composicin de las capturas abarc el periodo fueron utilizados al no disponer de los datos sobre el
2006-2008. As como en el caso del lobo marino de un peso capturado por especie a nivel de lance.
pelo se consider a cada estmago como unidad de Adems, se analizaron las tallas consumidas por la
muestreo, asumiendo que el contenido representa una
pesquera para algunas especies en particular. Los
ingesta diaria, en el caso de la pesquera se consider a
observadores separaron una muestra al azar de entre 6
cada lance de pesca como unidad de muestreo. La
importancia relativa de las diferentes especies y 10 cajones de la captura total de merluza comn,
capturadas fue calculada mediante la frecuencia de savorn Seriolella porosa y calamar Illex argentinus
ocurrencia y el porcentaje en nmero. Los ndices de (nicas especies muestreadas por el POP). Se registr
Lat. Am. J. Aquat. Res. 348

Tabla 2. Esfuerzo de muestreo anual del Programa de Observadores Pesqueros en funcin del nmero de lances,
desembarque de merluza comn y horas efectivas de pesca. Los totales de cada una de las variables fueron obtenidos de
las estadsticas pesqueras recopiladas por la Direccin de Pesca (Milln, 2009).
Table 2. Annual sampling effort of the Fishery Observer Program in terms of the number of hauls, common hake landings
and fishing effort. The totals of each variable were obtained from the fishery statistics compiled by the Direccin de Pesca
(Milln, 2009).

Total Muestra Porcentaje de cobertura


Lances Desembarque Esfuerzo Lances Desembarque Esfuerzo Lances Desembarque Esfuerzo
Ao (ton) (h) (h)
(N) (N) (ton) (N) (ton) (h)
2006 3097 4549,2 9561 167 276 534 5,39 6,08 5,59
2007 3612 7324,21 10874 130 281 393 3,6 3,83 3,61
2008 3871 7735,58 11777 85 209 260 2,2 2,7 2,21

el sexo y la talla (medido aproximando al centmetro s


inferior) de los peces (longitud total) y calamares nij
(longitud dorsal del manto). Esta rutina se repiti en c j = i =1
s
uno/dos lance/s de pesca por da. El periodo de Ni
muestreo se extendi entre 2006 y 2008. Los i =1 y
muestreos sobre composicin especfica de las nij
capturas y distribucin de frecuencias de tallas se pij =
realizaron en forma alternada a lo largo de cada Ni
jornada de pesca. Donde s es el nmero total de predadores, r es el
nmero total de clases de recurso, nij es el nmero de
Anlisis del solapamiento trfico ocurrencias de la presa j en el predador i, y Ni es la
El anlisis del solapamiento trfico entre el lobo sumatoria de los nij en el predador i. La hiptesis nula
marino de un pelo y la pesquera de arrastre demersal de un solapamiento completo (Ho: GO = 1 versus Ha:
del golfo San Matas involucr el clculo de dos GO 1) se puso a prueba utilizando el estadstico V.
ndices de solapamiento: el ndice de solapamiento Este estadstico se calcula como:
( ) lnGO
general (GO) y el ndice de solapamiento especfico
s
(SO) (Petrakis, 1979; Ludwig & Reynolds, 1988). v=2 N
i =1 i
(3)
Estos ndices fueron elegidos porque tienen
propiedades estadsticas que permiten poner a prueba el cul sigue una distribucin Chi-cuadrado con
la hiptesis nula de un solapamiento total (Petraitis (s-1)(r-1) grados de libertad (Ludwig & Reynolds,
1979, 1985; Ludwig & Reynolds, 1988). Por otro 1988).
lado, el GO es uno de los ndices que presenta la El SO es un ndice asimtrico que evala la
menor cantidad de sesgos, ya sea debido a la probabilidad de obtener la curva de utilizacin de un
variabilidad en la equitabilidad de los recursos o a predador i a partir de la curva de utilizacin de un
variaciones en el tamao muestral (Smith & Zaret, predador m. Se calcula como:
1982).
r
( ) ( )
r
El GO es un ndice simtrico (GOBA = GOAB) que pij ln p mj pij ln pij (4)
representa la probabilidad de que la curva de j =1
= e
j =1
utilizacin de cada predador provenga de la curva de
SOim
utilizacin comn a todos ellos. A los efectos
comparativos, el GO se ajusta para que vare entre 0 y donde pmj se define para la presa j del predador m, de
1, obtenindose un ndice ajustado (GOa) (Ludwig & la misma forma que pmj se define para la presa j del
Reynolds, 1988). El GO se define como: predador i. La hiptesis nula de un solapamiento
especfico completo (Ho: SOim = 1 versus Ha: SOim
s r
n ln c ln p 1) fue puesta a prueba utilizando el estadstico U
i = 1i = 1 ij j ij
(Ludwig & Reynolds, 1988). Este estadstico se
s calcula como:
N i
GO = e i = 1 Uim = -2NilnSOim (5)
(2) siendo
349 Solapamiento trfico lobo marino-pesquera de arrastre, golfo San Matas, Argentina

el cul sigue una distribucin Chi-cuadrado con (r-1) constituyendo temes frecuentes en la dieta del
grados de libertad. predador.
Los datos utilizados para el anlisis de Con referencia a los grupos ecolgicos, el mayor
solapamiento trfico fueron la frecuencia de componente correspondi a presas de hbitos
ocurrencia de aquellas especies con un %N > 1% en la demersal-pelgicos (Fig. 2), aunque la frecuencia de
muestra total, ya sea en la dieta del predador o en las ocurrencia de las presas demersal-bentnicas y
capturas pesqueras. bentnicas fueron igualmente altas. La merluza, el
La comparacin de las tallas de las presas savorn, el pampanito y el calamar fueron las
consumidas por el lobo marino de un pelo con las principales especies de hbitos demersal-pelgicos. La
capturadas por la flota pesquera se bas en las tallas alta frecuencia de ocurrencia del grupo demersal-
estimadas a partir de las regresiones alomtricas y las bentnico se atribuy a la presencia de la raneya y el
muestreadas por los observadores pesqueros. Las abadejo; mientras que el componente bentnico estuvo
diferencias estadsticas se evaluaron mediante la dado por el aporte de varias especies.
prueba U de Mann-Whitney. La LT media de los peces consumidos por el lobo
marino de un pelo present un rango de 6,85 a 65,21
cm. El rango de LDM de los cefalpodos presa fue
RESULTADOS
estimado entre 5,13 y 30,80 cm. Considerando todas
las especies presa, la longitud total estimada vari
Dieta del lobo marino de un pelo
entre 5,13 y 65,21 cm y la biomasa reconstruida entre
Del total de estmagos colectados, 26 contuvieron 0,34 y 3444,27 g.
restos de alimento. El estado de digestin de las presas
La distribucin de frecuencias de tallas fue
fue mayor en los animales varados en las costas que
unimodal para la merluza, raneya y savorn (Figs. 3 y
en los capturados incidentalmente, en los cuales fue
4). La merluza fue la presa que present el rango de
comn encontrar presas recin ingeridas. Un total de
tallas consumidas ms amplio, aunque prevalecieron
1.030 presas fueron recuperadas e identificadas a
las tallas pequeas, con una moda en 21 cm (Fig. 3).
partir de las muestras, correspondiendo a una biomasa
Aproximadamente el 90% de las merluzas ingeridas
total estimada de 115,11 kg. El nmero medio ( error
tuvieron una talla menor a 35 cm, correspondientes a
estndar, ES) de presas por estmago fue 39,6
individuos juveniles menores de 3 aos (Ocampo-
11,43; con un peso medio de 4,47 0,9 kg. De
acuerdo al origen de las muestras, el nmero medio de Reinaldo, 2010). El peso medio ( DS) de la merluza
presas por estmago fue 58,06 15,83 para animales fue 104,4 133,29 g.
capturados incidentalmente y 39,65 11,43 para
animales hallados muertos en las costas.
Veinticuatro especies presa fueron identificadas,
correspondientes a tres grupos zoolgicos: peces (15
especies), cefalpodos (6 especies) y crustceos (3
especies) (Tabla 3). Los peces fueron el grupo ms
importante, con un %IRI de 93%; mientras que los
moluscos slo representaron el 6,95% de la dieta. En
el caso de los crustceos, no fue posible calcular el
valor del %IRI debido a que no se pudo reconstruir el
peso de las presas al momento del consumo.
El nmero medio de especies presa por estmago
fue 3,46 0,46. La merluza comn fue la presa ms Figura 2. Composicin de la dieta Otaria flavescens en
importante, con un %IRI de 55,42%, representando el el golfo San Matas de acuerdo al grupo ecolgico de las
39,67% en nmero y el 37,09% en peso del total de presas. %N: porcentaje en nmero, %W: porcentaje en
presas consumidas. La raneya Raneya brasiliensis y el peso, %FO: frecuencia de ocurrencia, %IRI: ndice de
savorn tambin fueron presas significativas en la dieta importancia relativa porcentual.
del lobo marino de un pelo, con un %IRI de 15,14% y Figure 2. Diet composition of Otaria flavescens in the
9,57% respectivamente. Adems, seis especies presa San Matas gulf based on the ecological group of prey.
(pampanito Stromateus brasiliensis, abadejo %N: percentage by number; %W: percentage by
Genypterus blacodes, anchota Engraulis anchoita, regression-estimated wet weight; %FO: percent
calamar Illex argentinus, pulpo colorado Enteroctopus frequency of occurrence; %IRI: percent of Index of
megalocyathus) tuvieron un %IRI entre 1 y 5%, Relative Importance.
Lat. Am. J. Aquat. Res. 350

Figura 3. Distribucin de frecuencias de tallas de Figura 4. Curvas de selectividad de las tallas de savorn
merluza comn Merluccius hubbsi consumida por Otaria Seriolella porosa y calamar Illex argentinus consumidos
flavescens, capturada por la flota de arrastre de fondo y por Otaria flavescens (Of), capturado por la flota de
palangre que operan en el golfo San Matas. La arrastre de fondo que opera en el golfo San Matas (datos
estructura poblacional fue obtenida de la campaa de obtenidos a partir de los registros del Programa de
prospeccin de los recursos demersales del golfo 2007 Observadores Pesqueros).
(REDE07, Ocampo-Reinaldo et al., 2008).
Figure 4. Size selectivity curves of silver warehou
Figure 3. Length-frequency distribution of common hake Seriolella porosa and squid Illex argentinus preyed by
Merluccius hubssi consumed by Otaria flavescens, Otaria flavescens (Of), caught by the trawl demersal fleet
caught by the trawl demersal fleet in the San Matas gulf. in the San Matas gulf (data obtained from the Fishery
The population structure was obtained from a trawl Observer Program).
demersal survey carried out in 2007 (REDE07, Ocampo-
Reinaldo et al., 2008).
especies (entre ellas Paralichthys isosceles, Xistreuris
La longitu