Skip to main content
NCBI home page
Revista Brasileira de Parasitologia Veterinária / Brazilian Journal of Veterinary Parasitology logoLink to Revista Brasileira de Parasitologia Veterinária / Brazilian Journal of Veterinary Parasitology
. 2023 Oct 13;32(4):e008023. doi: 10.1590/S1984-29612023059

Diversity of rickettsiae in ticks (Acari: Ixodidae) collected from wild vertebrates in part of the Amazon, Cerrado, and Pantanal biomes in Brazil

Diversidade de riquétsias em carrapatos (Acari: Ixodidae) coletados de vertebrados silvestres em parte dos biomas Amazônia, Cerrado e Pantanal no Brasil

Anny Carolina Prati 1, Maerle Oliveira Maia 2, Thiago Fernandes Martins 3,4, Thaís Oliveira Morgado 2, Sandra Helena Ramiro Corrêa 2, Edson Junior Figueiredo Mendes 2, Rosa Helena dos Santos Ferraz 2, Jessica Rhaiza Mudrek 5, Christine Strüssmann 5, Dirceu Guilherme de Souza Ramos 6, Thiago Borges Fernandes Semedo 7,8,9, Make Kawatake Minetto 10, Daniel Moura de Aguiar 2, Richard Campos Pacheco 2,11,*, Andréia Lima Tomé Melo 1
PMCID: PMC10704879  PMID: 37851794

Abstract

Ticks parasitizing 102 wild animals in the states of Mato Grosso and Goiás, Brazil were collected between 2015 and 2018. A total of 2338 ticks (865 males, 541 females, 823 nymphs, and 109 larvae) belonging to four genera (Amblyomma, Dermacentor, Haemaphysalis, and Rhipicephalus) and at least 21 species were identified. DNA extraction and a molecular survey for rickettsial agents were performed on 650 ticks. The results revealed parasitism by the following species: Rickettsia amblyommatis in Amblyomma cajennense s.s., A. cajennense s.l., Amblyomma coelebs, Amblyomma humerale, Amblyomma longirostre, Amblyomma nodosum, Amblyomma scalpturatum, Amblyomma sculptum, and Amblyomma romitii; Rickettsia parkeri in Amblyomma nodosum, Amblyomma ovale, Amblyomma scalpturatum, and Amblyomma triste; Rickettsia rhipicephali in Haemaphysalis juxtakochi; Rickettsia sp. in A. cajennense s.s., A. nodosum, and A. sculptum, and lastly, ‘Candidatus Rickettsia andeanae’ in Amblyomma parvum and Rhipicephalus microplus. This study expands the body of knowledge about tick parasitism among wild animals, including new data concerning tick-host associations, and provides information about the epidemiology of tick-borne pathogens in the Center-West region of Brazil.

Keywords: Wildlife, Ixodidae, Rickettsiae, tick-borne diseases

Introduction

Ticks (Acari: Argasidae and Ixodidae) are ectoparasitic arthropods of numerous animal species, while humans are accidental hosts, and one of the most important arthropod vectors of infectious diseases around the world (Anderson & Magnarelli, 2008; Nava et al., 2009; Nogueira et al., 2022). Several studies have focused on ticks and their associations with wildlife in the Central-West region of Brazil (e.g., Aragão, 1936; Aragão & Fonseca, 1961; Szabó et al., 2007; Martins et al., 2011, 2023; Soares et al., 2015; Witter et al., 2016; Colle et al., 2020; Serpa et al., 2021), and an understanding of aspects pertaining both to these ectoparasites and to the infectious agents they can transmit to their hosts during hematophagy is extremely important.

Rickettsiae (Rickettsiales: Rickettsiaceae) are small obligate intracellular gram-negative bacteria that infect invertebrate and vertebrate hosts worldwide with transmission related to ectoparasitic arthropods, mainly ticks (Dumler et al., 2001). Currently, the genus Rickettsia has been classified in the Spotted Fever Group (SFG), the Typhus Group (TG), the Transitional Group (TRG), the Bellii Group (BG), the Canadensis Group (CG), and several other basal groups (Weinert et al., 2009).

In Brazil, the main tick-borne disease is Brazilian Spotted Fever (BSF), caused by the bacterium Rickettsia rickettsii, which is responsible for a high mortality rate among infected humans (Oliveira et al., 2016). This zoonosis is transmitted by the ticks Amblyomma sculptum, the most important vector in Brazil (Labruna, 2009) in many parts of endemic areas in southeastern Brazil, including the states of São Paulo, Rio de Janeiro, Espírito Santo, and Minas Gerais; and Amblyomma aureolatum, a recognized vector within the metropolitan area of São Paulo municipality within the Atlantic rainforest mountain domain (Binder et al., 2021). Furthermore, another pathogenic rickettsial agent, known as Rickettsia parkeri strain Atlantic rainforest (Krawczak et al., 2016), transmitted mainly by adult Amblyomma ovale ticks (Szabó et al., 2013), has been associated with mild cases among humans in Brazil in the States of São Paulo (Spolidorio et al., 2010), Bahia (Silva et al., 2011), and Santa Catarina (Krawczak et al., 2016). Lastly, other species of the genus Rickettsia have been identified in the SFG, namely R. amblyommatis and R. rhipicephali, infecting ticks, but pathogenicity in humans is still unknown (Parola et al., 2013).

Thus, the occurrence of tick species among varied wild hosts in different biomes (Amazon, Cerrado, and Pantanal), where domestic animals and humans also inhabit, considering the importance of ticks and rickettsial diseases for public health, reinforces the need for research focused on this subject. In view of the importance of the tick-host association and research on rickettsial infection in ticks, this investigation focused on the molecular detection of rickettsiae in ticks collected from free-living or captive wild animals in the Central-West region of Brazil.

Materials and Methods

Ticks were collected between 2015 and 2018 from free-living and captive wild animals in the states of Mato Grosso (MT) in part of the Amazon, Cerrado, and Pantanal biomes, and Goiás (GO) in the Cerrado biome, both located in the Central-West region of Brazil (Figure 1). Samples were obtained from road-killed wild animals and from wild animals (n= 94) treated at the Veterinary Hospital of the Federal University of Mato Grosso (UFMT) (Cuiabá, MT), and from wild animals (n= 8) sent to the Wild Animal Screening Center (CETAS) of the Brazilian Institute of Environment and Renewable Natural Resources (IBAMA) in Goiânia, GO (Table 1). Ticks were preserved in isopropyl alcohol for taxonomic identification and DNA extraction. Adult ticks were identified to species level, as described by Barros-Battesti et al. (2006), Martins et al. (2016), and Nava et al. (2018), while Amblyomma and Haemaphysalis nymphs were identified morphologically as specified by Martins et al. (2010, 2016) and Nava et al. (2017), respectively. The larvae of the genus Amblyomma could not be morphologically identified to the species level because there is insufficient literature available, then the larvae were retained as Amblyomma sp. according to Vieira et al. (2004), Barros-Battesti et al. (2006), and Nava et al. (2017). The larva of the genus Dermacentor was identified morphologically as described by Clifford & Anastos (1960), thus, the larva identified in the genus Dermacentor was considered to be D. nitens. Finally, adults of Rhipicephalus linnaei were identified based on Šlapeta et al. (2022). Tick specimens were deposited in the Tick Collection Coleção de Carrapatos da Universidade Federal de Mato Grosso at the Federal University of Mato Grosso, in Cuiabá, MT, under the following accession numbers: LDPP-UFMT/N.124-127; 129; 133; 135-137; 139-140; 142-144; 148-150; 155; 157-158; 160-163; 165-174; 176-179; 181; 185; 187-188; 190-195; 199-200; 203; 210; 214-217; 220; 224-227; 229; 231-239; 242; 244-247; 255-256; 260-266; 270-277; 283; 287-291; 294; 296-297 and 303-306.

Figure 1. Municipalities where the ticks examined in this study were collected between 2015 and 2018 in the states of Mato Grosso (MT): 1. Apiacás; 2. Colniza; 3. Aripuanã; 4. Sinop; 5. Querência; 6. Tangará da Serra; 7. Pontes e Lacerda; 8. Barra do Bugres; 9. Rosário Oeste; 10. Jangada; 11. Chapada dos Guimarães; 12. Cuiabá; 13. Várzea Grande; 14. Nossa Senhora do Livramento; 15. Poconé; 16. Santo Antônio de Leverger; 17. Dom Aquino; 18. Rondonópolis, and Goiás (GO): 19. Mineiros; 20. Serranópolis; 21. Jataí.

Figure 1

Open in a new tab

Table 1. Ticks (M: male; F: female; N: nymph; L: larva) parasitizing free-living (FL) and captive (C) wild animals, collected between 2015 and 2018, in the states of Mato Grosso (MT) and Goiás (GO), in the Central-West region of Brazil.

Hosts (n. of specimens when >1) Origin (Year) Municipality (State) Species (n. of collected ticks)
ORDER CARIAMIFORMES
Cariama cristata (2) FL (2017) Cuiabá (MT) Amblyomma sculptum (4M, 6F, 24N)
ORDER ANURA
Rhinella diptycha (2) FL (2017) Cuiabá (MT) Amblyomma rotundatum (7F, 14N)
R. diptycha (2) FL (2017) Jataí (GO) A. rotundatum (5F)
ORDER TESTUDINES
Chelonoidis carbonarius FL (2016) Cuiabá (MT) A. rotundatum (2F)
Chelonoidis denticulatus FL (2017) Apiacás (MT) Amblyomma cajennense sensu stricto (s.s.) (1F), Amblyomma humerale (9M, 1N), A. rotundatum (1F)
C. denticulatus FL (2017) Cuiabá (MT) A. rotundatum (3F)
Phrynops geoffroanus FL (2016) Cuiabá (MT) A. sculptum (2M, 1F)
ORDER CROCODYLIA
Caiman yacare FL (2015) Cuiabá (MT) Amblyomma dissimile (1M, 2F)
Paleosuchus palpebrosus (2) FL (2016) Cuiabá (MT) A. dissimile (1F), A. rotundatum (1F)
ORDER SQUAMATA
Suborder Sauria
Iguana iguana FL (2015) Cuiabá (MT) A. dissimile (19M, 23F, 8N), Amblyomma sp. (1L)
I. iguana (2) FL (2016) Cuiabá (MT) A. dissimile (7M, 1F)
I. iguana FL (2017) Cuiabá (MT) A. dissimile (2M, 1F)
I. iguana (2) FL (2018) Cuiabá (MT) A. dissimile (17M, 5F, 5N), Amblyomma sp. (2L)
Tupinambis sp. FL (2015) Poconé (MT) A. rotundatum (6N), Amblyomma sp. (4L)
Suborder Serpentes
Boa constrictor FL (2015) Cuiabá (MT) A. dissimile (84M, 50F, 133N)
B. constrictor FL (2017) Jataí (GO) A. rotundatum (3F)
B. constrictor (2) FL (2018) Cuiabá (MT) A. dissimile (5M, 2F)
B. constrictor FL (2018) Poconé (MT) A. dissimile (16M, 5N)
Bothrops mattogrossensis FL (2016) Poconé (MT) A. dissimile (2F)
Eunectes notaeus FL (2015) Poconé (MT) A. dissimile (3M, 2F)
ORDER ARTIODACTYLA
Mazama americana FL (2016) Colniza (MT) A. cajennense s.s. (1F, 22N), Amblyomma oblongoguttatum (1F), Haemaphysalis juxtakochi (3F, 1N)
Subulo gouazoubira FL (2016) Cuiabá (MT) A. sculptum (22Na)
S. gouazoubira FL (2016) Várzea Grande (MT) Rhipicephalus microplus (2F)
S. gouazoubira FL (2016) Cuiabá (MT) R. microplus (2M, 1F)
S. gouazoubira FL (2017) Cuiabá (MT) A. sculptum (5N), R. microplus (19M, 14F, 4N)
S. gouazoubira FL (2018) Cuiabá (MT) Amblyomma parvum (5M), R. microplus (4M, 2F, 2N)
S. gouazoubira FL (2018) Poconé (MT) R. microplus (5M, 2F, 4N)
Tayassu pecari FL (2017) Apiacás (MT) A. cajennense s.s. (2M, 2F), Amblyomma naponense (1F), A. oblongoguttatum (1F), Amblyomma scalpturatum (4N)
ORDER CARNIVORA
Cerdocyon thous FL (2018) Cuiabá (MT) A. ovale (1M, 1F)
C. thous (3) FL (2018) Poconé (MT) Amblyomma ovale (5M), A. sculptum (30N), Amblyomma sp. (8L), R. microplus (1N)
Chrysocyon brachyurus FL (2017) Serranópolis (GO) A. ovale (2F), Dermacentor nitens (1L)
C. brachyurus FL (2018) Serranópolis (GO) A. ovale (1M, 2F), Amblyomma sp. (1L)
Leopardus pardalis FL (2016) Barra do Bugres (MT) Amblyomma oblongoguttatum (1Nb), A. sculptum (3N, 15Lc), Amblyomma sp. (1L)
Nasua nasua FL (2018) Cuiabá (MT) A. ovale (1M), A. sculptum (8N), Amblyomma sp. (7L)
N. nasua FL (2018) Poconé (MT) A. ovale (1M), A. sculptum (37N), Amblyomma sp. (2L)
Procyon cancrivorus FL (2018) Poconé (MT) A. ovale (2F), A. sculptum (3N)
Puma concolor FL (2017) Colniza (MT) A. cajennense s.s. (8N)
P. concolor FL (2017) Tangará da Serra (MT) A. cajennense s.s. (1F), A. cajennense s.l. (1M, 3N), Amblyomma coelebs (1M), A. ovale (1M), Amblyomma sp. (14L), R. microplus (1N)
ORDER CINGULATA
Euphractus sexcinctus FL (2017) Colniza (MT) A. cajennense s.s. (2N), A. coelebs (6N), Amblyomma sp. (3L)
ORDER DIDELPHIMORPHIA
Didelphis marsupialis FL (2017) Aripuanã (MT) A. coelebs (6N), Amblyomma humerale (1N), Amblyomma sp. (16L)
ORDER PERISSODACTYLA
Tapirus terrestris FL (2016) Chapada dos Guimarães (MT) A. coelebs (2F), A. sculpum (39M, 20F, 92Nd)
T. terrestris FL (2016) Dom Aquino (MT) A. coelebs (1M, 3F), A. oblongoguttatum (1M), A. sculptum (23M, 8F, 2N), R. microplus (3F)
T. terrestris FL (2016) Pontes e Lacerda (MT) A. coelebs (1F), A. cajennense s.l. (10M)
T. terrestris FL (2016) Sinop (MT) A. cajennense s.s. (143M, 20F, 14N), A. coelebs (7M, 1F), A. ovale (1M)
T. terrestris FL (2017) Chapada dos Guimarães (MT) A. coelebs (2M), A. sculptum (5M, 13F, 1N)
T. terrestris (3) FL (2017) Colniza (MT) A. cajennense s.s. (2M, 9F, 3N), A. coelebs (3M, 4F), A. oblongoguttatum (1M, 2F),
A. scalpturatum (3M, 14F)
T. terrestris FL (2017) Poconé (MT) A. sculptum (34M, 7F)
T. terrestris (2) FL (2017) Pontes e Lacerda (MT) A. coelebs (13M, 9F, 1N), A. oblongoguttatum (1M, 3F), Amblyomma scalpturatum (39M, 14F), A. cajennense s.l. (29M) A. sculptum (31F, 2N), R. microplus (2F)
T. terrestris FL (2017) Rondonópolis (MT) A. coelebs (4M, 1F), A. ovale (1M), A. triste (5M, 6F), A. sculptum (60M, 12F, 1N),
R. microplus (5F, 1N)
T. terrestris FL (2017) Querência (MT) R. microplus (1M, 6F)
T. terrestris FL (2018) Colniza (MT) A. coelebs (2M), A. cajennense s.s. (1M, 4F, 1N), A. scalpturatum (1F)
ORDER PILOSA
Myrmecophaga tridactyla FL (2015) Cuiabá (MT) Amblyomma nodosum (4M, 5F), A. parvum (1F), A. sculptum (6M, 7F, 54N), Amblyomma sp. (8L)
M. tridactyla FL (2016) Barra do Bugres (MT) A. nodosum (3F), A. sculptum (1N)
M. tridactyla (2) C (2016) Cuiabá (MT) A. sculptum (3M, 1F, 7Ne)
M. tridactyla FL (2016) Mineiros (GO) A. nodosum (4M), A. sculptum (1F)
M. tridactyla FL (2016) Rosário Oeste (MT) A. nodosum (1M, 1F), A. sculptum (8M, 2F, 23Nf)
M. tridactyla FL (2016) Tangará da Serra (MT) A. nodosum (1M, 5F), A. cajennense s.l. (12M, 20Ng), A. cajennense s.s. (3Nh),
A. scalpturatum (2M), A. sculptum (10F, 5Ni)
M. tridactyla FL (2017) Poconé (MT) A. sculptum (7M, 1F)
M. tridactyla FL (2017) Várzea Grande (MT) A. sculptum (3M, 2F, 1N)
M. tridactyla (2) FL (2018) Cuiabá (MT) A. nodosum (2M), A. sculptum (17N), Amblyomma sp. (3L)
M. tridactyla FL (2018) Santo Antônio de Leverger (MT) A. nodosum (4M, 3F), A. sculptum (12N), Amblyomma sp. (8L)
Tamandua tetradactyla FL (2015) Cuiabá (MT) A. nodosum (2M)
T. tetradactyla FL (2016) Cuiabá (MT) A. nodosum (2M)
T. tetradactyla FL (2016) Jangada (MT) A. nodosum (1M, 2F)
T. tetradactyla (2) FL (2016) Mineiros (GO) A. nodosum (10M, 4F)
T. tetradactyla FL (2016) Várzea Grande (MT) A. nodosum (2F)
T. tetradactyla FL (2017) Chapada dos Guimarães (MT) Amblyomma calcaratum (23M), A. coelebs (1N), A. nodosum (1M), A. sculptum (1F),
Amblyomma sp. (7L)
T. tetradactyla FL (2017) Nossa Senhora do Livramento (MT) A. nodosum (4M, 4F), A. sculptum (1F, 1N)
T. tetradactyla (2) FL (2017) Poconé (MT) A. nodosum (4M, 4F), A. sculptum (2M, 2F, 1N)
T. tetradactyla FL (2017) Santo Antônio de Leverger (MT) A. nodosum (8M, 2F)
T. tetradactyla (4) FL (2018) Poconé (MT) A. nodosum (35M, 24F), A. sculptum (3F, 19N)
ORDER RODENTIA
Coendou longicaudatus FL (2015) Chapada dos Guimarães (MT) Amblyomma longirostre (8M, 1F)
Cuniculus paca FL (2015) Cuiabá (MT) A. naponense (2Nj)
Holochilus sciureus FL (2017) Poconé (MT) A. triste (6N)
Hydrochoerus hydrochaeris C (2016) Cuiabá (MT) A. sculptum (7M, 4F)
H. hydrochaeris (2) FL (2016) Cuiabá (MT) Amblyomma dubitatum (2Nl), A. sculptum (1M, 7F, 36Nm)
H. hydrochaeris FL (2016) Várzea Grande (MT) A. dubitatum (1M; 11F, 3Nn), A. sculptum (4M, 12F, 91No), Amblyomma sp. (8L)
H. hydrochaeris FL (2017) Colniza (MT) A. cajennense s.l. (1M), Amblyomma romitii (8M, 12F, 4N)
H. hydrochaeris FL (2017) Cuiabá (MT) A. dubitatum (2N), A. sculptum (7M, 4F, 19N)
H. hydrochaeris FL (2017) Poconé (MT) A. sculptum (2M, 4F, 3N)
H. hydrochaeris FL (2017) Pontes e Lacerda (MT) A. dubitatum (6M, 28F), A. sculptum (2N)
H. hydrochaeris FL (2017) Várzea Grande (MT) A. dubitatum (1M, 3F), A. sculptum (6M, 4F), Rhipicephalus linnaei (15M, 7F)
Open in a new tab
a

Reared from nymphs (n= 22) at the laboratory conditions which molted to the adult stage (n= 11 males, 11 females);

b

Reared from nymph (n= 1) at the laboratory conditions which molted to the adult stage (n= 1 male);

c

Reared from larvae (n= 15) at the laboratory conditions which molted to the nymph stage (n= 15), thus identified at species level;

d

Reared from nymphs (n= 30) at the laboratory conditions which molted to the adult stage (n= 11M, 19F);

e

Reared from nymphs (n= 6) at the laboratory conditions which molted to the adult stage (n= 2 males, 4 females);

f

Reared from nymphs (n= 23) at the laboratory conditions which molted to the adult stage (n= 11 males, 11 females);

g

Reared from nymphs (n= 20) at the laboratory conditions which molted to the adult stage (n= 8 males);

h

Reared from nymphs (n= 3) at the laboratory conditions which molted to the adult stage (n= 3 females);

i

Reared from nymphs (n= 5) at the laboratory conditions which molted to the adult stage (n= 5 females);

j

Reared from nymphs (n= 2) at the laboratory conditions which molted to the adult stage (n= 2 females);

l

Reared from nymph (n= 1) at the laboratory conditions which molted to the adult stage (n= 1 female);

m

Reared from nymphs (n= 36) at the laboratory conditions which molted to the adult stage (n= 11 males, 11 females);

n

Reared from nymphs (n= 3) at the laboratory conditions which molted to the adult stage (n= 1 male);

o

Reared from nymphs (n= 91) at the laboratory conditions which molted to the adult stage (n= 26 males, 45 females).

In the molecular screening for the detection of rickettsial agents, we attempted to choose all tick species identified, which had more than one specimen per host, including the largest number of vertebrate hosts among each order of animals sampled. Therefore, some whole ticks were subjected to DNA extraction using the guanidine isothiocyanate protocol, being placed in a 1.5-mL microtube containing 150 µL of TE buffer (Tris HCl 10 mmol/L, EDTA 1 mmol/L, pH 7.4) and homogenized by using a sterile pipette tip as described by Sangioni et al. (2005), and to amplification by a conventional polymerase chain reaction (cPCR). To this end, an initial cPCR was performed using CS-78 and CS-323 primers, which target a fragment of 401 bp (base pairs) of the citrate synthase (gltA) gene common to all Rickettsia species, according to Labruna et al. (2004). Positive samples were further tested by another cPCR protocol using Rr190.70p and Rr190.602n primers, which amplify a ~530 bp fragment of the 190-kDa outer membrane protein gene (ompA) found only in Rickettsia of the SFG (Regnery et al., 1991). Negative (nuclease-free water) and positive controls (R. rickettsii DNA) were included in each of these reactions.

Rickettsia amplicons of the expected size were purified using the Illustra GFX PCR DNA and Gel Band Purification Kit (GE Healthcare, Chicago, Illinois) and sent for sequencing at the company ACTGene (Porto Alegre, RS, Brazil) with the same primers used in the cPCR. To evaluate the quality of the sequences, electropherograms were verified with CLC Genomics Workbench software (Qiagen®). All the sequences obtained were then analyzed using the Basic Local Alignment Search Tool (BLAST; Altschul et al., 1990) to determine the closest identities with congeneric organisms available in GenBank.

Results

The ticks collected in this study were taken from 102 wild animals, three of which lived in captivity and 99 were free-living individuals, distributed among 12 orders in four classes, as follows: four amphibian species, 21 reptiles, two birds, and 75 mammals. These animals were parasitized by 2338 ticks (865 males, 541 females, 823 nymphs, and 109 larvae) belonging to four genera and at least 21 species: 1239 ticks of the Amblyomma cajennense complex [A. sculptum (223 males, 164 females, 522 nymphs, and 15 larvae), Amblyomma cajennense s.s. (148 males, 38 females, and 53 nymphs), A. cajennense s.l. (53 males, and 23 nymphs)], 394 Amblyomma dissimile (154 males, 89 females, and 151 nymphs), 142 Amblyomma nodosum (83 males and 59 females), 81 Rhipicephalus microplus (31 males, 37 females, and 13 nymphs), 77 Amblyomma scalpturatum (44 males, 29 females, and 4 nymphs), 68 Amblyomma coelebs (33 males, 21 females, and 14 nymphs), 57 Amblyomma dubitatum (8 males, 42 females, and 7 nymphs), 37 Amblyomma rotundatum (17 females and 20 nymphs), 24 Amblyomma romitii (8 males, 12 females, and 4 nymphs), 23 Amblyomma calcaratum (23 males), 22 R. linnaei (15 males and 7 females), 19 A. ovale (12 males and 7 females), 17 Amblyomma triste (5 males, 6 females, and 6 nymphs), 11 Amblyomma humerale (9 males and 2 nymphs), 11 Amblyomma oblongoguttatum (3 males, 7 females, and 1 nymph), 9 Amblyomma longirostre (8 males and 1 female), 6 Amblyomma parvum (5 males and 1 female), 3 Amblyomma naponense (1 female and 2 nymphs), and 4 Haemaphysalis juxtakochi (3 females and 1 nymph). In addition, one larva of D. nitens was identified, but 93 larvae could not be identified at the species level and were therefore classified as Amblyomma sp. (Table 1).

A total of 650 DNA-extracted random samples were tested individually (430 adults) and in pools (40 pools of 5 nymphs and two pools of 10 larvae) to screen for rickettsial agents by cPCR targeting the rickettsial gltA gene. These samples were as follows: Amblyomma spp. (20 larvae), A. cajennense s.s. (5 males, 1 female, and 30 nymphs), A. cajennense s.l. (15 males), A. calcaratum (20 males), A. coelebs (13 males, 14 females, and 5 nymphs), A. dissimile (43 males, 10 females, and 20 nymphs), A. dubitatum (5 males and 5 females), A. humerale (8 males), A. longirostre (4 males), A. naponense (1 female), A. nodosum (50 males and 19 females), A. oblongoguttatum (2 females), A. ovale (5 males and 2 females), A. parvum (4 males), A. romitii (7 males and 11 females), A. rotundatum (9 females and 15 nymphs), A. scalpturatum (40 males and 25 females), A. sculptum (32 males, 36 females, and 125 nymphs), A. triste (4 males, 3 females, and 5 nymphs), H. juxtakochi (3 females), and R. microplus (27 males and 7 females), as detailed in Table 2.

Table 2. Results of molecular tests on ticks (M: adult male; F: adult female; N: nymph; L: larva) collected from free-living and captive wild animals between 2015 and 2018, in the states of Mato Grosso (MT) and Goiás (GO), in the Central-West region of Brazil.

Hosts Municipalities Ticks (No. number of specimens) No. infected/ Closest GenBank identity (gene: accession number)
No. tested (%)
ORDER CARIAMIFORMES
Cariama cristata Cuiabá (MT) Amblyomma sculptum (2M, 2F, 20N) 1/24 (4.16a) 99% Rickettsia amblyommatis (ompA: MH818422)
ORDER ANURA
Rhinella diptycha Cuiabá (MT), Jataí (GO) Amblyomma rotundatum (3F, 10N) 0/13
ORDER TESTUDINES
Chelonoidis carbonarius Cuiabá (MT) A. rotundatum (1F) 0/1
Chelonoidis denticulatus Apiacás (MT), Cuiabá (MT) Amblyomma humerale (8M) 2/8 (25) 100% R. amblyommatis (ompA: MF188914)
A. rotundatum (2F) 0/2
Phrynops geoffroanus Cuiabá (MT) A. sculptum (1M) 0/1
ORDER CROCODYLIA
Caiman yacare Cuiabá (MT) Amblyomma dissimile (1F) 0/1
Paleosuchus palpebrosus Cuiabá (MT) A. dissimile (1F) 0/1
A. rotundatum (1F) 0/1
ORDER SQUAMATA
Suborder Sauria
Iguana iguana Cuiabá (MT) A. dissimile (20M, 1F, 10N) 0/31
Tupinambis sp. Poconé (MT) A. rotundatum (5N) 0/5
Suborder Serpentes
Boa constrictor Cuiabá (MT), Jataí (GO) A. dissimile (22M, 5F, 10N) 0/37
A. rotundatum (2F) 0/2
Bothrops mattogrossensis Poconé (MT) A. dissimile (1F) 0/1
Eunectes notaeus Poconé (MT) A. dissimile (1M, 1F) 0/2
ORDER ARTIODACTYLA
Mazama americana Colniza (MT) Amblyomma cajennense s.s. (1F, 20N) 5/21 (23.80a) 100% Rickettsia sp. (gltA: KY753118, MK441839, MK720995, MK720994)
100% R. amblyommatis (ompA: MN336348)
100% Rickettsia rhipicephali (ompA: KX434736)
Haemaphysalis juxtakochi (3F) 2/3 (66.66)
Amblyomma oblongoguttatum (1F) 0/1
Subulo gouazoubira Cuiabá (MT), Poconé (MT), Várzea Grande (MT) Amblyomma parvum (4M) 2/4 (50) 100% ‘Candidatus Rickettsia andeanae’ (gltA: MG887826)
Rhipicephalus microplus (27M, 1F) 2/28 (7.14) 100% ‘Ca. Rickettsia andeanae’ (gltA: MG887826)
A. sculptum (1M, 1F, 5N) 0/7
Tayassu pecari Apiacás (MT) A. cajennense s.s. (1M) 0/1
ORDER CARNIVORA
Cerdocyon thous Cuiabá (MT), Poconé (MT) Amblyomma ovale (3M) 0/3
A. sculptum (20N) 0/20
Chrysocyon brachyurus Serranópolis (GO) A. ovale (1M, 1F) 1/2 (50) 100% Rickettsia parkeri strain Atlantic rainforest (ompA: MK801772)
Leopardus pardalis Barra do Bugres (MT) A. sculptum (5N) 0/5
Nasua nasua Cuiabá (MT), Poconé (MT) A. sculptum (15N) 0/15
Procyon cancrivorus Poconé (MT) A. ovale (1F) 1/1 (100) 100% R. parkeri strain Atlantic rainforest (ompA: MK801772)
Puma concolor Colniza (MT), Tangará da Serra (MT) A. cajennense s.s. (5N) 0/5
Amblyomma sp. (10L) 0/10
ORDER CINGULATA
Euphractus sexcinctus Colniza (MT) A. coelebs (5N) 0/5
ORDER DIDELPHIMORPHIA
Didelphis marsupialis Aripuanã (MT) Amblyomma sp. (10L) 0/10
ORDER PERISSODACTYLA
Tapirus terrestris Chapada dos Guimarães (MT), Colniza (MT), Dom Aquino (MT), Poconé (MT), Pontes e Lacerda (MT), Querência (MT), Rondonópolis (MT), Sinop (MT) A. coelebs (13M, 14F) 6/27 (22.22) 100% R. amblyommatis (ompA: MW147461)
Amblyomma scalpturatum (39M, 25F) 4/64 (6.25) 100% R. amblyommatis (ompA: MW147461)
100% R. parkeri strain NOD (ompA: MK522487, KY008394, KP987310, KM262193, EU567180)
100% R. amblyommatis (ompA: MW147461)
A. sculptum (10M, 19F, 5N) 4/34 (11.76) 100% R. amblyommatis (ompA: MW147461)
A. cajennense s.l. (15M) 5/15 (33.33) 100% R. amblyommatis (ompA: MG787411, MN336348)
A. cajennense s. s. (4M, 5N) 4/9 (44.44a)
A. oblongoguttatum (1F) 0/1
A. ovale (1M) 0/1 100% R. parkeri sensu stricto (ompA: MG574938)
A. triste (4M, 3F) 1/7 (14.28)
R. microplus (6F) 0/6
ORDER PILOSA
Myrmecophaga tridactyla Barra do Bugres (MT), Cuiabá (MT), Mineiros (GO), Poconé (MT), Rosário Oeste (MT), Santo Antônio de Leverger (MT), Tangará da Serra (MT), Várzea Grande (MT) Amblyomma nodosum (10M, 6F) 2/16 (12.5) 100% R. amblyommatis (ompA: MW147461)
100% R. parkeri strain NOD (ompA: MK522487, KY008394, KP987310, KM262193, EU567180)
100% Rickettsia sp. (gltA: KY753118, MK441839, MK720995, MK720994)
A. sculptum (7M, 3F, 25N) 1/35 (2.85a)
A. scalpturatum (1M) 0/1
Tamandua tetradactyla Chapada dos Guimarães (MT), Cuiabá (MT), Jangada (MT), Mineiros (GO), Nossa Senhora do Livramento (MT), Poconé (MT), Santo Antônio de Leverger (MT), Várzea Grande (MT) A. nodosum (40M, 13F) 8/53 (15.09) 100% Rickettsia sp. (gltA: KY753118, MK441839, MK720995, MK720994)
100% R. parkeri strain NOD (ompA: MK522487, KY008394, KP987310, KM262193, EU567180)
Amblyomma calcaratum (20M) 0/20
A. sculptum (1M, 10N) 0/11
ORDER RODENTIA
Coendou longicaudatus Chapada dos Guimarães (MT) Amblyomma longirostre (4M) 1/4 (25) 100% R. amblyommatis (ompA: MG787411)
Cuniculus paca Cuiabá (MT) A. naponense (1F) 0/1
Hydrochoerus hydrochaeris Colniza (MT), Cuiabá (MT), Poconé (MT), Pontes e Lacerda (MT), Várzea Grande (MT) A. sculptum (10M, 11F, 20N) 1/41 (2.43a) 100% R. amblyommatis (gltA: MH257786)
Amblyomma romitii (7M, 11F) 1/18 (5.55) 100% R. amblyommatis (gltA: MH257786)
A. dubitatum (5M, 5F) 0/10
Holochilus sciureus Poconé (MT) A. triste (5N) 0/5
TOTAL 650 (282 males, 148 females, 200 nymphs, and 20 larvae) 54/650 (8.30 a )
Open in a new tab
a

Results refer to minimal infection rate because PCR-positive ticks included a pool of 5 nymphs or 10 larvae.

Among the 650 DNA-extracted samples from ticks evaluated by cPCR targeting the gltA gene, at least 54 (8.30%) were found to contain rickettsial DNA through the gltA-cPCR (Table 2). Furthermore, 43 of these gltA-PCR positive samples yielded amplicons after the ompA-PCR assay. Overall, 30 DNA sequences were generated, involving the following tick species: A. cajennense s.s. (1 adult individual and three nymphal pools), A. coelebs (4 adult individuals), A. cajennense s.l. (1 adult individual), A. humerale (1 adult individual), A. longirostre (1 adult individual), A. nodosum (7 adult individuals), A. ovale (2 adult individuals), A. parvum (1 adult individual), A. romitii (1 adult individual), A. scalpturatum (4 adult individuals), A. sculptum (1 adult individual and 3 nymphal pools), A. triste (1 adult individual), H. juxtakochi (1 adult individual) and R. microplus (1 adult individual).

Molecular screening for rickettsial agents and sequences obtained from A. cajennense s.s. (1 adult individual and two nymphal pools), A. cajennense s.l. (1 adult individual), A. coelebs (4 adult individuals), A. humerale (1 adult individual), A. longirostre (1 adult individual), A. nodosum (1 adult individual), A. scalpturatum (3 adult individuals), and A. sculptum (1 adult individual and one nymphal pool) showed five different haplotypes corresponding to sequences of R. amblyommatis (GeneBank accession numbers MH818422, MF188914, MW147461, MN336348, and MG787411), with a similarity of 99% (487/488 bp) to 100% (440/440 bp - 488/488 bp). Furthermore, partial sequences showed a 100% (447bp - 491bp) match to R. parkeri strains (MG574938, MK801772, MK522487) obtained from A. scalpturatum (1 adult individual), A. nodosum (4 adult individuals), A. ovale (2 adult individuals), and A. triste (1 adult individual) ticks. Lastly, a partial sequence of the ompA gene 100% (442/442 bp) identical to R. rhipicephali (KX434736) was found in H. juxtakochi (1 adult individual) (Table 2). Partial sequences of the ompA gene could not be obtained because of the low quality of amplified DNA. Thus, the partial gltA sequence from A. cajennense s.s. (one nymphal pool), A. nodosum (2 adult individuals) and A. sculptum (one nymphal pool) showed a 100% match (348/348 bp) to other SFG rickettsiae (KY753118, MK441839, MK720995, MK720994). In addition, we obtained partial gltA sequence 100% (326/326 bp) identical to R. amblyommatis (MH257786) in A. sculptum (1 nymphal pool) and A. romitii (1 adult individual). Lastly, sequences of the gltA gene found in A. parvum (1 adult individual) and R. microplus (1 adult individual) ticks were identical to each other and a 100% match (350/350 bp) to ‘Candidatus Rickettsia andeanae’ (MG887826), as shown in Table 2.

The GenBank nucleotide sequence accession numbers for the partial sequences generated in the present study are: OP823389, OP823390, OP823391, OP823392, and OP823393 for partial sequences of the ompA gene of R. amblyommatis, OP823395 and OP823396 of R. parkeri, OP823394 of R. rhipicephali; and OP823399 for partial sequences of the gltA gene of Rickettsia sp., OP823397 of R. amblyommatis, and OP484958 of ‘Ca. Rickettsia andeanae’.

Discussion

This study revealed the presence of at least 21 tick species parasitizing wild animals in the states of Mato Grosso and Goiás, in the Central-West region of Brazil, between 2015 and 2018. The most abundant species among the collected ticks was the A. cajennense complex, followed by A. dissimile, A. nodosum, R. microplus, A. scalpturatum, A. coelebs, A. dubitatum, A. rotundatum, A. romitii, A. calcaratum, R. linnaei, A. ovale, A. triste, A. humerale, A. oblongogutattum, A. longirostre, A. parvum, A. naponense, H. juxtakochi, and D. nitens.

Amphibians and reptiles are the main hosts of all the parasitic stages of A. dissimile and A. rotundatum ticks (Nava et al., 2017; Alcantara et al., 2018; Luz et al., 2018; Torres et al., 2018). This was corroborated in the present study by the discovery of lizard and snake species with terrestrial or semiaquatic habits. However, this study identified new tick-host relationships with the amphibian Rhinella diptycha and nymphs of A. rotundatum. Additionally, the current record of adult A. dissimile ticks on Eunectes notaeus and Paleosuchus palpebrosus corresponds to a new host-parasite association. With regard to adult A. humerale ticks, our records of this species parasitizing Chelonoidis denticulatus and Didelphis marsupialis represent previously described associations (Ogrzewalska et al., 2010; Soares et al., 2015; Witter et al., 2016; Colle et al., 2020). Testudines (Testudinidae) are the common hosts for adult A. humerale ticks, while an infestation of Crocodylia and Mammalia is unexpected (Guglielmone et al., 2014), as is the infestation of the reptile Phrynops geoffroanus by adult A. sculptum, which was observed here for the first time. This is an unusual discovery since A. sculptum ticks are usually found parasitizing mammals (Nava et al., 2014; Martins et al., 2016).

As for information about tick species, the largest number of ticks comprising the A. cajennense species complex, represented in Brazil by A. cajennense s.s. and A. sculptum (the vector of R. rickettsii, agent of Brazilian Spotted Fever) (Szabó et al., 2013; Nava et al., 2014; Martins et al., 2016) was expected, given the large numbers of tapirs (n=14), capybaras (n=9) and giant anteaters (n=12), usual hosts for adults and immature stages of A. sculptum (Martins et al., 2016, 2023). Birds have been recorded as hosts of all the stages of A. sculptum in Brazil (Nava et al., 2017), as reported by Luz et al. (2016) in the state of Goiás and observed in this study for A. sculptum nymphs and adult ticks infesting C. cristata in the Cerrado biome. Similarly, the large number of adult A. nodosum ticks is presumably associated with the occurrence of anteaters (Myrmecophaga tridactyla and Tamandua tetradactyla), reported to be the main hosts of adult stages of A. nodosum (Nava et al., 2017). Although A. cajennense s.s. has been observed on a wide range of domestic and wild animals, including tapirs and giant anteaters (Martins et al., 2016; Luz et al., 2020), this paper describes the first tick-host relationship with Mazama americana.

Rhipicephalus microplus is strongly associated with cattle (Nava et al., 2017; Martins et al., 2023), and all the records of parasitism on Subulo gouazoubira, Cerdocyon thous, Puma concolor, and Tapirus terrestris described herein have already been reported previously by other authors. Even though horses are the main host of D. nitens, this parasite has been found in a variety of mammals, including wild carnivores (Labruna et al., 2005b; Guglielmone et al., 2014; Nava et al., 2017). In this paper, we describe for the first time, a D. nitens larva parasitizing Chrysocyon brachyurus. Therefore, tick infestations among livestock and horses should be considered accidental findings, possibly attributable to the fact that these animals share pastures with cattle and horses (Ramos et al., 2020).

In the order Carnivora, two new tick-host associations were observed, involving the species A. cajennense s.s. and A. oblongoguttatum nymphs found on wild cats Puma concolor and Leopardus pardalis, respectively. Rhipicephalus linnaei, recently recognized as belonging to the so-called “tropical lineage” of Rhipicephalus sanguineus s.l. (Šlapeta et al., 2022), is a species of the R. sanguineus complex commonly known as the brown dog tick. It has occasionally been found on mammals of different orders, with all parasitic stages of this tick strongly associated with domestic dogs (Nava et al., 2017), and here it was found parasitizing a rodent, the capybara Hydrochoerus hydrochaeris. This is probably due to these rodents’ population growth in urban and peri-urban areas, where R. linnaei is distributed throughout most of Brazil, particularly in these areas.

This study also found a new tick-host association of A. cajennense s.s. nymphs on a six-banded armadillo Euphractus sexcinctus. Although tapirs are considered the usual hosts of adults of A. coelebs, and the largest number of ticks found on one animal in our study was on a host parasitized by 14 specimens, adults and immature stages of this tick present low host specificity (Nava et al., 2017). The remaining tick-host associations described here have been previously reported.

The molecular survey indicated infection by an uncharacterized Rickettsia species belonging to the SFG in A. cajennense s.s., A. nodosum, and A. sculptum. Other studies have described uncharacterized Rickettsia in A. humerale (Colle et al., 2020) and A. nodosum (Lugarini et al., 2015). So, this report can indicate the possibility that other rickettsiae species not yet described should be infecting ticks from wild animals. Detection of R. rhipicephali in H. juxtakochi was expected since various studies carried out in the country have previously described this agent infecting this tick species (Labruna et al., 2005a, 2007; Soares et al., 2015). Although its pathogenic potential for humans is still unknown, experimental infections in mice suggest that it can cause moderately severe disease (Wikswo et al., 2008; Parola et al., 2013).

Another rickettsial agent found infecting A. parvum, and for the first time, R. microplus ticks, was ‘Ca. R. andeanae.’ Several studies have described infection by ‘Ca. R. andeanae’ in Amblyomma ticks, including A. parvum (Pacheco et al., 2007; Ogrzewalska et al., 2014; Nieri-Bastos et al., 2014; Lugarini et al., 2015; Maia et al., 2018), A. auricularium (Lugarini et al., 2015), A. sculptum (Witter et al., 2016), A. maculatum (Blair et al., 2004; Paddock et al., 2010; Flores-Mendoza et al., 2013), A. pseudoconcolor (Sebastian et al., 2022), A. tigrinum (Arrais et al., 2021), and A. triste (Abarca et al., 2012). The role of this bacterium as a human pathogen is still unknown (Ferrari et al., 2013); however, Krawczak et al. (2023) have proposed that high infection rates by ‘Ca. R. andeanae’ may favor the exclusion of other Rickettsia species in tick populations, as observed in their study of R. parkeri and A. tigrinum in southern Brazil.

Infection by R. amblyommatis in at least six tick species (A. cajennense s.s., A. cajennense s.l., A. humerale, A. longirostre, A. sculptum, A. scalpturatum, and A. oblongoguttatum) was expected, since this Rickettsia species has been reported in 34 tick species worldwide (Richardson et al., 2023). However, here we provide new data on R. amblyommatis infecting A. romitii and A. nodosum ticks. Considering the possibility of the genetic variability between the different strains of R. amblyommatis in South American (Sebastian et al., 2020), it is evident the importance of new data encompassing infection by this bacterium in two species of the genus Amblyomma, also contributing to a better understanding of ecological relationships involving ticks and agents transmitted by them in a wild environment. Despite the numerous reports of infection in ticks, the pathogenicity of R. amblyommatis to humans is still unknown. However, it is suspected that this may be a potential pathogen, in view of several serological reports of human infection, as well as a possible association with the occurrence of disease in some patients in the United States (Apperson et al., 2008; Delisle et al., 2016). Moreover, there is molecular evidence that this organism can infect dogs (Barrett et al., 2014), and cause fever and pathological signs of the disease in guinea pigs (Rivas et al., 2015).

Finally, molecular analyses revealed the presence of R. parkeri strain NOD infecting A. scalpturatum and A. nodosum, beyond R. parkeri strain Atlantic rainforest in A. ovale, and R. parkeri sensu stricto (s.s.) infecting A. triste. Phylogenetic analysis of R. parkeri indicated the existence of different strains: R. parkeri s.s., R. parkeri strain Atlantic rainforest, R. parkeri strain NOD, and R. parkeri strain Parvitarsum (Nieri-Bastos et al., 2018). In Brazil, R. parkeri strain Atlantic rainforest is responsible for mild cases of human rickettsiosis, transmitted mainly by adult A. ovale ticks and occurring widely throughout the Brazilian Atlantic Forest (Szabó et al., 2013; Barbieri et al., 2014; Krawczak et al., 2016; Moerbeck et al., 2016; Sevá et al., 2019).

R. parkeri s.s. has also been described infecting A. triste in southeastern and midwestern Brazil (Silveira et al., 2007; Widmer et al., 2011; Melo et al., 2015), and A. tigrinum (Weck et al., 2016) and A. dubitatum (Weck et al., 2017) in the Pampa biome. However, human infection by R. parkeri s.s. has never been confirmed in the laboratory in Brazil, although Weck et al. (2016) reported a possible human case transmitted by A. tigrinum in this country.

Conclusions

This paper offers new information on tick-host associations with amphibians and reptiles, including nymphs of A. rotundatum parasitizing R. diptycha, adult A. dissimile ticks on E. notaeus and P. palpebrosus, and adult A. sculptum on P. geoffroanus. As for mammals, new associations were described for adults and nymphs of A. cajennense s.s. on M. americana and nymphs on M. tridactyla, larva of D. nitens on C. brachyurus, nymphal stages of A. cajennense s.s. and A. oblongoguttatum on P. concolor and L. pardalis, respectively, and lastly, the occurrence of A. cajennense s.s. nymphs on E. sexcinctus.

In addition, we have shown a wide diversity of rickettsiae infecting the tick fauna recorded, including a potentially human pathogen species, R. parkeri, demonstrating the importance of the study in the epidemiological context of One Health.

Acknowledgements

The authors gratefully acknowledge the financial support of the following research funding agencies: CAPES (Federal Agency for the Support and Improvement of Higher Education, Brazil) granted a scholarship to A.C.P.; CNPq (National Council for Scientific and Technological Development, Brazil) provided a research productivity grant to D.M.A. and R.C.P. (grant no. 310002/2022-2); the FCT (Foundation for Science and Technology, Portugal) granted a fellowship to T.B.F.S. (no. 202210212BD); and FAPESP (São Paulo Research Foundation, Brazil) supports the research work of T.F.M. (Process nos. 2019/03167-0, 2020/05987-1); and Graduate Program in Animal Bioscience from the University of Cuiabá (UNIC).

Footnotes

How to cite: Prati AC, Maia MO, Martins TF, Morgado TO, Corrêa SHR, Mendes EJF, et al. Diversity of rickettsiae in ticks (Acari: Ixodidae) collected from wild vertebrates in part of the Amazon, Cerrado, and Pantanal biomes in Brazil. Braz J Vet Parasitol 2023; 32(4): e008023. https://doi.org/10.1590/S1984-29612023059

References

  1. Abarca K, López J, Acosta-Jamett G, Lepe P, Soares JF, Labruna MB. A third Amblyomma species and the first tick-borne Rickettsia in Chile. J Med Entomol. 2012;49(1):219–222. doi: 10.1603/ME11147. [DOI] [PubMed] [Google Scholar]
  2. Alcantara EP, Silva CF, Ávila RW, Pacheco RC, Martins TF, Muñoz-Leal S, et al. Ticks (Acari: Argasidae and Ixodidae) infesting amphibians and reptiles in Northeastern Brazil. Syst Appl Acarol. 2018;23(8):1497–1508. doi: 10.11158/saa.23.8.1. [DOI] [Google Scholar]
  3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  4. Anderson JF, Magnarelli LA. Biology of ticks. Infect Dis Clin North Am. 2008;22(2):195–215. doi: 10.1016/j.idc.2007.12.006. [DOI] [PubMed] [Google Scholar]
  5. Apperson CS, Engber B, Nicholson WL, Mead DG, Engel J, Yabsley MJ, et al. Tick-borne diseases in North Carolina: is “Rickettsia amblyommii” a possible cause of rickettsiosis reported as Rocky Mountain spotted fever? Vector Borne Zoonotic Dis. 2008;8(5):597–606. doi: 10.1089/vbz.2007.0271. [DOI] [PubMed] [Google Scholar]
  6. Aragão HB, Fonseca F. Notas de ixodologia: VIII. Lista e chave para os representantes da fauna ixodológica brasileira: notas de ixolodologia. Mem Inst Oswaldo Cruz. 1961;59(2):115–129. doi: 10.1590/S0074-02761961000200001. [DOI] [PubMed] [Google Scholar]
  7. Aragão HB. Ixodidas brasileiros e de alguns paizes limitrophes. Mem Inst Oswaldo Cruz. 1936;31(4):759–843. doi: 10.1590/S0074-02761936000400004. [DOI] [Google Scholar]
  8. Arrais RC, Paula RC, Martins TF, Nieri-Bastos FA, Marcili A, Labruna MB. Survey of ticks and tick-borne agents in maned wolves (Chrysocyon brachyurus) from a natural landscape in Brazil. Ticks Tick Borne Dis. 2021;12(2):101639. doi: 10.1016/j.ttbdis.2020.101639. [DOI] [PubMed] [Google Scholar]
  9. Barbieri ARM, Moraes J, Fo, Nieri-Bastos FA, Souza JC, Jr, Szabó MPJ, Labruna MB. Epidemiology of Rickettsia sp. strain Atlantic rainforest in a spotted fever-endemic area of southern Brazil. Ticks Tick Borne Dis. 2014;5(6):848–853. doi: 10.1016/j.ttbdis.2014.07.010. [DOI] [PubMed] [Google Scholar]
  10. Barrett A, Little SE, Shaw E. “Rickettsia amblyommii” and R. montanensis infection in dogs following natural exposure to ticks. Vector Borne Zoonotic Dis. 2014;14(1):20–25. doi: 10.1089/vbz.2013.1325. [DOI] [PubMed] [Google Scholar]
  11. Barros-Battesti DM, Arzua M, Bechara GH. Carrapatos de importância médico-veterinária da Região Neotropical: um guia ilustrado para identificação de espécies. São Paulo: Vox/International Consortium on Ticks and Tick-borne Diseases/Butantan; 2006. [Google Scholar]
  12. Binder LC, Ramírez-Hernández A, Serpa MCA, Moraes-Filho J, Pinter A, Scinachi CA, et al. Domestic dogs as amplifying hosts of Rickettsia rickettsii for Amblyomma aureolatum ticks. Ticks Tick Borne Dis. 2021;12(6):101824. doi: 10.1016/j.ttbdis.2021.101824. [DOI] [PubMed] [Google Scholar]
  13. Blair PJ, Jiang J, Schoeler GB, Moron C, Anaya E, Cespedes M, et al. Characterization of spotted fever group Rickettsiae in flea and tick specimens from Northern Peru. J Clin Microbiol. 2004;42(11):4961–4967. doi: 10.1128/JCM.42.11.4961-4967.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Clifford CM, Anastos G. The use of chaetotaxy in the identification of larval ticks (Acarina: ixodidae) J Parasitol. 1960;46(5):567–578. doi: 10.2307/3274939. [DOI] [PubMed] [Google Scholar]
  15. Colle AC, Mendonça RFB, Maia MO, Freitas LC, Martins TF, Muñoz-Leal S, et al. Rickettsial survey and ticks infesting small mammals from the Amazon Forest in midwestern Brazil. Syst Appl Acarol. 2020;25(1):78–91. doi: 10.11158/saa.25.1.6. [DOI] [Google Scholar]
  16. Delisle J, Mendell NL, Stull-Lane A, Bloch KC, Bouyer DH, Moncayo AC. Human infections by multiple spotted fever group Rickettsiae in Tennessee. Am J Trop Med Hyg. 2016;94(6):1212–1217. doi: 10.4269/ajtmh.15-0372. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Dumler JS, Barbet AF, Bekker CP, Dasch GA, Palmer GH, Ray SC, et al. Reorganization of genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia, descriptions of six new species combinations and designation of Ehrlichia equi and ‘HE agent’ as subjective synonyms of Ehrlichia phagocytophila. Int J Syst Evol Microbiol. 2001;51(6):2145–2165. doi: 10.1099/00207713-51-6-2145. [DOI] [PubMed] [Google Scholar]
  18. Ferrari FAG, Goddard J, Moraru GM, Smith WEC, Varela-Stokes AS. Isolation of “Candidatus Rickettsia andeanae” (Rickettsiales: Rickettsiaceae) in embryonic cells of naturally infected Amblyomma maculatum (Ixodida: Ixodidae) J Med Entomol. 2013;50(5):1118–1125. doi: 10.1603/ME13010. [DOI] [PubMed] [Google Scholar]
  19. Flores-Mendoza C, Florin D, Felices V, Pozo EJ, Graf PC, Burrus RG, et al. Detection of Rickettsia parkeri from within Piura, Peru, and the first reported presence of Candidatus Rickettsia andeanae in the tick Rhipicephalus sanguineus. Vector Borne Zoonotic Dis. 2013;13(7):505–508. doi: 10.1089/vbz.2012.1028. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Guglielmone AA, Robbins RG, Apanaskevich DA, Petney TN, Estrada-Peña A, Horak IG. The hard ticks of the world: (Acari: Ixodida: Ixodidae) Amsterdam: Springer; 2014. [DOI] [Google Scholar]
  21. Krawczak FS, Binder LC, Gregori F, Martins TF, Pádua GT, Sponchiado J, et al. ‘Candidatus Rickettsia andeanae’ and probable exclusion of Rickettsia parkeri in ticks from dogs in a natural area of the Pampa biome in Brazil. Pathogens. 2023;12(3):446. doi: 10.3390/pathogens12030446. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Krawczak FS, Muñoz-Leal S, Guztzazky AC, Oliveira SV, Santos FC, Angerami RN, et al. Rickettsia sp. strain Atlantic rainforest infection in a patient from a spotted fever-endemic area in southern Brazil. Am J Trop Med Hyg. 2016;95(3):551–553. doi: 10.4269/ajtmh.16-0192. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Labruna MB, Camargo LMA, Camargo EP, Walker DH. Detection of a spotted fever group Rickettsia in the tick Haemaphysalis justakochi in Rondônia, Brazil. Vet Parasitol. 2005;127(2):169–174. doi: 10.1016/j.vetpar.2004.09.024. a. [DOI] [PubMed] [Google Scholar]
  24. Labruna MB, Jorge RS, Sana DA, Jácomo AT, Kashivakura CK, Furtado MM, et al. Ticks (Acari: Ixodida) on wild carnivores in Brazil. Exp Appl Acarol. 2005;36(1-2):149–163. doi: 10.1007/s10493-005-2563-1. b. [DOI] [PubMed] [Google Scholar]
  25. Labruna MB, Pacheco RC, Richtzenhain LJ, Szabó MPJ. Isolation of Rickettsia rhipicephali and Rickettsia bellii from Haemaphysalis juxtakochi ticks in the state of São Paulo, Brazil. Appl Environ Microbiol. 2007;73(3):869–873. doi: 10.1128/AEM.02249-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Labruna MB, Whitworth T, Horta MC, Bouyer DH, McBride JW, Pinter A, et al. Rickettsia species infecting Amblyomma cooperi ticks from an area in the state of São Paulo, Brazil, where Brazilian spotted fever is endemic. J Clin Microbiol. 2004;42(1):90–98. doi: 10.1128/JCM.42.1.90-98.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Labruna MB. Ecology of Rickettsia in South America. Ann N Y Acad Sci. 2009;1166(1):156–166. doi: 10.1111/j.1749-6632.2009.04516.x. [DOI] [PubMed] [Google Scholar]
  28. Lugarini C, Martins TF, Ogrzewalska M, Vasconcelos NCT, Ellis VA, Oliveira JB, et al. Rickettsial agents in avian ixodid ticks in northeast Brazil. Ticks Tick Borne Dis. 2015;6(3):364–375. doi: 10.1016/j.ttbdis.2015.02.011. [DOI] [PubMed] [Google Scholar]
  29. Luz HR, Faccini JLH, Landulfo GA, Costa SFC, No, Famadas KM. New records for Amblyomma sculptum (Ixodidae) on non-passerine birds in Brazil. Rev Bras Parasitol Vet. 2016;25(1):124–126. doi: 10.1590/S1984-29612016004. [DOI] [PubMed] [Google Scholar]
  30. Luz HR, Martins TF, Muñoz-Leal S, Costa FB, Gianizella SL, Faccini JLH, et al. In: Ecosystem and biodiversity of Amazonia. Mikkola H, editor. London: IntechOpen; 2020. Ticks from the Brazilian Amazon: species, distribution and host-relations; pp. 631–664. [DOI] [Google Scholar]
  31. Luz HR, Silva-Santos E, Costa-Campos CE, Acosta I, Martins TF, Muñoz-Leal S, et al. Detection of Rickettsia spp. in ticks parasitizing toads (Rhinella marina) in the northern Brazilian Amazon. Exp Appl Acarol. 2018;75(3):309–318. doi: 10.1007/s10493-018-0270-y. [DOI] [PubMed] [Google Scholar]
  32. Maia MO, Koppe VC, Muñoz-Leal S, Martins TF, Marcili A, Labruna MB, et al. Detection of Rickettsia spp. in ticks associated to wild mammals in Northeastern Brazil, with notes on an undetermined Ornithodoros sp. collected from marsupials. Exp Appl Acarol. 2018;76(4):523–535. doi: 10.1007/s10493-018-0323-2. [DOI] [PubMed] [Google Scholar]
  33. Martins TF, Barbieri ARM, Costa FB, Terassini FA, Camargo LMA, Peterka CRL, et al. Geographical distribution of Amblyomma cajennense (sensu lato) ticks (Parasitiformes: Ixodidae) in Brazil, with description of the nymph of A. cajennense (sensu stricto) Parasit Vectors. 2016;9:186. doi: 10.1186/s13071-016-1460-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Martins TF, Furtado MM, Jacomo ATA, Silveira L, Sollmann R, Tôrres NM, et al. Ticks on free-living wild mammals in Emas National Park, Goiás State, central Brazil. Syst Appl Acarol. 2011;16(3):201–206. doi: 10.11158/saa.16.3.2. [DOI] [Google Scholar]
  35. Martins TF, Onofrio VC, Barros-Battesti DM, Labruna MB. Nymphs of the genus Amblyomma (Acari: Ixodidae) of Brazil: descriptions, redescriptions, and identification key. Ticks Tick Borne Dis. 2010;1(2):75–99. doi: 10.1016/j.ttbdis.2010.03.002. [DOI] [PubMed] [Google Scholar]
  36. Martins TF, Yogui DR, Alves MH, Kluyber D, Massocato G, Labruna MB, et al. Surveillance of ticks (Acari: Ixodidae) on monitored free-ranging giant anteaters and on road-killed anteaters and armadillos in the State of Mato Grosso do Sul, Midwestern Brazil. Syst Appl Acarol. 2023;28(4):641–646. doi: 10.11158/saa.28.4.1. [DOI] [Google Scholar]
  37. Melo ALT, Alves AS, Nieri-Bastos FA, Martins TF, Witter R, Pacheco TA, et al. Rickettsia parkeri infecting free-living Amblyomma triste ticks in the Brazilian Pantanal. Ticks Tick Borne Dis. 2015;6(3):237–241. doi: 10.1016/j.ttbdis.2015.01.002. [DOI] [PubMed] [Google Scholar]
  38. Moerbeck L, Vizzoni VF, Machado-Ferreira E, Cavalcante RC, Oliveira SV, Soares CA, et al. Rickettsia (Rickettsiales: Rickettsiaceae) vector biodiversity in high altitude Atlantic Forest fragments within a semiarid climate: a new endemic area of spotted-fever in Brazil. J Med Entomol. 2016;53(6):1458–1466. doi: 10.1093/jme/tjw121. [DOI] [PubMed] [Google Scholar]
  39. Nava S, Beati L, Labruna MB, Cáceres AG, Mangold AJ, Guglielmone AA. Reassessment of the taxonomic status of Amblyomma cajennense (Fabricius, 1787) with the description of three new species, Amblyomma tonelliae n. sp., Amblyomma interandinum n. sp. and Amblyomma patinoi n. sp., and reinstatement of Amblyomma mixtum Koch, 1844, and Amblyomma sculptum Berlese, 1888 (Ixodida: Ixodidae) Ticks Tick Borne Dis. 2014;5(3):252–276. doi: 10.1016/j.ttbdis.2013.11.004. [DOI] [PubMed] [Google Scholar]
  40. Nava S, Beati L, Venzal J, Labruna ML, Szabó MPJ, Petney T, et al. Rhipicephalus sanguineus (Latreille, 1806): neotype designation, morphological redescription of all parasitic stages and molecular characterization. Ticks Tick Borne Dis. 2018;9(6):1573–1585. doi: 10.1016/j.ttbdis.2018.08.001. [DOI] [PubMed] [Google Scholar]
  41. Nava S, Guglielmone AA, Mangold AJ. An overview of systematics and evolution of ticks. Front Biosci. 2009;14(8):2857–2877. doi: 10.2741/3418. [DOI] [PubMed] [Google Scholar]
  42. Nava S, Venzal J, Acuña DG, Martins TF, Guglielmone A. Ticks of the Southern Cone of America: diagnosis, distribution and hosts with taxonomy, ecology and sanitary importance. London: Academic Press; 2017. [Google Scholar]
  43. Nieri-Bastos FA, Lopes MG, Cançado PHD, Rossa GAR, Faccini JLH, Gennari SM, et al. Candidatus Rickettsia andeanae, a spotted fever group agent infecting Amblyomma parvum ticks in two Brazilian biomes. Mem Inst Oswaldo Cruz. 2014;109(2):259–261. doi: 10.1590/0074-0276140283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Nieri-Bastos FA, Marcili A, Sousa R, Paddock CD, Labruna MB. Phylogenetic evidence for the existence of multiple strains of Rickettsia parkeri in the New World. Appl Environ Microbiol. 2018;84(8):e02872-17. doi: 10.1128/AEM.02872-17. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Nogueira BCF, Campos AK, Muñoz-Leal S, Pinter A, Martins TF. Soft and hard ticks (Parasitiformes: Ixodida) on humans: a review of Brazilian biomes and the impact of environmental change. Acta Trop. 2022;234:106598. doi: 10.1016/j.actatropica.2022.106598. [DOI] [PubMed] [Google Scholar]
  46. Ogrzewalska M, Literak I, Martins TF, Labruna MB. Rickettsial infections in ticks from wild birds in Paraguay. Ticks Tick Borne Dis. 2014;5(2):83–89. doi: 10.1016/j.ttbdis.2013.08.004. [DOI] [PubMed] [Google Scholar]
  47. Ogrzewalska M, Uezu A, Labruna MB. Ticks (Acari: Ixodidae) infesting wild birds in the eastern Amazon, northern Brazil, with notes on rickettsial infection in ticks. Parasitol Res. 2010;106(4):809–816. doi: 10.1007/s00436-010-1733-1. [DOI] [PubMed] [Google Scholar]
  48. Oliveira SV, Guimarães JN, Reckziegel GC, Neves BM, Araújo-Vilges KM, Fonseca LX, et al. An update on the epidemiological situation of spotted fever in Brazil. J Venom Anim Toxins Incl Trop Dis. 2016;22(1):22. doi: 10.1186/s40409-016-0077-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Pacheco RC, Moraes-Filho J, Nava S, Brandão PE, Richtzenhain LJ, Labruna MB. Detection of a novel spotted fever group rickettsia in Amblyomma parvum ticks (Acari: Ixodidae) from Argentina. Exp Appl Acarol. 2007;43(1):63–71. doi: 10.1007/s10493-007-9099-5. [DOI] [PubMed] [Google Scholar]
  50. Paddock CD, Fournier PE, Sumner JW, Goddard J, Elshenawy Y, Metcalfe MG, et al. Isolation of Rickettsia parkeri and identification of a novel spotted fever group Rickettsia sp. from Gulf Coast ticks (Amblyomma maculatum) in the United States. Appl Environ Microbiol. 2010;76(9):2689–2696. doi: 10.1128/AEM.02737-09. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Parola P, Paddock CD, Socolovschi C, Labruna MB, Mediannikov O, Kernif T, et al. Update on tick-borne rickettsioses around the world: a geographic approach. Clin Microbiol Rev. 2013;26(4):657–702. doi: 10.1128/CMR.00032-13. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Ramos VN, Lemos FG, Azevedo FC, Arrais RC, Lima CFM, Candeias IZ, et al. Wild carnivores, domestic dogs and ticks: shared parasitism in the Brazilian Cerrado. Parasitology. 2020;147(6):689–698. doi: 10.1017/S0031182020000335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Regnery RL, Spruill CL, Plikaytis BD. Genotypic identification of rickettsiae and estimation of intraspecies sequence divergence for portions of two rickettsial genes. J Bacteriol. 1991;173(5):1576–1589. doi: 10.1128/jb.173.5.1576-1589.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Richardson EA, Roe RM, Apperson CS, Ponnusamy L. Rickettsia amblyommatis in ticks: a review of distribution, pathogenicity, and diversity. Microorganisms. 2023;11(2):493. doi: 10.3390/microorganisms11020493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Rivas JJ, Moreira-Soto A, Alvarado G, Taylor L, Calderón-Arguedas O, Hun L, et al. Pathogenic potential of a Costa Rican strain of ‘Candidatus Rickettsia amblyommii’ in guinea pigs (Cavia porcellus) and protective immunity against Rickettsia rickettsii. Ticks Tick Borne Dis. 2015;6(6):805–811. doi: 10.1016/j.ttbdis.2015.07.008. [DOI] [PubMed] [Google Scholar]
  56. Sangioni LA, Horta MC, Vianna MC, Gennari SM, Soares RM, Galvão MA, et al. Rickettsial infection in animals and Brazilian spotted fever endemicity. Emerg Infect Dis. 2005;11(2):265–270. doi: 10.3201/eid1102.040656. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Sebastian PS, Tarragona EL, Bottero MNS, Nava S. Phylogenetic divergence between Rickettsia amblyommatis strains from Argentina. Review Comp Immunol Microbiol Infect Dis. 2020;69:101418. doi: 10.1016/j.cimid.2020.101418. [DOI] [PubMed] [Google Scholar]
  58. Sebastian PS, Winter M, Abate SD, Tarragona EL, Nava S. Molecular detection of Candidatus Rickettsia andeanae and Ehrlichia sp. in Amblyomma pseudoconcolor Aragão, 1908 (Acari: Ixodidae) from the Argentinian Patagonia. Animals. 2022;12(23):3307. doi: 10.3390/ani12233307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Serpa MCA, Luz HR, Costa FB, Weck BC, Benatti HR, Martins TF, et al. Small mammals, ticks and rickettsiae in natural and human-modified landscapes: diversity and occurrence of Brazilian spotted fever in Brazil. Ticks Tick Borne Dis. 2021;12(6):101805. doi: 10.1016/j.ttbdis.2021.101805. [DOI] [PubMed] [Google Scholar]
  60. Sevá AP, Martins TF, Muñoz-Leal S, Rodrigues AC, Pinter A, Luz HR, et al. A human case of spotted fever caused by Rickettsia parkeri strain Atlantic rainforest and its association to the tick Amblyomma ovale. Parasit Vectors. 2019;12(1):471. doi: 10.1186/s13071-019-3730-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Silva N, Eremeeva ME, Rozental T, Ribeiro GS, Paddock CD, Ramos EAG, et al. Eschar-associated spotted fever rickettsiosis, Bahia, Brazil. Emerg Infect Dis. 2011;17(2):275–278. doi: 10.3201/eid1702.100859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Silveira I, Pacheco RC, Szabó MP, Ramos HG, Labruna MB. Rickettsia parkeri in Brazil. Emerg Infect Dis. 2007;13(7):1111–1113. doi: 10.3201/eid1307.061397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Šlapeta J, Halliday B, Chandra S, Alanazi AD, Abdel-Shafy S. Rhipicephalus linnaei (Audouin, 1826) recognised as the “tropical lineage” of the brown dog tick Rhipicephalus sanguineus sensu lato: neotype designation, redescription, and establishment of morphological and molecular reference. Ticks Tick Borne Dis. 2022;13(6):102024. doi: 10.1016/j.ttbdis.2022.102024. [DOI] [PubMed] [Google Scholar]
  64. Soares HS, Barbieri AR, Martins TF, Minervino AHH, Lima JT, Marcili A, et al. Ticks and rickettsial infection in the wildlife of two regions of the Brazilian Amazon. Exp Appl Acarol. 2015;65(1):125–140. doi: 10.1007/s10493-014-9851-6. [DOI] [PubMed] [Google Scholar]
  65. Spolidorio MG, Labruna MB, Mantovani E, Brandão PE, Richtzenhain LJ, Yoshinari NH. Novel spotted fever group rickettsiosis, Brazil. Emerg Infect Dis. 2010;16(3):521–523. doi: 10.3201/eid1603.091338. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Szabó MPJ, Nieri-Bastos FA, Spolidorio MG, Martins TF, Barbieri AM, Labruna MB. 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. 2013;140(6):719–728. doi: 10.1017/S0031182012002065. [DOI] [PubMed] [Google Scholar]
  67. Szabó MPJ, Olegário MMM, Santos ALQ. Tick fauna from two locations in the Brazilian savannah. Exp Appl Acarol. 2007;43(1):73–84. doi: 10.1007/s10493-007-9096-8. [DOI] [PubMed] [Google Scholar]
  68. Torres AC, Minervino AHH, Santos AP, Jr, Sarturi C, Martins TF, Vale WG, et al. Amblyomma ticks infesting amphibians and Squamata reptiles from the lower Amazon region, Brazil. Exp Appl Acarol. 2018;75(4):399–407. doi: 10.1007/s10493-018-0277-4. [DOI] [PubMed] [Google Scholar]
  69. Vieira AML, Souza CE, Labruna MB, Mayo RC, Souza SSL, Camargo-Neves VLF. Manual de vigilância acarológica do estado de São Paulo. São Paulo: SUCEN; 2004. [Google Scholar]
  70. Weck B, Dall’Agnol B, Souza U, Webster A, Stenzel B, Klafke G, et al. Spotted fever group Rickettsia in the Pampa biome, Brazil, 2015-2016. Emerg Infect Dis. 2016;22(11):2014–2016. doi: 10.3201/eid2211.160859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Weck B, Dall’Agnol B, Souza U, Webster A, Stenzel B, Klafke G, et al. Rickettsia parkeri in Amblyomma dubitatum ticks in a spotted fever focus from the Brazilian Pampa. Acta Trop. 2017;171:182–185. doi: 10.1016/j.actatropica.2017.03.028. [DOI] [PubMed] [Google Scholar]
  72. Weinert LA, Werren JH, Aebi A, Stone GN, Jiggins FM. Evolution and diversity of Rickettsia bacteria. BMC Biol. 2009;7(1):6. doi: 10.1186/1741-7007-7-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Widmer CE, Azevedo FCC, Almeida AP, Ferreira F, Labruna MB. Tick-borne bacteria in free-living jaguars (Panthera onca) in Pantanal, Brazil. Vector Borne Zoonotic Dis. 2011;11(8):1001–1005. doi: 10.1089/vbz.2011.0619. [DOI] [PubMed] [Google Scholar]
  74. Wikswo ME, Hu R, Dasch GA, Krueger L, Arugay A, Jones K, et al. Detection and identification of spotted fever group rickettsiae in Dermacentor species from Southern California. J Med Entomol. 2008;45(3):509–516. doi: 10.1093/jmedent/45.3.509. [DOI] [PubMed] [Google Scholar]
  75. Witter R, Martins TF, Campos AK, Melo ALT, Corrêa SHR, Morgado TO, et al. Rickettsial infection in ticks (Acari: Ixodidae) of wild animals in midwestern Brazil. Ticks Tick Borne Dis. 2016;7(3):415–423. doi: 10.1016/j.ttbdis.2015.12.019. [DOI] [PubMed] [Google Scholar]

Articles from Revista Brasileira de Parasitologia Veterinária / Brazilian Journal of Veterinary Parasitology are provided here courtesy of Colégio Brasileiro de Parasitologia Veterinária

RESOURCES