International Journal for Parasitology: Parasites and Wildlife 2 (2013) 1–9 Contents lists available at SciVerse ScienceDirect International Journal for Parasitology: Parasites and Wildlife journal homepage: www.elsevier.com/locate/ijppaw Tick infestation patterns in free ranging African buffalo (Syncercus caffer): Effects of host innate immunity and niche segregation among tick species q ⇑ Kadie Anderson a, Vanessa O. Ezenwa b, Anna E. Jolles c, a Department of Biomedical Sciences, College of Veterinary Medicine, Oregon State University, Corvallis, OR 97331, United States b Odum School of Ecology, University of Georgia, Athens, GA 30602, United States c Department of Biomedical Sciences and Department of Zoology, Oregon State University, Corvallis, OR 97331, United States article info abstract Article history: Ticks are of vast importance to livestock health, and contribute to conflicts between wildlife conservation Received 21 September 2012 and agricultural interests; but factors driving tick infestation patterns on wild hosts are not well under- Received in revised from 30 October 2012 stood. We studied tick infestation patterns on free-ranging African buffalo (Syncercus caffer), asking (i) is Accepted 1 November 2012 there evidence for niche segregation among tick species?; and (ii) how do host characteristics affect var- iation in tick abundance among hosts? We identified ticks and estimated tick burdens on 134 adult female buffalo from two herds at Kruger National Park, South Africa. To assess niche segregation, we eval- Keywords: uated attachment site preferences and tested for correlations between abundances of different tick spe- Amblyomma hebraeum cies. To investigate which host factors may drive variability in tick abundance, we measured age, body Co-infestation Immunity condition, reproductive and immune status in all hosts, and examined their effects on tick burdens. Host traits Two tick species were abundant on buffalo, Amblyomma hebraeum and Rhipicephalus evertsi evertsi. A. Rhipicephalus evertsi evertsi hebraeum were found primarily in the inguinal and axillary regions; R. e. evertsi attached exclusively in the perianal area. Abundances of A. hebraeum and R. e. evertsi on the host were unrelated. These results suggest spatial niche segregation between A. hebraeum and R. e. evertsi on the buffalo. Buffalo with stron- ger innate immunity, and younger buffalo, had fewer ticks. Buffalo with low body condition scores, and pregnant buffalo, had higher tick burdens, but these effects varied between the two herds we sampled. This study is one of the first to link ectoparasite abundance patterns and immunity in a free-ranging mammalian host population. Based on independent abundances of A. hebraeum and R. e. evertsi on indi- vidual buffalo, we would expect no association between the diseases these ticks transmit. Longitudinal studies linking environmental variability with host immunity are needed to understand tick infestation patterns and the dynamics of tick-borne diseases in wildlife. Ó 2012 Australian Society for Parasitology Published by Elsevier Ltd. All rights reserved. Introduction 2010) and Theileria parva strains (causing Corridor Disease in South Africa, East Coast Fever in East Africa, and January Disease in Ticks are of considerable importance to wildlife and livestock Zimbabwe, Bishop et al., 2004) are examples of important health due to their role as vectors of an impressive array of infec- tick-borne pathogens causing clinical disease in livestock. These tious agents, as well as direct injury caused by piercing the host’s pathogens are often carried by wildlife species, and some also skin (Allen, 1994). Widely distributed infectious agents such as cause zoonotic disease in humans. As such, ticks and the pathogens Ehrlichia ruminantium (causative agent of heartwater, Allsopp, they transmit are particularly relevant at the wildlife/livestock/hu- 2010), Babesia bigemina (causative agent of bovine babesiosis/Afri- man interface (Smith and Parker, 2010). can redwater, Bock et al., 2004; Suarez and Noh, 2011), Anaplasma Despite this, few studies have focused on quantifying the abun- marginale (causative agent of bovine anaplasmosis, Kocan et al., dance and co-infestation patterns of different tick species on wild- life hosts. When parasites co-occur on a host they may compete for space or resources, facilitate one another, or avoid one another by q This is an open-access article distributed under the terms of the Creative segregating to occupy different ecological niches (Rohde, 1979; Commons Attribution-NonCommercial-ShareAlike License, which permits non- Chilton et al., 1992; Simkova et al., 2002; O’Callaghan et al., commercial use, distribution, and reproduction in any medium, provided the 2006). Niche segregation has been observed in both internal para- original author and source are credited. ⇑ Corresponding author. Tel.: +1 541 737 4719. sites (O’Callaghan et al., 2006) and ectoparasites (Spickett et al., E-mail address: [email protected] (A.E. Jolles). 1991; Simkova et al., 2002). Mechanisms of niche segregation in 2213-2244/$ - see front matter Ó 2012 Australian Society for Parasitology Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ijppaw.2012.11.002 2 K. Anderson et al. / International Journal for Parasitology: Parasites and Wildlife 2 (2013) 1–9 parasites include specialization of mouthparts to take advantage of reproductive status, and simple measures of innate and adaptive specific attachment sites (Simkova et al., 2002), utilizing different immunity, affect tick intensities? food sources (mites vs. ticks), or temporal separation (winter emer- gence vs. spring emergence; Mullen et al., 2009). Niche segregation Material and methods reduces competition over evolutionary time and may allow multi- ple tick species to coexist on the host. As such, niche segregation Study population may increase the risk of concurrent exposure to pathogens vectored by different tick species. By contrast, current competition among We sampled buffalo from two herds in the southern section of tick species would be expected to reduce vector co-occurrence on Kruger National Park (KNP), the Lower Sabie (LS) herd and the individual hosts, leading to disparate infection profiles for the dis- Crocodile Bridge (CB) herd. Each of our study herds comprises eases they transmit. Understanding tick co-infestation patterns approximately 800–1000 buffalo. KNP is located within the can thus lead to a better understanding of tick-associated morbidity Mpumalanga province of South Africa and covers 18,989 total as well as the epidemiology of tick-borne diseases. square kilometers, with a total buffalo population of approximately Spatial and temporal abundance patterns of ticks have been 30,000 individuals (Cross et al., 2009). Young adult female buffalo investigated in the context of environmental factors, such as climatic were captured via chemical immobilization by helicopter during variables (e.g. Jackson et al., 1996; Olwoch et al., 2007; Randolph, two separate capture periods from June 23 to July 5, 2008 (LS herd) 2008, Estrada-Pena, 2009; Gilbert, 2010), fire (e.g. Davidson et al., and October 1 to 8, 2008 (CB herd). These captures were conducted 1994; Horak et al., 2006a; Padgett et al., 2009), habitat type and con- to initiate a 4 year longitudinal study on disease ecology in the buf- figuration (Ostfeld et al., 1995; Fyumagwa et al., 2007; Thamm et al., falo. Animals were immobilized with a combination of etorphine 2009). In livestock species, host factors including genetic and immu- hydrochloride (M99) and ketamine and reversed with diprenor- nological traits that confer varying degrees of resistance to tick infes- phine (M5050) following data collection. Captures were performed tation have been of great interest (O’Neill et al., 2010; Berman, 2011; by South African National Parks (SANParks) veterinarians and Carvalho et al., 2011; Neto et al., 2011). Comparisons of tick burdens game capture staff, and all procedures approved by Oregon State among African ungulate species have indicated that host body size University (ACUP# 3267), University of Montana (AUP#: 027- and habitat preference affect tick abundance, with larger species 05VEDBS-082205), and SANParks Institutional Care and Use Com- and browsers more heavily infested with ticks than smaller species mittees. Two hundred buffalo were captured in total (100 per and grazers (Olubayo et al., 1993; Gallivan and Horak, 1997). Resis- herd); of these, 166 animals were sampled for ticks. Thirty-four tance to ticks has been invoked to explain low tick burdens (e.g. blue animals were omitted due to time constraints during captures. wildebeest: Horak et al., 1983), or failure of some tick species to de- velop on wildlife species (e.g. Rhipicephalus (Boophilus) decoloratus on African buffalo: Horak et al., 2006b). behavioral: traits such as Specimen collection grooming (Mooring et al., 2004) and aggregation of conspecifics (Monello and Gompper, 2010) may modify tick burdens, and individ- Ticks were collected from three body areas on each buffalo: ax- ual traits such as sex, developmental stage, and reproductive status illa, inguinal, and perianal. These areas were selected due to the have been shown to affect tick burdens in several wildlife species high density of tick attachment associated with these regions in (e.g. Cape ground squirrel: Hillegass et al., 2008; bison: Mooring cattle (Barnard et al., 1989), which we confirmed also to be the case