skip to main content


Title: Linking Bioenergetics and Parasite Transmission Models Suggests Mismatch Between Snail Host Density and Production of Human Schistosomes
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
NSF-PAR ID:
10115769
Author(s) / Creator(s):
 ;  
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
Integrative and Comparative Biology
Volume:
59
Issue:
5
ISSN:
1540-7063
Page Range / eLocation ID:
p. 1243-1252
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. null (Ed.)
    Abstract An animal's social behaviour both influences and changes in response to its parasites. Here we consider these bidirectional links between host social behaviours and parasite infection, both those that occur from ecological vs evolutionary processes. First, we review how social behaviours of individuals and groups influence ecological patterns of parasite transmission. We then discuss how parasite infection, in turn, can alter host social interactions by changing the behaviour of both infected and uninfected individuals. Together, these ecological feedbacks between social behaviour and parasite infection can result in important epidemiological consequences. Next, we consider the ways in which host social behaviours evolve in response to parasites, highlighting constraints that arise from the need for hosts to maintain benefits of sociality while minimizing fitness costs of parasites. Finally, we consider how host social behaviours shape the population genetic structure of parasites and the evolution of key parasite traits, such as virulence. Overall, these bidirectional relationships between host social behaviours and parasites are an important yet often underappreciated component of population-level disease dynamics and host–parasite coevolution. 
    more » « less
  3. Abstract Understanding the community ecology of vector-borne and zoonotic diseases, and how it may shift transmission risk as it responds to environmental change, has become a central focus in disease ecology. Yet, it has been challenging to link the ecology of disease with reported human incidence. Here, we bridge the gap between local-scale community ecology and large-scale disease epidemiology, drawing from a priori knowledge of tick-pathogen-host ecology to model spatially-explicit Lyme disease (LD) risk, and human Lyme disease incidence (LDI) in California. We first use a species distribution modeling approach to model disease risk with variables capturing climate, vegetation, and ecology of key reservoir host species, and host species richness. We then use our modeled disease risk to predict human disease incidence at the zip code level across California. Our results suggest the ecology of key reservoir hosts—particularly dusky-footed woodrats—is central to disease risk posed by ticks, but that host community richness is not strongly associated with tick infection. Predicted disease risk, which is most strongly influenced by the ecology of dusky-footed woodrats, in turn is a strong predictor of human LDI. This relationship holds in the Wildland-Urban Interface, but not in open access public lands, and is stronger in northern California than in the state as a whole. This suggests peridomestic exposure to infected ticks may be more important to LD epidemiology in California than recreational exposure, and underlines the importance of the community ecology of LD in determining human transmission risk throughout this LD endemic region of far western North America. More targeted tick and pathogen surveillance, coupled with studies of human and tick behavior could improve understanding of key risk factors and inform public health interventions. Moreover, longitudinal surveillance data could further improve forecasts of disease risk in response to global environmental change. 
    more » « less
  4. Predators and parasites are critical, interconnected members of the community and have the potential to shape host populations. Predators, in particular, can have direct and indirect impacts on disease dynamics. By removing hosts and their parasites, predators alter both host and parasite populations and ultimately shape disease transmission. Selective predation of infected hosts has received considerable attention as it is recognized to have important ecological implications. The occurrence and consequences of preferential consumption of uninfected hosts, however, has rarely been considered. Here, we synthesize current evidence suggesting this strategy of selectively predating uninfected individuals is likely more common than previously anticipated and address how including this predation strategy can change our understanding of the ecology and evolution of disease dynamics. Selective predation strategies are expected to differentially impact ecological dynamics and therefore, consideration of both strategies is required to fully understand the impact of predation on prey and host densities. In addition, given that different strategies of prey selectivity by predators change the fitness payoffs both for hosts and their parasites, we predict amplified coevolutionary rates under selective predation of infected hosts compared to uninfected hosts. Using recent work highlighting the critical role that predators play in disease dynamics, we provide insights into the potential mechanisms by which selective predation on healthy individuals can directly affect ecological outcomes and impact long‐term host–parasite coevolution. We contrast the consequences of both scenarios of selective predation while identifying current gaps in the literature and future research directions. 
    more » « less
  5. Abstract

    Hosts and their parasites exist within complex ecological communities. However, the role that non‐focal community members, species which cannot be infected by a focal pathogen, may play in altering parasite transmission is often only studied in the lens of the ‘diversity‐disease’ relationship by focusing on species richness. This approach largely ignores mechanistic species interactions and risks collapsing our understanding of the community ecology of disease down to defining the prominence of ‘amplification’ versus ‘dilution’ effects.

    However, non‐focal species vary in their traits, densities and types of interactions with focal hosts and parasites. Therefore, a community ecology approach based on the mechanisms underlying parasite transmission, host harm and dynamic species interactions may better advance our understanding of parasite transmission in complex communities.

    Using the concept of the parasite's basic reproductive ratio,R0, as a generalizable framework, we examine several critical mechanisms by which interactions among hosts, parasites and non‐focal species modulate transmission and provide examples from relevant literature.

    By focusing on the mechanism by which non‐focal species impact transmission, we can emphasize the similarities among classic paradigms in the community ecology of disease, gain new insights into parasite invasion and persistence, better predict community traits correlated with disease dilution or amplification, and gauge the feasibility of biocontrol for parasites of conservation, agricultural or human health concern.

    A freePlain Language Summarycan be found within the Supporting Information of this article.

     
    more » « less