This study reports 11 tick species and three tick-borne rickettsial agents in El Salvador. While the tick species A. dissimile, A. mixtum, A. ovale, A. cf. parvum, A. sabanerae and A. scutatum have been previously recorded on wild or domestic hosts in the country (Romero et al. 2021, 2023), we provide the first records of A. longirostre, D. panamensis, I. boliviensis, O. puertoricensis and O. megnini.. In addition, while R. amblyommatis has been reported in several tick species in El Salvador (Romero et al. 2021, 2023), this study reports for the first time in the country R. rhipicephali and a Rickettsia sp. endosymbiont of I. boliviensis.
The genus Amblyomma conforms the largest tick group in the Neotropical region, with at least 68 species, 55 of which are endemic to the region (Guglielmone et al. 2021; Soares et al. 2023). With our findings of A. longirostre, seven species of Amblyomma are currently recognized in El Salvador. For this compilation, we are considering previous records of A. parvum and Amblyomma auricularium as a single taxon for El Salvador, referred to as A. cf. parvum (Romero et al. 2021). Amblyomma longirostre has a wide distribution in the Neotropical region, occurring from southern Mexico to Uruguay. Previous records in Central America included Costa Rica, Belize, Honduras, and Panama (Guglielmone et al. 2021). The adult stage feeds mainly on porcupines (Guglielmone et al. 2021), supporting our finding of adults on S. mexicanus in El Salvador.
The genus Dermacentor is currently represented by nine species in the Neotropical region, where only four of them are endemic (Guglielmone et al. 2021). Previously, only two species of this genus, Dermacentor dissimilis and Dermacentor nitens, were recorded in El Salvador (Guglielmone et al. 2021). Our present records of D. panamensis expand its distribution in Central America, where it was previously described in Costa Rica, Guatemala, Honduras, Nicaragua and Panama (Apanaskevich and Bermúdez 2013). The major host for the adult stage of D. panamensis is the porcupine (S. mexicanus), whereas larvae and nymphs have been recorded in several rodent species, and nymphs also on porcupines and bats (Apanaskevich and Bermúdez 2013; Bermúdez et al. 2018). In line with these studies, we also found D. panamensis adults parasitizing the porcupine S. mexicanus. In addition, one free-living D. panamensis male was found in forest fragments at elevations of 1,761 m, also in the line with previous records from Panama, where D. panamensis inhabits cloud forests between 1,770–2,700 m (Apanaskevich and Bermúdez 2013; Bermúdez et al. 2018). This study provides the first genetic sequence of D. panamensis, showing that its 16S rRNA is at least 5% different from any other Dermacentor from GenBank.
The tick genus Ixodes is represented by 62 species in the Neotropical region, with 49 endemic (Guglielmone et al. 2021, Apanaskevich et al. 2022, Nava et al. 2023). Remarkably, I. boliviensis has been reported from southern North America to central South America, including the Central American countries Belize, Costa Rica, Honduras, Guatemala, Nicaragua, and Panama (Guglielmone et al. 2021). Ixodes boliviensis was originally described from Bolivia, but it also occurs in Colombia, Ecuador and Peru (Guglielmone et al. 2021). A recent study showed that I. boliviensis from Panama presented high genetic polymorphism (7–8% difference in the 16S rRNA gene) when compared to South American specimens (Bermúdez et al. 2021a). Due to this genetic and geographical differences, Bermúdez et al. (2021a) treated Panamanian specimens as I. cf. boliviensis. Interestingly, the 16S rRNA haplotypes of Salvadoran specimens were 3–4% different from specimens from Panama (GenBank sequences MW717932, MW717933, MW717934) and Costa Rica (OP470700, OP470701), and at the same time, 7% different from South American specimens (KM077437, OK557627). Genetic polymorphisms of I. boliviensis with different geographical origins throughout South America suggests that the taxon shows a high genetic diversity or it might represent a species complex to be evaluated in further studies.
In this study we also recorded an Ixodes sp. nymph whose 16S rRNA haplotype was 95–97% identical to I. silvanus, I. brunneus, I. turdus and I. frontalis, all parasites of birds. A recent phylogenetic study demonstrated that these four Ixodes species form a natural group, supporting their inclusion in the subgenus Trichotoixodes, which is composed by nine species, all associated with birds (Saracho-Bottero et al. 2021). Until 2021, only two Trichotoixodes species were known to occur in the Neotropical region: I. brunneus in Argentina, Colombia, Panama and Venezuela, and Ixodes copei in Jamaica (Guglielmone et al. 2021). A recent study concluded that I. brunneus is exclusively a Nearctic species and that previous reports of I. brunneus from Argentina represent a new taxon, described as I. silvanus (Saracho-Bottero et al. 2021). Moreover, reports of I. brunneus from Colombia, Panama and Venezuela could represent another taxon, yet to be elucidated (Saracho-Bottero et al. 2021). These authors also reported no discrete morphological differences between the nymph of I. brunneus and I. silvanus (the nymph of I. copei is undescribed). In fact, we were unable to highlight discrete morphological differences by comparing the photographs of the nymph of I. brunneus (Durden and Keirans 1996) with the nymph of I. silvanus (Saracho-Bottero et al. 2021). Morphological examination of the collected Ixodes sp. nymph from El Salvador revealed a high similarity to I. brunneus and I. silvanus; however, the Salvadoran specimen can be clearly separated from the other two species by the presence of long auriculae (Fig. 3), which are short in I. brunneus (Durden and Keirans 1996) and I. silvanus (Saracho-Bottero et al. 2021). This morphological feature, in conjunction with molecular and phylogenetic data, indicates that the Ixodes sp. nymph here reported represents an additional Ixodes species for El Salvador, that could represent either I. copei or another species closely related to I. brunneus pending formal description.
The genus Ornithodoros in the Neotropical region, have been reported in nearly 70 species, the majority endemic to this region (Guglielmone et al. 2004; Bermúdez et 2017; Muñoz-Leal et al. 2021). Ornithodoros puertoricensis is a nidicolous species with records in Central America, Caribbean islands, and northern South America (Guglielmone et al. 2004). This tick has been recorded from a wide array of vertebrates, included wild and domestic mammals, birds and humans (Bermúdez et al. 2017; López et al. 2021). In some rural areas of Colombia, O. puertoricensis was reported as a probably common parasite of domestic dogs (Paternina et al. 2009), which is in the line with the present record in El Salvador. Indeed, O. puertoricensis is of relevant public health because it is a human-biting tick that causes painful skin lesions (Bermúdez et al. 2017; López et al. 2021), and because a recent study reported the vector competence and isolation of a novel relapsing fever group agent, Borrelia puertoricensis, from O. puertoricensis in Panama (Bermúdez et al. 2021b).
The genus Otobius is composed by two species, but only O. megnini is present in the Neotropical region (Guglielmone et al. 2004). The nymphs have numerous spine-like processes and inhabit deeply in the host external ear canal; hence O. megnini is calling the spinous ear tick. It is the most widespread soft tick in Mexico, meanwhile records in Central America are restricted to Guatemala (Guglielmone et al. 2004; Nava et al. 2009; Hutcheson et al., 2021). Adults of O. megnini are not parasitic, meanwhile larvae and nymphs infest several domestic and wild animals included horses (as recorded here for El Salvador) and occasionally humans (Hutcheson et al. 2021). This tick is adapted to arid and semi-arid conditions but also is reported in humid localities (Nava et al. 2009). Our records in El Salvador were from moderately humid and warm areas. Otobius megnini is implicated in transmission of the agent of Q fever and causing myotonia in a horse (Zarate-Ram et al. 2014; Hutcheson et al. 2021).
The three rickettsial organisms detected in the present study belong to the SFG, which contains several agents that cause spotted fever illness in humans, such as R. rickettsii and R. parkeri (Parola et al. 2013). Rickettsia amblyommatis is the most common Rickettsia species detected in Central American ticks, associated with at least 10 tick species. Its pathogenic role in vertebrates and public health is not clear (Bermúdez and Troyo 2018). In Central America, there are reports of A. longirostre infected by R. amblyommatis in Costa Rica, Honduras, and Panama (Charles et al. 2021), and now in El Salvador (present study). Although there have been various records of R. rhipicephali in Dermacentor spp. ticks from North America (Parola et al. 2013), there are scattered information in Central America, where this agent has been detected only once in Dermacentor latus from Costa Rica (Moreira-Soto et al. 2023). Hence, this is the second report for Central America and the first record of any tick-borne agent in D. panamensis. The pathogenic potential of R. rhipicephali in humans remains unknown (Parola et al. 2013). Finally, our finding of a Rickettsia sp. endosymbiont in I. boliviensis is supported by previous records of such agent in I. boliviensis from Costa Rica and Panama (Troyo et al. 2014; Bermúdez et al. 2021a; Moreira-Soto et al. 2023). These previous studies showed that this rickettsial agent is phylogenetically related to rickettsial endosymbionts of other Ixodes spp. ticks, especially species belonging to the Ixodes ricinus species complex (Bermúdez et al. 2021a). Notably, at least one of these Ixodes-endosymbionts, named as Rickettsia monacensis, has been associated with clinical illness in humans in Europe (Parola et al. 2013).
With the present study, the current tick fauna of El Salvador is increased to 17 species, being 13 hard ticks (Ixodidae) and four soft ticks (Argasidae), including the addition of one genus to each of these two families (Ixodes and Otobius, respectively). The inclusion of Rickettsia sp. endosymbiont of I. boliviensis and R. rhipicephali increases to six the number of tick-borne rickettsial agents of El Salvador, with R. parkeri as the sole confirmed human pathogen infecting Salvadoran ticks.