Non-linear effects of non-host diversity on the removal of free-living infective stages of parasites.

Among the ecological functions and services of biodiversity is the potential buffering of diseases through dilution effects where increased biodiversity results in a reduction in disease risk for humans and wildlife hosts. Whether such effects are a universal phenomenon is still under intense debate and diversity effects are little studied in cases when non-host organisms remove free-living parasite stages during their transmission from one host to the next by consumption or physical obstruction. Here, we investigated non-host diversity effects on the removal of cercarial stages of trematodes, ubiquitous parasites in aquatic ecosystems. In laboratory experiments using response surface designs, varying both diversity and density at same time, we compared three combinations of two non-hosts at four density levels: predatory crabs that actively remove cercariae from the water column via their mouth parts and gills, filter feeding oysters that passively filter cercariae from the water column while not becoming infected themselves, and seaweed which physically obstructs cercariae. The addition of a second non-host did not generally result in increased parasite removal but neutralised, amplified or reduced the parasite removal exerted by the first non-host, depending on the density and non-host combination. These non-linear non-host diversity effects were probably driven by intra- and interspecific interactions and suggest the need to integrate non-host diversity effects in understanding the links between community diversity and infection risk.

Effect of predation risk on parasite transmission from first to second intermediate trematode hosts.

Predators can affect parasite-host interactions when directly preying on hosts or their parasites. However, predators may also have non-consumptive indirect effects on parasite-host interactions when hosts adjust their behaviour or physiology in response to predator presence. In this study, we examined how chemical cues from a predatory marine crab affect the transmission of a parasitic trematode from its first (periwinkle) to its second (mussel) intermediate host. Laboratory experiments revealed that chemical cues from crabs lead to a threefold increase in the release of trematode cercariae from periwinkles as a result of increased periwinkle activity. This positive effect on transmission was contrasted by a 10-fold reduction in cercarial infection rates in the second intermediate host when we experimentally exposed mussels to cercariae and predator cues. The low infection rates were caused by a substantial reduction in mussel filtration activity in the presence of predator cues, preventing cercariae from entering the mussels. To assess the combined net effect of both processes, we conducted a transmission experiment between infected periwinkles and uninfected mussels. Infection levels of mussels in the treatments with crab cues were sevenfold lower than in mussels without crab chemical cues. This suggests that predation risk effects on mussel susceptibility can counteract the elevated parasite release from first intermediate hosts, with negative net effects on parasite transmission. These experiments highlight that predation risk effects on parasite transmission can have opposing directions at different stages of the parasite's life cycle. Such complex non-consumptive predation risk effects on parasite transmission may constitute an important indirect mechanism affecting prevalence and distribution patterns of parasites in different hosts across their life cycle.

Taxa-specific activity loss and mortality patterns in freshwater trematode cercariae under subarctic conditions.

Cercarial activity and survival are crucial traits for the transmission of trematodes. Temperature is particularly important, as faster depletion of limited cercarial energy reserves occurs at high temperatures. Seasonal climate conditions in high latitude regions may be challenging to complete trematode life cycle during the 6-month ice-free period, but temperature effects on the activity and survival of freshwater cercariae have not been previously identified. After experimentally simulating natural subarctic conditions during warmer and colder months (13 and 6°C), a statistical approach identifying changes in the tendency of cercarial activity loss and mortality data was used to detect differences in three trematode genera, represented by four taxa (Diplostomum spp., Apatemon spp., small- and large-sized Plagiorchis spp.). A strong temperature-dependent response was identified in both activity loss and mortality in all taxa, with Diplostomum spp. cercariae showing the most gradual changes compared to other taxa. Furthermore, whilst activity loss and mortality dynamics could not be divided into 'fish- vs invertebrate-infecting cercariae' groups, the detected taxa-specific responses in relation to life-history traits indicate the swimming behaviour of cercariae and energy allocation among larvae individuals as the main drivers. Cercariae exploit the short transmission window that allows a stable continuance of trematodes' life cycles in high-latitude freshwater ecosystems.

Effects of first intermediate host density, host size and salinity on trematode infections in mussels of the south-western Baltic Sea.

Trematode prevalence and abundance in hosts are known to be affected by biotic drivers as well as by abiotic drivers. In this study, we used the unique salinity gradient found in the south-western Baltic Sea to: (i) investigate patterns of trematode infections in the first intermediate host, the periwinkle Littorina littorea and in the downstream host, the mussel Mytilus edulis, along a regional salinity gradient (from 13 to 22) and (ii) evaluate the effects of first intermediate host (periwinkle) density, host size and salinity on trematode infections in mussels. Two species dominated the trematode community, Renicola roscovita and Himasthla elongata. Salinity, mussel size and density of infected periwinkles were significantly correlated with R. roscovita, and salinity and density correlated with H. elongata abundance. These results suggest that salinity, first intermediate host density and host size play an important role in determining infection levels in mussels, with salinity being the main major driver. Under expected global change scenarios, the predicted freshening of the Baltic Sea might lead to reduced trematode transmission, which may be further enhanced by a potential decrease in periwinkle density and mussel size.

High prevalences of disseminated neoplasia in the Baltic tellin Limecola balthica in the Wadden Sea.

The Baltic tellin Limecola balthica is one of the most common bivalves in intertidal areas in the Northern Hemisphere. Over the last 2 decades, the species has been suffering from a decrease in adult survival in the European Wadden Sea. While several factors such as global warming and fisheries have been suggested to influence the population dynamics of this bivalve mollusc, the potential role of diseases has never been investigated. In this study, we investigated whether disseminated neoplasia, a common proliferative disorder in bivalve molluscs, could play a potential role in the recent population decline of Baltic tellins in the Wadden Sea. We conducted a field survey in the Dutch Wadden Sea to (1) determine whether the disease occurs in Baltic tellins in the Wadden Sea and (2) quantify the occurrence and severity of the disease via histology. Disseminated neoplasia occurred in L. balthica at each of the 10 sampled locations with very high prevalences (21-89%) compared to those reported elsewhere for this species. The highest severity category was found in 8 to 87% of affected individuals, with severity generally increasing with prevalence. Disseminated neoplasia usually increases mortality among affected individuals and may also be associated with important sub-lethal effects, especially regarding gametogenesis. Thus, we suggest that disseminated neoplasia may play a key role in the population dynamics of the Baltic tellin, the extent of which remains to be investigated in future studies.

Micro- and macroparasite species richness in birds: The role of host life history and ecology.

Identifying the factors shaping variation in parasite diversity among host species is crucial to understand wildlife diseases. Although micro- and macroparasites may exert different selective pressures on their hosts, studies investigating the determinants of parasite species richness in animals have rarely considered this divide. Here, we investigated the role of host life history and ecology in explaining the species richness of helminths (macroparasites) and haemosporidians (microparasites) in birds world-wide. We collated data from multiple global datasets on diverse bird traits (longevity, body mass, coloniality, migration distance/tendency, geographic range size and dietary and habitat breadths) and the species richness of their helminth and haemosporidian parasites. We tested predictors of helminth and haemosporidian parasite richness using phylogenetic generalized linear mixed models in a Bayesian framework. We found that, after controlling for research effort and host phylogeny, the richness of helminths, but not of haemosporidians, increased with host longevity, range size, migration distance and dietary breadth. Overall, these correlates were also important across different helminth groups (acanthocephalans, cestodes, nematodes and trematodes), and two additional ones (body mass, coloniality) emerged as important for cestodes and acanthocephalans. We propose that long life spans may promote the diversity of helminth parasite assemblages over evolutionary time, thus resulting in richer helminth faunas. Similarly, longer-distance migrations, larger ranges and broader dietary breadths are likely to lead to greater encounter rates and the accumulation of trophically transmitted helminths. In contrast, vector-borne haemosporidians may be influenced more by factors related to vector ecology than by the host traits included in the analyses. The lack of strong associations between haemosporidian species richness and host characteristics emphasizes the need to find appropriate traits to model the distribution and diversity of parasites with different environmental preferences in order to anticipate disease emergence risks associated with global change.

How invasive oysters can affect parasite infection patterns in native mussels on a large spatial scale.

There are surprisingly few field studies on the role of invasive species on parasite infection patterns in native hosts. We investigated the role of invasive Pacific oysters (Magallana gigas) in determining parasite infection levels in native blue mussels (Mytilus edulis) in relation to other environmental and biotic factors. Using hierarchical field sampling covering three spatial scales along a large intertidal ecosystem (European Wadden Sea), we found strong spatial differences in infection levels of five parasite species associated with mussels and oysters. We applied mixed models to analyse the associations between parasite prevalence and abundance in mussels and oysters, and 12 biological and environmental factors. For each parasite-host relationship, an optimal model (either a null, one-factor or two-factor model) was selected based on AIC scores. We found that the density of invasive oysters contributed to three of the 12 models. Other biological factors such as host size (six models), and the density of target or alternative host species (five models) contributed more frequently to the best models. Furthermore, for parasite species infecting both mussels and oysters, parasite population densities were higher in native mussels, attributed to the higher densities of mussels. Our results indicate that invasive species can affect parasite infection patterns in native species in the field, but that their relative contribution may be further mediated by other biological and environmental parameters. These results stress the usefulness of large-scale field studies for detailed assessments of the mechanisms underlying the impacts of invasive species on native host communities.

Consumer and host body size effects on the removal of trematode cercariae by ambient communities.

Parasite transmission can be altered via the removal of parasites by the ambient communities in which parasite-host interactions take place. However, the mechanisms driving parasite removal remain poorly understood. Using marine trematode cercariae as a model system, we investigated the effects of consumer and host body size on parasite removal rates. Laboratory experiments revealed that consumer or host body size significantly affected cercarial removal rates in crabs, oysters and cockles but not in shrimps. In general, cercarial removal rates increased with consumer (crabs and oysters) and host (cockles) body size. For the filter feeding oysters and cockles, the effects probably relate to their feeding activity which is known to correlate with bivalve size. Low infection levels found in cockle hosts suggest that parasite removal by hosts also leads to significant mortality of infective stages. The size effects of crab and shrimp predators on cercarial removal rates were more complex and did not show an expected size match-mismatch between predators and their cercarial prey, suggesting that parasite removal rates in predators are species-specific. We conclude that to have a comprehensive understanding of parasite removal by ambient communities, more research into the various mechanisms of cercarial removal is required.

Trophic relationship between the invasive parasitic copepod Mytilicola orientalis and its native blue mussel (Mytilus edulis) host.

Invasive parasites can spill over to new hosts in invaded ecosystems with often unpredictable trophic relationships in the newly arising parasite-host interactions. In European seas, the intestinal copepod Mytilicola orientalis was co-introduced with Pacific oysters (Magallana gigas) and spilled over to native blue mussels (Mytilus edulis), with negative impacts on the condition of infected mussels. However, whether the parasite feeds on host tissue and/or stomach contents is yet unknown. To answer this question, we performed a stable isotope analysis in which we included mussel host tissue and the primary food sources of the mussels, microphytobenthos (MPB) and particulate organic matter (POM). The copepods were slightly enriched in δ15N (mean Δ15N ± s.d.; 1·22 ± 0·58‰) and δ13C (Δ13C 0·25 ± 0·32‰) with respect to their host. Stable isotope mixing models using a range of trophic fractionation factors indicated that host tissue was the main food resource with consistent additional contributions of MPB and POM. These results suggest that the trophic relationship of the invasive copepod with its mussel host is parasitic as well as commensalistic. Stable isotope studies such as this one may be a useful tool to unravel trophic relationships in new parasite-host associations in the course of invasions.

Parasites as prey: the effect of cercarial density and alternative prey on consumption of cercariae by four non-host species.

In parasites with complex life cycles the transmission of free-living infective stages can be influenced by ambient community diversity, in particular via predation. Here, we experimentally investigated whether parasite density and the presence of alternative prey can alter predation rates on free-living cercarial stages of a marine trematode by several non-host predators. All four predator species consumed increasing numbers of cercariae with an increase in cercarial density, indicating that the removal of cercariae by predators is effective over a range of natural densities as well as in the presence of alternative prey for a number of predators typical of marine ecosystems. However, the relative removal rates and the effects of cercarial density and alternative prey differed among predator species. In barnacles and shrimps, significant interactive effects of cercarial density and alternative prey on cercarial predation occurred while in oysters and crabs cercarial removal rates were unaffected by both factors. As changes in cercarial densities directly translate into changes in infection levels in down-stream hosts in this parasite-host system, the observed predator-specific responses suggest that cercarial predation effects on disease risks will depend on the specific species composition of ambient communities and not on non-host biodiversity per se.

Effect of dose and frequency of exposure to infectious stages on trematode infection intensity and success in mussels.

Marine parasites such as trematodes often compromise the fitness of their hosts. Such effects are generally considered to be density-dependent, i.e. the greater the infection intensity in the host, the greater the detrimental impact on host fitness. However, the mechanisms determining infection in marine hosts are still poorly understood. Here, we investigated the effect of cercarial dose and exposure frequency (single vs. trickle infections) of a marine trematode parasite, Himasthla elongata (Trematoda: Echinostomatidae), on infection intensity and success in its second intermediate host, the blue mussel Mytilus edulis, an abundant and widely distributed bivalve in European coastal waters. In our laboratory experiment, we tested 4 levels of parasite doses and showed that mussels faced higher parasite infection intensity at higher doses of cercarial exposure and that they acquired more infections when repeatedly exposed to smaller doses compared to a single high dose. However, the infection success of cercariae did not differ among 4 dose levels but was only significantly different between trickle and single exposures. This indicates that cercariae were not subjected to a dose-dependent regulation of their infectivity, suggesting that infection intensity in mussels is largely driven by factors mediating the abundance of infective stages. With the combined investigation of the effect of cercarial dose and exposure frequency at realistic dose levels, our study contributes to our currently very limited understanding of the determinants of infection intensity in marine hosts and highlights the usefulness of experimental studies in advancing our knowledge in this field.

Parasites affect food web structure primarily through increased diversity and complexity.

Comparative research on food web structure has revealed generalities in trophic organization, produced simple models, and allowed assessment of robustness to species loss. These studies have mostly focused on free-living species. Recent research has suggested that inclusion of parasites alters structure. We assess whether such changes in network structure result from unique roles and traits of parasites or from changes to diversity and complexity. We analyzed seven highly resolved food webs that include metazoan parasite data. Our analyses show that adding parasites usually increases link density and connectance (simple measures of complexity), particularly when including concomitant links (links from predators to parasites of their prey). However, we clarify prior claims that parasites "dominate" food web links. Although parasites can be involved in a majority of links, in most cases classic predation links outnumber classic parasitism links. Regarding network structure, observed changes in degree distributions, 14 commonly studied metrics, and link probabilities are consistent with scale-dependent changes in structure associated with changes in diversity and complexity. Parasite and free-living species thus have similar effects on these aspects of structure. However, two changes point to unique roles of parasites. First, adding parasites and concomitant links strongly alters the frequency of most motifs of interactions among three taxa, reflecting parasites' roles as resources for predators of their hosts, driven by trophic intimacy with their hosts. Second, compared to free-living consumers, many parasites' feeding niches appear broader and less contiguous, which may reflect complex life cycles and small body sizes. This study provides new insights about generic versus unique impacts of parasites on food web structure, extends the generality of food web theory, gives a more rigorous framework for assessing the impact of any species on trophic organization, identifies limitations of current food web models, and provides direction for future structural and dynamical models.

Effects of predation risk on parasite-host interactions and wildlife diseases.

Landscapes of fear can determine the dynamics of entire ecosystems. In response to perceived predation risk, prey can show physiological, behavioral, or morphological trait changes to avoid predation. This in turn can indirectly affect other species by modifying species interactions (e.g., altered feeding), with knock-on effects, such as trophic cascades, on the wider ecosystem. While such indirect effects stemming from the fear of predation have received extensive attention for herbivore-plant and predator-prey interactions, much less is known about how they alter parasite-host interactions and wildlife diseases. In this synthesis, we present a conceptual framework for how predation risk-as perceived by organisms that serve as hosts-can affect parasite-host interactions, with implications for infectious disease dynamics. By basing our approach on recent conceptual advances with respect to predation risk effects, we aim to expand this general framework to include parasite-host interactions and diseases. We further identify pathways through which parasite-host interactions can be affected, for example, through altered parasite avoidance behavior or tolerance of hosts to infections, and discuss the wider relevance of predation risk for parasite and host populations, including heuristic projections to population-level dynamics. Finally, we highlight the current unknowns, specifically the quantitative links from individual-level processes to population dynamics and community structure, and emphasize approaches to address these knowledge gaps.

Warming effects on the life cycles of two parasitic copepods with different invasion histories.

Climate change may exacerbate the impact of invasive parasites from warmer climates through pre-existing temperature adaptations. We investigated temperature impacts on two closely related marine parasitic copepod species that share the blue mussel (Mytilus edulis) as host: Mytilicola orientalis has invaded the system from a warmer climate <20 years ago, whereas its established congener Mytilicola intestinalis has had >90 years to adapt. In laboratory experiments with temperatures 10-26°C, covering current and future temperatures as well as heat waves, the development of both life cycle stages of both species accelerated with increasing temperature. In the parasitic stages, the growth of the established invader increased evenly from 10°C to 22°C, whereas the recent invader barely grew at all at 10°C and grew faster already at 18°C. In contrast, temperature had little effect on the transition success between life cycle stages. However, the highest temperature (26°C) limited the egg development success of the established invader and the host entry success of both species, whereas the infection success of the established invader increased at 18°C and 22°C. In general, our experiments indicate that the main effect of temperature on both species is through development speed and not life cycle stage transition success. Based on regional long-term temperature data and predictions, the numbers of completed life cycles per year will increase for both parasites. The established invader seems better adapted for low current temperatures (around 10°C), whereas the more recent invader barely develops at these temperatures but can cope in high temperatures (around 26°C). Hence, pre-existing temperature adaptations of the recent invader may allow the species to better cope with heat waves.

Phylogeny determines the role of helminth parasites in intertidal food webs.

1. Parasites affect interactions among species in food webs and should be considered in any analysis of the structure, dynamics or resilience of trophic networks. 2. However, the roles of individual parasite species, such as their importance as connectors within the network, and what factors determine these roles, are yet to be investigated. Here, we test the hypotheses that the species roles of trematode, cestode and nematode parasites in aquatic food webs are influenced by the type of definitive host they use, and also determined by their phylogenetic affiliations. 3. We quantified the network role of 189 helminth species from six highly resolved intertidal food webs. We focused on four measures of centrality (node degree, closeness centrality, betweenness centrality and eigenvalue centrality), which characterize each parasite's position within the web, and on relative connectedness of a parasite species to taxa in its own module vs. other modules of the web (within-module degree and participation coefficient). 4. All six food webs displayed a significant modular structure, that is, they consisted of subsets of species interacting mostly with each other and less with species from other subsets. We demonstrated that the parasites themselves are not generating this modularity, though they contribute to intermodule connectivity. 5. Mixed-effects models revealed only a modest influence of the type of definitive host used (bird or fish) and of the web of origin on the different measures of parasite species roles. In contrast, the taxonomic affiliations of the parasites, included in the models as nested random factors, accounted for 37-93% of the total variance, depending on the measure of species role. 6. Our findings indicate that parasites are important intermodule connectors and thus contribute to web cohesion. We also uncover a very strong phylogenetic signal in parasite species roles, suggesting that the role of any parasite species in a food web, including new invasive species, is to some extent predictable based solely on its taxonomic affiliations.

Anthropogenic noise pollution and wildlife diseases.

There is a global rise in anthropogenic noise and a growing awareness of its negative effects on wildlife, but to date the consequences for wildlife diseases have received little attention. In this paper, we discuss how anthropogenic noise can affect the occurrence and severity of infectious wildlife diseases. We argue that there is potential for noise impacts at three main stages of pathogen transmission and disease development: (i) the probability of preinfection exposure, (ii) infection upon exposure, and (iii) severity of postinfection consequences. We identify potential repercussions of noise pollution effects for wildlife populations and call for intensifying research efforts. We provide an overview of knowledge gaps and outline avenues for future studies into noise impacts on wildlife diseases.

Filtration and respiration responses of mussels (Mytilus edulis) to trematode parasite infections (Renicola roscovita) and transient heat exposure.

The mussel Mytilus edulis, a host to various trematode species, experiences performance decrements due to these infections. Yet, the impact magnitude and potential interactions with environmental stressors remain largely unexplored. This study scrutinizes the effect of Renicola roscovita infections on mussel filtration and respiration. We first assessed performance in both uninfected and lab-infected mussels at a mild temperature (16 °C), following an acute heat ramp to 30.5 °C and subsequent cooling. The experiment revealed neither a significant direct impact of the infection on the mussels' performance, nor any significant interplay between the infection and temperature variations. To account for possible infection effects obscured by low sample sizes or mussel size disparities, we conducted a reassessment at 16 °C using both small and large mussels. Infection notably hampered filtration in large mussels, with a marginal impact on smaller ones. A positive correlation was found between infection intensity and mussel filtration capacity, though the infection had no discernible impact on respiration. Our consistent finding of an 11-12 % infection effect size across all experiments indicates a slight reduction in mussel filtration due to trematode infections. While the exacerbating effect of transient heat stress on the infection's impact on filtration was not statistically significant, future investigations should explore potential interactions with prolonged heat stress. Our findings underscore the nuanced ways in which parasitic infections can influence marine bivalve physiology, emphasizing the need for more comprehensive studies that incorporate environmental stressors, such as heat stress, to fully elucidate the impact of parasitism on marine ecosystem health and resilience.

Thermal optima of cercarial emergence in trematodes from a marine high-temperature ecosystem, the Persian Gulf.

Global warming may alter the dynamics of infectious diseases by affecting important steps in the transmission of pathogens and parasites. In trematode parasites, the emergence of cercarial stages from their hosts is temperature-dependent, being highest around a thermal optimum. If environmental temperatures exceed this optimum as a consequence of global warming, this may affect cercarial transmission. However, our knowledge of cercarial emergence patterns of species from high temperature environments is currently very limited. Here, we investigated the effect of temperature on the emergence of two common trematode species from an abundant mud snail Pirenella cingulata in the Persian Gulf, the warmest sea on Earth. Infected snails were incubated in the laboratory at 6 temperatures from 10 to 40 °C for 3 days. We found an optimal temperature for cercarial emergence of 32.0 °C and 33.5 °C for Acanthotrema tridactyla and Cyathocotylidae gen. sp., respectively, which are the warmest recorded thermal optima for any aquatic trematode species. Emergence of both species dropped at 40 °C, suggesting upper thermal limits to emergence. Overall, Persian Gulf trematodes may be among the most heat-tolerant marine trematode species, indicating a potential for dispersing to regions that will continue to warm in the future.

Parasite effects on host's trophic and isotopic niches.

Wild animals are usually infected with parasites that can alter their hosts' trophic niches in food webs as can be seen from stable isotope analyses of infected versus uninfected individuals. The mechanisms influencing these effects of parasites on host isotopic values are not fully understood. Here, we develop a conceptual model to describe how the alteration of the resource intake or the internal resource use of hosts by parasites can lead to differences of trophic and isotopic niches of infected versus uninfected individuals and ultimately alter resource flows through food webs. We therefore highlight that stable isotope studies inferring trophic positions of wild organisms in food webs would benefit from routine identification of their infection status.

The seafloor from a trait perspective. A comprehensive life history dataset of soft sediment macrozoobenthos.

Biological trait analysis (BTA) is a valuable tool for evaluating changes in community diversity and its link to ecosystem processes as well as environmental and anthropogenic perturbations. Trait-based analytical techniques like BTA rely on standardised datasets of species traits. However, there are currently only a limited number of datasets available for marine macrobenthos that contain trait data across multiple taxonomic groups. Here, we present an open-access dataset of 16 traits for 235 macrozoobenthic species recorded throughout multiple sampling campaigns of the Dutch Wadden Sea; a dynamic soft bottom system where humans have long played a substantial role in shaping the coastal environment. The trait categories included in this dataset cover a variety of life history strategies that are tightly linked to ecosystem functioning and the resilience of communities to (anthropogenic) perturbations and can advance our understanding of environmental changes and human impacts on the functioning of soft bottom systems.