skip to main content


Title: A novel schistosome species hosted by Planorbella (Helisoma) trivolvis is the most widespread swimmer's itch-causing parasite in Michigan inland lakes
Abstract Cercarial dermatitis (‘swimmer's itch’; SI), characterized by small itchy bumps caused by schistosome parasites of birds and mammals, is a common problem in Michigan. Research on avian schistosomes began nearly 100 years ago in Michigan inland lakes, yet scientists are still uncovering basic biological information including the identification of local snail and parasite species that cause SI. Previous research primarily focused on lakes in the northern half of Michigan's lower peninsula, although SI occurs throughout the state. We surveyed snails and snail-borne trematodes in lakes across Michigan's lower peninsula and used quantitative polymerase chain reaction analysis of filtered water samples to identify parasites to the species level, including a recently discovered parasite species that uses the snail Planorbella (Helisoma) trivolvis as its intermediate host. Most SI mitigation efforts have focused on a parasite species hosted by the snail Lymnaea catescopium ( = Stagnicola emarginata ); however, lymnaeid snails and their associated schistosome species were largely restricted to northern lakes. In contrast, P. trivolvis and its associated parasite species were common in both northern and southern Michigan lakes. A third schistosome species associated with physid snails was also present at low levels in both northern and southern lakes. These results indicate that the recently discovered parasite species and its planorbid snail intermediate host may be more important drivers of Michigan SI than previously thought, possibly due to increased definitive host abundance in recent decades. These results have potentially important implications for SI mitigation and control efforts.  more » « less
Award ID(s):
1651888
NSF-PAR ID:
10462992
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ;
Date Published:
Journal Name:
Parasitology
Volume:
150
Issue:
1
ISSN:
0031-1820
Page Range / eLocation ID:
88 to 97
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    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.

     
    more » « less
  2. Secor, W. Evan (Ed.)
    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. 
    more » « less
  3. Abstract

    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.

     
    more » « less
  4. 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 glabrataandBulinus 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.

     
    more » « less
  5. Abstract

    Non‐native freshwater snails can play important roles as consumers, hosts, and prey. Despite their potential ecological importance, global patterns in non‐native snail taxonomy, geography, and ecology have not been documented. Our objectives were to use a semi‐quantitative systematic review to describe non‐native freshwater snail global diversity, distribution, mechanisms of introduction, and interactions with natural enemies, including parasites and predators.

    Based on 506 relevant publications, we recorded 95 non‐native freshwater snail species from 16 families. Six taxonomic families, and pulmonate snails as a group, were over‐represented relative to the number of species expected by chance. Eight snail species represented 63% of the research records. A few snail taxa (15%) were widespread global invaders, reported from four or more continents, while most invasions were limited to a single continent. Australia and the Pacific Islands were the largest ‘sink’ for non‐native snails, with the greatest difference in the number of non‐native taxa relative to native taxa that had spread to other continents.

    Aquarium hobby sales were implicated as the most common mechanism of introduction (41% of species), followed by “hitchhiking” on aquatic vegetation, human consumption, use for biocontrol, transportation in canals, commercial shipping, and outdoor recreation. A search of internet sales posts indicated that four of the six over‐represented snail families were readily available for purchase online.

    Non‐native snails hosted parasites of wildlife, livestock, and human health importance, yet on average had 80% lower parasite richness in their non‐native compared to native range. At least 65 taxa were documented as consumers of non‐native snails, including native predators of conservation concern. These findings suggest that non‐native snails often are released from parasitism, but may commonly experience biotic resistance from predators.

    Our synthesis emphasizes the relatively high diversity of non‐native snails, but the disproportionate role of a few taxonomic groups in driving ecological, economic, and public health challenges. Moving forward, it will be important to limit new snail introductions through policy, education, and monitoring, particularly as the effective control of established snail invasions remains challenging in most ecosystems.

     
    more » « less