Evaluating inter-specific transmission of ticks, fleas and canine vector-borne pathogens between dogs and foxes in a human-dominated landscape
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2019
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en_US
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Universidad Andrés Bello
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Los patógenos pueden circular entre hospedadores domésticos y ocasionalmente cruzar la barrera de especie e infectar animales silvestres. Los patógenos generalistas pueden mantenerse dentro de las poblaciones de animales abundantes (animales domésticos) y infectar a una población menos abundante (animales silvestres). La antropización del paisaje puede además aumentar las oportunidades de contacto entre los animales domésticos y silvestres, lo que puede dar lugar a una redistribución de agentes infecciosos. El perro doméstico (Canis familiaris) es a menudo considerado un reservorio de enfermedades para otros carnívoros silvestres y la Región Metropolitana de Santiago se considera una de las regiones con mayor abundancia de perros sin confinamiento en Chile. El zorro culpeo (Lycalopex culpaeus), en cambio, es considerado un carnívoro con hábitos solitarios y bajas densidades poblacionales.
Los carnívoros silvestres albergan varias especies de parásitos artrópodos, la mayoría de los cuales se comparten con carnívoros domésticos. Esos ectoparásitos transmiten varios patógenos caninos transmitidos por vectores (CVBP), para los cuales el perro es un reservorio competente. La presencia de esos patógenos en Chile ha sido muy poco estudiada, y los reportes en carnívoros silvestres son casi inexistentes. Los parásitos mantenidos dentro de una población hospedadora abundante (en este caso, perros rurales) podrían eventualmente transmitir el parásito a una población menos abundante (los zorros culpeos). Por todo esto, el objetivo general de esta tesis es determinar si los perros rurales y los zorros silvestres comparten ectoparásitos y CVBP. En el Capítulo I se comparó la prevalencia observada y la abundancia de ectoparásitos (garrapatas y pulgas) y se caracterizó la relación filogenética de estos artrópodos entre las dos especies hospedadoras. Los resultados mostraron que varias especies de ectoparásitos tiene preferencia por uno de los hospedadores: Rhipicephalus sanguineus y Ctenocephalides spp. fueron más abundantes en perros y Amblyomma tigrinum y Pulex irritans lo fueron en zorros. El análisis genético mostró que, si bien no era frecuente, perros y zorros compartían
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algunos haplotipos de estos parásitos. Por tanto, los perros estarían actuando como una población de mantenimiento y que ocasionalmente se dé lugar a transmisiones interespecíficas de algunos ectoparásitos de perros a zorros, mientras que los zorros parecen ser hospedadores naturales de A. tigrinum y P. irritans. La misma aproximación se usó en el Capítulo II para evaluar los CVBP: Anaplasmataceae, hemoplasmas, Bartonella, Hepatozoon y piroplásmidos. Anaplasma platys y Candidatus Mycoplasma haematoparvum están ampliamente distribuidos en perros rurales y esporádicamente se transmitiría interespecíficas a los zorros. En contraste, dos especies de Hepatozoon spp. parecen ser enzoóticas en la población estudiada de zorros y no se encontraron en perros. Esto sigue los patrones de infestación de su vector sospechosos: R. sanguineus y A. tigrinum, respectivamente. Por último, la mayoría de los haplotipos de Mycoplasma haemocanis, bacteria frecuente tanto en perros como en zorros, parece mantenerse independientemente en las poblaciones de perros y zorros por transmisión intraespecífica, pero ocasionalmente estaría ocurriendo una transmisión interespecífica.
Para comprender cómo afecta la presión de los perros rurales en la dinámica de transmisión de esos patógenos en los zorros, en el Capítulo III se estudió cómo el tipo de transmisión de patógenos afecta a las asociaciones entre la probabilidad de ocurrencia de patógenos caninos en zorros y su contacto potencial con perros. Además de los ectoparásitos y los CVBP mencionados anteriormente, se evaluaron otros patógenos de transmisión indirecta (parvovirus canino; CPV) y con parásitos de transmisión directa (Sarcoptes scabiei, causante de sarna sarcóptica). El contacto potencial con perros se evaluó utilizando los siguientes indicadores de antropización: i) análisis espacial usando los tejados como indicador de presencia humana; ii) composición de la dieta mediante análisis de isótopos estables; y iii) análisis cuantitativo de la presencia de genes de resistencia frente a antibióticos. La falta de asociación de R. sanguineus, C. felis y M. haemocanis con los indicadores de antropización indica que la proximidad entre zorros y perros parece no ser necesaria para la transmisión potencial y que los perros en libertad podrían estar propagando esos artrópodos en el medio natural. La antropización del paisaje está asociado a la infestación por S. scabiei y exposición al CPV. En otros casos, la asociación entre la exposición al parásito y diferentes indicadores de la antropización
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del paisaje no concordó con lo esperado: Hepatozoon, A. tigrinum y P. irritans que serían enzoóticos en los zorros de acuerdo a lo hallado en los Capítulos I y II, se relacionaron positivamente con algunos representantes de antropización y negativamente con otros. Por lo tanto, las interpretaciones de estos indicadores deben hacerse con cuidado.
Al integrar todos los resultados, puedo concluir que, en términos generales, hay una transmisión limitada de pulgas, garrapatas y CVBP entre los perros rurales y zorros silvestres que viven en simpatría en la zona central de Chile.
Pathogens can circulate among domestic hosts, and occasionally cross the species barrier and infect wildlife. Generalist pathogens can be maintained within populations of abundant animals (i.e. domestic animals) and spillover to less abundant host population (i.e. wild animals). Alterations in landscape characteristic can increasing the opportunities for contact among domestic animals and wildlife, resulting in a redistribution of infective agents. The domestic dog (Canis familiaris) is often considered a reservoir of diseases for other wild carnivores and the Metropolitan Region of Santiago is considered a hotspot of free-ranging dog abundance in Chile. In contrast, the Andean fox (Lycalopex culpaeus) is considered a carnivore with solitary habits and low population densities. Wild carnivores harbor several arthropod parasitic species, most of which are shared with domestic dogs and cats. Those ectoparasites are able to transmit several canine vector-borne pathogens (CVBP) for which dogs are competent reservoir hosts. The presence of those pathogen in Chile has been very poorly studied, and reports in wildlife are almost nonexistent. Parasites maintained within abundant host (in this case, rural dogs) could eventually spillover to less abundant host (Andean foxes). In consequence the general objective of this thesis is to determine whether sympatric free-ranging dogs and wild foxes share ectoparasites and CVBP. In the first Chapter I, the prevalence and abundance of ectoparasites (ticks and fleas) were compared and phylogenetic relationship were characterized between two host species. The results showed that each ectoparasite species have a host preference: Rhipicephalus sanguineus and Ctenocephalides spp. were more abundant in dogs and Amblyomma tigrinum and Pulex irritans were more abundant in foxes. Genetic analysis showed that dogs and foxes shared a limited number of haplotypes, suggesting that dogs are acting as maintenance host population and occasional spillovers of those ectoparasites occur from dogs to foxes. In contrast, foxes appear to be natural hosts for A. tigrinum and P. irritans. A similar approach was used in the Chapter II to evaluate the some selected CVBP (Anaplasmataceae, 5 hemoplasmas, Bartonella, Hepatozoon and piroplasmids) Anaplasma platys and Candidatus Mycoplasma haematoparvum were prevalent in rural dogs, with only occasional spillover seem to be occurring to Andean foxes. In contrast, two Hepatozoon spp. seem to be enzootic in the studied Andean fox population, and no positive dogs were found. This follows the infestation patterns of their suspected vectors: R. sanguineus and A. tigrinum, respectively. Mycoplasma haemocanis was prevalent in both host species, and most haplotypes are independently maintained separately in dog and fox populations predominantly by intraspecific transmission, but sporadic interspecific transmission seems to occur. To understand how the pressure of free-ranging dogs affects the transmission dynamics of those pathogens to foxes, in the Chapter III, I to analyzed how the type of pathogen transmission affects the associations between the occurrence probability of canine pathogens in foxes and their potential contact with dogs. In addition to ectoparasites and CVBP, I also evaluated another indirectly transmitted pathogen (Canine Parvovirus; CPV) and a directly transmitted parasite (Sarcoptes scabiei, causal agent of Sarcoptic mange). Potential contact with dogs was evaluated using the following anthropization proxies: i) spatial analysis using roofs as proxy of human presence; ii) diet composition through stable isotope analysis; and iii) quantitative analysis of the presence of antimicrobial resistance genes. The lack of association of R. sanguineus, C. felis and M. haemocanis with anthropization proxies indicates that proximity between foxes and dogs seem not to be necessary for transmission, and that free-ranging dogs may be spreading those arthropods in the natural environment. As expected, landscape anthropization was associated with exposure to S. scabiei and CPV. The association of parasite exposure with different proxies of landscape anthropization in some cases were not according to the predictions: Hepatozoon, A. tigrinum and P. irritans, that according to Chapter I and II seem to be enzootic in foxes, were positively related to some anthropization proxies and negatively with others. Therefore, interpretations of these indicators should be done carefully. Integrating all the results, I can conclude that, in general terms, a limited transmission of fleas, ticks and CVBP between free-ranging rural dogs and sympatric wild foxes is taking place.
Pathogens can circulate among domestic hosts, and occasionally cross the species barrier and infect wildlife. Generalist pathogens can be maintained within populations of abundant animals (i.e. domestic animals) and spillover to less abundant host population (i.e. wild animals). Alterations in landscape characteristic can increasing the opportunities for contact among domestic animals and wildlife, resulting in a redistribution of infective agents. The domestic dog (Canis familiaris) is often considered a reservoir of diseases for other wild carnivores and the Metropolitan Region of Santiago is considered a hotspot of free-ranging dog abundance in Chile. In contrast, the Andean fox (Lycalopex culpaeus) is considered a carnivore with solitary habits and low population densities. Wild carnivores harbor several arthropod parasitic species, most of which are shared with domestic dogs and cats. Those ectoparasites are able to transmit several canine vector-borne pathogens (CVBP) for which dogs are competent reservoir hosts. The presence of those pathogen in Chile has been very poorly studied, and reports in wildlife are almost nonexistent. Parasites maintained within abundant host (in this case, rural dogs) could eventually spillover to less abundant host (Andean foxes). In consequence the general objective of this thesis is to determine whether sympatric free-ranging dogs and wild foxes share ectoparasites and CVBP. In the first Chapter I, the prevalence and abundance of ectoparasites (ticks and fleas) were compared and phylogenetic relationship were characterized between two host species. The results showed that each ectoparasite species have a host preference: Rhipicephalus sanguineus and Ctenocephalides spp. were more abundant in dogs and Amblyomma tigrinum and Pulex irritans were more abundant in foxes. Genetic analysis showed that dogs and foxes shared a limited number of haplotypes, suggesting that dogs are acting as maintenance host population and occasional spillovers of those ectoparasites occur from dogs to foxes. In contrast, foxes appear to be natural hosts for A. tigrinum and P. irritans. A similar approach was used in the Chapter II to evaluate the some selected CVBP (Anaplasmataceae, 5 hemoplasmas, Bartonella, Hepatozoon and piroplasmids) Anaplasma platys and Candidatus Mycoplasma haematoparvum were prevalent in rural dogs, with only occasional spillover seem to be occurring to Andean foxes. In contrast, two Hepatozoon spp. seem to be enzootic in the studied Andean fox population, and no positive dogs were found. This follows the infestation patterns of their suspected vectors: R. sanguineus and A. tigrinum, respectively. Mycoplasma haemocanis was prevalent in both host species, and most haplotypes are independently maintained separately in dog and fox populations predominantly by intraspecific transmission, but sporadic interspecific transmission seems to occur. To understand how the pressure of free-ranging dogs affects the transmission dynamics of those pathogens to foxes, in the Chapter III, I to analyzed how the type of pathogen transmission affects the associations between the occurrence probability of canine pathogens in foxes and their potential contact with dogs. In addition to ectoparasites and CVBP, I also evaluated another indirectly transmitted pathogen (Canine Parvovirus; CPV) and a directly transmitted parasite (Sarcoptes scabiei, causal agent of Sarcoptic mange). Potential contact with dogs was evaluated using the following anthropization proxies: i) spatial analysis using roofs as proxy of human presence; ii) diet composition through stable isotope analysis; and iii) quantitative analysis of the presence of antimicrobial resistance genes. The lack of association of R. sanguineus, C. felis and M. haemocanis with anthropization proxies indicates that proximity between foxes and dogs seem not to be necessary for transmission, and that free-ranging dogs may be spreading those arthropods in the natural environment. As expected, landscape anthropization was associated with exposure to S. scabiei and CPV. The association of parasite exposure with different proxies of landscape anthropization in some cases were not according to the predictions: Hepatozoon, A. tigrinum and P. irritans, that according to Chapter I and II seem to be enzootic in foxes, were positively related to some anthropization proxies and negatively with others. Therefore, interpretations of these indicators should be done carefully. Integrating all the results, I can conclude that, in general terms, a limited transmission of fleas, ticks and CVBP between free-ranging rural dogs and sympatric wild foxes is taking place.
Notas
Tesis (Doctor en Medicina de la Conservación)
Palabras clave
Animales Domésticos, Zorros, Parásitos, Artrópodos Vectores, Investigaciones