Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity
The demise of amphibians?
Rapid spread of disease is a hazard in our interconnected world. The chytrid fungus Batrachochytrium dendrobatidis was identified in amphibian populations about 20 years ago and has caused death and species extinction at a global scale. Scheele et al. found that the fungus has caused declines in amphibian populations everywhere except at its origin in Asia (see the Perspective by Greenberg and Palen). A majority of species and populations are still experiencing decline, but there is evidence of limited recovery in some species. The analysis also suggests some conditions that predict resilience.
Abstract
Anthropogenic trade and development have broken down dispersal barriers, facilitating the spread of diseases that threaten Earth’s biodiversity. We present a global, quantitative assessment of the amphibian chytridiomycosis panzootic, one of the most impactful examples of disease spread, and demonstrate its role in the decline of at least 501 amphibian species over the past half-century, including 90 presumed extinctions. The effects of chytridiomycosis have been greatest in large-bodied, range-restricted anurans in wet climates in the Americas and Australia. Declines peaked in the 1980s, and only 12% of declined species show signs of recovery, whereas 39% are experiencing ongoing decline. There is risk of further chytridiomycosis outbreaks in new areas. The chytridiomycosis panzootic represents the greatest recorded loss of biodiversity attributable to a disease.
Get full access to this article
View all available purchase options and get full access to this article.
Already a Subscriber?Sign In
Supplementary Material
Summary
Materials and Methods
Figs. S1 and S2
Tables S1 to S4
Data S1
Resources
Correction (23 March 2020): The Supplementary Materials for this article were updated on 23 March 2020. Minor amendments have been made to referencing and supporting details in Data S1. Additional references are now included in Data S1. The reference list that appears in the HTML version of the paper and the Supplementary Materials file has been updated to include sources cited in the main text, Supplementary Materials, and Data S1. The main text and results remain unaltered.
References and Notes
1
M. C. Fisher, D. A. Henk, C. J. Briggs, J. S. Brownstein, L. C. Madoff, S. L. McCraw, S. J. Gurr, Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186–194 (2012).
2
L. F. Skerratt, L. Berger, R. Speare, S. Cashins, K. R. McDonald, A. D. Phillott, H. B. Hines, N. Kenyon, Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4, 125–134 (2007).
3
K. R. Lips, Overview of chytrid emergence and impacts on amphibians. Philos. Trans. R. Soc. Lond. B Biol. Sci. 371, 20150465 (2016).
4
L. Berger, R. Speare, P. Daszak, D. E. Green, A. A. Cunningham, C. L. Goggin, R. Slocombe, M. A. Ragan, A. D. Hyatt, K. R. McDonald, H. B. Hines, K. R. Lips, G. Marantelli, H. Parkes, Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc. Natl. Acad. Sci. U.S.A. 95, 9031–9036 (1998).
5
A. Martel, M. Blooi, C. Adriaensen, P. Van Rooij, W. Beukema, M. C. Fisher, R. A. Farrer, B. R. Schmidt, U. Tobler, K. Goka, K. R. Lips, C. Muletz, K. R. Zamudio, J. Bosch, S. Lötters, E. Wombwell, T. W. J. Garner, A. A. Cunningham, A. Spitzen-van der Sluijs, S. Salvidio, R. Ducatelle, K. Nishikawa, T. T. Nguyen, J. E. Kolby, I. Van Bocxlaer, F. Bossuyt, F. Pasmans, Recent introduction of a chytrid fungus endangers Western Palearctic salamanders. Science 346, 630–631 (2014).
6
S. J. O’Hanlon, A. Rieux, R. A. Farrer, G. M. Rosa, B. Waldman, A. Bataille, T. A. Kosch, K. A. Murray, B. Brankovics, M. Fumagalli, M. D. Martin, N. Wales, M. Alvarado-Rybak, K. A. Bates, L. Berger, S. Böll, L. Brookes, F. Clare, E. A. Courtois, A. A. Cunningham, T. M. Doherty-Bone, P. Ghosh, D. J. Gower, W. E. Hintz, J. Höglund, T. S. Jenkinson, C.-F. Lin, A. Laurila, A. Loyau, A. Martel, S. Meurling, C. Miaud, P. Minting, F. Pasmans, D. S. Schmeller, B. R. Schmidt, J. M. G. Shelton, L. F. Skerratt, F. Smith, C. Soto-Azat, M. Spagnoletti, G. Tessa, L. F. Toledo, A. Valenzuela-Sánchez, R. Verster, J. Vörös, R. J. Webb, C. Wierzbicki, E. Wombwell, K. R. Zamudio, D. M. Aanensen, T. Y. James, M. T. P. Gilbert, C. Weldon, J. Bosch, F. Balloux, T. W. J. Garner, M. C. Fisher, Recent Asian origin of chytrid fungi causing global amphibian declines. Science 360, 621–627 (2018).
7
T. Y. James, L. F. Toledo, D. Rödder, D. da Silva Leite, A. M. Belasen, C. M. Betancourt-Román, T. S. Jenkinson, C. Soto-Azat, C. Lambertini, A. V. Longo, J. Ruggeri, J. P. Collins, P. A. Burrowes, K. R. Lips, K. R. Zamudio, J. E. Longcore, Disentangling host, pathogen, and environmental determinants of a recently emerged wildlife disease: Lessons from the first 15 years of amphibian chytridiomycosis research. Ecol. Evol. 5, 4079–4097 (2015).
8
D. H. Olson, D. M. Aanensen, K. L. Ronnenberg, C. I. Powell, S. F. Walker, J. Bielby, T. W. J. Garner, G. Weaver, M. C. Fisher; Bd Mapping Group, Mapping the global emergence of Batrachochytrium dendrobatidis, the amphibian chytrid fungus. PLOS ONE 8, e56802 (2013).
9
S. N. Stuart, J. S. Chanson, N. A. Cox, B. E. Young, A. S. L. Rodrigues, D. L. Fischman, R. W. Waller, Status and trends of amphibian declines and extinctions worldwide. Science 306, 1783–1786 (2004).
10
J. Bielby, N. Cooper, A. A. Cunningham, T. W. J. Garner, A. Purvis, Predicting susceptibility to future declines in the world’s frogs. Conserv. Lett. 1, 82–90 (2008).
11
K. R. Lips, J. D. Reeve, L. R. Witters, Ecological traits predicting amphibian population declines in Central America. Conserv. Biol. 17, 1078–1088 (2003).
12
The IUCN Red List of Threatened Species, Version 2017-3 (IUCN Species Survival Commission, Gland, Switzerland); www.iucnredlist.org.
13
T. S. Doherty, A. S. Glen, D. G. Nimmo, E. G. Ritchie, C. R. Dickman, Invasive predators and global biodiversity loss. Proc. Natl. Acad. Sci. U.S.A. 113, 11261–11265 (2016).
14
W. E. Thogmartin, C. A. Sanders-Reed, J. A. Szymanski, P. C. McKann, L. Pruitt, R. A. King, M. C. Runge, R. E. Russell, White-nose syndrome is likely to extirpate the endangered Indiana bat over large parts of its range. Biol. Conserv. 160, 162–172 (2013).
15
T. L. George, R. J. Harrigan, J. A. LaManna, D. F. DeSante, J. F. Saracco, T. B. Smith, Persistent impacts of West Nile virus on North American bird populations. Proc. Natl. Acad. Sci. U.S.A. 112, 14290–14294 (2015).
16
E. La Marca, K. R. Lips, S. Lotters, R. Puschendorf, R. Ibanez, J. V. Rueda-Almonacid, R. Schulte, C. Marty, F. Castro, J. Manzanilla-Puppo, J. E. Garcia-Perez, F. Bolanos, G. Chaves, J. A. Pounds, E. Toral, B. E. Young, Catastrophic population declines and extinctions in neotropical harlequin frogs (Bufonidae: Atelopus). Biotropica 37, 190–201 (2005).
17
D. J. Gower, T. Doherty-Bone, S. P. Loader, M. Wilkinson, M. T. Kouete, B. Tapley, F. Orton, O. Z. Daniel, F. Wynne, E. Flach, H. Müller, M. Menegon, I. Stephen, R. K. Browne, M. C. Fisher, A. A. Cunningham, T. W. J. Garner, Batrachochytrium dendrobatidis infection and lethal chytridiomycosis in caecilian amphibians (Gymnophiona). EcoHealth 10, 173–183 (2013).
18
J. Voyles, D. C. Woodhams, V. Saenz, A. Q. Byrne, R. Perez, G. Rios-Sotelo, M. J. Ryan, M. C. Bletz, F. A. Sobell, S. McLetchie, L. Reinert, E. B. Rosenblum, L. A. Rollins-Smith, R. Ibáñez, J. M. Ray, E. J. Griffith, H. Ross, C. L. Richards-Zawacki, Shifts in disease dynamics in a tropical amphibian assemblage are not due to pathogen attenuation. Science 359, 1517–1519 (2018).
19
A. Valenzuela-Sánchez, B. R. Schmidt, D. E. Uribe-Rivera, F. Costas, A. A. Cunningham, C. Soto-Azat, Cryptic disease-induced mortality may cause host extinction in an apparently stable host-parasite system. Proc. Biol. Sci. 284, 20171176 (2017).
20
D. B. Wake, V. T. Vredenburg, Colloquium paper: Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proc. Natl. Acad. Sci. U.S.A. 105 (suppl. 1), 11466–11473 (2008).
21
J. E. Houlahan, C. S. Findlay, B. R. Schmidt, A. H. Meyer, S. L. Kuzmin, Quantitative evidence for global amphibian population declines. Nature 404, 752–755 (2000).
22
B. L. Talley, C. R. Muletz, V. T. Vredenburg, R. C. Fleischer, K. R. Lips, A century of Batrachochytrium dendrobatidis in Illinois amphibians (1888–1989). Biol. Conserv. 182, 254–261 (2015).
23
D. B. Wake, Declining amphibian populations. Science 253, 860–860 (1991).
24
K. R. Lips, J. Diffendorfer, J. R. Mendelson III, M. W. Sears, Riding the wave: Reconciling the roles of disease and climate change in amphibian declines. PLOS Biol. 6, e72 (2008).
25
A. Catenazzi, E. Lehr, L. O. Rodriguez, V. T. Vredenburg, Batrachochytrium dendrobatidis and the collapse of anuran species richness and abundance in the Upper Manu National Park, Southeastern Peru. Conserv. Biol. 25, 382–391 (2011).
26
C. Morrison, J. M. Hero, Geographic variation in life-history characteristics of amphibians: A review. J. Anim. Ecol. 72, 270–279 (2003).
27
R. A. Knapp, G. M. Fellers, P. M. Kleeman, D. A. W. Miller, V. T. Vredenburg, E. B. Rosenblum, C. J. Briggs, Large-scale recovery of an endangered amphibian despite ongoing exposure to multiple stressors. Proc. Natl. Acad. Sci. U.S.A. 113, 11889–11894 (2016).
28
A. K. Wiethoelter, D. Beltrán-Alcrudo, R. Kock, S. M. Mor, Global trends in infectious diseases at the wildlife-livestock interface. Proc. Natl. Acad. Sci. U.S.A. 112, 9662–9667 (2015).
29
K. J. Olival, P. R. Hosseini, C. Zambrana-Torrelio, N. Ross, T. L. Bogich, P. Daszak, Host and viral traits predict zoonotic spillover from mammals. Nature 546, 646–650 (2017).
30
T. W. Garner, B. R. Schmidt, A. Martel, F. Pasmans, E. Muths, A. A. Cunningham, C. Weldon, M. C. Fisher, J. Bosch, Mitigating amphibian chytridiomycoses in nature. Philos. Trans. R. Soc. Lond. B Biol. Sci. 371, 20160207 (2016).
31
J. E. Longcore, A. P. Pessier, D. K. Nichols, Batrochochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia 91, 219–227 (1999).
32
B. C. Scheele, L. F. Skerratt, L. F. Grogan, D. A. Hunter, N. Clemann, M. McFadden, D. Newell, C. J. Hoskin, G. R. Gillespie, G. W. Heard, L. Brannelly, A. A. Roberts, L. Berger, After the epidemic: Ongoing declines, stabilizations and recoveries in amphibians afflicted by chytridiomycosis. Biol. Conserv. 206, 37–46 (2017).
33
I. Dohoo, S. Martin, H. Stryhn, Veterinary Epidemiologic Research (VER Inc., Charlottetown, Canada, ed. 2, 2009).
34
A. J. Crawford, K. R. Lips, E. Bermingham, Epidemic disease decimates amphibian abundance, species diversity, and evolutionary history in the highlands of central Panama. Proc. Natl. Acad. Sci. U.S.A. 107, 13777–13782 (2010).
35
The IUCN Red List of Threatened Species, Version 2016-1 (IUCN Species Survival Commission, Gland, Switzerland); www.iucnredlist.org.
36
A. Purvis, J. L. Gittleman, G. Cowlishaw, G. M. Mace, Predicting extinction risk in declining species. Proc. Biol. Sci. 267, 1947–1952 (2000).
37
K. A. Murray, D. Rosauer, H. McCallum, L. F. Skerratt, Integrating species traits with extrinsic threats: Closing the gap between predicting and preventing species declines. Proc. Biol. Sci. 278, 1515–1523 (2011).
38
K. A. Murray, R. W. R. Retallick, R. Puschendorf, L. F. Skerratt, D. Rosauer, H. I. McCallum, L. Berger, R. Speare, J. VanDerWal, Assessing spatial patterns of disease risk to biodiversity: Implications for the management of the amphibian pathogen, Batrachochytrium dendrobatidis. J. Appl. Ecol. 48, 163–173 (2011).
39
R. Puschendorf, A. C. Carnaval, J. VanDerWal, H. Zumbado-Ulate, G. Chaves, F. Bolaños, R. A. Alford, Distribution models for the amphibian chytrid Batrachochytrium dendrobatidis in Costa Rica: Proposing climatic refuges as a conservation tool. Divers. Distrib. 15, 401–408 (2009).
40
M. Plummer, in Proceedings of the 3rd International Workshop on Distributed Statistical Computing (DSC 2003), K. Hornik, F. Leisch, Eds. (Vienna, Austria, 2003).
41
S. E. Fick, R. J. Hijmans, WorldClim 2: New 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315 (2017).
42
B. F. Oliveira, V. A. São-Pedro, G. Santos-Barrera, C. Penone, G. C. Costa, AmphiBIO, a global database for amphibian ecological traits. Sci. Data 4, 170123 (2017).
43
K. M. Kriger, J. M. Hero, The chytrid fungus Batrachochytrium dendrobatidis is non‐randomly distributed across amphibian breeding habitats. Divers. Distrib. 13, 781–788 (2007).
44
AmphibiaWeb (University of California, Berkeley, 2017); https://amphibiaweb.org/.
45
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).
46
J. J. L. Rowley, R. A. Alford, Hot bodies protect amphibians against chytrid infection in nature. Sci. Rep. 3, 1515 (2013).
47
C. L. Richards-Zawacki, Thermoregulatory behaviour affects prevalence of chytrid fungal infection in a wild population of Panamanian golden frogs. Proc. Biol. Sci. 277, 519–528 (2010).
48
P. C. Eterovick, A. C. O. de Queiroz Carnaval, D. M. Borges-Nojosa, D. L. Silvano, M. V. Segalla, I. Sazima, Amphibian declines in Brazil: An overview. Biotropica 37, 166–179 (2005).
49
T. Carvalho, C. G. Becker, L. F. Toledo, Historical amphibian declines and extinctions in Brazil linked to chytridiomycosis. Proc. R. Soc. London Ser. B 284, 20162254 (2017).
50
K. R. McDonald, R. A. Alford, “Review of declining frogs in northern Queensland” in Declines and Disappearances of Australian Frogs, A. Campbell, Ed. (Environment Australia, Canberra, 1999), pp. 14–22.
51
L. Berger, R. Speare, A. Hyatt, “Chytrid fungi and amphibian declines: overview, implications and future directions” in Declines and Disappearances of Australian Frogs, A. Campbell, Ed. (Environment Australia, Canberra, 1999), pp. 23–33.
52
Ingram, G.J. and K.R. McDonald. “An update on the decline of Queensland’s frogs” in Herpetology in Australia: A Diverse Discipline, D. Lunney, D. Ayers, Eds. (Transactions of the Royal Zoological Society of New South Wales, Surrey Beatty & Sons, 1993), pp. 297–303.
53
G. Gillespie, H. Hines, “Status of temperate riverine frogs in south-eastern Australia” in Declines and Disappearances of Australian Frogs, A. Campbell, Ed. (Environment Australia, Canberra, 1999), pp. 109–130.
54
D. Newell, R. Goldingay, “Conserving reptiles and frogs in the forests of New South Wales” in Conservation of Australia’s Forest Fauna, D. Lunney, Ed. (Royal Zoological Society of New South Wales, ed. 2, 2004).
55
L.M. Enrique et al., Adenomera andreae. The IUCN Red List of Threatened Species 2004: e.T56304A11453385 (2004); .
56
W. R. Heyer, A. S. Rand, C. A. G. da Cruz, O. L. Peixoto, Decimations, extinctions, and colonizations of frog populations in southeast Brazil and their evolutionary implications. Biotropica 20, 230–235 (1988).
57
M. Hirschfeld, D. C. Blackburn, T. M. Doherty-Bone, L. N. Gonwouo, S. Ghose, M.-O. Rödel, Dramatic declines of montane frogs in a Central African biodiversity hotspot. PLOS ONE 11, e0155129 (2016).
58
J. A. Pounds, M. P. L. Fogden, J. M. Savage, G. C. Gorman, Tests of null models for amphibian declines on a tropical mountain. Conserv. Biol. 11, 1307–1322 (1997).
59
R. Puschendorf, F. Bolanos, G. Chaves, The amphibian chytrid fungus along an altitudinal transect before the first reported declines in Costa Rica. Biol. Conserv. 132, 136–142 (2006).
60
K. R. Lips, F. Brem, R. Brenes, J. D. Reeve, R. A. Alford, J. Voyles, C. Carey, L. Livo, A. P. Pessier, J. P. Collins, Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proc. Natl. Acad. Sci. U.S.A. 103, 3165–3170 (2006).
61
R. García-Roa et al., First record of Batrachochytrium dendrobatidis in Nicaragua. Herpetol. J. 24, 65–68 (2014).
62
A. R. Ellison, T. Tunstall, G. V. DiRenzo, M. C. Hughey, E. A. Rebollar, L. K. Belden, R. N. Harris, R. Ibáñez, K. R. Lips, K. R. Zamudio, More than skin deep: Functional genomic basis for resistance to amphibian chytridiomycosis. Genome Biol. Evol. 7, 286–298 (2014).
63
B. Gratwicke, H. Ross, A. Batista, G. Chaves, A. J. Crawford, L. Elizondo, A. Estrada, M. Evans, D. Garelle, J. Guerrel, A. Hertz, M. Hughey, C. A. Jaramillo, B. Klocke, M. Mandica, D. Medina, C. L. Richards-Zawacki, M. J. Ryan, A. Sosa-Bartuano, J. Voyles, B. Walker, D. C. Woodhams, R. Ibáñez, Evaluating the probability of avoiding disease‐related extinctions of Panamanian amphibians through captive breeding programs. Anim. Conserv. 19, 324–336 (2016).
64
S. Lötters, J. Kielgast, J. Bielby, S. Schmidtlein, J. Bosch, M. Veith, S. F. Walker, M. C. Fisher, D. Rödder, The link between rapid enigmatic amphibian decline and the globally emerging chytrid fungus. EcoHealth 6, 358–372 (2009).
65
K. R. Lips, Mass mortality and population declines of anurans at an upland site in western Panama. Conserv. Biol. 13, 117–125 (1999).
66
A. García‐Rodríguez, G. Chaves, C. Benavides-Varela, R. Puschendorf, Where are the survivors? Tracking relictual populations of endangered frogs in Costa Rica. Divers. Distrib. 18, 204–212 (2012).
67
A. Hertz et al., Field notes on findings of threatened amphibian species in the central range. Amphib. Reptile Conserv. 6, e46 (2012).
68
D. C. Woodhams, V. L. Kilburn, L. K. Reinert, J. Voyles, D. Medina, R. Ibáñez, A. D. Hyatt, D. G. Boyle, J. D. Pask, D. M. Green, L. A. Rollins-Smith, Chytridiomycosis and amphibian population declines continue to spread eastward in Panama. EcoHealth 5, 268–274 (2008).
69
K. G. Smith, K. R. Lips, J. M. Chase, Selecting for extinction: Nonrandom disease-associated extinction homogenizes amphibian biotas. Ecol. Lett. 12, 1069–1078 (2009).
70
P. Frías-Alvarez, V. T. Vredenburg, M. Familiar-López, J. E. Longcore, E. González-Bernal, G. Santos-Barrera, L. Zambrano, G. Parra-Olea, Chytridiomycosis survey in wild and captive mexican amphibians. EcoHealth 5, 18–26 (2008).
71
K. Jungfer et al., Agalychnis spurrelli. The IUCN Red List of Threatened Species 2008: e.T55295A11276251 (2008); .
72
A. Catenazzi, E. Lehr, V. T. Vredenburg, Thermal physiology, disease, and amphibian declines on the eastern slopes of the Andes. Conserv. Biol. 28, 509–517 (2014).
73
J. Icochea, T. Grant, W. Arizabal, Allobates alessandroi. The IUCN Red List of Threatened Species 2004: e.T55045A11245332 (2004); .
74
M. M. Ambiente, Lista Nacional Oficial de espécies da fauna ameaçadas de extinção. Diário Oficial da União (2014).
75
E. Izecksohn, S. P. de Carvalho, Anfíbios do município do Rio de Janeiro (Editora UFRJ, 2001).
76
P. Weygoldt, Changes in the composition of mountain stream frog communities in the Atlantic mountains of Brazil: Frogs as indicators of environmental deteriorations? Stud. Neotrop. Fauna Environ. 24, 249–255 (1989).
77
M. Mora et al., Estudios para la conservación de los anfibios altoandinos de Chile central. Boletín Chileno de Herpetología 2, 8–11 (2015).
78
L. D. Bacigalupe, C. Soto-Azat, C. García-Vera, I. Barría-Oyarzo, E. L. Rezende, Effects of amphibian phylogeny, climate and human impact on the occurrence of the amphibian-killing chytrid fungus. Glob. Chang. Biol. 23, 3543–3553 (2017).
79
I. Horta-Pizarro et al., Antecedentes preliminares del estudio de la batracofauna en la Reserva Nacional Río de Los Cipreses y el Alto Cachapoal, Región del Libertador Bernardo O’Higgins. Biodiversidata 2, 117–119 (2014).
80
D. Ramírez Álvarez, Nueva localidad para Alsodes tumultuosus Veloso, Iturra & Galleguillos, 1979 (Amphibia, Alsodidae) en la Cordillera de los Andes, Region de O’Higgins, Chile. Biodiversity & Natural History 1, 1–5 (2015).
81
G. Rosa, I. Anza, P. L. Moreira, J. Conde, F. Martins, M. C. Fisher, J. Bosch, Evidence of chytrid‐mediated population declines in common midwife toad in Serra da Estrela, Portugal. Anim. Conserv. 16, 306–315 (2013).
82
S. F. Walker, J. Bosch, V. Gomez, T. W. J. Garner, A. A. Cunningham, D. S. Schmeller, M. Ninyerola, D. A. Henk, C. Ginestet, C.-P. Arthur, M. C. Fisher, Factors driving pathogenicity vs. prevalence of amphibian panzootic chytridiomycosis in Iberia. Ecol. Lett. 13, 372–382 (2010).
83
J. Bosch, I. Martinez-Solano, M. Garcia-Paris, Evidence of a chytrid fungus infection involved in the decline of the common midwife toad (Alytes obstetricans) in protected areas of central Spain. Biol. Conserv. 97, 331–337 (2001).
84
D. S. Schmeller, M. Blooi, A. Martel, T. W. J. Garner, M. C. Fisher, F. Azemar, F. C. Clare, C. Leclerc, L. Jäger, M. Guevara-Nieto, A. Loyau, F. Pasmans, Microscopic aquatic predators strongly affect infection dynamics of a globally emerged pathogen. Curr. Biol. 24, 176–180 (2014).
85
C. Carey et al., “Biotic factors in amphibian population declines” in Amphibian Decline: An Integrated Analysis of Multiple Stressor Effects, G. Linder, Ed. (Society of Environmental Toxicology and Chemistry, 2003), pp. 153–208.
86
S. K. Taylor, E. S. Williams, E. T. Thorne, K. W. Mills, D. I. Withers, A. C. Pier, Causes of mortality of the Wyoming toad. J. Wildl. Dis. 35, 49–57 (1999).
87
C. Carey, J. E. Bruzgul, L. J. Livo, M. L. Walling, K. A. Kuehl, B. F. Dixon, A. P. Pessier, R. A. Alford, K. B. Rogers, Experimental exposures of boreal toads (Bufo boreas) to a pathogenic chytrid fungus (Batrachochytrium dendrobatidis). EcoHealth 3, 5–21 (2006).
88
C. Carey, Hypothesis concerning the causes of the disappearance of boreal toads from the mountains of Colorado. Conserv. Biol. 7, 355–362 (1993).
89
E. Muths, P. Stephen Corn, A. P. Pessier, D. Earl Green, Evidence for disease-related amphibian decline in Colorado. Biol. Conserv. 110, 357–365 (2003).
90
P. S. Corn, M. L. Jennings, E. Muths, Survey and assessment of amphibian populations in Rocky Mountain National Park. Northwest. Nat. 78, 34–55 (1997).
91
E. Muths, R. D. Scherer, D. S. Pilliod, Compensatory effects of recruitment and survival when amphibian populations are perturbed by disease. J. Appl. Ecol. 48, 873–879 (2011).
92
D. S. Pilliod, E. Muths, R. D. Scherer, P. E. Bartelt, P. S. Corn, B. R. Hossack, B. A. Lambert, R. McCaffery, C. Gaughan, Effects of amphibian chytrid fungus on individual survival probability in wild boreal toads. Conserv. Biol. 24, 1259–1267 (2010).
93
D. E. Green, C. K. Sherman, Diagnostic histological findings in Yosemite toads (Bufo canorus) from a die-off in the 1970s. J. Herpetol. 35, 92–103 (2001).
94
C.A.G.d. Cruz, S.P.d. Carvalho-e-Silva, A. M. Telles, Aplastodiscus musicus. The IUCN Red List of Threatened Species 2004: e.T55572A11319411 (2004); .
95
M. Lampo et al., Batrachochytrium dendrobatidis in Venezuela. Herpetol. Rev. 39, 449–454 (2008).
96
S. Lötters, R. Schulte, J. H. Córdova, M. Veith, Conservation priorities for harlequin frogs (Atelopus spp.) of Peru. Oryx 39, 343–346 (2005).
97
S. Lötters et al., Atelopus andinus. The IUCN Red List of Threatened Species 2004: e.T54487A11140726 (2004); .
98
L. A. Coloma, W. Duellman, A. A. C, S. R. Ron, A. Terán-Valdez, J. M. Guayasamin, Five new (extinct?) species of Atelopus (Anura: Bufonidae) from Andean Colombia, Ecuador, and Peru. Zootaxa 2574, 1–54 (2010).
99
A. Merino-Viteri, “Análisis de posibles causas de las disminuciones de poblaciones de anfibios en los Andes del Ecuador” (Pontificia Universidad Católica del Ecuador, Quito, Ecuador, 2001).
100
L. A. Coloma, M. C. Ardila-Robayo, S. Carvajal-Endara, Atelopus angelito, Centro Jambatu. 2011–2017, Anfibios de Ecuador (Fundación Otonga. Quito, Ecuador, 2016); www.anfibiosecuador.ec/index.php?aw,2 [accessed 2 February 2017].
101
M. R. Bustamante, S. R. Ron, L. A. Coloma, Cambios en la Diversidad en Siete Comunidades de Anuros en los Andes de Ecuador 1. Biotropica. J. Biol. Conserv. 37, 180–189 (2005).
102
L. A. Coloma, A. Quiguango, Atelopus arthuri, Centro Jambatu. 2011–2017, Anfibios de Ecuador (Fundación Otonga. Quito, Ecuador, 2016); www.anfibiosecuador.ec/index.php?aw,2.
103
L. A. Coloma, A. Quiguango, Atelopus balios, Centro Jambatu. 2011–2017, Anfibios de Ecuador (Fundación Otonga. Quito, Ecuador, 2016); www.anfibiosecuador.ec/index.php?aw,2 [accessed 2 February 2017].
104
S. R. Ron, A. Merino, Amphibian declines in Ecuador: Overview and first report of chytridiomycosis from South America. FrogLog 42, 2–3 (2000).
105
L. A. Coloma, S. Lotter, A. Quiguango, Atelopus bomolochos, Centro Jambatu. 2011–2017, Anfibios de Ecuador (Fundación Otonga. Quito, Ecuador, 2016); www.anfibiosecuador.ec/index.php?aw,2 [accessed 2 February 2017].
106
J. A. Peters, The frog genus Atelopus in Ecuador (anura: Bufonidae). Smithson. Contrib. Zool. 145, 1–49 (1973).
107
L. A. Coloma, A. Quiguango, Atelopus boulengeri, Centro Jambatu. 2011–2017, Anfibios de Ecuador (Fundación Otonga. Quito, Ecuador, 2016); www.anfibiosecuador.ec/index.php?aw,2 [accessed 2 February 2017].
108
M. Lampo et al., A chytridiomycosis epidemic and a severe dry season precede the disappearance of Atelopus species from the Venezuelan Andes. Herpetol. J. 16, 395–402 (2006).
109
E. La Marca, L. F. Esqueda, “Atelopus carbonerensis. Ranita amarilla de La Carbonera” in Ranas Arlequines, J. V. Rueda Almonacid, J. V. Rodríguez Mahecha, E. La Marca, S. Lötters, T. Kahn, A. Angulo, Eds. (Serie Libretas de Campo, Conservación Internacional, Bogotá, Colombia, 2005), p. 63.
110
K. R. Lips, Decline of a tropical montane amphibian fauna. Conserv. Biol. 12, 106–117 (1998).
111
K. R. Lips, D. E. Green, R. Papendick, Chytridiomycosis in wild frogs from southern Costa Rica. J. Herpetol. 37, 215–218 (2003).
112
K. Lips et al., Atelopus chiriquiensis. The IUCN Red List of Threatened Species 2010: e.T54498A11144381 (2010); .
113
E. La Marca, “Atelopus chrysocorallus. Ranita amarilla de Niquitao” in Ranas Arlequines, J. V. Rueda Almonacid, J. V. Rodríguez Mahecha, E. La Marca, S. Lötters, T. Kahn, A. Angulo, Eds. (Serie Libretas de Campo, Conservación Internacional, Bogotá, Colombia, 2005), p. 67.
114
K. Miyata, A new species of Atelopus (Anura: Bufonidae) from the cloud forests of northwestern Ecuador. Breviora 458, 1–10 (1980).
115
L. A. Coloma, A. Quiguango-Ubillús, Atelopus coynei, Centro Jambatu. 2011–2017, Anfibios de Ecuador (Fundación Otonga. Quito, Ecuador, 2016); www.anfibiosecuador.ec/index.php?aw,2 [accessed 2 February 2017].
116
E. Bonaccorso et al., Chytridiomycosis as a possible cause of population declines in Atelopus cruciger (Anura: Bufonidae). Herpetol. Rev. 34, 331–334 (2003).
117
C. Señaris, “Atelopus cruciger. Sapito rayado” in Ranas Arlequines, J. V. Rueda Almonacid, J. V. Rodríguez Mahecha, E. La Marca, S. Lötters, T. Kahn, A. Angulo, Eds. (Serie Libretas de Campo, Conservación Internacional, Bogotá, Colombia, 2005), p. 69.
118
S. Lötters, Atelopus dimorphus. The IUCN Red List of Threatened Species 2004: e.T54503A11152536 (2004) ;.
119
H. M. Ortega-Andrade, J. Bermingham, C. Aulestia, C. Paucar, Herpetofauna of the Bilsa Biological Station, province of Esmeraldas, Ecuador. Check List 6, 119–154 (2010).
120
L. A. Coloma, A. Quiguango-Ubillús, 2016. Atelopus elegans, Centro Jambatu. 2011–2017, Anfibios de Ecuador (Fundación Otonga. Quito, Ecuador, 2016); www.anfibiosecuador.ec/index.php?aw,2 [accessed 2 February 2017].
121
S. Lötters, R. Schulte, W. E. Duellman, A new and critically endangered species of Atelopus from the Andes of northern Peru (Anura: Bufonidae). Rev. Esp. Herpetol. 18, 101–109 (2004).
122
S. Lötters, Atelopus epikeisthos. The IUCN Red List of Threatened Species 2008: e.T136162A4253102 (2008); .
123
A. Angulo, et al., Atelopus erythropus. The IUCN Red List of Threatened Species 2004: e.T54506A11153518 (2004); .
124
P. J. Venegas et al., Two new harlequin frogs (Anura: Atelopus) from the Andes of northern Peru. Salamandra 44, 163–176 (2008).
125
IUCN SSC Amphibian Specialist Group, Atelopus eusebiodiazi. The IUCN Red List of Threatened Species 2011: e.T158466A5199200 (2011); .
126
L. A. Coloma, S. Lötters, A. W. Salas, Taxonomy of the Atelopus ignescens complex (Anura: Bufonidae): designation of a neotype of Atelopus ignescens and recognition of Atelopus exiguus. Herpetologica 56, 303–324 (2000).
127
L. A. Coloma, S. Lotter, A. Quiguango-Ubillús, Atelopus exiguus, Centro Jambatu. 2011–2017, Anfibios de Ecuador (Fundación Otonga. Quito, Ecuador, 2016); www.anfibiosecuador.ec/index.php?aw,2 [accessed 2 February 2017].
128
L. A. Coloma, Two new species of Atelopus (Anura: Bufonidae) from Ecuador. Herpetologica 58, 229–252 (2002).
129
L. A. Coloma, A. Quiguango-Ubillús, Atelopus helihelos, Centro Jambatu. 2011–2017, Anfibios de Ecuador (Fundación Otonga. Quito, Ecuador, 2016); www.anfibiosecuador.ec/index.php?aw,2 [accessed 2 February 2017].
130
S. R. Ron, W. E. Duellman, L. A. Coloma, M. R. Bustamante, Population decline of the Jambato toad Atelopus ignescens (Anura: Bufonidae) in the Andes of Ecuador. J. Herpetol. 37, 116–126 (2003).
131
J. M. Guayasamin, E. Bonaccorso, W. Duellman, L. A. Coloma, Genetic differentiation in the nearly extinct harlequin frogs (Bufonidae: Atelopus), with emphasis on the Andean Atelopus ignescens and A. bomolochos species complexes. Zootaxa 2574, 55–68 (2010).
132
L. A. Coloma, A. Quiguango-Ubillús, Atelopus ignescens, Centro Jambatu. 2011–2017, Anfibios de Ecuador (Fundación Otonga. Quito, Ecuador, 2016); www.anfibiosecuador.ec/index.php?aw,2 [accessed 2 February 2017].
133
E. E. Tapia, L. A. Coloma, G. Pazmiño-Otamendi, N. Peñafiel, Rediscovery of the nearly extinct longnose harlequin frog Atelopus longirostris (Bufonidae) in Junín, Imbabura, Ecuador. Neotrop. Biodivers. 3, 157–167 (2017).
134
L. A. Coloma, A. Quiguango-Ubillús, Atelopus longirostris, Centro Jambatu. 2011–2017, Anfibios de Ecuador (Fundación Otonga. Quito, Ecuador, 2016); www.anfibiosecuador.ec/index.php?aw,2 [accessed 2 February 2017].
135
L. A. Coloma, A. Quiguango-Ubillús, Atelopus lynchi, Centro Jambatu. 2011–2017, Anfibios de Ecuador (Fundación Otonga. Quito, Ecuador, 2016); www.anfibiosecuador.ec/index.php?aw,2 [accessed 2 February 2017].
136
L. A. Coloma, S. Lotters, A. Quiguango-Ubillús, Atelopus mindoensis, Centro Jambatu. 2011–2017, Anfibios de Ecuador (Fundación Otonga. Quito, Ecuador, 2016); www.anfibiosecuador.ec/index.php?aw,2 [accessed 2 February 2017].
137
E. La Marca, A. Rodriguez, S. Santiago, “Atelopus mucubajiensis. Ranita amarilla de Mucubají” in Ranas Arlequines, J. V. Rueda Almonacid, J. V. Rodríguez Mahecha, E. La Marca, S. Lötters, T. Kahn, A. Angulo, Eds. (Serie Libretas de Campo, Conservación Internacional, Bogotá, Colombia, 2005), p. 90.
138
M. Lampo, C. Barrio-Amorós, B. Han, Batrachochytrium dendrobatidis infection in the recently rediscovered Atelopus mucubajiensis (Anura, Bufonidae), a critically endangered frog from the Venezuelan Andes. EcoHealth 3, 299–302 (2006).
139
J. Gross, Declive en poblaciones de seis especies de anfibios anuros del Páramo de Mucubají, estado Mérida, Venezuela. Herpetotropicos 5, 9–20 (2009).
140
L. A. Coloma, A. Quiguango-Ubillús, Atelopus nanay, Centro Jambatu. 2011–2017, Anfibios de Ecuador (Fundación Otonga. Quito, Ecuador, 2016); www.anfibiosecuador.ec/index.php?aw,2 [accessed 2 February 2017].
141
M. H. Yánez-Muñoz et al., Descubrimiento de dos poblaciones sobrevivientes de Sapos Arlequín (Amphibia: Bufonidae: Atelopus) en los Andes de Ecuador. ACI Avances en Ciencias e Ingenierías 2, B74–B77 (2010).
142
L. A. Coloma, S. Lotters, A. Quiguango-Ubillús, Atelopus nepiozomus, Centro Jambatu. 2011–2017, Anfibios de Ecuador (Fundación Otonga. Quito, Ecuador, 2016); www.anfibiosecuador.ec/index.php?aw,2 [accessed 2 February 2017].
143
L. A. Coloma, S. Lotters, A. Quiguango-Ubillús, Atelopus onorei, Centro Jambatu. 2011–2017, Anfibios de Ecuador (Fundación Otonga. Quito, Ecuador, 2016); www.anfibiosecuador.ec/index.php?aw,2 [accessed 2 February 2017].
144
L. A. Coloma, W. E. Duellman, Atelopus orcesi, Centro Jambatu. 2011–2017, Anfibios de Ecuador (Fundación Otonga. Quito, Ecuador, 2016); www.anfibiosecuador.ec/index.php?aw,2 [accessed 2 February 2017].
145
I. J. García, R. Albornoz, E. La Marca, “Atelopus oxyrhynchus. Ranita amarilla de Mérida” in Ranas Arlequines, J. V. Rueda Almonacid, J. V. Rodríguez Mahecha, E. La Marca, S. Lötters, T. Kahn, A. Angulo, Eds. (Serie Libretas de Campo, Conservación Internacional, Bogotá, Colombia, 2005), p. 96.
146
L. A. Coloma, S. Lötters, W. Duellman, A. Miranda-Leiva, A taxonomic revision of Atelopus pachydermus, and description of two new (extinct?) species of Atelopus from Ecuador (Anura: Bufonidae). Zootaxa 1557, 1–32 (2007).
147
L. A. Coloma, Atelopus pachydermus. The IUCN Red List of Threatened Species 2008: e.T54536A11163524 (2008); .
148
L. A. Coloma, W. E. Duellman, S. Lotters, Atelopus pachydermus, Centro Jambatu. 2011–2017, Anfibios de Ecuador (Fundación Otonga. Quito, Ecuador, 2016); www.anfibiosecuador.ec/index.php?aw,2 [accessed 2 February 2017].
149
A. Almendáriz et al., Overview of the herpetofauna of the unexplored Cordillera del Cóndor of Ecuador. Amphibian Reptile Conserv. 8, 45–64 (2014).
150
L. A. Coloma, S. Lotter, Atelopus palmatus, Centro Jambatu. 2011–2017, Anfibios de Ecuador (Fundación Otonga. Quito, Ecuador, 2016); www.anfibiosecuador.ec/index.php?aw,2 [accessed 2 February 2017].
151
L. A. Coloma, W. E. Duellman, Atelopus pastuso, Centro Jambatu. 2011–2017, Anfibios de Ecuador (Fundación Otonga. Quito, Ecuador, 2016); www.anfibiosecuador.ec/index.php?aw,2 [accessed 2 February 2017].
152
IUCN SSC Amphibian Specialist Group, Atelopus patazensis. The IUCN Red List of Threatened Species 2013: e.T158467A43475921 (2013.); .
153
R. Schulte et al., Atelopus peruensis. The IUCN Red List of Threatened Species 2006: e.T54539A11164132 (2006); .
154
E. A. La Marca, A. Mijares, “Atelopus oxyrhynchus. Ranita amarilla de Mérida” in Ranas Arlequines, J. V. Rueda Almonacid, J. V. Rodríguez Mahecha, E. La Marca, S. Lötters, T. Kahn, A. Angulo, Eds. (Serie Libretas de Campo, Conservación Internacional, Bogotá, Colombia, 2005), p. 102.
155
L. A. Coloma, S. Lotters, Atelopus planispina, Centro Jambatu. 2011–2017, Anfibios de Ecuador (Fundación Otonga. Quito, Ecuador, 2016); www.anfibiosecuador.ec/index.php?aw,2 [accessed 2 February 2017].
156
L. A. Coloma, W. E. Duellman, Atelopus podocarpus, Centro Jambatu. 2011–2017, Anfibios de Ecuador (Fundación Otonga. Quito, Ecuador, 2016); www.anfibiosecuador.ec/index.php?aw,2 [accessed 2 February 2017].
157
IUCN SSC Amphibian Specialist Group, Atelopus podocarpus. The IUCN Red List of Threatened Species 2013: e.T18435550A18625726 (2013); .
158
S. Lötters, Atelopus pulcher. The IUCN Red List of Threatened Species 2006: e.T54544A11164921 (2006); .
159
P. Venegas, Atelopus pyrodactylus. The IUCN Red List of Threatened Species 2008: e.T135890A4216953 (2008); .
160
S. Lötters, J. L. Martinez, R. Schulte, Atelopus reticulatus. The IUCN Red List of Threatened Species 2004: e.T54546A11165230 (2004); .
161
E. La Marca, P. Soriano, “Atelopus sorianoi Ranita amarilla de Mérida” in Ranas Arlequines, J. V. Rueda Almonacid, J. V. Rodríguez Mahecha, E. La Marca, S. Lötters, T. Kahn, A. Angulo, Eds. (Serie Libretas de Campo, Conservación Internacional, Bogotá, Colombia, 2005), p. 112.
162
E. La Marca, J. E. García Pérez, “Atelopus sp.2 Arlequín de Guaramacal” in Ranas Arlequines, J. V. Rueda Almonacid, J. V. Rodríguez Mahecha, E. La Marca, S. Lötters, T. Kahn, A. Angulo, Eds. (Serie Libretas de Campo, Conservación Internacional, Bogotá, Colombia, 2005), p. 138.
163
S. Flechas, V. Vredenburg, A. Amézquita, Infection prevalence in three lowland species of harlequin toads from the threatened genus Atelopus. Herpetol. Rev. 46, 528–532 (2015).
164
E. La Marca, J. M. Renjifo, “Atelopus oxyrhynchus. Arlequín de Tamá” in Ranas Arlequines, J. V. Rueda Almonacid, J. V. Rodríguez Mahecha, E. La Marca, S. Lötters, T. Kahn, A. Angulo, Eds. (Serie Libretas de Campo, Conservación Internacional, Bogotá, Colombia, 2005), p. 114.
165
R. Aguayo, “Ecología de la comunidad de anuros en dos pisos bioclimáticos del Parque Nacional Carrasco (Cochabamba-Bolivia),” B.S. thesis, Universidad Mayor de San Simón, Cochabamba, Bolivia (2000).
166
I. De la Riva, S. Reichle, Diversity and conservation of the amphibians of Bolivia. Herpetol. Monogr. 28, 46–65 (2014).
167
A. Salas et al., Atelopus tricolor. The IUCN Red List of Threatened Species 2004: e.T54559A11167505 (2004); .
168
R. Aguayo, “Anfibios” in Libro Rojo de la fauna silvestre de Bolivia (Ministerio de Medio Ambiente y Agua, Bolivia, 2009), p. 91224.
169
D. C. Woodhams, J. Voyles, K. R. Lips, C. Carey, L. A. Rollins-Smith, Predicted disease susceptibility in a Panamanian amphibian assemblage based on skin peptide defenses. J. Wildl. Dis. 42, 207–218 (2006).
170
R. Puschendorf-Fahrenkrug, Atelopus varius (Harlequin Frog) fungal infection. Atelopus varius (Rana arlequín) infección fungosa. Herpetol. Rev. 34, 355 (2003).
171
C. L. Richards-Zawacki, Effects of slope and riparian habitat connectivity on gene flow in an endangered Panamanian frog, Atelopus varius. Divers. Distrib. 15, 796–806 (2009).
172
A. W. Ranvestel, K. R. Lips, C. M. Pringle, M. R. Whiles, R. J. Bixby, Neotropical tadpoles influence stream benthos: Evidence for the ecological consequences of decline in amphibian populations. Freshw. Biol. 49, 274–285 (2004).
173
M. H. Becker, C. L. Richards-Zawacki, B. Gratwicke, L. K. Belden, The effect of captivity on the cutaneous bacterial community of the critically endangered Panamanian golden frog (Atelopus zeteki). Biol. Conserv. 176, 199–206 (2014).
174
H. M. Bustamante, L. J. Livo, C. Carey, Effects of temperature and hydric environment on survival of the Panamanian Golden Frog infected with a pathogenic chytrid fungus. Integr. Zool. 5, 143–153 (2010).
175
G. V. Direnzo, P. F. Langhammer, K. R. Zamudio, K. R. Lips, Fungal infection intensity and zoospore output of Atelopus zeteki, a potential acute chytrid supershedder. PLOS ONE 9, e93356 (2014).
176
A. Angulo et al., Hypsiboas balzani. The IUCN Red List of Threatened Species 2004: e.T55405A11302013 (2004); .
177
A. B. M. Machado, C. S. Martins, G. M. Drummond, Lista da fauna brasileira ameaçada de extinção: incluindo as espécies quase ameaçadas e deficientes em dados (Fundação Biodiversitas, Belo Horizonte, 2005).
178
A. Acevedo, R. Franco, D. Carrero, Diversity of Andean amphibians of the Tamá National Natural Park in Colombia: A survey for the presence of Batrachochytrium dendrobatidis. Anim. Biodivers. Conserv. 39, 1–10 (2016).
179
A. A. Acevedo et al., Detection of Batrachochytrium dendrobatidis in amphibians from Northeastern Colombia. Herpetol. Rev. 47, 220–226 (2016).
180
S. M. Rovito, G. Parra-Olea, C. R. Vásquez-Almazán, T. J. Papenfuss, D. B. Wake, Dramatic declines in neotropical salamander populations are an important part of the global amphibian crisis. Proc. Natl. Acad. Sci. U.S.A. 106, 3231–3236 (2009).
181
IUCN SSC Amphibian Specialist Group, Bryophryne cophites. The IUCN Red List of Threatened Species 2012: e.T57206A3056795 (2012); .
182
IUCN SSC Amphibian Specialist Group, Bryophryne zonalis. The IUCN Red List of Threatened Species 2011: e.T190986A8841132 2011 (); .
183
C. Soto-Azat, A. Peñafiel-Ricaurte, S. J. Price, N. Sallaberry-Pincheira, M. P. García, M. Alvarado-Rybak, A. A. Cunningham, Xenopus laevis and emerging amphibian pathogens in Chile. EcoHealth 13, 775–783 (2016).
184
P. Acuña-O et al., Mortalidad de la población de rana grande chilena, Calyptocephalella gayi (Calyptocephalellidae), en la laguna Matanzas, del humedal El Yali. Chile central. Anales del Museo de Historia Natural de Valparaíso 27, 35–50 (2014).
185
C. Soto-Azat, A. Valenzuela-Sánchez, B. T. Clarke, K. Busse, J. C. Ortiz, C. Barrientos, A. A. Cunningham, Is chytridiomycosis driving Darwin’s frogs to extinction? PLOS ONE 8, e79862 (2013).
186
C.M. Vélez, P. Acuña, “Avances en el manejo ex situ de Calyptocephalella gayi (rana grande chilena)” in Conservación de Anfibios de Chile, C. Soto-Azat, A. Valenzuela-Sánchez, Eds. (Universidad Nacional Andrés Bello, 2012), pp. 77–82.
187
B. E. Velásquez et al., Infección por el hongo quitrido Batrachochytrium dendrobatidis en anuros de la Cordillera Occidental de Colombia. Herpetotropicos 4, 65–70 (2008).
188
G. Santos-Barrera, L. Canseco-Márquez, Charadrahyla altipotens. The IUCN Red List of Threatened Species 2004: e.T55384A11288683 (2004); .
189
V. Mata-Silva et al., Additional comments on the geographic distribution and conservation status of the recently rediscovered Voiceless Treefrog, Charadrahyla altipotens (Duellman, 1968) from Oaxaca, Mexico. Mesoamerican Herpetol. 3, 1073–1076 (2016).
190
S. N. Stuart et al., Threatened Amphibians of the World (Lynx Edicions, Barcelona, Spain, 2008).
191
K. R. Lips, J. R. Mendelson III, A. Muñoz-Alonso, L. Canseco-Márquez, D. G. Mulcahy, Amphibian population declines in montane southern Mexico: Resurveys of historical localities. Biol. Conserv. 119, 555–564 (2004).
192
T. L. Cheng, S. M. Rovito, D. B. Wake, V. T. Vredenburg, Coincident mass extirpation of neotropical amphibians with the emergence of the infectious fungal pathogen Batrachochytrium dendrobatidis. Proc. Natl. Acad. Sci. U.S.A. 108, 9502–9507 (2011).
193
G. Parra-Olea, M. García-París, D. B. Wake, Status of some populations of Mexican salamanders (Amphibia: Plethodontidae). Rev. Biol. Trop. 47, 217–223 (1999).
194
S. M. Whitfield, K. E. Bell, T. Philippi, M. Sasa, F. Bolaños, G. Chaves, J. M. Savage, M. A. Donnelly, Amphibian and reptile declines over 35 years at La Selva, Costa Rica. Proc. Natl. Acad. Sci. U.S.A. 104, 8352–8356 (2007).
195
B. Kubicki, Rediscovery of Hyalinobatrachium chirripoi (Anura: Centrolenidae) in southeastern Costa Rica. Rev. Biol. Trop. 52, 215–218 (2004).
196
D. Furlani, G. Francesco Ficetola, G. Colombo, M. Ugurlucan, F. De Bernardi, Deforestation and the structure of frog communities in the Humedale Terraba-Sierpe, Costa Rica. Zool. Sci. 26, 197–202 (2009).
197
G. Velo-Antón, D. Rodríguez, A. E. Savage, G. Parra-Olea, K. R. Lips, K. R. Zamudio, Amphibian-killing fungus loses genetic diversity as it spreads across the New World. Biol. Conserv. 146, 213–218 (2012).
198
P. Verburg, S. S. Kilham, C. M. Pringle, K. R. Lips, D. L. Drake, A stable isotope study of a neotropical stream food web prior to the extirpation of its large amphibian community. J. Trop. Ecol. 23, 643–651 (2007).
199
L. D. Wilson, J. R. McCranie, The conservation status of the herpetofauna of Honduras. Amphib. Reptile Conserv. 3, 6–33 (2004).
200
G. Cruz, L. D. Wilson, R. McCranie, Craugastor anciano. The IUCN Red List of Threatened Species 2004: e.T56413A11472780 (2004); .
201
R. Puschendorf, F. Castaneda, J. R. McCranie, Chytridiomycosis in wild frogs from Pico Bonito National Park, Honduras. EcoHealth 3, 178–181 (2006).
202
G. Köhler et al., Field notes on Craugastor azueroensis (Savage, 1975) (Amphibia: Anura: Craugastoridae). Herpetol. Notes 5, 157 (2012).
203
S. M. Whitfield, J. Kerby, L. R. Gentry, M. A. Donnelly, Temporal variation in infection prevalence by the amphibian chytrid fungus in three species of frogs at La Selva, Costa Rica. Biotropica 44, 779–784 (2012).
204
B. Folt, K. E. Reider, Leaf-litter herpetofaunal richness, abundance, and community assembly in mono-dominant plantations and primary forest of northeastern Costa Rica. Biodivers. Conserv. 22, 2057–2070 (2013).
205
M. D. Barquero et al., Composition and species richness of herpetofauna in two isolated regions of southern Nicaragua. Herpetol. Notes 3, 341–352 (2010).
206
B. Hilje, T. M. Aide, Recovery of amphibian species richness and composition in a chronosequence of secondary forests, northeastern Costa Rica. Biol. Conserv. 146, 170–176 (2012).
207
F. Solís et al., Craugastor catalinae. The IUCN Red List of Threatened Species 2008: e.T56498A11476342 (2008); .
208
G. Cruz, L. D. Wilson, R. McCranie, Craugastor chrysozetetes. The IUCN Red List of Threatened Species 2004: e.T56513A11488131 (2004); .
209
L. D. Wilson, R. McCranie, G. Cruz, Craugastor cruzi. The IUCN Red List of Threatened Species 2004: e.T56537A11494269 (2004); .
210
J. R. McCranie, L. V. Orellana, J. G. Himes, Rediscovery of two Honduran endemic streamside frogs, Craugastor emleni (Dunn) and Craugastor stadelmani (Schmidt). FrogLog 94, 12–15 (2010).
211
L. D. Wilson, R. McCranie, Craugastor emleni. The IUCN Red List of Threatened Species 2004: e.T56579A11485971 (2004); .
212
R. Jiménez, G. Alvarado, Craugastor escoces (Anura: Craugastoridae) reappears after 30 years: rediscovery of an “extinct” Neotropical frog. Amphib.-Reptil. 38, 257–259 (2017).
213
J. E. Kolby, J. R. Mccranie, Discovery of a surviving population of the montane streamside frog Craugastor milesi (Schmidt). Herpetol. Rev. 40, 282 (2009).
214
J. E. Kolby, G. E. Padgett-Flohr, R. Field, Amphibian chytrid fungus Batrachochytrium dendrobatidis in Cusuco National Park, Honduras. Dis. Aquat. Organ. 92, 245–251 (2010).
215
G. Cruz et al., Craugastor milesi. The IUCN Red List of Threatened Species 2009: e.T56765A11532463 (2009); .
216
IUCN SSC Amphibian Specialist Group and NatureServe, Craugastor obesus. The IUCN Red List of Threatened Species 2014: e.T56799A3050126 (2014); .
217
G. Cruz, L. D. Wilson, Craugastor omoaensis. The IUCN Red List of Threatened Species 2004: e.T56810A11536214 (2004); .
218
M. J. Ryan, K. R. Lips, M. W. Eichholz, Decline and extirpation of an endangered Panamanian stream frog population (Craugastor punctariolus) due to an outbreak of chytridiomycosis. Biol. Conserv. 141, 1636–1647 (2008).
219
R. Puschendorf-Fahrenkrug et al., Eleutherodactylus ranoides (NCN) dry forest population: Refuge or decline? Herpetol. Rev. 36, 53 (2005).
220
F. Solís et al., Craugastor rhyacobatrachus. The IUCN Red List of Threatened Species 2008: e.T56913A11551412 (2008); .
221
J. Abarca et al., Reconsidering extinction: rediscovery of Incilius holdridgei (Anura: Bufonidae) in Costa Rica after 25 years. Herpetol. Rev. 41, 150–152 (2010).
222
G. Cruz, L. D. Wilson, Craugastor stadelmani. The IUCN Red List of Threatened Species 2004: e.T56976A11562277 (2004); .
223
G. Chaves, H. Zumbado-Ulate, A. García-Rodríguez, E. Gómez, V. T. Vredenburg, M. J. Ryan, Rediscovery of the critically endangered streamside frog, Craugastor taurus (Craugastoridae), in Costa Rica. Trop. Conserv. Sci. 7, 628–638 (2014).
224
J. Bertoluci, W. Heyer, Boracéia update. FrogLog 14, 2–3 (1995).
225
B. V. S. Pimenta, C. A. G. da Cruz, U. Caramaschi, Taxonomic review of the species complex of Crossodactylus dispar A. Lutz, 1925 (Anura, Hylodidae). Arquivos de Zoologia (São Paulo) 45, 1–33 (2014).
226
B. Kubicki, Amphibian diversity in Guayacán, Limón province, Costa Rica. Brenesia 69, 35–42 (2008).
227
P. C. A. Garcia, “Anfíbios,” in Fauna ameaçada de extinção do estado de São Paulo, P. M Bressan, M. C. M. Kierulff, A. M. Sugieda, Eds. (Fundação Parque Zoológico de São Paulo, Secretaria do Meio Ambiente., Diário Oficial da União. 2014 Lista Nacional Oficial das Espécies da Fauna Ameaçadas de Extinção. Seção 1, São Paulo, 2010), pp. 329–347.
228
W. R. Heyer, Variation and systematics of frogs of the genus Cycloramphus (Amphibia, Leptodactylidae). Arq. Zool. 30, 235–339 (1983).
229
P. C. d. Anchieta Garcia, G. Vinciprova, Range extensions of some anuran species for Santa Catarina and Rio Grande do Sul states, Brazil. Herpetol. Rev. 29, 117 (1998).
230
D. L. Miller, S. Rajeev, M. Brookins, J. Cook, L. Whittington, C. A. Baldwin, Concurrent infection with ranavirus, Batrachochytrium dendrobatidis, and Aeromonas in a captive anuran colony. J. Zoo Wildl. Med. 39, 445–449 (2008).
231
J. Bielby, S. Bovero, G. Sotgiu, G. Tessa, M. Favelli, C. Angelini, S. Doglio, F. C. Clare, E. Gazzaniga, F. Lapietra, T. W. J. Garner, Fatal chytridiomycosis in the tyrrhenian painted frog. EcoHealth 6, 27–32 (2009).
232
Muñoz-Alonso, L.A. 2010. Riqueza, diversidad y estatus de los anfibios amenazados en el sureste de México; una evaluación para determinar las posibles causas de la declinación de las poblaciones. Departamento de Fauna Silvestre. 1-55.
233
IUCN SSC Amphibian Specialist Group, Duellmanohyla soralia. The IUCN Red List of Threatened Species 2014: e.T55313A54360566 (2014); .
234
J. R. Mendelson III, A. Eichenbaum, J. A. Campbell, Taxonomic review of the populations of the fringe-limbed treefrogs (Hylidae: Ecnomiohyla) in Mexico and nuclear Central America. South Am. J. Herpetol. 10, 187–194 (2015).
235
J. R. Mendelson III, J. M. Savage, E. Griffith, H. Ross, B. Kubicki, R. Gagliardo, Spectacular new gliding species of Ecnomiohyla (Anura: Hylidae) from central Panama. J. Herpetol. 42, 750–759 (2008).
236
J. R. Mendelson III, Shifted baselines, forensic taxonomy, and Rabbs’ fringe-limbed treefrog: The changing role of biologists in an era of amphibian declines and extinctions. Herpetol. Rev. 42, 21–25 (2011).
237
P. A. Burrowes, R. L. Joglar, D. E. Green, Potential causes for amphibian declines in Puerto Rico. Herpetologica 60, 141–154 (2004).
238
P. Burrowes, Geographic distribution of Batrachochytrium dendrobatidis in Puerto Rico. Herpetol. Rev. 39, 321 (2008).
239
P. F. Langhammer, K. R. Lips, P. A. Burrowes, T. Tunstall, C. M. Palmer, J. P. Collins, A fungal pathogen of amphibians, Batrachochytrium dendrobatidis, attenuates in pathogenicity with in vitro passages. PLOS ONE 8, e77630 (2013).
240
A. V. Longo, R. J. Ossiboff, K. R. Zamudio, P. A. Burrowes, Lability in host defenses: Terrestrial frogs die from chytridiomycosis under enzootic conditions. J. Wildl. Dis. 49, 197–199 (2013).
241
A. V. Longo, P. A. Burrowes, Persistence with Chytridiomycosis does not assure survival of direct-developing frogs. EcoHealth 7, 185–195 (2010).
242
A. V. Longo, P. A. Burrowes, R. L. Joglar, Seasonality of Batrachochytrium dendrobatidis infection in direct-developing frogs suggests a mechanism for persistence. Dis. Aquat. Organ. 92, 253–260 (2010).
243
P. A. Burrowes, A. V. Longo, C. A. Rodríguez, Potential fitness cost of Batrachochytrium dendrobatidis in Eleutherodactylus coqui, and comments on environment-related risk of infection. Herpetotropicos 4, 51–57 (2007).
244
R. L. Joglar, Los Coquíes de Puerto Rico (Editorial de la Universidad de Puerto Rico, 1998).
245
P. Burrowes, The reproductive biology and parental care of the Puerto Rican cave- dwelling frog Eleutherodactylus cooki. Herpetologica 56, 375–386 (2000).
246
B. S. Barker, A. Ríos-Franceschi, Population declines of mountain coqui (Eleutherodactylus portoricensis) in the cordillera central of Puerto Rico. Herpetol. Conserv. Biol. 9, 578–589 (2014).
247
S. Bovero, G. Sotgiu, C. Angelini, S. Doglio, E. Gazzaniga, A. A. Cunningham, T. W. J. Garner, Detection of chytridiomycosis caused by Batrachochytrium dendrobatidis in the endangered Sardinian newt (Euproctus platycephalus) in southern Sardinia, Italy. J. Wildl. Dis. 44, 712–715 (2008).
248
IUCN SSC Amphibian Specialist Group, Gastrotheca antoniiochoai. The IUCN Red List of Threatened Species 2017: e.T135833A89217413 (2017); .
249
A. Catenazzi, R. von May, Conservation status of amphibians in Peru. Herpetol. Monogr. 28, 1–23 (2014).
250
W. E. Duellman, A. Catenazzi, D. C. Blackburn, A new species of marsupial frog (Anura: Hemiphractidae: Gastrotheca) from the Andes of southern Peru. Zootaxa 3095, 1–14 (2011).
251
J. Icochea et al., Hemiphractus helioi. The IUCN Red List of Threatened Species 2004: e.T55368A11299186 (2004); .
252
B. Kubicki, Glass Frogs, Costa Rica (Editorial INBio, 2007).
253
M. Acevedo, B. E. Young, Dryophytes bocourti (amended version of 2004 assessment). The IUCN Red List of Threatened Species 2017: e.T55416A112712386 (2017); .
254
J. R. Mendelson III, E. Kabay, On the distribution and status of Plectrohyla hazelae (Taylor, 1940) (Amphibia: Hylidae) from Oaxaca, Mexico. Herpetol. Rev. 40, 301–302 (2009).
255
A. Angulo, S. Reichle, W. Arizabal. Hyloscirtus armatus. The IUCN Red List of Threatened Species 2004: e.T55398A11293387 (2004); .
256
J. Icochea, J. Lynch, E. Lehr, Hyloscirtus phyllognathus. The IUCN Red List of Threatened Species 2010: e.T55599A11327877 (2010); .
257
T. Grant, A new, toxic species of Colostethus (Anura: Dendrobatidae: Colostethinae) from the Cordillera Central of Colombia. Zootaxa 1555, 39–51 (2007).
258
G. Santos-Barrera et al., Hypopachus barberi (errata version published in 2016). The IUCN Red List of Threatened Species 2010: e.T57831A86524125 (2010); .
259
J. R. Mendelson III, E. D. Brodie Jr., J. H. Malone, M. E. Acevedo, M. A. Baker, N. J. Smatresk, J. A. Campbell, Factors associated with the catastrophic decline of a cloudforest frog fauna in Guatemala. Rev. Biol. Trop. 52, 991–1000 (2004).
260
M. Acevedo, B. Young, Incilius ibarrai. The IUCN Red List of Threatened Species 2004: e.T54667A11183794 (2004); .
261
J. R. Mendelson III, M. E. B. Jones, A. P. Pessier, G. Toledo, E. H. Kabay, J. A. Campbell, On the timing of an epidemic of amphibian chytridiomycosis in the highlands of Guatemala. South Am. J. Herpetol. 9, 151–153 (2014).
262
M. R. Bornschein, G. N. Maurício, M. R. Pie, Rectification of the type locality of Ischnocnema paranaensis (Anura: Brachycephalidae), a missing species of the Atlantic Forest of Brazil. Zootaxa 3957, 249–250 (2015).
263
F. Bolaños et al., Isthmohyla calypsa. The IUCN Red List of Threatened Species 2008: e.T55432A11310707 (2008); .
264
F. Solís et al., Isthmohyla debilis. The IUCN Red List of Threatened Species 2008: e.T55462A11301353 (2008); .
265
IUCN SSC Amphibian Specialist Group and NatureServe, Isthmohyla graceae. The IUCN Red List of Threatened Species 2014: e.T55492A3030233 (2014); .
266
F. Bolaños, G. Chaves, J. Savage, Isthmohyla pictipes. The IUCN Red List of Threatened Species 2008: e.T55603A11335341 (2008); .
267
B. D. Bell, S. Carver, N. J. Mitchell, S. Pledger, The recent decline of a New Zealand endemic: How and why did populations of Archey’s frog Leiopelma archeyi crash over 1996-2001? Biol. Conserv. 120, 189–199 (2004).
268
M. Ohmer, S. M. Herbert, R. Speare, P. J. Bishop, Experimental exposure indicates the amphibian chytrid pathogen poses low risk to New Zealand’s threatened endemic frogs. Anim. Conserv. 16, 422–429 (2013).
269
S. D. Shaw, L. F. Skerratt, A. Haigh, B. D. Bell, L. Daglish, P. J. Bishop, R. Summers, V. Moreno, S. Melzer, M. Ohmer, S. Herbert, D. Gleeson, L. Rowe, R. Speare, The distribution and host range of Batrachochytrium dendrobatidis in New Zealand, 1930–2010. Ecology 94, 2108–2111 (2013).
270
D. G. Newman, B. D. Bell, P. J. Bishop, R. Burns, A. Haigh, R. A. Hitchmough, M. Tocher, Conservation status of New Zealand frogs, 2009. N. Z. J. Zool. 37, 121–130 (2010).
271
M. A. Hudson, R. P. Young, J. D’Urban Jackson, P. Orozco-terWengel, L. Martin, A. James, M. Sulton, G. Garcia, R. A. Griffiths, R. Thomas, C. Magin, M. W. Bruford, A. A. Cunningham, Dynamics and genetics of a disease-driven species decline to near extinction: Lessons for conservation. Sci. Rep. 6, 30772 (2016).
272
M. A. Hudson, R. P. Young, J. Lopez, L. Martin, C. Fenton, R. McCrea, R. A. Griffiths, S.-L. Adams, G. Gray, G. Garcia, A. A. Cunningham, In-situ itraconazole treatment improves survival rate during an amphibian chytridiomycosis epidemic. Biol. Conserv. 195, 37–45 (2016).
273
A. Angulo et al., Leptodactylus rhodonotus. The IUCN Red List of Threatened Species 2004: e.T57161A11578741 (2004); .
274
R. W. Clarkson, J. C. Rorabaugh, Status of leopard frogs (Rana pipiens complex: Ranidae) in Arizona and southeastern California. Southwest. Nat. 34, 531–538 (1989).
275
R. Clarkson, J. Rorabaugh, J. Platz, Status and future of ranid frogs in Arizona. Proc. Arizona-Nevada Acad. Sci. 21, 21 (1986).
276
D. Adama, M. Beaucher, “Population monitoring and recovery of the northern leopard frog (Rana pipiens) in southeast British Columbia,” (Report to the Columbia Basin Fish and Wildlife Compensation Program, Nelson, BC, 2006), pp. 1–28.
277
Species at Risk Committee, “Species status report for Northern leopard frog (Lithobates pipiens) in the northwest territories” (Species at Risk Committee, Yellowknife, NT, 2013).
278
L. A. Rollins-Smith, L. K. Reinert, V. Miera, J. M. Conlon, Antimicrobial peptide defenses of the Tarahumara frog, Rana tarahumarae. Biochem. Biophys. Res. Commun. 297, 361–367 (2002).
279
S. F. Hale et al., “Effects of the chytrid fungus on the Tarahumara frog (Rana tarahumarae) in Arizona and Sonora, Mexico” in Connecting Mountain Islands and Desert Seas: Biodiversity and Management of the Madrean Archipelago II, G. J. Gottfried, B. S. Gebow, L. G. Eskew, C. B. Edminster, Carleton B., Comps. (Proc. RMRS-P-36, U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station, Fort Collins, CO, 2005), pp. 407–411.
280
S. F. Hale, J. L. Jarchow, “The status of the Tarahumara frog (Rana tarahumarae) in the United States and Mexico: part II” (Arizona Game and Fish Department and Region, Office of Endangered Species, U.S. Fish and Wildlife Service, 1998).
281
G. A. Bradley, P. C. Rosen, M. J. Sredl, T. R. Jones, J. E. Longcore, Chytridiomycosis in native Arizona frogs. J. Wildl. Dis. 38, 206–212 (2002).
282
A. E. Savage, K. R. Zamudio, MHC genotypes associate with resistance to a frog-killing fungus. Proc. Natl. Acad. Sci. U.S.A. 108, 16705–16710 (2011).
283
A. E. Savage, K. R. Zamudio, Adaptive tolerance to a pathogenic fungus drives major histocompatibility complex evolution in natural amphibian populations. Proc. Biol. Sci. 283, 20153115 (2016).
284
A. E. Savage, M. J. Sredl, K. R. Zamudio, Disease dynamics vary spatially and temporally in a North American amphibian. Biol. Conserv. 144, 1910–1915 (2011).
285
G. R. Gillespie, W. S. Osborne, N. A. McElhinney, The Conservation Status of Frogs in the Australian Alps: A Review (Report to Australian Alps Liaison Committee, 1995).
286
W. Osborne, M. Littlejohn, S. Thomson, Former distribution and apparent disappearance of the Litoria aurea complex from the Southern Tablelands of New South Wales and the Australian Capital Territory. Aust. Zool. 30, 190–198 (1996).
287
A. J. Hamer, S. J. Lane, M. J. Mahony, Using probabilistic models to investigate the disappearance of a widespread frog-species complex in high-altitude regions of south- eastern Australia. Anim. Conserv. 13, 275–285 (2010).
288
M. Mahony, 1999. “Review of the declines and disappearances within the bell frog species group (Litoria aurea species group) in Australia” in Declines and Disappearances of Australian Frogs, A. Campbell, Ed. (Environment Australia, Canberra, 1999), pp. 81–93.
289
Sydney Catchment Authority, Department of Environment and Climate Change, Terrestrial Vertebrate Fauna of the Greater Southern Sydney Region, vol. 2, Fauna of Conservation Concern and Priority Pest Species, Green Tree Frog (2005); https://www.environment.nsw.gov.au/-/media/OEH/Corporate-Site/Documents/Animals-and-plants/Threatened-species/terrestrial-vertebrate-fauna-greater-southern-sydney-region-pest-species-vol-02-070471.pdf.
290
G. R. Gillespie, E. McNabb, R. Gaborov, The biology and status of the large brown tree frog Litoria littlejohni in Victoria. Vic. Nat. 133, 128 (2016).
291
B. C. Scheele, F. Guarino, W. Osborne, D. A. Hunter, L. F. Skerratt, D. A. Driscoll, Decline and re-expansion of an amphibian with high prevalence of chytrid fungus. Biol. Conserv. 170, 86–91 (2014).
292
W. Osborne, “Declines and extinctions in populations of frogs in the ACT: A discussion paper” (Internal Report 92/8, ACT Parks and Conservation Service, Canberra, 1992).
293
W. Osborne, Declining frog populations and extinctions in the Canberra region. Bogong 11, 4–7 (1990).
294
W. Osborne, D. Hunter, G. Hollis, “Population declines and range contraction in Australian alpine frogs” in Declines and Disappearances of Australian Frogs, A. Campbell, Ed. (Environment Australia, Canberra, 1999), pp. 145–157.
295
D. A. Hunter, R. Speare, G. Marantelli, D. Mendez, R. Pietsch, W. Osborne, Presence of the amphibian chytrid fungus Batrachochytrium dendrobatidis in threatened corroboree frog populations in the Australian Alps. Dis. Aquat. Organ. 92, 209–216 (2010).
296
B. C. Scheele, D. A. Hunter, L. F. Skerratt, L. A. Brannelly, D. A. Driscoll, Low impact of chytridiomycosis on frog recruitment enables persistence in refuges despite high adult mortality. Biol. Conserv. 182, 36–43 (2015).
297
E. La Marca, Estatus de poblaciones de ranas de la familia Dendrobatidae (Amphibia: Anura) en sus localidades tipo en los Andes de Venezuela. Herpetotropicos 2, 73–86 (2005).
298
J. C. Guix et al., Natural history and conservation of bufonides in four Atlantic rainsforests areas of southeastern Brazil. Herpetol. Nat. Hist. 6, 1–12 (1998).
299
M. Mahony, “The status of frogs in the Watagan Mountains area, the central coast of New South Wales” in Herpetology in Australia (Surrey Beatty and Sons, Sydney, 1993), pp. 257–264.
300
F. Lemckert et al., Recent records of the southern barred frog (Mixophyes balbus) from the south coast of NSW. Herpetofauna 27, 43–45 (1997).
301
D. Hunter, G. R. Gillespie, “National Recovery Plan for the Stuttering Frog Mixophyes balbus” (Department of Sustainability and Environment, Victoria, Australia, 2011).
302
G. R. Gillespie et al., Gone but not forgotten: The status of the stuttering frog Mixophyes balbus in Victoria. Vic. Nat. 131, 64–71 (2014).
303
R. Knowles, K. Thumm, M. Mahony, H. Hines, D. Newell, M. Cunningham, Oviposition and egg mass morphology in barred frogs (Anura: Myobatrachidae: Mixophyes Günther, 1864), its phylogenetic significance and implications for conservation management. Aust. Zool. 37, 381–402 (2015).
304
H. B. Hines, M. Mahony, K. R. McDonald, “An assessment of frog declines in wet subtropical Australia” in Declines and Disappearances of Australian Frogs, A. Campbell, Ed. (Environment Australia, Canberra, 1999), pp. 44–63.
305
R. Goldingay, D. Newell, M. Graham, “The status of Rainforest Stream Frogs in north-eastern New South Wales: decline or recovery” in Declines and Disappearances of Australian Frogs, A. Campbell, Ed. (Environment Australia, Canberra, 1999), pp. 64–71.
306
D. A. Newell, R. L. Goldingay, L. O. Brooks, Population recovery following decline in an endangered stream-breeding frog (Mixophyes fleayi) from subtropical Australia. PLOS ONE 8, e58559 (2013).
307
G. Quick, R. L. Goldingay, J. Parkyn, D. A. Newell, Population stability in the endangered Fleay’s barred frog (Mixophyes fleayi) and a program for long-term monitoring. Aust. J. Zool. 63, 214–219 (2015).
308
K. M. Kriger, J. M. Hero, Survivorship in wild frogs infected with chytridiomycosis. EcoHealth 3, 171–177 (2006).
309
B. D. Lewis, D. A. Rohweder, Distribution, habitat, and conservation status of the Giant Barred Frog Mixophyes iteratus in the Bungawalbin catchment, northeastern New South Wales. Pac. Conserv. Biol. 11, 189–197 (2005).
310
C. Weldon et al., Disease driven extinction in the wild of the Kihansi spray toad (Nectophrynoides asperginis). bioRxiv 677971 [Preprint]. 21 June 2019. .
311
M. Makange, N. Kulaya, E. Biseko, P. Kalenga, S. Mutagwaba, G. Misinzo, Batrachochytrium dendrobatidis detected in Kihansi spray toads at a captive breeding facility (Kihansi, Tanzania). Dis. Aquat. Organ. 111, 159–164 (2014).
312
C. Weldon, L. Du Preez, Decline of the Kihansi spray toad, Nectophrynoides asperginis, from the Udzungwa mountains, Tanzania. FrogLog 62, 2–3 (2004).
313
IUCN SSC Amphibian Specialist Group, Nectophrynoides asperginis. The IUCN Red List of Threatened Species 2015: e.T54837A16935685 (2015); .
314
L. Rodríguez et al., Nymphargus pluvialis. The IUCN Red List of Threatened Species 2004: e.T54980A11222692 (2004); .
315
L. Rodríguez, J. L. Martinez, Nymphargus truebae. The IUCN Red List of Threatened Species 2004: e.T54999A11228389 (2004); .
316
F. Solís et al., Oedipina grandis. The IUCN Red List of Threatened Species 2008: e.T59315A11913881 (2008); .
317
Diário Oficial da União, 2014. Lista Nacional Oficial das Espécies da Fauna Ameaçadas de Extinção. Seção 1, ISSN 1677‒7042, 121‒130.
318
F. Solís et al., Oophaga arborea. The IUCN Red List of Threatened Species 2010: e.T55173A11250657 (2010); .
319
F. Solís et al., Oophaga granulifera. The IUCN Red List of Threatened Species 2008: e.T55186A11253972 (2008); .
320
S. V. Flechas, A. Paz, A. J. Crawford, C. Sarmiento, A. A. Acevedo, A. Arboleda, W. Bolívar-García, C. L. Echeverry-Sandoval, R. Franco, C. Mojica, A. Muñoz, P. Palacios-Rodríguez, A. M. Posso-Terranova, P. Quintero-Marín, L. A. Rueda-Solano, F. Castro-Herrera, A. Amézquita, Current and predicted distribution of the pathogenic fungus Batrachochytrium dendrobatidis in Colombia, a hotspot of amphibian biodiversity. Biotropica 49, 685–694 (2017).
321
J. P. Pombal Jr., C. F. Haddad, J. P. Pombal, C. F. B. Haddad, Frogs of the genus Paratelmatobius (Anura: Leptodactylidae) with descriptions of two new species. Copeia 1999, 1014–1026 (1999).
322
G. Hollis, “National Recovery Plan for the Baw Baw Frog Philoria frosti” (Department of the Environment, Canberra, 2011).
323
G. J. Hollis, “Ecology and conservation biology of the Baw Baw frog Philoria frosti (Anura: Myobatrachidae): Distribution, abundance, autoecology and demography,” thesis, University of Melbourne (2004), p. 390.
324
G. Hollis, Reassessment of the distribution, abundance and habitat of the Baw Baw frog (Philoria frosti). Vic. Nat. 112, 190–201 (1995).
325
D. Baêta, L. O. M. Giasson, J. P. Pombal Jr., C. F. B. Haddad, Review of the rare genus Phrynomedusa Miranda-Ribeiro, 1923 (Anura: Phyllomedusidae) with description of a new species. Herpetol. Monogr. 30, 49–78 (2016).
326
P. C. Eterovick, Use and sharing of calling and retreat sites by Phyllodytes luteolus in a modified environment. J. Herpetol. 33, 17–22 (1999).
327
M. G. Papp, C. O. Papp, Decline of the population of the treefrog Phyllodytes luteolus after fire. Herpetol. Rev. 31, 93 (2000).
328
C. Borteiro, J. C. Cruz, F. Kolenc, A. Aramburu, Chytridiomycosis in frogs from Uruguay. Dis. Aquat. Organ. 84, 159–162 (2009).
329
S. Carreira, R. Maneyro, Lista roja de los anfibios y reptiles del Uruguay. Una evaluación del estado de conservación de la herpetofauna de Uruguay sobre la base de los criterios de la Unión Internacional para la Conservación de la Naturaleza (Dirección Nacional de Medio Ambiente, Montevideo, 2015).
330
J. E. Kolby, S. D. Ramirez, L. Berger, K. L. Richards-Hrdlicka, M. Jocque, L. F. Skerratt, Terrestrial dispersal and potential environmental transmission of the amphibian chytrid fungus (Batrachochytrium dendrobatidis). PLOS ONE 10, e0125386 (2015).
331
J. E. Kolby, G. E. Padgett-Flohr, Reassessment of the historical timeline for Batrachochytrium dendrobatidis presence in Honduras and conservation implications for Plectrohyla dasypus. Herpetol. Rev. 40, 307–308 (2009).
332
G. Cruz et al., Plectrohyla dasypus. The IUCN Red List of Threatened Species 2010: e.T55873A11366211 (2010); .
333
G. Cruz et al., Plectrohyla exquisita. The IUCN Red List of Threatened Species 2010: e.T55874A11366549 (2010); .
334
L. A. M. Muñoz-Alonso, “Riqueza, diversidad y estatus de los anfibios amenazados en el sureste de México; una evaluación para determinar las posibles causas de la declinación de sus poblaciónes” (Departamento de Fauna Silvestre, 2010).
335
M. Acevedo, E. Smith, J. R. Mendelson III, Plectrohyla quecchi. The IUCN Red List of Threatened Species 2006: e.T55884A11371178 (2006); .
336
G. S. Natale, R. Maneyro, Amphibia, Anura, Leiuperidae, Pleurodema bibroni: Rediscovery. Check List 4, 47–49 (2008).
337
F. Kolenc, C. Borteiro, D. Baldo, D. P. Ferraro, C. Prigioni, The tadpoles and advertisement calls of Pleurodema bibroni Tschudi and Pleurodema kriegi (Muller), with notes on their geographic distribution and conservation status (Amphibia, Anura, Leiuperidae). Zootaxa 1969, 1–35 (2009).
338
C. Bardier et al., First case of chytridiomycosis in an adult specimen of a native anuran from Uruguay. Herpetol. Rev. 42, 65 (2011).
339
T. A. Seimon, A. Seimon, P. Daszak, S. R. P. Halloy, L. M. Schloegel, C. A. Aguilar, P. Sowell, A. D. Hyatt, B. Konecky, J. e Simmons, Upward range extension of Andean anurans and chytridiomycosis to extreme elevations in response to tropical deglaciation. Glob. Change Biol. 13, 288–299 (2007).
340
R. von May, A. Catenazzi, A. Angulo, J. L. Brown, J. Carrillo, G. Chávez, J. H. Córdova, A. Curo, A. Delgado, M. A. Enciso, R. Gutiérrez, E. Lehr, J. L. Martínez, M. Medina-Müller, A. Miranda, D. R. Neira, J. A. Ochoa, A. J. Quiroz, D. A. Rodríguez, L. O. Rodríguez, A. W. Salas, T. Seimon, A. Seimon, K. Siu-Ting, J. Suárez, C. Torres, E. Twomey, Current state of conservation knowledge on threatened amphibian species in Peru. Trop. Conserv. Sci. 1, 376–396 (2008).
341
IUCN SSC Amphibian Specialist Group, Pleurodema marmoratum. The IUCN Red List of Threatened Species 2015: e.T57289A79813238 (2015); .
342
L. Rodríguez, J. L. Martinez, W. Arizabal, Pristimantis cosnipatae. The IUCN Red List of Threatened Species 2004: e.T56526A11492437 (2004); .
343
L. Rodríguez et al., Pristimantis danae. The IUCN Red List of Threatened Species 2004: e.T56548A11495586 (2004); .
344
L. Rodríguez et al., Pristimantis rhabdolaemus. The IUCN Red List of Threatened Species 2004: e.T56908A11549839 (2004); .
345
L. Rodríguez et al., Pristimantis salaputium. The IUCN Red List of Threatened Species 2004: e.T56941A11557774 (2004); .
346
L. Rodríguez et al., Pristimantis toftae. The IUCN Red List of Threatened Species 2004: e.T57010A11565912 (2004); .
347
D. A. Hunter, “National Recovery Plan for the Southern Corroboree Frog, Pseudophryne corroboree, and the Northern Corroboree Frog, Pseudophryne pengilleyi” (Office of Environment and Heritage, Hurstville, New South Wales, Australia, 2012b).
348
B. C. Scheele, D. A. Hunter, L. A. Brannelly, L. F. Skerratt, D. A. Driscoll, Reservoir-host amplification of disease impact in an endangered amphibian. Conserv. Biol. 31, 592–600 (2017).
349
W. Osborne, D. Hunter, Frog declines in the Australian Alps: Where are we after ten years? Bogong 19, 3–6 (1998).
350
W. Osborne, “The conservation biology of Pseudophryne corroboree Moore (Anura: Myobatrachidae): A study of insular populations,” thesis, Australian National University (1990).
351
W. Osborne, Distribution, relative abundance and conservation status of corroboree frogs, Pseudophryne corroboree Moore (Anura: Myobatrachidae). Aust. Wildl. Res. 16, 537–547 (1989).
352
UCN SSC Amphibian Specialist Group, Ptychohyla hypomykter. The IUCN Red List of Threatened Species 2014: e.T55911A54364156 (2014); .
353
G. M. Fellers, C. A. Drost, Disappearance of the Cascades frog Rana cascadae at the southern end of its range, California, USA. Biol. Conserv. 65, 177–181 (1993).
354
K. Pope et al., Cascades Frog Conservation Assessment (United States Department of Agriculture, Forest Service, Pacific Southwest Research Station, 2014).
355
A. R. Blaustein, J. M. Romansic, E. A. Scheessele, B. A. Han, A. P. Pessier, J. Longcore, Interspecific variation in susceptibility of frog tadpoles to the pathogenic fungus Batrachochytrium dendrobatidis. Conserv. Biol. 19, 1460–1468 (2005).
356
C. J. Briggs, R. A. Knapp, V. T. Vredenburg, Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proc. Natl. Acad. Sci. U.S.A. 107, 9695–9700 (2010).
357
L. J. Rachowicz, R. A. Knapp, J. A. T. Morgan, M. J. Stice, V. T. Vredenburg, J. M. Parker, C. J. Briggs, Emerging infectious disease as a proximate cause of amphibian mass mortality. Ecology 87, 1671–1683 (2006).
358
C. J. Briggs, V. T. Vredenburg, R. A. Knapp, L. J. Rachowicz, Investigating the population-level effects of chytridiomycosis: An emerging infectious disease of amphibians. Ecology 86, 3149–3159 (2005).
359
V. T. Vredenburg, R. A. Knapp, T. S. Tunstall, C. J. Briggs, Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proc. Natl. Acad. Sci. U.S.A. 107, 9689–9694 (2010).
360
D. F. Bradford, Mass mortality and extinction in a high-elevation population of Rana muscosa. J. Herpetol. 25, 174–177 (1991).
361
V. T. Vredenburg, R. Bingham, R. Knapp, J. A. T. Morgan, C. Moritz, D. Wake, Concordant molecular and phenotypic data delineate new taxonomy and conservation priorities for the endangered mountain yellow‐legged frog. J. Zool. (Lond.) 271, 361–374 (2007).
362
K. Howard et al., “Green and Golden Bell Frog Litoria aurea: reassessment of historic sites in Victoria” (Arthur Rylah Institute for Environmental Research, Department of Sustainability and Environment, Heidelberg, Australia, 2010).
363
T. D. Penman, G. Muir, E. Magarey, E. Burns, Impact of a chytrid-related mortality event on a population of the green and golden bell frog Litoria aurea. Aust. Zool. 34, 314–318 (2008).
364
R. L. Goldingay, D. A. Newell, Population estimation of the green and golden bell frog Litoria aurea at Port Kembla. Aust. Zool. 33, 210–216 (2005).
365
G. Gillespie, Distribution, habitat and conservation status of the green and golden bell frog Litoria aurea (Lesson 1829) (Anura: Hylidae) in Victoria. Aust. Zool. 30, 199–207 (1996).
366
M. Mahony, The decline of the green and golden bell frog Litoria aurea viewed in the context of declines and disappearances of other Australian frogs. Aust. Zool. 30, 237–247 (1996).
367
M. J. Mahony et al., Identifying conservation and research priorities in the face of uncertainty: A review of the threatened bell frog complex in eastern Australia. Herpetol. Conserv. Biol. 8, 519–538 (2013).
368
W. Osborne, S. Patmore, D. Hunter, R. Pietsch, Preliminary observations on a highly-restricted tableland population of green and golden bell frogs on the Upper Molonglo River, NSW. Aust. Zool. 34, 271–284 (2008).
369
J. W. Valdez, M. P. Stockwell, K. Klop-Toker, S. Clulow, J. Clulow, M. J. Mahony, Factors driving the distribution of an endangered amphibian toward an industrial landscape in Australia. Biol. Conserv. 191, 520–528 (2015).
370
M. P. Stockwell, J. Clulow, M. J. Mahony, Evidence of a salt refuge: Chytrid infection loads are suppressed in hosts exposed to salt. Oecologia 177, 901–910 (2015).
371
S. D. Cashins, L. F. Grogan, M. McFadden, D. Hunter, P. S. Harlow, L. Berger, L. F. Skerratt, Prior infection does not improve survival against the amphibian disease Chytridiomycosis. PLOS ONE 8, e56747 (2013).
372
D. Hunter, “National Recovery Plan for the Booroolong Frog Litoria booroolongensis” (Office of Environment and Heritage, New South Wales, Australia, 2012a).
373
D. A. Hunter, “The conservation management of two threatened frog species in South- Eastern New South Wales, Australia” (Institute for Applied Ecology, University of Canberra, 2007), p. 176.
374
L. Berger, R. Speare, L. F. Skerratt, Distribution of Batrachochytrium dendrobatidis and pathology in the skin of green tree frogs Litoria caerulea with severe chytridiomycosis. Dis. Aquat. Organ. 68, 65–70 (2005).
375
M. Mahony, R. Knowles, R. R. Forster, S. Donnellan, Systematics of the Litoria citropa (Anura: Hylidae) complex in northern New South Wales and southern Queensland, Australia, with the description of a new species. Rec. Aust. Mus. 53, 37–48 (2001).
376
S. J. Richards, K. R. McDonald, R. A. Alford, Declines in populations of Australia’s endemic tropical rainforest frogs. Pac. Conserv. Biol. 1, 66–77 (1993).
377
M. Trenerry, W. F. Laurance, K. R. McDonald, Further evidence for the precipitous decline of endemic rainforest frogs in tropical Australia. Pac. Conserv. Biol. 1, 150–153 (1994).
378
K. R. McDonald, D. Méndez, R. Müller, A. B. Freeman, R. Speare, Decline in the prevalence of chytridiomycosis in frog populations in North Queensland, Australia. Pac. Conserv. Biol. 11, 114–120 (2005).
379
C. J. Hoskin, R. Puschendorf, “The importance of peripheral areas for biodiversity conservation: with particular focus on endangered rainforest frogs of the Wet Tropics and Eungella,” report to the National Environmental Research Program (Reef and Rainforest Research Centre Limited, Cairns, Australia, 2014)
380
C. J. Hoskin, H. B. Hines, E. Meyer, J. Clarke, M. Cunningham, A new treefrog (Hylidae: Litoria) from Kroombit Tops, east Australia, and an assessment of conservation status. Zootaxa 3646, 426–446 (2013).
381
R. Puschendorf, C. J. Hoskin, S. D. Cashins, K. McDonald, L. F. Skerratt, J. Vanderwal, R. A. Alford, Environmental refuge from disease-driven amphibian extinction. Conserv. Biol. 25, 956–964 (2011).
382
J. H. Daskin, R. A. Alford, R. Puschendorf, Short-term exposure to warm microhabitats could explain amphibian persistence with Batrachochytrium dendrobatidis. PLOS ONE 6, e26215 (2011).
383
G. Gillespie, D. Hunter, L. Berger, G. Marantelli, Rapid decline and extinction of a montane frog population in southern Australia follows detection of the amphibian pathogen Batrachochytrium dendrobatidis. Anim. Conserv. 18, 295–302 (2015).
384
Northern Queensland Threatened Frogs Recovery Team, “Recovery plan for the stream-dwelling rainforest frogs of the Wet Tropics biogeographic region of north-east Queensland 2000–2004,” unpublished report to Environment Australia, Canberra (Queensland Parks and Wildlife Service, Brisbane, 2001).
385
K. McDonald, M. Davies, Morphology and biology of the Australian tree frog Litoria pearsoniana (Copland)(Anura: Hylidae). Trans. R. Soc. S. Aust. 114, 145–156 (1990).
386
H. B. Hines, Southeast Queensland Threatened Frogs Recovery Team, “Recovery plan for stream frogs of south-east Queensland 2001-2005,” report to Environment Australia, Canberra (Queensland Parks and Wildlife Service, Brisbane, 2002).
387
K. A. Murray, L. F. Skerratt, R. Speare, H. McCallum, Impact and dynamics of disease in species threatened by the amphibian chytrid fungus, Batrachochytrium dendrobatidis. Conserv. Biol. 23, 1242–1252 (2009).
388
M. Mahony, R. Knowles, L. Pattinson, “Peppered tree frog Litoria piperata” in Threatened Frogs of New South Wales: Habitats, Status and Conservation, H. Ehmann, Ed. (Frog and Tadpole Study Group of NSW, Sydney, 1997), pp. 182–187.
389
S. Donnellan, K. McGuigan, R. Knowles, M. Mahony, C. Moritz, Genetic evidence for species boundaries in frogs of the Litoria citropa species-group (Anura: Hylidae). Aust. J. Zool. 47, 275–293 (1999).
390
S. Wassens, Review of the past distribution and decline of the southern bell frog Litoria raniformis in New South Wales. Aust. Zool. 34, 446–452 (2008).
391
G. W. Heard, C. D. Thomas, J. A. Hodgson, M. P. Scroggie, D. S. L. Ramsey, N. Clemann, Refugia and connectivity sustain amphibian metapopulations afflicted by disease. Ecol. Lett. 18, 853–863 (2015).
392
G. W. Heard, M. P. Scroggie, N. Clemann, D. S. L. Ramsey, Wetland characteristics influence disease risk for a threatened amphibian. Ecol. Appl. 24, 650–662 (2014).
393
M. Heard, K. F. Smith, K. Ripp, Examining the evidence for chytridiomycosis in threatened amphibian species. PLOS ONE 6, e23150 (2011).
394
N. Clemann, G. R. Gillespie, “National Recovery Plan for the Southern Bell Frog Litoria raniformis” (Department of the Environment, Canberra, 2013).
395
N. Clemann, M. P. Scroggie, M. J. Smith, G. N. L. Peterson, D. Hunter, Characteristics of refugia used by the threatened Australian growling grass frog (Litoria raniformis) during a prolonged drought. Wildl. Res. 40, 385–392 (2013).
396
L. F. Grogan, A. D. Phillott, B. C. Scheele, L. Berger, S. D. Cashins, S. C. Bell, R. Puschendorf, L. F. Skerratt, Endemicity of chytridiomycosis features pathogen overdispersion. J. Anim. Ecol. 85, 806–816 (2016).
397
H. B. Hines, Southeast Queensland Threatened Frogs Recovery Team, “National recovery plan for Stream Frogs of Southeast Queensland 2001–2005” (Australian Government, Department of Agriculture, Water, and the Environment, 2002); www.environment.gov.au/node/15990.
398
G. V. Czechura, G. J. Ingram, Taudactylus diurnus and the case of the disappearing frogs. Mem. Queensl. Mus. 29, 361–365 (1990).
399
K. R. McDonald, Rheobatrachus Liem and Taudactylus Straughan and Lee (Anura: Leptodactylidae) in Eungella National Park, Queensland: distribution and decline. Trans. R. Soc. S. Aust. 114, 187–194 (1990).
400
J. A. Covacevich, K. R. McDonald, Distribution and conservation of frogs and reptiles of Queensland rainforests. Mem. Queensl. Mus. 34, 189–199 (1993).
401
J. M. Padial, J. C. Chaparro, J. Köhler, I. De La Riva, Rediscovery, resurrection and redescription of Rhinella leptoscelis (Boulenger, 1912)(Anura: Bufonidae). Zootaxa 2115, 56–64 (2009).
402
J. S. Barrionuevo, R. Aguayo, E. O. Lavilla, First record of chytridiomycosis in Bolivia (Rhinella quechua; Anura: Bufonidae). Dis. Aquat. Organ. 82, 161–163 (2008).
403
J. Bourke, F. Mutschmann, T. Ohst, P. Ulmer, A. Gutsche, K. Busse, H. Werning, W. Boehme, Batrachochytrium dendrobatidis in Darwin’s frog Rhinoderma spp. in Chile. Dis. Aquat. Organ. 92, 217–221 (2010).
404
K. Busse, Biología de la reproducción del Sapito de Darwin (Rhinoderma darwinii) y su cría en cautividad. Cría en Cautividad de Fauna Chilena. Santiago de Chile. Servicio Agrícola y Ganadero 139, 146 (2004).
405
H. Werning, From Darwin’s treasure chest: Rhinoderma. IRCF Reptiles and Amphibians 16, 247–255 (2009).
406
R. Solís, G. Lobos, S. F. Walker, M. Fisher, J. Bosch, Presence of Batrachochytrium dendrobatidis in feral populations of Xenopus laevis in Chile. Biol. Invasions 12, 1641–1646 (2010).
407
C. Soto-Azat, A. Valenzuela-Sánchez, B. Collen, J. M. Rowcliffe, A. Veloso, A. A. Cunningham, The population decline and extinction of Darwin’s frogs. PLOS ONE 8, e66957 (2013).
408
A. Valenzuela‐Sánchez, G. Harding, A. A. Cunningham, C. Chirgwin, C. Soto-Azat, Home range and social analyses in a mouth brooding frog: Testing the coexistence of paternal care and male territoriality. J. Zool. (Lond.) 294, 215–223 (2014).
409
A. Valenzuela-Sánchez, A. A. Cunningham, C. Soto-Azat, Geographic body size variation in ectotherms: Effects of seasonality on an anuran from the southern temperate forest. Front. Zool. 12, 37 (2015).
410
K. Busse, Darwin’s frogs in danger: Rhinoderma, are there any Rhinoderma rufum left in Chile. Reptilia 25, 63–67 (2002).
411
J. Bourke, K. Busse, W. Böhme, Searching for a lost frog (Rhinoderma rufum): Identification of the most promising areas for future surveys and possible reasons of its enigmatic decline. North-West. J. Zool. 8, 99–106 (2012).
412
L. Rodríguez, J. L. Martinez, W. Arizabal, Rulyrana spiculata. The IUCN Red List of Threatened Species 2004: e.T54994A11227150 (2004); .
413
A. Martel, A. Spitzen-van der Sluijs, M. Blooi, W. Bert, R. Ducatelle, M. C. Fisher, A. Woeltjes, W. Bosman, K. Chiers, F. Bossuyt, F. Pasmans, Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians. Proc. Natl. Acad. Sci. U.S.A. 110, 15325–15329 (2013).
414
A. Spitzen-van der Sluijs, A. Spitzen-van der Sluijs, F. Spikmans, A. Spitzen-van der Sluijs, F. Spikmans, W. Bosman, A. Spitzen-van der Sluijs, F. Spikmans, W. Bosman, M. de Zeeuw, A. Spitzen-van der Sluijs, F. Spikmans, W. Bosman, M. de Zeeuw, T. van der Meij, A. Spitzen-van der Sluijs, F. Spikmans, W. Bosman, M. de Zeeuw, T. van der Meij, E. Goverse, A. Spitzen-van der Sluijs, F. Spikmans, W. Bosman, M. de Zeeuw, T. van der Meij, E. Goverse, M. Kik, A. Spitzen-van der Sluijs, F. Spikmans, W. Bosman, M. de Zeeuw, T. van der Meij, E. Goverse, M. Kik, F. Pasmans, A. Spitzen-van der Sluijs, F. Spikmans, W. Bosman, M. de Zeeuw, T. van der Meij, E. Goverse, M. Kik, F. Pasmans, A. Martel, Rapid enigmatic decline drives the fire salamander (Salamandra salamandra) to the edge of extinction in the Netherlands. Amphib.-Reptil. 34, 233–239 (2013).
415
R. Luria-Manzano, L. Conseco-Marquez, P. Frias-Alvarez, Batrachochytrium dendrobatidis in Plectrohyla arborescandens (Anura: Hylidae) larvae at a montane site in the Sierra Negra, Puebla, México. Herpetol. Rev. 42, 552–554 (2011).
416
A. Dennis, M. Mahony, “Experimental translocation of the endangered sharp- snouted dayfrog Taudactylus acutirostris and observations of the cause of declines among montane riparian frogs” (Final report to Wet Tropics Management Authority, Cairns, Queensland, Australia, 1994).
417
C. B. Banks, H. E. McCracken, “Captive management and pathology of sharp- snouted torrent frogs, Taudactylus acutirostris, at Melbourne and Taronga Zoos” in Frogs in the Community (Brisbane, 2002), pp. 94–102.
418
C. J. Marshall, The reappearance of Taudactylus (Anura: Myobatrachidae) in north Queensland streams. Pac. Conserv. Biol. 4, 39–41 (1998).
419
L. M. Schloegel, J.-M. Hero, L. Berger, R. Speare, K. McDonald, P. Daszak, The decline of the sharp-snouted day frog (Taudactylus acutirostris): The first documented case of extinction by infection in a free-ranging wildlife species? EcoHealth 3, 35–40 (2006).
420
R. W. R. Retallick, H. McCallum, R. Speare, Endemic infection of the amphibian chytrid fungus in a frog community post-decline. PLOS Biol. 2, e351 (2004).
421
H. B. Hines, Kroombit Tops: Endemism and outliers. Queensl. Nat. 52, 4–31 (2014).
422
A. Borsboom, J. Clarke, M. Cunningham, “Draft recovery plan for the Kroombit tinker frog Taudactylus pleione 1997–2001” (Queensland Department of Natural Recourses and Queensland Department Environment, 1998).
423
Threatened Species Scientific Committee, Commonwealth Listing Advice on Taudactylus pleione (Kroombit Tinker Frog) [Listing Advice] (2012); www.environment.gov.au/biodiversity/threatened/species/pubs/1889-conservation-advice-13072017.pdf.
424
A. Freeman, An observation of calling northern tinker frogs on Mount Bellenden Ker. Mem. Queensl. Mus. 49, 295–298 (2003).
425
J. Icochea, D. Neira, U. Sinsch, Telmatobius arequipensis. The IUCN Red List of Threatened Species 2004: e.T57324A11620957 (2004); .
426
C. Aguilar et al., Morphological variation of Telmatobius atahualpai (Anura: Telmatobiidae) with comments on its phylogenetic relationships and synapomorphies for the genus. J. Herpetol. 11, 37–49 (2012).
427
L. E. Jarvis, A. Angulo, A. Catenazzi, R. von May, J. L. Brown, E. Lehr, J. Lewis, A re-assessment of priority amphibian species of Peru. Trop. Conserv. Sci. 8, 623–645 (2015).
428
C. Aguilar, K. Siu-Ting, P. Venegas, The rheophilous tadpole of Telmatobius atahualpai Wiens, 1993 (Anura: Ceratophryidae). South Am. J. Herpetol. 2, 165–174 (2007).
429
IUCN SSC Amphibian Specialist Group, Telmatobius atahualpai. The IUCN Red List of Threatened Species 2014: e.T57325A43493919 (2014); .
430
J. Icochea et al., Telmatobius brevipes. The IUCN Red List of Threatened Species 2004: e.T57327A11621958 (2004); .
431
J. Icochea, E. Lehr, C. A. Puntriano, Telmatobius brevirostris. The IUCN Red List of Threatened Species 2004: e.T57328A11622086 (2004); .
432
J. Icochea et al., Telmatobius carrillae. The IUCN Red List of Threatened Species 2004: e.T57329A11622244 (2004); .
433
A. Merino-Viteri, L. Coloma, A. Almendáriz, Los Telmatobius de los Andes de Ecuador y su disminución poblacional. Monografias de Herpetologia 7, 9–37 (2005).
434
J. Icochea, E. Lehr, C. A. Puntriano, Telmatobius colanensis. The IUCN Red List of Threatened Species 2004: e.T57332A11622861 (2004); .
435
R. A. Berenguel, R. K. Elias, T. J. Weaver, R. P. Reading, Chytrid Fungus, Batrachochytrium dendrobatidis, in Wild Populations of the Lake Titicaca Frog, Telmatobius culeus, in Peru. J. Wildl. Dis. 52, 973–975 (2016).
436
J. Icochea et al., Telmatobius culeus. The IUCN Red List of Threatened Species 2004: e.T57334A11623098 (2004); .
437
J. Icochea et al., Telmatobius hockingi. The IUCN Red List of Threatened Species 2004: e.T57341A11624212 (2004); .
438
J. Icochea, E. Wild, C. A. Puntriano, Telmatobius ignavus. The IUCN Red List of Threatened Species 2004: e.T57344A11624617 (2004); .
439
A. Catenazzi, R. von May, V. T. Vredenburg, High prevalence of infection in tadpoles increases vulnerability to fungal pathogen in high-Andean amphibians. Biol. Conserv. 159, 413–421 (2013).
440
A. Catenazzi, R. von May, V. T. Vredenburg, “Conservation of the high Andean frog Telmatobius jelskii along the Peru LNG pipeline in the Regions of Ayacucho and Huancavelica, Peru” in Monitoring Biodiversity: Lessons From a Trans-Andean Megaproject, A. Alonso, F. Dallmeier, G. P. Servat, Eds. (Smithsonian Scholarly Press, Washington, DC, 2013).
441
J. Icochea, U. Sinsch, E. Lehr, Telmatobius jelskii. The IUCN Red List of Threatened Species 2004: e.T57346A11624854 (2004); https://dx.doi.org/10.2305/IUCN.UK.2004.RLTS.T57346A11624854.en.
442
J. Icochea, U. Sinsch, E. Lehr, Telmatobius latirostris. The IUCN Red List of Threatened Species 2004: e.T57348A11625189 (2004); https://dx.doi.org/10.2305/IUCN.UK.2004.RLTS.T57348A11625189.en.
443
R. Ghirardi, Estudio de quitridiomicosis por Batrachochytrium dendrobatidis en anfibios anuros del Litoral, Cuyo y Patagonia Argentina,” Ph.D. dissertation, Facultad de Ciencias Naturales y Museo, Universidad Nacional De la Plata (2012).
444
T. Seimon et al., Identification of chytridiomycosis in Telmatobius marmoratus at 4450 m in the Cordillera Vilcanota of southern Peru. Studies on the Andean Frogs of the Genera Telmatobius and Batrachophrynus. Monografías de Herpetología 7, 275–283 (2005).
445
IUCN SSC Amphibian Specialist Group, Telmatobius marmoratus. The IUCN Red List of Threatened Species 2015: e.T57349A3059350 (2015); .
446
J. Icochea, E. Lehr, Telmatobius mayoloi. The IUCN Red List of Threatened Species 2004: e.T57350A11625750 (2004); .
447
I. D. Riva, L. Trueb, W. E. Duellman, A new species of Telmatobius (Anura: Telmatobiidae) from montane forests of southern Peru, with a review of osteological features of the genus. South Am. J. Herpetol. 7, 91–109 (2012).
448
L. A. Coloma, Telmatobius niger, Centro Jambatu. 2011–2017, Anfibios de Ecuador (Fundación Otonga. Quito, Ecuador, 2016); www.anfibiosecuador.ec/index.php?aw,2.
449
I. De la Riva, Telmatobius sanborni. The IUCN Red List of Threatened Species 2010: e.T135889A4216760 (2010); .
450
IUCN SSC Amphibian Specialist Group, Telmatobius truebae. The IUCN Red List of Threatened Species 2017: e.T57365A3060175 (2017); .
451
A. Merino-Viteri, L. A. Coloma, R. Santiago, Telmatobius vellardi. The IUCN Red List of Threatened Species 2010: e.T57366A11615240 (2010); .
452
M. Lampo, C. J. Senaris, Unexplained amphibian mortalities in the secluded mountains of the Venezuelan Guayana: Is there evidence of chytridiomycosis? Herpetol. Rev. 37, 47–49 (2006).
453
T. A. Seimon, A. Seimon, K. Yager, K. Reider, A. Delgado, P. Sowell, A. Tupayachi, B. Konecky, D. McAloose, S. Halloy, Long-term monitoring of tropical alpine habitat change, Andean anurans, and chytrid fungus in the Cordillera Vilcanota, Peru: Results from a decade of study. Ecol. Evol. 7, 1527–1540 (2017).
454
U. Tobler, B. R. Schmidt, Within- and among-population variation in chytridiomycosis-induced mortality in the toad Alytes obstetricans. PLOS ONE 5, (2010).
455
J. Bosch, S. Fernández-Beaskoetxea, T. W. J. Garner, L. M. Carrascal, Long-term monitoring of an amphibian community after a climate change- and infectious disease-driven species extirpation. Glob. Chang. Biol. 24, 2622–2632 (2018).
456
U. Tobler, A. Borgula, B. R. Schmidt, Populations of a susceptible amphibian species can grow despite the presence of a pathogenic chytrid fungus. PLOS ONE 7, e34667 (2012).
457
A. Spitzen-Van Der Sluijs, A. Martel, C. A. Hallmann, W. Bosman, T. W. Garner, P. Van Rooij, R. Jooris, F. Haesebrouck, F. Pasmans, Environmental determinants of recent endemism of Batrachochytrium dendrobatidis infections in amphibian assemblages in the absence of disease outbreaks. Conserv. Biol. 28, 1302–1311 (2014).
458
K. A. Bates, F. C. Clare, S. O’Hanlon, J. Bosch, L. Brookes, K. Hopkins, E. J. McLaughlin, O. Daniel, T. W. J. Garner, M. C. Fisher, X. A. Harrison, Amphibian chytridiomycosis outbreak dynamics are linked with host skin bacterial community structure. Nat. Commun. 9, 693 (2018).
459
B. A. Mosher, L. L. Bailey, E. Muths, K. P. Huyvaert, Host-pathogen metapopulation dynamics suggest high elevation refugia for boreal toads. Ecol. Appl. 28, 926–937 (2018).
460
E. Muths, D. S. Pilliod, L. J. Livo, Distribution and environmental limitations of an amphibian pathogen in the Rocky Mountains, USA. Biol. Conserv. 141, 1484–1492 (2008).
461
F. M. Brem, K. R. Lips, Batrachochytrium dendrobatidis infection patterns among Panamanian amphibian species, habitats and elevations during epizootic and enzootic stages. Dis. Aquat. Organ. 81, 189–202 (2008).
462
R. Perez, C. L. Richards-Zawacki, A. R. Krohn, M. Robak, E. J. Griffith, H. Ross, B. Gratwicke, R. Ibáñez, J. Voyles, Field surveys in Western Panama indicate populations of Atelopus varius frogs are persisting in regions where Batrachochytrium dendrobatidis is now enzootic. Amphib. Reptile Conserv. 8, 30–35 (2014).
463
L. A. Brannelly, C. L. Richards-Zawacki, A. P. Pessier, Clinical trials with itraconazole as a treatment for chytrid fungal infections in amphibians. Dis. Aquat. Organ. 101, 95–104 (2012).
464
R. McCaffery, C. L. Richards-Zawacki, K. R. Lips, The demography of Atelopus decline: Harlequin frog survival and abundance in central Panama prior to and during a disease outbreak. Glob. Ecol. Conserv. 4, 232–242 (2015).
465
M. Ryan, E. Berlin, R. W. Gagliardo, C. Lacovelli, Further exploration in search of Atelopus varius in Costa Rica. FrogLog 69, 1–2 (2005).
466
J. F. González-Maya, J. L. Belant, S. A. Wyatt, J. Schipper, J. Cardenal, D. Corrales, I. Cruz-Lizano, A. Hoepker, A. H. Escobedo-Galván, F. Castañeda, A. Fischer, Renewing hope: The rediscovery of Atelopus varius in Costa Rica. Amphib.-Reptil. 34, 573–578 (2013).
467
M. Crump, F. R. Hensley, K. L. Clark, Apparent decline of the golden toad: Underground or extinct? Copeia 1992, 413–420 (1992).
468
L. A. Pounds, M. Crump, Amphibian declines and climate disturbance: The case of the golden toad and the harlequin frog. Conserv. Biol. 8, 72–85 (1994).
469
S. K. Jacobson, J. J. Vandenberg, Reproductive ecology of the endangered golden toad (Bufo periglenes). J. Herpetol. 25, 321–327 (1991).
470
S. E. Greenspan, C. Lambertini, T. Carvalho, T. Y. James, L. F. Toledo, C. F. B. Haddad, C. G. Becker, Hybrids of amphibian chytrid show high virulence in native hosts. Sci. Rep. 8, 9600 (2018).
471
T. Silva-Soares, P. V. Scherer, Amphibians of Parque Estadual do Forno Grande, State of Espírito Santo, Southeastern Brazil: Species composition and conservation. North-West. J. Zool. 9, 113–120 (2013).
472
M. V. Garey, D. B. Provete, I. A. Martins, C. F. B. Haddad, D. C. Rossa-Feres, Anurans from the Serra da Bocaina National Park and surrounding buffer area, southeastern Brazil. Check List 10, 308–316 (2014).
473
B. J. Doddington, J. Bosch, J. A. Oliver, N. C. Grassly, G. Garcia, B. R. Schmidt, T. W. J. Garner, M. C. Fisher, Context-dependent amphibian host population response to an invading pathogen. Ecology 94, 1795–1804 (2013).
474
I. De la Riva, “Bolivian frogs of the genus Telmatobius (Anura: Leptodactylidae): synopsis, taxonomic comments, and description of a new species” in Studies on the Andean Frogs of the Genera Telmatobius and Batrachophrynus, E. O. Lavilla, I. De la Riva, Eds. (Monografías de Herpetología, Asociacíon Herpetológica Española, 2005), vol. 7, pp. 65–101.
475
I. De la Riva, E. O. Lavilla, “Essay 9.2. Conservation status of the Andean frogs of the genera Telmatobius and Batrachophrynus” in Threatened Amphibians of the World, S. N. Stuart, M. Hoffmann, J. S. Chanson, N. A. Cox, R. Berridge, P. Ramani, B. E. Young, Eds. (Lynx Ediciones, with IUCN - The World Conservation Union, Conservation International, and NatureServe, Barcelona, 2008).
476
P. A. Burrowes, I. De la Riva, Unraveling the historical prevalence of the invasive chytrid fungus in the Bolivian Andes: Implications in recent amphibian declines. Biol. Invasions 19, 1781–1794 (2017).
477
S. Barrionuevo, S. Mangione, Chytridiomycosis in two species of Telmatobius (Anura: Leptodactylidae) from Argentina. Dis. Aquat. Organ. 73, 171–174 (2006).
478
S. Barrionuevo, M. L. Ponssa, Declines of three species of the genus Telmatobius (Anura: Leptodactylidae) from Tucumán Province, Argentina. Herpetologica 64, 47–62 (2008).
479
M. Vaira et al., Categorización del estado de conservación de los anfibios de la República Argentina. Cuad. Herpetol. 26, 131–159 (2012).
480
A. Catenazzi, A. Swei, J. Finkle, E. Foreyt, L. Wyman, V. T. Vredenburg, Epizootic to enzootic transition of a fungal disease in tropical Andean frogs: Are surviving species still susceptible? PLOS ONE 12, e0186478 (2017).
481
D. Burkart, S. V. Flechas, V. T. Vredenburg, A. Catenazzi, Cutaneous bacteria, but not peptides, are associated with chytridiomycosis resistance in Peruvian marsupial frogs. Anim. Conserv. 20, 483–491 (2017).
482
A. Catenazzi, S. V. Flechas, D. Burkart, N. D. Hooven, J. Townsend, V. T. Vredenburg, Widespread elevational occurrence of antifungal bacteria in Andean amphibians decimated by disease: A complex role for skin symbionts in defense against chytridiomycosis. Front. Microbiol. 9, 465 (2018).
483
C. Cortez, S. Reichle, L. Rodríguez, J. L. Martinez, J. Köhler, W. Arizabal, Pristimantis platydactylus. The IUCN Red List of Threatened Species 2004: e.T56866A11534791 (2004); .
484
A. Arteaga, L. Bustamante, J. M. Guayasamin, Amphibians and Reptiles of Mindo: Life in the Coudforest (Serie de Publicaciones Científicas, Universidad Tecnológica Indoamérica, Quito, Ecuador, 2013), pp. 1–257.
485
D. T. McKnight, R. A. Alford, C. J. Hoskin, L. Schwarzkopf, S. E. Greenspan, K. R. Zenger, D. S. Bower, Fighting an uphill battle: The recovery of frogs in Australia’s Wet Tropics. Ecology 98, 3221–3223 (2017).
486
D. Newell, “An update on frog declines from the forests of subtropical eastern Australia” in Status of Conservation and Decline of Amphibians: Australia, New Zealand, and Pacific Islands, H. Heatwole, J. Rowley, Eds. (CSIRO Publishing, 2018), chap. 5.
487
S. J. Richards, R. A. Alford, Structure and dynamics of a rainforest frog (Litoria genimaculata) population in northern Queensland. Aust. J. Zool. 53, 229–236 (2005).
488
M. Alvarado-Rybak, “Epidemiology of Batrachochytrium dendrobatidis in Chile and the role of the invasive African clawed frog (Xenopus laevis) as a vector,” thesis, Universidad Andres Bello, Chile (2019).
489
L. Bacigalupe, I. Vasquez, S. Estay, A. Valenzuela-Sánchez, M. Alvarado-Rybak, A. Peñafiel-Ricaurte, A. A. Cunningham, C. Soto-Azat, 20.9. Batrachochytrium dendrobatidis in a biodiversity hotspot: Identifying and validating high-risk areas and refugia. Ecosphere 10, e02724 (2019).
490
A. Valenzuela-Sánchez, G. Medina-Vogel, Importancia de las enfermedades infecciosas para la conservación de la fauna silvestre amenazada de Chile. Gayana (Concepc.) 78, 57–69 (2017).
491
M. Folly, A. M. Bezerra, J. Ruggeri, F. Hepp, A. M. P. T. Carvalho-e-Silva, M. R. Gomes, S. P. Carvalho-e-Silva, Anuran fauna of the high-elevation areas of the Parque Nacional da Serra dos Órgãos (PARNASO), southeastern Brazil. Oecol. Aust. 20, 109–120 (2016).
492
H. G. Bergallo, C. F. D. Rocha, M. A. S. Alves, M. Sluys, A fauna ameaçada de extinção do Estado do Rio de Janeiro (EdUERJ, Rio de Janeiro, 2000), p. 166.
493
C. F. B. Haddad et al., Avaliação do Risco de Extinção de Aplastodiscus flumineus (Cruz & Peixoto, 1985 “1984”). Processo de avaliação do risco de extinção da fauna brasileira (ICMBio, 2016); www.icmbio.gov.br/portal/biodiversidade/fauna-brasileira/estado- de-conservacao/7672-anfibios-aplastodiscus-flumineus.html.
494
IUCN SSC Amphibian Specialist Group, Telmatobius punctatus. The IUCN Red List of Threatened Species 2017: e.T136129A517865 (2017); .
Information & Authors
Information
Published In
Science
Volume 363 • Issue 6434 • 29 March 2019
Pages: 1459 - 1463
History
Received: 9 August 2018
Accepted: 6 February 2019
Copyright
Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.
This is an article distributed under the terms of the Science Journals Default License.
RE: Amphibian loss inWestern Oregon U.S.A.
Has any research been done to frog loss in my area or western Oregon. Anecdotally we have heard loud frog chorus's in our wetland area near creeks and small streams. For the past several years this spring time ritual has not been heard at all. I am not qualified to identify these frogs but they may be Pacific tree frogs ranadae ?