- NSF-PAR ID:
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- Proceedings of the National Academy of Sciences
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Background: Schistosomiasis is an emerging disease associated with changes to the environment that have increased human contact rates with disease-causing parasites, flatworms that are released from freshwater snails. For example, schistosomiasis remains a major public health problem in Northern Senegal, where prevalence in schoolchildren often reaches 90%. Aim: This study focuses on the impact of seasonality on the risk of human exposure (RHE) to Schistosoma mansoni, defined as the total number of cercariae (the free-living life stage that infects humans) shed from all Biomphalaria pfeifferi snails collected at a site using standardized methods. We focus on RHE because it is rarely quantified and a recent study demonstrated that snails stop shedding cercariae when snail densities increase and thus per capita snail resources become limited , suggesting that densities of snails might not be directly proportional to RHE to schistosomes. Method: We sampled four water access points in three villages every other week during the early (Dry1) and later dry seasons (Dry2) and the rainy season, quantifying the abundance of infected and non-infected snail intermediate hosts, cercariae released per infected snail, and water chemistry. We used simple and multiple linear regressions to assess how seasonality and environmental parameters affect non-infected and infected snail abundance and RHE. Results: Although RHE was found across all seasons, the abundance of infected and non-infected snail intermediate hosts and cercariae, as well as prevalence (23.71%), were all highest in the rainy season. In the rainy season, RHE was positively associated with the density of snail hosts and their periphyton food resource. Conclusion: Although previous studies have examined the influence of seasonality on snail densities, few studies have explored the effects of seasonality on cercarial densities, which is the primary source of infection to humans. Our study demonstrates that cercarial densities are greater in the rainy season than in the early or late dry seasons. Given that cercarial densities directly pose risk of infection to humans, unlike non-infected or infected snails, these finding should help to inform decision making and schistosomiasis control efforts in West Africa.more » « less
Mancinelli, Giorgio (Ed.)
The human burden of environmentally transmitted infectious diseases can depend strongly on ecological factors, including the presence or absence of natural enemies. The marbled crayfish (
Procambarus virginalis) is a novel invasive species that can tolerate a wide range of ecological conditions and colonize diverse habitats. Marbled crayfish first appeared in Madagascar in 2005 and quickly spread across the country, overlapping with the distribution of freshwater snails that serve as the intermediate host of schistosomiasis–a parasitic disease of poverty with human prevalence ranging up to 94% in Madagascar. It has been hypothesized that the marbled crayfish may serve as a predator of schistosome-competent snails in areas where native predators cannot and yet no systematic study to date has been conducted to estimate its predation rate on snails. Here, we experimentally assessed marbled crayfish consumption of uninfected and infected schistosome-competent snails ( Biomphalaria glabrataand Bulinus truncatus) across a range of temperatures, reflective of the habitat range of the marbled crayfish in Madagascar. We found that the relationship between crayfish consumption and temperature is unimodal with a peak at ~27.5°C. Per-capita consumption increased with body size and was not affected either by snail species or their infectious status. We detected a possible satiation effect, i.e., a small but significant reduction in per-capita consumption rate over the 72-hour duration of the predation experiment. Our results suggest that ecological parameters, such as temperature and crayfish weight, influence rates of consumption and, in turn, the potential impact of the marbled crayfish invasion on snail host populations.
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 predator
Chaetogaster 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 whether Chaetogasterand trematode infection of snails correlate negatively (‘protective predation’) or positively (‘predator augmentation’).
Here, we tested how parasite transmission mode affected
Chaetogaster–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 more Chaetogasterwere 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‐snail Chaetogasterabundance.
Our results suggest that trematode transmission mode mediates the net outcome of predation on parasites. For trematodes with active infectious stages, predatory
Chaetogasterlimited 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 higher Chaetogasterabundance, 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.
The consequences of parasite infection for individual hosts depend on key features of host–parasite ecology underpinning parasite growth and immune defense, such as age, sex, resource supply, and environmental stressors. Scaling these features and their underlying mechanisms from the individual host is challenging but necessary, as they shape parasite transmission at the population level. Translating individual-level mechanisms across scales could inherently improve the way we think about feedbacks among parasitism, the mechanisms driving transmission, and the consequences of human impact and disease control efforts. Here, we use individual-based models (IBMs) based on general metabolic theory, Dynamic Energy Budget (DEB) theory, to scale explicit life-history features of individual hosts, such as growth, reproduction, parasite production, and death, to parasite transmission at the population level over a range of resource supplies focusing on the major human parasite, Schistosoma mansoni, and its intermediate host snail, Biomphalaria glabrata. At the individual level, infected hosts produce fewer parasites at lower resources as competition increases. At the population level, our DEB–IBM predicts brief, but intense parasite peaks early during the host growth season when resources are abundant and infected hosts are few. The timing of these peaks challenges the status quo that high densities of infected hosts produce the highest parasite densities. As expected, high resource supply boosts parasite output, but parasite output also peaks at modest to high host background mortality rates, which parallels overcompensation in stage-structured models. Our combined results reveal the crucial role of individual-level physiology in identifying how environmental conditions, time of the year, and key feedbacks within host–parasite ecology interact to define periods of elevated risk. The testable forecasts from this physiologically-explicit epidemiological model can inform disease management to reduce human risk of schistosome infection.
Swimmer's itch is an emerging disease caused by flatworm parasites that often use water birds as definitive hosts. When parasite larvae penetrate human skin they initiate localized inflammation that leads to intense itching. Concerns about this issue have been growing recently due to an apparent increase in the global occurrence of swimmer's itch and its subsequent impacts on recreational activities and associated revenues. Past study has identified the common merganser as a key definitive host for these worms in the United States; a number of snail species serve as intermediate hosts. Although previous attempts at controlling swimmer's itch have targeted snails, a handful of efforts have concentrated on treating water birds with the anthelmintic drug, praziquantel. We construct a mathematical model of swimmer's itch and its treatment within the infected merganser population. Our goal is to identify merganser treatment regimes that minimize the number of infected snails thereby reducing the risk of human infections. Optimal control of bird hosts is defined analytically and we include numerical simulations assuming different resource‐allocation strategies. Results from the study may help identify treatment protocols that lower merganser infection rates and ultimately reduce the occurrence of swimmer's itch in freshwater systems throughout the Midwest.
Recommendations for Resource Managers
Regardless of the time and monetary resources available, praziquantel treatment frequency should increase as mergansers arrive on the lake with continued treatments (albeit at reduced levels) until the end of the residency period.
Allocating plenty of resources towards the treatment of mergansers predicted a sharp drop in infected birds, which then remained close to zero throughout the remainder of the residency period. This approach reduced schistosome infection in mergansers and kept snail infections within the idealized range during times of peak recreational activity. Consequently, human cases of swimmer's itch would be expected to be low to nonexistent. Furthermore, our treatment‐longevity computation suggested that subsequent praziquantel dosing would not be required for a number of years.
Under more limited resources, the number of birds treated per day was much smaller throughout the residency period; however, even under these circumstances (which equated to treating approximately one bird every 5 days), simulated infected merganser densities were reduced to the point where snail infections remained below epidemic levels through to the end of the recreational period. Treatment longevity was shorter compared with the high‐resource option, but still extended 122 days into Season 2 (posttreatment).
We also used our model to investigate situations where lake managers and/or federal agencies might be taxed in terms of the time available to continuously treat mergansers on a given lake. An individual scientist may only have a single day (or two) to dose birds, rather than continuously administering praziquantel throughout the birds' residency period. If <77% of the total number of arriving birds can be treated in a single day, we recommend praziquantel administrations when the number of mergansers reaches the maximum that can be successfully treated. In addition, model simulations demonstrate that if managers are able to treat a large number of birds, they should wait until the end of the migration period.