Amblyomma auricularium (Acari: Ixodidae) in Nine-Banded Armadillo, Dasypus novemcinctus: A New Record for the Neotropical Region of Mexico

Abstract

The nine-banded armadillo, Dasypus novemcinctus, is one of only two species of armadillo found in Mexico. Among the ectoparasites reported on this mammal are ticks of the genus Amblyomma. Between December 2022 and April 2024, 52 ticks of different developmental stages (females, males, and nymphs) were collected from five D. novemcinctus. All ticks were morphologically identified as A. auricularium. This study reports for the first time the presence of this tick species in the Municipality of Santiago Llano Grande, Oaxaca.

1. Introduction

Amblyomma auricularium [1], also known as Brazilian ear tick or Carrapato vérmelo do tatú, is a species with Neotropical distribution, with records in the Nearctic region of Mexico and the United States. The morphology of this species has been confused, and several species could probably be hidden under this name. This has been complicated by the fact that the type specimen of A. auricularium that would serve to make comparisons has been lost [2,3]. The main hosts of the adults of this species include members of the family Dasypodidae (order Cingulata), such as Cryptophractus sp. and Dasypus spp. while the larvae and nymphs have been reported on some members of the family Didelphidae (order Didelphimorphia) and Procyonidae (order Carnivora). Other hosts for the different developmental stages include the families Bovidae, Canidae, Caviidae, Chinchillidae, Mustelidae, Myrmecophagidae, Equidae, Iguanidae, Accipitridae, and several species of Passeriformes [4,5].

In Mexico, A. auricularium has been recorded parasitizing species of different groups of vertebrates, including iguanas (Iguanidae), armadillos (Dasypodidae), dogs (Canidae), pacas (Cuniculidae), ocelots (Felidae), and anteaters (Myrmecophagidae) [3].

In particular, two species of armadillos are distributed in the country, the naked-tailed armadillo (Cabassous centralis, Chlamyphoridae) [6] and the nine-banded armadillo (Dasypus novemcinctus, Dasypodidae) [7].

For the nine-banded armadillo (D. novemcinctus, knowledge about its ectoparasites includes some records of fleas (Pulex porcinus Jordan and Rothschild, 1923, and Rhopalopsyllus australis (Rothschild, 1904)), Trombiculidae mites (Axiogastia dasypi Loomis, 1966) and hard ticks of the Ixodidae family (A. auricularium and Amblyomma parvum Aragao, 1908) [3,8,9].

According to the Mexican Official Standard (NOM-O59-SEMARNAT-2010) [10], the nine-banded armadillo is subject to special protection since its populations are declining due to the loss of its habitat as a result of human activity, in addition to hunting for subsistence and commercial use [11,12].

In addition, in several indigenous communities in the country, their use includes traditional medicine, crafts, and leatherwork, besides to being highly appreciated for their meat [13,14]. Their consumption as meat is of interest in public health, since D. novemcinctus can be infected by bacteria, fungi, and protozoa that cause diseases related to consumption and direct contact with this species of mammal [15].

Based on the above, the objective of this study was to identify ticks that are associated with nine-banded armadillos captured in the Municipality of Santiago Llano Grande, Oaxaca, where the capture of this mammal is carried out mainly for human consumption.

2. Materials and Methods

This study was carried out in the Municipality of Santiago Llano Grande, in the state of Oaxaca (Figure 1), between December 2022 and April 2024. The municipality is located in the Pacific coast region (16°29′22″ N and 98°17′23″ W), at an altitude of 69 m above sea level. The area is 11,482 hectares and represents 0.12% of the total area of the state [16]. The climate is warm humid tropical, with a maximum temperature of 42 °C (average, 25–30 °C in summer, May–September) and a minimum of 14 °C (winter, December–March), and the annual rainfall average is 1350 mm, usually in summer [16].

The type of vegetation in the area is subdeciduous forest; however, the degree of deterioration of the primary vegetation is very high at present. Plants are represented by some specimens of Ceiba spp., Cordia boissieri, Enterolobium cyclocarpum, Gliricidia sepium, Quercus spp., and Swietenia macrophylla. The wildlife is mainly composed of mammals such as Dasypus novemcinctus, Herpailurus yagouaroundi, Martes martes, Nasua narica, Odocoileus virginianus, Procyon lotor, Spilogale pygmaea, Sylvilagus cunicularius. Reptiles as Basiliscus basiliscus, Boa constrictor, Crotalus spp., Ctenosaura pectinata, Iguana iguana, and Micrurus spp. Among birds, Anas spp, Cyrtonyx montezumae, Dendrocygna autumnalis, Ortalis poliocephala, and Zenaida spp. can be found [17].

Armadillos (Dasypus novemcinctus) were captured by trapping by hunters of the area for commercial purposes; the ticks collected from these mammals were fixed in 70% ethanol and subsequently transported to the Multidisciplinary Laboratory of the Faculty of Veterinary Medicine and Animal Husbandry No. 2 of the Universidad Autónoma de Guerrero, where they were analyzed.

All ticks were washed with distilled water and placed in Petri dishes for their observation and taxonomic determination, using a stereomicroscope (Amszoom, Mainland China, Model YK20230606) and specialized taxonomic keys [18,19,20].

3. Results

A total of 52 ticks (20 females, 24 males, and 8 nymphs) were collected from five armadillos (

Table 1. Number of ticks collected by development stage and ecological parameters of the species A. auricularium associated with D. novemcinctus in the Municipality of Santiago Llano Grande, Oaxaca.

Host	Total Ticks		Nymphs			Females		Males
		Uf	SE	E	Uf	SE	E
1	5	-	-	-	1	2	1	1
2	6	-	1	-	-	-	-	5
3	7	-	1	-	-	-	-	6
4	14	3	2	-	1	2	1	5
5	15	-	-	1	6	2	-	6
1	5	-	-	-	1	2	1	1
Total	52	3	4	1	9	8	3	24

Uf: unfed, SE: semi-engorged, E: engorged.

). The ticks were identified as A. auricularium, and the specimens were compared with the descriptions of females and males reported [5,21,22].

A brief description of the observed specimens is presented below.

Amblyomma auricularium (Conil, 1878) (Figure 2).

Female: total length (n = 1) 3.9 mm, width 2.3 mm. Scutum inornated, dark-brown on the margins and yellow-brown in the center, with small and fine shallow punctations, evenly distributed; cervical grooves short and comma-shaped; marginal groove complete, beginning at the posterior margin of the scutum. Eleven rectangular festoons. Eyes flat. Dorsal base of capitulum subrectangular, cornua very short; porose areas oval shaped. Hypostome length 0.8, width 0.2, apically rounded, dentition 3/3. Legs: coxae I with two subequal, blunt-tipped spurs (the outer slightly longer than the inner one); coxae II–IV with a small triangular spur; trochanters I–II with spurs, the first larger (Figure 3).

Male: total length (n = 1) 2.8 mm, width 1.7 mm. Body outline oval, widest at leg IV. Scutum inornated and yellowish-brown, with small and shallow punctations, evenly distributed; cervical groves short, almost straight; marginal grove complete. Slender festoons with rectangular chitinous plates beyond posterior edge. Eyes flat. Dorsal base of capitulum rectangular, cornuae small. Hypostome 3/3, length 0.7, width 0.2. Pedipalp segment I ventrally with a posteriorly directed spur. Legs: coxa I with two blunt-tipped spurs, the outer one longer than the inner one. Coxae II-IV with a single, triangular spur; trochanters I-II as in female (Figure 3).

Nymph: total length (n = 1) 2.9 mm, width 1.9 mm. Scutum inornate with shallow medium punctations, evenly distributed. Eyes not orbited. Basis capituli rectangular, posterior margin slightly concave, without cornua. Hypostome 2/2. Oval idiosoma, slightly elongated, with 11 festoons. Coxa I with two blunt-tipped spurs, the external longer than internal; coxae II–IV with a small spur. Trochanters without spur.

4. Discussion

Amblyomma auricularium was described from specimens collected from the big hairy armadillo, Chaeotophractus villosus, in Argentina [1]. Later, Robinson [23] synonymized A. auricularium with A. concolor (Neumann, 1899), but years later, Camicas et al. [24] considered it valid. Keirans and Hillyard [25] stated that A. concolor was actually a synonym of A. auricularium, since the latter species had been described first.

Guglielmone and Viñabal [26] grouped A. auricularium together with A. parvum Aragão, 1908, A. pseudoparvum Guglielmone, Mangold and Keirans, 1990, and A. pseudoconcolor Aragão, 1908, due to the fact that they presented spurs on the trochanters (those on leg I being more conspicuous). In addition, A. auricularium, A. pseudoconcolor, and A. pseudoparvum are characterized by a lack of ornamentation. However, it is worth mentioning that some authors have reported the presence of ornamentation on the shield of A. auricularium [27,28,29].

On the other hand, Camicas et al. [24] treated A. pseudoconcolor as a synonym of A. auricularium; however, this was not accepted by other authors who reported that the adults of both species could be separated morphologically [26,28,30]. Camicas et al. [24] also considered Amblyomma curruca (Schulze, 1936), as a valid taxon, even though Aragão and Fonseca [31] considered it a synonym of A. parvum, while Fairchild et al. [32] referred to it as a synonym of A. auricularium.

Likewise, in the illustration of A. curruca (Schulze, 1936), the male seems to present chitinous plates that extend posterior to the festoons, which is not characteristic of A. auricularium but of A. parvum [33,34]. In this context, Guglielmone et al. [35] referred to the need to reexamine the holotype of A. curruca to determine whether this species represents a synonym of A. parvum. In Mexico, Hoffmann [36] recorded the presence of A. curruca from specimens collected in 1937 from an armadillo from Yucatán, Mexico. In this work, she also redescribed the female, as well as the nymph and larva, which were assumed to belong to the same species.

The morphological characteristics observed in our specimens coincide with those indicated by Voltzit [21], who observed specimens collected of D. novemcinctus from Honduras, and that were identified as A. auricularium. The characters included the presence of small rectangular plates protruding from the margin of the festoons, a characteristic that also seems to be present in A. curruca (Schulze, 1936); however, according to Nava et al. [5], Bermúdez et al. [22], and Guglielmone et al. [34], this characteristic resembles A. parvum.

The designation of a type specimen for A. auricularium is necessary to provide a detailed redescription of the species. This will allow comparisons among specimens that were identified as A. auricularium and with those that have been synonymized with this species. New collections and the use of integrative taxonomy will be necessary to achieve this [3,4].

In Mexico, the presence of this tick has been recorded in the states of Chiapas, Michoacán, Nayarit, Sinaloa, Tabasco, Tamaulipas, and Yucatán [19,37,38,39,40]. From a medical and veterinary perspective, the presence of Rickettsia amblyommatis has been reported in Brazil and the United States in association with A. auricularium [41,42]; some isolates of this Rickettsia species are known to cause mild pathologies in both animals and humans [43,44]. Finally, the life cycle in nature is poorly understood, but it can be compared with that of other members of the genus Amblyomma [45]. However, some experimental data on its life cycle are available. According to the description by Faccini et al. [46] A. auricularium fed to rabbits and maintained at 27 °C, with relative humidity ≈70–90% and 24 h of darkness, can complete its life cycle in approximately 125 days (4 months). Other specific details are cited in the manuscript.

5. Conclusions

The natural distribution of species is key to understanding the planet’s biodiversity. This morphological study shows variations in what is known as A. auricularium; however, further studies with an integrative approach across its distribution are required to determine whether other species are masked under this name. Furthermore, it is necessary to determine the presence of pathogens that could potentially cause public and veterinary health problems.