Parasites alter food-web topology of a subarctic lake food web and its pelagic and benthic compartments.

We compared three sets of highly resolved food webs with and without parasites for a subarctic lake system corresponding to its pelagic and benthic compartments and the whole-lake food web. Key topological food-web metrics were calculated for each set of compartments to explore the role parasites play in food-web topology in these highly contrasting webs. After controlling for effects from differences in web size, we observed similar responses to the addition of parasites in both the pelagic and benthic compartments demonstrated by increases in trophic levels, linkage density, connectance, generality, and vulnerability despite the contrasting composition of free-living and parasitic species between the two compartments. Similar effects on food-web topology can be expected with the inclusion of parasites, regardless of the physical characteristics and taxonomic community compositions of contrasting environments. Additionally, similar increases in key topological metrics were found in the whole-lake food web that combines the pelagic and benthic webs, effects that are comparable to parasite food-web analyses from other systems. These changes in topological metrics are a result of the unique properties of parasites as infectious agents and the links they participate in. Trematodes were key contributors to these results, as these parasites have distinct characteristics in aquatic systems that introduce new link types and increase the food web's generality and vulnerability disproportionate to other parasites. Our analysis highlights the importance of incorporating parasites, especially trophically transmitted parasites, into food webs as they significantly alter key topological metrics and are thus essential for understanding an ecosystem's structure and functioning.

Parasite diversity at isolated, disturbed hydrothermal vents.

Habitat isolation and disturbance are important regulators of biodiversity, yet it remains unclear how these environmental features drive differences in parasite diversity between ecosystems. We test whether the biological communities in an isolated, frequently disturbed marine ecosystem (deep-sea hydrothermal vents) have reduced parasite richness and relatively fewer parasite species with indirect life cycles (ILCs) compared to ecosystems that are less isolated and less disturbed. We surveyed the parasite fauna of the biological community at the 9°50'N hydrothermal vent field on the East Pacific Rise and compared it to similar datasets from a well-connected and moderately disturbed ecosystem (kelp forest) and an isolated and undisturbed ecosystem (atoll sandflat). Parasite richness within host species did not differ significantly between ecosystems, yet total parasite richness in the vent community was much lower due to the low number of predatory fish species. Contrary to expectation, the proportion of ILC parasite species was not lower at vents due to a high richness of trematodes, while other ILC parasite taxa were scarce (nematodes) or absent (cestodes). These results demonstrate the success of diverse parasite taxa in an extreme environment and reinforce the importance of host diversity and food web complexity in governing parasite diversity.

Precision mapping of snail habitat provides a powerful indicator of human schistosomiasis transmission.

Recently, the World Health Organization recognized that efforts to interrupt schistosomiasis transmission through mass drug administration have been ineffective in some regions; one of their new recommended strategies for global schistosomiasis control emphasizes targeting the freshwater snails that transmit schistosome parasites. We sought to identify robust indicators that would enable precision targeting of these snails. At the site of the world's largest recorded schistosomiasis epidemic-the Lower Senegal River Basin in Senegal-intensive sampling revealed positive relationships between intermediate host snails (abundance, density, and prevalence) and human urogenital schistosomiasis reinfection (prevalence and intensity in schoolchildren after drug administration). However, we also found that snail distributions were so patchy in space and time that obtaining useful data required effort that exceeds what is feasible in standard monitoring and control campaigns. Instead, we identified several environmental proxies that were more effective than snail variables for predicting human infection: the area covered by suitable snail habitat (i.e., floating, nonemergent vegetation), the percent cover by suitable snail habitat, and size of the water contact area. Unlike snail surveys, which require hundreds of person-hours per site to conduct, habitat coverage and site area can be quickly estimated with drone or satellite imagery. This, in turn, makes possible large-scale, high-resolution estimation of human urogenital schistosomiasis risk to support targeting of both mass drug administration and snail control efforts.

Long-term change in the parasite burden of shore crabs (Hemigrapsus oregonensis and Hemigrapsus nudus) on the northwestern Pacific coast of North America.

The abundances of free-living species have changed dramatically in recent decades, but little is known about change in the abundance of parasitic species. We investigated whether populations of several parasites have shifted over time in two shore crab hosts, Hemigrapsus oregonensis and Hemigrapsus nudus, by comparing the prevalence and abundance of three parasite taxa in a historical dataset (1969-1970) to contemporary parasite abundance (2018-2020) for hosts collected from 11 intertidal sites located from Oregon, USA, to British Columbia, Canada. Our data suggest that the abundance of the parasitic isopod Portunion conformis has varied around a stable mean for the past 50 years. No change over time was observed for larval acanthocephalans. However, larval microphallid trematodes increased in prevalence over time among H. oregonensis hosts, from a mean of 8.4-61.8% between the historical and contemporary time points. The substantial increase in the prevalence of larval microphallid trematodes could be owing to increased abundances of their bird final hosts, increased production of parasite infective stages by snail intermediate hosts or both. Our study highlights the variability among parasite species in their temporal trajectories of change.

Parasite and host biomass and reproductive output in barnacle populations in the rocky intertidal zone.

The rocky intertidal zone has a long history of ecological study with barnacles frequently serving as a model system to explore foundational theories. Parasites are often ignored in community ecology studies, and this particularly holds for true for the rocky intertidal zone. We explore the role of the isopod parasite, Hemioniscus balani, on its host, the acorn barnacle, Chthamalus fissus. We use the currencies of biomass and reproduction measured at the individual level, then applied to the population level, to evaluate the importance of this parasite to barnacle populations. We found H. balani can comprise substantial biomass in 'apparent' barnacle populations, sometimes even equaling barnacle biomass. Additionally, parasite reproduction sometimes matched barnacle reproduction. Thus, parasites divert substantial energy flow from the barnacle population and to near-shore communities in the form of parasite larvae. Parasites appeared to decrease barnacle reproduction per area. Potentially, this parasite may control barnacle populations, depending on the extent to which heavily infected barnacle populations contribute to barnacle populations at larger scales. These findings regarding the importance of a particular parasite for host population dynamics in this well studied ecosystem call for the integration of disease dynamics into community ecological studies of the rocky intertidal zone.

Reduced transmission of human schistosomiasis after restoration of a native river prawn that preys on the snail intermediate host.

Eliminating human parasitic disease often requires interrupting complex transmission pathways. Even when drugs to treat people are available, disease control can be difficult if the parasite can persist in nonhuman hosts. Here, we show that restoration of a natural predator of a parasite's intermediate hosts may enhance drug-based schistosomiasis control. Our study site was the Senegal River Basin, where villagers suffered a massive outbreak and persistent epidemic after the 1986 completion of the Diama Dam. The dam blocked the annual migration of native river prawns (Macrobrachium vollenhoveni) that are voracious predators of the snail intermediate hosts for schistosomiasis. We tested schistosomiasis control by reintroduced river prawns in a before-after-control-impact field experiment that tracked parasitism in snails and people at two matched villages after prawns were stocked at one village's river access point. The abundance of infected snails was 80% lower at that village, presumably because prawn predation reduced the abundance and average life span of latently infected snails. As expected from a reduction in infected snails, human schistosomiasis prevalence was 18 ± 5% lower and egg burden was 50 ± 8% lower at the prawn-stocking village compared with the control village. In a mathematical model of the system, stocking prawns, coupled with infrequent mass drug treatment, eliminates schistosomiasis from high-transmission sites. We conclude that restoring river prawns could be a novel contribution to controlling, or eliminating, schistosomiasis.

Seroprevalence of Baylisascaris procyonis Infection among Humans, Santa Barbara County, California, USA, 2014-2016.

Baylisascaris procyonis (raccoon roundworm) infection is common in raccoons and can cause devastating pathology in other animals, including humans. Limited information is available on the frequency of asymptomatic human infection. We tested 150 adults from California, USA, for B. procyonis antibodies; 11 were seropositive, suggesting that subclinical infection does occur.

Predation on transmission stages reduces parasitism: sea anemones consume transmission stages of a barnacle parasite.

While parasites serve as prey, it is unclear how the spatial distribution of parasite predators provides transmission control and influences patterns of parasitism. Because many of its organisms are sessile, the rocky intertidal zone is a valuable but little used system to understand spatial patterns of parasitism and elucidate the underlying mechanisms driving these patterns. Sea anemones and barnacles are important space competitors in the rocky intertidal zone along the Pacific coast of North America. Anemones are voracious, indiscriminate predators; thus, they may intercept infectious stages of parasites before they reach a host. We investigate whether a sea anemone protects an associated barnacle from parasitism by Hemioniscus balani, an isopod parasitic castrator. At Coal Oil Point, Santa Barbara, California USA, 29% of barnacles were within 1 cm from an anemone at the surveyed tidal height. Barnacles associated with anemones had reduced parasite prevalence and higher reproductive productivity than those remote from sea anemones. In the laboratory, anemones readily consumed the transmission stage of the parasite. Hence, anemone consumption of parasite transmission stages may provide a mechanism by which community context regulates parasite prevalence at a local scale. Our results suggest predation may be an important process providing parasite transmission control.

Two's a crowd? Crowding effect in a parasitic castrator drives differences in reproductive resource allocation in single vs double infections.

The 'crowding effect' is a result of competition by parasites within a host for finite resources. Typically, the severity of this effect increases with increasing numbers of parasites within a host and manifests in reduced body size and thus fitness. Evidence for the crowding effect is mixed - while some have found negative effects, others have found a positive effect of increased parasite load on parasite fitness. Parasites are consumers with diverse trophic strategies reflected in their life history traits. These distinctions are useful to predict the effects of crowding. We studied a parasitic castrator, a parasite that usurps host reproductive energy and renders the host sterile. Parasitic castrators typically occur as single infections within hosts. With multiple parasitic castrators, we expect strong competition and evidence of crowding. We directly assess the effect of crowding on reproductive success in a barnacle population infected by a unique parasitic castrator, Hemioniscus balani, an isopod parasite that infects and blocks reproduction of barnacles. We find (1) strong evidence of crowding in double infections, (2) increased frequency of double infections in larger barnacle hosts with more resources and (3) perfect compensation in egg production, supporting strong space limitation. Our results document that the effects of crowding are particularly severe for this parasitic castrator, and may be applicable to other castrators that are also resource or space limited.

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.

Independent origins of parasitism in Animalia.

Nearly half of all animals may have a parasitic lifestyle, yet the number of transitions to parasitism and their potential for species diversification remain unresolved. Based on a comprehensive survey of the animal kingdom, we find that parasitism has independently evolved at least 223 times in just 15 phyla, with the majority of identified independent parasitic groups occurring in the Arthropoda, at or below the level of Family. Metazoan parasitology is dominated by the study of helminthes; however, only 20% of independently derived parasite taxa belong to those groups, with numerous transitions also seen in Mollusca, Rotifera, Annelida and Cnidaria. Parasitism is almost entirely absent from deuterostomes, and although worm-like morphology and host associations are widespread across Animalia, the dual symbiotic and trophic interactions required for parasitism may constrain its evolution from antecedent consumer strategies such as generalist predators and filter feeders. In general, parasitic groups do not differ from their free-living relatives in their potential for speciation. However, the 10 largest parasitic clades contain 90% of described parasitic species, or perhaps 40% of all animal species. Hence, a substantial fraction of animal diversity on the Earth arose following these few transitions to a parasitic trophic strategy.

Does biodiversity protect humans against infectious disease?

Control of human infectious disease has been promoted as a valuable ecosystem service arising from the conservation of biodiversity. There are two commonly discussed mechanisms by which biodiversity loss could increase rates of infectious disease in a landscape. First, loss of competitors or predators could facilitate an increase in the abundance of competent reservoir hosts. Second, biodiversity loss could disproportionately affect non-competent, or less competent reservoir hosts, which would otherwise interfere with pathogen transmission to human populations by, for example, wasting the bites of infected vectors. A negative association between biodiversity and disease risk, sometimes called the "dilution effect hypothesis," has been supported for a few disease agents, suggests an exciting win-win outcome for the environment and society, and has become a pervasive topic in the disease ecology literature. Case studies have been assembled to argue that the dilution effect is general across disease agents. Less touted are examples in which elevated biodiversity does not affect or increases infectious disease risk for pathogens of public health concern. In order to assess the likely generality of the dilution effect, we review the association between biodiversity and public health across a broad variety of human disease agents. Overall, we hypothesize that conditions for the dilution effect are unlikely to be met for most important diseases of humans. Biodiversity probably has little net effect on most human infectious diseases but, when it does have an effect, observation and basic logic suggest that biodiversity will be more likely to increase than to decrease infectious disease risk.

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.

New parasites and predators follow the introduction of two fish species to a subarctic lake: implications for food-web structure and functioning.

Introduced species can alter the topology of food webs. For instance, an introduction can aid the arrival of free-living consumers using the new species as a resource, while new parasites may also arrive with the introduced species. Food-web responses to species additions can thus be far more complex than anticipated. In a subarctic pelagic food web with free-living and parasitic species, two fish species (arctic charr Salvelinus alpinus and three-spined stickleback Gasterosteus aculeatus) have known histories as deliberate introductions. The effects of these introductions on the food web were explored by comparing the current pelagic web with a heuristic reconstruction of the pre-introduction web. Extinctions caused by these introductions could not be evaluated by this approach. The introduced fish species have become important hubs in the trophic network, interacting with numerous parasites, predators and prey. In particular, five parasite species and four predatory bird species depend on the two introduced species as obligate trophic resources in the pelagic web and could therefore not have been present in the pre-introduction network. The presence of the two introduced fish species and the arrival of their associated parasites and predators increased biodiversity, mean trophic level, linkage density, and nestedness; altering both the network structure and functioning of the pelagic web. Parasites, in particular trophically transmitted species, had a prominent role in the network alterations that followed the introductions.

Evidence gaps and diversity among potential win-win solutions for conservation and human infectious disease control.

As sustainable development practitioners have worked to "ensure healthy lives and promote well-being for all" and "conserve life on land and below water", what progress has been made with win-win interventions that reduce human infectious disease burdens while advancing conservation goals? Using a systematic literature review, we identified 46 proposed solutions, which we then investigated individually using targeted literature reviews. The proposed solutions addressed diverse conservation threats and human infectious diseases, and thus, the proposed interventions varied in scale, costs, and impacts. Some potential solutions had medium-quality to high-quality evidence for previous success in achieving proposed impacts in one or both sectors. However, there were notable evidence gaps within and among solutions, highlighting opportunities for further research and adaptive implementation. Stakeholders seeking win-win interventions can explore this Review and an online database to find and tailor a relevant solution or brainstorm new solutions.

Social organization in a flatworm: trematode parasites form soldier and reproductive castes.

In some of the most complex animal societies, individuals exhibit a cooperative division of labour to form castes. The most pronounced types of caste formation involve reproductive and non-reproductive forms that are morphologically distinct. In colonies comprising separate or mobile individuals, this type of caste formation has been recognized only among the arthropods, sea anemones and mole-rats. Here, we document physical and behavioural caste formation in a flatworm. Trematode flatworm parasites undergo repeated clonal reproduction of 'parthenitae' within their molluscan hosts forming colonies. We present experimental and observational data demonstrating specialization among trematode parthenitae to form distinct soldier and reproductive castes. Soldiers do not reproduce, have relatively large mouthparts, and are much smaller and thinner than reproductives. Soldiers are also more active, and are disproportionally common in areas of the host where invasions occur. Further, only soldiers readily and consistently attack heterospecifics and conspecifics from other colonies. The division of labour described here for trematodes is strongly analogous to that characterizing other social systems with a soldier caste. The parallel caste formation in these systems, despite varying reproductive mode and taxonomic affiliation, indicates the general importance of ecological factors in influencing the evolution of social behaviour. Further, the 'recognition of self' and the defence of the infected host body from invading parasites are comparable to aspects of immune defence. A division of labour is probably widespread among trematodes and trematode species encompass considerable taxonomic, life history and environmental diversity. Trematodes should therefore provide new, fruitful systems to investigate the ecology and evolution of sociality.

Colloquium paper: homage to Linnaeus: how many parasites? How many hosts?

Estimates of the total number of species that inhabit the Earth have increased significantly since Linnaeus's initial catalog of 20,000 species. The best recent estimates suggest that there are approximately 6 million species. More emphasis has been placed on counts of free-living species than on parasitic species. We rectify this by quantifying the numbers and proportion of parasitic species. We estimate that there are between 75,000 and 300,000 helminth species parasitizing the vertebrates. We have no credible way of estimating how many parasitic protozoa, fungi, bacteria, and viruses exist. We estimate that between 3% and 5% of parasitic helminths are threatened with extinction in the next 50 to 100 years. Because patterns of parasite diversity do not clearly map onto patterns of host diversity, we can make very little prediction about geographical patterns of threat to parasites. If the threats reflect those experienced by avian hosts, then we expect climate change to be a major threat to the relatively small proportion of parasite diversity that lives in the polar and temperate regions, whereas habitat destruction will be the major threat to tropical parasite diversity. Recent studies of food webs suggest that approximately 75% of the links in food webs involve a parasitic species; these links are vital for regulation of host abundance and potentially for reducing the impact of toxic pollutants. This implies that parasite extinctions may have unforeseen costs that impact the health and abundance of a large number of free-living species.

A food web including parasites for kelp forests of the Santa Barbara Channel, California.

We built a high-resolution topological food web for the kelp forests of the Santa Barbara Channel, California, USA that includes parasites and significantly improves resolution compared to previous webs. The 1,098 nodes and 21,956 links in the web describe an economically, socially, and ecologically vital system. Nodes are broken into life-stages, with 549 free-living life-stages (492 species from 21 Phyla) and 549 parasitic life-stages (450 species from 10 Phyla). Links represent three kinds of trophic interactions, with 9,352 predator-prey links, 2,733 parasite-host links and 9,871 predator-parasite links. All decisions for including nodes and links are documented, and extensive metadata in the node list allows users to filter the node list to suit their research questions. The kelp-forest food web is more species-rich than any other published food web with parasites, and it has the largest proportion of parasites. Our food web may be used to predict how kelp forests may respond to change, will advance our understanding of parasites in ecosystems, and fosters development of theory that incorporates large networks.

Schistosome infection in Senegal is associated with different spatial extents of risk and ecological drivers for Schistosoma haematobium and S. mansoni.

Schistosome parasites infect more than 200 million people annually, mostly in sub-Saharan Africa, where people may be co-infected with more than one species of the parasite. Infection risk for any single species is determined, in part, by the distribution of its obligate intermediate host snail. As the World Health Organization reprioritizes snail control to reduce the global burden of schistosomiasis, there is renewed importance in knowing when and where to target those efforts, which could vary by schistosome species. This study estimates factors associated with schistosomiasis risk in 16 villages located in the Senegal River Basin, a region hyperendemic for Schistosoma haematobium and S. mansoni. We first analyzed the spatial distributions of the two schistosomes' intermediate host snails (Bulinus spp. and Biomphalaria pfeifferi, respectively) at village water access sites. Then, we separately evaluated the relationships between human S. haematobium and S. mansoni infections and (i) the area of remotely-sensed snail habitat across spatial extents ranging from 1 to 120 m from shorelines, and (ii) water access site size and shape characteristics. We compared the influence of snail habitat across spatial extents because, while snail sampling is traditionally done near shorelines, we hypothesized that snails further from shore also contribute to infection risk. We found that, controlling for demographic variables, human risk for S. haematobium infection was positively correlated with snail habitat when snail habitat was measured over a much greater radius from shore (45 m to 120 m) than usual. S. haematobium risk was also associated with large, open water access sites. However, S. mansoni infection risk was associated with small, sheltered water access sites, and was not positively correlated with snail habitat at any spatial sampling radius. Our findings highlight the need to consider different ecological and environmental factors driving the transmission of each schistosome species in co-endemic landscapes.

High parasite diversity in the amphipod Gammarus lacustris in a subarctic lake.

Amphipods are often key species in aquatic food webs due to their functional roles in the ecosystem and as intermediate hosts for trophically transmitted parasites. Amphipods can also host many parasite species, yet few studies address the entire parasite community of a gammarid population, precluding a more dynamic understanding of the food web. We set out to identify and quantify the parasite community of Gammarus lacustris to understand the contributions of the amphipod and its parasites to the Takvatn food web. We identified seven parasite taxa: a direct life cycle gregarine, Rotundula sp., and larval stages of two digenean trematode genera, two cestodes, one nematode, and one acanthocephalan. The larval parasites use either birds or fishes as final hosts. Bird parasites predominated, with trematode Plagiorchis sp. having the highest prevalence (69%) and mean abundance (2.7). Fish parasites were also common, including trematodes Crepidostomum spp., nematode Cystidicola farionis, and cestode Cyathocephalus truncatus (prevalences 13, 6, and 3%, respectively). Five parasites depend entirely on G. lacustris to complete their life cycle. At least 11.4% of the overall parasite diversity in the lake was dependent on G. lacustris, and 16% of the helminth diversity required or used the amphipod in their life cycles. These dependencies reveal that in addition to being a key prey item in subarctic lakes, G. lacustris is also an important host for maintaining parasite diversity in such ecosystems.