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Mixed-Host Aggregations and Helminth Parasite Sharing in an East African

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Mixed-Host Aggregations and Helminth Parasite Sharing in an East African G Model VETPAR-7331; No. of Pages 9 ARTICLE IN PRESS Veterinary Parasitology xxx (2014) xxx–xxx Contents lists available at ScienceDirect Veterinary Parasitology jo urnal homepage: www.elsevier.com/locate/vetpar Mixed-host aggregations and helminth parasite sharing in an East African wildlife–livestock system a,b,∗ c d Kimberly VanderWaal , George Paul Omondi , Vincent Obanda a Animal Behavior Graduate Group, University of California, Davis, 1 Shields Avenue, Davis, CA 95616, USA b Wangari Maathai Institute for Peace and Environmental Studies, University of Nairobi, PO Box 29053-00625, Nairobi, Kenya c Wildlife Management Department, Ol Pejeta Conservancy, Private Bag – 10400, Nanyuki, Kenya d Veterinary Services Department, Kenya Wildlife Service, P.O. Box 40241-00100, Nairobi, Kenya a r t i a b s c t l e r a i n f o c t Article history: Parasitic infections transmitted between livestock and wildlife pose a significant risk to Received 21 December 2013 wildlife conservation efforts and constrain livestock productivity in tropical regions of the Received in revised form 20 May 2014 world. Gastrointestinal helminths are among the most ubiquitous parasites, and many par- Accepted 10 July 2014 asites within this taxon can readily infect a wide range of host species. Factors shaping bidirectional transmission of parasites in wildlife–livestock systems are understudied. In Keywords: this study, we investigate the prevalence and diversity of helminth infections in an East Wildlife–livestock interface African community of wild and domestic ungulates. We also identify pairs of host species Wildlife disease between which transmission may be possible based on shared parasite taxa, and explore Interspecific transmission the role of multi-host aggregations in shaping patterns of parasite sharing. Helminth taxa Social behavior detected included Trichostrongylus, Trichuris, Paramphistomum, Skrjabinema, Strongyloides, Parasite prevalence Savanna ecosystems Strongylus spp., and other strongyle-type nematodes. We found that nearly 50% of indi- viduals harbored at least one species of helminth, but certain species, such as zebra and impala, exhibited higher prevalence than others. High canopy feeders, like giraffe, had lower prevalence than hosts feeding at medium and low foraging heights. For helminths, patterns of parasite sharing likely emerge from shared space use, which is mediated in part by mixed-species aggregations. The frequency with which host species associated together in mixed-species aggregations was positively correlated with the number of parasite taxa shared. We suggest that variation among species in their tendency to form mixed-species aggregations creates heterogeneity in transmission opportunities, and consequently, par- asite sharing across ungulate species. These results enhance our understanding of the role of spatiotemporal relationships among host species in shaping parasite communities in mixed wildlife–livestock grazing systems. © 2014 Elsevier B.V. All rights reserved. 1. Introduction biologists and livestock owners (Cleaveland et al., 2000; Haydon et al., 2002; Kock, 2005; Osofsky, 2005; Delahay Parasitic infections are a concern for many wildlife pop- et al., 2009). Approximately 77% of livestock pathogens are ulations and are a growing issue for both conservation multi-host (Cleaveland et al., 2001), and pathogens shared among livestock and wild ungulates may have adverse effects on both populations. Indeed, most endangered ∗ Corresponding author at: Animal Behavior Graduate Group, Univer- species at risk from disease acquire their pathogens from sity of California, Davis, 1 Shields Avenue, Davis, CA 95616, USA. domestic populations (Altizer et al., 2003), and wildlife Tel.: +1 530 204 8555. serve as a reservoir for many economically important E-mail addresses: [email protected], livestock diseases (Wambwa, 2005; Michel and Bengis, [email protected] (K. VanderWaal). http://dx.doi.org/10.1016/j.vetpar.2014.07.015 0304-4017/© 2014 Elsevier B.V. All rights reserved. Please cite this article in press as: VanderWaal, K., et al., Mixed-host aggregations and helminth parasite sharing in an East African wildlife–livestock system. Vet. Parasitol. (2014), http://dx.doi.org/10.1016/j.vetpar.2014.07.015 G Model VETPAR-7331; No. of Pages 9 ARTICLE IN PRESS 2 K. VanderWaal et al. / Veterinary Parasitology xxx (2014) xxx–xxx 2012). Pathogen transmission is of particular concern perhaps because the diversity of closely related hosts cre- in sub-Saharan Africa because of the close proximity of ated opportunities for parasite sharing or host-switching. wildlife to livestock and the high prevalence and diver- In addition, ungulate species with higher levels of spatial sity of pathogens (Cleaveland et al., 2005; Wambwa, 2005). contact with heterospecifics were more likely to be infected Despite the potential importance of wildlife in pathogen with strongyle-type nematodes, suggesting that indirect transmission dynamics, many parasitological studies focus contact via shared space use generates interspecific trans- on domestic species while the potential for wildlife and mission opportunities (Ezenwa, 2003). However, the role livestock to share parasites is largely overlooked. of mixed-species aggregations in shaping parasite com- Gastrointestinal helminths are among the most ubiqui- munities remains less clear, and the importance of such tous parasites worldwide (Petney and Andrews, 1998). In spatiotemporal contact in African ecosystems where both central Kenya, helminth prevalence in cattle can approach cattle and wildlife are present has not yet been examined. 90% (Waruiru et al., 2000). These parasites can play a role in The objectives of this study were to survey helminth regulating wildlife populations (Gulland, 1992), and have parasites in a mixed system comprised of wild and domes- been shown to have detrimental health effects on wildlife tic ungulates in a semi-arid region of Kenya, and to and domestic animals, such as impaired growth and devel- investigate the risk of interspecific transmission at the opment (Falvey and Bambridge, 1975; Stein et al., 2002). In wildlife–livestock interface. We provide baseline data on domestic ruminants, infections can depress growth rates helminth prevalence and diversity, and identify pairs of by >25%, reduce fecundity and milk yields by 30%, and host species between which transmission is possible based increase risk of mortality (Carles, 1992; Thumbi et al., on shared parasite taxa. We further explore how mixed- 2013a; Thumbi et al., 2013b). Thus, helminths are an species aggregations contribute to parasite sharing. important factor limiting livestock productivity. In free- ranging wild ungulates, infected animals have been shown to have lower body mass, reduced fecundity, and higher mortality rates (Gulland, 1992; Stein et al., 2002). In addi- 2. Methods tion, helminths have strong effects on immune function and, consequently, host responses to secondary infections 2.1. Study site and species (Graham et al., 2007; Ezenwa and Jolles, 2011). For exam- ple, African buffalo (Syncerus caffer) are less able to tolerate This study was conducted in Ol Pejeta Conservancy 2 bovine tuberculosis infection if co-infected by helminths (OPC), a 364-km wildlife reserve and commercial cat- (Jolles et al., 2008), and buffalo treated with anthelmintic tle ranch in central Kenya. OPC is a semi-arid savanna ◦ ◦ drugs exhibit altered immune function relevant to tuber- ecosystem located on the equator (0 N, 36 56 E), receiv- culosis infection (Ezenwa et al., 2010). ing on average 900 mm of rainfall per year (Birkett, 2002). Interspecific transmission of helminths via fecal–oral Species included in this study included the African buf- mechanisms readily occurs between sympatric ungulates falo (S. caffer, Conservation status: Least concern), eland (Sachs and Sachs, 1968; Preston et al., 1979; Waruiru (Taurotragus oryx, status: Least concern), Thomson’s gazelle et al., 1995). However, in order to accurately quantify (Gazella thomsonii, status: Near threatened), reticulated transmission risk at the wildlife–livestock interface, we giraffe (Giraffa camelopardalis reticulata, sub-species status: need to better understand factors that impact interspecific Lower risk – conservation dependent), Jackson’s hartebeest transmission dynamics (Osofsky, 2005). Within a single (Alcelaphus buselaphus jacksonii, sub-species status: Endan- species, it has been well documented that patterns of con- gered), impala (Aepyceros melampus, status: Least concern), tact and interaction among conspecifics are crucial factors plains zebra (Equus burchelli, status: Least concern), and determining transmission patterns (Coté and Poulin, 1995; domestic cattle (Bos indicus). Cattle were minimally man- Altizer et al., 2003). Generally, higher levels of interac- aged and free-ranging within OPC. Cattle shared grazing tion create transmission opportunities among conspecifics pastures and water sources with wildlife during the day. (Altizer et al., 2003; Godfrey et al., 2009; VanderWaal et al., Cattle were not routinely de-wormed. 2014a), and parasite prevalence, intensity, and diversity Dietary niche is likely to affect both parasite exposure are correlated with intraspecific variation in group size and the internal environment within the gut (Dehority and (Hoogland, 1979; Brown and Brown, 1986; Rubenstein and Odenyo, 2003; Apio et al., 2006). Ungulate dietary niches Hohmann, 1989). In addition, neighboring social groups lay along a
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