Distribution of ectoparasites of Canis lupus familiaris L. (Carnivora: Canidae) from Panama Distribución de los ectoparásitos de Canis lupus familiaris L. (Carnivora: Canidae) de Panamá

Objetive. To determine the distribution of ectoparasites in dogs in Panama. Materials and methods. There were surveyed 720 canines belonging to 57 communities. Results. The results showed that 84% of the dogs were infested with at least one species of ectoparasite. Dogs from lowlands showed a higher percentage of parasitism and a greater biodiversity of parasites than dogs from highlands. There were found seven species of ticks, four species of fleas, two species of lice, and one specie of botfly. The ticks Rhipicephalus sanguineus, Amblyomma cajennense, A. ovale and the flea Ctenocephalides felis were widespread; however Ixodes boliviensis and Pulex simulans showed a much narrower geographic distribution and they were found only in dogs from highlands. The flea species Rhopalopsyllus cacicus and the tick Haemaphysalis juxtakochi were found for the first time in panamanian dogs. Conclusions. The environmental situation in Panama, can encourage that wildlife ectoparasites parasitized dogs in absence of their native hosts. This condition may increase transmission risk of some diseases where the ticks and fleas are vectors.


Conservation of ectoparasites.
The ectoparasites were preserved in 95% alcohol. Engorged ticks nymphs were collected and kept alive in plastic bottles plugged with cotton, and then placed in an incubator (average temperature of 29ºC and 80% of humity) until molt.

INTRODUCTION
Dogs were the first animal species to be domesticated by humans and have been used extensively as hunters, protection purposes and as food (1,2). The domestication process took place in several isolated geographic localities over a period of many centuries, producing the diversity of breeds that we know today (3). Presently, dogs are considered pets instead of wild animals, and live in close association with humans.

RESULTS
There were examined 720 dogs from 57 towns and found that 84% of the animals were infested by at least one ectoparasite ( Table  1). The highest prevalence of parasitism was observed in dogs from suburban and rural localities in lowlands (altitude: 0-1000 meters). Dogs from highland towns presented a much lower prevalence. Dogs from lowland towns exhibited a greater richness of ectoparasites than conspecifics from the highlands ( Table 2).
Seven species of ticks, four species of fleas, two species of lice and one botfly were observed ( Table 2). The only species that it could raise was Amblyomma cajennense. The species with greatest distributions were the flea Ctenocephalides felis and the ticks Rhipicephalus sanguineus s.l., A. cajennense and Amblyomma ovale. The tick, Ixodes boliviensis and the fleas Pulex simulans and Rhopalopsyllus cacicus, were restricted to high-lands.

DISCUSSION
Rhipicephalus sanguineus s.l. was found in all towns from rural and urban lowlands. This species was introduced to the New World from Old World dogs and infest multiple species of Carnivores with domestic cats and dogs being the preferred hosts (9). According to Guglielmone et al (9), the development of this tick, including an extra-parasite cycle after feeding, enables it to spread to new localities and infest new host, including humans.
This close proximity to humans makes R. sanguineus the most implicated pathogens in diseases dispersions, such as spotted fever on America (R. rickettsii) (10,11), mediterranean spotted fever (Rickettsia conorii) (12) and canine ehrlichiosis (Ehrlichia canis) (13). In Panama, genetic material of R. amblyommii has been found in R. sanguineus (14), species implicated to cause a mild fever, even when its impact to humans is unknown in many counties.
In this study, we found the co-existence of R. sanguineus with A. cajennense, A. oblongoguttatum, A. ovale, Haemaphysalis juxtakochi and Ixodes affinis on the same host or localities. The frequency of co-existence of R. sanguineus and 1 Urbans towns with a population between 50,100-100,000 habitants. 2 Urbans towns with a population between 10,000-50,000 habitants. 3 Urbans towns with a population between 5,000-10,000 habitants. 4 Rural towns. 5 Total dogs sampled, 6 Number of dogs with ectoparasites, 7 Percentage of parasitized dogs. A. cajennense on the same dogs was associated with horses and cattle in areas of pecuariam activities. In contrast to R. sanguineus, the immature and adults of A. cajennense infests a wide variety of host and is one of the most commons ticks species found on domesticated animals in Panama (5). This species show a preference for disturbed areas, especially sites where deforestation creates habitats that are more adequate for their establishment (15).
In Latin American, A. cajennense affects mostly humans and transmits R. ricketsii in many countries (16). In Panama, A. cajennense has been found as vector of R. rickettsii (17) and R. amblyommii was detected from the genetic material of horses and dogs (14). In this study, nymphs and adults of A. cajennense were collected in dogs.
The co-existence of R. sanguineus with A. oblongoguttatum, A. ovale, H. juxtakochi and I. affinis occurred in rural populations, indigenous towns and in sub-urban areas near forests. Dogs in communities close to forest were often used for hunting wild animals and this function may explain the infestations of dogs by these ticks. Immature stages from these species parasitize mostly small mammals and birds while adults infest medium to large-sized mammals, including dogs (5,9). The tick parasitism on domestic animals could allow alternate conditions for the establishment of new pathogens in humans populations increasing the associated risks for pathogen transmission. This is the first record of H. juxtakochi parasitized panamanian dogs. Former records of this species include host as Nasua nasua, tapirs, deer and the porcupine Coendou rothschildi (5,9).
Ixodes boliviensis was only found in rural communities within an elevation of 1100-1500 meters. Fairchild et al (5) stated that this species was most common in dogs from altitudes close to 850 meters (2500 feet); however, during this study, we found did not find any I. boliviensis in localities under this altitude. Instead, we observed R. sanguineus and A. ovale in towns with similar altitudes to those cited, as habits for I. boliviensis, by Fairchild et al (5). Differences between these studies can be explained by the increases in human populations in those communities that have created conditions favorable for the establishment of R. sanguineus.
In contrast to highlands communities as Boquete, Volcan and Cerro Punta (Table 2), which have also experienced a significant increase in human populations, only I. boliviensis has become established, suggesting that towns in altitudes greater than 1000 meters limit the distribution of R. sanguineus in Panama. Even though the possibility of infested dogs with R. sanguineus from lowlands can occur in these populations, the establishment of population of these ticks needs further verification.
The Costa Rican localities from the Province of Cartago (Puricil and Tapanti) have altitudes between 1300 and 1400 meters. In these areas, I. boliviensis is present but not R. sanguineus, a result that has also been observed in Panama (Carlos Víquez, personal communication). In urban areas from the Costa Rican cities like Heredia and San José, which has an average altitude of 1200 meters, R. sanguineus is commonly found, while I. boliviensis only is observed in rural zones (Grace Alpízar, personal communication).
These differences in the distribution between R. sanguineus and I. boliviensis in Costa Rica and Panama at similar altitudes, but different human population densities, can be explained by the extension of urban development.
A city with wide urban zones provides more opportunities for R. sanguineus to colonize and develop populations. Similarly, these conditions minimize opportunities for the establishment of I. boliviensis, due this species needs different hosts for immature stages as well as adequate oviposition sites. Additionally, high levels of urbanization increase the local temperature and influences general weather patterns; conditions that also favor the establishment of R. sanguineus. distribution across Panama, it was found on every dog from urban, suburban and rural localities within 0-1400 meters. A previous study showed that C. felis is the fleas with a major dispersion in Panama (8). In contrast, C. canis has a narrower range, being only found in rural localities from Darién and Kuna Yala ( Table 2). This flea is considered to be rare species and was included in the Tipton and Méndez (8) based upon only one reference point by Dunn (op. cit).

Ctenocephalides felis maintain a wide
Pulex similans were captured exclusively on dogs from Boquete and co-exists with I. boliviensis, C. felis and R. cacicus saeus. Tipton and Méndez (8) discussed the difference between P. irritans and P. simulans, and characterized P. simulans as a lowland species and P. irritans as highland species (over 5000 feet). To distinguish these species, we used the aedeagus, the main morphological character proposed by Smit (18). We reviewed this character in specimens of P. irritans from United States and Colombia (CoZEM), compared them with the specimens from Volcan and Boquete, and found that they exhibited the aedeagus morphology of P. simulans.
Rhopalopsyllus cacicus was only found in dogs from Boquete. Tipton  On the other hand, Trichodectes canis and Heterodoxus spiniger were collected from dogs from Central Provinces and Darien. These records provide new data regarding the distribution of these ectoparasites in Panama.
The only previously reported site was Panama City. Trichodectes canis is a primary ectoparasite of Canidae, and maintains a close relationship with its host (4). This species infests dogs, coyotes, foxes and wolves in different regions from America (7), whereas in Europe (Check Republic), it has been found on Nyctereutes procyonoides (19), demonstrating its adaptability to parasites wild canids.
Unlike T. canis, H. spiniger has also been found on cats and dogs, which are alternative hosts (20,21). These lice are primarily parasites of marsupials (e.g. kangaroos, wallabies), establishing associations with dogs only in modern times (22,23). This species is Pantropical, nevertheless, its distribution in many Neotropicals countries is poorly documented (21).
During this study, Dermatobia hominis was the only species found to be causing myiasis in dogs. According to Bermúdez et al (24), the myiasis produced by this species in dogs corresponded to 64% of reported cases in Panama during the 2002-2005. These same authors indicated the other flies as Cochliomyia macellaria and an unidentified species of Lucilia (=Phaenicia sp.) can cause myiasis in dogs. The parasitism is commonly associated with towns near forests of other wooded sites.
In conclusion, the environmental situation in Panama, can encourage that wildlife ectoparasites parasitized dogs in absence of their native hosts. This condition may increase transmission risk of some diseases where the ticks and fleas are vectors (as ehrlichiosis and rickettsiosis).