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Infection, specificity and host manipulation of Australapatemon sp. (Trematoda, Strigeidae) in two sympatric species of leeches (Hirudinea)

Published online by Cambridge University Press:  15 May 2017

ANSSI KARVONEN*
Affiliation:
Department of Biological and Environmental Science, University of Jyvaskyla, PO Box 35, 40014 Jyvaskyla, Finland
ANNA FALTÝNKOVÁ
Affiliation:
Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, Branišovská 31, 370 05 České Budějovice, Czech Republic
JOCELYN MAH CHOO
Affiliation:
Department of Biological and Environmental Science, University of Jyvaskyla, PO Box 35, 40014 Jyvaskyla, Finland
E. TELLERVO VALTONEN
Affiliation:
Department of Biological and Environmental Science, University of Jyvaskyla, PO Box 35, 40014 Jyvaskyla, Finland
*
*Corresponding author: Department of Biological and Environmental Science, University of Jyvaskyla, PO Box 35, 40014 Jyvaskyla, Finland. E-mail: anssi.t.karvonen@jyu.fi

Summary

Factors that drive parasite specificity and differences in infection dynamics among alternative host species are important for ecology and evolution of host–parasite interactions, but still often poorly known in natural systems. Here, we investigated spatiotemporal dynamics of infection, host susceptibility and parasite-induced changes in host phenotype in a rarely explored host–parasite system, the Australapatemon sp. trematode infecting two sympatric species of freshwater leeches, Erpobdella octoculata and Helobdella stagnalis. We show significant variation in infection abundance between the host species in both space and time. Using experimental infections, we also show that most of this variation likely comes from interspecific differences in exposure rather than susceptibility. Moreover, we demonstrate that the hiding behaviour of E. octoculata, but not that of H. stagnalis, was impaired by the infection irrespective of the parasite abundance. This may increase susceptibility of E. octoculata to predation by the final avian host. We conclude that differences in patterns of infection and in behavioural alterations among alternative sympatric host species may arise in narrow spatial scales, which emphasises the importance of local infection and transmission dynamics for parasite life cycles.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2017 

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Footnotes

Passed away during preparation of the final version of the manuscript.

References

REFERENCES

Benesh, D. P., Hasu, T., Seppälä, O. and Valtonen, E. T. (2009). Seasonal changes in host phenotype manipulation by an acanthocephalan: time to be transmitted? Parasitology 136, 219230.CrossRefGoogle ScholarPubMed
Bethel, W. M. and Holmes, J. C. (1974). Correlation of development of altered evasive behavior in Gammarus lacustris (Amphipoda) harboring cystacanths of Polymorphus paradoxus (Acanthocephala) with the infectivity to the definitive host. Journal of Parasitology 60, 272274.CrossRefGoogle Scholar
Byers, J. E., Blakeslee, A. M. H., Linder, E., Cooper, A. B. & Maguire, T. J. (2008). Controls of spatial variation in the prevalence of trematode parasites infecting a marine snail. Ecology 89, 439451.CrossRefGoogle ScholarPubMed
Combes, C. (2001). Parasitism: the Ecology and Evolution of Intimate Interactions. The University of Chicago Press, Chicago and London.Google Scholar
de Bekker, C., Quevillon, L. E., Smith, P. B., Fleming, K. R., Ghosh, D., Patterson, A. D. and Hughes, D. P. (2014). Species-specific ant brain manipulation by a specialized fungal parasite. BMC Evolutionary Biology 14, 166.CrossRefGoogle ScholarPubMed
Detwiler, J. T. and Minchella, D. J. (2009). Intermediate host availability masks the strength of experimentally-derived colonisation patterns in echinostome trematodes. International Journal for Parasitology 39, 585590.CrossRefGoogle ScholarPubMed
Dianne, L., Rigaud, T., Leger, E., Motreuil, S., Bauer, A. and Perrot-Minnot, M. J. (2010). Intraspecific conflict over host manipulation between different larval stages of an acanthocephalan parasite. Journal of Evolutionary Biology 23, 26482655.CrossRefGoogle ScholarPubMed
Drago, F. B. and Lunaschi, L. I. (2010). Digenea, Strigeidae, Australapatemon canadensis Dubois and Rausch, 1950: first record in South America and a new host record. Check List 6, 382384.CrossRefGoogle Scholar
Elliot, J. M. (1973). The life cycle and production of the leech Erpobdella octoculata (L.) (Hirudinea: Erpobdellidae) in a Lake District stream. Journal of Animal Ecology 42, 435448.CrossRefGoogle Scholar
Faltýnková, A., Niewiadomska, K., Santos, M. J. and Valtonen, E. T. (2007). Furcocercous cercariae (Trematoda) from freshwater snails in Central Finland. Acta Parasitologica 52, 310317.CrossRefGoogle Scholar
Faltýnková, A., Valtonen, E. T. and Karvonen, A. (2008). Spatial and temporal structure of the trematode component community in Valvata macrostoma (Gastropoda, Prosobranchia). Parasitology 135, 16911699.CrossRefGoogle ScholarPubMed
Faltýnková, A., Karvonen, A. and Valtonen, E. T. (2011). Establishment and interspecific associations in two species of Ichthyocotylurus (Trematoda) parasites in perch (Perca fluviatilis). Parasites & Vectors 4, 85.CrossRefGoogle ScholarPubMed
Galaktionov, K. V. and Dobrovolskiy, A. A. (2003). The Biology and Evolution of Trematodes. An Essay on the Biology, Morphology, Life Cycles, Transmission, and Evolution on Digenetic Trematodes. Kluwer Academic Publishers, Dordrecht, Netherlands.Google Scholar
Granovitch, A. I., Sergievsky, S. O. and Sokolova, I. M. (2000). Spatial and temporal variation of trematode infection in coexisting populations of intertidal gastropods Littorina saxatilis and L. obtusata in the White Sea. Diseases of Aquatic Organisms 41, 5364.CrossRefGoogle ScholarPubMed
Hafer, N. and Milinski, M. (2015). When parasites disagree: evidence for parasite-induced sabotage of host manipulation. Evolution 69, 611620.CrossRefGoogle ScholarPubMed
Hernandez, R. N. and Fredensborg, B. L. (2015). Experimental test of host specificity in a behaviour-modifying trematode. Parasitology 142, 16311639.CrossRefGoogle Scholar
Holmes, J. C. and Bethel, W. M. (1972). Modification of intermediate host behaviour by parasites. In Behavioural Aspects of Parasite Transmission (ed. Canning, E. U. and Wright, C. A.), pp. 123149. Academic Press, London, UK.Google Scholar
Jokela, J. and Lively, C. M. (1995). Spatial variation in infection by digenetic trematodes in a population of fresh-water snails (Potamopyrgus antipodarum). Oecologia 103, 509517.CrossRefGoogle Scholar
Karvonen, A., Seppälä, O. and Valtonen, E. T. (2004). Parasite resistance and avoidance behaviour in preventing eye fluke infections in fish. Parasitology 129, 159164.CrossRefGoogle ScholarPubMed
Karvonen, A., Cheng, G.-H. and Valtonen, E. T. (2005). Within-lake dynamics in the similarity of parasite assemblages of perch (Perca fluviatilis). Parasitology 131, 817823.CrossRefGoogle ScholarPubMed
Kufel, J. (1974/1975). Leeches (Hirudinea) of the reserve Stawy Milickie (Milicz Fishponds). Zeszyty Przyrodnicze. Opolskie Towarzystwo Przyjaciół Nauk 14/15, 219228.Google Scholar
Kutschera, U. (2003). The feeding strategies of the leech Erpobdella octoculata (L.): a laboratory study. International Review of Hydrobiology 88, 94101.CrossRefGoogle Scholar
Kutschera, U. and Wirtz, P. (2001). The evolution of parental care in freshwater leeches. Theory in Biosciences 120, 115137.CrossRefGoogle Scholar
Lafferty, K. D. and Morris, K. (1996). Altered behavior of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology 77, 13901397.CrossRefGoogle Scholar
Lagrue, C., Kaldonski, N., Perrot-Minnot, M. J., Motreuil, S. and Bollache, L. (2007). Modification of hosts’ behavior by a parasite: field evidence for adaptive manipulation. Ecology 88, 28392847.CrossRefGoogle ScholarPubMed
Lisney, T. J., Stecyk, K., Kolominsky, J., Schmidt, B. K., Corfield, J. R., Iwaniuk, A. N. and Wylie, D. R. (2013). Ecomorphology of eye shape and retinal topography in waterfowl (Aves: Anseriformes: Anatidae) with different foraging modes. Journal of Comparative Physiology A 199, 385402.CrossRefGoogle ScholarPubMed
Marklund, O., Blindow, I. and Hargeby, A. (2001). Distribution and diel migration of macroinvertebrates within dense submerged vegetation. Freshwater Biology 46, 913924.CrossRefGoogle Scholar
McCarthy, A. M. (1990). Experimental observations on the specificity of Apatemon (Australapatemon) minor (Yamaguti 1933) (Digenea: Strigeidae) toward leech (Hirudinea) second intermediate hosts. Journal of Helminthology 64, 161167.CrossRefGoogle ScholarPubMed
Moore, J. (1983). Responses of an avian predator and its isopod prey to an acanthocephalan parasite. Ecology 64, 10001015.CrossRefGoogle Scholar
Moore, J. (2002). Parasites and the Behavior of Animals. Oxford University Press, New York.CrossRefGoogle Scholar
Murphy, P. M. and Learner, M. A. (1982 a). The life history and production of the leech Erpobdella octoculata (Hirudinea Erpobdellidae) in the river Ely, South Wales. Journal of Animal Ecology 51, 5767.CrossRefGoogle Scholar
Murphy, P. M. and Learner, M. A. (1982 b). The life history and production of the leech Helobdella stagnalis (Hirudinea: Glossiphoniidae) in the river Ely, South Wales. Freshwater Biology 12, 321329.CrossRefGoogle Scholar
Niewiadomska, K. (2002 a). Cyathocotylidae Mühling, 1898. In Keys to the Trematoda, Vol. 1 (ed. Gibson, D. I., Jones, A. and Bray, R. A.), pp. 201214. Natural History Museum London and CAB International, Wallingford, UK.CrossRefGoogle Scholar
Niewiadomska, K. (2002 b). Strigeidiae Railliet, 1919. In Keys to the Trematoda, Vol. 1 (ed. Gibson, D. I., Jones, A. and Bray, R. A.), pp. 231241. Natural History Museum London and CAB International, Wallingford, UK.CrossRefGoogle Scholar
Poulin, R. (2007). Evolutionary Ecology of Parasites, 2nd Edn. Princeton University Press, New Jersey, USA.CrossRefGoogle Scholar
Poulin, R. and Keeney, D. B. (2008). Host specificity under molecular and experimental scrutiny. Trends in Parasitology 24, 2428.CrossRefGoogle ScholarPubMed
Poulin, R., Krasnov, B. R. and Mouillot, D. (2011). Host specificity in phylogenetic and geographic space. Trends in Parasitology 27, 355361.CrossRefGoogle ScholarPubMed
Rellstab, C., Louhi, K.-R., Karvonen, A. and Jokela, J. (2011). Analysis of trematode parasite communities in fish eye lenses by pyrosequencing of naturally pooled DNA. Infection, Genetics and Evolution 11, 12761286.CrossRefGoogle ScholarPubMed
Rothschild, M. (1962). Changes in behaviour in the intermediate hosts of trematodes. Nature 193, 13121313.CrossRefGoogle Scholar
Seppälä, O., Karvonen, A. and Valtonen, E. T. (2005). Manipulation of fish host by eye flukes in relation to cataract formation and parasite infectivity. Animal Behaviour 70, 889894.CrossRefGoogle Scholar
Seppälä, O., Karvonen, A. and Valtonen, E. T. (2008). Shoaling behaviour of fish under parasitism and predation risk. Animal Behaviour 75, 145150.CrossRefGoogle Scholar
Skírnisson, K., Galaktionov, K. V. and Kozminsky, V. (2004). Factors influencing the distribution of digenetic trematode infections in a mudsnail (Hydrobia ventrosa) population inhabiting salt marsh ponds in Iceland. Journal of Parasitology 90, 5059.CrossRefGoogle Scholar
Sparkes, T. C., Wright, V. M., Renwick, D. T., Weil, K. A., Talkington, J. A. and Milhalyov, M. (2004). Intra-specific host sharing in the manipulative parasite Acanthocephalus dirus: does conflict occur over host manipulation? Parasitology 129, 335340.CrossRefGoogle Scholar
Spelling, S. M. and Young, J. O. (1986 a). The population dynamics of metacercariae of Apatemon gracilis (Trematoda: Digenea) in three species of lake-dwelling leeches. Parasitology 93, 517530.CrossRefGoogle Scholar
Spelling, S. M. and Young, J. O. (1986 b). Seasonal occurrence of metacercariae of the trematode Cotylurus cornutus (Szidat) in three species of lake-dwelling leeches. Journal of Parasitology 72, 837845.CrossRefGoogle Scholar
Spelling, S. M. and Young, J. O. (1987). Predation on lake-dwelling leeches (Annellida: Hirudinea): an evaluation by field experiment. Journal of Animal Ecology 43, 131146.CrossRefGoogle Scholar
Streicker, D. G., Fenton, A. and Pedersen, A. B. (2013). Differential sources of host species heterogeneity influence the transmission and control of multihost parasites. Ecology Letters 16, 975984.CrossRefGoogle ScholarPubMed
Sudarikov, V. E., Shigin, A. A., Kurochkin, Y. V., Lomakin, V. V., Stenko, R. P. and Yurlova, N. I. (2002). Trematode metacercariae – parasites of freshwater animals in Central Russia. Rossiyskaya Akademia Nauk, Izdatelstvo Nauka, Moskva, Russia (in Russian).Google Scholar
Valtonen, E. T., Pulkkinen, K., Poulin, R. and Julkunen, M. (2001). The structure of parasite component communities in brackish water fishes of the northeastern Baltic Sea. Parasitology 122, 471481.CrossRefGoogle ScholarPubMed
Valtonen, E. T., Holmes, J. C., Aronen, J. and Rautalahti, I. (2003). Parasite communities as indicators of recovery from pollution: parasites of roach (Rutilus rutilus) and perch (Perca fluviatilis) in Central Finland. Parasitology 126, 4352.CrossRefGoogle Scholar
Vojtek, J., Opravilová, V. and Vojtková, L. (1967). The importance of leeches in the life-cycle of the order Strigeidida (Trematoda). Folia Parasitologica 14, 107119.Google Scholar
Young, J. O., Seaby, R. M. H. and Martin, A. J. (1995). Contrasting mortality in young freshwater leeches and triclads. Oecologia 101, 317323.CrossRefGoogle ScholarPubMed