Parasites in freshwater mussels: community ecology and conservation

Change log

Parasites can be studied with respect to their spatial distribution, abundance and diversity (a parasite-centric view), or with respect to their effects on host individuals, populations, communities and the wider ecosystem (a host-centric view). The former contributes to understandings of what drives parasite community structure across scales, while the latter furthers knowledge on how the conservation of host species or the functioning of ecosystems may be influenced by those parasite communities. In this thesis, I study both perspectives using a previously unexplored system: the ecosystem-engineering freshwater mussels (Unionida) and their macroparasites. As such, this thesis has three broad aims: to characterise knowledge to date on unionid mussel parasite communities and develop tools to further knowledge in this area; to analyse the drivers of parasite community assembly in their hosts; and to evaluate the implications of parasitism on freshwater mussel individuals, populations and the ecosystems that the mussels modify. In Chapter 2, I provide a review of all unionid-parasite records from Europe and North America to date, comprising 1476 records and at least 188 unique parasitic or endosymbiotic species. However, 53% of mussel species have no records, and few observations record the effects of the parasites, highlighting key research gaps that need to be filled. Chapters 3 and 4 provide novel methods to study the effect of digenean trematodes, a common and important class of parasite in freshwater mussels. Chapter 3 describes an efficient and reproducible method of accurately quantifying trematode infection in the gonad of freshwater mussels; this has been challenging due to the asexual growth of this parasite group and inability to count individuals. This method allows researchers to move past subjective judgements of infection intensity. Further, Chapter 4 describes a rapid way of non-destructively assessing trematode infection without killing the mussel, allowing even highly endangered bivalve species to be sampled for parasites. In Chapter 5, I analyse the drivers of parasite community structure in a single mussel species (Anodonta anatina) at a single site across a full year, and show that parasite assembly was influenced by a combination of environmental, host-level and within-host factors. Specifically, the time of year sampled, in addition to host size and host gravid status, vi influenced both the prevalence and intensity of the parasite communities inside individual hosts. Allowing for these factors also enables parasite-parasite interactions to be detected, showing that the distributions of individual freshwater mussel parasites are not independent and cannot be considered in isolation. Chapter 6 extends this approach by studying parasite communities across multiple host mussel species (A. anatina and Unio pictorum) and sites, and demonstrates that variation between sites and between host species is greater than expected, highlighting the operation of both abiotic and biotic filters on freshwater mussel parasites. Parasite-parasite interactions were once again detected, but only after accounting for site-level patterns of parasite prevalence and variation in the infection rates of individual hosts, highlighting the importance of considering interplay among ecological scales when characterising patterns in community ecology. Chapter 7 quantifies the effect of parasitic trematodes, mites and invasive zebra mussels (Dreissena polymorpha) on the reproductive capacity of A. anatina. Rather than just focus on individuals, I estimate the reduction in population-level reproductive capacity caused by parasites across multiple sites, showing that parasites alone reduce potential reproductive output by up to 13%, even at low prevalences. Chapter 8 demonstrates the role that trematodes and bitterling fish (Rhodeus amarus) embryos play in altering the filtration capacity of A. anatina and U. pictorum, and how this scales to the ecosystem level. Using a combination of field surveys, field experiments, laboratory experiments and ecological modelling I show that these parasites alter the time taken for mussel communities to filter the Old West River (Cambridgeshire, UK) by up to 50%, a statistic that depends on parasite and host community composition as well as the suspended particle concentration. Finally, Chapter 9 explores how parasites may affect the success of captive breeding or translocation programs for endangered freshwater mussels (and for endangered species generally), and how a failure to consider parasites and disease in these programs may amplify the spread of harmful pathogens to already threatened populations or species. While this thesis emphasises the possible implications of parasites for host individuals, populations and their ecosystems, it also introduces unionid mussels as a tractable system to further our knowledge of parasite community assembly across ecological scales. Both approaches are important to advance understandings in the ecological role of parasites in the context of global environmental change.

Aldridge, David
parasitology, freshwater, ecosystem ecology, community ecology, unionid, trematode, mite, bitterling, joint species distribution model, null model, markov random fields model, niche and neutral theory, scale
Doctor of Philosophy (PhD)
Awarding Institution
University of Cambridge
Woolf Fisher Trust