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YASMIN AKHTAR
BY
Supervisors Certificate
This is to certify that Ph.D student for the session 2005-2007 of Jinnah
University For Women; Ms.Yasmin Akhtar has completed her research
dissertation under my supervision for fulfillment of the requirement for the
degree of Ph.D. This is original work carried out by the candidate. The title of
dissertation is FEEDING HABITS AND NEMATODE PARASITES OF
SOME FISHES OF KARACHI COAST PAKISTAN.
Research supervisor
Prof.Dr.Bilqees Mujib
Ph.D (Can), Sc.D (USA), D.Sc
TABLE OF CONTENTS
Pages
ACKNOWLEDGEMENT---------------------------------
SUMMARY------------------------------------------ ii
CHAPTER 1
INTRODUCTION
1.1: Importance of Fishes----------------------------------
11
12
CHAPTER-2
REVIEW OF LITERATURE
2.1: Comprehensive account of feeding habits of fishes-- 21
CHAPTER-3
MATERIAL AND METHOD
3.1: Study Area----------------------------------------
31
31
32
32
33
33
34
35
35
CHAPTER-4
RESULTS AND DESCRIPTIONS
FEEDING HABITS-----------------------------------
36
39
46
51
52
4.8
CHAPTER-5
DESCRIPTIONS OF NEMATODES
5.1: History of the genus Dujardinascaris
Baylis,1947--------------------------------------------
77
79
81
109
121
132
134
137
138
143
156
157
163
CHAPTER-6
HISTOPATHOLOGY--------------------------------
165
165
166
167
168
6.5: Remarks------------------------------------------------
169
174
CHAPTER-7
DISCUSSION
7.1: Dietary habits of fishes---------------------
179
181
182
185
186
FUTURE PERSPECTIVE-------------------
190
CHAPTER-8
REFERENCES-----------------------------
LIST OF PUBLICATIONS-----------------
191
237
ACKNOWLEDGEMENT
I am grateful to the Vice Chancellor, Prof. Dr. Riaz Ahmed Hashmi, Jinnah
University for Women for providing financial support, working facilities and
kind suggestion at every step of this work.
I do here by acknowledge the fact that great help and guidance was provide to me
by my research supervisor Prof.Dr.Bilqees Mujib who was kind to me, at every
stage of the preparation of this dissertation. She has given guidance to me. I
deeply feel indebted to her efforts and contributions. With out her efforts and
help, such a piece of research work would not be possible.
My thankful acknowledgement is due to Prof. Dr. Rafia Azmat, Department of
Chemistry for fruitfull discussion, comments, suggestion and help in the
statistical analysis of data with all cooperation in finalizing the current thesis.
I am thankful to the heads and the staff of the department of Botany and
department of Zoology for helping me, to reconcile my study and work.
Similarly, I would like to appreciate research officer Ms. Rehmat Bibi for her
skilled assistance in the laboratory. I am also thankful to Mr. Yousaf, research
technical officer for his assistance in the Steroscan Micrographs in Centralized
laboratory of university of Karachi.
I am also thankful to Rupert Lee from the Natural History Museum in London
and Dr. Franick Moravec from institute of Parasitology, Czech Republic
Budejovice kindly provided literature for study.
My sincerest thanks are due to my husband and my children for all the joy of life
they have given and for their moral support.
ii
SUMMARY
Pakistan has two main fishing areas: Karachi and Sindh, extending southeast
from Karachi to the Indian border (about 180 miles) and the Mekran coast, west
of Karachi and along the coast of Baluchistan to the Iranian border (about 350
miles). The former area with Karachi harbor as its main base, is characterized
by a broad continental shelf (extending about 60 nautical miles out from the
coast to a depth of 200m), a coast line marked by innumerable small creeks and
the Delta of the Indus River, and by muddy, easily trawlable bottom. The
tropical and envoirmental conditions are generally tropical and subject to
monsoon during the summer to Autum. Upwelling of cold, nutrient-rich, lowoxygen water occurs all year round but is stronger during the Southwest
monsoon period.
.
As a group bony fishes can eat all sizes of plants and animals from smallest of
microscopic plant planktons to some largest marine animals. Several illnesses
are the result of planktonic toxic blooms. The amount of food, a bony fish eats
is directly related to its size, metabolic stages and temperature of its
environment.
The fish provide nutritive diet for the human beings. To get perfect nutrition
it is necessary that fishes must be healthy and free from parasitic and other
diseases. For the prevention of disease it is important to study the cause and
nature of disease in fish. Parasites are important group of pathogen, which
occurs at various stages of development in fish.
Fishes are the intermediate host for nematode parasites. Nematodes or round
worms are extremely diverse and successful group of invertebrate animals,
iii
belonged
to
genera,
including
Cucullanus
One new genus and new species was identified and described as Spirocotyle
otolithi (Camallanidae Railliet and Henry,1915) from Otolithus ruber.
ii)
Seven other new species were identified and described here of the genus
Dujardinascaris (Baylis, 1947) including, Dujardinascaris mujibi n.sp. from
Sphyraena forsteri; D. jello n.sp. from Sphyraena jello; D. maculatum n.sp.
vi
P.(S)
ruberii n.sp. from Otolithus ruber were also identified and described. Two
female specimens from Otolithus ruber were also reported. Species was not
designated, as male specimens were not available.
iv)
One new species of the genus Cucullanus Muller, 1777 was identified and
described here as C. alliyai n.sp. from Otolithus ruber
Tissue damage associated with nematode infection was also studied in
two fish species. Observations were made on the tissue sections of some
parts of infected intestine of Euthynnus alletteratus and
Pomadasys
vii
INTRODUCTION
chiefly of cod, haddock and hake are used. In Russia parts of sturgeon and
other fishes are used in making of certain glass and diamond cements (Russell
and Yonge, 1936). In countries where mosquitoes are abundant including
Pakistan, India, Sri Lanka, Bangladesh, Saudi Arabia, Nigeria fish can be used
as biological control agent for mosquitoes (WHO, 1981).
Fish flour for human consumption is manufactured from sharks and other
elasmobranchs fishes in Pakistan, while in India and other developing countries
shark is used for fish flour for livestock. This fish flour is useful for fortification
of cereal foods containing 85% high protein. The researches are based to
explore and examine the natural wealth of fish and shrimp, to develop most
economical and effective products and technologies for utilization of natural
resources, including import substitution and export promotion.
The major component of fish is protein. Fish proteins have a high biological
value. It contains variable quantities of calcium, phosphate, fate and other
nutrient important for human health and growth. Fish provides the worlds
prime source of high quality protein, 14-16% of the animal protein consumed
world wide; over one billion people rely on fish as their primary source of
animal protein. There is a considerable scope for aquaculture in Pakistan to
supplement the protein obtained from the livestock resources, a meager
attention has been given in past on these valuable resources and if efforts are
made Pakistan fish industries can become one of the most outstanding in the
world as we have a large part of the ocean It is only possible if lot of
investment is made and knowledge is gained about the economic importance
of fish, their life history, habitats, physiology, diseases and their control.
2
As mentioned previously Pakistan has two main fishing areas: Karachi to Sind,
extending south east from Karachi to the Indian boarder (about 180 miles) and
the Mekran coast, west of Karachi and along the coast of Baluchistan to the
Iranian boarder (about 350 miles). The former area with Karachi harbour as its
main base is characterized by a broad continental shelf (extending about 60
nautical miles out from the coast to a depth of 200m). Marine fishing is
undertaken fromright beyond the coast to 200 nautical miles in to the sea. The
distance has been divided into two broad categories for fishing known as: (1)
Coastal water fishing and (2) Deep-sea water fishing. The distance specified are
up to 12 nautical miles termed as coastal water fishing. Coastal water fishing is
done in the villages along the coast that are predominately inhabited by
fisherman whose main live hood is fishing. While the Deep Sea is further
divided into two Zones. Zone 1 is from 12-35 nautical miles and Zone 11 is
from 35-200 nautical miles. Major share of marine catch is within 12 nautical
miles
from
the
coast
(Pakissan.com.2001-2008).
The
tropical
and
contributing towards national economic growth and progress. Coastal zones are
capable of producing rich fisheries, minerals, oil and gas resources. The
importance of developing marine resources has not been fully perceived.
Pakistan interest requires an investment in ocean research to contribute towards
the national economy, conduct fundamental and applied research, lay claim on
its territorial and offshore boundaries.
The sea water of the coast of Sindh and Balochistan has the potential to
provide sea food to as many as twice the present population of Pakistan but
hardly more than 2% of the potential wealth is exploited (Syed, 1985).The
statistical data on actual fish production from the tropical oceans is very
unreliable and difficult to calculate. The tropical oceans include almost 50%
of the total area of all open waters and 30% of the total area of continental
shelf however its reported production does not exceed 16% of the global fish
production. Life in warm tropical areas develops faster with early and
reproductive capabilities and its high diversity enable to occupy every niche
and the whole ecosystem appears a huge aggregation of species complex
(Hussain, 2003).
Pakistan marine recreational commercial fisheries exploit a large numberof
coastal fish species. Out of 760 species of fishes belonging to 164 families and
370 genera recorded from the coast of Pakistan, about 114 species are of the
commercial importance; marine fisheries production reached a peak at 2,78,149
metric tons in 1982 (Hoda, 1985; Majid et al., 1992). In 1999, the total marine
fish production was 1,82,995 metric tons, in which 1,64,450 metric tons have
been locally consumed while 18545 metric tons have been exported. In 1999,
out of the total locally consumed fish production, 70.18% was utilized for
5
human consumption. The share marketed as fresh, frozen, canned and cured
was 45.86% 11.42%, 0.00% and 7.37% respectively, where as 5.53% for
subsistence. Out of total export of fish and fishery products in 1998, the
percentage of fish, shellfish and fishery products was 62.5%, 35.1% and 2.4%
respectively. In 1999, an increase in quantity was registered i.e. 90,384 metric
tons and in value Rs. 7.02 billions. This showed an increase of 26.9% in
quantity and 18.6% in value over proceeding year. The export mainly composed
of frozen fish, frozen shrimps, lobsters, crabs, dried fish and mollusks. Among
the fish products only small quantity of fish meal was exported. In 2001, total
world production of fisheries was reported to be 130.2 million tons, of which
37.9 million tons was from aquaculture practices and 92.3 million tons from
captured fisheries production. China was the leading producer with 42.6 million
tons. In parallel with the increase in production, international trade has
continued to grow, and at an accelerating rate in recent years. In 2001, more
than 80% of the total world import value was concentrated in developed
countries, in particular in Japan, the USA and in several other countries. Japan
was the major importer accounting for about 23% of total import value. USA
was the second main importer with a share of 17%, followed by Spain, France,
Italy, Germany and the UK. (Source: FAO). According to the Food and
Agriculture Organization (FAO), the world harvest in 2005 consisted of 93.3
million captured by commercial fishing in wild fisheries, plus 48.1 million
tones produced by fish farm. I addition, 1.3 million tons of aquatic
plants(seaweeds etc) were captured in wild fisheries.
Pakistans exports of fishery products stand at about 0.25% of world exports.
Pakistans domestic consumption is termed as one of the lowest in the world, at
1.6 kg per person per year (compared to world average of 16.2 kg per person per
6
year). By adopting modern techniques of fishing, Pakistan can exploit the huge
opportunity that exits in the fisheries sectors (2001-2007 Pakissan.com.).
productivity is in the form of tiny plankton, which are the lowest link in oceans
food chain. (Najjar www.eesi.psu.edu/news_events/archives/ Monsoons.shtml ).
There is a considerable scope for aquaculture in Pakistan to supplement the
protein obtained from the livestock resources, a meager attention has been
given in past on these valuable resources and if efforts are made Pakistan fish
industries can become one of the most outstanding in the world as we have a
large part of the ocean It is only possible if lot of investment is made and more
and more knowledge is gained about the economic importance of fish, their life
history, habitat, physiology, diseases and their control. The high commercial
value of food fishes which are mainly marine, has led to a great impact on
research over the last hundred of years. Fishery biologists are much interested
in the growth because obviously it is a major component of fishery that is used
to calculate yields at different level.
trenches. Further, there are a great many parasitic forms, including in most
plants, animals and humans.
Nematodes are by nature aquatic organisms. Recent observations indicatethat
various nematode species respond differently to degradation of environmental
quality thus the degree of nature of change in the community structure of
aquatic nematodes may be an excellent indicator of water quality or pollutant
levels. Most fish nematodes are oviparous and their eggs, which may or may
not be embryonated, are passed with the feaces of the host. The eggs hatch to
release a free swimming larva which must be ingested by crustacean or other
invertebrates as first intermediate host and a fish as second intermediate host
and bird or mammal as the definitive host, depending on the genus or species
concerned.
11
Fish diseses are important from two points of view: Parasites from fishes can
affect fishes, or can affect human. In the first case, some parasites affect only
12
fishes, making them not avaliable for human consumption, or diminishing the
size of the fish, being not atractive for commercial purpose. In the second
case, parasites present in fishes can affect human, provoking diseases,
including death.The diseases of marine animals or fishes are as old as the
animal life in the seas. Early reports on disease of aquatic animals include the
fish diseases especially of helminth infection, (Cheng, 1964). Kinne, (1980)
has given a bibliography on parasites and disease of fish. At that time the
scientific studies on fish disease remained largely unexploited but recently
fish diseases are one of the important problems and great attention is being
paid to get more and more information about it.Many parasites are host specific
to at least some extent and are capable of infecting one or only a limited
number of host species. Individual
and number of parasites vary seasonally, geography and with age of the host.
He observed that differential mortality may also vary seasonally or with age of
the host. Parasites cause damage to various organs of fish. Their host affecting
the yield of fish products such as liver oil etc. a large number of nematodes live
as internal parasites in fish, one such example is Cucullanus elegans (Zedar,
1917) the larvae of which live in Cyclops.The adults inhabit intestine or eyes.
Most of the nematodes of family Camallanidae occur in swim bladder.
Glandular secretion and metabolites of parasites may be toxic for the fish
resulting in weight losses, ill growth and inhibition of fertilization in hosts.
Parasites produce protiolytic enzymes, which are so strong that liquefy the
effective muscles. A strong invasion of gut nematodes may destroy the intestine
partially or wholly, as a consequence, the intestine stiffens, its peristaltic
movements slow down and digestion is hampered. The severity of disease in
fish will vary depending upon the life stage, species and number of nematodes
present; the age and species of infected fish; and the site of infection. Visible
signs of infection may include hemorrhaging, cyst formation, external lumps or
nodules, inflammation and necrosis.
Adult nematodes in the intestinal tract damage its lining and robe the fish and
effect their development. Robert et al.,(1995) studied the Phylogeny, Ecology
and Richness of parasites in vertebrates. Many species of nematodes migrate
within the body of the fish causing worm tracts which are seen in the form of
tunnels in the tissues. Extensive migration by large number of nematodes may
cause significant physical damage to a fish. Juvenile fish with nematode
infection are often more severely infected than adults, displaying reduced
growth, wasting or more obvious disease symptoms and mortality.The larval
14
nematodes are present almost in every organs of the host. Most adults inhabit
the intestinal tract. Anisakis (Nematode) is easily penetrated in to stomach of
fishes, including Hilsa ilisha and Cybium guttatum (Bilqees &Fatima, 1993;
Bilqees &Parveen, 1996).
From the viewpoint of fish as food, fish diseases are important for two main
reasons: (a) the number of fish available for consumption is reduced (b) the
disease fish may look unsightly, both these making unacceptable for human
consumption. The fish disease may be due to parasite or non-parasitic causes,
the former being the most numerous and from both pathological and economic
viewpoint, the most important. Many parasites are host specific to at least some
extent and are capable of infecting one or only a limited number of host species.
Individual parasites may have widely differing effect on different host species.
There is no doubt that every parasite which live internally or externally in fish,
exert some harmful influence on the basic phenomena of life of their hosts,
specially life span, life cycle, abundance, distribution, metabolic performance,
nutritional requirements, growth, reproduction, evolution as well as organisms
tolerances to natural and man made environmental stress( Kinne, 1980 ). There
is a usual concept that extensive mortality in the natural environment occurs
from the infestation of larger parasites, such as trematodes, acanthocephala,
nematodes which are common in fish. In crowded hatchery conditions,
infestation of these larger parasites may often cause death.
Nematodes infect many different species of aquaculture and wild fishes.
Nematodes are found in all the body parts of fish either as larvae oradults. The
diseases due to the adult and larval nematodes are very common in marine
fishes and worldwide in distribution. The organs commonly infected are
15
intestine, liver and body cavity. While other organs involved are heart, kidney,
spleen, reproductive organs eyes and gills. Nematodes especially larvae may
cause blockage of organs. This is caused when the worms are in great quantity.
If these are present in the capillaries of the gills, they block or obstruct the
capillaries, fish become unable to respire and die. Most species of the
nematodes in adult stage live in the alimentary canal except the family
Philometridae which are found in body cavity, liver and gonads. A number of
genera of the family Anisakidae occur in the digestive tracts of marine fish.
They live free in the lumen of the stomach or intestine; some attach to or invade
the wall of these organs and cause local tissue damage. Pathogenesis is a result
of their modes of feeding, attachment and movement or migration within the
host. Sea foods are the principal sources of human infections with these larval
worms. The disease is transmitted by raw, undercooked or insufficiently frozen
fish and shellfish.
Some parasites from fishes are important because of the human become
infected during the consumption of edible fishes. Anisakis simplex,
Contracaecum sp., and Hysterothylacium sp. are anisakid nematodes that have
been implicated in human infections caused by the consumption of raw or
undercooked seafood. Asami et al., (1965) discussed two cases of stomach
granulae by Anisakis-like larvae The adults of the nematode parasite
Gnathostoma spinigerum (Bashirullah, 1972) are normally found in the
stomach of felids, raccoons, dogs. The first intermediate host is cyclopoid
copepods, and the second intermediate host is a fresh water fish. If human
consume fresh water fishes infected with G. spinigerum, the larva migrate
throughout the intestine to muscles and skin, causing the 'larval migrans '
syndrome. The nematode Dioctophyma renale (Goeze, 1782) is found as an
16
adult in the kidney of wild carnivores and has been recorded from man (Myers,
1970). Normally the lifecycle involves only an oligochaete annelid intermediate
host but if a fish eats an infected annelid the larval nematode may penetrate into
the visceral cavity and encysts there. Larvae have been found in pike in the
Russia (Karmanova, 1961) and bullhead in North America (Mace & Anderson,
1975). Ruben et al.,(2001) also studied human infection by Pseudoterranova
decipiens in Chile. In the Far East and pacific areas, both freshwater and marine
fish can act as paratenic hosts for the parasite although the normal intermediate
host is a molluse (Sindermann, 1970).
Study of the fish disease is one of the important problems because it has an
indirect and some times direct effect on the productivity of fish and on human
health. Previously no attention has been paid for the study of larval nematodes
in the fishes in Pakistan in spite of their importance as one of the fish disease
agents and causative agents of gastric problem in man. Considering the parasitic
problems in the fish, it is necessary to conduct different studies on aspect of
biology related to nutritional values and parasitic infections to help the
production of worm free fish in our country.
Among fresh water and marine fishes, the marine fishes face much more
danger. Most of marine fishes are included among the group of edible fishes.
Some of these including, Scomberomorus
Sphyraena
edible fishes in Pakistan, due to their delicious taste and are full of nourishment
such as proteins and vitamins particularly vitamin E and vitamin D. A lot of
work has been reported on the diagnosis, description and analysis of the
17
18
reveals that a lot of work has been carried out by many researchers separately
on dietary habits, nematode parasites and histopathology of marine edible
fishes, but the relation in between these three major parameters has not been
established yet. Therefore the study is focused on relationship in between these
three parameters.
1: The first objective of this work is focused on food and feeding habits of
marine edible fishes with the aim of determining the dietary requirements,
categorizing them as herbivorous, carnivorous, Omnivorous and detritivorous.
This will give help in seasonal Variations of dietary habits and will support the
aquaculturing. Studies based on literature from varying habitat, have showed
that the stomach content analysis is widely used in fish diversity. A survey is
conducted for the marine fish diversity of Karachi coast, Pakistan.
2: As stated by Sasal et al., (1999) the diet of the host species is the main factor
affecting parasite community structure. The second objective of the present
work is to study the taxonomy of the nematode parasites and their prevalence
and intensity in marine fishes. Helminths are the part of stomach contents but
according to Siglar, (1958) they might have been swallowed along with the
miscellaneous items in fishes. According to these statements, a relationship will
be found between dietary habits and nematode parasites.
19
20
2: REVIEW OF LITERATURE
2.1 Comprehensive account of feeding habits of fishes
Most studies of food and feeding habits of fishes, from varying habitats, have
showed that those of any one species differ in time and space and at different stage
of growth, thereby, emphasizing the need to study in more detail the food habits of
a species (Staples, 1975). The study of dietary habits of fish, based on stomach
content analysis, is widely used in fish ecology as an important means of
investigating tropic relationship in the aquatic communities (Fagbenro et al.,
2000).
Fish have wide range of food and feeding habits such as herbivores, pisnivorous,
omnivorous, carnivorous, detritivorous and have diverse ecological diversity.
Information on food and feeding habits of fishes facilitates understanding of their
feeding adaptation, growth, fecundity, migration and other related aspects.
Comprehensive account of food and feeding habits of marine fishes have been
published by several workers. (Todd, 1914; Suyehiro, 1934; 1942; Quershi, 1945;
Kuthlingum, 1957; Pradhan, 1959; Natarjan and Jhingram, 1961; Keast, 1968;
Suselam and Nair, 1969; Braber and Degroot, 1973; Hamellin and Bouchon, 1976;
Hyslope, 1980; Ghandi, 1982; Data & Das, 1983; Mohan, 1985;
Hoda, 1991;
Khan & Hoda,1993; Yamamura et al, 1993; Hussain & Abbas, 1995; Poulin, 1995;
Schulz & Schoonbii, 1999; Fagbenro et al., 2000; Fugi et al., 1996; Hailu, 2001;
Katsuhiro and Mahyam, 2003;
Seven et al.,2003;
Gregory, 2005; Takeuchi et al., 2005; Campo and Mostarda et al., 2006; Balik et
al., 2006; Bhuiyan et al.,2006; Mostarda et al., 2007; Laurent et al., 2007;
Ayotunde et al., 2007).
21
Annereaux,1946; Karve & Naik, 1951; Ali, 1960; Dogiel et al., 1961;
1962;Yamaguti,1961;
Lal,
1965;
Chakravarty,
1932;
1942;
Khan & Yasin, 1969; Berland, 1970; Khan & Begum, 1971;
22
Bilqees et al., 1971; 1977; 1978; 2004; 2005; Bilqees & Kazmi, 1974;
Akram,1975;1999; Gibson, 1975;Kalyankar&Palladwar,1977;Petter,1978;1979;
Hazen et al., 1978;
Numerous species of adult nematodes were described and reported in the coast from
Pakistan. Between them, several nematodes were found parasitizing the intestine
such as Cucullanu quadrii Bilqees and Fatima, 1980 (Cucullanidae) from Arius
serratus (Day, 1877).. Bilqee et al., (1971) reported marine fish nematodes of West
Pakistan and described seven new species from Karachi coast. Bilqees et al.,
(1977) reported marine fish nematodes of Pakistan describing Dujardinascaris
sciaenae from a sciaenid fish, Fatima and Bilqees (1987) review the Anisakis
nematodes. Fatima (1988) described seasonal variation and histopathology of
nematodes and Acanthocephala in some edible fishes of Karachi coast. Fatima
(1985) also reported some larval nematodes from the fishes of Karachi coast. Khan
and Yaseen (1969) had surveyed the helminth parasites of marine fishes from
Bangladesh and recovered Porrocaecum trichiuri. Chandler (1935) reported
23
Contracaecum brevicaecum from the body cavity of saw fish and Raphidascaris
panijii from the intestine of Sillaginopsis panijus. (Hamilton, 1822). Khan (1969)
reported a new species of the genus Indocucullanus from Pakistan. Khan and
Begum (1971) recovered Echinocephalus uncinatus from the mesentery of
Cyanoglossus sindensis(Lac.) and Lates calcarifer(Bl.); Contracaecum vittatii from
the body cavity of Upeneus vittatus(Forsk.) C. collieri (Chandler,1935) from the
body cavity of Mugil parsia(Ham.). They also reported Dujardinascaris magna
from the stomach of Sciaena sp. Bilqees and Fatima (1992) reported
Echinocephalus
muraenesocis
and
Contracaecum
synpapillus
from
Chiloscyllium
griseum
(Muller&Hen.),Galeocerdo
Railliet&
Henry,1905)19
species
from
family
2000; Bilqees and Khan, 1994; Bilqees and Parveen, 1996; Khatoon & Bilqees,
1996; 1999;Khatoon et al., 1999a; 1999b; Bilqees et al., 1998; 1999 ; 2001; ).
Most fishes of the Karachi coast are commonly infected either with nematode
larvae or Acanthocephalans or both. Seasonal variations and intensity of
infection of these parasites have already been reported by Bilqees and Fatima
(1986) and Fatima and Bilqees (1989). A number of genera of the family
Anisakidae occur in the digestive tracts of marine fish. They live free in the
lumen of the stomach or intestine; some attach to or invade the wall of these
organs and cause local tissue damage. Pathogenesis is a result of their mode of
feeding, attachment and movement or migration within the host. Anisakis larvae
are commonly found in the fishes of Karachi coast and have been reported from
several fishes including Cybium guttatum (Bilqees and Fatima,1986). Bilqees
and Fatima( 1993) have reported that the intensity of infection may be as high as
26
90% in Hilsa ilisha. In fishes of Karachi coast the larval forms reported are
Anisakis
sp;
Porrocaecum
sp;
Contracaecum
sp;
Thynascaris
sp;
(China). Anai (1969) has given described preliminary report on the parasites of
certain marine fishes of British Columbia. Koyama et al., (1969) described
morphological and taxonomical studies on Anisakidae larvae found in marine
fishes and squids. Kurochkin and Leonteva (1970) described medical significance
and distribution in marine fish of Anisakid larvae. Henning (1974) described the
effect of a larval Anisakis on the South West African anchovy, Engraulis capensis.
Stern et al., (1975) examined Anisakid larvae in the edible portions in sixteen
species of commercial marine fishes caught from Washington State. Hauck (1977)
reported occurance and survival of the larval nematode Anisakis sp., in pacific
herring Clupea harengus Hauck and May (1977) described histopathologic
alterations associated with Anisakis larvae in Pacific herring from Oregon. Smith
and Wootten (1978) reviewed many and varied aspects of the extensive world
literature on Anisakis and Anisakiasis including use of the nematodes as biological
tag in applied fishery sciences in Scotland. Deardorff and Overstreet (1981a)
reported larval Hysterothylacium (Nematoda: Anisakidae) from fishes and
invertebrates in the gulf of Maxico.
Matthews (1982) studied behaviour and enzyme release by Anisakis sp. Larvae.He
found that Bagrov (1983) described morphological variability of larvae of
nematodes of the genus Anisakis (Nematoda: Anisakidae). Petter et al., (1984)
studied teleost fishes from Yugoslavia for parasitic nematodes and found several
species of the genus Anisakis sp.As Anisakid nematodes are important from human
health point of view, attention is being paid on the study of these nematodes in
various parts of the world. Asami et al., (1965) reported two cases of stomach
granuloma, with associated necrosis and extensive eosinophilic infiltration. Thiel
and Houten (1967) described the localization of the herring worm Anisakis marina
in and outside the human gastrointestinal wall. Andreassen, (1970) described the
28
(Sood, 1967) from Mystus vittatus in Lucknow; P.(S.) ottuei (Verma &Verma
1971; P.(S.) ompoci(Majumdar&Data1972) ; P.(S.) intestinscolas (Bashirullah&
Hafizuddin ,1973); P.(S.) notopteri (Bashirullah& Hafizuddin,1973); P.(S.) timmi
(Bashirullah, 1973); P.(S.) ditchella (Gupta& Garg, 1977) ; P.(S.) gupta (Arya
,1978) from Schizothorax richardsonii(Grey) ; P.(S.) kashmirensis (Dhar&Fotedar
,1980); P.(S.) daleneae (Boomker,1993) ; P.(S.) guttatusi (Andrade-Salas et al.,
1994; (Olsen, 1952; Noble, 1966; Machida and Taki, 1985; Rigby and Adamson,
1997; Rigby and Font, 1997); P.(S.) kakinadensis and P.(S.) lutjanusi (Lakshmi,
2000a,b); P.(S.) chetumaleusis (Gonzalez-Solis et al., 2002); P.(S.) fulvidroconis
(Moravec et al., 2003) redescription ; P.(S.) variolae and P.(S.) longrus (Moravec
et al., 2006) and P.(S.) anguillae (Moravec et al., 2006).
From the present investigation 272 nematode specimens were recovered including,
new and known species. A prevalence of 62% was recorded. From the infected fish
specimens 131 new nematode specimens and 141 known nematode specimens were
recorded. ( 37 nematode specimens were damaged, kept for DNA sequences) Only the
new nematode species are described here. The recovered new nematode species
belong to one new genus and three known genera, including Spirocotyle n.gen.
(Camallanidae Railliet and Henry, 1915); Dujardinascaris
Baylis, 1947;
30
31
X 100
Miscellaneous.
33
Platyhelminth and Nematyhelminth were not the food items but were the part
of food content.
34
35
4: FEEDING HABITS
Food is an important factor in the biology of fishes, to the extant of
governing their growth, parasitic movement, maturity and migratory
movements. The food choices of different edible marine fishes were
investigated. The study of dietary habit of fish based on stomach content
analysis is widely used in fish ecology as an important means of investigating
tropic relationship in the aquatic communities (Fagbenro et al., 2000).
The pattern of food and feeding habits of 8 edible fishes were studied during
the period from Feb. 2005 to June 2007 from Karachi coast, Pakistan.. Fishes
were identified by fin-formula method; Qureshi (1955); Fisher and Bianchi,
(1984) FAO field guide; Hoda, (1985); Majid and Khan, 1995; Eschmeyers,
(2001). The length and weight of each fish specimen in the sample were
recorded.
The taxonomic lists of fish species under investigation are given in table 1.
The compositions of food items were categorized in table 2-4. The food
categories mainly consist of crustaceans, molluscs, Helminthes, planktons,
fishes, detritus and miscellaneous,
37
4.1
S.No
Order
Family
Mugiliformes
Mugilidae
1824)(Boi)
Sardinella albella
2
Clupeiformes
Clupeidae
(Valenciennes,1847)
(Tarli)
Scomberomorus guttatus
Perciformes
Scomridae
(Bloch&Schneider,
1801)(Surmai)
Pomadasys olivaecum(Day,
1875) (Dohtar)
Perciformes
Haemulidae
Pomadasys maculatum
(Bloch, 1797)
Pomadasys stridens(Forskal,
1775)
Otolithus ruber
Perciformes
Sciaenidae
(Schneider, 1801)
(Mushka)
38
Siluriformes
Ariidae
Arius maculates
(Thunberg, 1792)(Khagga)
Sphyraena forsteri
Peryciformes
Sphyraenida
Sphyraena jello
(Cuvier, 1829)(Kund)
Perciformes
Perciformes
10
Centropomi
dae
Sillaginidae
Thunniformes Thunnidae
Lates calcarifer
(Bloch, 1790)(Dangri)
compare to other food items. These were found in near about all fish
specimens and in larger quantities (Table 6). Soil nematodes were also
present but these were not the part of food. The analysis of data on the basis
of diet composition indicates that Liza vargiensis is an herbivorous fish.
40
A pelagic schooling species, found in coastal waters. The main diet items
observed in the stomach of S. albella on the basis of percentage occurrence
were plankton (75%) followed by detritus (66.7%). miscellaneous (64%)
ranked 3rd among the food categories (Table 5). Copepods (16.66%) were the
least observed food items on the basis of percentage frequency occurrence
(F%) (Table-7). The observation of the stomach content revealed that
Sardinella albella is herbivorous in nature.
Diet of Scomberomorus guttatus (Bloch&Schneider, 1801)
Local name=Surmai
N=70
TL=50-70cm
(Mean=60.59, Variance=50.56, Std.Dev.=7.11, SEM= 2.24).
Lancet-shaped teeth ,much longer in the lower jaw, color bluish above and
silvery beneath, back and side with three rows of horizontal oral spots edible
fish ,commonly landed at fish harbour.It dose not remain fresh for long. A
total of 14 organisms were identified in the stomach of S.gutattus (Table 3).
Organism by name, total, percentage occurrence (Table 5) and percentage of
frequency occurence of stomach can be seen in (Table 8) with histograme
representation ( Fig 3) . Miscellaneous (90.16%) ranked at the top as compare
to other food items. Crustaceans (81.96%) ranked second followed by
molluscs(32.78%). The detritus (8.19%) and teleosts(6.55%) were in
decreasing order. Helminthes (14.75%) were also observed but they were not
the part of food items (Table 5). On the basis of observation of food content
Scomberomorus guttatus is carnivorous fish.
41
detritus,
1.67).
4.70).
Body elongate ,without scales, dorsal and pectorals fins with spines. Caudal
fin forked. Head with three pairs of barbells. Common along the coast in
creeks and estuaries common in local fish market. The main diet categories
were crustaceans (70%) (Table 5) dominated by Penied sp.(70%) with
decreasing
order
of
Copepods
and
Amphipods(60%)>Nepton
44
The fish is found in tropical and subtropical Coastal waters over shallow
banks closed to the bottom. Large-mouthed with the lower jaw projecting
forward bearing strong teeth. Upper jaw non-protractile, an adaptation to
feeding on large prey.
The crustaceans and miscellaneous were on the 1st rank in the diet of
S.forsteri constituting about (85%) on the percentage of occurrence (Table
5).The food items of crustacean category in descending order were
Parpenaeopsis(57%)> Cephalopods(50%)> Peneid and Acetes sp.(35%).
The miscellaneous mainly consisted of mantis shrimps, larvae of crabs,
chelae, scales, shell fragments, prawn eyes, head and appendages prawn
mysis. The teleosts (54%) ranked second in importance including small
unidentified fishes as the food constituents. The molluscs (31%) having
lowest frequency in the stomach on the basis of occurrence dominated by
Squilla sp. (Table 12). Helminthes belonging to different phyla including,
Acanthocephala, Cestodes and Nematodes but not the part of the food
contents. S. forsteri has been found to be a carnivorous fish which mainly
feed upon crustaceans, teleosts and molluscs.
45
3.60).
Large oblique mouth with lower jaw projecting, upper profile of head some
what concave, color golden brown dorsally and silvery beneath found in
coastal waters and estuaries. The main food contents are given in (Table 4).
The percentage of frequency occurrence (F,F%) is given in (Table 13).
According to this observation the crustaceans and miscellaneous (64%) were
the top priority food categories followed by teleosts (57%) and molluscs
(29%) on the basis of percentage of occurrence. The least observed food
items were planktons.
4.3 Remarks
Different food categories were studied in 8 different edible fishes from
February 2005 to June 2007.
Sujehiro(1942) observed that the fishes, which do not possess great
swimming powers, have well developed teeth to hold the prey once it is
caught the conical and pointed teeth of the jaws and pharynx of fishes under
study help in seizing, holding and tearing the prey . The pharyngeal teeth
also appear to macerate the prey while swallowing. Unlike mammalian
intestine tissue, multicellular glands or other specialized structures in the
intestine of teleost are rare.The intestine in carnivorous fish is shorter than
the Omnivorous and herbivorous mucosal area, however may compensate
for the relative length of the gut (Al-Hussain, 1949; Suyehiro 1942).
Food and feeding habits of different edible fishes were found to be
comparable to Pakistani fishes( Huda, 1993; Ajazuddin, 1991; 2000; 2001;
Khan and Huda, 1993; Imtiaz and Khan, 2005;).
46
Khan & Hoda, 1993 point out 8 food categories in marine edible fish
Euryglossa orientalis on monthly basis. According to their observation
miscellaneous items were found to be the most dominant category in all
respect including percentage of occurrence, average points and percentage of
total points. sand grains formed the second group on the basis of percentage
of occurrence, mollusces and crustaceans were seen through out the years.
Ajazuddin, 2000; 2001, observed the food and feeding habits of Otolithus
cuvieri and Johnius elongatus respectively the fishes were observed to be
carnivorous on the basis of their feeding habits. he observed in Johnius
elongatus that feeding intensity were higher in fishes of larger size group
while poor feeding condition were exhibted by smaller size groups, he
calculated the composition of food of different size and seasons. According
to his observations, the polychactes, crustaceans and semi-digested food
material were the most frequent food items for smaller size group while the
diet constituent shifted to molluses, teleosts and miscellaneous food in larger
size groups.
Imtiaz and Khan (2005) observed the food and feeding habits of edible
carnivorous fish Pomadasys stridens from Karachi coast. according to their
observation of different food groups, the semi-digested food material were
the most dominant food group by percentage of occurrence, where
crusteaceauns, molluscs, teleosts and Polychaetes occupied the successive
position by percentage of total occurrence. According to the present
observation based on percentage of occurrence method and Percentage of
frequency occurrence the principal organisms observed in Pomadasys
47
analysis of stomach contents of fish could provide information about the nich
of a particular of fish in its ecosystem and this has become a standard practice
in fish ecology works(Hyslop, 1980). Rao (1979), Suscclan and Naik (1969)
recorded the occurrence of prawns, crabs, isopods, amphipods and fishes in
the stomach of Sciaenid.
The present analysis also agree with Ghandi(1982), who remarked that
feeding habits depended on the availability of fish food in the environment.
Muthia (1982) concluded in Johnicops vogleri that the main food items were
crustaceans and were encountered almost through out the year in different
proportions.
Katsuhiro and Mahyam (2003) studied the distribution and feeding habits of
Lutjanus johnius in mangrove estuary in Malaysia the analysis of their study
showed that type of food varied with size. large-size individuals fed manily
on natantia and small-sized individuals on Mysidaceae. Hajisami et al.,
(2004) analysis the food habits and trophic interrelationships between nine
fish species, utilizing on impacted coastal habitat revealed that the diet of
most species underwent marked changes with ontogeny. The analysis
demonstrated that diet composition of the nine fish species differ from each
other. Teleost fishes employ a wide range of feeding technique, but these
rarely involve direct manipulation of object to uncover prey.
A strong relationship between infection with a parasite species and the
corresponding intermediate host from the stomach content of individual
charr, indicated an individual feeding specialization. (Knudsen et al., 1996).
The infection variations seemed to be due to differences in host growth rate,
host feeding habit, and the distribution of marine mammal final hosts. Larval
49
nematodes are useful biological indicators for the population study of walleye
pollock in Japanese waters.( Konishi, 2002).
Hirasawa et. al., 2004 discuss the relationships between nematode parasitism
and the feeding habitats of their intermediate hosts and found that the
principal intermediate hosts of the two nematodes were filter-feeding
mayflies of the genera Ephemera, Photamanthus and Isonychia. Ephemera
strigata seemed to be the most important intermediate host of these
nematodes. Adult R. coronacauda were found mainly in Hemibarbus
longirostris and Rhinogobius flumineus, which are benthic fishes that feed on
benthic aquatic insects, including
therefore, the feeding habits of the definitive hosts facilitate host alternation
by this species.
Bhuiyan et al., (2006) studied the food and feeding habits of Channa
punctatus. During their analysis Channa punctatus is a carnivorous fish, its
food consist mainly of crustaceans, insects, molluses, fishes, plants and semi
digested materials. Monthly variation in the percentage composition of food
items in both juvenile and adults were recorded. The fish changed its food and
feeding habits seasonally. The feeding intensity was very poor in mature
fishes during the spawning period.
Laurent et al., (2007) studied the food composition and feeding habits of
Euthymus alletteratus in continental shelf waters of West Africa. the type and
quantity of prey ingested change seasonally. Out side the major upwelling
period the diet was more varied. Overall fishes were the dominant prey of all
sizes of little tunny, far exceeding crustaceans of which shrimps and prawns
were commonest but were not found in the stomach of juveniles or larger
50
adults they observed that little tunny are carnivorous fish that feed
opportunistically. a relation ship was found between the size of the prey and
the size of the predators.
Mosterda et al., (2007) observed the feeding habits of the bullet tuna Auxis
rochel in the southern Tyrrhenian Sea. The result of his study showed that the
bullet tunna is an epipelagic off-shore predators feeding on whatever
abundant resource is available in the environment with a preference for
planktons, crustaceans, small cephalopods and fish larvae. All prey was
pelagic organisms. A size related change in the diet composition was
observed. The average prey weight per stomach increased significantly in the
larger predators which mostly fed on fish larvae belonging to several
commercially important demersal and pelagic species
4.4 Statistical Analysis
51
S.No
Food Contents
1
2
3
4
5
6
Polychaetes
Crustaceans
Molluscs
Platyhelminthes
Nematyhelminthes
Teleosts
Planktons
Sardinella albella
(Tarli)n=70
---Copepods
-------------
Phytoplankton(, Diploneis,
Gyrosigma sp, pleurosigmaelongatum, normaris,),
Zooplankton(Harpactacticoid)
Anabaena, Microsystis
Chlorella
8
Miscellaneous
52
Sand,mud
Molluses larvae, unidentified
crustaceans
S.N
o
1
Food
Contents
Polychaetes
Scomberomorus
guttatus
(Surmai)n=70
Neries
Pomadasys maculatum
(Dhotar)n=75
Sphyraena forsteri
(Kund) n=70
Neries
---Penied, cephalopods,
Copepods,
Parapenaeopsis sp,
Acetes sp.
Crustaceans
Shrimps,
Copepodes
Amphipods,Shrimps,
(Penied sp)
Copepodes,Crabs (Acetes
sp)
Molluscs
Decapods,
Dentalium sp..
Loligo sp.
Oratosqilla sp.
,Sepia sp.,Dentalium
sp.
Platy
helminthes
Liver flukes
----
Acanthocephala sp.
Nematy
helminthes
Nematodes
(Dujadinascaris sp.)
Nematodes
(Dujadinascaris s.p)
6
7
Teleosts
Planktons
Nematodes
(Spirocamallanus,
Bulbocephalus)
---zooplanktons
Leiognathus sp.
----
Detritus
Sand
----
Cynoglossus sp.
Zooplanktons
----
Miscellaneous
Larvae of fishes
crustaceans,fin,sca
les of fishes,
pieces of
molluscs,crab
remains
53
Carapace of fishes,
eggs, chlae,and
antennae of
crustaceans
S.
N
o
1
2
Food Contens
Polychaetes
Crustaeans
Arius maculates
(Cat fish)n=50
Otolithus ruber
(Mushka)n=150
Heteroneries
Amphipods,Shrimps,
(Penied sp)
Copepods,Crabs
(Neptorn sp)
---Penaeus sp,Dioptera
sp,Grapsid
sp,Amphipodes
sp,Copepodes
Lates calcarifer
(Dangri)n=70
---Shrimps,Crabs,
Copepods
Molluscs
Soletella sp,Ensis
sp,Bullia,Soleno sp
Gastropods,Solen
sp,Sepia sp
Cephalopods
(Loligo,squila)
Platy
helminthes
----
Acanthocephala,
Trematodes
Acanthocephala,
Nematy
helminthes
Bulbocephalus sp.
Spirocamallanus sp
----
Teleosts
Juvenile of eel,Fish
part(head,spine,fins,bo
ne and scales)
Gobeid sp
Unidentified fishes
Planktons
Zoea larvae,
gammrous sp.
Cyclops,Gammrous
sp,Scratillaria,Zoea
larvae
Detritus
----
Sand,mud
----
Miscellaneous
Carapace of fishes,
eggs, chelae, and
antennae, compound
eye of crustaceans
Part of mandible
crabes,cycloid and
ctenoid scales,undigested
part of animals,Shell
fragments
Compound eyes,
Carapace,mantis,scal
es of fishes
54
FISH SPECIES
FOOD CATEGORIES
Polycheates
Crustaceans
Molluscs
Liza
verigensis
----
----
----
Sardinella albella
Scomberomous
guttatus
Pomadasys
maculatum
Otolithus
ruber
--------
16.66
81.96
---32.78
7.14
71.42
8.69
82.60
Arius maculates
Spharyena
forsteri
Lates
calcarifer
10
---------
Helminthes
25
Teleosts
----
Plankton
s
85
Detritus
Miscellane
us
100
50
---14.75
--6.55
75
----
66.7
8.19
64
90.16
50
35.7
35.7
----
----
71.42
78.26
30.43
60.08
66.08
4.34
80.86
70
84.61
60
30.76
4
15.38
10
53.84
70
-----
6
30.76
70
84.65
64.28
28.57
12.85
57.14
7.14
55
---
64.25
Statistical Calculation
Mean
Polycheates
0.49
Crustaceans
0.2.09
Helminthes
0.490
Molluscs
0.032
3.69
67.36143
40.05286
16.15857
1.767316
8.926165
9.551812
4.899
Median
71.42
32.78
14.75
Mode
Standard Error
#N/A
#N/A
#N/A
4.675878
23.61641
25.27172
12.96153
21.86383
557.7349
638.6598
168.0014
Kurtosis
-2.37994
4.79605
0.206456
-0.8125
Skewness
0.493746
-2.09915
-0.03267
0.462161
Maximum
10
84.61
78.26
35.7
25.83
471.53
280.37
113.11
Largest (1)
10
84.61
78.26
35.7
Smallest (1)
16.66
4.324469
21.84155
23.37246
11.98743
Sum
Count
Confidence
Level(95.0%)
56
Statistical
Calculation
Teleosts
Planktons
Detritus
0.40
2.00
Miscellaneous
0.400
0.15
Mean
Standard Error
Median
Mode
Kurtosis
Skewness
Maximum
Sum
Count
Largest (1)
Smallest (1)
Confidence
Level(95.0%)
31.90143
9.84017
35.7
#N/A
26.03464
677.8027
-2.40654
-0.13487
31.17429
13.92129
7.14
0
36.83226
1356.616
-2.70889
0.375727
16.57
9.251802
6
0
24.47797
599.1708
3.10952
1.847657
75.04857
3.878052
71.42
#N/A
10.26036
105.275
-1.56373
0.377555
60.08
223.31
7
60.08
0
75
218.22
7
75
0
66.7
115.99
7
66.7
0
90.16
525.34
7
90.16
64
24.07805
34.06419
22.63836
9.489258
57
Organism identified
Polychaetes
Crustaceans
Molluscs
Platyhelminthes
Nematyhelminthes
Unidentified Soil nematode
Teleosts
Planktons
acanathes hungrica,
gomphonema globiform,
Scenedesmus
Melosira arenaria
Pennularia
tabellaria
Pleurosigma- elongatum
pleurosigma- normaris
Diploneis
Gyrosigma sp
Green filamentous algae
Oscillatoria sp.
Detritus (Sand )
Miscellaneous
58
F
-------
F%
------50
----
25
45
40
25
170
22.5
20
12.5
12.5
15
15
50
75
35
85
88
200
100
49
100
50
25
30
30
100
150
70
Table . 7:
Organism identified
Polychaetes
Crustaceans
Copepods
Molluscs
Helminthes
Platyhelminthes
Nematyhelminthes
Teleosts
Phytoplanktons
Pleurosigma- elongatum
pleurosigma- normaris
Diploneis sp.
Gyrosigma sp.
Zooplanktons
Harpacticoid sp.
Detritus(mud)
Miscellaneous
59
F
----
F%
10
----
16.66
---------45
30
35
40
75
50
58.4
66.7
20
40
40
33.33
66.7
66.7
Table .8:
Organism identified
F
-----
F%
20
30
32.78
49.2
Ensis sp.
6.55
8.19
14.75
8.19
4
10
5
6.55
16.39
8.19
25
55
25
35
14
50
90.16
41
57.37
22.95
Polychaetes
Crustaceans
Shrimps
Copepods
Molluscs
Helminthes
Platyhelminthes
Acanthocephala
Nematyhelminthes
Bulbocephalus
Teleosts
johnius sp.
Planktons(Zooplanktons)
Detritus
Miscellaneous
Larvae of fishes
Crustaceans
Fin
Scales of fishes
Pieces of molluscs
60
Table .9:
Organisms identified
Polychaetes
Neries
Crustaceans
Shrimps
Copepods
Amphipods
Crabs(Acetes sp)
Molluscs
Solen sp.
Sepia sp.
Pholas sp.
Lologo sp.
Helminthes
Platyhelminthes
Nematyhelminthes
Nematode (Dujrdinascaris
sp.)
Teleosts
Johnius sp
Sardine sp.
Leiognathus sp.
Planktons
Detritus
Miscellaneous
Compound eye
Legs
Chelae
Mantis of shrimps
Crustacean
61
F%
7.14
50
32
40
50
71.4
45.71
57.14
6
25
12
20
8.57
35.71
17.14
28.57
25
5
35.71
25
10
5
-------
35.71
14.28
7.14
---z
24
34.28
42.85
71.42
37.14
40
30
50
26
28
Table . 10:
62
F
10
F%
8.69
50
70
60
43.5
60.9
52.17
83
8
72.17
6.95
32
36.52
10
30.43
30
26.08
73
54
21
76
5
63.47
46.95
18.26
66.08
17.39
45
60
65
75
93
39.13
52.17
56.52
65.21
80.85
Table. 11:
Organism identified
Polychaetes
Dioptera sp.
Hetero neries
Crustaceans
Amphipods
Parapenaeopis sp.
Penied sp
Copepodes
Nepton sp
Molluscs
Solen sp
Bullia sp
Ensis sp
Helminthes
Platy helminthes
Nematohelminthes
(Unidentified)
Teleosts
Juvenile of eel fish
Zooplanktons
Gammrous sp.
Zoea larvae
Detritus
Miscellaneus
Carpaceae of crustaceans
Molluscan shell fragments
F
5
3
F%
10
6
30
7
35
30
20
---10
6
7
60
14
70
60
40
---2
10
35
30
3
70
60
6
35
70
26
52
12
50
63
20
12
14
24
71
Table. 12:
Organism identified
Polychaetes
Crustaceans
Peneid sp.
Cephalopods
Parapenaeopsis
Acetes sp
Molluscs
Oratosquilla sp
Sepia sp
Dentalium sp.
Helminthes
Platyhelminthes
Nematyhelminth
Dujadinascaris sp.
Teleosts
Unidentified small Fishes
planktons
Detritus
Miscellaneous
Carapace of fishes
Eggs, chlae,and antennae of
crustaceans
64
F
----
F%
25
35
40
25
---3
5
10
35
50
57
35
4.6
7.6
14
---10
14
35
50
20
28
50
71
55
78
Table .13:
Lates calcarifer(Dangri)
N=70 (Empty=nil)
Organism identified
Polychaetes
Crustaceans
Shrimps
Copepods
Crabs
Molluscs
Loligo sp.
Squila sp.
Helminthes
Platyhelminthes
Acanthocephala
Nematyhelminthes
Teleosts
Unidentified fishes
Zooplanktons
Detritus
Miscellaneous
Carpace of fishes
Mantis,scale,antennae and
compound eye ocrustaceans
65
F
----
F%
30
20
45
42
28
64
15
5
21
6
---9
----
12
40
5
----
57
6
30
42
45
64
4.8:
Soil nematodes
Acanthes hungrica
Gomphonema globiform
Scenedesmus
Melosira arenaria
Pennularia
Tabellaria
Pleurosigma elongatum
Pleurosigma normaris
Diploneis
Gyrosigma
Oscillatoria
sand
Miscellaneous
Food items
Fig. 1
Sardinella
albella
Sardinella
albella
Food items
copepodes
80
60
Pleurosigma
elongatum
% 40
P. normaris
20
0
Food items
Fig. 2
66
Diploneis
Scomberomous
Scomberomorus guttatus
guttatus
Shrimps sp.
copepodes
Ensis sp.
100
80
60
%
40
20
0
Lutjanus sp.
Acanthocephala
Bulbocephalus
Johnius sp.
Food items
Fish larvae
Crustaceans legs
Fig. 3
67
Neries
Pomadasys maculatum
Pomadasys
maculatum
Shrimps sp.
copepodes
80
Amphipodes
Acetes sp.
70
Solen sp.
60
Sepia sp.
Pholas sp.
50
Loligo
% 40
Dujardinascaris
Johnius sp.
30
Sardine sp.
Leipgnathus
20
Compound eyes
10
legs of crustaceans
chelae
0
Food items
mantis of shrimps
shrimp eyes& uropodes
40
Fig. 4
68
Otolithus
ruber ruber
Otolithus
Polychaetes
Grapsid
Isopodes
Copepodes
Gastropodes
90
Solen sp.
80
Acanthocephala
70
Spirocamallanus sp.
fishes
60
Gammrous
50
Scratillaria
Cyclops
40
Zoea larvae
30
Detritus
20
fish parts
Chelae
10
Crab appendages
0
Food items
Shrimp uropodes
Fish skelton,fins,scales
Fig. 5
69
Diopt er a sp.
Arius
maculates
Arius
maculates
80
Penid sp.
Copepodes
70
Nept on sp.
60
Solen sp.
Bullia sp.
50
Ensis sp.
% 40
nemat odes
Juvenile of eel f ish
30
Gammr ous
20
10
Food items
Fig. 6
70
Spharyenaforsteri
foresteri
Spharyena
80
Peneid sp.
Cephalopodes
70
Parapenaeopis
60
Acetes sp.
% 50
40
Oratosquilla
Sepia sp.
Dentalium
30
Dujardinascaris
20
small fishes
Detritus
10
0
Carapace of crustaceans
Food items
Fig. 7
Lates calcarifer
Lates calcarifer
shrimps sp.
80
copepodes
crabe sp.
60
Loligo
Squila
40
Acanthocephala
fishes
zooplanktons
20
Carapace of crustaceans
Detritus
Food items
Fig. 8
71
Fig:12 Pleurosigma sp
72
73
Fig:26
Fig:28
74
Crustacean parts
Detritus
75
76
5: NEMATODE PARASITES
Only the nematode genera recovered during the present studies are
reviewed and the species are identified and described within each of
the genera
5.1 HISTORY OF THE GENUS DUJARDINASCARIS
BAYLIS, 1947
Dujardinascaris (synonym Dujardinria gedoelst, 1916,pre occupied) was
created by Baylis in 1947.The species of genus normally occur in crocodiles
and lizards. Yamaguti (1961) listed 13 species in the genus. Of these two have
been reported from fishes and 11 from reptiles. The species reported from
fishes include, D.melapteuri Baylis, 1923 from Melapteurius electricus from
Sudan and D.cennotae (Pearsc1936) described from Rhamdia guatemalensis
from Yuncatan. Later on few more species have been reported from fishes.
Sood (1989) presented a key to the species of Dujardinascaris Baylis(1947),
reported from fishes of South Asia .Five species have been reported under the
genus Dujardinascaris by sood (1988). Four of them have been reported from
Karachi coast and one from Lahore, Pakistan. The species reported from
Karachi coast includ, D.magna (Khan and Begum, 1971)in sciaena species ,
D.qadrii ( Zubari & Farooq 1976)from sciaena species, D. sciaena diacanthus,
D.cybii (Arya & Johnson,1978) from the fish Cybium guttatum and D.ritai
(Zaidi & Khan, 1975) in Rita rita of fresh water fish from Lahore. Bilqees et
al., (2004) reported D.karachiensis from pomadasys olivaceum from Karchi
coast.
77
All the above-mentioned 5 species have been described from Pakistan except D.
cybii which is originally described by Arya & Johnson (1978) from India. It
appears that genus Dujardinascaris is one of the common genera found in
fishes of Pakistan. During the present studies it was noted that species of the
genus were also more common in fishes of Karachi coast. Seven new species
of the genus are identified and described here. Dujardinascaris mujibi, D. jello,
D. maculatum, D. dentatus, D. multiporous, D. sphyraenaii, and D. sinjarii.
78
Ascarididea
Family:
Heterocheilidae
Sub. Family:
Filocapsularinae
Genus:
Type host:
Prevalence:
Intensity:
Holotype (male):
JUW. N.26
Allotype (Female):
JUW. N.27
80
Remarks:
The genus Dujardinascaris was created by Baylis in 1947. This genus
normally occurs in crocodiles, lizards and alligators. Diaz andGallardo
(1968); Sprent(1977, 1990); Hazen et al.,(1978);Cherry and Ager(1982);
Gold berg,et al.,(1991); Machida et al., (1992);Scot et al.,(1999); Sprent,et
al., (1998); Moravec (2001); Sood (1989); Bursy ,et al., (2005); Junker, et
al., (2006); Yamaguti (1961) listed two species of nematodes from fish
under the genus, Dujardinascaris, D. . cenotae( Pearse, 1936) from Rhandia
guatemaensis in Yucatan; D. melapteruri (Baylis, 1923) in Melapterus
elecricus. Sood(1989) presented a key to the species of Dujardinascaris
Baylis 1947 reported from fishes in South Asia. Five species have been
listed under the genus Dujardinascaris by Sood (1989) namely; D. magna
(Khan & Begum, 1971, in Sciaena sp. from Karachi coast; D. ritai (Zaidi &
Khan, 1975) in Rita rita of fresh water fish from Lahore, D. quadrii (Zubari
and Farooq, 1976) from Sciaena sp., from Karachi coast; D. Sciaena
(Bilqees et al., 1977) in Sciaena diacanthus from Karachi coast, D. cybii
(Arya and Johnson, 1978) from fish Cybium guttatum from India, Lakshmi
and Sudha, (2000) give notes on D. cybii Arya and Johnson from a new host
Mugil cephalus. Bilqees et al., 2004 describe D. karachiensis from
Pomadsays olivaecum from Karachi coast.
The present species is considered as a new species and named as D. mujibi.
Differential diagnosis is compared with described species of genus
Dujardinascaris. The present species is different from all the above
mentioned species in body length, length of esophagus, length of spicules ,
number of papillae in male, length of intestinal caecum and other
morphological variation such as prominent zigzag patterns embossed on
81
upper part of the lips as revealed by SEM. This pattern of lips has not been
described previously. The description of D. cenotae is based on three poorly
described female specimens while the description of D. malapteruri and D.
magna is based only on male specimens In D. magna the number of caudal
papillae are 30, including 20 preanal and 10 postanal and the length of
spicules are 1.70-1.76, tail is 0.50 in length, indicating that the present
species having less number of papillae and spicules longer than D. magna.
D. ritai is described by immature female only. While D. ritai is from fresh
water fish.
D. sciaena is smaller in size, and the esophagus is larger in size, length of
spicules are 5.25.5. Caudal papillae are 23 pairs, including 19 preanal and
4 postanal, tail length is 0.1200.166. The present species is also different
from D. quadrii in length of spicules (5.42-5.52), number of caudal papillae
(23 including, 19 preanal and 4 post anal). The present species have shorter
spicule length, having 14 pairs of caudal papillae and short tail as compared
to D. sciaena. The present species differs from D. karachiensis by lips
structure, length of esophagus, length of intestinal caecum, length of
spicules,(1.701.71) number of caudal papillae (25 pairs, including 4
preanal and 21 post anal) and distance of cloeca from the posterior end. The
main differences in addition to the above mention structures observed in the
present species by SEM are the zigzag embossment and the structure of
female tail having concentric appearance.
The comparative morphology of the present species with other species
recovered from South Asia and the species recovered during the present
82
83
Type locality:
Prevalence :
Intensity:
Holotype(male):
JUW. N.23
Allotype(female):
JUW. N.24
Diagnosis: Stout and elongated worms, whitish in color, the head carries
three prominent lips. The lips are clearly separated from each other. The
space between the two adjacent lips is occupied by prominent interlabia and
lips are interlocked by which these are connected together like a zip. Dorsal
lip with rounded end fit into the cavities of the two subventral lips. Right
subventral lips have a cavity, which fits into the rounded end of dorsal lips
and also fits itself into the cavity of adjacent lips. Nerve ring is a distance of
0.16-0.23. Cuticle is thick and striated at the head region forming a zigzag
pattern; the left of the body is striated sparsely. The cuticular striations are
present throughout the body, most prominent at posterior region above the
tail region in female. Gubernaculums is absent.
Male: (7 specimen including holotype ).The total length of worm is 2627.5 and 0.43---0.48 in breath. The lips are 0.07-0.09 in length and 0.10-84
86
Site of infection
Intestine
Type locality:
Prevalence:
Intensity:
Holotype(male):
Allotype (female):
JUW. N. 11
JUW. N.12
Diagnosis: Stout, long cylindrical, dark brown worms, tapering toward both
extremities with pointed posterior end in male and conical posterior end with
round tip in female. Mouth is bounded by three lips, without dentigerous
ridges. Cuticle finely striated, these striations are prominent at the anterior
end in male and at posterior end in female. Esophagus is entirely muscular,
intestinal caceum well developed. Anal opening is prominent in male.
Male:
worms, body length 9.0510.0 and maximum width is 6.077.02. The lips
are 0.160.18 x 0.350.45 in size. Esophagus is 0.50.8 in length and
0.150.25 in width. Intestinal caecum is 0.40-0-0.49 in length. 13-- 16 pairs
of caudal papillae are present, including 13 pairs precloacal,
2pairs
postcloacal and 1 adanal . Two unequal spicules are present, 0.910.95 and
87
Remarks:
There are six species in this genus namely; D. magna (Khan & Begum,
1971) in Sciaena sp. from Karachi coast; D. ritai (Zaidi & Khan, 1975) in
Rita rita of fresh water fish from Lahore, D. quadrii (Zubari and Farooq,
1976) from Sciaena sp., from Karachi coast; D. Sciaena (Bilqees et al.,
1977) in
Johnson, 1978) from fish Cybium guttatum from India and D. karachiensis
(Bilqees et al., 2004) from Pomadsays olivaecum, Karachi coast.
The present species is regarded a new species D. maculatum n.sp. and is
compared with described species of genus
Dujardinascaris. The
morphological variations are shown in table 14-15, with figures 49-51. The
present species is different from all Pakistani species, and the species
described from other parts of the world. (Table 16-17). According to SEM
88
89
Site of infection:
Intestine
Type locality:
12 % & 2.14
( 7 fishes infected/ 58 fish examined,
with 6 male and 10 female nematodes)
Holotype (male)
JUW. N. 14
Allotype (female)
JUW. N. 15
the genus
Dujardinascaris recovered from South Asian are given in tables 14-17. The
present species is different in both sexes from D. mujibi; D. jello and D.
maculatum ,in the structure of tail which is bluntly pointed in male and
sharply pointed in female. The present recovered species is also provided
with area rugosa-like structures at posterio-ventral side. The papillae are
91
Etymology:
host species
92
Prevalence:
Intensity:
1.66
Holotype(male):
JUW. N. 18
Allotype (female):
JUW. N. 19
are 18---20 pairs, sessile, 9 pairs are precloacal and 9-11 pairs are
postcloacal. Posterior of the body is provided with 13---17 pore-like
depressions, dorso-lateral in position, situated at regular intervals. Nerve
ring is at a distance of 0.35-0.42 and excretory pore is 0.37-0.45 from
anterior end of the body. Tail is pointed with 2---3 pore-like depressions
sparsely.
Female: (13 specimen including allotype) Body length 6.5---7.9 and 0.25--0.30 in its width. The lips are 0.055---0.075x 0.80---0.110 in size. The
esophagus is 0.38---0.45 in length and 0.14---0.19 in its maximum breadth.
Intestinal caecum is inconspicuous. Nerve ring is at a distance of 0.38-0.40
and excretory pore is 0.40-0.44 from anterior end of the body. Vulva is
conspicuous, at a distance of 0.37-0.39 from its posterior extremity. The
posterior part of body is provided with 7---10 pore-like depressions at
irregular intervals. The tail is conical.
Remarks:
The dimension of various structures of the species under discussion are
given in table 1417. The peculiar character of the present species is the
presence of cuticular pore-like depressions in both sexes as shown by SEM.,
which distinguish it from all south Asian species. It is also different in other
morphological characters, including body length in both sexes, (6.10-7.90);
length of spicules(0.59-0.75) and in number(18, including 9 pre anal and 911 post anal) and position of caudal papillae (dorso-lateral).The present
species is also different from the new recovered species including D.mujibi,
D.jello, D. maculatums and D. sphyraenaii in the above mentioned and
94
The present
95
Site of infection:
Intestine.
Type locality:
Prevalence :
Intensity:
6%
1.66
Holotype(male):
JUW. N. 36
Allotype(female):
JUW. N. 38
Diagnosis:
whitish in color. The cutical investing the body is expanded throughout its
length, frill-like at the anterior region of the body and not provided with spines
or other raised structures. The head carries three prominent lips having four
teeth like structures capable of being interlocked. Interlabia are present, with
prominent grooves running from the tips to the base. Esophagus is large
muscular tube, ventriculus is absent but esophageal bulb is present. Tail is
pointed in both the sexes.
96
Remarks:
Dujardinascaris sinjarii is different in important diagrammatic features from
other species of the genus Dujardinascaris including D. . cenotae ( Pearse,
1936) from Rhamdia guatemalensis;
The present species is also different in some morphological characters from the
specimens reported by Sood(1989) from fishes in South Asia namely;
D.
magna (Khan & Begum, 1971), in Sciaena sp. from Karachi coast; D. ritai
(Zaidi & Khan, 1975) in Rita rita from Lahore, D. quadrii (Zubari and Farooq,
1976) from Sciaena sp., from Karachi coast; D. Sciaena (Bilqees et al., 1977) in
Sciaena diacanthus from Karachi coast, D. cybii (Arya and Johnson, 1978)
from fish the Cybium guttatum from India and D. karachiensis (Bilqees et al.,
2004) from Pomadsays olivaecum, Karachi coast. D. sciaena is smaller in size,
and the oesophagus is larger in size, length of spicules are 5.25.5, papillae are
23 pairs, including 19 preanal and 4 postanal, tail length is 0.1200.166. The
present species is shorter in spicule length, having 14 pairs of caudal papillae
and also short tail as compared to D. sciaena.The present species is considered
as a new species and named as D. sinjarii. It is compared with all the described
species of genus Dujardinascaris (Table. 14&15). The present species is
different from all the above mentioned species in body length, length of
esophagus, length of spicules , number of caudal papillae in male, but resemble
in some extent with D. karachiensis in the presence of esophageal bulb and in
body length of male specimens but
98
Etymology: The specific name D. sinjarii refers to the local name of the fish
host.
99
Site of infection:
intestine
Type locality :
Prevalence:
Intensity:
1.3
Holotype(male):
JUW. N. 29
Allotype(female):
JUW. N. 30
Diagnosis: Stout, whitish, elongate worms, female is larger than male, body
striated throughout its length. Head is provided with three lips, lips are
embossed with zigzag pattern. Lips are without dentigerous ridges but cuticle
of their internal surface is produced into large teeth- like structures capable of
being interlocked. Esophagus is muscular. Intestinal caecum is conspicuous.
According to SEM, the tail is with snout spine at its tips in female. Anal
opening is prominent in male. Vulva is preequatorial and eggs are sub
globular.
Male:( 4 specimen including holotype) Body is 17.80 ---18.50 in length and
0.38---0.4 in its maximum bredth. The lips are 0.27---0.3x 0.24---0.26 in size.
The esophagus is 3.954.25 in length and 0.31---1.35 in its width. An
intestinal caecum is present anteriorly measuring 0.180.76 in length. Nerve
ring is at a distance of 0.28-0.31. Excretory pore is situated at a distance of
0.56-0.57 from anterior end.
Remarks:
The dimensions of various structures of the species under discussion are given
in table 14-17. It shows that this species is different from all south Asian
species in respect of each morphological chracter as shown in table no.but it
resemble with D. mujibi and D. jello in embossment of zigzag pattern except
in the pattern of embossment. The present species is also differ from D, mujibi
and D. jello in number and arrangment of caudal papillae, pre cloacal in the
previous two species and in the present specimen 6 pairs are pre cloacal and 8
are post cloacal. The present recovered species is also different in position of
anal opening in male which is pre equtorial and from the posterior
extremity. And in the dentate posterior end of female (as revealed by SEM)
but the posterior end of two male specimens was destroyed during scanning
electron microscopy. The present species is regarded a new species D.
dentatus n.sp..
Etymology: The species name D. dentatus refers to the caudal teethLike structure in female specimens.
101
Species
D.mujibi
(male)
D.mujibi
(female)
D.jello
(male)
D.jello
(female)
D.maculatum
(male)
D.maculatum
(female)
D.sphernaii
(male)
D.sphernaii
(female)
Host
Sphyraena
forsteri
Sphyraena
forsteri
50.05-51.85
1.05-1.07
0.140.16x
0.22-0.24
3.60
4.70
Sphyraena
jello
Sphyraena
jello
31.20-33.25
1.30-1.34
Pomadasys
maculatum
Pomadasys
maculatum
Sphyraena
jello
Sphyraena
jello
9.05-10.0
13-19
20.5-24.9
22.4-25.4
6.077.02
0.42-0.50
0.32-0.36
0.25-0.37
0.1518x
0.25-0.27
0.160.18x
0.35-0.45
0.090.15x
0.18-0.30
0.05-0.08
0.05-0.08x
0.05x0.09
1.84-1.87
1.50--1.60
0.50--0.80
0.55-0.64
0.72-0.88
0.84-0.94
0.15-0.25
0.20-0.22
0.11-0.16
0.13-0.15
0.32-0.36
0.30-0.33
0.32-0.39
Body(L)
Body(W)
Head
diameter
Muscular
esophagus(L)
Muscular
esophagus(W)
Nerve ring
from anterior
region
Intestinal
cecum (L)
Intestinal
cecum (W)
Spicule 1 (L)
Spicule 2 (L)
No of caudal
papilae
Pre-anal
Post cloacal
Adanal
Pedunculate
Valva from
posterior
extremity
Tail(L)
30-31
1.22-1.34
0.05-0.14
3.60--4.19
26.0--27.5
0.43-0.48
0.07
.09x
0.10-0.13
0.17-0.22
0.17-0.20
0.15-0.18
0.14-0.18
0.16-0.23
0.24-0.36
0.17-0.28
0.18-0.30
3.00--3.50
2.30--2.80
1.60-1.72
1.68-1.79
.40-0.49-
0.120.15
1.59-1.67
1.60-1.71
0.20
0.13--0.17
2.20-2.22
2.20-2.22
1.69-1.70
1.80-2.00
0.91-0.95
0.50--0.60
0.64
0.64
12-14
17
13--16
15
9-10
2
7
2
13
2
11
2
2
6
0.95
0.98
0.54--0.60
0.050.06
0.27-0.30
0.10-0.12
0.01
0.0600.07
0.05
0.025
0.05
102
Species
Host
Body(L)
Body(W)
Head
diatmeter
Lips(W)
Muscular
esophagus(L)
Muscular
esophagus(W)
Nerve ring
from anterior
region
Intestinal
cecum (L)
Spicule 1 (L)
Spicule 2 (L)
No of caudal
papilae
Pre-anal
Post-anal
Vulva from
posterior
extremity
Tail(L)
D.multiporus
(male)
D.multiporus
(femle)
D.sinjarii
(male)
D.sinjarii
(female)
D.dentatus
(male)
Pomadasys
olivaceum
6.10-7.50
0.20-0.29
Otolithus
argenteus
50-54
0.08-1.2
Otolithus
argenteus
10.5-11.1
0.33-0.35
Sillago
sihama
17.80-18.50
0.38-0.40
0.20-0.22
0.12-0.13
0.27-0.30x
0.24-0.26
0.31-0.38x
0.50-0.56
0.8-0.10
Pomadasys
olivaceum
6.50--7.90
0.25-0.30
0.0550.075x0.80.11
0.8-0.11
0.23-0.26
0.13-0.16
0.19-0.26
0.50-0.56
0.35-0.50
0.38-0.45
1.2-1.6
0.65-0.76
2.24-2.26
3.95-4.25
0.15-0.20
0.14-0.19
0.3-0.5
0.08-0.1
0.68-2.75
0.31-0.35
0.36-0.39
0.16-0.25
0.18-0.76
0.19-0.75
0.61
0.75
1.17-1.19
0.05-0.07
0.800.90
0.740.75
18
12
17
9
9--11
6
6
5
12
0.37
0.34
0.14
0.04--0.05
0.07
0.045-0.070x0.80.10
0.27
103
D.dentatus
(female)
Sillago sihama
28.4-32.5
0.45-0.50
D.ritai
Zaidi &
Khan
(female)
Species
D.Karachiensis
Bilqees et. al.,
(male)
D.Karachiensis
Bilqees et. al.,
(female)
D.cybii
Arya &
Jonson
(male)
D.cybii
Arya &
Jonson
(female)
D.magna
Khan &
Begum
(male)
Host
Pomadasys
olivaceum
Pomadasys
olivaceum
Cybium
gutattum
Cybium
gutattum
Sciaena sp
Rita rita
50-61
61-65
7.5-11.0
12.5-17.5
66.4671.60
23.0-27.2
1.5
2.52
0.08-0.27
0.33-0.53
1.72-2.03
0.19-0.26
0.20
0.21-0.29
0.16
0.24
-
10.140.16
0.08-0.12
0.05-0.07
4.32-4.7
5.10-5.1
1.06
1.07
4.10-4.17
1.90-3.64
0.42-0.46
0.97-1.13
1.18
1.60
0.40-0.44
0.14-0.16
1.08-1.15
0.25-0.38
1.39
0.50
0.12
0.48-0.74
0.36
0.62
0.22
0.34-0.35
0.090.12
1.70-1.71
1.70-1.71
0.05
0.10
1.70
1.76
25
13
30
4
21
8
5
20
10
0.50-0.59
Body(L)
Body(W)
Lips(L)
Lips(W)
Muscular
esophagus(L)
Muscular
esophagus(W)
Nerve ring
from anterior
region
Intestinal
cecum (L)
Intestinal
cecum (W)
Spicule 1 (L)
Spicule 2 (L)
No of caudal
papilae
Pre-anal
Post-anal
Valva from
posterior
extremity
Tail(L)
104
Species
D.quadrii
Zubairi & Farooq
(Male)
D.quadrii
Zubairi & Farooq
(Female)
D.sciaenae
(Male)
Host
Sciaena sp
Sciaena sp
Sciaena
diacanthus
Body(L)
Body(W)
Lips(L)
Lips(W)
Muscular esophagus(L)
Muscular esophagus(W)
Glandular esophagus(L)
Glandular esophagus(W)
Nerve ring from anterior
region
Intestinal cecum (L)
Intestinal cecum (W)
Spicule 1 (L)
Spicule 2 (L)
No of caudal papilae
Pre-anal
Post-anal
Valva from posterior
extremity
Tail(L)
9.5-22.74
0.25-0.51
0.088-0.128
3.055-3.300
0.060-0.14
-
11.4-27.2
0.14-0.35
1.90-3.64
-
15.81-22.74
0.3-0.51
0.088-0.128
0.055-0.072
3.005-3.300
0.108-0.133
-
0.160-0.266
0.288
0.4
5.2-5.3
5.4-5.52
23
19
4
0.349-0.450
-
0.228-0.348
0.048-0.072
5.2-5.3
5.4-5.5
23
19
4
8.9-10
0.120-0.166
105
0.1
20-0.166
106
107
108
109
110
111
112
113
114
115
116
117
118
120
121
122
123
124
bimaculatus in West Bengal; P.(S.) bilaspurensis (Gupta and Duggal, 1973) from
Mastacembelus armatus in Bilaspur; P.(S.) intestinecolas (Bashirullah and Ahmed,
1976) from Channa striatus in Dacca; P.(S.) inglisi (Bashirullah& Hafizuddin,
1973) from Clupisoma murius in Dacca; P.(S.) notopteri (Bashirullah&
Hafizuddin, 1973) from Notoptrrus notopterus in Dacca; P.(S.) timmi (Bashirullah,
1973) from Heteropneusies fossilis in Bangladesh; P.(S.) sprentii( Bashirullah and
Hafizuddin, 1974) from Heteropneusies fossilis in Dacca; P.(S.) ditchella (Gupta&
Garg, 1977) from Pellona ditchela in Nicobo Island; P.(S.) nainitalensis (Arya,
1978) from Barilius vagra in Nainital; P.(S.) kashmirensis (Dhar&Fotedar, 1980)
from Wallago attu in Kashmir; P.(S.) khatibi (Naidu and Murhar, 1980) from
Heteropneusies fossilis in Nagpur; P.(S.) ramteki (Naidu and Murhar, 1980) from
Heteropneusies fossilis in Nagpur; P.(S.) meszarosi (Arya, 1984) from
Mastacembelus armatus in Nainital; P.(S.) ritai (Misra, 1985) from Rita rita in
Lucknow;
127
During the present studies one new genus Spirocotyle n.gen. is identified and the
species S.otolithi n.gen. n.sp. is described. Two new species, P. (S.) riaziaii n.sp.
and P.(S.) ruberii n.sp.and one female specimen is also identified and reported
here. All these new species are recovered from Otolithus ruber from Karachi coast
Pakistan.
128
Family:
Spirocotyle n. gen.
Spirocotyle otolithi n.gen. n.sp.
Type Host:
Type Locality:
Location:
Prevalence:
Intestine
4% 13 host examined,( one infected with, one male
and one female.
Intensity:
Holotype (male):
Allotype(female):
JUW.N.20
JUW.N.21
Diagnosis: These are moderate sized worms, male is smaller than female.
The body of the worms tapers gradually at its anterior and posterior
extremity which is curved ventrally. The cuticle of the body is striated
throughout its length. The buccal capsule is oval in shape in both the sexes,
with simple well-developed basal ring. Inner surface of the whole capsule is
provided with 15 spiral thickenings. A prominent sucker is present at the
anterior region of buccal capsule. Muscular esophagus is shorter and
129
from the anterior end of the body, subterminal, 0.17 from posterior
extremity.
Remarks
The genus Spirocamallanus of family Camallanidae Railliet & Henry, 1915
and sub family Camallaninae Yeh, 1960 has spiral thickenings in the buccal
capsule. Similar nematodes were recovered during the present studies. The
genus under study resembles in the buccal with Spirocamallanus with some
differences in diagnostic features like, a prominent sucker in buccal capsule
in both male and female, size of the body, size of the esophagus, in number
of spiral thickenings and size of spicules in male specimen and pear-shaped
excretory vesicle in female specimen, three cuticular projections at posterior
end of female specimen. Therefore, it is desirable to propose a new genus
Spirocotyle. The genus name Spirocotyle refers to the sucker-like structure
in the buccal capsule and its relation to Spirocamallanus, the species name
to the fish host.
Generic Diagnosis: Camallanidae, spirocotyle n.gen. Camallaninae,
moderate sized worms. Buccal capsule is provided with 15 spiral
thickenings; a prominent sucker is present in buccal capsule; tridents absent;
esophagus divided into an anterior muscular, and a longer and wider
posterior glandular part. Posterior extremity in male, curved ventrally; tail
conical, caudal alae present, with 7 pairs pre-anal, 5 pairs post-anal, caudal
papillae, spicules unequal. Posterior extremity in female is flat with three
short, blunt processes; excretory pore terminal; vulva is sub terminal;
parasites of marine fish.
131
Type species:
Type locality:
132
Family
Sub family
Genus
Procamallanus(Spirocamallanus ( Olsen
1952) Petter, 1979.)
Synonymy:
Type Host :
Type Locality :
Location :
Intestine
Prevalance::
Intensity:
Holotype(male):
JUW. N.20
Allotype (female):
JUW. N.20
134
Remarks
The Spirocamallanoids are the parasites of the digestive tract of the hosts,
most frequently in the intestine and less often in the stomach and only
rarely in the swim bladder of fish.
Spirocamallanoids are equally dominated in Asia and South America, while
in North America, Africa and Australia these are less common. Sood(1982)
listed 75 species of Procamallanus(Spirocamallanus) from South Asia, of
which 9 species have been reported from marine fish of Karachi coast
Pakistan, including Procamallanus(Spirocamallanus) spiralis (Khan&
Begum, 1971) having 4 tooth-like structures at anterior end of buccal
capsule and tail is bluntly pointed with spike; P.(S.) pereirai (Rasheed,
1970) having 4 papillae and amphid on external circlet and 6 band-shaped
papillae on inner circlet of head and female has digit-like process on tail;
P.(S.) dussumieri (Bilqees et al., 1971); P.(S.) sihamai (Khan & Begum,
1971) the tail is slightly forked; P.(S.) crossohombii (Zaidi & Khan,1975);
P.(S.) sparus (Akram, 1975) 2 have sub-median papillae on mouth and tail
with spines in both sexes; in P.(S.) otolithi (Ashraf et al., 1977 ), the tail is
forked.
The present camallanid P.(S.) riaziaii belong to the morphological group of
Procamallanus(Spirocamallanus) species characterized by the presence of
three rows of cephalic papillae and pore situated near the inner margin of
cephalic papillae of the second circlet as observed by SEM., presence of
cervical alae, caudal papillae, two unequal spicules and forked tail with
digit-like projections . Many species of this group have been described from
different geographical zones, so it is impossible to make a through
135
Rigby and
Adamson (1997) and Rigby and Font (1997) are followed who used the
division of Procamallanus (Spirocamallanus) species according to
geographical zones by Andrade-Salas et al., (1994) for the comparison of
species. The present
Philppines. (Olsen, 1952; Noble, 1966; Machida and Taki, 1985); Rigby
and Adamson, 1997) from Indo-Pacific region, for comparisons with P.(S.)
anguillae (Moravec and Tarachewski, 2006). He mentioned the presence of
two digit-like projections of the broad tail in female. The present species is
similar to some morphological features with P.(S.) anguillae specially in
position of cephalic papillae and the pores situated near the inner margin of
cephalic papillae of the second circlet, as observed by SEM, during the
present studies. This has not been reported from similar species recovered
from Pakistan. But P.(S.)riazaii n.sp. is different from P.(S.) anguillae in
many morphological features including, absence of gubernaculums, length
136
137
5.14: Procamallanus(Spirocamallanus)ruberii
( Figs. 65-66)
Type Host:
Type Locality:
Location:
Intestine
Prevalence:
Intensity:
1.44
Holotype (male) :
Allotype (female):
Diagnosis: Moderate sized worms, the body of the worms tapers gradually
at its anterior and posterior extremity which is curved ventrally. The cuticle
of the body is striated at its anterior and posterior extremities. The buccal
capsule is oval in shape, surrounded by eight submedian cephalic papillae
arranged in two circles. Inner surface of the whole capsule provided with 16--18 spiral thickenings. With simple well developed- basal ring. Muscular
esophagus is shorter and narrower than glandular esophagus. Intesine
narrow, brown. Excretory pore slightly posterior to the anterior part of the
glandular esophagus. The tail is pointed in male and dull pointed in female.
Male(4 specimens, including holotype): Length of body 10.5-12.0,
maximum width 0.43.The wall of the buccal capsule is provided with 11-13
spiral thinkenings, 0.10x0.12x 0.11x0.14 in its diameter. The anterior
muscular part of the esophagus is 0.65- 0.77 in length and 0.15 at its
138
mazimum breadth. The longer posterior glandular part measures 0.84- 0.91
in length and 0.11 in its maximum breadth. The nerve ring is 0.24 from
anterior extremity. The spicules are similar in shape, unequal in length,
measuring 0.37 and 0.29 in length. Gubernaculum not observed. 12-14 pairs
of caudal papillae are present, including 4 pairs preanal, 4 pairs post anal and
4 pairs of subventral pendulacute papillae. The tail is curved, 0.19 long with
pointed end.
Female(6 specimens including allotype): Length of body 10.10, maximum
width 0.41. The mouth leads into a buccal capsule, it measures 0.09---0.10 in
its diameter, wall of the buccal capsule is provided with 13 spiral
thickenings, the anterior muscular part of the esophagus is 0.36 in length and
0.16 at its maximum breadth. The longer posterior glandular part
measure0.57 in length and 0.21 in its maximum breadth. The never ring is
0.27 from its anterior extremity. The valva is sub terminal, 0.10 from its
posterior extremity. Vagina muscular, directed posteriorly from vulva. The
tail is dull pointed
Remarks:
Several species of the genus have been described from Pakistan,
Procamallanus (Spirocamallanus) spiralis (Khan& Begum, 1971) from
Tachysurus caelatus in Karachi; the species was originally reported in
Heterobranchus anguillaris from Egypt. P.(S.) pereirai(Annereaux,1946)
after Rasheed, 1970 is described from variety of marine fish in Karachi, The
head bears four large submedian papillae and a pair of amphids in external
circle,the buccal capsule of the species have 8-10 spiral ridges and 11 pairs
of caudal papillae in male but in female the spiral ridges are 11-13 in
139
Karachi with 13 buccal ridges and 9 pairs of caudal papillae. P.(S.) sparus
(Akram, 1975) from Argyrops spinifer in Karachi, mouth bounded by two
pairs of submedian papillae and one pair of lateral amphids, caudal papillae
are 10 in numbers and tail is provided with spines. P.(S.) otolithi (Ashraf et
al., 1977 ) from Otolithus argenteus in Karachi; P.(S.) kalriai (Rehana &
Bilqees, 1979) from Wallago attu in Pakistan; P.(S.) karachii (Rehana &
Bilqees, 1979) from Wallago attu in Pakistan. But there are no electronscanning micrographs so it is difficult to compare with these species.
The present species P.(S.) ruberii is different from the standing point of
length and width of body, length of esophagus, number of spiral bands,
arrangement of papillae, spicule length, and also host, from the species
reported from South Asia including Pakistan.
The present species having ventrally bent posterior end of body, provided
with subventral pedunculate papillae is similar to P.(S.) longus (Moravec et
al.,2006). The present species is different from P.(S.) longus (Morevac et al.,
2006) having 22 ridges but there are only 16-18 spiral ridges in the present
species. The number and position of cephalic and caudal papillae in male
(except the first post anal, close to the anal region) are more or less similar
to P.(S.) longus (Morevec et al.,2006). The described species resemble only
140
by the shape of female tail (dull point) with P.(S.) colei (Rigby et
Adamson,1997) reported from coral reef perciform fish Acanthurus achiles
from French Polynesia. Deirids are absent in the present species but present
in P.(S.) longus, and also in P.(S.) colei.
141
5.15:
Type Host :
Type Locality :
Location :
Intestine
Prevalance :
Female specimen:
142
Remarks
By the shape of the female tail with a digit-like projection bearing two
terminal spikes, and in the same number of spiral ridges, this specimen
resemble P.(S.) anguille (Moravec et al., 2006) from the Indonesian shortfin
eel Anguilla bicolor from Thailand. P.(S.) monataxis (Olsen, 1952) have
also projection bearing two terminal spikes on female tail.
And was
originally described from a lethrinid fish from Hawaii (Olsen, 1952) and
later reported by(Rigby and Adamson, 1997) from fishes reported from
French Polynesia. However, since only female specimens are available from
Karachi coast, so it is assigned as P.(S.) anguille( Moravec et al.).
143
144
145
146
147
148
149
150
C.
C. callichori (Stewart,
151
studied the
Sood,( 1989) studied fish nematodes from South Asia. Petter and Sey,
(1997) described C. trachinoti from Tachinotus blochi.
Lakshmi, (2000)
155
156
Family:
Sub family:
Genus:
Type host:
Prevalence:
Intensity:
Holotype(male):
JUW. N. 40
Allotype(female):
JUW. N. 41
Remarks:
The genus Cucullanus Muller, 1777(Cucullanidae) contains a large number
of species parasitizing various fresh water and marine water fishes around
the world. Due to minute differences in the morphology and because of
inadequate descriptions, a detail comparison among species is very
complicated (Moravec et al., 1993) Therefore the present new species C.
aliyaii is compared with the species recovered from South Asia, especially
158
Pakistan and some related species from other parts of the world. The species
reported from marine fishes of Pakistan are all from fishes of Karachi coast.
These include C.armatus (Yamaguti, 1954) reported by Rasheed (1968)
from Tachysurus serratus; C. diminutus (Rasheed, 1968) from Stromateus
niger. Rasheed (1968) also reported C.hians (Dujardin,1945) from Lates
cacarifier, Sciaena sp., Belone strongylurus, Acanthopagrus berda and
Sparus sp. At the same time Rasheed described C. identatus from Polynemus
tetradactylus and Pristopoma hasta. He also redescribed C fastigatus
(Chandler, 1935) from Pristopona hasta. C. theraponi (Rasheed, 1968) was
described from Hilsa sp., and Therapon sp., C. bilqeesi (Petter, 1974) was
originally described by Bilqees et al., (1971) as C.elongatus from Erethistes
elongate and Petter renamed it as the species name was pre- occupied. C.
quadrii (Bilqees, & Fatima,1980) from Arius serratus; C. olivaceus (Akram,
1975-1976) was described from Tachysurus serratus and Pomadosys
olivaceus. Akram (1975-1976) also described C. sparus from Sparus spinifer
and Arius dussumieri and C. tachysuri from Tachysurus serratus and T.
dussumieri. Indocucullanus karachii (Zaidi & Khan, 1975) from the fish
Engraulis indica was transferred to the genus Cucullanus by Soota (1983)
with a combination as C. karachii.
Petter (1974) regarded C. tachysurusi as C. arabiense (Ali & Kalyankar,
1967) from Maharshtra, Mangalore and Karnataka. Petter (1974) restricted
its occurrence in Siluriform hosts and gave only three pair of preanal caudal
papillae for the species. Similarly he transferred Indocucullanus calcariferi
(Zaidi and Khan, 1975) to C. jaiswali (Ali, 1957). This species has been
reported from Puntius sarana, Lates calcarifer, Andhra Perdesh, Calicut and
Karala, India.
159
(Ali,
1956);
C.indica
(Agrawal,
1965);
C.
pseudotropi
Etymology:
163
164
165
6: HISTOPATHOLOGY
Histopathology is the study of tissue damage. Causes of tissue damage are of
varied nature including parasitic infections. Tissue damage could be
traumatic due to physical pressure exerted by the parasites or may be caused
by the toxic secretory or excretory products of the parasites which may some
times lead to hypersensitivity reactions. Many abnormal conditions may be
encountered in various organs infected with parasites.
Histopathology of fish is relatively a neglected field of study especially
histopathology caused by nematode parasites in Pakistan. . The study was
based of the intestine of two fish species of Karachi coast.
During the present investigation The intestine of the two infected fish
species including Euthynnus alletteratus (Refin.,1810) and Pomadasys
maculatum (Bloch, 1797)
nematode parasites.
long blind sac, as in all the tunas, extending almost the full length of the body
cavity. This originates at the anterior end and on the left side of the stomach.
It loops anteriorly across the ventral wall of the stomach and reaching the
proximal end of the body cavity on the right side, it runs directly back
without fold or undulation, to the vent.
work
has
been
done
on
histopathology
of
Euthynnus
infected
intestine
revealed
destruction
and
atrophy
of
intestinal
of villi and epithelial surface cells were dysplastic with loss of columner
orientation. In certain areas
villi
nearly 200 species of marine fish that are wide spread in tropical seas but also
range in to temperate water. The grunts are group of marine edible fishes. But
little is known of their histopathology. All grunts are carnivores in order to
find out a relation that may exit between the normal diet and the structure of
the alimentary tract, the functional anatomy of the digestive tract needs a
detail study. The alimentary canal of Pomadasys maculatum can
conveniently be regarded as divided into two main regions(Banki, 1936), the
Kopfdarm comprising the buccal cavity and pharynx, and the Rumpfdarm
comprising the forgut( Esophagus and stomach), midgut (Intestine) and
hindgut (rectum). Black (1930, 1936) and Rogick (1931) studied the
alimentary tract of fishes from American water, Suyehiro (1934), Ghazzawi
(1935), Al-Hussain (1947), Barmington, 1957; Kapoor (1958, 1975); Toor
168
histopathological
conditions
in
Pomadasys
maculatum
(blch.)
structures resulted into formation of large spaces at the periphery(Figs.8889). The muscular layers were also affected. Ulcerative lesions were
prominent at submucosal region(Figs. 88-89). Degeneration of tissues was
also obvious (Figs. 77-78). In more severe condition all the intestinal
morphology was lost. Villious structures was not differentiated and appear as
strings of tissues(Fig.85).
6.5: Remarks:
Present observations are similar to those described in other fishes of Karachi
coast with nematode larvae (Bilqees and Fatima, 1995). Other workers have
also reported enlargement and inflammation of intestine (Bullock, 1963).
Columnar epithelium cells line the intestine the microvilli layer has been
termed a stratified layer or brush border by Al-Hussaini (1947), Al-Hussaini
and Kholy(1950-1953); and ciliated epithelium by Ishida (1935-1936)
studying a variety of teleosts.Lile, 1998 studied the alimentary tract
helminthes of flat fishes. Miyazaki et al.,2006 observed infection by larval
nematodes which penetrate deeply into the stomach and intestine caused
formation of capsuler granulation. Akinsanya, 2007 observed mucosal
oedema, haemorrhage with haemosiderosis in some tissues of the fishes
infected by helminthes including Acanthocephala, Nematoda, Cestoda and
Trematoda.
170
From the very beginning of the twentieth century anatomists have paid a
great deal of attention to the structural details of the gastrointestinal tract of
the fish. The four basic histopathological layers such as serosa, muscularies,
submucosa and mucosa are present in the region from the esophagus to the
tip of the intestine, including the caeca. Among the vertebrates, only
teleostean fish species have appendages such as caeca at the gastrointestinal
junction (Khanna, 1961; Romer, 1970; Kent, 1983). The caecal development
appears to be intiated by a constriction between the stomach and intestine, the
role of constriction should be considered with caution since not all stomachbearing fishes have caeca (Suyehiro, 1942; Lagler et al., 1977).
The interest and research is being developed in the recent years in the applied
branches of functional morphology, which include structural changes and
parasitic diseases with contaminated situations resulting in abnormal growth
of cell with histopathological changes in fishes. Histopathology is an
important tool to observe the extent of tissue damage due to various
infections. Histopathology of intestine and stomach of some fish species of
Karachi coast has been carried out only by Bilqees and her coworkers,
including marine fishes Hilsa ilisha (Bilqees & Fatima, 1993) infected with
Anisakis larvae; and Rachycentron canadus (Khatoon & Bilqees, 1996)
stomach infected with Raphidascaris sp Cybium guttatum, ( Bilqees et al,
1998; Bilqees & Parveen, 1996) infected with nematode larvae; Otolithus
argenteus ( Khatoon & Bilqees, 1999); Lutjanus argentimaculatus ( Khatoon
et al., 1999a) stomach infected with Goezia species. and Anisakis gastric
granuloma has been described by (Khatoon et al. 1999b) in the fish Arius sp.(
Rizwana et al., 2000) described Goezia argentimaculatus from the fish
Lutjanus argentimaculatus from Karachi coast. In all these cases severe
171
destruction has been reported to the tissue. Other workers have also reported
enlargement and inflammation of intestine (Bullock, 1963).
The importance of intestine can be evaluated by analysis of the interaction
with effect of various parasites including the out side environment. The fish
digestive tract has more direct contact with parasites and the external
environment than any other internal organ. The food comes directly from
outside into the gut. So it may be accepted that any significant alteration will
induce some changes in the structure and function of the gut and its
diverticulae (Hussain, 1988).some studies have correlated environmental
changes with structural and functional variability of the fish gut (Tyler, 1973;
Singh and Bahuguna, 1983).It may be possible that tissue reaction may be
similar in two different fish hosts. an Anisakid nematode larvae found in
fishes are able to produce gastrointestinal lesions and diseases in human
being (Ishikura et al., 1993) Anisakid nematode are known to infest fishes
since last six centuries and lesion in marine mammals were reported about
two hundred years ago(Sakanari,1990). Public health significance of Anisakis
nematode is well known as cases of anisakiasis are being continuously
reported through out Europe, Japan, North America, Hawaii and several other
countries including Russia, Germany, Canada and Korea.
In fishes of Karachi coast anisakid larvae specially of genus Anisakis are one
of the most common type of larvae infecting viscera of various species
(Bilqees & Fatima, 1986) and these also have public health impotance
(Bilqees et al., 1999).In spite of severe Anisakis larvae infection in several
species of edible fishes of Karachi coast, this infection has not been yet
reported in human in Karachi. As these larvae are commonly found in several
172
174
175
176
177
178
179
7: DISCUSSION
The present research and investigated results provide information for food and
feeding habits, nematode parasites and histopathology of the infected intestine
of some marine edible fishes of Karachi coast; also provide preliminary
information on correlation between the investigated parameters.
180
Oscillatoria
and
Microsystis.(Cynobacteria),
Gyrosigma,
181
The nematode occurred generally in those months in which the fish stomachs
were gorged, full or 1/2 full. Which suggest the correlation between the
dietary habits and occurrence of nematodes parasites.
A total of 1500 fish specimens were examined for nematode parasites. In
herbivorous fishes (n=300) soil nematodes were found while in carnivorous
fishes (n=745) parasitic nematodes were recovered including new (n=131) and
184
new
genus
and
Spirocotyle
three
known
genera,
including
ii)
Seven new species identified and described here from the known
Dujardinascaris
(Baylis,
1947)
identified
and
described
genus
including
(Figs. 74-79).
surface(Fig.76).
inflammatory
reaction
was
obvious.
The
190
FUTURE PROSPECTIVE
Although a lot of work have been carried out on taxonomy and morphology
of nematodes parasite but still there are some more significant aspects on
which further work can be carried out in future.
191
8. REFERENCES
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a local siluroid fish Wallago attu. Allahabad Univ. Stud., 6 (2) sc. Sect,:
59-64.
Agarwal, S.C. 1958. On a new species of Procamallanus Baylis, 1923
(Nematode). Curr. Sci., 27 : 348-349.
Agarwal, V. 1965. Some new nematode parasites from fresh water fishes of
Lucknow Indian. J. Helminth., 17: 1-17.
Agarwal, V. 1966. On anew nematode, Procamallanus muelleri n.sp. from
the stomach of a freshwater fish, Heteropneustes fossilis. Proc.helminth.
Soc. Wash., 33 (2) : 204-208.
Agarwal, V. 1967. Some new Camallanoidea (Spirurida) nematodes from
fishes, Amphibians and Reptiles. Ann. Oarasit. Hum. Compar., 42(3): 327342.
Agersborg, H.P.K. 1918. Nematodes on marketable fishes. Science, 48: 493495.
Ajazuddin, S. 1991. Studies on the seasonal variation in gonads and
feeding habits of some common Sciaenids from the Karachi coast, M.
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249
Fish Host
Cucullanus Muller,
(1777)
Dichelyne Jugerskiold,
(1902)
Ecihnocephalus Molin,
(1858)
Heliconema Travassos
(1919)
Bulbocephalus Rasheed,
(1966)
Rahbdochona Railliet,
( 1916)
Parastromateus niger,
Heptochona Rasheed
(1964)
Cyrnea (Procynea)
Rasheed, (1965 )
Pampus spp.
Goezia Zeder,
(1800)
Lappetascaris Rasheed
(1965)
,
Raphidascaroides Yamaguti,
( 1941)
Sphyrna blochii
Paranisakis Baylis,
( 1923 )
Johnius sp.
Dujardinascaris Baylis,
(1947)
Philometra Costa,
(1845)
Procamallanus Baylis,
( 1923 )
Philometroides Yamaguti,
(1935)
Hepatonema Rasheed,
( 1965 )
Apolectus niger;
Neospinitectus Kalyankar,
( 1971 )
Neogoezia Kreis,
( 1937 )
Pampus spp.
Otolithus rubber
252