skip to main content

Attention:

The NSF Public Access Repository (NSF-PAR) system and access will be unavailable from 11:00 PM ET on Friday, July 12 until 2:00 AM ET on Saturday, July 13 due to maintenance. We apologize for the inconvenience.


Title: Consumption of trematode parasite infectious stages: from conceptual synthesis to future research agenda
Abstract Given their sheer cumulative biomass and ubiquitous presence, parasites are increasingly recognized as essential components of most food webs. Beyond their influence as consumers of host tissue, many parasites also have free-living infectious stages that may be ingested by non-host organisms, with implications for energy and nutrient transfer, as well as for pathogen transmission and infectious disease dynamics. This has been particularly well-documented for the cercaria free-living stage of digenean trematode parasites within the Phylum Platyhelminthes. Here, we aim to synthesize the current state of knowledge regarding cercariae consumption by examining: (a) approaches for studying cercariae consumption; (b) the range of consumers and trematode prey documented thus far; (c) factors influencing the likelihood of cercariae consumption; (d) consequences of cercariae consumption for individual predators (e.g. their viability as a food source); and (e) implications of cercariae consumption for entire communities and ecosystems (e.g. transmission, nutrient cycling and influences on other prey). We detected 121 unique consumer-by-cercaria combinations that spanned 60 species of consumer and 35 trematode species. Meaningful reductions in transmission were seen for 31 of 36 combinations that considered this; however, separate studies with the same cercaria and consumer sometimes showed different results. Along with addressing knowledge gaps and suggesting future research directions, we highlight how the conceptual and empirical approaches discussed here for consumption of cercariae are relevant for the infectious stages of other parasites and pathogens, illustrating the use of cercariae as a model system to help advance our knowledge regarding the general importance of parasite consumption.  more » « less
Award ID(s):
1754171
NSF-PAR ID:
10420896
Author(s) / Creator(s):
; ;
Date Published:
Journal Name:
Journal of Helminthology
Volume:
97
ISSN:
0022-149X
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Predation on parasites is a common interaction with multiple, concurrent outcomes. Free‐living stages of parasites can comprise a large portion of some predators' diets and may be important resources for population growth. Predation can also reduce the density of infectious agents in an ecosystem, with resultant decreases in infection rates. While predator–parasite interactions likely vary with parasite transmission strategy, few studies have examined how variation in transmission mode influences contact rates with predators and the associated changes in consumption risk.

    To understand how transmission mode mediates predator–parasite interactions, we examined associations between an oligochaete predatorChaetogaster limnaeithat lives commensally on freshwater snails and nine trematode taxa that infect snails.Chaetogasteris hypothesized to consume active (i.e. mobile), free‐living stages of trematodes that infect snails (miracidia), but not the passive infectious stages (eggs); it could thus differentially affect transmission and infection prevalence of parasites, including those with medical or veterinary importance. Alternatively, when infection does occur,Chaetogastercan consume and respond numerically to free‐living trematode stages released from infected snails (cercariae). These two processes lead to contrasting predictions about whetherChaetogasterand trematode infection of snails correlate negatively (‘protective predation’) or positively (‘predator augmentation’).

    Here, we tested how parasite transmission mode affectedChaetogaster–trematode relationships using data from 20,759 snails collected across 4 years from natural ponds in California. Based on generalized linear mixed modelling, snails with moreChaetogasterwere less likely to be infected by trematodes that rely on active transmission. Conversely, infections by trematodes with passive infectious stages were positively associated with per‐snailChaetogasterabundance.

    Our results suggest that trematode transmission mode mediates the net outcome of predation on parasites. For trematodes with active infectious stages, predatoryChaetogasterlimited the risk of snail infection and its subsequent pathology (i.e. castration). For taxa with passive infectious stages, no such protective effect was observed. Rather, infected snails were associated with higherChaetogasterabundance, likely owing to the resource subsidy provided by cercariae. These findings highlight the ecological and epidemiological importance of predation on free‐living stages while underscoring the influence of parasite life history in shaping such interactions.

     
    more » « less
  2. Predicting and disrupting transmission of human parasites from wildlife hosts or vectors remains challenging because ecological interactions can influence their epidemiological traits. Human schistosomes, parasitic flatworms that cycle between freshwater snails and humans, typify this challenge. Human exposure risk, given water contact, is driven by the production of free-living cercariae by snail populations. Conventional epidemiological models and management focus on the density of infected snails under the assumption that all snails are equally infectious. However, individual-level experiments contradict this assumption, showing increased production of schistosome cercariae with greater access to food resources. We built bioenergetics theory to predict how resource competition among snails drives the temporal dynamics of transmission potential to humans and tested these predictions with experimental epidemics and demonstrated consistency with field observations. This resource-explicit approach predicted an intense pulse of transmission potential when snail populations grow from low densities, i.e., when per capita access to resources is greatest, due to the resource-dependence of cercarial production. The experiment confirmed this prediction, identifying a strong effect of infected host size and the biomass of competitors on per capita cercarial production. A field survey of 109 waterbodies also found that per capita cercarial production decreased as competitor biomass increased. Further quantification of snail densities, sizes, cercarial production, and resources in diverse transmission sites is needed to assess the epidemiological importance of resource competition and support snail-based disruption of schistosome transmission. More broadly, this work illustrates how resource competition can sever the correspondence between infectious host density and transmission potential. 
    more » « less
  3. Abstract

    Many planktonic consumers alter their behavior depending on the concentration of food in the environment, but responses to changes in food quality, as characterized by its elemental stoichiometry, are less well understood. Because of different nutritional demands across life history stages, consumer's responses to prey quality may vary across ontogeny. We build on previous observations of consumer selectivity and responses to prey presence by examining responses of displacement and movement patterns to prey stoichiometry. We used high‐speed videography to quantify displacement and movement patterns of the marine copepod,Acartia tonsa, as they varied with elemental content of microalgal food offered during preconditioning and during imaging trials. Life stages were sensitive to different nutrient elements in prey, with movement in copepodites generally varying with nitrogen content, and in adults with both nitrogen and phosphorus content. Net displacement was lower when adults and copepodites were offered fully replete and nitrogen‐replete food, respectively. Displacement of adults was more sensitive to the quality of food offered during preconditioning, and displacement of copepodites was affected by food quality during both preconditioning and trials. Naupliar displacement and movement patterns were generally insensitive to food quality. Only adults significantly altered movement patterns associated with feeding in response to food quality; adult helical swimming significantly increased in the treatments in which stoichiometrically replete food was offered in both preconditioning and behavioral trials. Older stages ofA. tonsaalter movement in response to food quality in ways that may allow the selective use of patches of high‐quality prey.

     
    more » « less
  4. Abstract

    Although parasites are increasingly recognized for their ecosystem roles, it is often assumed that free‐living organisms dominate animal biomass in most ecosystems and therefore provide the primary pathways for energy transfer.

    To examine the contributions of parasites to ecosystem energetics in freshwater streams, we quantified the standing biomass of trematodes and free‐living organisms at nine sites in three streams in western Oregon, USA. We then compared the rates of biomass flow from snailsJuga pliciferainto trematode parasites relative to aquatic vertebrate predators (sculpin, cutthroat trout and Pacific giant salamanders).

    The trematode parasite community had the fifth highest dry biomass density among stream organisms (0.40 g/m2) and exceeded the combined biomass of aquatic insects. Only host snails (3.88 g/m2), sculpin (1.11 g/m2), trout (0.73 g/m2) and crayfish (0.43 g/m2) had a greater biomass. The parasite ‘extended phenotype’, consisting of trematode plus castrated host biomass, exceeded the individual biomass of every taxonomic group other than snails. The substantial parasite biomass stemmed from the high snail density and infection prevalence, and the large proportional mass of infected hosts that consisted of trematode tissue (M = 31% per snail).

    Estimates of yearly biomass transfer from snails into trematodes were slightly higher than the combined estimate of snail biomass transfer into the three vertebrate predators. Pacific giant salamanders accounted for 90% of the snail biomass consumed by predators.

    These results demonstrate that trematode parasites play underappreciated roles in the ecosystem energetics of some freshwater streams.

     
    more » « less
  5. Vermeij, Geerat J. (Ed.)
    Rapid warming and sea-level rise are predicted to be major driving forces in shaping coastal ecosystems and their services in the next century. Though forecasts of the multiple and complex effects of temperature and sea-level rise on ecological interactions suggest negative impacts on parasite diversity, the effect of long term climate change on parasite dynamics is complex and unresolved. Digenean trematodes are complex life cycle parasites that can induce characteristic traces on their bivalve hosts and hold potential to infer parasite host-dynamics through time and space. Previous work has demonstrated a consistent association between sea level rise and increasing prevalence of trematode traces, but a number of fundamental questions remain unanswered about this paleoecological proxy. Here we examine the relationships of host size, shape, and functional morphology with parasite prevalence and abundance, how parasites are distributed across hosts, and how all of these relationships vary through time, using the bivalve Chamelea gallina from a Holocene shallow marine succession in the Po coastal plain. Trematode prevalence increased and decreased in association with the transition from a wave-influenced estuarine system to a wave-dominated deltaic setting. Prevalence and abundance of trematode pits are associated with large host body size, reflecting ontogenetic accumulation of parasites, but temporal trends in median host size do not explain prevalence trends. Ongoing work will test the roles of temperature, salinity, and nutrient availability on trematode parasitism. Parasitized bivalves in one sample were shallower burrowers than their non-parasitized counterparts, suggesting that hosts of trematodes can be more susceptible to their predators, though the effect is ephemeral. Like in living parasite-host systems, trematode-induced malformations are strongly aggregated among hosts, wherein most host individuals harbor very few parasites while a few hosts have many. We interpret trace aggregation to support the assumption that traces are a reliable proxy for trematode parasitism in the fossil record. 
    more » « less