Science & Society
Special Issue: Wildlife Parasitology
Foodborne parasites from wildlife: how wild are they? Christian M.O. Kapel and Brian L. Fredensborg Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark
The majority of wild foods consumed by humans are sourced from intensively managed or semi-farmed populations. Management practices inevitably affect wildlife density and habitat characteristics, which are key elements in the transmission of parasites. We consider the risk of transmission of foodborne parasites to humans from wildlife maintained under natural or seminatural conditions. A deeper understanding will be useful in counteracting foodborne parasites arising from the growing industry of novel and exotic foods.
‘Farmed’ wildlife and foodborne parasites In the overall global food supply, a decreasing proportion of wildlife species are sourced from entirely naturally sustained populations. Thus, sylvatic (truly wild) hosts are predominantly relevant regarding only the transmission of parasitic disease to hunters in native/traditional communities with a non-industrialized food supply. The vast majority of wildlife consumed by humans originates from managed or semi-domesticated wildlife populations, raising the question of how ‘wild’ the majority of wildlife harvested for human consumption actually are (Box 1). This is true for traditional game species, where release of raised animals and provision of additional feed to boost natural populations are common practice. However, a fast-growing aquaculture industry and the culture of shellfish in natural habitats demonstrate that traditional aquatic wildlife used for human consumption is also intensively managed. From a public health perspective, why should we care whether wildlife for consumption comes from naturally sustained or heavily managed populations? First, the degree of wildlife management/farming is likely to impact on the abundance of parasites via manipulation of the host population density, structure, and/or behavior. For example, wildlife kept at artificially high population densities in habitats that resemble their natural environment may facilitate the transmission of parasites with life cycles which require close contact between hosts. Second, wildlife produced in natural habitats interact with other fauna (e.g., hosts harboring parasite infective stages), and they are potentially exposed to an influx of infective stages from the surrounding environment. Surprisingly little is known about the effects of wildlife farming/management on the abundance and composition of foodborne parasites. Corresponding author: Kapel, C.M.O. ([email protected]). Keywords: wildlife parasites; foodborne; zoonotic; management; transmissions. 1471-4922/ ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.pt.2014.12.005
However, increased consumption of ‘farmed’ wildlife, globalization of the food supply, and emerging foodborne diseases from exotic foods indicate that the type and extent of management should be a focus area in future risk assessments of foodborne parasites. Management of wildlife and foodborne parasite transmission to humans The types of human management of wildlife populations of relevance to the transmission of foodborne parasites comprise those that affect the density of wildlife, and those that alter habitat characteristics of importance to parasite transmission. In the following, the potential effects of human intervention on the transmission of foodborne parasites are considered for wildlife harvested from natural ecosystems, and also for wildlife farmed or maintained under semi-natural conditions. Foodborne parasites from commercially exploited natural wildlife populations Intensive exploitation of wildlife in natural ecosystems generally reduces the population density and induces a shift in the age-structure of the exploited populations towards smaller and younger individuals. The consequences of a changing age-structure may be two-fold. First, in mammals, young and naı¨ve individuals are often more sensitive to initial exposure, and thus may contribute significantly more to parasite biomass, particularly in co-infections with other pathogens [1]. In wildlife where acquired immunity is less important, young individuals display a lower parasite burden because they have had less time and opportunity to accumulate parasites. Marine fisheries provide a classic example where overexploitation changes the age-structure of overfished species, thereby reducing the diversity and intensity of parasite infections [2]. The most important foodborne parasites of wild-caught fish are nematodes of the family Anisakidae (primarily from the genera Anisakis and Pseudoterranova). Juvenile anisakids acquired from eating raw or undercooked fish invade the intestinal mucosa and may cause severe epigastric pain, eosinophilic granuloma formation, and chronic allergic conditions [3]. Despite heavy exploitation of fish populations, reported cases of anisakiasis have increased in recent years, perhaps as a consequence of better diagnostic tools in combination with increased transmission from growing populations of definitive hosts (seals and small whales). Hunting practices may provide an overlooked but potentially important route of transmission of foodborne parasites. Thus, carcasses of marine mammals in Greenland and wolves in Russia are often left exposed to Trends in Parasitology, April 2015, Vol. 31, No. 4
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Science & Society
Trends in Parasitology April 2015, Vol. 31, No. 4
Box 1. What is the definition of wildlife? To understand the drivers of parasite transmission among wildlife, and their interaction with human activity, we first need to define what wildlife is. Traditionally the term wildlife was used for undomesticated vertebrate game species (birds and mammals) living in terrestrial ecosystems. The problem with that definition is that many game species to a greater or lesser degree are managed, although they remain under natural conditions. It also does not adequately address other groups of animals (vertebrates and invertebrates) used for human consumption. Later, as part of the US Endangered Species Act of 1973, wildlife was redefined to encompass all living organisms out of the direct control of man, including undomesticated or cultivated plants and animals. Although more fitting than the traditional definition, the transition from natural to domesticated populations may be subtle (see Table 1 in main text), and foodborne parasites from wildlife may eventually be more likely to be acquired if the wildlife is under human management compared to truly natural populations. In terms of parasite transmission, a more relevant definition of wildlife could therefore include all living organisms living in and interacting with their natural environment.
dogs, foxes, and other scavengers, thereby increasing the local abundance of the roundworm Trichinella spp. which are transmitted by ingestion of undercooked meat containing infective tissue cysts [4,5]. Foodborne parasites from semi-farmed wildlife Semi-natural wildlife encompasses species that are managed but maintained under conditions that allow interactions with the surrounding natural habitat. This group represents a gradient in human intervention, ranging from managed game species in natural habitats to the farming of shellfish, fish, and other wildlife used for human consumption (Table 1). In terms of volume and economic value, this group represents the vast majority of wild foods used for human consumption. Classic game species. Game species used for commercial hunting are often managed in ways that increase the population density of exploited species. The release of raised individuals boosts natural populations, and supplemental feeding may increase interactions among individuals. For example, wild boar aggregate around feeders,
thereby increasing the transmission of endoparasites [6]. An important foodborne parasite from game is Trichinella, acquired especially from wild boar or bear. Trichinella may be transmitted by boars feeding on infected carcasses or scraps left in the habitat after hunting. Thus, increased population density in a game resort where other animals with higher prevalence may be hunted (foxes, raccoon dogs, etc.) may also intensify transmission. Fish farming. More than 50 species of fish-borne parasites are known to infect humans [7]. Most of these originate from freshwater fish. A rapidly growing aquaculture industry in Asia with export of fresh fish to the rest of the World comprises a significant risk of transmission to humans [8]. Larval stages of trematodes are commonly found in meat of farmed fish, which, if consumed raw or undercooked, may be infective to humans. Their transmission relies on the presence of snails (first intermediate host), and the highly eutrophic fish ponds may constitute an ideal habitat for these. The artificially high density of fish greatly increases the transmission from snails to fish, and also elevates infection levels in fish [9]. Finally, the presence of potential definitive (reservoir) hosts, the traditional use of human feces as fertilizer, terrestrial run-off, and water from surrounding natural habitat may supply trematode eggs infective to snails. Shellfish. Shellfish are often cultured in productive estuaries (river deltas), biotops rich in nutrients that facilitate high production yields and increased stocking densities. Estuaries are ideal habitats for many parasites with complex life cycles that exploit the abundance of potential hosts and trophic interactions in the relatively shallow and productive ecosystems. Many estuarine mollusks serve as intermediate hosts for helminths, in particular trematodes, where the larval stage (metacercaria) that can infect birds and mammals is found in soft tissues of clams and oysters. Several representatives of the family Echinostomatidae have been found in humans after eating raw clams or oysters [10]. Most human cases are from Southeast Asia, where infections lead to intestinal pain and discomfort. However, echinostomatids are also
Table 1. Gradient of human intervention in wildlife consumed by humans from unaffected (sylvatic) to domesticated, and the predicted effect on population density and parasite transmission Level of management None (sylvatic) Commercial harvesting of natural populations a
Effects on wildlife population None (i) Reduced host density (ii) Changed age-structure
Release of individuals; provision of additional food into the natural habitat (game) a Farming of wildlife in natural habitats (mussel/oyster cultures in estuaries) a Habitat alteration but interacting with surrounding environment (aquaculture) a
Increased host density; hosts cluster around feeders (transmission foci)
Domestication and separation from natural habitat (e.g., deer farm)
Increased host density; reduced contact with infective stages and treatment of infected individuals
a
Examples of wildlife discussed in the text.
126
Increased host density Increased host density, alteration of host habitat, monocultures
Effect(s) on parasite transmission None (i) Reduced transmission (ii) Altered age-structure may increase (mammals) or decrease (fish, invertebrates) transmission Increased transmission of directly transmitted parasites Provision of food reduces trophic transmission Increased transmission Increased transmission for directly transmitted parasites and for parasites with complex life cycles that depend on intermediate hosts and infective stages from the surrounding environment Reduced transmission
Science & Society abundant in oysters and clams in other parts of the World [11], and they may constitute an overlooked group of foodborne parasites in developed countries where commercial and recreational harvest of oysters is increasing. Interestingly, studies show that the infection of mollusks may be reduced by the presence of other non-host species that feed on infective cercariae or that reduce transmission of cercariae to bivalves in other ways [12]. The diversity of non-host species may therefore create a dilution effect on the transmission of infective stages to the next host in the life cycle, with potential implications for the abundance of foodborne parasites [13]. Estuarine cultures of shellfish may also be exposed to environmentally-resistant cysts of zoonotic protozoans that enter estuaries from terrestrial run-off [11]. In particular, Cryptosporidium spp., which may cause severe diarrhea and which constitute a serious health threat to immunocompromised persons, are abundant in agricultural run-off. The filter-feeding capacity of mollusks makes them likely to concentrate oocysts of Cryptosporidium spp. Experimental studies indicate that oocysts of Cryptosporidium may remain in oyster tissue for several days after exposure [14], but currently nothing is known about the transmission risk to humans who eat raw oysters containing protozoan oocysts. Novel and exotic foods. The consumption of meat from former commercially unimportant sources has increased significantly over the past few decades. Thus, the consumption of reptile and amphibian meat has become ‘trendy’ in developed countries. In addition, an increasing demand for protein-rich food-sources has led to the search of alternative sources of protein, in particular the use of insects and other invertebrates for human consumption and as domesticated animal feed [15]. Insects have the advantage of reduced rearing costs and feasibility of containment at very high densities. However, the potential transmission of foodborne parasites must be considered carefully for these novel and unusual foods. Insects serve as hosts for larval stages of foodborne helminths, and rearing facilities should be constructed to minimize potential transmission of helminths to humans. In particular, care should be taken to avoid fecal contamination from rodents and birds which may provide helminth eggs, for example of tapeworms infective to insects.
Trends in Parasitology April 2015, Vol. 31, No. 4
In conclusion, although natural wildlife is exposed to a much greater diversity of pathogens and parasites than are intensively managed species, a combination of high population densities and habitat alterations may facilitate higher than natural prevalence and parasite burden in semi-farmed wildlife. This issue deserves more attention, and it will become increasingly important in a world where ‘novel’ wildlife is becoming a commercialized industry. References 1 Cattadori, I.M. et al. (2007) Variation in host susceptibility and infectiousness generated by co-infection: the myxoma–Trichostrongylus retortaeformis case in wild rabbits. J. R. Soc. Interface 4, 813–840 2 Wood, C.L. et al. (2010) Fishing out marine parasites? Impacts of fishing on rates of parasitism in the ocean. Ecol. Lett. 13, 761–775 3 Baird, F.J. et al. (2014) Foodborne anisakiasis and allergy. Mol. Cell. Probes 28, 167–174 4 Kapel, C.M.O. et al. (1996) Epidemiologic and zoogeographic studies on Trichinella nativa in arctic foxes, Alopex lagopus, in Greenland. J. Helm. Soc. Wash. 63, 226–232 5 Pozio, E. et al. (2001) Hunting practices increase the prevalence of Trichinella infections in wolves from European Russia. J. Parasitol. 87, 1498–1501 6 Navarro-Gonzalez, N. et al. (2013) Supplemental feeding drives endoparasite infections in wild boar in Western Spain. Vet. Parasitol. 196, 114–123 7 Orlandi, P. et al. (2002) Parasites and the food supply. Food Technol. 56, 72–80 8 Chai, J-Y. et al. (2005) Fish-borne parasitic zoonoses: Status and issues. Int. J. Parasitol. 35, 1233–1254 9 Clausen, J.H. et al. (2012) Relationship between snail population density and infection status of snails and fish with zoonotic trematodes in Vietnamese carp nurseries. PLoS Negl. Trop. Dis. 6, e1945 10 Graczyk, T.K. and Fried, B. (1998) Echinostomiasis: a common but forgotten food-borne disease. Am. J. Trop. Med. Hyg. 58, 501–504 11 Fredensborg, B.L. et al. (2013) Acanthoparyphium sp. and other metazoan symbionts of the American oyster, Crassostrea virginica, from South Texas. J. Parasitol. 99, 1129–1132 12 Thieltges, D.W. et al. (2008) Ambient fauna impairs parasite transmission in a marine parasite–host system. Parasitology 135, 1111–1116 13 Johnson, P.T.J. and Thieltges, D.W. (2010) Diversity, decoys and the dilution effect: how ecological communities affect disease risk. J. Exp. Biol. 213, 961–970 14 Willis, J.E. et al. (2014) Bioaccumulation and elimination of Cryptosporidium parvum oocysts in experimentally exposed Eastern oysters (Crassostrea virginica) held in static tank aquaria. Int. J. Food Microbiol. 173, 72–80 15 Broglia, A. and Kapel, C.M.O. (2011) Changing dietary habits in a changing world: emerging drivers for the transmission of foodborne parasitic zoonoses. Vet. Parasitol. 182, 2–13
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Special Issue: Wildlife Parasitology
Foodborne parasites from wildlife: how wild are they? Christian M.O. Kapel and Brian L. Fredensborg Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark
The majority of wild foods consumed by humans are sourced from intensively managed or semi-farmed populations. Management practices inevitably affect wildlife density and habitat characteristics, which are key elements in the transmission of parasites. We consider the risk of transmission of foodborne parasites to humans from wildlife maintained under natural or seminatural conditions. A deeper understanding will be useful in counteracting foodborne parasites arising from the growing industry of novel and exotic foods.
‘Farmed’ wildlife and foodborne parasites In the overall global food supply, a decreasing proportion of wildlife species are sourced from entirely naturally sustained populations. Thus, sylvatic (truly wild) hosts are predominantly relevant regarding only the transmission of parasitic disease to hunters in native/traditional communities with a non-industrialized food supply. The vast majority of wildlife consumed by humans originates from managed or semi-domesticated wildlife populations, raising the question of how ‘wild’ the majority of wildlife harvested for human consumption actually are (Box 1). This is true for traditional game species, where release of raised animals and provision of additional feed to boost natural populations are common practice. However, a fast-growing aquaculture industry and the culture of shellfish in natural habitats demonstrate that traditional aquatic wildlife used for human consumption is also intensively managed. From a public health perspective, why should we care whether wildlife for consumption comes from naturally sustained or heavily managed populations? First, the degree of wildlife management/farming is likely to impact on the abundance of parasites via manipulation of the host population density, structure, and/or behavior. For example, wildlife kept at artificially high population densities in habitats that resemble their natural environment may facilitate the transmission of parasites with life cycles which require close contact between hosts. Second, wildlife produced in natural habitats interact with other fauna (e.g., hosts harboring parasite infective stages), and they are potentially exposed to an influx of infective stages from the surrounding environment. Surprisingly little is known about the effects of wildlife farming/management on the abundance and composition of foodborne parasites. Corresponding author: Kapel, C.M.O. ([email protected]). Keywords: wildlife parasites; foodborne; zoonotic; management; transmissions. 1471-4922/ ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.pt.2014.12.005
However, increased consumption of ‘farmed’ wildlife, globalization of the food supply, and emerging foodborne diseases from exotic foods indicate that the type and extent of management should be a focus area in future risk assessments of foodborne parasites. Management of wildlife and foodborne parasite transmission to humans The types of human management of wildlife populations of relevance to the transmission of foodborne parasites comprise those that affect the density of wildlife, and those that alter habitat characteristics of importance to parasite transmission. In the following, the potential effects of human intervention on the transmission of foodborne parasites are considered for wildlife harvested from natural ecosystems, and also for wildlife farmed or maintained under semi-natural conditions. Foodborne parasites from commercially exploited natural wildlife populations Intensive exploitation of wildlife in natural ecosystems generally reduces the population density and induces a shift in the age-structure of the exploited populations towards smaller and younger individuals. The consequences of a changing age-structure may be two-fold. First, in mammals, young and naı¨ve individuals are often more sensitive to initial exposure, and thus may contribute significantly more to parasite biomass, particularly in co-infections with other pathogens [1]. In wildlife where acquired immunity is less important, young individuals display a lower parasite burden because they have had less time and opportunity to accumulate parasites. Marine fisheries provide a classic example where overexploitation changes the age-structure of overfished species, thereby reducing the diversity and intensity of parasite infections [2]. The most important foodborne parasites of wild-caught fish are nematodes of the family Anisakidae (primarily from the genera Anisakis and Pseudoterranova). Juvenile anisakids acquired from eating raw or undercooked fish invade the intestinal mucosa and may cause severe epigastric pain, eosinophilic granuloma formation, and chronic allergic conditions [3]. Despite heavy exploitation of fish populations, reported cases of anisakiasis have increased in recent years, perhaps as a consequence of better diagnostic tools in combination with increased transmission from growing populations of definitive hosts (seals and small whales). Hunting practices may provide an overlooked but potentially important route of transmission of foodborne parasites. Thus, carcasses of marine mammals in Greenland and wolves in Russia are often left exposed to Trends in Parasitology, April 2015, Vol. 31, No. 4
125
Science & Society
Trends in Parasitology April 2015, Vol. 31, No. 4
Box 1. What is the definition of wildlife? To understand the drivers of parasite transmission among wildlife, and their interaction with human activity, we first need to define what wildlife is. Traditionally the term wildlife was used for undomesticated vertebrate game species (birds and mammals) living in terrestrial ecosystems. The problem with that definition is that many game species to a greater or lesser degree are managed, although they remain under natural conditions. It also does not adequately address other groups of animals (vertebrates and invertebrates) used for human consumption. Later, as part of the US Endangered Species Act of 1973, wildlife was redefined to encompass all living organisms out of the direct control of man, including undomesticated or cultivated plants and animals. Although more fitting than the traditional definition, the transition from natural to domesticated populations may be subtle (see Table 1 in main text), and foodborne parasites from wildlife may eventually be more likely to be acquired if the wildlife is under human management compared to truly natural populations. In terms of parasite transmission, a more relevant definition of wildlife could therefore include all living organisms living in and interacting with their natural environment.
dogs, foxes, and other scavengers, thereby increasing the local abundance of the roundworm Trichinella spp. which are transmitted by ingestion of undercooked meat containing infective tissue cysts [4,5]. Foodborne parasites from semi-farmed wildlife Semi-natural wildlife encompasses species that are managed but maintained under conditions that allow interactions with the surrounding natural habitat. This group represents a gradient in human intervention, ranging from managed game species in natural habitats to the farming of shellfish, fish, and other wildlife used for human consumption (Table 1). In terms of volume and economic value, this group represents the vast majority of wild foods used for human consumption. Classic game species. Game species used for commercial hunting are often managed in ways that increase the population density of exploited species. The release of raised individuals boosts natural populations, and supplemental feeding may increase interactions among individuals. For example, wild boar aggregate around feeders,
thereby increasing the transmission of endoparasites [6]. An important foodborne parasite from game is Trichinella, acquired especially from wild boar or bear. Trichinella may be transmitted by boars feeding on infected carcasses or scraps left in the habitat after hunting. Thus, increased population density in a game resort where other animals with higher prevalence may be hunted (foxes, raccoon dogs, etc.) may also intensify transmission. Fish farming. More than 50 species of fish-borne parasites are known to infect humans [7]. Most of these originate from freshwater fish. A rapidly growing aquaculture industry in Asia with export of fresh fish to the rest of the World comprises a significant risk of transmission to humans [8]. Larval stages of trematodes are commonly found in meat of farmed fish, which, if consumed raw or undercooked, may be infective to humans. Their transmission relies on the presence of snails (first intermediate host), and the highly eutrophic fish ponds may constitute an ideal habitat for these. The artificially high density of fish greatly increases the transmission from snails to fish, and also elevates infection levels in fish [9]. Finally, the presence of potential definitive (reservoir) hosts, the traditional use of human feces as fertilizer, terrestrial run-off, and water from surrounding natural habitat may supply trematode eggs infective to snails. Shellfish. Shellfish are often cultured in productive estuaries (river deltas), biotops rich in nutrients that facilitate high production yields and increased stocking densities. Estuaries are ideal habitats for many parasites with complex life cycles that exploit the abundance of potential hosts and trophic interactions in the relatively shallow and productive ecosystems. Many estuarine mollusks serve as intermediate hosts for helminths, in particular trematodes, where the larval stage (metacercaria) that can infect birds and mammals is found in soft tissues of clams and oysters. Several representatives of the family Echinostomatidae have been found in humans after eating raw clams or oysters [10]. Most human cases are from Southeast Asia, where infections lead to intestinal pain and discomfort. However, echinostomatids are also
Table 1. Gradient of human intervention in wildlife consumed by humans from unaffected (sylvatic) to domesticated, and the predicted effect on population density and parasite transmission Level of management None (sylvatic) Commercial harvesting of natural populations a
Effects on wildlife population None (i) Reduced host density (ii) Changed age-structure
Release of individuals; provision of additional food into the natural habitat (game) a Farming of wildlife in natural habitats (mussel/oyster cultures in estuaries) a Habitat alteration but interacting with surrounding environment (aquaculture) a
Increased host density; hosts cluster around feeders (transmission foci)
Domestication and separation from natural habitat (e.g., deer farm)
Increased host density; reduced contact with infective stages and treatment of infected individuals
a
Examples of wildlife discussed in the text.
126
Increased host density Increased host density, alteration of host habitat, monocultures
Effect(s) on parasite transmission None (i) Reduced transmission (ii) Altered age-structure may increase (mammals) or decrease (fish, invertebrates) transmission Increased transmission of directly transmitted parasites Provision of food reduces trophic transmission Increased transmission Increased transmission for directly transmitted parasites and for parasites with complex life cycles that depend on intermediate hosts and infective stages from the surrounding environment Reduced transmission
Science & Society abundant in oysters and clams in other parts of the World [11], and they may constitute an overlooked group of foodborne parasites in developed countries where commercial and recreational harvest of oysters is increasing. Interestingly, studies show that the infection of mollusks may be reduced by the presence of other non-host species that feed on infective cercariae or that reduce transmission of cercariae to bivalves in other ways [12]. The diversity of non-host species may therefore create a dilution effect on the transmission of infective stages to the next host in the life cycle, with potential implications for the abundance of foodborne parasites [13]. Estuarine cultures of shellfish may also be exposed to environmentally-resistant cysts of zoonotic protozoans that enter estuaries from terrestrial run-off [11]. In particular, Cryptosporidium spp., which may cause severe diarrhea and which constitute a serious health threat to immunocompromised persons, are abundant in agricultural run-off. The filter-feeding capacity of mollusks makes them likely to concentrate oocysts of Cryptosporidium spp. Experimental studies indicate that oocysts of Cryptosporidium may remain in oyster tissue for several days after exposure [14], but currently nothing is known about the transmission risk to humans who eat raw oysters containing protozoan oocysts. Novel and exotic foods. The consumption of meat from former commercially unimportant sources has increased significantly over the past few decades. Thus, the consumption of reptile and amphibian meat has become ‘trendy’ in developed countries. In addition, an increasing demand for protein-rich food-sources has led to the search of alternative sources of protein, in particular the use of insects and other invertebrates for human consumption and as domesticated animal feed [15]. Insects have the advantage of reduced rearing costs and feasibility of containment at very high densities. However, the potential transmission of foodborne parasites must be considered carefully for these novel and unusual foods. Insects serve as hosts for larval stages of foodborne helminths, and rearing facilities should be constructed to minimize potential transmission of helminths to humans. In particular, care should be taken to avoid fecal contamination from rodents and birds which may provide helminth eggs, for example of tapeworms infective to insects.
Trends in Parasitology April 2015, Vol. 31, No. 4
In conclusion, although natural wildlife is exposed to a much greater diversity of pathogens and parasites than are intensively managed species, a combination of high population densities and habitat alterations may facilitate higher than natural prevalence and parasite burden in semi-farmed wildlife. This issue deserves more attention, and it will become increasingly important in a world where ‘novel’ wildlife is becoming a commercialized industry. References 1 Cattadori, I.M. et al. (2007) Variation in host susceptibility and infectiousness generated by co-infection: the myxoma–Trichostrongylus retortaeformis case in wild rabbits. J. R. Soc. Interface 4, 813–840 2 Wood, C.L. et al. (2010) Fishing out marine parasites? Impacts of fishing on rates of parasitism in the ocean. Ecol. Lett. 13, 761–775 3 Baird, F.J. et al. (2014) Foodborne anisakiasis and allergy. Mol. Cell. Probes 28, 167–174 4 Kapel, C.M.O. et al. (1996) Epidemiologic and zoogeographic studies on Trichinella nativa in arctic foxes, Alopex lagopus, in Greenland. J. Helm. Soc. Wash. 63, 226–232 5 Pozio, E. et al. (2001) Hunting practices increase the prevalence of Trichinella infections in wolves from European Russia. J. Parasitol. 87, 1498–1501 6 Navarro-Gonzalez, N. et al. (2013) Supplemental feeding drives endoparasite infections in wild boar in Western Spain. Vet. Parasitol. 196, 114–123 7 Orlandi, P. et al. (2002) Parasites and the food supply. Food Technol. 56, 72–80 8 Chai, J-Y. et al. (2005) Fish-borne parasitic zoonoses: Status and issues. Int. J. Parasitol. 35, 1233–1254 9 Clausen, J.H. et al. (2012) Relationship between snail population density and infection status of snails and fish with zoonotic trematodes in Vietnamese carp nurseries. PLoS Negl. Trop. Dis. 6, e1945 10 Graczyk, T.K. and Fried, B. (1998) Echinostomiasis: a common but forgotten food-borne disease. Am. J. Trop. Med. Hyg. 58, 501–504 11 Fredensborg, B.L. et al. (2013) Acanthoparyphium sp. and other metazoan symbionts of the American oyster, Crassostrea virginica, from South Texas. J. Parasitol. 99, 1129–1132 12 Thieltges, D.W. et al. (2008) Ambient fauna impairs parasite transmission in a marine parasite–host system. Parasitology 135, 1111–1116 13 Johnson, P.T.J. and Thieltges, D.W. (2010) Diversity, decoys and the dilution effect: how ecological communities affect disease risk. J. Exp. Biol. 213, 961–970 14 Willis, J.E. et al. (2014) Bioaccumulation and elimination of Cryptosporidium parvum oocysts in experimentally exposed Eastern oysters (Crassostrea virginica) held in static tank aquaria. Int. J. Food Microbiol. 173, 72–80 15 Broglia, A. and Kapel, C.M.O. (2011) Changing dietary habits in a changing world: emerging drivers for the transmission of foodborne parasitic zoonoses. Vet. Parasitol. 182, 2–13
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