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Epidemic Mycoses Devastating Wild Animal Populations

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A special issue of Journal of Fungi (ISSN 2309-608X). This special issue belongs to the section "Fungal Pathogenesis and Disease Control".

Deadline for manuscript submissions: closed (15 July 2021) | Viewed by 36808

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Prof. Dr. Daniel Elad

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Guest Editor

Kimron Veterinary Institute, Israeli Ministry of Agriculture and Koret School of Veterinary Medicine, Hebrew University of Jerusalem, Rehovot, Israel
Interests: veterinary clinical bacteriology; veterinary clinical mycology
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

This Special Issue will review large-scale mycoses afflicting wild animal populations at scales that endanger the species’ survival and pose a significant threat to biodiversity. The overall aim of the SI is to present to the medical mycology community the various aspects of an important group of fungal infections with which it might be relatively unfamiliar. The mycoses to be included are the white-nose syndrome of bats, batrachomycosis of frogs and salamanders, snake fungal disease, and Fusarium spp. infections of sea turtles (additional suggestions for other mycoses that correspond to the above-mentioned criteria are welcome). Aspects to be reviewed for each disease are history, epidemiology, mycology, pathogenesis, pathology, and mitigation efforts. Where relevant, the possible anthropogenic influence on the introduction and spread of these mycoses as well as their economic and public health impact (i.e., spread of arthropod-borne diseases and damage to agriculture due to insects not consumed by bats) will be discussed.

Prof. Dr. Daniel Elad
Guest Editor

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Keywords

white nose syndrome
batrachomycosis
ophidiomycosis
fusariosis
bats
amphibians
snakes
Pseudogymnoascus destructans
Batrachochytrium dendrobatidis
Batrachochytrium salamandrivorans
Ophidiomyces ophiodiicola
Fusarium species
epidemiology
pathogenesis
pathology
mitigation

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Published Papers (9 papers)

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19 pages, 5440 KiB

Open AccessArticle

Beyond Sea Turtles: Fusarium keratoplasticum in Eggshells of Podocnemis unifilis, a Threatened Amazonian Freshwater Turtle

by Joaquina M. García-Martín, Jullie M. Sarmiento-Ramírez and Javier Diéguez-Uribeondo

J. Fungi 2021, 7(9), 742; https://doi.org/10.3390/jof7090742 - 9 Sep 2021

Cited by 9 | Viewed by 3306

Abstract

The endangered yellow-spotted river turtle (Podocnemis unifilis) has experienced a dramatic population decline in the Ecuadorian Amazonia, mainly due to overexploitation of its eggs. To reverse this trend, the Wildlife Conservation Society has developed a head-start program in Yasuní National Park since 2008, but the potential risk that microbes associated with its eggs might represent for hatching success has not been evaluated yet. Members of the Fusarium solani species complex (FSSC) are involved in egg failure in sea turtles under natural and hatchery conditions, but their role in infecting the eggs of P. unifilis is unknown. In this study, we collected eggshells of P. unifilis and obtained 50 fungal and bacterial isolates. Some potentially pathogenic fungi of the genera Fusarium, Penicillium and Rhizopus were identified based on molecular data. Most importantly, the sea turtle pathogenic species F. keratoplasticum not only was present, but it was the most frequently found. Conversely, we have also isolated other microorganisms, such as Pseudomonas or Phoma-like species, producing a wide spectrum of antifungal compounds that may have a protective role against fungal diseases. Our survey provides useful information on potential pathogens found in P. unifilis eggshells, upon which the success of conservation programs may depend. Full article

(This article belongs to the Special Issue Epidemic Mycoses Devastating Wild Animal Populations)

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15 pages, 1553 KiB

Open AccessArticle

Batrachochytrium salamandrivorans Threat to the Iberian Urodele Hotspot

by Jaime Bosch, An Martel, Jarrod Sopniewski, Barbora Thumsová, Cesar Ayres, Ben C. Scheele, Guillermo Velo-Antón and Frank Pasmans

J. Fungi 2021, 7(8), 644; https://doi.org/10.3390/jof7080644 - 7 Aug 2021

Cited by 11 | Viewed by 4242

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. Full article

(This article belongs to the Special Issue Epidemic Mycoses Devastating Wild Animal Populations)

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11 pages, 4935 KiB

Open AccessArticle

Distribution and Genetic Diversity of the Amphibian Chytrid in Japan

by Koichi Goka, Jun Yokoyama and Atsushi Tominaga

J. Fungi 2021, 7(7), 522; https://doi.org/10.3390/jof7070522 - 29 Jun 2021

Cited by 4 | Viewed by 3985

Abstract

While research on frog chytrid fungus Batrachochytrium dendrobatidis (Bd), an infectious disease that threatens amphibian diversity, continues to advance worldwide, little progress has been made in Japan since around 2010. The reason for this is, which we pointed out in 2009, that the origin of frog chytrid fungus may be in the East Asian region, including Japan based on the Bd ITS-DNA variation, and as few cases of mass mortality caused by this fungus have been observed in wild amphibian populations in Japan, the interest of the Japanese government and the general public in Bd has waned. However, we believe that organizing the data obtained so far in Japan and distributing the status of frog chytrid fungus in Japan to the world will provide useful insight for future risk management of this pathogen. We collected more than 5500 swab samples from wild amphibians throughout Japan from 2009 to 2010. Then, we investigated the infection status using the Nested-PCR method. We sequenced the obtained DNA samples and constructed a maximum-parsimony (MP) tree to clarify the phylogenetic diversity of Bd. We detected Bd infection in 11 (nine native and two alien) amphibian species in Japan and obtained 44 haplotypes of Bd ITS-DNA. The MP tree showed a high diversity of Bd strains in Japan, suggesting that some strains belong to Bd-GPL and Bd-Brazil. Except for local populations of the Japanese giant salamanders Andrias japonicus in Honshu Island and the sword tail newts Cynops ensicauda in Okinawa Island, the Bd infection prevalence in native amphibian species was very low. The alien bullfrog Aquarana catesbeiana had high Bd infection rates in all areas where they were sampled. No Bd infection was detected in other native amphibians in the areas where giant salamanders, sword tail newts, and bullfrogs were collected, suggesting that many native amphibians are resistant to Bd infection. The sword tail newt of Okinawa Island had both the highest infectious incidence and greatest number of haplotypes. The giant salamanders also showed relatively high infection prevalence, but the infected strains were limited to those specific to this species. These two Caudata species are endemic to a limited area of Japan, and it was thought that they may have been refugia for Bd, which had been distributed in Japan Islands for a long time. Full article

(This article belongs to the Special Issue Epidemic Mycoses Devastating Wild Animal Populations)

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14 pages, 885 KiB

Open AccessArticle

Soil Reservoir Dynamics of Ophidiomyces ophidiicola, the Causative Agent of Snake Fungal Disease

by Lewis J. Campbell, Joanna Burger, Robert T. Zappalorti, John F. Bunnell, Megan E. Winzeler, Daniel R. Taylor and Jeffrey M. Lorch

J. Fungi 2021, 7(6), 461; https://doi.org/10.3390/jof7060461 - 8 Jun 2021

Cited by 22 | Viewed by 4286

Abstract

Wildlife diseases pose an ever-growing threat to global biodiversity. Understanding how wildlife pathogens are distributed in the environment and the ability of pathogens to form environmental reservoirs is critical to understanding and predicting disease dynamics within host populations. Snake fungal disease (SFD) is an emerging conservation threat to North American snake populations. The causative agent, Ophidiomyces ophidiicola (Oo), is detectable in environmentally derived soils. However, little is known about the distribution of Oo in the environment and the persistence and growth of Oo in soils. Here, we use quantitative PCR to detect Oo in soil samples collected from five snake dens. We compare the detection rates between soils collected from within underground snake hibernacula and associated, adjacent topsoil samples. Additionally, we used microcosm growth assays to assess the growth of Oo in soils and investigate whether the detection and growth of Oo are related to abiotic parameters and microbial communities of soil samples. We found that Oo is significantly more likely to be detected in hibernaculum soils compared to topsoils. We also found that Oo was capable of growth in sterile soil, but no growth occurred in soils with an active microbial community. A number of fungal genera were more abundant in soils that did not permit growth of Oo, versus those that did. Our results suggest that soils may display a high degree of both general and specific suppression of Oo in the environment. Harnessing environmental suppression presents opportunities to mitigate the impacts of SFD in wild snake populations. Full article

(This article belongs to the Special Issue Epidemic Mycoses Devastating Wild Animal Populations)

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13 pages, 5788 KiB

Open AccessArticle

Application of Disinfectants for Environmental Control of a Lethal Amphibian Pathogen

by Leni Lammens, An Martel and Frank Pasmans

J. Fungi 2021, 7(6), 406; https://doi.org/10.3390/jof7060406 - 21 May 2021

Cited by 2 | Viewed by 3018

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. Full article

(This article belongs to the Special Issue Epidemic Mycoses Devastating Wild Animal Populations)

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12 pages, 496 KiB

Open AccessArticle

Dual Detection of the Chytrid Fungi Batrachochytrium spp. with an Enhanced Environmental DNA Approach

by David Lastra González, Vojtech Baláž, Jiří Vojar and Petr Chajma

J. Fungi 2021, 7(4), 258; https://doi.org/10.3390/jof7040258 - 30 Mar 2021

Cited by 10 | Viewed by 3729

Abstract

Environmental DNA (eDNA) is becoming an indispensable tool in biodiversity monitoring, including the monitoring of invasive species and pathogens. Aquatic chytrid fungi Batrachochytrium dendrobatidis (Bd) and B. salamandrivorans (Bsal) are major threats to amphibians. However, the use of eDNA for detecting these pathogens has not yet become widespread, due to technological and economic obstacles. Using the enhanced eDNA approach (a simple and cheap sampling protocol) and the universally accepted qPCR assay, we confirmed the presence of Bsal and Bd in previously identified sites in Spain, including four sites that were new for Bsal. The new approach was successfully tested in laboratory conditions using manufactured gene fragments (gBlocks) of the targeted DNA sequence. A comparison of storage methods showed that samples kept in ethanol had the best DNA yield. Our results showed that the number of DNA copies in the Internal Transcribed Spacer region was 120 copies per Bsal cell. Eradication of emerging diseases requires quick and cost-effective solutions. We therefore performed cost-efficiency analyses of standard animal swabbing, a previous eDNA approach, and our own approach. The procedure presented here was evaluated as the most cost-efficient. Our findings will help to disseminate information about efforts to prevent the spread of chytrid fungi. Full article

(This article belongs to the Special Issue Epidemic Mycoses Devastating Wild Animal Populations)

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22 pages, 4047 KiB

Open AccessArticle

Landscape Genetic Connectivity and Evidence for Recombination in the North American Population of the White-Nose Syndrome Pathogen, Pseudogymnoascus destructans

by Adrian Forsythe, Karen J. Vanderwolf and Jianping Xu

J. Fungi 2021, 7(3), 182; https://doi.org/10.3390/jof7030182 - 3 Mar 2021

Cited by 4 | Viewed by 2573

Abstract

White-Nose Syndrome is an ongoing fungal epizootic caused by epidermal infections of the fungus, Pseudogymnoascus destructans (P. destructans), affecting hibernating bat species in North America. Emerging early in 2006 in New York State, infections of P. destructans have spread to 38 US States and seven Canadian Provinces. Since then, clonal isolates of P. destructans have accumulated genotypic and phenotypic variations in North America. Using microsatellite and single nucleotide polymorphism markers, we investigated the population structure and genetic relationships among P. destructans isolates from diverse regions in North America to understand its pattern of spread, and to test hypotheses about factors that contribute to transmission. We found limited support for genetic isolation of P. destructans populations by geographic distance, and instead identified evidence for gene flow among geographic regions. Interestingly, allelic association tests revealed evidence for recombination in the North American P. destructans population. Our landscape genetic analyses revealed that the population structure of P. destructans in North America was significantly influenced by anthropogenic impacts on the landscape. Our results have important implications for understanding the mechanism(s) of P. destructans spread. Full article

(This article belongs to the Special Issue Epidemic Mycoses Devastating Wild Animal Populations)

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Review

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30 pages, 2519 KiB

Open AccessReview

Saprolegniosis in Amphibians: An Integrated Overview of a Fluffy Killer Disease

by Sara Costa and Isabel Lopes

J. Fungi 2022, 8(5), 537; https://doi.org/10.3390/jof8050537 - 22 May 2022

Cited by 4 | Viewed by 4152

Abstract

Amphibians constitute the class of vertebrates with the highest proportion of threatened species, with infectious diseases being considered among the greatest causes for their worldwide decline. Aquatic oomycetes, known as “water molds”, are fungus-like microorganisms that are ubiquitous in freshwater ecosystems and are capable of causing disease in a broad range of amphibian hosts. Various species of Achlya sp., Leptolegnia sp., Aphanomyces sp., and mainly, Saprolegnia sp., are responsible for mass die-offs in the early developmental stages of a wide range of amphibian populations through a disease known as saprolegniosis, aka, molding or a “Saprolegnia-like infection”. In this context, the main objective of the present review was to bring together updated information about saprolegniosis in amphibians to integrate existing knowledge, identify current knowledge gaps, and suggest future directions within the saprolegniosis–amphibian research field. Based on the available literature and data, an integrated and critical interpretation of the results is discussed. Furthermore, the occurrence of saprolegniosis in natural and laboratory contexts and the factors that influence both pathogen incidence and host susceptibility are also addressed. The focus of this work was the species Saprolegnia sp., due to its ecological importance on amphibian population dynamics and due to the fact that this is the most reported genera to be associated with saprolegniosis in amphibians. In addition, integrated emerging therapies, and their potential application to treat saprolegniosis in amphibians, were evaluated, and future actions are suggested. Full article

(This article belongs to the Special Issue Epidemic Mycoses Devastating Wild Animal Populations)

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24 pages, 2101 KiB

Open AccessReview

Immunological Aspects of Chytridiomycosis

by Laura F. Grogan, Josephine E. Humphries, Jacques Robert, Chantal M. Lanctôt, Catherine J. Nock, David A. Newell and Hamish I. McCallum

J. Fungi 2020, 6(4), 234; https://doi.org/10.3390/jof6040234 - 19 Oct 2020

Cited by 23 | Viewed by 6587

Abstract

Amphibians are currently the most threatened vertebrate class, with the disease chytridiomycosis being a major contributor to their global declines. Chytridiomycosis is a frequently fatal skin disease caused by the fungal pathogens Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal). The severity and extent of the impact of the infection caused by these pathogens across modern Amphibia are unprecedented in the history of vertebrate infectious diseases. The immune system of amphibians is thought to be largely similar to that of other jawed vertebrates, such as mammals. However, amphibian hosts are both ectothermic and water-dependent, which are characteristics favouring fungal proliferation. Although amphibians possess robust constitutive host defences, Bd/Bsal replicate within host cells once these defences have been breached. Intracellular fungal localisation may contribute to evasion of the induced innate immune response. Increasing evidence suggests that once the innate defences are surpassed, fungal virulence factors suppress the targeted adaptive immune responses whilst promoting an ineffectual inflammatory cascade, resulting in immunopathology and systemic metabolic disruption. Thus, although infections are contained within the integument, crucial homeostatic processes become compromised, leading to mortality. In this paper, we present an integrated synthesis of amphibian post-metamorphic immunological responses and the corresponding outcomes of infection with Bd, focusing on recent developments within the field and highlighting future directions. Full article

(This article belongs to the Special Issue Epidemic Mycoses Devastating Wild Animal Populations)

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