Ectoparasitas em morcegos (Mammalia: Chiroptera) e seus patógenos na região central de Rondônia, oeste da Amazônia brasileira

doi:10.21203/rs.3.rs-4301330/v1

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Ectoparasitas em morcegos (Mammalia: Chiroptera) e seus patógenos na região central de Rondônia, oeste da Amazônia brasileira

https://doi.org/10.21203/rs.3.rs-4301330/v1

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In Brazil, few people know that in the Tupi language bats are called ‘andirá’, ‘guandira’, or ‘guandiruçu’. The lack of knowledge about these animals is not restricted to these names but to the diversity of species, their biological complexity and their ecological importance. Bats (Chiroptera) are among the most diverse and geographically dispersed mammals. They are of great importance to the ecosystem, as pollinators, seed dispersers, and controllers of pests, and they are also hosts of several ectoparasites. Ectoparasites include a variety of arthropods, such as ticks (Ixodida), mites (Mesostigmata, Sarcoptiformes, and Trombidiformes), lice (Anoplura), fleas (Siphonaptera) and flies (Diptera), and their diet includes tissues and blood or other bodily fluids of bats. Bats are reservoirs of various disease-causing agents, many of them pathogenic to humans, such as bacteria of the genera Borrelia, Bartonella, Coxiella, Orientia and Rickettsia, as well as protozoa (among the most important, Leishmania spp. and Trypanosoma cruzi), viruses (the most important being rabies and Ebola) and fungi (Histoplasma and Crytococcus). This study was carried out in Monte Negro, Rondônia, and the occurrence of ectoparasites in bats was evaluated, as well as the bacteria of medical importance carried by these ectoparasites. Through a total of 69 nocturnal captures, 217 specimens of chiropterans representing 23 species and six families were sampled. A total of 592 specimens of ectoparasites were collected from the bats. Bacteria of the genus Bartonella were found in two species of bat flies (Trichobius joblingi and Strebla mirabilis). We report for the first time in Rondônia the argasid tick Ornithodoros hasei and its infection by a bacterium of the spotted fever group Candidatus Rickettsia wissemanii.

Chiroptera

Brazilian Amazon

Ectoparasites

Pathogens

Spillover Phenomena

Bats are mammals of the order Chiroptera and are among the most diverse and geographically dispersed mammals, comprising approximately 20% of all mammalian species worldwide [2]. They are divided into 18 families, 202 genera and 1,200 species. In Brazil, nine families, 64 genera, and 182 species are known, of which 150 species are found in the Amazon region of Brazil and 86 species with 16 genera in the state of Rondônia [1, 3–6].

Bats are of great importance to the ecosystem, as pollinators, seed dispersers, and controllers of pest, and are the only mammals truly capable of flight. They are present all over the world, except in Antarctica, and range in size from small (Yangochiroptera) to large species (Yinpterochiroptera). They can be found in almost all types of habitats, from forests to urban areas [7] and are nocturnal animals. Their ability to fly is the result of unique adaptations in their wings, which are formed by a thin, elastic membrane stretched between their fingers and arms. These animals have a varied diet that includes insects, fish, fruit, nectar, small terrestrial vertebrates and blood. Hematophagous bats are a minority and usually feed on birds and large mammals [1–8].

Bats are hosts of various arthropod ectoparasites, which live either part or all of their lives associated with the habitat created by the skin and body appendages of an individual of a different species. These ectoparasites include a variety of organisms, such as ticks (Argasidae, Ixodidae), mites (Mesostigmata, Sarcoptiformes, and Trombidiformes), lice (Anoplura), fleas (Siphonaptera), and flies (Diptera), and their diet includes blood or other bodily fluids and tissues, of the bats [9]. The presence of ectoparasites can cause irritation and stress for bats, which can affect their health and behavior [10]. However, it is important to note that not all bats have ectoparasites, and the prevalence and diversity of these ectoparasites vary between bat species and their habitats [11].

Regarding ectoparasites on bats, in the world, there are currently records of the occurrence of 18 families, composed of mites (Chirodiscidae, Ereynetidae, Labidocarpidae, Leeuwenhoekiidae, Macronyssidae, Myobiidae, Rosensteiniidae, Sarcoptidae, Spelaeorhynchidae, Spinturnicidae and Trombiculidae), ticks (Argasidae and Ixodidae) and insects (Cimicidae, Ischnopsyllidae, Nycteribiidae, Polyctenidae, Streblidae and Tungidae), with approximately 100 genera and 1,200 species [12–28].

In the Amazon, arthropods of the class Arachnida, represented by three families, five genera, and 60 species have been reported in bats and, in the state of Rondônia, three families, four genera and 16 species have been reported so far [29–31]. Regarding the class Insecta, 43 species in 16 genera of the Streblidae family and four species in two genera of the Nycteribiidae family have been reported [32–33].

Chiroptera and their ectoparasites are reservoirs of etiological agents of various diseases, and many of them are pathogenic to humans, such as bacteria of the genera Rickettsia, Coxiella, Borrelia, Bartonella and Orientia, as well as protozoa (among the most important, Leishmania spp. and Trypanosoma cruzi), viruses (the most important being rabies and Ebola) and fungi (Histoplasma and Cryptococcus).

This group of bacteria mentioned above are obligate intracellular bacteria and have in common the fact that they respond well to the use of doxycycline in human patients. Most cases of symptoms in human infections are subclinical or generic (headache, myalgia, high fever > 41°C, arthralgia), and some cases, if left untreated and/or with comorbidities, may evolve into more severe forms with involvement of the heart, kidneys, lungs and central nervous system.

According to Hayman [33] and Subudhi et al. [34], in recent years, the interest in bat research has increased due to the occurrence of what is known as the spillover phenomenon, in other words, the transmission of a pathogen from its natural reservoir or host species to a new host species, thus enhancing the possibility of spreading diseases to humans and other mammals.

Despite several studies over the past years, the study of ectoparasites in bats is still an underexplored field. The study by Graciolli and Bernard [12] formally recommended the exploration of areas such as south-central Rondônia to carry out new inventories in the Amazon. Thus, in this context, the present study aimed to record the ectoparasite fauna of bats in the south-central area of Rondônia and their pathogens in the context of the spillover phenomenon. The results of this study provide baseline data that contribute to the understanding of the epidemiology of certain pathologies of human and veterinary importance in Rondônia and in the western Brazilian Amazon.

Ethical aspects

The study was approved by the Biodiversity Authorization and Information System (SISBio) of the Instituto Chico Mendes de Conservação da Biodiversidade - ICMBio (No. 77013) and the capture procedures were in accordance with the resolutions of the Animal Experimentation Ethics Committee of ICB/USP (approved under CEUA No. 7946291123).

Study site

The study was carried out between November 2020 and November 2022 in Monte Negro, a central region in the state of Rondônia, 250 km southwest of the capital Porto Velho. It is located at a latitude of 10º 17' 40" S and longitude of 63º 19' 31" W, at an altitude of 123 meters, and occupies a territorial area of 1,931.378 km² with an estimated population of 11,548 inhabitants, according to data from the 2022 IBGE census (Fig. 1). The region is characterized by mixed soils and equatorial vegetation and a hot and humid climate, with high rainfall with an annual average varying between 1,440 mm in November to April and 557 mm in the dry period from May to October, with average temperatures of 25 to 29 ºC and relative humidity between 70 and 80% throughout the year [36].

Bat capture and sample collection

To capture the bats, we used ten mist nets measuring five meters long and two meters wide, suspended at a height of 1.5 meters from the ground. Additionally, we conducted active searches in artificial shelters in urban areas, resulting in the capture of 18% of the bats in the roof spaces of homes.

The mist nets were strategically positioned close to fruit trees and animal breeding areas, previously analyzed in terms of the location and behavior of bats in the environment. As necessary, these nets were occasionally relocated to meet the specific demands of the situation. In order to prevent escape or predation of captured specimens, the nets were inspected at 15-minute intervals.

This procedure was carried out with extreme caution, aiming to avoid any damage or injuries to the animals. After carrying out the procedures (biometric data collection processes, external morphology analysis, and photographing), the bats were promptly sent to the fields to be released. Taxonomic identification of the bats followed specialized scientific literature [3, 37, 38]. The nomenclature of the species and the taxonomic arrangement in the categories of order, family, and subfamily followed Abreu Jr et al. [5].

Captures took place from 6:00 pm to 11:00 pm, for three consecutive periods, each month, during the waning moon, for 25 months, totaling 345 hours. The capture effort, measured as the total area (m²) of the nets multiplied by the exposure time (hours) [39], was 157,500 m²/h.

The bats were initially kept in individual cloth bags and subsequently handled and thoroughly examined for the presence of ectoparasites. These were removed using tweezers and placed in DNA-free microtubes containing 100% ethanol. Each microtube housed the ectoparasites collected from a single bat and was identified by a tracing paper label containing the animal’s code written in graphite pencil and inserted inside the tube. Detection of vector-borne pathogens was based on the genomic investigation of the ectoparasites (procedures described below). No blood was taken from the bats.

Ticks

The ticks collected from the bats were morphologically identified at the species level following Jones and Clifford [40] and Labruna et al. [41] In addition, 25 larval ticks were identified at the species level by molecular analysis. For this purpose, larvae were individually submitted to DNA extraction using the guanidine isothiocyanate phenol technique [42] and tested via a polymerase chain reaction (PCR) assay targeting a ≈ 460-bp fragment of the ticks’ 16S rRNA mitochondrial gene, as described by Mangold et al. [43]. The PCR products were purified and sequenced with the Big Dye Terminator Cycle Sequencing kit (Applied Biosystems, Foster City, CA, USA) in an automatic sequencer (ABI 3500 Genetic Analyzer, Applied Biosystems) according to the manufacturer’s protocol. The generated sequences were submitted to BLAST analysis (www.ncbi.nlm.nih.gov/blast) to infer the closest identities to the tick DNA sequences available in GenBank.

A sample of 87 ticks was selected for testing for molecular detection of organisms of the genera Rickettsia, Borrelia, and Coxiella. This sample included the 25 individual larvae mentioned above, plus 62 larvae that were processed individually (8 larvae) or in pools, each containing 2 to 3 individuals (a total of 19 pools containing 54 larvae), using the same DNA extraction protocol mentioned above. This procedure resulted in a total of 55 extracted DNA samples, which were initially tested using a TaqMan real-time PCR assay targeting the rickettsial citrate synthase gene (gltA), as described elsewhere [44–45]. Samples that were positive according to the real-time PCR (cycle threshold ≤ 35) were tested via a conventional PCR that targeted a 401-bp fragment of the Rickettsia gltA gene [33]. In each set of reactions, negative control tubes containing water and a positive control tube containing Rickettsia vini DNA were included. The PCR products were DNA-sequenced and submitted to BLAST analyses as described above.

For the detection of Borrelia DNA, all 55 tick samples were tested via a TaqMan real-time PCR assay that targeted the 16S rRNA gene of organisms of the genus Borrelia, as described elsewhere [46]. Negative control tubes containing water and a positive control tube containing Borrelia anserina DNA were included. For the detection of Coxiella DNA, the 55 tick samples were tested via a conventional PCR that targeted a 687-bp fragment of the transposase elements gene (IS1111) of organisms of the genus Coxiella, as described elsewhere [47]. Negative control tubes containing water and a positive control tube containing C. burnetii DNA were included.

Mites

The mites (Spinturnicidae) were morphologically identified to species level following the keys available in Rudnick (1960) [48], Machado-Allison (1965a, b) [49–50] and Herrin and Tipton (1975) [51]. All the other mites were under identification at the time of writing and will be identified to species level in future studies.

For the molecular analysis, the DNA extraction of the spinturnicid mites was performed using the DNeasy Blood & Tissue kit (Qiagen, Hilden, Germany), following the manufacturer’s instructions. Each mite DNA sample was subjected to a conventional PCR targeting a fragment of ~ 800 bp of the 18S rRNA gene (endogenous control) [52] to verify the success of the DNA extraction procedure. Negative (Milli-Q water free of DNA) and positive (pool of dust mites) controls were included in each reaction.

One hundred and fifteen spinturnicid mites were selected for the detection of organisms of the genera Bartonella, Rickettsia, Borrelia and Coxiella. The protocols for the last three bacterial genus were the same used for the ticks; while, for Bartonella, we used a cPCR screening based on the nuoG gene according to Colborn et al. [52]. In order to characterize the positive samples, conventional PCR assays based on six different other Bartonella molecular markers were made: 16S rRNA [53], rpoB [54], pap31 [55], gltA [56], groEL [53–58], and ftsZ [53].

All the PCR products with concentrations over 20 ng/µL were selected and purified with ExoSap-IT (GE Healthcare Pittsburgh, PA). Sanger sequencing was performed at the Centro de Pesquisa sobre Genoma Humano e Células Tronco do Instituto de Biociências da USP, São Paulo, SP, Brazil. The obtained sequences were assembled with Sequencing Analysis 5.3.1 and submitted to BLAST analysis (Altschul et al. [59]) to infer similarities with Bartonella sequences available in GenBank. Different haplotypes were visually discriminated after an alignment using the CLUSTAL W algorithm (Thompson et al. [60]) implemented in Geneious R11 [58].

Diptera

The bat flies from the families Streblidae and Nycteribiidae that were collected were identified using the key of Carvalho et al. [61], and were identified up to species level using the keys proposed by Guerreiro [28]. The molecular analysis for the dipteran was performed in the same way that the mites’ DNA were extracted. Additionally, the material was tested for the same organisms using the protocols used for ticks and mites, as described above.

Bats

After 75 nocturnal samplings, with a sampling effort totaling 157,500 m²/h, 217 individual bats were captured, belonging to 23 species and six families as shown in Table 1. In peri-urban areas, characterized by having small sites and patches of forests with dense vegetation, 65% of the specimens were captured. In the urban area, an area characterized by a higher human population density and with a diameter of 4 km² per area, 1% belonged to the family Phyllostomidae, 67% to the family Vespertilionidae, 60% to the family Emballonuridae and 77% to the family Molossidae. These bats were captured in residential roof spaces through active search.

In the forest and peri-urban areas, the families Noctilionidae and Mormoopidae accounted 100% of all sampling efforts, followed by the family Phyllostomidae (99%), Emballonuridae (40%), Molossidae (23%) and Vespertilionidae (33%). (Fig. 2).

Ectoparasites

A total of 592 specimens of ectoparasites were collected from 14 bats and identified into seven families, as shown in Table 1. Overall, 37% of the bats were infested by at least one type of ectoparasite.

Among the 217 captured bats, 23 (10.6%) were found to be infested by ticks. A total of 308 ticks were collected, giving a mean intensity of infestation of 13.4 ticks/infested bat. In most of the infested bats, less than 10 ticks were collected; however, in two bats, a total of 87 and 100 ticks were collected. The 308 ticks were morphologically identified as Ornithodoros hasei (302 larvae collected from 20 Noctilio leporinus and one Pteronotus rubiginosus) and Ornithodoros marinkellei (six larvae collected from three P. rubiginosus). One P. rubiginosus was co-infested by the two tick species. Overall, O. hasei was collected from 20 (37.7%) out of 53 N. leporinus and one (11.1%) out of nine P. rubiginosus, whereas O. marinkellei was collected from 33.3% (3/9) of P. rubiginosus. No ticks were found in the remaining 21 bat species captured in the present study.

Taxonomic identification of the ticks was confirmed via molecular analyses in 23 O. hasei larvae, which generated a single 16S rRNA haplotype (426 bp). Through the BLAST analysis, this haplotype was 100% identical to a sequence of O. hasei from southeastern Brazil (KX099896). Two specimens of O. marinkellei generated a 16S rRNA haplotype (426 bp) that was 100% identical to a sequence of O. marinkellei from Porto Velho, Rondônia (HM582438).

A total of 55 tick samples containing 87 larvae (84 O. hasei, 3 O. marinkellei) were tested for the presence of DNA of organisms of the genera Rickettsia, Borrelia and Coxiella. Only one larva of O. hasei yielded amplicons for the genus Rickettsia, via both the real-time PCR and the conventional PCR assays. For the latter assay, a 350-bp fragment of the gltA gene was generated, which was 100% identical to GenBank available sequences of “Candidatus Rickettsia wissemanii” from O. hasei from French Guiana (MH614266) and the state of Amapá, Brazil (MH614266).

In this study, 17 species of captured bats were infested with parasitic Diptera (Table 1). A total of 98 bat fly samples were tested for the presence of DNA of Rickettsia, Bartonella, Borrelia and Coxiella. All the samples were positive for the endogenous control (18S rRNA) and, right after being submitted to the screening for pathogens, two of the 98 samples were positive for the nuoG gene of Bartonella spp., while all the samples were negative for the other tested bacterial genera. One sequence for the nuoG gene was detected in Trichobius joblingi collected on Carollia brevicauda, and another in Strebla mirabilis collected on Trachops cirrhosis. When compared with the sequences available in GenBank, these sequences were respectively 93.44 and 90.57% (e-value: 3 x 10^− 149, 1 x 10^− 132; query cover: 100%) identical to Bartonella sp. from Diphylla ecaudata blood collected in São Paulo, Brazil [64] (GenBank accession numbers PP445025 and PP445026).

In addition, 27 individual bat-associated mites (4 Trombiculidae, 1 Macronyssidae and 22 Spinturnicidae) were tested. All the samples were positive for the endogenous control (18S rRNA). However, all were negative for the tested bacteria.

Bats of the family Phyllostomidae showed a great richness of species; in total, 13 species were captured. Considering the most-used capture method in this study (mist nets installed at 1.5 meters above ground level), the high richness of phyllostomids was predictable, given the greater diversity of these bats in the tropics, as well as their foraging characteristics [38]. However, it is crucial to point out that using only this method may underestimate other families, such as Vespertilionidae and Molossidae [65], and can thus be considered a selective method. Therefore, the importance of adopting a combination of methods, such as mist nets (canopy), active searches and harp traps is recommended to ensure a comprehensive and representative sampling of bats [66, 67–68].

The relevance of the family Phyllostomidae is undeniable, as it plays crucial roles at all trophic levels, performing essential functions such as pollination, seed dispersal, and regulation of arthropod and small vertebrate populations. As pointed out by Medellin et al. [69], the diversity of feeding habits of this family of bats plays a fundamental role in the preservation and balance of forest ecosystems.

Members of the family Molossidae, whose eating habits are exclusively insectivorous, were identified in 13% of the sampling effort carried out in urban areas, establishing direct contact with human beings when they lodge in the roof spaces of homes. Despite harboring a diverse microbiota, made up of pathogenic and non-pathogenic agents, the intensification of contact between these bats and humans can result in highly pathogenic zoonotic incidents, which can be triggered by the phenomenon known as spillover. Factors such as the reduction in food supply and the loss of natural habitat for these bats contribute to this spillover since these factors lead them to move even closer to environments inhabited by humans [35–70].

Two tick species, O. hasei and O. marinkellei, were found infesting bats in the present study. Previous reports of O. hasei in Brazil were in the eastern Brazilian Amazon, in the states of Pará [71] and Amapá [63], and in the Pantanal and Caatinga biomes [72–73]. Therefore, our reports are the first for the western Brazilian Amazon. On the other hand, the present report of O. marinkellei just expand its geographic range in the state of Rondônia, since previous records of this tick species were restricted to the northern part of the state [74].

Despite a richness of 17 bat species, ticks were found on only two species, N. leporinus and P. rubiginosus. A previous study reported N. leporinus as a host for O. hasei in the Pantanal biome [73]; thus, this is the first report for the Brazilian Amazon. Interestingly, the relatively high prevalence (37.7%) of O. hasei on N. leporinus in the present study is similar to a previous study that reported this tick species infesting 40% of the bat Artibeus planirostris in the Caatinga [72]. In the Pantanal biome, where O. hasei was the only tick species associated with bats, Muñoz-Leal et al. [73] proposed that A. planirostris was the most important host for O. hasei, despite several other infested bat species, including N. leporinus, being also found. Our results suggest that N. leporinus is the most important host species for the study area in the municipality of Monte Negro, western Brazilian Amazon. Finally, we provide the first report of O. hasei on P. rubiginosus, which has been reported as the main host for O. marinkellei [41].

We detected the presence of “Candidatus R. wissemanii” in only one specimen of O. hasei, giving an infection rate of 1.2% (1/84). Previous studies reported this rickettsial agent in one out of three pools of O. hasei larvae from the state of Amapá, eastern Brazilian Amazon [63], in 28.9% (31/107) of O. hasei larvae from French Guiana [77], and in three O. hasei larvae from Argentina [78]. Our report is the first for the western Amazon. Although “Candidatus R. wissemanii” is a member of the spotted fever group of Rickettsia species, its pathogenic role in humans or animals remains to be evaluated [63–76]. Finally, Tahir et al. [75] also tested the O. hasei ticks for Borrelia and Coxiella DNA; similarly to the present study, no ticks were infected by these agents.

Some Rickettsia species are the etiological agents of spotted fever in humans, who acquire the infection through the bite of infected ticks; in Brazil, this is chiefly through ticks of the genus Amblyomma. The disease manifests itself a few days after the bite and evolves with a rash at the site of the bite, severe headache, chills, high fever and skin lesions (punctiform). If not treated early, the disease can progress to serious complications such as neurological disorders, kidney failure, respiratory problems and death [75]. Despite “Candidatus R. wissemanii” never having been associated with disease in humans or animals, it is novel tick-borne agent that was only recently described [63, 75, 76]. Therefore, this result should be better investigated in further studies.

In this study, the genomic investigations of the ectoparasites did not identify the genus Orientia; however, the disease caused by organisms of this genus, once limited to the Middle East, was recently identified in South America in mites and in serological surveys in humans, with a seroprevalence of 0.4%. Silva de La Fuente et al. [78] and Abarca et al. [79] describe the occurrence of Orientia sp. in southern Chile.

Though we did not detect Borrelia spp. in the present study, this bacterial genus has been recently reported in argasid ticks of the genus Ornithodoros in Brazil, including bat-associated ticks [80]. In the state of Ceará, Muñoz-Leal et al. [80] reported the presence of a Borrelia species of the relapsing fever group in O. hasei. Further studies are warranted to verify the circulation of relapsing fever in the state of Rondônia, where the argasid fauna is the richest in Brazil [80–81].

Coxiella burnetii is the etiologic agent of Q fever, a disease with acute and chronic presentations that is transmitted mainly by aerosols containing the bacteria. Cattle, sheep and goats are the main reservoirs. Less frequently, transmission can occur by the tick that becomes infected in a reservoir. Its clinical manifestations are similar to those of the other diseases mentioned above but the disease has low lethality [82]. This study did not detect this bacterium in the ectoparasite sample. Q fever is a disease with generic clinical manifestations, there are a few cases of the disease identified in Brazil [83]. Oliveira et al. [84] detected a high prevalence of C. burnetti DNA in the placental tissue of goats in the northeast of Brazil, which demonstrates the circulation of the pathogen and its threat to humans. Pacheco et al. [85] recently described two new strains of Coxiella in Amblyomma spp. ticks from Argentina, further confirming the circulation of the pathogen in South America. Mioni et al. [86], using seropositive samples of cattle blood, with antibodies against Coxiella, identified a significant prevalence of 12.2% using qPCR for C. burnetii DNA. This indicates the need for more intensive epidemiological surveillance by the governments of Brazil and Argentina. Serological studies should also be carried out in humans to estimate the burden of the disease.

The role of ticks in the transmission of Bartonella spp. is controversial, even though they has been found infected in nature (which does not necessarily class it as a vector). Other arthropods (lice and sandflies) are confirmed vectors. A cat’s scratch and/or bite can transmit the bacteria, as can the saliva, urine, and feces of bats. Depending on the species of Bartonella, it can have acute and chronic systemic clinical manifestations, mainly affecting the skin and heart, though it has low lethality [90].

The occurrence of Bartonella sp. has been found in five families of chiropterans [88] and in bat flies of the families Nycteribiidae and Streblidae. Regarding bats from the family Phyllostomidae, Ferreira [91] provided evidence on Bartonella, which is also prevalent in populations of bats and their ectoparasites in Brazil, helping to clarify the distribution of Bartonella sp. related to bat ectoparasites in South America [89]. In this study, infection by Bartonella is recorded for the first time in bat flies (Trichobius joblingi and Strebla mirabilis) in the Brazilian Amazon. Previously in the Amazon, Morse et al. [86] reported Bartonella in parasite flies in French Guyana. In Brazil, the occurrence of infections by Bartonella in parasitic bat flies was reported by Braga et al. [89] in the state of Maranhão, and by Amaral [87] in the state of Rio de Janeiro.

Hayman [33] and Subudhi et al. [34] highlight that, in recent years, interest in bat research has increased due to the occurrence of the spillover phenomenon, in other words, the transmission of a pathogen from its natural reservoir or host species to a new host species, thus enhancing the possibility of spreading diseases to humans and other mammals. In Brazil, the number of complaints of human infestations by bat ticks inside urban and rural households has increased substantially in recent years [93–96]. Indeed, health authorities should be aware of the possibility of emerging vector-borne diseases linked to bats in Brazil.

The Amazon has a great diversity of animals, much more than any other Brazilian biome; however, the state of Rondônia has little information regarding the diversity of bats and ectoparasites. In this study, it was possible to observe the diversity of bats of the Phyllostomidae family with 13 species being found; this is a diverse and versatile family in terms of its exploration of food, which includes fruit, nectar, insects, vertebrates and blood, among others. Furthermore, we can highlight the first report of O. hasei and “Candidatus R. wissemanii” for Rondônia. This study does not present new reports on the distribution of fly species and their relationship with chiropterans. Bacteria of the genus Bartonella with zoonotic potential were found in the bats Carollia brevicauda and Trachops cirrhosus in rural locations and forest fragments. The presence of this bacteria highlights the potential role in transmission between animals and humans. The family Molossidae, for the most part, was found in urban areas; however, there were no ectoparasites, but this raises the great possibility of spillover considering that chiropterans are often large reservoirs of disease.

Table 1

Ectoparasites and their detected organisms collected from bats in Monte Negro, Rondônia, Brazil.
BATS		Number		ECTOPARASITES	Number			Detected organisms
BATS		M	F	ECTOPARASITES	M	F	L	Detected organisms
Emballonuridae
	Emballonurinae
	Saccopteryx bilineata (Temminck, 1838)	3	3	Hooperella sp.	-	-	56	-
	Rhynchonycteris naso (Wied-Neuwied, 1820)	7	12	Basilia sp.	1	2	-	-
	Rhynchonycteris naso (Wied-Neuwied, 1820)	7	12	Spinturnix sp.	7	-	-	-
	Saccopteryx bilineata (Temminck, 1838)	-	1	-	-	-	-	-
Molossidae
	Molossinae
	Molossus Molossus (Pallas, 1766)	7	12	-	-	-	-	-
	Eumops perotis (Schinz, 1821)	2	5	Steatonyssus sp.	-	-	25	-
Mormoopidae
	Pteronotus rubiginosus (Wagner, 1843)	8	1	Trichobius sp.	9	9	-	-
				Paradyschira sp.	-	1	-	-
				Ornithodoros marinkellei	-	-	6	-
				Ornithodoros hasei*	-	-	10	-
				Cameronieta almaensis	23	2	-	-
Noctilionidae
	Noctilio leporinus (Linnaeus, 1758)	19	34	Ornithodoros hasei*	-	-	308	Candidatus Rickettsia wissemanii*
Phyllostomidae
	Carollinae
	Carollia brevicauda (Schinz, 1821)	13	21	Trichobius joblingi Strebla guajiro	17	20	-	Bartonella sp.
				Macronyssus sp.	6	-	-	-
	Carollia perspicillata (Linnaeus, 1758)	1	3	-	-	-	-	-
	Desmodontinae
	Desmodus rotundus (Geoffroy, 1810)	2	-	Trombiculidae	-	-	8	-
	Diphylla ecaudata (Spix, 1823)	3	1	-	-	-		-
	Glossophaginae
	Glossophaga soricina (Pallas, 1766)	2	-	Trichobius dugesii	-	3	-	-
	Glossophaga soricina (Pallas, 1766)	2	-	Periglischrus caligus	1		-	-
	Phyllostominae
	Lophostoma silvícola (d'Orbigny, 1836)	-	2	-	-	-	-	-
	Phylloderma stenops (Peters, 1865)	1	-	Periglischrus torrealbai	17	4	-	-
	Phyllostomus hastatus (Pallas, 1767)	2	-	Periglischrus acutisternus	19	4	-	-
	Phyllostomus latifolius (Thomas, 1901)	1	-	-	-	-	-	-
	Trachops cirrhosus (Spix, 1823)	-	1	Strebla mirabilis	4	1	-	Bartonella sp.
	Stenodermatinae							-
	Artibeus obscurus (Schinz, 1821)	12	33	Periglischrus iheringi	13	11	-	-
	Vampyrodes caraccioli (Thomas, 1889)	1	-	P. iheringi	2	1	-	-
	Sturnira lilium (Geoffroy Saint-Hilaire, 1810)	1	-	Periglischrus sp.	1	-	-	-
Vespertilionidae
	Myotinae			-	-	-	-	-
	Myotis riparius (Handley, 1960)	1	-	-	1	-	-	-
	Vespertilioninae						-
	Lasiurus villosissimus (Geoffroy St.-Hilaire, 1806)	-	1	-	-	-	-	-
	Lasiurus sp. (Gray, 1831)	-	1	-	-	-	-	-
TOTAL		86	131		121	58	413	-

* New records for Rondônia. M – male, F – female, L – larvae.

Acknowledgments

The authors are grateful to the Brazilian Government for the funding and Camila Maiara Silva Bonassi for her valuable help in the field

Funding

This study was funded by the National Institute of Science and Technology (EpiAmo), Brazilian Government

Author Contributions

LMAC: Conception, design of the work; interpretation of data; drafting of the work or substantial revision of it.

LFDJ: Capture and identification of bats, collection, and identification of ectoparasites, molecular analyses of ectoparasites and pathogens, and preparation of the manuscript.

INC: Identification of bats and preparation of the manuscript.

FRJ: Molecular analyses of ectoparasites and pathogens.

GG: Identification of Diptera and preparation of the manuscript.

RB-S: Molecular analyses of ectoparasites and pathogens and preparation of the manuscript.

FCJ: Molecular analyses of ectoparasites and pathogens and preparation of the manuscript.

MCAS: Molecular analyses of ectoparasites and pathogens.

MBL: Molecular analyses of ectoparasites and pathogens and preparation of the manuscript.

FACP: Preparation of the manuscript.

Availability of data and materials

Data is available from the National Institute of Science and Technology (EpiAmo), Brazilian Government

Ethical Approval

This study was submitted to and approved by Animal Ethics Committee of the University of São Paulo and licensed by SISBio Ministry of Science and Technology of the Brazilian Government.

Consent to publication

The following authors consent to the publication of the article “Ectoparasites that parasitizes bats (Mammalia, Chiroptera) and their pathogens in the central area of Rondônia, western Brazilian Amazon”.

Luís Marcelo Aranha Camargo____________________________________

Leormando Fortunato Dornelas Júnior______________________________

Irineu Norberto Cunha __________________________________________

Felipe Rodrigues Jorge__________________________________________

Gustavo Graciolli______________________________________________

Ricardo Bassini-Silva___________________________________________

Fernando de Castro Jacinavicius___________________________________

Maria Carolina A. Serpa_________________________________________

Marcelo Bahia Labruna__________________________________________

Felipe Arley Costa Pessoa _______________________________________

Competing interests

The authors declare that there are no competing interests

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No competing interests reported.

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Ectoparasitas em morcegos (Mammalia: Chiroptera) e seus patógenos na região central de Rondônia, oeste da Amazônia brasileira

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Bat capture and sample collection

Ticks

Mites

Diptera

Results

Bats

Ectoparasites

Discussion

Conclusion

Declarations

References

Additional Declarations

Status:

Version 1