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Combined effects of anthropogenic stressors and parasitism on the genetic variation, behaviour, physiology and functional role of Gammarus freshwater amphipods – MultiStress

Combined effects of anthropogenic stressors and parasitism on the biology of freshwater crustaceans

The aim of the project is to study the combined effects of anthropological stressors (pollution, global warming) and parasitism on the genetic variation, the behavior, the physiology and the functional role of freshwater amphipods of the genus Gammarus (Gammarids).

Predict the effects of the anthropological changes and their interaction with parasite infections on the scavenging freshwater macrofauna

A first aim of the present project is to examine how combinations of abiotic stressors such as contaminants (metal, endocrine disruptor and neurotoxic compounds) and temperature, with a biotic stressor (parasitism) can impact the behaviour and physiology of the freshwater amphipod Gammarus pulex. A second aim of the project is to assess to what extent the alterations of the phenotype amphipods resulting from simultaneous exposure to multiple stressors can affect species coexistence and the functional role of amphipods in freshwater ecosystems. A third and final aim, is to assess to what extent genetic variation is involved in the response of amphipods to multiple stressors, at the individual and population level. Given the crucial ecosystemic role played by amphipod species, the results of the project are likely to increase our understanding of the predictable dynamics of the quality of freshwater ecosystems exposed to global change and increasing anthropic pressure.

By nature, this project relies on various analytical techniques: behavioral analyses (anti-predatory behavior, food foraging behavior; laboratory controlled exposure to various types of stressors (temperature variations, pollutants, macroparasites); monitoring of natural populations; techniques of population genetics (analysis of variable genetic markers); techniques of physiological analyses (metabolism, expression of toxicity markers: neurotoxins, endocrine disruptors)

In the work package « multiple stressors and genetic variation in amphipods”, we sampled 130 natural populations of gammarids belonging to 5 watersheds, where we previously identified potentially polluted sites (heavy metals or organic contaminations) and preserved sites. The first analysis of 1200 gammarid samples did not revealed any link between pollution and genetic variation for the more widespread gammarid cryptic species. However, in some rivers, some gammarid rarer species were associated with absence of contamination. Furthermore, we evidenced that two species of Gammarus living in sympatry are not equally sensitive to parasitic infection. Finally, we produced a review paper on potential consequences of conflicting parasites during multiple infections.
In the work package “effects of abiotic stressors on parasitic infectivity”, we first experimentally investigated the effects of variations in food availability. High - quality food induced a better exploitation of the hosts by parasites, but hosts showed a best survival.
The work package “Single and combined effects of parasitic infection and abiotic stressors on gammarids physiology” began in 2015. Preliminary results showed that, while both parasitism and exposure to pollutant (cadmium) negatively impact the metabolism and behavior of amphipods, their interaction did not always act synergistically.
In the work package “Single and combined effects of parasitic infection and abiotic stressors on the trophic ecology of gammarids”, we found that high-quality food allows gammarids to tolerate acute high-dose exposure to cadmium, while it depress tolerance to a chronic, low-dose, exposure.

The first results of the work package “multiple stressors and genetic variation in amphipods” (i.e. absence of link between genetic variation and contamination ion the more widespread gammarid species) suggest that tolerance to pollution could result of plasticity rather than selection. This hypothesis should be verified by analyzing genetic markers more variable that those already used. In addition, our results suggest that some gammarid species could be less tolerant than others to contamination. This hypothesis will be tested by investigating rivers at a fine grain and by experimentally expose different genotypes to pollutants.
In the work package “effects of abiotic stressors on parasitic infectivity”, we will investigate a second important abiotic factor: variation of temperature.
Finally, in the work package “Single and combined effects of parasitic infection and abiotic stressors on the trophic ecology of gammarids”, we will analyse the effects of parasitic infection in addition to heavy metals.

Submitted papers :
- Labaude S., Cézilly F., Tercier X. and 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. Submitted to Parasite and Vectors.
- Bauer A. and Rigaud T. Field prevalence versus infection sensitivity between two sympatric amphipod hosts in a trophically transmitted manipulative acanthocephalan parasite: potential consequences for parasite transmission. Submitted to Parasitology.
- Arce Funck J., Crenier C., Felten V., and Danger M. High food quality reduces resistance to midterm exposure to contaminants in the detritivore, Gammarus fossarum., Submitted to Aquatic Toxicology.
- Labaude S., Rigaud T. and Cézilly F. Host manipulation in the face of environmental changes: ecological consequences. Submitted to International Journal for Parasitology: Parasites and Wildlife.

Published paper :
- Cézilly F., Perrot-Minnot M.J. and Rigaud T. 2014. Cooperation and conflict in host manipulation:interactions among macro-parasites and micro-organisms. Frontiers in Microbiology, 5, 248, doi: 10.3389/fmicb.2014.00248.

Living organisms most often face multiple stressors in natural environments. However, the cumulative effects of multiple stressors, acting synergistically or antagonistically on species and ecosystems, remain poorly appreciated. In particular, the combined effect of parasites with abiotic stressors deserves particular attention, at a time where anthropogenic stress and climate change appear to be two major causes of parasitic diseases emergence in natural populations. The existing literature suggests that the interaction between parasitic or pathogenetic organisms and abiotic stressors is a complex one. Furthermore, the interactions between parasitic infections and abiotic stressors may have far-reaching and subtle consequences in ecosystems. For example, given the role of trophically-transmitted parasites as ecosystem engineers, any impact of stressors on host-parasite associations can have cascade effects throughout the entire food web.
Gammarid amphipods represent, in many freshwater communities, the dominant macroinvertebrate species in terms of biomass. As detritivores and scavengers, they play a central role in freshwater ecosystems. Their distribution is influenced by abiotic factors such as temperature, salinity, oxygen, acidity and pollution. Amphipods are considered to be a good and robust biomonitor of the quality of freshwater ecosystems, and the effect of contaminants or other abiotic stresses begins to be very well documented. Parallel to this, gammarids are known to be infected by acanthocephalans, a widespread group of trophically-transmitted parasites, for which they are intermediate hosts. The influence of acanthocephalans on the physiology and behaviour of their amphipod hosts has been largely documented as well. However, the effect of interactions between these biotic stressors and the abiotic ones remains poorly documented. The present project aims at studying i) how macroparasites interact with abiotic stressors such as thermal stress and contaminants in affecting the physiology and behaviour of the freshwater amphipod Gammarus pulex and ii) their functional role in freshwater ecosystems, and iii) to investigate to what extent genetic variability between and within populations is involved in the ability of individuals to cope with multiple stressors. Given the crucial ecosystemic role played by amphipod species, the results of the project are likely to increase our understanding of the predictable dynamics of the quality of freshwater ecosystems exposed to global change and increasing anthropic pressure.

Project coordination

Thierry RIGAUD (Laboratoire Biogéosciences)

The author of this summary is the project coordinator, who is responsible for the content of this summary. The ANR declines any responsibility as for its contents.

Partner

Biogéosciences Laboratoire Biogéosciences
IRSTEA - UR MAEP IRSTEA - UR Milieux Aquatiques, Ecologie et Pollutionse Mili

Help of the ANR 406,744 euros
Beginning and duration of the scientific project: December 2013 - 48 Months

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