Panzootic fungal amphibians causes catastrophic and ongoing loss of biodiversity

Publicado em 28 março 2019

The fall of amphibians?

The rapid spread of the disease is a threat in our connected world. Sly fungus Batrachochytrium dendrobatidis was identified in amphibian populations about 20 years ago and caused species death and extinction on a global scale. Scheele et al. found that the fungus caused declines in the amphibian population everywhere, except its origin in Asia (see perspective of Greenberg and Palen). Most species and populations are still experiencing decline, but there is evidence of limited recovery in some species. The analysis also suggests some conditions that provide resistance.

Anthropogenic trade and development broke disruptive barriers, facilitating the spread of diseases threatening the Earth's biological diversity. We present a global, quantitative assessment of panzootic chytridiomycosis of amphibians, one of the most influential examples of disease spreading, and we demonstrate its role in at least 501 species of amphibians over the last half century, including 90 possible extinctions. The effects of chytridiomycosis were greatest in large anurans with limited range in humid climates in both Americas and Australia. The declines peaked in the 1980s, with only 12% of the rejected species showing signs of recovery, while 39% experiencing a continuous decline. There is a risk of further outbreaks of chytridiomycosis in new areas. Panzootic chytridiomycosis is the largest recorded loss of biodiversity associated with the disease.

Highly pathogenic wildlife diseases contribute to the sixth mass extinction of the Earth (1). One of them is chytridiomycosis, which caused mass extinction of amphibians all over the world (2. 3). Chytridiomycosis is caused by two species of fungi, Batrachochytrium dendrobatidis [Odkrytew1998r([Discoveredin1998([odkrytew1998r([discoveredin1998(4)]and B. salamandrivorans [Odkrytew2013r([Discoveredin2013([odkrytew2013r([discoveredin2013(5)]. Both Batrachochytrium species probably originated in Asia, and their recent spread was facilitated by people (5. 6). Twenty years after the discovery of chytridiomycosis, significant studies have provided insight into its epidemiology (2. 3. 7. 8), but there are still serious gaps in knowledge. First of all, the global extent of the decline of species associated with chytridiomycosis is unknown[see([See([widziec([see(2. 9) for initial assessment]. Secondly, although some regional drops are well studied, global spatial and temporal patterns of chytridiomycosis interactions remain poorly quantified. The third, ecological and vital traits have only been examined for some of the rejected species (10. 11). Finally, after the initial decreases, it is not known which part of the rejected species shows improvement, stabilizes at lower numbers or continues to decline. Below we present a global epidemiological analysis of the spatial and temporal extent of biodiversity loss of amphibians caused by chytridiomicosis.

We have conducted a comprehensive examination of evidence from a variety of sources, including the European Union Red List of Threatened Species (IUCN) (IUCN) (12), peer-reviewed literature and consultations with specialists in amphibians around the world (data S1). We classified species that were rejected into five categories of severity loss corresponding to a reduction in numbers. Drops of species were attributed to chytridiomycosis based on the diagnosis of an infection causing mortality in the wild or, if this was not possible, evidence consistent with the key epidemiological features of this disease. Most of the evidence is retrospective because many species have fallen prior to the discovery of chytridiomycosis (data S1).

Conservatively, chytridiomycosis has contributed to the decline of at least 501 species of amphibians (6.5% described amphibian species, Figures 1 and 2). This is the largest documented loss of biodiversity attributable to the pathogen and sites B. dendrobatidis among the most destructive invasive species, comparable to rodents (threatening 420 species) and cats (Felis catus) (threatens 430 species) (13). Losses associated with chytridiomycosis are an order of magnitude greater than other loud wild animal pathogens, such as white nose syndrome (Pseudogymnoascus destructans) in bats (six species) (14) or West Nile virus (flavivirus sp.) in birds (23 species) (15). Of the 501 rejected species of amphibians, 90 (18%) are confirmed or found to be extinct in the wild, and another 124 (25%) experience> 90% reduction in numbers (Figures 1 and 2). Drops of all species except one (Salamandra salamander under the influence B. salamandrivorans) have been assigned B. dendrobatidis.

Bar charts indicate the number (N) of rejected species, grouped by continental area and classified according to severity. Brazilian species are deleted separately from all other South American species (South America W); Mesoamerica covers Central America, Mexico and the Caribbean Islands; and Oceania includes Australia and New Zealand. There were no drops in Asia. n, total number of inheritances by region.[Prawadozdjec(zgodniezruchemwskazówekzegaraodgórypolewej)[Photocredits(clockwisefromtopleft)[Prawadozdjec(zgodniezruchemwskazówekzegaraodgórypolewej):[Photocredits(clockwisefromtopleft):Anaxyrus boreas, C. Brown, US Geological Survey; Atelopus varius, B.G.; Salamandra salamander, D. Descouens, Wikimedia Commons; Telmatobius sanborni, I.D.l.R; Cycloramphus boraceiensis, L.F.T .; Cardioglossa melanogaster, M.H .; and Pseudophryne corroboree, C. Doughty]

Each bar represents one species, and the color indicates the degree of its fall. Concentric circles indicate, from internal to external, order (Caudata or Anura), family and gender. Full names are given only for families and types that contain> 5 and> 2 species respectively; details for all taxa can be found in table S4. Within each taxonomic level, the sublevels are arranged alphabetically. Protruding rods indicate species for which there is evidence of recovery.[Kredytyfotograficzne(odlewejdoprawej)[Photocredits(leftToRight)[Kredytyfotograficzne(odlewejdoprawej):[Photocredits(lefttoright):Telmatobius bolivianus, I.D.l.R .; Atelopus zeteki, B.G.; and Craugastor crassidigitus, B.G.]

The decreases were proportional to the taxonomic abundance, and the Anurans had 93% of serious falls (89% of all amphibian species). Taxonomic grouping of inheritances was noted in anurans, with 45% of serious decreases and extinctions occurring in neotropical types Atelopus. Craugastor, and Telmatobius (Fig. 2) (16). Chytridiomycosis is fatal to the caecum (17), but there were no drops of cekilian due to illness, although the data is limited. Ability to B. dendrobatidis serious falls can be attributed to maintaining high pathogenicity (2. 18), a wide range of hosts (8), a high transmission rate within and between host species (2. 7) and durability in the host-reservoir species and environment (19). For many species, chytridiomycosis is the main driver of the decline, as exemplified by rapid mass mortality in an undisturbed environment (2). In other species, chytridiomycosis interacts with the loss of habitats, altered climatic conditions, and invasive species to exacerbate the deterioration of species (20).

Most amphibian falls have occurred in the tropics of Australia, Mesoamerica and South America (Figure 1), confirming the hypothesis that B. dendrobatidis has spread from Asia to the New World (6). Asia, Africa, Europe and North America have seen a significant decline in chitridiomyosis, despite widespread occurrence B. dendrobatidis (8). The relative lack of documented declines may reflect a lower knowledge of the amphibian population in Asia and Africa (3. 21), early introduction and potential co-evolution of amphibians and B. dendrobatidis in parts of Africa and the Americas[Eg([Eg([np([eg(22)], relatively recent appearance B. dendrobatidis in western and north-eastern Africa (6) or inappropriate conditions for chytridiomycosis. It is not known whether chytridiomycosis has contributed to the widespread decline in the number of amphibians recorded in North America and Europe in 1950-1960 (3. 21. 22) or the current enigmatic salamander falls in eastern North America. Although the number of new falls has now decreased (Figure 3), additional declines may occur if B. dendrobatidis or B. salamandrivorans are introduced into new areas, highly virulent lines are introduced into areas that currently have less virulent lines (6) and / or environmental changes previously change the stable pathogen-host dynamics (3).

(BEHIND) Declines to one year. Bars indicate the number of falls in a given year, depending on the degree of decline. In the case of species for which the exact year of decline is uncertain, the number shows the middle year of the uncertainty interval, as stated by the experts or inferred from the available data. (b) Accumulated drops. Curves indicate the total number of drops in each severity category of decline over time. In (A) and (B) arrows indicate the discovery of chytridiomycosis in 1998.

The decreases associated with chytridiomycosis peaked around the world in the 1980s, between one and two hundred years before the discovery of the disease (Figure 3 and Table S1), and coincided with an anecdotal decline in the number of amphibians in the 1990s (23). The second, smaller peak occurred at the beginning of the year 2000, associated with the increase in declines in Western South America (Fig. 3 and Fig. S1). Regional, time-dependent drop patterns are variable (Figure S1). For example, in some areas of South America and Australia, declines began in the late 1970s (2. 24), while in other areas declines started in 2000 (25). B. dendrobatidis is associated with ongoing decreases in 197 species assessed. Continuous drops after switching to the dynamics of the enzootic disease (19) may be due to the lack of effective defense of the host, maintaining high pathogenicity (18) and presence B. dendrobatidis in amphibian and non-amphibious tanks (7. 19).

We analyzed the characteristics of the host's life history and environmental conditions to understand why some species fell more than others, using polynomial logistic regression and taking into account the degree of proof that chytridiomycosis was associated with the fall of each species (Figure S2 and Table S2). Reduction in severity was greatest for species with a higher weight, occurring in regions that were constantly moist and strongly associated with multi-annual water habitats. These patterns are probably due to favorable environmental conditions B. dendrobatidis in humid regions (7), because the fungus dies after drying, as well as the general pattern of lengthening the time to maturity in large amphibians, resulting in a lower spawning potential to offset the mortality caused by chytridiomycosis (26). The decreases were less severe for species with large geographic and elevation ranges (Figure 4), potentially due to the greater chance of their range including unfavorable environmental conditions B. dendrobatidis (3) and / or bias information, because population extinction can be assessed with more certainty in species with limited range. Our results are consistent with previous studies that show that the risk of chytridiomycosis is related to the use of the host's aquatic environment, large body size and a narrow range of heights (10. 11).

(BEHIND) Decrease in relation to the geographical range. Each dot indicates the species, located randomly along the circumference of the circle with a radius equal to the log10 geographical range of the species in square kilometers. (b) Drop in relation to the reach of the hill. The horizontal bars, fields and vertical bars indicate the average, first and second quartiles and 95% of quantiles of height ranges in each fall severity category, respectively.

Interestingly, of the 292 survivors for whom population trends are known, 60 (20%) showed initial signs of recovery. However, recoveries generally represent a small increase in the size of individual populations, not a total recovery at the species level. Logistic regression showed that the probability of recuperation was lower for species that experienced newer or more serious falls, for species with high weight or night species, and for species found at higher altitudes (Figure S2 and Table S3). Keeping these predictors of recovery at their average value, the chance that the species will heal from a serious (> 90%) drop would be less than 1 in 10. The low probability of recovery for high-altitude species may be related to the appropriate climatic conditions for fungal durability, as well as limited communication with source populations and / or a longer host generation time (26). Some recovery may be supported by the choice of increased host immunity (18), while the management of co-existing threats could be facilitated by other recoveries (a promising way of intervention in terms of protection) (27). Unfortunately, the remaining 232 species did not show signs of recovery.

The unprecedented mortality of a single disease affecting the entire class of vertebrates underlines the risk of the spread of pathogens in a globalized world. World trade recreated functional Pangea for infectious diseases in wild animals, with far-reaching impact on biodiversity (this study), livestock (28) and human health (29). Effective biosecurity and immediate reduction of trade in wild animals are urgently needed to reduce the risk of pathogens spreading. Because the mitigation of chytridiomycosis in nature remains unproven (thirty) new research and intensive monitoring using emerging technologies are needed to identify species recovery mechanisms and to develop new mitigation measures for declining species.

References and comments

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S. N. Stuart, M. Hoffmann, J. S. Chanson, N. A. Cox, R. J. Berridge, P. Ramani, B. E. Young, Threatened amphibians of the world (Lynx Edicions, Barcelona, ??Spain; IUCN, Gland, Switzerland; Conservation International, Arlington, VA, 2008).

Thanks: We thank M. Arellano, E. Courtois, A. Cunningham, K. Murray, S. Ron, R. Puschendorf, J. Rowley and V. Vredenburg for discussions on the decline of amphibians. The comments of two anonymous reviewers greatly improved the manuscript. Financing: B.C.S. and D.B.L. were supported by the Australian National Environmental Science Program. L.B., L.F.S., T.A.K. and B.C.S. were supported by the Australian Research Council (subsidies FT100100375, LP110200240 and DP120100811), the NSW Environment and Heritage Office and the Taronga Conservation Science Initiative. S.C., W.B., A.M. and F.P. received support from the Flanders Research Foundation subsidies FWO3E001916 and FWO11ZK916N – 11ZK918N and a grant from the University in Ghent BOF16 / GOA / 024. S.C. was supported by the Flemish Research Foundation, awarding FWO16 / PDO / 019. A.A.A. was supported by the Conservation Leadership Program (0621310), Vicerrectoría de Investigaciones, Universidad de Pamplona-Colombia and Colciencias (1121-659-44242). T. C. was supported by coordination for the improvement of higher education staff. A.C. was supported by the Amazon Conservation Association, the Amphibian Specialist Group, the Disney Worldwide Conservation Fund, the Eppley Foundation, the Mohammed bin Zayed Species Conservation Fund, the NSF, the Rufford Small Grants Foundation and the Swiss National Foundation. I.D.l.R. was supported by the Spanish government (CGL2014-56160-P). M.C.F. was supported by NERC (NE / K014455 / 1), Leverhulme Trust (RPG-2014-273) and Morris Animal Foundation (D16ZO-022). S.V.F. he was supported by the USFWS Wildlife without Borders (96200-0-G228), AZA – Conservation Endowment Fund (08-836) and the Conservation International Critically Endangered Species Fund. P.F.Á. he was supported by a postdoctoral fellowship from the Mexican Research Council (CONACYT, 171465). T.W.J.G. was supported by NERC (NE / N009967 / 1 and NE / K012509 / 1). J.M.G. was supported by the Universidad San Francisco de Quito (grants for cooperation 11164 and 5447). M. H. he was supported by scholarships from the Elsa-Neumann Foundation and the German Academic Exchange (DAAD). CAM. he was supported by Atkinson's Sustainable Future Center and Vertebrate Genomics Center. G.P.-O. he was supported by DGAPA-UNAM and CONACYT while staying at the University of Otago in New Zealand. C.L.R.-Z. was supported by NSF (1660311). S.M.R. was supported by the CONACYT Problemas Nacionales grant (PDCPN 2015-721) and the UC Mexus-Conacy cooperative grant. C.S.-A. was supported by the Chilean National Fund for Science and Technology (Fondecyt No. 1181758). L.F.T. was supported by the São Paulo Research Foundation (FAPESP 2016 / 25358-3) and the National Council for Scientific and Technological Development (CNPq 300896 / 2016-6). J.V. was supported by NSF (DEB-1551488 and IOS-1603808). CW he was supported by the South African National Research Foundation. Author's contributions: B.C.S., F., L.B., L.F.S., A.M. go. developed studies. B.C.S. he compiled data and coordinated data collection. All authors brought ideas and data. S.C. carried out the analysis using data from B.C.S., F.P., A.M., C.N.F. and W.B. B.C.S., F.P., L.B., L.F.S., A.M., C.N.F. go. they wrote an article with the contribution of all authors. Competitive interests: The authors declare a lack of competitive interests. Availability of data and materials: All data is available in the manuscript or additional materials.