Quince años de seguimiento de las poblaciones de anfibios del macizo de Peñalara (Parque Nacional de la Sierra de Guadarrama, Madrid)

Fecha de aceptación: 14 de enero de 2015Peer reviewe

Infection and transmission heterogeneity of a multi-host pathogen (Batrachochytrium dendrobatidis) within an amphibian community

The majority of parasites infect multiple hosts. As the outcome of the infection is different in each of them, most studies of wildlife disease focus on the few species that suffer the most severe consequences. However, the role that each host plays in the persistence and transmission of infection can be crucial to understanding the spread of a parasite and the risk it poses to the community. Current theory predicts that certain host species can modulate the infection in other species by amplifying or diluting both infection prevalence and infection intensity, both of which have implications for disease risk within those communities. The fungus Batrachochytrium dendrobatidis (Bd), the causal agent of the disease chytridiomycosis, has caused global amphibian population declines and extinctions. However, not all infected species are affected equally, and thus Bd is a good example of a multi-host pathogen that must ultimately be studied with a community approach. To test whether the common midwife toad Alytes obstetricans is a reservoir and possible amplifier of infection of other species, we used experimental approaches in captive and wild populations to determine the effect of common midwife toad larvae on infection of other amphibian species found in the Peñalara Massif, Spain. We observed that the most widely and heavily infected species, the common midwife toad, may be amplifying the infection loads in other species, all of which have different degrees of susceptibility to Bd infection. Our results have important implications for performing mitigation actions focused on potential ‘amplifier’ hosts and for better understanding the mechanisms of Bd transmission.Peer reviewe

Short term minimum water temperatures determine levels of infection by the amphibian chytrid fungus in Alytes obstetricans tadpoles

Received: September 11, 2014; Accepted: February 4, 2015; Published: March 20, 2015Amphibians are one of the groups of wildlife most seriously threatened by emerging infectious disease. In particular, chytridiomycosis, caused by the aquatic fungus Batrachochytrium dendrobatidis, is responsible for amphibian species declines on a worldwide scale. Population-level outcomes following the introduction of the pathogen are context dependent and mediated by a large suite of abiotic and biotic variables. In particular, studies have shown that temperature has a key role in determining infection dynamics owing to the ectothermic nature of the amphibian host and temperature-dependency of pathogen growth rates. To assess the temperature-dependent seasonality of infectious burdens in a susceptible host species, we monitored lowland populations of larval midwife toads, Alytes obstetricians, in Central Spain throughout the year. We found that infections were highly seasonal, and inversely correlated against water temperature, with the highest burdens of infection seen during the colder months. Short-term impacts of water-temperature were found, with the minimum temperatures occurring before sampling being more highly predictive of infectious burdens than were longer-term spans of temperature. Our results will be useful for selecting the optimal time for disease surveys and, more broadly, for determining the key periods to undertake disease mitigation.The study was funded by Fundación General CSIC and Banco Santander.Peer reviewe

Joint effects of habitat, zooplankton, host stage structure and diversity on amphibian chytrid

Received: 13 April 2016, Accepted: 5 July 2016Why does the severity of parasite infection differ dramatically across habitats? This question remains challenging to answer because multiple correlated pathways drive disease. Here, we examined habitat–disease links through direct effects on parasites and indirect effects on parasite predators (zooplankton), host diversity and key life stages of hosts. We used a case study of amphibian hosts and the chytrid fungus, Batrachochytrium dendrobatidis, in a set of permanent and ephemeral alpine ponds. A field experiment showed that ultraviolet radiation (UVR) killed the free-living infectious stage of the parasite. Yet, permanent ponds with more UVR exposure had higher infection prevalence. Two habitat-related indirect effects worked together to counteract parasite losses from UVR: (i) UVR reduced the density of parasite predators and (ii) permanent sites fostered multi-season host larvae that fuelled parasite production. Host diversity was unlinked to hydroperiod or UVR but counteracted parasite gains; sites with higher diversity of host species had lower prevalence of infection. Thus, while habitat structure explained considerable variation in infection prevalence through two indirect pathways, it could not account for everything. This study demonstrates the importance of creating mechanistic, food web-based links between multiple habitat dimensions and disease.Peer reviewe

Re-introduction program for the common midwife toad and Iberian frog in the Natural Park of Peñalara in Madrid, Spain: can we defeat chytridiomycosis and trout introductions?

Peer Reviewe

Early exposure to Batrachochytrium dendrobatidis causes profound immunosuppression in amphibians

Fungal pathogens have evolved a broad suite of strategies aiming at evading the host immune response. Amphibians are globally infected by the panzootic chytrid fungus Batrachochytrium dendrobatidis (Bd) and, while robust innate immune defences have been characterised, there is little evidence for the existence of effective adaptive immunity. We determine the immune response of the common midwife toad following challenge by Bd as larvae. Immune function was described for both the cell-mediated and antibody-mediated immune responses following infectious challenge as larval amphibians. While there were no significant differences in the ratio of neutrophils/lymphocytes between infected and uninfected individuals, early exposure of tadpoles to Bd significantly dampened the levels of circulating immunoglobulins (IgM and IgY) in the serum of juveniles after metamorphosis. Our results show that Bd immunosuppresses amphibians when infection occurs as larvae with potentially broad effects on the remodelling of immunity during metamorphosis.AFL was funded by Fundación General CSIC and Banco Santander. MCF was funded by the Leverhulme Trust RPG 2014 273.Peer Reviewe

Long-term monitoring of an amphibian community after a climate change- and infectious disease-driven species extirpation

Infectious disease and climate change are considered major threats to biodiversity and act as drivers behind the global amphibian decline. This is, to a large extent, based on short-term studies that are designed to detect the immediate and strongest biodiversity responses to a threatening process. What few long-term studies are available, although typically focused on single species, report outcomes that often diverge significantly from the short-term species responses. Here, we report the results of an 18-year survey of an amphibian community exposed to both climate warming and the emergence of lethal chytridiomycosis. Our study shows that the impacts of infectious disease are ongoing but restricted to two out of nine species that form the community, despite the fact all species can become infected with the fungus. Climate warming appears to be affecting four out of the nine species, but the response of three of these is an increase in abundance. Our study supports a decreasing role of infectious disease on the community, and an increasing and currently positive effect of climate warming. We caution that if the warming trends continue, the net positive effect will turn negative as amphibian breeding habitat becomes unavailable as water bodies dry, a pattern that already may be underway.Peer Reviewe

Demography of common toads after local extirpation of co-occurring midwife toads

© Copyright 2014 by Koninklijke Brill NV, Leiden, The Netherlands. Estimating demographic parameters like survival or recruitment provides insight into the state and trajectory of populations, but understanding the contexts influencing those parameters, including both biotic and abiotic factors, is particularly important for management and conservation. At a high elevation national park in Central Spain, common toads (Bufo bufo) are apparently taking advantage of the near-extirpation of the midwife toad (Alytes obstetricans), as colonization into new breeding ponds is evident.Within this scenario, we expected demographic parameters of common toad populations to be affected favorably by the putative release from competition. However, we found the population growth rate was negative in 4 of 5 years at the long-standing population; survival probability at the long-standing population and newly-colonised breeding ponds was lower than reported for other toads living at high elevations and the probability of recruitment was inadequate to compensate for the survival rate in maintaining a positive trajectory for either of the breeding ponds. We assessed weather covariates and disease for their contribution to the context thatmay be limiting the common toad's successful use of the niche vacated by the midwife toad.Peer Reviewe

Ambient ultraviolet B radiation and prevalence of infection by Batrachochytrium dendrobatidis in two amphibian species

[EN]: Chytridiomycosis, the emerging disease caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd) is responsible for declines and extirpations of amphibian populations worldwide. Environmental covariates modify the host-Bd interaction and thus affect the ongoing spread of the pathogen. One such covariate may be the intensity of ultraviolet B (UV-B) radiation. In a field experiment conducted in Laguna Grande de Peñalara (central Spain), a mountainous region where the presence of Bd has been documented since 1997, we analyzed the potential effect of environmental UV-B (daily maximum 2.5-3.9 W/m2) on the susceptibility of larvae of the common toad (Bufo bufo) to Bd. The proportion of infected individuals increased as tadpoles developed. The prevalence of Bd was significantly lower in tadpoles exposed to environmental UV-B intensities (2.94%) than in tadpoles not exposed to the radiation (9.72%). This finding mirrors that seen for a second amphibian species, the European midwife toad (Alytes obstetricans), for which conditional prevalence (i.e., prevalence of infection conditioned on the probability of a site being infected) across the Iberian Peninsula was inversely correlated with the intensity of UV-B.[ES]: La quitridiomicosis, la enfermedad emergente provocada por el hongo quitridio Batrachochytrium dendrobatidis (Bd), es responsable de las declinaciones y extirpaciones de poblaciones de anfibios en todo el mundo. Las covariables ambientales modifican la interacción huésped–Bd y por lo tanto afectan a la dispersión del patógeno. La intensidad de la radiación ultravioleta B (UV-B) puede ser una de tales covariables. En un experimento de campo llevado a cabo en Laguna Grande de Peñalara (España central), una región montañosa donde se ha documentado la presencia de Bd desde 1997, analizamos el efecto potencial de la radiación UV-B ambiental (máximo diario 2.5–3.9 W·m−2) sobre la susceptibilidad de larvas de Bufo bufo a Bd. La proporción de individuos infectados incrementó a medida que se desarrollaron los renacuajos. La prevalencia de Bd fue significativamente menor en los renacuajos expuestos a intensidades ambientales de UV-B (2.94%) que en renacuajos no expuestos a la radiación (9.72%). Estos hallazgos son semejantes a los encontrados en una segunda especie de anfibio, Alytes obstetricans, en la que la prevalencia condicional (i. e., prevalencia de la enfermedad condicionada a la probabilidad de que un sitio esté infectado) en la Península Ibérica se correlacionó inversamente con la intensidad de UV-B.This research was funded by Ministerio de Ciencia e Innovación of Spain (projects EU12008-03637 and 200630I115 CSIC (J.B.).Peer Reviewe