Ticks (Acari: Ixodidae) on Dogs from Uberlândia, Minas Gerais, Brazil

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Ticks (Acari: Ixodidae) on Dogs from Uberlaˆndia, Minas Gerais, Brazil M. P. J. Szabo´1, L. G. A. de Souza1, M. M. M. Olega´rio1, F. A. Ferreira2 and A. de Albuquerque Pajuaba Neto2 1 2

Faculdade de Medicina Veterina´ria da Universidade Federal de Uberlaˆndia, Uberlaˆndia, MG, Brazil Centro de Controle de Zoonoses, Uberlaˆndia, Minas Gerais, Brazil

Keywords: Uberlaˆndia; Brazil; dog; tick; infestation; urban; rural; ixodidae Correspondence: M. P. J. Szabo´. Faculdade de Medicina Veterina´ria da Universidade Federal de Uberlaˆndia, Av. Para´, 1720, Campus Umuarama-Bloco 2T, Uberlaˆndia, MG, Brazil CEP 38400-902. Tel.: +55 (034) 3218-2228; Fax: +55(034) 3218 2521; E-mail: [email protected] Received for publication July 03, 2009 doi:10.1111/j.1865-1682.2010.01111.x

Summary Uberlaˆndia in Minas Gerais State, southeastern Brazil, has 622 000 inhabitants and is located in the Cerrado biome, the South American savannah. The city dog population is estimated at 82 000 and identification of tick species and infestation prevalence on this host has not been determined. A major infectious disease of dogs in the city, canine ehrlichiosis, is transmitted by Rhipicephalus sanguineus ticks. At the same time, autochthonous leishmaniosis has been recently described in the city and a role for dog ticks in the disease transmission has been supposed in Brazil. In this work, we present general information on dog ticks in Uberlaˆndia municipality and region. Dogs from 33 farms and 31 districts were examined for ticks from July 2007 to February 2009. On the whole, 413 dogs were examined, 311 (75.3%) from the city and 102 (24.6%) from rural area. Overall infestation rate of dogs from Uberlaˆndia was 37.3% and the mean infestation intensity was 3.25 parasites per dog. In the urban area, 100 dogs (32.2%) had ticks whereas 54 dogs (52.9%) from rural areas were infested. Four tick species were found: Rhipicephalus sanguineus, Amblyomma cajennense, Amblyomma ovale and Boophilus microplus. In the city, only R. sanguineus and one A. cajennense was found on dogs and R. sanguineus and A. ovale were the main dog ticks in rural areas.

Introduction Ticks are important ectoparasites of both humans and animals and, among their wide array of deleterious effects, pathogen transmission to hosts is outstanding. Dog ticks are particularly important, not only because dogs are domestic and companion animals, but, dogs with their worldwide distribution and many times unrestricted movement may carry ticks and pathogens to preserved environments becoming wildlife conservation issue, and, dog ticks may transmit zoonotic diseases to humans. For instance, ticks carried by dogs have been implicated in the transmission to humans of the Rocky Mountain (Demma et al., 2005) and Brazilian Spotted Fever (Pinter and Labruna, 2006). Thus, knowledge on tick infestations of dogs may be crucial information for 72

public and animal health and many times for wildlife conservation. Even though several recent works reported dog tick fauna in various Brazilian municipalities, these are still very few and scattered. At the same time, Brazil is a vast country with an amazing biodiversity and there is an increasing awareness towards conservation. We herein describe for the first time the dog tick fauna from Uberlaˆndia, an important municipality from Minas Gerais State, Brazil. Materials and Methods Study site and landscape Uberlaˆndia is located in Minas Gerais State, southeastern Brazil (18º55¢07¢’ S, 48º16¢38¢’ WGR) at an average

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altitude of 863 m above see level. The municipality of 622 000 inhabitants is 556 km distant from the State Capital, Belo Horizonte, and has close to 4000 km2 whereas the urban area covers, approximately, 135 km2. The municipality is located in the Cerrado biome, the South American savannah, and the region is characterized by a subtropical climate with two well-defined seasons: a dry winter (May to September) and a rainy summer (October to April). The mean annual temperature and precipitation are 22C and 1650 mm, respectively. The city dog population is estimated at 82 000. Data collection Ticks from dogs were collected from both urban and rural areas. Urban sampling occurred during the rabies vaccination campaign of 2007 (July and August) at 31 districts distributed all over the city. At each district, approximately 10 dogs were examined for ticks. Rural areas were sampled during the same campaign and additional collections were done until February 2009 among 33 properties (small farms) with ticks being collected from one to nine dogs at each location. With the permission of the animal owners, a thorough examination for ticks of approximately 5 min was performed on each dog. A tick infestation level score was set up as follows: 0 (no tick found); + (1 to 10 ticks); ++ (11 to 100); +++ (more than 100). Tick identification Collected ticks were identified according to the key of Barros-Battesti et al. (2006). Since there is no complete and reliable key for Amblyomma immatures of South America, they were retained as Amblyomma sp. Voucher samples were deposited in the Tick collection of the Federal University of Uberlaˆndia, accession numbers 466–469. Results On the whole, 413 dogs were examined, 311 (75.3%) from urban areas and 102 (24.6%) from rural properties. Rhipicephalus sanguineus (Latreille, 1806) was the most numerous species with 262 (97%) adults and 7 (2.6%) nymphs on urban dogs and 369 (65.3%) adults and 36 (6.4%) nymphs on rural dogs. Only one (0.4%) adult Amblyomma cajennense (Fabricius, 1787) was found on urban dogs whereas five adults (0.9%) were recovered from rural dogs. All other species were found only on rural dogs and included seven (1.2%) Amblyomma ovale (Koch 1844) adults, 137 (24.2%) nymphs and nine (1.6%) larvae of Amblyomma sp. and two (0.4%) Boophilus microplus (Canestrini, 1887) nymphs.

Dog Ticks in Uberlaˆndia, Brazil

The overall infestation rate was of 37.3%, the mean infestation intensity of 3.25 parasites and density of two ticks per animal. In the urban area 100 dogs (32.2%) had ticks whereas 54 dogs (52.9%) from rural areas were infested. Mean infestation intensity was 2.7 ticks in urban areas and 10.5 in rural areas and tick density 0.87 and 5.54, respectively. In the urban area, 71% of the dogs had low (1–10 ticks), 26% medium (11–100 ticks) and 3% high (more than 100 ticks) infestation levels. In the rural area, 74.1% of the dogs had low, 18.5% medium and 7.4% high infestation levels. Host ears where the preferred location of parasitism (36.1% of the ticks) followed by inter-digital space (18.3%), back (16.3%) and neck (13.4%). Discussion As observed before in the Neotropics, R. sanguineus ticks dominated urban infestations with approximately 30% of prevalence (Szabo´ et al., 2001; Barros-Battesti et al., 2006). In this regard, it is important to mention that this tick species was brought to Brazil with colonization and its biosystematic status is still uncertain (Szabo´ et al., 2005). It is the main vector of canine erlichiosis in the country and might be implicated in zoonotic disease transmission. The only other tick species found in the urban area was A. cajennense, a horse tick in domestic environment. The source of this tick was attributed to a horse grazing on an abandoned and neighbouring property. Rhipicephalus sanguineus also dominated infestations in rural areas. This tick species was associated with dogs restricted by fences or tied to their houses and thus living in a microenvironment similar to those of urban dogs. However, in rural areas, many Amblyomma ticks were found as well. More than half of the estimated 61 Brazilian tick species are Amblyomma and they parasitize wild and domestic animals (Barros-Battesti et al., 2006). Hunting dogs and/or those living unrestricted were those displaying Amblyomma tick infestations. Infestation of dogs in such cases occurred in areas used also by wild animals or horses. For instance, A. ovale is a tick associated with wild carnivores and A. cajennense with tapirs, capybaras and horses (Labruna et al., 2002; Barros-Battesti et al., 2006). It must be emphasized, however, that Amblyomma infestations must have been underestimated. Unrestricted dogs harbouring these ticks are more difficult to find, hold and examine. Likewise infestation of dogs with the cattle tick (B. microplus) has also been reported before (Szabo´ et al., 2001) and shows the frequent access of the carnivore host to highly infested bovine pastures. Unfortunately, there are no reliable keys for the identification of Brazilian Amblyomma immatures and they

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Dog Ticks in Uberlaˆndia, Brazil

could not be identified. At the same time, high numbers of nymphs found could be attributed to a seasonal influence. Most of the ticks were collected during winter and, although seasonal distribution of ticks is not known for most of the Neotropical ticks, Amblyomma species studied so far display a 1-year generation pattern with adults predominating in spring and summer, larvae in autumn and nymphs in winter and spring (Labruna et al., 2002; Szabo´ et al., 2009). Results herein presented can only be viewed as initial data on dog tick infestations from such a big inland municipality in Brazil. Data collection was restricted by seasonal influences. Moreover, high infestation rates in a few animals precluded collection of all ticks and tick density and abundance are thus underestimated. Tick pathogens by themselves should deserve specific research. Such research will certainly rely on these results and will provide a better picture of dog infestations. Acknowledgement This research was supported by Conselho Nacional de Desenvolvimento Cientı´fico e Tecnolo´gico – CNPq (scholarship to L.G. A. Souza and Academic Career Research Fellowship to M.P.J. Szabo´). References Barros-Battesti, D. M. B., M. Arzua, and G. H. Bechara, 2006: Carrapatos de Importaˆncia Medico-Veterina´ria da Regia˜o

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Neotropical: Um Guia Ilustrado Para Identificac¸a˜o de Espe´cies. Vox/ICTTD-3/Butantan, Sa˜o Paulo. Demma, L. J., M. S. Traeger, W. L. Nicholson, C. D. Paddock, D. M. Blau, M. E. Eremeeva, G. A. Dasch, M. L. Levin, J. Singleton, S. R. Zaki, J. E. Cheek, D. L. Swerdlow, and J. H. McQuiston, 2005: Rocky Mountain spotted fever from an unexpected tick vector in Arizona. New Engl. J. Med. 353, 587–594. Labruna, M. B., N. Kasai, F. Ferreira, J. L. H. Faccini, and S. M. Gennari, 2002: Seasonal dynamics of ticks (Acari: Ixodidae) on horses in the state of Sa˜o Paulo, Brazil. Vet. Parasitol. 105, 65–77. Pinter, A., and M. B. Labruna, 2006: Isolation of Rickettsia rickettsii and Ricketttsia felis in cell culture from the tick Amblyomma aureolatum in Brazil. Ann. NY Acad. Sci. 1078, 523–530. Szabo´, M. P. J., T. M. Cunha, A. Pinter, and F. Vicentini, 2001: Ticks (Acari: Ixodidae) associated with domestic dogs in Franca region, Sa˜o Paulo, Brazil. Exp. Appl. Acarol. 25, 909–916. Szabo´, M. P. J., A. J. Mangold, J. F. Carolina, G. H. Bechara, and A. A. Guglielmone, 2005: Biological and DNA evidence of two dissimilar populations of the Rhipicephalus sanguineus tick group (Acari: Ixodidae) in South America. Vet. Parasitol. 130, 131–140. Szabo´, M. P. J., M. B. Labruna, M. V. Garcia, A. Pinter, K. C. Castagnolli, R. C. Pacheco, M. B. Castro, V. A. Veronez, G. M. Magalha˜es, A. Vogliotti, and J. M. B. Duarte, 2009: Ecological aspects of free-living ticks (Acari: Ixodidae) on animal trails in an Atlantic rainforest of Southeastern Brazil. Ann. Trop. Med. Parasitol. 103, 57–72.

ª 2010 Blackwell Verlag GmbH • Transboundary and Emerging Diseases. 57 (2010) 72–74

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