Open access peer-reviewed chapter

Ticks from the Brazilian Amazon: Species, Distribution and Host-Relations

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Hermes R. Luz, Thiago F. Martins, Sebastián Muñoz-Leal, Francisco B. Costa, Sérgio L. Gianizella, João Luiz H. Faccini and Marcelo B. Labruna

Submitted: July 5th, 2020 Reviewed: November 1st, 2020 Published: December 23rd, 2020

DOI: 10.5772/intechopen.94862

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Abstract

Ticks are important ectoparasites and can transmit a wide variety of pathogens to animals and humans worldwide. These ectoparasites are the most important vectors of diseases causing pathogens in domestic and wild animals, and the second for man. In Brazil, Spotted Fever is the only disease transmitted to humans by ticks, while for animals we can highlight babesiosis, ehrlichiosis and anaplasmosis. Although ticks are found in all of Brazil’s biomes, little is known about its diversity and host-relations in the Amazon biome. The existing gaps and the lack of research indicate that the diversity of ticks and their possible pathogens are underestimated in the Brazilian Amazon. Therefore, in order to guide the next studies in the Amazon biome, we present in this chapter a compilation of the records of hard ticks and soft ticks parasitizing wild and domestic animals, and humans. We present the general list of ticks for this biome, their distribution, hosts and importance for public health and veterinary. Finally, the ixodofauna found in the Brazilian Amazon and presented here does not match the vertebrate diversity of this biome, which is one of the largest on the planet. Therefore, more acarologists and epidemiologists are needed in this region.

Keywords

  • Ixodida
  • domestic animals
  • wild animals
  • humans
  • Amazon
  • Brazil

1. Introduction

The Amazon or Amazon Rainforest is the largest remnant of tropical forest in the world, occupying a region of approximately 6.7 million/km2, covering nine countries in South America: Ecuador (≅ 2%), Suriname (≅ 2%), Bolivia (≅ 4%), Venezuela (≅ 4%), Guyana (≅ 3%), French Guiana (≅ 2%), Colombia (≅ 10%), Peru (≅ 13%), and Brazil (≅ 60%) (Figure 1) [1, 2]. In Brazil, the Amazon biome, also known as “Legal Amazon” occupies approximately 49% of its territory, covering the states of Acre, Amapá, Amazonas, Mato Grosso, Pará, Rondônia, Roraima, Tocantins and Maranhão (Figure 1). The Brazilian Amazon is known for its high richness of landscapes composed of 23 ecoregions, whose main domain is the humid rainforest (≅ 78%). Due to this heterogeneity, the Amazon has an immeasurable amount of essential habitats for the maintenance of flora and fauna, represented with high biological diversity, which is regarded as the largest in the world [3, 4] The Amazon has approximately 45,000 species of flora (39,474 species) and fauna (5,526 species) [2, 5]. However, even with this expressive diversity and the numerous faunal studies carried out in the region, there are still many gaps in the biological diversity of the Amazon. Due to its enormous extension and high degree of preservation (e.g., unexplored areas), new bioecological associations and new species are discovered every year. In the past 20 years, more than 1,200 new species have been described in the Amazon region from which we can highlight 16 birds, 39 mammals, 55 reptiles and ≅ 100 amphibians [2]. However, anthropic action has negatively impacted the animal-forest relationships for decades, resulting in the extinction of ecologically demanding species and, at the same time, the appearance of opportunistic and/or generalist species [6].

Figure 1.

Diversity of reptiles, amphibians, birds and mammals in Brazil, including the Brazilian Amazon.

Many domestic and wild animals are responsible for the maintenance and dispersion of ticks in nature. In addition, vertebrates act as amplifiers and/or reservoirs for viruses, protozoa and bacteria transmitted by these ectoparasites. The antropic action affects the population dynamics of both ticks and their wild hosts directly or indirectly, and consequently, the epidemiology of tick-borne diseases once restricted to wild fauna can reach domestic animal and humans interfaces [7]. Ticks are responsible for more than 100,000 cases of diseases in humans and animals worldwide [8], therefore a concern for public health professional. In Brazil, ticks are vectors of diseases such as babesiosis, ehrlichiosis, anaplasmosis and rickettsioses, including Brazilian Spotted Fever (BSF) [9, 10].

Ticks belong to the Sub-Class Acari, Super-Order Parasitiformes, Order Ixodida, and four families: Ixodidae, Argasidae, Nuttallielidae and Deinocrotonidae [11, 12], the latter extinct. Of these, only the Ixodidae and Argasidae families occur in Brazil, with nine genera and 75 species [11, 13, 14, 15, 16]. Ixodidae family is the most diverse with 51 species and five genera: Amblyomma (33 species), Ixodes (12 species), Rhipicephalus (two species), Haemaphysalis (three species) and Dermacentor (one species). Argasidae family is represented by 24 species and four genera: Ornithodoros (18 species), Antricola (three species), Argas (one species) and Nothoaspis (two species). In general, the immature stages (larvae and nymphs) of two or three host ticks feed on small mammals and birds, while adults exploit medium to large-sized hosts [17]. One-host species Dermacentor nitens and Rhipicephalus microplus, complete the life cycle mainly on large animals such as horses and cattle, respectively. Second Esser et al. [18] the diversity of ticks increases with the increase of diversity of hosts, inasmuch as these hematophagous arthropods rely on the hosts to complete their life cycles. Therefore, if we take into account the high diversity of hosts living in this biome and the amount of unexplored ecoregions, it is reasonable to infer that the diversity of ticks in the Amazon biome is insufficiently addressed. Thus, a review on the subject is necessary to point out the existing gaps and encourage new studies on ticks in the Brazilian Amazon.

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2. Hard ticks associated with amphibians and reptiles

The class Amphibia includes the orders Anura, Caudata, Gymnophiona, whereas the class Reptilia includes the orders Squamata, Testudines and Crocodylia. There are 331 amphibian and 550 reptile species in the Brazilian Amazon (Figure 1), although that faunal records are far from complete [2, 19]. Brazil has witnessed an increasing number of reports on tick parasitism of amphibians and reptiles over the past few years [20, 21, 22, 23, 24]. However, knowledge of this tick fauna as their hosts remains incomplete. To date, major tick-amphibian associations reported in Brazil are the ixodids Amblyomma dissimile, Amblyomma rotundatum, Amblyomma humerale, Amblyomma fuscum and Amblyomma goeldii [20, 21, 22, 23, 24], and the argasids Ornithodoros saraivai and Ornithodoros faccinii associated with species Cycloramphus boraceiensis and Thoropa miliaris, respectively [25, 26]. Occasional records on reptiles have also been reported for Ornithodoros mimon and Ornithodoros rietcorreai [22]. However, none of these argasids have been reported in the Amazon biome. Although the Brazilian Amazon has a high diversity of amphibians and reptiles, studies on ticks in association with these hosts are still rare, with a dominance of species A. dissimile, A. rotundatum and A. humerale [21, 22, 23, 27, 28].

The tick A. dissimile is constantly misidentified with the morphologically similar A. rotundatum. Recently, the distribution of A. dissimile in the country was reorganized, showing that this tick is restricted to the Pantanal and Amazon biomes [28]. Therefore, reports outside these biomes are considered misidentifications and must be viewed with caution. Most publications on this species are simple records of occurrence with some authors including data on prevalence and intensity of infestation both in the Amazon biome and elsewhere. According to Luz et al. [29] 12 (54.5%) out of 22 Rhinella marina toads captured in Amapá state, were parasitized by a total of 97 ticks (6 males, 39 females, 31 nymphs, 21 larvae) and mean intensity of 8.1 ticks per infested toad. In the Amazonian biome, A. dissimile is common on R. marina (Anura) and Boidae (Squamata) (Table 1). The experimental life cycle including pre-attachment periods for each parasitic stage lasts approximately 350 days, as reported by Schumaker et al. [43] who started a colony from one engorged female collected from the Amazonian biome. Ogrzewalska et al. [37] reported Rickettsia bellii and ‘Candidatus Rickettsia colombianensi’ in ticks collected from Bothrops atrox from Pará state. Luz et al. [29] reported ‘Ca. R. colombianensi’ in ticks collected on R. marina from Amapá state.

HostSpecieA. dissimileA. rotundatum
LNALNA
Amphibian (Anura)
BufonidaeRhinella marina3712M; 16F164133F[23, 29, 30, 31, 32, 33]
Rhinella major2F152F[33, 34, 35]
Rhaebo guttatus11F[23]
Rhinella margaritifera31F[23]
Rhinella gildae1[36]
LeptodactylidaeLeptodactylus pentadactylus1F[23]
Reptile
BoidaeBoa constrictor1703723M; 1346F121M; 77F[23, 30, 32, 33, 34, 36, 37, 38, 39, 40]
Corallus hortulanus31M[31, 34]
Eunectes murinus30521M; 3F[31, 40]
ViperidaeBothrops atrox41124M; 14F1M; 2F[32, 33, 36, 37]
Crotalus durissus1M; 1F[34]
Lachesis muta1[34]
ElapidaeMicrurus averyi3F[31]
Micrurus lemniscatus12M; 9F[31]
ColubridadeLeptophis ahaetulla3[33]
Chironius multiventris3[33]
Chironius scurrulus1M; 1F[34]
Chironius laevicollis1215M; 6F[31]
Mastigodryas boddaerti1[33]
Hydrodynastes gigas17F[30]
Helicops polylepis1[34]
Leptodeira annulata1[34]
Phimophis guerini1F[34]
Erythrolamprus reginae1[34]
Spilotes pullatus7242M; 9F[31]
Erythrolamprus reginae semilineatus1[34]
DipsadidaeXenodon severus8[40]
TestudinidaeChelonoidis denticulatus3M32M; 42F[31, 41]
Chelonoidis carbonaria11M; 1F11[32, 39]
PodocnemididaePodocnemis expansa1F[39]
Podocnemis unifilis1[39]
Trachemys dorbigni212F[39]
KinosternidaeKinosternon scorpioides2F[42]
ChelidaePlatemys platycephala5F[32]
TropiduridadeUranoscodon superciliosus76F[33]
Tropidurus sp.1M[38]
TeiidaeAmeiva ameiva41F[31, 34]
IguanidaeIguana iguana31118M; 69F2F[31, 36, 39, 40]
DactyoloidaeNorops auratus1[34]
GekkonidaeHemidactylus mabouia1[34]
AlligatoridaePaleosuchus trigonatus9M; 15F412F[31, 32]
Caiman crocodilus3[31, 39]
Total42189983M; 1496F221307F

Table 1.

Hosts of Amblyomma dissimile and Amblyomma rotundatum in the Brazilian Amazon.

The tick A. rotundatum is an obligate parthenogenetic species, although there are six reports of adult males, two males in the laboratory [44] and six in the Amazon region parasitizing Tropidurus sp., Boa constrictor, Iguana iguana, Chelonoidis denticulatus and B. atrox [30, 36, 44, 45, 46, 47]. Most publications on A. rotundatum are simple records of its occurrence with some additional data on prevalence and intensity of infestation in the Cerrado, Atlantic forest and Amazon biomes [22, 23, 31, 34, 48]. In the Brazilian Amazon, the families Bufonidae (Amphibian) and Boidae (Reptilia) are the most frequently parasitized by A. rotundatum, but there are reports on other species of Amphibian and Reptiles (Table 1). Recently, Gianizella et al. [31] reported A. rotundatum in different municipalities of the Amazonas state, on B. constrictor and several unknown hosts. The bioecology of this species under quasi-natural environment demonstrated a peak of larvae and nymphs in the dry season and females in the rainy season; however, there is a hypothesis of the absence of seasonality in this tick [48, 49]. Although A. rotundatum is a three-host tick on amphibians, it can behave as a two-host tick when feeding on snakes [50]. The complete experimental life cycle, including pre-attachment periods for each parasitic stage, ranged from 126 to 228 days on toads [51] or 56 to 163 days on snakes [50] and ulcerative lesions and hemorrhages after A. rotundatum feeding [48] were reported for ticks collected on toads from the Cerrado biome. Transmission of the hemogregarine Hemolivia stellata by R. marina collected in Belém, state of Pará was reported by Petit et al. [52]. This tick has also been found infected with R. bellii in the state of Amazon in the municipalities of Cacaulândia and Monte Negro, in the state of Rondônia; in the municipalities of Amapá (Ilha de Maracá) and Santana, in the state of Amapá; and in the municipality of Rio Branco, in the state of Acre [29, 53, 54].

Most reports of A. humerale mention the adult stage parasitizing species of tortoises, namely the “yellow-footed tortoise” C. denticulatus and the “red-footed tortoise” Chelonoidis carbonarius [27, 55]. There is also a record of A. humerale on Rhinoclemmys punctularia in central Amazon [56]. Labruna et al. [27] collected 215 adult ticks from six C. denticulatus and nine Chelonoidis sp. from state of Rondônia, with mean infestation of 14.3 ± 12.0 ticks per tortoise. In addition, seven engorged nymphs were collected on lizards. Morais et al. [57] collected 120 adult ticks from 18 (75%) out of 24 C. denticulatus captured in a transitional area between the biomes Cerrado and southwestern Amazon rainforest, in the state of Mato Grosso. The mean intensity of infestation was 6.7 ticks/tortoise. In both surveys, male ticks were mostly attached in clusters on the carapace whereas females were found attached to the tortoise skin. The sex ratio (males:females) for A. humerale were different in both surveys, 10.3:1 [27] and 1.1:1 [57]. There is one additional record of two nymphs on Paleosuchus trigonatus (Crocodylia) [32]. The life-cycle in the laboratory, including pre-feeding periods for each of the parasitic stages, could be completed in an average period of ca. 200 days [58]. Rickettsia bellii and Rickettsia amblyommatis have been detected in A. humerale [42, 53]. The records of A. fuscum in association with amphibians and reptiles are rare in Brazil. Dantas-Torres et al. [59] collected one male tick in one out of 490 caimans (Caiman latirostris and Paleosuchus palpebrosus) trapped in the Atlantic rainforest biome in Pernambuco state, north-eastern Brazil. Amblyomma goeldii has been recorded only in the Amazonas state. Martins et al. [60] reported two males collected on B. constrictor and recovery of ≈100 (20%) engorged larvae out of ≈500 unfed larvae experimentally infested on a B. constrictor.

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3. Hard ticks associated with wild birds

The importance of birds to maintain biodiversity and ecological balance of nature is notorious [61]. Due to migration, wild birds are of concern to human and animal health worldwide [62] because they can carry infected ticks over long distances, directly influencing the epidemiology of tick-borne diseases in animals and humans. In addition, wild birds themselves can be reservoirs of Borrelia burgdorferi sensu lato, and potentially to Anaplasma phagocytophilum and Rickettsia spp. [62, 63]. Wild birds play an important role in maintaining and dispersing immatures (larvae and nymphs) of several tick species into new locations [61, 64].

Of the total genera of ticks described in Brazil, five have at least one species recorded in association with wild birds. The most common are the hard ticks of the genera Amblyomma, Haemaphysalis and Ixodes [61, 64]. There are also occasional reports of the genera Rhipicephalus and Ornithodoros. Ticks of the genus Amblyomma are the most common on wild birds in the Brazil including the Amazon biome, exclusively for the larvae and nymphs [61, 64]. Adult ticks are only occasionally found on wild birds, with the exception of Ixodes paranaensis and Ixodes auritulus, which have the entire cycle synchronized with birds [65]. In Brazil, there are no reports of wild birds as a source of pathogens transmitted by ticks to humans, but they can serve as disperser hosts for vectors of Brazilian Spotted Fever (BSF) as Amblyomma sculptum, Amblyomma aureolatum and Amblyomma ovale, in the larvae and nymph stages [64]. Therefore, wild birds act indirectly in the epidemiology of BSF by dispersing and maintaining their vectors in nature.

Over more than 1,900 birds recorded in Brazil, approximately 1,300 reside in the Brazilian Amazon, with a 20% of endemism [66] (Figure 1). Of these, approximately 7% are migrants from the northern hemisphere and southern South America, including migrations from other Brazilian biomes [67]. To date, 86 bird species of Brazilian Amazonian have been recorded in association with at least one tick species (Table 2). This is equivalent to approximately only 7% of bird species found in this biome and 5% of the total birds recorded in Brazil (Table 2). Similar to other studies regarding tick-bird associations in Brazil [73, 74, 75], Passeriformes birds were the most parasitized in the Amazon biome, including 14 families and 72 species (Figure 2 and Table 2). In this group, the greatest diversity of parasitized birds was Thamnophilidae (20 species) followed by Dendrocolaptidae (16 species) and Tyrannidade (10 species) (Figure 2). The least parasitized families were Conopophagidae, Furnariidae, Xenopidae, Tityridae, Cardinalidae, Columbidae, Cuculidae, Momotidae, Capitonidae, Ramphastidae, Psittacidae, Accipitridae and Falconidae with only one species of parasitized bird each (Figure 2 and Table 2). Non-Passerines were represented by 10 different orders and 11 families, with emphasis on Bucconidae with three species (Figure 2 and Table 2). To date, approximately 1,068 specimens of ticks have been collected from birds in the Brazilian Amazon, in the stages of larvae (884/83%), nymphs (184/17%) and no adults (Figure 3). These are included in the genera Amblyomma and Haemaphysalis. The genus Amblyomma was the dominant with eight species (Table 2). The greatest diversity of ticks was reported for the Thamnophilidae family with seven species: A. longirostre, A. nodosum, A. humerale, A. calcaratum, A. geayi, A. coelebs and Haemaphysalis juxtakochi. The Dendrocolaptidae family was the second with five species: A. longirostre, A. nodosum, A. humerale, A. calcaratum and A. geayi (Figure 2 and Table 2).

HostsTicksReferences
SpeciesStages
LLNN
PasseriformesThamnophilidaeThamnomanes schistogynusA. humerale
A. nodosum
1
1
[68]
Thamnophilus doliatusA. nodosum2[68]
Thamnophilus schistaceusA. nodosum
Amblyomma sp.
22[68]
Thamnophilus aethiopsA. calcaratum
A. longirostre
5
1
[68]
Myrmelastes hyperythrusA. nodosum9[68]
Sciaphylax hemimelaenaA. nodosum1[68]
Schistocichla leucostigmaA. humerale
Amblyomma sp.
4
5
[69]
Phlegopsis nigromaculataA.coelebs
A. longirostre
A. nodosum
Amblyomma sp.
1
1
24
5[68, 69]
Hypocnemis subflavaAmblyomma sp.3[70]
Hylophylax naeviusH. juxtakochi
A. humerale
A. longirostre
A. calcaratum
Amblyomma sp.
1
3
1
8
1
2
1
[69]
Hylophylax punctulatusAmblyomma sp.1[69]
Thamnomanes caesiusA. geayi
A. longirostre
A. humerale
Amblyomma sp
1
3
4
2
1
[69, 71]
Hylophylax poecilinotusA. geayi
A. humerale
A. longirostre
Amblyomma sp.
H. juxtakochi
1
1
3
22
1
1
1
1
[69]
Myrmornis torquataAmblyomma sp.3[69]
Myrmotherula hauxwelliAmblyomma sp.1[69]
Myrmotherula longipennisA. longirostre
Amblyomma sp.
3
3
[69]
Pyriglena leuconotaA. coelebs
A. humerale
A. longirostre
Amblyomma sp.
1
1
9
4
1[69]
Myrmoborus myotherinusA. longirostre1[69]
Epinecrophylla leucophthalmaA. longirostre1[71]
Willisornis poecilinotusA. calcaratum1[71]
ConopophagidaeConopophaga auritaAmblyomma sp.1[69]
ScleruridaeSclerurus cf. rufigularisA. humerale1[68]
Sclerurus caudacutusA. humerale1[69]
FurnariidaeAutomolus paraensisAmblyomma sp.1[69]
DendrocolaptidaeDendrocincla merulaA. longirostre
Amblyomma sp.
7
34
1[68, 69, 71]
Dendrocincla fuliginosaAmblyomma sp.10[31, 70]
Deconychura longicaudaA. longirostre
Amblyomma sp.
4
39
1[69, 71]
Deconychura stictolaemaA. longirostre
Amblyomma sp.
1
1
1[69]
Dendrocolaptes hoffmannsiA. calcaratum
A. geayi
A. humerale
A. longirostre
Amblyomma sp.
1
2
4
39
59
2
1
3
[69]
Dendrocolaptes certhiaA. longirostre1[71]
Glyphorynchus spirurusA. longirostre1[71]
Glyphorynchus spirurusA. geayi
A. longirostre
Amblyomma sp.
1
6
16
1
2
[69]
Hylexetastes brigidaiA. geayi
A. longirostre
Amblyomma sp.
1
6
21
2[69]
Sittasomus griseicapillusA. humerale
Amblyomma sp.
21[70]
Xiphorhynchus guttatusA. longirostre
A. nodosum
2
1
[68]
Xiphorhynchus guttatoidesA. humerale
Amblyomma sp.
12[70]
Xiphorhynchus elegansA. longirostre
Amblyomma sp.
3
2
2[69]
Xiphorhynchus ocellatusA. calcaratum1[71]
Xiphorhynchus pardalotusAmblyomma sp.3[31]
Dendroplex picusA. longirostre
A. nodosum
3
3
[68, 70]
XenopidaeXenops minutusA. nodosum2[69]
PipridaePipra filicaudaA. geayi
Amblyomma sp.
1[68, 70]
Pipra fasciicaudaA. longirostre
A. nodosum
Amblyomma sp.
1
8
7[68]
Machaeropterus pyrocephalusA. longirostre1[68]
Dixiphia pipraA. geayi
A. longirostre
1
1
1
1
[69]
Lepidothrix nattereriAmblyomma sp.1[71]
RhynchocyclidaeLeptopogon amaurocephalusA. geayi1[68]
Rhynchocyclus olivaceusA. geayi
A. humerale
A. longirostre
A. nodosum
Amblyomma sp.
1
1
4
2
1
17
[68]
Todirostrum maculatumA. nodosum1[68]
Poecilotriccus latirostrisA. nodosum
Amblyomma sp.
63[70]
Hemitriccus flammulatusAmblyomma sp.1[70]
TyrannidaeMyiozetetes similisA. nodosum1[68]
Empidonax alnorumA. nodosum
A. longirostre
41[68]
Platyrinchus saturatusAmblyomma sp.1[69]
Hemitriccus minorA. longirostre1[69]
Mionectes macconnelliA. longirostre
Amblyomma sp.
4
5
[69]
Attila spadiceusA. geayi
Amblyomma sp.
1
3
[69]
Myiobius barbatusA. longirostre3[69]
Onychorhynchus coronatusA. longirostre
Amblyomma sp.
3
6
[69]
Ramphotrigon megacephalumA. nodosum
Amblyomma sp.
13[70]
Knipolegus poecilocercusAmblyomma sp.1[71]
TroglodytidaePheugopedius genibarbisA. nodosum
Amblyomma sp.
3631[68]
Microcerculus marginatusAmblyomma sp.3[69]
TityridaeSchiffornis turdinaA. longirostre
Amblyomma sp.
3
14
[69]
TurdidaeTurdus hauxwelliA. longirostre2[68]
Turdus sanchezorumA. longirostre1[68]
Turdus ignobilisA. geayi
A. nodosum
A. longirostre
Amblyomma sp.
21
1
1
[68]
Turdus amaurochalinusAmblyomma sp.1[70]
Turdus albicollisA. longirostre
A. coelebs
Amblyomma sp.
2
3
3[31, 69]
ThraupidaeRamphocelus carboA. nodosum
A. longirostre
Amblyomma sp.
4415
4
[30, 68, 70, 71]
Tachyphonus surinamusA. humerale
A. longirostre
Amblyomma sp.
1
1
5
CardinalidaeCyanoloxia cyanoidesAmblyomma sp.1[71]
ColumbiformesColumbidaeColumbina talpacotiA. nodosum1[68]
CuculiformesCuculidaeCrotophaga majorA. nodosum1[68]
CoraciiformesMomotidaeMomotus momotaA. longirostre
A. humerale
1
1
[68, 70]
PiciformesCapitonidaeCapito auratus insperatusA. nodosum
A. longirostre
2
1
[68]
RamphastidaeRamphastos vitellinusA. geayi3[31]
Pteroglossus bitorquatusA. longirostre1[30]
GalbuliformesBucconidaeMonasa nigrifronsAmblyomma sp.1[70]
Malacoptila rufaAmblyomma sp.1[69]
Galbula cyanicollisAmblyomma sp.2[69]
PsittaciformesPsittacidaePrimolius maracanaA. dissimile1[72]
AccipitriformesAccipitridaeHarpia harpyjaA. cajennense16[41]
H. juxtakochi1[41]
CariamiformesCariamidaeCariama cristataA. cajennense5[39]
GalliformesCracidaePenelope superciliarisA. cajennense11[42]
FalconiformesFalconidaeMicrastur ruficollisA. longirostre1[71]
Total884184

Table 2.

Ticks identified on wild birds in the Brazilian Amazon biome.

Figure 2.

Diversity of hard ticks parasitizing wild birds from the Brazilian Amazon.

Figure 3.

Distribution of studies reporting the association of hard ticks on wild birds from the Brazilian Amazon.

Overall, A. longirostre and A. nodosum are the two most common species on wild birds in the Brazilian Amazon [68, 69, 70, 71] (Figure 4 and Table 2). The tick A. longirostre was the most common, recorded in 12 families and 40 species of birds (36 Passerines and 4 non-Passerines) (Figure 2). Amblyomma longirostre has been treated as an arboreal tick, with immatures parasitizing birds and adults parasitizing rodents Erethizontidae (e.g., Sphiggurus spp.) [73, 76]. This tick was also the most abundant with 110 larvae and 39 nymphs. Amblyomma longirostre was found in co-infestation with the following species: A. calcaratum, A. nodosum, A. coelebs, A. humerale, A. geayi and H. juxtakochi (Table 2). In addition, as it is frequent on birds, A. longirostre is popularly known as “bird tick” or “bird earring” [77]. Amblyomma nodosum was the second most common species collected on 12 families and 22 species of birds. This tick was recorded in co-infestation with A. longirostre, A. coelebs, A. humerale and A. geayi (Table 2 and Figures 2 and 4). The birds most infested by A. nodosum were Rhynchocyclus olivaceus and Ramphocelus carbo with 17 and 15 nymphs, respectively. These birds inhabit the forest understory and visit the soil occasionally [67]. As Xenartha mammals (Myrmecophaga tridactyla, Tamandua tetradactyla) are the primary hosts of A. nodosum [17], it is believed that the low areas of the understory are a major source of infestation. Interestingly, T. tetradactyla may have arboreal habits [78], which helps to explain the presence of A. nodosum also on birds of different forest strata.

Figure 4.

Hard tick species parasitizing wild birds from the Brazilian Amazon.

To date, of the total of ticks collected, 736 (70%) were larvae identified as Amblyomma sp. due to lack of reliable tools for larval identification, thus, indicating that the diversity of ticks on birds of the Amazon may be underestimated. Luz et al. [75], using molecular biology, identified more than 90% of the larvae collected from birds in the Atlantic Forest biome, reporting the greatest diversity of ticks on birds in a single study in Brazil and description of the new tick Amblyomma romarioi [14]. Therefore, the identification of all larvae by molecular biology in addition to morphological identification is extremely important to ascertain the diversity of ticks in the Amazon biome.

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4. Hard ticks associated with wild and domestic mammals

The fauna of wild mammals in Brazil is quite diverse and more than half lives in the Amazon biome [79]. Like birds, amphibians and reptiles, mammals play an important role in preserved or anthropized ecosystems. Therefore, the knowledge of the local diversity of wild mammals, and their relationship with ticks is considered an important tool for public conservation policies and consequently for public health. The alteration of wild habitats can determine changes in the patterns of parasitic specificity, inducing tick species to seek new groups of hosts, increasing the risk of disease transmission [79, 80]. Some wild mammals (small, medium and large) are directly or indirectly involved in the transmission cycles of many tick-borne pathogens worldwide, including Anaplasma spp., Babesia spp., Borrelia spp., and Rickettsia spp. [80, 81]. In Brazil, the main zoonosis transmitted by ticks is Brazilian Spotted Fever caused by the bacterium Rickettsia rickettsii, which has the rodent Hydrochoerus hydrochaeris as its main amplifier. In addition, there is evidence that marsupials and small rodents can serve as amplifier hosts for R. rickettsii in nature [82].

In Brazil there are approximately 755 species of mammals distributed in all its six biomes, including the Amazon biome [78, 79]. Of the total mammal species, 41% (≅ 311 species) occur in the Amazon biome (Figure 1) [2, 76]. These vertebrates are distributed in 11 orders, 51 families and 249 genera [78, 79]. Among the families, Cricetidae is the most diverse, with 144 species [78, 79]. The vast majority of tick species, including all life stages, in Brazil have records on wild mammals of different sizes [17]. In general, small mammals of the orders Rodentia and Didelphimorphia are those that have a greater number of studies in association with ticks, especially the families Cricetidae and Didelphidae [17, 82]. In general, medium and large mammals are parasitized by ticks in all stages (larva, nymph and adult), while in small mammals the stages of larva and nymph are more common. In this last group of hosts we can highlight the cricetids Akodon spp., Calomys spp., Oligoryzomys spp. and Nectomys spp. as the most parasitized by immature ticks in nature.

Nine orders and 24 families of wild mammals have representatives in association with ticks in the Brazilian Amazon (Figure 5). Rodentia was the most diverse with 16 species of mammals, followed by the orders Carnivora (13 species) and Didelphimorphia (12 species) (Figure 5). However, it was the family Didelphidae that presented a greater number of parasitized species, followed by Dasyproctidae (seven species) and Mustelidae (four species). These records corroborate with numerous studies of tick parasitism on wild animals from South America, with emphasis on the orders Rodentia and Didelphimorphia [17, 82, 83].

Figure 5.

Diversity of hard ticks parasitizing wild mammals from the Brazilian Amazon.

Hard ticks parasitizing wild mammals in the Brazilian Amazon are represented by five genera: Amblyomma, Ixodes, Haemaphysalis, Dermacentor and Rhipicephalus. Of these, the genus Amblyomma was more frequently recorded with 23 species (Figure 5). The orders Rodentia, Pilosa and Didelphimorphia are hosts for highest diversity to Amblyomma species 17, 15 and eight, respectively. All these species are also recorded on a variety of wild mammals in Brazil [83, 84, 85, 86, 87], except for A. rotundatum and A. dissimile, which are more specific ticks of cold-blooded animals (Amphibians and Reptiles), although there are occasional reports on mammals in South America [20, 83]. Amblyomma humerale, of which the adult stage is more specific to tortoises, immature stages have been found on a variety of small mammals, reptiles and birds [17, 68, 71, 83].

The second most common genus in the Amazon is Ixodes, with six reported species: Ixodes amarali, Ixodes bocatorensis, Ixodes lasallei, Ixodes luciae, Ixodes schulzei and Ixodes spinosus (Table 3). Although there are two exclusive species on birds in Brazil [65], all species recorded in the Brazilian Amazon parasitize mainly wild mammals [13, 16, 31, 32, 88, 99, 102]. Ixodes spp. were found on families Didelphidae, Dasyproctidae, Cricetidae, Myrmecophagidae, Bradypodidae and Cyclopedidae (Figure 5 and Table 3). In general Ixodes ticks mainly parasitize rodents (e.g., Cricetidae) in the larvae and nymph stages, with adults feeding mostly on marsupials (e.g., Didelphis spp., Monodelphis spp.) [17, 83], and agoutis (e.g., Dasyprocta) [13, 16]. Most species were found parasitizing Monodelphis glirina (I. amarali, I. schulzei, I. luciae) and Monodelphis touan (I. amarali, I. schulzei), with some reports of I. amarali on the rodent Hylaeamys megacephalus [30, 38, 92, 99, 100]. Also on rodents the species I. spinosus, I. lasallei and I. bocatorensis have been recorded [30, 31, 38], although these previous records referred to them erroneously as Ixodes fuscipes, which according to more recent data, does not occur in the Amazon biome (Figure 5 and Table 3) [13, 16].

Tick speciesDomestic mammalsWild mammalsStatesReferences
Amblyomma auriculariumCabassous unicinctus4, Dasypus novemcinctus4,5,7, Dasypus septemcinctus4,9, Euphractus sexcinctu4,9, Galactis cuja4,9, Galictis vittata4, Lycalopex vetulus9, Myrmecophaga tridactyla9, Pecari tajacu9, Tamandua tetradactyla4, Thrichomys inermis4MA4, MT5, RO7, TO9[30, 32, 36, 39]
Amblyomma cajennense sensu strictoEquus caballus4,5,6,7,8,9, Sus scrofa4,9, Canis familiaris4,9, Bubalus bubalis7Caluromys philander5, Cerdocyon thous5, Didelphis marsupialis5,6Dasyprocta azarae5, Hydrochoerus hydrochaeris5, Mazama gouazoubira4, Metachirus nudicaudatus4, Myrmecophaga tridactyla5,9, Nasua nasua5, Panthera onca5, Pecari tajacu5, Pteronura brasiliensis3, Tapirus terrestris5, Tayassu pecari5AM3, MA4, MT5, PA6, RO7, RR8, TO9[32, 36, 42, 88, 89, 90, 91]
Amblyomma calcaratumMyrmecophaga tridactyla7, Tamandua tetradactyla45,6MA4, MT5, PA6; RO7[36, 38, 42]
Amblyomma coelebsEquus caballus7Agouti paca7, Cuniculus paca6, Dasyprocta azarae5, Dasyprocta sp7; Didelphis albiventris5, Didelphis marsupialis3,5, Hydrochoerus hydrochaeris7, Metachirus myosuros5, Nasua nasua5, Neacomys spinosus5, Panthera onca5, Sapajus macrocephalus3, Tayassu pecari6, Pecari tajacu7, Tapirus terrestris3,5,7AM3, MT5, PA6, RO7[30, 31, 32, 38, 42, 88]
Amblyomma dissimileBradypus tridactylus3, Choleopus didactylus3, Coendou sp3, Dasyprocta leporina3AM3[31, 36, 40]
Amblyomma dubitatumHydrochoerus hydrochaeris1,5,7, Tamandua tetradactyla9AC1, MT5, RO7, TO9[30, 32, 39, 54]
Amblyomma geayiAlouatta nigerrima6, Artibeus lituratus3, Bradypus tridactylus3,6, Bradypus variegatus1,3,4,6,9, Caluromys lanatus3, Choloepus hoffmanni7, Choloepus didactylus3,7, Cyclopes didactylus3, Didelphis marsupialis6, Philander opossum3, Proechimys sp3, Oecomys sp6, Saguinus bicolor3, Tamandua tetradactyla3AC1, AM3, MA4, PA6, RO7, TO9[30, 31, 33, 36, 39, 40, 42, 92]
Amblyomma goeldiiTamandua tetradactyla,3,6, Bradypus tridactylus3AM3, PA6[31, 40, 42]
Amblyomma humeraleBradypus tridactylus3, Chrotopterus auritus3, Cyclopes didactylus7, Dasypus novemcinctus5,6, Didelphis marsupialis3,5,6, Hydrochoerus hydrochaeris1, Marmosa constantiae5, Marmosa sp3, Metachirus myosuros5, Philander opossum3, Proechimys roberti5, Tamandua tetradactyla3,6AC1, AM3, MT5, PA6, RO7[30, 31, 32, 33, 38, 39, 40, 42, 54, 88]
Amblyomma incisumTapirus terrestris7RO7[38, 93]
Amblyomma latepunctatunTapirus terrestris3,6,7, Tayassu pecari3, Dasyprocta fuliginosa3, Didelphis marsupialis3AM3; PA6; RO7[31, 38, 93]
Amblyomma longirostreCoendou sp3, Coendou prehensilis6,7, Coendou nycthemera6AM3, PA6, RO7[30, 31, 33, 40, 42]
Amblyomma naponenseDasyprocta fuliginosa3, Galictis sp3, Hydrochoerus hydrochaeris1, Mazama gouazoubira4, Myoprocta acouchy3, Tapirus terrestris7, Tayassu pecari3,4AC1, AM3, MA4, RO7[31, 36, 38, 54]
Amblyomma nodosumTamandua tetradactyla4,5,6,7,9; Bradypus variegatus9, Myrmecophaga tridactyla9MA4, MT5, PA6, RO7, TO9[30, 32, 38, 39, 40, 42]
Amblyomma oblongoguttatumCanis familiaris4,6,9, Sus scrofa7Agouti paca7, Cuniculus paca9, Dasyprocta sp7, Myrmecophaga tridactyla9, Tayassu tacaju7, Tayassu pecari3,5,6,7, Dasyprocta fuliginosa3, Mazama americana3, Tapirus terrestris5,7, Panthera onca7AM3, MA4, MT5, PA6, RO7, TO9[31, 32, 38, 39, 42, 91, 94, 95]
Amblyomma ovaleCanis familiaris3,4,9, Sus scrofa7Panthera onca,3,5,7,9, Tapirus terrestres3, Leopardus pardalis3, Proechimys quadruplicatus3, Proechimys sp3, Tapirus terrestres3, Pauxi tuberosa5, Puma concolor5, Procyon cancrivorus7, Tayassu tacaju7, Tayassu pecari7, Agouti paca7, Dasyprocta sp7, Eira barbara7, Nasua nasua7, Cerdocyon thous9AM3, MA4, MT5, RO7, TO9,[30, 31, 32, 38, 39, 42, 91, 94]
Amblyomma pacaeCanis familiaris7Hydrochoerus hydrochaeris1, Cuniculus paca5, Tamandua tetradactyla6, Monodelphis glirina6, Didelphis marsupialis7AC1, MT5, PA6, RO7[38, 42, 54, 92]
Amblyomma parkeriDidelphis marsupialis5MT5[32]
Amblyomma romitiiHydrochoerus hydrochaeris5,6,7MT5, PA6, RO7[32, 41, 96]
Amblyomma rotundatumHydrochoerus hydrochaerisi, Xenodon merremii9RO7, TO9[30, 31, 32, 33, 36, 38, 39, 41, 42, 54]
Amblyomma scalpturatumCanis familiaris7, Sus scrofa7Agouti paca7, Dasyprocta fuliginosa3, Didelphis marsupialis5, Pecari tajacu5,7, Tapirus terrestris5,7, Hydrochoerus hydrochaeris7AM3, MT5, RO7[30, 31, 32, 38, 88]
Amblyomma sculptumEquus caballus,4,7,9Myrmecophaga tridactyla9MA4, RO7, TO9[88]
Amblyomma variumBradypus tridactylus3, Bradypus sp3, Bradypus variegatus7Choleopus didactylus3,7, Choleopus hoffmanni3,7, Choloepus sp7Dasyprocta aguti3, Tamandua tetradactyla3AM3, PA6, RO7[30, 31, 33, 38, 40, 97]
Dermacentor nitensBos taurus4, Canis familiaris4,7, Equus caballus,4,7,8,9Capra hircus4, Ovis aires4Agouti paca7, Mazama gouazoubira9MA4, RO7, RR8, TO9[36, 38, 39, 95, 98]
Ixodes amaraliHylaeamys megacephalus6, Monodelphis glirina6, Monodelphis touan6,PA6[99]
Ixodes bocatorensisBradypus tridactylus3, Cyclopes didactylus3, Dasyprocta leporina3, Tamandua tetradactyla3AM3[16]
Ixodes spinosusDasyprocta sp7, Myoprocta pratti1RO7, AC1[13]
Ixodes lasalleiDasyprocta variegata7RO7[16]
Ixodes luciaeDidelphis marsupialis1,3,4,7, Marmosa murina6, Marmosa demerarae3, Monodelphis sp7, Oecomys sp.7, Orysomys sp.7, Oligorysomys sp.7, Philander opossum6AC1, AM3, MA4, PA6, RO7[31, 36, 38, 100]
Ixodes schulzeiMonodelphis touan6PA6[92]
Haemaphysalis juxtakochiCanis familiaris4,7,Mazama americana3,9, Mazama p7, Dasyprocta azarae5; Dasyprocta fuliginosa3,AM3, MA4, MT5; RO7, TO9[31, 36, 38, 39, 42]
Rhipicephalus microplusBos taurus4,7,8,9, Canis familiaris4,7,9, Felis catus7, Equus caballus,4,7,8,9, Capra hircus4,7, Ovis aires4Alouatta puruensis7, Mazama gouazoubira5,9, Mazama sp.7, Tapirus terrestres7,9, Tayassu sp7MA4, MT5; RO7, RR8; TO9[32, 33, 36, 38, 39, 95, 98]
Rhipicephalus sanguineus sensu latoCanis familiaris1,3,4,7,9Bradypus tridactylus3, Galictis cuja4, Saquinus bicolor3AC1, AM3, MA4, RO7[30, 31, 32, 33, 36, 38, 39, 95, 98, 101]

Table 3.

Records of ticks in the Amazon biome, Brazil, according to tick species, hosts (domestic and wild animals), states, references.

Acre – AC.


Amapá – AP.


Amazonas – AM.


Maranhão – MA.


Mato Grosso – MT.


Pará – PA.


Rondônia – RO.


Roraima – RR.


Tocantins – TO.


In general, the greatest diversity of ticks was recorded on T. tetradactyla with 10 species, followed by the rodent H. hydrochaeris with nine species. These records indicates the importance of these hosts for maintaining local tick diversity, in addition to act as dispersers of these ectoparasites. Additional hosts have also been shown to be important in maintaining diversity of tick in the Amazon: Tapirus terrestris, Tayassu pecari, Pecari tajacu, Agouti paca, Dasyprocta fuliginosa, Bradypus tridactylus, Bradypus variegatus, Panthera onca, Nasua nasua, Choleopus didactylus, Choloepus hoffmanni, Cyclopes didactylus, Dasyprocta azarae, Dasyprocta leporina, Philander opossum, M. glirina, M. touan, Mazama gouazoubira, Mazama americana and M. tridactyla (Table 3), because they are parasitized by more than one species of ticks. There is also a record of A. cajennense s.s. on Pteronura brasiliensis a semi-aquatic animal [89].

Interestingly, three species of ticks commonly found on domestic animals have also been found parasitizing wild animals: Rhipicephalus sanguineus sensu lato, R. microplus and D. nitens. Although occasional, the encounter of these species of ticks on wild animals is possible, especially when wild animals coexist with domestic animals infested by ticks (e.g., pastures, corrals, houses). A total of 11 species of ticks have been recorded parasitizing domestic animals in Amazon (Table 3).

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5. Hard ticks associate with humans

Spotted fevers caused by R. rickettsii and Rickettsia parkeri are currently the only confirmed tick-borne disease affecting humans in the country, and A. sculptum, A. aureolatum, A. ovale are the main vectors. The disease is severe and highly lethal when caused by the bacterium R. rickettsii (vectors A. sculptum and A. aureolatum) and moderate, non-lethal, when caused by R. parkeri, vectored mainly by A. ovale [10]. Only A. sculptum and A. ovale have been recorded in the Brazilian Amazon, the first in rare reports and the second frequently recorded and populations established in this biome. In fact, considering only the tick adult stage, A. ovale has been reported as the most common human-biting tick in the Amazon [38].

In the last century, papers about ticks on human beings have been published in the Brazilian Amazon, however these studies are fragmented and scarce. At least 14 species of hard ticks have already been found and documented parasitizing humans within the limits of the Brazilian Amazon. Of these, the vast majority (11 species) belong to the genus Amblyomma: A. cajennense s.s., A. coelebs, A. dissimile, A. latepunctatum, A. naponense, A. oblongoguttatum, A. ovale, A. romitii, A. rotundatum, A. scalpturatum and A. sculptum. The other three species belong to the genus Rhipicephalus, including R. microplus and R. sanguineus s.l., and the genus Haemaphysalis with only H. juxtakochi. The public health importance of human–tick associations in the Amazon biome is unclear and further research are needed to clarify the issue.

Nymphs of H. juxtakochi have been reported on humans in the states of Rondônia (municipality not precisely indicated) and Amazonas, in the municipality of Santa Isabel do Rio Negro [31, 38]. H. juxtakochi has been found infected with the bacterium Rickettsia rhipicephali in the Amazon region, more precisely in the municipalities of Monte Negro and Confresa, states of Rondônia and Mato Grosso, respectively [42, 93]. Human parasitism by R. microplus was expected, since this species can parasitize humans when it comes into direct contact with domestic cattle, as reported by [38]. Therefore, its importance is much more economical, causing severe losses to livestock in the country than for public health.

Despite sporadic records of R. sanguineus s.l. on humans in Brazil, this association in the Brazilian Amazon requires confirmation. Records of approximately 4,020 R. sanguineus s.l. (larva, nymph, and adult), supposedly collected on humans, in the state of Pará by Serra-Freire et al. [103] do not corroborate the common findings in country. The bioecology of this endophilic and introduced tick is well studied. In other countries, R. sanguineus s.l. is vector of some zoonotic agents for humans (Rickettsia conorii, Rickettsia massiliae and R. rickettsii) [83]. Adults of A. cajennense s.s. have been reported on humans in the municipality of Monte Alegre (Pará state) [90]. Reports of Amblyomma cajennense sensu lato parasitizing humans published by Martins et al. [90] in the municipalities of Sinop and Tucuruí in the states of Mato Grosso and Pará, is possibly A. cajennense s.s. taking into account the area of ​​occurrence of this species. This tick is aggressive to humans. In the Amazon biome the R. bellii bacterium was detected in this species in Mato Grosso state and R. amblyommatis in Mato Grosso, Maranhão and Rondônia state [32, 42, 53, 83, 88, 90, 91, 104, 105].

Nymphs and adult of A. coelebs were found on humans in Rondônia state [38]. An adult of this tick was found on human in Roraima state, municipality of Caroebe [106]. The nymph and adult stages of A. colelebs were also found on humans in Amazonas state, in the municipalities of Coari, Fonte Boa, Presidente Figueiredo and Santa Isabel do Rio Negro [31, 107]. There are reports of infection by R. amblyommatis in A. coelebs in the Amazon region in the states of Rondônia and Mato Grosso, respectively [32, 53, 88]. Adult of A. dissimile was recorded on humans in the Maicurú River/Amazon biome, located in Pará state [106]. Adults of the species A. latepunctatum have been reported on humans in Coari and Santa Isabel do Rio Negro, both municipalities located in the state of Amazonas [31].

Adults of the tick A. naponense (published as Amblyomma mantiquirense) were found on humans in the state of Pará (municipality not reported) [108]. Human parasitism also by adults was later reported on the Maicurú River, located in this same state [106]. However, nymphs have been found on humans in the states of Rondônia (municipality not specified precisely) and Amazonas, in the municipalities of Coari and Santa Isabel do Rio Negro [31, 38]. The bacteria R. bellii and Rickettsia sp. strain PA were identified in this species in the Amazon region of the municipalities of Santarém and Rurópolis, in the state of Pará [42]. Rickettsia sp. strain Tapirapé was found in this tick in the municipalities of Confresa and Rio Branco, in the states of Mato Grosso and Acre, respectively [42, 54].

Adults of the species A. oblongoguttatum were recorded parasitizing humans in the state of Pará, in the Maicurú River and in the municipality of Uruará [106, 108, 109]. Human parasitism by nymphs and adults of this tick was recorded in the state of Rondônia (municipality not specified with precision) [38]. However, the nymphal stage of this species was later recorded on humans in the municipality of Monte Negro in the same state [106]. Human parasitism by adult of this tick was also recorded in the municipality of Caroebe, state of Roraima [106]. Nymphs and adults of this species have been recorded parasitizing humans in three municipalities (Coari, Manacapuru and Santa Isabel do Rio Negro), all located in the state of Amazonas [31, 106, 107]. On the other hand, the life cycle of this tick has already been studied under laboratory conditions [110]. The bacteria R. bellii and R. amblyommatis were detected in this species in the Amazon in the municipalities of Governador Jorge Teixeira and Pimenta Bueno, in the state of Rondônia [53, 105].

Adults of the tick A. ovale have been reported to parasitize humans in several areas of the state of Rondônia [38]. As previously reported in this chapter, adults of A. ovale parasitize mainly domestic and wild carnivores, while immature (larva and nymph) parasitize rodents of the families Cricetidae and Echimyidae, with sporadic reports on wild birds [17, 75, 83]. This preference for such host groups was observed in the laboratory [111]. This tick is a vector of the protozoan Hepatozoon canis and the bacterium R. parkeri, agents of importance in veterinary and human medicine, respectively [83]. In the Amazon region, the bacterium R. bellii was identified in this species in the municipalities of Governador Jorge Teixeira and Monte Negro, in the state of Rondônia; and in the municipality of Cururupu, in the state of Maranhão [53, 91].

The adult stage of the species A. romitii (published as Amblyomma tasquei) was found parasitizing humans in the north of the state of Pará (municipality not reported) [108]. In this same state, the larval and adult stages of this tick were found on humans in the municipality of Rurópolis [96, 112]. The life cycle of this tick was studied under laboratory conditions [113].

Parasitism by adults of A. rotundatum was recorded in the municipality of Belém in the state of Pará on a human who worked in frequent contact with reptiles in the Zoobotanical Park of the Museu Paraense Emílio Goeldi [114].

Adults of the A. scalpturatum have been reported to parasitize humans in the state of Pará (municipality not reported) [108], and in the Maicurú River located in this state [93, 106]. Human parasitism by the nymphal and adult stages of this species has been reported in the states of Mato Grosso (municipality of Jauru) and Rondônia (municipality not precisely indicated), however in this latter state it was not specified whether these adult ticks were fixed or walking on humans [38, 93]. The nymphal stage was also collected from a human who was probably infested with this tick in the municipality of Porto Velho in the state of Rondônia [115]. The nymph and adult stages of this species were also found parasitizing humans in the state of Amazonas, in the municipalities of Coari, Fonte Boa, Jutaí, Presidente Figueiredo and Santa Isabel Rio Negro [31, 107]. In the Amazon biome, two species of rickettsiae (R. bellii and R. amblyommatis) were detected in A. scalpturatum, in the municipalities of Governador Jorge Teixeira and Sinop, states of Rondônia and Mato Grosso, respectively [53, 88].

Human parasitism by adults of A. sculptum was recorded in the municipality of Jauru in the state of Mato Grosso [90]. The Jauru territory comprises 90% of the Amazon biome and 10% of the Cerrado biome, so this human record in this region is in accordance with the transition area of ​​the occurrence of this species in sympatry with A. cajennense s. s. [90]. The bioecology of this native tick has been extensively studied due to its aggressive parasitism towards domestic animals and humans in the Brazilian territory. In the geographical area in which this species occurs, it completes an annual generation, with larvae occurring mostly during autumn, nymphs during winter, and adults during spring and summer, with larval behavioral diapause being the main regulating factor of its life cycle [116, 117]. Besides being considered a pest for domestic animals (dogs, cattle and horses), the species can transmit to humans the Brazilian Spotted Fever caused by the bacterium R. rickettsii, being this the most important zoonotic disease transmitted by ticks within the limits of the National territory. Additionally, A. sculptum has also been identified with the bacterium R. amblyommatis in the municipality of Pium, state of Tocantins [118].

There is a trend of seasonal behavior for some species of Amblyomma in the Amazon biome, with immatures predominating in the dry period (June to October), and adults in the rainy period (October to March) [119]. Similar to the pattern observed for A. sculptum in areas outside the Amazon biome [116].

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6. Soft ticks in the Brazilian Amazon

Taxonomy of Argasidae is currently questionable and relies on five schemes that divide the family in up to ten genera [120]. Achieving a consensus between soft tick taxonomists depends now chiefly on the molecular characterization of early collected type specimens for some genera. For instance, elucidating the status of pivotal taxa such as Alectorobius is mandatory if we are to understand the systematics of the Argasidae, particularly in the American Continent. Considering a practical approach, in this chapter we adopt but not necessarily endorse the classification of soft ticks into five genera, namely: Antricola, Argas, Nothoaspis, Ornithodoros, and Otobius [121].

The fauna of argasid ticks in Brazil is currently composed by 24 species [15]. Ticks of this family parasitize terrestrial vertebrates including amphibians in this country [25, 26]. With the exception of larvae from an undetermined Ornithodoros sp. collected on Potus flavus (Procionidae) [84], reports of soft ticks parasitizing mammals in the Brazilian Amazon are few and almost restricted to larvae collected on bats. Adults and nymphs have been collected either inside bat-inhabited caves or over massive rock formations where bats shelter (Table 4).

SpeciesStateLocalityMilieu of collection/HostReference
Antricola delacruziRondôniaPorto VelhoBat inhabited cave/Pteronotus spp.[122]
Antricola guglielmoneiRondôniaPorto VelhoBat inhabited cave/Pteronotus spp[122]
Nothoaspis amazoniensisRondôniaPorto VelhoBat inhabited cave/Pteronotus parnellii[123]
Nothoaspis setosusRondôniaMonte NegroRock formation/
Molossus molossus
[124]
Ornithodoros cavernicolousRondôniaMonte NegroBat inhabited caves/Unknown[125]
Ornithodoros haseiAmapáunknownMistneted bat Artibeus planisrostris[87]
ParáMarajó IslandBat-inhabited three hole/Unknown[126]
Ornithodoros kohlsiRondôniaMonte NegroMistneted bat Molossops mattogrossensis[30]
Ornithodoros marinekelleiRondôniaPorto VelhoBat inhabited cave/Pteronotus spp[127]
ParáCarajás, Paraupebas, Canaã dos CarajásBat inhabited caves/Unknown[128]
Ornithodoros peropteryxRondôniaMonte NegroBat inhabited cave/Unknown[125]
Ornithodoros rondoniensisRondôniaPorto VelhoBat inhabited cave/Unknown[122]
ParáCarajás, Paraupebas, Canaã dos CarajásBat inhabited caves/Unknown[128]
Ornithodoros stageriRondôniaUnknownUnknown/Noctilio albiventris, Nyctinomops laticaudatus[129]
[11]

Table 4.

Soft ticks and their respective hosts occurring in the Brazilian Amazon.

The first record of a soft tick in the Brazilian Amazon was published by North American entomologists Robert A. Cooley and Glen M. Kohls back in 1941. They received a tick collected inside a bat-inhabited three hole at Marajó Island (Pará state) and identified it as female of Ornithodoros hasei (mentioned as Ornithodoros dunni) [126]. Nowadays, we know that O. hasei is a wide spread species in Brazil and that three-roosting bats Artibeus planirostris and Noctilio spp. could act as main hosts [87, 130, 131, 132]. With the exception of recent collection of larvae on A. planirostris [87], knowledge on the distribution of O. hasei along the Brazilian Amazon is still poorly vague.

Tadarida laticaudata were the first bats reported to be parasitized by soft ticks in the Brazilian Amazon [133]. This report referred to Ornithodoros setosus, which was recently reclassified as Nothoaspis setosus [124]. In 1972, the bats Noctilio labialis and T. laticaudata were reported to be parasitized by Ornithodoros stageri in the Brazilian Amazon [129], which was recently confirmed [11]. A report in the Brazilian Amazon is a remarkable fact for O. stageri, since it also has distribution in Southern United States and Mexico [126, 134].

Bat inhabited caves constitute excellent niches to find argasid ticks. In particular, special, large colonies of insectivorous bats dwelling inside small chambers create high temperature conditions (28-40°C) where hundreds of Antricola, Nothoaspis and Ornithodoros ticks might occur [135]. Between 2004 to 2010 collections of ticks performed in hot caves from Porto Velho (Rondônia) fostered the description of two novel species (e.g., Nothoaspis amazoniensis and Ornithodoros rondoniensis) [122, 123]; the redescription of larvae and description of postlarval stages of Ornithodoros marinkellei [127], and the expansion of geographical distribution of Antricola delacruzi and Antricola guglielmonei into Brazilian Amazon [122]. At least for two species, O. marinkellei and O. rondoniensis, further collections performed in caves from Pará state underpined a larger distribution along the Amazon ecosystems [128].

Most amazing feature of soft ticks inhabiting hot caves, is that adaptation to this particular milieu seems to have modified their morphology and biology drastically. For instance, evidence showing that adults of Antricola ticks lack the capacity to digest blood has been gained after transcriptomic analyses of their saliva [136]. In fact, scoop-like short mouth parts suggest that adults of Antricola do not suck blood [137]. Moreover, adults of Antricola, O. marinkellei and O. rondoniensis possess huge spiracular plates [122, 127, 137], perhaps necessary to thrive in such hot and extremely humid environments.

Except for larvae of Ornithodoros kohlsi collected on the bat Molossops mattogrossensis [30], prospections performed by our group between 2016 and 2019 focused mainly in the search for soft ticks inside natural cavities over massive rock formations. During these expeditions, Ornithodoros cavernicolous and Ornithodoros peropteryx were collected for the first time in caves from Monte Negro (Rondônia), extending their distribution of both species to the Brazilian Amazon [125]. Furthermore, analyses performed on large larvae isolated from Molossus molossus bats clarified that O. setosus was incorrectly classified in its original description. Indeed, O. setosus matches morphologically and molecularly within the genus Nothoaspis therefore the statement of N. setosus n. comb. was proposed [124]. It is important to note that our last collections performed at Monte Negro included several morphotypes of Ornithodoros pending formal description. Consequently, the fauna of soft ticks occurring in the Brazilian Amazon is likely to increase soon.

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7. Conclusion

Ticks parasitize a wide variety of vertebrates around the world such as amphibians, reptiles, mammals and birds, including humans. Although there are a variety of studies of parasitism by ticks on animals and humans in the different ecoregions of Brazil, in the Amazon biome they are scarce and fragmented. Because of this, it is possible to infer that the diversity of ticks in the Brazilian Amazon is underestimated. In the Amazon, amphibians and reptiles were important hosts for A. rotundatum, A. dissimile and A. humerale, hard ticks common in these hosts in other regions of the country. Birds and mammals, on the other hand, proved important for the maintenance and dispersion of over 30 species of hard ticks in the Amazon, but there are still many gaps between hosts and their ticks in this region. Interestingly, immature A. humerale appears to be frequent on wild birds in this biome. No soft ticks have been reported parasitizing amphibians, reptiles, birds and/or non-flying mammals (except for a single record of Ornithodoros sp. on P. flavus), possibly due to scarcity of more studies in this biome. Some studies show that bats seem to have an important role spreading soft tick populations along Amazonian caves and that the diversity described for this group is still very poor. Two vector species of spotted fevers were found in the Amazon biomes parasitizing humans (A. sculptum and A. ovale). However, to date, there are no reports of BSF in humans in the region. Finally, it is of paramount importance that researchers (acarologists and epidemiologists) direct their attention to the Amazon biome, in order to fill the numerous existing gaps in the diversity of ticks in Brazil and prevent possible outbreaks of diseases transmitted by these ectoparasites to animals and humans.

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Conflict of interest

No conflict of interest declared.

References

  1. 1. Silva JMC, Rylands AB, Fonseca GAB. The fate of the Amazonian areas of endemism. Conservation Biology. 2005; 19: 689-694
  2. 2. MMA. Ministério do Meio Ambiente. 2018. Acessed: 03/10/2120
  3. 3. Vieira ICG, Toledo PM, Silva JMC, Higuchi H. Deforestation and threats to the biodiversity of Amazonia. Brazilian Journal of Biology. 2008; Suppl 0
  4. 4. Evans KL, Newson SE, Storch D, Greenwood JJ, Gaston KJ. Spatial scale, abundance and the species-energy relationship in British birds. Journal of Animal Ecology. 2008; 77: 395-405
  5. 5. Rylands AB. Amazonia. In: Wilderness: Earth’s last wild places. Agrupación Serra Madre, S. C. Mexico: CEMEX, 2002; 56–107
  6. 6. Parrotta JA, Wildburger C, Mansourian S. Understanding relationships between biodiversity, carbon, forests and people: the key to achieving REDD+ objectives. A global assessment report prepared by the Global Forest Expert Panel on Biodiversity, Forest Management and REDD. 2012; 31: 161, 2012
  7. 7. Duscher GG, Fuehrer HP, Kübber-Heiss A. Fox on the run – molecular surveillance of fox blood and tissue for the occurrence of tick-borne pathogens in Austria. Parasites & Vectors. 2014; 7: 521
  8. 8. de la Fuente J. Controlling ticks and tick-borne diseases looking forward. Ticks and Tick Borne Diseases. 2018; 9: 1354–1357
  9. 9. Massard CL, Fonseca AH. Carrapatos e doenças transmitidas, comuns ao homem e aos animais. A Hora Veterinária. 2004. 135; 1: 15-23
  10. 10. Szabó MP, Pinter A, Labruna MB. Ecology, biology and distribution of spotted-fever tick vectors in Brazil. Front Cell Infect Microbiol. 2013; 3: 27
  11. 11. Dantas-Torres F, Martins TF, Muñoz-Leal S, Onofrio VC, Barros-Battesti DM. Ticks (Ixodida: Argasidae, Ixodidae) of Brazil: Update species checklist and taxonomic keys. Ticks and Tick Borne Diseases. 2019; 10: 101252
  12. 12. Peñalver EA, Arillo X, Delclòs D, Peris DA, Grimaldi SR, Anderson PC. Nascimbene, and R. Pérez-de la Fuente. Ticks parasitised feathered dinosaurs as revealed by Cretaceous amber assemblages. Nature Communications.2017; 8: 1924
  13. 13. LabrunaMB, OnofrioVC, Barros-Battesti, GianizellaSL, VenzalJM, GuglielmoneAA. Synonymy of Ixodes aragaoi with Ixodes fuscipes, and reinstatement of Ixodes spinosus (Acari: Ixodidae). Ticks and Tick-borne Diseases. 2020; 11: 101349
  14. 14. Martins TF, Luz HR, Muñoz-Leal S, Ramirez DG, Milanelo L, Marques S, et al. A new species of Amblyomma (Acari: Ixodidae) associated with monkeys and passerines of the Atlantic rainforest Biome, southeastern Brazil. Ticks and Tick-borne Diseases, 2019; 10: 1-10
  15. 15. Muñoz-Leal S, Martins MM, Nava S, Landulfo GA, Simons SM, Rodrigues VS, et al. Ornithodoros cerradoensis n. sp. (Acari: Argasidae), a member of the Ornithodoros talaje (Guérin-Méneville, 1849) group, parasite of rodents in the Brazilian Savannah, Ticks and Tick-borne Diseases. 2020; 11: Issue 5
  16. 16. OnofrioVC, Guglielmone AA, BattestiDM, GianizellaSL, MarciliA, QuadrosRM, et al. Description of a new species of Ixodes (Acari: Ixodidae) and first report of Ixodes lasallei and Ixodes bocatorensis in Brazil. Ticks and Tick-borne Diseases. 2020; 11: 101423
  17. 17. Guglielmone AA, Robbins RG, Apanaskevich DA, PetneyTN, Estrada-Peña A, Horak IG. The hard ticks of the world: (Acari: Ixodida: Ixodidae). London: Springer; 2014; 738 p
  18. 18. Esser HJEA, Herre R, Kays YL, Jansen PA. “Local Host-Tick Coextinction in Neotropical Forest Fragments.” International Journal for Parasitology 2019; 49: 225–233
  19. 19. Ferreira GC, Sturaro MJ, Peloso PLV. Amphibians and reptiles from Floresta Nacional de Pau-Rosa, Amazonas, Brazil: an important protected area at the heart of Amazonia. Acta Amazonica. 2017; 47: 259 – 268
  20. 20. Luz HR, Faccini JLH. Parasitim on anurans in Brazil (in portuguese). Vet Zootec. 2013; 20: 100-111
  21. 21. Horta MC, Saraiva DG, Oliveira GMB, Martins TF, Labruna MB. Rickettsia bellii in Amblyomma rotundatum ticks parasitizing Rhinella jimi from northeastern Brazil. Microbes Infect. 2015;17: 856–858
  22. 22. Alcântara 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. Systematic and Applied Acarology. 2018; 23: 1497–1508
  23. 23. Oda FH, Kitagawa C, Noronha JC, Rodrigues DJ, Martins TF, Valadão MC, et al. Amblyomma species infesting amphibians and reptiles in the seasonally dry Amazon forest, with new host records for Amblyomma rotundatum (Acari: Ixodida: Ixodidae). Systematic and Applied Acarology. 2018; 23: 387-392
  24. 24. Fonseca, MS, Campanharo TB, Borges AAS, Castilho VO, Doria TB, ParanáSBM, et al. Ticks and Associated Pathogens From Rescued Wild Animals in Rainforest Fragments of Northeastern Brazil. Frontiers in Veterinary Science. 2020; 7: 177
  25. 25. Barros-Battesti DM, Landulfo GA, Luz HR, Marcili A, Onofrio VC, Famadas KM. Ornithodoros faccinii n. sp. (Acari: Ixodida: Argasidae) parasitizing the frog Thoropa miliaris (Amphibia: Anura: Cycloramphidae) in Brazil. Parasites & Vectors 2015; 8: 268
  26. 26. Muñoz-Leal S, Toledo LF, Venzal JM, Marcili A, Martins TF, Acosta ICL, et al. Description of a new soft tick species (Acari: Argasidae: Ornithodoros) associated with stream-breeding frogs (Anura: Cycloramphidae: Cycloramphus) in Brazil. Ticks and Tick-Borne Diseases. 2017; 8: 682-692
  27. 27. Labruna MB, Camargo LMA, Terrassini FA, Schumaker TTS, Camargo EP, Notes on Parasitism by Amblyomma humerale (Acari: Ixodidae) in the State of Rondônia, Western Amazon, Brazil. Journal of Medical Entomology. 2002; 39: 814–817
  28. 28. Polo G, Luz HR, Martins TF, Regolin AL, Silva HR, Winker G, et al. Distribution modeling of Amblyomma rotundatum and Amblyomma dissimile in Brazil: estimates of environmental suitability. Parasitology Research. 2020; https://doi.org/10.1007/s00436-020-06924-9s
  29. 29. Luz HR, Silva-Santos E, Costa-Campos CE, Acosta I, Martins TF, Munhoz-Leal S, et al. Detection of Rickettsia spp. in ticks parasitizing toads (Rhinella marina) in the northern Brazilian Amazon. Experimental and Applied Acarology. 2018; 75: 309-318
  30. 30. Martins TF, Venzal JM, Terrassini FA, Costa FB,; Marcili A, Camargo LMA, et al. New tick records from the state of Rondônia, western Amazon, Brazil. Experimental and Applied Acarology 2013; 62: 121-128
  31. 31. Gianizella SL, Martins TF, Onofrio VC, Aguiar NO, Gravena W, Nascimento CAR, et al. Ticks (Acari: Ixodidae) of the state of Amazonas, Brazil. Experimental & Applied Acarology. 2018; 74: 177-183
  32. 32. Witter R, Martins TF. Campos AK, Melo ALT, Correa SHR, Morgado TO, et al. Rickettsial infection in ticks (Acari: Ixodidae) of wild animals in midwestern Brazil. Ticks and Tick-borne Diseases. 2016; 7, 415–423
  33. 33. Zimmermann NP, Aguirre AAR, Rodrigues VS, Garcia MV, Medeiros JF, Blecha IMZ, et al. Wildlife species, Ixodid fauna and new host records for ticks in an Amazon forest area, Rondônia, Brazil. Brazilian Journal Veteriany Parasitology. 2018; 27: 177-182
  34. 34. Torres AC, Minervino AHH, Santos Júnior AP, Sarturi C, Martins TF, Vale WG, Morini AC, et al. Amblyomma ticks infesting amphibians and Squamata reptiles from the lower Amazon region, Brazil. Experimental & Applied Acarology. 2018; 75: 399–407
  35. 35. Pedroso-Santos F, Santos ES, Sanches PR, Campos EC, Luz HR, Faccini JLH. First record of Amblyomma dissimile (Acari: Ixodidae) infesting the Granular Toad Rhinella major (Anura: Bufonidae) in the Eastern Amazon region. Herpetology Notes. 2020; 13:385-387
  36. 36. Costa FB, Martins TF, Muñoz-Leal S, Serpa MC, OgrzewalskaM, Luz HR, et al. Retrospective and new records of ticks (Acari: Argasidae, Ixodidae) from the state of Maranhão, an Amazon-Cerrado transition area of Brazil Veterinary Plarasitology: Regional Studies and Reports. 2020; 21: 100413
  37. 37. Ogrzewalska M, Machado CR, Forneas T, Cunha DLE, Lemos, ERS. Microorganisms in the ticks Amblyomma dissimile Koch 1844 and Amblyomma rotundatum Koch 1844 collected from snakes in Brazil. Medical and Veterinary Entomology. 2019; 33: 154–161
  38. 38. Labruna MB, Camargo LMA, Terrassini FA, Ferreira F, Schumaker TTS, Camargo EP. Ticks (Acari: Ixodidae) from the State of Rondônia, western Amazon, Brazil. Systematic & Applied Acarology, 2005; 10: 17–32
  39. 39. Martins TF, Reis J L, Viana EB, Luz HR, Oda FH, Dantas SP, et al. Ticks (Acari: Ixodidae) on captive and free-ranging wild animals in Tocantins State, a Cerrado-Amazon transition region of northern Brazil. International Journal Acarology. 2020; 46: 254-257
  40. 40. Nascimento KKG, Veríssimo SMM, Raia VA, Guimarães RCS, Seade GCC, Azevedo ACP, et al. Tick fauna of wild animals received and attended at the Santarém Zoological Park, western Pará State, Brazil. Ciencia Rural. 2017; 47: 20170159
  41. 41. Labruna MB, Barbieri FS, Martins TF, Brito LG, Ribeiro FDS. New tick records in Rondônia, Western Brazilian Amazon. Revista Brasileira Parasitologia Veterinária. 2010; 19: 192-194
  42. 42. Soares HS, Barbieri ARM, Martins TF, Minervino AHH, Lima JTR, Marcili A, et al. Ticks and rickettsial infection in the wildlife of two regions of the Brazilian Amazon. Experimental & Applied Acarology. 2015; 65: 125–140
  43. 43. Schumaker TTS, Barros DM. Note on the biology of Amblyomma dissimile Koch, 1844 (Acari: Ixodidae) on Bufo marinus (Linnaeus, 1758) from Brazil. Memórias do Instituto Oswaldo Cruz. 1994; 89: 29–31
  44. 44. Keirans JE, Oliver Jr JH. First description of the male and redescription of the immature stages of Amblyomma rotundatum (Acari: Ixodidae), a recently discovered tick in the U.S.A. Journal of Parasitology. 1993; 79: 860-865
  45. 45. Labruna MB, Terrassini FA, Camargo LM. First report of the male of Amblyomma rotundatum (Acari: Ixodidae) from a field-collected host. Journal of Medical Entomology. 2005; 42: 945-947
  46. 46. Silva TKS, Blanco CM, Lemos ERS, Ogrzewalska M. Notes on parasitism and screening for microorganism of ticks Amblyomma (Acari: Ixodidae), Amazon, Brazil. Virus Reviews & Research. 2016; 21:41–44
  47. 47. Gianizella SL, Moraes JJr, Nascimento CAR, Martins TF. Primeiro registro de machos de Amblyomma rotundatum (Acari: Ixodidae) em jabuti-tinga (Chelonoidis denticulatus) no estado do Amazonas, Amazônia brasileira: relato de caso. Arquivo Brasileiro de Medicina Veterinária e Zootecnia. 2018; 70: 195-198
  48. 48. Luz HR, Faccini JLH, Silva HR. Patterns of parasitism by Amblyomma rotundatum (Ixodidae) on Rhinella schneideri (Bufonidae) in islands of São Francisco River, Minas Gerais, Brazil. Pesquisa Veterinária Brasileira. 2015; 35: 579-582
  49. 49. Oliveira GMB, Araújo AC, Santos JR, Silva IWG, Labruna MB, Horta MC. Lack of seasonality of Amblyomma rotundatum (Acari: Ixodidade) on Rhinella jimi (Anura: Bufonidae) in a semi-arid region of northeastern Brazil. Ticks and Tick-borne Diseases. 2018; 9: 1350-1353
  50. 50. Rodrigues DS, Maciel R, Cunha LM, Leite RC, Oliveira PR. Amblyomma rotundatum (Koch, 1844) (Acari: Ixodidae) two-host life-cycle on Viperidae snakes. Revista Brasileira de Parasitologia Veterinária. 2010; 19: 174–178
  51. 51. Luz HR, Faccini JLH, Pires MS, Silva HR, Barros-Battesti DM. Life cycle and behavior of Amblyomma rotundatum (Acari: Ixodidae) under laboratory conditions and remarks on parasitism of toads in Brazil. Experimental & Applied Acarology. 2013; 58: 89-99
  52. 52. Petit G, Landau I, Baccam D, Lainson R. Description et cycle biologique d’Hemolivia stellata, n.g., n.sp., hemogrégarine de Crapauds brésiliens. Annales de Parasitologie Humaine et Comparee. 1990; 65:3-15
  53. 53. Labruna MB, Whitworth T, Bouyer DH, McBride J, Camargo LMA, Camargo P, et al. Rickettsia bellii and Rickettsia amblyommii in Amblyomma ticks from the state of Rondônia, Western Amazon, Brazil. Journal of Medical Entomology. 2004; 41: 1073-1081
  54. 54. Gruhn KD, Ogrzewalska M, Rozental T, Farikoski IO, Blanco C, Freitas L S, et al. Evaluation of rickettsial infection in free-range capybaras (Hydrochoerus hydrochaeris Linneaus, 1766) (Rodentia: Caviidae) and ticks (Acari: Ixodidae) in Western Amazon, Brazil. Ticks and Ticks-Borne Diaseases. 2019; 10: 981-986
  55. 55. Barros-Battesti DM, Jerozolimski A, Onofrio VC, Arzua M. 2002. Amblyomma humerale Koch, 1844 (Acari: Ixodidade) on tortoises Geochelone denticulatus (L.) and G. carbonarius (Spix) from the Kayapó Indian land, state of Pará, northern Brazil. XI International Congress of Acarology. Program and Abstract Book, Mérida, México. 160 p
  56. 56. Souza AR, Gianizella SL, Roberto IJ. Rhinoclemmys punctularia (Eastern Spot-Legged Wood Turtle). Ectoparasites. Herpetological Review. 2018; 49: 713
  57. 57. Morais DH, Carvalho VT, Bonora L, Kawashita-Ribeiro RA, Strussmann C. Patterns of Parasitism by Amblyomma humerale (Acari: Ixodidae) on Chelonoidis denticulatus (Testudines: Testudinidae) in the Brazilian Midwest. Herpetological Review. 2017; 48: 316-319
  58. 58. Martins TF, Teixeira RHF, Benatti HR, Minervino AHH, Soares HS, Soares JF, et al. Life cycle of the tick Amblyomma humerale (Parasitiformes: Ixodida) in the laboratory, International Journal of Acarology. 2020. https://doi.org/10.1080/01647954.2020.1802510
  59. 59. Dantas-Torres F, Mascarenhas-Junior PB, Anjos HR, Santos EM, Correia JMS. Tick infestation on caimans: a casual tick-host association in the Atlantic rainforest biome?. Experimental & Applied Acarology. 2019; 79: 411–420
  60. 60. Martins TF, Gianizella SL, Nunes PH, Faria DC, Nascimento CA, Abrahão CR, et al. New records of Amblyomma goeldii (Acari: Ixodidae) and description of the nymphal stage. Zootaxa. 2015; 3949: 439-444
  61. 61. Luz HR, Faccini JLH. Ticks on brazilian birds: overview. In: Ruiz, L., Iglesias, F. (Eds.), Birds – Evolution, Behavior and Ecology 1. Nova Science Publishers, Inc, New York. 2013; 97–125
  62. 62. Hasle G. Transport of ixodid ticks and tick-borne pathogens by migratory birds. Frontiers in Cellular and Infection Microbiology. 2013; 3: 48
  63. 63. Comstedt PS, Bergstrom B, Olsen U, Garpmo L, Marjavaara H. Mejlon, A. G. Barbour, and J. Bunikis. Migratory passerine birds as reservoirs of Lyme borreliosis in Europe. Emerging Infectious Diseases. 2006; 12: 1087-1095
  64. 64. Ogrzewalska M, Pinter A. Ticks (Acari: ixodidae) as ectoparasites of Brazilian wild birds and their association with rickettsial diseases Brazilian Journal Veterinary Animmal Sciense. 2016; 53: 1-31
  65. 65. Barros-Battesti DM, Arzua M, Pichorim M, Keirans JE. Ixodes (Multidentatus) paranaensis n. sp. (Acari: Ixodidae) a parasite of Streptoprocne biscutata (Sclater 1865) (Apodiformes: Apodidae) birds in Brazil. Memórias do Instituto Oswaldo Cruz. 2003; 98: 93–91
  66. 66. CBRO – Comitê Brasileiro de Registros Ornitológicos. 2014. Listas das aves do Brasil. 10 ed. Disponível em<http://www.cbro.org.br>. Acessed in: 02.10.2020
  67. 67. Sick H. Ornitologia Brasileira. Editora Nova Fronteira, Rio de Janeiro. 1997. 912 p
  68. 68. Lima MA, Martins TF, Muñoz-Leal S, Guilherme E, Ogrzewalska M, Labruna MB. Ticks and tick-associated spotted fever group Rickettsia from birds in the Southwestern Brazilian Amazon. Revista Colombiana de Ciencias Pecuárias. 2018; 31: 26-35
  69. 69. 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: 809–816
  70. 70. Souza VL, Martins TF, Guilherme E, Santos FGA. New records of ticks (Acari: Ixodidae) infesting wild birds in a forest fragment in Acre, Brazilian Amazon. 2020. DOI: 10.5433/1679-0359.2020v41n5Supl1p2163
  71. 71. Martins TF, Fecchio A, Labruna MB (2014) Ticks of the genus Amblyomma (Acari: Ixodidae) on wild birds in the Brazilian Amazon. Systematic and Applied Acarology. 2010; 19: 385–392
  72. 72. Scofield A, Bahia M, Martins AL, Góes-Cavalcante G, Martins TF, Labruna MB. Amblyomma dissimile Koch (Acari: Ixodidae) attacking Primolius maracana Vieillot (Psittaciformes: Psittacidae) in the Amazon Region, State of Pará, Brazil. Neotropical Entomology. 2011; 40: 509-511
  73. 73. Labruna MB, Sanfilippo LF, Demetrio C, Menezes AC, Pinter A, Guglielmone AA. Ticks collected on birds in the state of São Paulo, Brazil. Experimental & Applied Acarology. 2007; 43: 147-160
  74. 74. Lugarini C, Martins TM, Ogrzewalska M, Vasconcelos NCT, Ellis VA, Oliveira JB, et al. Rickettsial agents in avian ixodid ticks in northeast Brazil. Ticks and Tick Borne Diseases. 2015; 6: 364–375
  75. 75. Luz HR, Faccini JLH, McIntosh D. Molecular analyses reveal an abundant diversity of ticks and rickettsial agents associated with wild birds in two regions of primary Brazilian Atlantic Rainforest. Ticks and Tick Borne Diseases. 2017; 8:657–665
  76. 76. Luz HR, Martins TF, Teixeira RHF, Terassini FA, Soares HS, Soares JF, et al. Some biological and behavioral aspects of Amblyomma longirostre (Acari: Ixodidae) under laboratory and natural conditions. Systematic and Applied Acarology. 2018; 23:10. 1965
  77. 77. Aragão HB. Ixodidas brasileiros e de algunos paízes limitrophes. Memórias do Instituto Oswaldo Cruz. 1936; 31: 759–843
  78. 78. Reis NL, Perachi AL, Pedro WA, Lima IP. Mamíferos do Brasil. Universidade Estadual de Londrina, Brazil. 2006
  79. 79. Abreu-Jr EF, Casali DM, Garbino GST, Loretto D, Loss AC, Marmontel M, et al. Lista de Mamíferos do Brasil. Comitê de Taxonomia da Sociedade Brasileira de Mastozoologia (CT-SBMz). Disponível em: <https://www.sbmz.org/mamiferos-do-brasil/>. Acessed em: 03/10/2020
  80. 80. Bown KJ, Begon M, Bennett M, Woldehiwet Z, Ogden N. Seasonal dynamics of Anaplasma phagocytophila in a rodent-tick (Ixodes trianguliceps) system, United Kingdom. Emerging Infectious Diseases. 2003; 9: 63–70
  81. 81. Zhan L, Cao WC, Chu CY, Jiang BG, Zhang F, Liu W, et al. Tick-borne agents in rodents, China, 2004–2006. Emerging Infectious Diseases. 2009; 15: 1904-1908
  82. 82. Horta MC, Moraes-Filho J, Casagrande RA, Saito TB, Rosa SC, Ogrzewalska M, et al. Experimental Infection of opossums Didelphis aurita by Rickettsia rickettsii and evaluation of the transmission of the infection to ticks Amblyomma cajennense. Vector Borne Zoonotic Diseases. 2009; 9: 109-118
  83. 83. Nava S, Venzal JM, González-Acuña D, Martins TF, Guglielmone AA. Ticks of the Southern Cone of America. Elsevier Academic Press, London, San Diego, Cambridge, Oxford. 2017. 348 p
  84. 84. Labruna MB, Jorge RS, Sana DA, Jácomo AT, Kashivakura CK, Furtado MM, et al. Ticks (Acari: Ixodida) on wild carnivores in Brazil. Experimental & Applied Acarology. 2005; 36: 149-163
  85. 85. Martins TF, Milanelo L, Krawczak FS, Furuya HR, Fitorra LS, Dores FT, et al. Diversity of ticks in the wildlife screening center of São Paulo city, Brazil. Ciência Rural. 2017; 47: 1-6
  86. 86. Luz HR, Neto SFC, Weksler M, Gentile R, Faccini JLH. Ticks parasitizing wild mammals in Atlantic Forest areas in the state of Rio de Janeiro, Brazil. Brazilian Journal Veterinary Parasitology. 2018; 27:409–414
  87. 87. Luz HR, Muñoz-Leal S, de Carvalho WD, Castro IJ, Xavier BS, Toledo JJ, et al. Detection of “Candidatus rickettsia wissemanii” in ticks parasitizing bats (Mammalia: Chiroptera) in the northern Brazilian Amazon. Parasitology Research. 2019; 118: 3185–3189
  88. 88. 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. Systematic and Applied Acarology. 2020; 25:78–91
  89. 89. Rosas FCW, Sicsu da Cruz TM, Gianizella SL, dos Santos Ramalheira C, Martins TF. A first record of ticks in free-ranging giant otter (Pteronura brasiliensis) in the Brazilian Amazon. IUCN Otter Species Group Bulletim. 2016; 33: 3–7
  90. 90. 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). Parasites & Vectors. 2016; 9: 14 p
  91. 91. Costa FB, da Costa AP, Moraes-Filho J, Martins TF, Soares HS, Ramirez DG, et al. Rickettsia amblyommatis infecting ticks and exposure of domestic dogs to Rickettsia spp. in an Amazon-Cerrado transition region of northeastern Brazil. PLoS ONE. 2017; 12: e0179163
  92. 92. Leal PF. Distribuição e relação trófica entre carrapatos e pequenos mamíferos da Ordem Rodentia e Didelphimorphia na floresta nacional de Carajás, estado do Pará, Dissertação. Belém, 2014
  93. 93. Labruna MB, Keirans JE, Camargo LMA, Ribeiro AF, Soares RM, Camargo EP. Amblyomma latepunctatum, a valid tick species (Acari: Ixodidae) long misidentified with both Amblyomma incisum and Amblyomma scalpturatum. Journal of Parasitology. 2005; 91: 527–541
  94. 94. Furtado MM, Metzger B, Jácomo ATA, Labruna MB, Martins TF, O'Dwyer LH, et al. Hepatozoon spp. Infect Free-Ranging Jaguars (Panthera onca) in Brazil. Journal Parasitology. 2017; 3: 243-250
  95. 95. Martins TF, Spolidorio MG, Batista TCA, Oliveira IAS, Yoshinari NH, Labruna MB. 2009. Occurrence of ticks (Acari: Ixodidae) in the municipality of Goiatins, Tocantins. Revista Brasileira Parasitologia Veterinária. 2009; 18:50-52
  96. 96. Sampaio JS, Martins TF, Labruna MB, Onofrio VC, Faccini JLH, Barros-Battesti DM. A second record of Amblyomma romitii Tonelli-Rondelli, 1939 (Acari: Ixodidae) from the State of Pará, Brazil. Systematic & Applied Acarology. 2010; 15: 184–186
  97. 97. Marques S, Barros-Battesti DM, Faccini JLH, Onofrio VC. Brazilian distribution of Amblyomma varium Koch, 1844 (Acari: Ixodidae), a common parasite of sloths (Mammalia: Xenarthra). Mem Inst Oswaldo Cruz. 2002; 97: 1141-6
  98. 98. Oliveira SVde, Pereira SVC, Pinna FV, Fonseca LX, Serra-Freire NM, Cardoso KM, et al. Vigilância de ambientes da febre maculosa: explorando as áreas silenciosas do Brasil. Revista Pan-Amazônica de Saúde. 2016; 7: 65-72
  99. 99. Martins TF, Bernardi LFO, Munoz-Leal S, Marcili A, Labruna MB. New records of Ixodes amarali (Acari: Ixodidae) in the Amazon biome, with description of the male. Systematic and Applied Acarology. 2009; 24: 2552–2558
  100. 100. Luz HR, Faccini JLH, Landulfo GA, Sampaio JS, Neto SFC, Famadas KM et al. New host records of Ixodes luciae (Acari: Ixodidae) in the State of Pará, Brazil. Revista Brasileira Parasitologia Veterinária. 2013; 22: 152–154
  101. 101. Fernandes MMP, Medeiros FER, Carvalho YK, Ribeiro VMF, Souza SF. Ectoparasitas de cães domiciliados e errantes do município de Rio Branco-Acre. Enciclopédia Biosfera. 2018; 15: 442-450
  102. 102. Onofrio VC, Barros-Battesti DM, Labruna MB, Faccini JL. Diagnoses of and illustrated key to the species of Ixodes Latreille, 1795 (Acari: Ixodidae) from Brazil. Systematic and Applied Acarology. Parasitology. 2009; 72: 143–157
  103. 103. Serra-Freire NM. Occurrence of ticks (Acari: Ixodidae) on human hosts, in three municipalities in the State of Pará, Brazil. Revista Brasileira de Parasitologia Veterinária. 2010; 19: 141–147
  104. 104. Lopes LB, Guterres A, Rozental T, Carvalho de Oliveira R, Mares-Guia M, Fernandes J, et al. Rickettsia bellii, Rickettsia amblyommii, and Laguna Negra hantavirus in an Indian reserve in the Brazilian Amazon. Parasites & Vectors. 2014; 7: 191
  105. 105. Aguirre A AR, Rodrigues VS, Costa IN, Garcia MV, Higa LOS, Medeiros JF, Andreotti R. Biological parameters of Amblyomma coelebs Neumann, 1906 (Acari: Ixodidae) under experimental conditions. Brazilian Journal Veterinary Parasitology. 2018; 27: 81-86
  106. 106. Guglielmone AA, Beati L, Barros-Battesti DM, Labruna MB, Nava S, Venzal JM, et al. Ticks (Ixodidae) on humans in South America. Experimental & Applied Acarology. 2006; 40: 83–100
  107. 107. Silva TKS, Blanco CM, Lemos ERS, Ogrzewalska M. Notes on parasitism and screening formicroorganism of ticks Amblyomma (Acari: Ixodidae), Amazon, Brazil. Virus Reviews & Research. 2016; 21: 41–44
  108. 108. Aragão HB, Fonseca F. nota de ixodologia. VIII. Lista e chave para os representantes da fauna ixodológica brasileira. Memórias do Instituto Oswaldo Cruz. 1961; 59: 115–129
  109. 109. Labruna MB, Homem VSF, Heinemann MB, Neto JSF. Ticks (Acari: Ixodidae) associated with rural dogs in Uruará, Eastern Amazon, Brazil. Journal of Medical Entomology. 2000; 37: 774–776
  110. 110. Martins TF, Luz HR, Faccini JLH, Labruna MB. Life-cycle of Amblyomma oblongoguttatum (Acari: Ixodidae) under laboratory condition. Experimental & Applied Acarology. 2017; 71: 415–424
  111. 111. Martins TF, Moura MM, Labruna MB. Life-cycle and host preference of Amblyomma ovale (Acari: Ixodidae) under laboratory conditions. Experimental & Applied Acarology. 2012; 56: 151–158
  112. 112. Guglielmone AA, Robbins RG. Tick species found feeding on humans. In: Guglielmone AA, Robbins RG, editors. Hard ticks (Acari: Ixodida: Ixodidae) parasitizing humans: a global overview. 1st ed. London: Springer. 2018. 205 p
  113. 113. Landulfo GA, Luz HR, Sampaio JS, Faccini JLH, Barros-Battesti DM. Life Cycle of Amblyomma romitii (Acari: Ixodidae) Under Laboratory Conditions. Journal of Medical Entomology. 2015; 53: 48-53
  114. 114. Serra Freire NM, Peralta ASL, Teixeira RHF, Gazeta GS, Amorim M. Amblyomma rotundatum parasitando Homo sapiens no parque zoobotánico do MPEG e em Itaboraí. Arquivos da Sociedade de Zoológicos do Brasil. 1995; 16: 20
  115. 115. Aguirre AAR, Rodrigues VS, Costa IN, Garcia MV, Csordas BG, Andreotti R, Medeiros JF. Amblyomma scalpturatum Neumann, 1906 (Acari: Ixodidae): confirmation in Acre State, Brazil, and description of parasitism in a human. Brazilian Journal of Veterinary Parasitology. 2019; 28: 473-478
  116. 116. Labruna MB, Kasai N, Ferreira F, Faccini JL, Gennari SM. Seasonal dynamics of ticks (Acari: Ixodidae) on horses in the state of São Paulo Brazil. Veterinary Parasitology. 2002; 19: 65–77
  117. 117. Labruna MB, Amaku M, Metzner JA, Pinter A, Ferreira F. Larval behavioral diapause regulates life cycle of Amblyomma cajennense (Acari: Ixodidae) in Southeast Brazil. Journal of Medical Entomology. 2003; 40: 170-178
  118. 118. Bitencourth K, Amorim M, De Oliveira SV, Caetano, RL, Voloch CM, Gazêta GS. Amblyomma sculptum: genetic diversity and rickettsias in the Brazilian Cerrado biome. Medical and Veterinary Entomology. 2017; 3: 1-11
  119. 119. Labruna MB, Terassini FA, Camargo LM. Notes on population dynamics of Amblyomma ticks (Acari: Ixodidae) inBrazil. Journal Parasitology. 2009; 95: 1016-8
  120. 120. Mans BJ, Featherston J, Kvas M, Pillay K, de Klerk DG, Pienaar R, et al. Argasid and ixodid systematics: Implications for soft tick evolution and systematics, with a new argasid species list. Ticks and Tick-borne Diseases. 2019; 10: 219-240
  121. 121. Hoogstraal H. Mint: Argasid and nuttalliellid ticks as parasites and vectors. Advances in Parasitology. 1985; 24: 135-238
  122. 122. Labruna MB, Terassini FA, Camargo LMA, Brandão PE, Ribeiro AF, Estrada-Peña A. New reports of Antricola guglielmonei and Antricola delacruzi in Brazil, and a description of a new argasid species (Acari). Journal of Parasitology. 2008; 94: 788-792
  123. 123. Nava S, Venzal JM, Terassini FA, Mangold AJ, Camargo LMA, Labruna MB. Description of a new argasid Tick (Acari: Ixodida) from bat caves in Brazilian Amazon. Journal of Parasitology. 2010; 96: 1089-1101
  124. 124. Muñoz-Leal S, Terassini FA, Marcili A, Oliveira GMB, Camargo LMA, Labruna MB. A third species of Nothoaspis Keirans &amp; Clifford, 1975 (Acari: Argasidae): Nothoaspis setosus (Kohls, Clifford &amp; Jones, 1969) n. comb. Systematic Parasitology. 2019; 96 :595-602
  125. 125. Muñoz-Leal S, Terassini FA, Luz HR, Fontana I, Camargo LMA, Labruna MB. First report of Ornithodoros peropteryx in Brazil, and the occurrence of Ornithodoros cavernicolous in the western Brazilian Amazon. Systematic & Applied Acarology. 2018; 23: 2113–2121
  126. 126. Cooley RA, Kohls GM. The Argasidae of North America, Central America and Cuba, The American Midland Naturalist. Monograph N°1. 1944
  127. 127. Labruna MB, Nava S, Terassini FA, Onofrio VC, Barros-Battesti D, et al. Description of adults and nymph, and resdescription of the larva, of Ornithodoros marinekellei (Acari: Argasidae), with data on its phylogenetic position. Journal of Parasitology. 2011; 97: 207-217
  128. 128. Henrique-Simões M, Bernardi LFO, Ogrzewalska M, Labruna MB, Ferreira RL. New records of rare Ornithodoros (Acari: Argasidae) species in caves of the Brazilian Amazon. Persian Journal of Acarology. 2012; 1: 127-135
  129. 129. Jones EK, Clifford CM, Keirans JE, Kohls GM. The ticks of Venezuela (Acarina: Ixodoidea) with a key to the species of Amblyomma in the Western Hemisphere. Brigham Young University Science Bulletin - Biological Series. 1972; 17: 1-40
  130. 130. Muñoz-Leal S, Eriksson A, Santos CF, Fischer E, Almeida JC, Luz HR, Labruna MB. Ticks infesting bats (Mammalia: Chiroptera) in the Brazilian Pantanal. Experimental & Applied Acarology. 2016; 69: 73-85
  131. 131. Muñoz-Leal S, Barbier E, Soares FAM, Bernard E, Labruna MB, Dantas-Torres F. New records of ticks infesting bats in Brazil, with observations on the first nymphal stage of Ornithodoros hasei. Experimental & Applied Acarology. 2018; 76: 537-549
  132. 132. Luz HR, Muñoz-Leal S, Almeida JC, Faccini LH, Labruna MB. Ticks parasitizing bats (Mammalia: Chiroptera) in the Caatinga Biome, Brazil. Brazilian Journal Veterinary Parasitology. 2018; 35: 484-491
  133. 133. Kohls GM, Clifford CM, Jones EK. The systematics of the subfamily Ornithodorinae (Acarina: Argasidae). IV. Eight new species of Ornithodoros from the Western Hemisphere. Annals of the Entomological Society of America. 1969; 62: 1035–1043
  134. 134. Guzmán-Cornejo C, Herrera-Mares A, Robbins RG, Rebollo-Hernández A. The soft ticks (Parasitiformes: Ixodida: Argasidae) of Mexico: species, hosts, and geographical distribution. Zootaxa. 2019; 4623: 485-525
  135. 135. De La Cruz J. Mint: Bioecologia de las grutas de calor. Mundos Subterraneos, UMAE, Mexico, DF. 1992; 3: 7-21
  136. 136. Ribeiro JMC, Labruna MB, Mans BJ, Marumaya SR, Francischetti IMB, Barizon GC, Santos IKFM. The sialotranscriptome of Antricola delacruzi female ticks is compatible with non-hematophagous behavior and an alternative source of food. Insect Biochemistry Molecular Biology. 2012; 42: 332-342
  137. 137. Estrada-Peña A, Venzal JM, Barros-Battesti DM, Onofrio VC, Trajano E, Firmino JVL. Three new species of Antricola (Acari: Argasidae) from Brazil, with a key to the known species in the genus. Journal of Parasitology. 2004; 90: 490-498

Written By

Hermes R. Luz, Thiago F. Martins, Sebastián Muñoz-Leal, Francisco B. Costa, Sérgio L. Gianizella, João Luiz H. Faccini and Marcelo B. Labruna

Submitted: July 5th, 2020 Reviewed: November 1st, 2020 Published: December 23rd, 2020