Spillover of an alien parasite reduces expression of costly behaviour in native host species.

Sciurus carolinensis Sciurus vulgaris Mirror Image Stimulation test Open Field Test helminths invasive alien species macroparasites personality traits

Journal

The Journal of animal ecology
ISSN: 1365-2656
Titre abrégé: J Anim Ecol
Pays: England
ID NLM: 0376574

Informations de publication

Date de publication:
07 2020
Historique:
received: 27 11 2019
accepted: 10 03 2020
pubmed: 16 4 2020
medline: 27 2 2021
entrez: 16 4 2020
Statut: ppublish

Résumé

Understanding the effects of invasive alien species (IAS) on native host-parasite relationships is of importance for enhancing ecological theory and IAS management. When IAS and their parasite(s) invade a guild, the effects of interspecific resource competition and/or parasite-mediated competition can alter existing native host-parasite relationships and the dependent biological traits such as native species' behaviour. We used a natural experiment of populations of native red squirrels Sciurus vulgaris that were colonized by the alien grey squirrel Sciurus carolinensis, comparing repeated measurements of red squirrel parasite infection and personality with those taken in sites where only the native species occurred. We explored two alternative hypotheses: (a) individual differences in personality traits (activity and/or sociability) of native red squirrel positively affect the probability of macroparasite spillover and thus the likelihood to acquire the alien's parasitic helminth Strongyloides robustus; (b) the combined effects of grey squirrel presence and parasite infection result in a reduction of costly personality traits (activity and/or exploration). Using data from 323 arena tests across three experimental (native species and IAS) and three control sites (only native species), we found negative correlations between native species' activity and infection with S. robustus in the sites invaded by the alien species. Activity was also negatively correlated with infection by its native helminth Trypanoxyuris sciuri but only when grey squirrels were present, while in the red-only sites there was no relationship of T. sciuri infection with any of the personality traits. Moreover, individuals that acquired S. robustus during the study reduced their activity after infection, while this was not the case for animals that remained uninfected. Our results show that parasite-mediated competition is costly, reducing activity in individuals of the native species, and altering the native host-native parasite relationships.

Identifiants

pubmed: 32291765
doi: 10.1111/1365-2656.13219
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1559-1569

Informations de copyright

© 2020 British Ecological Society.

Références

Anderson, R. C. (2000). Nematode parasites of vertebrates: Their development and transmission (2nd ed.). Wallingford, UK: CABI Publishing.
Anderson, R. C., & May, R. (1979). Population biology of infectious diseases: Part I. Nature, 280, 361-367. https://doi.org/10.1038/280361a0
Barber, I., & Dingemanse, N. J. (2010). Parasitism and the evolutionary ecology of animal personality. Philosophical Transactions of the Royal Society B: Biological Sciences, 365, 4077-4088. https://doi.org/10.1098/rstb.2010.0182
Bell, A. M., Hankinson, S. J., & Laskowski, K. L. (2009). The repeatability of behaviour: A meta-analysis. Animal Behaviour, 77, 771-783. https://doi.org/10.1016/j.anbehav.2008.12.022
Bertolino, S., Montezemolo, N. C., Preatoni, D. G., Wauters, L. A., & Martinoli, A. (2014). A grey future for Europe: Sciurus carolinensis is replacing native red squirrels in Italy. Biological Invasions, 16, 53-62. https://doi.org/10.1007/s10530-013-0502-3
Bohn, S. J., Webber, Q. M. R., Florko, K. R. N., Paslawski, K. R., Peterson, A. M., Piche, J. E., … Willis, C. K. R. (2017). Personality predicts ectoparasite abundance in an asocial sciurid. Ethology, 123, 761-771. https://doi.org/10.1111/eth.12651
Boyer, N., Réale, D., Marmet, J., Pisanu, B., & Chapuis, J.-L. (2010). Personality, space use and tick load in an introduced population of Siberian chipmunks Tamias sibiricus. Journal of Animal Ecology, 79, 538-547.
Carter, A. J., Feeney, W. E., Marshall, H. H., Cowlishaw, G., & Heinsohn, R. (2013). Animal personality: What are behavioural ecologists measuring? Biological Reviews, 88, 465-475. https://doi.org/10.1111/brv.12007
Ezenwa, V. O. (2016). Helminth-microparasite co-infection in wildlife: Lessons from ruminants, rodents and rabbits. Parasite Immunology, 38, 527-534. https://doi.org/10.1111/pim.12348
Ezenwa, V. O., Archie, E. A., Craft, M. E., Hawley, D. M., Martin, L. B., Moore, J., & White, L. (2016). Host behaviour-parasite feedback: An essential link between animal behaviour and disease ecology. Proceedings of the Royal Society of London B: Biological Sciences, 283, 2015-3078. https://doi.org/10.1098/rspb.2015.3078
Fenton, A., Viney, M. E., & Lello, J. (2010). Detecting interspecific macroparasite interactions from ecological data: Patterns and process. Ecology Letters, 13, 606-615. https://doi.org/10.1111/j.1461-0248.2010.01458.x
Fiegna, C., Dagleish, M. P., Coulter, L., Milne, E., Meredith, A., Finlayson, J., … McInnes, C. J. (2016). Host-pathogen dynamics of squirrelpox virus infection in red squirrels (Sciurus vulgaris). Veterinary Microbiology, 182, 18-27. https://doi.org/10.1016/j.vetmic.2015.10.012
Foreyt, W. J. (2011). Veterinary parasitology reference manual (5th ed.). London, UK: Wiley-Blackwell.
Gelman, A., & Rubin, D. B. (1992). Inference from iterative simulation using multiple sequences. Statistical Science, 7, 457-472. https://doi.org/10.1214/ss/1177011136
Geweke, J. (1992). Evaluating the accuracy of sampling-based approaches to the calculation of posterior moments. In J. M. Bernardo, A. P. Berger, A. P. Dawid, & A. F. M. Smith (Eds.). Bayesian statistics 4 (pp. 169-193). Oxford, UK: Oxford University Press.
Goedknegt, M. A., Feis, M. E., Wegner, K. M., Luttikhuizen, P. C., Buschbaum, C., Camphuysen, K. C., … Thieltges, D. W. (2016). Parasites and marine invasions: Ecological and evolutionary perspectives. Journal of Sea Research, 113, 11-27. https://doi.org/10.1016/j.seares.2015.12.003
Gurnell, J., Wauters, L. A., Lurz, P. W., & Tosi, G. (2004). Alien species and interspecific competition: Effects of introduced eastern grey squirrels on red squirrel population dynamics. Journal of Animal Ecology, 73, 26-35. https://doi.org/10.1111/j.1365-2656.2004.00791.x
Hadfield, J. D. (2010). MCMC methods for multi-response generalized linear mixed models: The MCMCglmm R package. Journal of Statistical Software, 33, 1-22. https://doi.org/10.18637/jss.v033.i02
Hänninen, L., & Pastell, M. (2009). CowLog: Open-source software for coding behaviors from digital video. Behavior Research Methods, 41, 472-476. https://doi.org/10.3758/BRM.41.2.472
Hatcher, M. J., Dick, J. T. A., & Dunn, A. M. (2006). How parasites affect interactions between competitors and predators. Ecology Letters, 9, 1253-1271. https://doi.org/10.1111/j.1461-0248.2006.00964.x
Hawley, D. M., Etienne, R. S., Ezenwa, V. O., & Jolles, A. E. (2011). Does animal behavior underlie covariation between hosts' exposure to infectious agents and susceptibility to infection? Implications for disease dynamics. Integrative and Comparative Biology, 51, 528-539. https://doi.org/10.1093/icb/icr062
Henrichs, B., Oosthuizen, M. C., Troskie, M., Gorsich, E., Gondhalekar, C., Beechler, B. R., … Jolles, A. E. (2016). Within guild co-infections influence parasite community membership: A longitudinal study in African Buffalo. Journal of Animal Ecology, 85, 1025-1034. https://doi.org/10.1111/1365-2656.12535
Hicks, O., Burthe, S. J., Daunt, F., Newell, M., Butler, A., Ito, M., … Green, J. A. (2018). The energetic cost of parasitism in a wild population. Proceedings of the Royal Society B: Biological Sciences, 285, 20180489. https://doi.org/10.1098/rspb.2018.0489
Hofmannová, L., Romeo, C., Štohanzlová, L., Jirsová, D., Mazzamuto, M. V., Wauters, L. A., … Modrý, D. (2016). Diversity and host specificity of coccidia (Apicomplexa: Eimeriidae) in native and introduced squirrel species. European Journal of Protistology, 56, 1-14. https://doi.org/10.1016/j.ejop.2016.04.008
Kekäläinen, J., Lai, Y.-T., Vainikka, A., Sirkka, I., & Kortet, R. (2014). Do brain parasites alter host personality? - Experimental study in minnows. Behavioral Ecology and Sociobiology, 68, 197-204. https://doi.org/10.1007/s00265-013-1634-2
Kelly, D. W., Paterson, R. A., Townsend, C. R., Poulin, R., & Tompkins, D. M. (2009). Parasite spillback: A neglected concept in invasion ecology? Ecology, 90, 2047-2056. https://doi.org/10.1890/08-1085.1
Kortet, R., Hedrick, A. V., & Vainikka, A. (2010). Parasitism, predation and the evolution of animal personalities. Ecology Letters, 13, 1449-1458. https://doi.org/10.1111/j.1461-0248.2010.01536.x
Lymbery, A. J., Morine, M., Gholipour Kanani, H., Beatty, S. J., & Morgan, D. L. (2014). Co-invaders: The effects of alien parasites on native hosts. International Journal for Parasitology: Parasites and Wildlife, 3, 171-177. https://doi.org/10.1016/j.ijppaw.2014.04.002
Mathot, K. J., & Dingemanse, N. J. (2015). Energetics and behavior: Unrequited needs and new directions. Trends in Ecology & Evolution, 30, 199-206. https://doi.org/10.1016/j.tree.2015.01.010
Mazzamuto, M. V., Cremonesi, G., Santicchia, F., Preatoni, D. G., Martinoli, A., & Wauters, L. A. (2018). Rodents in the arena: A critical evaluation of methods measuring personality traits. Ethology, Ecology and Evolution, 31, 38-58. https://doi.org/10.1080/03949370.2018.1488768
Paterson, S., & Viney, M. E. (2002). Host immune responses are necessary for density dependence in nematode infections. Parasitology, 125, 283-292. https://doi.org/10.1017/s0031182002002056
Patterson, L. D., & Schulte-Hostedde, A. I. (2011). Behavioural correlates of parasitism and reproductive success in male eastern chipmunks, Tamias striatus. Animal Behaviour, 81, 1129-1137. https://doi.org/10.1016/j.anbehav.2011.02.016
Petkova, I., Abbey-Lee, R. N., & Løvlie, H. (2018). Parasite infection and host personality: Glugea-infected three-spined sticklebacks are more social. Behavioral Ecology and Sociobiology, 72, 173. https://doi.org/10.1007/s00265-018-2586-3
Poirotte, C., Kappeler, P. M., Ngoubangoye, B., Bourgeois, S., Moussodji, M., & Charpentier, M. J. E. (2016). Morbid attraction to leopard urine in Toxoplasma-infected chimpanzees. Current Biology, 26, R83-R101. https://doi.org/10.1016/j.cub.2015.12.020
Poulin, R. (2013). Parasite manipulation of host personality and behavioural syndromes. The Journal of Experimental Biology, 216, 18-26. https://doi.org/10.1242/jeb.073353
Power, A. G., & Mitchell, C. E. (2004). Pathogen spillover in disease epidemics. The American Naturalist, 164(5), S79-S89. https://doi.org/10.1086/424610
R Core Team. (2019). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from https://www.R-project.org/
Réale, D., Reader, S. M., Sol, D., McDougall, P. T., & Dingemanse, N. J. (2007). Integrating animal temperament within ecology and evolution. Biological Reviews, 82, 291-318. https://doi.org/10.1111/j.1469-185X.2007.00010.x
Rhoades, O. K., Best, R. J., & Stachowicz, J. J. (2018). Assessing feeding preferences of a consumer guild: Partitioning variation among versus within species. The American Naturalist, 192, 287-300. https://doi.org/10.1086/698325
Romeo, C., Ferrari, N., Lanfranchi, P., Saino, N., Santicchia, F., Martinoli, A., & Wauters, L. A. (2015). Biodiversity threats from outside to inside: Effects of alien grey squirrel (Sciurus carolinensis) on helminth community of native red squirrel (Sciurus vulgaris). Parasitology Research, 114, 2621-2628. https://doi.org/10.1007/s00436-015-4466-3
Romeo, C., Pisanu, B., Ferrari, N., Basset, F., Tillon, L., Wauters, L. A., … Chapuis, J.-L. (2013). Macroparasite community of the Eurasian red squirrel (Sciurus vulgaris): Poor species richness and diversity. Parasitology Research, 112, 3527-3536. https://doi.org/10.1007/s00436-013-3535-8
Romeo, C., Wauters, L. A., Cauchie, S., Martinoli, A., Matthysen, E., Saino, N., & Ferrari, N. (2014). Faecal egg counts from field experiment reveal density dependence in helminth fecundity: Strongyloides robustus infecting grey squirrels (Sciurus carolinensis). Parasitology Research, 113, 3403-3408. https://doi.org/10.1007/s00436-014-4005-7
Romeo, C., Wauters, L. A., Ferrari, N., Lanfranchi, P., Martinoli, A., Pisanu, B., … Saino, N. (2014). Macroparasite fauna of alien grey squirrels (Sciurus carolinensis): Composition, variability and implications for native species. PLoS ONE, 9, e88002. https://doi.org/10.1371/journal.pone.0088002
Romero, L. M. (2004). Physiological stress in ecology: Lessons from biomedical research. Trends in Ecology & Evolution, 19, 249-255. https://doi.org/10.1016/j.tree.2004.03.008
Rothenburger, J. L., Himsworth, C. G., Nemeth, N. M., Pearl, D. L., Treuting, P. M., & Jardine, J. M. (2019). The devil is in the details-Host disease and co-infections are associated with zoonotic pathogen carriage in Norway rats (Rattus norvegicus). Zoonoses and Public Health, 66, 622-635. https://doi.org/10.1111/zph.12615
Santicchia, F., Dantzer, B., van Kesteren, F., Palme, R., Martinoli, A., Ferrari, N., & Wauters, L. A. (2018). Stress in biological invasions: Introduced invasive grey squirrels increase physiological stress in native Eurasian red squirrels. Journal of Animal Ecology, 87, 1342-1352. https://doi.org/10.1111/1365-2656.12853
Santicchia, F., Romeo, C., Ferrari, N., Matthysen, E., Vanlauwe, L., Wauters, L. A., & Martinoli, A. (2019). The price of being bold? Relationship between personality and endoparasitic infection in a tree squirrel. Mammalian Biology, 97, 1-8. https://doi.org/10.1016/j.mambio.2019.04.007
Santicchia, F., Romeo, C., Martinoli, A., Lanfranchi, P., Wauters, L. A., & Ferrari, N. (2015). Effects of habitat quality on parasite abundance: Do forest fragmentation and food availability affect helminth infection in the Eurasian red squirrel? Journal of Zoology, London, 296, 38-44. https://doi.org/10.1111/jzo.12215
Santicchia, F., Wauters, L. A., Piscitelli, A. P., Van Dongen, S., Martinoli, A., Preatoni, D., … Ferrari, N. (2020). Data from: Spillover of an alien parasite reduces expression of costly behaviour in native host species. Zenodo, https://doi.org/10.5281/zenodo.3693785
Sih, A., Cote, J., Evans, M., Fogarty, S., & Pruitt, J. (2012). Ecological implications of behavioural syndromes. Ecology Letters, 15, 278-289. https://doi.org/10.1016/j.anbehav.2017.09.008
Sorci, G., Skarstein, F., Morand, S., & Hugot, J.-P. (2003). Correlated evolution between host immunity and parasite life histories in primates and oxyurid parasites. Proceedings of the Royal Society of London. Series B: Biological Sciences, 270, 2481-2484. https://doi.org/10.1098/rspb.2003.2536
Strauss, A., White, A., & Boots, M. (2012). Invading with biological weapons: The importance of disease-mediated invasions. Functional Ecology, 26, 1249-1261. https://doi.org/10.1111/1365-2435.12011
Taffs, L. F. (1976). Pinworm infections in laboratory rodents: A review. Laboratory Animals, 10, 1-13. https://doi.org/10.1258/002367776780948862
Tompkins, D. M., Sainsbury, A. W., Nettleton, P., Buxton, D., & Gurnell, J. (2002). Parapoxvirus causes a deleterious disease in red squirrels associated with UK population declines. Proceedings of the Royal Society of London. Series B: Biological Sciences, 269, 529-533. https://doi.org/10.1098/rspb.2001.1897
Tompkins, D. M., White, A. R., & Boots, M. (2003). Ecological replacement of native red squirrels by invasive greys driven by disease. Ecology Letters, 6, 189-196. https://doi.org/10.1046/j.1461-0248.2003.00417.x
VanderWaal, K. L., & Ezenwa, V. O. (2016). Heterogeneity in pathogen transmission: Mechanisms and methodology. Functional Ecology, 30, 1606-1622. https://doi.org/10.1111/1365-2435.12645
Wauters, L. A., & Dhondt, A. A. (1989). Body weight, longevity and reproductive success in red squirrels (Sciurus vulgaris). Journal of Animal Ecology, 58, 637-651. https://doi.org/10.2307/4853
Wauters, L. A., & Dhondt, A. A. (1992). Spacing behaviour of red squirrels, Sciurus vulgaris: Variation between habitats and the sexes. Animal Behaviour, 43, 297-311. https://doi.org/10.1016/S0003-3472(05)80225-8
Wauters, L., Gurnell, J., Martinoli, A., & Tosi, G. (2002). Interspecific competition between native Eurasian red squirrels and alien grey squirrels: Does resource partitioning occur? Behavioral Ecology and Sociobiology, 52, 332-341. https://doi.org/10.1007/s00265-002-0516-9
Wauters, L. A., Mazzamuto, M. V., Santicchia, F., Van Dongen, S., Preatoni, D. G., & Martinoli, A. (2019). Interspecific competition affects the expression of personality traits in natural populations. Scientific Reports, 9, 11189. https://doi.org/10.1038/s41598-019-47694-4
Wauters, L., Tosi, G., & Gurnell, J. (2002). Interspecific competition in tree squirrels: Do introduced grey squirrels (Sciurus carolinensis) deplete tree seeds hoarded by red squirrels (S. vulgaris)? Behavioral Ecology and Sociobiology, 51, 360-367. https://doi.org/10.1007/s00265-001-0446-y
Wauters, L. A., Vermeulen, M., Van Dongen, S., Bertolino, S., Molinari, A., Tosi, G., & Matthysen, E. (2007). Effects of spatio-temporal variation in food supply on red squirrel Sciurus vulgaris body size and body mass and its consequences for some fitness components. Ecography, 30, 51-65. https://doi.org/10.1111/j.2006.0906-7590.04646.x
Wilson, A. J., Réale, D., Clements, M. N., Morrissey, M. M., Postma, E., Walling, C. A., … Nussey, D. H. (2010). An ecologist's guide to the animal model. Journal of Animal Ecology, 79, 13-26. https://doi.org/10.1111/j.1365-2656.2009.01639.x

Auteurs

Francesca Santicchia (F)

Environment Analysis and Management Unit "Guido Tosi Research Group", Department of Theoretical and Applied Sciences, Università degli Studi dell'Insubria, Varese, Italy.

Lucas A Wauters (LA)

Environment Analysis and Management Unit "Guido Tosi Research Group", Department of Theoretical and Applied Sciences, Università degli Studi dell'Insubria, Varese, Italy.
Department of Biology, University of Antwerp, Wilrijk, Belgium.

Anna Pia Piscitelli (AP)

Dipartimento di Biologia e Biotecnologie "Charles Darwin", Università "La Sapienza" di Roma, Rome, Italy.

Stefan Van Dongen (S)

Department of Biology, University of Antwerp, Wilrijk, Belgium.

Adriano Martinoli (A)

Environment Analysis and Management Unit "Guido Tosi Research Group", Department of Theoretical and Applied Sciences, Università degli Studi dell'Insubria, Varese, Italy.

Damiano Preatoni (D)

Environment Analysis and Management Unit "Guido Tosi Research Group", Department of Theoretical and Applied Sciences, Università degli Studi dell'Insubria, Varese, Italy.

Claudia Romeo (C)

Department of Veterinary Sciences and Public Health, Università degli Studi di Milano, Milan, Italy.

Nicola Ferrari (N)

Department of Veterinary Sciences and Public Health, Università degli Studi di Milano, Milan, Italy.

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