Experimental investigation of alternative transmission functions: Quantitative evidence for the importance of nonlinear transmission dynamics in host-parasite systems

1. Understanding pathogen transmission is crucial for predicting and managing disease. Nonetheless, experimental comparisons of alternative functional forms of transmission remain rare, and those experiments that are conducted are often not designed to test the full range of possible forms. 2. To di...

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Published inThe Journal of animal ecology Vol. 87; no. 3; pp. 703 - 715
Main Authors Orlofske, Sarah A., Flaxman, Samuel M., Joseph, Maxwell B., Fenton, Andy, Melbourne, Brett A., Johnson, Pieter T. J.
Format Journal Article
LanguageEnglish
Published England John Wiley & Sons Ltd 01.05.2018
Blackwell Publishing Ltd
John Wiley and Sons Inc
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Abstract 1. Understanding pathogen transmission is crucial for predicting and managing disease. Nonetheless, experimental comparisons of alternative functional forms of transmission remain rare, and those experiments that are conducted are often not designed to test the full range of possible forms. 2. To differentiate among 10 candidate transmission functions, we used a novel experimental design in which we independently varied four factors—duration of exposure, numbers of parasites, numbers of hosts and parasite density—in laboratory infection experiments. 3. We used interactions between amphibian hosts and trematode parasites as a model system and all candidate models incorporated parasite depletion. An additional manipulation involving anaesthesia addressed the effects of host behaviour on transmission form. 4. Across all experiments, nonlinear transmission forms involving either a power law or a negative binomial function were the best-fitting models and consistently out-performed the linear density-dependent and density-independent functions. By testing previously published data for two other host-macroparasite systems, we also found support for the same nonlinear transmission forms. 5. Although manipulations of parasite density are common in transmission studies, the comprehensive set of variables tested in our experiments revealed that variation in density alone was least likely to differentiate among competing transmission functions. Across host-pathogen systems, nonlinear functions may often more accurately represent transmission dynamics and thus provide more realistic predictions for infection.
AbstractList Understanding pathogen transmission is crucial for predicting and managing disease. Nonetheless, experimental comparisons of alternative functional forms of transmission remain rare, and those experiments that are conducted are often not designed to test the full range of possible forms. To differentiate among 10 candidate transmission functions, we used a novel experimental design in which we independently varied four factors—duration of exposure, numbers of parasites, numbers of hosts and parasite density—in laboratory infection experiments. We used interactions between amphibian hosts and trematode parasites as a model system and all candidate models incorporated parasite depletion. An additional manipulation involving anaesthesia addressed the effects of host behaviour on transmission form. Across all experiments, nonlinear transmission forms involving either a power law or a negative binomial function were the best‐fitting models and consistently outperformed the linear density‐dependent and density‐independent functions. By testing previously published data for two other host–macroparasite systems, we also found support for the same nonlinear transmission forms. Although manipulations of parasite density are common in transmission studies, the comprehensive set of variables tested in our experiments revealed that variation in density alone was least likely to differentiate among competing transmission functions. Across host–pathogen systems, nonlinear functions may often more accurately represent transmission dynamics and thus provide more realistic predictions for infection. The authors tested 10 candidate functions representing the transmission of trematode parasites to amphibian hosts using laboratory experiments varying the duration of exposure, numbers of parasites, numbers of hosts and parasite density. Nonlinear functions outperformed classical frequency‐ and density‐dependent transmission functions and may provide more realistic predictions for infection.
1. Understanding pathogen transmission is crucial for predicting and managing disease. Nonetheless, experimental comparisons of alternative functional forms of transmission remain rare, and those experiments that are conducted are often not designed to test the full range of possible forms. 2. To differentiate among 10 candidate transmission functions, we used a novel experimental design in which we independently varied four factors—duration of exposure, numbers of parasites, numbers of hosts and parasite density—in laboratory infection experiments. 3. We used interactions between amphibian hosts and trematode parasites as a model system and all candidate models incorporated parasite depletion. An additional manipulation involving anaesthesia addressed the effects of host behaviour on transmission form. 4. Across all experiments, nonlinear transmission forms involving either a power law or a negative binomial function were the best-fitting models and consistently out-performed the linear density-dependent and density-independent functions. By testing previously published data for two other host-macroparasite systems, we also found support for the same nonlinear transmission forms. 5. Although manipulations of parasite density are common in transmission studies, the comprehensive set of variables tested in our experiments revealed that variation in density alone was least likely to differentiate among competing transmission functions. Across host-pathogen systems, nonlinear functions may often more accurately represent transmission dynamics and thus provide more realistic predictions for infection.
Understanding pathogen transmission is crucial for predicting and managing disease. Nonetheless, experimental comparisons of alternative functional forms of transmission remain rare, and those experiments that are conducted are often not designed to test the full range of possible forms. To differentiate among 10 candidate transmission functions, we used a novel experimental design in which we independently varied four factors-duration of exposure, numbers of parasites, numbers of hosts and parasite density-in laboratory infection experiments. We used interactions between amphibian hosts and trematode parasites as a model system and all candidate models incorporated parasite depletion. An additional manipulation involving anaesthesia addressed the effects of host behaviour on transmission form. Across all experiments, nonlinear transmission forms involving either a power law or a negative binomial function were the best-fitting models and consistently outperformed the linear density-dependent and density-independent functions. By testing previously published data for two other host-macroparasite systems, we also found support for the same nonlinear transmission forms. Although manipulations of parasite density are common in transmission studies, the comprehensive set of variables tested in our experiments revealed that variation in density alone was least likely to differentiate among competing transmission functions. Across host-pathogen systems, nonlinear functions may often more accurately represent transmission dynamics and thus provide more realistic predictions for infection.
Abstract Understanding pathogen transmission is crucial for predicting and managing disease. Nonetheless, experimental comparisons of alternative functional forms of transmission remain rare, and those experiments that are conducted are often not designed to test the full range of possible forms. To differentiate among 10 candidate transmission functions, we used a novel experimental design in which we independently varied four factors—duration of exposure, numbers of parasites, numbers of hosts and parasite density—in laboratory infection experiments. We used interactions between amphibian hosts and trematode parasites as a model system and all candidate models incorporated parasite depletion. An additional manipulation involving anaesthesia addressed the effects of host behaviour on transmission form. Across all experiments, nonlinear transmission forms involving either a power law or a negative binomial function were the best‐fitting models and consistently outperformed the linear density‐dependent and density‐independent functions. By testing previously published data for two other host–macroparasite systems, we also found support for the same nonlinear transmission forms. Although manipulations of parasite density are common in transmission studies, the comprehensive set of variables tested in our experiments revealed that variation in density alone was least likely to differentiate among competing transmission functions. Across host–pathogen systems, nonlinear functions may often more accurately represent transmission dynamics and thus provide more realistic predictions for infection.
Author Flaxman, Samuel M.
Melbourne, Brett A.
Johnson, Pieter T. J.
Joseph, Maxwell B.
Orlofske, Sarah A.
Fenton, Andy
AuthorAffiliation 1 Department of Ecology and Evolutionary Biology University of Colorado Boulder Boulder CO USA
3 Department of Biology University of Wisconsin Stevens Point Trainer Natural Resources Building 446 Stevens Point WI USA
2 Institute of Integrative Biology University of Liverpool Liverpool UK
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ContentType Journal Article
Copyright 2018 British Ecological Society
2017 The Authors. published by John Wiley & Sons Ltd on behalf of British Ecological Society.
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Journal of Animal Ecology © 2018 British Ecological Society
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Issue 3
Keywords mathematical model
epidemiology
behaviour
macroparasite
Ribeiroia ondatrae
infectious disease
Language English
License Attribution
2017 The Authors. Journal of Animal Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society.
This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
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Snippet 1. Understanding pathogen transmission is crucial for predicting and managing disease. Nonetheless, experimental comparisons of alternative functional forms of...
Understanding pathogen transmission is crucial for predicting and managing disease. Nonetheless, experimental comparisons of alternative functional forms of...
Abstract Understanding pathogen transmission is crucial for predicting and managing disease. Nonetheless, experimental comparisons of alternative functional...
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SubjectTerms Anesthesia
Animals
Anura
behaviour
Density
Disease control
Disease transmission
epidemiology
Experimental design
Experiments
Host-Parasite Interactions
Infections
infectious disease
macroparasite
mathematical model
Mathematical models
Metacercariae - growth & development
Metacercariae - physiology
Models, Biological
Nonlinear Dynamics
Nonlinear systems
Parasite and Disease Ecology
Parasites
Pathogens
Population Density
Predictions
Ribeiroia ondatrae
Trematoda - growth & development
Trematoda - physiology
Trematode Infections - parasitology
Trematode Infections - transmission
Trematode Infections - veterinary
Title Experimental investigation of alternative transmission functions: Quantitative evidence for the importance of nonlinear transmission dynamics in host-parasite systems
URI https://www.jstor.org/stable/45023883
https://onlinelibrary.wiley.com/doi/abs/10.1111%2F1365-2656.12783
https://www.ncbi.nlm.nih.gov/pubmed/29111599
https://www.proquest.com/docview/2024432547/abstract/
https://search.proquest.com/docview/1961642988
https://pubmed.ncbi.nlm.nih.gov/PMC6849515
Volume 87
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