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FEEDING HABITS AND NEMATODE PARASITES OF

SOME FISHES OF KARACHI COAST

YASMIN AKHTAR

Department of Botany, Jinnah University For Women,


Nazimabad, Karachi, Pakistan.
2008

FEEDING HABITS AND NEMATODE


PARASITES OF SOME FISHES OF KARACHI
COAST

BY

YASMIN AKHTAR M.Sc, M.Phil.

THESIS SUBMITED TO JINNAH UNIVERSITY FOR WOMEN FOR


FULFILMENT OF THE REQUIRMENT FOR THE
DEGREE OF DOCTOR OF PHILOSOPHY (Ph.D.)
IN BOTANY

Department of Botany, Jinnah University For Women,


Nazimabad, Karachi, Pakistan.
2008

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----------------------------------

1.2: Fish and fisheries---------------------------------------

1.3: Pakistan coastline------------------------------------

1.4: Fish dietary habits--------------------------------------

1.5: Fish parasitic fauna (nematodes) --------------------- 9


1.6: Nematode diversity------------------------------------

11

1.7: Fish diseases ------------------------------------------

12

Objective of the present work--------------------------------------19

CHAPTER-2
REVIEW OF LITERATURE
2.1: Comprehensive account of feeding habits of fishes-- 21

2.2: Effect of temperature on food-------------------------- 22


2.3: Nematoda (Round worms) --------------------------- 22
2.4: Fish Pathology due to nematodes --------------------- 25

CHAPTER-3
MATERIAL AND METHOD
3.1: Study Area----------------------------------------

31

3.2: Collection of material--------------------------------

31

3.3: Method for the study of feeding habits ------------

32

3.4: Occurrence method ----------------------------------

32

3.5: Frequency of occurrence-----------------------------

33

3.6: Examination of material for feeding habits---------

33

3.7: Collection and Examination of specimen for


nematode parasites------------------------------------

34

3.8: Preparation of nematode specimen for SEM------

35

3.9: Procedure for histopathology----------------------

35

CHAPTER-4
RESULTS AND DESCRIPTIONS
FEEDING HABITS-----------------------------------

36

4.1: Table 1: Taxonomic position of different edible


marine fish species studied for their feeding habits
and nematode parasites.----------------------------38
4.2: Diets of different fishes-------------------------

39

4.3: Remarks -------------------------------------------

46

4.4: Statistical Analysis ------------------------------

51

4.5 Table 2-4: Food contents of different fish species


from Karachi coast ------------------------------------

52

4.6: Table 5: Occurrence of food categories in relation to


total number of stomach analyse of different marine
edible fishes from Karachi coast--------- ------------- 55
Table 5.1- 5.2: Statistical calculation of Table 5. - 56
4.7

Table 6-13: Frequency of occurrence in relation


to total number of stomach analysed of different
marine edible fishes of Karachi coast --------------- 58

4.8

Figures: 1-8 (histograms)-Comparison of the food


items in the gut of different edible fishes from
Karachi coast------------------------------------------- 66

4.9 Figures: 9-42. Photographic representation of some


organisms present within the stomachs of different
marine edible fishes---------------------------------72

CHAPTER-5
DESCRIPTIONS OF NEMATODES
5.1: History of the genus Dujardinascaris
Baylis,1947--------------------------------------------

77

5.2: Diagnosis of Dujardinascaris mujibi n.sp.--------Remarks-------------------------------------------------

79
81

5.3: Diagnosis of Dujardinascaris jello n.sp.------------ 84


Remarks--------------------------------------------------- 85
5.4: Diagnosis of Dujardinascaris maculatum n.sp.----- 87
Remarks--------------------------------------------------- 88
5.5: Diagnosis of Dujardinascaris sphyraenii n.sp.----- 90
Remarks-------------------------------------------------- 91
5.6: Diagnosis of Dujardinascaris multiporous n.sp.-- 93
Remarks--------------------------------------------------- 94
5.7: Diagnosis of Dujardinascaris sinjarii n.sp.--------- 96
Remarks--------------------------------------------------- 97
5.8: Diagnosis of Dujardinascaris dentatus n.sp---------- 100
Remarks-------------------------------------------------- 101
5.9: Table: (14-17) Morphological varations in the new
and known species of the genus Dujardinascaris
Baylis---------------------------------------------------- 102

5.10: List of figures:


Figs. (4345)Dujardinascaris mujibi n.sp.------------- 106
Figs. (4648)Dujardinascaris jello n.sp.----------------

109

Figs (4951) Dujardinascaris maculatum n.sp.-------- 112


Figs.(5254) Dujardinascaris sphyraenii n.sp.---------- 115
Figs. (5557)Dujardinascaris multiporous n.sp.--------- 118
Figs. (58)

Dujardinascaris sinjarii n.sp. ------------

121

Figs.(5960) Dujardinascaris dentatu n.sp.------------- 122

5.11: History of the genusProcamallanus(Spirocamallanus


Olsen, 1952)------------------------------------------------ 124
5.12: Diagnosis of Spirocotoyle otolithi n.gen. n.sp.-------128
Remarks---------------------------------------------130
5.13: Diagnosis of Procamallanus(Spirocamallanus)
riaziaii n.sp. --------------------------------------Remarks
---------------------------------------

132
134

5.14: Diagnosis of Procamallanus(Spirocamallanus)


ruberii n.sp. ---------------------------------------Remarks----------------------------------------------

137
138

5.15: Diagnosis of Procamallanus(Spirocamallanus)


female sp. ----------------------------------------------- 141
Remarks ----------------------------------------------- 142

5.16: List of Figures (6166)


Figs. (61): Spirocotoyle otolithi n.gen. n.sp---------------

143

Figs. (6264): Procamallanus(Spirocamallanus)


riaziaii n.sp----------------------------- ------- 144
Figs. (6566): Procamallanus(Spirocamallanus)
ruberii n.sp.------------------------------------147
Figs. (67): Procamallanus(Spirocamallanus)
Female specimen------------------------------ 149

5.17: History of the genus Cucullanus Muller, 1777-----150


5.18:Diagnosis of Cucullanus aliyaii n.sp.----------Remarks--------------------------------------------5.19:Figs. (68-69) ------------------------------------

156
157
163

CHAPTER-6
HISTOPATHOLOGY--------------------------------

165

6.1: Discription and distribution of Euthynnus


alletteratus(Refin, 1810)-------------------------------

165

6.2: Histopathology of infected intestine of


Euthynnus alletteratus----------------------------------

166

6.3: Discription and distribution of Pomadasys


maculatum (Blch, 1797)-----------------------------

167

6.4: Histopathology of infected intestine of


Pomadasys maculatum-------------------------------

168

6.5: Remarks------------------------------------------------

169

6.6: Figs. (70-89)-----------------------------------------

174

CHAPTER-7
DISCUSSION
7.1: Dietary habits of fishes---------------------

179

7.2: Seasonal variations in dietary habits-------

181

7.3: Correlation of dietary habits and nematode


parasites---------------------------------------

182

7.4: Parasitic diversity-------------------------

185

7.5: Histopathology of fishes-------------------

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

consisting of 255 families. It is the second largest phylum in the animal


kingdom encompassing 500,000 species. They are important parasites of
animals and plants and are of major medical and agricultural importance. They
are generally free living while the parasitic nematodes exploit a great variety of
hosts. Some nematodes are very important which cause pathological changes in
fishes. The diseases due to the adult and larval nematodes are very common in
marine fishes and are distributed all over the world. The parasites invade
various tissues and organs of fish, including skin, gills, eye, kidney, liver,
intestine, spleen, heart and brain. Parasitic infection tends to decrease the
growth rate resulting in stunning of fishes.
An investigation was conducted for food and feeding habits, nematode parasites
and histopathology of the infected intestine to get more information on this
subject as relatively little work was carried out previously. For the present work
a total of 1500 fishes belonging to 10 genera, 14 species, 10 families and 6
orders were collected from February 2005 to June 2007 from fresh landing of
fish harbor Karachi coast Pakistan.
The fishes under investigation were Liza vaigiensis, Sardinella albella,
Scomberomous gutattus, Pomadasys olivaceum, Pomadasys maculatum,
Pomadasys stridens, Otolithus ruber, Arius maculates , Sphyraena frosteri,
Sphyraena jello, Lates calcarifer, Sillago sihama and Euthynnus alletteratus.
For food and feeding habits 780 (out of 1500) fishes were dissected to analyze
the stomach contents. Almost all the samples from which complete digestive
tract were extracted (89%, n=700) had stomach content present whereas 10%
stomachs were empty. From the 89% extracted digestive tracts, 9 taxonomic
iv

categories were identified.


The percentages of occurrence of various food items were different in
carnivorous and herbivorous fishes. Planktons and detritus were the most
dominant food items in herbivorous fishes. Whereas in carnivorous fishes the
crustaceans, molluscs and miscellaneous items were dominating food categories
followed by teleosts (fishes). And the least observed food items were planktons
and polycheates.
The data obtained from the stomach contents of the investigated fishes revealed
the feeding habits of the fishes. From the graphical plots of stomachs against
the percentage frequency of occurrence, statistical analysis was performed.
Value of confidence interval falls within the limits, from which the current
results were satisfied.
During the analysis of food contents, nematode parasites were observed and
recovered. A total of 1500 fish specimens were examined for nematode
parasites investigations. No infection of nematodes was found in herbivorous
fishes, Liza vaigiensis and Sardinella albella. On the other hand, carnivorous
fishes (Scomberomous guttatus, Pomadasys olivaceum, Pomadasys maculatum,
Pomadasys stridens, Otolithus ruber, Arius maculates, Sphyraena forsteri,
Sphyraena jello, Lates calcarifer, Sillago sihama and Euthynnus alletteratus)
harbored different parasites. This is attributed to the fact that the carnivorous
fishes feed on other organisms, which may be serving as intermediate or
reservoir hosts. A prevalence of 62% was recorded and a total of 272 nematode
specimens were recovered including, new (n=131) and known (n=141,
previously described from Pakistan) nematode specimens. All infections
v

observed and recovered were restricted to the intestine. Identification and


descriptions were made possible by the help of literature provided by Rupert
Lee Research service of British museum and also by comparing the literature
obtained by Dr. Franick Moravec from institute of Parasitology, Czech
Republic Budejovice.
The microscopic examination and Steroscan electron microscopy (SEM) of
cephalic and tail regions of the 272 holotype and allotype nematodes was
carried out. Out of which 131 nematode specimens were new and 141 nematode
specimens were already recorded from Pakistan. The known nematode
specimens

belonged

to

genera,

including

Cucullanus

Procamallanus(Spirocamallanus), Dujardinascaris and Bulbocephalus. Only


the new nematode species are described here:
The investigated new nematode species belong to one new genus and three
known genera, including Spirocotyle

n.gen. ( Camallanidae Railliet and

Henry,1915); Dujardinascaris Baylis, 1947; Procamallanus (Spirocamallanus)


( Olsen 1952) Petter 1979, and Cucullanus Muller, 1777. From the above 4
genera, a total of 11 nematode species, (not reported in Pakistan yet) were
recorded as follows:
i)

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

from Pomadasys maculatum; D. dentatus n.sp. from Sillago sihama; D.


multiporous n.sp. from Pomadasys olivaceum; D. sphyraenaii n.sp. from
Sphyraena jello; and D. sinjarii n.sp. from Otolithus ruber.
iii)

Two new species of genus Procamallanus (Spirocamallanus) (Olsen, 1952)


Petter, 1979), Procamallanus (Spirocamallanus) riaziaii n.sp. and

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

maculatum . The intestine of Euthynnus alletteratus, infected with nematode


species revealed various stages of necrosis, degeneration and morphological
alteration in villi of the intestinal tissues. The infected intestine of Pomadasys
maculatum with nematode showed severe damage to some parts of intestine
involving whole thickness of the bowl wall, atrophy of surface tissue and villi.
All the layers were involved with sloughing, flatting and fusion of villi.

vii

INTRODUCTION

1.1 Importance of fishes


Fishes are one of the most important groups of vertebrates, which benefit
human being in various ways. Fishes were used even at prehistoric ages and it
was supposed to be beneficial to long life and intelligence (Hamilton, 1971).
Many countries are working to search out the importance of fishes for men. A
study conducted in Netherlands reported that eating a pound of fish a week
could reduce the coronary heart diseases in man. Some fishes specially cold
water species such as cod, salmon, mackerel and sardines contain some oils that
are not found in other food and have major effects on body chemistry, which
reduces the tendency of blood to clot and helps in lowering cholesterol level in
the blood.In manufacturing of color paints and margarine, oil of herring,
meckeral and salmon are used commercially. The medical value of fish oil
cannot be ignored, many patients who are suffering with lack of vitamin A and
D, use oils of cod and sharks. Scales of fishes are used for decorations of
houses. Skin of fishes has its own importance in leather industry.
Fish and other marine life are also used for many other uses, pearls and
mother of pearls, shark skin and rayskin. Sea horses, star fish, sea urchin and
sea cucumber are used in traditional Chinese medicine. Tyrian purple is a
pigment made from marine snail, Sepia is a pigment made from the inky
secretions of cuttlefish.(Wiwikipedia.Org. Fish as food). In manufacturing of
soap, oils of fish are mostly used. It is also used in fungicides and
insecticides.For supply of adrenaline and insulin, pharmaceutical companies
use-frozen adrenal glands and pancreas. For the production of glue skin
1

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

Pakistan is one of the protein-deficient countries of the world. There is no


carbohydrates, no dietary fibers because many high on the food chain are highly
contaminated with environmental chemicals and parasites. Due to the
importance of fish, in a large part of world especially where there is a high
potential for development of fisheries, people are expanding and industrializing
their fisheries and improving their living conditions by utilizing the fish catch
more effectively. Japan has long been the leading nation in fishing recovering
about 74 percent animal proteins from fish. In Pakistan the Karachi coast and
many other lakes and canals are present. Due to availability of port at Karachi
(Sindh), the fish supply is abundant, but the cost is high for poor families and
they suffer for protein and balance diet.

1.1 Fish and fisheries


Pakistan has a coastline of 1,050 km and a total fishing area of approximately
300,270 sq. km. Pakistans fishing waters are termed as highly rich in marine
life with a vast variety of species having great commercial value. Pakistans
consumption of fish is very low, and thus most of the produce is exported. Most
of the fish catch is marine which comprises 71% of the total fish exports
(SMEDA, 2002). An analysis of the current status of the more important fish
stocks is made yearly (MFD, 2002). Various fleets fishing along the coast of
Pakistan share these stock.. The party boat fishery, in which fishermen rent
space abroad a boat for a day or more, has been popular in Karachi. Fishing
from private boats, shorelines, piers and jetties is also very popular (Neelofer,
1995).

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

environmental conditions are generally tropical and subject to monsoon during


the summer to Autmen. Upwelling of cold, nutrient-rich, low-oxygen water
occurs all year round but is stronger during the Southwest monsoon period and
greatly effect the distribution and and migration of the fish in the region.
One fifth of the worlds populations live in some of the least developed nations
around the rim of the Indian Ocean. These nations are dependent on their
environmental, coastal and marine resources. In the recent years it has become
clear that man is capable of disturbing the natural system of our planet on
global scale, including the oceanic system. Coastal zones are one of the most
important national assets of a countary where socio-economic activities are
highly concentrated. Coastal marine resources have an immense potential in
4

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.).

1.2 Pakistan coastline


The coastline of Pakistan extends 1,050 km (650 mi), 250 km falling in Sind
province and 800 km in Balochistan. It borders the productive NE Arabian Sea
famous for its upwelling phenomenon. Its Exclusive Economic Zone (EEZ)
covers an area of 196,600 sq.km and the territorial waters cover an area of 24,000
km2. The continental shelf of the Sindh coast extends to a distance of 150 km
whereas that of Balochistan only measures 15-40 km. The prevailing ocean
current direction is clockwise during the southwest monsoon season and anticlockwise during the northeast monsoon season. The salinity value is generally
36 ppt. Tides are neither very high nor very low, but intermediate; the mean
average height is about 10-11 feet. Tides are higher on the eastern side and their
velocity is generally between 1-2 knots but may increase to 4 knots in narrow
creeks. (Wildlife Biodiversity of Pakistan).
Because of a combination of wind and earths rotation, the summer monsoon
pushes water away from the Somalian coast and edge of the Arabian Peninsula.
The water that leaves these coastal areas is replaced by water that wells up from
depths and is very high in nutrients. In the winter, the monsoon reverses and
blows from the northeast. This monsoon does not have as much impact because
it pushes water towards the Arabian Peninsula resulting in down welling, not
upwelling. However, the strong winds cause turbulent mixing, which brings up
some nutrients, but not on the scale of the summer monsoon. The productivity
of the Arabian Sea increase dramatically with an increase in nitrate. This

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.

1.3 Fish Dietary habits


As a group, bony fishes have a diverse range of food preferences.(a) Bony fish
may be Herbivorous (plant eaters), (b) Carnivorous (meat
eater), (c) Detritivorous (that eat decomposing plants and animals).Bony
fishes can eat all sizes of plants and animals. The amount of food a bony
fish eat is directly related to its size, its metabolic stages and the temperature of
its environment.
Nature offers a great diversity of organisms that are used as food by fish and
these differ in size and taxonomic group.Smaller fishes generally have a higher
metabolic rate as compared to the fishes of the same species, thus small fishes
generally eat more relative to their body size. Fishes are cold blooded that is
8

body temperature is determined by the temperature of their environment. Warm


water fishes generally have higher metabolic rate and require more food than
cold water species of the same sizes.
Herbivory is the main route by which photosynthetic energy is transferred to
marine organisms ( Elton, 1927). Marine herbivorous fishes have a great
diversity of gut microorganisms. Despite their importance in terms of
microorganisms structural elements to cell contents. According to (Hata and
Kato,2002) the non-weeded species were more nutritious than the weeded
species. Fish eat other fish that eat planktons and algae, which are contaminated
with environmental pollutant because these chemicals are concentrated in the
fat of the fish. Fish most heavily laden with chemicals are those such as tuna,
swordfishes and sharks, which are predators of smaller sea life. Several
illnesses are a result of algal toxic blooms. For example most commonly
reported marine toxic disease in the world is ciguatera, which presents primarily
as diarrhea, abdominal cramps, vomiting, pain on urination and heart block.

1.4 Fish parasitic fauna (nematodes)


Helminths are an important group of animal parasites occurring in the adult
stage usually in vertebrate hosts, practically invading every organ system of
the host, and in the larval stage in the invertebrate hosts.These worms are
widespred in almost all animals in every part of the world, though the
intensity of infection may differ from time to time or place to place and they
produce a wide variety of direct effects, thus they play a vital role in
undermining the welfare of man and the animal he is associated to smaller or
greater extent. The later is mainly responsible for the development of the
helminthological research.
9

Helminth parasites of fish in marine system are often considered to be


generalists, lacking host specificity for both intermediate and definitve hosts. In
addition, many parasites in marine water posses life cycles consisting of longlived larval stages residing in intermediate and parasitic host. These properties
are believed to be adaptation to the long food chains and the low distribution of
organisms over broad spatial scales that are characteristic of open marine
system. Moreover such properties are predicted to lead to the homogenization
of parasitic communities among fish species.
Fishes are the predator- prey pyramid within fresh water as well as in marine
water and therefore tend to be infected by a considerable range of parasites,
which occur in large number. Most helminth parasites carried by fishes are
nematodes, acanthocephala, cestodes and trematodes.
Ones the helminth has reached its residence in the definitive host, its primary
concern is to secure nourishment. For this purpose it has usually chosen a
position, where digested or semi-digested food is abundantly supplied.
About one thousand species of fishes are found in marine and fresh water in
Pakistan. Majority of these are edible. And very few are examined for their
nematode parasites. The nematodes or roundworms (Phylum Nematoda from
Greek (nema): "thread" + - -ode "like") are one of the most common
phyla of animals, with over 20,000 different described species (over 15,000 are
parasitic). They are ubiquitous in freshwater, marine, and terrestrial
environments, where they often outnumber other animals in both individual and
species counts, and are found in localaties as diverse as Antarctica and oceanic
10

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.

1.5 Nematode Diversity


Nematodes of marine fishes exhibit great biodiversity. These are usually
nonspecific. One nematode species can be found in various fish host. While
several different nematode species can be found in one fish. Biological diversity
is a measure of the relative diversity among organisms present in different
ecosystems. Diversity in this definition includes diversity within species and
among species, and comparative diversity among ecosystems. The other
definition of diversity is the totality of genus, species, and ecosystem of a
region (Heip et al.,1985), however species richness varies much among
habitats. The presence of one species of nematode in a fish indicates that he is
eating or swimming in a determinate area of the sea(bentonic, planktonic or
migratory).

11

Biodiversity found on Earth today is the result of 4 billon years of evolution.


New species are regularly discovered and many though discovered, are not yet
classified. Biodiversity has contributed in many ways to the development of
human culture and in turn, human communities have played a major role in
shaping the diversity of nature at the genetic and ecological levels benefits of
biodiversity. Diversity is the most important parameters used in the description
of a community. Several theories relating diversity to other phenomena such as
predation, competition and stability have been proposed (Pianka, 1966) As a
result of the increasing interesting diversity a number of studies have appeared
during recent years an important feature of nematode communities, perhaps the
most important in understanding their ecological success, is the large number of
species present in any one habitat usually an order of magnitude greater than for
any other major taxon. Certain host features, i.e. host body size and host diet,
appear to influence the total number of parasite species exploiting a host
species, whereas other host features, i.e. depth range, appear to influence the
variety of parasites taxa that a host will accumulate over evolutionary time
(Luque & Poulin, 2004).
The Karachi coast has rich fish fauna and favorable hosts of nematodes. These
nematodes belong to several different families, subfamilies and genera. The
nematodes of fishes of Karachi coast exhibit great biodiversity; one species
infecting several fish hosts and one fish may be infected with several nematode
species (is given in tabulated form at the end of thesis).
1.7: Fish disease

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

parasites may have widely differing

effects on different host species.


There is no doubt that every parasite which lives internally or externally in
fish, exerts some harmful influence on the basic phenomena of life of their
hosts, for example life span, life cycle, abundance, distribution, metabolic
performance, nutritional requirements, growth, reproduction, evolution as well
as organism tolerances to natural and man-made environmental stress
(Kinne,1980 ). The host reaction may be expressed in tissue proliferation,
degeneration, and inflammation and probably in the development of immunity
as described by Bauer ,1958; Davis, 1953; Reichenbach- Klinke and Elkan
,1965; William and Jones, 1967; Smith and Wooten, 1978.
Cross (1933) showed that the parasitic infection tend to decrease the growth
rate resulting in the stunting of fish. Sinderman and Rosenfield, (1954) studied
the migration of herring on the basis of their parasites and showed that the kinds
13

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

guttatus, Pomadasys olivaceum,

Pomadasys maculatum, Pomadasys stridens, Otolithus ruber,


forsteri, Sphyraena jello, Lates calcarifer and

Sphyraena

Sillago sihama are popular

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

diseases of marine fishes (Petrushevsky and Kogteva, 1954; Sindermann and


Rosenfield, 1954; Getsevichyute, 1955; Bauer, 1958; Amlacher, 1961;Dogiel,
1962; Mikhailova et al., 1964; Sindermann, 1966; 1970; Andreessen, 1970;
Williams and Jones, 1967; Roberts, 1978a; Kinne, 1980; Kim et al., 1991;
Iskikura et al. 1993; Meunier & Desse, 1994; Amin et al., 2000; Akinsanya,
2007.
Most work in Pakistan was carried out by Bilqees and her coworkers.
Bilqees (1993) published dictionary for terminology of diseases, and for
pathological and histopathological terms commonly used. Bilqees and Fatima,
1986 reported Anisakis larvae from the fish Cybium guttatum. Bilqees and
Fatima (1993) also reported that the intensity of infection may be as high as
90% in Hilsa ilisha. The histopathology of the liver, stomach and intestine
infected with Anisakid and other larval nematodes were also studied by
(Bilqees and Fatima, 1993; 1995; 2000; Bilqees & Khan, 1994; Bilqees &
Parveen, 1996; Khatoon & Bilqees, 1996; 1999; Khatoon et al., 1999a; 1999b.;
Bilqees et al., 1993;1998; 1999; 2001).

18

OBJECTIVES OF THE PRESENT WORK


The objective of the present work is to study the dietary habits, nematode
parasites of marine fishes of Karachi coast, Pakistan, including the knowledge
about fish pathology by nematode parasites.

Meticulous literature survey

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

3: Infestation caused by these endoparasites is analyzed as stated by


Kabata,(1985) parasite and disease reduce fish production by effecting the
normal physiology of fish. And which, if left uncontrolled can result in mass
mortalities, or in some cases, infection of man and other vertebrate that
consumed them.

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;

Hajisamae et al., 2004;

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

2.2 Effect of temperature on fish food


The fish consumes less food at low than at high temperature. The temperature
changes influence food consumption directly or indirectly (Belding, 1928;
Baldwin, 1956; Molnar and tolg, 1962; Keast, 1968. Under natural condition food
consumption of most fishes changes with age and therefore, with size occurring in
different seasons. Smaller fishes generally have a higher metabolic rate than large
fishes of the same species. Thus small fishes generally eat more relative to their
body size. Fishes are cold blooded; their body temperature is determined by the
temperature of their environment. Warm water fishes generally have higher
metabolic rates and require more food than cold-water species of the same size.
Food organisms of different species of fish in any region may influence
respectively the horizontal and vertical movement of the fish stock; hence a correct
knowledge of the relationship between the fishes and food organisms is essential
for the prediction and exploitation of the fish stock.

2.3 Nematoda (roundworms)


Parasite assemblages of marine fishes include an important number of larval stages
of helminth parasite species that use fish as intermediate or as paratenic hosts.
Roundworms called nematodes are the most common parasite found in marine
fishes.
Nematodes have long been known to parasitize marine fish and are found
throughout the seas of the world

(Baylis,1923;1932; Kulkarni, 1935;

Annereaux,1946; Karve & Naik, 1951; Ali, 1960; Dogiel et al., 1961;
1962;Yamaguti,1961;

Lal,

1965;

Chakravarty,

1932;

1942;

Chakravarty&Mujumdar, 1959; 1960; Chakravarty et al., 1961; Sood, 1967;


1988; 1969;

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;

Ahmed&Rehman,1979; Gupta&Gupta, 1979; 1980;

Moravec, 1979; 1983; 2001; Dhar&Fotedar,1980; Bilqees & Fatima, 1980a;


1980b; 1986; Arya,1980;1990;Dhar&Fotedar,1980;Ahmed,1981; Bilqees &
Akram, 1982; Malakhov & Valovaya, 1984; Fatima & Bilqees, 1987; 1989;
Goldberg et al., 1991 Boomker, 1993; Duran et al., 1989; Laakshmi & Sudha,
2000; Lakshmi, 2000a,b; Damin el al,.2004; Moravec et al.,1993;1997;2000;
2003; 2004; Ana, et al., 2004; Luque et. al., 2004; Moravec & Lou, 2005;
Moravec &Taraschewski, 2006; Ayotunde et al 2007; Cruz et al., 2007).
Yamaguti (1961) listed about 300 species, representing more than 40 genera in
17 families from marine fishes. A considerable number of new species and
genera have been added recently and many more remain to be discovered.

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

Muraenesox(Forsk.); Porrocaecum ruberum, Procamallanus dussumieri. They also


reported Dujardinascaris sciaenae from Pseudosciaena diacanthus(Lac.) in
(1977a). Khan and Begum (1971) described heliminth parasites of fishes from West
Pakistan ( Pakistan). Rasheed (1965) reported a new nematode Lappetascaris
lutjani (Anisakidae: Ascaridoidea) from marine fishes of Karachi coast. Also were
reported cases of larval nematodes parasitizing fishes in the coast from
Pakistan.Bilqees and Rashid (1982) reported Contracaecum otolithi from Otolithius
argenteus(Cuv.). Bilqees and Fatima (1986) reported larval stages of Contracaecum
and Anisakis from the fishes, Cybium guttatum(Schn.), Pseudosciaena diacanthus
(Lac.), Muraenesox cinereus (Forsk.),

Parastromateus niger (Bl.), Pampus

argenteus (Euph.), Arius serratus(Ham.),


olivaceum(Day.),

Chiloscyllium

Hilsa ilisha(Ham.), Pomadasys

griseum

arcticus(Faber), Mugil sp.(Mugilidae), and

(Muller&Hen.),Galeocerdo

Stegostoma varium (Hermann), of

Karachi coast, Pakistan.


Species of marine fish nematode reported so far from fishes of Karachi coast belong
to various families and genera. According to a recent checklist Akhtar& Bilqees,
(2006) 71 species of nematodes belonging to 23 genera, 9 sub families and 7
24

families from 68 species of marine fishes belonging to 46 genera and 31 families


have been reported from karachi coast of Pakistan. Of 71 species of nematodes
about 18 are from family Cucullanidae Cobbold, (1864), 21 are from family
Heterocheilidae(

Railliet&

Henry,1905)19

species

from

family

Camallanidae(Railliet& Henry,1915), 4 species from family Philometridae Baylis&


Daubney(1926),2 species from family Gnathostomatidae Railliet(1895), 3 species
from family Physalopteridae Railliet (1893), and 5 species are from family
Rhabdochonidae Skrjabin, (946). (Checklist is attached).
2.4 Fish pathology due to Nematodes
Various parasites have been reported from many fishes and information about
these parasites is increasing day by day. In recent years much attention has been
paid on the studies of parasites. The diseases due to the adult and larval nematodes
are very common in marine fishes and are world wide in distribution. The parasites
invade various tissues and organs of fish. Among the known sites of infection are
the stomach, intestine, liver, gonads, visceral mesenteries, peritoneum body cavity,
blood vessels, swim bladder, and connective tissues, fin, orbits of the eye and
brain. Most species of nematodes in adult stage live in the alimentary canal except
the family Philometridae which are found in body cavity, liver and gonads.
There are hundreds of published reports on naturally occurring larval nematodes
in fish including several reports from Pakistan. It is known that larvae are more
harmful than adults and can penetrate in the tissues of various organs, causing
severe tissue damage and destruction of cell of the organ. Most of the researches
have been done and are being added are towards the diagnosis, description and
analysis of the diseases of the marine fishes (Bauer,1958; Dogiel, 1962;
Getsevichyute, 1955; Mikhaylova, et al., 1964; Petrushevsky and shulman, 1955;
25

Reichenbachklinke, 1965;Sindermann, 1966, 1970; Lagler, 1977; Robert, 1978;


Smith and Wootten, 1978; Kinne, 1980; Deardorff et al 1987; Roberts, 1978;
Kinne, 1980; Kabata, 1985; Iskikura et al. 1993; Meunier & Desse, 1994; Bernet
et al., 1999; Konishi, and Sakura, 2002; Miyazaki et al.,2006; Akinsanya, 2007.
Sindermann (1970) has quoted a total of 555 references devoted to diseases of
marine fishes, of these only 27 appeared before 1900. The motivation for this
impressive increase on fish disease research is an attempt to avoid economic losses
and to disclose the life histories of causative agents, which may also interfere with
human health.
Attempts have been made to study the histopathology of organs of various fish
species of Karachi coast infected with Anisakid and other larval nematodes
(Fatima & Bilqees, 1989;

Bilqees, 1997; Bilqees and Fatima, 1993; 1995;

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;

Echinocephalus sp.(Bilqees and Fatima,1986). Bilqees (1993) published


dictionary of pathology and histopathology. In 1996, Bilqees and Parveen
discussed the pathological variation in the tissues of stomach of Cybium
guttatum (Bl.&Schn.) of Karachi coast parasitized with nematode larvae while
tissue eosinophilia in same fish associated with nematode larvae reported by
Bilqees et al.,(1998), also discussed the public health importance of the
infection. Khatoon et al., (1999) reported Goezia sp.(Zedar.) from the stomach
of Lutjanus argentimaculatus(Forsk.) and discussed the histopathology of
stomach showed severe destruction in the whole thickness of stomach wall, with
gastric mucosa partly or completely destroyed in the affected regions. Their
study showed that destruction and necrosis of all layers of stomach has occurred
depending on the extent of penetration of the nematodes. Rizwana (1999)
reported the high infestation rate in Lutjanus argentimaculatus (Forsk.) by the
larval stages of Anisakais and Contracacum in approximately all fishes but
smaller group of fishes were more infested as compare to larger one. According
to her it might be due to the consumption of more crustaceans by the smaller
fishes. Rizwana et al., (2000) also recovered Goezia argentimaculatus from
Lutjanus argentimaculatus (Forsk.)
Many authors in other parts of the world have worked on Anisakis nematodes.
Agersborg (1918) reported nematodes on marketable fishes. Snieszko (1970)
described fish diseases. Bauer (1958) described relationships between host fish and
their parasites. Bishop and Margolis (1955) examined the prevalence of larval
Anisakis nematodes in herring ( Clupea pallasi) of the British Colmbia coast. Tsai
and Cross (1966) reported Anisakis like larvae from marine fish of Taiwan
27

(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

first known case of Anisakiasis in Denmark. Deardorff et al., (1987) described


human Anisakiasis with two case reports from the state of Washington. Little,
(1973) report Aniskid larvae from throat of a woman in New York. According to
Kim et al., (1991) Anisakiasis can cause intestinal obstruction. Anisakiasis of
colon also occurs which is rare as compared to gastric anisakiasis (Minamoto et al.,
1991; Matsumoto et al., 1992). Bhargava et al., (1996) reported the first tonsillitis
case associated with Anisakis infection. Ruben et al., (2001) reported seven humen
cases infected by Pseudoterranova decipiens (Nematoda, Anisakidae) in Chile.
Camallanus species infect the gastrointestinal tract of fishes. Camallanus species
can be identified by their red color; their location further toward the posterior of
the intestinal tract than other worm-like parasites (typically very near, and often
protruding from, the anus of the fish); the presence of a buccal capsule (mouth
structure) that is divided into two lateral valves, giving the mouth a slit- like
appearance; and, if gravid females are present, the presence of both eggs and larvae
within their bodies. The spirocamallanids are the parasites of the digestive tract of
the host, most frequently in the intestine and the less often in the stomach and only
rarely in the swim bladder.
Camallanid nematodes are also common in Pakistan and other parts of the world.
Procamallanus(Spirocamallanus)mehrii (Agarwal, 1930); P. (S.) planoratus(
Kulkarmi, 1935); P. (S.) pereirai (Annereaux, 1946); P (S.) bagarii( Karve&Naike
,1951); P.(S.) ahiri (Karve, 1952); P.(S.) mysti (Karve, 1952) ; P.(S.) saccobranchi
(Karve ,1952) P.(S.) aspiculus (Khera, 1955);P.(S.) gubernaculus (Khera,1955);
P.(S.) heteropneustus, , P.(S.) hyderabadensis from Mystus seenghala, P.(S.)
singhi (Ali, 1956); P.(S.) mozabukae (Yeh, 1957); P.(S.) daccai (Gupta, 1959);
P.(S.) confuses (Fernando& Furtado, 1963); P.(S.) hindensis (Lal ,1965)
Heteropneusies fossilis in Meerut; P.(S.) istiblenni (Noble, 1966); P.(S.) vittatusi
29

(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;

Procamallanus (Spirocamallanus) (Olsen 1952) Petter 1979), and Cucullanus Muller,


1777. A total number of 11 new species were recovered from the above 4 genera.

30

3: MATERIAL AND METHOD

3.1 Study Area:


Pakistan is located in the northern part of the Arabian Sea a coastline of 1,120
Km. with broad continental shelf. There are more than 16,000 fishing boats in
coastal area of Pakistan, which operate in coastal water as well as in offshore
areas. Karachi is one of the major fish harbor of Pakistan, handles about 90% of
fish and sea food catch in Pakistan. (Pakissan.com. 2001-2007).

3.2 Collection of material:


A total of 1500 fishes belonging to 14 species, 10 families and 6 orders were
collected monthly during February 2005 to June 2007 from fresh landing of fish
harbor Karachi coast, Pakistan. The fishes were examined fresh or preserved
whole in 10% formalin for later examination in Laboratory of Jinnah University
for women. After washing on subsequent days, the fishes were identified
(Qureshi, 1955; Fishers and Bianchi, 1984; FAO Field guide; Hoda, 1985;
Majid and Khan, 1995; Eschmeyer, 2001 and by fin-formula method). The
length and weight of each fish in the sample were taken from the tip of snout to
the end of caudal fin using measuring scale and weighting by using Bango
digital scale.
The fishes under investigation were Liza vaigiensis, Sardinella albella,
Scomberomorus guttatus, Pomadasys olivaceum, Pomadasys maculatum,
Pomadasys stridens, Otolithus ruber, Arius maculates, Sphyraena forsteri,
Sphyraena jello, Lates calcarifer, Sillago sihama and Euthynnus alletteratus.

31

The investigation on fishes was conducted as follows:


a): Food and feeding habits.
b): Nematode parasites.
c): Histopathology.

3.3 Method for the study of feeding habits:


A total of 780 (out of 1500) fishes were dissected to analyze the stomach
contents. Almost all the samples from which complete digestive tract were
extracted (89%, n=700) has stomach content present whereas Only 80(10%)
of stomachs were empty. From the 89% extracted digestive tracts, 9 taxonomic
categories were identified.
Various techniques are available to scientists when undertaking the gut analysis
of fish. The simplest available method takes organism occurrence as as the main
consideration. The analysis of the stomach contents was carried out by
percentage occurrence of stomachs and Frequency of Occurrence methods
(Hyslop, 1980).
3.4 Occurrence method (Hyslop, 1980),
The number of stomach in which a particular food category occurs is listed as
a percentage of the total number of stomach of fish species containing food in
the gut (Table 5, 5.1, 5.2). This method is qualitative, laying emphasis on the
frequency of occurrence of items in the gut contents. The analysis of
percentage of each food category was summed divided by the total number of
stomach in the sample (excluding those with empty stomach) and calculated
by using the formula given below;
32

No. of stomachs in which particular food category occurred


---------------------------------------------------------------------

X 100

Total number of stomachs examined (Non-empty)


3.5 Frequency of Occurrence (Hyslope, 1980)
Another method used for assessment of food items was frequency of
occurrence (F. F %) in relation to total number of stomachs. (The number of
stomachs in which a food item occurred was expressed as a percentage of total
number of stomachs. (Table 6- 13)
3.6 Examination of material for feeding habits
For this purpose the fishes were dissected and the stomachs were removed,
weighed and persevered in 8 % formalin solution. In laboratory the samples
were removed from the jar. The content of each gut were mixed with 100 ml
water per gram of gut contents to remove unpleasantness of the formalin and
filtered through 100 um and 500um mesh size. Caution was taken not to leave
samples in the water for more than 48 hrs to prevent the sample from
deteriorating. An attempt was made to identify the food items to species. But
the level of discrimination depended on the completeness of the food items.
Polychaetes, small crustaceans and some fishes were particularly difficult to
identify as they were rapidly digested and were rarely in good conditions. For
phytoplankton, the microscopic preparations per filtrate were observed under
the microscope for taxonomic identification. Food contents were grouped into
9 categories such as:
(1) Polychaetes, (2) Crustaceans, (3) Molluscs, (4) Platyhelminth, (5)
Nematyhelminth, (6)

Teleosts (fishes), (7) Planktons, (8) Detritus (9)

Miscellaneous.
33

Platyhelminth and Nematyhelminth were not the food items but were the part
of food content.

3.7: Collection and Examination of specimens for nematode parasites:


A total of 1500 fish specimens were examined for nematode parasites
investigation. 745 fish specimens were infected. A prevalence of 62 %
was recorded and a total of 272 nematode specimens (including 131 new and
141 known specimens) 37 damaged specimens were kept for DNA sequences.
Only the new nematode species are described here. All infection observed and
recovered were restricted to the intestine.
In order to collect the parasites the body cavity of fish was opened and the gut
and liver were removed by cuts in the region of the anus and the division
between esophagus and anterior stomach. The mesenteries and connective
tissues connecting loops of the gut and the liver were cut and the organs
separated. The gut was then placed in a large Petri dish stretched out and cut in
to five regions i.e. the stomach, the anterior middle and posterior intestine and
the rectum. The division of the intestine was equivalent to one third of the
whole intestinal length. The section of the gut was opened with a longitudinal
cut, and the whole inner surface lightly scraped to remove the parasites with
mucus. The species of nematode parasites in each region of the gut was
recorded. The nematode found were washed in physiological saline water and
then fixed in boiling 70% ethanol and preserved in 70% ethanol. For light
microscopy the nematodes were cleared in glycerin. Diagrams were prepared
with camera Lucida E 200 Nikon Drawing Tube. Measurements are given
length by width in millimeter.

34

3.8: Preparation of nematode specimens for Steroscan


Electron Microscopy (SEM)
Specimen for scanning electron microscopy were fixed in cold 4%
glutaraldehyde in buffer (P.H 7.2) and kept in it for 24 hours, then dehydrated
through a graded series of alcohol, infiltrated with amylacetate, after critical
drying mounted on stubs, coated with gold and photographs were taken with
the help of SEM. Joel Japan JSM 6380A at an accelerating voltage of 15KV
at Karachi University, central laboratory. The SEM measurements are in
micrometer.

3.9 Procedure for histopathology:


Histopathology of infected intestine of two fishes was carried out including,
Euthynnus alletteratus (Refinisque) and Pomadasys maculatum (bloch,).
For histological studies of intestine, small pieces of infected intestine were
fixed in 10% formalin for 24 hours, washed several times with water,
dehydrated in graded series of alcohols. Cleared in Cedar wood oil and
xylene.blocks were made in cavity blocks by usual method. Thick sections
were cut with a rotary microtome. After removing the wax by xylene,
hydration was carried out. Sections were stained with haematoxylin and eosin,
dehydrated, cleared in clove oil and xylene and mounted permanently in
Canada balsam. Photographs were taken with a photomicroscope Nikon
(Optiphoto20 using Agfa color film.

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,

while the organisms by name, total,

percentage occurrence (O%) and percentage of frequency occurrence (F%)of


stomachs can be seen in Tables (5-13) with histogram representation in (fig.
7-17).The purpose of this study was to examine the relation ship between fish
feeding habit and their diet related parasites.
Analysis of stomach content of 780 marine fishes belonging to 8 genera and
13 species shows that out of these 10 genera 2 fish species(Liza.verigensis
36

and Sardinella albella ) are herbivorous and 11 fish species (Scomberomous


gutattus, Pomadasys olivaceum, pomadasys maculatum, Pomadasys
stridens, Otolithus ruber, Lates calcalifer, Arius maculates, Sillago sihama,
Sphyraena jello, Spharyena forsteri and Euthynnus alletteratus) are
carnivorous. Only 8 fish species are described for their dietary habits.
There was no significant difference in seasonal variation of the food
composition of these fishes .All the food items appeared in the stomach all
year round. Different parasites species were also found in food content of
some fishes. But these are not the part of the food content and may be
swallowed with some food items, as the fish is an intermediate host for
nematode parasites. The most dominant parasites were nematodes in
different fish species and might be the best indicator for food analysis. But
to find the correlation between these parasites and food contents, the
Percentage of frequency occurrence of these parasites were also calculated.

37

4.1

Table: 1 Taxonomic position of different edible marine


fish species studied for their feeding habits, nematode
parasites and histopathology

S.No

Order

Family

Species (Local name)


Liza vaigiensis (Quoy&Gaimard,

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)

Sillago sihama(Forskal, 1775)


(Bhanmbhor)
Euthynnus alletteratus
(Refinisque, 1810)(Dewan)

4.2 Diets of different investigated fishes


Diet of Liza vaigiensis (Quoy&Gaimard, 1824)
Local name=Boi
N=225
T.L=15.0-35cm
(Mean=26.71, Variance=71.74, Std.Dev.=8.47, SEM= 2.67).
(TL) is for total length and (N) is for number of fishes
It is edible fish found in shore, off shore and estuarine waters.
Color is brownish dorsally, becoming dull white on ventral side.
Pectoral fins are deep black, Caudal fin truncate.
39

A total of 14 organisms were identified within the stomach of L.


vargiensis.(Table 2) The food mainly consisted of detritus, and planktons
(including phytoplankton and zooplanktons), blue green and green
(unicellular, and filamentous) algae (Table 2). Detritus (100%) (Sand and
blackish mud) were found to be of most dominant categories on the basis of
percentage of occurrence (Table 5). Phytoplanktons were present in all size
of fishes and in large quantity. The increase was observed in the month of
April, May, June and July. The Observed phytoplanktons belonge to class
Cyanobacteria,

Bacillariophyceae and Cholorophyceae (Figs. 9-20).

Anabaena, Oscillatoria sp., and Microsystis sp.,.(Cynobacteria), Gyrosigm


sp., Pinnulari sp., Tabelaria sp., Melosira sp., Navicula sp., Diploneis sp.,
Schroderella sp., Odontella sp., (Bacillariophyceae), scenedesmus, Chlorella
(Chlorophyceae) were found in all fish sizes. The phytoplankton category
was doThe Gyrosigma sp.(85%) and
common on the basis of

Plurosigma sp.,(75%) were most

percentage of frequency occurrence (F%) as

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.

Diet of Sardinella albella (Valenciennes, 1847)


Local name= Tarli
N=70
T.L=6.5-14cm
(Mean=10.44, Variance=8.05, Std.Dev. =2.83, SEM= 0.89).

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

Diet of Pomadasys maculatum (Bloch, 1797)


Local name: Dhothar
N= 75
T.L=16-50cm
(Mean=30.29, Variance=207.10, Std. Dev. =14.39, SEM= 4.55).
Mouth small, slightly protractile. Lips thick and folded back. Lower jaw
with two pores followed by a narrow groove on chin .No canine teeth. Color
olive grey; head glossed with purple; a large black blotch bordered in front
with yellow at the upper angle of operculum. It occurs in sub tropical and
tropical estuaries, common on Sindh and Makran Coast, much esteemed as
food due to its excellent taste.
Different food categories were observed in the gut of Pomadasys maculatum
(Table 3 & 5), belonging to crustaceans, molluscs, teleosts,

detritus,

polycheates and helminthes. According to the present analysis the


crustacean(71.42%) and miscellaneus(71.42%) ranked on the top among the
other food categories on the basis of percentage occurrence(Table 5) and
frequency occurrence(Table 9). Principal food items (F %) in crustacean
category were shrimp sp.,(71.4%), Acetes sp.,(71.4%) and different species of
closely related copepods(57.14%).Sepia sp.,(35.71%) was dominating in
molluscs category occupying the 2nd rank.. Johnius sp.,(35.71%) followed by
Sardine sp.,(14.28%) and Leiognathus sp.,(7.14%) were observed in teleost
group.(Table 9). Different species of other fishes were also observed but no
positive identification was made to the taxonomic level so were included in
miscellaneous category. Miscellaneous were dominant food group observed in
every stomach with the majority consist of small fish species, compound eyes,
42

legs of shrimps and prawn, with some unidentified material.(Table 9).


Nematodes (28.57%) Acanthocephala and trematode (7.14%) were also found
in addition to food content. The present analysis of food categories and food
items indicate that P. maculatum is a carnivorous fish.
Diet of Otolithus ruber (Schn, 1792)
Local name=Mushka
N=150
T.L=50-105
(Mean=59.34, Variance=28.16, Std. Dev. =5.30, SEM=

1.67).

A common Sciaenid fish caught in good number in coastal waters. Color


silvery, darkish along the back. A dark spot on the opercula. Pectoral, pelvic
and anal fins orange colored. Outer edge of the dorsal fins grayish. Mouth
wide, with one pair of strong canines on each side. Lower jaw larger.
The data on the stomach content of Otolithus ruber through out the study
are shown in table 4.The crustaceans (82.60%) ranked 1st in importance as
the food constituent (Table 5). Miscellaneous item (80.86%) occupy 2nd
position on the basis of percentage frequency occurrence. It included parts
of mandible crabes, cycloid and ctenoid scales, undigested part of animals
and shell fragments. Due to the dominancy of the Gastropods sp., (72.17%)
molluscs occupy 3rd position on the basis of percentage of frequency
occurrence. The planktons (66%) were in decreasing order followed by
teleost (60%). Polycheates were least observed food items. Nematodes
(36.42%) and Acanthocephala (30.43%) occurred generally in those month
in which gut were gorged, full or half full. According to the present
43

investigation Otolithus ruber was found to be carnivorous fish which


mainly feed upon crustaceans and molluscs.
Diet of Arius maculates (Thunberg, 1792)
Local name=Cat fish
N=50
T.L=45.089.5cm
(Mean=64.73, Variance=221.55, Std. Dev. =14,88, SEM=

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

ap.(40%)>Parapenaeopis sp. (14%). The miscellaneous (70%) and


Planktons (70%) were also dominating food categories (Table 5).
Gammerous sp. (70%) was common on the basis of percentage of
frequency occurrence (Table 11) among the plankton category.

Diet of Sphyraena forsteri (Cuvier, 1829)


Local name=Kund
N=70
T.L=40-67cm
(Mean=54.40, Variance=104.0, Std. Dev. =10.21, SEM= 4.56).

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.

Diet of Lates calcarifer (Bloch 1790)


N=70
Local name=Dangri
T.L=35-70cm
(Mean=57.16, Variance=129.8, Std. Dev. =11.39, SEM=

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

maculatum were crustaceans and miscellaneous food items. The molluscs


ranked second among the food categories. planktons were the least observed
food items, Nematohelminthes were also observed but as stated earlier that
they were not the part of food contents.

In the present study percentages of Occurrence of various food items were


different in carnivorous and herbivorous fishes. Planktons were the most
dominent food items in herbivorous fishe giving variable species. Whereas
in carnivorous fishes the crustaceans and miscellaneous were dominating
food categories. While molluses and teleosts ranked on second in number
among the food categories. Polycheates and plankton were in descending
order.
The food and feeding habits of different edible marine fishes were also
found to comparable to fishes from other parts of the world. Although it is
very difficult to compare to all species. Many works have been done on food
and feeding habits of different fish species from different geographical
zones. So it is impossible to make a through comparison with all of them.
An attempt is made to compare the food and feeding habits to possible way.
The present analysis also incorporate with different observations made by
biologist, As Rao (1964) observed during the analysis of stomach content of
different fishes that there is a wide variation in the food and feeding habits
between the different groups of fishes obtained at the bottom and also between
different species within a group and there was marked diurnal differences in
the composition of food items. Berg(1979) and Pillay(1952) reported that the
48

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

E. strigata. For R. coronacauda,

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

The data obtained were reported in the tables 5 13 and subjected to


statistical analysis for the confirmation of results through statistics.

51

4.5: Food contents of different fish species from Karachi coast


Table. 2:

Food contents of Liza vaigiensis and Sardinella albella

S.No

Food Contents

Liza vaigiensis (Boi) n=225

1
2
3
4
5
6

Polychaetes
Crustaceans
Molluscs
Platyhelminthes
Nematyhelminthes
Teleosts

------------Unidentified Soil nematode


---Phytoplankton(acanathes
hungrica, gomphonema
globiform, Scenedesmus,
melosira arenaria, Pennularia,
Tabellaria, Pleurosigmaelongatum, normaris,
Diploneis,Gyrosigma sp,
green filamentous
algae,Oscillatoria)

Planktons

Sardinella albella
(Tarli)n=70
---Copepods
-------------

Phytoplankton(, Diploneis,
Gyrosigma sp, pleurosigmaelongatum, normaris,),
Zooplankton(Harpactacticoid)

Anabaena, Microsystis
Chlorella
8

Detritus (Sand grain)

Miscellaneous

Sand, black mud gravels


Unidentified bottom organisms

52

Sand,mud
Molluses larvae, unidentified
crustaceans

Table = 3: Food contents of Scomberomous gutattus, Pomadasys


maculatum and Sphyraena forsteri

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

Compound eye, legs,


chelaeand mantis of
shrimps

53

Carapace of fishes,
eggs, chlae,and
antennae of
crustaceans

Table.4: Food contents of Arius maculates, Otolithus ruber and


Lates calarifer

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

Table. 5: Occurrence of food categories in relation to total number of


stomach analyzed (O %) of different marine edible fishes from Karachi
coast

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

Table 5.1.: Statistical Calculations of Table 5.

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

Table 5.2 : Statistical Calculations of Table 5.

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

4.7 : Table 6. Frequency of Occurrence in relation to total number of


Stomachs analyzed (F, F%) of different marine edible
fishes from Karachi Coast.
Liza vaigiensis (Boi)
N=225 (Empty=11.11%)

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:

Sardinella albella (Tarli)


N=70(Empty=14.28%)

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:

Scomberomorus guttatus (Surmai)


N=70 (Empty=12.85%)

Organism identified

F
-----

F%

20
30

32.78
49.2

Ensis sp.

6.55

Juvenile of Lutjanus sp.

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:

Pomadasys maculatum (Dhotar)


N=75(Empty= 6.66%)

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:

Otolithus ruber (Mushka)


N=150 (Empty=23.33%)
Organisms identified
Polychaetes
Crustaceans
Crabs(Grapsid sp.)
Isopods
Copepods(Different sp,)
Molluscs
Gastropods
Solen sp
Helminthes
Platy helminthes
Acanthocephala
Nematohelminthes
(Spirocamallanus sps)
Teleosts
Unidentified fishes
Zooplanktons
Gammrous sp.
Scratillaria sp.
Cyclops
Zoeae larvae
Detritus
Miscellaneous
Parts of fishes
Unidentified specimens
appendages of crabs
Shrimp eyes & uropodes
Skeleton,fins,scales of
fishes

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:

Arius maculates (Cat fish)


N=50 (Empty=nil)

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

Gill pieces of bivalves

12

Eggs, chelae, antennae and


compound eye crustaceans

50

63

20
12
14

24
71

Table. 12:

Sphyraenaa forsteri (Kund)


N=70 (Empty=7.14)

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:

Frequency of occurrence of the food items in relation


to stomach analyzed of marine edible fishes from Karachi
Coast.
Liza vaigiensis
100
80
% 60
40
20
0

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

Het er oner ies


Amphipodes
Par apenaeopis sp.

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

Zoea lar vae


Det r it us

10

f ish car paceae

Molluscan shell f r ag.

Food items

Bivalves gill pieces


Eggs,chelae,ant ennae

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

eggs, chelae, antennae

Fig. 7

Lates calcarifer
Lates calcarifer
shrimps sp.

80

copepodes
crabe sp.

60

Loligo

Squila

40

Acanthocephala
fishes
zooplanktons

20

Carapace of crustaceans
Detritus

mantis, compound eyes

Food items

Fig. 8

71

Figs.9-42: Photographic representation of some organisms present


with in the stomach of different marine edible fishes

Fig:9 Diatoms(Different species)

Fig:10 Oscillatoria sp. (Filamentous algae)

Fig:11 Pleurosigma Wm.Smith

Fig:12 Pleurosigma sp

Fig:13 Gyrosigma Wansbeekii(Donkin)

Fig:14 Gyrosigma Sp.

Fig:15 Foraminifora shells

Fig:16 Diploneis Ehrenberg

72

Fig:17 Schroderella sp.

Fig:18 Rhizosolemia sp.

Fig:19 Pinnularia sp.

Fig:20 Odontella sp.

Fig:21 copepode sp.

Fig:22 copepode sp.

73

Fig:23 Loligo sp.

Fig:24 Zoea larvae

Fig:25 Cyclops sp.

Fig:26

Fig:27 Chella of crab

Fig:28

74

Crustacean parts

Detritus

Fig:29 Cyclops sp.

Fig:30 Zoea larvae

Fig:31 Harpacticoid sp.

Fig:32 Soil nematode

Fig. 33. Zooplankton sp.

Fig. 34 Zooplankton sp.

75

Fig. 35 Zooplankton sp.

Fig.36 Broken parts of shrimp

Fig:37 Zoea larvae

Fig:38 Unidentified organism

Fig: 39 Coelenterate sp.

Fig:40 Parapaneopsis sp.

Fig: 41 Fish sp.

Fig: 42 Algae sp.

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

5.2 Dujardinascaris mujibi n.sp.


(Fig. 43-45)
Order:

Ascarididea

Family:

Heterocheilidae

Sub. Family:

Filocapsularinae

Genus:

Dujardinascaris Baylis, 1947


(Syn. Dujardinie Gedoelst, 1916, preoccupied)

Type host:

Sphyraena forsteri (Cuvier, 1829)

Site of infection: Intestine.


Type locality:

Fish harbour, Karachi coast, Pakistan

Prevalence:
Intensity:

14% (7 fish infected/ 50 fish examined)


2.28 (with 6 male and 10 female nematodes)

Holotype (male):

JUW. N.26

Allotype (Female):

JUW. N.27

Diagnosis: Stout worms, body elongated whitish in color, narrow at the


anterior region and greatest width is at posterior region. The head is
provided with 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. Dorsal lips have four pointed ends, which
fit, in the cavities of the subventral lips. Apical one fourth of the lips are
79

embossed with regular zigzag pattern as revealed by SEM. This is a


peculiar character. The cuticle investing the body is expanded throughout
the length of the body. Esophagus is divided into two portions, an anterior
muscular portion, and a posterior glandular portion, Intestine is long, and
caecum is thrust out anteriorly. Tail is very short and conical and is
provided with helical.

Male: (6 specimens including holotype): Body length is 30.0531.01 and


width is 1.22---1.34. The head diameter is 0.05---0.14. The esophagus is
3.60---4.19 in length and 0.22 in width, Nerve ring at 0.16-0.23 and
excretory pore 0.50 from anterior end. Intestinal caecum is 3.003.50 in
length and 0.20 in width. The spicules are equal and are 2.202.22 in
length. Gubernaculum is absent. 12- 14 pairs of sessile caudal papillae are
present, including 10 pairs are precloacal, 2 adanal and 2 postcloacal.
Excretory pore is 0.49-0.52 from anterior end. Tail is short and pointed,
0.1--0.12 in length.
Female:(10 specimens including allotypes): Body length is 50.05---51.85;
1.051.07 in greatest width at middle. The diameter of the head is 0.14--0.16 x 0.220.24. Esophagus is muscular measuring 3.604.70 in length
and 0.17---0.20 in breadth. Nerve ring is at a distance of 0.24-0.36 from
anterior end. Intestinal caecum is 2.30---2.80 in length and 0.13- 0.17 in
breadth. Vulva is postequatorial, 0.95-0.98 from posterior extremity,
vagina is muscular and long. Eggs thick-shelled, rounded, 0.021-0.035.
Tail is short and conical with cuticular ring-shaped striations.

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

investigation from Pakistan is shown in table 14-17. Accordingly the present


is regarded a new species D. mujibi.
Etymology: The specific name D. mujibi is in honor of Prof. Dr. Bilqees
Mujib a parasitologist of Pakistan.

83

5.3 Dujardinascaris jello n. sp.


(figs 46-48)
Type host:
Site of infection:

Sphyraena jello (Cuvier, 1829)


Intestine

Type locality:

Fish harbor Karachi coast Pakistan.

Prevalence :

13.11 % (8 fish infected/ 61 fish examined

Intensity:

(with 7 male and 9 female nematodes)

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

0.13 in breath .Esophagus is muscular, 1.84---1.87 in length and 0.15---0.18


in its maximum breath .An intestinal caecum is present, directed anteriorly
measuring 1.60-1.72 in length . Nerve ring is at a distance of 0.17-0.28 and
excretory pore is 0.51- 0.56 from anterior end. Two large unequal spicules
are present measuring 1.69- 1.70 and 1.80-2.00 in length. There are 17 pairs
of caudal papillae including 11 pairs are sessile [( 7+2+2) 7 preanal, 2
postanal, 2 adanal] and 6 pairs are pedunculate and are preanal .The tail is
short, pointed 0.01 in length.
Female: ( 9 specimen including allotype ).Body length is 31.2---33.25 and
width at maximum is 1.30---1.34 at the middle of body length. The lips are
0.150.18x0.250.27 in diameter. The esophagus is 1.5-1.6 in length and
0.14-0.18 in its maximum breadth. Nerve ring is at a distance of 0.18-0.30
and excretory pore is 0.53- 0.57 from anterior end. Intestinal caecum is
prominent measuring 1.68-1.79 in length. Vulva is at a distance of 0.540.60 from posterior extremity .The tail is blunt in female.
Remarks:
The present species is regarded a new species Dujardinascaris jello n.sp.
The morphological variations are shown in table 14---17. The present
species is morphologically different from the species known in Pakistan
including D. magna (Khan and Begum, 1971); D. ritai (Zaidi and Khan
1975); D. sciaena (Bilqees et al.,1977); D. karachiensis (Bilqees et al.,
2004) and also from other parts of the world including D. melapteuri
(Baylis, 1923); D. cennotae (Pearse, 1936); D. cybii (Arya & Johnson,1980).
Along with morphological differences like body size, length of esophagus,
shorter tail in male, length of spicules and number and arrangement of
85

papillae. There are also some distinguishing characters, like zigzag


embossment on head region, presence of pedunculate papillae, and female
tail structure. These characters are not yet found in any South Asian species.
But it resemble with the above mentioned new species D. mujibi in some
respect like- zigzag pattern on head region, length of spicules and
arrangement of sessile caudal papillae. But as reavled by SEM differences
were observed in some structures like female tail region, having blunt
conical end and also prominent cuticular striations on postequatorial region
of the body in the present species. It is also different from D. mujibi in the
pattern of zigzag embossment, which is more prominent in the head region
of D. mujibi.
The species under discussion is different from all other species of the genus
and is regarded as new species Dujardinascaris jello, as jello is the specific
name of the host.

86

5.4 Dujardinascaris maculatum n.sp.


(Figs. 4951)
Type host:

Pomadasys maculatum (Bloch, 1787)

Site of infection

Intestine

Type locality:

Fish harbor, Karachi coast Pakistan

Prevalence:
Intensity:

24.19% (15 fishes infected/ 62 fish examined)


1
(with 6 male and 9 female nematodes)

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:

(6 specimen including holotype ) Stout, elongated, dark brown

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

0.500.60 in length. Gubernaculums is absent. Excretory pore is 0.43 from


anterior end. Tail is pointed, 0.060.07 in length.
Female:

(9 female including allotype). Body is 1319 in length and

0.420.50 in its greatest width. Cuticular striations are very prominent at


posterior half of the body, just above the tail. The lips are 0.090.15x
0.180.30 in size. Esophagus measuring 0.550.64 in length and 0.20
0.22 in its maximum width. Nerve ring is at a distance of 0.32-0.36 from
anterior end. Excretory pore 0.45-0.52. Intestinal caecum is 0.12-0.15 in
length. Vulva is pre equatorial at a distance of 0.05 from posterior extremity
opening in to muscular atrium. Vagina muscular and slender. Tail is bluntly
conical.

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

Sciaena diacanthus from Karachi coast, D. cybii (Arya and

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

the differentiating characters in the present species is the presence of alate


spicules (figs. 50 D) , subequal, 0.910.95 and 0.500.60 in length,
posterior half of the body is provided with striations, prominent on the
bluntly conical tail, structure of caudal end in female(figs. 51 B&C). The
caudal papillae are 1517 pairs, similar to D. jello n.sp.(13+2+1) but the
position and arrangement of papillae(14 +3) is different in the present
species.
Etymology: The species name D. maculatum refers to the host species

89

5.5 Dujardinascaris sphyraenaii n.sp.


(Figs. 52-- 54)
Type host:

Sphyraena jello (Cuvier, 1829)

Site of infection:

Intestine

Type locality:

Fish harbor, Karachi coast Pakistan

Prevalence & intensity:

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

Diagnosis: Stout, long, cylindrical, dark brown worms, tapering toward


both extremities with pointed posterior end in male and female. Mouth
bounded by three prominent lips, with out dentigerous ridges. Cuticle is
finely striated through out the body. Esophagus is entirely muscular,
intestinal caceum well developed. Anal opening is prominent in male.
Male: (6 specimen including holotype) Stout, medium-sized, dark brown
worms, body length 20.50---24.90 and 0.32---0.36 at its maximum width.
Mouth bounded by three lips, with out dentigerous ridges. Interlabia present.
Body is sparsely striated. The lips are 0.3020.06 x
0.050.08. The esophagus is 0.720.88 in its length and 0.110.16 in
width. Nerve ring is at a distance of 0.30-0.33 from anterior end. Intestinal
90

caecum is 1.59-1.67 in length.

15 pairs of caudal papillae are present

including 11 pairs preanal, 2 pairs postanal and 2 adanal Two equal


spicules are present, 0.64-0.75 in length. Gubernaculum is absent .tail is
pointed, 0.025-0.027 in length.
Female: ( 10 female including allotype) Body is 22.4---25.4 in length and
0.250.37 in its maximum breadth. The lips are 0.050.08x0.050.09 in
diameter. Esophagus measuring 0.840.94 in length and 0.130.15 in
width. Nerve ring is at a distance of 0.32-0.39 from anterior end of the body.
Intestinal caecum is 1.60-1.71 in length. Vulva is prominent, pre equatorial
at a distance of 0.27 from posterior extremity. Tail is pointed , 0.05-0.06 in
length, with area rogosa -like structures on its posterio-ventral end.
Remarks
The present specimen is regarded a new species D. sphyraenaii n.sp. The
morphological variations are shown in table 14----17. The present species
resemble in body size with D. sciaena , but the spicules are much smaller
and there are 15 pairs of caudal papillae, as compared to D. sciaena
including 23 pairs of caudal papillae are present. D. magna and D.
karachiensis are much larger in body length, body width, size of esophagus
and length of spicules as compare to the present species.
A comparative account in the morphological variations of

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

ventral in position in the present species while in D. mujibi; D. jello and D.


maculatum, the papillae are lateral in position.

Etymology:
host species

Species name D. sphyraenaii refers to the local name of the

92

5.6 Dujardinascaris multiporous n.sp.


(Figs. 5557)
Type host:

Pomadasys olivaceum ( Day, 1875)

Site of infection: intestine


Type locality :

Fish harbor Karachi coast Pakistan

Prevalence:

20% (12 fish infected/60 fish examined)

Intensity:

1.66

(with 7 male and 13 female nematodes)

Holotype(male):

JUW. N. 18

Allotype (female):

JUW. N. 19

Diagnosis: Stout, medium sized worms, narrow at both ends, whitish in


color, worms. The cuticle is striated throughout its body length and provided
with depressions appearing as pores-like in SEM. Esophagus is muscular.
The patterns of these cuticular pores are different in male and female. The
tail in male is pointed and is bluntly conical in female. Cuticle is thick with
deep transverse grooves in male and indistinct in female in anterior most
region, mouth is surrounded by three lips. Intestinal caecum is absent.
Male: (7 specimen including holotype). Body is 6.10 ---7.50 in length and
0.20---0.29 in its maximum breadth at the middle of the body. The lips are
0.045---0.070x 0.80---0.10 in size. The esophagus is 0.35---0.50 in length
and 0.15---0.20 in its width. Two, small, subequal spicules are present 0.61--0.64 and 0.72---0.75 in length. Gubernaculums is absent. Caudal papillae
93

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

other morhphological characters as shown in table 14-15.

The present

species is regarded a new species and the name D. multiporous n. sp. is


proposed.
Etymology: The species name D. multiporous refers to the presence of
cuticular pore-like depressions on posterior half of the body

95

5.7 Dujardinascarus sinjarii n.sp.


(Fig. 58)
Type host :

Otolithus ruber (Sciaenidae )

Site of infection:

Intestine.

Type locality:

Fish harbor, Karachi coast Pakistan

Prevalence :
Intensity:

6%
1.66

( 3 fish infected/ 50 fish examined)


(with 2 male and 3 female nematodes)

Holotype(male):

JUW. N. 36

Allotype(female):

JUW. N. 38

Diagnosis:

These are relatively large and stout worms, body elongated.

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.

Male: (2 specimens including holotype): Body length is 50--54 in length and


width is 0.081.20. The head size is 0.20-0.22 x 0.23-0.26. The

96

esophagus is 1.20-1.60 in length and 0.30-0.50 in width, esophageal bulb is


0.046-0.049 in size. Nerve ring is at a distance of 0.36-0.39 from anterior end of
body extremity. Excretory pore is at a distance of 0.41-0.42 from anterior end
of body. Spicules are unequal, 1.171.19 and 0.05-0.07 in length. There are
11- 12 pairs of sessile, caudal papillae, including 6 pairs precloacal and 6
postcloacal. Cloaca is located at a distance of 0.10 from the posterior end. Tail
is pointed, 0.26--0.27 in length.
Female: (3 specimens including allotypes): Body length is 10.5-11.10 and 0.330.35 in breadth at middle. The size of the head is 0.12-0.13 x 0.13-0.16.
Interlabia is similar to that of male in size. Esophagus is 0.650.76 in length
and 0.08---0.10 in breadth. Esophageal bulb is 0.030-0.035 in size. Vulva is
postequatorial situated at a distanance of 0.40-0.41 from posterior extremity,
vagina is muscular and long. Eggs are thin shelled and rounded measuring
0.046-0.051 in diameter. Tail is pointed 0.07 in length.

Remarks:
Dujardinascaris sinjarii is different in important diagrammatic features from
other species of the genus Dujardinascaris including D. . cenotae ( Pearse,
1936) from Rhamdia guatemalensis;

D. melapteruri (Baylis, 1923) in

Melapterus elecricus. 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 0.550.59, tail is 0.50 long. The present species have less number of
papillae and unequal spicules. D. ritai is reported from freshwater fish, and is
described by immature female only.
97

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

differ from D. karachiensis by lips

structure, length of oesophagus, 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 present species is similar in numbers of
caudal papillae( 10-11) with D. sphyernaii n.sp. (11), but the position and
arrangement of papillae are different in both new recovered species.
The comparative morphology of the present species with other species
recovered from Pakistan is shown in table 14--17. Accordingly the present
species is regarded a new species D. sinjarii.

98

Etymology: The specific name D. sinjarii refers to the local name of the fish
host.

99

5.8 Dujardinascaris dentatus n. sp.


(Figs.59-60)
Type host:

Sillago sihama ( Forskal, 1775)

Site of infection:

intestine

Type locality :

Fish harbour Karachi Coast Pakistan

Prevalence:

13.33% (10 fish infected/ 75 fish examined)

Intensity:

1.3

(With 4 male and 9 female nematodes)

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.

Two, small, slender, subequal, spicules are


100

present 0.8---0.9 in length. Gubernaculum is absent. 17 pairs of Sessile caudal


papillae of which 6 pairs are precloacal and 8 pairs are post cloacal.
Female: (9 specmen including allotype) Body length 28.4---32.5, 0.45--0.50 width. The lips are 0.31---0.38x 0.50---0.56 in size. The esophagus is
3.95-4.25 in length and 0.311.35 in its breadth. Nerve ring is at a distance
of 0.27-0.31 and excretory pore 0.58 from anterior end of the body. Intestinal
caecum is prominent measuring 1.68-1.79.Vulva is at a distance of 0.54- 0.60
from posterior extremity .The tail is blunt in female.

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

Table.14: Morphological variations in the new species of the genus


Dujardinascaris Baylis, 1947
(All measurements are in mm)

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

Table.15: Morphological variations in the new species of the genus


Dujardinascaris Baylis 1947
(All measurements are in mm)

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

Table.16: Morphological variations in the species of the genus


Dujardinascaris Baylis 1947 described so far from various localities
(All measurements are in mm)

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

Table.17: Morphological variations in the species of the


genus Dujardinascaris Baylis 1947 described so far from
various localities (all measurements are in mm)

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

5.11: HISTORY OF THE GENUS PROCAMALLANUS BAYLIS, 1923


(SPIROCAMALLANUS (OLSEN 1952) PETTER, 1979)

Species of the genus Procamallanus Baylis, 1923, subgenus Spirocamallanus,


Olsen, 1952, have been reported in a variety of piscine hosts in different
geographical zones, and in both freshwater and marine systems. Although many
authors consider Spirocamallanus Olsen, 1952 a distinct genus, we agree with
Moravec and Sey(1988) in considering Spirocamallanus a subgenus of
Procamallanus. This subgenus is characterized by the presence of a buccal capsule
with internal spiral thicking in both males and females(Moravec and Thatcher,
1997). Thus those species were formally transferred to Procamallanus(
Spirocamallanus). Spirocamallanids are equally dominated in Asia and South
America and also found in North America, Africa and Australia. The species
appear to be originated in tropical Asia as parasites of catfishes then invaded
marine fishes. The transmission and development of this genus has been little
studied but a number of species in fish have been investigated. First larval stages
are attracted by the copepods and perhaps, other crustaceans (intermediate host).
The definitive host becomes infected by ingesting the copepods with the larval
stage of the parasite. However, the larvae will persist in gut or became
encapsulated in the tissues of plankton-omnivorous fishes, which consumes
copepods. This paratenic hosts move the larva in the food chain to the piscivorous
definitive host(Anderson, 2000). The African may be derived from the Asian fauna
by the dispersal of spirocamallanids with catfishes. The South American fauna
points to a freshwater dispersal pattern, probably from Africa before the continents
drifted apart. But it is not relevant to mention all the species of Procamallanus
(Spirocamallanus) from all geographical zones.
125

Procamallanus(Spirocamallanus) are the the common parasites of fishes of South


Asia. Sood (1989) presented a key to the species reported from South Asia.
Procamallanus(Spirocamallanus)mehrii (Agarwal ,1930) from wallago attu in
Allaabad; P. (S.) planoratus( Kulkarni ,1935) from Clarias batrachus in Nagpur;
P. (S.) pereirai (Annereaux, 1946) from Mugil speigleri, Otolithus ruber and
Pomadasys hasta; P (S.) bagarii (Karve&Naike, 1951) from Bagarius bagarius in
Pona; P.(S.) ahiri (Karve, 1952) from Anguilla bengalensis in Poona; P.(S.) mysti
(Karve ,1952) from Mystus carvasius in Poona; P.(S.) saccobranchi (Karve, 1952)
from Heteropeutes forsitis in Nagpur P.(S.) aspiculus (Khera, 1955) from Bagarius
bagarius; P.(S.) gubernaculus (Khera ,1955) from Rita rita in Luknow; P.(S.)
clarius (Ali, 1956) from Clarius batrachus, P.(S.) heteropneustus (Ali, 1956) from
Heteropneustes fossilis , P.(S.) hyderabadensis ( Ali, 1956)from Mystus seenghala,
P. (S.) Singhi(Ali, 1956) from Ompok bimaculatus in Hyderabad; P.(S.)
mozabukae (Yeh ,1957) from Polydactylus indicus in Khulna; P (S.)
spiculogubernaculus (Agarwal, 1958) in Allahabad; P.(S.) daccai (Gupta ,1959)
from cat fish in Dacca; P (S.) globoconchus (Ali, 1960) from Rita kuturnee in
Hyderabad; P.(S.) Ophicephalus (Ali, 1960) from Channa punctatus in
Hyderabad; P.(S.) attui (Pande et al.,1963) from Wallago attu; P.(S.) confuses
(Fernando and Furtado, 1963) from Heteropneusies fossilis from Sri Lanka; P. (S.)
mathurai (Pande et al., 1963) from Heteropneusies fossilis ; P.(S.) magurii (Lal,
1965) from Clarias batrachus in Meerut; P.(S.) vachai (Sinha and Sahay, 1965)
from Eutropiichthys vacha in Patna; P.(S.) hindensis (Lal, 1965) Heteropneusies
fossilis in Meerut; P.(S.)muelleri(Agarwal, 1966) from Lucknow; P.(S.) fasciatusi(
Sood, 1967) from Trichogaster fasciatus in Lucknow; P.(S.) gomtii (Sood,1967)
from Eutropiichthys vacha in Lucknow; P.(S.) vittatusi (Sood, 1967) from Mystus
vittatus in Lucknow; P.(S.) ottuei (Varma and Varma, 1971) from Heteropneusies
fossilis in Haryana;

P.(S.) ompoci (Majumdar&Data, 1972) from Ompok


126

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;

P.(S.) kakinadensis and P.(S.) lutjanusi (Lakshmi,2000a,b) from

perciform fish in India.

The species described from Karachi coast, Pakistan are Procamallanus


(Spirocamallanus) spiralis (Khan& Begum,1971) from Tachysurus caelatus; P.(S.)
pereirai (Rasheed,1970) from variety of marine fish; P.(S.) dussumieri (Bilqees et
al.,1971) from Jhonius dussumeieri; P.(S.) sihamai (Khan & Begum 1971) from
Sillago sihama; P.(S.) crossohombii (Zaidi & Khan,1975) from Crossorhombus
azureus; P.(S.) sparus (Akram, 1975) from Argyrops spinifer; P.(S.) otolithi
(Ashraf et al., 1977) from Otolithus argenteus; P.(S.) wallagus (Rehana & Bilqees
,1973) from Wallago attu in Sindh.

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

5.12: Spirocotyle otolithi n.gen. n.sp.


(Fig.61)
Order :

Spiruidea Diesing, 1861

Family:

Camallanidae Railliet and henry, 1915

Sub family: Camallaninae Yeh, 1960


Genus:
Species:

Spirocotyle n. gen.
Spirocotyle otolithi n.gen. n.sp.

Type Host:
Type Locality:

Otolithus ruber ( Sciaenidae)


Fish harbor, Karachi coast

Location:
Prevalence:

Intestine
4% 13 host examined,( one infected with, one male
and one female.

Intensity:

2.5 (In other collection 3females were also recorded


from one fish out of 7 hosts)

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

narrower than glandular esophagus. Excretory vesicle is prominent. The tail


is pointed in male and blunt in female.
Male :(One specimen holotype) Length of body 10.4, maximum width 0.34.
The wall of the buccal capsule is provided with 15 spiral thickenings, 0.11 in
length and 0.09 in its maximum width at its glandular esophagus region. A
prominent sucker is present at the anterior region of buccal capsule. The
nerve ring is 0.048 from anterior extremity. Esophagus is divided into
anterior muscular portion and posterior club shaped curved glandular
portion. The anterior muscular portion measures 0.65 in length and 0.15 in
width, while the glandular portion is much wider and measures 0.98 in its
length and 0.28 at its maximum width. The nerve ring, 0.3 in length and
0.11 in its width. The spicules similar in shape, unequal in length, large
spicules is 0.71 long and small spicule is 0.34 long. Twelve pairs of caudal
papillae are present, including seven pairs pre-anal, five pairs post-anal. The
tail is conical, 0.05 long with pointed end.
Female :(4 female including allotype): Length of body is 14.8, maximum
width 0.6. The mouth leads into a buccal capsule which is similar in
structure to that of male specimen having a prominent sucker. It measures
0.11 in length and 0.1 in its width. The esophagus is similar to that of male
specimen except in size. The anterior muscular part is 0.45 in length and
0.26 at its maximum breadth. The longer posterior glandular part measures
1.18 in length and 0.43 in its maximum breadth. The nerve ring is 0.27 from
its anterior extremity. The tail is straight and oval with three prominent
cuticular projections measuring about 0.1, 0.5, 0.8 from one groove to other.
A pear shaped excretory vesicle is present, 0.02 in length. The vulva is
130

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:

Spirocotyle otolithi n.gen. n.sp.


Karachi coast, Pakistan

Etymology: The sucker-like structure is not found in any of the


previously described spirocamalanid nematodes or other related genera.

132

5.13: Procamallanus(Spirocamallanus)riaziaii n. sp.


(Fig. 62----- 64)
Order

Spiruidea Diesing, 1861

Family

Camallanidae Railliet and henry, 1915

Sub family

Camallaninae Yeh, 1960

Genus

Procamallanus(Spirocamallanus ( Olsen
1952) Petter, 1979.)

Synonymy:

Spirocamallanus (Olsen, 1952) (in parts);


Procamallanus Baylis, 1923 (in parts).

Type Host :

Otolithus ruber( Sciaenidae)

Type Locality :

Fish harbor, Karachi coast.

Location :

Intestine

Prevalance::

28.57% (/20 infected/ 70 host examined )

Intensity:

0.869 ( with 8 male and 15 female)

Holotype(male):

JUW. N.20

Allotype (female):

JUW. N.20

Diagnosis: These are medium-sized worms, with transversely striated


cuticle, tapering anteriorly, buccal capsule is yellowish brown, chitinzed,
oval to rounded, not divided in to two lateral valves, surrounded by 12
submedian cephalic papillae arranged in two circlets. A small protuberance
is situated at the inner base of each papillae of the second circlet (fig. 64 D).
The anterior end of the body is bent ventrally and is provided with cervical
133

alae, forming a kind of pseudosucker.; with spiral thickenings; tridents are


absent; esophagus is divided into an anterior muscular and longer posterior
glandular part; tail bluntly conical with two terminal spikes in both the
sexes; caudal alae present, uniting in front; spicules unequal ; vulva post
equatorial; Parasites of fishes, occasionally of amphibians
Male: (8 males including holotype ) The body length is 11.0---12.8,
maximum width is 0.23---0.25. The inner surface of the capsule is provided
with 11---12 spiral thickings in a lateral view.and the diameter of the
capsule is 0.08 x 0.07. The length of muscular oesophagus is 0.39---0.41
and its maximum width is 0.16 while the glandular oesophagus is 1.00--1.05 in length. The nerve ring is a distance of 0.22---0.25 from anterior
extremity. The caudal papillae are 16 pairs, of which 4 pairs are pedunclate
papillae are post cloacal, 5 pairs are sessile and precloacal. Two unequal
spicules are present, measuring about 0.27---0.28 and 0.14---0.16 in length.
The tail is bluntly pointed, 0.05 in length.
Female: (15 females including allotype ) The body length is 9.0---9.4 and
the maximum width 0.23---0.24. The inner surface of the capsule is
provided with 9---10 spiral thickings in a lateral view. and the diameter of
the capsule is 0.075x0.070. The length of muscular esophagus is 0.39---0.41
and its maximum width 0.0750.090, while the glandular esophagus is
0.75--- 0.80 in length and 0.110.12 in width. The nerve ring is 0.22--0.24 from its anterior extremity Excretory pore inconspicuous. Ovary
single, vulva postequatorial 3.0-4.3 from anterior end. . The tail is bluntly
conical, 0.023---0.26 in length.

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

comparison of the new species with all of them. And here

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

nematode species P.(S.) riaziaii is different in

important morphological features from all Pakistani species in all


morphological features except forked tail, as there were no scanning
electron micrographs of any one of the described species of the marine
fishes of Pakistan. Although Khan &Begum (1971) in P. (S.) spiralis
mentioned 4 tooth-like structures of buccal capsule, but it is impossible to
make a through comparison due to the micrographs, may be these structures
are those which are observed by SEM during the present study.
Species of other geographical zones can be compared with P.(S.) riaziaii
n.sp .Moravec et al., (2006) listed three valid species Procamallanus
(Spirocamallanus) monotaxis (Olsen, 1952); P.(S.) istiblenni (Noble ,1966);
and P.(S.) guttatusi

(Salas et al., 1994) from perciform fish in the

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

of the body, absence of amphids, size of spicules and presence of cervical


ala at one side of cervical region. The other morphological features are
presence of pedunculate papillae, but not similar in number and
arrangement of caudal papillae and digit-like tail.
Etymology: The specific name P.(S.) riaziaii is in honor of Prof. Dr. Riaz
Ahmed Hashmi, the first Vice chancellor of Jinnah University For Women
Karachi, Pakistan.

137

5.14: Procamallanus(Spirocamallanus)ruberii
( Figs. 65-66)
Type Host:

Otolithus ruber (Schiender)

Type Locality:

Fish harbor, Karachi coast.

Location:

Intestine

Prevalence:

11.66% ( 7 infected /60 host examined)

Intensity:

1.44

Holotype (male) :
Allotype (female):

( with 4 male and 6 female)


JUW.N.23
JUW.N.24

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

numbers with digit-Like tail.P.(S.) dussumieri (Bilqees et al., 1971) from


Jhonius dussumeieri in Karachi, having 13 spiral thickings and 9 pairs of
caudal papillae.P.(S.) sihamai (Khan & Begum, 1971) from Sillago sihama
in Karachi having 11 spiral ridges and 6 pairs of caudal papillae. P.(S.)
wallagus (Rehana & Bilqees, 1973) from Wallago attu in Sind; P.(S.)
crossohombii

(Zaidi & Khan, 1975) from Crossorhombus azureus in

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:

Procamallanus (Spirocamallanus) sp.


(Fig. 67)

Type Host :

Otolithus ruber( Sciaenidae)

Type Locality :

Fish harbour, Karachi coast.

Location :

Intestine

Prevalance :

Female specimen:

13.33%(15 host examined/ 2 fish Infected)


with 3 females only
JUW. N. 24

Diagnosis: (Description is based on one subgravid specimen). Body length


is 23.5mm,and the maximum width is 1.0mm. The inner surface of the of the
orange-yellow capsule is provided with 11-13 spiral thickings in a lateral
view. and the diameter of the capsule is 0.18x0.15. The length of the
muscular esophagus is 1.0 mm and its maximum width is 0.2mm, while the
glandular esophagus is1.05mm in length and 0.2mm in width. The nerve
ring is 0.20 from its anterior extremity. The distance of excretory pore is
from anterior end. Vulva is pre-equatorial, 0.10 from posterior extremity.
vagina muscular, directed posteriorly from vulva. uterus filled with larvae.
tail rounded, with digit-like projection bearing two minute cuticular spikes.

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

5.17: HISTORY OF THE GENUS CUCULLANUS( MUELLER, 1777).


The genus Cucullanus Muller,1777( Cucullanidae, Seuratoidae)comprises
over 50 species, mainly from fishes. Some studies on the biology and
seasonal dynamics of Cucullanus spp. have been reported( Petter & Sey,
1997; Sardella, 1997; Moravec, F. 1998; Kie ,2000; Daniel et al., 2002;
Lanfranchi et al., 2004; Moravec et al., 2005; Timi & Lanfranchi, 2006;
Gonzlez-Sols, 2007; Moravec et al., 2008). The first species described was
Cucullanus cirratus Muller, 1777

parasitizing different hosts. It was

synonymzed, C. truttae (Fabricius, 1794); C. acipenseris (Viborg, 1795) in


Acipensar sturio, A. ruthemus, A. schypa, A. stellatus, A. gulenstadti etc.
from Atlantic and Mediterranean. Cucullanus heterochrous (Rud., 1802).
syn. C. platessae (Rud., 1809); C. sphaerocephala (Rud., 1809) were found
in Orthagoriseus mola. Cucullanus esuriens (Duj., 1845); C. praecinctus
(Duj., 1845) were found in Conger vulgaris; C. squati (Duj., 1845); C.
attenuatus . C. rotundatum (Molin, 1859) in Cantharus vulgaris.
longicollis (Stossich, 1899) in Mullus barbatus.

C.

C. callichori (Stewart,

1914) in Callichrous macropthalmus from Lucknow.. C. bulbus (Lane,


1916) syn. Bulbodacnitis b. in Caranx melampygus from Ceylon, ( Sri
Lanka). C. pulcherrimus (Barreto, 1918) in Caranex lugubris from Brazil.
C. dodsworthi (Barreto, 1922) in Sheriodes testudineus from Brazil. C. barbi
(Baylis, 1923) in Barbus bynni from Egypt. C. incertus (Gendre, 1927) in
Sebastes dactyloptera from Morocco. C. gigi (Fujita,1928) in Fluvidraco
nudiceps from Japan and C. elongates (Smedley, 1933) in Ophiodon
elongates from Pacific coast. C. filiformis (Yamaguti, 1935) in Conger
myriaster and Anguilla japonica of Japan. C. amadai (Yamaguti, 1941) from

151

Branchiostejus japonicus from Japan. C. girellae (Yamaguti, 1941) in


Cyprinus carpio and Girella punctata from Japan.
Cucullanus mogi (Travassos, 1948) was reported in Leporinus sp. from
Brazil. C. hansoni (Olsen, 1952) in Balistes capistratus from Hawaii. C.
exigus (Yamaguti, 1954) in Lates calcarifer from Borneo. C. gendrei
(Campana-Rouget, 1957) in Synacium micrirum from West Africa.. Berland
(1970) described in detail C. cirratus, C.heterochrous and C.minutus.
Ejsymont (1970) recorded C.truttae for the first time from Poland. Soota and
Chaturvedi (1971) described C. pangasius from Pangasius pangasius in
Madras state, India. The species has been differentiated from C. robustus.
Maggenti (1971) gave a review of the family Cucullanidae Cobbold, (1864)
and the genus Bulbodacnitis (Lane, 1916) with description of B.
ampullastoma sp.n. (Nematoda: Cucullanidae), from Salmo gairdnerii. He
has also given a Key to the genera and has made some new combinations
which are B. truttae n. comb., for C.truttae and B.lebedevi n. comb. for
C.lebedevi .
Gibson (1972) studied and described the larval and adult development and
the life history of C.minutus and C.heterochrous from the host Platyichthys
flesus in the Ythan-Estuary. The larvae of C. heterochrous were described
for the first time. The author has discussed the possible influence of the
water temperature on the host and the parasites and has concluded with the
help of the geographical records of distribution the C. minutus parasitizes
fish in the warmer waters than C.heterochrous. It was also recorded that the
life cycle of C.heterochrous takes two years while the life cycle of
C.minutus takes one year. Kumar and Gupta (1979) described a new species
152

C. egrettae from the intestine of Egretta garzetta from Lucknow, India.


During the same year Santos et al described a new species C. oswaldocruzi
from the intestine of Zungaro zungaro from the Amazon river. Popova et al.,
(1979) reported the host range and life cycle of C. cirratus.
Moravec (1979) reported the development stages (from egg to adult) of C.
truttae. encysted 3rd stage larvae were obtained from naturally infected larval
lampreys ( Lampetra planeri) and 3rd-4th- stage larvae plus adults were
obtained from experimentally infected trout. A variety of invertebrates, the
fish Poecilia reticulatus and trout were fed 2nd- stage larva (free or within
the egg) of C.truttae and were examined from 3 to 68 days later but none
was infected. From field observations lampreys are the main source of
infection of C.truttae for the trout. However, the parasite can also mature in
the adult of the lamprey. The parasite in lampreys is usually known as
C.stelmoides but this is infact synonymous with C. truttae.
Moravec (1983) studies the life history of C.truttae, a parasite of trout in
Czechoslovakia. Earlier during 1981 Kakacheva- Avramova and Menkova
studies its life-cycle and found Lampetra planeri served as an intermediate
host. C. truttae was found to be a parasite of trout in the rivers Rilska, Ilina
and Blagoevgradska Bistrista in Bulgaria. Minmim (1984) described a new
species C.spirocaudus from the intestine of Liza haematecheila collected
from Penglai, China. Malakhov and Valovaya (1984)

studied the

evolutionary adaptation to parasitic way of life of the cephalic sensory


orgsns in Cucullania. Valovaya (1984) described the pseudobuccal cavity
and surface cephalic structure of C.cirratus Muller, (1977) from SEM
studies. Lebre and Peter(1984) described a new species C. campanae found
153

in the Mediterranean coast of France at Sete (type locality) and at Banylus,


in Atlantic Ocean, at Arcachon and in the Adriatic Sea (at Kotor,
Yugoslavia).
Conneely and McCarthy (1986) studied the parasites of 121 eels from 3
contrasting sites in the Corrib catchments area, western Ireland. Thirteen
species of parasites were recovered including C.truttae. Microhabitat
preferences of the parasites were noted. Variation in the occurrence and
intestines of the parasites observed were analyzed in relation to sampling
period, host habitat and characteristics of the eel populations observed.
Factors shown to be important included composition of the fish communities
and distributional patterns of intermediate hosts and piscivorous birds.
Differences were noted in the parasitocoenoses of eels in still and running
water sites.The occuirence and intensity of infection of C.truttae was shown
to be related to either age or size of eels, which is accounted for by the fact
that eels become increasingly piscivorous with age and increasing size.
Ingrid et al.,(2002) described C. marplatensis parasitizing Odontesthes
argentinensis from Argentinean waters. Lafranchi et al., (2004) reported
C.bonaerensis parasitizing Urophycis brasiliensis from Argentinean waters.
Moravec et al., (2005) described C. oceaniensis from Anguilla sp. from
Futuna Island.

Timi and Lanfranchi,( 2006) described C. pedroi

parasitizing Conger orbignianus from Argentinean waters. David et al.,


(2007) describe C. pargi from the grey snapper Lutjanus griseus of the
southern coast of Quintana Roo, Mexico. Moravec et al., (2008) also
describe C. maldivensis from Lutjanid fish, Macolor nigar of Maldive
Islands.
154

Sood,( 1989) studied fish nematodes from South Asia. Petter and Sey,
(1997) described C. trachinoti from Tachinotus blochi.

Lakshmi, (2000)

give the presence of gubernaculums in C. baylist reported from Arius


thalassinus.
Several species of the genus Cucullanus Muller, 1777 have been described
both from marine and fresh water fishes of Pakistan. Species reported from
marine fishes are all from fishes of Karachi coast. These include C.armatus,
(Rasheed, 1968) from Tachysurus serratus; C. diminutus (Rasheed, 1968)
from Stromateus niger; C. exiguous,( Rasheed, 1968) from Lates calcarifer
and Pseudosciaena sp. Rasheed (1968) also reported C. hians 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 by Bilqees et al.,
(1971) as C.elongatus from Erethistes elongate. C. olivaceus (Akram, 19751976) 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.
C. quadrii (Bilqees, & Fatima, 1980 ) from Arius serratus; 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. Bilqees et al., (2005) described C.mujibi from Arius serratus.
And C. pakistanensis from Sciaena diacanthus from Karachi coast.

155

The freshwater fish Cucullanids reported from Pakistan include C.


pseudoannulatus (Rehana and Bilqees, 1986) from Mystus cavasius; C.
gonii (Khan et al., 1991) and C. khalili (Khan et al., 1991) from Labeo
goniusand Labeo rohita. C. annulatus (Margolis, 1960) has also been
reported in the fish Mystus cavacius (Rehana and Bilqees, 1976). C. dogielli
(Krotas, 1959) was reported by Khan and Yaseen (1969) in Chanda sp.

156

5.18 Cucullanus aliyaii n. sp.


(Fig.68-69)
Order:

Spiruridea Diesing 1861

Family:

Cuculanidae Cobbold 1864

Sub family:

Cucullaninae Yorke & Maplestone 1926

Genus:

Cucullanus Muller, 1777

Type host:

Otolithus ruber(Schneider, 1801)

Site of infection: Intestine


Type locality:

Fish harbor, Karachi coast Pakistan

Prevalence:

15 % (20 fish examined / 3 fish infected)

Intensity:

(with 2 male and 4 females).

Holotype(male):

JUW. N. 40

Allotype(female):

JUW. N. 41

Diagnosis: Relatively small nematodes, body whitish slender, with slightly


tranversly striated cutical. Female larger than male. Broader anteriorly,
posterior end pointed, provided with small bifurcated spike at the tip of the
tail. Lateral alae absent. Oral opening dorsoventrally elongate, surrounded
by narrow membranous flange or collarette supported by row of numerous
teeth. Three submedian cephalic papillae and a pair of prominent lateral
amphids are present. Pseudobuccal capsule or esophastome wider than
posterior part of esophagus. Deirids simple, just aanterior to esophagus and
intestinal junction. Tail broadly conical, bifurcated at the tip.
Male (2 specimens including holotype): Length of body 2.02-2.29, greatest
width 0.35-0.40, entire esophagus 0.36-0.38 in length. Its minimum width is
157

in the middle 0.10, Length of esophastome is 0.18-0.20, maximum width at


esophastome 0.13-0.15, posterior club- shaped part of esophagus in 0.340.37 in length and 0.09-0.11 in width .Nerve ring at a distance of 0.22-0.29
from the anterior extremity. Testis situated in posterior half of body or
slightly anteriorly. Precloacal sucker is absent but few weak muscle fibers
can be send. Spicules sub equal and 0.59-0.61 and 0.70-0.77 in length.
Gubernaculums is absent. 12 pairs of caudal papillae are present including, 7
pairs preanal, 4 pairs are post anal and 1 pair is adanal. Tail is 0.01 in
length.
Female ( 4 specimens including allotype):

Length of body is 3.24,

maximum width is 0.30. Entire esophagus is 0.50 in length, Greatest width


0.15 at esophastome , minimum width almost at the middle. Posterior clubshaped portion 0.15 in widths. Distance of nerve ring from the anterior
extremity 0.30. Vulva 0.17-0.18 post equatorial, prominent, vulvar lips
elevated at a distance of 1.80 from the anterior extremity. each containing
elongated gland cells, extruding out of body wall. Vagina long, muscular
tube and is directed upward. Uterus thin- walled, containing numerous
relatively large, thin- shelled eggs 0.07x0.04. Tail is 0.011 in length.

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

Yamaguti, (1961) has listed 60 species in the genus Cucullanus including


the genotype. In addition to this Gupta and Masoodi (1982) described C.
sootai and listed another 30 species including C. ritali (Karve, 1952); C.
jaiswali

(Ali,

1956);

C.indica

(Agrawal,

1965);

C.

pseudotropi

(Agrawal,1967); C. arabianse (Ali and Kalyankar,1967; Petter, 1974); C.


theraponi (Rasheed,1968); C.pangasius (Soota and chaturvedi., 1971); C.
jalnaensis; C. alii Kalyankar, (1971); C. malvanae Kalyankar, (1971); C.
tachysuri (Kalyankar, 1971); C. bilqeesi, (Bilqees et al., 1971; Petter, 1974);
C. carioca (Vicente and Fernandes, 1973);C. rougetae (Vicente and Dos,
1974); C. bagrae (Petter,1974); C. karachii (Zaidi & Khan, 1975);
C.olivaceus (Akram, 1975-1976); C. guerrori (Arya and Jhonson, 1975); C.
ariusi (Srivastava and Gupta, 1976); C. sciaenai (Gupta and Gupta, 1979);
C. rivulatus (Soota and Sarkar, 1980); C trichiurisi (Gupta and Naqvi,
1983); C. simhai (Gupta and Naqvi, 1983); C. thapari (Gupta and
Srivastava, 1984) and C. mastacembeli (Gupta and Srivastava, 1984).
Later on more species have been described both from fresh water and marine
fishes of various localities including C. rhamphicthdis (Moravec et al.,
1979); C. campanae (Labre and Petter, 1984); C. fugianensis (Wang, 1984);
C. brevispiculus (Moravec et al., 1993); C. riograndensis (Fortes et al.,
1993a); C. fabrigasi (Fortes et al., 1993b); C. mexicanus (CapsetaMandujanoi,2000); C. marplatensis (Ingrid et al., 2002); C.oceaniensis
(Moravec et al.,2005); C.pedroi (Timi and Lanfranchi, 2006). David et al.,
(2007) describe C. pargi from the grey snapper Lutjanus griseus of the
southern coast of Quintana Roo, Mexico. Moravec et al., (2008) also
describe C. maldivensis from marine fishes of Maldive Islands.
160

The present species C.aliyaii is different from C. Alti (Kalyankar, 1971)


Peter, 1974; C. arabianse (Ali & Kalyankar, 1967; Petter, 1974); C. ariusi
(Srivastava & Gupta, 1976) Soota, (1983); C. armatus (Yamaguti, 1954); C.
bulbosa(Lane,1916) Barreto, 1918; C. chrysophrydis (Gendre, 1927); C.
guerreroi (Arya & Johnson, 1975) Soota, 1983; C. jaiswali (Ali, 1957)
Petter, 1974; C. jalnaensis (Kalyankar, 1971) Petter, 1974; C. karachii
(Zaidi & Khan, 1975) Soota, 1983; C. malvanae (Kalyankar, 1971) Petter,
1974; C. pangasius (Soota & Chaturvedi, 1971); C. pseudotropi (Agrawal,
1967); C. ritai Karve, 1952; C. rivulatus Soota & Sarker, 1980; C. sciaenai
(Gupta & Gupta, 1979) Soota, 1983; C. theraponi (Rasheed, 1968); C.
indica (Agrawal, 1965); C. tachysuri (Kalyankar, 1971) Petter, 1974; C.
mystusi (Gupta & Naqvi, 1985) Gupta & Masoodi, 1986; C. vinodae (Gupta
& Naqvi, 1985) Gupta & Masoodi, 1986; C. schizothoraxi Gupta &
Masoodi, 1986; C. sootai(Gupta & Masoodi, 1986); C. fujianesis (Wang,
1984); C. baylisi (Lakshmi, 2000); as all these species have a gubernaculum.
While gubernaculums is absent in the present new species. Species described
by Moravec et al., (1993a-b, 1997) also have gubernaculums. Similarly
gubernaculums is present in C. paloi(Fortes et al., 1992); C. riograndensis
(Fortes et al., 1993a) and C. fabrigasi (Fortes et al., 1993b).
Present species C. aliyaii is also different from C. marplatensis (Ingrid et
al.,2002); C.bonaerensis ( Lafranchi et al., 2004) ; C. oceaniensi ( Moravec
et al., 2005); C. pedroi (Timi and Lanfranchi,2006) ; C. pargi ( David et al.,
2007) and from C. maldivensis ( Moravec et al., 2008) in variable
combination of characters, specially in size of esophagus, spicule length and
number and position of caudal papillae in male. But the present species C.
161

aliyaii resemble in the presence of deirids with C. oceaniensis (Moravec et


al.,2005) .C. bilqeese (Bilqees et al., 1971) Petter, 1974 and C. olivaceus are
described only by females. These are also different from the present species
in the size of body, esophagus and eggs. The presence of deirids are not
reported previously from Pakistan. As mentioned the morphological
characters and presence of deirids, the present nematodes of the genus
Cucullanus appear an undescribed species for which the name C. aliyaii n.
sp., is proposed.
Soota (1983) regarded C. quadrii as synonym of C. armatus. This species
was originally described by Yamaguti (1954) from Tachysurus sp., (Arius
sp.) in Borneo and later on by Rasheed (1968) from T. serratus. Even if C.
quadrii is considered synonym to C. armatus, the present species is different
having different host,

lacking a gubernaculums and precloacal sucker,

longer subequal spicule (0.59-0.61 and 0.70-0.77) in length), vulvular lips


are prominent elevated and protruded. The caudal papillae in the present
species are 12 in number and in T. armatus caudal papillae are(9-10) pairs.
Characters such as the presence of deirids, absence of gubernaculums,
precloacal sucker, number of caudal papillae, spicules length, and
morphology of vulva, egg sizes and tail length are considered valuable
differentiating diagnostic features. Therefore, present specimens are
regarded a new species and its name C. aliyaii n.sp. is proposed. Present
species resemble in some morphological features with C .pakistanensis
Bilqees et al., 2005, including sub equal spicules, length of tail and
bifurcation at its tip, absence of gubernaculums and precloacal sucker. But
body size, length of esophagus, presence of deirids and morphology of vulva
is different from C. pakistanensis.
162

The species in which gubernaculums is absent such as C. bengalensis (Gupta


and Masoodi, 1985), But the caudal papillae are same (12 in numbers) as in
the present species.
Gubernaculum is present in C. armatus (Yamaguti, 1954); C. bulbosa
(Barreto, 1918); C. indica (Agrawal, 1965); C. tachysuri (Kalyankar, 1971)
Petter, (1974); C. mystusi, (Gupta and Masoodi, 1986); C. riograndensis,
(Fortes et al; 1993a) C. fabrigasi (Fortes et al; 1993b); C. baylist (Lakshmi,
2000). Lakshmi (2000) described C. baylisi from the related host Arius
thalassinus in India. Present new species is also separated from C baylisi
which has a gubernaculums and much smaller spicules (0.237- 0.198mm in
length), smaller eggs (0.069 x 0.048) and smaller tail (0.348 in female and
0.16- 0.18in male ). in addition a large number of sessile caudal papillae are
also present in C. baylisi. Lakshmi probably did not consider C. quadrii a
synonym of C. armatus or was unaware about this.

Etymology:

The species name Cucullanus aliyaii n. sp refers to the

honor of my best friend because of her help in this project

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)

were used for the tissue damage caused by

nematode parasites.

6.1:Description and distribution of Euthynnus alletteratus(Refinisque,


1810)
This species, commonly called little tunny and locally Dawan, can be
superficially separated from others species in the genus by the absence of
vomerine teeth, and by the pattern of dorsal markings. These markings are
more continuous and regular posteriorly. Anteriorly the bars are replaced by
short irregularly curved lines, blotches or by spots. There are approximately
25 to 35 teeth on each side of the lower jaw; the palatine teeth are sharp,
strong and quite conspicuous. There are no vomerine teeth. The stomach is a
166

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.

6.2:Histopathology of Euthynnus alletteratus (Refinisque, 1810)


No

work

has

been

done

on

histopathology

of

Euthynnus

alletteratus(Refinisque) specially with reference to fishes of Pakistan. An


attempt is made here to provide information about histopathological
conditions of Euthynnus alletteratus(Refinisque) from Karachi coast, caused
associated with nematode infection.
During the present observation histological changes are noted in the intestine
of

Euthynnus alletteratus,(70-81) infected with nematode parasites. The

infected

intestine

revealed

destruction

and

atrophy

of

intestinal

mucosa(fig.70). The section of intestine shows the section of parasites with


various stages of necrosis and degeneration of the intestinal tissue, causing
damage to the whole thickness of the bowl wall due to nematode larvae (7172). Sections of nematodes were obvious in the villi, lamina propria and
submucosa. The mucosa appeared congested and edematous. The
deformation of mucosa and submucosa result in separation of muscle
fibers(74-75)The shape of villi are changed as compared with the normal
shapes. Irregular or haphazard growth of villi is observed. Individual
epithelial cells at the tip of villi were atrophied and necrotic and showed a
variety of alteration. Villi were broadened and look-like mucosa of stomach
(Figs.78-79). Marked increase of mucus secretion was noted with sloughing
167

of villi and epithelial surface cells were dysplastic with loss of columner
orientation. In certain areas

villi

disappeared leaving flattened surface.

(Figs. 74-76). Damage to the surface epithelium resulting in desquamation of


cells leading to progressive shortening and flattening of the villi was obvious
throughout the affected areas. Chronic inflammatory reaction was obvious
(Fig.73). Shrinkage of muscular layers was observed. Thickening of blood
vessel wall and reduced lumen was also a common finding (Figs.71-74). The
inflammatory reaction produced dark aggregation of white cells in these areas
as well as scattered through out the sections.

6.3:Description and distribution of Pomadasys maculatum(Bloch, 1797)


The family Pomadasyidae (Haemalidae) of grunts is the one among 150
families of Perciformis (Ajaz, 1991). The main fishing season is from August
to October and small quantities are caught from the month of November to
January and also from February to March.

Grunt is common names for

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

(1965);Clark and Witcomb, 1980 came to the conclusion regarding the


structural adaptation of the alimentary tract to the normal diet. No
information on histopathology of infected intestine of pomadasys
maculatum(Blch) is not available and hence the work was focused on this
aspect.

6.4:Histopathology of infected intestine of Pomadasys maculatum (Bloch,


1797).
The

histopathological

conditions

in

Pomadasys

maculatum

(blch.)

encountered in sections revealed that the site of penetration is usually


edematous accompanied with hyperemia of various degrees of erosion and
bleeding in some cases. The abnormal conditions of Pomadasys
maculatum(Blch) observed and described here are inflammation, necrosis
and degeneration. Intestinal wall of Pomadasys maculatum with nematode
show severe host tissue reaction were observed. (Figs.82-89).
The infected intestine of Pomadasys maculatum shows severe damage in the
whole thickness of its wall. Erosion of intestinal wall with loss of villous
epithelial lining is usually seen. Flattening and fusion of the villi also occurs
with sloughing of epithelial covering of the villi.(82, 85-87). The villi were
abrophied becoming long and irregular with vaculation of submucosa which
also indicate atrophy (figs.88-89). At higher magnification sloughing of
epithelial cells and complete atrophy of villi and underline tissue were more
obvious (Fig.85). Several sections of nematode larvae were also observed(8384). Atrophy of tissue resulted into shrinkage and vacuolation of lamina
propria and total loss of villous structures which is a common finding
involving the deeper tissues(88-89). Shrinkage and atrophy of glandular
169

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.

In the present observation the columnar epithelial cells are

reduced in height, fragmented and sloughed. The disorganized necrotic


elements within which degenerating parasite can be seen and under this
condition inflammation are obvious (Figs. 70-73).

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

marine fish species of Karachi coast including Hilsa ilisha, Pseudosciaena


diacanthus, parastromateus niger, Mugil spp., Muraenesox cinereus, Arius
serratus, Pomadasys olivaceus, Chondroplites chinensis( Bilqees & Fatima,
1986; Fatima & Bilqees, 1987, 1989).
No further documented research was carried out on larval nematode of fish in
Pakistan beyond the publication mentioned above. Beside no information is
available on intensity and histopathology of these infection in Euthynnus
alletteratus (Dawan) and Pomadasys maculatum (Dhothar). Euthynnus
alletteratus( Dawan) are found in large number and the approximate period
of these fish is from November to January. And this is the cold season in
Pakistan where the fish demand is very high. The Pomadasys maculatum is
one of the popular and expensive edible fish.
During the present work histopathology of Euthynnus alletteratus and
Pomadasys maculatum associated with nematode parasites is carried out.
The damage caused by these parasites in intestine is observed and presented
here; Photomicrographs of parts of histological sections are prepared in
support of observation. The objective of the present study is to determine the
histopathological changes in the fish due to various infections, as the parasite
and disease of the fish constitute one of the most important problem
confronting the modern fish culture, farming and also produce human
infections.
In the present study the intestine of Euthynnus alletteratus ( Dawan), and
Pomadasys maculatum (Dhothar),infected with nematodes caused destruction
of epithelial cells and inflammation at the sites of attachment of parasites due
173

to various parasites infection. The columnar epithelial cells are reduced in


height fragmented and sloughed. The disorganized necrotic element within
which degenerating parasite can be seen and under this condition
inflammation is obvious (Figs. 70-89).
Studies related to fish infection and their effect on various fish organs is
important. In Pakistan authorities do not pay any attention to parasite diseases
in spite of the fact that parasites have adverse effects on the growth and
survival of fish specially if these infect the vital organs and are present in
large numbers or in young fish.

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.

7.1: Dietary habits


The study of the stomach contents of data of 10 marine fish species showed a
broad variation in the food and feeding habits of these fishes, which allows to
categorize them as herbivorous (Liza.verigensis and Sardinella albella) and
carnivorous (Scomberomous gutattus, Pomadasys olivaceum, pomadasys
maculatum, Otolithus ruber, Lates calcalifer, Arius maculates Sphyraena jello
and Spharyena foresteri) (Table 2-13).
.The compositions of food items are presented in table 2-4. whereas the
organisms by name, total, percentage occurrence(O%) and percentage of
frequency occurrence(F, F%) of stomachs are shown in (table 5-13).The food
categories mainly consisted of crustaceans, molluscs, helminthes, planktons,
teleosts, detritus and miscellaneous.
The analysis of the stomach contents revealed a broad range of food items,
accompanied by large amounts of detritus such as sand, mud and rock grains.
Items observed included planktons, algae, teleosts, crustaceans, mollusces,
polycheates and helminthes.

180

Data presented in this study confirmed that Liza.verigensis and Sardinella


albella were herbivores as the diet covers a wide spectrum of food ranging
from phytoplankton to zooplanktons, algae and other accessory prey items.
(Table 2-4).The main phytoplankton genera found in fish stomachs belongs to
Cyanobacteria and Bacillariophyceae and cholorophyceae (Figs. 9-20).
Anabaena,

Oscillatoria

and

Microsystis.(Cynobacteria),

Gyrosigma,

Pinnularia, Melosira, Navicula (Bacillariophyceae), scenedesmus, Chlorella


(Chlorophyceae) were found in all fish sizes (Table 5-7).The Phytoplanktons
were identified by Anjum & Hussain ,(1983); Anon ,(1987); Battish,
(1992);Nazeen & Bari, (1984) and by the help of Botany Department of Jinnah
University For Women.
Various investigations have been conducted into the food and feeding habits of
fish with the aim of determining their dietary requirements found in the
stomachs. this information is also essential in the analysis of aquaculturing.
The study of dietary habits of fish based on stomach content analysis is widely
used in fish ecology, Fagbenro et al,.( 2000). Ghandhi (1982) remarked that
feeding habits depended on the availability of fish food in the environment. It
is well known that gut length is closely related to the properties of food
consumed by fish. According to Gerking (1994) herbivorous species posses
longer guts as compared to carnivorouses allowing the consumption of food
with low digestibility. Buddington et al., (1997) and Kubitza, (1999) stated that
shorter digestive tracts as observed in carnivorous fishes, present a greater
number of villi and pyloric caeca, which amplify manifold and compensates
for a relatively short intestine.

181

7.2: Seasonal variations in dietary habits


The season consideration was also taken in the gut content of fishes. During the
present investigation of herbivorous fishes, the guts were found gorged, full and
with diversity of organisums in the months of March, April, May, June & July
but were half full and empty and with less diversity of organisms in October,
November & December. The planktons were abundant in month of March,
April, May, and June and less frequent in the months of September, October
and December.
In carnivores fishes the stomach were gorged in months of February, March and
April. Molluscs and crustaceans were dominant in April, but were frequently
seen through out the year, and polycheates were absent in August ,September,
October and January ,but were present in March, April and May. Squilla sp. and
Loligo sp. were seen in month of February and March.
There was no significant seasonal variations in food and feedng habits but the
percentage occurrence and frequency occurrence were found to be change with
season through out the study of different edible marine fishes. Similar
observation has also been reported by De-Groot (1971) Lande (1973) Dewan and
Saha (1979) and Bhuiyan & Nazrul Islam (1991).
The data obtained for feeding habits of collected fish during this investigation
were subjected for statistical analysis to check the accuracy of occurrence and
frequency occurrence of different food items found within stomachs. The value
of confidence interval falls within the limits where current results were
satisfied. In herbivorous fishes the highest frequency groups on the stomachs,
(F %) was detritus followed by planktons and copepods. While in carnivorous
182

the highest frequency group on the stomachs (F %) were miscellaneous


followed by crustaceans> mollusks> polycheates. The detritus (sand and mud)
were found in least quantity.
The data of the herbivorous fishes revealed on the basis of stomach contents
that detritus (sand, mud) were found to be of most dominant categories
(100%)

followed by planktons (85%) and copepods in all respect e.g.

percentage of occurrence and frequency of occurrence. While in all


investigated carnivores fishes, the miscellaneous items (90%) were found to
be the most dominant category in all respects e.g. percentage of occurrence
and frequency of occurrence in all size fishes. Crustaceans formed the second
important group followed by mollusks and teleosts on the basis of frequency
of occurrence. The least observed food items were polycheates.

7.3: Correlation of dietary habits and nematode parasites.


During the analysis of dietary habits, altough helminthes were mostly found in
stomach contents but as Siglar states (1958) that platyhelminthes and
nematyhelminthes do not form a part of the food material and they might have
been swallowed along with the miscellaneous in carnivorous fishes.
According to Williams et al., (1992); Marcogliex and Cone (1997) many
helminthes parasites (Parasitic worms) have complex life cycle involving
several different host depending on tropic interaction for transmission. They
can also provide valuable information on host migration and diet.
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
183

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 E. strigata. For R. coronacauda, therefore,
the feeding habits of the definitive hosts facilitate host alternation by this
species. 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 2005).
The infection variations seemed to be due to differences in host growth rate,
host feeding habit, and the distribution of marine mammal final hosts. The
results indicate that larval nematodes are useful biological indicators for the
population study of walleye pollock in Japanese waters.( Konishi, 2002)
The present study detected some patterns including correlation of Parasites
with the feeding habits of the fish, nematodes dominance among the other
helminth parasites, and infection of fish by these parasites. These studies
support the statement of Sasal et al. (1999), that the diet of the host species
is the main factor effecting parasitic community structure.

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

known (n=141) specimens. A prevalence of 62 % was observed from 745


infected fishes. All nematode recovered were restricted to the intestine.
An attempt is also made to identify and describe the new nematode species.
Identification and descriptions were made possible by the help of literature
from Yamaguti,1966; Sood, 1985; Bilqees, 2007 and also provided by Nadja
Noel and Rupert Lee Research service of British Library and also by
comparing the literature obtained by Dr. Franick Moravec from institute of
Parasitology, Czech Republic Budejovice.
One

new

genus

and

Spirocotyle

three

known

genera,

including

Dujardinascaris(Baylis, 1947); Procamallanus (Spirocamallanus (Olsen


1952) Petter 1979) and Cucullanus Muller, 1777 were identified. From these
four genera a total of 11 new species including one known (but not reported
from Pakistan yet) were recorded as follows.
i)

One new genus Spirocotyle (Camallanidae Railliet and Henry,1915)and one


new species S. otolithi was identified and described from Otolithus rubber.

ii)

Seven new species identified and described here from the known
Dujardinascaris

(Baylis,

1947)

identified

and

described

genus

including

Dujardinascaris mujibi n.sp. from Sphyraena forsteri; D. jello n.sp. from


Sphyraena jello;, D. maculatum n.sp. from Pomadasys maculatum; D.
dentatus n.sp. from Sillago sihama; D. multiporous n.sp. from Pomadasys
olivaceum; D. sphyraenaii n.sp. from Sphyraena jello; and D. sinjarii n.sp.
from Otolithus rube
iii) Two new species of the genus Procamallanus (Spirocamallanus ( Olsen 1952)
Petter 1979), were also identified and described here
185

including, Procamallanus (Spirocamallanus) riaziaii n.sp.and P.(S.) ruberii.


Both species were recovered from Otolithus ruber
Two female specimens of unidentified species were also reported here
from Otolithus ruber. Species is not identified as male specimens were
not available.
iv)One new species of the genus Cucullanus Muller, 1777 was identified and
described here as C. aliyaii n.sp. from Otolithus ruber.

7.4 : Parasitic diversity


Most studies of food and feeding habits of fishes, from varying habitat, 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
habit of a species (Staples, 1975).One would examine interspecific variation in
parasitic diversity among a group of host species from the same area, all
examined in a standard way by the same researchers ( Luque et al, 2004).The
parasitic way of life is probably one of the most common life found on earth
(May, 1988, winder 1997,1998). Virtually every species is parasitized at some
point during its life time (Price, 1980) in a heavy infection a parasite could
cause harm and become pathogenic to a host individual (Anderson & May
1979, May & Anderson 1979). The host size variations and endoparasitic
communities was studied by Poulin & Valtonen(2001). There is increasing
evidence that parasites are an important element of marine biodiversity (
Mariaux, 1996; Palm et al., 1999; Kilmpel et al.2001).
During the present study diversity was notable as one parasites is found in
186

many hosts(genus Dujardinascaris in different hosts, Pomadasys, Sillago


sihama and Sphyraena)and diferent nematode species were found in a single
host e.g. ( different species of Procamallanus(S.) were found in a single host
of the genus Otolithus.

7.5: Histopathology of fishes


During nematode investigation parasitic infestation were checked at intestinal
level and find out that Parasites and disease reduce fish production by affecting
the normal physiology of fish as stated by Kabata (1985) and which, if left
uncontrolled can result in mass mortalities or in some cases infection of man
and other vertebrates that consume them. The diseases due to the adult and
larval nematodes are very common in marine fishes and world wide in
distribution. The parasites invade various tissues and organs of fish. Among
the known sites of infection are the stomach, intestine, liver, gonads, visceral
mesenteries, peritoneum body cavity, blood vessels, swim bladder, and
connective tissues, fin, orbits of the eye and brain. Most species of 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.
A considerable number of new species and genera have added recently and
many more remain to be discovered. The diseases due to the adult and larval
nematodes are very common in marine fishes and world wide in distribution.
The parasites invade various tissues and organs of fish. In fisheries biology,
187

parasitological studies have increasing importance, because parasites may


serve as natural markers for the identification of fish stock ( MacKenzie, 1983;
Williams et al, 1992). Moreover, parasites can help to analyses the diet of fish
species, serving as biological indicator of the prey species and their origin(
Campbell et al. 1980; Palm et al. 1998).
Small fish species are frequent food items for piscivorous fish. Predatory fish
largely acquire and accumulate parasites by ingesting small fish species that
are infested and serve as carriers ( Lile, 1998). Asor and Arenc (2000) stated
that the site of information varied with the parasite, but the site most affected
generally is the intestine
During the present study observations were made on the tissue section of
various parts of intestine infected with nematodes.
During the present observation histological changes are noted in the
intestine of Euthynnus alletteratus, infected with nematode species.(Fifs. 7081).The infected intestine revealed damage to the whole thickness of the bowl
wall due to nematode larvae. The mucosa appeared congested and edematous.
The section of intestine shows the section of parasites with various stages of
necrosis and degeneration of the intestinal tissue. The shapes of villi were
changed as compared with the normal shapes. Irregular or haphazard growth of
villi was observed villi were broadened and look-like mucosa of stomach
(Figs.78-79). Sections of nematodes were obvious showed necrosis in mucosa
and submucosa (Figs 71-72). Marked increase of mucus secretion was noted
with sloughing of villi and epithelial surface cells were dysplastic with loss of
columner orientation. Villi were broadened and look-like mucosa of stomach
188

(Figs. 74-79).
surface(Fig.76).

In certain areas villi disappeared leaving flattened


Chronic

inflammatory

reaction

was

obvious.

The

inflammatory reaction produced dark aggregation of white cells in these areas


as well as scattered through out the section.
The infected intestine of Pomadasys maculatum shows severe damage in the
whole thickness of its wall(Figs. 82-89). Erosion of intestinal wall with loss of
villous epithelial lining is usually seen. Flattening and fusion of the villi also
occurs with sloughing of epithelial covering of the villi.The villi were
abrophied becoming long and irregular with vaculation of submucosa which
also indicate atrophy(Figs.82-89). At higher magnification sloughing of
epithelial cells and complete atrophy of villi and underline tissues were more
obvious (Figs.82, 85-87).Several sections of nematode larvae were
observed(Figs.83-84). Atrophy of tissue resulted into shrinkage and
vacuolation of lamina propria and total loss of villous structures which is a
common finding involving the deeper tissue (Figs.88-89) with the crypt glands
lengthening and degenerating of its structure also occurred. Shrinkage and
atrophy of glandular structures resulted into formation of large spaces at the
periphery. The muscular layers were also affected. Degeneration of tissue was
also obvious. In more severe condition all the intestinal morphology was lost.
Villius structures were not differentiated and appear as strings of tissue. The
crypt glands were degenerated leaving the cell remnant of glandular structure
fragments and remnant of glandular structure as dark staining patches of tissue
and lumens of the crypt glands were obliterated.
These observations are similar to those described in other fishes of Karachi
coast with nematode larvae (Bilqees and Fatima, 1995). Other workers have
189

also reported enlargement and inflammation of intestine (Bullock, 1963). Some


workers observed destruction of epithelium at the point of attachment.
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.
In the present study, the columnar epithelial cells are reduced in height,
fragmented and sloughed(Figs.88-89). The disorganized necrotic elements
within which degenerating parasite can be seen and under this condition
inflammation is obvious.

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.

Identification of nematodes with help of high technology.


Disease caused by nematode parasite
Effect of nematodes on fish.
Establishment of the relationship between weight and length of these
parasites with fish growth.
Weight and length of fish in presence and absence of nematode.
Establishment of the relationship between the food content and presence of
nematode parasite.
Histopathology of fish infected with nematode parasite
Weight and length of fish in presence and absence of nematode

191

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Table 1: PARASITE HOST LIST SHOWING BIODIVERSITY OF


NEMATODES
Nematode genera

Fish Host

Cucullanus Muller,
(1777)

Tachysurus maculates; Tachysurus


serratus; Erethistea elongate;
Lates calcarifer; Johnius spp., Strongylura
strongylurus; Sparus sp.; Acanthopagrus berda;
Stolephorus indicus; Pomadasys olivaceus;
Therapon sp.; Lisha sp.; Arius serratus; Sciaena
diacanthus;

Dichelyne Jugerskiold,
(1902)

Apolectus niger; Chirocentrus dorab;


Eleutheronema
tetradactylum; Lates calcarifer; Protonibea
dicanthus;
Pomadasys hasta; Pomadasys olivaceus; Puntius
thalassimus;

Camallanus Raillliat & Henry,


(1915)

Scomberoides tala; Protonibea


diacanthus, Muraenesox cinerius
Scomberomorus guttatus; Rastrelliger kanagurta;
Mastacembalus punctatus., Scomberomorus
interruptum

Ecihnocephalus Molin,
(1858)

Dasyatis brucco; D. pastinaca, D.


sephan; D. walga ; Urogymnus
asperrimus; Cynoglossus snidenses; Lates
calcarifer; Thrissocles spp.; Aetobatis narinari;
Muraenesox cinereus.

Heliconema Travassos
(1919)

Mugil hamiltonii; Echidna catenata;


Muraenesox spp.;

Bulbocephalus Rasheed,
(1966)

Eleutneronema tatradactylum, Jhikar


spp.
250

Rahbdochona Railliet,
( 1916)

Parastromateus niger,

Heptochona Rasheed
(1964)

Scomberoides tala; Apolectus niger;


Parastromateus niger

Cyrnea (Procynea)
Rasheed, (1965 )

Pampus spp.

Goezia Zeder,
(1800)

Apolectus niger; Myrmillo manazo;


Rachcentron canadus.

Lappetascaris Rasheed
(1965)
,

Lutjanus sp.; Ilisha ilisha;Anadontostoma


chacunda; Johnius sp.; Kurtus indicus.

Raphidascaroides Yamaguti,
( 1941)

Sphyrna blochii

Paranisakis Baylis,
( 1923 )

Johnius sp.

Contracaecum Railliet & Henry


(1918)

Muraenesox cinereus, Upeneus vittatus,


Otolitus argenteus,Otolithus rubber.

Dujardinascaris Baylis,
(1947)

Johnius sp. Protonibea diacanthus,


Sciaena sp. Otolithus rubber

Philometra Costa,
(1845)

Lateolabracis japonicus; Parapristipoma


trilineatum; Epinephelus akara;
Sciaena schlegeli; S. coiter; S glevui; Lates
calcarifer; Johnius sp. Otolithus rubber;
Hemisphanus georgii; Scomberomorus sp.
Protonibea diacanthus; Eleutheronema
tetradactylum; Mugil cephalus Pomodasys
251

hasta; Otilithus argenteus;


Spirocamallanus Olsen ,
(1950)

Procamallanus Baylis,
( 1923 )

Johnius dussumieri; Protonibea


diacanthus;Otolithus argenteus;
Otolithus rubber; Otolithus rubber;
MugilSpeigleri;Pomadasys hasta;
Sillago sihama; Argyrops spinifer ;
Sparus berda;Tachysurus berda;
Sphaeroides lunaris.

Sparus spinifer; Otolithus argenteus;

Philometroides Yamaguti,
(1935)

Pomadasys hasta; Otolithus rubber;


Otolithus argenteus.

Hepatonema Rasheed,
( 1965 )

Apolectus niger;

Neospinitectus Kalyankar,
( 1971 )
Neogoezia Kreis,
( 1937 )

Pampus spp.

Myrmillo manazo; Rachycentron anadus

Porrocaecum Railliet &


Henry,
( 1912 )

Otolithus rubber

252

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