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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.

INTRODUCTION

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.

CONCLUSION

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.

http://dx.doi.org/10.1590/0103-8478cr20161Q52

ACKNOWLEDGMENTS

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).

REFERENCES

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LABRUNA, M.B. et al. Redescription of the female, description of the male, and several new records of Amblyomma parkeri (Acari: Ixodidae), a South American tick species. Experimental and Applied Acarology, v.49, n.3, p.243-260, 2009. Available from: <http://link.springer.com/article/10.1007%2Fs10493-009-9257-z>. Accessed: Dec. 25, 2015.

LAVINA, M.S. et al. Ixodids in wild animals of the mountainous plateau Region of Santa Catarina State, Brazil. Semina Ciencias Agrarias, v.36, n.5, p.3173-3180, 2015. Available from: <http://www.uel.br/revistas/uel/index.php/semagrarias/article/ viewFile/19119/17169>. Accessed: Dec. 25, 2015.

MARTINS, J.R. et al. First record of Amblyomma aureolatum (Pallas, 1772) (Acari: Ixodidae) parasitizing Alouatta guariba (Humboldt, 1812) (Primata: Atelidae) in Southern Brazil. Revista Brasileira de Parasitologia Veteterinaria, v. 15, p.203-205, 2006. Available from: <http://www.cbpv. org.br/rbpv/documentos/1542006/c 154203_2 05.pdf>. Accessed: Dec. 15, 2015.

MARTINS, T.F. et al. Nymphs of the genus Amblyomma (Acari: Ixodidae) of Brazil: descriptions, redescriptions, and identification key. Ticks and Tick-borne Diseases, v.1, n.2, p.75-99, 2010. Available from: <http://dx.doi.org/10.1016/jzttbdis.2010.03.002>. Accessed: May 26, 2016.

MARTINS, T.F. et al. Ticks on free-living wild mammals in Emas National Park, Goias State, central Brazil. Systematic and Applied Acarology, v.16, n.3, p.201-206, 2011. Available from: <http://dx.doi.org/10.11158/saa.16.3.2>. Accessed: May 26, 2016.

MARTINS, T.F. et al. Morphological description of the nymphal stage of Amblyomma geayi and new nymphal records of Amblyomma parkeri. Ticks and Tick-borne Diseases, v.4, n.3, p.181-184, 2013. Available from: <http://dx.doi.org/10.1016/j. ttbdis.2012.11.015>. Accessed: May 26, 2016.

MARTINS, T.F. et al. Ocorrencia de carrapatos em animais silvestres recebidos e atendidos pelo Parque Zoologico Municipal Quinzinho de Barros, Sorocaba, Sao Paulo, Brasil. Brazilian Journal of Veterinary Research and Animal Science, v.52, n.4, p.319-324, 2015. Available from: <http://dx.doi.org/10.11606/ issn.1678-4456.v52i4p319-324>. Accessed: May 26, 2016.

MARTINS, T.F. et al. Geographical distribution of Amblyomma cajennense (sensu lato) ticks (Parasitiformes: Ixodidae) in Brazil, with description of the nymph of A. cajennense (sensu stricto). Parasites and Vectors, v.9, n.186, p.1-14, 2016. Available from: <http://parasitesandvectors.biomedcentral.com/articles/10.1186/ s13071-016-1460-2>. Accessed: May 26, 2016.

MEDIANNIKOV, O.; FENOLLAR, F. Looking in ticks for human bacterial pathogens. Microbial Pathogenesis, v.77, p.142-148, 2014. Available from: <http://dx.doi.org/10.1016/j. micpath.2014.09.008>. Accessed: Nov. 02, 2016.

MILANELO, L.; FITORRA, L.S. Centro de recuperacao de animais silvestres "Orlando Vilas Boas"--Parque Ecologico do Tiete (CRAS-PET-DAEE). Centros de Triagem e Areas de Soltura de Animais Silvestres no Estado de Sao Paulo.

Sao Paulo: Revista CETAS e ASMs no Estado de Sao Paulo Relatorio de Atividades 2012, Superintendencia do IBAMA no Estado de Sao Paulo, Ministerio do Meio Ambiente, 2012. p.23-27. Available from: <http://www.ceo.org.br/campanhas/soltura/ Revista%20IBAMA%20CETAS%20e%20ASMS%204%20 -%202012.pdf>. Accessed: Nov. 03, 2016.

NAVA, S. et al. Hosts, distribution and genetic divergence (16S rDNA) of Amblyomma dubitatum (Acari: Ixodidae). Experimental and Applied Acarology, v.51, n.4, p.335-351, 2010. Available from: <http://link.springer.com/article/10.1007% 2Fs10493-009-9331-6>. Accessed: Nov. 14, 2016.

PEREIRA, M.C. et al. Ticks (Acari: Ixodidae) associated with wild animals in the Pantanal region of Brazil. Journal of Medical Entomology, v.37, n.6, p.979-983, 2000. Available from: <http://dx.doi.org/10.1603/0022-2585 37.6.979>. Accessed: June 16, 2016.

SANGIONI, L.A. et al. Rickettsial infection in animals and Brazilian spotted fever endemicity. Emerging Infectious Diseases, v.11, n.2, p.265-270, 2005. Available from: <https:// www.ncbi.nlm.nih.gov/pmc/articles/PMC3320454/pdf/04-0656. pdf>. Accessed: July 01, 2016.

SARAIVA, D.G. et al. Ticks (Acari: Ixodidae) associated with small terrestrial mammals in the state of Minas Gerais, southeastern Brazil. Experimental and Applied Acarology, v.58, n.2, p.159-166, 2012. Available from: <http://link.springer.com/article/10.10 07%2Fs10493-012-9570-9>. Accessed: Jan. 19, 2016.

SOARES, H.S. et al. Ticks and rickettsial infection in the wildlife of two regions of the Brazilian Amazon. Experimental and Applied Acarology, v.61, n.1, p.125-140, 2015. Available from: <http:// link.springer.com/article/10.1007%2Fs10493-014-9851-6>. Accessed: Jan. 14, 2016.

SPOLIDORIO, M.G. et al. Rickettsial infection in ticks collected from road-killed wild animals in Rio de Janeiro, Brazil. Journal of Medical Entomology, v.49, n.6, p.1510-1514, 2012. Available from: <http://dx.doi.org/10.1603/ME12089>. Accessed: Sept. 26, 2016.

TEIXEIRA, R.H.F. et al. Ixodideos coletados parasitando animais selvagens no Zoologico de Sorocaba, Estado de Sao Paulo, Brasil.

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WITTER, R. et al. Rickettsial infection in ticks (Acari: Ixodidae) of wild animals in midwestern Brazil. Ticks and Tick-borne Diseases, v.7, n.3, p.415-423, 2016. Available from: <http://dx.doi. org/10.1016/j.ttbdis.2015.12.019>. Accessed: Nov. 06, 2016.

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: thiagodogo@hotmail.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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Title Annotation:PARASITOLOGY
Author:Martins, Thiago Fernandes; Milanelo, Liliane; Krawczak, Felipe da Silva; Furuya, Haroldo Ryoiti; Fit
Publication:Ciencia Rural
Article Type:Ensayo
Date:May 1, 2017
Words:3777
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