Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-29T05:59:14.709Z Has data issue: false hasContentIssue false
  • English
  • Français

Parasite biodiversity and its determinants in coastal marine teleost fishes of Brazil

Published online by Cambridge University Press:  13 May 2004

J. L. LUQUE ,
D. MOUILLOT  and
R. POULIN
J. L. LUQUE
Affiliation:
Departamento de Parasitologia Animal, Universidade Federal Rural do Rio de Janeiro, Caixa Postal 74.508, CEP 23851-970, Seropédica, RJ, Brazil
D. MOUILLOT
Affiliation:
UMR CNRS-UMII 5119 Ecosystèmes Lagunaires, Université Montpellier II, CC 093, 34095 Montpellier cedex 5, France
R. POULIN
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin, New Zealand
Get access Rights & Permissions [Opens in a new window]

Abstract

Recent studies of the forces behind the diversification of parasite assemblages have shed light on many aspects of parasite biodiversity. By using only parasite species richness as their measure of diversity, however, previous investigations have ignored the relatedness among parasite species and the taxonomic structure of the assemblages, which contain much information about their evolutionary origins. Here, we performed a comparative analysis across 50 species of fish from the coast of Brazil; we evaluated the effects of several host traits (body size, social behaviour, feeding habits, preference for benthic vs. pelagic habitats, depth range, and ability to enter brackish waters) on the diversity of their assemblages of metazoan parasites. As measures of diversity, we used parasite species richness, as well as the average taxonomic distinctness of the assemblage and its variance; the latter measures are based on the average taxonomic distance between any two parasite species in an assemblage. Unlike parasite species richness, taxonomic distinctness was unaffected by the number of host individuals examined per species. Fish body length proved to be the main predictor of parasite species richness, even when controlling for the confounding influences of host phylogeny and sampling effort, although it did not correlate with measures of parasite taxonomic distinctness. Predatory fish also had higher parasite species richness than planktivores, but this trend could not be confirmed using phylogenetically independent contrasts between host taxa. The main host feature associated with the taxonomic diversity of parasites was schooling behaviour, with schooling fish having more taxonomically diverse parasite assemblages than those of their non-schooling relatives. When focusing on endoparasite species only, both predatory feeding habits and a broad depth range were associated with the taxonomic distinctness of parasites. Our results suggest that certain host traits (i.e. body size) determine how many parasite species a host can accumulate over evolutionary time, whereas different host features influence the processes causing the taxonomic diversification of parasite assemblages.

Keywords

comparative analysishost phylogenytaxonomic distinctness
Type
Research Article
Information
Parasitology , Volume 128 , Issue 6 , June 2004 , pp. 671 - 682
Copyright
2004 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

AHO, J. M. & BUSH, A. O. ( 1993). Community richness in parasites of some freshwater fishes from North America. In Species Diversity in Ecological Communities: Historical and Geographical Perspectives (ed. Ricklefs, R. E. & Schluter, D.), pp. 185–193. University of Chicago Press, Chicago.
ALVES, D. R. & LUQUE, J. L. ( 2001). Community ecology of the metazoan parasites of the white croaker Micropogonias furnieri (Osteichthyes: Sciaenidae) from the coastal zone of the State of Rio de Janeiro, Brazil. Memórias do Instituto Oswaldo Cruz 96, 145–153.CrossRefGoogle Scholar
ALVES, D. R., LUQUE, J. L. & PARAGUASSÚ, A. R. ( 2002 a). Community Ecology of the Metazoan Parasites of Pink Cusk-eel, Genypterus brasiliensis (Osteichthyes: Ophidiidae), from the Coastal Zone of the State of Rio de Janeiro, Brazil. Memórias do Instituto Oswaldo Cruz 97, 683–689.Google Scholar
ALVES, D. R., LUQUE, J. L., PARAGUASSÚ, A. R., JORGE, D. S. & VIÑAS, R. A. ( 2002 b). Ecologia da comunidade de metazoários parasitos da abrótea Urophycis mystaceus (Osteichthyes: Phycidae) do litoral do Estado do Rio de Janeiro. Revista Brasileira de Zoociências 4, 19–30.Google Scholar
AMIN, O. M. ( 1985). Classification. In Biology of the Acanthocephala ( ed. Crompton, D. W. T. & Nickol, B. B. ), pp. 27–72. Cambridge University Press, Cambridge.
ANDERSON, R. C. ( 2000). Nematode Parasites of Vertebrates, 2nd Edn. CABI Publishing, Wallingford, UK.
APAKUPAKUL, K., SIDDALL, M. E. & BURRESON, E. M. ( 1999). Higher level relationships of leeches (Annelida: Clitellata: Euhirudinea) based on morphology and molecular gene sequences. Molecular Phylogenetics and Evolution 12, 350–359.CrossRefGoogle Scholar
ARNEBERG, P. ( 2002). Host population density and body mass as determinants of species richness in parasite communities: comparative analyses of directly transmitted nematodes of mammals. Ecography 25, 88–94.CrossRefGoogle Scholar
BELL, G. & BURT, A. ( 1991). The comparative biology of parasite species diversity: internal helminths of freshwater fish. Journal of Animal Ecology 60, 1047–1064.CrossRefGoogle Scholar
BEVERIDGE, I., CHILTON, N. B. & SPRATT, D. M. ( 2002). The occurrence of species flocks in the nematode genus Cloacina (Strongyloidea: Cloacininae), parasitic in the stomachs of kangaroos and wallabies. Australian Journal of Zoology 50, 597–620.CrossRefGoogle Scholar
BIZERRIL, C. R. S. F. & COSTA, P. A. S. ( 2001). Peixes Marinhos do Estado do Rio de Janeiro. Fundação Estudos do Mar, Rio de Janeiro, Brazil.
BOEGER, W. A. & KRITSKY, D. C. ( 1993). Phylogeny and a revised classification of the Monogenoidea Bychowsky, 1937 (Platyhelminthes). Systematic Parasitology 26, 1–32.CrossRefGoogle Scholar
BOXSHALL, G. A. & MONTÚ, M. ( 1997). Copepods parasitic on Brazilian coastal fishes: A handbook. Nauplius 5, 1–225.Google Scholar
BRAGA, A. C. ( 2001). O ambiente e a biodiversidade. In Peixes Marinhos do Estado do Rio de Janeiro ( ed. Bizerril, C. R. S. F. & Costa, P. A. S. ), pp. 13–32. Fundação de Estudos do Mar, Rio de Janeiro.
BROOKS, D. R. & McLENNAN, D. A. ( 1993). Parascript: Parasites and the Language of Evolution. Smithsonian Institution Press, Washington, DC.
BUNKLEY-WILLIAMS, L. & WILLIAMS Jr., E. H. ( 1998). Isopods associated with fishes: a synopsis and corrections. Journal of Parasitology 84, 893–896.CrossRefGoogle Scholar
BURT, A. ( 1989). Comparative methods using phylogenetically independent contrasts. Oxford Surveys in Evolutionary Biology 6, 33–53.Google Scholar
CARO, A., COMBES, C. & EUZET, L. ( 1997). What makes a fish a suitable host for Monogenea in the Mediterranean? Journal of Helminthology 71, 203–210.Google Scholar
CARPENTER, K. E., COLLETTE, B. B. & RUSSO, J. L. ( 1995). Unstable and stable classifications of scombroid fishes. Bulletin of Marine Science 56, 379–405.Google Scholar
CARVALHO FILHO, A. ( 1999). Peixes: Costa Brasileira. Melro Publisher, São Paulo, Brazil.
CEZAR, A. D. & LUQUE, J. L. ( 1999). Metazoan parasites of the Atlantic Spadefish, Chaetodipterus faber (Teleostei: Ephippidae) from the coastal zone of the State of Rio de Janeiro, Brazil. Journal of the Helmintological Society of Washington 66, 14–20.Google Scholar
CHAVES, N. D. & LUQUE, J. L. ( 1999). Ecology of metazoan parasites of Menticirrhus americanus (Osteichthyes: Sciaenidae), coast area from Rio de Janeiro State, Brazil. Revista Brasileira de Parasitologia Veterinária 8, 137–144.Google Scholar
CHEN, W.-J., BONILLO, C. & LECOINTRE, G. ( 2003). Repeatability of clades as a criterion of reliability: a case study for molecular phylogeny of Acanthomorpha (Teleostei) with larger number of taxa. Molecular Phylogenetics and Evolution 26, 262–288.CrossRefGoogle Scholar
CLARKE, K. R. & WARWICK, R. M. ( 1998). A taxonomic distinctness index and its statistical properties. Journal of Applied Ecology 35, 523–531.CrossRefGoogle Scholar
CLARKE, K. R. & WARWICK, R. M. ( 1999). The taxonomic distinctness measure of biodiversity: weighting of step lengths between hierarchical levels. Marine Ecology Progress Series 184, 21–29.CrossRefGoogle Scholar
CLARKE, K. R. & WARWICK, R. M. ( 2001). A further biodiversity index applicable to species lists: variation in taxonomic distinctness. Marine Ecology Progress Series 216, 265–278.CrossRefGoogle Scholar
CORDEIRO, A. S. & LUQUE, J. L. ( 2004). Community ecology of the metazoan parasites of moon fish Selene setapinnis (Osteichthyes: Carangidae) from the coastal zone of the State of Rio de Janeiro, Brazil. Brazilian Journal of Biology (in the Press).CrossRefGoogle Scholar
DOBSON, A. P. & ROBERTS, M. ( 1994). The population dynamics of parasitic helminth communities. Parasitology 109, S97–S108.CrossRefGoogle Scholar
DOGIEL, V. A., PETRUSHEVSKI, G. K. & POLYANSKI, Y. I. ( 1961). Parasitology of Fishes. Oliver & Boyd, Edinburgh.
FELSENSTEIN, J. ( 1985). Phylogenies and the comparative method. American Naturalist 125, 1–15.CrossRefGoogle Scholar
FIGUEIREDO, J. L. & MENEZES, N. A. ( 1978). Manual de Peixes Marinhos do Sudeste do Brasil II. Teleostei (1). Museu de Zoologia, Universidade de São Paulo, Brazil.
FIGUEIREDO, J. L. & MENEZES, N. A. ( 1980). Manual de Peixes Marinhos do Sudeste do Brasil III. Teleostei (2). Museu de Zoologia, Universidade de São Paulo, Brazil.
FIGUEIREDO, J. L. & MENEZES, N. A. ( 2000). Manual de Peixes Marinhos do Sudeste do Brasil VI. Teleostei (5). Museu de Zoologia, Universidade de São Paulo, Brazil.
FROESE, R. & PAULY, D. ( 2003). FishBase. World Wide Web electronic publication. www.fishbase.org, version 21, April 2003.
GARLAND, T. Jr., HARVEY, P. H. & IVES, A. R. ( 1992). Procedures for the analysis of comparative data using phylogenetically independent contrasts. Systematic Biology 41, 18–32.CrossRefGoogle Scholar
GIBSON, D. I., JONES, A. & BRAY, R. A. ( 2002). Keys to the Trematoda, vol. 1. CABI Publishing, Wallingford, UK.
GREGORY, R. D., KEYMER, A. E. & HARVEY, P. H. ( 1996). Helminth parasite richness among vertebrates. Biodiversity and Conservation 5, 985–997.CrossRefGoogle Scholar
HAIMOVICI, M., MARTINS, A. S. & VIEIRA, P. C. ( 1996). Distribuição e abundância de peixes teleósteos demersais sobre a plataforma continental do Sul do Brasil. Revista Brasileira de Biologia 56, 27–50.Google Scholar
HARVEY, P. H. & PAGEL, M. D. ( 1991). The Comparative Method in Evolutionary Biology. Oxford University Press, Oxford.
HOBERG, E. P. & KLASSEN, G. J. ( 2002). Revealing the faunal tapestry: co-evolution and historical biogeography of hosts and parasites in marine systems. Parasitology 124, S3–S22.CrossRefGoogle Scholar
KENNEDY, C. R. & BUSH, A. O. ( 1992). Species richness in helminth communities: the importance of multiple congeners. Parasitology 104, 189–197.CrossRefGoogle Scholar
KHALIL, L. F., JONES, A. & BRAY, R. A. ( 1994). Keys to the Cestode Parasites of Vertebrates. CABI International, Wallingford, UK.
KNOFF, M., LUQUE, J. L. & AMATO, J. F. R. ( 1997). Community ecology of the metazoan parasites of grey mullets, Mugil platanus (Osteichthyes: Mugilidae) from the littoral of the State of Rio de Janeiro, Brazil. Revista Brasileira de Biologia 57, 441–454.Google Scholar
KURIS, A. M., BLAUSTEIN, A. R. & ALIÓ, J. J. ( 1980). Hosts as islands. American Naturalist 116, 570–586.CrossRefGoogle Scholar
LUQUE, J. L. & CHAVES, N. D. ( 1999). Ecologia da comunidade de metazoários parasitos de Pomatomus saltator (Teleostei: Pomatomidae) do litoral do Estado do Rio de Janeiro. Revista Brasileira de Zoologia 16, 711–723.CrossRefGoogle Scholar
LUQUE, J. L. & ALVES, D. R. ( 2001). Ecologia das comunidades parasitárias do xaréu, Caranx hippos e do xerelete, Caranx latus (Osteichthyes: Carangidae) do litoral do Estado do Rio de Janeiro, Brasil. Revista Brasileira de Zoologia 18, 399–410.CrossRefGoogle Scholar
LUQUE, J. L., AMATO, J. F. R. & TAKEMOTO, R. M. ( 1996). Comparative analysis of the communities of metazoan parasites of Orthopristis ruber and Haemulon steindachneri (Osteichthyes: Haemulidae) from the southeastern Brazilian littoral: I. Structure and influence of the size and sex of hosts. Revista Brasileira de Biologia 56, 279–292.Google Scholar
LUQUE, J. L., SOARES, F. P. & ALVES, D. R. ( 2002). Community ecology of the metazoan parasites of Argentine goatfish Mullus argentineus (Osteichthyes: Mullidae) from the coastal zone of the State of Rio de Janeiro, Brazil. Revista Brasileira de Parasitologia Veterinária 11, 33–38.Google Scholar
LUQUE, J. L., SILVA, R. & ALVES, D. R. ( 2003). Community ecology of the metazoan parasites of banded croaker Paralonchurus brasiliensis (Osteichthyes: Sciaenidae) from the coastal zone of the State of Rio de Janeiro, Brazil. Acta Scientiarum (in the Press).Google Scholar
LUQUE, J. L., VIÑAS, R. A., PARAGUASSÚ, A. R. & ALVES, D. R. ( 2000). Metazoários parasitos das sardinhas Sardinella brasiliensis e Harengula clupeola (Osteichthyes: Clupeidae) do litoral do Estado do Rio de Janeiro, Brasil. Revista da Universidade Rural – Série Ciências da Vida 22, 71–76.Google Scholar
MacARTHUR, R. H. & WILSON, E. O. ( 1967). The Theory of Island Biogeography. Princeton University Press, Princeton.
MENEZES, N. A. & FIGUEIREDO, J. L. ( 1980). Manual de Peixes Marinhos do Sudeste de Brasil IV. Teleostei (3). Museu de Zoologia, Universidade de São Paulo, Brazil.
MENEZES, N. A. & FIGUEIREDO, J. L. ( 1985). Manual de Peixes Marinhos do Sudeste de Brasil V. Teleostei (4). Museu de Zoologia, Universidade de São Paulo, Brazil.
MIYA, M., TAKESHIMA, H., ENDO, H., ISHIGURO, N. B., INOUE, J. G., MUKAI, T., SATOH, T. P., YAMAGUCHI, M., KAWAGUCHI, A., MABUCHI, K., SHIRAI, S. M. & NISHIDA, M. ( 2003). Major patterns of higher teleostean phylogenies: a new perspective based on 100 complete mitochondrial DNA sequences. Molecular Phylogenetics and Evolution 26, 121–138.CrossRefGoogle Scholar
MORAN, M. D. ( 2003). Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100, 403–405.CrossRefGoogle Scholar
MORAND, S. ( 2000). Wormy world: comparative tests of theoretical hypotheses on parasite species richness. In Evolutionary Biology of Host–Parasite Relationships: Theory Meets Reality ( ed. Poulin, R., Morand, S. & Skorping, A.), pp. 63–79. Elsevier Science, Amsterdam.
MORAND, S., CRIBB, T. H., KULBICKI, M., CHAUVET, C., DUFOUR, V., FALIEX, E., GALZIN, R., LO, C., LO-YAT, A., PICHELIN, S. P., RIGBY, M. C. & SASAL, P. ( 2000). Determinants of endoparasite species richness of New Caledonian Chaetodontidae. Parasitology 121, 65–73.CrossRefGoogle Scholar
MORAND, S. & POULIN, R. ( 1998). Density, body mass and parasite species richness of terrestrial mammals. Evolutionary Ecology 12, 717–727.CrossRefGoogle Scholar
NELSON, J. S. ( 1994). Fishes of the World, 3rd Edn. Wiley, New York.
PAGE, R. D. M. ( 2003). Tangled Trees: Phylogeny, Cospeciation, and Coevolution. University of Chicago Press, Chicago.
PARAGUASSÚ, A. R., LUQUE, J. L. & ALVES, D. R. ( 2002). Community ecology of metazoan parasites of red porgy Pagrus pagrus (Osteichthyes: Sparidae) from the coastal zone of the State of Rio de Janeiro, Brazil. Acta Scientiarum 24, 461–467.Google Scholar
PATERSON, A. M. & GRAY, R. D. ( 1997). Host–parasite cospeciation, host switching, and missing the boat. In Host–Parasite Evolution: General Principles and Avian Models ( ed. Clayton, D. H. & Moore, J. ), pp. 236–250. Oxford University Press, Oxford.
POULIN, R. ( 1995). Phylogeny, ecology, and the richness of parasite communities in vertebrates. Ecological Monographs 65, 283–302.CrossRefGoogle Scholar
POULIN, R. ( 1997). Species richness of parasite assemblages: evolution and patterns. Annual Review of Ecology and Systematics 28, 341–358.CrossRefGoogle Scholar
POULIN, R. (1998). Evolutionary Ecology of Parasites: From Individuals to Communities. Chapman and Hall, London.
POULIN, R. & MORAND, S. ( 2000). The diversity of parasites. Quarterly Review of Biology 75, 277–293.CrossRefGoogle Scholar
PRICE, P. W. & CLANCY, K. M. ( 1983). Patterns in number of helminth parasite species in freshwater fishes. Journal of Parasitology 69, 449–454.CrossRefGoogle Scholar
PURVIS, A. & HECTOR, A. ( 2000). Getting the measure of biodiversity. Nature, London 405, 212–219.CrossRefGoogle Scholar
PURVIS, A. & RAMBAUT, A. ( 1994). Comparative Analysis by Independent Contrasts, CAIC version 2.0. Oxford University, Oxford.
RAIBAUT, A., COMBES, C. & BENOIT, F. ( 1998). Analysis of the parasitic copepod species richness among Mediterranean fish. Journal of Marine Systems 15, 185–206.CrossRefGoogle Scholar
RANTA, E. ( 1992). Gregariousness versus solitude: another look at parasite faunal richness in Canadian freshwater fishes. Oecologia 89, 150–152.CrossRefGoogle Scholar
REED, D. L., CARPENTER, K. E. & DEGRAVELLE, M. J. ( 2002). Molecular systematics of the jacks (Perciformes: Carangidae) based on mitochondrial cytochrome b sequences using parsimony, likelihood, and Bayesian approaches. Molecular Phylogenetics and Evolution 23, 513–524.CrossRefGoogle Scholar
ROBERTS, M. G., DOBSON, A. P., ARNEBERG, P., DE LEO, G. A., KRECEK, R. C., MANFREDI, M. T., LANFRANCHI, P. & ZAFFARONI, E. ( 2002). Parasite community ecology and biodiversity. In The Ecology of Wildlife Diseases ( ed. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. & Dobson, A. P. ), pp. 63–82. Oxford University Press, Oxford.
ROGERS, S. I., CLARKE, K. R. & REYNOLDS, J. D. ( 1999). The taxonomic distinctness of coastal bottom-dwelling fish communities of the North-east Atlantic. Journal of Animal Ecology 68, 769–782.CrossRefGoogle Scholar
ROHDE, K., HAYWARD, C. J. & HEAP, M. ( 1995). Aspects of the ecology of metazoan ectoparasites of marine fishes. International Journal for Parasitology 25, 945–970.CrossRefGoogle Scholar
SANTOS, C. P. & CARBONEL, C. A. A. ( 2000). The role of physical factors in the distribution of the monogenean fauna in the midwestern and southwestern Atlantic. In Metazoan Parasites in the Neotropics: A Systematic and Ecological Perspective ( ed. Salgado-Maldonado, G., Garcia-Aldrete, A. N. & Vidal-Martinez, V. M. ), pp. 61–75. Instituto de Biologia, UNAM, México.
SASAL, P. & MORAND, S. ( 1998). Comparative analysis: a tool for studying monogenean ecology and evolution. International Journal for Parasitology 28, 1637–1644.CrossRefGoogle Scholar
SASAL, P., MORAND, S. & GUÉGAN, J.-F. ( 1997). Determinants of parasite species richness in Mediterranean marine fish. Marine Ecology Progress Series 149, 61–71.CrossRefGoogle Scholar
SCHAD, G. A. ( 1963). Niche diversification in a parasite species flock. Nature, London 198, 404–406.CrossRefGoogle Scholar
SHIMATANI, K. ( 2001). On the measurement of species diversity incorporating species differences. Oikos 93, 135–147.CrossRefGoogle Scholar
SILVA, L. G. O., LUQUE, J. L., ALVES, D. R. & PARAGUASSÚ, A. R. ( 2000). Ecologia da comunidade parasitária do peixe-espada Trichiurus lepturus (Osteichthyes: Trichiuridae) do litoral do estado do Rio de Janeiro, Brasil. Revista Brasileira de Zoociências 2, 115–133.Google Scholar
TAKEMOTO, R. M., LUQUE, J. L. & AMATO, J. F. R. ( 1996). Comparative analysis of the metazoan parasite communities of leatherjackets, Oligoplites palometa, O. saurus and O. saliens (Osteichthyes: Carangidae) from Sepetiba Bay, Rio de Janeiro, Brazil. Revista Brasileira de Biologia 56, 639–650.Google Scholar
TAVARES, L. E. R. & LUQUE, J. L. ( 2004 a). Community ecology of the metazoan parasites of common snook Centropomus undecimalis (Osteichthyes: Centropomidae) from the coastal zone of the State of Rio de Janeiro, Brazil. Brazilian Journal of Biology (in the Press).Google Scholar
TAVARES, L. E. R. & LUQUE, J. L. ( 2004 b). Community ecology of the metazoan parasites of White catfish Netuma barba (Osteichthyes: Ariidae) from the coastal zone of the State of Rio de Janeiro, Brazil. Brazilian Journal of Biology 64, 1–8.Google Scholar
TAVARES, L. E. R., LUQUE, J. L. & BOTELHO NETO, S. L. ( 2001). Ecologia da comunidade parasitária do olho-de-cão, Priacanthus arenatus (Osteichthyes: Priacanthidae) do litoral do Estado do Rio de Janeiro, Brasil. Revista Brasileira de Zoociências 3, 45–59.Google Scholar
TAVARES, L. E. R., LUQUE, J. L. & BICUDO, A. ( 2004 a). Metazoan parasites of Brazilian menhaden Brevoortia aurea (Osteichthyes: Clupeidae) from the coastal zone of the State of Rio de Janeiro, Brazil. Brazilian Journal of Biology (in the Press).Google Scholar
TAVARES, L. E. R., LUQUE, J. L. & BICUDO, A. ( 2004 b). Community ecology of the metazoan parasites of anchovy Anchoa tricolor (Osteichthyes: Engraulidae) from the coastal zone of the state of Rio de Janeiro, Brazil. Brazilian Journal of Biology (in the Press).Google Scholar
WALTHER, B. A., COTGREAVE, P., PRICE, R. D., GREGORY, R. D. & CLAYTON, D. H. ( 1995). Sampling effort and parasite species richness. Parasitology Today 11, 306–310.CrossRefGoogle Scholar
WARWICK, R. M. & CLARKE, K. R. ( 2001). Practical measures of marine biodiversity based on relatedness of species. Oceanography and Marine Biology Annual Review 39, 207–231.Google Scholar
YAMAGUTI, S. ( 1963). Parasitic Copepoda and Branchiura of Fishes. Interscience Publishers, New York.