Ticks parasitizing wild mammals in Atlantic Forest areas in the state of Rio de Janeiro, Brazil

Carrapatos parasitando mamíferos silvestres em áreas da Floresta Atlântica no estado do Rio de Janeiro, Brasil

Hermes Ribeiro Luz Sócrates Fraga da Costa Neto Marcelo Weksler Rosana Gentile João Luiz Horacio Faccini About the authors

Abstract

Mammals captured in the Serra dos Órgãos National Park (PARNASO) and the Pedra Branca State Park (PBSP) between 2012 and 2015 were examined for the presence of ticks. In total, 140 mammals were examined, and 34 specimens were found to be parasitized by ticks. Didelphis aurita, Akodon montensis and Oligoryzomys nigripes were the species most parasitized. From these specimens, 146 ticks were collected, including 10 larvae. The ticks belonged to eight species: one in the genus Ixodes and seven in the genus Amblyomma. This study reports new associations of ticks and wild mammals in Brazil.

Keywords:
PARNASO; Amblyomma; Ixodes; mammals; parasitism

Resumo

Mamíferos capturados no Parque Nacional da Serra dos Órgãos (PARNASO) e no Parque Estadual Pedra Branca (PBSP) entre 2012 e 2015 foram examinados quanto à presença de carrapatos. No total, 140 mamíferos foram examinados, e 34 espécimes foram parasitados por carrapatos. Didelphis aurita, Akodon montensis e Oligoryzomys nigripes foram as espécies mais parasitadas. A partir desses espécimes, 146 carrapatos foram coletados, incluindo 10 larvas. Os carrapatos pertenciam a oito espécies: uma no gênero Ixodes e sete no gênero Amblyomma. Este estudo relata novas associações de carrapatos e mamíferos silvestres no Brasil.

Palavras-chave:
PARNASO; Amblyomma; Ixodes; mamíferos; parasitismo

Introduction

Ticks have wide distribution throughout the world, parasitizing a variety of wild and domestic animals and humans ( LABRUNA et al., 2005 Labruna MB, Jorge RS, Sana DA, Jácomo AT, Kashivakura CK, Furtado MM, et al. Ticks (Acari: Ixodida) on wild carnivores in Brazil. Exp Appl Acarol 2005; 36(1-2): 149-163. http://dx.doi.org/10.1007/s10493-005-2563-1. PMid:16082932.
http://dx.doi.org/10.1007/s10493-005-25...
; BARROS-BATTESTI et al., 2006 Barros-Battesti DM, Arzua M, Bechara GH. Carrapatos de importância Médico-Veterinário da região neotropical: um guia ilustrado para identificação de espécies . São Paulo: Vox/ ICTTD-3/Butantan; 2006. ; GUGLIELMONE et al., 2014 Guglielmone AA, Robbins RG, Apanaskevich DA, Petney TN, Estrada-Peña A, Horak IG. The hard ticks of the world: (Acari: Ixodida: Ixodidae). London: Springer; 2014. 738 p. http://dx.doi.org/10.1007/978-94-007-7497-1.
http://dx.doi.org/10.1007/978-94-007-74...
). These ixodids have direct and indirect impacts on human and animal health by feeding and acting as vectors for pathogenic microorganisms ( PAROLA, 2004 Parola P. Tick-borne rickettsial diseases: emerging risks in Europe. Comp Immunol Microbiol Infect Dis 2004; 27(5): 297-304. http://dx.doi.org/10.1016/j.cimid.2004.03.006. PMid:15225980.
http://dx.doi.org/10.1016/j.cimid.2004....
; BORCHERS et al., 2015 Borchers AT, Keen CL, Huntley AC, Gershwin ME. Lyme disease: a rigorous review of diagnostic criteria and treatment. J Autoimmun 2015; 57: 82-115. http://dx.doi.org/10.1016/j.jaut.2014.09.004. PMid:25451629.
http://dx.doi.org/10.1016/j.jaut.2014.0...
). The numbers of studies on the ecology and geographical distribution of ticks that parasitize wild mammals and on transmission of pathogens have been increasing worldwide over the last few years, along with studies on the major zoonotic pathogens they transmit to humans ( DE LA FUENTE et al., 2004 De la Fuente J, Naranjo V, Ruiz-Fons F, Vicente J, Estrada-Peña AN, Almazán C, et al. Prevalence of tick-borne pathogens in ixodid ticks (Acari: Ixodidae) collected from European wild boar (Sus scrofa) and Iberian red deer (Cervus elaphus hispanicus) in central Spain. Eur J Wildl Res 2004; 50(4): 187-196. http://dx.doi.org/10.1007/s10344-004-0060-1.
http://dx.doi.org/10.1007/s10344-004-00...
; PADURARU et al., 2012 Paduraru OA, Buffet JP, Cote M, Bonnet S, Moutailler S, Paduraru V, et al. Zoonotic transmission of pathogens by Ixodes ricinus ticks, Romania. Emerg Infect Dis 2012; 18(12): 2089-2090. http://dx.doi.org/10.3201/eid1812.120711. PMid:23171510.
http://dx.doi.org/10.3201/eid1812.12071...
).

Although there are numerous studies on ticks that are associated with wild mammals in Brazil (e.g. LABRUNA et al., 2005 Labruna MB, Jorge RS, Sana DA, Jácomo AT, Kashivakura CK, Furtado MM, et al. Ticks (Acari: Ixodida) on wild carnivores in Brazil. Exp Appl Acarol 2005; 36(1-2): 149-163. http://dx.doi.org/10.1007/s10493-005-2563-1. PMid:16082932.
http://dx.doi.org/10.1007/s10493-005-25...
; SARAIVA et al., 2012 Saraiva DG, Fournier GFSR, Martins TF, Leal KPG, Vieira FN, Câmara EMVC, et al. Ticks (Acari: Ixodidae) associated with small terrestrial mammals in the state of Minas Gerais, southeastern Brazil. Exp Appl Acarol 2012; 58(2): 159-166. http://dx.doi.org/10.1007/s10493-012-9570-9. PMid:22585005.
http://dx.doi.org/10.1007/s10493-012-95...
; MARTINS et al., 2016 Martins TF, Peres MG, Costa FB, Bacchiega TS, Appolinario CMJ, Antunes J, et al. Ticks infesting wild small rodents in three areas of the state of São Paulo, Brazil. Cienc Rural 2016; 46(5): 871-875. http://dx.doi.org/10.1590/0103-8478cr20150671.
http://dx.doi.org/10.1590/0103-8478cr20...
), there are still gaps that need to be filled. In the state of Rio de Janeiro, there are few studies on this topic, and the records have mainly been on domestic animals ( GAZÊTA et al., 2001 Gazêta GS, Guerim L, Amorim M, Serra-Freire NM. Seasonal analysis of the number of aeropiles in Anocentor nitens (Neumann, 1897) (Acari: Ixodidae) from the State of Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz 2001; 96(5): 733-736. http://dx.doi.org/10.1590/S0074-02762001000500028. PMid:11500781.
http://dx.doi.org/10.1590/S0074-0276200...
; LUZ et al., 2014 Luz HR, Mathias C, Faccini JLH. Carrapatos parasitando cães em uma área insular do estado do Rio de Janeiro, RJ, Brasil. Rev Bras Med Vet 2014; 36(4): 437-442. ). In this context, the aim of the present study was to report on tick species parasitizing mammals in two areas of the Atlantic Forest in the state of Rio de Janeiro, thus contributing to improve our knowledge of the host- tick relationships.

Materials and Methods

This study was carried out in preserved areas of the Serra dos Órgãos National Park (PARNASO) (22°30’S 43°07’W, 22°29°S 43°07’W and 22°27’S 43°05’W), altitude 700-1200 meters, and in a sylvatic-urban interface area on the Atlantic Forest Campus of the Oswaldo Cruz Foundation (Campus Fiocruz da Mata Atlântica) (22°56’S 43°24’W and 22°55’S 43°26’W), altitude 30-100 meters, which is a buffer zone of the Pedra Branca State Park (PBSP). In PARNASO hosts were captured in November 2014 and in July 2015 whereas in PBSP they were captured between July 2012 and April 2015 with Sherman® and Tomahawk® traps for small mammals which were sat along transects, at ground level. In addition, ticks of medium-sized and large mammals were also collected from road-killed animals, on the highway that crosses the PARNASO. Trapping effort was of 1200 per period in PBSP totalizing 9600 trap-nights. In PARNASO it was 1800 trap-nights per period totalizing 3600 trap-nights. In PARANSO, 80 pitfall traps were also used per night, totalizing 1600 pitfall-nights.

The animals caught in the traps were anesthetized and euthanized for parasite recovery and for other studies. Mammal species were identified morphologically ( REIS et al., 2006 Reis NR, Peracchi AL, Pedro WA, Lima IP. Mamíferos do Brasil. Londrina: Universidade Estadual de Londrina; 2006. ; BONVICINO et al., 2008 Bonvicino CR, Oliveira JA, D’Andrea PS. Guia dos Roedores do Brasil com chaves para gêneros baseadas em caracteres externos. Rio de Janeiro: Centro Pan-Americano de Febre Aftosa; 2008. ), except for rodent hosts, which were identified by external and cranial morphology, and by cytogenetic analysis (2N and FN) for Oligoryzomys nigripes (Olfers, 1818) and Akodon montensis (Thomas, 1913). Voucher specimens were deposited in the scientific collection of the National Museum of the Federal University of Rio de Janeiro (UFRJ) under access numbers: 83165; 83167; 83170; 83174; 83175 83768-83769; 83998; 83999; 84000-84014. All procedures followed the guidelines for animal capture, handling and care of the Ethics Committee for Animal Use of the Oswaldo Cruz Foundation (license numbers L-39/14 and LW81/12). These animals were captured under authorization from the Chico Mendes Institute for Biodiversity and Conservation (Instituto Chico Mendes de Conservação da Biodiversidade, ICMBio; license numbers 13373 and 45839-2) and by the Environmental Institute of the State of Rio de Janeiro (Instituto Estadual do Ambiente, INEA; license number 020/2011). Biosafety practices and protective equipment were used during all procedures involving animal handling and biological sampling.

The ticks were identified in the Acarology Laboratory of the Federal Rural University of Rio de Janeiro (UFRRJ). Larvae and engorged nymphs, when alive, were kept under 27o C and 80% humidity in BOD’s in order to obtain the respective molts to nymphs and adults. Identification of ticks was based on the following dichotomous keys: Martins et al. (2010) Martins TF, Onofrio VC, Barros-Battesti DM, Labruna MB. Nymphs of the genus Amblyomma (Acari: Ixodidae) of Brazil: descriptions, redescriptions, and identification key. T T Born Dis 2010; 1(2): 75-99. http://dx.doi.org/10.1016/j.ttbdis.2010.03.002. PMid:21771514.
http://dx.doi.org/10.1016/j.ttbdis.2010...
for nymphs; Barros-Battesti et al. (2006) Barros-Battesti DM, Arzua M, Bechara GH. Carrapatos de importância Médico-Veterinário da região neotropical: um guia ilustrado para identificação de espécies . São Paulo: Vox/ ICTTD-3/Butantan; 2006. for adults of Amblyomma; and Onofrio et al. (2009) Onofrio VC, Barros-Battesti DM, Labruna MB, Faccini JL. Diagnoses of and illustrated key to the species of Ixodes Latreille, 1795 (Acari: Ixodidae) from Brazil. Syst Parasitol 2009; 72(2): 143-157. http://dx.doi.org/10.1007/s11230-008-9169-z. PMid:19115087.
http://dx.doi.org/10.1007/s11230-008-91...
for adults of Ixodes. Tick prevalence and intensity of infestation were calculated as described by Bush et al. (1997) Bush AO, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 1997; 83(4): 575-583. http://dx.doi.org/10.2307/3284227. PMid:9267395.
http://dx.doi.org/10.2307/3284227 ...
. Voucher specimens were deposited in the tick collection “Coleção Nacional de Carrapatos Danilo Gonçalves Saraiva” (CNC) of the FMVZ-USP under the numbers 3655-3658. Nymphs of A. aureolatum and A. ovale were photographed for morphological comparisons ( Figure 1 ), these were photographed under a stereomicroscope (Zeiss Stemi SV 11, Zeiss, Münich, Germany).

Figure 1
Amblyomma aureolatum (A, C and E) and Amblyomma ovale (B, D and F) infesting wild mammals in the Serra dos Órgãos National Park (PARNASO), Rio de Janeiro. A and B = arrows indicating eye location; C and D = arrows indicating presence of auriculae in the basis capitulum in A. ovale letter D; E and F = arrows indicating spurs of the coxa I.

Results

Overall, 140 mammals were examined. Five orders of mammals were found parasitized: Didelphimorphia (17 specimens), Rodentia (11 specimens), Pilosa (three specimens), Carnivora (two specimens) and Cingulata (one specimen) ( Table 1 ). Three rodent species, three marsupials, two carnivores, one sloth, one anteater and one armadillo species were found parasitized by ticks in PARNASO ( Table 1 ), while in PBSP only the common black-eared opossum (Didelphis aurita Wied-Neuwied, 1826) was found parasitized by ticks. The seven-banded armadillo (Dasypus septemcinctus Linnaeus, 1758) was the species most infested, with 43 ticks on one specimen, followed by D. aurita, the montane grass mouse A. montensis and the black-footed colilargo (O. nigripes) ( Table 1 ).

Table 1
Species of ticks infesting wild mammals in the Serra dos Órgãos National Park (PARNASO) and Pedra Branca State Park (PBSP): N = nymph, F = female and M = male. EX = number of examined hosts, PA = number of parasitized hosts and P= prevalence (%). Larvae (=10) were identified as Amblyomma sp.

A total of 146 ticks were collected, including 10 larvae. In PARNASO, eight species of ticks were observed, while only one was observed in PBSP ( Table 1 ). Ixodes loricatus Neumann, 1899, parasitized several hosts and was found in both areas. The other tick species found belonged to the genus Amblyomma: Amblyomma auricularium (Conil, 1878), Amblyomma ovale (Koch, 1844), Amblyomma longirostre (Koch, 1844), Amblyomma sculptum (Nava et al., 2014), Amblyomma aureolatum (Pallas, 1772), Amblyomma varium Koch, 1844, and Amblyomma nodosum Neumann, 1899. Larvae of Amblyomma with non-identified morphotypes were collected on the rodents A. montensis (two larvae), Delomys dorsalis Hensel, 1873 (one larva), O. nigripes (five larvae) and Oligoryzomys flavescens (Waterhose, 1837) (two larvae).

Overall, 34/140 (24.3%) mammals were found to be parasitized by adult, nymph and larva of ticks and the average intensity of parasitism was 4.3 ticks per host. All tick species had prevalence greater than 10%, except for A. aureolatum on D. aurita in PARNASO which was recorded in only one out of 13 examined hosts ( Table 1 ).

Discussion

All tick-host associations recorded here had previously been reported elsewhere in Brazil ( BARROS-BATTESTI et al., 2006 Barros-Battesti DM, Arzua M, Bechara GH. Carrapatos de importância Médico-Veterinário da região neotropical: um guia ilustrado para identificação de espécies . São Paulo: Vox/ ICTTD-3/Butantan; 2006. ; SARAIVA et al., 2012 Saraiva DG, Fournier GFSR, Martins TF, Leal KPG, Vieira FN, Câmara EMVC, et al. Ticks (Acari: Ixodidae) associated with small terrestrial mammals in the state of Minas Gerais, southeastern Brazil. Exp Appl Acarol 2012; 58(2): 159-166. http://dx.doi.org/10.1007/s10493-012-9570-9. PMid:22585005.
http://dx.doi.org/10.1007/s10493-012-95...
; SZABÓ et al., 2013 Szabó MP, Nieri-Bastos FA, Spolidorio MG, Martins TF, Barbieri AM, Labruna MB. In vitro isolation from Amblyomma ovale (Acari: Ixodidae) and ecological aspects of the Atlantic rainforest Rickettsia, the causative agent of a novel spotted fever rickettsiosis in Brazil. Parasitology 2013; 140(6): 719-728. http://dx.doi.org/10.1017/S0031182012002065. PMid:23363571.
http://dx.doi.org/10.1017/S003118201200...
; GUGLIELMONE et al., 2014 Guglielmone AA, Robbins RG, Apanaskevich DA, Petney TN, Estrada-Peña A, Horak IG. The hard ticks of the world: (Acari: Ixodida: Ixodidae). London: Springer; 2014. 738 p. http://dx.doi.org/10.1007/978-94-007-7497-1.
http://dx.doi.org/10.1007/978-94-007-74...
; OLIVEIRA et al., 2014 Oliveira HH, Quinelato IPF, Gomes V, Amorim M, Gazêta GS, Serra-Freire NM, et al. Ixodofauna em roedores e marsupiais capturados no Parque Estadual da Pedra Branca, Rio de Janeiro, Brasil. Rev Bras Med Vet 2014; 36(2): 137-143. ; KRAWCZAK et al., 2016b Krawczak FS, Binder LC, Oliveira CS, Costa FB, Moraes-Filho J, Martins TF, et al. Ecology of a tick-borne spotted fever in southern Brazil. Exp Appl Acarol 2016b; 70(2): 219-229. http://dx.doi.org/10.1007/s10493-016-0070-1. PMid:27392739.
http://dx.doi.org/10.1007/s10493-016-00...
; MARTINS et al., 2016 Martins TF, Peres MG, Costa FB, Bacchiega TS, Appolinario CMJ, Antunes J, et al. Ticks infesting wild small rodents in three areas of the state of São Paulo, Brazil. Cienc Rural 2016; 46(5): 871-875. http://dx.doi.org/10.1590/0103-8478cr20150671.
http://dx.doi.org/10.1590/0103-8478cr20...
; 2017 Martins TF, Milanelo L, Krawczak FS, Furuya HR, Fitorra LS, Dores FT, et al. Diversity of ticks in the wildlife screening center of São Paulo city, Brazil. Cienc Rural 2017; 47(5): 1-6. http://dx.doi.org/10.1590/0103-8478cr20161052.
http://dx.doi.org/10.1590/0103-8478cr20...
), except for records of A. longirostre on Trinomys dimidiatus and B. torquatus. This tick species has wide distribution throughout the Neotropical region, and its adults have commonly been reported parasitizing rodent species, especially of the genus Coendou ( BARROS-BATTESTI et al., 2006 Barros-Battesti DM, Arzua M, Bechara GH. Carrapatos de importância Médico-Veterinário da região neotropical: um guia ilustrado para identificação de espécies . São Paulo: Vox/ ICTTD-3/Butantan; 2006. ; NAVA et al., 2010 Nava S, Velazco PM, Guglielmone AA. First record of Amblyomma longirostre (Koch, 1844) (Acari: Ixodidae) from Peru, with a review of this tick’s host relationships. Syst Appl Acarol 2010; 15(1): 21-30. http://dx.doi.org/10.11158/saa.15.1.2.
http://dx.doi.org/10.11158/saa.15.1.2 ...
; 2017 Nava S, Venzal JM, Acuña DG, Martins TF, Guglielmone AA. Ticks of the Southern Cone of America: diagnosis, distribution and hosts with taxonomy, ecology and sanitary importance . USA: Elsevier; 2017. ). Immature stages prefer wild birds, especially Passeriformes ( OGRZEWALSKA et al., 2009 Ogrzewalska M, Pacheco RC, Uezu A, Richtzenhain LJ, Ferreira F, Labruna MB. Ticks (Acari: Ixodidae) infesting birds in an Atlantic rain forest region of Brazil. J Med Entomol 2009; 46(5): 1225-1229. http://dx.doi.org/10.1603/033.046.0534. PMid:19769058.
http://dx.doi.org/10.1603/033.046.0534 ...
; LUZ & FACCINI, 2013 Luz HR, Faccini JLH. Ticks on Brazilian birds: overview. In: Ruiz L, Iglesias F. Birds: evolution and behavior, breeding strategies, migration and spread of disease . New York: Nova Science Publishers, Inc.; 2013. p. 98-124. ; LUZ et al., 2017 Luz HR, Faccini JLH, McIntosh D. Molecular analyses reveal an abundant diversity of ticks and rickettsial agents associated with wild birds in two regions of primary Brazilian Atlantic Rainforest. Ticks Tick Borne Dis 2017; 8(4): 657-665. http://dx.doi.org/10.1016/j.ttbdis.2017.04.012. PMid:28479066.
http://dx.doi.org/10.1016/j.ttbdis.2017...
). Among the sloths, only Bradypus tridactylus had previously been reported parasitized by A. longirostre ( NAVA et al., 2010 Nava S, Velazco PM, Guglielmone AA. First record of Amblyomma longirostre (Koch, 1844) (Acari: Ixodidae) from Peru, with a review of this tick’s host relationships. Syst Appl Acarol 2010; 15(1): 21-30. http://dx.doi.org/10.11158/saa.15.1.2.
http://dx.doi.org/10.11158/saa.15.1.2 ...
). Thus, the present study provides a new record for A. longirostre in B. torquatus, which is regarded as an endangered species ( BRASIL, 2003 Brasil. Ministério do Meio Ambiente. Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis – IBAMA. Instrução Normativa nº 003, de 27 de maio de 2003. Lista das Espécies da Fauna Brasileira Ameaçadas de Extinção [online]. Diário Oficial da República Federativa do Brasil, Brasília, 2003 [cited 2017 June 19]. Available from: http://www.mma.gov.br/estruturas/179/_arquivos/179_05122008034002.pdf
http://www.mma.gov.br/estruturas/179/_a...
; IUCN, 2004 União Internacional para a Conservação da Natureza – IUCN. Red List of Threatened Species [online]. 2004 [cited 2017 June 19]. Available from: http://www.iucnredlist.org/
http://www.iucnredlist.org/ ...
). The arboreal habits of this mammal probably enable parasitism by this tick species as has already been hypothesized by Labruna et al. (2007) Labruna MB, Sanfilippo LF, Demetrio C, Menezes AC, Pinter A, Guglielmone AA, et al. Ticks collected on birds in the state of São Paulo, Brazil. Exp Appl Acarol 2007; 43(2): 147-160. http://dx.doi.org/10.1007/s10493-007-9106-x. PMid:17882514.
http://dx.doi.org/10.1007/s10493-007-91...
for the association of A. longirostre and porcupine rodents.

The species A. ovale, which was recorded on two rodent species ( O. nigripes and A. montensis) had previously been reported in association with a variety of species of small mammals in South America ( SARAIVA et al., 2012 Saraiva DG, Fournier GFSR, Martins TF, Leal KPG, Vieira FN, Câmara EMVC, et al. Ticks (Acari: Ixodidae) associated with small terrestrial mammals in the state of Minas Gerais, southeastern Brazil. Exp Appl Acarol 2012; 58(2): 159-166. http://dx.doi.org/10.1007/s10493-012-9570-9. PMid:22585005.
http://dx.doi.org/10.1007/s10493-012-95...
; KRAWCZAK et al., 2016b Krawczak FS, Binder LC, Oliveira CS, Costa FB, Moraes-Filho J, Martins TF, et al. Ecology of a tick-borne spotted fever in southern Brazil. Exp Appl Acarol 2016b; 70(2): 219-229. http://dx.doi.org/10.1007/s10493-016-0070-1. PMid:27392739.
http://dx.doi.org/10.1007/s10493-016-00...
; MARTINS et al., 2016 Martins TF, Peres MG, Costa FB, Bacchiega TS, Appolinario CMJ, Antunes J, et al. Ticks infesting wild small rodents in three areas of the state of São Paulo, Brazil. Cienc Rural 2016; 46(5): 871-875. http://dx.doi.org/10.1590/0103-8478cr20150671.
http://dx.doi.org/10.1590/0103-8478cr20...
; NAVA et al., 2017 Nava S, Venzal JM, Acuña DG, Martins TF, Guglielmone AA. Ticks of the Southern Cone of America: diagnosis, distribution and hosts with taxonomy, ecology and sanitary importance . USA: Elsevier; 2017. ). Immature stages of A. ovale are commonly found in association with rodents of the families Cricetidae and Echimyidae ( SARAIVA et al., 2012 Saraiva DG, Fournier GFSR, Martins TF, Leal KPG, Vieira FN, Câmara EMVC, et al. Ticks (Acari: Ixodidae) associated with small terrestrial mammals in the state of Minas Gerais, southeastern Brazil. Exp Appl Acarol 2012; 58(2): 159-166. http://dx.doi.org/10.1007/s10493-012-9570-9. PMid:22585005.
http://dx.doi.org/10.1007/s10493-012-95...
; SZABÓ et al., 2013 Szabó MP, Nieri-Bastos FA, Spolidorio MG, Martins TF, Barbieri AM, Labruna MB. In vitro isolation from Amblyomma ovale (Acari: Ixodidae) and ecological aspects of the Atlantic rainforest Rickettsia, the causative agent of a novel spotted fever rickettsiosis in Brazil. Parasitology 2013; 140(6): 719-728. http://dx.doi.org/10.1017/S0031182012002065. PMid:23363571.
http://dx.doi.org/10.1017/S003118201200...
; SPONCHIADO et al., 2015 Sponchiado J, Melo GL, Martins TF, Krawczak FS, Labruna MB, Cáceres NC. Association patterns of ticks (Acari: Ixodida: Ixodidae, Argasidae) of small mammals in Cerrado fragments, western Brazil. Exp Appl Acarol 2015; 65(3): 389-401. http://dx.doi.org/10.1007/s10493-014-9877-9. PMid:25633262.
http://dx.doi.org/10.1007/s10493-014-98...
; MARTINS et al., 2016 Martins TF, Peres MG, Costa FB, Bacchiega TS, Appolinario CMJ, Antunes J, et al. Ticks infesting wild small rodents in three areas of the state of São Paulo, Brazil. Cienc Rural 2016; 46(5): 871-875. http://dx.doi.org/10.1590/0103-8478cr20150671.
http://dx.doi.org/10.1590/0103-8478cr20...
; NAVA et al., 2017 Nava S, Venzal JM, Acuña DG, Martins TF, Guglielmone AA. Ticks of the Southern Cone of America: diagnosis, distribution and hosts with taxonomy, ecology and sanitary importance . USA: Elsevier; 2017. ). Adults of this tick species mostly infest wild and domestic carnivores ( GUGLIELMONE et al., 2003b Guglielmone AA, Estrada-Peña A, Mangold AJ, Barros-Battesti DM, Labruna MB, Martins JR, et al. Amblyomma aureolatum (Pallas, 1772) and Amblyomma ovale Koch, 1844 (Acari: Ixodidae): hosts, distribution and 16S rDNA sequences. Vet Parasitol 2003b; 113(3-4): 273-288. http://dx.doi.org/10.1016/S0304-4017(03)00083-9. PMid:12719142.
http://dx.doi.org/10.1016/S0304-4017(03...
, 2014 Guglielmone AA, Robbins RG, Apanaskevich DA, Petney TN, Estrada-Peña A, Horak IG. The hard ticks of the world: (Acari: Ixodida: Ixodidae). London: Springer; 2014. 738 p. http://dx.doi.org/10.1007/978-94-007-7497-1.
http://dx.doi.org/10.1007/978-94-007-74...
; LABRUNA et al., 2005 Labruna MB, Jorge RS, Sana DA, Jácomo AT, Kashivakura CK, Furtado MM, et al. Ticks (Acari: Ixodida) on wild carnivores in Brazil. Exp Appl Acarol 2005; 36(1-2): 149-163. http://dx.doi.org/10.1007/s10493-005-2563-1. PMid:16082932.
http://dx.doi.org/10.1007/s10493-005-25...
). They can also parasitize animals of the orders Artiodactyla, Didelphimorphia, Perissodactyla and Primates ( GUGLIELMONE et al., 2014 Guglielmone AA, Robbins RG, Apanaskevich DA, Petney TN, Estrada-Peña A, Horak IG. The hard ticks of the world: (Acari: Ixodida: Ixodidae). London: Springer; 2014. 738 p. http://dx.doi.org/10.1007/978-94-007-7497-1.
http://dx.doi.org/10.1007/978-94-007-74...
). Sporadically, A. ovale larvae have been found parasitizing wild birds ( LUZ & FACCINI, 2013 Luz HR, Faccini JLH. Ticks on Brazilian birds: overview. In: Ruiz L, Iglesias F. Birds: evolution and behavior, breeding strategies, migration and spread of disease . New York: Nova Science Publishers, Inc.; 2013. p. 98-124. ; LUZ et al., 2017 Luz HR, Faccini JLH, McIntosh D. Molecular analyses reveal an abundant diversity of ticks and rickettsial agents associated with wild birds in two regions of primary Brazilian Atlantic Rainforest. Ticks Tick Borne Dis 2017; 8(4): 657-665. http://dx.doi.org/10.1016/j.ttbdis.2017.04.012. PMid:28479066.
http://dx.doi.org/10.1016/j.ttbdis.2017...
). This is the second record of this tick species parasitizing O. nigripes , the first one has been recorded in São Paulo state ( MARTINS et al. 2016 Martins TF, Peres MG, Costa FB, Bacchiega TS, Appolinario CMJ, Antunes J, et al. Ticks infesting wild small rodents in three areas of the state of São Paulo, Brazil. Cienc Rural 2016; 46(5): 871-875. http://dx.doi.org/10.1590/0103-8478cr20150671.
http://dx.doi.org/10.1590/0103-8478cr20...
). A. ovale is a possible vector for a new human rickettsiosis in Brazil, named Atlantic Rainforest Rickettsiosis ( SZABÓ et al., 2013 Szabó MP, Nieri-Bastos FA, Spolidorio MG, Martins TF, Barbieri AM, Labruna MB. In vitro isolation from Amblyomma ovale (Acari: Ixodidae) and ecological aspects of the Atlantic rainforest Rickettsia, the causative agent of a novel spotted fever rickettsiosis in Brazil. Parasitology 2013; 140(6): 719-728. http://dx.doi.org/10.1017/S0031182012002065. PMid:23363571.
http://dx.doi.org/10.1017/S003118201200...
; BARBIERI et al., 2014 Barbieri AR, Filho JM, Nieri-Bastos FA, Souza JC Jr, Szabó MP, Labruna MB. Epidemiology of Rickettsia sp. strain Atlantic rainforest in a spotted fever-endemic area of southern Brazil. Ticks Tick Borne Dis 2014; 5(6): 848-853. http://dx.doi.org/10.1016/j.ttbdis.2014.07.010. PMid:25108786.
http://dx.doi.org/10.1016/j.ttbdis.2014...
; KRAWCZAK et al., 2016a Krawczak FS, Agostinho WC, Polo G, Moraes-Filho J, Labruna MB. Comparative evaluation of Amblyomma ovale ticks infected and noninfected by Rickettsia sp. strain Atlantic rainforest, the agent of an emerging rickettsiosis in Brazil. Ticks Tick Borne Dis 2016a; 7(3): 502-507. http://dx.doi.org/10.1016/j.ttbdis.2016.02.007. PMid:26895674.
http://dx.doi.org/10.1016/j.ttbdis.2016...
). In the present study, all nymphs of A. ovale were recorded at altitudes 720 and 740m, reinforcing the findings of Barbieri et al. (2015) Barbieri JM, Rocha CMBM, Bruhn FRP, Cardoso DL, Pinter A, Labruna MB. Altitudinal assessment of Amblyomma aureolatum and Amblyomma ovale (Acari: Ixodidae), vectors of spotted fever group rickettsiosis in the state of São Paulo, Brazil. J Med Entomol 2015; 52(5): 1170-1174. http://dx.doi.org/10.1093/jme/tjv073. PMid:26336213.
http://dx.doi.org/10.1093/jme/tjv073 ...
, where this species was reported at altitudes ranging from <100 to 700 meters, with sporadic records above 700 meters (range 2 - 1,040 meters). Possibly this is a region (≅ 700 meters) altitude limit for the establishment of populations of A. ovale in the latitudes between 21° and 23°.

The tick A. auricularium, which was recorded exclusively on D. septemcinctus, has wide distribution in the Americas, and has been recorded on several vertebrates in the Neotropical region, preferentially on species of the family Dasypodidae ( GUGLIELMONE et al., 2003a Guglielmone AA, Estrada-Peña A, Luciani CA, Mangold AJ, Keirans JE. Hosts and distribution of Amblyomma auricularium (Conil 1878) and Amblyomma pseudoconcolor Aragão, 1908 (Acari: Ixodidae). Exp Appl Acarol 2003a; 29(1-2): 131-139. http://dx.doi.org/10.1023/A:1024251020035. PMid:14580065.
http://dx.doi.org/10.1023/A:10242510200...
; BARROS-BATTESTI et al., 2006 Barros-Battesti DM, Arzua M, Bechara GH. Carrapatos de importância Médico-Veterinário da região neotropical: um guia ilustrado para identificação de espécies . São Paulo: Vox/ ICTTD-3/Butantan; 2006. ; NAVA et al., 2017 Nava S, Venzal JM, Acuña DG, Martins TF, Guglielmone AA. Ticks of the Southern Cone of America: diagnosis, distribution and hosts with taxonomy, ecology and sanitary importance . USA: Elsevier; 2017. ). Within this family, high parasitism on Dasypus spp. can be seen, especially on D. novemcinctus ( GUGLIELMONE et al., 2003a Guglielmone AA, Estrada-Peña A, Luciani CA, Mangold AJ, Keirans JE. Hosts and distribution of Amblyomma auricularium (Conil 1878) and Amblyomma pseudoconcolor Aragão, 1908 (Acari: Ixodidae). Exp Appl Acarol 2003a; 29(1-2): 131-139. http://dx.doi.org/10.1023/A:1024251020035. PMid:14580065.
http://dx.doi.org/10.1023/A:10242510200...
; NAVA et al., 2017 Nava S, Venzal JM, Acuña DG, Martins TF, Guglielmone AA. Ticks of the Southern Cone of America: diagnosis, distribution and hosts with taxonomy, ecology and sanitary importance . USA: Elsevier; 2017. ).

The species A. sculptum and A. aureolatum were only recorded parasitizing didelphids. Both of these species were previously reported in association with these hosts in Brazil ( SPONCHIADO et al., 2015 Sponchiado J, Melo GL, Martins TF, Krawczak FS, Labruna MB, Cáceres NC. Association patterns of ticks (Acari: Ixodida: Ixodidae, Argasidae) of small mammals in Cerrado fragments, western Brazil. Exp Appl Acarol 2015; 65(3): 389-401. http://dx.doi.org/10.1007/s10493-014-9877-9. PMid:25633262.
http://dx.doi.org/10.1007/s10493-014-98...
; NAVA et al., 2017 Nava S, Venzal JM, Acuña DG, Martins TF, Guglielmone AA. Ticks of the Southern Cone of America: diagnosis, distribution and hosts with taxonomy, ecology and sanitary importance . USA: Elsevier; 2017. ). A. sculptum and A. aureolatum have been proved to transmit Rickettsia rickettsii to humans in Brazil ( PINTER & LABRUNA, 2006 Pinter A, Labruna MB. Isolation of Rickettsia rickettsii and Rickettsia bellii in cell culture from the tick Amblyomma aureolatum in Brazil. Ann N Y Acad Sci 2006; 1078(1): 523-529. http://dx.doi.org/10.1196/annals.1374.103. PMid:17114770.
http://dx.doi.org/10.1196/annals.1374.1...
; LABRUNA et al., 2011 Labruna MB, Mattar VS, Nava S, Bermudez S, Venzal JM, Dolz G, et al. Rickettsioses in Latin America, Caribbean, Spain, and Portugal. Rev Mvz Cordoba 2011; 16(2): 2435-2457. http://dx.doi.org/10.21897/rmvz.282.
http://dx.doi.org/10.21897/rmvz.282 ...
). In this way, didelphids may have an important role in relation to Brazilian spotted fever, through maintaining and dispersing these ixodids in different regions ( HORTA et al., 2009 Horta MC, Moraes-Filho J, Casagrande RA, Saito TB, Rosa SC, Ogrzewalska M, et al. Experimental Infection of Opossums Didelphis aurita by Rickettsia rickettsii and Evaluation of the Transmission of the Infection to Ticks Amblyomma cajennense. Vector Borne Zoonotic Dis 2009; 9(1): 109-118. http://dx.doi.org/10.1089/vbz.2008.0114. PMid:18945194.
http://dx.doi.org/10.1089/vbz.2008.0114...
). Specimens of A. aureolatum were recorded at altitudes 780, 820 and 1200m, agreeing with reports by Barbieri et al. (2015) Barbieri JM, Rocha CMBM, Bruhn FRP, Cardoso DL, Pinter A, Labruna MB. Altitudinal assessment of Amblyomma aureolatum and Amblyomma ovale (Acari: Ixodidae), vectors of spotted fever group rickettsiosis in the state of São Paulo, Brazil. J Med Entomol 2015; 52(5): 1170-1174. http://dx.doi.org/10.1093/jme/tjv073. PMid:26336213.
http://dx.doi.org/10.1093/jme/tjv073 ...
at high altitudes (> 700 meters) in the southeast region.

Our records of I. loricatus on D. aurita and on P. frenatus confirm the reports that adults of I. loricatus mostly parasitize didelphids in the Neotropical region ( BARROS-BATTESTI et al., 2000 Barros-Battesti DM, Yoshinari NH, Bonoldi VLN, Gomes AC. Parasitism by Ixodes didelphidis and I. loricatus (Acari: Ixodidae) on small wild mammals from an Atlantic Forest in the State of Sao Paulo, Brazil. J Med Entomol 2000; 37(6): 820-827. http://dx.doi.org/10.1603/0022-2585-37.6.820. PMid:11185614.
http://dx.doi.org/10.1603/0022-2585-37....
, 2006 Barros-Battesti DM, Arzua M, Bechara GH. Carrapatos de importância Médico-Veterinário da região neotropical: um guia ilustrado para identificação de espécies . São Paulo: Vox/ ICTTD-3/Butantan; 2006. ; DANTAS-TORRES et al., 2012 Dantas-Torres F, Aléssio FM, Siqueira DB, Mauffrey JF, Marvulo MFV, Martins TF, et al. Exposure of small mammals to ticks and rickettsiae in Atlantic Forest patches in the metropolitan area of Recife, North-eastern Brazil. Parasitology 2012; 139(1): 83-91. http://dx.doi.org/10.1017/S0031182011001740. PMid:22217620.
http://dx.doi.org/10.1017/S003118201100...
; OLIVEIRA et al., 2014 Oliveira HH, Quinelato IPF, Gomes V, Amorim M, Gazêta GS, Serra-Freire NM, et al. Ixodofauna em roedores e marsupiais capturados no Parque Estadual da Pedra Branca, Rio de Janeiro, Brasil. Rev Bras Med Vet 2014; 36(2): 137-143. ). In the state of Rio de Janeiro, this species had previously been reported in association with Didelphis aurita in PBSP ( BITTENCOURT & ROCHA, 2003 Bittencourt EB, Rocha CFD. Host-ectoparasite specificity in a small mammal community in an area of Atlantic Rain Forest (Ilha Grande, State of Rio de Janeiro), Southeastern Brazil. Mem Inst Oswaldo Cruz 2003; 98(6): 793-798. http://dx.doi.org/10.1590/S0074-02762003000600015. PMid:14595458.
http://dx.doi.org/10.1590/S0074-0276200...
; OLIVEIRA et al., 2014 Oliveira HH, Quinelato IPF, Gomes V, Amorim M, Gazêta GS, Serra-Freire NM, et al. Ixodofauna em roedores e marsupiais capturados no Parque Estadual da Pedra Branca, Rio de Janeiro, Brasil. Rev Bras Med Vet 2014; 36(2): 137-143. ).

Acknowledgements

We are grateful to the coordination of Campus Fiocruz da Mata Altântica at Fundação Oswaldo Cruz for providing local facilities and support, to the staff of Serra dos Órgãos National Park and Pedra Branca State Park for the licenses and local facilities and to the staff of Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios at Fundação Oswaldo Cruz for helping in the field work. We also thank Instituto Oswaldo Cruz/Fiocruz, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq-PPBio), Coordenadoria de Apoio à Pesquisa e Desenvolvimento (CAPES) and Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro Estado (FAPERJ).

References

  • Barbieri AR, Filho JM, Nieri-Bastos FA, Souza JC Jr, Szabó MP, Labruna MB. Epidemiology of Rickettsia sp. strain Atlantic rainforest in a spotted fever-endemic area of southern Brazil. Ticks Tick Borne Dis 2014; 5(6): 848-853. http://dx.doi.org/10.1016/j.ttbdis.2014.07.010. PMid:25108786.
    » http://dx.doi.org/10.1016/j.ttbdis.2014.07.010
  • Barbieri JM, Rocha CMBM, Bruhn FRP, Cardoso DL, Pinter A, Labruna MB. Altitudinal assessment of Amblyomma aureolatum and Amblyomma ovale (Acari: Ixodidae), vectors of spotted fever group rickettsiosis in the state of São Paulo, Brazil. J Med Entomol 2015; 52(5): 1170-1174. http://dx.doi.org/10.1093/jme/tjv073. PMid:26336213.
    » http://dx.doi.org/10.1093/jme/tjv073
  • Barros-Battesti DM, Arzua M, Bechara GH. Carrapatos de importância Médico-Veterinário da região neotropical: um guia ilustrado para identificação de espécies . São Paulo: Vox/ ICTTD-3/Butantan; 2006.
  • Barros-Battesti DM, Yoshinari NH, Bonoldi VLN, Gomes AC. Parasitism by Ixodes didelphidis and I. loricatus (Acari: Ixodidae) on small wild mammals from an Atlantic Forest in the State of Sao Paulo, Brazil. J Med Entomol 2000; 37(6): 820-827. http://dx.doi.org/10.1603/0022-2585-37.6.820. PMid:11185614.
    » http://dx.doi.org/10.1603/0022-2585-37.6.820
  • Bittencourt EB, Rocha CFD. Host-ectoparasite specificity in a small mammal community in an area of Atlantic Rain Forest (Ilha Grande, State of Rio de Janeiro), Southeastern Brazil. Mem Inst Oswaldo Cruz 2003; 98(6): 793-798. http://dx.doi.org/10.1590/S0074-02762003000600015. PMid:14595458.
    » http://dx.doi.org/10.1590/S0074-02762003000600015
  • Bonvicino CR, Oliveira JA, D’Andrea PS. Guia dos Roedores do Brasil com chaves para gêneros baseadas em caracteres externos Rio de Janeiro: Centro Pan-Americano de Febre Aftosa; 2008.
  • Borchers AT, Keen CL, Huntley AC, Gershwin ME. Lyme disease: a rigorous review of diagnostic criteria and treatment. J Autoimmun 2015; 57: 82-115. http://dx.doi.org/10.1016/j.jaut.2014.09.004. PMid:25451629.
    » http://dx.doi.org/10.1016/j.jaut.2014.09.004
  • Brasil. Ministério do Meio Ambiente. Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis – IBAMA. Instrução Normativa nº 003, de 27 de maio de 2003. Lista das Espécies da Fauna Brasileira Ameaçadas de Extinção [online]. Diário Oficial da República Federativa do Brasil, Brasília, 2003 [cited 2017 June 19]. Available from: http://www.mma.gov.br/estruturas/179/_arquivos/179_05122008034002.pdf
    » http://www.mma.gov.br/estruturas/179/_arquivos/179_05122008034002.pdf
  • Bush AO, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 1997; 83(4): 575-583. http://dx.doi.org/10.2307/3284227. PMid:9267395.
    » http://dx.doi.org/10.2307/3284227
  • Dantas-Torres F, Aléssio FM, Siqueira DB, Mauffrey JF, Marvulo MFV, Martins TF, et al. Exposure of small mammals to ticks and rickettsiae in Atlantic Forest patches in the metropolitan area of Recife, North-eastern Brazil. Parasitology 2012; 139(1): 83-91. http://dx.doi.org/10.1017/S0031182011001740. PMid:22217620.
    » http://dx.doi.org/10.1017/S0031182011001740
  • De la Fuente J, Naranjo V, Ruiz-Fons F, Vicente J, Estrada-Peña AN, Almazán C, et al. Prevalence of tick-borne pathogens in ixodid ticks (Acari: Ixodidae) collected from European wild boar (Sus scrofa) and Iberian red deer (Cervus elaphus hispanicus) in central Spain. Eur J Wildl Res 2004; 50(4): 187-196. http://dx.doi.org/10.1007/s10344-004-0060-1.
    » http://dx.doi.org/10.1007/s10344-004-0060-1
  • Gazêta GS, Guerim L, Amorim M, Serra-Freire NM. Seasonal analysis of the number of aeropiles in Anocentor nitens (Neumann, 1897) (Acari: Ixodidae) from the State of Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz 2001; 96(5): 733-736. http://dx.doi.org/10.1590/S0074-02762001000500028. PMid:11500781.
    » http://dx.doi.org/10.1590/S0074-02762001000500028
  • Guglielmone AA, Estrada-Peña A, Luciani CA, Mangold AJ, Keirans JE. Hosts and distribution of Amblyomma auricularium (Conil 1878) and Amblyomma pseudoconcolor Aragão, 1908 (Acari: Ixodidae). Exp Appl Acarol 2003a; 29(1-2): 131-139. http://dx.doi.org/10.1023/A:1024251020035. PMid:14580065.
    » http://dx.doi.org/10.1023/A:1024251020035
  • Guglielmone AA, Estrada-Peña A, Mangold AJ, Barros-Battesti DM, Labruna MB, Martins JR, et al. Amblyomma aureolatum (Pallas, 1772) and Amblyomma ovale Koch, 1844 (Acari: Ixodidae): hosts, distribution and 16S rDNA sequences. Vet Parasitol 2003b; 113(3-4): 273-288. http://dx.doi.org/10.1016/S0304-4017(03)00083-9. PMid:12719142.
    » http://dx.doi.org/10.1016/S0304-4017(03)00083-9
  • Guglielmone AA, Robbins RG, Apanaskevich DA, Petney TN, Estrada-Peña A, Horak IG. The hard ticks of the world: (Acari: Ixodida: Ixodidae) London: Springer; 2014. 738 p. http://dx.doi.org/10.1007/978-94-007-7497-1.
    » http://dx.doi.org/10.1007/978-94-007-7497-1
  • Horta MC, Moraes-Filho J, Casagrande RA, Saito TB, Rosa SC, Ogrzewalska M, et al. Experimental Infection of Opossums Didelphis aurita by Rickettsia rickettsii and Evaluation of the Transmission of the Infection to Ticks Amblyomma cajennense. Vector Borne Zoonotic Dis 2009; 9(1): 109-118. http://dx.doi.org/10.1089/vbz.2008.0114. PMid:18945194.
    » http://dx.doi.org/10.1089/vbz.2008.0114
  • Krawczak FS, Agostinho WC, Polo G, Moraes-Filho J, Labruna MB. Comparative evaluation of Amblyomma ovale ticks infected and noninfected by Rickettsia sp. strain Atlantic rainforest, the agent of an emerging rickettsiosis in Brazil. Ticks Tick Borne Dis 2016a; 7(3): 502-507. http://dx.doi.org/10.1016/j.ttbdis.2016.02.007. PMid:26895674.
    » http://dx.doi.org/10.1016/j.ttbdis.2016.02.007
  • Krawczak FS, Binder LC, Oliveira CS, Costa FB, Moraes-Filho J, Martins TF, et al. Ecology of a tick-borne spotted fever in southern Brazil. Exp Appl Acarol 2016b; 70(2): 219-229. http://dx.doi.org/10.1007/s10493-016-0070-1. PMid:27392739.
    » http://dx.doi.org/10.1007/s10493-016-0070-1
  • Labruna MB, Jorge RS, Sana DA, Jácomo AT, Kashivakura CK, Furtado MM, et al. Ticks (Acari: Ixodida) on wild carnivores in Brazil. Exp Appl Acarol 2005; 36(1-2): 149-163. http://dx.doi.org/10.1007/s10493-005-2563-1. PMid:16082932.
    » http://dx.doi.org/10.1007/s10493-005-2563-1
  • Labruna MB, Mattar VS, Nava S, Bermudez S, Venzal JM, Dolz G, et al. Rickettsioses in Latin America, Caribbean, Spain, and Portugal. Rev Mvz Cordoba 2011; 16(2): 2435-2457. http://dx.doi.org/10.21897/rmvz.282.
    » http://dx.doi.org/10.21897/rmvz.282
  • Labruna MB, Sanfilippo LF, Demetrio C, Menezes AC, Pinter A, Guglielmone AA, et al. Ticks collected on birds in the state of São Paulo, Brazil. Exp Appl Acarol 2007; 43(2): 147-160. http://dx.doi.org/10.1007/s10493-007-9106-x. PMid:17882514.
    » http://dx.doi.org/10.1007/s10493-007-9106-x
  • Luz HR, Faccini JLH. Ticks on Brazilian birds: overview. In: Ruiz L, Iglesias F. Birds: evolution and behavior, breeding strategies, migration and spread of disease . New York: Nova Science Publishers, Inc.; 2013. p. 98-124.
  • Luz HR, Mathias C, Faccini JLH. Carrapatos parasitando cães em uma área insular do estado do Rio de Janeiro, RJ, Brasil. Rev Bras Med Vet 2014; 36(4): 437-442.
  • Luz HR, Faccini JLH, McIntosh D. Molecular analyses reveal an abundant diversity of ticks and rickettsial agents associated with wild birds in two regions of primary Brazilian Atlantic Rainforest. Ticks Tick Borne Dis 2017; 8(4): 657-665. http://dx.doi.org/10.1016/j.ttbdis.2017.04.012. PMid:28479066.
    » http://dx.doi.org/10.1016/j.ttbdis.2017.04.012
  • Martins TF, Milanelo L, Krawczak FS, Furuya HR, Fitorra LS, Dores FT, et al. Diversity of ticks in the wildlife screening center of São Paulo city, Brazil. Cienc Rural 2017; 47(5): 1-6. http://dx.doi.org/10.1590/0103-8478cr20161052.
    » http://dx.doi.org/10.1590/0103-8478cr20161052
  • Martins TF, Onofrio VC, Barros-Battesti DM, Labruna MB. Nymphs of the genus Amblyomma (Acari: Ixodidae) of Brazil: descriptions, redescriptions, and identification key. T T Born Dis 2010; 1(2): 75-99. http://dx.doi.org/10.1016/j.ttbdis.2010.03.002. PMid:21771514.
    » http://dx.doi.org/10.1016/j.ttbdis.2010.03.002
  • Martins TF, Peres MG, Costa FB, Bacchiega TS, Appolinario CMJ, Antunes J, et al. Ticks infesting wild small rodents in three areas of the state of São Paulo, Brazil. Cienc Rural 2016; 46(5): 871-875. http://dx.doi.org/10.1590/0103-8478cr20150671.
    » http://dx.doi.org/10.1590/0103-8478cr20150671
  • Nava S, Velazco PM, Guglielmone AA. First record of Amblyomma longirostre (Koch, 1844) (Acari: Ixodidae) from Peru, with a review of this tick’s host relationships. Syst Appl Acarol 2010; 15(1): 21-30. http://dx.doi.org/10.11158/saa.15.1.2.
    » http://dx.doi.org/10.11158/saa.15.1.2
  • Nava S, Venzal JM, Acuña DG, Martins TF, Guglielmone AA. Ticks of the Southern Cone of America: diagnosis, distribution and hosts with taxonomy, ecology and sanitary importance . USA: Elsevier; 2017.
  • Ogrzewalska M, Pacheco RC, Uezu A, Richtzenhain LJ, Ferreira F, Labruna MB. Ticks (Acari: Ixodidae) infesting birds in an Atlantic rain forest region of Brazil. J Med Entomol 2009; 46(5): 1225-1229. http://dx.doi.org/10.1603/033.046.0534. PMid:19769058.
    » http://dx.doi.org/10.1603/033.046.0534
  • Oliveira HH, Quinelato IPF, Gomes V, Amorim M, Gazêta GS, Serra-Freire NM, et al. Ixodofauna em roedores e marsupiais capturados no Parque Estadual da Pedra Branca, Rio de Janeiro, Brasil. Rev Bras Med Vet 2014; 36(2): 137-143.
  • Onofrio VC, Barros-Battesti DM, Labruna MB, Faccini JL. Diagnoses of and illustrated key to the species of Ixodes Latreille, 1795 (Acari: Ixodidae) from Brazil. Syst Parasitol 2009; 72(2): 143-157. http://dx.doi.org/10.1007/s11230-008-9169-z. PMid:19115087.
    » http://dx.doi.org/10.1007/s11230-008-9169-z
  • Paduraru OA, Buffet JP, Cote M, Bonnet S, Moutailler S, Paduraru V, et al. Zoonotic transmission of pathogens by Ixodes ricinus ticks, Romania. Emerg Infect Dis 2012; 18(12): 2089-2090. http://dx.doi.org/10.3201/eid1812.120711. PMid:23171510.
    » http://dx.doi.org/10.3201/eid1812.120711
  • Parola P. Tick-borne rickettsial diseases: emerging risks in Europe. Comp Immunol Microbiol Infect Dis 2004; 27(5): 297-304. http://dx.doi.org/10.1016/j.cimid.2004.03.006. PMid:15225980.
    » http://dx.doi.org/10.1016/j.cimid.2004.03.006
  • Pinter A, Labruna MB. Isolation of Rickettsia rickettsii and Rickettsia bellii in cell culture from the tick Amblyomma aureolatum in Brazil. Ann N Y Acad Sci 2006; 1078(1): 523-529. http://dx.doi.org/10.1196/annals.1374.103. PMid:17114770.
    » http://dx.doi.org/10.1196/annals.1374.103
  • Reis NR, Peracchi AL, Pedro WA, Lima IP. Mamíferos do Brasil. Londrina: Universidade Estadual de Londrina; 2006.
  • Saraiva DG, Fournier GFSR, Martins TF, Leal KPG, Vieira FN, Câmara EMVC, et al. Ticks (Acari: Ixodidae) associated with small terrestrial mammals in the state of Minas Gerais, southeastern Brazil. Exp Appl Acarol 2012; 58(2): 159-166. http://dx.doi.org/10.1007/s10493-012-9570-9. PMid:22585005.
    » http://dx.doi.org/10.1007/s10493-012-9570-9
  • Sponchiado J, Melo GL, Martins TF, Krawczak FS, Labruna MB, Cáceres NC. Association patterns of ticks (Acari: Ixodida: Ixodidae, Argasidae) of small mammals in Cerrado fragments, western Brazil. Exp Appl Acarol 2015; 65(3): 389-401. http://dx.doi.org/10.1007/s10493-014-9877-9. PMid:25633262.
    » http://dx.doi.org/10.1007/s10493-014-9877-9
  • Szabó MP, Nieri-Bastos FA, Spolidorio MG, Martins TF, Barbieri AM, Labruna MB. In vitro isolation from Amblyomma ovale (Acari: Ixodidae) and ecological aspects of the Atlantic rainforest Rickettsia, the causative agent of a novel spotted fever rickettsiosis in Brazil. Parasitology 2013; 140(6): 719-728. http://dx.doi.org/10.1017/S0031182012002065. PMid:23363571.
    » http://dx.doi.org/10.1017/S0031182012002065
  • União Internacional para a Conservação da Natureza – IUCN. Red List of Threatened Species [online]. 2004 [cited 2017 June 19]. Available from: http://www.iucnredlist.org/
    » http://www.iucnredlist.org/

Publication Dates

  • Publication in this collection
    24 May 2018
  • Date of issue
    Jul-Sep 2018

History

  • Received
    03 Jan 2018
  • Accepted
    07 Mar 2018
Colégio Brasileiro de Parasitologia Veterinária FCAV/UNESP - Departamento de Patologia Veterinária, Via de acesso Prof. Paulo Donato Castellane s/n, Zona Rural, , 14884-900 Jaboticabal - SP, Brasil, Fone: (16) 3209-7100 RAMAL 7934 - Jaboticabal - SP - Brazil
E-mail: cbpv_rbpv.fcav@unesp.br