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

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 ; BARROS-BATTESTI et al., 2006 ; GUGLIELMONE et al., 2014 ). These ixodids have direct and indirect impacts on human and animal health by feeding and acting as vectors for pathogenic microorganisms ( PAROLA, 2004 ; BORCHERS et al., 2015 ). 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 ; PADURARU et al., 2012 ).

Although there are numerous studies on ticks that are associated with wild mammals in Brazil (e.g. LABRUNA et al., 2005 ; SARAIVA et al., 2012 ; MARTINS et al., 2016 ), 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 ; LUZ et al., 2014 ). 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 ; BONVICINO et al., 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 27^o 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) for nymphs; Barros-Battesti et al. (2006) for adults of Amblyomma; and Onofrio et al. (2009) for adults of Ixodes. Tick prevalence and intensity of infestation were calculated as described by Bush et al. (1997) . 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.

Host Order/Species	Date	Local	EX/PA	Altitude (meters)	P (%)	Mean intensity	Ixodes loricatus	Amblyomma auricularium	Amblyomma ovale	Amblyomma longirostre	Amblyomma sculptum	Amblyomma aureolatum	Amblyomma varium	Amblyomma nodosum
Rodentia
Echimyidae
Trinomys dimidiatus	November 2014	PARNASO	10/1	1000	10	2.0				2F
Cricetidae
Akodon montensis	July 2015	PARNASO	26/5	720	19	1.6			8N
Oligoryzomys nigripes	July 2015	PARNASO	24/5	740	20.8	1.4			7N
Didelphimorphia
Didelphidae
Didelphis aurita	November 2014	PARNASO	13/4	1000	30	3.5	11F/3M
	July 2015	PARNASO	13/1	1200	7	2.0						2N
	April 2015	PBSP	26/7	100	27	3.2	16F/7M
Monodelphis scalops	November 2014	PARNASO	4/3	1000	75	2.0	6F
Philander frenatus	November 2014	PARNASO	8/1	1000	12	3.0	3F
	July 2015	PARNASO	8/1	800	12	2.0					2N
Pilosa
Bradypodidae
Bradypus torquatus	November 2014	PARNASO	1/1	700	100	2.0				2F
		PARNASO	1/1	700	100	8.0							8F
Tamandua tetradactyla	November 2014	PARNASO	2/1	800	50	7.0								7F
Cingulata
Dasypodidae
Dasypus septemcintus	November 2014	PARNASO	2/1	700	50	43.0		43 F
Carnivora
Felidae
Leopardus pardalis	November 2014	PARNASO	1/1	820	100	2.0						2F
Canidae
Cerdocyon thous	November 2014	PARNASO	1/1	780	100	7.0						5F/2M

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 ; SARAIVA et al., 2012 ; SZABÓ et al., 2013 ; GUGLIELMONE et al., 2014 ; OLIVEIRA et al., 2014 ; KRAWCZAK et al., 2016b ; MARTINS et al., 2016 ; 2017 ), 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 ; NAVA et al., 2010 ; 2017 ). Immature stages prefer wild birds, especially Passeriformes ( OGRZEWALSKA et al., 2009 ; LUZ & FACCINI, 2013 ; LUZ et al., 2017 ). Among the sloths, only Bradypus tridactylus had previously been reported parasitized by A. longirostre ( NAVA et al., 2010 ). Thus, the present study provides a new record for A. longirostre in B. torquatus, which is regarded as an endangered species ( BRASIL, 2003 ; IUCN, 2004 ). The arboreal habits of this mammal probably enable parasitism by this tick species as has already been hypothesized by Labruna et al. (2007) 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 ; KRAWCZAK et al., 2016b ; MARTINS et al., 2016 ; NAVA et al., 2017 ). Immature stages of A. ovale are commonly found in association with rodents of the families Cricetidae and Echimyidae ( SARAIVA et al., 2012 ; SZABÓ et al., 2013 ; SPONCHIADO et al., 2015 ; MARTINS et al., 2016 ; NAVA et al., 2017 ). Adults of this tick species mostly infest wild and domestic carnivores ( GUGLIELMONE et al., 2003b , 2014 ; LABRUNA et al., 2005 ). They can also parasitize animals of the orders Artiodactyla, Didelphimorphia, Perissodactyla and Primates ( GUGLIELMONE et al., 2014 ). Sporadically, A. ovale larvae have been found parasitizing wild birds ( LUZ & FACCINI, 2013 ; LUZ et al., 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 ). A. ovale is a possible vector for a new human rickettsiosis in Brazil, named Atlantic Rainforest Rickettsiosis ( SZABÓ et al., 2013 ; BARBIERI et al., 2014 ; KRAWCZAK et al., 2016a ). In the present study, all nymphs of A. ovale were recorded at altitudes 720 and 740m, reinforcing the findings of Barbieri et al. (2015) , 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 ; BARROS-BATTESTI et al., 2006 ; NAVA et al., 2017 ). Within this family, high parasitism on Dasypus spp. can be seen, especially on D. novemcinctus ( GUGLIELMONE et al., 2003a ; NAVA et al., 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 ; NAVA et al., 2017 ). A. sculptum and A. aureolatum have been proved to transmit Rickettsia rickettsii to humans in Brazil ( PINTER & LABRUNA, 2006 ; LABRUNA et al., 2011 ). 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 ). Specimens of A. aureolatum were recorded at altitudes 780, 820 and 1200m, agreeing with reports by Barbieri et al. (2015) 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 , 2006 ; DANTAS-TORRES et al., 2012 ; OLIVEIRA et al., 2014 ). In the state of Rio de Janeiro, this species had previously been reported in association with Didelphis aurita in PBSP ( BITTENCOURT & ROCHA, 2003 ; OLIVEIRA et al., 2014 ).

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).

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Publication Dates

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

History

• Received
  03 Jan 2018
• Accepted
  07 Mar 2018