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

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].

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.

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.

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.

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).

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.

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.

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].

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].

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).

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].

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).

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.

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.

Conflict of interest

No conflict of interest declared.