Pathogenesis is strongly dependent on microbial context, but development of probiotic therapies has neglected the impact of ecological interactions. Dynamics among microbial communities, host immune ...responses, and environmental conditions may alter the effect of probiotics in human and veterinary medicine, agriculture and aquaculture, and the proposed treatment of emerging wildlife and zoonotic diseases such as those occurring on amphibians or vectored by mosquitoes. Here we use a holistic measure of amphibian mucosal defenses to test the effects of probiotic treatments and to assess disease risk under different ecological contexts. We developed a non-invasive assay for antifungal function of the skin mucosal ecosystem (mucosome function) integrating host immune factors and the microbial community as an alternative to pathogen exposure experiments. From approximately 8500 amphibians sampled across Europe, we compared field infection prevalence with mucosome function against the emerging fungal pathogen Batrachochytrium dendrobatidis. Four species were tested with laboratory exposure experiments, and a highly susceptible species, Alytes obstetricans, was treated with a variety of temperature and microbial conditions to test the effects of probiotic therapies and environmental conditions on mucosome function. We found that antifungal function of the amphibian skin mucosome predicts the prevalence of infection with the fungal pathogen in natural populations, and is linked to survival in laboratory exposure experiments. When altered by probiotic therapy, the mucosome increased antifungal capacity, while previous exposure to the pathogen was suppressive. In culture, antifungal properties of probiotics depended strongly on immunological and environmental context including temperature, competition, and pathogen presence. Functional changes in microbiota with shifts in temperature provide an alternative mechanistic explanation for patterns of disease susceptibility related to climate beyond direct impact on host or pathogen. This nonlethal management tool can be used to optimize and quickly assess the relative benefits of probiotic therapies under different climatic, microbial, or host conditions.
Rare and threatened species are the most frequent focus of conservation science and action. With the ongoing shift from single-species conservation towards the preservation of ecosystem services, ...there is a greater need to understand abundance trends of common species because declines in common species can disproportionately impact ecosystems function. We used volunteer-collected data in two European countries, the United Kingdom (UK) and Switzerland, since the 1970s to assess national and regional trends for one of Europe's most abundant amphibian species, the common toad (Bufo bufo). Millions of toads were moved by volunteers across roads during this period in an effort to protect them from road traffic. For Switzerland, we additionally estimated trends for the common frog (Rana temporaria), a similarly widespread and common amphibian species. We used state-space models to account for variability in detection and effort and included only populations with at least 5 years of data; 153 populations for the UK and 141 for Switzerland. Common toads declined continuously in each decade in both countries since the 1980s. Given the declines, this common species almost qualifies for International Union for the Conservation of Nature (IUCN) red-listing over this period despite volunteer conservation efforts. Reasons for the declines and wider impacts remain unknown. By contrast, common frog populations were stable or increasing in Switzerland, although there was evidence of declines after 2003. "Toads on Roads" schemes are vital citizen conservation action projects, and the data from such projects can be used for large scale trend estimations of widespread amphibians. We highlight the need for increased research into the status of common amphibian species in addition to conservation efforts focusing on rare and threatened species.
In surveillance of subterranean fauna, especially in the case of rare or elusive aquatic species, traditional techniques used for epigean species are often not feasible. We developed a non-invasive ...survey method based on environmental DNA (eDNA) to detect the presence of the red-listed cave-dwelling amphibian, Proteus anguinus, in the caves of the Dinaric Karst. We tested the method in fifteen caves in Croatia, from which the species was previously recorded or expected to occur. We successfully confirmed the presence of P. anguinus from ten caves and detected the species for the first time in five others. Using a hierarchical occupancy model we compared the availability and detection probability of eDNA of two water sampling methods, filtration and precipitation. The statistical analysis showed that both availability and detection probability depended on the method and estimates for both probabilities were higher using filter samples than for precipitation samples. Combining reliable field and laboratory methods with robust statistical modeling will give the best estimates of species occurrence.
Chytridiomycosis is a fungal disease linked to local and global extinctions of amphibians. Susceptibility to chytridiomycosis varies greatly between amphibian species, but little is known about ...between- and within-population variability. However, this kind of variability is the basis for the evolution of tolerance and resistance evolution to disease.
In a common garden experiment, we measured mortality after metamorphosis of Alytes obstetricans naturally infected with Batrachochytrium dendrobatidis. Mortality rates differed significantly among populations and ranged from 27 to 90%. Within populations, mortality strongly depended on mass at and time through metamorphosis.
Although we cannot rule out that the differences observed resulted from differences in skin microbiota, different pathogen strains or environmental effects experienced by the host or the pathogen prior to the start of the experiment, we argue that genetic differences between populations are a likely source of at least part of this variation. To our knowledge, this is the first study showing differences in survival between and within populations under constant laboratory conditions. Assuming that some of this intraspecific variation has a genetic basis, this may suggest that there is the potential for the evolution of resistance or tolerance, which might allow population persistence.
Emerging wildlife diseases are taking a heavy toll on animal and plant species worldwide. Mitigation, particularly in the initial epidemic phase, is hindered by uncertainty about the epidemiology and ...management of emerging diseases, but also by vague or poorly defined objectives. Here, we use a quantitative analysis to assess how the decision context of mitigation objectives, available strategies and practical constraints influences the decision of whether and how to respond to epidemics in wildlife. To illustrate our approach, we parametrized the model for European fire salamanders affected by
, and explored different combinations of conservation, containment and budgetary objectives. We found that in approximately half of those scenarios, host removal strategies perform equal to or worse than no management at all during a local outbreak, particularly where removal cannot exclusively target infected individuals. Moreover, the window for intervention shrinks rapidly if an outbreak is detected late or if a response is delayed. Clearly defining the decision context is, therefore, vital to plan meaningful responses to novel outbreaks. Explicitly stating objectives, strategies and constraints, if possible before an outbreak occurs, avoids wasting precious resources and creating false expectations about what can and cannot be achieved during the epidemic phase.
ABSTRACT
Mountain areas are biodiversity hotspots and provide a multitude of ecosystem services of irreplaceable socio‐economic value. In the European Alps, air temperature has increased at a rate of ...about 0.36°C decade−1 since 1970, leading to glacier retreat and significant snowpack reduction. Due to these rapid environmental changes, this mountainous region is undergoing marked changes in spring phenology and elevational distribution of animals, plants and fungi. Long‐term monitoring in the European Alps offers an excellent natural laboratory to synthetize climate‐related changes in spring phenology and elevational distribution for a large array of taxonomic groups. This review assesses the climatic changes that have occurred across the European Alps during recent decades, spring phenological changes and upslope shifts of plants, animals and fungi from evidence in published papers and previously unpublished data. Our review provides evidence that spring phenology has been shifting earlier during the past four decades and distribution ranges show an upwards trend for most of the taxonomic groups for which there are sufficient data. The first observed activity of reptiles and terrestrial insects (e.g. butterflies) in spring has shifted significantly earlier, at an average rate of −5.7 and −6.0 days decade−1, respectively. By contrast, the first observed spring activity of semi‐aquatic insects (e.g. dragonflies and damselflies) and amphibians, as well as the singing activity or laying dates of resident birds, show smaller non‐significant trends ranging from −1.0 to +1.3 days decade−1. Leaf‐out and flowering of woody and herbaceous plants showed intermediate trends with mean values of −2.4 and −2.8 days decade−1, respectively. Regarding species distribution, plants, animals and fungi (N = 2133 species) shifted the elevation of maximum abundance (optimum elevation) upslope at a similar pace (on average between +18 and +25 m decade−1) but with substantial differences among taxa. For example, the optimum elevation shifted upward by +36.2 m decade−1 for terrestrial insects and +32.7 m decade−1 for woody plants, whereas it was estimated to range between −1.0 and +11 m decade−1 for semi‐aquatic insects, ferns, birds and wood‐decaying fungi. The upper range limit (leading edge) of most species also shifted upslope with a rate clearly higher for animals (from +47 to +91 m decade−1) than for plants (from +17 to +40 m decade−1), except for semi‐aquatic insects (−4.7 m decade−1). Although regional land‐use changes could partly explain some trends, the consistent upward shift found in almost all taxa all over the Alps is likely reflecting the strong warming and the receding of snow cover that has taken place across the European Alps over recent decades. However, with the possible exception of terrestrial insects, the upward shift of organisms seems currently too slow to track the pace of isotherm shifts induced by climate warming, estimated at about +62 to +71 m decade−1 since 1970. In the light of these results, species interactions are likely to change over multiple trophic levels through phenological and spatial mismatches. This nascent research field deserves greater attention to allow us to anticipate structural and functional changes better at the ecosystem level.
Mitigating amphibian chytridiomycoses in nature Garner, Trenton W. J.; Schmidt, Benedikt R.; Martel, An ...
Philosophical transactions of the Royal Society of London. Series B. Biological sciences,
12/2016, Letnik:
371, Številka:
1709
Journal Article
Recenzirano
Odprti dostop
Amphibians across the planet face the threat of population decline and extirpation caused by the disease chytridiomycosis. Despite consensus that the fungal pathogens responsible for the disease are ...conservation issues, strategies to mitigate their impacts in the natural world are, at best, nascent. Reducing risk associated with the movement of amphibians, non-amphibian vectors and other sources of infection remains the first line of defence and a primary objective when mitigating the threat of disease in wildlife. Amphibian-associated chytridiomycete fungi and chytridiomycosis are already widespread, though, and we therefore focus on discussing options for mitigating the threats once disease emergence has occurred in wild amphibian populations. All strategies have shortcomings that need to be overcome before implementation, including stronger efforts towards understanding and addressing ethical and legal considerations. Even if these issues can be dealt with, all currently available approaches, or those under discussion, are unlikely to yield the desired conservation outcome of disease mitigation. The decision process for establishing mitigation strategies requires integrated thinking that assesses disease mitigation options critically and embeds them within more comprehensive strategies for the conservation of amphibian populations, communities and ecosystems.
This article is part of the themed issue ‘Tackling emerging fungal threats to animal health, food security and ecosystem resilience’.
The recent arrival of Batrachochytrium salamandrivorans in Europe was followed by rapid expansion of its geographical distribution and host range, confirming the unprecedented threat that this ...chytrid fungus poses to western Palaearctic amphibians. Mitigating this hazard requires a thorough understanding of the pathogen's disease ecology that is driving the extinction process. Here, we monitored infection, disease and host population dynamics in a Belgian fire salamander (Salamandra salamandra) population for two years immediately after the first signs of infection. We show that arrival of this chytrid is associated with rapid population collapse without any sign of recovery, largely due to lack of increased resistance in the surviving salamanders and a demographic shift that prevents compensation for mortality. The pathogen adopts a dual transmission strategy, with environmentally resistant non-motile spores in addition to the motile spores identified in its sister species B. dendrobatidis. The fungus retains its virulence not only in water and soil, but also in anurans and less susceptible urodelan species that function as infection reservoirs. The combined characteristics of the disease ecology suggest that further expansion of this fungus will behave as a 'perfect storm' that is able to rapidly extirpate highly susceptible salamander populations across Europe.
Disease can be an important driver of host population dynamics and epizootics can cause severe host population declines. Batrachochytrium dendrobatidis (Bd), the pathogen causing amphibian ...chytridiomycosis, may occur epizootically or enzootically and can harm amphibian populations in many ways. While effects of Bd epizootics are well documented, the effects of enzootic Bd have rarely been described. We used a state-space model that accounts for observation error to test whether population trends of a species highly susceptible to Bd, the midwife toad Alytes obstetricans, are negatively affected by the enzootic presence of the pathogen. Unexpectedly, Bd had no negative effect on population growth rates from 2002-2008. This suggests that negative effects of disease on individuals do not necessarily translate into negative effects at the population level. Populations of amphibian species that are susceptible to the emerging disease chytridiomycosis can persist despite the enzootic presence of the pathogen under current environmental conditions.
Summary
The use of environmental DNA (eDNA) to detect species in aquatic environments such as ponds and streams is a powerful new technique with many benefits. However, species detection in ...eDNA‐based surveys is likely to be imperfect, which can lead to underestimation of the distribution of a species.
Site occupancy models account for imperfect detection and can be used to estimate the proportion of sites where a species occurs from presence/absence survey data, making them ideal for the analysis of eDNA‐based surveys. Imperfect detection can result from failure to detect the species during field work (e.g. by water samples) or during laboratory analysis (e.g. by PCR).
To demonstrate the utility of site occupancy models for eDNA surveys, we reanalysed a data set estimating the occurrence of the amphibian chytrid fungus Batrachochytrium dendrobatidis using eDNA. Our reanalysis showed that the previous estimation of species occurrence was low by 5–10%. Detection probability was best explained by an index of the number of hosts (frogs) in ponds.
Per‐visit availability probability in water samples was estimated at 0·45 (95% CRI 0·32, 0·58) and per‐PCR detection probability at 0·85 (95% CRI 0·74, 0·94), and six water samples from a pond were necessary for a cumulative detection probability >95%. A simulation study showed that when using site occupancy analysis, researchers need many fewer samples to reliably estimate presence and absence of species than without use of site occupancy modelling.
Our analyses demonstrate the benefits of site occupancy models as a simple and powerful tool to estimate detection and site occupancy (species prevalence) probabilities despite imperfect detection. As species detection from eDNA becomes more common, adoption of appropriate statistical methods, such as site occupancy models, will become crucial to ensure that reliable inferences are made from eDNA‐based surveys.
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