Showing papers by "An Martel published in 2021"

Epidermal galactose spurs chytrid virulence and predicts amphibian colonization.

Abstract: The chytrid fungal pathogens Batrachochytrium dendrobatidis and Batrachochytrium salamandrivorans cause the skin disease chytridiomycosis in amphibians, which is driving a substantial proportion of an entire vertebrate class to extinction. Mitigation of its impact is largely unsuccessful and requires a thorough understanding of the mechanisms underpinning the disease ecology. By identifying skin factors that mediate key events during the early interaction with B. salamandrivorans zoospores, we discovered a marker for host colonization. Amphibian skin associated beta-galactose mediated fungal chemotaxis and adhesion to the skin and initiated a virulent fungal response. Fungal colonization correlated with the skin glycosylation pattern, with cutaneous galactose content effectively predicting variation in host susceptibility to fungal colonization between amphibian species. Ontogenetic galactose patterns correlated with low level and asymptomatic infections in salamander larvae that were carried over through metamorphosis, resulting in juvenile mortality. Pronounced variation of galactose content within some, but not all species, may promote the selection for more colonization resistant host lineages, opening new avenues for disease mitigation.

Diet diversity and environment determine the intestinal microbiome and bacterial pathogen load of fire salamanders.

Abstract: Diverse communities of symbiotic microbes inhabit the digestive systems of vertebrates and play a crucial role in animal health, and host diet plays a major role in shaping the composition and diversity of these communities. Here, we characterized diet and gut microbiome of fire salamander populations from three Belgian forests. We carried out DNA metabarcoding on fecal samples, targeting eukaryotic 18S rRNA of potential dietary prey items, and bacterial 16S rRNA of the concomitant gut microbiome. Our results demonstrated an abundance of soft-bodied prey in the diet of fire salamanders, and a significant difference in the diet composition between males and females. This sex-dependent effect on diet was also reflected in the gut microbiome diversity, which is higher in males than female animals. Proximity to human activities was associated with increased intestinal pathogen loads. Collectively, the data supports a relationship between diet, environment and intestinal microbiome in fire salamanders, with potential health implications.

Diversity, multifaceted evolution, and facultative saprotrophism in the European Batrachochytrium salamandrivorans epidemic.

Abstract: While emerging fungi threaten global biodiversity, the paucity of fungal genome assemblies impedes thoroughly characterizing epidemics and developing effective mitigation strategies. Here, we generate de novo genomic assemblies for six outbreaks of the emerging pathogen Batrachochytrium salamandrivorans (Bsal). We reveal the European epidemic currently damaging amphibian populations to comprise multiple, highly divergent lineages demonstrating isolate-specific adaptations and metabolic capacities. In particular, we show extensive gene family expansions and acquisitions, through a variety of evolutionary mechanisms, and an isolate-specific saprotrophic lifecycle. This finding both explains the chytrid’s ability to divorce transmission from host density, producing Bsal’s enigmatic host population declines, and is a key consideration in developing successful mitigation measures. B. salamandrivorans (Bsal) is a fungus of amphibians that has been implicated in the collapse of salamander populations. Here, the authors sequence nine Bsal isolates from six epidemic sites and describe variation in genome size and composition.

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

Abstract: Trophic interactions may strongly depend on body size and environmental variation, but this prediction has been seldom tested in nature. Many spiders are generalist predators that use webs to intercept flying prey. The size and mesh of orb webs increases with spider size, allowing a more efficient predation on larger prey. We studied to this extent the orb-weaving spider Araneus diadematus inhabiting forest fragments differing in edge distance, tree diversity, and tree species. These environmental variables are known to correlate with insect composition, richness, and abundance. We anticipated these forest characteristics to be a principle driver of prey consumption. We additionally hypothesized them to impact spider size at maturity and expect shifts toward larger prey size distributions in larger individuals independently from the environmental context. We quantified spider diet by means of metabarcoding of nearly 1,000 A. diadematus from a total of 53 forest plots. This approach allowed a massive screening of consumption dynamics in nature, though at the cost of identifying the exact prey identity, as well as their abundance and putative intraspecific variation. Our study confirmed A. diadematus as a generalist predator, with more than 300 prey ZOTUs detected in total. At the individual level, we found large spiders to consume fewer different species, but adding larger species to their diet. Tree species composition affected both prey species richness and size in the spider's 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. We conclude that both intraspecific size variation and tree species composition shape the consumed prey of this generalist predator.

Overstorey composition shapes across-trophic level community relationships in deciduous forest regardless of fragmentation context

Abstract: 1. Communities across trophic levels, and the functional roles they play, are vital for the sustained provision of ecosystem services. In forest systems, diversification of overstorey composition has been shown to be a key driver of biodiversity, but its influence on across-trophic level relationships remains scarcely known. Species across trophic levels in varied overstorey compositions are also differentially susceptible to fragmentation context. We hypothesise that fragmentation will disrupt community relationships associated with particular overstorey compositions. 2. We test this hypothesis using a tree diversity research platform across 53 deciduous woodland plots in central Belgium. We estimate species' abundances within nine, generally taxonomic, community groups across trophic levels: understorey vegetation; leaf miners and gall formers; woodlice, millipedes; carabid beetles, harvestmen, spiders, birds, bats. We use multiple co-inertia analyses to examine how taxonomic and trophic role community matrices covary across gradients of overstorey composition, via three different tree species diversification pathways, and fragmentation. 3. For all trophic role groups, across all plots, there was at least one significant pairwise comparison. Apart from comparisons involving bats, there was at least one significant pairwise correlation between taxonomic groups too. These results indicate correlated community matrices across trophic levels. Overstorey composition related to community tightness, that is, the level of co-ordinated change among taxonomic and/or trophic role groups as revealed by multiple co-inertia analyses. Notably, diversifying woodlands of beech Fagus sylvatica or red oak Quercus rubra with pedunculate oak Quercus robur correlated with increased taxonomic community tightness. Diversifying pedunculate oak forest stands with other overstorey species related to unchanged community tightness. Evidence was lacking for fragmentation affecting community tightness, singly or by interacting with overstorey composition. 4. Synthesis. Overall, changing tree species composition and fragmentation level affected across-trophic level community relationships differently. Yet, we demonstrated a clear signal that diversifying monoculture stands with particular species correlated with greater community tightness, and co-ordinated change among sets of community groups, across trophic levels and regardless of fragmentation context. We postulate that having tighter community relationships suggests that measures to improve biodiversity at one trophic level (i.e. trees) could affect other groups, and their associated roles, in a co-ordinated manner.

Landscape epidemiology of Batrachochytrium salamandrivorans : reconciling data limitations and conservation urgency

Abstract: Starting in 2010, rapid fire salamander (Salamandra salamandra) population declines in northwestern Europe heralded the emergence of Batrachochytrium salamandrivorans (Bsal), a salamander-pathogenic chytrid fungus. Bsal poses an imminent threat to global salamander diversity owing to its wide host range, high pathogenicity, and long-term persistence in ecosystems. While there is a pressing need to develop further research and conservation actions, data limitations inherent to recent pathogen emergence obscure necessary insights into Bsal disease ecology. Here, we use a hierarchical modeling framework to describe Bsal landscape epidemiology of outbreak sites in light of these methodological challenges. Using model selection and machine learning, we find that Bsal presence is associated with humid and relatively cool, stable climates. Outbreaks are generally located in areas characterized by low landscape heterogeneity and low steepness of slope. We further find an association between Bsal presence and high trail density, suggesting that human-mediated spread may increase risk for spillover between populations. We then use distribution modeling to show that favorable conditions occur in lowlands influenced by the North Sea, where increased survey effort is needed to determine how Bsal impacts local newt populations, but also in hill- and mountain ranges in northeastern France and the lower half of Germany. Finally, connectivity analyses suggest that these hill- and mountain ranges may act as stepping stones for further spread southward. Our results provide initial insight into regional environmental conditions underlying Bsal epizootics, present updated invasibility predictions for northwestern Europe, and lead us to discuss a wide variety of potential survey and research actions needed to advance future conservation and mitigation efforts.

Love bites: male frogs (Plectrohyla, Hylidae) use teeth scratching to deliver sodefrin precursor-like factors to females during amplexus.

Abstract: BACKGROUND Efficient transfer of chemical signals is important for successful mating in many animal species. Multiple evolutionary lineages of animals evolved direct sex pheromone transmission during traumatic mating-the wounding of the partner with specialized devices-which helps to avoid signal loss to the environment. Although such direct transmission modes of so-called allohormone pheromones are well-documented in invertebrates, they are considered rare in vertebrates. Males of several species of the frog genus Plectrohyla (Hylidae, Anura) have elongated teeth and develop swollen lips during the breeding season. Here we investigated the possibility that these structures are used to scratch the females' skin and apply allohormone pheromones during traumatic mating in several Plectrohyla species. RESULTS Our behavioural observations revealed that males press their upper jaw onto the females' dorsum during amplexus, leaving small skin scratches with their teeth. Histological examinations of the males' lips identified specialized mucus glands, resembling known amphibian pheromone glands. Whole-transcriptome sequencing of these breeding glands showed high expression of sodefrin precursor-like factor (SPF) proteins, which are known to have a pheromone function in multiple amphibian species. CONCLUSIONS Our study suggests SPF delivery via traumatic mating in several anuran species: the males have specialized breeding glands in the lips for production and secretion and use their elongated teeth as wounding devices for application. We hypothesize that these SPF proteins end up in the females' circulatory system, where understanding their exact function will require further molecular, physiological and behavioural testing.

Batrachochytrium salamandrivorans Threat to the Iberian Urodele Hotspot

Abstract: The recent introduction of the chytrid fungus Batrachochytrium salamandrivorans into northeastern Spain threatens salamander diversity on the Iberian Peninsula. We assessed the current epidemiological situation with extensive field sampling of urodele populations. We then sought to delineate priority regions and identify conservation units for the Iberian Peninsula by estimating the susceptibility of Iberian urodeles using laboratory experiments, evidence from mortality events in nature and captivity and inference from phylogeny. None of the 1395 field samples, collected between 2015 and 2021 were positive for Bsal and no Bsal-associated mortality events were recorded, in contrast to the confirmed occurrence of Bsal outbreak previously described in 2018. We classified five of eleven Iberian urodele species as highly susceptible, predicting elevated mortality and population declines following potential Bsal emergence in the wild, five species as intermediately susceptible with variable disease outcomes and one species as resistant to disease and mortality. We identified the six conservation units (i.e., species or lineages within species) at highest risk and propose priority areas for active disease surveillance and field biosecurity measures. The magnitude of the disease threat identified here emphasizes the need for region-tailored disease abatement plans that couple active disease surveillance to rapid and drastic actions.

Exploring the faecal microbiome of the Eurasian nuthatch (Sitta europaea)

Abstract: Gastrointestinal microbiota fulfill pivotal roles in providing a host with nutrition and protection from pathogenic microorganisms. Up to date, most microbiota research has focused on humans and other mammals, whereas birds and especially wild birds lag behind. Within the field of the avian gut microbiome, research is heavily biased towards poultry. In this study, we analyzed the gut microbiome of the Eurasian nuthatch (Sitta europaea), using faecal samples of eight nestlings originating from three nuthatch nests in the south of Ghent (Belgium), using Illumina sequencing of the 16S rRNA gene. Relative frequency analysis showed a dominance of Firmicutes and Actinobacteria and to a lesser extent Proteobacteria. Bacteroidetes and other phyla were relatively rare. At higher taxonomic levels, a high degree of inter-individual variation in terms of overall microbiota community structure as well as dominance of certain bacteria was observed, but with a higher similarity for the nestlings sharing the same nest. When comparing the nuthatch faecal microbiome to that of great tit nestlings that were sampled during the same breeding season and in the same forest fragment, differences in the microbial community structure were observed, revealing distinct dissimilarities in the relative abundancy of taxa between the two bird species. This study is the first report on the nuthatch microbiome and serves as a reference study for nuthatch bacterial diversity and can be used for targeted screening of the composition and general functions of the avian gut microbiome.

Widespread Disease in Hedgehogs (Erinaceus europaeus) Caused by Toxigenic Corynebacterium ulcerans.

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

Alternative food sources interfere with removal of a fungal amphibian pathogen by zooplankton

Abstract: While the amphibian disease chytridiomycosis is causing ongoing population declines and biodiversity losses around the globe, efficient mitigation strategies are lacking. The free-living zoospores of the causative agents of this disease, the chytrid pathogens Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal), are a potential food source for filter-feeding micropredators as part of the aquatic food web. While consumption of zoospores can lower environmental pathogen loads, alternative food sources may interfere with pathogen removal rates. We compared the ability of three filter-feeding zooplankton species, the cladoceran Daphnia magna, the rotifer Brachionus calyciflorus and the ostracod Heterocypris incongruens, to remove Bd zoospores in water and investigated the effect of alternative food sources, the green algae Pseudokirchneriella subcapitata and Chlorella vulgaris, on zoospore ingestion by D. magna. Daphnia magna was the only micropredator candidate that effectively removed Bd zoospores from its environment, with an average removal rate of 1,012 +/- 542 GE ind.(-1) hr(-1) within our test system. High concentrations (1 x 10(5) cells/ml) of large and easily ingestible P. subcapitata reduced pathogen removal rates, whereas the small and less edible C. vulgaris did not interfere with pathogen removal. Synthesis and applications. We showed that Daphnia spp., which are keystone species in all sorts of aquatic habitats worldwide, are promising target agents for biologically mitigating chytridiomycosis infections and how natural food sources may interfere with this strategy. We also suggest potential management actions for biological disease mitigation, aiming to optimize environmental conditions for these target filter feeders, thereby reducing pathogen densities and eventually infection pressure in amphibian hosts. Examples of such management actions include, but are not limited to, removal of planktivorous fish, habitat restoration, nutrient control or agrochemical regulation in the vicinity of amphibian breeding ponds. Further studies, including field trials, are needed to confirm the effects of pathogen consumption on infection dynamics in natural situations and investigate the impact of intervention actions.

Does Chytridiomycosis Affect Tree Frog Attachment

Abstract: The pandemic disease chytridiomycosis, caused by the fungus Batrachochytrium dendrobatidis (Bd), is a major threat to amphibian biodiversity. For most species, the exact mechanisms of chytridiomycosis that lead to negative population dynamics remain uncertain, though mounting evidence suggests that sublethal effects could be an important driver. In this review, we propose that tree frog attachment is a promising case to study the sublethal effects of a Bd infection on amphibians. A synthesis of the current knowledge on the functional morphology of the adhesive toe pads of tree frogs, on the underlying mechanisms of tree frog attachment, and on the epidermal pathology of chytridiomycosis substantiates the hypothesis that Bd-induced epidermal alterations have the potential to disrupt tree frog attachment. We highlight a series of (biomechanical) experiments to test this hypothesis and to shed some light on the sublethal disease mechanisms of chytridiomycosis. The knowledge generated from such an approach could contribute to future research on Bd epidemiology and ultimately to the conservation of the biodiversity of arboreal anurans.

Persecution of Birds of Prey in Flanders: A Retrospective Study 2011–19

Abstract: For decades birds of prey have been under the protection of European law, but deliberate or unintentional killing is still a large-scale problem in Europe. In an effort to monitor illegal practices, the Flemish government established several bird of prey hotlines in 2006. Since then, every suspicious death of a bird of prey has been investigated. This retrospective study reviews the necropsy results of every bird of prey submitted for investigation from January 2011 to December 2019, with a focus on illegal practices. In 36.7% (83/226) of all necropsy cases, an illegal cause of death was found, with poisoning being demonstrated in 88% (73/83) of these cases. Cholinesterase inhibitors were the most commonly used toxins, despite being prohibited in Europe. With a prevalence of 82.5% (260/315) of all cases, the Common Buzzard (Buteo buteo) was the species most submitted for necropsy.

Application of Disinfectants for Environmental Control of a Lethal Amphibian Pathogen.

Abstract: Chytridiomycosis is an emerging infectious disease threatening amphibian populations worldwide. While environmental disinfection is important in mitigating the disease, successful elimination of Batrachochytrium dendrobatidis (Bd) without excessively harming ecosystems is challenging. We selected peracetic acid (PAA) as the most potent of six commercially available products regarding their ability to inhibit growth of a highly virulent Bd strain. PAA killed Bd after 5 min of exposure to approximately 94.7 mg/L. We examined the toxicity of PAA against three invertebrate species and Discoglossus pictus tadpoles. 93% of invertebrates, but none of the tadpoles survived 5 min of exposure to 94.7 mg/L. Tadpoles showed no adverse effects after 5 min exposure to concentrations of approximately 37.9 mg/L or lower. Addition of PAA to aquatic microcosms decreased pH, while dissolved oxygen (DO) initially increased. Degradation of PAA reversed the pH drop, but caused a massive drop in DO, which could be remedied by aeration. As proof of concept, microcosms that were aerated and treated with 94.7 mg/L PAA sustained survival of tadpoles starting 48 h after treatment. Disinfecting aquatic environments using PAA could contribute to mitigating chytridiomycosis, while preserving at least some invertebrate diversity, but requires temporary removal of resident amphibians.