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Global Parasite and Rattus Rodent Invasions

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Global Parasite and Rattus Rodent Invasions Integrative Zoology 2015; 10: 409–423 doi: 10.1111/1749-4877.12143 1 REVIEW 1 2 2 3 3 4 4 5 5 6 6 7 Global parasite and Rattus rodent invasions: The consequences 7 8 8 9 for rodent-borne diseases 9 10 10 11 11 12 12 13 Serge MORAND,1,2 Frédéric BORDES,3 Hsuan-Wien CHEN,4 Julien CLAUDE,3 Jean-François 13 14 5,6 5 7 7 3,8 14 15 COSSON, Maxime GALAN, Gábor Á CZIRJÁK, Alex D GREENWOOD, Alice LATINNE, 15 16 Johan MICHAUX1,8 and Alexis RIBAS9 16 17 17 1 18 Centre National de la Recherche Scientifque (CNRS)-Centre de coopération Internationale en Recherche Agronomique pour le 18 19 Développement (CIRAD) Animal et Gestion Intégrée des Risques, Centre d’Infectiologie Christophe Mérieux du Laos, Vientiane, 19 20 Lao PDR, 2Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand, 3Institut des 20 21 Sciences de l’Evolution, Centre National de la Recherche Scientifque (CNRS)-Université de Montpellier-Institut de Recherche 21 22 pour le Développement (IRD), Montpellier, France, 4Department of Biological Resources, National Chiayi University, Chiayi 22 23 City, Taiwan, China, 5Institut National de la Recherche Agronomique (INRA), Centre de Biologie et de Gestion des Populations, 23 24 Baillarguet, France, 6Institut National de la Recherche Agronomique (INRA), UMR Biologie et Immunologie Parasitaire Agence 24 25 25 Nationale de Sécurité Sanitaire de l’Alimentation, de l’Environnement et du Travail ses, Maisons-Alfort, France, 7Leibniz Institute 26 26 for Zoo and Wildlife Research. Department of Wildlife Diseases, 10315 Berlin, Germany, 8Conservation Genetics Unit. University 27 27 9 28 of Liège 4000 Liège, Belgium and Biodiversity Research Group, Faculty of Science, Udon Thani Rajabhat University, Udon Thani, 28 29 Thailand 29 30 30 31 Abstract 31 32 32 33 We summarize the current knowledge on parasitism-related invasion processes of the globally invasive Rattus 33 34 lineages, originating from Asia, and how these invasions have impacted the local epidemiology of rodent-borne 34 35 diseases. Parasites play an important role in the invasion processes and successes of their hosts through multi- 35 36 ple biological mechanisms such as “parasite release,” “immunocompetence advantage,” “biotic resistance” and 36 37 “novel weapon.” Parasites may also greatly increase the impact of invasions by spillover of parasites and other 37 38 pathogens, introduced with invasive hosts, into new hosts, potentially leading to novel emerging diseases. An- 38 39 other potential impact is the ability of the invader to amplify local parasites by spillback. In both cases, local 39 40 fauna and humans may be exposed to new health risks, which may decrease biodiversity and potentially cause 40 41 increases in human morbidity and mortality. Here we review the current knowledge on these processes and pro- 41 42 pose some research priorities. 42 43 43 Key words: biological invasion, immunocompetence, parasite release, spillback, spillover 44 44 45 45 46 46 47 47 48 Correspondence: Serge Morand, Centre d’Infectiologie INTRODUCTION 48 Christophe Mérieux du Laos, PO Box 3888, Samsenthai Road, 49 Emerging infectious diseases share several patterns 49 Vientiane, Lao PDR. 50 and processes with free-living invasive organisms. How- 50 51 Email: [email protected] 51 © 2015 International Society of Zoological Sciences, Institute of Zoology/ 409 Chinese Academy of Sciences and Wiley Publishing Asia Pty Ltd S. Morand et al. 1 ever, host–parasite (in a broad sense including macro colonized ecosystems in different ways (Courchamp et 1 2 microparasites and microparasites) interactions are more al. 2003; Banks & Hughes 2012) and can also have eco- 2 3 complex due to interactions operating at the level of the nomic impacts. Moreover, these species display suffi- 3 4 individual (e.g. life-history trait, defense and virulence), cient ecological differences that they would be expected 4 5 population (e.g. dynamics and disease regulation), com- to interact differently with local small mammal commu- 5 6 munity (e.g. co-interactive networks of parasitism, com- nities (Courchamp et al. 2003; SingLeton et al. 2007). 6 7 petition and predation) and ecosystem (e.g. parasites in All these Rattus species have radically and explosive- 7 8 food webs, and disease spread within habitat connectivi- ly expanded their geographic range as a consequence of 8 9 ty). human activities. Interestingly, all of these rodents orig- 9 10 Parasites play an important role in the invasion pro- inated in Asia, and they can be found in sympatry in 10 11 cesses and successes of their hosts through multiple bio- many localities, even far from their original distribution 11 12 logical mechanisms, such as “parasite release” (Torchin (Bastos et al. 2011; Blanks & Hugues 2012; Lack et al. 12 13 13 et al. 2003), “immunocompetence advantage” (Møller 2012) due to their synanthropic behavior (Khlyap & 14 14 & Cassey 2004), “biotic resistance” (Britton 2012), and Warshavsky 2010; McFarlane et al. 2012). As these rat 15 15 “novel weapon” (Strauss et al. 2012), among others species are closely associated with humans, the timing 16 16 (Prenter et al. 2004; BeLL et al. 2009; Dunn 2009; KeL- of their invasion is related to current and historical glob- 17 17 ly et al. 2009; Morand et al. 2010). Parasites may also al trade. 18 greatly increase the impact of invasions through spill- 18 Rodents are recognized as hosts of at least 60 zoo- 19 over of parasites/pathogens into new hosts, potential- 19 notic diseases that represent a serious threat to human 20 ly leading to novel emerging diseases and/or the emer- 20 21 gence of already known diseases in new geographic health (Meerburg et al. 2009; Luis et al. 2013; Chai- 21 22 areas (Hulme 2014). A second local potential impact is siri et al. 2015). Historically, Asian rodents of the ge- 22 23 the ability of the invader to amplify local parasites by nus Rattus have been implicated in the emergence and 23 24 spillback. Spillover and local acquisition of parasites spread of infectious diseases of importance to human 24 25 and pathogens have important consequences for ecolog- health such as plague, murine typhus, scrub typhus, lep- 25 26 ical systems, wildlife and domestic species (Wood et al. tospirosis and hantavirus hemorrhagic fever, among oth- 26 27 2012). In both cases, local fauna and humans may be ers (Kosoy et al. 2015). They can cause considerable 27 28 exposed to new or elevated health risks (Hatcher et al. economic loss (Stenseth et al. 2003; SingLeton et al. 28 29 2012). 2010; John 2014) and have great impact on biodiversity 29 30 30 Few host–parasite systems permit an overall view of (Atkinson 1985; Lowe et al. 2001; Wyatt et al. 2008). 31 31 the consequences of biological invasions at multiple lev- Our aims are to review the ecological and biologi- 32 32 els of biological organization, at different global scales cal knowledge on Rattus invaders and the consequences 33 33 and linking risks of emerging diseases. Invasive rodents of their invasion success on rodent-borne diseases and, 34 34 are one of the few models that allow such a comprehen- based on this review, to emphasize gaps in knowledge 35 35 sive scalable analysis to be performed. Among the nu- and recommend some future research priorities. 36 36 merous species within Rattus (66 species according to 37 37 Musser & Carlton 2005), the Norway or brown rat Rat- 38 PARASITES IN THE INVASION 38 tus norvegicus (Berkenhout, 1769), the black or roof rat 39 39 Rattus rattus (Linnaeus, 1758), and the Asian black rat PROCESSES: CAUSES AND LIKELY 40 40 Rattus tanezumi Temminck, 1844 have colonized urban 41 CONSEQUENCES 41 ecosystems globally (Aplin et al. 2011). A fourth inva- 42 42 sive species, the Pacifc rat Rattus exulans (Peale, 1848) Biotic invasions are often compared to epidemics as 43 43 is limited to tropical Asia-Pacific areas. Finally, oth- several important factors in disease epidemiology are 44 44 er species in the group [Rattus argentiventer (Robinson common to invasion biology (Mack et al. 2000): the 45 45 and Kloss, 1916], Rattus nitidus (Hodgson, 1845) and chance of establishment, the minimum population size 46 46 Rattus tiomanicus (Miller, 1900) have shown an expan- necessary for establishment in the invaded habitat, the 47 47 sion associated with human activities but to a less geo- population growth and the fate of interacting species in 48 48 graphical extent (Aplin et al. 2003). It is well known the new range (Drake 2003). These factors are the core 49 49 that, once introduced, all these species can strongly in- of the invasion process, which has been defned as a se- 50 50 teract with indigenous fauna and fora, and can alter the quence of 3 steps: introduction, initial establishment and 51 51 410 © 2015 International Society of Zoological Sciences, Institute of Zoology/ Chinese Academy of Sciences and Wiley Publishing Asia Pty Ltd Global parasite and Rattus invasions 1 spread (Williamson 1996; Kolar & Lodge 2001; Facon parasites in the introduced range; any co-introduced par- 1 2 et al. 2006; Fig. 1). asites may be useful for the control of native hosts by 2 3 The first step, introduction, is associated to the dis- spillover, which may have few opportunities for invest- 3 4 persal ability of the species, although introduction is ment in defense, especially if living on islands (Hoch- 4 5 mainly dependent on human activities. The second step, berg & Møller 2001). Fourth, in the absence of parasites 5 6 initial establishment, depends mainly on the fate of in- in the invaded localities, invasive species can reallocate 6 7 teraction with the local environmental characteristics. energetic resources from unnecessary costly defenses 7 8 The last step, spread or population growth, clearly de- into ftness (e.g.
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