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Distribucion de los ectoparasitos de Canis lupus familiaris L. (Carnivora: Canidae) de Panama.

Distribution of ectoparasites of Canis lupus familiar's L. (Carnivora: Canidae) from Panama

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.

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]

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 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).

Acknowledgements

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.

REFERENCES

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(2.) Germonpre M, Sablin M, Stevens R, Hedges R, Hofreiter M. Stiller M, Despres V. Fossil dogs and wolves from Palaeolithic sites in Belguim, the Ukraine and Russia: Osteometry, ancient DNA and stable isotopes. J Arch Sci 2008; 36(2):473-490.

(3.) Leonard J, Wayne R, Wheeler J, Valadez R, Guillen S, Vila C. Ancient DNA evidence for Old World origin of New World dogs. Science 2002; 298:1613-1616.

(4.) Guimaraes J, Tucci E, Barros-Battesti D. Brasil: Fapesp. Edit. Pleide; 2002.

(5.) Fairchild G, Kohls G, Tipton V. The ticks of Panama. In: Ectoparasites of Panama. Chicago: Field Museum of Natural History; 1966.

(6.) Onofrio V, Labruna M, Pinter A, Giacomin F, Barros-Battesti D. Comentarios e chaves as especies do genero Amblyomma. Carrapatos de Importancia Medico-Veterinaria da Regiao Neotropical Brazil: Instituto Butantan, SP; 2006.

(7.) Price R, Hellenthal R, Palma R, Johnson K, Clayton D. The chewing lice world checklist and biological overview. Illinois: Natural History Survey Special Publication; 2003.

(8.) Tipton V, Mendez E. The fleas of Panama (Siphonaptera). Ectoparasites of Panama. Chicago: Field Museum of Natural History; 1966.

(9.) Guglielmone A, Estrada-Pena A, Keirans J, Robbins R. Las garrapatas (Acari: Ixodida) de la region zoogeografica neotropical. Argentina: Inst Nac Tec Agrop; 2004.

(10.) Child J, Paddock C. Rocky Mountain Spotted Fever. Rickettsial Diseases. New York: Informa HealthCare; 2006.

(11.) Cunha N, Fonseca A, Rezende J, Rozental T, Ravacho A, Barreira J. et al. First identification of natural infection of Rickettsia rickettsii in the Rhipicephalus sanguineus tick, in the State of Rio de Janeiro. P Vet Bras 2006; 29(2):105-108.

(12.) Rovery C, Raoult D. Rickettsia conorii Infections (Mediterranean Spotted Fever, Israeli Spotted Fever, Indian Tick Typhus, Astrakhan Fever). New York: Rickettsial Diseases. Informa HealthCare; 2007.

(13.) Unver A, Perez M, Orellana N, Huang, H, Rikihisa Y. Molecular and antigenic comparasion of Ehrlichia canis from dogs, ticks and human in Venezuela. J Clin Microbiol 2001; 39:2789-2793.

(14.) Bermudez S, Eremeeva M, Karpathy S, Samudio F, Zambrano M, Zaldivar Y et al. Detection and identification of Rickettsial Agents in ticks from domestic mammals in eastern Panama. J Med Entomol 2009; 46(4): 856-861.

(15.) Labruna M, Jorge R, Sana D, Jacomo A, Kashivakura C, Furtado M. et al. Ticks (Acari: Ixodidae) on wild carnivores in Brazil. Exp Appl Acarol 2005; 36:149-163.

(16.) Labruna, M. Ecology of Rickettsia on South America. Ann N Y Acad Sci 2009; 1166:156-166.

(17.) Rodaniche E. 1953. Natural infection of the tick, Amblyomma cajennense, with Rickettsia rickettsii in Panama. Am J Trop Hyg 1953; 2(4):696-699.

(18.) Smit F. A preliminary note the occurrence of Pulex irritans and P. simulans in North America. J Parasitol 1958; 523-526.

(19.) Badr V, Stefan P, Preisler J. Trichodectes canis (De Geer, 1778) (Phthiraptera, Ischnocera), a new ectoparasite of the raccoon dog (Nyctereutes procyonoides) in the Czech Republic. Eur J Wildlife Researches 2005; 51:133-135.

(20.) Colless D. Heterodoxus spiniger (Mallophaga: Boopidae) from cats in Singapore. J Parasitol 1959; 45:248.

(21.) Dantas-Torres F, Figueredo L. Heterodoxus spiniger (Enderlein, 1909) on domestic dogs (Canis familiaris, L. 1758) from the city of Recife, Pernambuco State, Brazil. Braz J Vet Res Ann Sci 2007; 44(2):77-80.

(22.) Thompson G. The distribution of Heterodoxus spiniger (Enderlein). Pap Proc Roy Soc Tasmania 1940; 27-31.

(23.) Emerson K, Price R. Evolution of Mallophaga on Mammals. In: Coevolution of Parasitic arthropods and mammals. New York: John Wiley & Son; 1985.

(24.) Bermudez S, Espinosa J, Cielo A, Clavel F, Subia J, Barrios S, Medianero E. Incidence of myiasis in Panama during the eradication of Cochliomyia hominivorax (Coquerel 1858) (Diptera: Calliphoridae). Mem Inst O Cruz 2007; 102(6):675-679.

Sergio Bermudez C, [1] * M.Sc, Roberto Miranda C, [1] M.Sc.

[1] Instituto Conmemorativo Gorgas de Estudios de la Salud, Ciudad de Panama, Panama, * Correspondencia: bermudezsec@gmail.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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Article Details
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Author:Bermudez C., Sergio; Miranda C., Roberto
Publication:Revista MVZ (Medicina Veterinaria y Zootecnia)
Article Type:Report
Date:Jan 1, 2011
Words:3581
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