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

  1. Thierry Rigaud
  2. Aude Balourdet
  3. Alexandre Bauer

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Abstract

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.

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  1. Version published to 10.24072/pcjournal.346
  2. Peer Community In Zoology

    The intricate relationships between parasites and their hosts often involve a choreography of behavioral changes, with parasites manipulating their hosts in a way that enhances - or seemingly enhances – their transmission (Hughes et al., 2012; Moore, 2002; Poulin, 2010). Host manipulation is increasingly acknowledged as a pervasive adaptive transmission strategy employed by parasites, and as such is one of the most remarkable manifestations of the extended phenotype (Dawkins, 1982).

    In this laboratory study, Rigaud et al. (2023) delved into the time course of antipredator behavioral modifications induced by the acanthocephalan Pomphorhynchus laevis in its amphipod intermediate host Gammarus pulex. This system has a good foundation of prior knowledge (Bakker et al., 2017; Fayard et al., 2020; Perrot-Minnot et al., 2023), nicely drawn upon for the present work. This parasite orchestrates a switch from predation suppression, during the noninfective phase, to predation enhancement upon maturation. Specifically, G. pulex infected with the non-infective acanthella stage of the parasite can exhibit increased refuge use and reduced activity compared to uninfected individuals (Dianne et al., 2011, 2014), leading to decreased predation by trout (Dianne et al., 2011). In contrast, upon reaching the infective cystacanth stage, the parasite can enhance the susceptibility of its host to trout predation (Dianne et al., 2011).

    The present work aimed to understand the temporal sequence of these behavioral changes across the entire ontogeny of the parasite. The results confirmed the protective role of P. laevis during the acanthella stage, wherein infected amphipods exhibited heightened refuge use. This protective manipulation, however, became significant only later in the parasite's ontogeny, suggesting a delayed investment strategy, possibly influenced by the extended developmental time of P. laevis. The protective component wanes upon reaching the cystacanth stage, transitioning into an exposure strategy, aligning with theoretical predictions and previous empirical work (Dianne et al., 2011; Parker et al., 2009). The switch was behavior-specific. Unlike the protective behavior, a decline in the amphipod activity rate manifested early in the acanthella stage and persisted throughout development, suggesting potential benefits of reduced activity for the parasite across multiple stages. Furthermore, the findings challenge previous assumptions regarding the condition-dependency of manipulation, revealing that the parasite-induced behavioral changes predominantly occurred in the presence of cues signaling potential predators. Finally, while amphipods infected with acanthella stages displayed survival rates comparable to their uninfected counterparts, increased mortality was observed in those infected with cystacanth stages.

    Understanding the temporal sequence of host behavioral changes is crucial for deciphering whether it is adaptive to the parasite or not. This study stands out for its meticulous examination of multiple behaviors over the entire ontogeny of the parasite highlighting the complexity and condition-dependent nature of manipulation. The protective-then-expose strategy emerges as a dynamic process, finely tuned to the developmental stages of the parasite and the ecological challenges faced by the host. The delayed emergence of protective behaviors suggests a strategic investment by the parasite, with implications for the host's survival and the parasite's transmission success. The differential impact of infection on refuge use and activity rate further emphasizes the need for a multidimensional approach in studying parasitic manipulation (Fayard et al., 2020). This complexity demands further exploration, particularly in deciphering how trophically-transmitted parasites shape the behavioral landscape of their intermediate hosts and its temporal dynamic (Herbison, 2017; Perrot-Minnot & Cézilly, 2013).  As we discover the many subtleties of these parasitic manipulations, new avenues of research are unfolding, promising a deeper understanding of the ecology and evolution of host-parasite interactions.

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    Rigaud, T., Balourdet, A., & Bauer, A. (2023). 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. bioRxiv, ver. 6 peer-reviewed and recommended by Peer Community in Zoology. https://doi.org/10.1101/2023.04.25.538244

  3. Version published to 10.1101/2023.04.25.538244 on bioRxiv