Distribucion de los ectoparasitos de Canis lupus familiaris L. (Carnivora: Canidae) de Panama.
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.
The domestication of the dog also created new ecological interactions between the ectoparasites of these canines and humans, exposing people to new pathogenic agents. There are many ectoparasites of dogs that serve as reservoirs, vectors, or intermediate hosts for pathogenic bacteria, fungi and metazoan parasites (e.g., tapeworms and roundworms). Bacteria such as Rickettsia rickettsii, Rickettsia felis, Ehrlichia chaffeensis and parasitic helminths like Dipylidium caninum and Hymelonepis nana, are examples of microorganisms that are associated with ectoparasites of dogs and that also can affect humans (4).
Studies of ectoparasites of panamanian dogs are scarce. The only complete checklist was published in 1966 in the "Ectoparasites of Panama", by Fairchild et al (5) and there have been no other published studies on this subject. The objective of this paper is to present new data regarding the distribution of the ectoparasites infesting Panamanian dogs and to describe their ecological relationships.
MATERIALS AND METHODS
Study site. From June 2007-April 2009, we collected ectoparasites from dogs representing 57 communities in Panama (Figura 1) as part of a larger effort from several different research projects (see acknowledgement). The selection of dogs depended on the owners consent.
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 29[degrees]C and 80% of humity) until molt.
Identification of ectoparasites. For the identification we using published descriptions for ticks (5, 6), lice (7), fleas (8). In addition, we revised the reference material from the Coleccion Zoologica "Dr. Eustorgio Mendez" of the Gorgas Memorial Institute for Health Research (CoZEM-ICGES for Spanish acronomy) in Panama City. The ectoparasites were placed in CoZEM-ICGES collection.
[FIGURE 1 OMITTED]
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.
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 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 Viquez, personal communication). In urban areas from the Costa Rican cities like Heredia and San Jose, which has an average altitude of 1200 meters, R. sanguineus is commonly found, while I. boliviensis only is observed in rural zones (Grace Alpizar, 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.
Ctenocephalides felis maintain a wide 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 Darien and Kuna Yala (Table 2). This flea is considered to be rare species and was included in the Tipton and Mendez (8) based upon only one reference point by Dunn (op. cit).
Pulex similans were captured exclusively on dogs from Boquete and co-exists with I. boliviensis, C. felis and R. cacicus saeus. Tipton and Mendez (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 and Mendez (8), affirm that R. cacicus is a parasite of several species of mammals, such as opossums (Metachirus nudicaudatus and Philander opossum), armadillos (Dasypus novencinctus), rodents (Proechimys semispinosus, Agouti paca and Dasyprocta punctata) and carnivores (Nasua nasua). Our observation represents the first geographical record of this ectoparasite for Panamanian dogs. Previously, these authors registered R. australis tupinus in dogs of a non-specified locality.
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 Bermudez 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).
This work was sponsored by the following projects: "Estudios de las enfermedades asociadas a ectoparasitos de Cerro Chuganti, con enfasis en Rickettsiales" (data from Western Darien and supported by SENACYT, grant 00046852), "Vigilancia Epidemiologica Panama-Colombia" (data from East Panama and financed by Panama Government), "Proyecto Hantavirus" (data from Central Provinces Azuero, by SENACYT, MINSA, ICGES); "Determinacion de los ectoparasitos de mamiferos en El Valle" (data from El Valle with partial sponsor by ICGES). Special thanks to Mauricio Caballero for sent material, Enrique Medianero for the facilities in Chiriqui highlands and Bocas del Toro; Grace Alpizar (Ministerio de Agricultura of Costa Rica) and Carlos Viquez (Instituto Nacional de la Biodiversidad, Costa Rica) for their comments; Victor Townsend (Virginia Wesleyan College) for editorial suggestions, and Marcelo Labruna (University of Sao Paulo, Brazil) for comments on an earlier version of this manuscript.
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Sergio Bermudez C,  * M.Sc, Roberto Miranda C,  M.Sc.
 Instituto Conmemorativo Gorgas de Estudios de la Salud, Ciudad de Panama, Panama, * Correspondencia: email@example.com
Recibido: Junio de 2010; Aceptado: Diciembre de 2010
Table 1. Conditions of the towns and numbers of dogs samples. Province Type of town /Town A (1) B (2) C (3) D (4) Bocas del Almirante # Toro Bocas del Toro # Chanquinola # Srilico Creek # Cocle Aquadulce-EI Roble # Anton # El Valle # Las Guias # Nata # Penonome # Colon Gamboa # Colon-Marqarita # Donoso-Guayabalito # San Lorenzo # Chiriqui Alanje # Alto Boquete # Boqueron # Cerro Punta # David # # Puerto Armuelles # Rio Sereno # Volcan-Renacimiento # Darien Jaque-Biroquera # Meteti-Rio Iqlesias # Santa Fe # Yaviza # Herrera Chitre # El Toro # Monaqrilo # Ocu # Pese # Potuqa # Los Santos Aqua Buena # La Villa # Paritilla # Pedasi # Tonosi # Panama Arraiian-Bique # Chame-Beiuco # Chepo # Ciudad de Panama # La Chorrera # Lidice # Torti # Veraguas Canazas # La Mesa # Las Palmas # Montiio # San Bartolo # Santa Fe # Sona # Comarca Cerro Banco # Nobe Buqle Soloy # Comarca Armila # Kuna Yala La Miel # Mulatupo # Puerto Obaldia # TOTAL Province Dogs sampling /Town Altitude (N) (5) (n) (6) (meters) Bocas del Almirante 5 4 4 Toro Bocas del Toro 25 7 7 Chanquinola 10 7 7 Srilico Creek 50 13 17 Cocle Aquadulce-EI Roble 40 21 15 Anton 50 4 4 El Valle 600-800 51 34 Las Guias 50-120 2 2 Nata 30-50 11 11 Penonome 75 3 5 Colon Gamboa 80 7 6 Colon-Marqarita 20 3 5 Donoso-Guayabalito 40 5 5 San Lorenzo 20 2 2 Chiriqui Alanje 30 18 15 Alto Boquete 1100-1500 5 4 Boqueron 120 3 3 Cerro Punta 2100-2200 17 4 David 30 21 18 Puerto Armuelles 0-20 13 8 Rio Sereno 750 5 5 Volcan-Renacimiento 1500 7 2 Darien Jaque-Biroquera 0-15 21 21 Meteti-Rio Iqlesias 50 34 27 Santa Fe 45 16 16 Yaviza 34 47 38 Herrera Chitre 20 5 2 El Toro 30-70 16 16 Monaqrilo 80-120 3 5 Ocu 110 11 11 Pese 30 8 8 Potuqa 100 5 5 Los Santos Aqua Buena 80 11 11 La Villa 70 7 7 Paritilla 40-100 3 3 Pedasi 0-20 13 13 Tonosi 300 7 7 Panama Arraiian-Bique 0-30 2 2 Chame-Beiuco 0-80 6 6 Chepo 50-80 17 17 Ciudad de Panama 0-80 27 17 La Chorrera 50-120 62 45 Lidice 80 8 8 Torti 50 52 52 Veraguas Canazas 200 5 5 La Mesa 80 4 4 Las Palmas 100 3 3 Montiio 10 1 1 San Bartolo 70 6 6 Santa Fe 400-600 6 6 Sona 110 6 6 Comarca Cerro Banco 580 4 4 Nobe Buqle Soloy 120 5 5 Comarca Armila 0-5 15 15 Kuna Yala La Miel 0-10 6 6 Mulatupo 0-20 5 3 Puerto Obaldia 0-50 20 20 TOTAL 720 604 Province Dogs sampling /Town (%) (7) Bocas del Almirante 100 Toro Bocas del Toro 100 Chanquinola 100 Srilico Creek 83 Cocle Aquadulce-EI Roble 71 Anton 100 El Valle 66 Las Guias 100 Nata 100 Penonome 55 Colon Gamboa 85 Colon-Marqarita 55 Donoso-Guayabalito 100 San Lorenzo 100 Chiriqui Alanje 83 Alto Boquete 80 Boqueron 100 Cerro Punta 23 David 85 Puerto Armuelles 61 Rio Sereno 100 Volcan-Renacimiento 28 Darien Jaque-Biroquera 100 Meteti-Rio Iqlesias 73 Santa Fe 100 Yaviza 100 Herrera Chitre 4 El Toro 100 Monaqrilo 55 Ocu 100 Pese 100 Potuqa 100 Los Santos Aqua Buena 100 La Villa 100 Paritilla 100 Pedasi 100 Tonosi 100 Panama Arraiian-Bique 100 Chame-Beiuco 100 Chepo 100 Ciudad de Panama 62 La Chorrera 72 Lidice 100 Torti 100 Veraguas Canazas 100 La Mesa 100 Las Palmas 100 Montiio 100 San Bartolo 100 Santa Fe 100 Sona 100 Comarca Cerro Banco 100 Nobe Buqle Soloy 100 Comarca Armila 100 Kuna Yala La Miel 100 Mulatupo 100 Puerto Obaldia 100 TOTAL 84 (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. Note: All filled cell are indicated with #. Table 2. Species of ectoparasites for town. Ectoparasites Collected Province Amblyomma Amblyomma /Town cajennense oblongoguttatum Bocas del Almirante Toro Bocas del Toro Chanquinola Srlllco Creek # Cocle Aquadulce-EI Roble Anton # El Valle Las Guias # Nata Penonome Colon Gamboa # Colon-Marqarlta # Donoso-Guayabalito San Lorenzo # # Chiriqui Alanje # Alto Boquete Boqueron Cerro Punta David # Puerto Armuelles Rio Sereno Volcan-Renacimiento Darien Jaque-Biroquera Meteti-Rio Iqlesias # Santa Fe # Yaviza Herrera Chitre El Toro Monaqrilo # Ocu # Pese # Potuqa # Los Santos Aqua Buena La Villa # Paritilla Pedasi Tonosi # Panama Arraiian-Bique # Chame-Beiuco Chepo # Ciudad de Panama # # La Chorrera # Lidice # Torti # Veraguas Canazas # La Mesa Las Palmas Montiio # San Bartolo # Santa Fe Sona # Comarca Cerro Banco # Nube Buqle Soloy # Comarca Armila # Kuna Yala La Miel Mulatupo # Puerto Obaldia Ectoparasites Collected Province Amblyomma Haemaphysalis Ixodes Ixodes /Town ovale juxtakochi affinis bollvlensis Bocas del # Toro # # Cocle # # # # # # Colon # # # Chiriqui # # # # # Darien # # # # Herrera Los Santos # # Panama # # # # Veraguas # Comarca # Nube Buqle # Comarca # Kuna Yala # # # Ectoparasites Collected Province Rhipicephalus Ctenocephalides Ctenocephalides /Town sanguineus canis felis Bocas del # Toro # # Cocle # # # # # # # # # # # # Colon # # # # # # # # Chiriqui # # # # # # # # # # # Darien # # # # # # # # # Herrera # # # # # # # # # # # # Los Santos # # # # # # # # Panama # # # # # # # # # # # # # # Veraguas # # # # # # # # # # # # # Comarca # Nube Buqle # Comarca # # Kuna Yala # # # # # Ectoparasites Collected Province Pulex Rh opalopsyllus Heterodoxus Trichodectes /Town similans cacicus spiniger canis Bocas del Toro # Cocle # # Colon Chiriqui # # # # Darien # # # # # # Herrera Los Santos Panama # # # Veraguas # # Comarca Nube Buqle Comarca Kuna Yala Ectoparasites Collected Province Dermatobia /Town hominis Bocas del # Toro # Cocle # Colon # Chiriqui Darien # Herrera # Los Santos # Panama # # # Veraguas Comarca Nube Buqle Comarca Kuna Yala Note: All filled cell are indicated with #.
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|Author:||Bermudez C., Sergio; Miranda C., Roberto|
|Publication:||Revista MVZ (Medicina Veterinaria y Zootecnia)|
|Date:||Jan 1, 2011|
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