Epidemiology of Batrachochytrium dendrobatidis in Chile and the role of the invasive African clawed frog (Xenopus laevis) as a vector
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2020
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en
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Universidad Andrés Bello
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La quitidiomicosis en anfibios, es una enfermedad causada por el hongo Batrachochytrium
dendrobatidis (Bd), se considera uno de los principales impulsores de la crisis mundial de disminución de anfibios. Un linaje panzoótico global de Bd (Bd-GPL), está asociado con
eventos de mortalidad masiva, extirpación de poblaciones locales y la extinción de
especies en múltiples continentes. Además, se ha descrito recientemente que la expansión
de este patógeno coincide con la expansión global del comercio de anfibios. En este
contexto, el comercio internacional de la rana Africana (Xenopus laevis) podría haber
contribuido a la propagación inicial de Bd en Chile. Este hongo infecta todos los órdenes
de anfibios y muchas de estas especies pueden desarrollar la enfermedad letal y la
disminución de la población En este contexto, al analizar la prevalencia y la diseminación
de Bd a escala regional, es posible identificar los factores de riesgo para la ocurrencia de
Bd. En esta disertación, propongo evaluar la epidemiología de Bd en Chile, incluida su
distribución, el papel de las especies invasoras y la variabilidad genética de Bd. Además,
proporciono resultados aplicables a otros procesos ecológicos que podrían ser relevantes
para la dinámica de la población de anfibios en general, y para la dinámica del huéspedBd en particular. Utilizamos qPCR para detectar la infección por Bd en anuros en el punto
de acceso a la biodiversidad de Chile y realizamos análisis de exploración espacial para
detectar patrones de distribución de Bd. Además, evaluamos si la prevalencia de Bd y la
carga de infección (ZE) que se distribuyeron entre familias de anfibios, regiones,
ecorregiones o historia de vida. Analizamos información de muestreos realizados durante
la última década (2008-2018) para identificar áreas de bajo y alto riesgo para Bd en Chile.
Los datos comprendieron 4,155 muestras específicas de Bd de 162 sitios del norte al sur
de Chile (18º a 51ºS). Batrachochytrium dendrobatidis también se cultivó de anfibios
silvestres y de cría en cautiverio en Chile, para describir la variabilidad genética de Bd.
Finalmente, exploramos los impactos de los anuros infectados con Bd (X.laevis y el sapito
de cuatro ojos; Pleurodema thaul), la cobertura del suelo y las condiciones climáticas en
la probabilidad de detección (p) y de ocupación (ψ) de dos anfibios nativos del centro de
Chile: Calyptocephalella gayi y P. thaul. Utilizamos datos empíricos de presencia/ausencia
en 23 sitios (cuerpos de agua) en el centro de Chile. Detectamos especies de anfibios en
19 de 23 sitios muestreados. En general, se encontró Bd en 24 de las 40 especies
estudiadas, y 97 de 162 sitios muestreados, con una prevalencia general estimada del
19.1%. Además, los resultados muestran áreas de riesgo significativos de Bd, con la
identificación de un grupo local situado en las áreas central y sur (es decir, ecorregiones
de bosques templados Valdiviano y matorral chileno); algunos grupos se superponen con a distribución de X. laevis. Además, encontramos que los factores de riesgo de que un
incremento en la altitud, temperatura media anual y precipitación anual, cobertura del
suelo, biomas antropogénicos y ecorregiones, se asociaron con una mayor prevalencia de
Bd. Además, se obtuvieron tres aislamientos: AVS7 de C. gayi de Valdivia, PA1 y PA2 de
C. gayi de Santiago. El grupo de aislados chilenos dentro del linaje Bd-GPL con sus
parientes más cercanos son genotipos provenientes del Reino Unido. Finalmente, X. laevis
fue la especie más común detectada en 14 de los sitios (60.8%), seguida de los anuros
nativos P. thaul en 12 (52.2%), C. gayi en 6 (26.1%). La infección con Bd se detectó en 13
de los 19 sitios que contienen anfibios con una prevalencia general de infección del 21,7%.
Calyptocephalella gayi exhibió la mayor prevalencia de Bd (28.5%), seguido de X. laevis
(25.2%) y P. thaul (17.9%). Además, C. gayi exhibió la mayor intensidad de infección
(16,785 ZE), seguido de P. thaul (975 ZE) y X. laevis (106 ZE). En el modelo de ocupación
de un-sitio, una-temporada y una-especie con mejor soporte, se observó que un aumento
de anuros positivos para Bd, la probabilidad de detección disminuye.Además, la
modificación antropogénica de la cubierta terrestre disminuye la probabilidad de detección
y ocupación de P. thaul. Además, encontramos el efecto opuesto del aumento de la
precipitación, en la que la probabilidad de ocupación de X. laevis disminuye mientras que
en C. gayi aumenta. En total, mis resultados proporcionan evidencia de que la infección
por Bd está ampliamente distribuida en Chile, infectando una gran cantidad de especies
de anfibios. Además, extiendo la distribución conocida de la infección por Bd y los aislados
de Bd-GPL en Chile y Sudamérica, y la introducción relativamente reciente de Bd-GPL en
el país, brindando apoyo adicional al papel de la actividad antropogénica en la propagación
de este linaje panzoótico global. Mis hallazgos también indican que la presencia de Bd y
la cubierta de tierra antropogénica, disminuye la probabilidad de detección y ocupación de
los anfibios nativos e introducidos en el centro de Chile. En total, mi disertación aporta
información importante para el desarrollo de estrategias de conservación de anfibios y
mitigación de Bd en Chile.
Amphibian chytridiomycosis, a disease caused by the fungus Batrachochytrium dendrobatidis (Bd), is considered to be one of the main drivers behind the world’s amphibian decline crisis. A global panzootic lineage of Bd (Bd-GPL) is associated with mass mortality events, the extirpation of local populations and the extinction of species on multiple continents. Also, it has been recently described that the expansion of this pathogen coincides with the global expansion of amphibian trade. In this context, the international trade of the invasive African clawed frog (Xenopus laevis) might have contributed to the initial spread of Bd in Chile. This fungus infects all amphibian orders which many species may develop lethal disease and population declines. In this context, by analysing Bd prevalence and spread at the regional scale, it is possible to identify risk factors for Bd occurrence. In this dissertation, In this study, I propose to assess the epidemiology of Bd in Chile, including its distribution, the role of invasive amphibian species and the genetic variability of Bd. Additionally, I provide findings applicable to other ecological processes that might be relevant to amphibian population dynamics in general, and for host-Bd dynamics in particular. We used qPCR to detect Bd infection in anurans across the Chilean biodiversity hotspot and we performed spatial scan analyses to detect patterns of Bd distribution. Also, we evaluated whether Bd prevalence and infection load (ZE) were randomly distributed across amphibian families, regions, ecoregions or life history. We analysed information from surveys that have been carried out during the last decade (2008- 2018) to identify low and high-risk areas for Bd in Chile. Data comprised 4,155 Bd-specific assays from 162 study sites from north to south Chile (18º to 51º S). Batrachochytrium dendrobatidis was also cultured from wild and farmed amphibians in Chile to describe genetic variability of Bd. Finally, we explored the impacts of anurans Bd prevalence (the invasive X. laevis and the native four-eyed frogs; Pleurodema thaul), land cover and climatic conditions on the detection (p) and occupancy (ψ) probability of two native amphibians of central Chile: Calyptocephalella gayi and P. thaul. We used empirical presence/absence data across 23 sites (water bodies) in central Chile. We detected amphibian species across 19 of 23 surveyed sites. Overall, Bd was found in 24 of 40 studied species, and 97 of 162 sampled sites, with an estimated overall prevalence of 19.1%. Also, results show significant clustering of Bd, with the identification of a local clusters situated in the central and south areas (i.e. Chilean Matorral and Valdivian Temperate Forest ecoregions); some clusters overlapped with the distribution of invasive X. laevis. Moreover, we found that risk factors that an increasing altitude, annual mean temperature and annual precipitation, landcover index, anthropogenic biomes and ecoregions, were associated with a higher prevalence of Bd. Also, three isolates were obtained: AVS7 from C. gayi from Valdivia, PA1 and PA2 from C. gayi from Santiago. Chilean isolates group within the Bd-GPL lineage with their closest relatives being genotypes in the United Kingdom. Finally, X. laevis was the most common species detected in 14 of the sites (60.8%), followed by the native anurans P. thaul in 12 (52.2%), C. gayi in 6 (26.1%). Infection with Bd was detected in 13 of the 19 sites containing amphibians at an overall infection prevalence of 21.7%. Calyptocephalella gayi exhibited the highest Bd prevalence (28.5%), followed by X. laevis (25.2%) and P. thaul (17.9%). Also, C. gayi exhibited the highest infection intensity (16,785 ZE), followed by P. thaul (975 ZE) and X. laevis (106 ZE). In the best supported single-season, single-species siteoccupancy model we observed that an increase of anurans Bd prevalence, detection proability decreases. Also, anthropogenic land cover modification decreases the detection and occupancy probability of P. thaul. In addition, we find the opposite effect of the increase in precipitation, in which the occupancy probability of X. laevis decreases while in C. gayi increases. Altogether, my results provide evidence that Bd infection it is widely distributed in Chile infecting a large number of amphibian species. Additionally, I extend the known distribution of Bd-infection and Bd-GPL isolates in Chile and South America, and relatively recent introduction of Bd-GPL into the country, providing additional support to the role of anthropogenic activity in the global spread of this panzootic lineage. My findings also indicate that the presence of Bd and anthropogenic land cover, decreases the detection and occupancy probability of native and introduced amphibians in central Chile. All together, my dissertation contributes important information for the development of amphibian conservation and Bd mitigation strategies in Chile.
Amphibian chytridiomycosis, a disease caused by the fungus Batrachochytrium dendrobatidis (Bd), is considered to be one of the main drivers behind the world’s amphibian decline crisis. A global panzootic lineage of Bd (Bd-GPL) is associated with mass mortality events, the extirpation of local populations and the extinction of species on multiple continents. Also, it has been recently described that the expansion of this pathogen coincides with the global expansion of amphibian trade. In this context, the international trade of the invasive African clawed frog (Xenopus laevis) might have contributed to the initial spread of Bd in Chile. This fungus infects all amphibian orders which many species may develop lethal disease and population declines. In this context, by analysing Bd prevalence and spread at the regional scale, it is possible to identify risk factors for Bd occurrence. In this dissertation, In this study, I propose to assess the epidemiology of Bd in Chile, including its distribution, the role of invasive amphibian species and the genetic variability of Bd. Additionally, I provide findings applicable to other ecological processes that might be relevant to amphibian population dynamics in general, and for host-Bd dynamics in particular. We used qPCR to detect Bd infection in anurans across the Chilean biodiversity hotspot and we performed spatial scan analyses to detect patterns of Bd distribution. Also, we evaluated whether Bd prevalence and infection load (ZE) were randomly distributed across amphibian families, regions, ecoregions or life history. We analysed information from surveys that have been carried out during the last decade (2008- 2018) to identify low and high-risk areas for Bd in Chile. Data comprised 4,155 Bd-specific assays from 162 study sites from north to south Chile (18º to 51º S). Batrachochytrium dendrobatidis was also cultured from wild and farmed amphibians in Chile to describe genetic variability of Bd. Finally, we explored the impacts of anurans Bd prevalence (the invasive X. laevis and the native four-eyed frogs; Pleurodema thaul), land cover and climatic conditions on the detection (p) and occupancy (ψ) probability of two native amphibians of central Chile: Calyptocephalella gayi and P. thaul. We used empirical presence/absence data across 23 sites (water bodies) in central Chile. We detected amphibian species across 19 of 23 surveyed sites. Overall, Bd was found in 24 of 40 studied species, and 97 of 162 sampled sites, with an estimated overall prevalence of 19.1%. Also, results show significant clustering of Bd, with the identification of a local clusters situated in the central and south areas (i.e. Chilean Matorral and Valdivian Temperate Forest ecoregions); some clusters overlapped with the distribution of invasive X. laevis. Moreover, we found that risk factors that an increasing altitude, annual mean temperature and annual precipitation, landcover index, anthropogenic biomes and ecoregions, were associated with a higher prevalence of Bd. Also, three isolates were obtained: AVS7 from C. gayi from Valdivia, PA1 and PA2 from C. gayi from Santiago. Chilean isolates group within the Bd-GPL lineage with their closest relatives being genotypes in the United Kingdom. Finally, X. laevis was the most common species detected in 14 of the sites (60.8%), followed by the native anurans P. thaul in 12 (52.2%), C. gayi in 6 (26.1%). Infection with Bd was detected in 13 of the 19 sites containing amphibians at an overall infection prevalence of 21.7%. Calyptocephalella gayi exhibited the highest Bd prevalence (28.5%), followed by X. laevis (25.2%) and P. thaul (17.9%). Also, C. gayi exhibited the highest infection intensity (16,785 ZE), followed by P. thaul (975 ZE) and X. laevis (106 ZE). In the best supported single-season, single-species siteoccupancy model we observed that an increase of anurans Bd prevalence, detection proability decreases. Also, anthropogenic land cover modification decreases the detection and occupancy probability of P. thaul. In addition, we find the opposite effect of the increase in precipitation, in which the occupancy probability of X. laevis decreases while in C. gayi increases. Altogether, my results provide evidence that Bd infection it is widely distributed in Chile infecting a large number of amphibian species. Additionally, I extend the known distribution of Bd-infection and Bd-GPL isolates in Chile and South America, and relatively recent introduction of Bd-GPL into the country, providing additional support to the role of anthropogenic activity in the global spread of this panzootic lineage. My findings also indicate that the presence of Bd and anthropogenic land cover, decreases the detection and occupancy probability of native and introduced amphibians in central Chile. All together, my dissertation contributes important information for the development of amphibian conservation and Bd mitigation strategies in Chile.
Notas
Tesis (Doctor en Medicina de la Conservación)
Palabras clave
Quitridiomicosis, Xenopus Laevis, Enfermedades, Anfibios, Chile