Abstract
Parasite avoidance is increasingly considered to be a potential driving factor in animal migrations. In many marine and freshwater benthic fish, migration into a pelagic environment by developing larvae is a common life history trait that could reduce exposure to parasites during a critical window of developmental susceptibility. We tested this hypothesis on congeneric fish (family Galaxiidae, genus Galaxias) belonging to a closely related species complex sampled from coastal streams in southeastern New Zealand. Migratory Galaxias have larvae that migrate to pelagic marine environments, whereas the larvae of non-migratory species rear close to adult habitats with no pelagic larval phase. Both migratory and non-migratory fish are hosts to two species of skin-penetrating trematodes that cause spinal malformations and high mortality in young fish. Using generalized linear models within an Akaike information criterion and model averaging framework, we compared infection levels between migratory and non-migratory fish while taking into account body size and several other local factors likely to influence infection levels. For one trematode species, we found a significant effect of migration: for any given body length, migratory fish harboured fewer parasites than non-migratory fish. Also, no parasites of any kind were found in juvenile migratory fish sampled in spring shortly after their return to stream habitats. Our results demonstrate that migration spares juvenile fish from the debilitating parasites to which they would be exposed in adult stream habitats. Therefore, either the historical adoption of a migratory strategy in some Galaxias was an adaptation against parasitism, or it evolved for other reasons and now provides protection from infection as a coincidental side-effect.
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References
Allibone RM, Wallis GP (1993) Genetic variation and diadromy in some native New Zealand galaxiids (Teleostei: Galaxiidae). Biol J Linn Soc 50:19–33
Altizer S, Bartel R, Han BA (2011) Animal migration and infectious disease risk. Science 331:296–302
Bartoñ K (2009) MuMIn: multi-model inference. Available at: http://r-forge.r-project.org/projects/mumin/
Bouillon DR, Curtis MA (1987) Diplostomiasis (Trematoda: Strigeidae) in Arctic charr (Salvelinus alpinus) from Charr Lake, northern Labrador. J Wildl Dis 23:502–505
Boyle WA (2008) Partial migration in birds: tests of three hypotheses in a tropical lekking frugivore. J Anim Ecol 77:1122–1128
Brooks DR, Hoberg EP (2007) How will global climate change affect parasite–host assemblages? Trends Parasitol 23:571–574
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York
de Roij J, Harris PD, MacColl ADC (2011) Divergent resistance to a monogenean flatworm among three-spined stickleback populations. Funct Ecol 25:217–226
Dingle H (1996) Migration: the biology of life on the move. Oxford University Press, Oxford
Dingle H, Drake VA (2007) What is migration? Bioscience 57:113–121
Ferguson JA, Koketsu W, Ninomiya I, Rossignol PA, Jacobson KC, Kent ML (2011) Mortality of coho salmon (Oncorhynchus kisutch) associated with burdens of multiple parasite species. Int J Parasitol 41:1197–1205
Folstad I, Nilssen AC, Halvorsen O, Andersen J (1991) Parasite avoidance: the cause of postcalving migrations in Rangifer? Can J Zool 69:2423–2429
Fredensborg BL, Poulin R (2006) Parasitism shaping host life-history evolution: adaptive responses in a marine gastropod to infection by trematodes. J Anim Ecol 75:44–53
Gordon DM, Rau ME (1982) Possible evidence for mortality induced by the parasite Apatemon gracilis in a population of brook sticklebacks (Culaea inconstans). Parasitology 84:41–47
Gross MR, Coleman RM, McDowall RM (1988) Aquatic productivity and the evolution of diadromous fish migration. Science 239:1291–1293
Grutter AS, Cribb TH, McCallum H, Pickering JL, McCormick MI (2010) Effects of parasites on larval and juvenile stages of the coral reef fish Pomacentrus moluccensis. Coral Reefs 29:31–40
Herrmann KK, Poulin R (2011) Encystment site affects the reproductive strategy of a progenetic trematode in its fish intermediate host: is host spawning an exit for parasite eggs? Parasitology 138:1183–1192
Hine PM, Jones JB, Diggles BK (2000) A checklist of parasites of New Zealand fishes, including previously unpublished records. NIWA Tech Rep 75:1–93
Jacobson KC, Teel D, Van Doornik DM, Castillas E (2008) Parasite-associated mortality of juvenile Pacific salmon caused by the trematode Nanophyetus salmincola during early marine residence. Mar Ecol Prog Ser 354:235–244
Kelly DW, Paterson RA, Townsend CR, Poulin R, Tompkins DM (2009) Has the introduction of brown trout altered disease patterns in native New Zealand fish? Freshw Biol 54:1805–1818
Kelly DW, Thomas H, Thieltges DW, Poulin R, Tompkins DM (2010) Trematode infection causes malformations and population effects in a declining New Zealand fish. J Anim Ecol 79:445–452
Lafferty KD (2009) The ecology of climate change and infectious diseases. Ecology 90:888–900
Lemly A, Esch G (1984) Effects of the trematode Uvulifer ambloplitis on juvenile bluegill sunfish, Lepomis macrochirus: ecological implications. J Parasitol 70:475–492
Levin LA (2006) Recent progress in understanding larval dispersal: new directions and digressions. Integr Comp Biol 46:282–297
Loehle C (1995) Social barriers to pathogen transmission in wild animal populations. Ecology 76:326–335
Lucas M, Barras E (2001) Migration of freshwater fishes. Blackwell Science, Oxford
Macfarlane WV (1945) The life cycle of the heterophyoid trematode Telogaster opisthorchis n.g., n. sp. Trans R Soc N Z 75:218–230
Macfarlane WV (1951) The life cycle of Stegodexamene anguillae n. g., n. sp., an allocreadiid trematode from New Zealand. Parasitology 41:1–10
Macfarlane WV (1952) Bionomics of two trematode parasites of New Zealand eels. J Parasitol 38:391–397
McDowall RM (1988) Diadromy in fishes: migrations between freshwater and marine environments. Croom Helm, London
McDowall RM (2008) Diadromy, history and ecology: a question of scale. Hydrobiologia 602:5–14
Mouritsen KN, Poulin R (2002) Parasitism, climate oscillations and the structure of natural communities. Oikos 97:462–468
Mueller JC, Pulido F, Kempenaers B (2011) Identification of a gene associated with avian migratory behaviour. Proc R Soc B 278:2848–2856
Ohlberger J, Langangen Ø, Edeline E, Olsen EM, Winfield IJ, Fletcher JM, James JB, Stenseth NC, Vøllestad LA (2011) Pathogen-induced rapid evolution in a vertebrate life-history trait. Proc R Soc B 278:35–41
Olsson IC, Greenberg LA, Bergman E, Wysujack K (2006) Environmentally induced migration: the importance of food. Ecol Lett 9:645–651
Piersma T (1997) Do global patterns of habitat use and migration strategies co-evolve with relative investments in immunocompetence due to spatial variation in parasite pressure? Oikos 80:623–631
Poulin R (1993) Age-dependent effects of parasites on anti-predator responses in two New Zealand freshwater fish. Oecologia 96:431–438
Poulin R (2000) Variation in the intraspecific relationship between fish length and intensity of parasitic infections: biological and statistical causes. J Fish Biol 56:123–137
Poulin R, Lefebvre F (2006) Alternative life-history and transmission strategies in a parasite: first come, first served? Parasitology 132:135–141
R Development Core Team (2009) R: a language and environment for statistical computing. Version 2.11.2. R Foundation for Statistical Computing, Vienna. Availiable at: http://www.r-project.org.
Taylor CM, Norris DR (2007) Predicting conditions for migration: effects of density dependence and habitat quality. Biol Lett 3:280–283
Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, Berlin
Waters JM, Rowe DL, Burridge CP, Wallis GP (2010) Gene trees versus species trees: reassessing life-history evolution in a freshwater fish radiation. Syst Biol 59:504–517
Wilcove DS, Wikelski M (2008) Going, going, gone: is animal migration disappearing? PLoS Biol 6:1361–1364
Wilson K, Grenfell BT (1997) Generalized linear modelling for parasitologists. Parasitol Today 13:33–38
Acknowledgments
We thank Abbas Akbaripasand, Kim Garrett, Rachel Paterson, Bronwen Presswell, Yannick Pons and Amélie Saunier for field and/or laboratory assistance, and Ken Miller for preparing the figure in the ESM. Permission to sample certain localities was given by the Department of Conservation, and approval to collect and euthanize fish was given by the University of Otago Animal Ethics Committee. This project was funded by a University of Otago Research Grant.
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Communicated by Øyvind Fiksen.
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Poulin, R., Closs, G.P., Lill, A.W.T. et al. Migration as an escape from parasitism in New Zealand galaxiid fishes. Oecologia 169, 955–963 (2012). https://doi.org/10.1007/s00442-012-2251-x
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DOI: https://doi.org/10.1007/s00442-012-2251-x