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Parasites shape community structure and dynamics in freshwater crustaceans

Published online by Cambridge University Press:  04 November 2019

Olwyn C. Friesen Open the ORCID record for Olwyn C. Friesen [Opens in a new window] ,
Sarah Goellner Open the ORCID record for Sarah Goellner [Opens in a new window] ,
Robert Poulin Open the ORCID record for Robert Poulin [Opens in a new window]  and
Clément Lagrue
Olwyn C. Friesen*
Affiliation:
Department of Zoology, 340 Great King St, University of Otago, Dunedin9016, New Zealand
Sarah Goellner
Affiliation:
Center for Integrative Infectious Diseases, Im Neuenheimer Feld 344, University of Heidelberg, Heidelberg69120, Germany
Robert Poulin
Affiliation:
Department of Zoology, 340 Great King St, University of Otago, Dunedin9016, New Zealand
Clément Lagrue
Affiliation:
Department of Zoology, 340 Great King St, University of Otago, Dunedin9016, New Zealand Department of Biological Sciences, CW 405, Biological Sciences Building, University of Alberta, Edmonton, AlbertaT6G 2E9, Canada
*
Author for correspondence: Olwyn C. Friesen, E-mail: olwynfriesen@gmail.com
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Abstract

Parasites directly and indirectly influence the important interactions among hosts such as competition and predation through modifications of behaviour, reproduction and survival. Such impacts can affect local biodiversity, relative abundance of host species and structuring of communities and ecosystems. Despite having a firm theoretical basis for the potential effects of parasites on ecosystems, there is a scarcity of experimental data to validate these hypotheses, making our inferences about this topic more circumstantial. To quantitatively test parasites' role in structuring host communities, we set up a controlled, multigenerational mesocosm experiment involving four sympatric freshwater crustacean species that share up to four parasite species. Mesocosms were assigned to either of two different treatments, low or high parasite exposure. We found that the trematode Maritrema poulini differentially influenced the population dynamics of these hosts. For example, survival and recruitment of the amphipod Paracalliope fluviatilis were dramatically reduced compared to other host species, suggesting that parasites may affect their long-term persistence in the community. Relative abundances of crustacean species were influenced by parasites, demonstrating their role in host community structure. As parasites are ubiquitous across all communities and ecosystems, we suggest that the asymmetrical effects we observed are likely widespread structuring forces.

Keywords

Host communityparasitespopulation dynamicsspecies composition
Type
Research Article
Information
Parasitology , Volume 147 , Issue 2 , February 2020 , pp. 182 - 193
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Copyright
Copyright © Cambridge University Press 2019

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References

Alizon, S (2013) Co-infection and super-infection models in evolutionary epidemiology. Interface Focus 3, 1–13.CrossRefGoogle ScholarPubMed
Alizon, S, de Roode, JC and Michalakis, Y (2013) Multiple infections and the evolution of virulence. Ecology Letters 16, 556–567.CrossRefGoogle ScholarPubMed
Anderson, RM and May, RM (1981) The population dynamics of microparasites and their invertebrate hosts. Philosophical Transactions of the Royal Society B: Biological Sciences 291, 451–524.Google Scholar
Balmer, O, Stearns, SC, Schötzau, A and Brun, R (2009) Intraspecific competition between co-infecting parasite strains enhances host survival in African trypanosomes. Ecology 90, 3367–3378.CrossRefGoogle ScholarPubMed
Barber, I, Huntingford, FA and Crompton, DWT (1995) The effect of hunger and cestode parasitism on the shoaling decisions of small freshwater fish. Journal of Fish Biology 47, 524–536.CrossRefGoogle Scholar
Begon, M and Bowers, RG (1994) Host-host-pathogen models and microbial pest control: the effect of host self regulation. Journal of Theoretical Biology 169, 275–287.CrossRefGoogle ScholarPubMed
Begon, M, Bowers, RG, Kadianakis, N and Hodgkinson, DE (1992) Disease and community structure: the importance of host self-regulation in a host-host-pathogen model. American Naturalist 139, 1131–1150.CrossRefGoogle Scholar
Bierbower, SM and Sparkes, TC (2007) Parasite-related pairing success in an intermediate host, Caecidotea intermedius (Isopoda): effects of male behavior and reproductive physiology. Journal of Parasitology 93, 445–449.CrossRefGoogle Scholar
Bollache, L, Gambade, G and Cézilly, F (2001) The effects of two acanthocephalan parasites, Pomphorhynchus laevis and Polymorphus minutus, on pairing success in male Gammarus pulex (Crustacea: Amphipoda). Behavioral Ecology and Sociobiology 49, 296–303.CrossRefGoogle Scholar
Bollache, L, Rigaud, T and Cézilly, F (2002) Effects of two acanthocephalan parasites on the fecundity and pairing status of female Gammarus pulex (Crustacea: Amphipoda). Journal of Invertebrate Pathology 79, 102–110.CrossRefGoogle Scholar
Chadderton, WL, Ryan, PA and Winterbourn, MJ (2003) Distribution, ecology, and conservation status of freshwater Idoteidae (Isopoda) in southern New Zealand. Journal of the Royal Society of New Zealand 33, 529–548.CrossRefGoogle Scholar
Chapman, MA, Lewis, MH and Winterboum, MJ (2011) Chapter 11: Amphipoda. In Guide to Freshwater Crustacea of New Zealand. Christchurch, NZ: Freshwater Sciences Society, pp. 132–143.Google Scholar
Coors, A and De Meester, L (2008) Synergistic, antagonistic, and additive effects of multiple stressors: predation threat, parasitism, and pesticide exposure in Daphnia magna. Journal of Applied Ecology 45, 1820–1828.CrossRefGoogle Scholar
de Roode, JC, Culleton, R, Cheesman, SJ, Carter, R and Read, AF (2004) Host heterogeneity is a determinant of competitive exclusion or coexistence in genetically diverse malaria infections. Proceedings of the Royal Society B: Biological Sciences 271, 1073–1080.CrossRefGoogle ScholarPubMed
Esch, GW, Whitfield Gibbosn, J, Bourque, JE, Gibbons, JW and Bourque, JE (1975) An analysis of the relationship between stress and parasitism. American Midland Naturalist 93, 339–353.CrossRefGoogle Scholar
Fredensborg, BL, Mouritsen, KN and Poulin, R (2004) Intensity-dependent mortality of Paracalliope novizealandiae (Amphipoda: Crustacea) infected by a trematode: experimental infections and field observations. Journal of Experimental Marine Biology and Ecology 311, 253–265.CrossRefGoogle Scholar
Friesen, OC, Poulin, R and Lagrue, C (2017) Differential impacts of shared parasites on fitness components among competing hosts. Ecology and Evolution 7, 4682–4693.CrossRefGoogle ScholarPubMed
Friesen, OC, Poulin, R and Lagrue, C (2018) Parasite-mediated microhabitat segregation between congeneric hosts. Biology Letters 14, 20170671.CrossRefGoogle ScholarPubMed
Goellner, S, Selbach, C and Friesen, OC (2018) Do behavioural defence mechanisms explain different levels of trematode infections in congeneric hosts? Journal of Helminthology 93, 379–382.CrossRefGoogle ScholarPubMed
Gotelli, NJ and Ellison, AM (2004) The analysis of multivariate data. In Andrew D. Sinauer (ed) A Primer of Ecological Statistics. Sunderland, MA: Sinauer Associates Inc, pp. 383–446.Google Scholar
Goulson, D, Nicholls, E, Botías, C and Rotheray, EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347, 1255957.CrossRefGoogle ScholarPubMed
Greenman, JV and Hudson, PJ (1999) Host exclusion and coexistence in apparent and direct competition: an application of bifurcation theory. Theoretical Population Biology 56, 48–64.CrossRefGoogle ScholarPubMed
Greenman, JV and Hudson, PJ (2000) Parasite-mediated and direct competition in a two-host shared macroparasite system. Theoretical Population Biology 57, 13–34.CrossRefGoogle Scholar
Grunberg, RL and Sukhdeo, MVK (2017) Temporal community structure in two gregarines (Rotundula gammari and Heliospora longissima) co-infecting the amphipod Gammarus fasciatus. Journal of Parasitology 103, 6–13.CrossRefGoogle ScholarPubMed
Hatcher, MJ and Dunn, AM (2011) Parasites and Competitors, 1st Edn.Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Hatcher, MJ, Dick, JTA and Dunn, AM (2012) Diverse effects of parasites in ecosystems: linking interdependent processes. Frontiers in Ecology and the Environment 10, 186–194.CrossRefGoogle Scholar
Hatcher, MJ, Dick, JTA and Dunn, AM (2014) Parasites that change predator or prey behaviour can have keystone effects on community composition. Biology Letters 10, 20130879–20130879.CrossRefGoogle ScholarPubMed
Hay, KB, Fredensborg, BL and Poulin, R (2005) Trematode-induced alterations in shell shape of the mud snail Zeacumantus subcarinatus (Prosobranchia: Batillariidae). Journal of the Marine Biological Association of the United Kingdom 85, 989–992.CrossRefGoogle Scholar
Hechinger, RF (2012) Faunal survey and identification key for the trematodes (Platyhelminthes: Digenea) infecting Potamopyrgus antipodarum (Gastropoda: Hydrobiidae) as first intermediate host. Zootaxa 27, 1–27.CrossRefGoogle Scholar
Hine, PM (1977) Acanthocephalus galaxii n.sp. Parasitic in Galaxias maculatus (Jenyns, 1842) in the Waimeha Stream, New Zealand. Journal of the Royal Society of New Zealand 7, 51–57.CrossRefGoogle Scholar
Holt, RD (1977) Predation, apparent competition, and the structure of prey communities. Theoretical Population Biology 229, 197–229.CrossRefGoogle Scholar
Holt, RD and Pickering, J (1985) Infectious disease and species coexistence: a model of Lotka-Volterra Form. American Naturalist 126, 196–211.CrossRefGoogle Scholar
Holt, RD and Lawton, JH (1994) The ecological consequences of shared natural enemies. Annual Review of Ecology and Systematics 25, 495–520.CrossRefGoogle Scholar
Holton, AL (1984) Progenesis as a means of abbreviating life histories in two New Zealand trematodes, Coitocaecum parvum Crawcroft, 1945 and Stegodexamene anguillae MacFarlane, 1951. Mauri Ora 11, 63–70.Google Scholar
Hudson, PJ and Greenman, JV (1998) Competition mediated by parasites: biological and theoretical progress. Trends in Ecology & Evolution 13, 387–390.CrossRefGoogle ScholarPubMed
Hudson, PJ, Dobson, AP and Lafferty, KD (2006) Is a healthy ecosystem one that is rich in parasites? Trends in Ecology & Evolution 21, 381–385.CrossRefGoogle Scholar
Hughes, WOH and Boomsma, JJ (2004) Let your enemy do the work: within-host interactions between two fungal parasites of leaf-cutting ants. Proceedings of the Royal Society B: Biological Sciences 271, S104–S106.CrossRefGoogle ScholarPubMed
Hunter, MD and Price, PW (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73, 724–732.Google Scholar
Jaenike, J (1995) Interactions between mycophagous Drosophila and their nematode parasites: from physiological to community ecology. Oikos 72, 235–244.CrossRefGoogle Scholar
Kiesecker, JM and Blaustein, AR (1999) Pathogen reverses competition between larval amphibians. Ecology 80, 2442–2448.CrossRefGoogle Scholar
Klein, SL (2005) Parasite manipulation of host behavior: mechanisms, ecology, and future directions. Behavioural Processes 68, 219–221.CrossRefGoogle ScholarPubMed
Kunz, AK and Pung, OJ (2004) Effects of Microphallus turgidus (Trematoda: Microphallidae) on the predation, behavior, and swimming stamina of the grass shrimp Palaemonetes pugio. Journal of Parasitology 90, 441–445.CrossRefGoogle ScholarPubMed
Lafferty, KD and Kuris, AM (1999) How environmental stress affects the impacts of parasites. Limnology and Oceanography 44, 925–931.CrossRefGoogle Scholar
Lafferty, KD, Allesina, S, Arim, M, Briggs, CJ, De Leo, G, Dobson, AP, Dunne, JA, Johnson, PTJ, Kuris, AM, Marcogliese, DJ, Martinez, ND, Memmott, J, Marquet, PA, McLaughlin, JP, Mordecai, EA, Pascual, M, Poulin, R and Thieltges, DW (2008) Parasites in food webs: the ultimate missing links. Ecology Letters 11, 533–546.CrossRefGoogle ScholarPubMed
Lagrue, C and Poulin, R (2007) Life cycle abbreviation in the trematode Coitocaecum parvum: can parasites adjust to variable conditions? Journal of Evolutionary Biology 20, 1189–1195.CrossRefGoogle ScholarPubMed
Lagrue, C and Poulin, R (2008) Intra- and interspecific competition among helminth parasites: effects on Coitocaecum parvum life history strategy, size and fecundity. International Journal for Parasitology 38, 1435–1444.CrossRefGoogle ScholarPubMed
Lagrue, C and Poulin, R (2015) Local diversity reduces infection risk across multiple freshwater host-parasite associations. Freshwater Biology 60, 2445–2454.CrossRefGoogle Scholar
Lagrue, C, Kaldonski, N, Perrot-Minnot, MJ, Motreuil, S and Bollache, L (2007) Modification of hosts’ behavior by a parasite: field evidence for adaptive manipulation. Ecology 88, 2839–2847.CrossRefGoogle ScholarPubMed
Lagrue, C, Poulin, R and Cohen, JE (2015) Parasitism alters three power laws of scaling in a metazoan community: Taylor's law, density-mass allometry, and variance-mass allometry. Proceedings of the National Academy of Sciences 112, 1791–1796.CrossRefGoogle Scholar
Lange, B, Reuter, M, Ebert, D, Muylaert, K and Decaestecker, E (2014) Diet quality determines interspecific parasite interactions in host populations. Ecology and Evolution 4, 3093–3102.CrossRefGoogle ScholarPubMed
Larsen, MH, Jensen, KT and Mouritsen, KN (2011) Climate influences parasite-mediated competitive release. Parasitology 138, 1436–1441.CrossRefGoogle ScholarPubMed
Lefèbvre, F, Fredensborg, BL, Armstrong, A, Hansen, EK and Poulin, R (2005) Assortative pairing in the amphipod Paracalliope fluviatilis: a role for parasites? Hydrobiologia 545, 65–73.CrossRefGoogle Scholar
Lefèvre, T, Lebarbenchon, C, Gauthier-Clerc, M, Missé, D, Poulin, R and Thomas, F (2009) The ecological significance of manipulative parasites. Trends in Ecology & Evolution 24, 41–48.CrossRefGoogle ScholarPubMed
Luque, JL, Vieira, FM, Herrmann, K, King, TM, Poulin, R and Lagrue, C (2010) New evidence on a cold case: trophic transmission, distribution and host-specificity in Hedruris spinigera (Nematoda: Hedruridae). Folia Parasitologica 57, 223–231.CrossRefGoogle Scholar
MacNeil, C, Fielding, NJ, Dick, JTA, Briffa, M, Prenter, J, Hatcher, MJ and Dunn, AM (2003) An acanthocephalan parasite mediates intraguild predation between invasive and native freshwater amphipods (Crustacea). Freshwater Biology 48, 2085–2093.CrossRefGoogle Scholar
Médoc, V, Rigaud, T, Bollache, L and Beisel, JN (2009) A manipulative parasite increasing an antipredator response decreases its vulnerability to a nonhost predator. Animal Behaviour 77, 1235–1241.CrossRefGoogle Scholar
Médoc, V, Firmat, C, Sheath, DJ, Pegg, J, Andreou, D and Britton, JR (2017) Parasites and biological invasions: predicting ecological alterations at levels from individual hosts to whole networks. In Advances in Ecological Research, Academic Press., pp. 1–54. doi: 10.1016/bs.aecr.2016.10.003.Google Scholar
Mikheev, VN, Pasternak, AF, Taskinen, J and Valtonen, ET (2010) Parasite-induced aggression and impaired contest ability in a fish host. Parasites & Vectors 3, 1–8.CrossRefGoogle Scholar
Morley, NJ (2012) Cercariae (Platyhelminthes: Trematoda) as neglected components of zooplankton communities in freshwater habitats. Hydrobiologia 691, 7–19.CrossRefGoogle Scholar
Mouritsen, KN and Poulin, R (2003) Parasite-induced trophic facilitation exploited by a non-host predator: a manipulator's nightmare. International Journal for Parasitology 33, 1043–1050.CrossRefGoogle ScholarPubMed
Mouritsen, KN and Poulin, R (2005) Parasites boosts biodiversity and changes animal community structure by trait-mediated indirect effects. Oikos 108, 344–350.CrossRefGoogle Scholar
Park, T (1948) Interspecies competition in populations of Tribolium confusum Duval and Tribolium castaneum Herbst. Ecological Monographs 18, 265–307.CrossRefGoogle Scholar
Pedersen, AB and Fenton, A (2007) Emphasizing the ecology in parasite community ecology. Trends in Ecology & Evolution 22, 133–139.CrossRefGoogle ScholarPubMed
Poulin, R (1995) ‘Adaptive’ changes in the behaviour of parasitized animals: a critical review. International Journal for Parasitology 25, 1371–1383.CrossRefGoogle Scholar
Poulin, R (2001) Progenesis and reduced virulence as an alternative transmission strategy in a parasitic trematode. Parasitology 123, 623–630.CrossRefGoogle Scholar
Presswell, B, Blasco-Costa, I and Kostadinova, A (2014) Two new species of Maritrema nicoll, 1907 (Digenea: Microphallidae) from New Zealand: morphological and molecular characterisation. Parasitology Research 113, 1641–1656.CrossRefGoogle ScholarPubMed
Price, PW, Westoby, M, Rice, B, Atsatt, PR, Fritz, RS, Thompson, JN and Mobley, K (1986) Parasite mediation in ecological interactions. Annual Review of Ecology and Systematics 17, 487–505.CrossRefGoogle Scholar
Rabajante, JF, Tubay, JM, Uehara, T, Morita, S, Ebert, D and Yoshimura, J (2015) Red Queen dynamics in multi-host and multi-parasite interaction system. Scientific Reports 5, 1–7.CrossRefGoogle ScholarPubMed
Rauque, CA, Paterson, RA, Poulin, R and Tompkins, DM (2011) Do different parasite species interact in their effects on host fitness? A case study on parasites of the amphipod Paracalliope fluviatilis. Parasitology 138, 1176–1182.CrossRefGoogle ScholarPubMed
Read, AF (1988) Sexual selection and the role of parasites. Trends in Ecology & Evolution 3, 97–102.CrossRefGoogle ScholarPubMed
Reisinger, LS and Lodge, DM (2016) Parasites alter freshwater communities in mesocosms by modifying invasive crayfish behavior. Ecology 97, 1497–1506.CrossRefGoogle ScholarPubMed
Reisinger, LS, Petersen, I, Hing, JS, Davila, RL and Lodge, DM (2015) Infection with a trematode parasite differentially alters competitive interactions and antipredator behaviour in native and invasive crayfish. Freshwater Biology 60, 1581–1595.CrossRefGoogle Scholar
Rivero, A and Ferguson, HM (2003) The energetic budget of Anopheles stephensi infected with Plasmodium chabaudi: is energy depletion a mechanism for virulence? Proceedings of the Royal Society B: Biological Sciences 270, 1365–1371.CrossRefGoogle ScholarPubMed
Roitberg, BD, Boivin, G and Vet, LEM (2001) Fitness, parasitoids, and biological control: an opinion. The Canadian Entomologist 133, 429–438.CrossRefGoogle Scholar
Ruiz-Daniels, R, Beltran, S, Poulin, R and Lagrue, C (2012) Do parasites adopt different strategies in different intermediate hosts? Host size, not host species, influences Coitocaecum parvum (Trematoda) life history strategy, size and egg production. Parasitology 140, 1–9.Google Scholar
SAS Institute Inc (2015) JMP 12. SAS Institute., Cary, North Carolina.Google Scholar
Schall, JJ (1992) Parasite-mediated competition in Anolis lizards. Oecologia 92, 58–64.CrossRefGoogle ScholarPubMed
Seppälä, O and Jokela, J (2008) Host manipulation as a parasite transmission strategy when manipulation is exploited by non-host predators. Biology Letters 4, 663–666.CrossRefGoogle ScholarPubMed
Seppälä, O, Valtonen, ET and Benesh, DP (2008) Host manipulation by parasites in the world of dead-end predators: adaptation to enhance transmission? Proceedings of the Royal Society B: Biological Sciences 275, 1611–1615.CrossRefGoogle ScholarPubMed
Sieber, M, Malchow, H and Hilker, FM (2013) Disease-induced modification of prey competition in eco-epidemiological models. Ecological Complexity 18, 74–82.CrossRefGoogle Scholar
Sparkes, TC, Weil, KA, Renwick, DT and Talkington, JA (2006) Development-related effects of an acanthocephalan parasite on pairing success of its intermediate host. Animal Behaviour 71, 439–448.CrossRefGoogle Scholar
Sutcliffe, DWDW (1992) Reproduction in Gammarus (crustacea, Amphipoda): basic processes. Freshwater Forum 2, 102–128.Google Scholar
Thieltges, DW, Amundsen, PA, Hechinger, RF, Johnson, PTJ, Lafferty, KD, Mouritsen, KN, Preston, DL, Reise, K, Zander, CD and Poulin, R (2013) Parasites as prey in aquatic food webs: implications for predator infection and parasite transmission. Oikos 122, 1473–1482.Google Scholar
Thomas, F, Renaud, F, Demee, T and Poulin, R (1998) Manipulation of host behaviour by parasites: ecosystem engineering in the intertidal zone? Proceedings of the Royal Society B: Biological Sciences 265, 1091–1096.CrossRefGoogle Scholar
Thomas, F, Poulin, R, De Meeüs, T, Guégan, J and Renaud, F (1999) Parasites and ecosystem engineering: what roles could they play? Oikos 84, 167–171.CrossRefGoogle Scholar
Thompson, SN, Redak, RA and Wang, L-W (2001) Altered dietary nutrient intake maintains metabolic homeostasis in parasitized larvae of the insect Manduca sexta L. Journal of Experimental Biology 204, 4065–4080.Google ScholarPubMed
Thomas, F, Adamo, S and Moore, J (2005) Parasitic manipulation: where are we and where should we go? Behavioural Processes 68, 185–199.CrossRefGoogle Scholar
Thumbi, SM, Bronsvoort, BMDC, Poole, EJ, Kiara, H, Toye, PG, Mbole-Kariuki, MN, Conradie, I, Jennings, A, Handel, IG, Coetzer, JAW, Steyl, JCA, Hanotte, O and Woolhouse, MEJ (2014) Parasite co-infections and their impact on survival of indigenous cattle. PLoS One 9, e76324.CrossRefGoogle ScholarPubMed
Tompkins, DM, Draycott, RAH and Hudson, PJ (2000) Field evidence for apparent competition mediated via the shared parasites of two gamebird species. Ecology Letters 3, 10–14.CrossRefGoogle Scholar
Tompkins, DM, Greenman, JV and Hudson, PJ (2001) Differential impact of a shared nematode parasite on two gamebird hosts: implications for apparent competition. Parasitology 122, 187–193.CrossRefGoogle ScholarPubMed
Vannatta, JT and Minchella, DJ (2018) Parasites and their impact on ecosystem nutrient cycling. Trends in Parasitology 34, 452–455.CrossRefGoogle ScholarPubMed
Vivas Muñoz, JC, Staaks, G and Knopf, K (2017) The eye fluke Tylodelphys clavata affects prey detection and intraspecific competition of European perch (Perca fluviatilis). Parasitology Research 116, 2561–2567.CrossRefGoogle Scholar
Weinstein, S, Titcomb, G, Agwanda, B, Riginos, C and Young, H (2017) Parasite responses to large mammal loss in an African savanna. Ecology 98, 1839–1848.CrossRefGoogle Scholar
Wood, CL, Byers, JE, Cottingham, KL, Altman, I, Donahue, MJ and Blakeslee, AMH (2007) Parasites alter community structure. Proceedings of the National Academy of Sciences 104, 9335–9339.CrossRefGoogle ScholarPubMed
Yan, G (1996) Parasite-mediated competition: a model of directly transmitted macroparasites. American Naturalist 148, 1089–1112.CrossRefGoogle Scholar
Yan, G and Stevens, L (1995) Selection by parasites on components of fitness in Tribolium beetles – the effect of intraspecific competition. American Naturalist 146, 795–813.CrossRefGoogle Scholar
Zohar, S and Holmes, JC (1998) Pairing success of male Gammarus lacustris infected by two acanthocephalans: a comparative study. Behavioral Ecology 9, 206–211.CrossRefGoogle Scholar
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