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Global Change, Parasite Transmission and Disease Control: Lessons from Ecology

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Global change, parasite transmission and disease control: lessons from ecology Cable, J., Baber, I., Boag, B., Ellison, AR., Morgan, E., Murray, K., Pascoe, EL., Sait, SM., Wilson, AJ., & Booth, M. (2017). Global change, parasite transmission and disease control: lessons from ecology. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 372, [20160088]. https://doi.org/10.1098/rstb.2016.0088 Published in: Philosophical Transactions of the Royal Society of London B: Biological Sciences Document Version: Publisher's PDF, also known as Version of record Queen's University Belfast - Research Portal: Link to publication record in Queen's University Belfast Research Portal Publisher rights Copyright 2017 the authors. This is an open access article published under a Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium, provided the author and source are cited. General rights Copyright for the publications made accessible via the Queen's University Belfast Research Portal is retained by the author(s) and / or other copyright owners and it is a condition of accessing these publications that users recognise and abide by the legal requirements associated with these rights. Take down policy The Research Portal is Queen's institutional repository that provides access to Queen's research output. Every effort has been made to ensure that content in the Research Portal does not infringe any person's rights, or applicable UK laws. If you discover content in the Research Portal that you believe breaches copyright or violates any law, please contact [email protected]. Download date:26. Sep. 2021 Downloaded from http://rstb.royalsocietypublishing.org/ on February 7, 2018 Global change, parasite transmission and disease control: lessons from ecology rstb.royalsocietypublishing.org Joanne Cable1, Iain Barber2, Brian Boag3, Amy R. Ellison1, Eric R. Morgan4, Kris Murray5, Emily L. Pascoe1,6, Steven M. Sait7, Anthony J. Wilson8 and Mark Booth9 Review 1School of Biosciences, Cardiff University, Cardiff CF10 3AX, UK 2Department of Neuroscience, Psychology and Behaviour, University of Leicester, Leicester LE1 7RH, UK Cite this article: Cable J et al. 2017 Global 3The James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK change, parasite transmission and disease 4School of Veterinary Sciences, University of Bristol, Bristol BS40 5DU, UK 5 control: lessons from ecology. Phil. Grantham Institute – Climate Change and the Environment, Faculty of Natural Sciences, Imperial College London, Exhibition Road, London SW7 2AZ, UK Trans. R. Soc. B 372: 20160088. 6Department of Biodiversity and Molecular Ecology, Centre for Research and Innovation, Fondazione Edmund http://dx.doi.org/10.1098/rstb.2016.0088 Mach, Via E. Mach 1, 38010 S. Michele all’Adige, Trentino, Italy 7School of Biology, University of Leeds, Leeds LS2 9JT, UK 8Vector-borne Viral Diseases Programme, The Pirbright Institute, Ash Road, Pirbright, Woking GU24 0NF, UK Accepted: 25 August 2016 9School of Medicine, Pharmacy and Health, Durham University, Durham TS17 6BH, UK JC, 0000-0002-8510-7055; IB, 0000-0003-3955-6674; AJW, 0000-0002-2000-2914 One contribution of 16 to a theme issue ‘Opening the black box: re-examining the Parasitic infections are ubiquitous in wildlife, livestock and human popu- ecology and evolution of parasite transmission’. lations, and healthy ecosystems are often parasite rich. Yet, their negative impacts can be extreme. Understanding how both anticipated and cryptic changes in a system might affect parasite transmission at an individual, Subject Areas: local and global level is critical for sustainable control in humans and live- health and disease and epidemiology stock. Here we highlight and synthesize evidence regarding potential effects of ‘system changes’ (both climatic and anthropogenic) on parasite Keywords: transmission from wild host–parasite systems. Such information could infectious disease, climate change, sustainable inform more efficient and sustainable parasite control programmes in dom- estic animals or humans. Many examples from diverse terrestrial and aquatic control, stressors natural systems show how abiotic and biotic factors affected by system changes can interact additively, multiplicatively or antagonistically to influ- Author for correspondence: ence parasite transmission, including through altered habitat structure, Joanne Cable biodiversity, host demographics and evolution. Despite this, few studies of e-mail: [email protected] managed systems explicitly consider these higher-order interactions, or the subsequent effects of parasite evolution, which can conceal or exaggerate measured impacts of control actions. We call for a more integrated approach to investigating transmission dynamics, which recognizes these complexities and makes use of new technologies for data capture and monitoring, and to support robust predictions of altered parasite dynamics in a rapidly changing world. This article is part of the themed issue ‘Opening the black box: re-examining the ecology and evolution of parasite transmission’. 1. Introduction The current epoch of ecological time is driven by human interference [1]. Multiple anthropogenic stressors—including climate change, pollution, ocean acidification, habitat loss and fragmentation, urbanization, agricultural expansion and intensification, together with other changes in the use of water and land resources—are directly or indirectly impacting all species on earth (e.g. [2–5]). These changes may lead to the crossing or corrosion of critical thresholds, or ‘planetary boundaries’ ([6,7], see glossary), that induce physio- logical stress or complete system dysfunction, with negative consequences for & 2017 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited. Downloaded from http://rstb.royalsocietypublishing.org/ on February 7, 2018 stressor response mechanism effect 2 rstb.royalsocietypublishing.org human demographic change leading to urbanization altered abiotic and biotic interactions abiotic stressors (incl. parasite evolution in parallel pollution, soil and water with repeated MDA, alters chemistry, hydrodynamic control campaign outcome changes) parasite life cycle range shift, resilience and plasticity, migration of hosts/vectors from habitat loss, fragmentation increased/decreased force of adaptability, mutation, or into control locations alters and biodiversity loss infection, specialization/ host switching, control expectations increased/decreased host generalization Phil. Trans. R. Soc. B genetic diversity, changing patterns of infection farm intensification increased host density militate against non-flexible control programme success resistance, increased/ mass drug administration decreased virulence or localized hotspots, localized programmes pathogenicity, altered gut extinction affects outcome of microbiota persistent intervention 372 Figure 1. Stress–response impacts on parasite control programmes. (Online version in colour.) : 20160088 individuals, populations and species. Such processes will globally, prevalence has fallen from 50% to 4% of those at have significant impacts on parasite natural history and risk in the endemic population [13]; however, the implications infectious disease risks. of environmental changes for the long-term efficacy of this and The anticipation of global change is not currently other treatment programmes are not well understood. reflected in programmes of intervention against parasites of Elsewhere, problems remain in terms of attributing caus- humans—instead the emphasis is on identifying vulnerable ality to, or quantifying the success of, MDA programmes [8]. communities from retrospective data, and targeting those First, the historical data are imprecise and patchy; diagnosis communities for intervention. In an attempt to synthesize of some infections has been characterized for decades by a and implement cost-effective interventions against the neg- lack of sensitive and/or specific tools [14]. Second, global cli- lected tropical diseases (NTDs), there has been a concerted mate models reveal an ever-changing pattern of land surface effort to distribute human medicines through mass drug temperature, rainfall and vegetation cover across the surface administration (MDA) programmes in areas of high trans- of the planet [15]. Thus, contemporaneous environmental mission [8], aided by donations from large pharmaceutical changes could potentially confound the effects of MDAs. companies. These MDA campaigns rely largely on the pre- Third, host range shifts may spread parasites into areas sumptive treatment of putatively exposed individuals in ‘at where monitoring and MDA are not being applied. Finally, risk’ populations [9]. The expectation, translated from the the programmes themselves may have generated selection outputs of mathematical models, is that repeated MDA will pressures, as has been observed in other systems such as reduce the size of the parasite population and simultaneously malaria [16], leading potentially to resistance, adaptation reduce levels of morbidity attributable to infection [9]. and other evolutionary consequences. Such intervention programmes are possible because of In looking to the future sustainability and success of developments
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  • Impact of Trematode Parasitism on the Fauna of a North Sea Tidal Flat

    Impact of Trematode Parasitism on the Fauna of a North Sea Tidal Flat

    HELGOI~NDER MEERESUNTERSUCHUNGEN Helgol~nder Meeresunters. 37, 185-199 (1984) Impact of trematode parasitism on the fauna of a North Sea tidal flat G. Lauckner Biologische Anstalt Helgoland (Litoralstation]; D-2282 List/Sylt, Federal Republic of Germany ABSTRACT: The impact of larval trematodes on the fauna of a North Sea tidal flat is considered at the individual and at the population level, depicting the digenean parasites of the common periwinkle, Littorina littorea, and their life cycles, as an example. On the German North Sea coast, L. fittorea is first intermediate host for 6 larval trematodes representing 6 digenean families - Cryptocotyle lingua (Heterophyidae), Himasthla elongata (Echinostomatidae), Renicola roscovita (Renicolidae), Microphallus pygmaeus (Microphallidae), Podocotyle atomon (Opecoelidae} and Cercaria lebouri (Notocotylidae). All except P. atomon utilize shore birds as final hosts; adult P. atomon parasitize in the intestine of teleosts, mainly pleuronectid flatfish. Second intermediate hosts of C. lingua are various species of fish; the cercariae of H. elongata encyst in molluscs and polychaetes, those of R. roscovita in molluscs; Iv[. pygmaeus has an abbreviated life cycle; C. lebouri encysts free on solid surfaces; and the fish trematode P. atomon utilizes benthic crustaceans, mainly amphipods, as second intermediate hosts. On the tidal flats of the K6nigshafen (Sylt), up to 77 % of the periwinkles have been found to be infested by larval trematodes. Maximum infestations in individual samples were 23 % for C. lingua, 47 % for H. etongata and 44 To for R. roscovita. The digeneans cause complete 'parasitic castration' of their carriers and hence exclude a considerable proportion of the snails from the breeding population.