This study reports ticks collected from wild carnivores from different habitat types in Panama. We examined 94 individual wild carnivores and we found 87 parasitized by ticks: seven coyotes, six crab-eating foxes, 54 coatis, four raccoons, five ocelots, two pumas, two gray foxes, two skunks, and one each of kinkajou, jaguar, jaguaroundi, greater grison and tayra. We identified 13 species of tick: Ornithodoros puertoricensis, Amblyomma auricularium, A. dissimile, A. mixtum, A. oblongoguttatum, A. ovale, A. parvum, A. pecarium, A. tapirellum, A. varium, Haemaphysalis juxtakochi, Ixodes affinis, Rhipicephalus sanguineus s.l. and immatures of Ixodes and Amblyomma. Amblyomma ovale and A. oblongoguttatum were the most common species, found on nine and six carnivore species respectively. This is the first report of A. oblongoguttatum on Puma yagouaroundi and Procyon lotor; of A. dissimile, A. pecarium, A. tapirellum and A. varium on Nasua narica; and A. auricularium on P. lotor. Our data do not enable us to establish incidence of tick parasitism, but add valuable information to the current knowledge of the tick species that infest wild carnivores in Panama.
Ticks comprise a group of blood-feeding mites that parasitize all classes of terrestrial vertebrates (Labruna et al. 2005). Around 188 species have been reported for the Neotropics (Guglielmone et al. 2003a, Labruna & Guglielmone 2009), 47 of which are known to occur in Panama (Fairchild et al. 1966). Because ticks cause serious economic losses in animal husbandry and have severe effects on human health, most studies focus on synanthropic ticks. As a result, the species that parasitize wild animals remain poorly studied, despite their importance for understanding tick ecology pathogen transmission dynamics (Durden & Keirans 1996, Szabó et al. 2003).
The difficulty of capturing wildlife is among the major drawbacks for establishing reliable host-parasitic relationships. This is especially true for wild carnivores, which are usually cryptic and elusive. Carnivores remain difficult to study despite the advent of new technologies, such as camera traps or GPS telemetry enabling the collection of substantial information about their behavior and ecology (Moreno 2006, Moreno et al. 2012). Wild carnivores are interesting in the context of parasite ecology, because many species have large home ranges and could be exposed to many species of ticks, depending on preferred habitats and preys (Labruna et al. 2005). In contrast to South America (Labruna et al. 2005, Martins et al. 2011), few studies have reported tick species parasitizing wild carnivores in Central America.
In Panama, Fairchild et al. (1966) listed 11 species of ticks that parasitize wild carnivores. Additional data on ticks parasitizing captive and road-killed carnivores were recently collected, including the firsts reports of ticks from Panamanian coyotes (Canis latrans) and crab-eating fox (Cerdocyon thous) (Bermúdez et al. 2013, Murgas et al. 2013). In this paper we present new data about ticks collected from wild carnivores in Panama, complementing the sparse information currently available.
From 2010 to 2014, ticks collected from wild carnivores from different environments throughout Panama were donated to the Instituto Conmemorativo Gorgas de Estudios de la Salud (ICGES) by wildlife researchers (see acknowledgments). We complemented the data with that presented in previous reports (Bermúdez et al. 2013, Murgas et al. 2013). Collected ticks were preserved in 70% ethanol, except for engorged immature and females, which were kept alive in a controlled environmental incubator (78% RH, 26°C).
Larvae from the engorged females and unfed larvae collected from the carnivores, were infested on naïve rabbits and guinea pigs to facilitate molting; later, nymphs obtained were infested again on rabbits to reach the adult stage. These adults, and the adults obtained from engorged nymphs from the carnivores, were used for morphological identification.
The taxonomic keys of Fairchild et al. (1966) were used for tick species identification; however, we followed the taxonomic criteria of Nava et al. (2014) for the Amblyomma cajennense species group. In addition, we identified 22 nymphs using DNA barcoding, by amplifying the 5′region of the COI mitochondrial gene using standard invertebrate primers (LCO 1490 and HCO2198; Folmer et al. 1994). Sequences were compared with those belonging to adult ticks from Panama that were identified to species morphologically and whose sequences have been deposited in BOLD. Voucher specimens of each species were deposited in the Dr. Eustorgio Méndez Zoological Collection of ICGES or remain at the Smithsonian Tropical Research Institute (STRI).
Results and Discussion
Of the 95 individual carnivores examined in different habitat types, ticks parasitized 87, belonging 14 of the 22 species of wild carnivores present in Panama: three out of four species of wild canids, four of six species of felids, two of four species of mustelids, four of seven species of procyonids and the single species of Mephitidae (Conepatus semistriatus). The site characteristics where wild carnivores were examined are listed in Table 1.
A total of 13 tick species were collected, one Argasidae, Ornithodoros puertoricensis, and 12 Ixodidae, Amblyomma auricularium, A. dissimile, A. mixtum, A. oblongoguttatum, A. ovale, A. ci. parvum, A. pecarium, A. tapirellum, A. varium, Haemaphysalis juxtakochi, Ixodes affinis, and Rhipicephalus sanguineus s.l. In addition, many immatures of Ixodes and Amblyomma were collected. Adults of A. oblongoguttatum, A. ovale, A. tapirellum and A. mixtum were molted to the adult stage in the laboratory. In addition, by comparing DNA barcoding of adults morphologically identified and immatures it was possible to recognize nymphs of A. oblongoguttatum, A. pecarium and A. tapirellum. We also found engorged females of A. ovale and A. oblongoguttatum on different hosts, and a partially engorged. dissimile female was collected from a coati. In addition, six mating pairs of I. affinis were collected from ocelots. Table 2 provides the number, stage and sex of ticks recorded from each host species.
Habitat characteristics for sites where wild carnivores were examined for ticks in Panama.
Various factors can influence a host's level of parasitism by ticks. Each wild carnivore species has different activity patterns and behavior such as foraging (including hunting), reproduction, resting and grooming. Some species of mustelids and felids avoid human presence, while other species (e.g. coyotes and raccoons) have high tolerance to human activity (Sunquist & Sunquist 2002, Hunter 2012). Each tick species is adapted to thrive under specific environmental conditions (e.g. weather, microclimate and type of vegetation), which limits its distribution to specific habitat types, and also affects its ability to survive under new conditions or establish in new sites (Fairchild et al. 1966, Estrada-Peña et al. 2013). Furthermore, depending on the species and life stage, ticks have adopted different strategies for finding their hosts: some are endophilic (i.e. live in host burrows and nests), while others are exophilic (i.e. seek or wait for hosts on vegetation) (Walker et al. 2003).
Ticks recorded from carnivores in Panama.
Rhipicephalus sanguineus s.l. and A. mixtum are common in both rural and disturbed areas, and are strongly associated with domestic animals and synanthropic wildlife (Guglielmone et al. 2003a). Rhipicephalus sanguineus s. 1. colonized the Americas with the introduction of Old World dogs during the European colonization, and currently parasitize dogs in all kinds of human environments, even thriving in highly urbanized cities (Guglielmone et al. 2003, Moraes-Filho et al. 2011). In rural towns, wandering dogs could disperse engorged specimens of R. sanguineus s. 1. to peridomestic areas, and hunting dogs may introduce this tick into secondary or primary forest. Because R. sanguineus s. 1. did not evolve in Neotropical ecosystems, further study is needed to determine pathways by which this tick might move from domesticated to wild animals. Under these conditions, wildlife is susceptible to being parasitized by R. sanguineus s.l. (Labruna et al. 2005, Bermúdez et al. 2010).
In contrast, A. mixtum is a native species that prefers dry habitats such as shrubs and herbaceous patches (Fairchild et al. 1966, mentioned as A. cajennense). Currently, logging of native forest has caused the expansion of this type of vegetation along the Pacific slopes of Panamanian lowlands, which has favored the dispersion of A. mixtum. Immatures and adults of this species are considered to be catholic parasites, because they feed from different groups of vertebrates in these areas. Thus, finding mid-sized carnivores parasitized by R. sanguineus s.l. suggests their presence near to human dwellings, while parasitism by A. mixtum in these mammals is related to their presence in landscape dominated by pastures or shrubs.
In degraded dry areas, A. auricularium, A. parvum and O. puertoricensis were found on wild carnivores. The regular hosts of A. auricularium are armadillos, with only occasional findings on other groups of mammals (Guglielmone et al. 2003b). However, both A. parvum and O. puertoricensis appear to be generalist ticks, because they have many species of hosts reported along their entire distribution. In the case of A. parvum, 46 species of mammals are reported as hosts (Nava et al. 2008), and the hosts of O. puertoricensis include more than 20 species of mammals, one bird, two reptiles and one toad, which can be attributed to their nidicolous behavior (Endris et al. 1989, Bermúdez et al. 2013).
Amblyomma ovale, A. oblongoguttatum and I. affinis seem to have wild carnivores among their preferred hosts in primary and secondary rain forests (Guglielmone et al. 2003a, Labruna et al. 2005). In this study, this was demonstrated by the presence of many immature and adults of these species, including engorged females, and by the finding of mating pairs of I. affinis on ocelots. These tick species exhibit an opportunistic behavior with their environment, tolerating a certain degree of anthropogenic disturbance, that permits feeding from domestic mammals in small towns adjacent to forests (Bermúdez & Miranda 2011, Szabó et al. 2012, Murgas et al. 2013). The plasticity of A. ovale and A. oblongoguttatum explains their parasitism on felids, coatis and mustelids in both intact and degraded forest, but also on coyotes, gray foxes and raccoons in rural environments.
Our records of adults of A. varium and A. dissimile on N. narica are notable, as adults of these ticks are typically parasites of sloths and ectothermic vertebrates, respectively (Fairchild et al. 1966, Guglielmone et al. 2003a, Guglielmone and Nava 2010). Secondary and primary forests are the preferred habitat for A. varium, and A. dissimile. Thus, coatis parasitized with these ticks may reflect an opportunistic parasitic behavior in response to the presence of these hosts in the habitat. To find A. dissimile on endothermic vertebrates is an unusual event, especially a partially engorged female (Guglielmone and Nava 2010).
Forested areas allow immatures of other tick species to parasitize wild carnivores, as shown by our data. In the case of H. juxtakochi, its principal hosts as adults are Artiodactyla, but the immature stages are eclectic parasites (Fairchild et al. 1966, García et al. 2014). To our knowledge, these are the probably first records of carnivores as hosts for nymphs of both A. tapirellum and A. pecarium. Although both species have been recorded previously from Panama (Dunn 1933), there is little information about their hosts of the immature life stages.
In addition to data presented in this study, Fairchild et al. (1966) reported: Ixodes rubidus on Mustela frenata, Bassaricyon gabii, C. semistriatus and Eyra barbara, Ixodes boliviensis on puma, j aguar, raccoon and coati; Amblyomma naponense on crab-eating raccoon and coati, and unidentified Ixodes ticks on Neotropical river otter Lutra annectes (probably Lontra longicaudis) in Panama.
In conclusion, our results add a significant contribution to the current knowledge of tick-host relationships in Panama. Further studies using diverse methodologies are necessary to gain a better understanding of the parasitic relationship between ticks and wild carnivores, including sampling highlands, banks of rivers and forest canopy. Moreover, since ticks are important vectors of pathogens that can affect domestic animals and humans, further ecological research investigating the role of wild carnivores as disease reservoirs is warranted.
The authors thank Pedro Méndez-Carvajal (Fundación Pro-Conservación de los Primates Panameños), Nestor Correa (Asociación Panamericana para la Conservación), Ben Hirsch, Patrick A. Jansen, Roland Kays (Smithsonian Tropical Research Institution), Rodrigo Chang (Autoridad del Canal de Panamá), Nataniel Kadoch (Ministerio de Desarrollo Agropecuario), Daniel González and Aydee Comejo-Remice (ICGES) for providing ticks. We are also grateful to Celestino Aguilar and Matthew Miller for DNA barcoding, to Ninon Meyer (STRI) and Robyn Nadolny (Old Dominion University, Virginia, US) for the English revision, and Alberto Guglielmone (Instituto Nacional de Tecnología Agropecuaria, Argentina) for his comments on an earlier version of the manuscript. HJE received funds from the Smithsonian Grand Challenges Award and the graduate school of Production Ecology and Resource Conservation of Wageningen University.
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