Global drivers of parasitism in freshwater plankton communities

Zooplankton and phytoplankton communities play host to a wide diversity of parasites, which have been found to play a significant role in a number of ecosystem processes, such as facilitating energy transfer and promoting species succession through altering interspecific competition. Yet we know little about the mechanisms that drive parasite dynamics in aquatic ecosystems. Recent mathematical models have shown how habitat can shape parasite dynamics through influencing the efficacy of parasite transmission; however, these predictions have yet to be tested at larger ecological scales. Here, we present a comparative analysis of parasitism in planktonic communities, assembling data from a range of host and parasite taxa, habitat types, and geographic regions. Our results suggest that the prominent depth-prevalence relationship observed in studies on Daphnia in temperate lakes of North America is applicable to a wide range of aquatic habitats, hosts, and parasites; however, differences in transmission strategies between parasites can lead to considerable variation in parasite dynamics. Observational studies which incorporate a diversity of habitat types will be important in uncovering the mechanisms which underlie this relationship. In particular, more experimental work on transmission stage survivability and infectivity in aquatic environments will be necessary before we can make accurate predictive models of parasite spread in these ecosystems. Microparasites are a common component of freshwater plankton communities and their diversity, particularly in larger host taxa, e.g., Daphnia or Asterionella, can be remarkably high (Sparrow 1960; Green 1974; Ebert 2005; Kagami et al. 2007). Daphnia represents one of the most commonly investigated hosts, with studies documenting anywhere from 16 to 20 epiparasitic and endoparasitic taxa infecting a single population or metapopulation (Stirnadel and Ebert 1997; Ebert et al. 2001). The full extent of this diversity has only recently begun to be appreciated through advances in molecular systematics, particularly of those parasites belonging to the Phyla Oomycota and Chytridiomycota (Lefevre et al. 2007; Wolinska et al. 2009). Although there exists a large number of taxa capable of infecting plankton species, most populations coexist with only a small subset of their potential parasites (Ebert et al. 2001) and some populations appear not to harbour any parasites at all. In Lake Brienz (Switzerland), for instance, a comprehensive survey over 2 yr found no parasites within its Daphnia population, despite infections occurring in the surrounding lakes (Wolinska et al. 2007). Similar landscape scale studies (e.g., Gaiser and Bachmann 1993; Schoebel et al. 2013; Goren and Ben-Ami 2013) have found that the distributions of plankton parasites are not strongly dependent on their host range, but point to a more complex relationship than that predicted by simple epidemiological models. A number of ecological factors have been proposed to explain the variation in the presence or absence of specific parasite taxa as well as changes in parasite prevalence and duration of epidemics among lakes. Hall et al. (2010) outlined three overlapping routes in which among-lakes differences may affect rates of parasitism. These include differences in habitat quality, through its influence on growth and survival of both the host and parasite, changes in community structure (e.g., competitors, predators) and physical habitat differences that could promote the transfer of free-living (transmission) parasite stages. Transmission to a new host is a fundamental challenge for parasites and the success of transmission stages is a key determinant of parasite fitness (Anderson and May 1979). In the aquatic environment, parasites infect new hosts using either immobile or mobile transmission stages. Immobile stages drift in the water column until they are ingested by a susceptible host and can remain infective for months, especially at cold temperatures (Decaestecker et al. 2004), while mobile stages actively swim through the water column in search of a host and are generally shorter lived (Sparrow 1960). Parasite transmission stages are highly vulnerable; grazing, temperature, irradiance, and UV radiation have all been implicated as Additional Supporting Information may be found in the online version of this article *Correspondence: [email protected] 1707 LIMNOLOGY and OCEANOGRAPHY Limnol. Oceanogr. 60, 2015, 1707–1718 VC 2015 Association for the Sciences of Limnology and Oceanography doi: 10.1002/lno.10127 factors which can significantly affect their survival (see reviews by Pietrock and Marcogliese 2003 and Gleason and Lilje 2009). Within lakes, annual and seasonal parasite dynamics are common and are thought to be driven by environmental variables which can affect transmission stage survival as well as encounter rates with susceptible hosts (C aceres et al. 2006). These seasonal drivers include factors such as temperature and lake stratification as well as host density (Doggett and Porter 1996; Perez-Martinez et al. 2001; Vale et al. 2008). For instance, in Lake Maarseveen (The Netherlands), the severity of infection of the diatom Asterionella by a chytrid fungus was shown to be lower in years with mild winters, which reduced Asterionella densities, suggesting a tight coupling between host and parasite densities at the lake scale (Ibelings et al. 2011). A similar relationship was not evident in Daphnia parasitized by the fungus Metschnikowia bicuspidata in lakes in southern Michigan (U.S.A.), where interactions between lake morphology and late summer cooling resulted in large fluctuations in maximum prevalence irrespective of host density (C aceres et al. 2006). Relationships between seasonal changes in host density and parasite prevalence, intensity, and diversity have been shown to be quite variable and may be modulated by differences in parasite life history strategies (e.g., Cote and Poulin 1995; Morand and Poulin 1998; Arneberg 2001). Ecological patterns are dependent on the spatial and temporal scale at which they are viewed, and patterns in parasite prevalence are no different (e.g., Duffy et al. 2010; Thieltges et al. 2013). Combining studies from a number of different regions can be informative because, although rates of parasitism are proximately driven by local environmental conditions, ultimately those factors may be correlated over large spatial scales (Byers et al. 2008). Using a cross-continental dataset of trematode infections in marine gastropods, Thieltges et al. (2013) were able to establish a strong positive relationship between local prevalence and the geographical distribution of trematodes. In addition, they were able to identify the type of definitive host (fish vs. bird) as a significant driver of this relationship, pointing to a stronger role of definitive host dispersal than local environmental factors in shaping the biogeographic distributions of these parasites. More studies such as these are needed to resolve the role of local and regional processes in explaining global patterns in parasite distribution and prevalence. The primary objective of this study was to examine largescale patterns of parasitism in planktonic communities and how these patterns vary among different hosts and parasite species. To do this, a large dataset of prevalence data was compiled from a number of studies representing a diverse range of hosts, parasite types, and waterbodies. Our first objective was to examine within-lake patterns of parasite prevalence; e.g., relationships with host density, seasonality, and annual variation in maximum prevalence. We expected that parasites with mobile transmission stages would show a stronger relationship with host density relative to parasites with immobile transmission stages. Our second objective was to examine the relative contribution of amongwaterbody (e.g., size and trophic status) and withinwaterbody factors to variation in maximum parasite prevalence and how this may differ relative to parasite life history strategies using methods similar to those of Duffy et al. (2010). We expected to see higher parasite prevalence in shallower waterbodies due to a reduction in barriers to parasite transmission (e.g., parasite spores lost to the hypolimnion). By revealing patterns in prevalence across such a broad spatial scale and encompassing a diversity of parasites and hosts, we offer general insights into the most likely drivers of parasite prevalence in planktonic organisms.