Biodiversity Journal , 2019, 10 (2): 151–158 https://doi.org/10.31396/Biodiv.Jour.2019.10.2.151.158

Digenean parasites in two congeneric sparid and of commercial importance, erythrinus (Linnaeus, 1758) and Pagellus acarne (Risso, 1827), from the western Mediter - ranean coast of Algeria

Sihem Abid-Kachour, Omar Rouane Hacene, Salim Mouffok & Mohammed Bouderbala

University of Oran 1 Ahmed Ben Bella, Laboratoire Réseau de Surveillance Environnementale (LRSE), Department of Bio - logy, BP 1524 El M’naouer, 31000 Oran, Algeria *Corresponding Author, email: [email protected]

ABSTRACT The investigation into the digenean fauna of two congeneric sparid fishes ( Spari - dae), Pagellus erythrinus (Linnaeus, 1758) and Pagellus acarne (Risso, 1827), was carried out in the Algerian coasts (Western Mediterranean). These fishes of commercial importance represent an important biological resource for the human population along the Mediterranean coasts. However, the data on their digenean parasites in Algeria are incomplete and the aim of this study is to provide new data on the diversity and species composition of digeneans from these hosts. A total of 240 fishs (120 of each species) were collected from Oran (North- western Algeria) during 12 months between September 2016 and August 2017. Eleven species of digeneans were found in the two hosts: (i) Lepocreadium pegorchis (Lepocreadiidae); Lepocreadium album (Lepocreadiidae); Holorchis pychnoporus (Lepocreadiidae); Holorchis spp (Lepocreadiidae); Hemiurus comminus (Hemiuridae); Hemiurus luehei (Hemiuridae); Lepidauchen stenostoma (Acanthocolpidae) and Pachycreadium carnosum (Opecoelidae); Macvicaria crassigula (Opecoelidae) in Pagellus erythrinus ; (ii) Lepocreadium pegorchis (Lepocreadiidae); Macvicaria crassigula (Opecoelidae); Zoogonus spp () and Hemiurus communis (Hemiuridae) in Pagellus acarne . In the evaluation of the dynamics of the epidemiological index of the community of digenean parasites, two species of fish show seasonal variations. Furthermore, higher prevalence of infestation were registered during the summer season for the Opecaelidae family in the two hosts.

KEY WORDS ; P agellus; congeneric; Digenean; epidemiological index; Algerian coasts. Received 26.02.2019; accepted 28.05.2019; published online 30.06.2019

INTRODUCTION Pagellus acarne (Risso, 1827). The study area was the west coast of Algeria. This approach is an at - Through this study we have identified and com - tempt to highlight the influence of biotic and abi - pared the digenean endoparasites of two con - otic factors in structuring the community of generic sympatric sparid fishes (Perciformes digenean parasites. Indeed, the niches of parasite Sparidae), which are also of great commercial im - species are strongly influenced by the environment, portance, Pagellus erythrinus (Linnaeus, 1758) and particularly the quality of the food resources and 152 SIHEM ABID -K ACHOUR ET ALII

their abundance (Price & Clancy, 1983; Bates & ecology (Brooks & Hoberg, 2000; Khan & Chan - Kennedy, 1990; Holmes, 1990; Holmes & Bartoli, dra, 2006). 1993). Some authors (Holmes, 1973; Pianka, 1974; Rohde, 1979) suggest that interspecific and in - traspecific competition between sympatric host MATERIAL AND METHODS species favor niche restriction for the parasite. A morpho-anatomical study has been carried out to A total of 240 fishes (120 of each species) from put the digeneans collected from each host in their Oran’s coasts, north western Algeria (Fig. 1) dur - taxonomic context and a quantitative and qualita - ing the 12 months between September 2016 and tive study was carried out in order to compare the 2017, have been sampled. The digeneans found in community of the digeneans in both congeneric digestive tract of Pagellus erythrinus and P. sparid fishes. The digenean fauna of sparid fish has acarne have been set into alcohol of 70%, put for been the subject of various studies in the Mediter - some minutes in Borax Carmine solution ranean Sea, among them we will cite the works of: (Grenacher) and after in chlorhydric acid, dehy - Bartoli, 1987a, 1987b; Bartoli & Gibson, 1989; drated in successive baths of alcohol of 70, 85, Bartoli et al., 1989a, 1989b; 2005; Saad-Fares & 95%, then in two baths of absolute ethanol 100%. Maillard, 1990; Bartoli & Bray, 1996; Sasal et al., They have been cleared in Eugenol and mounted 1999; Kostadinova & Gibson, 2009; Sanchez et al., in Canada balsam. All the parasitic digenans har - 2013, 2014. Moreover, we can also mention recent vested in this study were identified with taxo - works undertaken on the parasitofauna of sparidae nomic keys (Yamaguti, 1934 ; Gibson et al., 2002). fishes in the Mediterranean Sea, including the work The different ecological terms used for digenean of Merzoug et al., 2012; Abid Kachour et al., 2013; communities (prevalence, mean intensity and Antar & Gargouri Ben Abdallah, 2013; Abid Ka - abundance) were calculated as described by Bush chour, 2014; Antar et al., 2015; Bellal et al., 2016. et al. (1997). However, this contribution is still incomplete, Terms used as “dominant species” (prevalence> knowing that sparidae are considered as ideal host 50%), “satellite species” or common (prevalence fish for the larval and adult stages. The biodiverty 10%-50%) and “rare species” (prevalence <10%) of the community of the digenean parasites within were defined according to Valtonen et al. (1997). each host will allow us to highlight their trophic Statistical analysis was performed using the STA -

Figure 1. Study area: Oran’s coasts, north western Algeria. Digenean parasites in two sparid fishes congeneric and of commercial importance from Algeria 153

TISTICA software (Statsoft statistica version geneans belonging to different families. However, 12.5.192.7). the composition of the digenean community does not evolve in the same direction in two host fishes and show differences with the seasons. A total of 11 RESULTS digenean species belonging to 4 families have been identified (Table 1). The two host fishes of this study have in their In P. erythrinus , the family Opecoelidae was digestive system a large and variable number of di - dominant, largely represented by the species Macvi -

Table. 1. Parasitological indices for digeneans from two Sparid fishes off the western Mediterranean coast of Algeria. Sites: A, stomach; B, pyloric caeca; C, duodenum; D, mid-intestine; E, posterior intestine; F, rectum. 154 SIHEM ABID -K ACHOUR ET ALII

caria crassigula (51.66%) occupying a large part This variation concerns, in particular, Macvi - of the intestine, followed by Pachycreadium garia crassigula , in which we observed a preva - carnosum found in the duodenum and mid-intestine lence of 26.66% in winter, a clear progression from (25%). The family Lepocreadiidae is represented by spring, reaching its maximum in summer (83.33%) Lepocreadium pegorchis (41.66%), L. album while a decrease is recorded during the autumn (33.33%), found at the duodenum and mid-intestine (Fig. 2). Pachycredium carnosum also showed a levels, Holorchis pycnoporus (7.5 %), and H. sp. significant rate of for the summer period (3.33%) both collected in the duodenum, mid-intes - of about 66.66%. The family of Lepocreadiidae is tine and rectum. Hemiurus communis (8.33%) and especially represented by Lepocreadium genus, also H. luehei (3.33%), are species belonging to the fam - frequent during the summer. We did not find any ily Hemiuridae. They are rare and were all found at significant seasonal change for other digenean par - the stomach level. The family Acanthocolpidae was asites (Fig. 2). We recorded variations of digenean marked by the presence of Lepidauchen stenostoma fauna according to the change of seasons also in P. in the duodenum with a prevalence of 3.33%. For acarne (Fig. 3). Macvicaria crassigula is prevalent P. acarne , we recorded the presence on the intes - with 3.33% in winter, reaching 73.33% in summer tinal level of the species Lepocreadium pegorchis period. Lepocreadium pegorchis (70%) and (Lepocreadiidae) with a prevalence of 25 %. Macvi - Zoogonus sp. (50%) are prevalent too during the caria crassigula (Opeceolidae) was recorded in the summer, while no change of the prevalence accord - duodenal part (29%) and mid internal (16%), ing to the seasons was observed for Hemiurus com - Zoogonus sp. (Zoogonidae) on the anus level munis . (17.5%), and Hemiurus communis (Hemiuridae) was found in the stomach (3.33%). Concerning the ecological aspect, we noted that DISCUSSION the community of digenean parasites of two host fishes ( P. erythrinus and P. acarne ) varies according Through these results, we found that the struc - to the seasons. The strongest values of prevalence ture of the digenean community was not com - of some species were observed in summer. The his - pletely identical and homogeneous in both the host togram of seasonal variations for P. erythrinus (Fig. fishes. These two sparidae belong to the same 2) shows that the prevalence of parasitic species genus. They are very close phylogenetically and varies with a minimum rate of 3.33 in winter up to sharing the same biotope and food habits (Bauchot at 83.33% in summer. et al., 1990) can determine the infestation of the

Figure 2. Comparative study of the variances of parasitic spe - Figure 3. Comparative study of the variances of parasitic spe - cies according to the seasons in Pagellus erythrinus . Data with cies according to the seasons in Pagellus acarne . Data with different letters expressed significant differences between sea - different letters expressed significant differences between sons (p <0.05) for each species of parasitic digenean. seasons (p <0.05) for each species of parasitic digenean. Digenean parasites in two sparid fishes congeneric and of commercial importance from Algeria 155

larval stages of the digenean species by trophic dae) and Lepocredium pegorchis (Lepocreadiidae), way (Morand, 1996). Indeed, these two congeneric hosted by both Pagellus , present this specificity in sparidae nourish mainly on shellfish and molluscs, relation to the seasons. Indeed, if one refers to the generally the first and second intermediary hosts work already done on the fluctuations of the para - of the majority of the digenean species. Despite all site abundance of different taxa, especially the di - these convergences, the digenean community in P. geneans, according to the changes of seasons, show erythrinus was both important and richer com - that the various factors, like the increase of the pared to that of P. acarne . This difference may be temperature or the salinity can alter the specificity the result of trophic competition between con - of parasites (Williams et al., 1994; Sasal et al., geners. Indeed, some studies suggest that compe - 1997). However, in certain digenean parasites the tition for a resource such as food may be more increase of the temperature during the summer fa - intense between closely related host species vors their pululation (De Kinkelin, 1971). Re - (Harmelin-Vivien et al., 1989; Sala & Ballesteros, cently, studies have confirmed the effect of light 1997; Azzurro et al., 2007). However, we found and temperature on their determining role in the that some digenean species such as Macvicaria emission of digeneans (Desclaux, 2003). With re - crassigula (Opeceolidae) and Lepocreadium pe - gard to parasites that show no significant variation gorchi s (Lepocreadiidae) were recorded in both with the seasons, as is the case for Hemiurus com - host fishes in the same microbiotope with a high munis (Hemiuridae), a generalist species, some prevalence, giving them the rank of dominant and studies are concerned with temperature, an envi - generalist parasite (Sasal et al., 1999). These ronmental parameter involved in the inhibition or species have already been reported several times reduction of the emission of certain cercariae in the in sparidae, notably in P. erythrinus in the Mediter - first intermediate host gastropods, thus disturbing ranean Sea (Bartoli et al., 2005; Antar & Gargouri, the evolutionary cycle of a given species (Prévot, 2013). This specificity is qualified strictly from a 1974, Williams & Jones, 1994). In addition, the coevolutive adaptation (Brooks & Hoberg, 2000). trophic behavior of the two host fishes ( P. erythri - In addition, many authors have hypothesized that nus and P. acarne ) changes with the seasons (Bau - the parasite's preferential microbiotope is the re - chot et al., 1990; Fanelli et al., 2011). sult of the influence of immune host responses (Holmes, 1990; Holmes & Bartoli, 1993). Others support the theory of the influence of the trophic CONCLUSIONS network (Bartoli et al., 2005). Various studies also show that parasite populations will fluctuate We notice in this study that the composition of within their hosts depending on the surrounding the community of digenean parasites of these two environmental conditions (Khan & Chandra, sympatric and congeneric host species does not 2006). We also found that the rate of infestation systematically exhibit the same digenean structure was lower at the stomach level, compared to the in terms of quantity and quality and does not re - intestine. These results concur with the hypothesis spond with the same variations in prevalence in proposed by several authors in which they suggest according to the seasons. Except for some domi - that the stomach remains a hostile environment be - nant and common species as is the case of Macvi - cause of its chemical and physical contribution caria crassigula and Lepocreadium pegorchis , the (Holmes, 1990). results were similar in both host fishes. Indeed, Concerning the variations of parasite preva - these results corroborate the work of some authors lence according to the seasons, and after use of the such as Poulin (2002) and Sasal & Thomas (2005) statistical test, the impact of the temperature is not and who suggest that host fish sharing the same similar for all the digenean species resumed in the biotope could develop a parasite exchange be - two host fishes. However, some digeneans show a tween them. However, divergences in the results significant difference in their prevalence with a of digenean species in both sparidae, as mentioned consequent increase during the summer period, by some authors such as Bartoli (1987b) and Bar - these results coincide with those obtained by De - toli et al. (2005), are related to the food web and sclaux (2003). Macvicaria crassicula (Opecoeli - partitioning available to both host fishes. More - 156 SIHEM ABID -K ACHOUR ET ALII

over, our results respond mainly to the competition Bartoli P. & Bray R.A., 1996. Description of three theory that exists between parasitic species: when species of Holorchis Stossich, 1901 (: Lep - one species colonizes a host, it prevents the even - ocreadiidae) from marine fishes of Corsica. System - tual installation of the other (Sasal & Thomas, atic Parasitology, 35: 133–143. 2005). Bartoli P. & Gibson D.I., 1989. Wardula sarguicola n. sp. (Digenea, Mesometridae), a rectal parasite of Diplo - dus sargus (Teleostei, Sparidae) in western Mediter - ranean. Annales de Parasitologie Humaine et REFERENCES Comparée, 64: 20–29. Bartoli P., Bray R.A. & Gibson D.I., 1989a. The Opecoel - Abid-Kachour S., Mouffok S. & Boutiba Z., 2013. De- idae (Digena) of sparid fishes of the western Mediter - scription of a new species of S phincteristomum from ranean. II. Pycnadenoides Yamaguti, 1938, Sparid Fishes of the algerian Coast (Western Mediter- Pseudopycnadena Saad Fares & Maillard, 1986. Sys - ranean). Journal of Environmental Protection, 4: tematic Parasitology, 13: 35–51. 1129–1136. https://doi.org/10.4236/jep.2013.410129 Bartoli P., Bray R.A. & Gibson D.I., 1989b. The Opecol - Abid-Kachour S., 2014. Contribution à l’étude despara- idae (Digenea) of sparid fishes of the western sites Digènes chez trois Poissons téléostéens Merlu Mediterranean. III. Systematic Parasitology, 13: 167– (Merlucciu s merluccius ), Pageot ( Pagellus erythri - 192. nus ) et Chinchard ( Trachurus trachurus ) de la côte Bartoli P., Gibson D.I. & Bray R.A., 2005. Digenean oranaise. Thèse Doctorat, Université d’Oran Es- species diversity in teleost fish from a nature reserve Senia, Algeria, 190 pp. of Corsica, France (Western Mediterranean), and a Antar R. & Gargouri Ben Abdallah L., 2013. Trematodes comparison with other Mediterranean regions. Jour - in fishes of the genus D iplodus (Teleostei, Sparidae) nal of Natural History, 39: 47–70. https://doi.org/10. from Bizerte Lagoon (Northern coast of Tunisia). Eu- 1080/00222930310001613557 ropean association of Fish Pathologists, 33: 44–52. Bates R.M. & Kennedy C.R., 1990. Interactions between Antar R., Georgieva S., Gargouri L. & Kostadinova A., the Acanthocephala Pomphorhynchus laevis and 2015. Molecular evidence for the existence of species Acanthocephalus anguillae in rainbow trout: testing complexes within Macvicaria Gibson & Bray, 1982 an exclusion hypothesis. Parasitology, 100: 435–444. (Digenea: Opecoelidae) in the western Mediter- Bellal A., Brahim Tazi NA., Hadjou Z. & Zitouni ranean, with descriptions of two new species. Sys - tematic Parasitology, 91: 211–229. https://doi.org/10. Boutiba, 2016. First records of digenean trematodes 1007/s11230-015-9577-9 of two fishes (Teleostei, Sparidae) from the West al - Azzurro E., Fanelli E., Mostarda E. & Catra M., 2007. gerian coast and comparative study with Tunisian Resource partitioning among early colonizing coast (Mediterranean Sea). Biodiversity Journal, 7: Siganus luridus and native herbivorous fish in the 233–240. Mediterranean: an integrated study based on gut-con- Bray R.A. & Gibson. D.I., 1989. The Lepocreadiidae tent analysis and stable isotope signatures. Journal of (Digenea) of fishes from the north-east Atlantic: re - the Marine Biological Association of the United view of the genus Neolepidapedon Manter 1954, with Kingdom, 7: 991–998. https://doi.org/10.1017/ a description of N. smithi n. sp. Systematic Parasitol - S0025315407056342 ogy, 131: 11–23. Bartoli P. 1987a. Les Trématodes digénétiques parasites- Bray R.A. & Gibson D.I., 1998. Further observations on des poissons Sparidés de la Reserve Naturelle de the Digenea (Platyhelminthes) of deep-sea fishes in Scandola. Travaux Scientifiques du Parc Naturel Ré- the northeastern Atlantic: Fellodistomidae and gional et des Réserves Naturelles de Corse, 10: 1– Zoogonidae. Acta Parasitologica, 43: 194–199. 158. Bray R.A. & Bartoli P., 1996. A redescription of Lepi - Bartoli P. 1987b. Caractères adaptatifs originaux des dauchen stenostoma Nicoll, 1913 (Digenea), and a Digènes intestinaux de S arpa salpa (Teleostei, Spari- reassessment of the status of the genus Lepidauchen dae) et leur interprétation en termes d’évolution. An- Nicoll, 1913. Systematic Parasitology, 33: 167–176. nales de Parasitologie Humaine et Comparée, 62: Bauchot M.L., Hureau J.C. & Quero J.C., 1990. Spari - 542–576. dae. Check-list of the fishes of the eastern tropical Bartoli P., Gibson D.I. & Bray R.A., 2005. Digenean Atlantic (CLOFETA). JNICT, Lisbon; SEI, Paris; and species diversity in teleost fish from a nature reserve UNESCO, Paris. Vol. 2: 790–812. off Corsica, France (Western Mediterranean), and a Brooks D.R. & Hoberg E.P., 2000. Triage for the bios - comparison with other Mediterranean regions. Jour- phere: the need and rationale for taxonomic invento - nal of Natural History, 39: 47–70. https://doi.org/10. ries and phylogenetic studies of parasites. 1080/00222930310001613557 Comparative Parasitology, 67: 1–25. Digenean parasites in two sparid fishes congeneric and of commercial importance from Algeria 157

Bush A.O., Lafferty K.D., Lotz J.M. & Shostak A.W., Morand S., 1996. Biodiversity of parasites in relation 1997. Parasitology meets ecology on its own terms: with their life cycle. The Genesis and Maitenance of Margolis et al. Revisited. Journal of Parasitology, 83: Biological Diversity, Oxford University Press, 243– 575–583. 260. De Kinkelin P., 1971. Précis de pathologie des Poissons, Pianka E.R., 1974. Evolutionary Ecology. Harper and Institut national de la recherche agronomique, Mas - Row, New York, 356 pp. son, 487 pp. Poulin R., 1992. Determinants of host specificity in par - Descalaux C., 2003. Interactions hotes-parasites: diver - asites of freshwater fishes. International Journal for sité, mécanismes d’infestation et impact des tréma - Parasitology, 22: 753–758. todes digènes sur les coques Cerastoderma edule Poulin R., 2002. The evolution of monogenean diversity. (Mollusques Bivalve) en milieu lagunaire. Thèse de International Journal of Parasitology, 37: 245–245. Doctorat Université de Bordeaux, 247 pp. Prévot G., 1974. Recherches sur le cycle biologique et Fanelli E., Badalamenti F., D’Anna, G., Pipitone C., Rig - l’écologie de quelques tréma- todes nouveaux para - inella E. & Azzurro E., 2011. Food partitioning and sites de Larus argentatus michaellis Naumann dans diet temporal variation in two coexisting sparids, le midi de la France. Thèse Sciences, Aix-Marseille, Pagellus erythrinus and Pagellus acarne . Journal of 319 pp. Fish Biology, 78: 869–900. https://doi.org/10.1111/j. Price P.W. & Clancy K.M., 1983. Patterns in number of 1095-8649.2011.02915.x. helminth parasite species in freshwater fishes. Journal Gibson D.I., Jones.A., & Bray R.A, 2002. Keys to the of Parasitology, 69: 449–454. . Vol. 1. CABI Publishing, London, 544 Rohde k., 1979. A critical evaluation of intrinsic andex - pp. trinsic factors responsible for niche restriction inpar - Harmelin-Vivien M.L., Kaim-Malka R.A., Ledoyer M. asites. The American Naturalist, 114: 648–671. & Jacob-Abraham S.S., 1989. Food partitioning Saad-Fares A. & Maillard C., 1990. Digenetic Trema - among scorpaenid fishes in Mediterranean seagrass todes of Lebanese coast fishes : the species complexes beds. Journal of Fish Biology, 34: 715–734. Lepocreadium album (Stossich, 1890) and Lepocre - Holmes J.C., 1973. Site selection by parasitic helminths: adium pegorchis (Stossich, 1900) Lepocreadiidae. interspecic interactions, site segregation, and their Systematic Parasitologie, 17: 87–95. importance to the development of helminth commu - Sánchez-García N., Raga J.A. & Montero F.E., 2014. nities. Canadian Journal of Zoology, 51: 333–347. Risk assessment for parasites in cultures of Diplodus Holmes J.C., 1990. Competition, contacts and other fac - puntazzo (Sparidae) in the Western Mediterranean: tors restricting niches of parasitic Helminthes. An - prospects of cross infection with Sparus aurata . Vet - nales de Parasitologie Humaine et Comparée, 65: erinary Parasitology, 204: 120–133. https://doi.org/ 69–72. 10.1016/j.vetpar.2014.05.013. Holmes J.C. & Bartoli P., 1993. Spatio-temporalstruc - Sánchez-García N., Ahuir-Baraja A., Raga J.A. & Mon - ture of the communities of helminths in the digestive tero F.E., 2013. Morphometric, molecular andecolog - tract of Sciaena umbra L. 1758 (Teleostei). Parasitol - ical analyses of the parasites of the sharpsnout sea ogy, 106: 519–525. bream Diplodus puntazzo Cetti (Sparidae) from the Khan R.A. & Chandra C.V., 2006. Influence of climatic Spanish Mediterranean: implications for aquaculture. changes on the parasites of Atlantic cod Gadus Journal of Helminthology, 89: 217–231. https://doi. morhua off coastal Labrador, Canada. Journal of org/10.1017/S0022149X13000813 Helminthology, 80: 193–197. https://doi.org/10.10 Sasal P. & Thomas F., 2005. Parasite induced changes in 79/JOH2006352 host behavior and morphology. In: K. Rohde (Ed.), Kostadinova A. & Gibson D.I., 2009. New records of Marine Parasitology, pp. 259–264. CSIRO Publish - rarederogenids (Digenea: Hemiuroidea) from ing, Collingwood, 565 pp. Mediterranean sparids, including the description of a Sasal P., Morand S. & Guégan J.F., 1997. Parasite species new species of Magnibursatus Naidenova, 1969 and richness for fish of the Mediterranean Sea. Marine redescription of Derogenes adriaticus Nikolaeva, Ecology Progress Series, 149: 61–71. 1966. Systematic Parasitology, 74: 187–198. Sasal P., Niquil N. & Bartoli P., 1999. Community struc - https://doi.org/10.1007/s11230-009-9214-6. ture of digenean parasites of sparid and labrid fishes Marzoug D., Boutiba Z., Kostadinova A. & Pérezdel- of the Mediterranean Sea: a new approach. Parasitol - Olmo A., 2012. Effects of fishing on parasitism in a ogy, 119: 635–648. sparid fish: contrasts between two areas of the West - Sala E. & Ballesteros E., 1997. Partitioning of space and ern Mediterranean. Parasitology International, 61: food resources by three fish genus Diplodus (Spari - 414–420. https://doi.org/10.1016/j.parint.2012.02. dae) in a Mediterranean rocky infralittoral ecosystem. 002 Marine Ecology Progress Series, 152: 273–283. 158 SIHEM ABID -K ACHOUR ET ALII

Valtonen E.T., Holmes J.C. & Koskivaara M., 1997. Eu - Williams H. & Jones A., 1994. Parasitic Worms of Fish. trophication, pollution and fragmentation: effects on Taylor & Francis, 593 pp. parasite communities in roach ( Rutilus rutilus ) and Yamaguti S., 1934 Studies on the helminth fauna of perch ( Perca fluviatilis ) in four lakes in the Central Japan. Part 2. Trematodes of fishes. Japanese Jour - Finland. Canadian Journal of Fisheries and Aquatic nal of Applied Entomology and Zoology, 6: 159– Sciences, 54: 572–585. 182.