Академический Документы
Профессиональный Документы
Культура Документы
1093/conphys/coy046
Research article
1
Zoológico Nacional Simón Bolívar, Barrio Amón, Calle 13, Apdo. 11594-1000, San José, Costa Rica
2
Department of Biology, University of North Carolina, Chapel Hill, NC 27599, USA
3
College of Veterinary Medicine, Department of Clinical Sciences, North Carolina State University, 1060 William Moore Drive Raleigh, NC 27607,
USA
4
Galaṕ agos Science Center GSC (Universidad San Francisco de Quito-University of North Carolina at Chapel Hill), Av. Alsacio Northia, Isla San
Cristobal, Galaṕ agos, Ecuador
5
Universidad San Francisco de Quito USFQ, Galapagos Science Center GSC, Colegio de Ciencias Biológicas y Ambientales COCIBA, Campus
Cumbayá Av. Diego de Robles S/N e Interoceánica, Galápagos Casilla Postal 17-1200-841, Quito 170901, Ecuador
*Corresponding author: Zoológico Nacional Simón Bolívar, Barrio Amón, Calle 13, Apdo. 11594-1000, San José, Costa Rica. Email: ranarg@
gmail.com
..............................................................................................................................................................
The San Cristóbal lava lizard, Microlophus bivittatus, is one of nine species of lava lizards endemic to the Galápagos Islands
of Ecuador. No information presently exists about baseline health parameters for any of these species. We analysed blood
samples drawn from 47 lizards (25 males and 22 females) captured at two locations on San Cristóbal Island. A portable
blood analyser (iSTAT) was used to obtain near-immediate field results for total CO2, lactate, sodium, potassium, ionized
calcium, glucose and haemoglobin. Standard laboratory haematology techniques were employed for differential white
blood cell counts and haematocrit determination. Body temperature, heart rate and body measurements were also
recorded. We found significant differences in haematocrit values between males and females. The values reported in this
study provide baseline data that may be useful in detecting changes in health status among lava lizards affected by natural
disturbances or anthropogenic threats. Our findings might also be helpful in future efforts to demonstrate associations
between specific biochemical or haematological parameters and disease. Because there are several related species on dif-
ferent islands in the Galápagos archipelago, comparisons between populations and species will be of interest.
Key words: Biochemistry, Galápagos, haematology, health assessment, Microlophus bivittatus, San Cristóbal lava lizard
Editor: Steven Cooke
Received 10 May 2018; Revised 11 July 2018; Editorial Decision 23 July 2018; accepted 26 July 2018
Cite as: Arguedas R, Steinberg D, Lewbart GA, Deresienski D, Lohmann KJ, Muñoz-Pérez JP, Valle CA (2018) Haematology and biochemistry of
the San Cristóbal Lava Lizard (Microlophus bivittatus). Conserv Physiol 6(1): coy046; doi:10.1093/conphys/coy046.
..............................................................................................................................................................
..............................................................................................................................................................
© The Author(s) 2018. Published by Oxford University Press and the Society for Experimental Biology. 1
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/
by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
Downloaded from https://academic.oup.com/conphys/article-abstract/6/1/coy046/5075450
by guest
on 17 August 2018
Research article Conservation Physiology • Volume 6 2018
..............................................................................................................................................................
endemic species that are experiencing rapid change, such as six lizards (Nmale = 13, Nfemale = 13) were captured along a
the Galapagos Archipelago. walking trail to Punta Carola (0°53′32″ and 89°36′43″) on 5
July 2017. On the following day, 21 lizards (Nmale = 12,
The Galapagos Archipelago has nine endemic species of Nfemale = 9) were captured along Tijeretas trail (0°53′34″and
lava lizard in the South American genus Microlophus (Family: 89°36′32″).
Tropiduridae) (Benavides et al., 2009; Jiménez-Uzcátegui et al.,
2017). Microlophus bivittatus (Fig. 1), which is restricted to Each lizard was captured by noose, placed in a cloth bag,
the island of San Cristóbal and nearby Islote Lobos, inhabits and transported to a temporary field laboratory for process-
xeric, low-elevation areas, such as coastal scrubland and rocky ing (see below). Afterwards, to avoid recapturing the same
beaches. This lizard is listed as near threatened (Márquez and individuals, each was marked on its dorsum with a spot of
Cisneros-Heredia, 2016) and is particularly vulnerable to pre- non-toxic, red acrylic paint used previously in other studies
dation by feral cats (Carrión Avilés, 2012; Carrion and Valle, (Berriozabal et al., 2017; Keogh et al., 2012; Pasek and
2018). At present, no blood chemistry or haematology data Collver, 2001) and known to wash or rub off within 10 days
have been acquired for the genus Microlophus, which compli- of application (C.A. Valle, personal observation). Because the
cates efforts to evaluate or monitor the health of wild lava liz- study was conducted outside of the breeding season and
ard populations. In this study, we report baseline biochemical the paint fades quickly, the marking was unlikely to affect
and haematological values, along with basic physiological the behaviour, fitness or survival of the lizards.
measures, for the San Cristóbal lava lizard.
Morphological measurements and body
Methods temperature
Ethics statement A flexible measuring tape was used to determine snout-vent
length (SVL) and total length (TL). Head length (HL), head
This study was conducted on San Cristóbal Island in the width (HW), head depth (HD), forelimb length (FLL) and
Galápagos archipelago of Ecuador as part of a population hindlimb length (HLL) measurements were made using
health assessment authorized by the Galápagos National digital calipers. Body weight was measured with a spring
® ®
Park Service (Permit No. PC-23-17, PI Carlos A. Valle, PhD) scale (Pesola ). An EBRO Compact J/K/T/E Thermocouple
and approved by the Universidad San Francisco de Quito Thermometer was used to obtain all temperature readings
ethics and animal handling protocol. All handling and sam- (model EW-91 219–40; Cole-Parmer, Vernon Hills, IL,
pling procedures were consistent with standard vertebrate USA). Core body temperatures were recorded from the clo-
protocols and veterinary practices. aca using the probe T PVC epoxy tip 24GA, usually within
five minutes of capture. Finally, sex was determined on the
Capture and marking basis of external sexual dimorphism: males are larger and
have two white bands on each side of the body, while
Lizards were captured in locations within 2 km of the
females are smaller with orange coloration on the ventral–
Galapagos Science Center on San Cristobal Island. Twenty-
frontal area (Troya-Zuleta, 2012).
Biochemistry parameters
Blood gas, electrolyte and biochemistry results were obtained
Figure 1: Female individual of a San Cristóbal Lava Lizard using an iSTAT Portable Clinical Analyzer (Heska
(Microlophus bivittatus). Corporation, Fort Collins, CO, USA) with CG8+ cartridges.
..............................................................................................................................................................
The iSTAT is a portable, hand-held, battery-operated elec- Table 1: Morphometric measurement of San Cristóbal Lava Lizards
tronic device that measures a wide variety of blood gas, (Microlophus bivittatus) separated by sex
chemistry and haematology parameters using only a few
drops (0.095 ml) of whole, non-coagulated blood. The fol- Male Female
lowing parameters were measured: anion gap, TCO2, haem- Morphometrics
n = 25 n = 22
atocrit, haemoglobin, sodium (Na), chloride (Cl), potassium
(K), ionized calcium (iCa) and glucose. Mean corpuscular TL (mm) 195.7 156.4
haemoglobin concentration (MCHC) was also calculated (30.3) (19.8)
[Hb (g/L)/Htc (%) * 100].
127.0–237.0 96.0–182
Haematology SVL (mm) 80.6 64.7
..............................................................................................................................................................
Table 2: Blood biochemical values of San Cristobal Lava Lizards Table 2: continued
(Microlophus bivittatus) separated by sex
Analyte Male Female
Analyte Male Female
Haematocrit (%) n = 24 n = 21
Na (mmolol/l) n = 23 n=9
33.39 27.80
165.77 168.26
(5.90) (7.85)
(6.99) (3.66)
23–43 8–39
149–180 160–171
MCHC (g/l) n = 21 n=9
K (mmol/l) n = 22 n=9
(37.82) (44.22)
4.26 3.51
7.41 15.2
(1.90) (0.97)
27.94–54.78 25.67–75
2–8.1 2–4.9
Values represent n, means, standard deviation (parenthesis) and range (minimum–
Cl (mmol/l) n = 21 n=9 maximum). Sample sizes vary because some females were too small to extract the
amount of blood required for all analyses.
138.44 138.52
(2.87) (3.12) Monocytes: Large round to amoeboid cells, nucleus semi-
131–140 132–140 lobed with less condensed chromatin and a pale blue cyto-
plasm (Fig. 3).
iCa (mmol/l) n = 23 n=9
1.56 1.67 Heterophils: Round with eosinophilic granules and a bilobed
(sometimes four lobules) nucleus (Fig. 3).
(0.14) (0.25)
Eosinophils: Large amoeboid to round cells with rather pur-
1.31–1.9 1.4–2.24
ple conspicuous granules and round nuclei (Fig. 3).
tCO2 (mmol/l) n = 23 n=9
Basophils: Small round cells with purple granules obscuring
9.17 10.44 the nucleus.
(2.55) (2.50)
6–15 7–14
Glucose (mg/dl) n = 23 n=9 Discussion
272.30 241.22 Our results provide the first data on the morphometrics,
(45.96) (19.79) body temperature, biochemistry and haematology of San
Cristóbal lava lizards (M. bivittatus). Such baseline data on
199–401 218–273
the morphology and physiology of wild animals is crucial to
Lactate (mmol/l) n = 24 n = 22 understanding various aspects of a population’s biology and
17.08 17.04 health (Innis, 2014) and can be especially important in evalu-
ating the cause of morbidity events and population declines.
(2.06) (2.62)
13.6–22.2 8.8–21.1 Morphometrics can be helpful in evaluating cases of disease
or environmental stress, as optimal body condition can be cal-
Total protein (mg/dl) n = 22 n = 21 culated using body weight and size (Donoghue, 2006; Lazić
8.10 8.77 et al., 2013). Similarly, the typical ranges of body temperatures
and heart rates of a species are critical metrics useful to veterin-
(1.06) (2.07)
ary professionals during medical interventions (e.g. anaesthesia
5–10.2 5–12 and surgery). These parameters are known to vary with hand-
Haemoglobin (g/l) n = 22 n=9 ling stress in reptiles (e.g. Murray, 2006), so the values reported
here should be used only as approximations.
12.14 10.26
(1.65) (1.33) The measurement of biochemical and haematological
parameters can serve as a valuable tool for evaluating and
8.5–14.3 7.8–12.2
monitoring the health of wild reptile populations (Stacy et al.,
(Continued) 2011; Campbell, 2014). To determine the significance of
..............................................................................................................................................................
Figure 2: Haematocrit, haemoglobin and glucose box plots for males and females of the San Cristobal lava lizard (M. bivittatus). Significant
differences were found between sexes. Haematocrit (P = 0.009), haemoglobin (P = 0.005), glucose (P = 0.011).
Eosinophil (%) 1.08 0.32 For lactate values, we found higher levels than reported
(1.58) (0.65)
by González-Morales et al. (2015) in Sceloporus torquatus,
González-Morales et al. (2017) in S. grammicus, and
0–6 0–2 Lewbart et al. (2015) for marine iguanas (Amblyrhynchus
Basophil (%) 0.64 0.54 cristatus). Very few studies have reported lactate levels in
squamate reptiles (Lewbart et al., 2015; González-Morales
(1.22) (1.22)
et al., 2015, 2017), and most evaluated lactate production
0–5 0–5 after exercise in diving reptiles (Bartholomew et al., 1976;
Values represent means, standard deviation (parenthesis) and range (minimum– Seymour, 1979; Harms et al., 2003; Warren and Jackson,
maximum). 2008). In squamates, blood lactate levels may be affected by
altitude (González-Morales et al., 2015, 2017), exercise
changes in biochemical and haematological values associated (Bennett et al., 1981; Gleeson and Dalessio, 1989; Schuett
with factors such as disease, injury, pollutants or starvation, and Grober, 2000) and handling (Lewbart et al., 2015).
it is essential to establish species-specific (or at least taxon- Lactate levels may also be influenced by glucose and oxygen
..............................................................................................................................................................
Figure 3: Photographs of selected San Cristóbal lava lizard (Microlophus bivittatus) blood cells stained with Diff-Quick stain at 100×.
(a) Heterophil. (b) Monocyte. (c) The black arrow indicates an eosinophil and the red arrow indicates a lymphocyte. (d) Intraerythrocytic
haemoparasite.
levels (Gleeson and Dalessio, 1989; Bennett, 1973), but greater in women as a result of higher glucose disposal by
apparently there is little dependence on body temperature skeletal muscles (Mauvais-Jarvis, 2017). The mechanisms for
(Bennett and Litch, 1972). In mammal medicine, hyperlacta- facilitated glucose homoeostasis are unclear, but could be
temia usually correlates with disease severity and mortality due at least in part to the effect of circulating oestrogen
(Gillespie et al., 2016) and with capture myopathy and mus- (Mauvais-Jarvis, 2017). Although a similar process may
cle damage in birds (Burgdorf-Moisuk et al., 2012). Little is explain our findings in Microlophus, it is important to note
known, however, about its clinical use in reptile medicine that Dickinson et al. (2002) found that male tortoises had
and further study is needed. higher glucose levels than females, raising questions about
whether such patterns are conserved across amniotes.
Glucose levels can vary in reptiles depending on nutri-
tional or environmental conditions (Campbell, 2014). In M. Blood cell counts and morphology can vary greatly
bivittatus glucose was significantly lower in females than among species of reptile, even among members of the same
males. Such sex-based variation was not identified in a study genus (Stacy et al., 2011; Innis, 2014). In addition, numerous
of the agamid genus Calotes (Chandavar and Naik, 2012), factors, including age, sex, environment, season, presence of
and the prevalence of this pattern in other lizard families, environmental stressors, parasite load, nutritional state and
including Tropiduridae, is unknown. Because glucose meta- restraint, can complicate the evaluation of haematological
bolism in reptiles is similar to that in mammals, a known dif- data in reptiles (Campbell, 2014). Therefore, published refer-
ference between human sexes may provide insight (Anish ence intervals provide only a baseline for interpretation, and
et al., 2013; Mauvais-Jarvis, 2017). Compared to men of the veterinarians need to be aware of these factors to accurately
same age, healthy women have lower skeletal muscle mass interpret and correlate haematological and clinical findings
and higher adipose tissue mass, more circulating free fatty in reptile patients (Stacy et al., 2011).
acids, and higher intramyocellular lipid content, all of which
might promote insulin resistance in women relative to men Cellular morphology of M. bivittatus is similar to that reported
(Mauvais-Jarvis, 2017). In addition, insulin sensitivity is in the closely related families Iguanidae, Corytophanidae, and
..............................................................................................................................................................
Liolaemidae. As in other lizards that have been studied [e.g. Microlophus lava lizards, a small and interesting group of
Cyclura nubila, (Alberts et al., 1998); Amblyrhynchus cristatus reptiles in the Galápagos. Because there are several closely
(Lewbart et al., 2015); Salvator (Tupinambis) merianae (Troiano related species on various islands in the Archipelago, future
et al., 2008); Pogona vitticeps (Ellman, 1997)], the highest leuco- studies should determine the extent to which the parameters
cyte population was the lymphocytes. measured here vary across species.
One caveat about our study is that the iSTAT unit used to Bartholomew GA, Bennett AF, Dawson WR (1976) Swimming, diving
analyse blood chemistry was designed as a fast and efficient and lactate production of the marine iguana, Amblyrhynchus crista-
way to determine blood gas and chemistry parameters in tus. Copeia 1976: 709–720.
humans. For this reason, future work should involve corrob- Benavides E, Baum R, Snell HM, Snell HL, Sites JW Jr (2009) Island bio-
orating these results with methods that are more commonly geography of Galápagos lava lizards (Tropiduridae: Microlophus):
used for reptile work in veterinary laboratories (Steinmetz species diversity and colonization of the archipelago. Evolution 63:
et al., 2007; Harter et al., 2015), which was impractical in 1606–1626.
our study due to export constraints and logistical challenges.
Bennett AF (1973) Blood physiology and oxygen transport during
In sum, our study represents an initial step toward produ- activity in two lizards, Varanus gouldii and Sauromalus hispidus.
cing a foundation for future health assessment work on Comp Biochem Physiol A Physiol 46: 673–690.
..............................................................................................................................................................
Bennett AF, Licht P (1972) Anaerobic metabolism during activity in Ellman MM (1997) Hematology and plasma chemistry of the inland
lizards. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 81: bearded dragon, Pogona vitticeps. Bull Assoc Reptile Amphib
277–288. Veterinarians 7: 10–12.
Bennett AF, Gleeson TT, Gorman GC (1981) Anaerobic metabolism in Gillespie Í, Rosenstein PG, Hughes D (2016) Update: clinical use of
a lizard (Anolis bonairensis) under natural conditions. Physiol Zool plasma lactate. Vet Clin: Small Anim Pract 47: 325–342.
54: 237–241.
Gleeson TT, Dalessio PM (1989) Lactate and glycogen metabolism in
́
Berriozabal-Islas C, Badillo-Saldañ a IM, Ramirez-Bautista A, Moreno CE the lizard Dipsosaurus dorsalis following exhaustive exercise. J Exp
(2017) Effects of habitat disturbance on lizard functional diversity Biol 144: 377–393.
in a tropical dry forest of the Pacific coast of Mexico. Trop Conserv
González-Morales JC, Quintana E, Díaz-Albiter H, Guevara-Fiore P,
Sci 10: 1–11.
Fajardo V (2015) Is erythrocyte size a strategy to avoid hypoxia in
Burgdorf-Moisuk A, Wack R, Ziccardi M, Larsen RS, Hopper K (2012) Wiegmann’s torquate lizards (Sceloporus torquatus)? Field evi-
Validation of lactate measurement in American flamingo dence. Can J Zool 93: 377–382.
(Phoenicopterus ruber) plasma and correlation with duration and
González-Morales JC, Beamonte-Barrientos R, Bastiaans E, Guevara-
difficulty of capture. J Zoo Wildl Med 43: 450–458.
Fiore P, Quintana E, Fajardo V (2017) A Mountain or a Plateau?
Calle P, Rodríguez J, Matamoros Y. (Eds.) With the collaboration of: Hematological traits vary nonlinearly with altitude in a highland
Cunningham A, Travis D, Rideout B, Jiménez G, Sutherland-Smith lizard. Physiol Biochem Zool 90: 638–645.
M, Ponder J, Nieto A, Huyvaert K, Dary L, Lewbart G, et al. (2017)
Harms CA, Mallo KM, Ross PM, Segars AL (2003) Venous blood gases
Workshop to develop a Wildlife Health Plan for the Galápagos
and lactates of wild loggerhead sea turtles (Caretta caretta) follow-
Islands. Wildlife Conservation Society (WCS). http://www.wcs.org
ing two capture techniques. J Wildl Dis 39: 366–374.
(last accessed July 2018).
Harr KE, Alleman AR, Dennis PM, Maxwell LK, Lock BA, Bennett RA,
Campbell TW (2014) Clinical pathology. In Mader DR, Divers SJ, eds.
Jacobson ER (2001) Morphologic and cytochemical characteristics
Current Therapy in Reptile Medicine and Surgery. Iowa State
of blood cells and hematologic and plasma biochemical reference
University Press, Elsevier, Canada, pp 70–92.
ranges in green iguanas. J Am Vet Med Assoc 218: 915–921.
Carrión Avilés PL (2012) Depredación de gatos domésticos y ferales
Harter TS, Morrison PR, Mandelman JW, Rummer JL, Farrell AP, Brill
sobre las lagartijas de lava de San Cristóbal (Microlophus bivittatus),
RW, Brauner CJ (2015) Validation of the i-STAT system for the ana-
Galápagos. Bachelor’s thesis. USFQ, Quito.
lysis of blood gases and acid–base status in juvenile sandbar shark
Carrion PL, Valle CA (2018) The diet of introduced cats on San (Carcharhinus plumbeus). Conserv Physiol 3: cov002. doi:10.1093/
Cristobal Island, Galapagos: cat feces as a proxy for cat predation. conphys/cov002.
Mammalian Biol 90: 74–77. He J, Xiu M, Tang X, Yue F, Wang N, Yang S, Chen Q (2013) The differ-
Chandavar VR, Naik PR (2012) The endocrine pancreas of the lizard ent mechanisms of hypoxic acclimatization and adaptation in liz-
Calotes versicolor: an immunocytochemical and physiological study ard Phrynocephalus vlangalii living on Qinghai‐Tibet Plateau. J Exp
with respect to its reproductive cycle. J Cytol Histol 3: 143. Zoolog A Ecol Genet Physiol 319: 117–123.
Dallwig RK, Paul-Murphy J, Thomas C, Medlin S, Vaughan C, Sullivan L, Innis CJ (2014) Conservation issues. In Mader DR, Divers SJ, eds.
Herrera G (2011) Hematology and clinical chemistry values of free- Current Therapy in Reptile Medicine and Surgery. Iowa State
ranging basilisk lizards (Basiliscus plumifrons) in Costa Rica. J Zoo University Press, pp 296–303.
Wildl Med 42: 205–213. James SB, Iverson J, Greco V, Raphael BL (2006) Health assessment of
Dennis PM, Bennett RA, Harr KE, Lock BA (2001) Plasma concentration Allen Cays rock iguana, Cyclura cychlura inornata. J Herpetol Med
of ionized calcium in healthy iguanas. J Am Vet Med Assoc 219: Surg 16: 93–8.
326–328. Jiménez-Uzcátegui G, Márquez C, Snell HL (2017) CDF Checklist of
Dickinson VM, Jarchow JL, Trueblood MH (2002) Hematology and Galápagos Reptiles—FCD Lista de especies de Reptiles Galápagos.
plasma biochemistry reference range values for free-ranging des- In Bungartz F, Herrera H, Jaramillo P, Tirado N, Jiménez-Uzcátegui
ert tortoises in Arizona. J Wildl Dis 38: 143–153. G, Ruiz D, Guézou A, Ziemmeck F, eds. Charles Darwin Foundation
Galapagos Species Checklist—Lista de Especies de Galápagos de la
Divers SJ, Redmayne G, Aves EK (1996) Haematological and biochemical Fundación Charles Darwin. Charles Darwin Foundation/Fundación
values of 10 green iguanas (Iguana iguana). Vet Rec 138: 203–204. Charles Darwin. Puerto Ayora, Galapagos. http://darwinfoundation.
Donoghue S (2006) Nutrition. In Mader DR, ed. Reptile Medicine and org/datazone/checklists/vertebrates/reptilia/ (last accessed 30
Surgery, Ed 2. Elsevier, Canada, pp 251–298. August 2017).
Dunlap KD (2006) Ontogeny and scaling of hematocrit and blood vis- Keogh JS, Noble DWA, Wilson EE, Whiting MJ (2012) Activity predicts male
cosity in Western Fence Lizards, Sceloporus occidentalis. Copeia reproductive success in a polygynous lizard. PLoS One 7, doi:http://dx.
2006: 535–538. doi.org.libproxy.lib.unc.edu/10.1371/journal.pone.0038856.
..............................................................................................................................................................
Lazić MM, Kaliontzopoulou A, Carretero MA, Crnobrnja-Isailović J Scorza JV (1971) Some haematological observations on Tropidurus
(2013) Lizards from urban areas are more asymmetric: using fluctu- torquatus (Sauria, Iguanidae) from Venezuela. J Zool 165:
ating asymmetry to evaluate environmental disturbance. PLoS One 557–561.
8: e84190. doi:10.1371/journal.pone.0084190.
Schuett GW, Grober MS (2000) Post-fight levels of plasma lactate and
Lewbart GA, Hirschfeld M, Brothers JR, Muñoz-Pérez JP, Denkinger J, corticosterone in male copperheads, Agkistrodon contortrix
Vinueza L, Lohmann KJ (2015) Blood gases, biochemistry and (Serpentes, Viperidae): differences between winners and losers.
haematology of Galápagos marine iguanas (Amblyrhynchus crista- Physiol Behav 71: 335–341.
tus). Conserv Physiol 3: cov034. doi: 10.1093/conphys/cov034.
Stacy NI, Alleman AR, Sayler KA (2011) Diagnostic hematology of rep-
Maia JP, Harris DJ, Carranza S, Gómez-Díaz E (2014) A comparison of tiles. Clin Lab Med 31: 87–108.
multiple methods for estimating parasitemia of hemogregarine
Steinmetz HW, Vogt R, Kästner S, Riond B, Hatt JM (2007) Evaluation
hemoparasites (Apicomplexa: Adeleorina) and its application for
of the i-STAT portable clinical analyzer in chickens (Gallus gallus).
studying infection in natural populations. PLoS One 9: e95010.
J Vet Diagn Invest 19: 382–388.
doi:10.1371/journal.pone.0095010.
Troiano JC, Gould EG, Gould I (2008) Hematological reference intervals
Maria R, Ramer J, Reichard T, Tolson PJ, Christopher MM (2007)
in argentine lizard Tupinambis merianae (Sauria—Teiidae). Comp
Biochemical reference intervals and intestinal microflora of free-
Clin Pathol 17: 93.
ranging Ricord’s iguanas (Cyclura ricordii). J Zoo Wildl Med 38: 414–419.
Troya-Zuleta MA (2012) Genética poblacional de la lagartija de lava
Márquez C, Cisneros-Heredia DF (2016) Microlophus bivittatus. The
endémica (Microlophus bivittatus) de la Isla San Cristóbal e islote Lobos,
IUCN Red List of Threatened Species 2016.
Galapagos-Ecuador, mediante microsatélites como parte de la línea
Mauvais-Jarvis F (2017) Gender differences in glucose homeostasis base para su manejo y conservación. Bachelor’s thesis. USFQ, Quito.
and diabetes. Physiol Behav 187: 20–23.
Wagner RA, Wetzel R (1999) Tissue and plasma enzyme activities in
Murray M (2006) Cardiopulmonary anatomy and physiology. In Mader DR, juvenile green iguanas. Am J Vet Res 60: 201–203.
ed. Reptile Medicine and Surgery, Ed 2. Elsevier Canada, pp 124–134.
Warren DE, Jackson DC (2008) Lactate metabolism in anoxic turtles:
Pasek KM, Collver ME (2001) Technique for temporarily marking an integrative review. J Comp Physiol B 178: 133–148.
lizards that does not require capture. Herpetol Rev 32: 30.
Williams TD, Challenger WO, Christians JK, Evanson M, Love O, Vezina F
Seymour RS (1979) Blood lactate in free-diving sea snakes. Copeia (2004) What causes the decrease in haematocrit during egg produc-
1979: 494–497. tion? Funct Ecol 18: 330–336.
..............................................................................................................................................................