Larval size in acanthocephalan parasites: Influence of intraspecific competition and effects on intermediate host behavioural changes

Particle and Fibre Toxicology

Thierry Rigaud²  Nathalie Franceschi²  Clément Lagrue¹  Loïc Bollache²  Lucile Dianne² 

[1] Present address: Department of Zoology, University of Otago, P.O. Box 56, Dunedin, 9054, New Zealand;Equipe Ecologie Evolutive, UMR CNRS 6282 Biogéosciences, Université de Bourgogne, 6 Boulevard Gabriel, 21000, Dijon, France

关键词: Phototaxis;    Host behavioural manipulation;    Parasite larval size;    Intraspecific competition;    Gammarus pulex;    Pomphorhynchus laevis;   

Others  :  1231723
DOI  :  10.1186/1756-3305-5-166

 received in 2012-07-09, accepted in 2012-07-31,  发布年份 2012

【 摘 要 】

Background

Parasites often face a trade-off between exploitation of host resources and transmission probabilities to the next host. In helminths, larval growth, a major component of adult parasite fitness, is linked to exploitation of intermediate host resources and is influenced by the presence of co-infecting conspecifics. In manipulative parasites, larval growth strategy could also interact with their ability to alter intermediate host phenotype and influence parasite transmission.

Methods

We used experimental infections of Gammarus pulex by Pomphorhynchus laevis (Acanthocephala), to investigate larval size effects on host behavioural manipulation among different parasite sibships and various degrees of intra-host competition.

Results

Intra-host competition reduced mean P. laevis cystacanth size, but the largest cystacanth within a host always reached the same size. Therefore, all co-infecting parasites did not equally suffer from intraspecific competition. Under no intra-host competition (1 parasite per host), larval size was positively correlated with host phototaxis. At higher infection intensities, this relationship disappeared, possibly because of strong competition for host resources, and thus larval growth, and limited manipulative abilities of co-infecting larval acanthocephalans.

Conclusions

Our study indicates that behavioural manipulation is a condition-dependant phenomenon that needs the integration of parasite-related variables to be fully understood.

【 授权许可】

   
2012 Dianne et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Rosen R, Dick TA: Development and infectivity of the procercoid of Triaenophorus crassus Forel and mortality of the first intermediate host. Can J Zool 1983, 61:2120-2128.
• [2]Steinauer ML, Nickol BB: Effect of cystacanth body size on adult success. J Parasitol 2003, 89:251-254.
• [3]Benesh DP, Hafer N: Growth and ontogeny of the tapeworm Schistocephalus solidus in its copepod first host affects performance in its stickleback second intermediate host. Parasit Vectors 2012, 5:90. BioMed Central Full Text
• [4]Fredensborg BL, Poulin R: Larval helminths in intermediate hosts: Does competition early in life determine the fitness of adult parasites? Int J Parasitol 2005, 35:1061-1070.
• [5]Lafferty KD, Kuris AM: Trophic strategies, animal diversity and body size. Trends Ecol Evol 2002, 17:507-513.
• [6]Gordon DM, Whitfield PJ: Interactions of the cysticercoids of Hymenolepis diminuta and Raillietina cesticillus in their intermediate host, Tribolium confusum. Parasitology 1985, 90:421-431.
• [7]Wedekind C, Christen M, Scharer L, Treichel N: Relative helminth size in crustacean hosts: in vivo determination, and effects of host gender and within-host competition in a copepod infected by a cestode. Aquatic Ecol 2000, 34:279-285.
• [8]Dezfuli BS, Giari L, Poulin R: Costs of intraspecific and interspecific host sharing in acanthocephalan cystacanths. Parasitology 2001, 122:483-489.
• [9]Brown SP, De Lorgeril J, Joly C, Thomas F: Field evidence for density-dependent effects in the trematode Microphallus papillorobustus in its manipulated host, Gammarus insensibilis. J Parasitol 2003, 89:668-672.
• [10]Dezfuli BS, Volponi S, Beltrami I, Poulin R: Intra- and interspecific density-dependent effects on growth in helminth parasites of the cormorant, Phalacrocorax carbo sinensis. Parasitology 2002, 124:537-544.
• [11]Thomas F, Fauchier J, Lafferty KD: Conflict of interest between a nematode and a trematode in an amphipod host: test of the “sabotage” hypothesis. Behav Ecol Sociobiol 2002, 51:296-301.
• [12]Poulin R, Giari L, Simoni E, Dezfuli BS: Effects of conspecifics and heterospecifics on individual worm mass in four helminth species parasitic in fish. Parasitol Res 2003, 90:143-147.
• [13]Poulin R, Nichol K, Latham ADM: Host sharing and host manipulation by larval helminths in shore crabs: cooperation or conflict? Int J Parasitol 2003, 33:425-433.
• [14]Benesh DP, Valtonen ET: Proximate factors affecting the larval file history of Acanthocephalus lucii (Acanthocephala). J Parasitol 2007, 93:742-749.
• [15]Lagrue C, McEwan J, Poulin R, Keeney DB: Co-occurences of parasites clones and altered host phenotype in a snail-trematode system. Int J Parasitol 2007, 37:1459-1467.
• [16]Lagrue C, Poulin R: Intra- and interspecific competition among helminth parasites: Effects on Coitocaecum parvum life history strategy, size and fecundity. Int J Parasitol 2008, 38:1435-1444.
• [17]Dianne L, Rigaud T, Léger E, Motreuil S, Bauer A, Perrot-Minnot MJ: Intraspecific conflict over host manipulation between different larval stages of an acanthocephalan parasite. J Evol Biol 2010, 23:2648-2655.
• [18]Benesh DP: Intensity-dependent host mortality: what can it tell us about larval growth strategies in complex life cycle helminths? Parasitology 2011, 138:913-925.
• [19]Michaud M, Milinski M, Parker GA, Chubb JC: Competitive growth strategies in intermediate hosts: Experimental tests of a parasite life-history model using the cestode, Schistocephalus solidus. Evol Ecol 2006, 20:39-57.
• [20]Moore J: Parasites and the behavior of animals. New-York: Oxford University Press; 2002.
• [21]Thomas F, Adamo S, Moore J: Parasitic manipulation: where are we and where should we go? Behav Proc 2005, 68:185-199.
• [22]Lefèvre T, Lebarbenchon C, Gauthier-Clerc M, Missé D, Poulin R, Thomas F: The ecological significance of manipulative parasites. Trends Ecol Evol 2009, 24:41-48.
• [23]Franceschi N, Bollache L, Cornet S, Bauer A, Motreuil S, Rigaud T: Co-variation between the intensity of behavioural manipulation and parasite development time in an acanthocephalan-amphipod system. J Evol Biol 2010, 23:2143-2150.
• [24]Ness JH, Foster SA: Parasite-associated phenotype modifications in threespine stickleback. Oikos 1999, 85:127-134.
• [25]Brown SP, Loot G, Grenfell BT, Guégan JF: Host manipulation by Ligula intestinalis: accident or adaptation? Parasitology 2001, 123:519-529.
• [26]Franceschi N, Bauer A, Bollache L, Rigaud T: The effects of parasite age and intensity on variability in acanthocephalan-induced behavioural manipulation. Int J Parasitol 2008, 38:1161-1170.
• [27]Bauer A, Trouvé S, Grégoire A, Bollache L, Cézilly F: Differential influence of Pomphorhynchus laevis (Acanthocephala) on the behaviour of native and invasive species. Int J Parasitol 2000, 30:1453-1457.
• [28]Perrot-Minnot MJ: Larval morphology, genetic divergence, and contrasting levels of host manipulation between forms of Pomphorhynchus laevis (Acanthocephala). Int J Parasitol 2004, 34:45-54.
• [29]Kaldonski K, Perrot-Minnot MJ, Cézilly F: Differential influence of two acanthocephalan parasites on the antipredator behaviour of their common intermediate host. Anim Behav 2007, 74:1311-1317.
• [30]Lagrue C, Kaldonski N, Perrot-Minnot MJ, Motreuil S, Bollache L: Modification of hosts' behavior by a parasite: Field evidence for adaptive manipulation. Ecology 2007, 88:2839-284.
• [31]Dianne L, Perrot-Minnot MJ, Bauer A, Gaillard M, Léger E, Rigaud T: Protection first then facilitation: a manipulative parasite modulates the vulnerability to predation of its intermediate host according to its own developmental stage. Evolution 2011, 65:2692-2698.
• [32]Cornet S: Density-dependent effects on parasite growth and parasite-induced host immunodepression in the larval helminth Pomphorhynchus laevis. Parasitology 2011, 138:257-265.
• [33]Špakulová M, Perrot-Minnot MJ, Neuhaus B: Resurrection of Pomphorhynchus tereticollis (Rudolphi, 1809) (Acanthocephala: Pomphorhynchidae) based on new morphological and molecular data. Helminthologia 2011, 48:268-277.
• [34]Poulin R, Wise M, Moore J: A comparative analysis of adult body size and its correlates in acanthocephalan parasites. Int J Parasitol 2003, 33:799-805.
• [35]Frank SA: A kin selection model for the evolution of virulence. Proc R Soc B: Biol Sci 1992, 250:195-197.
• [36]Griffin AS, West SA: Kin selection: fact and fiction. Trends Ecol Evol 2002, 17:15-20.
• [37]Parker GA, Chubb JC, Roberts GN, Michaud M, Milinski M: Optimal growth strategies of larval helminths in their intermediate hosts. J Evol Biol 2003, 16:47-54.
• [38]Keeney DB, Bryan-Walker K, Khan N, King TM, Poulin R: The influence of clonal diversity and intensity-dependence on trematode infections in an amphipod. Parasitology 2009, 136:339-348.
• [39]Benesh DP, Seppälä O, Valtonen ET: Acanthocephalan size and sex affect the modification of intermediate host colouration. Parasitology 2009, 136:847-854.
• [40]Franceschi N, Cornet S, Bollache L, Dechaume-Moncharmont FX, Bauer A, Motreuil S, Rigaud T: Variation between populations and local adaptation in acanthocephalan-induced parasite manipulation. Evolution 2011, 64:2417-2430.
• [41]Thomas F, Brodeur J, Maure F, Franceschi F, Blanchet S, Rigaud T: Intraspecific variability in host manipulation by parasites. Infect Genet Evol 2011, 11:262-269.