First report of Amblyomma latepunctatum and the second record of Ixodes luciae in the state of Acre, Brazil

Primeiro relato de Amblyomma latepunctatum e o segundo registro de Ixodes luciae no estado do Acre, Brasil

Abstract

The state of Acre is in the western part of the Brazilian Amazon region and few studies involving ticks are available. The aim of the present study was to provide the first report of occurrence of Amblyomma latepunctatum and the second record of Ixodes luciae in Acre. Ticks were collected in October 2020 inside an open forested area in the municipality of Rio Branco, the state capital of Acre. Ixodid ticks were identified according to their external morphological characteristics. Three specimens were found on the vegetation by means of a visual search and were identified as Amblyomma scalpturatum (one male and one female) and Amblyomma latepunctatum (one male). Another specimen was found parasitizing a Didelphis marsupialis female that was caught using a Tomahawk trap; this was identified as Ixodes luciae (one male). This first report of A. latepunctatum in the state of Acre increases the number of species recorded here to 22. In addition, presence of I. luciae is confirmed in this state (second record), in the western Brazilian Amazon region.

Keywords:
Ixodidae; Amazon; parasitism; opossum

Resumo

O estado do Acre está localizado na Amazônia ocidental brasileira e apresenta poucos estudos envolvendo carrapatos. O presente estudo objetivou relatar, pela primeira vez, a ocorrência da espécie Amblyomma latepunctatum e o segundo registro de Ixodes luciae no estado do Acre, Brasil. A coleta de carrapatos foi realizada em outubro de 2020 no interior de uma floresta aberta no município de Rio Branco, capital do estado do Acre. Carrapatos ixodídeos foram identificados de acordo com suas características morfológicas externas. Três espécimes foram encontrados sobre a vegetação pelo método de inspeção visual e identificados como as espécies Amblyomma scalpturatum (um macho e uma fêmea) e Amblyomma latepunctatum (um macho); e outro foi encontrado parasitando uma fêmea de Didelphis marsupialis que foi capturada por uma armadilha Tomahawk, e identificado como Ixodes luciae (um macho). Este primeiro relato de A. latepunctatum no estado do Acre aumenta o número de espécies registradas aqui para 22. Além disso, a presença de I. luciae é confirmada no estado do Acre (segundo registro), na região da Amazônia ocidental brasileira.

Palavras-chave:
Ixodidae; Amazônia; parasitismo; gambá

Amblyomma latepunctatum was originally described by Tonelli-Rondelli (1939) through examining two females deposited in the Museo Zoologico, Università Degli Studi de Firenzi, Florença, Italy (Onofrio, 2007). Aragão & Fonseca (1953) relegated A. latepunctatum to a synonym of Amblyomma scalpturatum Neumann, 1906 and this remained the situation until Labruna et al. (2005a) redescribed the adult stages of these species based on morphological and molecular analyses, and confirmed A. latepunctatum as a valid species.

Currently, the geographical distribution of this ixodid species is in South America, with reports from Peru, Ecuador, Venezuela, Guiana (published as British Guyana), Brazil (Labruna et al., 2005a) and, most recently, French Guiana (Binetruy et al., 2019). In Brazil, it was previously reported in the states of Amazonas (Labruna et al., 2005a; Gianizella et al., 2018), Rondônia and Pará, all in the northern region of this country (Labruna et al., 2005a, b).

The adult stages of A. latepunctatum seem to show specificity of parasitism for Tapirus terrestris (tapirs), since they are frequently found on these mammals (Binetruy et al., 2019; Gianizella et al., 2018; Labruna et al., 2005a, b, 2010). The nymph stage of A. latepunctatum has already been reported parasitizing Tayassu pecari (peccaries) in Brazil (Gianizella et al., 2018) and Peru (Labruna et al., 2010); and Dasyprocta fuliginosa (agoutis), Didelphis marsupialis (opossums) (Guglielmone et al., 2014; Gianizella et al., 2018) and Hydrochoerus hydrochaeris (capybaras) in Brazil (Martins et al., 2014).

Although Labruna et al. (2005a) reported that they encountered adults of A. latepunctatum “crawling” on humans, the first record of adult ticks of this species feeding on humans was made by Gianizella et al. (2018) in the state of Amazonas, Brazil. Presence of its immature stages parasitizing humans was reported in French Guiana by Binetruy et al. (2019), whose larval stage of A. latepunctatum had not been reported yet (Guglielmone et al., 2014).

The state of Acre is one of the Brazilian states in which few studies on ticks have been conducted. Its ixodid fauna currently consists of 21 species (Tojal et al., 2020). In the present study, the presence of A. latepunctatum in the state of Acre was shown for the first time, along with a second record of Ixodes luciae.

In 2020, ticks were collected along animal trails inside an open forested area in the municipality of Rio Branco (10°00’48.4” S 68°14’31.5” W), the capital of the state of Acre (northern Brazil) (Figure 1A, B), in the western part of the Amazon region (Tojal et al., 2020). During one of these collections, in October 2020, were realized the visual search method in the search for ticks (Terassini et al., 2010) and Tomahawk traps for capturing animals, using corn, bacon and ground peanut candy (paçoca) as bait. After tick collection, the animal specimen was released in the same place where it had been caught.

Figure 1
(A) Map of Rio Branco, Acre; (B) Trail in open forest; Didelphis marsupialis (C).

The tick specimens were collected with permission from the Chico Mendes Institute for Biodiversity Conservation (ICMBio), under license number 69.943-4; and with permission from the Ethics Committee for Animal Use of the Federal University of Acre (UFAC), under protocol 36/2019.

The tick specimens thus collected were placed in plastic tubes containing absolute ethyl alcohol and were taken to the Tropical Medicine Laboratory (LABMEDT) of the Federal University of Acre, to be identified and stored under refrigeration at -20 °C, Subsequently, they were sent to the Coleção Nacional de Carrapatos Danilo Gonçalves Saraiva, at the University of São Paulo (CNC-FMVZ/USP). The specimens were identified under a Leica M205 stereoscope, using the dichotomous keys for adult ticks of Onofrio et al. (2006, 2010) and redescriptions by Labruna et al. (2005a).

Three adult specimens of ixodid ticks, comprising two males (M) and one female (F), were found at heights of 70 cm (M) and 55 cm (F) above ground level, on vegetation (adaxial position). Another male was found feeding on a female of the Didelphis marsupialis opossum (Mammalia: Didelphimorphia), which is known in that region as “mucura” (Figure 1C). One tick was observed, attached to its skin, so we decided to collect it with the aid of tweezers, directly from the host still imprisoned.

The male specimens were morphologically identified as Amblyomma latepunctatum Tonelli-Rondelli, 1939 (Figure 2A, B), and Amblyomma scalpturatum Neumann, 1906, and the female also as A. scalpturatum. The specimen collected from the opossum was identified as Ixodes luciae Sénevet, 1940 (Figure 2C, D).

Figure 2
(A, B) Amblyomma latepunctatum male; (C, D) Ixodes luciae male.

The male of A. latepunctatum that was collected on the vegetation presented the diagnosis described by Labruna et al. (2005a) for this species, especially the presence of deep punctations throughout the scutum and the absence of brown elevations without punctations. In contrast, males of A. scalpturatum and Amblyomma incisum Neumann, 1906 have elevations without punctations in the scutum (Labruna et al., 2005a). Another characteristic that was observed in the specimen of this study was the presence of chitinous blades incised in all festoons, characteristic that can be confused with the species A. incisum (Labruna et al., 2005a). In this regard, in a review on the tick species of the state of Acre, Lima et al. (2018) suggested that there was a need to confirm the species A. incisum, which may have been confused with the species A. latepunctatum and A. scalpturatum. As so, A. incisum had only been reported once, by Aragão (1936), through examining the material in the Ixodid Collection of the Oswaldo Cruz Institute. About A. scalpturatum was confirmed by Aguirre et al. (2019) through morphological and molecular analyses (subjected to sequencing of the ITS2 gene). Now, through the present study, occurrence of the species A. latepunctatum in the state of Acre has been confirmed.

These findings of A. latepunctatum and A. scalpturatum in the same environment and presenting ambush behavior at the edges of leaves, at a height equivalent to that of their main host (tapirs), confirm what Labruna et al. (2005a) reported. They considered the species A. latepunctatum, A. scalpturatum and A. incisum (northern group) to be sympatric in the Amazon region. This had already been observed in studies in the state of Rondônia (Labruna et al., 2005a). This also suggests that in the future it will be possible to confirm the presence of A. incisum (northern group) in the state of Acre.

The finding of occurrence of A. latepunctatum in Acre expands the geographical distribution of this species in the Amazon biome and in Brazilian territory, where it had previously been described in the states of Amazonas, Rondônia and Pará (Labruna et al., 2005a). This also demonstrates that this species is not restricted to dense forest, as in the study conducted by Labruna et al. (2005a), but can also be found on vegetation that allows light to penetrate to the understory layer of an open forested (Silveira et al., 2008), which is a characteristic of our study area.

Less is known about the population of the tick A. latepunctatum than about the populations of the other two sympatric species. Therefore, more information needs to be gathered, such as in relation to its life cycle dynamics, seasonality in this region, presence of immature stages in the hosts and its vector capacity for infectious agents. It is important to mention that A. latepunctatum is a tick species that bite humans (Gianizella et al., 2018). It is closely related to A. scalpturatum, which has been found infected with Rickettsia amblyommatis (spotted fever group - SFG) in the Amazon biome (Colle et al., 2020).

A thorough investigation of genotypes of the genus Rickettsia found in ticks collected in French Guiana yielded three Rickettsia strains that were present in all A. latepunctatum tick samples (Binetruy et al., 2020). The analyses revealed that two of these strains were related to the Rickettsia species in the SFG and that the other was the species Rickettsia bellii (Binetruy et al., 2020). However, further studies are needed in order to elucidate whether A. latepunctatum might have the capacity to become infected with a pathogenic Rickettsia species.

The species I. luciae, which was found parasitizing D. marsupialis, is widely distributed from southern Mexico to Argentina and the Caribbean islands (Díaz et al., 2009), in the following countries: Argentina, Bolivia, Peru, Brazil, Ecuador, Colombia, Venezuela, Surinam, French Guiana, Costa Rica, Guatemala, Belize, Honduras, Mexico, Nicaragua, Panama and Trinidad and Tobago (Labruna et al., 2009; Onofrio et al., 2010).

Morphological examination of the I. luciae male found in this study showed that this species had larger scutal punctations (Figure 2C) and a longer external spur on coxa I (Figure 2D). These characteristics distinguish it from other, closely related Ixodes species (Ixodes loricatus, Ixodes schulzei and Ixodes amarali) (Onofrio et al., 2010).

The main aspects of the ecology of I. luciae are basically unknown (Díaz et al., 2009), but it has frequently been mentioned in the literature that its adult stage is primarily found on marsupials and that the immature stages parasitize small marsupials and rodents (Labruna et al., 2005b, 2009). A study conducted in the Peruvian Amazon region demonstrated that in the natural cycle of I. luciae, the nymphal stage of this species parasitizes rodents, while knowledge of the preferred hosts of the larval stage still seems to be uncertain (Díaz et al., 2009).

There is no evidence that this species should be considered to be a vector for humans (Díaz et al., 2009). However, given that infection by R. belli in I. luciae has been confirmed in French Guiana (Binetruy et al., 2020) and that there is one record of females of I. luciae parasitizing humans in Argentina (Ivancovich & Luciani, 1992), special attention should be paid to this tick species as a possible vector of potentially pathogenic agents.

Ixodes luciae has been reported in Brazil in the following states: Acre, Amazonas, Mato Grosso do Sul, Pará and Rondônia (Onofrio et al., 2010; Lima et al., 2018). In Acre, adults of I. luciae were found to be present at CNC-FMVZ/USP, which resulted in the first report of this species in the state (Guglielmone et al., 2011; Lima et al., 2018). The present in situ finding confirms the presence of the species I. luciae in Acre.

Thus, the present study provides the first report of the species A. latepunctatum in the state of Acre and confirms the presence of the species I. luciae. This finding of A. latepunctatum in Acre increases the ixodid fauna of the state to a total of 22 species.

Acknowledgements

This study was supported by the National Epidemiological Institute of the Western Amazon Region (Instituto Nacional de Epidemiologia na Amazônia Ocidental, INCT-EpiAmO), National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico, CNPq) and Pro-Rectorate for Research and Postgraduation (Pró-Reitoria de Pesquisa e Pós-Graduação) of the Federal University of Acre (UFAC).

• How to cite: Tojal SD, Meneguetti DUO, Martins TF, Labruna MB, Aguirre AAR, Siebra EAM, et al. First report of Amblyomma latepunctatum and the second record of Ixodes luciae in the state of Acre, Brazil. Braz J Vet Parasitol 2021; 30(3): e007221. https://doi.org/10.1590/S1984-29612021063

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Publication Dates

• Publication in this collection
  09 July 2021
• Date of issue
  2021

History

• Received
  16 Apr 2021
• Accepted
  15 June 2021