Diversity increases biomass production for trematode parasites in snails

Hechinger, Ryan F.; Lafferty, Kevin D.; Kuris, Armand M.

doi:10.1098/rspb.2008.0875

Cited by 8 publications

(6 citation statements)

References 43 publications

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“…When parasite communities were assembled additively, however, with concurrent increases in total parasite load and richness, higher parasite diversity had negative or neutral effects on host fitness. Data from the field surveys and previous parasitological research also support an unsaturated assembly pattern (30,45,46), but more research is needed to examine this issue in a broader range of disease systems (31).…”

Section: Discussionmentioning

confidence: 99%

Parasite diversity and coinfection determine pathogen infection success and host fitness

Johnson

Hoverman

2012

Proc. Natl. Acad. Sci. U.S.A.

159

161

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While the importance of changes in host biodiversity for disease risk continues to gain empirical support, the influence of natural variation in parasite diversity on epidemiological outcomes remains largely overlooked. Here, we combined field infection data from 2,191 amphibian hosts representing 158 parasite assemblages with mechanistic experiments to evaluate the influence of parasite richness on both parasite transmission and host fitness. Using a guild of larval trematode parasites (six species) and an amphibian host, our experiments contrasted the effects of parasite richness vs. composition, observed vs. randomized assemblages, and additive vs. replacement designs. Consistent with the dilution effect hypothesis extended to intrahost diversity, increases in parasite richness reduced overall infection success, including infections by the most virulent parasite. However, the effects of parasite richness on host growth and survival were context dependent; pathology increased when parasites were administered additively, even when the presence of the most pathogenic species was held constant, but decreased when added species replaced or reduced virulent species, emphasizing the importance of community composition and assembly. These results were similar or stronger when community structures were weighted by their observed frequencies in nature. The field data also revealed the highly nested structure of parasite assemblages, with virulent species generally occupying basal positions, suggesting that increases in parasite richness and antagonism in nature will decrease virulent infections. Our findings emphasize the importance of parasite biodiversity and coinfection in affecting epidemiological responses and highlight the value of integrating research on biodiversity and community ecology for understanding infectious diseases.microbiome | parasite competition | emerging infectious disease | ecosystem function | amphibian decline E cological research has focused increasingly on the importance of changes in biodiversity, thereby forming a fundamental link between community and ecosystem ecology (1-4). The loss or gain of species into a community, often in association with anthropogenic activities, can have remarkable effects on productivity, carbon storage, nutrient cycling, and species invasions (5-8). More recently, this line of inquiry has been extended to explore the role of biodiversity in affecting parasite transmission (i.e., the dilution effect; ref. 9). Building from historical research on agricultural plant communities (10), a series of recent studies has reported an inverse relationship between host diversity and the risk of disease in humans, plants, birds, amphibians, and corals (9). On the basis of experimental manipulations of host diversity, common mechanisms for this relationship involve changes in susceptible host density, such that higher diversity leads to a concomitant decline in susceptible hosts, or in encounter reduction, with added species interfering with parasite transmission (11,12).Des...

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Section: Discussionmentioning

confidence: 99%

Parasite diversity and coinfection determine pathogen infection success and host fitness

Johnson

Hoverman

2012

Proc. Natl. Acad. Sci. U.S.A.

159

161

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“…The present study is to the best of our knowledge the first one experimentally showing that the effect of castrating parasites can lead to increased hosts' lifespan, although previous circumstantial evidence suggested this effect in several animal-parasite systems [6] , [9] , [13] , [15] , [16] . This may simply be that parasite reproduction and transmission is somehow less costly than plant reproduction or it may result from an active manipulation of the host, i.e.…”

Section: Discussionmentioning

confidence: 71%

“…Few experimental data are available so far to test theoretical predictions regarding the effects on host survivorship of castrating parasites that are transmitted throughout a host's life ( i.e. , not parasitoids or other parasites only transmitted after host's death) [2] , but see [15] , [16] .…”

Section: Introductionmentioning

confidence: 99%

Influence of Multiple Infection and Relatedness on Virulence: Disease Dynamics in an Experimental Plant Population and Its Castrating Parasite

et al. 2014

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The level of parasite virulence, i.e., the decrease in host's fitness due to a pathogen, is expected to depend on several parameters, such as the type of the disease (e.g., castrating or host-killing) and the prevalence of multiple infections. Although these parameters have been extensively studied theoretically, few empirical data are available to validate theoretical predictions. Using the anther smut castrating disease on Silene latifolia caused by Microbotryum lychnidis-dioicae, we studied the dynamics of multiple infections and of different components of virulence (host death, non-recovery and percentage of castrated stems) during the entire lifespan of the host in an experimental population. We monitored the number of fungal genotypes within plants and their relatedness across five years, using microsatellite markers, as well as the rates of recovery and host death in the population. The mean relatedness among genotypes within plants remained at a high level throughout the entire host lifespan despite the dynamics of the disease, with recurrent new infections. Recovery was lower for plants with multiple infections compared to plants infected by a single genotype. As expected for castrating parasites, M. lychnidis-dioicae did not increase host mortality. Mortality varied across years but was generally lower for plants that had been diseased the preceding year. This is one of the few studies to have empirically verified theoretical expectations for castrating parasites, and to show particularly i) that castrated hosts live longer, suggesting that parasites can redirect resources normally used in reproduction to increase host lifespan, lengthening their transmission phase, and ii) that multiple infections increase virulence, here in terms of non-recovery and host castration.

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“…However, it can be very difficult to separate host and parasite tissue (Kuris et al ., 2008), leading to estimates of parasite mass based on cross-sections of host tissue (e.g. Hechinger et al ., 2008), a method that has the potential to result in similar errors to those associated with histology. In addition, weighing such light quantities can be a long and complex procedure (e.g.…”

Section: Discussionmentioning

confidence: 99%

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

Brian

Aldridge

2020

Parasitology

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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.

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Diversity increases biomass production for trematode parasites in snails

Cited by 8 publications

References 43 publications

Parasite diversity and coinfection determine pathogen infection success and host fitness

Parasite diversity and coinfection determine pathogen infection success and host fitness

Influence of Multiple Infection and Relatedness on Virulence: Disease Dynamics in an Experimental Plant Population and Its Castrating Parasite

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

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