Diversity of ticks in the wildlife screening center of Sao Paulo city, Brazil/Diversidade de carrapatos no centro de triagem de animais silvestres na cidade de Sao Paulo, Brasil.
Ticks are arthropods of the Ixodida order and Acarina subclass, comprising ectoparasites that are highly specialized in hematophagy. Different species of mammals, birds, reptiles, and amphibians serve as hosts feeding stages of ticks, namely larvae, nymphs, and adults. Ticks are considered the second largest group of vectors of human diseases, behind only mosquitoes, and the most important vectors of pathogens to wild and domestic animals (MEDIANNIKOV & FENOLLAR, 2014).
The Wildlife Recovery Center (CRAS) of the Tiete Ecological Park (PET) of the Water and Electric Power Department (DAEE) is a Wildlife Screening Center (CETAS) class "A", according to IBAMA's 169th normative instruction from February 20th, 2008. The CETAS receives wild animals from illegal wildlife trade, from apprehensions made by the Environmental Military Police, Brazilian Institute of the Environment and Renewable Natural Resources (IBAMA), Civilian, Municipal and Federal Police inspections; those rescued by the City Hall, Fire Departments, Urban Parks, Private Companies or even those brought by common citizens. Since CETAS's opening, CRAS has received more than 72 thousand wild animals, on average birds represent 84% of the animals received; mammals 5% and reptiles 11%, adding up to 520 species (MILANELO & FITORRA, 2012).
Due to the importance of knowledge of ticks fauna and the parasite-host relation in wild animals and the pathogens transmitted by ticks that parasite the Brazilian wild fauna, the aim of the present study was to analyze the ixodid fauna biodiversity and rickettsial infection in these same ticks coming from the animals received and treated at PET's CETAS.
MATERIALS AND METHODS
A total of 96 wild animals were received by the PET during the period from March 2003 to November 2016. Animals were rescued in 28 different municipalities, including Sao Paulo city and nearby municipalities (Table 1 and 2). Sampled animals belonged to different age groups and genders, and were identified by the PET's veterinarians and biologists. Animals comprised 21 bird and 75 mammals specimens (Table 1 and 2).
During the treatment at the PET's Veterinarian Hospital of those animals received at the CETAS, in every inspection the ticks reported on the animals were collected and forwarded alive in 70% alcohol to the Parasitic Disease Laboratory of the Faculty of Veterinary Medicine and Animal Science of University of Sao Paulo (FMVZ-USP). Some engorged immature ticks were placed in B.O.D incubators for ecdysis, as detailed elsewhere (LABRUNA et al., 2002). Ticks were taxonomically identified according to current taxonomic literature (BARROS-BATTESTI et al., 2006; MARTINS et al., 2010, 2016). Voucher specimens were deposited in the tick collection "Colecao Nacional de Carrapatos Danilo Goncalves Saraiva" (CNC) of the FMVZ-USP (Table 1 and 2).
Some tick specimens (n=67, Table 2) had their DNA extracted by the guanidine isothiocyanate method (SANGIONI et al., 2005) and tested for rickettsiae by a Taqman Real-Time PCR (qPCR) targeting the citrate synthase gene (gltA) of the genus Rickettsia, according to LABRUNA et al. (2004b). This protocol uses a pair of primers (CS5 e CS6) that amplify a 147 nucleotide fragment of the rickettsial gltA gene, combined with an internal fluorogenic probe (5' 6-FAM-BHQ-1 3') of 23 nucleotides. This protocol has shown to be sensitive to the detection of one single gene copy of spotted fever group Rickettsia spp. (LABRUNA et al., 2004b). To ensure the viability of the extracted DNA, all samples that were analyzed by the qPCR for molecular detection of rickettsiae were also tested by a conventional PCR targeting a 460-bp fragment of the tick 16S mitochondrial rDNA gene (BLACK & PIESMAN, 1994).
RESULTS AND DISCUSSION
A total of 936 tick specimens (58 larvae, 303 nymphs, 319 males and 256 females) were collected from 96 sampled wild animals, comprising 16 bird and 18 mammal species. Overall, 936 tick specimens were collected and identified to 12 distinct ixodid species (Table 1 and 2).
No rickettsial DNA was detected in any of the 67 tick specimens that were tested by qPCR targeting the gltA gene (Table 2). These same ticks yielded visible amplicons by the PCR protocol targeting the mitochondrial 16S rDNA, validating our DNA extraction protocol.
While the majority of tick-host species associations reported in this study has been previously described in the literature (BARROS & BAGGIO, 1992; PEREIRA et al., 2000; ARZUA et al., 2005; LABRUNA et al., 2005, 2009; MARTINS et al., 2006; MARTINS et al., 2011, 2013, 2015, 2016; SARAIVA et al., 2012; LAVINA et al., 2015; TEIXEIRA et al., 2017), the present study records for the first time in Brazil, the parasitism of Amblyomma longirostre larva and nymph on Asio clamator, and nymphs on Megascops choliba and Pyroderus scutatus, in addition to a nymphal record of Amblyomma sculptum on Caprimulgus parvulus, A. clamator, Buteo brachyurus, Coragyps atratus, Amazona aestiva, and Aramus guarauna in the country.
We reported a nymph of A. sculptum (molted to a male in the laboratory) in Tyto furcata in the municipality of Guarulhos. While there is one previous report of A. sculptum (published as Amblyomma cajennense) parasitizing T. furcata (published as Tyto alba) at the Belo Horizonte CETAS, Minas Gerais State (ANDERY et al., 2013), these authors did not specify the tick stage that was collected. Noteworthy, A. sculptum is the main vector of Rickettsia rickettsii in Brazil (MARTINS et al., 2016).
Even though Amblyomma parkeri has been stated parasitizing various species of birds and mammals in the Brazilian territory (LABRUNA et al., 2009; MARTINS et al., 2013), we demonstrated in this research for the first time the occurrence of A. parkeri nymphs on Penelope obscura, and Callicebus nigrifrons, and adult on Nasua nasua.
Still unprecedentedly, we reported nymphs of Amblyomma dubitatum on Sphiggurus villosus in the Brazilian territory, corroborating with previous reports that rodents are the main hosts for all stages of this tick species (LABRUNA et al., 2004a; NAVA et al., 2010). Additionally, the present study reported for the first time a nymph of A. dubitatum on Alouatta guariba.
While LABRUNA et al. (2005) reported Amblyomma aureolatum as one of the most common tick species of wild carnivores in Brazil, we reported an A. aureolatum female on Bradypus variegatus in the municipality of Mogi das Cruzes. Such unusual record has been previously reported by GUGLIELMONE et al. (2003), who recorded two A. aureolatum females on Bradypus spp. sloths.
This research does not reported the presence of rickettsiae in the analyzed tick specimens, it is unequivocally accepted that there has been an increase of reports of rickettsiae in ticks from wild animals during recent years in Brazil (SPOLIDORIO et al., 2012; SOARES et al., 2015; ACOSTA et al., 2016; WITTER et al., 2016). The proportion of undiagnosed diseases, especially inland, may suggest that there are even more rickettsiae associated to ticks in the national territory.
The present study contributed with important data to the ixodid fauna of wild animals in Brazil as well as on the parasite-host interface, bringing various unpublished records of ectoparasitism of ticks on wild animals in the country. These data may contribute to a more comprehensive knowledge in the biology and behavior of these arthropods in relation to their hosts in the Brazilian territory.
The authors thank Alberto A. Guglielmone (INTA, Rafaela, Argentina) for providing data from his extensive archives of ticks from the Neotropical region. The present work has received financial support from the Fundacao de Amparo a Pesquisa do Estado de Sao Paulo (FAPESP) and Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq).
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Thiago Fernandes Martins (1) * Liliane Milanelo (2) Felipe da Silva Krawczak (1) Haroldo Ryoiti Furuya (2) Lilian Sayuri Fitorra (2) Fabio Toledo das Dores (2) Valeria da Silva Pedro (2) Alicia Giollo Hippolito (2) Marcelo Bahia Labruna (1)
(1) Departamento de Medicina Veterinaria Preventiva e Saude Animal, Faculdade de Medicina Veterinaria e Zootecnia, Universidade de Sao Paulo (USP), Av. Prof. Orlando Marques de Paiva, 87, 05508-000, Sao Paulo, SP, Brasil. E-mail: email@example.com. * Corresponding author.
(2) Departamento de Aguas e Energia Eletrica, Centro de Triagem de Animais Silvestres (CETAS), Parque Ecologico do Tiete, Sao Paulo, SP, Brasil.
Table 1--Ticks collected from wild birds and mammals received and treated by the Wildlife Screening Center in Sao Paulo city, Brazil, from March 2003 to November 2016. Hosts+ Municipality Dates Birds Tyto furcata Guarulhos III-2003 Saltator similis Sao Paulo VIII-2010 S. similis Diadema X-2015 S. similis Sao Paulo VI-2015 Celeus flavescens Mogi das Cruzes XI-2012 Caprimulgus Sao Paulo IX-2012 parvulus Megascops choliba Sao Paulo II-2014 Penelope obscura Sao Paulo X-2013 Asio clamator Sao Paulo VII-2014 A. clamator Guarulhos VIII 2016 A. clamator (2) Sao Paulo XI-2016 Buteo brachyurus Rio Grande IX-2016 da Serra Cariama cristata Cacapava IX-2010 Crotophaga ani Guarulhos VII-2016 Carcara plancus Guararema IX 2014 Tachyphonus Suzano V-2015 coronatus Pyroderus scutatus Osasco XII-2015 Aramus guarauna Sao Paulo XI-2016 Coragyps atratus Sao Paulo VI-2013 Amazona aestiva Sao Paulo X-2016 Mammals Didelphis aurita Guarulhos IX-2005 D. aurita (3) Sao Paulo IX-2005; XI 2013 D. aurita Embu das Artes XI-2013 D. aurita Francisco Morato XI-2016 Alouatta guariba Sao Paulo I-2014 A. guariba Mairipora I-2014 A. guariba (2) Itapecerica IX-2013 da Serra A. guariba (2) Sao Paulo X, XII-2015 Callicebus Nazare Paulista VII-2013 nigrifrons Bradypus Bertioga XII-2010 variegatus B. variegatus (2) Mogi das Cruzes XII-2010 B. variegatus Itapecerica IV-2016 da Serra B. variegatus Atibaia XI-2016 B. variegatus Mogi das Cruzes VIII-2015 Tamandua Registro VII-2016 tetradactyla T. tetradactyla Pariquera-Acu IV-2015 Dasypus Sao Paulo I-2013 novemcinctus Hosts+ Ticks Accession number Birds Tyto furcata 1N[phi] Amblyomma CNC-797 sculptum Saltator similis 1L Amblyomma sp. CNC-2419 S. similis 2N Amblyomma CNC-3421 longirostre S. similis 1N A. longirostre CNC-3422 Celeus flavescens 1N A. longirostre CNC-2420 Caprimulgus 1N A. sculptum CNC-2485 parvulus Megascops choliba 1N A. longirostre CNC-2736 Penelope obscura 1N Amblyomma parkeri CNC-2737 Asio clamator 11L[o] A. longirostre; CNC-2822 9L Amblyomma sp. A. clamator 1N A. longirostre; CNC-3401 3N A. sculptum A. clamator (2) 13N A. sculptum CNC-3423 Buteo brachyurus 5N A. sculptum CNC-3402 Cariama cristata 35N A. sculptum; 5L CNC-3424 Amblyomma sp. Crotophaga ani 2L Amblyomma sp. CNC-3425 Carcara plancus 5N A. sculptum; 1L CNC-3426 Amblyomma sp. Tachyphonus 3L Amblyomma sp. CNC-3427 coronatus Pyroderus scutatus 2N A. longirostre CNC-3428 Aramus guarauna 2N A. sculptum CNC-3429 Coragyps atratus 1N A. sculptum CNC-3430 Amazona aestiva 2N A. sculptum CNC-3431 Mammals Didelphis aurita 1F Ixodes loricatus CNC-921 D. aurita (3) 1M, 5F I. loricatus CNC-922, 923, 2734 D. aurita 1F I. loricatus CNC-2433 D. aurita 1F I. loricatus CNC-3432 Alouatta guariba 1F Amblyomma CNC-2738 aureolatum; 1N A. sculptum A. guariba 2N A. parkeri CNC-2739 A. guariba (2) 1M, 3F A. aureolatum; CNC-3433 1N A. sculptum 1N Amblyomma dubitatum; A. guariba (2) 1M, 24N A. sculptum; 1L CNC-3434 Amblyomma sp. Callicebus 3N A. parkeri CNC-3435 nigrifrons CNC-1777 Bradypus 1F Amblyomma varium variegatus B. variegatus (2) 1F A. aureolatum; CNC-2437 1M, 2F A. varium B. variegatus 2M A. varium CNC-3436 B. variegatus 2M A. varium CNC-3437 B. variegatus 6M, 2F A. varium CNC-3438 Tamandua 1F Amblyomma CNC-3439 tetradactyla calcaratum T. tetradactyla 6F A. calcaratum CNC-3440 Dasypus 1F A. sculptum CNC-2424 Novemcinctus M: male; F: female; L: larva; N: nymph. + One specimen of each animal species, except when stated in parenthesis. [phi] This tick was collected as an engorged nymph, which molted to adult in the laboratory. [o] These ticks were collected as engorged larvae, which molted to nymphs in the laboratory. CNC: Tick collection "Colecao Nacional de Carrapatos Danilo Goncalves Saraiva" of the Faculty of Veterinary Medicine and Animal Science of the University of Sao Paulo. Table 2--Ticks collected from wild mammals received and treated by the Wildlife Screening Center in Sao Paulo city, Brazil, from March 2003 to November 2016. Hosts+ Municipality Dates Mammals Leopardus pardalis Salesopolis IX-2012 Leopardus guttulus Biritiba Mirim III-2013 Eira barbara Sao Bernardo IV-2007 do Campo Cerdocyon thous Mogi das Cruzes X-2012 C. thous Sao Paulo V-2013 Nasua nasua (4) Sao Paulo IX-2012; VI, X-2013 N. nasua (8) Sao Paulo V, VIII, X-2013; X-2015; VII-2016 Sphiggurus Sao Paulo III-2003; villosus (3) IX-2012; I-2014 S. villosus Itaquaquecetuba VIII-2010 S. villosus Poa II-2011 S. villosus Caieiras VIII-2006 S. villosus (3) Mogi das Cruzes IX-2012; I-2014 S. villosus Sao Paulo X-2013 Guerlinguetus Sao Paulo IV-2015 ingrami Tapirus Sao Paulo II-2010; terrestris (2) VI-2012 Pecari tajacu Sete Barras II-2013 P. tajacu (2) Sao Paulo I, II-2015 Mazama Mogi das Cruzes V-2012; II, gouazoubira (3) IX-2013 M. gouazoubira Sao Paulo XII-2013 M. gouazoubira Osasco I-2014 M. gouazoubira Juquia V-2015 Myocastor coypus Mogi das Cruzes VIII-2016 Hydrochoerus Sao Paulo VII-2005; hydrochaeris (6) XII-2012; VI, XI-2013 H. hydrochaeris Itaquaquecetuba I-2014 H. hydrochaeris (2) Guarulhos VII, X-2013 H. hydrochaeris Sao Paulo IX-2013 H. hydrochaeris (2) Cubatao IX-2013 H. hydrochaeris Mogi das Cruzes XI-2016 Hosts+ Ticks Accession number Mammals Leopardus pardalis 2F+2F* Amblyomma CNC-2421 aureolatum Leopardus guttulus 1F A. aureolatum CNC-2422 Eira barbara 1M+2M*, 1F+3F* CNC-2425 Amblyomma ovale Cerdocyon thous 2M+7M*, 2F A. aureolatum; CNC-2426 2N Amblyomma sculptum C. thous 1F A. aureolatum CNC-2486 5N Amblyomma CNC-2431, brasiliense; 1M 2484, 2735 Nasua nasua (4) A. ovale; 1F Amblyomma parkeri; 1F, 3N A. sculptum; 1L Amblyomma sp. N. nasua (8) 1F, 25N A. sculptum; CNC-3441 14L Amblyomma sp. Sphiggurus 4N Amblyomma dubitatum; CNC-761, villosus (3) 4M, 2F Amblyomma 2434, 2741 longirostre; 1L Amblyomma sp. S. villosus 1M A. longirostre CNC-2428 S. villosus 1F A. longirostre CNC-2429 S. villosus 1M A. longirostre CNC-2430 S. villosus (3) 4M, 2F+1F*, CNC-2432, 2740 1N A. longirostre; 1M A. parkeri S. villosus 5M, 1F A. longirostre CNC-3442 Guerlinguetus 12L Amblyomma sp. CNC-3443 ingrami Tapirus 2M, 7F, 1N A. CNC-2423, 2742 terrestris (2) sculptum; 8M, 8F Haemaphysalis juxtakochi Pecari tajacu 118M+15M*, 33F+10F* CNC-2427 A. sculptum P. tajacu (2) 15M, 34F A. sculptum CNC-3444 Mazama 3N A. sculptum; 31M+15M*, CNC-2436, 2745 gouazoubira (3) 15F+12F*, 10N H. juxtakochi M. gouazoubira 2F H. juxtakochi CNC-2743 M. gouazoubira 2N A. sculptum; 1M, 1F H. CNC-2744 juxtakochi; 2F Rhipicephalus microplus M. gouazoubira 1N A. brasiliense CNC-3445 Myocastor coypus 73N A. dubitatum; CNC-3446 7L Amblyomma sp. Hydrochoerus 31M, 23F, 2N A. CNC-2435, hydrochaeris (6) dubitatum; 9M, 2487, 2748 10F A. sculptum; 1L Amblyomma sp. H. hydrochaeris 14M, 11F A. dubitatum; CNC-2746 1F, 1N A. sculptum H. hydrochaeris (2) 6M, 5F, 1N A. dubitatum; CNC-2747 1F, 5N A. sculptum H. hydrochaeris 5F, 36N A. dubitatum -- H. hydrochaeris (2) 7M, 21F, 1N A. dubitatum -- H. hydrochaeris 2M, 5F, 6N A. dubitatum; CNC-3447 1M, 2F, 2N A. sculptum M: male; F: female; L: larva; N: nymph. + One specimen of each animal species, except when stated in parenthesis. * Ticks tested by the PCR. CNC: Tick collection "Colecao Nacional de Carrapatos Danilo Goncalves Saraiva" of the Faculty of Veterinary Medicine and Animal Science of the University of Sao Paulo.
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|Author:||Martins, Thiago Fernandes; Milanelo, Liliane; Krawczak, Felipe da Silva; Furuya, Haroldo Ryoiti; Fit|
|Date:||May 1, 2017|
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