×

Parasitism effects on coexistence and stability within simple trophic modules. (English) Zbl 1406.92682

Summary: Parasites are important components of food webs. Although their direct effects on hosts are well-studied, indirect impacts on trophic networks, thus on non-host species, remain unclear. In this study, we investigate the consequences of parasitism on coexistence and stability within a simple trophic module: one predator consuming two prey species in competition. We test how such effects depend on the infected species (prey or predator). We account for two effects of parasitism: the virulence effect (parasites affect the infected species intrinsic growth rate through direct effects on fecundity or mortality) and the interaction effect (increased vulnerability of infected prey or increased food intake of infected predators). Results show that coexistence is favored when effects have intermediate intensity. We link this result to modifications of direct and apparent competitions among prey species. Given a prey infection, accounting for susceptible-infected population structure highlights that coexistence may also be reduced due to predator-parasite competition. Parasites affect stability by modulating energy transfer from prey to predator. Predator infection therefore has a stabilizing effect due to increased energy fluxes and/or predator mortality. Our results suggest that parasites potentially increase species coexistence. Precise predictions however require an assessment of various parasite effects. We discuss the implications of our results for the functioning of trophic networks.

MSC:

92D40 Ecology
92D25 Population dynamics (general)
92D30 Epidemiology

References:

[1] Amundsen, P.-A.; Lafferty, K. D.; Knudsen, R.; Primicerio, R.; Klemetsen, A.; Kuris, A. M., Food web topology and parasites in the pelagic zone of a subarctic lake, J. Anim. Ecol., 78, 563-572 (2009)
[2] Anderson, R. M.; May, R. M., Regulation and stability of host-parasite population interactions: i. regulatory processes, J. Anim. Ecol., 47, 219-247 (1978)
[3] Anderson, R. M.; May, R. M., The invasion, persistence and spread of infectious diseases within animal and plant communities, Philos. Trans. R. Soc. B Biol. Sci., 314, 533-570 (1986)
[4] Bairagi, N.; Adak, D., Complex dynamics of a predator-prey-parasite system: an interplay among infection rate, predator’s reproductive gain and preference, Ecol. Complex., 22, 1-12 (2015)
[5] Banerji, A.; Duncan, A. B.; Griffin, J. S.; Humphries, S.; Petchey, O. L.; Kaltz, O., Density- and trait-mediated effects of a parasite and a predator in a tri-trophic food web, J. Anim. Ecol., 84, 723-733 (2015)
[6] Bernot, R. J.; Lamberti, G. A., Indirect effects of a parasite on a benthic community: an experiment with trematodes, snails and periphyton, Freshwater Biol., 53, 322-329 (2008)
[7] Bethel, W. M.; Holmes, J. C., Increased vulnerability of amphipods to predation owing to altered behavior induced by larval acanthocephalans, Can. J. Zool., 55, 110-115 (1977)
[8] Buck, J. C.; Ripple, W. J., Infectious agents trigger trophic cascades, Trends Ecol. Evol., 32, 681-694 (2017)
[9] Cáceres, C. E.; Davis, G.; Duple, S.; Hall, S. R.; Koss, A.; Lee, P.; Rapti, Z., Complex Daphnia interactions with parasites and competitors, Math. Biosci., 258, 148-161 (2014) · Zbl 1314.92122
[10] Callaway, R. M.; Pennings, S. C., Impact of a parasitic plant on the zonation of two salt marsh perennials, Oecologia, 114, 100-105 (1998)
[11] Case, T. J., An Illustrated Guide to Theoretical Ecology (2000), Oxford University Press: Oxford University Press New York
[12] Cézilly, F.; Thomas, F.; Médoc, V.; Perrot-Minnot, M.-J., Host-manipulation by parasites with complex life cycles: adaptive or not?, Trends Parasitol., 26, 311-317 (2010)
[13] Coors, A.; De Meester, L., Fitness and virulence of a bacterial endoparasite in an environmentally stressed crustacean host, Parasitology, 138, 122-131 (2011)
[14] Decaestecker, E.; Vergote, A.; Ebert, D.; De Meester, L., Evidence for strong host clone-parasite species interactions in the daphnia microparasite system, Evolution (N. Y)., 57, 784-792 (2003)
[15] Decaestecker, E.; Verreydt, D.; De Meester, L.; Declerck, S. A.J., Parasite and nutrient enrichment effects on Daphnia interspecific competition, Ecology, 96, 1421-1430 (2015)
[16] Dick, J. T.A.; Armstrong, M.; Clarke, H. C.; Farnsworth, K. D.; Hatcher, M. J.; Ennis, M.; Kelly, A.; Dunn, A. M., Parasitism may enhance rather than reduce the predatory impact of an invader, Biol. Lett., 6, 636-638 (2010)
[17] Dobson, A. P., Population dynamics of pathogens with multiple host species, Am. Nat., 164, S64-S78 (2004)
[18] Dobson, A. P.; Crawley, M., Pathogens and the structure of plant communities, Trends Ecol. Evol., 9, 393-398 (1994)
[19] Duffy, M. A.; Hall, S. R.; Tessier, A. J.; Huebner, M., Selective predators and their parasitized prey: are epidemics in zooplankton under top-down control?, Limnol. Oceanogr., 50, 412-420 (2005)
[21] Gehman, A.-L. M.; Byers, J. E., Non-native parasite enhances susceptibility of host to native predators, Oecologia, 183, 919-926 (2017)
[22] Gerber, L. R.; McCallum, H.; Lafferty, K. D.; Sabo, J. L.; Dobson, A., Exposing extinction risk analysis to pathogens: is diesase just another form of density dependence?, Ecol. Appl., 15, 1402-1414 (2005)
[23] Goren, L.; Ben-Ami, F., To eat or not to eat infected food: a bug’s dilemma, Hydrobiologia, 798, 25-32 (2017)
[24] Grenfell, B. T., Parasitism and the dynamics of ungulate grazing systems, Am. Nat., 139, 907-929 (1992)
[25] Hall, S. R.; Becker, C. R.; Cáceres, C. E., Parasitic castration: a perspective from a model of dynamic energy budgets, Integr. Comp. Biol., 47, 295-309 (2007)
[26] Hartley, L. M.; Detling, J. K.; Savage, L. T., Introduced plague lessens the effects of an herbivorous rodent on grassland vegetation, J. Appl. Ecol., 46, 861-869 (2009)
[27] Hatcher, M. J.; Dick, J. T.a; Dunn, A. M., Parasites that change predator or prey behaviour can have keystone effects on community composition, Biol. Lett., 10, Article 20130879 pp. (2014)
[28] Hatcher, M. J.; Dick, J. T.A.; Dunn, A. M., How parasites affect interactions between competitors and predators, Ecol. Lett., 9, 1253-1271 (2006)
[29] Hatcher, M. J.; Dunn, A. M., Parasites in Ecological Communities (2011), Cambridge University Press: Cambridge University Press Cambridge
[30] Hethcote, H. W.; Wang, W.; Han, L.; Ma, Z., A predator - prey model with infected prey, Theor. Popul. Biol., 66, 259-268 (2004)
[31] Hilker, F. M.; Schmitz, K., Disease-induced stabilization of predator-prey oscillations, J. Theor. Biol., 255, 299-306 (2008) · Zbl 1400.92487
[32] Holt, R. D., Predation, apparent competition, and the structure of prey communities, Theor. Popul. Biol., 12, 197-229 (1977)
[33] Holt, R. D.; Grover, J.; Tilman, D., Simple rules for interspecific dominance in systems with exploitative and apparent competition, Am. Nat., 144, 741-771 (1994)
[34] Holt, R. D.; Pickering, J., Infectious disease and species coexistence: a model of lotka-volterra form, Am. Nat., 126, 196-211 (1985)
[35] Hudson, P. J.; Dobson, A. P.; Lafferty, K. D., Is a healthy ecosystem one that is rich in parasites?, Trends Ecol. Evol., 21, 381-385 (2006)
[36] Hudson, P. J.; Dobson, A. P.; Newborn, D., Do parasites make prey vulnerable to predation? Red grouse and parasites, J. Anim. Ecol., 61, 681 (1992)
[37] Hudson, P. J.; Dobson, A. P.; Newborn, D., Prevention of population cycles by parasite removal, Science, 282, 2256-2258 (1998)
[38] Hutson, V.; Vickers, G. T., A criterion for permanent coexistence of species, with an application to a two-prey one-predator system, Math. Biosci., 63, 253-269 (1983) · Zbl 0524.92023
[39] Ives, A. R.; Murray, D. L., Can sublethal parasitism destabilize predator-prey population dynamics? A model of snowshoe hares, predators and parasites, J. Anim. Ecol., 66, 265-278 (1997)
[40] Jacquin, L.; Mori, Q.; Médoc, V., Does the carotenoid-based colouration of Polymorphus minutus facilitate its trophic transmission to definitive hosts?, Parasitology, 140, 1310-1315 (2013)
[41] Kermack, W. O.; McKendrick, A. G., A contribution to the mathematical theory of epidemics, Proc. R. Soc. A Math. Phys. Eng. Sci., 115, 700-721 (1927) · JFM 53.0517.01
[42] Khokhlova, I. S.; Krasnov, B. R.; Kam, M.; Burdelova, N. I.; Degen, A. A., Energy cost of ectoparasitism: the flea Xenopsylla ramesis on the desert gerbil Gerbillus dasyurus, J. Zool., 258, 349-354 (2002)
[43] Kiesecker, J. M.; Blaustein, A. R., Pathogen reverses competition between larval amphibians, Ecology, 80, 2442-2448 (1999)
[44] Kuris, A. M.; Hechinger, R. F.; Shaw, J. C.; Whitney, K. L.; Aguirre-Macedo, L.; Boch, C. A.; Dobson, A. P.; Dunham, E. J.; Fredensborg, B. L.; Huspeni, T. C.; Lorda, J.; Mababa, L.; Mancini, F. T.; Mora, A. B.; Pickering, M.; Talhouk, N. L.; Torchin, M. E.; Lafferty, K. D., Ecosystem energetic implications of parasite and free-living biomass in three estuaries, Nature, 454, 515-518 (2008)
[45] Lafferty, K. D., Fishing for lobsters indirectly increases epidemics in sea urchins, Ecol. Appl., 14, 1566-1573 (2004)
[46] Lafferty, K. D.; Allesina, S.; Arim, M.; Briggs, C. J.; De Leo, G.; Dobson, A. P.; Dunne, J. A.; Johnson, P. T.J.; Kuris, A. M.; Marcogliese, D. J.; Martinez, N. D.; Memmott, J.; Marquet, P. A.; McLaughlin, J. P.; Mordecai, E. A.; Pascual, M.; Poulin, R.; Thieltges, D. W., Parasites in food webs: the ultimate missing links, Ecol. Lett., 11, 533-546 (2008)
[47] Lefèvre, T.; Lebarbenchon, C.; Gauthier-Clerc, M.; Missé, D.; Poulin, R.; Thomas, F., The ecological significance of manipulative parasites, Trends Ecol. Evol., 24, 41-48 (2009)
[48] Lettini, S. E.; Sukhdeo, M. V.K., The energetic cost of parasitism in isopods, Ecoscience, 17, 1-8 (2010)
[49] Lindström, E. R.; Andrén, H.; Angelstam, P.; Cederlund, G.; Hörnfeldt, B.; Jäderberg, L.; Lemnell, P.; Martinsson, B.; Sköld, K.; Swenson, J. E., Disease reveals the predator: sarcoptic mange, red fox predation, and prey populations, Ecology, 75, 1042-1049 (1994)
[50] May, R. M.; Anderson, R. M., Regulation and stability of host-parasite population interactions: II. Destabilizing processes, J. Anim. Ecol., 47, 249-267 (1978)
[51] McCann, K. S.; Hastings, A.; Huxel, G. R., Weak trophic interactions and the balance of nature, Nature, 395, 794-798 (1998)
[52] Ong, T. W.Y.; Vandermeer, J. H., Coupling unstable agents in biological control, Nat. Commun., 6, 5991 (2015)
[53] Packer, C.; Holt, R. D.; Hudson, P. J.; Lafferty, K. D.; Dobson, A. P., Keeping the herds healthy and alert: implications of predator control for infectious disease, Ecol. Lett., 6, 797-802 (2003)
[54] Park, T., Interspecies competition in populations of trilobium confusum duval and trilobium castaneum herbst, Ecol. Monogr., 18, 265-307 (1948)
[55] Peterson, R. O.; Page, R. E., The Rise and fall of isle royale wolves, 1975-1986, J. Mammal., 69, 89-99 (1988)
[56] Poulin, R., Parasite manipulation of host behavior, Advances in the Study of Behavior (2010), Elsevier Inc
[57] Poulin, R.; Maure, F., Host manipulation by parasites: a look back before moving forward, Trends Parasitol., 31, 563-570 (2015)
[58] Price, P. W.; Westoby, M.; Rice, B., Parasite-mediated competition: some predictions and tests, Am. Nat., 131, 544-555 (1988)
[59] Rip, J. M.K.; McCann, K. S., Cross-ecosystem differences in stability and the principle of energy flux, Ecol. Lett., 14, 733-740 (2011)
[60] Rosenzweig, M. L., Paradox of enrichment: destabilization of exploitation ecosystems in ecological time, Science, 171, 385-387 (1971)
[61] Schall, J. J., Parasite-mediated competition in Anolis lizards, Oecologia, 92, 58-64 (1992)
[62] Schwartz, S. S.; Cameron, G. N., How do parasites cost their hosts? Preliminary answers from trematodes and Daphnia obtusa, Limnol. Oceanogr., 38, 602-612 (1993)
[63] Sieber, M.; Hilker, F. M., Prey, predators, parasites: intraguild predation or simpler community modules in disguise?, J. Anim. Ecol., 80, 414-421 (2011)
[64] Thomas, F.; Poulin, R.; Brodeur, J., Host manipulation by parasites: a multidimensional phenomenon, Oikos, 119, 1217-1223 (2010)
[65] Tompkins, D. M.; Dunn, A. M.; Smith, M. J.; Telfer, S., Wildlife diseases: from individuals to ecosystems, J. Anim. Ecol., 80, 19-38 (2011)
[66] Welch, K. D.; Harwood, J. D., Predator-pathogen interactions: synergy between mortality causes and failure of the healthy herds hypothesis, Funct. Ecol., 25, 943-944 (2011)
[67] Wilmers, C. C.; Post, E.; Peterson, R. O.; Vucetich, J. A., Predator disease out-break modulates top-down, bottom-up and climatic effects on herbivore population dynamics, Ecol. Lett., 9, 383-389 (2006)
[68] Wood, C. L.; Byers, J. E.; Cottingham, K. L.; Altman, I.; Donahue, M. J.; Blakeslee, A. M.H., Parasites alter community structure, Proc. Natl. Acad. Sci., 104, 9335-9339 (2007)
[69] Wood, C. L.; Johnson, P. T.J., A world without parasites: exploring the hidden ecology of infection, Front. Ecol. Environ., 13, 425-434 (2015)
[70] Wright, H. A.; Wootton, R. J.; Barber, I., The effect of Schistocephalus solidus infection on meal size of three-spined stickleback, J. Fish Biol., 68, 801-809 (2006)
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. In some cases that data have been complemented/enhanced by data from zbMATH Open. This attempts to reflect the references listed in the original paper as accurately as possible without claiming completeness or a perfect matching.