SHORT COMMUNICATIONS
Ticks (Acari: Ixodidae) Infesting Birds in an Atlantic Rain Forest Region of Brazil MARIA OGRZEWALSKA,1,2 RICHARD C. PACHECO,1 ALEXANDRE UEZU,3 LEONARDO J. RICHTZENHAIN,1 FERNANDO FERREIRA,1 AND MARCELO B. LABRUNA1
J. Med. Entomol. 46(5): 1225Ð1229 (2009)
ABSTRACT Brazil has the third richest bird diversity of the world; however, there are few data concerning ticks (Acari: Ixodidae) parazitizing birds. The aim of the study was to report tick infestations on wild birds from an Atlantic rain forest region of Brazil. During 2 yr, ticks were collected from birds and from the environment in 12 forest sites. A total of 1,725 birds were captured representing 80 species from 24 families. In total, 223 (13%) birds were found infested by immature stages of Amblyomma ticks: 1,800 larvae and 539 nymphs. The prevalence of ticks was higher among birds from the families Thamnophilidae, Conopophagidae, and Momotidae. The most common tick parasitizing birds was Amblyomma nodosum Koch. Other tick species, Amblyomma coelebs Neumann, Amblyomma cajennense (F.), Amblyomma ovale Koch, Amblyomma longirostre (Koch), Amblyomma calcaratum Neumann, and Amblyomma naponense (Packard), were found sporadically. Among freeliving ticks collected in the environment, A. cajennense was the most common, followed by A. coelebs, A. naponense, Amblyomma brasilense Araga˜o, and Hemaphysalis juxtakochi Cooley. KEY WORDS birds, Atlantic rain forest, Amblyomma ticks
Wild birds serve as important hosts for ticks (Acari: Ixodidae) and are reservoirs of many tick-borne pathogens. Consequently, wild birds are responsible for transportation of infected ticks for long distances, even between continents (Olsen et al. 1995, Bjoersdorff et al. 2001). Despite that Brazil has one of the largest bird fauna of the world, comprising by ⬇1,590 species (Sick 1997), there are few data concerning ticks infesting Brazilian birds (Labruna et al. 2007). This scarcity of data is certainly linked to the lack of taxonomic keys for proper identiÞcation of the immature stages of South American Amblyomma, a genus representing 33 of the 56 species of ticks occurring in Brazil (Labruna et al. 2007). That is the reason why ticks collected from birds in some studies have been identiÞed only to the genus level (Marini et al. 1996, Neves et al. 2000). Thus, the most trustworthy ways of identifying immature stages of Amblyomma species from Brazil are by rearing them to the adult stage or by using molecular tools such as DNA sequencing of speciÞc molecular markers, for example, 12S or 16S mitochondrial rDNA gene fragments followed by comparisons with previous sequences obtained from adult ticks of different tick species (Arzua et al. 2003, Venzal et al. 2005, Mangold 2006). The aim of our study was to report tick infestations on wild birds in a region of the Atlantic rain forest in Brazil. In addition, 1 Faculty of Veterinary Medicine, University of Sa ˜o Paulo, Sa˜o Paulo, SP, Brazil. 2 Corresponding author, e-mail:
[email protected]. 3 Instituto de Pesquisas Ecolo ´ gicas (IPEˆ ), Nazare´ Paulista, SP, Brazil.
free-living ticks collected in bird macrohabitats are reported. Materials and Methods This study was conducted in the “Pontal do Paranapanema” region, in the southwestern corner of the state of Sa˜o Paulo, mainly within the Teodoro Sampaio Municipality (22⬚ 53⬘ S, 52⬚ 09⬘ W). It is an extremely fragmented region of Atlantic rain forest, where the landscape is composed predominantly of pastures and sugarcane (Saccharum spp.) crops interspersed by forest fragments. Capture of birds was performed inside 12 forest patches by using mist nets at 3-mo intervals every season from May 2004 to December 2006, totaling 23,688 net-hours. Birds were identiÞed to the species, ringed, and examined for ticks through checking carefully the whole body by deßecting the feathers. Any tick found attached to a bird was removed with forceps. Thereafter, birds were released at the same site. We followed the protocol, which agrees with Ethical Principles in Animal Research adopted by the Brazilian College of Animal Experimentation (COBEA), and which was approved by the Faculdade de Medicina Veterina´ria e Zootecnia /USP-Ethical Committee for Animal Research. Permits and approvals are on Þle in the ofÞce of M.B.L. During each bird capture, free-living ticks were collected in the environment of the same forest patch as the bird capture by dragging the vegetation with a white ßannel (100 by 50 cm) along 1,000 m, as de-
0022-2585/09/1225Ð1229$04.00/0 䉷 2009 Entomological Society of America
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scribed previously (Oliveira et al. 2000). Dragging was always performed in animal trails around the mist net site, where a dense understory composed of woody shrubs, bushes, and lianas was present. The drag cloth was passed along the trails, over the ground litter layer and over plants up to 50 cm above ground level. For counting purposes, nymphs and adult ticks were counted individually, whereas larvae were counted as the number of clusters, i.e., each larval cluster collected from the environment was considered a single unit. Collected larvae and nymphs from birds and environment were brought alive to the laboratory, where attempts to rear them to the adult stage were conducted by feeding them on tick-naõ¨ve rabbits, as described previously (Labruna et al. 2002). Engorged nymphs collected from birds were left in an incubator (25⬚C and 95% RH) for molting. Adults obtained from the engorged nymphs were used for species identiÞcation of the former immature ticks. Larvae and nymphs that died in the laboratory before reaching the adult stage were preserved in absolute isopropanol. The species of any adults obtained from each larval cluster collected in the environment was used for species identiÞcation of the larval cluster as a single unit. Attempts to identify the tick species of dead larvae and nymphs were performed by molecular methods. For this purpose, each isopropanol-preserved nymph or a group of larvae representing a single cluster from the environment were processed by DNA extraction as described previously (Sangioni et al. 2005) and submitted to polymerase chain reaction (PCR) by using primers that amplify ⬇460 bp of the tick mitochondrial rDNA gene (Mangold et al. 1998). AmpliÞed products were puriÞed and DNA sequenced as described previously (Labruna et al. 2004) and compared with National Center for Biotechnology Information Nucleotide BLAST searches (Altschul et al. 1990) and with mitochondrial 16S rDNA gene partial sequences obtained in our laboratory during the current study, by processing adult ticks of the following species (locality of origin in parentheses): Amblyomma nodosum Koch (Sao Paulo City, state of Sa˜o Paulo, 23⬚ 40⬘ S, 45⬚ 44⬘ W), Amblyomma brasiliense Araga˜o (Teodoro Sampaio: 22⬚ 53⬘ S, 52⬚ 09⬘ W), Amblyomma calcaratum Neumann (Piraju, Sa˜o Paulo: 23⬚ 11⬘S,49⬚ 23⬘W), Amblyomma naponense (Packard) (Teodoro Sampaio), Amblyomma oblongoguttatum Koch (Monte Negro, Rondonia: 10⬚ 17⬘ S, 63⬚ 14⬘ W), Amblyomma cajennense (F.) (Teodoro Sampaio), Amblyomma incisum Neumann (Ribeira˜o Grande, Sa˜o Paulo: 24⬚ 18⬘ S, 48⬚ 24⬘ W), and Amblyomma coelebs Neumann (Teodoro Sampaio). Field data of ticks on birds were used to calculate the prevalence, and mean intensity of the tick infestations for each bird species. These calculations were performed according to the concepts reported by Bush et al. (1997); applied to our study, prevalence is the number of infested birds/number of examined birds ⫻ 100 for each bird species, and mean intensity
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is total number of ticks/number of infested birds for each bird species. Results and Discussion In total, 1,725 birds were captured representing 80 species from 24 families within 10 orders. Passeriformes constituted the most numerous bird order, with 54 species encompassing 1,485 (86.1%) individual birds. In total, 223 (13%) birds of 29 species were infested with 2,339 ticks, which were all immature stages of Amblyomma (1,800 larvae and 539 nymphs). In total, 2,305 ticks (98.6%) were collected from Passeriformes, whereas only 34 ticks (1.4%) were collected from non-Passeriformes (Table 1). In total, nine larvae and 237 nymphs collected from birds were reared to the adult stage in the laboratory, being identiÞed as A. nodosum (six larvae, 222 nymphs), Amblyomma longirostre (Koch) (two larvae, three nymphs), A. cajennense (four nymphs), A. calcaratum (two nymphs), A. coelebs (one larva, two nymphs), and Amblyomma ovale Koch (four nymphs). In total, 69 larvae and 192 nymphs collected from birds were identiÞed by molecular analysis (Table 2), being identiÞed as A. nodosum (52 larvae, 172 nymphs), A. longirostre (two larvae), A. cajennense (eight nymphs), A. coelebs (10 larvae, 10 nymphs), A. naponense (one nymph), and A. ovale (Þve larvae, one nymph). In total, 1,722 larvae and 110 nymphs collected from birds died before reaching the adult stage or did not generate high-quality DNA sequence; therefore, they were identiÞed morphologically as Amblyomma sp. A. nodosum comprised 89.1% of all ticks identiÞed to the species level and was by far the most common tick species infesting Passeriformes birds. Adults of this Neotropical species feed primarily on anteaters (Tamandua spp. and Myrmecophaga tridactyla L.) (Jones et al. 1972), whereas subadult stages were previously reported on specimens of the Passerifomes Dysithamnus mentalis (Temminck) and Manacus manacus (L.) (Labruna et al. 2007). The current study reports this tick for the Þrst time on 16 bird species (15 Passeriformes and one Coraciiformes) (Table 1). Five tick species were collected by dragging on vegetation in the environment (Table 3), where A. cajennense was far the most abundant species. No A. nodosum specimen was collected in the environment. Possibly, immature stages of A. cajennense and A. nodosum may use distinct microhabitats in the forest, a condition that could have contributed to our Þndings, i.e., even though numerous A. cajennense were found in the environment, they were not questing in a proper site to get in contact with many birds, as did the A. nodosum ticks. The opposite could be said for A. nodosum questing ticks, which were present in the forest, probably in one site where the vegetation structure prevented the dragging ßannel contacting them. A. coelebs, A. ovale, and A. naponense are reported for the Þrst time parasitizing birds. Three other species, A. calcaratum, A. longirostre, and A. cajennense, have been previously reported on birds (Jones et al. 1972, Arzua et al. 2005, Labruna et al. 2007). A. cal-
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Table 1. Amblyomma ticks collected on birds in an Atlantic rain forest area in the region of Pontal do Paranapanema, state of Sao Paulo, Brazil Bird order, family Columbiformes Columbidae Momotidae Cracidae Bucconidae Strigidae Conopophagidae Corvidae Dendrocolaptidae Emberizidae Formicariidae Parulidae Pipridae Thamnophilidae Thraupidae Turdidae Tyrannidae
No. infested/ no. captured
Preva-lence
Mean intensity
Ticksa
Leptotila verreauxi Baryphthengus ruficapillus Momotus momota Penelope superciliaris Malacoptila striata Glaucidium brasilianum Glaucidium minutissimum Conopophaga lineata Cyanocorax chrysops Dendrocolaptes platyrostris Sittasomus griseicapillus Arremon flavirostris Dysithamnus mentalis Formicivora rufa Basileuterus culicivorus Basileuterus flaveolus Pipra fasciicauda Thamnophilus caerulescens Thamnophilus pelzenii
1/21 11/76 2/9 1/2 1/19 1/11 1/3 43/149 1/2 1/13 1/66 9/145 6/43 1/1 2/69 8/63 4/145 8/18 98/313
4.8 14.5 22.2 50.0 5.3 9.1 33.3 28.9 50.0 7.7 1.5 6.2 13.9 100 2.9 12.7 2.8 44.4 31.3
10.0 1.6 1.0 1.0 1.0 1.0 1.0 29.6 1.0 1.0 3.0 66.8 1.7 1.0 1.5 1.0 1.0 4.9 3.4
Habia rubica Trichothraupis melanops Turdus amaurochalinusb Turdus subalarisb Casiornis rufab Cnemotriccus fuscatusb Elaenia mesoleucab Hemitriccus margaritaceiventer Leptopogon amaurocephalus Platyrinchus mystaceus
1/13 1/1 1/18 1/2 1/7 10/78 1/8 1/10 2/27 4/92
7.7 100 5.5 50.0 14.2 12.8 12.5 10.0 7.4 4.3
1.0 1.0 2.0 1.0 3.0 1.2 1.0 3.0 1.0 1.0
L: Aco N: Ano, Aca, Acl, Aco, Asp N: Aca, Aco N: Aca N: Aco N: Asp N: Asp L, N: Ano, Asp; N: Aco N: Asp N: Ano L: Alo L, N: Aov, Asp; N: Ano, Aca N: Ano, Aca, Asp N: Ano N: Ano N: Ano, Asp N: Alo, Asp N: Ano, Asp L, N: Ano, Aco, Asp; N: Aça, Aov, Ana N: Ano N: Ano N: Ano, Aco N: Aov N: Ano N: Ano, Alo, Asp N: Asp L, N: Ano; N: Asp L, N: Alo N: Ano
Species
a L, larva; N, nymph; Aco, Amblyomma coelebs; Ano, Amblyomma nodosum; Aca, Amblyomma cajennense; Acl, Amblyomma calcaratum; Alo, Amblyomma longirostre; Aov, Amblyomma ovale; Ana, Amblyomma naponense; Asp, Amblyomma sp. b Reported to be migratory species (Chesser 1994, Ridgely and Tudor 1994, Sick 1997).
caratum is morphologically and ecologically closely related to A. nodosum, as its adult stages parasitize chießy anteaters, and subadults seem to feed primarily on birds (Jones et al. 1972, Labruna et al. 2007). We found only two nymphs on B. ruficapillus, which is the Þrst record of A. calcaratum on this bird species. Adults of A. longirostre feed primarily on porcupines (Coendou spp.), whereas it is well known that its subadult Table 2. Ticks identified by molecular analysis of partial 16S rDNA in the present study Tick stage (no.)
Tick species sequence with highest similarity (sourcea)
% similarityb
Larvae (52) Nymphs (172) Larvae (2) Larvae (31) Nymphs (8) Larvae (16) Nymphs (10) Larvae (2) Nymph (1) Larvae (4) Larva (5) Nymph (1)
Amblyomma nodosum (present study) Amblyomma nodosum (present study) Amblyomma longirostre (EU805564) Amblyomma cajennense (present study) Amblyomma cajennense (present study) Amblyomma coelebs (present study) Amblyomma coelebs (present study) Amblyomma naponense (present study) Amblyomma naponense (present study) Amblyomma brasiliense (present study) Amblyomma ovale (AF541255) Amblyomma ovale (AF541255)
99.9 99.9 99.7 100 100 100 100 100 100 100 97.9 97.9
a GenBank accession numbers or sequences generated from adult ticks processed in the present study. b Compared with the corresponding sequence of adult ticks.
stages feed primarily on birds, mostly Passeriformes (Labruna et al. 2007). In some other regions of the state of Sao Paulo, A. longirostre was the most common tick parasitizing Passeriformes (Labruna et al. 2007, Ogrzewalska et al. 2008), a situation very different from the Þndings in our study site. Bird species sampled but not found infested by ticks were (number of individuals in parentheses) as follows: Apodiformes, Trochilidae: Chlorostilbon aureoventris dÕOrbigny and Lafresnaye (6), Hylocharis chrysura Shaw (2), Phaethornis eurynome (Lesson) (1), Phaethornis pretrei (Lesson and Delattre) (10), Thalurania glaucopis (Gmelin) (14); Columbiformes, Columbidae: Claravis Table 3. Free-living ticks collected in an Atlantic rainforest area in the region of Pontal do Paranapanema, state of Sao Paulo, Brazil No. ticks Tick species Amblyomma cajennense Amblyomma coelebs Amblyomma brasiliense Amblyomma naponense Haemaphysalis juxtakochi Amblyomma spp. Total
Adults Nymphs 227 8 9 7 251
1,992 47 22 34 4 1,010 3,109
Larval clusters 31 6 4 2 32 75
Total 2,250 (65.5) 61 (1.8) 35 (1.0) 43 (1.3) 4 (0.1) 1,042 (30.3) 3,435 (100)
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pretiosa (Ferrari-Perez, 1886) (4), Leptotila rufaxilla (Richard and Bernard) (2); Cuculiformes, Cuculidae: Coccyzus melacoryphus Vieillot (1), Piaya cayana L. (3); Piciformes, Bucconidae: Non-nula rubecula (Spix) (8); Ramphastidae: Pteroglossus castanotis (Gould) (1); Picidae: Picumnus albosquamatus DÕOrbigny (19), Veniliornis passerinus (L.) (2), Colaptes melanochloros (Gmelin) (1), Celeus flavescens (Gmelin) (12); Strigiformes, Strigidae: Otus choliba (Vieillot) (1); Tinamiformes, Tinamidae: Crypturellus tataupa (Temminck) (5); Trogoniformes, Trogonidae: Trogon rufus Gmelin (4), Trogon surrucura (Vieillot) (3); Passeriformes, Dendrocolaptidae: Dendrocincla fuliginosa Vieillot (2), Lepidocolaptes fuscus (Vieillot) (2), Xiphocolaptes albicollis (Vieillot) (12); Emberizidae: Coryphospingus cucullatus (Muller) (2), Volatinia jacarina (L.) (2); Formicariidae: Chamaeza campanisona (1), Herpsilochmus atricapillus (Lichtenstein) (3), Pyriglena leucoptera (Vieillot) (21); Furnariidae: Philydor lichtensteini Cabanis and Heine (1), Xenops minutus Sparrman (3), Xenops rutilans Temminck (5); Icteridae: Cacicus hemorrhous (L.) (5); Parulidae: Conirostrum speciosum (L.) (1), Parula pitiayumi (Vieillot) (1); Pipridae: Chiroxiphia caudata (Shaw and Nodder) (8), M. manacus (4), Neopelma pallescens (Lafresnaye) (3), Schiffornis virescens (Lafresnaye) (10); Thraupidae: Tachyphonus coronatus (Vieillot) (1); Turdidae: Turdus leucomelas Vieillot (12); Tyrannidae: Corythopis delalandi (Lesson) (64), Euscarthmus meloryphus Wied (3), Hemitriccus orbitatus (Wied) (7), Lathrotriccus euleri (Cabanis) (1), Myiarchus ferox (Gmelin) (3), Myiarchus tyrannulus (Muller) (1), Myiodynastes maculatus (Muller) (1), Myiopagis viridicata (Vieillot) (5), Myiornis auricularis (Vieillot) (15), Pachyramphus polychopterus (Vieillot) (1), Pitangus sulfuratus (L.) (1), Todirostrum plumbeiceps Lafresnaye (1). GenBank nucleotide sequence accession numbers for the partial mitochondrial 16S rDNA sequences obtained in the current study are FJ424399 (A. brasiliense adult), FJ424400 (A. calcaratum adult), FJ424401 (A. longirostre larva), FJ424402 (A. nodosum nymph) FJ424403 (A. nodosum adult), FJ424404 (A. cajennense adult), FJ424405 (A. incisum adult), FJ424406 (A. naponense adult), FJ424407 (A. oblongoguttatum adult), FJ424408 (A. coelebs adult), and FJ424409 (A. ovale larva). Voucher tick specimens collected during this study have been deposited in the tick collection (Colec a˜ o Nacional dos Carrapatos) of the University of Sa˜ o Paulo (accessions 879, 885, 891, and 1171Ð1251). Herein, we provide a series of new host records for Neotropical Amblyomma species, indicating that birds are much more important than currently recognized for the life histories of these ticks. Notably some of the tick species found on birds in the current study have been previously reported to be infected by zoonotic agents, such as Rickettsia rickettsii (the etiological agent of Rocky Mountain spotted fever) in A. cajennense; Rickettsia amblyommii (suspected to be a human pathogen) in A. cajennense, A. coelebs, and A. longirostre; and Rickettsia bellii (unknown pathogenicity) in A. ovale ticks (Labruna 2009). This later tick
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species also has been found infected by Hepatozoon canis, the etiological agent of canine hepatozoonosis in Brazil (Forlano et al. 2005).
Acknowledgments We thank the staff of Institute for Ecological Research, especially Cicero Jose´ da Silva Filho for valuable help during Þeldwork, and Sheila Oliveira de Souza for technical support in DNA sequencing. This work was supported by a grant from Fundac¸ a˜o de Amparo a` Pesquisa do Estado de Sa˜o Paulo (to M.B.L. and scholarship to M.O. and A.U.) and Fundac¸ a˜o de Amparo a` Pesquisa do Estado de Sa˜o Paulo (Academic Career Scholarship to L.J.R., F.F., and M.B.L.).
References Cited Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403Ð 410. Arzua, M., N. da Silva, K. M. Famadas, L. Beati, and D. M. Barros-Battesti. 2003. Amblyomma aureolatum and Ixodes auritulus (Acari: Ixodidae) on birds in southern Brazil, with notes on their ecology. Exp. Appl. Acarol. 31: 238 Ð296. Arzua, M., V. C. Onofrio, and D. M. Barros-Battesti. 2005. Catalogue of the tick collection (Acari: Ixodida) of the Museu de Histo´ ria Natural Capa˜o da Imbuia, Curitiba, Parana´, Brazil. Rev. Bras. Zool. 22: 623Ð 632. Bjoersdorff, A., S. Bergstro¨ m, R. F. Massung, P. D. Haemig, and B. Olsen. 2001. Ehrlichia-infected ticks on migrating birds. J. Med. Entomol. 7: 877Ð 879. Bush, A. O., K. D. Lafferty, J. M. Lotz, and A. W. Shostaka. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. J. Parasitol. 83: 575Ð583. Chesser, R. T. 1994. Migration in South America, an overview of the austral system. Bird Conserv. Int. 4: 91Ð107. Forlano, M., A. Scofield, C. Elisei, K. R. Fernandes, S. A. Ewing, and C. L. Massard. 2005. Diagnosis of Hepatozoon spp. in Amblyomma ovale and its experimental transmission in domestic dogs in Brazil. Vet. Parasitol. 25: 1Ð7. Jones, E. K., C. M. Clifford, J. E. Keirans, and G. M. Kohls. 1972. The ticks of Venezuela (Acarina: Ixodoidea) with a key to the species of Amblyomma in the Western hemisphere. Brigham Young Univ. Sci. Bull. Biol. Ser. 17: 1Ð 40. Labruna, M. B. 2009. Ecology of Rickettsia in South America. Ann. N.Y. Acad. Sci. 1166: 156 Ð166. Labruna, M. B., C. D. de Paula, T. F. Lima, and D. A. Sana. 2002. Ticks (Acari: Ixodidae) on wild animals from the Porto-Primavera hydroelectric power station area, Brazil. Mem. Inst. Oswaldo Cruz 8: 1133Ð1136. Labruna, M. B., T. Whitworth, M. C. Horta, D. H. Bouyer, J. W. McBride, A. Pinter, V. Popov, S. M. Gennari, and D. H. Walker. 2004. Rickettsia species infecting Amblyomma cooperi ticks from an area in the state of Sao Paulo, Brazil, where Brazilian spotted fever is endemic. J. Clin. Microbiol. 42: 90 Ð98. Labruna, M. B., L. F. Sanfilippo, C. Demetrio, A. C. Menezes, A. Pinter, A. A. Guglielmone, and L. F. Silveira. 2007. Ticks collected form birds in the state of Sa˜o Paulo, Brazil. Exp. Appl. Acarol. 43: 147Ð160. Mangold, A. J., M. D. Bargues, and S. Mas-Coma. 1998. Mitochondrial 16S rDNA sequences and phylogenetic relationships of species of Rhipicephalus and other tick genera among Metastriata (Acari: Ixodidae). Parasitol. Res. 84: 478 Ð 484.
September 2009
OGRZEWALSKA ET AL.: TICKS ON BIRDS FROM BRAZIL
Mangold, A. J. 2006. Utilizac¸ a˜o de sequ¨ eˆ ncias de DNA mitochondrial e nuclear na taxonomia de carrapatos, pp. 165Ð174. In D. M. Barros-Battesti, M. Arzua, and G. H. Bechara [eds.], Carrapatos de importaˆncia me´ dico-veterina´ria da Regia˜o Neotropical: Um guia ilustrado para identiÞcac¸ a˜o de espe´ cies. Vox/International Consortium on Ticks and Tick-borne Diseases (ICTTD-3)/Butantan, Sao Paulo, Brazil. Marini, M. A., B. L. Reinert, M. R. Bornschein, J. C. Pinto, and M. A. Pichorim. 1996. Ecological correlates of ectoparasitism on Atlantic Forest birds, Brazil. Ararajuba 4: 93Ð 103. Neves, R. L., A.M.I. Farias, W. R. Telino Junior, M. Arzua, M.C.N. Botelho, and M.C.A. Lima. 2000. Ectoparasitismo em aves silvestres (Passeriformes-Emberizidae) de Mata Atlaˆntica, Igarassu, Pernambuco. Melopsittacus 3: 64 Ð71. Ogrzewalska, M., R. Pacheco, A. Uezu, F. Ferreira, and M. B. Labruna. 2008. Ticks (Acari: Ixodidae) infesting wild birds in an Atlantic Forest area in the state of Sa˜o Paulo, Brazil, with isolation of Rickettsia from the tick Amblyomma longirostre. J. Med. Entomol. 45: 770 Ð774. Oliveira, P. R., L.M.F. Borges, C.M.L. Lopes, and R. C. Leite. 2000. Population dynamics of the free-living stages of
1229
Amblyomma cajennense (Fabricius, 1787) (Acari: Ixodidae) on pastures of Pedro Leopoldo, Minas Gerais State, Brazil. Vet. Parasitol. 92: 295Ð301. Olsen, B., T.G.T. Jaenson, and S. Bergstro¨ m. 1995. Prevalence of Borrelia burgdorferi sensu lato-infected ticks on migrating birds. Appl. Environ. Microbiol. 61: 3082Ð 3087. Ridgely, R. S., and G. Tudor. 1994. The birds of South America. Volume 2. The suboscine passerines. University of Texas Press, Austin, TX. Sangioni, L. A., M. C. Horta, M.C.B. Vianna, S. M. Gennari, R. M. Soares, M.A.M. Galva˜ o, T.T.S. Schumaker, F. Ferreira, O. Vidotto, and M. B. Labruna. 2005. Rickettsial infection in animals and Brazilian spotted fever endemicity. Emerg. Infect. Dis. 11: 265Ð270. Sick, H. 1997. Ornitologia brasileira. Nova Fronteira, Rio de Janeiro, Brazil. Venzal, J. M., M. L. Fe´lix, A. Olmos, A. J. Mangold, and A. A. Guglielmone. 2005. A collection of ticks (Ixodidae) from wild birds in Uruguay. Exp. Appl. Acarol. 36: 325Ð 331. Received 15 February 2009; accepted 15 May 2009.
