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Inter-population variation in the intensity of host manipulation by the fish acanthocephalan Pomphorhynchus tereticollis: are differences driven by predation risk?

Published online by Cambridge University Press:  28 June 2019

M. Fayard Open the ORCID record for M. Fayard [Opens in a new window] ,
F. Cezilly  and
M.-J. Perrot-Minnot
M. Fayard*
Affiliation:
Biogéosciences, UMR 6282 CNRS, Université Bourgogne Franche-Comté, 6 Boulevard Gabriel, 21000 Dijon, France
F. Cezilly
Affiliation:
Biogéosciences, UMR 6282 CNRS, Université Bourgogne Franche-Comté, 6 Boulevard Gabriel, 21000 Dijon, France
M.-J. Perrot-Minnot
Affiliation:
Biogéosciences, UMR 6282 CNRS, Université Bourgogne Franche-Comté, 6 Boulevard Gabriel, 21000 Dijon, France
*
Author for correspondence: M. Fayard, E-mail: [email protected]
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Abstract

Many trophically-transmitted parasites induce behavioural alteration in their intermediate hosts that tend to increase host vulnerability to predation. Inter-population variability in parasite-induced alterations is expected to arise from variable local opportunities for trophic transmission. Yet, this hypothesis has not been investigated so far. We addressed the issue in four populations of the fish parasite Pomphorhynchus tereticollis (Acanthocephala), using variable fish biomass density as a proxy for transmission opportunities. We found variation in the intensity of parasite-induced changes in phototaxis and refuge use among populations. Two of the populations with the lowest predator biomass exhibited the highest levels of behavioural manipulation and prevalence, as expected at low transmission opportunities. They also exhibited micro-habitat segregation between infected and uninfected gammarids in the field. In addition, infection had variable effects on two physiological defence systems, immunity and antioxidant capacity, and on total protein content. Overall, our study brings partial support to the prediction that host manipulation and prevalence should be higher at low predator biomass. Although stronger evidence should be sought by increasing population replicates, our study points to the importance of the ecological context, specifically transmission opportunities brought about by predation pressure, for the evolution of parasite manipulation in trophically-transmitted parasites.

Keywords

Antioxidant capacityGammarus fossarumhost manipulationphenoloxidasePomphorhynchus tereticollispredation riskprey–predator interactiontrophic transmissionvariation
Type
Research Article
Information
Parasitology , Volume 146 , Issue 10 , September 2019 , pp. 1296 - 1304
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Copyright
Copyright © Cambridge University Press 2019 

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References

Akaike, H (1973) Maximum likelihood identification of Gaussian autoregressive moving average models. Biometrika 60, 255–265.Google Scholar
Bartoń, K (2016) Package “MuMIn”: Multi-Model Inference. ‘MuMIn’ R package, Version 1.15.6. Available at https://cran.rproject.org/web/packages/MuMIn/MuMIn.pdf.Google Scholar
Bates, D, Maechler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.Google Scholar
Bentley, CR and Hurd, H (1995) Depressed protein and copper content of the midgut gland in an intermediate host, Gammarus pulex (Crustacea), infected with cystacanths of Pomphorhynchus laevis (Acanthocephala). Journal of Invertebrate Pathology 66, 1–5.Google 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.Google Scholar
Caddigan, SC, Pfenning, AC and Sparkes, TC (2017) Competitive growth, energy allocation, and host modification in the acanthocephalan Acanthocephalus dirus: field data. Parasitology Research 116, 199–206.Google Scholar
Cézilly, F and Perrot-Minnot, MJ (2005) Studying adaptive changes in the behaviour of infected hosts: a long and winding road. Behavioural Processes 68, 223–228.Google Scholar
Cézilly, F, Favrat, A and Perrot-Minnot, M-J (2013) Multidimensionality in parasite-induced phenotypic alterations: ultimate versus proximate aspects. Journal of Experimental Biology 216, 27–35.Google Scholar
Cornet, S, Franceschi, N, Bauer, A, Rigaud, T and Moret, Y (2009) Immune depression induced by acanthocephalan parasites in their intermediate crustacean host: consequences for the risk of super-infection and links with host behavioural manipulation. International Journal for Parasitology 39, 221–229.Google Scholar
Cribari-Neto, F and Zeileis, A (2010) Beta Regression in R. Journal of Statistical Software 34, 1–24.Google Scholar
Davies, A (2001) The use and limits of various methods of sampling and interpretation of benthic macroinvertebrates. Journal of Limnology 60(suppl. 1.1), 1–6.Google Scholar
de Vries, LJ and van Langevelde, F (2018) Two different strategies of host manipulation allow parasites to persist in intermediate–definitive host systems. Journal of Evolutionary Biology 31, 393–404.Google Scholar
Dianne, L, Perrot-Minnot, M-J, Bauer, A, Gaillard, M, Léger, E and Rigaud, T (2011) Protection first then facilitation: a manipulative parasite modulates the vulnerability to predation of its intermediate host according to its own developmental stage. Evolution 65, 2692–2698.Google Scholar
Dianne, L, Perrot-Minnot, M-J, Bauer, A, Guvenatam, A and Rigaud, T (2014) Parasite-induced alteration of plastic response to predation threat: increased refuge use but lower food intake in Gammarus pulex infected with the acanothocephalan Pomphorhynchus laevis. International Journal for Parasitology 44, 211–216.Google Scholar
Fayard, M, Dechaume-Moncharmon, F-X, Perrot-Minnot, M-J and Cézilly, F (2019) Variation in the intensity of host manipulation by parasites: a meta-analysis in Acanthocephalans. Manuscript in preparation.Google Scholar
Ferrari, S and Cribari-Neto, F (2004) Beta regression for modelling rates and proportions. Journal of Applied Statistics 31, 799–815.Google Scholar
Fossat, P, Bacqué-Cazenave, J, De Deurwaerdère, P, Delbecque, JP and Cattaert, D (2014) Anxiety-like behavior in crayfish is controlled by serotonin. Science 344, 1293–1297.Google Scholar
Franceschi, N, Bauer, A, Bollache, L and Rigaud, T (2008) The effects of parasite age and intensity on variability in acanthocephalan-induced behavioural manipulation. International Journal for Parasitology 38, 1161–1170.Google Scholar
Franceschi, N, Cornet, S, Bollache, L, Dechaume-Moncharmont, FX, Bauer, A, Motreuil, S and Rigaud, T (2010) Variation between populations and local adaptation in acanthocephalan-induced parasite manipulation. Evolution 64, 2417–2430.Google Scholar
Galipaud, M, Gillingham, MAF, David, M and Dechaume-Moncharmont, FX (2014) Ecologists overestimate the importance of predictor variables in model averaging: a plea for cautious interpretations. Methods in Ecology and Evolution 5, 983–991.Google Scholar
Galipaud, M, Bollache, L and Lagrue, C (2017) Variations in infection levels and parasite-induced mortality among sympatric cryptic lineages of native amphipods and a congeneric invasive species: are native hosts always losing? International Journal for Parasitology: Parasites and Wildlife 6, 439–447.Google Scholar
Gotthard, K (2001) Growth strategies of ectothermic animals in temperate environments. In: Atkinson, D, Thorndyke, M, editors. Environment and animal development: Genes, life histories and plasticity. Oxford: BIOS. pp. 287–303.Google Scholar
Hafer-Hahmann, N (2019) Experimental evolution of parasitic host manipulation. Proceedings of the Royal Society B: Biological Sciences 286. 20182413, doi: 10.1098/rspb.2018.2413.Google Scholar
Janssens, L and Stoks, R (2013) Predation risk causes oxidative damage in prey. Biology Letters 9. 20130350, doi: 10.1098/rsbl.2013.0350.Google Scholar
Lafferty, KD (1992) Foraging on prey that are modified by parasites. The American Naturalist 140, 854–867.Google Scholar
Lafferty, KD (1999) The evolution of trophic transmission. Parasitology Today 15, 111–115.Google 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.Google Scholar
MacNeil, C, Dick, JTA, Hatcher, MJ and Dunn, AM (2003) Differential drift and parasitism in invading and native Gammarus spp. (Crustacea: Amphipoda). Ecography 26, 467–473.Google Scholar
Maurer, KM, Stewart, TW and Lorenz, FO (2014) Direct and indirect effects of fish on invertebrates and tiger salamanders in prairie pothole wetlands. Wetlands 34, 735–745.Google Scholar
Moore, J (2002) Parasites and the Behavior of Animals. New York, USA: Oxford University Press.Google Scholar
Perrot-Minnot, MJ, Kaldonski, N and Cézilly, F (2007) Increased susceptibility to predation and altered anti-predator behaviour in an acanthocephalan-infected amphipod. International Journal for Parasitology 37, 645–651.Google Scholar
Perrot-Minnot, MJ, Sanchez-Thirion, K and Cézilly, F (2014) Multidimensionality in host manipulation mimicked by serotonin injection. Proceedings of the Royal Society B: Biological Sciences 281, 20141915.Google Scholar
Perrot-Minnot, MJ, Banchetry, L and Cézilly, F (2017) Anxiety-like behaviour increases safety from fish predation in an amphipod crustacea. Royal Society Open Science 4, 171558.Google Scholar
Perrot-Minnot, MJ, Guyonnet, E, Bollache, L and Lagrue, C (2019) Differential patterns of definitive host use by two fish acanthocephalans occurring in sympatry: Pomphorhynchus laevis and Pomphorhynchus tereticollis. International Journal for Parasitology: Parasites and Wildlife 8, 135–144.Google Scholar
Plaistow, SJ, Troussard, JP and Cézilly, F (2001) The effect of the acanthocephalan parasite Pomphorhynchus laevis on the lipid and glycogen content of its intermediate host Gammarus pulex. International Journal for Parasitology 31, 346–351.Google Scholar
Poulin, R (2010) Parasite Manipulation of Host Behavior: An Update and Frequently Asked Questions. Advances in the Study of Behavior 41, 151–186.Google Scholar
R Core Team (2018) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for statistical computing. URL: http://www.R-project.org.Google Scholar
Re, R, Pellegrini, N, Proteggente, A, Pannala, A, Yang, M and Rice-Evans, C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free radical in biology and medicine 26, 1231–1237.Google Scholar
Rigaud, T and Moret, Y (2003) Differential phenoloxidase activity between native and invasive gammarids infected by local acanthocephalans: differential immunosuppression? Parasitology 127, 571–577.Google Scholar
Romano, J, Kromrey, JD, Coraggio, J, Skowronek, J and Devine, L (2006) Exploring methods for evaluating group differences on the NSSE and other surveys: Are the t-test and Cohen's d indices the most appropriate choices? In annual meeting of the Southern Association for Institutional Research, 14–17 October 2006, Arlington, VA, USA.Google Scholar
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.Google Scholar
Slos, S and Stoks, R (2008) Predation risk induces stress proteins and reduces antioxidant defense. Functional Ecology 22, 637–642.Google Scholar
Smithson, M and Verkuilen, J (2006) A better lemon squeezer? Maximum-likelihood regression with beta-distributed dependent variables. Psychological Methods 11, 54–71.Google Scholar
Tain, L, Perrot-Minnot, MJ and Cézilly, F (2006) Altered host behaviour and brain serotonergic activity caused by acanthocephalans: evidence for specificity. Proceedings of the Royal Society B: Biological Sciences 273, 3039–3045.Google Scholar
Thomas, F, Adamo, S and Moore, J (2005) Parasitic manipulation: where are we and where should we go? Behavioural Processes 68, 185–199.Google Scholar
Thomas, F, Brodeur, J, Maure, F, Franceschi, N, Blanchet, S and Rigaud, T (2011) Intraspecific variability in host manipulation by parasites. Infection, Genetics and Evolution 11, 262–269.Google Scholar
Thomas, F, Rigaud, T and Brodeur, J (2012) Evolutionary routes leading to host manipulation by parasites. In Host Manipulation by Parasites. Oxford, UK: Oxford University Press, pp. 16–35.Google Scholar
Torchiano, M (2017) effsize: Efficient Effect Size Computation. R package version 0.7.1.Google Scholar
Turner, AM and Trexler, JC (1997) Sampling aquatic invertebrates from marshes: evaluating the options. Journal of the North American Benthological Society 16, 694–709.Google Scholar
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