Host and parasite identity interact in scale-dependent fashion to determine parasite community structure.

Understanding the ecological assembly of parasite communities is critical to characterise how changing host and environmental landscapes will alter infection dynamics and outcomes. However, studies frequently assume that (a) closely related parasite species or those with identical life-history strategies are functionally equivalent, and (b) the same factors will drive infection dynamics for a single parasite across multiple host species, oversimplifying community assembly patterns. Here, we challenge these two assumptions using a naturally occurring host-parasite system, with the mussel Anodonta anatina infected by the digenean trematode Echinoparyphium recurvatum, and the snail Viviparus viviparus infected by both E. recurvatum and Echinostoma sp. By analysing the impact of temporal parasite dispersal, host species and size, and the impact of coinfection (moving from broader environmental factors to within-host dynamics), we show that neither assumption holds true, but at different ecological scales. The assumption that closely related parasites can be functionally grouped is challenged when considering dispersal to the host (i.e. larger scales), while the assumption that the same factors will drive infection dynamics for a single parasite across multiple host species is challenged when considering within-host interspecific competition (i.e. smaller scales). Our results demonstrate that host identity, parasite identity and ecological scale require simultaneous consideration in studies of parasite community composition and transmission.

A mechanistic framework of enemy release.

The enemy release hypothesis (ERH) is the best-known hypothesis explaining high performance (e.g. rapid population growth) of exotic species. However, the current framing of the ERH does not explicitly link evidence of enemy release with exotic performance. This leads to uncertainty regarding the role of enemy release in biological invasions. Here, we demonstrate that the effect of enemy release on exotic performance is the product of three factors: enemy impact, enemy diversity, and host adaptation. These factors are modulated by seven contexts: time since introduction, resource availability, phylogenetic relatedness of exotic and native species, host-enemy asynchronicity, number of introduction events, type of enemy, and strength of growth-defence trade-offs. ERH-focused studies frequently test different factors under different contexts. This can lead to inconsistent findings, which typifies current evidence for the ERH. For example, over 80% of meta-analyses fail to consider ecological contexts which can alter study findings; we demonstrate this by re-analysing a recent ERH synthesis. Structuring the ERH around factors and contexts promotes generalisable predictions about when and where exotic species may benefit from enemy release, empowering effective management. Our mechanistic factor-context framework clearly lays out the evidence required to support the ERH, unifies many enemy-related invasion hypotheses, and enhances predictive capacity.

Parasites in biodiversity conservation: friend or foe?

Parasites stabilise food webs and facilitate species coexistence but can also lead to population- or species-level extinctions. So, in biodiversity conservation, are parasites friends or foes? This question is misleading: it implies that parasites are not part of biodiversity. Greater integration of parasites into global biodiversity and ecosystem conservation efforts is required.

Factors at multiple scales drive parasite community structure.

Understanding how ecological communities are assembled remains a key goal of ecosystem ecology. Because communities are hierarchical, factors acting at multiple scales can contribute to patterns of community structure. Parasites provide a natural system to explore this idea, as they exist as discrete communities within host individuals, which are themselves part of a community and metacommunity. We aimed to understand the relative contribution of multi-scale drivers in parasite community assembly and assess how patterns at one level may mask those occurring at another. Specifically, we wanted to disentangle patterns caused by passive sampling from those determined by ecological drivers, and how these vary with scale. We applied a Markov Random Fields model and assessed measures of ß-diversity and nestedness for 420 replicate parasite infracommunities (parasite assemblages in host individuals) across two freshwater mussel host species, three sites and two time periods, comparing our results to simulations from four different ecologically relevant null models. We showed that ß-diversity between sites (explaining 25% of variation in parasite distribution) and host species (41%) is greater than expected, and ß-diversity between individual hosts is smaller than expected, even after accounting for parasite prevalence and characteristics of host individuals. Furthermore, parasite communities were significantly less nested than expected once parasite prevalence and host characteristics were both accounted for, but more nested than expected otherwise, suggesting a degree of modularity at the within-host level that is masked if underlying host and parasite characteristics are not taken into account. The Markov Random Fields model provided evidence for possible competitive within-host parasite interactions, providing a mechanism for the observed infracommunity modularity. An integrative approach that examines factors at multiple scales is necessary to understand the composition of ecological communities. Furthermore, patterns at one level can alter the interpretation of ecologically important drivers at another if variation at higher scales is not accounted for.

Mussel parasite richness and risk of extinction.

Parasite conservation is important for the maintenance of ecosystem diversity and function. Conserving parasites relies first on understanding parasite biodiversity and second on estimating the extinction risk to that biodiversity. Although steps have been taken independently in both these areas, previous studies have overwhelmingly focused on helminths in vertebrate hosts over broad scales, providing low resolution and excluding a large proportion of possible host and parasite diversity. We estimated both total obligate parasite richness and parasite extinction risk in freshwater mussels (Unionidae and Margaritiferidae) from Europe and the United States to provide a case study for considering parasite conservation in a severely understudied system. We used currently reported host-parasite relationships to extrapolate parasite diversity to all possible mussel hosts and then used the threat levels of those hosts to estimate the extinction risk for both described and undescribed parasites. An estimated 67% of parasite richness in freshwater mussels is undescribed and over 80% of the most host-specific groups (digenean trematodes and ciliates) are undescribed. We estimated that 21% of this total parasite fauna is at immediate risk of extinction, corresponding to 60 unique species, many of which will likely go extinct before being described. Given the important roles parasites play in community structure and function and the strong ecosystem engineering capacities of freshwater mussels, such extinctions are likely to severely affect freshwater ecosystems. Our detailed study of mussel parasites provides compelling evidence for the hidden conservation threat to parasites through extinction cascades and shows parasites are deserving of immediate attention.

La conservación de parásitos es importante para el mantenimiento de la diversidad y funcionamiento de los ecosistemas. La conservación de parásitos depende en primera instancia del entendimiento de la biodiversidad de parásitos y, en segunda, de la estimación del riesgo de extinción de esa biodiversidad. Mientras que se han tomado medidas en ambas áreas, estudios previos se han enfocado abrumadoramente en helmintos de hospederos vertebrados, proporcionando baja resolución y excluyendo a una amplia proporción de una probable diversidad de hospederos y parásitos. Estimamos tanto la riqueza de parásitos obligados como el riesgo de extinción de mejillones de agua dulce (Unionidae y Margaritiferidae) de Europa y Estados Unidos para proporcionar un caso de estudio para considerar la conservación de parásitos en un sistema severamente poco estudiado. Utilizamos las relaciones hospedero-parásito registradas hasta la fecha para extrapolar la diversidad de parásitos a todas las especies posibles de mejillones hospederos y luego utilizamos los niveles de amenaza de aquellos hospederos para estimar el riesgo de extinción tanto para parásitos descritos y no descritos. Alrededor de 67% de la riqueza de parásitos de mejillones de agua dulce no esta descrito, así como mas de 80% de los grupos específicos de hospederos (trematodos digeneos y ciliados) tampoco están descritos. Estimamos que 21% del total de esta fauna de parásitos está en riesgo inminente de extinción, correspondiendo a 60 especies únicas, muchas de las cuales probablemente se extinguirán antes de ser descritas. Dado la importancia del papel que desempeñan los parásitos en la estructura y función de la comunidad y las notables capacidades de los mejillones de agua dulce para la ingeniería del ecosistema, es muy probable que tales extinciones afecten severamente a los ecosistemas dulceacuícolas. Nuestro estudio detallado de los parásitos de mejillones proporciona evidencia convincente de la amenaza oculta para los parásitos mediante cascadas de extinción y muestra que los parásitos son merecedores de atención inmediata.

Abundance data applied to a novel model invertebrate host shed new light on parasite community assembly in nature.

Understanding how environmental drivers influence the assembly of parasite communities, in addition to how parasites may interact at an infracommunity level, are fundamental requirements for the study of parasite ecology. Knowledge of how parasite communities are assembled will help to predict the risk of parasitism for hosts, and model how parasite communities may change under variable conditions. However, studies frequently rely on presence-absence data and examine multiple host species or sites, metrics which may be too coarse to characterise nuanced within-host patterns. We utilised a novel host system, the freshwater mussel Anodonta anatina, to investigate the drivers of community structure and explore parasite interactions. In addition, we aimed to highlight consistencies and inconsistencies between PA and abundance data. Our analysis incorporated 14 parasite taxa and 720 replicate infracommunities. Using Redundancy Analysis, a joint species distribution model and a Markov random field approach, we modelled the impact of both host-level and environment-level characteristics on parasite structure, as well as parasite-parasite correlations after accounting for all other factors. This approach was repeated for both the presence and abundance of all parasites. We demonstrated that the regional species pool, individual host characteristics (mussel length and gravidity) and predicted parasite-parasite interactions are all important but to varying degrees across parasite species, suggesting that applying generalities to parasite community construction is too simplistic. Furthermore, we showed that PA data fail to capture important density-dependent effects of parasite load for parasites with high abundance, and in general performs poorly for high-intensity parasites. Host and parasite traits, as well as broader environmental factors, all contribute to parasite community structure, emphasising that an integrated approach is required to study community assembly. However, care must be taken with the data used to infer patterns, as presence-absence data may lead to incorrect ecological inference.

An efficient photograph-based quantitative method for assessing castrating trematode parasites in bivalve molluscs.

Parasitic castration of bivalves by trematodes is common, and may significantly reduce the reproductive capacity of ecologically important species. Understanding the intensity of infection is desirable, as it can indicate the time that has passed since infection, and influence the host's physiological and reproductive response. In addition, it is useful to know the developmental stage of the trematode, to understand trematode population trends and reproductive success. However, most existing methods (e.g. visually estimating the degree of infection) to assess intensity are approximate only and not reproducible. Here, we present a method to accurately quantify the percentage of bivalve gonad filled with digenean trematode tissue, based on small squashes of gonad tissue rapidly photographed under light microscopy. A maximum of 15 photographs is required to determine the percentage of the whole gonad occupied by trematodes with a minimum of 90% confidence, with smaller mussels requiring fewer. In addition, the stage of trematode infection can be assessed because full sporocysts, spent sporocysts and free cercariae are clearly distinguishable. Although variation exists in the distribution of trematodes in gonad tissue, and thus in the estimate of percentage of the gonad filled with trematodes, this method represents a marked improvement on current coarse assessments of infection which typically focus on binary presence/absence measures. This technique can be used to facilitate a more sophisticated understanding of host-parasite interactions in bivalves, and can inform the conservation and reproductive biology of environmentally crucial species.

Multi-gene incongruence consistent with hybridisation in Cladocopium (Symbiodiniaceae), an ecologically important genus of coral reef symbionts.

Coral reefs rely on their intracellular dinoflagellate symbionts (family Symbiodiniaceae) for nutritional provision in nutrient-poor waters, yet this association is threatened by thermally stressful conditions. Despite this, the evolutionary potential of these symbionts remains poorly characterised. In this study, we tested the potential for divergent Symbiodiniaceae types to sexually reproduce (i.e. hybridise) within Cladocopium, the most ecologically prevalent genus in this family. With sequence data from three organelles (cob gene, mitochondrion; psbAncr region, chloroplast; and ITS2 region, nucleus), we utilised the Incongruence Length Difference test, Approximately Unbiased test, tree hybridisation analyses and visual inspection of raw data in stepwise fashion to highlight incongruences between organelles, and thus provide evidence of reticulate evolution. Using this approach, we identified three putative hybrid Cladocopium samples among the 158 analysed, at two of the seven sites sampled. These samples were identified as the common Cladocopium types C40 or C1 with respect to the mitochondria and chloroplasts, but the rarer types C3z, C3u and C1# with respect to their nuclear identity. These five Cladocopium types have previously been confirmed as evolutionarily distinct and were also recovered in non-incongruent samples multiple times, which is strongly suggestive that they sexually reproduced to produce the incongruent samples. A concomitant inspection of next generation sequencing data for these samples suggests that other plausible explanations, such as incomplete lineage sorting or the presence of co-dominance, are much less likely. The approach taken in this study allows incongruences between gene regions to be identified with confidence, and brings new light to the evolutionary potential within Symbiodiniaceae.