Parasitol Res (2011) 108:665–670 DOI 10.1007/s00436-010-2111-8
ORIGINAL PAPER
Ticks (Acari: Ixodidae) infesting wild birds in the Atlantic Forest in northeastern Brazil, with notes on rickettsial infection in ticks Maria Ogrzewalska & Alexandre Uezu & Marcelo B. Labruna
Received: 16 September 2010 / Accepted: 30 September 2010 / Published online: 16 October 2010 # Springer-Verlag 2010
Abstract A total of 232 individuals representing 46 species of birds were mist-netted and screened for ticks in a region of the Atlantic Forest, State of Bahia, Brazil. Thirty-eight (16.4%) of these birds representing 17 species were found infested by immature stages of Amblyomma ticks, namely, Amblyomma longirostre (Koch, 1844) (15 larvae and seven nymphs), Amblyomma nodosum (Neumann, 1899) (nine nymphs), Amblyomma calcaratum (Neumann, 1899) (five nymphs), Amblyomma cajennense (Fabricius, 1787) (seven larvae), and Amblyomma parkeri (Fonseca and Aragão, 1952) (four larvae). Overall, 21 larvae and five nymphs collected from birds could not be identified to species and were morphologically identified as Amblyomma spp. Among 13 A. longirostre larvae and two A. parkeri larvae, two individuals of A. longirostre (15.4%) were found infected by Rickettsia amblyommii. This study provides some bird species found infested by A. longirostre, A. parkeri, A. calcaratum, A. nodosum, or A. cajennense for the first time and expands the distribution of R. amblyommiiinfected A. longirostre ticks.
M. Ogrzewalska (*) : M. B. Labruna Departamento de Medicina Veterinaria Preventiva e Saude Animal, Faculdade de Medicina Veterinaria e Zootenia, Universidade de São Paulo, São Paulo, Av. Prof. Dr. Orlando Marques de Paiva 87, São Paulo, São Paulo 05508-270, Brazil e-mail:
[email protected] A. Uezu Instituto de Pesquisas Ecológicas (IPÊ), Rod. Dom Pedro I, km 47, Nazaré Paulista, São Paulo 12960-000, Brazil
Introduction Wild birds are important to public health because they can carry zoonotic pathogens, either as a reservoir host or by dispersing infected arthropod vectors including ticks (Hoogstraal 1961). Moreover, bird migration may provide a mechanism for the establishment of new endemic foci of disease at great distances from where an infection was acquired (Elfving et al. 2010; Hildebrandt et al. 2010; Smith et al. 1996). Bacteria of the genus Rickettsia are obligate intracellular organisms that infect invertebrate hosts (Raoult and Roux 1997). Some of the known Rickettsia species are capable of causing diseases in humans, to whom they are transmitted by hematophagous vectors, namely, ticks, mites, fleas, and lice (Raoult and Roux 1997). In Brazil, the Atlantic Forest bioma stands out as a biodiversity hotspot for its high species richness and high level of species endemism (Myers et al. 2000). However, the ixodid tick fauna parasitizing wild birds is poorly studied, and the role of birds in maintaining pathogens is not clear. The present study evaluated tick infestations on wild birds in a region of the Atlantic Forest, state of Bahia, northeastern Brazil. In addition, we tested part of these ticks for rickettsial infection.
Materials and methods Bird capture was conducted in the Serra do Condurú State Park, located among Ilhéus, Itacaré, and Uruçuca Municipalities in the state of Bahia, northeastern Brazil. (Central Point UTM/SAD69, Zone 24S, x-485192, y-8397685). The Park is an Integral Protection Conservation Unit of the Atlantic Forest Biosphere Reserve and encompasses an area
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of about 10,000 ha. The Park is composed of a mosaic of forest patches in different stages of development (Piotto et al. 2009). Flora and fauna of the park are very rich and shelter many endemic species. Despite its conservation importance, the park suffers from timber extraction and hunting. Two bird captures were performed between 16 and 21 May, and between 14 and 18 June 2009. For this purpose, 20 mist nets (12 m long×2 m wide, 36 mm mesh) were displayed along human and animal trails within three forest areas (two work-days per area). In each area, mist nets were left open from 6:00 a.m. to 5:00 p.m. in the first day and from 6:00 a.m. to 12:00 p.m. on the second day. Mist nets were checked approximately every 40 min; captured birds were identified to species according to Sigrist (2007) and examined for the presence of ticks by checking their whole body. All ticks found attached to birds were removed with forceps. Before releasing captured birds, they were marked by cutting head feathers in order to verify any recapture, which was not considered in the counting. Fully engorged ticks (larvae and nymphs) removed from birds were placed in plastic vials containing several grass leaves and covered by a cork containing several minute holes to keep ticks alive until arriving at the laboratory. In the laboratory, engorged ticks were placed in an incubator at 25°C and RH 90% to allow them to molt to nymphs or adults. Each nymph or adult specimen obtained from an engorged larvae or nymph, respectively, was used for taxonomic identification (Barros-Battesti et al. 2006; Martins et al. 2010). Either non-engorged or partially engorged larvae collected from birds were immediately preserved in absolute isopropanol. For the identification of these larvae, we used molecular tools as described elsewhere (Ogrzewalska et al. 2009). Briefly, each tick was submitted to DNA extraction and to polymerase chain reaction (PCR) using primers that amplify a ≈460-bp of the tick mitochondrial rDNA gene (Mangold et al. 1998). Amplified products were purified and DNA sequenced as previously described (Labruna et al. 2004a) and compared with NCBI Nucleotide BLAST searches (Altschul et al. 1990). Prevalence of ticks on birds and mean intensity of the tick infestations on each bird species were calculated; prevalence is the number of infested birds/number of examined birds×100 within each bird species, and mean intensity is total number of ticks/number of infested birds within each bird species. Some of the ticks identified to the species level were individually tested for the presence of Rickettsia by PCR using primers CS-78 and CS-323, which target a 401-bp fragment of the gltA gene that occurs in all Rickettsia species (Labruna et al. 2004a), and primers Rr190.70F and Rr190.602R targeting a fragment of 532 bp of the ompA
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gene present only in Rickettsia species belonging to the spotted fever group (SFG; Regnery et al. 1991). PCR products were DNA sequenced and submitted to BLAST analysis to determine similarities to other Rickettsia species (Altschul et al. 1990).
Results A total of 232 birds were captured, representing 46 species. Overall, 38 (16.4%) birds representing 17 species were parasitized by immature forms of Amblyomma ticks. Overall, tick prevalence was 17.1% (20/117) and 15.6% (18/115) in May and June, respectively. Five species of ticks were recovered from birds during this study: Amblyomma longirostre (Koch, 1844) (15 larvae and seven nymphs), Amblyomma nodosum (Neumann, 1899) (nine nymphs), Amblyomma calcaratum (Neumann, 1899) (five nymphs), Amblyomma cajennense (Fabricius, 1787) (seven larvae), and Amblyomma parkeri (Fonseca and Aragão, 1952) (four larvae). Three engorged nymphs that molted to adults in the laboratory were identified to species level through adult morphology (Barros-Battesti et al. 2006). Eleven engorged larvae that molted to nymphs plus 18 unengorged nymphs collected directly from birds were identified to species according to nymphal morphology (Martins et al. 2010). The remaining immature larvae were identified through molecular methods. However, larvae that died before reaching the nymphal stage or larvae that did not generate high quality DNA sequence or nymphs that were partially damaged were identified morphologically as Amblyomma sp. (21 larvae and five nymphs). All bird species parasitized by ticks are presented in Table 1. Individual infestations usually consisted of few ticks, with mean intensity values equal or lower than two ticks/bird at most of the times. No ticks were found on the following bird species (number of individuals in parentheses): Apodiformes, Trochilidae: Florisuga fusca (Vieillot, 1817) (1); Glaucis dohrnii (Bourcier and Mulsant, 1852) (7); Glaucis hirsutus (Gmelin, 1788) (1); Phaethornis idaliae (Bourcier and Mulsant, 1856) (1); Phaethornis margarettae (Ruschi, 1972) (2); Columbiformes, Columbidae: Claravis pretiosa (Ferrari-Perez, 1886) (1); Falconiformes, Falconidae: Micrastur ruficollis (Vieillot, 1817) (2); Passeriformes, Cotingidae: Lipaugus vociferans (Wied, 1820) (2); Dendrocolaptidae: Xiphorhynchus fuscus (Vieillot, 1818) (2); Xiphorhynchus picus (Gmelin, 1788) (1); Formicariidae: Formicarius colma (Boddaert, 1783) (1); Fringillidae: Euphonia pectoralis (Latham, 1801) (4); Euphonia violacea (Linnaeus, 1758) (2); Furnariidae: Automolus leucophthalmus (Wied, 1821) (3); Pipridae: Chiroxiphia caudate (Shaw and Nodder, 1793) (5); Machaeropterus
Birds
Ticks
Order
Family
Species
Apodiformes Columbiformes
Trochilidae Columbidae
Thalurania glaucopis Geotrygon violacea
1/4 1/1
25 100
1 10
Passeriformes
Cardinalidae
Saltator maximus
1/1
100
1
Conopophagidae
Conopophaga melanops
3/9
Dendrocolaptidae
Fringillidae Furnariidae
Pipridae
No. infested/No. captured
Prevalence
33.3
Mean intensity
1.6
Dendrocincla turdina Glyphorynchus spirurus
1/4 2/23
25 8.7
7 2
Xiphorhynchus guttatus Euphonia xanthogaster Xenops minutus
1/2 1/1 1/8
50 100 12.5
1 1 3
Dixiphia pipra
6/45
13.3
1.7
Manacus manacus
7/26
26.9
1.3
Thamnophilidae
Drymophila squamata
2/8
25
2
Turdidae
Thamnomanes caesius Turdus leucomelas
3/4 4/11
75 36.3
1 1
Species
No. larvae
A. parkeri A. cajennense Amblyomma sp. A. nodosum
1a 7 3
A. parkeri A. longirostre A. calcaratum Amblyomma sp. Amblyomma sp. A. longirostre Amblyomma sp. A. longirostre A. longirostre A. longirostre A. nodosum Amblyomma sp. A. longirostre A. calcaratum A. nodosum Amblyomma sp. A. longirostre A. calcaratum
1a 1a
A. parkeri Amblyomma sp. A. nodosum Amblyomma sp. A. nodosum A. longirostre A. nodosum Amblyomma sp.
No. nymphs
1
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Table 1 Ticks collected on birds in the Serra do Conduru State Park, State of Bahia, Brazil
2 1 7 3a 1 1 1 1a 1 1 1a
2a 1 1
3 1 1 1 3 2 1 2 1 3
1a 1 2
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1, 4a 2 A. longirostre Amblyomma sp. 3.5
Ticks identified by molecular analysis of partial 16S rDNA gene in the present study a
2/9 Myiobius barbatus
22.2
1 2 3 Amblyomma sp. A. longirostre Amblyomma sp. 1 5 1/1 1/3 Elaenia flavogaster Mionectes oleagineus Tyrannidae
100 33.3
Species Species Family Order
Birds
Table 1 (continued)
No. infested/No. captured
Prevalence
Mean intensity
Ticks
No. larvae
No. nymphs
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regulus (Hahn, 1819) (10); Pipra rubrocapilla Temminck, 1821 (4); Thamnophilidae: Myrmotherula axillaris (Vieillot, 1817) (2); Myrmotherula minor (Salvadori, 1864) (1); Myrmotherula urosticta (Sclater, 1857) (5); Pyriglena leucoptera (Vieillot, 1818) (2); Thamnophilus caerulescens (Vieillot, 1816) (1); Thamnophilus pelzelni (Hellmayr, 1924) (1); Thraupidae: Dacnis cayana (Linnaeus, 1766) (1); Tityridae: Schiffornis turdina (Wied, 1831) (3); Turdidae: Turdus amaurochalinus (Cabanis, 1850) (2); Turdus rufiventris (Vieillot, 1818) (3); Tyrannidae: Leptopogon amaurocephalus (Tschudi, 1846) (1); and Piciformes, Picidae: Picumnus exilis (Lichtenstein, 1823) (1). Among 13 larvae of A. longirostre and two larvae of A. parkeri tested by PCR for rickettsial infection, two individuals (15.4%) of A. longirostre were found infected by Rickettsia amblyommii. The gltA product from these ticks was sequenced and was shown to be identical to each other and 100% (316/316 bp) identical to the corresponding sequence of R. amblyommii strain AL (GenBank accession number EU274654), previously detected in A. longirostre ticks collected from birds in the state of São Paulo (Ogrzewalska et al. 2008). The ompA product of these ticks showed to be 99.8% (487/488 bp) identical to the corresponding sequence of R. amblyommii strain AL (EU274656) and R. amblyommii strain Aranha (AY360213) detected in A. longirostre from the state of Rondônia, Brazil (Labruna et al. 2004c), and 98.9% (483/488 bp) with R. amblyommii (EU544295) from USA. Voucher tick specimens collected during this study have been deposited in the “Coleção Nacional de Carrapatos” (CNC) of the Faculty of Veterinary Medicine, University of São Paulo, São Paulo, Brazil (accession numbers, 1605– 1621). GenBank nucleotide sequence accession numbers are HQ231758 and HQ231759 for the partial sequences of R. amblyommii (ompA and gltA genes, respectively) generated in the present study.
Discussion The present study reports immature stages of five Amblyomma species parasitizing wild birds in a region of the Atlantic Forest, Bahia, northeastern Brazil. The predominant tick species infesting birds was A. longirostre. This tick is widely distributed in the Neotropical region (Guglielmone et al. 2003). Adults of A. longirostre feed primarily on rodent porcupines of the genera Coendou, Chaetomys, and Sphiggurus, whereas subadult stages feed primarily on arboreal passerine birds (Aragão 1936; Labruna et al. 2007a, 2009; Nava et al. 2010; Ogrzewalska et al. 2010; Tolesano-Pascoli et al. 2010). In the present study, we found three additional species being parasitized for the first time by this tick: Conopophaga melanops
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(Vieillot, 1818) (Passeriformes; Conopophagidae), Euphonia xanthogaster (Sundevall, 1834) (Passeriformes; Fringillidae), and Xenops minutus (Sparrman, 1788) (Passeriformes; Furnariidae; Table 1). The tick A. parkeri, so far endemic to southeastern and southern Brazil (Labruna et al. 2009), is reported for the first time in northeastern Brazil. This tick is morphologically and genetically closely related to A. longirostre and Amblyomma geayi (Neumann, 1899) (Labruna et al. 2009). While adults of A. parkeri also parasitize porcupines (Coendou spp. and Sphigurus spp.; Guglielmone et al. 2003; Labruna et al. 2009), there has been only two bird records for immature stages of this tick, which refer to larvae on the Passeriformes T. caerulescens (Vieillot, 1816) (Thamnophilidae) and Trichothraupis melanops (Vieillot, 1818) (Emberezidae) in the state of São Paulo, southeastern Brazil (Ogrzewalska et al. 2008). Here, we add three other species being parasitized for the first time by this tick: Thalurania glaucopis (Gmelin, 1788) (Apodiformes; Trochilidae), C. melanops (Vieillot, 1818) (Passeriformes; Conopophagidae), and Manacus manacus (Linnaeus, 1766) (Passeriformes; Pipridae). These results suggest that A. parkeri is ecologically similar to A. longirostre, with immature ticks feeding primarily on birds. The ticks A. calcaratum, A. nodosum, and A. cajennense have been previously reported on wild birds in other South American biomes (Beldomenico et al. 2003; Labruna et al. 2007a; Ogrzewalska et al. 2009, 2010). Our bird records for these three ticks are all new, except for A. nodosum on Saltator maximus (Statius Muller, 1776) (Passeriformes; Cardinalidae), which was recently reported by TolesanoPascoli et al. (2010) in the state of Minas Gerais, southeastern Brazil. The adult stage of both A. calcaratum and A. nodosum feeds chiefly on anteaters, Tamandua spp. and Myrmecophaga tridactyla L. (Guglielmone et al. 2003), while subadults seem to feed primarily on birds (Labruna et al. 2007a; Ogrzewalska et al. 2009, 2010). A. cajennense is a tick widely distributed in South America parasitizing a wide variety of medium- to large-sized mammals, including humans, and sporadically parasitizing birds with ground feeding habits (Barros-Battesti et al. 2006; Labruna et al. 2007a; Ogrzewalska et al. 2009). Overall, 15.4% A. longirostre ticks were found to be infected by the SFG agent R. amblyommii. Different strains of this Rickettsia have been reported infecting at least five Amblyomma species from the USA to Argentina, including A. longirostre from the state of Rondônia, western Brazilian Amazon, and from the state of São Paulo, southeastern Brazil (Bermúdez et al. 2009; Labruna et al. 2004b, c; Labruna et al. 2007b; Ogrzewalska et al. 2008; Parola et al. 2007; Weller et al. 1998). While R. amblyommii is not currently recognized as human or animal pathogen, there has been serological evidence for human and canine infection by
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this agent in the USA and in the Brazilian western Amazon, respectively (Apperson et al. 2008; Labruna et al. 2007c). In fact, it has been proposed that some of the rickettsiosis cases reported as Rocky Mountain spotted fever (presumably caused by Rickettsia rickettsii) in the USA may have been caused by R. amblyommii (Apperson et al. 2008). In conclusion, this study provides bird species found infested by A. longirostre, A. parkeri, A. calcaratum, A. nodosum, and A. cajennense for the first time and expands the distribution of R. amblyommii-infected A. longirostre ticks. Acknowledgments This work was supported by FAPESP (grant to M.B.L. and scholarship to M.O. and A.U.), CNPq (Academic Career Scholarship to M.B.L.), and IPÊ Institute for Ecological Research.
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