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The family Ixodidae, whose members are commonly known as hard ticks, is composed of 758 species distributed around the world, of which 137 are present in the Neotropics, and are represented by the genera Ixodes, Dermacentor, Haemaphysalis, Rhipicephalus and Amblyomma (Guglielmone et al. 2021). Amblyomma spp. inhabit diverse habitat types throughout their geographic distribution (Nava et al. 2017).
Three species have been described in Chile: adult individuals of A. triste Koch, 1844, recorded in the extreme north of the country, near the border with Perú (Abarca et al. 2012), A. parvitarsum Neumann, 1901, present in the altiplano in Chile (González-Acuña et al. 2004a) and immature individuals of this species were collected in the periarid mediterranean zone bordering the Chilean altiplano (Muñoz-Leal et al. 2014), and A. tigrinum Koch, 1844, which is present from the Coquimbo to Aysén regions (Guglielmone et al. 2021; Abarca et al. 2016). The first record of A. tigrinum in Chile was located in the central-southern zone, with findings of ticks parasitizing wild canids, which was mistakenly identified as A. maculatum by Tagle & Álvarez (1957), and then, corrected by the same authors (Tagle & Álvarez 1959). Adult stages of A. tigrinum are classified as strictly or moderately specific for the order Carnivora (Hoogstraal & Aeschlimann 1982), usually parasitising wild canids and dogs mainly in rural areas (Abarca et al. 2016) and occasionally humans and other hosts (Eberhardt et al. 2020; Nava et al. 2017; Abarca et al. 2016; Abarca et al. 2013; González-Acuña et al. 2003; Muñoz & Casanueva 2002; Guglielmone et al. 2000). While immature stages can be found parasitizing small rodents (Cricetidae and Caviidae) and ground forest feeding birds, constituting crucial hosts for the maintenance of the life cycle of A. tigrinum in natural environments (Nava et al. 2017; Guglielmone & Nava 2010; Nava et al. 2006; González-Acuña et al. 2004b; Guglielmone et al. 2000).
The Molina’s hog-nosed skunk (Conepatus chinga Molina, 1782) is a South American medium-sized mammal belonging to the Mephitidae family, which is distributed across the southern limit of Brazil, northern Argentina, Uruguay, Bolivia and central Chile (Kasper et al. 2009), inhabiting shrubby open and rocky hillside habitats (Donadio et al. 2001). In Chile, the species is distributed from Coquimbo to Los Lagos regions (Muñoz-Pedreros & Yáñez 2009). Currently, the scientific literature has been mostly focused in ecological (Kasper et al. 2012; Castillo et al. 2011; Reppucci et al. 2009), dietary (Montalvo et al. 2008; Donadio et al. 2004) and taxonomic (Schiaffini et al. 2013) aspects of Molina’s hog-nosed skunk. While the role of this mammal as endoparasite host has been previously reported (Gómez-Puerta et al. 2012; Gómez- Puerta et al. 2009; Pietrokovsky et al. 1991), there is still scarce evidence on ectoparasite species parasitizing skunks along its native range (Labruna et al. 2005; Almeida et al. 2003).
Here, we documented the first finding of A. tigrinum parasitizing a Molina’s hog-nosed skunk captured at a rural area in north-central Chile. We performed morphological identification and description of collected tick individuals.
The study was conducted in the coastal zone of the Coquimbo region in north-central Chile (71°12’ to 71°40’W, 29°58’ to 30°39’S). The study area poses a semiarid weather with a mean annual rainfall of 126.8 mm, with 90% of rainfall concentrated during winter months (May-September), and warm, dry summers (December-March) (Montecinos et al. 2016). Mean temperature ranges from 12ºC to 18ºC (measured at 2 m above ground nearby the coast), and relative air humidity can reach 90 to 100% at higher altitudes. Field site was a private 31 km2-site inserted into the “El Tangue” ranch, a farm of nearly 45,000 ha situated 10 km south of Tongoy town. The property is characterized by a mosaic of agricultural fields, grasslands, and a mixture of exotic shrub plantations (i.e., Atriplex nummularia Lindl.) and pioneer native vegetation, with small properties scattered along the westward border distance up to 3 km of the field site.
In April 2020, we sampled a male Molina’s hog-nosed skunk to assess their tick loads at the sampling location. Within capture efforts targeting wild foxes, the skunk was captured with a soft leg-hold trap, which was kept active for a minimum of seven consecutive days, baited with tuna and a commercial lure (Murray’s Wolf Urine, West Virginia, USA), and checked at least every six hours to reduce animal stress. After physical immobilization, we anesthetized the skunk with a mixture of ketamine (2.5mg/kg) and dexmedetomidine (70μg/kg), and reverted with atipamezole (350μg/kg), modified from wild carnivore protocols reported by Acosta- Jamett et al. (2010). The skunk was aged as adult based on incisor wear and eruption (Olifiers et al. 2010), while its weight was estimated to be ~3 kg for the calculation of anesthetic doses. While anesthetized, we inspected the animal body coat and collected ticks during 10 minutes. The skunk was released at the site of capture. Ticks were stored into a 2 ml Corning® cryovial (Corning Incorporated, Lowell, Massachusetts, USA), labeled with a unique code and kept with ice packs. After ticks were preliminary identified, sexed and counted, they were placed in liquid nitrogen, transported to the Universidad Austral de Chile in Valdivia, and stored at -80 ºC (for other research purposes). Two ticks were placed into 70% ethanol before definitive morphological characterization. All procedures for animal trapping and handling were approved by Universidad Austral’s Bioethics Committee for Research Animal Use (314/2018 - 315/2018) and Chilean Livestock and Agricultural Service (Resolución Exenta Nº 6184/2019 - 2128/2020).
Two ticks were analyzed morphologically following the key of Estrada-Peña et al. (2005). Ticks were photographed in a scanning electron microscope (SEM) (Hitachi SU3500) utilized Ultra Variable-pressure Detector (UVD), backscattered electrons y cool stage system, and an Euromex (NexiusZoom) stereo microscopic.
We collected a total of nine ticks (eight males and one female), which corresponded to A. tigrinum. The two morphologically analyzed ticks corresponded to males of this species, which have a long and strong spine on coxa I and IV, spur on coxa IV not reaching anus, coxa II and III with a short and obtuse spine (Fig. 1A), one spine on tibiae II to IV (Fig. 1B), spiracular plate comma-shaped (Fig. 1C), ornate scutum (Fig. 2A), absent of tubercles on ventral side of festoons, marginal groove complete (Fig. 2B), mouthparts longer than the base of the capituli (Fig. 2C). (Santa Cruz et al. 2011; Estrada-Peña et al. 2005).
The literature referred to ectoparasites hosted by Molina’s hog-nosed skunk is mostly restricted to records of Ornithodoros brasiliensis Aragao, 1923 (Labruna et al. 2005) and Neotrichodectes spp. (Tricodectidae) (Almeida et al. 2003), being our study the first record of the occurrence of A. tigrinum in this mephitid in Chile and South America. Although adult stages of A. tigrinum typically parasite wild and domestic canids
(Guglielmone et al. 2021), other carnivores belonging to the families Felidae (i.e., Leopardus colocolo Molina, 1782 (Martins et al. 2011), Puma concolor Linnaeus, 1771 and Pathera onca Linnaeus, 1758 (Durden et al. 2006)) and Procyonidae (i.e., Nasua nasua Linnaeus, 1766 (Magalhães-Matos et al. 2017)) can also harbor this tick species; including domestic dogs (Tomassone et al. 2010; Guglielmone et al. 2000) and cats (Guglielmone et al. 2000), and other non-carnivore species as suids, cervids and bovines (Nava et al. 2017; González-Acuña et al. 2006).
FIGURE 1 Amblyomma tigrinum male ventral view in SEM. A. Black arrow: Long and strong spine on coxa I and IV. White arrow: coxa II and III with a short and obtuse spine. Sp: Spiracle. B. Star: one spine on tibiae II. C. Spiracular plate comma-shaped. / Vista ventral del macho de Amblyomma tigrinum en SEM. A. Flecha negra: Espina larga y pronunciada en las coxas I y IV. Flecha blanca: coxa II y III con una espina corta y obtusa. Sp: Espiráculo. B. Estrella: una espina en las tibias II. C. Placa espiracular en forma de coma.
FIGURE 2 Amblyomma tigrinum male. A. Dorsal view in stereo microscopic, s: ornate scutum. B. Dorsal view in SEM, Black arrow: Marginal groove complete, f: Festoons. C. Ventral view in SEM, p: Palps, h: Hypostome. / Macho de Amblyomma tigrinum. A. Vista dorsal en microscopio estereoscópico, s: escutum ornamentado. B. Vista dorsal en SEM, Flecha negra: Surco marginal completo, f: Festones. C. Vista ventral en SEM, p: Palpos, h: Hipostoma.
Given the plasticity of A. tigrinum to thrive across areas with contrasting climatic conditions across its geographic distribution (Mendoza-Uribe & Chávez-Chorocco 2004; Guglielmone et al. 2000), and tick moderate specificity for canid hosts (Hoogstraal & Aeschlimann 1982), may support Molina’s hog-nosed skunk as a potentially suitable A. tigrinum host. Indeed, previous studies have characterized the wild carnivore community inhabiting the study area, which is compounded mostly by canids as culpeo (Lycalopex culpaeus Molina, 1782) and chilla (Lycalopex griseus Gray, 1837) foxes that inhabit the study area (Hernández et al. 2021); both fox species have been reported to harbor A. tigrinum and they co-occur with Molina’s hog-nosed skunk across this zone (data not published); perhaps suggesting potential cross-species tick infestation from environments they share. Our finding contributes to expand the records about other carnivore species acting as A. tigrinum hosts, which may have certain epidemiological interest considering this tick species may act as vector of zoonotic infectious agents (Romer et al. 2014; Abarca et al. 2013; Pacheco et al. 2013).
