Systematic & Applied Acarology 22(6): 779–784 (2017) http://doi.org/10.11158/saa.22.6.3
ISSN 1362-1971 (print) ISSN 2056-6069 (online)
Article
Ticks (Acari: Ixodidae) and lice (Phthiraptera: Trichodectidae) infesting freeliving coatis (Nasua nasua Linnaeus, 1766) with sylvatic and synanthropic habits in the Atlantic rainforest of Southern Brazil PAULO C. MAGALHÃES-MATOS1, MARCELA F. D. MORAES2, JAQUELINE R. A. VALIM1, GUSTAVO N. S. CASTRO1, PRISCILLA N. SANTOS1, BRUNA S. M. L. MANIER1 & ADIVALDO H. FONSECA1 1
Parasitic Diseases Laboratory, Department of Epidemiology and Public Health, Federal Rural University of Rio de Janeiro – UFRRJ. Rodovia BR-465, Km 7, Zipcode 23891-000, Seropedica, Rio de Janeiro, Brazil. 2 Postgraduate Program in Preventive Veterinary Medicine, College of Agricultural and Veterinary Sciences, Estadual Paulista University – UNESP. Access way Prof. Paulo Donato Castellane, s/n, Zipcode 14887-900, Jaboticabal, São Paulo, Brazil. E-mail:
[email protected]
Abstract This research describes the infestation by ticks and lice in free-living coatis (Nasua nasua Linnaeus, 1766) with sylvatic and synanthropic habits living at the Iguaçu National Park (INP), state of Parana, southern Brazil. During the months of September 2014 and from March to April 2015, ticks and lice were collected from 86 freeliving coatis from INP. Among the animals analyzed, 99% (85/86) were infested with ectoparasites, Amblyomma spp. larvae (n=23), nymphs of Amblyomma brasiliense (n=77), Amblyomma coelebs (n=427) and Haemaphysalis juxtakochi (n=6) being observed, as well as Amblyomma ovale adults (n=46). Lice were found in lower prevalence (13%, 11/86), nymphs (n=31) and adults (n=9) of Neotrichodectes pallidus. Summary results show feral coatis with sylvatic and synanthropic habits as competent hosts for ixodid ticks and lice, arthropods responsible for the transmission of pathogens for carnivores, others wildlife and humans. This paper presents the first record of H. juxtakochi infesting coatis in Brazil. Key words: Procyonidae, Ticks, lice, Atlantic forest, Iguaçu National Park, Brazil
Introduction Ticks, lice, and fleas are considered the main arthropods infesting animals. These ectoparasites are important not only because they suck blood and/or cause epithelial lesions in hosts, but also because of the ability some species have to transmit pathogens to animals, including humans (Tuff 1977, Linardi & Guimarães 2000, Barros-Battesti et al. 2006). Wild animals present a substantial diversity of species of ectoparasites (Barros-Battesti et al. 2006), although not much is known about the ecoepidemiology of such infestations in different regions of Brazil. The Iguaçu National Park (INP) is one of the largest conservation areas of the Atlantic forest, comprising 457,794 acres. It comprises the Iguaçu Falls (Cáceres 2011), receiving annually around 1.5 million visitors from many regions of the world (ICMBio 2016). INP has a very diverse fauna, deserving highlight mammals such as the jaguar, tapir, coati, deer, agouti, and the collared peccary, among other species. The coatis (Nasua nasua Linnaeus, 1766) are carnivores from the Procyonidae family, widely distributed all over South America, and it is one of the species presenting the largest synanthropy in the areas of visitation at the INP, especially near the viewpoint of the Iguaçu falls (Cáceres 2011). © Systematic & Applied Acarology Society
779
The knowledge about the dynamics of the infestation by ectoparasites in coatis is important, since it establishes the role of this species as the host of different ectoparasites, including the ones transmitting pathogens to other animals and to humans living in the same habitats. Thus, this study has the purpose of describing the infestation with ticks and lice in coatis with sylvatic and synanthropic habits in the areas of visitation at the INP, in the state of Parana, south of Brazil.
Material and methods The animals analyzed in this research were randomly sampled from the touristic visitation area at INP, located in the city of Foz do Iguaçu, state of Parana, south of Brazil. The areas sampled comprise the Iguaçu Falls viewpoint (25°41'03"S, 54°26'24"W, with a total length of around 1.2 km) and the access to two trails inside the forest (25°39'05"S, 54°26'16"W and 25°37'36"S, 54°27'39"W). During the month of September 2014, and from March to April 2015, totalizing 42 days of collection in the morning and in the afternoon, ticks and lice were collected from free-living coatis. The animals were attracted with a bait of peanut butter and were captured actively with a hand net. After holding them manually, the coatis were anesthetized with a combination of tiletamine and zolazepam (zoletil 50®, 7mg/Kg dose) and xylazine 2% (2mg/Kg), via intramuscular injection. All coatis analyzed were identified with numbered eartags to avoid recapture. After recovered from anesthesia, the animals were reintroduced in their original habitats. Road-killed coatis at the BR-469 highway, which runs inside the park, were also analyzed. The ticks and lice were searched across the body surface of the animals, collected manually, preserved in isopropanol, and sent to the laboratory for analyses. The taxonomic identification of the ticks was carried out in a stereomicroscope (Olimpus® SZX16, program cellSens 1.12), based on their morphologic aspects, as per Barros-Battesti et al. (2006) for adults, as per Cooley (1946) and Kohls (1960) for Haemaphysalis nymphs, and as per Martins et al. (2010) for Amblyomma nymphs. Larvae from ticks were identified only at their genus level, since in Brazil there is no literature for specific identification. Lice were clarified with a mix of potassium hydroxide 10% and identified in an optical microscope (Olympus BX45®) based on Tuff (1977) and compared with Werneck’s (1936) description. The parasites ecology parameters were calculated according to Bush et al. (1997). After identified, the species of ticks and lice were deposited at the collection “Coleção de Artrópodes Vetores Ápteros de Importância na Saúde das Comunidades” (Collection of Aptera Vector Arthropods of Importance in the Health of Communities) of the Oswaldo Cruz Institute (CAVAISC – FIOCruz), in Rio de Janeiro, with deposit numbers CAVAISC-IXO 2424 at 2429 for ticks, and CAVAISC-PHT 190 and 191 for lice. Other ectoparasites such as fleas and mites were not considered for this study. The capture of these animals and the research of ectoparasites were authorized by the Chico Mendes Biodiversity Institute (ICMBio), through the Sistema de Autorização e Informação em Biodiversidade (SISBio, Authorization and Information on Biodiversity System), number 43614-2. The research was also approved by the research ethics committee at the Federal Rural University of Rio de Janeiro (UFRRJ), number 058/2014.
Results and discussion Samples of 86 free-living coatis from the INP (84 captured, 2 road-killed) were collected, totalizing 619 ectoparasites, among ticks (n=579) and lice (n=40). These coatis were infested by Amblyomma spp. larvae, nymphs of Amblyomma brasiliense, Amblyomma coelebs and Haemaphysalis 780
SYSTEMATIC & APPLIED ACAROLOGY
VOL. 22
juxtakochi, as well as Amblyomma ovale adults. Lice were found in lower prevalence, being nymphs and adults of Neotrichodectes pallidus. The prevalence and ecological parameters of the infestation are presented in Table 1. The coatis analyzed presented high prevalence (99%) and abundance (7.2) of infestation by ectoparasites, mainly represented by ticks, which corresponded to 93% of the total ectoparasites obtained. The most abundant species of ticks and the one that has also infested most of the animals was Amblyomma coelebs Neumann, 1899, suggesting that coatis have an importance for the ecology of this species of tick at the INP. TABLE 1. Ectoparasites and parasitological ecology data obtained from free-living coatis from the Iguaçu National Park, Parana, Brazil. Taxon
Stage
Number of parasites
Prevalence (+/t)
Mean intensity ± SD
Mean abundance ± SD
Amblyomma sp.
Larvae
23
14% (12/86)
1.9±1.3
0.3±0.8
Amblyomma brasiliense
Nymph
77
45% (39/86)
2.0±1.0
0.9±1.2
Amblyomma coelebs
Nymph
427
96% (83/86)
5.1±4.5
5.0±4.5
Haemaphysalis juxtakochi
Nymph
6
6% (5/86)
1.2±0.4
0.1±0.3
Adult
46(22♂, 24♀)
23% (20/86)
2.3±2.5
0.5±1.5
Nymph, Adult
40(31n, 6♂, 3♀)
13% (11/86)
3.6±2.6
0.5±1.5
619
99% (85/86)
7.3±6.1
7.2±6.1
Ixodidae
Amblyomma ovale Phthiraptera Neotrichodectes pallidus Total
+/t: infested animals/total. SD: Standard deviation.
In Brazil, previous records of the infestation by ticks in coatis report a parasitism by Amblyomma aureolatum (Pallas, 1772), A. brasiliense Aragão, 1908, Amblyomma cajennense Fabricius, 1787, A. coelebs Neumann, 1899, Amblyomma humerale Koch, 1844, Amblyomma naponense (Packhard, 1869), Amblyomma oblongoguttatum Koch, 1844, Amblyomma ovale Koch, 1844, Amblyomma parvum Aragão, 1908, Amblyomma rotundatum Koch, 1844, Amblyomma sculptum Berlese, 1888, Amblyomma tigrinum Koch, 1844, Ixodes loricatus Neumann, 1899, and Amblyomma spp. larvae (Aragão 1936, Barros & Baggio 1992, Pereira et al. 2000, Arzua et al. 2005, Labruna et al. 2005a, Rodrigues et al. 2006, Acosta et al. 2016, Witter et al. 2016). It is important to highlight the occurrence of A. ovale infesting coatis from the INP, a species of tick that usually infests carnivores (Labruna et al. 2005a) and which is the vector of Rickettsia parkeri Lackman et al., 1965 strain Atlantic forest, an etiologic agent from a rickettsioses recently described as important to humans (Szabó et al. 2013). This paper also reports on the infestation of coatis by Haemaphysalis juxtakochi Cooley, 1946, a species in which Labruna et al. (2005b) isolated the Rickettsia rhipicephali Burgdorfer et al., 1978 bacteria in the state of Rondonia, in the Brazilian Amazon. A. coelebs, A. brasiliense Aragão, 1908, and A. ovale were recently registered infesting coatis from the Iguazu National Park, in Puerto Iguazu, Argentina (Lamattina et al. 2014). Although this area is physically separated from the INP by the Iguazu River, similarities between the fauna of ectoparasites from both areas could be observed. This can be explained by the similarity of the climatic and environmental conditions of both parks, such as temperature, humidity and rainfall levels, as well as by the co-occurrence of species hosting adult forms of these ticks, that is, tapirs (Tapirus terrestris Linnaeus, 1758), peccaries (Pecari tajacu Linnaeus, 1758, Tayassu pecari Link, 1795 and carnivores, respectively (Barros-Battesti et al. 2006). Unlike what was reported in Argentina by Lamattina et al. (2014), in the present study there were observed infestations with nymphs of H. juxtakochi, a species whose adults infest mammals of 2017
MAGALHÃES-MATOS ET AL.: TICKS AND LICE INFESTING FREE-LIVING COATIS
781
the Cervidae family (Barros-Battesti et al. 2006), such as Mazama americana Erxleben, 1777 (Jones et al. 1972), and Mazama nana Hensel, 1872 (Martins et al. 2007). Immature forms of H. juxtakochi can parasitize birds such as Pyrrhocoma ruficeps Strickland, 1844 (Arzua et al. 2005) and Harpia harpyja Linnaeus, 1958 (Labruna et al. 2010), as well as mammals such as rodents, primates, tapirs, and peccaries (Jones et al. 1972). Although H. juxtakochi nymphs have been reported parasitizing coatis in Panama (Fairchild et al. 1966), this is the first report of this species infesting coatis in Brazil. Less prevalent and abundant (13%; 0.47), infestation by Neotrichodectes pallidus (Piaget, 1880) lice was observed, different from the observations made by Rodrigues et al. (2006). This study was carried out in the Atlantic forest area in the city of Juiz de Fora, state of Minas Gerais, Brazil, where this species was observed in 52.6% (10/19) of the coatis and in higher abundance (3.21) than the one from this present work. These data suggest that the coatis analyzed in the Atlantic forest of Juiz de Fora have an epidemiologic role which is more important to the maintenance of lice than the coatis from the INP, which, in turn, have been more important to the maintenance of ticks of the genus Amblyomma, because of their high prevalence, intensity, and parasitical abundance. Coatis with sylvatic and synanthropic habits in the touristic areas of the INP are highly infested with ectoparasites, mainly by ticks, acting as hosts and dispersers of ticks vectors, such as A. ovale and H. juxtakochi.
Acknowledgement We would like to express our gratitude to the National Council of Scientific and Technological Development (CNPq) and the Rio de Janeiro State Research Support Foundation (FAPERJ), for their financial assistance; to the officials of the Projeto Carnívoros do Iguaçu (Project Iguazu Carnivores) and to the Iguaçu National Park, Marina Xavier, Raphael Xavier, Mauro Costa and Pedro Fogaça, for their essential contribution during the collections.
References Acosta, I.C.L., Martins, T.F., Marcili, A., Soares, H.S., Krawczak, F.S., Vieira, F.T. & Labruna, M.B. (2016) Ticks (Acari: Ixodidae, Argasidae) from humans, domestic and wild animals in the state of Espírito Santo, Brazil, with notes on rickettsial infection. Veterinary Parasitology: Regional Studies and Reports, 3–4, 66–69. http://dx.doi.org/10.1016/j.vprsr.2016.08.001 Aragão, H.B. (1936) Ixodidas brasileiros e de alguns países limítrofes. Memórias do Instituto Oswaldo Cruz, 31, 759–843. https://doi.org/10.1590/S0074-02761936000400004 Arzua, M., Onofrio, V.C. & Barros-Battesti, D.M. (2005) Catalogue of the tick collection (Acari, Ixodida) of the Museu de Historia Natural Capão da Imbuia, Curitiba, Paraná, Brazil. Revista Brasileira de Zoologia, 22, 623–632. https://doi.org/10.1590/S0101-81752005000300015 Barros, D.M. & Baggio, D. (1992) Ectoparasites Ixodida Leach, 1817 on wild mammals in the State of Paraná, Brazil. Memórias do Instituto Oswaldo Cruz, 87, 291–296. http://dx.doi.org/10.1590/S0074-02761992000200018 Barros-Battesti, D.M., Arzua, M. & Bechara, B.H. (2006) Carrapatos de importância médico-veterinária da região neotropical: um guia ilustrado para identificação de espécies. São Paulo, Vox/ICTTD-3/Butantan, 223 pp. Bush, A.O., Lafferty, K.D, Lotz, J.M. & Shostak, A.W. (1997) Parasitology meets ecology: on its own terms: Margolis et al. revisited. Journal of Parasitology, 83, 575–583. http://dx.doi.org/10.2307/3284227
782
SYSTEMATIC & APPLIED ACAROLOGY
VOL. 22
Cáceres, N.C. (2011) Mamíferos. In: Fernandes, C.R., Garcia, H. (eds.) Parque Nacional do Iguaçu: Patrimônio natural da humanidade. São Paulo, Ipsis Gráfica e Editora, pp. 198–215. Cooley, R.A. (1946) The genera Boophilus, Rhipicephalus, and Haemaphysalis (Ixodidae) of the new world. Washington, Government Printing Office, 54 pp. Fairchild, G.B., Kohls, G.M. & Tipton, V.J. (1966) The ticks of Panamá (Acarina: Ixodoidea). In: Wenzel, R.L. & Tipton, V.J. (eds) Ectoparasites of Panama. Chicago, Field Museum of Natural History, pp. 167–219. ICMBio (Instituto Chico Mendes de Conservação da Biodiversidade) (2016). Dados de visitação (2007–2015), Ranking de visitantes 2012–2015. Available from http://www.icmbio.gov.br/portal/images/stories/ Dados_de_visita%C3%A7%C3%A3o_DCOM.pdf (accessed 16 Oct. 2016). Jones, E.K., Clifford, C.M., Keirans, J.E. & Kohls, G.M. (1972) The ticks of Venezuela (Acarina: Ixodoidea) with a key to the species of Amblyomma in the western hemisphere. Provo, Brigham Young University Science Bulletin, 40 pp. Kohls, G.M. (1960) Records and new synonymy of new world Haemaphysalis ticks, with descriptions of the nymph and larva of H. juxtakochi Cooley. Journal of Parasitology, 46, 355–361. http://dx.doi.org/10.2307/3275499 Labruna, M.B., Jorge, R.S.P., Sana, D.A., Jácomo, A.T.A., Kashivakura, C.K., Furtado, M.M., Ferro, C., Perez, S.A., Silveira, L., Santos Jr., T.S., Marques, S.R., Morato, R.G., Nava, A., Adania, C.H., Teixeira, R.H.F, Gomes, A.A.B, Conforti, V.A., Azevedo, F.C.C., Prada, C.S., Silva, J.C.R., Batista, A.F., Marvulo, M.F.V, Morato, R.L.G., Alho, C.J.R, Pinter, A., Ferreira, P.M., Ferreira, F. & Barros-Battesti, D.M. (2005a) Ticks (Acari: Ixodida) on wild carnivores in Brazil. Experimental and Applied Acarology, 36, 149–163. http://dx.doi.org/10.1007/s10493-005-2563-1 Labruna, M.B., Camargo, L.M.A., Camargo, E.P. & Walker, D.H. (2005b) Detection of a spotted fever group Rickettsia in the tick Haemaphysalis juxtakochi in Rondonia, Brazil. Veterinary Parasitology, 127, 169– 174. http://dx.doi.org/10.1016/j.vetpar.2004.09.024 Labruna, M.B., Barbieri, F.S., Martins, T.F., Brito, L.G. & Ribeiro, F.D.S. (2010) New tick records in Rondônia, Western Brazilian Amazon. Revista Brasileira de Parasitologia Veterinária, 19, 192–194. http://dx.doi.org/10.1590/S1984-29612010000300014 Lamattina, D., Tarragona, E.L., Costa, S.A., Guglielmone, A. & Nava, S. (2014) Ticks (Acari: Ixodidae) of northern Misiones Province, Argentina. Systematic and Applied Acarology, 19, 393–398. http://dx.doi.org/10.11158/saa.19.4.2 Linardi, P.M. & Guimarães, L.R. (2000) Sifonápteros do Brasil. São Paulo, Museu de Zoologia USP/FAPESP, 291 pp. Martins, J.R., Salomão, E.L., Doyle, R.L., Onofrio, V.C., Barros-Battesti, D.M. & Guglielmone, A.A. (2007) Haemaphysalis juxtakochi Cooley, 1946 (Acari: Ixodidae) parasitando Mazama nana (Hensel, 1872) (Artiodactyla: Cervidae) no Estado do Rio Grande do Sul. Revista Brasileira de Parasitologia Veterinária, 16, 171–173. http://dx.doi.org/10.1590/S1984-29612007000300012 Martins, T.F., Onofrio, V.C., Barros-Battesti, D.M. & Labruna, M.B. (2010) Nymphs of the genus Amblyomma (Acari: Ixodidae) of Brazil: descriptions, redescriptions, and identification key. Ticks and Tick-Borne Diseases, 1, 75–99. http://dx.doi.org/10.1016/j.ttbdis.2010.03.002 Pereira, M.C., Szabó, M.P.J., Bechara, G.H., Matushima, E.R., Duarte, J.M.B., Rechav, Y., Fielden, L. & Keirans, J.E. (2000) Ticks on wild animals from the Pantanal region of Brazil. Journal of Medical Entomology, 37, 979–983. http://dx.doi.org/10.1603/0022-2585-37.6.979 Rodrigues, A.F.S.F., Daemon, E. & Massard, C.L. (2006) Ectoparasites of Nasua nasua (Carnivora, Procyonidae) from an urban Forest in Southeastern Brazil. Arquivos Brasileiros de Medicina Veterinária e Zootecnia, 58, 969–97. http://dx.doi.org/10.1590/S0102-09352006000500043 Szabó, M.P.J., Nieri-Bastos, F.A., Spolidorio, M.G., Martins, T.F., Barbieri, A.M. & Labruna, M.B. (2013) 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, 140, 719–728. http://dx.doi.org/10.1017/S0031182012002065 Tuff, D.W. (1977) A key to lice of man and domestic animals. Texas Journal of Science, 28, 145–159. Witter, R., Martins, T.F., Campos, A.K., Melo, A.L.T, Corrêa, S.H.R., Morgado, T.O., Wolf, R.W., May-Júnior,
2017
MAGALHÃES-MATOS ET AL.: TICKS AND LICE INFESTING FREE-LIVING COATIS
783
J.A., Sinkoc, A.L., Strüssmann, C., Aguiar, D.M., Rossi, R.V., Semedo, T.B.F., Campos, Z., Desbiez, A.L.J., Labruna, M.B. & Pacheco, R.C. (2016) Rickettsial infection in ticks (Acari: Ixodidae) of wild animals in midwestern Brazil. Ticks and Tick-borne Diseases, 7, 415–423. http://dx.doi.org/10.1016/j.ttbdis.2015.12.019 Werneck, F.L. (1936) Contribuição ao conhecimento dos Mallophagos de mamíferos sul-americanos. Memórias do Instituto Oswaldo Cruz, 31, 391–589. https://doi.org/10.1590/S0074-02761936000300001 Submitted: 2 Nov. 2016; accepted by Trevor Petney: 13 Apr. 2017; published: 19 May 2017
784
SYSTEMATIC & APPLIED ACAROLOGY
VOL. 22
