Time-course of antipredator behavioral changes induced by the helminth Pomphorhynchus laevis in its intermediate host Gammarus pulex: the switch in manipulation according to parasite developmental stage differs between behaviors

10.24072/pcjournal.346 - Peer Community Journal, Volume 3 (2023), article no. e109.

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Many trophically transmitted parasites with complex life cycles manipulate their intermediate host’s antipredatory defenses in ways facilitating their transmission to final host by predation. Some parasites also protect the intermediate host from predation when noninfective during its ontogeny. The acanthocephalan Pomphorynchus laevis, a fish intestinal helminth, infecting freshwater gammarid amphipods as intermediate hosts, is using such a strategy of protection-then-exposure to predation by the definitive host. However, the whole time-course of this sequence of behavioral switch is not yet known, and only one antipredator behavior has been studied to date.  Here we show that the protective part of this manipulation begins quite late during the parasite ontogeny, suggesting that the advantages overpass the costs induced by this protective manipulation only at this stage. We confirmed that the refuge use behavior is showing a switch in the few days following the stage mature for the definitive host (switching from overuse to underuse). However, such a switch was not observed for the gammarids activity rate, a behavior also known to make the host less conspicuous to predators when weak. While we predicted a low activity during early development stages, then a switch to high activity, we observed general decrease in activity during the parasite ontogeny. The possible causes for this discrepancy between behaviors are discussed. All these behavioral changes were observed mostly when animals were tested in water scented by potential predators (here brown trout), suggesting condition-dependent manipulation.

Published online:
DOI: 10.24072/pcjournal.346
Keywords: parasite-induced behavioral manipulation, acanthocephalan, freshwater amphipod
Rigaud, Thierry 1; Balourdet, Aude 1; Bauer, Alexandre 1

1 Université de Bourgogne, Laboratoire Biogéosciences, UMR CNRS 6282, équipe Ecologie Evolutive, 6 boulevard Gabriel, 21000 Dijon, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
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Rigaud, Thierry; Balourdet, Aude; Bauer, Alexandre. Time-course of antipredator behavioral changes induced by the helminth Pomphorhynchus laevis in its intermediate host Gammarus pulex: the switch in manipulation according to parasite developmental stage differs between behaviors. Peer Community Journal, Volume 3 (2023), article  no. e109. doi : 10.24072/pcjournal.346. https://peercommunityjournal.org/articles/10.24072/pcjournal.346/

Peer reviewed and recommended by PCI : 10.24072/pci.zool.100215

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Åbjörnsson, K.; Hansson, L.-A.; Brönmark, C. Responses of prey from habitats with different predator regimes: local adaptation and heritability, Ecology, Volume 85 (2004) no. 7, pp. 1859-1866 | DOI

[2] Andersson, K. G.; Brönmark, C.; Herrmann, J.; Malmqvist, B.; Otto, C.; Sjörström, P. Presence of sculpins (Cottus gobio) reduces drift and activity of Gammarus pulex (Amphipoda), Hydrobiologia, Volume 133 (1986) no. 3, pp. 209-215 | DOI

[3] Bailly, Y.; Cézilly, F.; Rigaud, T. Stage-dependent behavioural changes but early castration induced by the acanthocephalan parasite Polymorphus minutus in its Gammarus pulex intermediate host, Parasitology, Volume 145 (2017) no. 3, pp. 260-268 | DOI

[4] Bauer, A.; Rigaud, T. Identifying a key host in an acanthocephalan-amphipod system, Parasitology, Volume 142 (2015) no. 13, pp. 1588-1594 | DOI

[5] Benesh, D. P. Tapeworm manipulation of copepod behaviour: parasite genotype has a larger effect than host genotype, Biology Letters, Volume 15 (2019) no. 9 | DOI

[6] Berdoy, M.; Webster, J. P.; Macdonald, D. W. Fatal attraction in rats infected with Toxoplasma gondii, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 267 (2000) no. 1452, pp. 1591-1594 | DOI

[7] Berger, C. S.; Laroche, J.; Maaroufi, H.; Martin, H.; Moon, K.-M.; Landry, C. R.; Foster, L. J.; Aubin-Horth, N. The parasite Schistocephalus solidus secretes proteins with putative host manipulation functions, Parasites & Vectors, Volume 14 (2021) no. 1 | DOI

[8] Bethel, W. M.; Holmes, J. C. Increased vulnerability of amphipods to predation owing to altered behavior induced by larval acanthocephalans, Canadian Journal of Zoology, Volume 55 (1977) no. 1, pp. 110-115 | DOI

[9] Bollache, L.; Kaldonski, N.; Troussard, J.-P.; Lagrue, C.; Rigaud, T. Spines and behaviour as defences against fish predators in an invasive freshwater amphipod, Animal Behaviour, Volume 72 (2006) no. 3, pp. 627-633 | DOI

[10] Cézilly, F.; Thomas, F.; Médoc, V.; Perrot-Minnot, M.-J. Host-manipulation by parasites with complex life cycles: adaptive or not?, Trends in Parasitology, Volume 26 (2010) no. 6, pp. 311-317 | DOI

[11] Cliff, N. Dominance statistics: Ordinal analyses to answer ordinal questions., Psychological Bulletin, Volume 114 (1993) no. 3, pp. 494-509 | DOI

[12] Dianne, L.; Perrot-Minnot, M.-J.; 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, Volume 65 (2011) no. 9, pp. 2692-2698 | DOI

[13] Dianne, L.; Perrot-Minnot, M.-J.; Bauer, A.; Guvenatam, A.; Rigaud, T. 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, Volume 44 (2014) no. 3-4, pp. 211-216 | DOI

[14] Fayard, M.; Dechaume‐Moncharmont, F.; Wattier, R.; Perrot‐Minnot, M. Magnitude and direction of parasite‐induced phenotypic alterations: a meta‐analysis in acanthocephalans, Biological Reviews, Volume 95 (2020) no. 5, pp. 1233-1251 | DOI

[15] Fossat, P.; Bacqué-Cazenave, J.; De Deurwaerdère, P.; Delbecque, J.-P.; Cattaert, D. Anxiety-like behavior in crayfish is controlled by serotonin, Science, Volume 344 (2014) no. 6189, pp. 1293-1297 | DOI

[16] Franceschi, N.; Bauer, A.; Bollache, L.; Rigaud, T. The effects of parasite age and intensity on variability in acanthocephalan-induced behavioural manipulation, International Journal for Parasitology, Volume 38 (2008) no. 10, pp. 1161-1170 | DOI

[17] 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, Journal of Evolutionary Biology, Volume 23 (2010) no. 10, pp. 2143-2150 | DOI

[18] Franceschi, N.; Cornet, S.; Bollache, L.; Dechaume-Moncharmont, F.-X.; Bauer, A.; Motreuil, S.; Rigaud, T. Variation between populations and local adaptation in acanthocephalan-induced parasite manipulation, Evolution, Volume 64 (2010), pp. 2417-2430 | DOI

[19] Hafer, N. Differences between populations in host manipulation by the tapeworm Schistocephalus solidus – is there local adaptation?, Parasitology, Volume 145 (2017) no. 6, pp. 762-769 | DOI

[20] Hafer-Hahmann, N. Experimental evolution of parasitic host manipulation, Proceedings of the Royal Society B: Biological Sciences, Volume 286 (2019) no. 1895 | DOI

[21] Hammerschmidt, K.; Koch, K.; Milinski, M.; Chubb, J. C.; Parker, G. A. When to go: optimization of host switching in parasites with complex life cycles, Evolution, Volume 63 (2009) no. 8, pp. 1976-1986 | DOI

[22] Hughes, D.; Brodeur, J.; Thomas, F.; UK, P. Host Manipulation by Parasites, Oxford University Press, 2012 | DOI

[23] Jensen, C. H.; Weidner, J.; Giske, J.; Jørgensen, C.; Eliassen, S.; Mennerat, A. Adaptive host responses to infection can resemble parasitic manipulation, Ecology and Evolution, Volume 13 (2023) no. 7 | DOI

[24] Kraemer, H. C.; Kupfer, D. J. Size of Treatment Effects and Their Importance to Clinical Research and Practice, Biological Psychiatry, Volume 59 (2006) no. 11, pp. 990-996 | DOI

[25] Labaude, S.; Cézilly, F.; De Marco, L.; Rigaud, T. Increased temperature has no consequence for behavioral manipulation despite effects on both partners in the interaction between a crustacean host and a manipulative parasite, Scientific Reports, Volume 10 (2020) no. 1 | DOI

[26] Labaude, S.; Cézilly, F.; Tercier, X.; Rigaud, T. Influence of host nutritional condition on post-infection traits in the association between the manipulative acanthocephalan Pomphorhynchus laevis and the amphipod Gammarus pulex, Parasites & Vectors, Volume 8 (2015) no. 1 | DOI

[27] Labaude, S.; Rigaud, T.; Cézilly, F. Additive effects of temperature and infection with an acanthocephalan parasite on the shredding activity of Gammarus fossarum (Crustacea: Amphipoda): the importance of aggregative behavior, Global Change Biology, Volume 23 (2016) no. 4, pp. 1415-1424 | DOI

[28] Lagrue, C.; Kaldonski, N.; Perrot-Minnot, M. J.; Motreuil, S.; Bollache, L. Modification of hosts' behavior by a parasite: field evidence for adaptive manipulation, Ecology, Volume 88 (2007) no. 11, pp. 2839-2847 | DOI

[29] Lefèvre, T. Exploring manipulative strategies of a trophically-transmitted parasite across its ontogeny, Peer Community in Zoology (2023) | DOI

[30] Levri, E. P. Parasite-induced change in host behavior of a freshwater snail: parasitic manipulation or byproduct of infection?, Behavioral Ecology, Volume 10 (1999) no. 3, pp. 234-241 | DOI

[31] McCahon, C. P.; Maund, S. J.; Poulton, M. J. The effect of the acanthocephalan parasite (Pomphorhynchus laevis) on the drift of its intermediate host (Gammarus pulex), Freshwater Biology, Volume 25 (1991) no. 3, pp. 507-513 | DOI

[32] Médoc, V.; Beisel, J. When trophically‐transmitted parasites combine predation enhancement with predation suppression to optimize their transmission, Oikos, Volume 120 (2011) no. 10, pp. 1452-1458 | DOI

[33] Moore, J. Responses of an Avian Predator and Its Isopod Prey to an Acanthocephalan Parasite, Ecology, Volume 64 (1983) no. 5, pp. 1000-1015 | DOI

[34] Moore, J. Parasites and the Behavior of Animals, Oxford University PressNew York, NY, 2002 | DOI

[35] Noguchi, K.; Gel, Y. R.; Brunner, E.; Konietschke, F. nparLD: An R Software Package for the Nonparametric Analysis of Longitudinal Data in Factorial Experiments, Journal of Statistical Software, Volume 50 (2012) no. 12 | DOI

[36] Normant, M.; Dziekonski, M.; Drzazgowski, J.; Lamprecht, I. Metabolic investigations of aquatic organisms with a new twin heat conduction calorimeter, Thermochimica Acta, Volume 458 (2007) no. 1-2, pp. 101-106 | DOI

[37] Parker, G. A.; Ball, M. A.; Chubb, J. C.; Hammerschmidt, K.; Milinski, M. When should a trophically transmitted parasite manipulate its host?, Evolution, Volume 63 (2009) no. 2, pp. 448-458 | DOI

[38] Perrot-Minnot, M.-J.; Banchetry, L.; Cézilly, F. Anxiety-like behaviour increases safety from fish predation in an amphipod crustacea, Royal Society Open Science, Volume 4 (2017) no. 12 | DOI

[39] Perrot-Minnot, M.-J.; Kaldonski, N.; Cézilly, F. Increased susceptibility to predation and altered anti-predator behaviour in an acanthocephalan-infected amphipod, International Journal for Parasitology, Volume 37 (2007) no. 6, pp. 645-651 | DOI

[40] Perrot‐Minnot, M.; Maddaleno, M.; Cézilly, F. Parasite‐induced inversion of geotaxis in a freshwater amphipod: a role for anaerobic metabolism?, Functional Ecology, Volume 30 (2015) no. 5, pp. 780-788 | DOI

[41] Perrot-Minnot, M.-J.; Sanchez-Thirion, K.; Cézilly, F. Multidimensionality in host manipulation mimicked by serotonin injection, Proceedings of the Royal Society B: Biological Sciences, Volume 281 (2014) no. 1796 | DOI

[42] Poulin, R. The evolution of parasite manipulation of host behaviour: a theoretical analysis, Parasitology, Volume 109 (1994) no. S1 | DOI

[43] Poulin, R. Evolutionary Ecology of Parasites: (Second Edition), Princeton University Press, 2007 (https://www.jstor.org/stable/j.ctt7sn0x)

[44] Poulin, R. Parasite Manipulation of Host Behavior, Advances in the Study of Behavior, Elsevier, 2010, pp. 151-186 | DOI

[45] Poulin, R.; Maure, F. Host Manipulation by Parasites: A Look Back Before Moving Forward, Trends in Parasitology, Volume 31 (2015) no. 11, pp. 563-570 | DOI

[46] Rigaud, T. Time course of behavioral of manipulation of Gammarus pulex by Pomphorhynchus laevis, Recherche Data Gouv, V1. , 2023 | DOI

[47] Schäffer, M.; Winkelmann, C.; Hellmann, C.; Benndorf, J. Reduced drift activity of two benthic invertebrate species is mediated by infochemicals of benthic fish, Aquatic Ecology, Volume 47 (2013) no. 1, pp. 99-107 | DOI

[48] Svensson, P. A.; Eghbal, R.; Eriksson, R.; Nilsson, E. How cunning is the puppet-master? Cestode-infected fish appear generally fearless, Parasitology Research, Volume 121 (2022) no. 5, pp. 1305-1315 | DOI

[49] Tain, L.; Perrot-Minnot, M.-J.; Cézilly, F. Altered host behaviour and brain serotonergic activity caused by acanthocephalans: evidence for specificity, Proceedings of the Royal Society B: Biological Sciences, Volume 273 (2006) no. 1605, pp. 3039-3045 | DOI

[50] Takahashi, K. Changes in the anxiety-like and fearful behavior of shrimp following daily threatening experiences, Animal Cognition, Volume 25 (2021) no. 2, pp. 319-327 | DOI

[51] Vargha, A.; Delaney, H. D. A Critique and Improvement of the CL Common Language Effect Size Statistics of McGraw and Wong, Journal of Educational and Behavioral Statistics, Volume 25 (2000) no. 2, pp. 101-132 | DOI

[52] Weinreich, F.; Benesh, D. P.; Milinski, M. Suppression of predation on the intermediate host by two trophically-transmitted parasites when uninfective, Parasitology, Volume 140 (2012) no. 1, pp. 129-135 | DOI

[53] Williams, D. D.; Moore, K. A. The Role of Semiochemicals in Benthic Community Relationships of the Lotic Amphipod Gammarus pseudolimnaeus: A Laboratory Analysis, Oikos, Volume 44 (1985) no. 2 | DOI

[54] Wudkevich, K.; Wisenden, B. D.; Chivers, D. P.; Smith, R. J. F. Reactions of Gammarus lacustris to Chemical Stimuli from Natural Predators and Injured Conspecifics, Journal of Chemical Ecology, Volume 23 (1997) no. 4, pp. 1163-1173 | DOI

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