Subscribe Now Subscribe Today
Research Article
 

Ecology of Metazoan Parasite Community of Marine Threadfin Fish, Polydactylus sextarius (Bloch and Schneider, 1801) from Visakhapatnam Coast, Bay of Bengal



Mani Gudivada, Anuprasanna Vankara, M. Hemalatha and C. Vijayalakshmi
 
Facebook Twitter Digg Reddit Linkedin StumbleUpon E-mail
ABSTRACT

In this study, the structure and diversity of metazoan parasite community and their interactions with 696 Polydactylus sextarius have been studied for two consecutive years 2005-2006 and 2006-2007 from Visakhapatnam (17.67°’N and 83.32°’E), in the coastal zone of Bay of Bengal Andhra Pradesh. Of the 676 host species examined, 563 (83%) hosts were parasitized by at least one or more metazoan parasite species. A total of 5911 specimens were obtained representing 24 species comprising 2 monogenetic trematodes, 11 digenetic trematodes, 2 cestode larvae, 1 nematode, 4 Acanthocephalans, 3 copepods and 1 isopod. Endoparasites preponderate the majority of the components of the infracommunities analysed and represented 92.6% of the total parasites obtained. Larval cestodes (3515) and digeneans (1165) were the most prevalent in the parasite community of the host. Larval cestode, Scolex pleuronectis is the only secondary species while the remaining are satellite species being less in number. Impact of abiotic factors like temperature, water currents and biotic factors like feeding habit, diet, immunity, lifespan of host on parasitization; the relationship between host size and prevalence of infection were thoroughly investigated but the host sex was not taken into consideration due to protandrous nature of the host.

Services
Related Articles in ASCI
Search in Google Scholar
View Citation
Report Citation

 
  How to cite this article:

Mani Gudivada, Anuprasanna Vankara, M. Hemalatha and C. Vijayalakshmi, 2014. Ecology of Metazoan Parasite Community of Marine Threadfin Fish, Polydactylus sextarius (Bloch and Schneider, 1801) from Visakhapatnam Coast, Bay of Bengal. Asian Journal of Animal Sciences, 8: 47-55.

DOI: 10.3923/ajas.2014.47.55

URL: https://scialert.net/abstract/?doi=ajas.2014.47.55
 
Received: November 26, 2013; Accepted: February 08, 2014; Published: April 11, 2014



INTRODUCTION

Marine environment is complex and provides extremely diverse habitat for a host and their parasites. Every host population within a habitat therefore acquires a characteristic array of parasites and these parasitic communities in their turn can also characterize the habitat (Dogiel et al., l962) and this concept forms the basis of modern ecological parasitology which deals with distribution and abundance of parasites in time and space (Kennedy, 1975). Ecological concepts are essential in the study of parasites to understand host-parasite relationships and their environment. In this association, parasites have to encounter different types of hazards like risks in transmission from host to host, vulnerability of free living stages in the environment, difficulty in host parasitic defensive responses offered by the host. The parasite community is influenced by the macro environment in which the host lives and the micro environment in which the parasite lives. Parasites act as bioindicators or sensitive probes (MacKenzie et al., 1995; Kennedy, 1997; Lafferty, 1997, 2008; Overstreet, 1997; Sures et al., 1997, 1999; Valtonen et al., 1997; Lafferty and Kuris, 1999; Sures, 2001; Ferrer-Castello et al., 2007; Vidal-Martinez et al., 2010). Parasite community ecology is a recent discipline that defines the patterns in parasite community structure, richness and diversity (Esch et al., 1990; Kennedy, 1995; Gudivada and Vankara, 2010; Martinez-Aquino et al., 2011). Marine fish parasite communities have greater species richness and abundance because of their greater vagility and wider breadth of diet when compared with their freshwater counterparts (Kennedy et al., 1986). Polynemids or threadfin fish represents an ideal model to assess parasite community structure from Visakhapatnam coast (17.67°’N and 83.32°’E), along the east coast of Bay of Bengal andhra Pradesh as they have anecdotal feeding habits and wide distribution. Of the available six species of Polynemid fish along this coast, Polydactylus sextarius (Schneider), Polydactylus plebeius (Broussonet) and Eleutheronema tetradactylum (Shaw) were of common occurrence throughout the year and F. heptadactyla (Cuvier), Leptamelanosoma indicum (Shaw) and P. sexfilis (Valenciennes) showed seasonal occurence. Only partial data is available on the metazoan parasites of polynemid fish and consequential work has not been performed so far in these fish (Gudivada and Vankara, 2010). Regardless of their nutritive value and accessibility as a profitable sea food to the local communities, this fish has become a highly neglected group in terms of their parasitological studies. The present study is designed to determine the structure of parasitic community and seasonal influence on metazoan parasite fauna of P. sextarius Bloch and Schneider, 1801 which is available at this coast throughout the year.

MATERIALS AND METHODS

Study area: The study has been designed for two successive years from July 2005 to June 2007. Total samples of 676 P. sextarius were analysed. Fishes were sexed, measured for its length and weight independently and all organs were carefully investigated to collect the parasites. Conventional techniques (Hiware et al., 2003; Madhavi et al., 2007) were employed for the preparation of permanent slides. P. sextarius measured 6-25 cm in total length. The correlation between the host’s length and prevalence of parasites was evaluated by Pearson’s correlation coefficient r. Berger-Parker index of dominance (Magurran, 1988) was employed to study the dominance frequencies of each parasite infracommunity. Effect of host sex on prevalence and abundance of parasites was not considered due to protandrous nature of the fish. Shannon-Weiner index (H’) was employed to study the parasite species diversity. Seasonal influence on the rate of infection was calculated by a Chi-square test to depict the significance between the season and prevalence of parasite species.

RESULTS

Of the 676 fishes examined, 563 (83%) fish were frequently parasitized with one or more than one parasite species. 24 species of metazoan parasites (2 monogenetic trematodes, Choricotyle polynemi and Polynemicola sextariusii n.sp.; 11 species of Digeneans-two species were larval forms, Metacercariae of Prosorhynchus (553) and Didymozoid larvae (80) and the remaining 9 species are adults-Lecithochirium polynemi, L. glandulum, Erilepturus hamatus, Aponurus laganculus, Didymozoid sp., Timonia cabellaria, Helicometrina nimia, Allopodocotyle argyropsi; 2 cestode larvae-Scolex pleuronectis and trypanorhynchids; 1 nematode-Camallanus cotti; 4 Acanthocephalans-Raorhynchus polynemi, Neoechinorhynchus topseyi, Gorgorhynchoides indicus and Serrasentis sagittifer; 3 copepods-Caligus phipsoni, C. laticaudus and Chalimus stages of C. polynemi n.sp. and 1 isopod, Gnathia maxillaris) were explored from the host (Table 1).

Table 1: Metazoan parasites of Polydactylus sextarius
Image for - Ecology of Metazoan Parasite Community of Marine Threadfin Fish, Polydactylus sextarius (Bloch and Schneider, 1801) from Visakhapatnam Coast, Bay of Bengal

Table 2: Frequency distribution of No. of parasitic groups per individual in P. sextarius
Image for - Ecology of Metazoan Parasite Community of Marine Threadfin Fish, Polydactylus sextarius (Bloch and Schneider, 1801) from Visakhapatnam Coast, Bay of Bengal
n = 676, Σx = 5, x = 5/676 = 0.007, Range: 1-5

Endoparasites prevail the majority of the components of the infracommunities and represented 92.6% of the total parasites collected which was evidenced by Berger-parker’s dominance indices and mean total parasites (Table 2). The parasitic fauna of P. sextarius is outweighed by larval cestodes (58%) followed by digeneans, acanthocephalans, nematodes, copepods, monogeneans and isopods. 122 hosts (18.1%) were infected with single parasitic groups, 194 (28.7%) with any two parasitic groups, 162 (24%) with 3 parasitic groups and 71 (10.5%) with 4 and 14 hosts (2.07%) with 5 parasitic groups, respectively. Not even a single fish was infected with all the parasitic groups (Table 2). Scolex pleuronectis (3511) constitute 46.3% of the total parasites collected. Metacercariae of Prosorhynchus (553) outweighs the parasite fauna subsequently followed by an acanthocephalan, Raorhynchus polynemi (453).

Table 3: Diversity parameters of metazoan parasite communities of P. sextarius
Image for - Ecology of Metazoan Parasite Community of Marine Threadfin Fish, Polydactylus sextarius (Bloch and Schneider, 1801) from Visakhapatnam Coast, Bay of Bengal

Table 4: No. of parasites obtained, dominance index and mean total parasites of different parasitic groups in P. sextarius
Image for - Ecology of Metazoan Parasite Community of Marine Threadfin Fish, Polydactylus sextarius (Bloch and Schneider, 1801) from Visakhapatnam Coast, Bay of Bengal

A total of 5911 individual parasites were collected with 8 parasites/fish. The mean parasite diversity (Shannon’s H’ index) is 0.81±0.35 though the community is very rich in parasite species; the diversity index values are comparatively low (Table 3). Only two species, Scolex pleuronectis and Raorhynchus polynemi are common with a prevalence ranging between 30-50%. Six species, namely Metacercariae Prosorhynchus, L. glandulum, Didymozoid sp., Caligus phipsoni, Chalimus stages of Caligus n.sp. and Camallanus cotti are frequent with prevalence ranging between 10-30%. Two species namely, Didymozoid larvae and Gorgorhynchoides indicus are rare with prevalence of 4-10% and the remaining species, P. sextarius n.sp., H. nimia, A. argyropsi, L. polynemi, A. laganculus, C. laticaudus, G. maxillaris, N. topseyi, S. sagittifer and Trypanorhynchid larvae are sporadic with <4% prevalence. There was no core species in the host. Scolex pleuronectis was the only secondary species while the remaining 23 species are satellite species. Scolex pleuronectis presented the highest dominance value of 0.576 followed by Metacercariae Prosorhynchus (0.090) and R. polynemi (0.074). Mean of total parasite species of S. pleuronectis, Metacercariae Prosorhynchus and R. polynemi was 5.19, 0.82 and 0.67 respectively (Table 4 and 5). Prevalence of parasites was appreciably in relation to site of infection. Infections were more in intestine when compared to other locations. Mean intensity (11.2) and mean abundance (5.2) was high in S. pleuronectis. Host size operates as a crucial factor in determining the parasitic burden in a host. To find out the possible correlation between the host size and total parasitic infection, fishes ranging from 6-25 cm were examined and categorized into 4 groups i.e., Group 1 (6.0-10.0 cm), Group 2 (10.1-15.0 cm), Group 3 (15.1-20.0 cm) and Group 4 (20.1-25.0 cm). Overall parasitization was high in moderate fishes ranging from 10.0-20.0 cm (Group 3 and 2) but fish belonging to Group 1 and 4 showed low parasitization. Correlation coefficient ‘r’ was calculated for parasites encountered and the calculated values of ‘r’ 0.14 portray a meager positive correlation (Table 6). Host sex was not considered due to protandrous nature of the host.

Seasonal influence: Chi-square test was applied to reveal the significance in the rate of parasitization during different seasons-Rainy, winter and summer. Seasonal influence was not significant on parasitism in P. sextarius. The calculated value of chi-square is 1.86 for the year 2005-06, based on a standard of 0.05 alpha, the expected p-value of 0.3950 proposed that there is not a statistically considerable association between the comparison variables. For the year 2006-2007 the chi-square value is 3.23 and the expected p-value of 0.1990 implied no significant association (Table 7).

Table 5: Diversity parameters and distribution of parasitic species infecting P. sextarius
Image for - Ecology of Metazoan Parasite Community of Marine Threadfin Fish, Polydactylus sextarius (Bloch and Schneider, 1801) from Visakhapatnam Coast, Bay of Bengal
No.of fish examined: 676, Common: 30-50%, Frequent: 10-30%, Rare: 4-10%, Sporadic: ≤4% Core, sp’s: ≥66%, Secondary sp’s: Between 66-33%, Satellite sp’s: ≤33%

Table 6: Correlation of host size with the parasitization
Image for - Ecology of Metazoan Parasite Community of Marine Threadfin Fish, Polydactylus sextarius (Bloch and Schneider, 1801) from Visakhapatnam Coast, Bay of Bengal

Table 7: Influence of seasons on parasitization of P. sextarius
Image for - Ecology of Metazoan Parasite Community of Marine Threadfin Fish, Polydactylus sextarius (Bloch and Schneider, 1801) from Visakhapatnam Coast, Bay of Bengal

DISCUSSION

Both the years portrayed good resemblance in overall prevalence, mean intensity and mean abundance with negligible deviation. These variations depend on factors such as maturity and density of the host population and its stage. Temperature serves as one of the crucial factors in controlling the parasitic infections (Hedgpeth, 1957; Hopkins, 1959; Chubb, 1963; Awachie, 1966; Manter, 1966; Kennedy, 1971, 1975, 1977, 1997; Muralidhar, 1989; Rohde, 1993; Rodrigues and Saraiva, 1996; Chapman et al., 2000; Turner, 2000; Wang et al., 2001; Mouritsen and Poulin, 2002). Rohde (1993) had the same opinion that more infections are seen in warm seas than the colder ones. Temperature plays an important role in controlling the parasitic fauna either directly or indirectly in the present study. Though, statistically there was no significant association between the seasons and prevalence of infection but parasitization was comparatively high during winter months than in other months. The environmental circumstances of tropical waters are fairly complimentary in winter months as the waters will be warm but not ice cold and these moderate temperatures are favorable to zooplankton, invertebrate and smaller vertebrate fauna to flourish. The calmness in the sea during this season obviously naturally corresponds to the peak in feeding activities of the fish and recruitment of infection takes place after summer and reaches their climax in winter months. There is only a meager positive correlation between the host size and total parasitic infection. Pearson (1968), Dogiel (1970), Kuperman (1973), Cannon (1977), Williams and Jones (1994), Luque et al. (1996) and Johnson et al. (2004) has emphasized the impact of diet and feeding habits on the parasitic infection in the hosts. Impact of food and feeding habits of the host serve as prime causes of larval parasitic abundance as P. sextarius being carnivorous feed on crustaceans, molluscs, snails and shrimps which are primary intermediate hosts for the most of the digeneans and cestodes). Variations in the infection rate with age groups might be due to the less feeding capacity in younger fish and resistance or immunity in older fish which averts the novel extra parasite burdens (Lo et al., 1998; Zelmer and Arai, 1998; Johnson et al., 2004). Parasite life span also plays its role with number of parasites diminishing in the host with growing age. Thus, abundance of parasite population is attributed to feeding capacity of the host which is governed by biotic and abiotic factors like temperature, water currents etc. Host sex was not found to be a significant factor in determining the infection rate in helminth parasites according to Lawrence (1970), Kennedy (1975), Muzzall (1980), Belghyti et al. (1994) and Abdallah et al. (2005) and in the present study host sex is not taken into consideration due to protandrous nature of the host.

CONCLUSION

Thus from the present survey it can be said that parasite community of a host are predictable and hierarchical. The parasite diversity of a host can be attributed to its phylogeny and also to the presence of intermediate host population in that area. But the abundance of parasite population can be attributed to the vagility and feeding capacity of the host which is governed by the external ecological factors like temperature. Kennedy et al. (1986) and Holmes (1990) compared the intestinal helminth community diversity in a series of freshwater fish and bird hosts and found that the diversity is rich in birds than in freshwater fish. They also suggested that marine fish helminth communities should be more diverse than that of freshwater since there is greater diversity of invertebrates (possible intermediate hosts) in the sea. The present investigation is in concordance with the views of Kennedy et al. (1986) and Holmes (1990) suggesting that poylnemid fish operate as potential intermediate hosts with rich and diversified parasitic fauna than their freshwater counterparts.

ACKNOWLEDGMENTS

The first author is grateful to the UGC for providing financial assistance under the Fellow Improvement Programme (FIP) and the second author is thankful to Council of Scientific and Industrial Research, New Delhi for providing the financial assistance as senior research fellow.

REFERENCES

1:  Abdallah, V.D., R.K. De Azevedo and J.L. Luque, 2005. Ecologia da comunidade de metazoarios parasitos do sairu Cyphocharax gilbert (Quoy e Gaimard, 1824) (Characiformes: Curimatidae) Do Rio Guandu, Estado do Rio de Janeiro, Brasil [Community ecology of metazoan parasites of Cyphocharax gilbert (Quoy e Gaimard, 1824) (Characiformes: Curimatidae) from Guandu river, State of Rio de Janeiro, Brazil]. Revista Brasileira Parasitologia Veterinaria, 14: 154-159 (In Brazilian).
Direct Link  |  

2:  Martinez-Aquino, A., D.I. Hernondez-Mena, R. Pnrez-Rodriguez, R. Aguilar-Aguilar and G.P.P. de Leon, 2011. Endohelminth parasites of the freshwater fish Zoogoneticus purhepechus (Cyprinodontiformes: Goodeidae) from two springs in the Lower Lerma River, Mexico. Revista Mexicana de Biodiversidad, 82: 1132-1137.
Direct Link  |  

3:  Awachie, J.B.E., 1966. Observations on Cyathocephalus truncates pallas, 1781 (Cestoda: Spathebothriidea) in its intermediate and definitive hosts in a trout stream, North Wales. J. Helminthol., 40: 1-10.
Direct Link  |  

4:  Belghyti, D., O. Berrada-Rkhami, V. Boy, P. Aguesse and C. Gabrian, 1994. Population biology of two helminth parasites of flatfishes from the Atlantic coast of Morocco. J. Fish Biol., 44: 1005-1021.
CrossRef  |  Direct Link  |  

5:  Cannon, L.R.G., 1977. Some ecological relationships of larval ascaridoids from south-eastern Queensland marine fishes. Int. J. Parasitol., 7: 227-232.
CrossRef  |  PubMed  |  

6:  Chapman, L.J., C.A. Lanciani and C.A. Chapman, 2000. Ecology of a diplozoon parasite on the gills of the African cyprinid Barbus neumayeri. Afr. J. Ecol., 38: 312-320.
CrossRef  |  Direct Link  |  

7:  Chubb, J.C., 1963. On the characterization of the parasite fauna of the fish of Llyn Tegid. Proc. Zool. Soc. London, 141: 609-621.
CrossRef  |  Direct Link  |  

8:  Dogiel, V.A., 1962. Ecology of Parasites of Freshwater Fishes. In: Parasitology of Fishes, Dogiel, V.A., G.K. Petrushevski and Y.I. Polyyanski (Eds.). Oliver and Boyd, London, UK., pp: 1-47

9:  Dogiel, V., 1970. Ecology of the Parasites of Freshwater Fishes. In: Parasitology of Fishes, Dogiel, V.A., G.K. Petrushevski and Y.I. Polyanski (Eds.). T.F.H. Publications Inc. Ltd., Hong Kong, pp: 1-47

10:  Esch, G.W., A.O. Bush and J.M. Aho, 1990. Parasite Communities: Patterns and Process. Chapman and Hall, London, ISBN: 9780412335402, Pages: 335

11:  Ferrer-Castello, E., J.A. Raga and F.J. Aznar, 2007. Parasites as fish population tags and pseudoreplication problems: The case of striped red mullet Mullus surmuletus in the Spanish Mediterranean. J. Helminthol., 81: 169-178.
CrossRef  |  Direct Link  |  

12:  Hedgpeth, J.W., 1957. Marine Biogeography. In: Treatise on Marine Ecology and Paleoecology, Hedgpeth, J.W. (Ed). Vol. 67, Geological Society of America, USA., pp: 359-382

13:  Hiware, C.J., B.V. Jadhav and A.D. Mohekar, 2003. Applied Parasitology: A Practical Manual. Mangal Deep Publications, Jaipur, India, ISBN-13: 978-8175941151

14:  Holmes, J.C., 1990. Competition, contacts and other factors restricting niches of parasitic helminths. Ann. Parasitol. Hum. Comp., 65: 69-72.
CrossRef  |  PubMed  |  Direct Link  |  

15:  Hopkins, C.A., 1959. Seasonal variations in the incidence and development of cestode Proteocephalus fillicolis (Rud, 1810) in Gasterosteus aculeatus L. I1766). Parasitology, 49: 529-542.

16:  Johnson, M.W., P.A. Nelson and T.A. Dick, 2004. Structuring mechanisms of yellow perch (Perca flavescens) parasite communities: Host age, diet and local factors. Can. J. Zool., 82: 1291-1301.
Direct Link  |  

17:  Kennedy, C.R., 1971. The effect of temperature upon the establishment and survival of the cestode Caryophyllaeus laticeps in orfe, Leuciscus idus. Parasitology, 63: 59-66.
CrossRef  |  Direct Link  |  

18:  Kennedy, C.R., 1975. Ecological Animal Parasitology. John Wiley and Sons, Oxford, UK., ISBN-13: 9780470469101, Pages: 163

19:  Kennedy, C.R., 1977. The Regulation of Fish Parasite Populations. In: Regulation of Parasite Populations, Esch, G.W. (Ed.). Academic Press, USA., pp: 61-109

20:  Kennedy, C.R., 1997. Freshwater fish parasites and environmental quality: An overview and caution. Parassitolgia, 39: 249-254.
PubMed  |  Direct Link  |  

21:  Kennedy, C.R., A.O. Bush and J.M. Aho, 1986. Patterns in helminth communities: Why are birds and fish different? Parasitology, 93: 205-215.
PubMed  |  

22:  Kennedy, C.R., 1995. Richness and diversity of macroparasite communities in tropical eels Anguilla reinhardtii in Queensland, Australia. Parasitology, 111: 233-245.
CrossRef  |  

23:  Kuperman, B.I., 1973. Tapeworms of the Genus Triaenophorus: Parasites of Fishes. Amerind Publishing Co. Pvt. Ltd., New Delhi

24:  Lafferty, K.D., 1997. Environmental parasitology: What can parasites tell us about human impacts on the environment? Parasitol. Today, 13: 251-255.
Direct Link  |  

25:  Lafferty, K.D., 2008. Ecosystem consequences of fish parasites. J. Fish Biol., 73: 2083-2093.
CrossRef  |  Direct Link  |  

26:  Lafferty, K.D. and A.M. Kuris, 1999. How environmental stress affects the impacts of parasites. Limnol. Oceanogr., 44: 925-931.

27:  Lawrence, J.L., 1970. Effects of season, host age and sex on endohelminths of Catostomi commersoni. J. Parasitol., 56: 567-571.
CrossRef  |  Direct Link  |  

28:  Lo, C.M., S. Morand and R. Galzin, 1998. Parasite diversity\host age and size relationship in three coral-reef fishes from French Polynesia. Int. J. Parasitol., 28: 1695-1708.
CrossRef  |  Direct Link  |  

29:  Luque, J.L., J.F.R. Amato and R.M. Takemoto, 1996. Comparative analysis of the communities of metazoan parasites of Orthopristis rubber and Haemulon steindachneri (Osteichthyes: Haemulidae) from the Southeastern Brazilian littoral: I. Structure and influence of size and sex of the hosts. Revista Brasileira Biologia, 56: 279-292.

30:  MacKenzie, K., H.H. Williams, B. Williams, A.H. McVicar and R. Siddall, 1995. Parasites as indicators of water quality and the potential use of helminth transmission in marine pollution studies. Adv. Parasitol., 35: 85-144.
CrossRef  |  Direct Link  |  

31:  Madhavi, R., C. Vijayalakshmi and K. Shyamasundari, 2007. Collection, Staining and identification of Different Helminth Parasites: A Manual of the Workshop on Fish Parasites-Taxonomy Capacity Building. Andhra University Press, India

32:  Magurran, A.E., 1988. Ecological Diversity and its Measurement. 1st Edn., Princeton University Press, Princeton, ISBN: 0691084858

33:  Gudivada, M. and P. Vankara, 2010. Population dynamics of metazoan parasites of Marine threadfin fish, Polydactylus sextarius (bloch and schneider, 1801) from Visakhapatnam coast, Bay of Bengal. Bioscan, 5: 555-561.
Direct Link  |  

34:  Manter, H.W., 1966. Parasites of Fishes as Biological Indicators of Recent and Ancient Conditions. In: Host Parsite Relationships, McCauley, J.E. (Ed.). Oregon state University Press, USA., pp: 59-71

35:  Mouritsen, K.N. and R. Poulin, 2002. Parasitism, climate oscillations and the structure of natural communities. Oikos, 97: 462-468.
CrossRef  |  Direct Link  |  

36:  Muralidhar, A., 1989. Seasonal variation of helminth parasites in marine fishes at East coast of India. Ind. J. Helminthol., 41: 1-4.

37:  Muzzall, P.M., 1980. Population biology and host-parasite relationships of Triganodistomum attenuatum (Trematoda: Lissorchiidae) infecting the white sucker, Catostomus commersoni (Lacepede). J. Parasitol., 66: 293-298.
Direct Link  |  

38:  Overstreet, R.M., 1997. Parasitological data as monitors of environmental health. Parassitologia, 39: 169-175.
PubMed  |  Direct Link  |  

39:  Pearson, J.C., 1968. Observations on the morphology and life-cycle of Paucivitellosus fragilis Coil, Reid and Kuntz, 1965 (Trematoda: Bivesiculidae). Parasitology, 58: 769-788.
CrossRef  |  

40:  Rodrigues, A.A. and A. Saraiva, 1996. Spatial distribution and seasonality of Pseudodactylogyrus anguillae and P. bini (Monogenea: Pseudodactylogyridae) on the gills of the European eel Anguilla anguilla from portugal. Bull. Eur. Asso. Fish Pathol., 16: 85-88.

41:  Rohde, K., 1993. Ecology of Marine Parasites: An Introduction To Marine Parasitology. 2nd Edn., CAB International, Wallingford CT., USA., ISBN: 13-9780851988450, Pages: 298

42:  Sures, B., 2001. The use of fish parasites as bioindicators of heavy metals in aquatic ecosystems: A review. Aquatic Ecol., 35: 245-255.
CrossRef  |  Direct Link  |  

43:  Sures, B., H. Taraschewski and R. Siddall, 1997. Heavy metal concentrations in adult acanthocephalans and cestodes compared to their fish hosts and to established free-living bioindicators. Parassitologia, 39: 213-218.
PubMed  |  Direct Link  |  

44:  Sures, B., R. Siddall and H. Taraschewski, 1999. Parasites as accumulation indicators of heavy metal pollution. Parasitol. Today, 15: 16-21.
CrossRef  |  Direct Link  |  

45:  Turner, H.M., 2000. Seasonality of Alloglossoides cardicola (Trematoda: Macroderiodea) infection in the cray fish, Procambarus acutus. South Western Nat., 45: 69-71.

46:  Valtonen, E.T., J.C. Holmes and M. Koskivaara, 1997. Eutrophication, pollution and fragmentation: Effects on parasite communities in roach (Rutilus rutilus) and perch (Perca fluviatilis) in four lakes in central Finland. Can. J. Fish. Aquatic Sci., 54: 572-585.
CrossRef  |  

47:  Vidal-Martinez, V.M., P. Daniel, B. Sures, S.T. Purucker and R. Poulin, 2010. Can Parasites Really Reveal Environmental Impact. Cell Press, USA., pp: 1-8

48:  Wang, G.T., W.J. Yao and P. Nie, 2001. Seasonal occurrence of Dollfustrema vaneyi (Digenea: Bucephalidae) metaceraria in the bull head cat fish Pseudobagnus fluvidraeo in a reservoir in china. Dis. Aquatic Org., 44: 127-131.

49:  Williams, H.M. and A. Jones, 1994. Parasitic Worms of Fish. Taylor and Francis, London, Pages: 563

50:  Zelmer, D.A. and H.P. Arai, 1998. The contributions of host age and size to the aggregated distribution of parasites in yellow perch, Perca flavescens, from Garner Lake, Alberta, Canada. J. Parasitol., 84: 24-28.
CrossRef  |  Direct Link  |  

©  2021 Science Alert. All Rights Reserved