scholarly journals Disease driven extinction in the wild of the Kihansi spray toad (Nectophrynoides asperginis)

2019 ◽  
Author(s):  
C. Weldon ◽  
A. Channing ◽  
G. Misinzo ◽  
A.A. Cunningham

AbstractThe Kihansi spray toad, Nectophrynoides asperginis, became extinct in the wild despite population monitoring and conservation management of its habitat in the Kihansi gorge, Tanzania. Anecdotal evidence has indicated human induced habitat modification, predators, pesticides and disease as possible causes of a rapid population decline and the species extirpation. Here, we systematically investigate the role of disease in the extinction event of the wild toad population. The amphibian chytrid fungus, Batrachochytrium dendrobatidis, was detected in spray toads that died during the extinction event and subsequently in other amphibian species in Kihansi Gorge and the adjacent Udagaji Gorge, but not in any toads collected prior to this. Following the population decline, the remnant spray toad population gradually disappeared over a nine-month period. We demonstrate how demographic and behavioral attributes predisposed the spray toads to chytridiomycosis, due to B. dendrobatidis infection, and how epidemic disease could have been exacerbated by altered environmental conditions in the spray wetlands. Our results show that chytridiomycosis was the proximate cause of extinction in the wild of N. asperginis. This represents the first known case of extinction by disease of an amphibian species in Africa. A captive breeding program in the US and Tanzania ensures the survival of the species and a reintroduction program is underway. However, we caution that chytridiomycosis remains an existing threat that requires a comprehensive mitigation strategy before the desired conservation outcome of an established population of repatriated toads can be achieved.


2021 ◽  
Author(s):  
Thomas R Sewell ◽  
Lucy van Dorp ◽  
Pria Ghosh ◽  
Claudia Wierzbicki ◽  
Cristian Caroe ◽  
...  

Outbreaks of emerging infectious diseases are trained by local biotic and abiotic factors, with host declines occurring when conditions favour the pathogen. Extinction of the Tanzanian Kihansi spray toad (Nectophrynoides asperginis) in 2004 was contemporaneous with the construction of a dam, implicating habitat modification in the loss of this species. However, high burdens of a globally emerging infection, Batrachochytrium dendrobatidis (Bd) were synchronously observed implicating infectious disease in this toads extinction. Here, by shotgun sequencing skin DNA from archived toad mortalities and assembling chytrid mitogenomes, we prove this outbreak was caused by the BdCAPE lineage and not the panzootic lineage BdGPL that is widely associated with global amphibian extinctions. Molecular dating showed an invasion of BdCAPE across Southern Africa overlapping with the timing of the extinction event. However, post-outbreak surveillance of conspecific species inhabiting this mountainous region showed widespread infection by BdCAPE yet no signs of amphibian ill-health or species decline. Our findings show that despite efforts to mitigate the environmental impact caused by dams construction, invasion of the pathogen ultimately led to the loss of the Kihansi spray toad; a synergism between emerging infectious disease and environmental change that likely heralds wider negative impacts on biodiversity in the Anthropocene.



2017 ◽  
Vol 284 (1863) ◽  
pp. 20171176 ◽  
Author(s):  
Andrés Valenzuela-Sánchez ◽  
Benedikt R. Schmidt ◽  
David E. Uribe-Rivera ◽  
Francisco Costas ◽  
Andrew A. Cunningham ◽  
...  

The decline of wildlife populations due to emerging infectious disease often shows a common pattern: the parasite invades a naive host population, producing epidemic disease and a population decline, sometimes with extirpation. Some susceptible host populations can survive the epidemic phase and persist with endemic parasitic infection. Understanding host–parasite dynamics leading to persistence of the system is imperative to adequately inform conservation practice. Here we combine field data, statistical and mathematical modelling to explore the dynamics of the apparently stable Rhinoderma darwinii – Batrachochytrium dendrobatidis (Bd) system. Our results indicate that Bd-induced population extirpation may occur even in the absence of epidemics and where parasite prevalence is relatively low. These empirical findings are consistent with previous theoretical predictions showing that highly pathogenic parasites are able to regulate host populations even at extremely low prevalence, highlighting that disease threats should be investigated as a cause of population declines even in the absence of an overt increase in mortality.



2018 ◽  
Vol 27 (Supplement) ◽  
pp. 81-90
Author(s):  
A.A. Cunningham

The unexplained decline of amphibian populations across the world was first recognised in the late 20th century. When investigated, most of these “enigmatic” declines have been shown to be due to one of two types of infectious disease: ranavirosis caused by infection with FV3-like ranavirus or with common midwife toad virus, or chytridiomycosis caused by infection with Batrachochytrium dendrobatidis or B. salamandrivorans. In all cases examined, infection has been via the human-mediated introduction of the pathogen to a species or population in which it has not naturally co-evolved. While ranaviruses and B. salamandrivorans have caused regionally localised amphibian population declines in Europe, the chytrid fungus, B. dendrobatidis, has caused catastrophic multi-species amphibian population declines and species extinctions globally. These diseases have already caused the loss of amphibian biodiversity, and over 40% of known amphibian species are threatened with extinction. If this biodiversity loss is to be halted, it is imperative that regulations are put in place – and enforced – to prevent the spread of known and yet-to-be discovered amphibian pathogens. Also, it is incumbent on those who keep or study amphibians to take measures to minimise the risk of disease spread, including from captive animals to those in the wild.



2013 ◽  
Vol 82 (4) ◽  
pp. 351-355 ◽  
Author(s):  
Vojtech Baláž ◽  
Martina Kubečková ◽  
Petr Civiš ◽  
Roman Rozínek ◽  
Jiří Vojar

A parasitic fungus,Batrachochytrium dendrobatidisis now recognised as an important factor in the amphibian biodiversity crisis. Toad species of the genusBufoare among those susceptible to infection by the pathogen in Europe. The aim of this study was to observe the presence and impact of infection in adults of two toad species collected for captive breeding. The total number of animals included in the study was 162, but only subsets were used for sampling at different occasions (35 specimens in the initial sampling in summer 2011, 48 post hibernation during winter 2011, and 31 in summer 2012, after all toads in captivity were treated with itraconazole). We performed TaqMan real-time quantification PCR to detect and quantify the pathogen. We found that a large infection load was linked to mortality in a single adult green toad (Bufo viridis). However, low infection loads observed in fiveB. viridisand five natterjack toads (B. calamita)were lost over time, with no apparent adverse effect. Intraconazole treated animals were all clear of infection. As infection in these two toad species either led to mortality or recovery, it seems unlikely they could act as permanent carriers ofB. dendrobatidisand therefore persistence of the pathogen is likely maintained by different host species. This is the first study to date that has detected infection and observed its impact and persistence in wild-infected toads in Europe.



2016 ◽  
Vol 37 (4) ◽  
pp. 345-357 ◽  
Author(s):  
Adeline Loyau ◽  
Jérémie H. Cornuau ◽  
Frances C. Clare ◽  
Dirk S. Schmeller

Itraconazole is the most widely used treatment against Batrachochytrium dendrobatidis (Bd), the fungal pathogen causing chytridiomycosis, a proximate cause of amphibian declines. Several side effects of itraconazole treatment, ranging in severity from depigmentation to death have been reported in different amphibian species and life stages, and these side effects were observed at commonly used dosages of itraconazole. However, no studies have investigated side-effects of itraconazole in conjunction with environmental stress. Post-metamorphic midwife toads (Alytes obstetricans) that were treated with itraconazole and subsequently exposed to a cold stress (exposure to 4°C cold water) had higher mortality rates compared to untreated individuals. Moreover, adults of booroolong frogs (Litoria booroolongensis) treated with itraconazole had a higher probability to become infected when subsequently exposed to Bd. Our results suggest that a post-metamorphosis itraconazole treatment of infected midwife toads combined with a subsequent release into the wild may be an ineffective disease mitigation strategy, as the cold stress during hibernation and/or exposure to Bd in the wild may reduce the hibernation emergence rate of treated individuals in this species.



2021 ◽  
Vol 45 ◽  
pp. 225-235
Author(s):  
PC Gardner ◽  
B Goossens ◽  
SBA Bakar ◽  
MW Bruford

Widespread and unregulated hunting of ungulates in Southeast Asia is resulting in population declines and localised extinctions. Increased access to previously remote tropical forest following logging and changes in land-use facilitates hunting of elusive wild cattle in Borneo, which preferentially select secluded habitat. We collated the first population parameters for the Endangered Bornean banteng Bos javanicus lowi and developed population models to simulate the effect of different hunting offtake rates on survival and the recovery of the population using reintroduced captive-bred individuals. Our findings suggest that the banteng population in Sabah is geographically divided into 4 management units based on connectivity: the Northeast, Sipitang (West), Central and Southeast, which all require active management to prevent further population decline and local extinction. With only 1% offtake, population growth ceased in the Northeast and Sipitang. In the Southeast and Central units, growth ceased at 2 and 4% offtake, respectively. Extinction was estimated at 21-39 yr when offtake was 5%, occurring first in Sipitang and last in the Central unit. Supplementing the population with captive-bred individuals suggested that inbreeding was likely to limit population growth if using ≤20 founder individuals. Translocating 2 individuals for a 10 yr period, starting after 20 yr of captive breeding resulted in a faster population recovery over 100 yr and a lower extinction probability. Our results suggest that shielding the population against further losses from hunting will be key to their survival in the wild, provided that active management in the form of captive breeding is developed in the interim.



PeerJ ◽  
2017 ◽  
Vol 5 ◽  
pp. e3594 ◽  
Author(s):  
Sandra V. Flechas ◽  
Ailin Blasco-Zúñiga ◽  
Andrés Merino-Viteri ◽  
Valeria Ramírez-Castañeda ◽  
Miryan Rivera ◽  
...  

Many amphibian species are at risk of extinction in their natural habitats due to the presence of the fungal pathogen Batrachochytrium dendrobatidis (Bd). For the most highly endangered species, captive assurance colonies have been established as an emergency measure to avoid extinction. Experimental research has suggested that symbiotic microorganisms in the skin of amphibians play a key role against Bd. While previous studies have addressed the effects of captivity on the cutaneous bacterial community, it remains poorly studied whether and how captive conditions affect the proportion of beneficial bacteria or their anti-Bd performance on amphibian hosts. In this study we sampled three amphibian species of the highly threatened genus, Atelopus, that remain in the wild but are also part of ex situ breeding programs in Colombia and Ecuador. Our goals were to (1) estimate the diversity of culturable bacterial assemblages in these three species of Atelopus, (2) describe the effect of captivity on the composition of skin microbiota, and (3) examine how captivity affects the bacterial ability to inhibit Bd growth. Using challenge assays we tested each bacterial isolate against Bd, and through sequencing of the 16S rRNA gene, we identified species from thirteen genera of bacteria that inhibited Bd growth. Surprisingly, we did not detect a reduction in skin bacteria diversity in captive frogs. Moreover, we found that frogs in captivity still harbor bacteria with anti-Bd activity. Although the scope of our study is limited to a few species and to the culturable portion of the bacterial community, our results indicate that captive programs do not necessarily change bacterial communities of the toad skins in a way that impedes the control of Bd in case of an eventual reintroduction.



2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Surya Prasad Sharma ◽  
Mirza Ghazanfarullah Ghazi ◽  
Suyash Katdare ◽  
Niladri Dasgupta ◽  
Samrat Mondol ◽  
...  

AbstractThe gharial (Gavialis gangeticus) is a critically endangered crocodylian, endemic to the Indian subcontinent. The species has experienced severe population decline during the twentieth century owing to habitat loss, poaching, and mortalities in passive fishing. Its extant populations have largely recovered through translocation programmes initiated in 1975. Understanding the genetic status of these populations is crucial for evaluating the effectiveness of the ongoing conservation efforts. This study assessed the genetic diversity, population structure, and evidence of genetic bottlenecks of the two managed populations inhabiting the Chambal and Girwa Rivers, which hold nearly 80% of the global gharial populations. We used seven polymorphic nuclear microsatellite loci and a 520 bp partial fragment of the mitochondrial control region (CR). The overall mean allelic richness (Ar) was 2.80 ± 0.40, and the observed (Ho) and expected (He) heterozygosities were 0.40 ± 0.05 and 0.39 ± 0.05, respectively. We observed low levels of genetic differentiation between populations (FST = 0.039, P < 0.05; G’ST = 0.058, P < 0.05 Jost’s D = 0.016, P < 0.05). The bottleneck analysis using the M ratio (Chambal = 0.31 ± 0.06; Girwa = 0.41 ± 0.12) suggested the presence of a genetic bottleneck in both populations. The mitochondrial CR also showed a low level of variation, with two haplotypes observed in the Girwa population. This study highlights the low level of genetic diversity in the two largest managed gharial populations in the wild. Hence, it is recommended to assess the genetic status of extant wild and captive gharial populations for planning future translocation programmes to ensure long-term survival in the wild.



PeerJ ◽  
2020 ◽  
Vol 8 ◽  
pp. e9763
Author(s):  
Mizraim Olivares-Miranda ◽  
Vance T. Vredenburg ◽  
Julio C. García-Sánchez ◽  
Allison Q. Byrne ◽  
Erica B. Rosenblum ◽  
...  

The fungal pathogen Batrachochytrium dendrobatidis (Bd) is implicated in global mass die-offs and declines in amphibians. In Mesoamerica, the Bd epidemic wave hypothesis is supported by detection of Bd in historic museum specimens collected over the last century, yet the timing and impact of the early stages of the wave remain poorly understood. Chiropterotriton magnipes, the only obligate troglodytic Neotropical salamander, was abundant in its small range in the decade following its description in 1965, but subsequently disappeared from known localities and was not seen for 34 years. Its decline is roughly coincident with that of other populations of Neotropical salamanders associated with the invasion and spread of Bd. To determine the presence and infection intensity of Bd on C. magnipes and sympatric amphibian species (which are also Bd hosts), we used a noninvasive sampling technique and qPCR assay to detect Bd on museum specimens of C. magnipes collected from 1952 to 2012, and from extant populations of C. magnipes and sympatric species of amphibians. We also tested for the presence of the recently discovered Batrachochytrium salamandivorans (Bsal), another fungal chytridiomycete pathogen of salamanders, using a similar technique specific for Bsal. We did not detect Bd in populations of C. magnipes before 1969, while Bd was detected at low to moderate prevalence just prior to and during declines. This pattern is consistent with Bd-caused epizootics followed by host declines and extirpations described in other hosts. We did not detect Bsal in any extant population of C. magnipes. We obtained one of the earliest positive records of the fungus to date in Latin America, providing additional historical evidence consistent with the Bd epidemic wave hypothesis. Genotyping results show that at least one population is currently infected with the Global Panzootic Lineage of Bd, but our genotyping of the historical positive samples was unsuccessful. The lack of large samples from some years and the difficulty in genotyping historical Bd samples illustrate some of the difficulties inherent in assigning causality to historical amphibian declines. These data also provide an important historical baseline for actions to preserve the few known remaining populations of C. magnipes.



2021 ◽  
Vol 4 ◽  
Author(s):  
Omneya Osman ◽  
Johan Andersson ◽  
Tomas Larsson ◽  
Mats Töpel ◽  
Alexander Eiler

National monitoring programs provide the basis for evaluating the integrity of ecosystems, their responses to disturbances, and the success of actions taken to conserve or recover biodiversity. In this study, we successfully established a national program for the invasive chytrid fungus Batrachochytrium dendrobatidis (Bd) based on dual TaqMan assays. Amphibian diversity based on metabarcoding of the mitochondrial 12S rRNA gene was also performed. Assays were optimized for sensitive detection of target species from a wide range of amphibian ponds with variable potential of inhibitions for eDNA based detection. An amphibian mock community of 5 species was used to validate the metabarcoding approach while internal standards were used in the case of the dual TaqMan assays. First sampling of over 170 ponds in Norway resulted in Bd detection in 12 environmental samples and one swab sample taken over multiple years indicating the establishment of Bd in Norway. Five amphibian species Bufo bufo, Lissotriton vulgaris, Triturus cristatus, Rana arvalis and Rana temporaria as predicted from data in long-term citizen science reporting systems were widely detected in the collected eDNA samples. Our large scale-monitoring program indicates a low risk of a Bd outbreak and amphibian decline caused by chytridiomycosis but continued monitoring is recommended in the future. These findings indicate that eDNA is an effective method to detect invasive species, and to monitor endangered amphibian species. Still, several shortcomings (such as PCR inhibitors and sample volume) were identified that need to be addressed to improve eDNA-based monitoring at the national level.



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