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      Effects of the acanthocephalan Polymorphus minutus and the microsporidian Dictyocoela duebenum on energy reserves and stress response of cadmium exposed Gammarus fossarum

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          Amphipods are commonly parasitized by acanthocephalans and microsporidians and co-infections are found frequently. Both groups of parasites are known to have severe effects on their host. For example, microsporidians can modify host sex ratio and acanthocephalans can manipulate the behavior of the amphipod to promote transmission to the final host. These effects influence host metabolism in general and will also affect the ability of amphipods to cope with additional stressors such as environmental pollution, e.g., by toxic metals. Here we tested the effects of sub-lethal concentrations of cadmium on glycogen and lipid levels, as well as on the 70kDa heat shock protein (hsp70) response of field collected Gammarus fossarum, which were naturally infected with microsporidians and the acanthocephalan Polymorphus minutus. Infected and uninfected G. fossarum were exposed to a nominal Cd concentration of 4 µg/L, which resembled measured aqueous Cd concentration of 2.9 µg/L in reconstituted water for 7 d at 15 °C in parallel to an unexposed control. After exposure gammarids were snap frozen, weighed, sexed and tested for microsporidian infection by PCR. Only individuals containing the microsporidian Dictyocoela duebenum were used for the further biochemical and metal analyses. P. minutus infected amphipods were significantly smaller than their uninfected conspecifics. Mortality was insignificantly increased due to cadmium exposure, but not due to parasite infection. Microsporidian infection in combination with cadmium exposure led to increased glycogen levels in female gammarids. An increase of glycogen was also found due to interaction of acanthocephalan and microsporidian infection. Elevated lipid levels were observed in all groups infected with microsporidians, while acanthocephalans had the opposite effect. A positive correlation of lipid and glycogen levels was observed. The general stress response measured in form of hsp70 was significantly increased in microsporidian infected gammarids exposed to cadmium. P. minutus did not affect the stress response of its host. Lipid levels were correlated negatively with hsp70 response, and indicated a possible increased stress susceptibility of individuals with depleted energy reserves. The results of our study clearly demonstrate the importance of parasitic infections, especially of microsporidians, for ecotoxicological research.

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          Is a healthy ecosystem one that is rich in parasites?

          Historically, the role of parasites in ecosystem functioning has been considered trivial because a cursory examination reveals that their relative biomass is low compared with that of other trophic groups. However there is increasing evidence that parasite-mediated effects could be significant: they shape host population dynamics, alter interspecific competition, influence energy flow and appear to be important drivers of biodiversity. Indeed they influence a range of ecosystem functions and have a major effect on the structure of some food webs. Here, we consider the bottom-up and top-down processes of how parasitism influences ecosystem functioning and show that there is evidence that parasites are important for biodiversity and production; thus, we consider a healthy system to be one that is rich in parasite species.
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            Ecosystem energetic implications of parasite and free-living biomass in three estuaries.

            Parasites can have strong impacts but are thought to contribute little biomass to ecosystems. We quantified the biomass of free-living and parasitic species in three estuaries on the Pacific coast of California and Baja California. Here we show that parasites have substantial biomass in these ecosystems. We found that parasite biomass exceeded that of top predators. The biomass of trematodes was particularly high, being comparable to that of the abundant birds, fishes, burrowing shrimps and polychaetes. Trophically transmitted parasites and parasitic castrators subsumed more biomass than did other parasitic functional groups. The extended phenotype biomass controlled by parasitic castrators sometimes exceeded that of their uninfected hosts. The annual production of free-swimming trematode transmission stages was greater than the combined biomass of all quantified parasites and was also greater than bird biomass. This biomass and productivity of parasites implies a profound role for infectious processes in these estuaries.
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              Parasites of the superorganism: are they indicators of ecosystem health?

              The concept of ecosystem health is derived from analogies with human health, which subsequently leads to the implication that the ecosystem has organismal properties, a 'superorganism' in the Clementsian sense. Its application and usefulness has been the subject of a contentious debate; yet, the term 'ecosystem health' has captured the public's imagination and woven its way into the current lexicon, even incorporated into public policy. However, the application of parasites as bioindicators of ecosystem health poses a curious conundrum. Perceptions of parasites range from mild distaste to sheer disgust among the general public, the media, environmental managers and non-parasitologists in the scientific community. Nevertheless, the biological nature of parasitism incorporates natural characteristics that are informative and useful for environmental management. The helminths in particular have evolved elegant means to ensure their transmission, often relying on complex life cycle interactions that include a variety of invertebrate and vertebrate hosts. The assemblage of these diverse parasites within a host organism potentially reflect that host's trophic position within the food web as well as the presence in the ecosystem of any other organisms that participate in the various parasite life cycles. Perturbations in ecosystem structure and function that affect food web topology will also impact upon parasite transmission, thus affecting parasite species abundance and composition. As such, parasite populations and communities are useful indicators of environmental stress, food web structure and biodiversity. In addition, there may be useful other means to utilise parasitic organisms based on their biology and life histories such as suites or guilds that may be effective bioindicators of particular forms of environmental degradation. The challenge for parasitology is to convince resource managers and fellow scientists that parasites are a natural part of all ecosystems, each species being a potentially useful information unit, and that healthy ecosystems have healthy parasites.

                Author and article information

                PeerJ Inc. (San Francisco, USA )
                29 October 2015
                : 3
                [1 ]Department of Life Science, National Taiwan University , Taipei, Taiwan
                [2 ]Aquatic Ecology and Centre for Water and Environmental Research, University of Duisburg–Essen , Essen, Germany
                [3 ]Department of Zoology, University of Johannesburg , Johannesburg, South Africa
                © 2015 Chen et al.

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.

                Funded by: German Academic Exchange Service (DAAD)
                Funded by: Ministry of Science and Technology
                The German Academic Exchange Service (DAAD) and the Ministry of Science and Technology, Taiwan funded the research stay of Ms. Hui-Yu Chen. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Environmental Sciences


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