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Can parasites use predators to spread between primary hosts?

Published online by Cambridge University Press:  29 May 2013

JOANNE CABLE ,
GABRIELLE A. ARCHARD ,
RYAN S. MOHAMMED ,
MARK MCMULLAN ,
JESSICA F. STEPHENSON ,
HAAKON HANSEN  and
COCK van OOSTERHOUT
JOANNE CABLE*
Affiliation:
School of Biological Sciences, Cardiff University, Cardiff CF10 3AX, UK
GABRIELLE A. ARCHARD
Affiliation:
School of Biological Sciences, Cardiff University, Cardiff CF10 3AX, UK
RYAN S. MOHAMMED
Affiliation:
Department of Life Sciences, The University of West Indies, St. Augustine, Trinidad and Tobago
MARK MCMULLAN
Affiliation:
School of Environmental Sciences, University of East Anglia, Norwich NR4 7TJ, UK
JESSICA F. STEPHENSON
Affiliation:
School of Biological Sciences, Cardiff University, Cardiff CF10 3AX, UK
HAAKON HANSEN
Affiliation:
Norwegian Veterinary Institute, P.O. Box 750 Sentrum, NO-0106 Oslo, Norway
COCK van OOSTERHOUT
Affiliation:
School of Environmental Sciences, University of East Anglia, Norwich NR4 7TJ, UK
*
*Corresponding author: School of Biological Sciences, Cardiff University, Cardiff CF10 3AX, UK. E-mail: [email protected]
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Summary

Parasites typically have low reproductive fitness on paratenic hosts. Such hosts offer other significant inclusive fitness benefits to parasites, however, such as increased mobility and migration potential. The parasite fauna of the guppy (Poecilia reticulata) is dominated by the directly transmitted ectoparasites Gyrodactylus bullatarudis and Gyrodactylus turnbulli. In the wild, close predatory and competitive interactions occur between the guppy and the killifish Rivulus hartii. Previous observations suggest that these fish can share gyrodactylids, so we tested experimentally whether these parasites can use R. hartii as an alternative host. In aquaria, G. bullatarudis was the only species able to transmit from prey to predator. Both parasite species transferred equally well to prey when the predator was experimentally infected. However, in semi-natural conditions, G. bullatarudis transmitted more successfully to the prey fish. Importantly, G. bullatarudis also survived significantly longer on R. hartii out of water. As R. hartii can migrate overland between isolated guppy populations, G. bullatarudis may have an enhanced ability to disperse and colonize new host populations, consistent with its wider distribution in the wild. To our knowledge, this is the first empirical study demonstrating a predator acting as a paratenic host for the parasites of its prey.

Keywords

Gyrodactylusheterospecific interactionsparatenicPoecilia reticulatapredator–preytransmission
Type
Research Article
Information
Parasitology , Volume 140 , Issue 9 , August 2013 , pp. 1138 - 1143
Copyright
Copyright © Cambridge University Press 2013 

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References

REFERENCES

Bakke, T. A., Harris, P. D. and Cable, J. (2002). Host specificity dynamics: observations on gyrodactylid monogeneans. International Journal for Parasitology 32, 281–308.CrossRefGoogle ScholarPubMed
Bakke, T. A., Cable, J. and Harris, P. D. (2007). The biology of gyrodactylid monogeneans: the ‘Russian-doll killers’. Advances in Parasitology 64, 161–376.CrossRefGoogle ScholarPubMed
Barson, N. J., Cable, J. and van Oosterhout, C. (2009). Population genetic analysis of microsatellite variation of guppies (Poecilia reticulata) in Trinidad and Tobago: evidence for a dynamic source-sink metapopulation structure, founder events and population bottlenecks. Journal of Evolutionary Biology 22, 485–497.CrossRefGoogle ScholarPubMed
Brooks, D. R. and McLennan, D. A. (2002). The Nature of Diversity: An Evolutionary Voyage of Discovery. The University of Chicago Press, Chicago, IL, USA.CrossRefGoogle Scholar
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 85, 575–583.CrossRefGoogle Scholar
Cable, J. (2011). Poecilid parasites. In Evolution & Ecology of Poeciliid Fishes (eds. Evans, J. P., Pilastro, A. and Schlupp, I.), pp. 82–94. The University of Chicago Press, Chicago, IL, USA.Google Scholar
Cable, J. and Harris, P. D. (2002). Gyrodactylid developmental biology: historical review, current status and future trends. International Journal for Parasitology 32, 255–280.CrossRefGoogle ScholarPubMed
Cable, J. and van Oosterhout, C. (2007). The impact of parasites on the life history evolution of the guppies (Poecilia reticulata): the effects of host size on parasite virulence. International Journal for Parasitology 37, 1449–1458.CrossRefGoogle ScholarPubMed
Combes, C. (2001). Parasitism: The Ecology and Evolution of Intimate Interactions. The University of Chicago Press, Chicago, IL, USA.Google Scholar
De Meester, L., Gómez, A., Okamura, B. and Schwenk, K. (2002). The monopolisation hypothesis and the dispersal gene-flow paradox in aquatic organisms. Acta Oecologica 23, 121–135.CrossRefGoogle Scholar
Diamond, J. M. (1974). Colonisation of exploded volcanic islands by birds: the supertramp strategy. Science 184, 803–806.CrossRefGoogle ScholarPubMed
Fraser, D. F., Brousseau, C. J., Cohen, K. L. and Morse-Goetz, S. A. (2011). Guppies as heterospecific facilitators: a precursor of exploratory behaviour? Behavioural Ecology and Sociobiology 65, 1113–1122. doi:10.1007/s00265-010-1123-9.CrossRefGoogle Scholar
Galvani, A. P. (2003). Epidemiology meets evolutionary ecology. Trends in Ecology and Evolution 18, 132–139.CrossRefGoogle Scholar
Gilliam, J. F. and Fraser, D. F. (2001). Movement in corridors: enhancement by predation threat, disturbance, and habitat structure. Ecology 82, 258–273.CrossRefGoogle Scholar
Godin, J.-G. and McDonough, H. E. (2003). Predator preference for brightly colored males in the guppy: a viability cost for a sexually selected trait. Behavioral Ecology 14, 194–200.CrossRefGoogle Scholar
Harris, P. D., Cable, J., Tinsley, R. C. and Lazarus, C. M. (1999). Combined ribosomal DNA and morphological analysis of individual gyrodactylid monogeneans. Journal of Parasitology 95, 188–191.CrossRefGoogle Scholar
Houde, A. E. (1997). Sex, Colour and Mate Choice in Guppies. Princeton University Press, Princeton, NJ, USA.Google Scholar
Jowers, M. J., Cohen, B. L. and Downie, J. R. (2008). The cyprinodont fish Rivulus (Alocheilodei Rivulidae) in Trinidad and Tobago: molecular evidence for marine dispersal, genetic isolation and local differentiation. Journal of Zoological Systematics and Evolutionary Research 46, 48–55.Google Scholar
Kennedy, C. E. J., Endler, J. A., Poynton, S. L. and McMinn, H. (1987). Parasite load predicts mate choice in guppies (Poecilia reticulata). Behavioural Ecology and Sociobiology 21, 291–295.CrossRefGoogle Scholar
King, T. A. and Cable, J. (2007). Experimental infections of the monogenean Gyrodactylus turnbulli indicate that it is not a strict specialist. International Journal for Parasitology 37, 663–672.CrossRefGoogle Scholar
King, T. A., van Oosterhout, C. and Cable, J. (2009). Experimental infections with the tropical monogenean, Gyrodactylus bullatarudis: potential invader or experimental fluke? Parasitology International 58, 249–254.CrossRefGoogle ScholarPubMed
Lafferty, K. D., Dobson, A. P. and Kuris, A. M. (2006). Parasites dominate food web links. Proceedings of the National Academy of Sciences USA 103, 11211–11216.CrossRefGoogle ScholarPubMed
Liley, N. R. and Seghers, B. H. (1975). Factors affecting the morphology and behaviour of guppies in Trinidad. In Function and Evolution in Behaviour (eds. Baerends, G. P., Beer, C. and Manning, A.), pp. 92–118. Clarendon Press, Oxford, UK.Google Scholar
López, S. (1999). Parasitized female guppies do not prefer showy males. Behavioural Ecology 57, 1129–1134.Google Scholar
Magurran, A. E. (2005). Evolutionary Ecology: The Trinidadian Guppy. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Marcogliese, D. J. (1995). The role of zooplankton in the transmission of helminth parasites to fish. Reviews in Fish Biology and Fisheries 5, 336–371.CrossRefGoogle Scholar
Mattingly, H. T. and Butler, M. J. (1994). Laboratory predation on the Trinidadian guppy: implications for the size-selective predation hypothesis and guppy life history evolution. OIKOS 69, 54–64.CrossRefGoogle Scholar
Orlofske, S. A., Jadin, R. C., Preston, D. L. and Johnson, P. T. J. (2012). Parasite transmission in complex communities: predators and alternative hosts alter pathogenic infections in amphibians. Ecology 93, 1247–1253.CrossRefGoogle ScholarPubMed
Reznick, D. N. (1982). The impact of predation on life history evolution in Trinidadian guppies: genetic basis of observed life history patterns. Evolution 36, 1236–1250.CrossRefGoogle ScholarPubMed
Reznick, D. N. (1995). Life history evolution in guppies: a model system for the empirical study of adaptation. Netherlands Journal of Zoology 46, 172–190.CrossRefGoogle Scholar
Reznick, D. N. and Endler, J. A. (1982). The impact of predation on life history evolution in Trinidadian guppies (Poecilia reticulata). Evolution 36, 160–177.Google ScholarPubMed
Richards, E. L. and Chubb, J. C. (1998). Longer-term population dynamics of Gyrodactylus bullatarudis and G. turnbulli (Monogenea) on adult guppies (Poecilia reticulata) in 50-l experimental arenas. Parasitology Research 84, 753–756.CrossRefGoogle Scholar
Richards, G. R. and Chubb, J. C. (1996). Host response to initial and challenge infections, following treatment, of Gyrodactylus bullatarudis and G. turnbulli (Monogenea) on the guppy (Poecilia reticulata). Parasitology Research 82, 242–247.CrossRefGoogle Scholar
Schelkle, B., Shinn, A. P., Peeler, E. and Cable, J. (2009). Treatment of gyrodactylid infections in fish. Diseases of Aquatic Organisms 86, 65–75.Google ScholarPubMed
Schelkle, B., Paladini, G., Shinn, A. P., King, S., Johnson, M., van Oosterhout, C., Mohammed, R. and Cable, J. (2011). Ieredactylus rivuli gen. et. sp. nov. (Monogenea, Gyrodactylidae) from Rivulus hartii (Cyprinodontiformes: Rivulidae) from Trinidad. Acta Parasitologica 56, 360–370.CrossRefGoogle Scholar
Seghers, B. H. (1978). Feeding behavior and terrestrial locomotion in the cyprinodontid fish, Rivulus hartii (Boulenger). Vol. Ph.D. University of British Columbia, Vancouver, Canada.CrossRefGoogle Scholar
Valtonen, E. T. and Julkunen, M. (1995). Influence of the transmission of parasites from prey fishes on the composition of the parasite community of a predatory fish. Canadian Journal of Fisheries and Aquatic Sciences 52(S1), 233–245.CrossRefGoogle Scholar
van Oosterhout, C., Harris, P. D. and Cable, J. (2003). Marked variation in parasite resistance between two wild populations of the Trinidadian guppy, Poecilia reticulata (Pisces: Poeciliidae). Biological Journal of the Linnean Society 79, 645–651.CrossRefGoogle Scholar
van Oosterhout, C., Mohammed, R. S., Hansen, H., Archard, G. A., McMullan, M., Weese, D. J. and Cable, J. (2007). Selection by parasites in spate conditions in wild Trinidadian guppies (Poecilia reticulata). International Journal for Parasitology 37, 805–812.CrossRefGoogle ScholarPubMed
Walsh, M. R., Fraser, D. F., Bassar, R. D. and Reznick, D. N. (2011). The direct and indirect effects of guppies: implications for life-history evolution in Rivulus hartii. Functional Ecology 25, 227–237.CrossRefGoogle Scholar
Walter, R. P., Blum, M. J., Snider, S. B., Paterson, I. G., Bentzen, P., Lamphere, B. A. and Gilliam, J. F. (2011). Isolation and differentiation of Rivulus hartii across Trinidad and neighboring islands. Molecular Ecology 20, 601–618.CrossRefGoogle ScholarPubMed