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An experimental field test of susceptibility to ectoparasitic gnathiid isopods among Caribbean reef fishes

Published online by Cambridge University Press:  18 March 2013

A. M. COILE  and
P. C. SIKKEL
A. M. COILE
Affiliation:
Department of Biological Sciences, Arkansas State University, P.O. Box 599, State University, AR 72467-3082, USA
P. C. SIKKEL*
Affiliation:
Department of Biological Sciences, Arkansas State University, P.O. Box 599, State University, AR 72467-3082, USA
*
*Corresponding author: Department of Biological Sciences, Arkansas State University, P.O. Box 599, State University, AR 72467-3082, USA. Tel: +1 270 293-5489. Fax +1 870 972 2638. E-mail: [email protected]
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Summary

Susceptibility to infestation by a gnathiid isopod (Gnathia marleyi: Crustacea: Isopoda) was examined among 16 species from 9 families and 3 orders of common Caribbean reef fishes off St. John, United States Virgin Islands. Fish were placed in cages during times of peak gnathiid activity. Individuals from most (n=14) species were compared against a single species (French Grunt, Haemulon flavolineatum) that served as a standard and effectively controlled for the effects of habitat and variation in gnathiid abundance on exposure to and the likelihood and intensity of host infestation by gnathiids. All species were susceptible to infestation by gnathiids, with individual hosts harbouring up to 368 gnathiids. However, there was significant variation in levels of infestation among the 14 comparison species. Controlling for body size, nocturnal species from the families Haemulidae and Lutjanidae had the highest gnathiid infestation. Our finding that haemulids and lutjanids are particularly susceptible has important implications for the role of gnathiids in Caribbean reef food webs, given the role members of these families play in trophic connectivity between reefs and associated habitats. To our knowledge this is the first manipulative field study to examine variation among potential hosts in susceptibility to an ectoparasite in any terrestrial or aquatic system and is the greatest number of teleost hosts documented for any gnathiid species.

Keywords

host preferencehost susceptibilityectoparasitegnathiid isopodGnathia marleyicoral reef fishesHaemulidaeLutjanidae
Type
Research Article
Information
Parasitology , Volume 140 , Issue 7 , June 2013 , pp. 888 - 896
Copyright
Copyright © Cambridge University Press 2013 

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References

REFERENCES

Adlard, R. D. and Lester, R. J. G. (1994). Dynamics of the interaction between the parasitic isopod Anilocra pomacentri, and the coral reef fish, Chromis nitida. Parasitology 109, 311–324.CrossRefGoogle ScholarPubMed
Allen, G. R. (1991). Damselfishes of the World. Mergus, Melle, Germany.Google Scholar
Appledoorn, R. S., Aguilar-Perera, A., Bouwmeester, B. L. K., Dennis, G. D., Hill, R. L., Merten, W., Recksiek, C. W. and Williams, S. J. (2009). Movement of fishes (Grunts: Haemulidae) across the coral reef seascape: a review of scales, patterns and processes. Caribbean Journal of Science 45, 304–316.CrossRefGoogle Scholar
Arnal, C., Côté, I. M. and Morand, S. (2001). Why clean and be cleaned? The importance of client ectoparasites and mucus in a marine cleaning symbiosis. Behavioral Ecology and Sociobiology 51, 1–7. doi: 10.1007/s002650100407.Google Scholar
Bandilla, M., Hakalahti, T., Hudson, P. J. and Valtonen, E. T. (2005). Aggregation of Argulus coregoni (Crustacea: Branchiura) on rainbow trout (Oncorhynchus mykiss): a consequence of host susceptibility or exposure? Parasitology 130, 169–176.CrossRefGoogle ScholarPubMed
Bize, P., Jeanneret, C., Klophenstein, A. and Roulin, A. (2008). What makes a host profitable? Parasites balance host nutritive resources against immunity. American Naturalist 171, 107–118.CrossRefGoogle ScholarPubMed
Bunkley-Williams, L. and Williams, E. (1998). Isopods associated with fishes: a synopsis and corrections. Journal of Parasitology 84, 893–896.CrossRefGoogle ScholarPubMed
Christe, P., Giorgi, M. S., Vogel, P. and Arlettaz, R. (2003). Differential species-specific ectoparasitic mite intensities in two intimately coexisting sibling bat species: resource mediated host attractiveness or parasite specialization? Journal of Animal Ecology 72, 866–872.CrossRefGoogle Scholar
Clark, K. L., Oliver, J. H., Grego, J. M., James, A. M., Durden, L. A. and Banks, C. W. (2001). Host associations of ticks parasitizing rodents at Borrelia burgdorferi enzootic sites in South Carolina. Journal of Parasitology 87, 1379–1386.CrossRefGoogle ScholarPubMed
Clark, R. D., Pittman, S., Caldow, C., Christensen, J., Roque, B., Appeldoorn, R. S. and Monaco, M. E. (2009). Nocturnal fish movement and trophic flow across habitat boundaries in a coral reef ecosystem (SW Puerto Rico). Caribbean Journal of Science 45, 282–303.CrossRefGoogle Scholar
Combes, C. (1997). Fitness of parasites: pathology and selection. International Journal for Parasitology 27, 1–10.CrossRefGoogle ScholarPubMed
Côté, I. M. (2000). Evolution and ecology of cleaning symbioses in the sea. Annual Review of Marine Science 38, 311–355.Google Scholar
Côté, I. M. and Molloy, P. P. (2003). Temporal variation in cleanerfish and client behavior: does it reflect ectoparasite availability? Ethology 109, 487–499.CrossRefGoogle Scholar
Davies, A. J., Smit, N. J., Seddon, A. M. and Wertheim, D. (2004). Haemogregarina bigema (Protozoa: Apicomplexa: Adeleorina)—past, present and future. Folia Parasitologica 51, 99–108.CrossRefGoogle ScholarPubMed
Dobson, A., Lafferty, K. D., Kuris, A. M., Hechinger, R. F. and Jetz, W. (2008). Homage to Linnaeus: how many parasites? How many hosts? Proceedings of the National Academy of Sciences USA 105, 11482–11489.CrossRefGoogle ScholarPubMed
Edmunds, P. J. (2000). Patterns in the distribution of juvenile corals and coral reef community structure in St. John, US Virgin Islands. Marine Ecology Progress Series 202, 113–124.CrossRefGoogle Scholar
Edmunds, P. J. (2002). Long-term dynamics of coral reefs in St. John, US Virgin Islands. Coral Reefs 21, 357–367.CrossRefGoogle Scholar
Farquharson, C., Smit, N. J. and Sikkel, P. C. (2012). Gnathia marleyi sp. Nov. (Crustacean, Isopoda, Gnathiidae) from the Eastern Caribbean. Zootaxa 3381, 47–61.CrossRefGoogle Scholar
Fast, M. D., Ross, N. W., Mustafa, A., Simes, D. E., Johnson, G. A. and Burka, J. F. (2002). Susceptibility of rainbow trout Oncorhynchus mykiss, Atlantic salmon Salmo salar and coho salmon Oncorhynchus kisutch to experimental infection with sea lice Lepeophtheirus salmonis. Diseases of Aquatic Organisms 52, 57–68.CrossRefGoogle ScholarPubMed
Ferreira, M. L., Smit, N. J., Grutter, A. S. and Davies, A. J. (2009). A new species of gnathiid (Crustacea: Isopoda) parasitizing teleosts from Lizard Island, Great Barrier Reef, Australia. Journal of Parasitology 95, 1066–1075.CrossRefGoogle ScholarPubMed
Friedlander, A. and Monaco, M. (2007). Acoustic Tracking of Reef Fishes to Elucidate Habitat Utilization Patterns and Residence Times Inside and Outside Marine Protected Areas in the US Virgin Islands. Interim Project Report. NOAA/NOS/NCCOS/CCMA – Biogeography Branch. p. 43.Google Scholar
Friend, W. G., Choy, C. H. T. and Cartwright, E. (1965). The effect of nutrient intake on the development and the egg production of Rhodnius prolixus Ståhl (Hemiptera: Reduviidae). Canadian Journal of Zoology 4, 892–904.Google Scholar
Giorgi, M. S., Arlettaz, R., Guillaume, F., Nussle, S., Ossola, C., Vogel, P. and Christie, P. (2004). Causal mechanisms underlying host specificity in bat ectoparasites. Oecologia 138, 648–654. doi: 10.1007/s00442-003-1475-1.CrossRefGoogle ScholarPubMed
Graca-Souza, A. V., Maya-Monteiro, C., Paiva-Silva, G. O., Braz, G. R. C., Paes, M. C., Sorgine, M. H. F., Oliveira, M. F. and Oliveira, P. L. (2006). Adaptations against heme toxicity in blood-feeding arthropods. Insect Biochemistry and Molecular Biology 36, 322–335.CrossRefGoogle ScholarPubMed
Grol, M. G. G., Nagelkerken, I., Rypel, A. L. and Layman, G. A. (2011). Simple ecological trade-offs give rise to emergent cross-ecosystem distributions of coral reef fish. Oecologia 165, 79–88. doi: 10.1007/s00442-010-1833-8.CrossRefGoogle ScholarPubMed
Grutter, A. S. (1994). Spatial and temporal variations of the ectoparasites of seven reef fish species from Lizard Island, Australia. Marine Ecology Progress Series 115, 21–30.CrossRefGoogle Scholar
Grutter, A. S. (1999). Infestation dynamics of gnathiid isopod juveniles parasitic on coral-reef fish Hemigymnus melapterus (Labridae). Marine Biology 135, 545–552.CrossRefGoogle Scholar
Grutter, A. S. (2002). Cleaning symbioses from the parasites’ perspective. Parasitology 124, 65–81.CrossRefGoogle ScholarPubMed
Grutter, A. S. and Poulin, R. (1998). Intraspecific and interspecific relationships between host size and the abundance of parasitic larval gnathiid isopods on coral reef fishes. Marine Ecology Progress Series 164, 263–271.CrossRefGoogle Scholar
Grutter, A. S., Pickering, J. L., McCallum, H. and McCormick, M. I. (2008). Impact of micropredatory gnathiid isopods on young coral reef fishes. Coral Reefs 27, 655–661. doi: 10.1007/s00338-008-0377-4.CrossRefGoogle Scholar
Grutter, A. S., Rumney, J. G., Sinclair-Taylor, T., Waldie, P. and Franklin, C. E. (2011). Fish mucous cocoons: the ‘mosquito nets’ of the sea. Biology Letters 7, 292–294.CrossRefGoogle ScholarPubMed
Hadfield, K. A., Smit, N. J. and Avenant-Oledwage, A. (2009). Life cycle of the temporary fish parasite, Gnathia pilosus (Crustacea: Isopoda: Ganthiidae) from the East Coast of South Africa. Journal of the Marine Biological Association of the United Kingdom 89, 1331–1339.CrossRefGoogle Scholar
Halstead, B. W. (1978). Poisonous and Venomous Marine Animals of the World. The Darwin Press, Pennington, NJ.Google Scholar
Harris, P. D., Soleng, A. and Bakke, T. A. (1998). Killing of Gyrodacylus salaris (Platyhelminthes, Monogenea) mediated by host complement. Parasitology 117, 137–143.CrossRefGoogle ScholarPubMed
Hatcher, M. J. and Dunn, A. M. (2011). Parasites in Ecological Communities: From Interactions to Ecosystems. Cambridge University Press, New York, USA.CrossRefGoogle Scholar
Helfman, G. S., Collette, B. B., Facey, D. E. and Bowen, B. W. (2009). The Diversity of Fishes: Biology, Evolution, and Ecology, 2nd Edn.Wiley–Blackwell, Oxford, UK.Google Scholar
Hitt, S., Pittman, S. J. and Brown, K. A. (2011a). Tracking and mapping sun-synchronous migrations and diel space use patterns on Haemulon sciurus and Lutjanus apodus in the U.S. Virgin Islands. Environmental Biology of Fishes 92, 525–538. doi: 10.1007/s10641-011-9875-2.CrossRefGoogle Scholar
Hitt, S., Pittman, S. J. and Nemeth, R. S. (2011b). Diel movements of fishes linked to benthic seascape structure in a Caribbean coral reef ecosystem. Marine Ecology Progress Series 427, 275–291. doi: 10.3354/meps09093.CrossRefGoogle Scholar
Holbrook, S. J., Forrester, G. E. and Schmitt, R. J. (2000). Spatial patterns in abundance of a damselfish reflect availability of suitable habitat. Oecologia 122, 109–120.CrossRefGoogle ScholarPubMed
Horton, T. and Okamura, B. (2003). Post-hemorrhagic anemia in sea bass (Dicentrarchus labrax (L.), caused by blood feeding of Ceratothoa oestroides (Isopoda: Cymothoidae). Journal of Fish Diseases 26, 401–406.CrossRefGoogle Scholar
Huebner, L. K. and Chadwick, N. E. (2012). Patterns of cleaning behaviour on coral reef fish by the anemone shrimp Anclyomenes pedersoni. Journal of the Marine Biological Association of the United Kingdom 92, 1557–1562.CrossRefGoogle Scholar
Hudson, P. J., Dobson, A. P. and Lafferty, K. D. (2006). Is a healthy ecosystem one that is rich in parasites? Trends in Ecology and Evolution 21, 381–385.CrossRefGoogle Scholar
Jaenike, J. (1990). Host specialization in phytophagous insects. Annual Review of Ecology and Systematics 21, 243–273.CrossRefGoogle Scholar
Johnson, P. T. J., Dobson, A., Lafferty, K. D., Marcogliese, D. J., Memmott, J., Orlofske, S. A., Poulin, R. and Thieltges, D. W. (2010). When parasites become prey: ecological and epidemiological significance of eating parasites. Trends in Ecology and Evolution 25, 362–371.CrossRefGoogle ScholarPubMed
Jones, C. M. and Grutter, A. S. (2005). Parasitic isopods (Gnathia sp) reduce haematocrit in captive blackeye thicklip (Labridae) on the Great Barrier Reef. Journal of Fish Biology 66, 860–864.CrossRefGoogle Scholar
Jones, C. M., Nagel, L., Hughes, G. L. and Grutter, A. S. (2007). Host specificity of two species of Gnathia (Isopoda) determined by DNA sequencing blood meals. International Journal for Parasitology 37, 927–935.CrossRefGoogle ScholarPubMed
Jones, S. R. (2001). The occurrence and mechanisms of innate immunity against parasites in fish. Developmental and Comparative Immunology 25, 841–852.CrossRefGoogle ScholarPubMed
Kells, V. and Carpenter, K. (2011). A Field Guide to Coastal Fishes; from Maine to Texas. The Johns Hopkins University Press, Baltimore, MD, USA.CrossRefGoogle Scholar
Kubanek, J., Whalen, K. E., Engel, S., Kelly, S. R., Henkel, T. P. M., Fenical, W. and Pawlik, J. R. (2002). Multiple defensive roles for triterpene glycosides from two Caribbean sponges. Oecologia 131, 125–136.CrossRefGoogle ScholarPubMed
Lafferty, K. and Kuris, A. (2002). Trophic strategies, animal diversity and body size. Trends in Ecology and Evolution 17, 507–513.CrossRefGoogle Scholar
Lafferty, K. D., Allesina, S., Artim, M., Briggs, C. J., De Leo, G., Dobson, A. P., Dunne, J. A., Johnson, P. T., Kuris, A. M., Marcogliese, D. J., Martinez, N. D., Memmott, J., Marquet, J. P., Mordecai, E. A., Pascual, M., Poulin, R. and Thieltges, D. W. (2008). Parasites in food webs: the ultimate missing links. Ecology Letters 11, 533–546.CrossRefGoogle ScholarPubMed
Manship, B. M., Walker, A. J., Jones, L. A. and Davies, A. J. (2012). Blood feeding in juvenile Paragnathia formica (Isopoda: Gnathiidae): biochemical characterization of trypsin inhibitors, detection of anticoagulants, and molecular identification of fish hosts. Parasitology 139, 744–754.CrossRefGoogle ScholarPubMed
Martin, L. B., Han, P., Lewittes, J., Kuhlman, J. R., Klasing, K. C. and Wikelski, M. (2006). Phytohemagglutinin-induced skin swelling in birds: histological support for a classic immunoecological technique. Functional Ecology 20, 290–299.CrossRefGoogle Scholar
McCoy, K. D., Boulinier, T., Tirard, C. and Mickalakis, Y. (2001). Host specificity of a generalist parasite: genetic evidence of sympatric host races in the seabird tick Ixodes uriae. Journal of Evolutionary Biology 14, 395–405.CrossRefGoogle Scholar
Monod, T. (1926). Les Gnathiidae. Essai Monographique (Morphologie, Biologie, Systematique). Memories de la Societé Royal des Scences natural du Maroc 13, 1–668.Google Scholar
Munday, P. L., Schubert, M., Baggio, J. A., Jones, G. P., Caley, M. J. and Grutter, A. S. (2003). Skin toxins and external parasitism of coral-dwelling gobies. Journal of Fish Biology 62, 976–981. doi: 10.1046/j.1095-8649.2003.00078.x.CrossRefGoogle Scholar
Muñoz, G., Grutter, A. S. and Cribb, T. H. (2006). Endoparasite communities of five fish species (Labridae: Cheilininae) from Lizard Island: how important is the ecology and phylogeny of the hosts? Parasitology 132, 363–374.CrossRefGoogle ScholarPubMed
Nagel, L. and Grutter, A. S. (2007). Host preference and specialization in Gnathia sp., a common parasitic isopod of coral reef fishes. Journal of Fish Biology 70, 497–508.CrossRefGoogle Scholar
Nolan, D. T., Reilly, P. and Wendelaar Bonga, S. E. (1999). Infection with low numbers of sea louse Lepeophtheirus salmonis induces stress-related effects in postmolt Atlantic salmon (Salomo salar). Canadian Journal of Fisheries and Aquatic Sciences 56, 947–959.CrossRefGoogle Scholar
Ota, Y., Hoshino, O., Hirose, M., Tanaka, K. and Hirose, E. (2012). Third-stage larva shifts host fish from teleost to elasmobranch in the temporary parasitic isopod, Gnathia trimaculata (Crustacea; Gnathiidae). Marine Biology 159, 2333–2347. doi: 10.1007/s00227-012-2018-2.CrossRefGoogle Scholar
Paperna, I. and Por, F. D. (1977). Preliminary data on the Gnathiidae (Isopoda) of the Northern Red Sea, the Bitter Lakes and the Eastern Mediterranean and the Biology of Gnathia piscivora n. sp. Rapports de la Commission Internationale pour la Mer Méditerranée 24, 195–197.Google Scholar
Penfold, R., Grutter, A. S., Kuris, A. M., McCormick, M. I. and Jones, C. M. (2008). Interactions between juvenile marine fish and gnathiid isopods: predation versus micropredation. Marine Ecology Progress Series 357, 111–119.CrossRefGoogle Scholar
Poulin, R. (2007). Evolutionary Ecology of Parasites. 2nd Edn.Princeton University Press, Princeton, NJ, USA.CrossRefGoogle Scholar
Poulin, R., Krasnov, B. R. and Shenbrot, G. I. (2008). Interaction frequency across the geographical range as a determinant of host specialization in generalist fleas. International Journal for Parasitology 38, 989–997.CrossRefGoogle Scholar
Poulin, R., Krasnov, B. R. and Mouillot, D. (2011). Host specificity in phylogenetic and geographic space. Trends in Parasitology 27, 355–361.CrossRefGoogle ScholarPubMed
Randall, J. E., Oshima, A. K. and Hoshimato, Y. (1981). Occurrence of a crinotoxin and hemagglutinin in the skin mucus of the moray eel. Lycodontis nudivomer. Marine Biology 62, 179–184.CrossRefGoogle Scholar
Ravichandran, S., Rameshkumar, G. and Balasubramanian, T. (2010). Infestation of isopod parasites in commercial marine fishes. Journal of Parasitic Diseases 34, 97–98.CrossRefGoogle ScholarPubMed
Rhode, K. and Stauffer, D. (2005). Simulation of geographical trends in Chowdhury ecosystem model. Advances in Complex Systems 8, 1–14.Google Scholar
Ribeiro, J. M. and Francischetti, I. M. (2003). Role of arthropod saliva in blood feeding: sialome and post-sialome perspectives. Annual Review of Entomology 48, 73–88.CrossRefGoogle ScholarPubMed
Rocha, E. C. and Molina, W. F. (2008). Cytogenetic analysis in western Atlantic snappers (Perciformes, Lutjanidae). Genetics and Molecular Biology 31, 461–467.CrossRefGoogle Scholar
Romoser, W. S. (1996). The vector alimentar system. In The Biology of Disease Vectors (ed. Beaty, B. J. and Marquardt, W. C.), pp. 298–317. University Press of Colorado, CO, USA.Google Scholar
Sadd, B. M. and Schmid-Hempel, P. (2006). Insect immunity shows specificity in protection upon secondary pathogen exposure. Current Biology 16, 1206–1210. doi: 10.1016/j.cub.2006.04.047.CrossRefGoogle ScholarPubMed
Schneider, C. A., Rasband, W. S. and Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671–675.CrossRefGoogle ScholarPubMed
Seneviratne, S. S., Fernando, H. C. and Udagama-Randeniya, P. V. (2009). Host specificity in bat ectoparasites: a natural experiment. International Journal for Parasitology 39, 995–1002.CrossRefGoogle ScholarPubMed
Shima, J. S., Osenberg, C. W. and St. Mary, C. M. (2008). Quantifying site quality in a heterogeneous landscape: recruitment of a reef fish. Ecology 89, 86–94.CrossRefGoogle Scholar
Sikkel, P. C., Schaumburg, C. S. and Mathenea, J. K. (2006). Diel infestation dynamics of gnathiid isopod larvae parasitic on Caribbean reef fish. Coral Reefs 25, 683–689.CrossRefGoogle Scholar
Sikkel, P. C., Ziemba, R. E., Sears, W. T. and Wheeler, J. C. (2009). Diel ontogenetic shift in parasitic activity in a gnathiid isopod on Caribbean coral reefs. Coral Reefs 28, 489–495. doi: 10.1007/s00338-009-0474-z.CrossRefGoogle Scholar
Sikkel, P. C., Sears, W. T., Weldon, B. and Tuttle, B. C. (2011). An experimental field test of host-finding mechanisms in a Caribbean gnathiid isopod. Marine Biology 158, 1075–1083. doi: 10.1007/s00227-011-1631-9.CrossRefGoogle Scholar
Smit, N. J. and Davies, A. J. (2004). The curious life-style of the parasitic stages of gnathiid isopods. Advances in Parasitology 58, 289–391.CrossRefGoogle ScholarPubMed
Smit, N. J., Grutter, A. S., Adlard, R. D. and Davies, A. J. (2006). Hematozoa of teleosts from Lizard Island, Australia, with some comments on their possible mode of transmission and the description of a new Hemogregarine species. Journal of Parasitology 92, 778–788.CrossRefGoogle ScholarPubMed
Soares, M. C., Bshary, R. and Côté, I. M. (2008). Does cleanerfish service quality depend on client value or choice options? Animal Behavior 76, 123–130. doi: 10.1016/j.anbehav.2008.01.015.CrossRefGoogle Scholar
Stapp, P., Salkeld, D. J., Franlin, H. A., Kraft, J. P., Tripp, D. W., Antolin, M. F. and Gage, K. L. (2009). Evidence for the involvement of an alternate rodent host in the dynamics of introduced plague in prairie dogs. Journal of Animal Ecology 78, 807–817.CrossRefGoogle ScholarPubMed
Stark, K. and James, A. (1996). Anticoagulants in vector arthropods. Parasitology Today 12, 430–437.CrossRefGoogle ScholarPubMed
Tanaka, K. (2007). Life history of gnathiid isopods – current knowledge and future directions. Plankton and Benthos Research 2, 1–11.CrossRefGoogle Scholar
Tanaka, K. and Aoki, M. (1998). Crustacean infauna of the demosponge Halichondria okadai (Kadota) with reference to the life cycle of Gnathia sp. (Isopoda: Gnathiidea). In Sponge Sciences – Multidisciplinary Perspectives (ed. Watanabe, Y. and Fusetani, N.), pp. 259–267. Springer-Verlag, Tokyo, Japan.Google Scholar
Thomson, D. A. (1964). Ostracitoxin: an ichthyotoxic stress secretion of the boxfish, Ostracion lentiginosus. Science 146, 244–245.CrossRefGoogle ScholarPubMed
Tschirren, B., Bischoff, L. L., Saladin, V. and Richner, H. (2007). Host condition and host immunity affect parasite fitness in a bird–ectoparasite system. Functional Ecology 21, 372–378.CrossRefGoogle Scholar
Valera, F., Hoi, H., Darolová, A. and Kristofic, J. (2004). Size versus health as a cue for host choice: a test of the tasty chick hypothesis. Parasitology 129, 59–68.CrossRefGoogle Scholar
Walker, P. D., Harris, J. E., van der Velde, G. and Wendelaar Bonga, S. E. (2008). Differential host utilization by different life history stages of the fish ectoparasite Argulus foliaceus (Crustacea: Branchiura). Folia Parasitologica 55, 141–149.CrossRefGoogle ScholarPubMed
Wells, P. R. and Cone, D. K. (1990). Experimental studies on the effect of Gyrodactylus colemanensis and G. salmois (Monogenea) on the density of mucous cells in the epidermis of fry of Oncoryhynchus mykiss. Journal of Fish Biology 37, 599–603. doi: 10.1111/j.1095-8649.1990.tb05892.x.CrossRefGoogle Scholar