Ticks infesting captive and free-roaming wild animal species at the São Paulo Zoo , São Paulo , Brazil

Ticks are ectoparasites of worldwide distribution that affect vertebrates and can transmit pathogens to animals and humans. The Zoological Park Foundation of São Paulo (FPZSP) is located in a Conservation Unit in one of the most important remaining fragments of the Atlantic Rainforest biome in the suburbs of São Paulo, Brazil. The FPZSP houses more than 3,000 wild animals on exhibit, in breeding programs and in environmental education programs, and also attracts migratory birds and free-roaming wildlife. This study focused on identifying the diversity of tick species that infest captive and free-roaming animals at the FPZSP. The collection of ticks kept at the FPZSP contains 523 specimens that were collected from different host species between 1990 and 2017. Ten tick species were found. In addition, Amblyomma aureolatum (Pallas) was found on stray cats living in the Atlantic forest fragment in the FPZSP. This study reveals a low occurrence of parasitism in captive animals and a high diversity of tick species collected from hosts in this Atlantic forest fragment, contributing information about host-parasite relationships and potential vectors of zoonotic diseases, since the vectors of Brazilian spotted fever, A. aureolatum and Amblyomma sculptum Berlese, were found in some hosts.

Ticks are ectoparasites of worldwide distribution that affect vertebrates and can transmit pathogens to animals and humans (GUGLIELMONE et al., 2014;NAVA et al., 2017).The host specificity of ticks is variable; some species are associated with specific groups of hosts while other species are less selective.Generally, larvae and nymphs of species that must infest more than one host species to complete their life cycles feed on small animals, while adult ticks prefer to parasitize medium and large sized-animals (BARROS-BATTESTI et al., 2006;ESSER et al., 2016).
The Zoological Park Foundation of São Paulo (FPZSP) is located in a Conservation Unit covering an area of 824,529 square meters in the Fontes do Ipiranga State Park (PEFI), one of the most important remaining fragments of the Atlantic forest biome in the suburbs of São Paulo, southeastern Brazil.The FPZSP, which maintains more than 3,000 wild mammal, bird, reptile, amphibian and invertebrate species, in breeding programs, also provides sanctuary for migrating birds and free-roaming animals (ZOOLÓGICO DE SÃO PAULO, 2017) The role played by modern zoos is not only to preserve the quality of life of captive animals but also to find ways to preserve wild animals and their habitats.Thus, when a free-roaming wild animal is debilitated it is cared for by a specialized support team from the FPZSP, which includes a close examination to detect the presence of ectoparasites.As a result, this institution started a collection of ticks removed from captive and free-living wildlife, which now contains hundreds of specimens.
The purpose of this study was to identify the tick species that have been collected from captive animals in the FPZSP, and from free-roaming animals living in the PEFI.
From 1990 to 2017, ticks were collected from animals kept by the Department of Applied Research, including captive and free-living wild animals at the FPZSP and PEFI.During the handling or clinical examination of animals, ticks were manually removed from their hosts and immediately stored in plastic vials containing 70% ethanol for subsequent taxonomic identification under a stereomicroscope, based on taxonomic keys and corresponding literature (ARAGÃO & FONSECA, 1961;ONOFRIO et al., 2006aONOFRIO et al., , b, 2009;;MARTINS, T., et al., 2010MARTINS, T., et al., , 2016)).The nomenclature used for the identification of bird and mammals followed Sick (1997) 1.
Nymphs of A. varium have been recorded on Bradypus tridactylus Linnaeus, and Bradypus torquatus Illiger in Brazil (MARQUES et al., 2002).The present record of nymphs of A. varium on B. variegatus in the FPZSP is consistent with an earlier study which found that nymphs of this tick species use sloths of the genus Bradypus as hosts.
We report for the first time the occurrence of R. sanguineus s.l. on a captive T. terrestris.In Brazil, R. sanguineus s.l. is described as a nidicolous tick that is associated with human dwellings usually inhabited by domestic dogs, the primary host of this tick species (LABRUNA et al., 2005).While we have no information about habitat sharing by the R. sanguineus infested tapir and domestic dogs, this finding confirms the potential of this exotic tick to infest native wild mammals, provided they are reared under artificial conditions.
The present report of females of A. sculptum on T. terrestris supports a recent study at another zoo located in the state of São Paulo (MARTINS, T., et al., 2015).It should be noted that A. sculptum is considered the main vector of Rickettsia rickettsii, the etiological agent of Brazilian spotted fever, a potentially fatal tick-borne disease in Brazil (MARTINS, T., et al., 2016).
During our study, three stray cats [Felis catus (Linnaeus)] were also captured inside the FPZSP, and one male and three females of A. aureolatum were collected from these cats.The tick A. aureolatum is incriminated as the main vector of R. rickettsii in Atlantic forest fragments in the São Paulo metropolitan region, where domestic dogs (its main hosts) are considered to be carriers of infected ticks from the forest to human dwellings, thereby increasing the risk of human cases of Brazilian spotted fever (SZABÓ et al., 2013;SARAIVA et al., 2014).Our findings indicate that stray domestic cats are also potential carriers of A. aureolatum ticks to human dwellings, a fact that should also be taken into account in the surveillance of Brazilian spotted fever in the metropolitan area of São Paulo, since human cases of the disease have been recorded in the surroundings of this forest fragment (OGRZEWALSKA et al., 2012).
This paper describes the relatively low occurrence of tick parasitism on captive wild animals at the FPZSP, and at the same time demonstrates a high diversity of tick species in free-roaming animal species living in the Atlantic forest fragment of the PEFI.These findings contribute with information about host-parasite relationships and potential vectors of tick-borne diseases transmitted to animals and humans, as indicated by two main vectors of R. rickettsii, the ticks A. aureolatum and A. sculptum, which were found in the study area.Martins, T., et al. (2015) (number of examined animals).M: male; F: female; N: nymph; L: larvae; *New host association for the tick stage.

Table 1 .
Ticks collected from wild animals at the Zoological Park Foundation of São Paulo and the Fontes do Ipiranga State Park in São Paulo, Brazil, from 1990 to 2017, and previous records of tick-host relationship.