Showing papers by "An Martel published in 2020"

Integral chain management of wildlife diseases

Abstract: The chytrid fungus Batrachochytrium dendrobatidis has caused the most prominent loss of vertebrate diversity ever recorded, which peaked in the 1980s. Recent incursion by its sister species B. salamandrivorans in Europe raised the alarm for a new wave of declines and extinctions in western Palearctic urodeles. The European Commission has responded by restricting amphibian trade. However, private amphibian collections, the main end consumers, were exempted from the European legislation. Here, we report how invasion by a released, exotic newt coincided with B. salamandrivorans invasion at over 1000 km from the nearest natural outbreak site, causing mass mortality in indigenous marbled newts (Triturus marmoratus), and posing an acute threat to the survival of nearby populations of the most critically endangered European newt species (Montseny brook newt, Calotriton arnoldi). Disease management was initiated shortly after detection in a close collaboration between policy and science and included drastic on site measures and intensive disease surveillance. Despite these efforts, the disease is considered temporarily contained but not eradicated and continued efforts will be necessary to minimize the probability of further pathogen dispersal. This precedent demonstrates the importance of tackling wildlife diseases at an early stage using an integrated approach, involving all stakeholders and closing loopholes in existing regulations.

Dampened virulence and limited proliferation of Batrachochytrium salamandrivorans during subclinical infection of the troglobiont olm (Proteus anguinus).

Abstract: Emerging infections add to existing threats to the survival of amphibians worldwide. The olm (Proteus anguinus) is a vulnerable, troglobiont urodele species with a small European range and restricted to underground karstic systems. Population declines to emerging threats like the chytrid fungus Batrachochytrium salamandrivorans, are likely to go unnoticed due to inaccessibility of the species’ habitat. We here studied the interaction between olms and B. salamandrivorans. Experimental inoculation of olms resulted in low-level, asymptomatic but persistent infections, with limbs as predilection sites. The lack of exponential fungal growth in the olms’ epidermis correlated with limited fungal proliferation and dampened virulence gene expression after exposure to olm skin compounds. The olm is one of few western Palearctic urodeles that is tolerant to B. salamandrivorans infection and may act as a subterranean disease reservoir, yet costs of subclinical infection may compromise olm fitness on the long term.

Presence of low virulence chytrid fungi could protect European amphibians from more deadly strains

Abstract: Wildlife diseases are contributing to the current Earth’s sixth mass extinction; one disease, chytridiomycosis, has caused mass amphibian die-offs. While global spread of a hypervirulent lineage of the fungus Batrachochytrium dendrobatidis (BdGPL) causes unprecedented loss of vertebrate diversity by decimating amphibian populations, its impact on amphibian communities is highly variable across regions. Here, we combine field data with in vitro and in vivo trials that demonstrate the presence of a markedly diverse variety of low virulence isolates of BdGPL in northern European amphibian communities. Pre-exposure to some of these low virulence isolates protects against disease following subsequent exposure to highly virulent BdGPL in midwife toads (Alytes obstetricans) and alters infection dynamics of its sister species B. salamandrivorans in newts (Triturus marmoratus), but not in salamanders (Salamandra salamandra). The key role of pathogen virulence in the complex host-pathogen-environment interaction supports efforts to limit pathogen pollution in a globalized world. The pathogen Batrachochytrium dendrobatidis (BD) associated with widespread amphibian declines is present in Europe but has not consistently caused disease-induced declines in that region. Here, the authors suggest that an endemic strain of BD with low virulence may protect the hosts upon co-infection with more virulent strains.

Response to Comment on “Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity”

Abstract: Lambert et al question our retrospective and holistic epidemiological assessment of the role of chytridiomycosis in amphibian declines. Their alternative assessment is narrow and provides an incomplete evaluation of evidence. Adopting this approach limits understanding of infectious disease impacts and hampers conservation efforts. We reaffirm that our study provides unambiguous evidence that chytridiomycosis has affected at least 501 amphibian species.

Batrachochytrium salamandrivorans kills alpine newts (Ichthyosaura alpestris) in southernmost Germany

Abstract: The European amphibian fauna is threatened by several different pathogens. We currently know of mortalities linked to ranaviruses (Kik et al. 2011), and to two fungal pathogens, the widespread Batrachochytrium dendro­ batidis, causing amphibian mortalities in several European countries (Fisher et al. 2009), and the invasive chytrid fungus B. salamandrivorans (Bsal), affecting especially urodeles (Martel et al. 2013, 2014). A modelling study suggests that currently much of the ecological niche of Bsal remains unoccupied in Europe (Beukema et al. 2018). A further successful spread of this pathogen is therefore likely. In Europe, Germany has been counting about 50 known Bsal-positive sites (Lötters et al. 2020 in this issue) which makes it currently the most severely impacted country. Several new observations of Bsal-related amphibian mortalities in the South of Germany have been made in recent years (Lötters et al. 2020 in this issue), including the first proof of Bsal in Bavaria in 2020 (Thein et al. 2020 in this issue). Here we provide evidence of the first Bsal occurrence in the German region of Allgovia (northern Alps, Bavaria). Several mortality events of alpine newts (Ichthyo­ saura alpestris) have been observed in garden ponds in a small village north east of the town of Memmingen (Allgovia, Germany, N48.05883°, E10.32297°, Fig. 1) beginning of April 2020. Characteristic Bsal-lesions were observed on the skin of these specimens (N = 10, Fig. 2). We tested eight tissue samples of the specimens from one garden pond via qPCR analysis (standard protocol see Blooi et al. 2013), detecting the presence of Bsal (mean GE = 36,145.5 ± 12436.8, GE range: 104–94,800). Histological analyses confirmed the presence of sporangia in typical ulcerative skin lesions in five specimens. In the close vicinity of the site of mortality events several additional dead alpine newts were observed, but neither collected nor analyzed. Alpine newts have been demonstrated to be susceptible to Bsal infection (Martel et al. 2014) and identified as potential Bsal reservoirs (Stegen et al. 2017). Our report confirms Bsal-induced field mortality in this species (Schulz et al. 2018, 2020 in this issue). The impact at the level of populations remains unclear since alpine newts are potentially able to cure themselves when affected by only a low load of Bsal zoospores (Stegen et al. 2017). Transmission pathways of batrachochytrids are poorly understood. Bsal was estimated to spread slowly under natural conditions due to the low migration ability of urodeles (Trochet et al. 2014). Long-distance spread may mainly be anthropogenic (Spitzen-van der Sluijs et al. 2018, Martel et al. 2020), especially given that the here reported mortalities were observed in a garden pond. The geographically closest known occurrence of Bsal is located at a distance of ca. 170 km of this outbreak in the Bavarian Steigerwald (Thein et al. 2020 in this issue). These new observations of mortalities suggest that Bsal is spreading or is being spread by humans across large distances. Aquatic plants bought e.g. in garden centers may be possible vectors, as it is known that amphibians can hide in those plants and then are transported together with pathogens over longer distances and released in suitable habitats (a garden pond, pers. observ. DSS).

Microclimate limits thermal behaviour favourable to disease control in a nocturnal amphibian.

Abstract: While epizootics increasingly affect wildlife, it remains poorly understood how the environment shapes most host-pathogen systems. Here, we employ a three-step framework to study microclimate influence on ectotherm host thermal behaviour, focusing on amphibian chytridiomycosis in fire salamanders (Salamandra salamandra) infected with the fungal pathogen Batrachochytrium salamandrivorans (Bsal). Laboratory trials reveal that innate variation in thermal preference, rather than behavioural fever, can inhibit infection and facilitate salamander recovery under humidity-saturated conditions. Yet, a 3-year field study and a mesocosm experiment close to the invasive Bsal range show that microclimate constraints suppress host thermal behaviour favourable to disease control. A final mechanistic model, that estimates range-wide, year-round host body temperature relative to microclimate, suggests that these constraints are rule rather than exception. Our results demonstrate how innate host defences against epizootics may remain constrained in the wild, which predisposes to range-wide disease outbreaks and population declines.

Using environmental DNA for detection of Batrachochytrium salamandrivorans in natural water

Abstract: Rapid, early, and reliable detection of invasive pathogenic microorganisms is essential in order to either predict or delineate an outbreak, and monitor appropriate mitigation measures. The chytrid fungus Batrachochytrium salamandrivorans is expanding in Europe, and infection with this fungus may cause massive mortality in urodelans (salamanders and newts). In this study, we designed and validated species‐specific primers and a probe for detection of B. salamandrivorans in water. In a garden pond in close proximity to the B. salamandrivorans index site in the Netherlands, B. salamandrivorans‐infected newts had been detected in 2015 and have been monitored since. In 2016 and 2017, no B. salamandrivorans was detected at this site, but in 2018 B. salamandrivorans flared up in this isolated pond which allowed validation of the technique in situ. We here present the development of an environmental DNA technique that successfully detects B. salamandrivorans DNA in natural waterbodies even at low concentrations. This technique may be further validated to play a role in B. salamandrivorans range delineation and surveillance in both natural waterbodies and in captive collections.

Forest edges, tree diversity and tree identity change leaf miner diversity in a temperate forest

Abstract: In forests, besides tree diversity, tree identity can determine herbivore species diversity. Herbivore species diversity can also depend on spatial factors, such as edge effects; however, empirical evidence for this remains scarce. Furthermore, patterns in herbivore diversity may differ between forest stand level and responses at individual tree species. It is therefore important to disentangle stand-level patterns from associational responses specific to certain host species. We studied the effects of edge distance, tree diversity and tree species composition on leaf miner abundance, richness and diversity in temperate forests. We disentangled leaf miners' responses at stand level from those of miners associated with each of three individual tree species: Quercus robur L., Quercus rubra L. and Fagus sylvatica L. We found that tree diversity increased stand-level leaf miner richness and diversity. Fagus sylvatica and stand-level leaf miner abundance increased closer to edges. This was suppressed at stand level in more diverse mixtures. Underlying tree diversity effects, stand-level leaf miner metrics are strongly associated with tree species composition, due to many unique species found on F. sylvatica and Q. robur. Additionally, F. sylvatica experienced associational susceptibility to abundance in mixtures with Q. robur. Quercus robur experienced association susceptibility to miner richness in the mixture with Q. rubra. Studying the herbivore community at different spatial scales is a first step towards better understanding tree identity effects underlying tree diversity effects. Our findings emphasise context dependency of positive diversity effects on herbivores in terms of edge effects and tree species composition.

Preliminary report on the occurrence of Batrachochytrium salamandrivorans in the Steigerwald, Bavaria, Germany

Abstract: 1) Büro für Faunistik und Umweltbildung, Herrleinstr. 2, 97437 Haßfurt, Germany 2) Freundeskreis Nationalpark Steigerwald (Naturschutzverbände), Rathausplatz 4, 96157 Ebrach, Germany 3) Museum für Naturkunde Leibniz-Institut für Evolutionsund Biodiversitätsforschung, Invalidenstr. 4,10115 Berlin, Germany 4) Wildlife Health Ghent, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium 5) University of Leipzig, Institute of Biology, Molecular Evolution and Systematics of Animals, Talstr. 33, 04103 Leipzig, Germany 6) Technische Universität Braunschweig, Zoological Institute, Mendelssohnstr. 4, 38106 Braunschweig, Germany 7) Bayerisches Landesamt für Umwelt, Referat 55 Artenund Lebensraumschutz, Bürgermeister-Ulrich-Str. 160, 86179 Augsburg, Germany

Instant killing of pathogenic chytrid fungi by disposable nitrile gloves prevents disease transmission between amphibians

Abstract: To prevent transmission of the pathogenic chytrid fungi Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal), hygiene protocols prescribe the single use of disposable gloves for handling amphibians. We discovered that rinse water from nitrile gloves instantly kills 99% of Bd and Bsal zoospores. Transmission experiments using midwife toads (Alytes obstetricans) and Bd, and Alpine newts (Ichthyosaura alpestris) and Bsal, show that the use of the same pair of gloves for 2 subsequent individuals does not result in significant transmission of any chytrid fungus. In contrast, handling infected amphibians bare-handed caused transmission of Bsal in 4 out of 10 replicates, but did not result in transmission of Bd. Based on the manufacturer’s information, high resolution mass spectrometry (HRMS) and colorimetric tests, calcium lactate and calcium nitrate were identified as compounds with antifungal activity against both Bd and Bsal. These findings corroborate the importance of wearing gloves as an important sanitary measure in amphibian disease prevention. If the highly recommended single use of gloves is not possible, handling multiple post-metamorphic amphibians with the same pair of nitrile gloves should still be preferred above bare-handed manipulation.

Landscape Connectivity Limits the Predicted Impact of Fungal Pathogen Invasion.

Abstract: Infectious diseases are major drivers of biodiversity loss. The risk of fungal diseases to the survival of threatened animals in nature is determined by a complex interplay between host, pathogen and environment. We here predict the risk of invasion of populations of threatened Mediterranean salamanders of the genus Lyciasalamandra by the pathogenic chytrid fungus Batrachochytrium salamandrivorans by combining field sampling and lab trials. In 494 samples across all seven species of Lyciasalamandra, B. salamandrivorans was found to be absent. Single exposure to a low (1000) number of fungal zoospores resulted in fast buildup of lethal infections in three L. helverseni. Thermal preference of the salamanders was well within the thermal envelope of the pathogen and body temperatures never exceeded the fungus’ thermal critical maximum, limiting the salamanders’ defense opportunities. The relatively low thermal host preference largely invalidates macroclimatic based habitat suitability predictions and, combined with current pathogen absence and high host densities, suggests a high probability of local salamander population declines upon invasion by B. salamandrivorans. However, the unfavorable landscape that shaped intraspecific host genetic diversity, lack of known alternative hosts and rapid host mortality after infection present barriers to further, natural pathogen dispersal between populations and thus species extinction. The risk of anthropogenic spread stresses the importance of biosecurity in amphibian habitats.

Host-pathogen co-existence incurs reproductive costs

Abstract: Widespread endemism of host-adapted pathogens poses a heavy burden on animal and human health. Mechanisms underpinning long-term host pathogen co-existence and concurrent costs are poorly understood. We use infections in pigeons with pathogenic, pigeon adapted Salmonella Typhimurium to explain how host and pathogen trade-offs and benefits sustain long-term pathogen endemism. An experimentally infected group of pigeons that was studied for 15 months showed that pathogen persistence decreased host condition and reproductive success, but conferred protection against Salmonella-induced clinical disease. The relevance of these findings was confirmed in nature, where this pathogen was shown to widely occur in feral pigeons (Columba livia), yet without clinical disease. Pathogen transmission and long-term persistence were associated with intermittent faecal shedding, which markedly increased during crop feeding and natural stress periods. Exploiting host specific traits in the presence of protective host population immunity thus facilitates long-term co-existence, be it at a significant reproductive cost.

Season as a discriminating factor for faecal metabolomic composition of great tits (Parus major)

Abstract: The microbiome of wild birds has been associated with health status and risk of disease development, but underlying metabolomic mechanisms are still unknown. Metabolites produced by microbial organisms may affect host metabolic processes and by doing so influence host health. Here we provide for the first time data on the faecal metabolome of wild great tits ( Parus major ) by analyzing metabolites associations with age, sex, season and body condition. Using untargeted metabolomics, we analyzed faecal samples from 112 great tits that were caught in a deciduous forest fragment in Flanders (Belgium) during late autumn and 19 animals that were re-captured during early spring. In this study, no significant associations between the faecal metabolites and age, sex and body condition were observed. However, season was shown to be a discriminating factor for the metabolomic composition of great tits, suggesting an impact of environmental factors.

Toxigenic and zoonotic Corynebacterium ulcerans emerges from widespread hedgehog disease

Abstract: Toxin-producing Corynebacterium ulcerans, causing diphtheria in humans, were isolated from 53 diseased hedgehogs during spring 2020 in Belgium. Isolates showed low levels of acquired antimicrobial resistance. Pronounced strain diversity suggests emergence from an endemic situation. These findings stress the need for raising public awareness and improved wildlife disease surveillance.

A New Family of Diverse Skin Peptides from the Microhylid Frog Genus Phrynomantis.

Abstract: A wide range of frogs produce skin poisons composed of bioactive peptides for defence against pathogens, parasites and predators. While several frog families have been thoroughly screened for skin-secreted peptides, others, like the Microhylidae, have remained mostly unexplored. Previous studies of microhylids found no evidence of peptide secretion, suggesting that this defence adaptation was evolutionarily lost. We conducted transcriptome analyses of the skins of Phrynomantis bifasciatus and Phrynomantis microps, two African microhylid species long suspected to be poisonous. Our analyses reveal 17 evolutionary related transcripts that diversified from to those of cytolytic peptides found in other frog families. The 19 peptides predicted to be processed from these transcripts, named phrynomantins, show a striking structural diversity that is distinct from any previously identified frog skin peptide. Functional analyses of five phrynomantins confirm the loss of a cytolytic function and the absence of insecticidal or proinflammatory activity, suggesting that they represent an evolutionary transition to a new, yet unknown function. Our study shows that peptides have been retained in the defence poison of at least one microhylid lineage and encourages research on similarly understudied taxa to further elucidate the diversity and evolution of skin defence molecules.

Body size and tree species composition determine variation in prey consumption in a forest-inhabiting generalist predator

Abstract: O_LIDue to physiological, behavioural or ecological mechanisms, generalist predators may show individual variation in prey consumption. This individual specialization can result from both environmental and trait variation, with especially body size strongly connected to diet. Environmental variation can thus affect consumer-predator interactions by the joint action of changes in prey community composition and predator size. C_LIO_LIWe studied whether and how changes in forest environmental conditions, such as variation in tree species identity and forest fragmentation, affect predator-prey interactions. More specifically we anticipate tree diversity or spatial context to impact the predator diet directly via prey availability and prey size, but also indirectly through shifts in predator size. We used the orb-weaving spider Araneaus diadematus inhabiting forest fragments differing in edge distance, tree diversity and tree species as a model species. The species diet was quantified by an unprecedented metabarcoding campaign. A total of 983 spiders were subjected to molecular diet analysis, from in total of 53 forest plots. C_LIO_LIA. diadematus showed to be a generalist predator, with 298 prey items detected in total. At the individual level, we found large spiders to consume less different species, but consistently larger species. Tree species composition affected both prey species richness and size in the spiders diet, although tree diversity per se had no influence on the consumed prey. Edges had an indirect effect on the spider diet as spiders closer to the forest edge were larger and therefore consumed larger prey. C_LIO_LIWe attribute the structural complexity of the understory related to tree species composition as a driver of prey composition and its size distribution as reflected in the predators diet. Although large spiders may specialize on large prey, we found no firm evidence for either ecological opportunism or strong specialization. Finally, we conclude that intraspecific size variation and tree species composition define the consumed prey of this generalist predator, and that the many feeding interactions of this spider underlie the species success in a large diversity of habitats. C_LI

Mixing tree species is especially beneficial for biodiversity and forest functioning in highly fragmented landscapes

Abstract: Contemporary forest management strives to satisfy contrasting demands on forest ecosystems by promoting multiple ecosystem services. These services are affected in varied manners by alternative management actions operating at local or landscape scales, potentially leading to trade-offs and synergies. We here studied ecosystem functions and biodiversity data across ecosystem compartments in 53 mature forest plots varying in stand-level (tree species composition) and landscape-level (degree of fragmentation) characteristics. We show that more than two-thirds of the 20 trade-offs and synergies between functions and diversity variables were driven by variation in tree species composition and fragmentation. Interestingly, more fragmented landscapes had higher landscape-level forest functioning, but this came at the expense of forest biodiversity. At the same time, mixed forest stands had higher levels of biodiversity than monocultures without affecting forest functioning. Diversifying forest stands thus represents a potential management strategy that promotes both ecosystems functioning and biodiversity in fragmented landscapes.