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Invasive species challenge the global response to emerging diseases
Science & Society
Invasive species challenge the global response to emerging diseases Philip E. Hulme The Bio-Protection Research Centre, Lincoln University, PO Box 84, Canterbury, New Zealand
Forecasts of emerging zoonoses neglect the threat alien species pose in disease transmission to humans. A review of alien parasites, hosts, and vectors introduced to Europe highlights the wide range of potential public health risks, the need for better surveillance and risk assessment, and major policy gaps in global preparedness.
The problem with introductions There is growing concern regarding the rising number of emerging and re-emerging zoonotic diseases worldwide, which will place a significant burden on global economies [1]. Predictions of these future risks have focused on how climate change might shift the distribution of hosts and/or vectors, alter the timing of their life cycles, and subsequently facilitate the establishment of novel host–parasite assemblages leading to atypical disease scenarios [2]. As a result, both the US Centers for Disease Control and Prevention and the European Centre for Disease Prevention and Control monitor environmental conditions relating to infectious disease threats. Yet climate, although important, is only part of the story, and disease emergence is also driven by socioeconomic and ecological factors. Global trade has facilitated the worldwide introduction of zoonotic agents, and the interaction of alien species with environmental degradation has the potential to pose as great a threat of emerging zoonotic diseases as climate change [3]. Zoonotic infectious agents are far more localised in their geographical distribution than other human pathogens and parasites [4], and their redistribution as a result of globalisation might have severe public health consequences; yet, how big is this problem? The magnitude of the threat is difficult to discern because few regions of the world possess detailed knowledge of the alien parasites, pathogens, vectors, and hosts of public health concern. However, recently updated data for Europe provide insights into the impact of alien species introductions on the likelihood of predicting and preventing emerging zoonotic diseases (http://www.europe-aliens.org). More than just mosquitoes The increasing movement of goods and people into and within Europe has led to the introduction of numerous alien parasites, vectors, and hosts (Table S1 in the supplementary material online). More than 60 mammal, 70 bird, Corresponding author: Hulme, P.E. ([email protected]). 1471-4922/ ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.pt.2014.03.005
and 40 reptile species have become established in Europe following deliberate or accidental introductions and have brought with them a cryptic cargo of intestinal worms, pathogens, and ticks of human disease significance [5]. Several introduced endoparasites are responsible for zoonotic diseases that are new to Europe such as baylisascariasis, strongyloidiasis, and coenurosis. Over a dozen ectoparasites that can potentially transmit disease to humans have also been introduced. These include fleas associated with infective carditis and bubonic plague, ticks that are vectors of Lyme disease and Crimean–Congo haemorrhagic fever, as well as mites that can transmit typhus. Although much attention has focused on the risks posed by the Asian tiger mosquito, four additional mosquitoes recently introduced from Asia are also significant vectors of human viral infections. Alien vertebrates are important reservoir hosts of diseases transmitted by arthropod vectors, especially Lyme disease, tularaemia, Far East scarlet-like fever, and rickettsial infections. Vertebrates also act as vectors of parasites and pathogens, particularly through their faeces. The latter route includes transmission of the fox tapeworm, which is one of the most serious diseases vectored by mammals to humans in Central Europe. In addition, many introduced mammals, for example, coypu, American mink, muskrat, and the Canadian beaver, have strong affinities with aquatic environments where they contaminate water resources with pathogens responsible for salmonellosis, toxoplasmosis, and leptospirosis. Adding to this contamination are over 20 alien waterfowl species that have established breeding populations in Europe and produce a substantial faecal coliform load spreading cryptosporidiosis, giardiasis, and microsporidiosis [6]. A further route to infection is through food because several introduced deer, fish, and crustaceans established in the wild are consumed by humans and might become sources of foodborne zoonoses such as sarcosporidiosis and anisakiasis. Although the above examples are drawn from Europe, the diversity and complexity of potential zoonoses arising from biological invasions are likely to be similar in other continental regions that have become increasingly globalised (Box 1). Critics might argue that such forecasts are alarmist and that alien species introductions need to be seen in the context of the many native hosts, parasites, and vectors already responsible for zoonotic diseases. Nevertheless, there are several reasons why these additions to the much larger native species pool matter (Figure 1). First, compared to native species, alien species may be more effective hosts or vectors in the transmission of existing diseases. Second, they potentially open the door to the establishment Trends in Parasitology, June 2014, Vol. 30, No. 6
267
Science & Society Box 1. A smoking gun? Tracing the role of alien introductions in the current pattern of zoonotic pathogens or parasites throughout the world is often challenging. Historical records describe clear cases where humans moved parasites, pathogens, and vectors into new biogeographical realms with major effects [4]. The Columbian Exchange resulted in the introduction into the Americas of both yellow fever and dengue with its mosquito vector (Aedes aegypti) from Africa, as well as plague from Asia transmitted by fleas on alien black rats (Rattus rattus). Europeans also moved parasites native to the Americas to other regions of the globe such as the chigoe flea (Tunga penetrans) to Africa with devastating effects. In New Zealand, the non-volant mammal wildlife is entirely composed of taxa introduced by humans, and several are recognised as important vectors of both giardiasis and leptospirosis for which rates of human infection are among the highest in the developed world. Hydatid tapeworms (Echinoccus granulosus) were introduced to New Zealand with sheep, but zoonotic transmission via domestic and stray dogs led to over 800 documented human deaths between 1891 and 1956 until a national control programme resulted in the country being declared hydatid-free in 2002. The biogeographical isolation and recent European colonisation of New Zealand has facilitated the understanding of the link between human health and alien wildlife [14], but in many cases determining the routes of introduction of zoonotic agents relies on detailed molecular detective work [15]. Such data highlight that the canine variant of rabies virus in the Americas originated from dogs introduced from Europe, and similarly Bartonella pathogens have crossed the Atlantic with alien Norway rats, while the agent of Lyme disease (Borrelia burgdorferi sensu stricto) probably originated in North America and has since been translocated by humans to Europe. The introduction of alien wildlife certainly poses a significant human health risk through the introduction of new pathogens and parasites. But to what extent have alien animals introduced to Europe led to increased rates of existing diseases? Medical practitioners report the incidence of disease but the original host and/or vector is rarely identified unless clearly unambiguous (e.g., introduced mosquito-borne diseases such as Chikungunya fever). Although there are few quantitative data on how the increasing diversity and synanthropy of alien wildlife in Europe might affect transmission rates, their potential contribution to the increasing prevalence of leishmaniasis, Lyme disease, and tularaemia in Europe should not be ignored.
of new emerging diseases with which they have coevolved in their own native ranges. The establishment of the Asian tiger mosquito resulted in outbreaks of Chikungunya fever in Italy in 2007 and dengue in Croatia in 2010. Third, alien species thrive in anthropogenic environments, increasing the risk of transmission to humans, and urban heat island effects can facilitate the establishment of diseases from warmer climatic zones. Fourth, they exhibit higher dispersal rates [7], and many high-risk species are continuing to spread across Europe [5], limiting options for management. Finally, integration of even a single new host, parasite, or vector into an established zoonotic network can potentially have dramatic outcomes for disease transmission [8]. Globalisation has created a melting pot of introduced taxa from different biogeographical origins, climates, and habitats, increasing the likelihood of unforeseen species jumps, hybridisation, and evolutionary change. Alien pathogens and parasites may quickly evolve to infect local vectors, alien vectors may adapt to exploit native hosts, and alien hosts may establish critical epidemiological links with native primary, intermediate, and/or amplifying hosts. 268
Trends in Parasitology June 2014, Vol. 30, No. 6
Slipping through gaps in policy and science What are the options for a policy response? The rate of vertebrate introductions to Europe has continued to increase over the past century [9]. Preventing the introduction of species that pose a current or future risk to public health should be a priority. Because a significant proportion of alien wildlife species are the result of escapes or releases arising from the deliberate introduction of animals as pets or for hunting and farming, there should be tighter regulation of this route of entry. The World Trade Organisation does provide legislative scope to secure clean trade in wildlife that would significantly reduce the inadvertent introduction of unwanted parasites [10]. However, international wildlife trade regulations pay scant attention to the risks of imported species establishing in the wild [11], and even less consideration is given to the fact that once established they may harbour new or existing zoonotic agents of public health concern. This situation largely results from the way biosecurity strategies fall into distinct camps addressing plant, animal, or human health but rarely the intersection of these disciplines. Thus, whereas some aspects of public health ensuing from the introduction of alien species such as human pathogens and mosquitoes are managed, others, including potential vertebrate hosts and ectoparasites, are less effectively addressed. Initiatives such as One Health attempt to bring together veterinary and medical perspectives to tackle the role of domestic animals in public health, but an equivalent focus examining the importance of alien wildlife in zoonoses is urgently required. Robust evidence implicating alien species in measurably increased transmission rates of a zoonotic pathogen will be needed to catalyse the required action in international policy. Yet such evidence is often challenging to obtain (Box 1). Most countries monitor notifiable infections and foodborne diseases, while many have surveillance programmes targeting disease vectors, particularly mosquitoes. However, assessment of the changes in the prevalence of wildlife hosts of human pathogens and parasites is limited and often restricted to a few species (e.g., foxes) or the investigation of mass animal mortality events. Systematic monitoring would appear essential where alien populations have the potential for rapid range expansion, abrupt increases in local abundance, and/or shifts in habitat occupancy. Such changes in the spatiotemporal dynamics of hosts and vectors may be precisely the trigger for a disease outbreak. Data on the prevalence and abundance of parasites, pathogens, and vectors of human diseases associated with high-risk alien hosts would be critical, but even for widespread alien species presumed to pose public health problems, such as the raccoon in Europe, these data are patchy at best [12]. However, even these data would be insufficient on their own without an understanding of the epidemiological risks of transmission. Therefore, a further challenge is to develop effective risk assessment tools that predict potential public health threats before they occur. Although >300 procedures have been developed to predict the risks posed by alien species, most do not adequately quantify potential impacts on human health [13]. Such tools would not only need to ascertain the likelihood that an alien host or vector could
Science & Society
Trends in Parasitology June 2014, Vol. 30, No. 6
(A)
(C)
(B)
(D)
TRENDS in Parasitology
Figure 1. The country-level occurrence and status of alien species in Europe selected to illustrate the range of potential risks such taxa might pose to human health. (A) Compared to native rodent hosts, the Siberian chipmunk, Tamias sibiricus, not only harbours more diverse genotypes of bacteria responsible for Lyme disease but also supports a richer tick fauna consequentially transforming a popular pet into a particularly effective prospective zoonotic agent. (B) Breeding of the red-eared slider, Trachemys elegans, a vector of salmonellosis, is limited by temperature, but populations often persist in warmer urban areas that will probably provide foci for future spread because of climate warming. (C) Canada geese, Branta canadensis, are potential vectors of Cryptosporidium, Campylobacter, and Escherichia coli O157:H7; their substantial population increase across Europe since the 1950s and the ability to migrate widely between breeding and wintering grounds, including as far as Siberia, presents an opportunity for widespread disease spread. (D) The raccoon dog, Nyctereutes procyonoides, a reservoir host of leishmaniasis, has spread from Russia into Southern Europe where the disease is endemic and thus could increase disease transmission considerably in this region. Key: red – species has self-sustaining, expanding populations in the country; orange – species previously or currently occurs in the country, but populations are small, transient, or non-breeding; grey – no record of the species in the country. Apart from the Canada goose, for which a small vagrant population is found, none of the species occur in Iceland. Sources of occurrence data and background information for each species can be found in Table S1 in the supplementary material online.
establish but also estimate subsequent disease prevalence in the wild and the probability of transmission to humans; this would necessitate coupling risk assessment to comprehensive national and international databases of zoonotic agents. The absence of fit-for-purpose risk assessment and databases is a major impediment to implementing legislation to manage the entry of zoonotic agents associated with alien species introductions. Yet, even these systems are not foolproof, and risks will occur through illegal wildlife trade and accidental introduction via the international movement of people and commodities. The fact that most forecasts of the risk of emerging diseases have largely neglected the potential role of alien species [1,2,8] highlights a major gap in global preparedness against zoonoses.
Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.pt.2014.03.005.
References 1 Jones, K.E. et al. (2008) Global trends in emerging infectious diseases. Nature 451, 990–993 2 Altizer, S. et al. (2013) Climate change and infectious diseases: from evidence to a predictive framework. Science 341, 514–519 3 Kilpatrick, A.M. (2011) Globalization, land use, and the invasion of West Nile Virus. Science 334, 323–327 4 Smith, K.F. and Guegan, J.F. (2010) Changing geographic distributions of human pathogens. Annu. Rev. Ecol. Evol. Syst. 41, 231–250 5 DAISIE (2009) Handbook of Alien Species in Europe, Springer 6 Hulme, P.E. (2012) Invasive species unchecked by climate change. Science 335, 537–538 269
Science & Society 7 Graczyk, T.K. et al. (2008) The role of birds in dissemination of human waterborne enteropathogens. Trends Parasitol. 24, 55–59 8 Keesing, F. et al. (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468, 647–652 9 Hulme, P.E. et al. (2009) Will threat of biological invasions unite the European Union? Science 324, 40–41 10 World Trade Organisation (2002) WTO Agreements and Public Health, WTO Secretariat 11 Convention on Biological Diversity (2012) COP 11 Decision XI/28 Invasive Alien Species, (UNEP/CBD/COP/11/35), Convention on Biological Diversity
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Trends in Parasitology June 2014, Vol. 30, No. 6 12 Beltran-Beck, B. et al. (2012) Raccoons in Europe: disease hazards due to the establishment of an invasive species. Eur. J. Wildl. Res. 58, 5–15 13 Leung, B. et al. (2012) TEASIng apart alien species risk assessments: a framework for best practices. Ecol. Lett. 15, 1475–1493 14 Wilks, C.R. and Humble, M.W., eds (1997) Zoonoses in New Zealand – A Combined Veterinary and Medical Per-spective (2nd edn), VetLearn Foundation 15 Childs, J.E. et al. (1999) Shared vector-borne zoonoses of the Old World and New World: home grown or translocated? Schweiz. Med. Wochenschr. 129, 1099–1105
Invasive species challenge the global response to emerging diseases Philip E. Hulme The Bio-Protection Research Centre, Lincoln University, PO Box 84, Canterbury, New Zealand
Forecasts of emerging zoonoses neglect the threat alien species pose in disease transmission to humans. A review of alien parasites, hosts, and vectors introduced to Europe highlights the wide range of potential public health risks, the need for better surveillance and risk assessment, and major policy gaps in global preparedness.
The problem with introductions There is growing concern regarding the rising number of emerging and re-emerging zoonotic diseases worldwide, which will place a significant burden on global economies [1]. Predictions of these future risks have focused on how climate change might shift the distribution of hosts and/or vectors, alter the timing of their life cycles, and subsequently facilitate the establishment of novel host–parasite assemblages leading to atypical disease scenarios [2]. As a result, both the US Centers for Disease Control and Prevention and the European Centre for Disease Prevention and Control monitor environmental conditions relating to infectious disease threats. Yet climate, although important, is only part of the story, and disease emergence is also driven by socioeconomic and ecological factors. Global trade has facilitated the worldwide introduction of zoonotic agents, and the interaction of alien species with environmental degradation has the potential to pose as great a threat of emerging zoonotic diseases as climate change [3]. Zoonotic infectious agents are far more localised in their geographical distribution than other human pathogens and parasites [4], and their redistribution as a result of globalisation might have severe public health consequences; yet, how big is this problem? The magnitude of the threat is difficult to discern because few regions of the world possess detailed knowledge of the alien parasites, pathogens, vectors, and hosts of public health concern. However, recently updated data for Europe provide insights into the impact of alien species introductions on the likelihood of predicting and preventing emerging zoonotic diseases (http://www.europe-aliens.org). More than just mosquitoes The increasing movement of goods and people into and within Europe has led to the introduction of numerous alien parasites, vectors, and hosts (Table S1 in the supplementary material online). More than 60 mammal, 70 bird, Corresponding author: Hulme, P.E. ([email protected]). 1471-4922/ ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.pt.2014.03.005
and 40 reptile species have become established in Europe following deliberate or accidental introductions and have brought with them a cryptic cargo of intestinal worms, pathogens, and ticks of human disease significance [5]. Several introduced endoparasites are responsible for zoonotic diseases that are new to Europe such as baylisascariasis, strongyloidiasis, and coenurosis. Over a dozen ectoparasites that can potentially transmit disease to humans have also been introduced. These include fleas associated with infective carditis and bubonic plague, ticks that are vectors of Lyme disease and Crimean–Congo haemorrhagic fever, as well as mites that can transmit typhus. Although much attention has focused on the risks posed by the Asian tiger mosquito, four additional mosquitoes recently introduced from Asia are also significant vectors of human viral infections. Alien vertebrates are important reservoir hosts of diseases transmitted by arthropod vectors, especially Lyme disease, tularaemia, Far East scarlet-like fever, and rickettsial infections. Vertebrates also act as vectors of parasites and pathogens, particularly through their faeces. The latter route includes transmission of the fox tapeworm, which is one of the most serious diseases vectored by mammals to humans in Central Europe. In addition, many introduced mammals, for example, coypu, American mink, muskrat, and the Canadian beaver, have strong affinities with aquatic environments where they contaminate water resources with pathogens responsible for salmonellosis, toxoplasmosis, and leptospirosis. Adding to this contamination are over 20 alien waterfowl species that have established breeding populations in Europe and produce a substantial faecal coliform load spreading cryptosporidiosis, giardiasis, and microsporidiosis [6]. A further route to infection is through food because several introduced deer, fish, and crustaceans established in the wild are consumed by humans and might become sources of foodborne zoonoses such as sarcosporidiosis and anisakiasis. Although the above examples are drawn from Europe, the diversity and complexity of potential zoonoses arising from biological invasions are likely to be similar in other continental regions that have become increasingly globalised (Box 1). Critics might argue that such forecasts are alarmist and that alien species introductions need to be seen in the context of the many native hosts, parasites, and vectors already responsible for zoonotic diseases. Nevertheless, there are several reasons why these additions to the much larger native species pool matter (Figure 1). First, compared to native species, alien species may be more effective hosts or vectors in the transmission of existing diseases. Second, they potentially open the door to the establishment Trends in Parasitology, June 2014, Vol. 30, No. 6
267
Science & Society Box 1. A smoking gun? Tracing the role of alien introductions in the current pattern of zoonotic pathogens or parasites throughout the world is often challenging. Historical records describe clear cases where humans moved parasites, pathogens, and vectors into new biogeographical realms with major effects [4]. The Columbian Exchange resulted in the introduction into the Americas of both yellow fever and dengue with its mosquito vector (Aedes aegypti) from Africa, as well as plague from Asia transmitted by fleas on alien black rats (Rattus rattus). Europeans also moved parasites native to the Americas to other regions of the globe such as the chigoe flea (Tunga penetrans) to Africa with devastating effects. In New Zealand, the non-volant mammal wildlife is entirely composed of taxa introduced by humans, and several are recognised as important vectors of both giardiasis and leptospirosis for which rates of human infection are among the highest in the developed world. Hydatid tapeworms (Echinoccus granulosus) were introduced to New Zealand with sheep, but zoonotic transmission via domestic and stray dogs led to over 800 documented human deaths between 1891 and 1956 until a national control programme resulted in the country being declared hydatid-free in 2002. The biogeographical isolation and recent European colonisation of New Zealand has facilitated the understanding of the link between human health and alien wildlife [14], but in many cases determining the routes of introduction of zoonotic agents relies on detailed molecular detective work [15]. Such data highlight that the canine variant of rabies virus in the Americas originated from dogs introduced from Europe, and similarly Bartonella pathogens have crossed the Atlantic with alien Norway rats, while the agent of Lyme disease (Borrelia burgdorferi sensu stricto) probably originated in North America and has since been translocated by humans to Europe. The introduction of alien wildlife certainly poses a significant human health risk through the introduction of new pathogens and parasites. But to what extent have alien animals introduced to Europe led to increased rates of existing diseases? Medical practitioners report the incidence of disease but the original host and/or vector is rarely identified unless clearly unambiguous (e.g., introduced mosquito-borne diseases such as Chikungunya fever). Although there are few quantitative data on how the increasing diversity and synanthropy of alien wildlife in Europe might affect transmission rates, their potential contribution to the increasing prevalence of leishmaniasis, Lyme disease, and tularaemia in Europe should not be ignored.
of new emerging diseases with which they have coevolved in their own native ranges. The establishment of the Asian tiger mosquito resulted in outbreaks of Chikungunya fever in Italy in 2007 and dengue in Croatia in 2010. Third, alien species thrive in anthropogenic environments, increasing the risk of transmission to humans, and urban heat island effects can facilitate the establishment of diseases from warmer climatic zones. Fourth, they exhibit higher dispersal rates [7], and many high-risk species are continuing to spread across Europe [5], limiting options for management. Finally, integration of even a single new host, parasite, or vector into an established zoonotic network can potentially have dramatic outcomes for disease transmission [8]. Globalisation has created a melting pot of introduced taxa from different biogeographical origins, climates, and habitats, increasing the likelihood of unforeseen species jumps, hybridisation, and evolutionary change. Alien pathogens and parasites may quickly evolve to infect local vectors, alien vectors may adapt to exploit native hosts, and alien hosts may establish critical epidemiological links with native primary, intermediate, and/or amplifying hosts. 268
Trends in Parasitology June 2014, Vol. 30, No. 6
Slipping through gaps in policy and science What are the options for a policy response? The rate of vertebrate introductions to Europe has continued to increase over the past century [9]. Preventing the introduction of species that pose a current or future risk to public health should be a priority. Because a significant proportion of alien wildlife species are the result of escapes or releases arising from the deliberate introduction of animals as pets or for hunting and farming, there should be tighter regulation of this route of entry. The World Trade Organisation does provide legislative scope to secure clean trade in wildlife that would significantly reduce the inadvertent introduction of unwanted parasites [10]. However, international wildlife trade regulations pay scant attention to the risks of imported species establishing in the wild [11], and even less consideration is given to the fact that once established they may harbour new or existing zoonotic agents of public health concern. This situation largely results from the way biosecurity strategies fall into distinct camps addressing plant, animal, or human health but rarely the intersection of these disciplines. Thus, whereas some aspects of public health ensuing from the introduction of alien species such as human pathogens and mosquitoes are managed, others, including potential vertebrate hosts and ectoparasites, are less effectively addressed. Initiatives such as One Health attempt to bring together veterinary and medical perspectives to tackle the role of domestic animals in public health, but an equivalent focus examining the importance of alien wildlife in zoonoses is urgently required. Robust evidence implicating alien species in measurably increased transmission rates of a zoonotic pathogen will be needed to catalyse the required action in international policy. Yet such evidence is often challenging to obtain (Box 1). Most countries monitor notifiable infections and foodborne diseases, while many have surveillance programmes targeting disease vectors, particularly mosquitoes. However, assessment of the changes in the prevalence of wildlife hosts of human pathogens and parasites is limited and often restricted to a few species (e.g., foxes) or the investigation of mass animal mortality events. Systematic monitoring would appear essential where alien populations have the potential for rapid range expansion, abrupt increases in local abundance, and/or shifts in habitat occupancy. Such changes in the spatiotemporal dynamics of hosts and vectors may be precisely the trigger for a disease outbreak. Data on the prevalence and abundance of parasites, pathogens, and vectors of human diseases associated with high-risk alien hosts would be critical, but even for widespread alien species presumed to pose public health problems, such as the raccoon in Europe, these data are patchy at best [12]. However, even these data would be insufficient on their own without an understanding of the epidemiological risks of transmission. Therefore, a further challenge is to develop effective risk assessment tools that predict potential public health threats before they occur. Although >300 procedures have been developed to predict the risks posed by alien species, most do not adequately quantify potential impacts on human health [13]. Such tools would not only need to ascertain the likelihood that an alien host or vector could
Science & Society
Trends in Parasitology June 2014, Vol. 30, No. 6
(A)
(C)
(B)
(D)
TRENDS in Parasitology
Figure 1. The country-level occurrence and status of alien species in Europe selected to illustrate the range of potential risks such taxa might pose to human health. (A) Compared to native rodent hosts, the Siberian chipmunk, Tamias sibiricus, not only harbours more diverse genotypes of bacteria responsible for Lyme disease but also supports a richer tick fauna consequentially transforming a popular pet into a particularly effective prospective zoonotic agent. (B) Breeding of the red-eared slider, Trachemys elegans, a vector of salmonellosis, is limited by temperature, but populations often persist in warmer urban areas that will probably provide foci for future spread because of climate warming. (C) Canada geese, Branta canadensis, are potential vectors of Cryptosporidium, Campylobacter, and Escherichia coli O157:H7; their substantial population increase across Europe since the 1950s and the ability to migrate widely between breeding and wintering grounds, including as far as Siberia, presents an opportunity for widespread disease spread. (D) The raccoon dog, Nyctereutes procyonoides, a reservoir host of leishmaniasis, has spread from Russia into Southern Europe where the disease is endemic and thus could increase disease transmission considerably in this region. Key: red – species has self-sustaining, expanding populations in the country; orange – species previously or currently occurs in the country, but populations are small, transient, or non-breeding; grey – no record of the species in the country. Apart from the Canada goose, for which a small vagrant population is found, none of the species occur in Iceland. Sources of occurrence data and background information for each species can be found in Table S1 in the supplementary material online.
establish but also estimate subsequent disease prevalence in the wild and the probability of transmission to humans; this would necessitate coupling risk assessment to comprehensive national and international databases of zoonotic agents. The absence of fit-for-purpose risk assessment and databases is a major impediment to implementing legislation to manage the entry of zoonotic agents associated with alien species introductions. Yet, even these systems are not foolproof, and risks will occur through illegal wildlife trade and accidental introduction via the international movement of people and commodities. The fact that most forecasts of the risk of emerging diseases have largely neglected the potential role of alien species [1,2,8] highlights a major gap in global preparedness against zoonoses.
Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.pt.2014.03.005.
References 1 Jones, K.E. et al. (2008) Global trends in emerging infectious diseases. Nature 451, 990–993 2 Altizer, S. et al. (2013) Climate change and infectious diseases: from evidence to a predictive framework. Science 341, 514–519 3 Kilpatrick, A.M. (2011) Globalization, land use, and the invasion of West Nile Virus. Science 334, 323–327 4 Smith, K.F. and Guegan, J.F. (2010) Changing geographic distributions of human pathogens. Annu. Rev. Ecol. Evol. Syst. 41, 231–250 5 DAISIE (2009) Handbook of Alien Species in Europe, Springer 6 Hulme, P.E. (2012) Invasive species unchecked by climate change. Science 335, 537–538 269
Science & Society 7 Graczyk, T.K. et al. (2008) The role of birds in dissemination of human waterborne enteropathogens. Trends Parasitol. 24, 55–59 8 Keesing, F. et al. (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468, 647–652 9 Hulme, P.E. et al. (2009) Will threat of biological invasions unite the European Union? Science 324, 40–41 10 World Trade Organisation (2002) WTO Agreements and Public Health, WTO Secretariat 11 Convention on Biological Diversity (2012) COP 11 Decision XI/28 Invasive Alien Species, (UNEP/CBD/COP/11/35), Convention on Biological Diversity
270
Trends in Parasitology June 2014, Vol. 30, No. 6 12 Beltran-Beck, B. et al. (2012) Raccoons in Europe: disease hazards due to the establishment of an invasive species. Eur. J. Wildl. Res. 58, 5–15 13 Leung, B. et al. (2012) TEASIng apart alien species risk assessments: a framework for best practices. Ecol. Lett. 15, 1475–1493 14 Wilks, C.R. and Humble, M.W., eds (1997) Zoonoses in New Zealand – A Combined Veterinary and Medical Per-spective (2nd edn), VetLearn Foundation 15 Childs, J.E. et al. (1999) Shared vector-borne zoonoses of the Old World and New World: home grown or translocated? Schweiz. Med. Wochenschr. 129, 1099–1105