Golden toad

Last updated

Golden toad
Bufo periglenes2.jpg
Male golden toad
Status iucn3.1 EX.svg
Extinct  (1989)  (IUCN 3.1) [1]
Scientific classification Red Pencil Icon.png
Kingdom: Animalia
Phylum: Chordata
Class: Amphibia
Order: Anura
Family: Bufonidae
Genus: Incilius
I. periglenes
Binomial name
Incilius periglenes
(Savage, 1966)

Bufo periglenes
Cranopsis periglenes
Ollotis periglenes


The golden toad (Incilius periglenes, formerly Bufo periglenes) is an extinct species of true toad that was once abundant in a small, high-altitude region of about 4 square kilometres (1.5 sq mi) in an area north of the city of Monteverde, Costa Rica. [2] It was endemic to elfin cloud forest. [3] Also called the Monte Verde toad, Alajuela toad and orange toad, it is commonly considered the "poster child" for the amphibian decline crisis. [4] This toad was first described in 1966 by herpetologist Jay Savage. [2] The last sighting of a single male golden toad was on 15 May 1989, and it has since been classified as extinct by the International Union for Conservation of Nature (IUCN). [1]


The golden toad was one of about 500 species in the family Bufonidae—the "true toads". Males were orange and sometimes slightly mottled on the belly, while females showed a greater variety of colors, including black, yellow, red, green, and white; both sexes had smooth skin. While males had brilliant orange that attracted females to mate, females are covered with a dark, charcoal colored outlined with yellow lines. [5] Sexual dimorphism played a key role in identifying females, who were typically larger than males. Body length ranged from 39 to 48 mm in males and from 42 to 56 mm in females. Males had proportionally longer limbs and longer, more acute noses than females. [6] Females also had enlarged cranial crests above the level of the orbit (eye socket), while in males the crests were much lower. [7]

Individuals spent the majority of their lives in moist burrows, in particular during the dry season. [3] The average lifespan of the golden toad is unknown, but other amphibian species in the family Bufonidae have an average lifespan of 10–12 years. [8]

Habitat and distribution

The golden toad inhabited northern Costa Rica's Monteverde Cloud Forest Reserve, in a cloud forest area north of the city of Monteverde.[ citation needed ] It was distributed over an area no more than 8 km2 and possibly as little as 0.5 km2 in extent, at an average elevation of 1,500 to 1,620 m. [9] The species seemed to prefer the lower elevations. [7]


The golden toad's main habitat was on a cold, wet ridge called Brillante. They would emerge in late March through April to mate for the first few weeks in rainwater pools amongst tree roots, where they also laid their eggs. [3] [10] 1500 golden toads were reported to breed at the site since 1972. The last documented breeding episode occurred from April–May 1987. [11]

For a few weeks in April, after the dry season ended and the forest became wetter, males would gather in large numbers near ground puddles and wait for the females. Golden toads were found to breed explosively when it rained heavily from March to June. [12] Males would clasp onto any other individuals encountered and only then identify the partner's gender. As soon as a male found a female golden toad, he would engage in amplexus with the female until she laid spawned. [13] The males would fight with each other for opportunities to mate until the end of their short mating season, after which the toads retreated to their burrows. [14]

Males outnumbered females, in some years by as many as ten to one, a situation that often led bachelors to attack amplectant pairs and form what has been described as a "writhing masses of toad balls". [2] During the 1977 and 1982 seasons, males outnumbered females by over 8 to 1 at breeding pools. Each toad couple produced 200–400 eggs each week for the six-week mating period, with each egg approximately 3 mm in diameter. The eggs of the golden toad, black and tan spheres, were deposited in small pools often no more than one-inch deep. Tadpoles emerged in a matter of days but required another four or five weeks for metamorphosis. During this period, they were highly dependent on the weather. Too much rain and they would be washed down the steep hillsides; too little and their puddles would dry up.

In 1987, an American ecologist and herpetologist, Martha Crump, recorded the golden toad's mating rituals. In her book, In Search of the Golden Frog, she described it as "one of the most incredible sights I've ever seen", and said they looked like "statues, dazzling jewels on the forest floor". On April 15, 1987, Crump recorded in her field diary that she counted 133 toads mating in one "kitchen sink-sized pool" that she was observing. Five days later, she witnessed the pools in the area drying, which she attributed to the effects of the El Niño-Southern Oscillation, "leaving behind desiccated eggs already covered in mold". The toads attempted to mate again that May. Of the 43,500 eggs that Crump found, only twenty-nine tadpoles survived the drying of the forest's ground. [15]

Conservation history

The Monteverde Cloud Forest Preserve, the golden toad's previous habitat Monte verde.jpg
The Monteverde Cloud Forest Preserve, the golden toad's previous habitat

Jay Savage discovered the golden toad in 1964. [2] From their discovery in 1964 for about 17 years, and from April to July in 1987, population sizes of ~1500 adult toads were reported. [16] As the population was very small and localized, a reserve of 4 km2 was established around the known locality, eventually expanded to cover 105 km2. [17] Only ten [1] or eleven toads were seen in 1988, [16] including one seen by Martha Crump, and none have been seen since May 15, 1989, when Crump last saw the same solitary male toad that she had seen the year before. [14]

In the period between its discovery and disappearance, the golden toad was commonly featured on posters promoting the biodiversity of Costa Rica. [18] Another species, Holdridge's toad, was declared extinct in 2008 but has since been rediscovered. [19]


The Global Amphibian Assessment (GAA) listed 427 species as "critically endangered" in its extensive analysis, including 122 species that could be “possibly extinct”.[ citation needed ] A majority of species, including the golden toad, have declined in numbers even in seemingly undisturbed environments. [7] As late as 1994, five years after the last sighting, researchers still hoped that I. periglenes continued to live in burrows, as similar toad species have lifespans of up to twelve years. [16] By 2004 IUCN listed the species as extinct, after an evaluation involving Savage (who had first discovered them 38 years earlier). IUCN's conclusion was based on the lack of sightings since 1989 and the "extensive searching" that had been done since without result. [1] In August 2010 a search organised by the Amphibian Specialist Group of the International Union for Conservation of Nature, aiming to verify the status of various species of frogs thought to be extinct in the wild, failed to find evidence of surviving specimens. [20]

Since records of golden toads were consistently collected, their rapid disappearance was well documented, yet the causes remain poorly understood. After 1989, there have been no verified documented sightings. The disappearance was originally attributed to a severe neotropical drought in 1987–1988, but other factors have since been treated as more likely causes. [17] The IUCN has given numerous possible reasons for the species' extinction, including its "restricted range, global warming, chytridiomycosis and airborne pollution". [1] Jennifer Neville examined the different hypotheses explaining the extinction in her article "The Case of the Golden Toad: Weather Patterns Lead to Decline", and concluded that Crump's El Niño hypothesis is "clearly supported" by the available data. [16] In her article, Neville discussed the flaws in other hypotheses explaining the toad's decline. The UV-B radiation theory, which suggest that the decline in golden toads resulted from an increase in UV-B radiation, has little evidence supporting it because there was no high elevation UV-B radiation recorded, also, there is little evidence that an increase in UV-B radiation would have an effect on anurans. [16] Another theory is that the anuran water loss from dry conditions helped cause high mortality rates among adults, although this point is hotly contested. [3]

In 1991, ML Crump, FR Hensley and KL Clark attempted to understand whether the decline of the golden toad in Costa Rica meant that the species was underground or extinct. They found that each year from the early 1970s–1987 golden toads emerged from retreats to breed during April–June. During the time of the study in 1991, the most recent known breeding episode occurred during April/May 1987. Over 1500 adults were observed at five breeding pools, but a maximum of 29 tadpoles metamorphosed from these sites. During April–June 1988–90, Crump et al. found only 11 toads during surveys of the breeding habitat. To study the species' decline, they analyzed rainfall, water temperature, and pH of the breeding pools. The data on weather patterns and characteristics of the breeding habitat unveiled that warmer water temperatures and less precipitation during dry season after 1987 could have caused adverse breeding conditions. The toads may have actually been alive and hiding in retreats, waiting for appropriate weather conditions. The scarcity of toads could have been a normal population response to an unpredictable environment. [9] However this hypothesis is unlikely to be still valid after close to 30 years. Furthermore, there have been many mating seasons since 1987 with very favorable conditions but no reappearance of the species. [16]

Climate hypothesis

Climate variability is strongly dominated by dry season influences from the El Niño Southern Oscillation events. [21] In 1986–87, El Niño caused the lowest recorded rainfall and highest temperature in Monteverde, Costa Rica. The shift of climate during El Niño is caused by the increased atmospheric pressure in the Atlantic and decreased in the Pacific. The wind reduced the amount of rains on the Pacific-facing slopes, and the temperature during the dry season was dramatically higher than usual. [13] At that time, researchers were not certain if the toads were waiting for wetter mating conditions to return or if they had simply died off.

Fungus infection hypotheses

In Atelopus , another genus found in the tropical Americas, an estimated 67% of the ~110 species of have become extinct or endangered, and the pathogenic chytrid fungus Batrachochytrium dendrobatidis , which causes chytridiomycosis, is implicated in this regard. [7]

Three hypotheses of how the chytrid fungus could have caused the extinction of the golden toad were reviewed by Rohr et al. [22] They include the spatiotemporal-spread hypothesis, the climate-linked-epidemic hypothesis, and the chytrid-thermal-optimum hypothesis. The spatiotemporal-spread hypothesis claims that B. dendrobatidis related decreases in population are a result of the introduction and spread of B. dendrobatidis, independent of climate changes. The climate-linked-epidemic hypothesis says the decline was a result of a climate change interacting with a pathogen. This hypothesis leads to a paradox because B. dendrobatidis is a cold-tolerant pathogen. [23] The chytrid-thermal-optimum hypothesis proposes that global warming increased cloud cover in warm years, resulting in the concurrence of daytime cooling and nighttime warming, temperatures that are the optimal thermal temperature for B. dendrobatidis growth. [22] This theory is controversial. [24]

Another explanation has been termed the chytrid thermal optimum hypothesis. An earlier study by Pounds and Crump based on the El Niño event in 1986–1987 [25] had concluded, after observing the dry conditions from higher temperatures and lower seasonal rainfall, that this could potentially have caused the extinction. When chytridiomycosis was eventually identified as a major cause of amphibian extinctions throughout the world, a connection between these causes was hypothesized. [26] To test it, they used radiocarbon and chronology validation to test the amount of δ18O (delta-O-18) which is commonly used as a measure of the temperature of precipitation. They found that in the El Niño Southern Oscillation (ENSO) years showed a strong mean positive anomaly of 2.0% for 1983, 1987, and 1998 which is greater than 2σ above the mean. These strong positive anomalies are indicators of periods of lower precipitation and temperature differences of greater than 1 degree Celsius. [26]

In conjunction with the chytrid-thermal-optimum hypothesis, the climate-linked-epidemic hypothesis also suggests a correlation between climate change and the amphibian pathogen. Unlike the chytrid-thermal-optimum hypothesis, the climate-linked-epidemic hypothesis does not assume a direct chain of events between warmer weather and disease outbreak. This interpretation assumes that global climate change has a direct link to species extinctions, arguing that "the patterns of increasing dry days implicate rising global temperatures due to anthropogenic greenhouse gas emissions." [21] Taking the results and recent findings that tie the golden toad's population crash to disease, the authors concluded that climate-driven epidemics are an immediate threat to biodiversity. It also points to a chain of events whereby this warming may accelerate disease development by translating into local or microscale temperature shifts—increases and decreases—favourable to Bd. [7]

Notably, B. dendrobatidis becomes increasingly malignant under cold and moist conditions. Hence, the idea that the pathogen spreads in warmer climates is paradoxical. It is possible that the warmer climate made the species more susceptible to disease, or that warm years could have favored Batrachochytrium directly. [7]

In contrast to both the chytrid-thermal-optimum hypothesis and the climate-linked-epidemic hypothesis, the spatiotemporal-spread hypothesis suggests that population decline due to B. dendrobatidis was caused by the introduction and spread of B. dendrobatidis from a finite amount of introduction sites in a way unaffected by climate change. Mantel tests of all the possible origins of B. dendrobatidis were used to see if their hypothesis was correct. They did see positive correlations between spatial distance and distance in timing of declass and the lat year observed. "Coincident mass extirpation of neotropical amphibians with the emergence of the infectious fungal pathogen Batrachochytrium dendrobatidis" by Tina L. Cheng et al., also parallels with the spatiotemporal-spread hypothesis by tracking the origins of B. dendrobatidis and tracking it from Mexico to Costa Rica. Furthermore, this study also shows that local amphibian species could have extreme susceptibility to B. dendrobatidis which could result in population decline. [27]

There has been evidence that contradicts the theory of fungus killing off the golden toads. Three collected and preserved specimens of I. periglenes were found to be negative for B. dendrobatidis. There is a possibility that the B. dendrobatidis was too damaged to detect, but even with this data, there is not enough to prove that climate change had a significant enough impact on the growth and spreading of the deadly fungus. It is possible that either the testing methods were not robust enough to detect the nascent infection, or that the specimens were too damaged to be tested. The more likely explanation is that the specimens were collected prior to the presumptive emergence and documentation of B. dendrobatidis in Monteverde. It is very likely that B. dendrobatidis played a role in the extinction of the golden toad, but there are still not enough data for a conclusive verdict. [4]

See also

Related Research Articles

Chytridiomycota division of fungi

Chytridiomycota are a division of zoosporic organisms in the kingdom Fungi, informally known as chytrids. The name is derived from the Greek χυτρίδιον chytridion, meaning "little pot", describing the structure containing unreleased zoospores. Chytrids are one of the early diverging fungal lineages, and their membership in kingdom Fungi is demonstrated with chitin cell walls, a posterior whiplash flagellum, absorptive nutrition, use of glycogen as an energy storage compound, and synthesis of lysine by the α-amino adipic acid (AAA) pathway.

Decline in amphibian populations Ongoing mass extinction of amphibian species worldwide

The decline in amphibian populations is an ongoing mass extinction of amphibian species worldwide. Since the 1980s, decreases in amphibian populations, including population crashes and mass localized extinctions, have been observed in locations all over the world. These declines are known as one of the most critical threats to global biodiversity

Chytridiomycosis disease affecting amphibians

Chytridiomycosis is an infectious disease in amphibians, caused by the chytrid fungi Batrachochytrium dendrobatidis and Batrachochytrium salamandrivorans, a nonhyphal zoosporic fungus. Chytridiomycosis has been linked to dramatic population declines or even extinctions of amphibian species in western North America, Central America, South America, eastern Australia, East Africa (Tanzania), and Dominica and Montserrat in the Caribbean. Much of the New World is also at risk of the disease arriving within the coming years. The fungus is capable of causing sporadic deaths in some amphibian populations and 100% mortality in others. No effective measure is known for control of the disease in wild populations. Various clinical signs are seen by individuals affected by the disease. A number of options are possible for controlling this disease-causing fungus, though none has proved to be feasible on a large scale. The disease has been proposed as a contributing factor to a global decline in amphibian populations that apparently has affected about 30% of the amphibian species of the world. However recent research has shown the evidence linking chytrid fungi and chytridiomycosis to global amphibian declines is minimal to-date.

Mountain yellow-legged frog species of amphibian

The mountain yellow-legged frog, also known as the southern mountain yellow-legged frog is a species of true frog endemic to California in the United States. It occurs in the San Jacinto Mountains, San Bernardino Mountains, and San Gabriel Mountains in Southern California and the Southern Sierra Nevada. It is a federally listed endangered species.

<i>Atelopus</i> genus of amphibians

Atelopus is a large genus of true toads, commonly known as harlequin toads or stubfoot toads, from Central and South America, ranging as far north as Costa Rica and as far south as Bolivia. Atelopus species are small, generally brightly colored, and diurnal. Most species are associated with mid-to-high elevation streams. This genus has been greatly affected by amphibian declines, and many species are now considered endangered, while others already are extinct. While threatened by habitat loss, pollution, and introduced species, the primary cause of these declines appears to be the chytrid fungus Batrachochytrium dendrobatidis. For example, there are 32 known Atelopus species in Ecuador. One of these is data deficient, two are endangered and the remaining are critically endangered. Almost half the Ecuador species have not been recorded in a decade or more and are likely extinct. In some species conservationists have established captive colonies as a safeguard.

Wyoming toad Species of amphibian

The Wyoming toad or Baxter's toad is an extremely rare amphibian that exists only in captivity and within Mortenson Lake National Wildlife Refuge in Wyoming in the United States. The Wyoming toad was listed as an endangered species in 1984, and listed as extinct in the wild since 1991. As with ferrets at the Tom Thorne and Beth Williams Wildlife Research Center at Sybille, the effort to save the Wyoming toad, Bufo baxteri, has also been a cooperative effort among state and federal agencies and private landowners. The Wyoming toad was common from the 1950s through the early 1970s, but its distribution was limited to the Laramie Basin in Albany County. The population crashed around 1975 and was extremely rare by 1980. The Wyoming toad was federally listed as endangered in January 1984. To prevent extinction, a captive breeding program was begun in 1989 at the Thorne Williams Unit. This program produced enough offspring in the first few years to supply seven different zoos, and in 1998 the Saratoga National Fish Hatchery received captive breeding stock. Between 1995 and 2006, when the remaining captive stock was moved from the Thorne Williams Unit to the Red Buttes Environmental Biology Laboratory south of Laramie, nearly 46,000 offspring were produced at the Thorne Williams Unit and released back into the wild. Before the sharp declines occurred, this toad was classified as a subspecies of the Canadian toad.

Holdridge's toad is a species of toad endemic to Costa Rica. In October 2008, it was declared extinct by the International Union for the Conservation of Nature in its Red List since the species had not been seen since 1987, despite years of extensive searches. However, the species was rediscovered in 2010 by a Costa Rican herpetologist and is now classified as critically endangered. It is believed that the species is most threatened by the presence of the chytrid fungus in its habitat.

Boreal toad subspecies of amphibian

The boreal toad is a subspecies of the western toad. They are commonly found in the Southern Rocky Mountains and in recent, their population has been on the decline due to an emerging amphibian disease, chytrid fungus. The boreal toad is currently listed as an endangered species by Colorado and New Mexico. It is known in Colorado as the only alpine species of toad.

<i>Batrachochytrium dendrobatidis</i> species of fungus

Batrachochytrium dendrobatidis, also known as Bd or the amphibian chytrid fungus, is a fungus that causes the disease chytridiomycosis in amphibians.

The extinction risk of global warming is the risk of species becoming extinct due to the effects of global warming. This may be Earth's sixth major extinction, often called the Anthropocene or Holocene extinction.

Panamanian golden frog Species of amphibian

The Panamanian golden frog, also known as Cerro Campana stubfoot toad and other names, is a species of toad endemic to Panama. Panamanian golden frogs inhabit the streams along the mountainous slopes of the Cordilleran cloud forests of west-central Panama. While the IUCN lists it as critically endangered, it may in fact have been extinct in the wild since 2007. Individuals have been collected for breeding in captivity in a bid to preserve the species. The alternative common name, Zetek's golden frog, and the epithet zeteki both commemorate the entomologist James Zetek.

<i>Atelopus varius</i> species of amphibian

Atelopus varius, the Costa Rican variable harlequin toad or clown frog, is a small Neotropical true toad from the family Bufonidae. Once ranging from Costa Rica to Panama, A. varius is now listed as critically endangered and has been reduced to a single remnant population near Quepos, Costa Rica and has only relict populations in western Panama (IUCN). Recent variation in air temperature, precipitation, stream flow patterns, and the subsequent spread of a pathogenic chytrid fungus (Batrachochytrium dendrobatidis) linked to global climate change have been the leading cause of decline for A. varius. A. zeteki has been considered a subspecies of A. varius, but is now generally considered a separate species.

Guajira stubfoot toad species of amphibian

The Guajira stubfoot toad or Carrikeri harlequin frog, Atelopus carrikeri, is a species of toad in the family Bufonidae. It is about 5 cm (2.0 in) long and typically black, though some populations have orange coloration. This species is endemic to the Sierra Nevada de Santa Marta mountain range of northern Colombia. It is critically endangered because of the chytrid fungus, Batrachochytrium dendrobatidis, and habitat destruction due to agriculture. The species had not been seen from 1994 until it was rediscovered in early 2008.

<i>Espadarana prosoblepon</i> species of amphibian

Centrolene prosoblepon is a species of frog in the family Centrolenidae, commonly known as the emerald glass frog or Nicaragua giant glass frog. This species can be found in Ecuador, Colombia, Panama, Costa Rica, Nicaragua, and Honduras. Its natural habitats are lowland tropical forests and montane cloud forests. It is a nocturnal species occurring in low vegetation in mature forests only. It is not considered threatened overall by the IUCN although deforestation and pollution are potential threats, as is chytridiomycosis.

Costa Rica brook frog species of amphibian

The Costa Rica brook frog or red-eyed stream frog is a species of frog in the family Hylidae found in Costa Rica and Panama. Its natural habitats are tropical moist lowland forests, subtropical or tropical moist montane forests, and rivers.

Green-eyed treefrog species of amphibian

The green-eyed treefrog is a species of Australasian treefrog in the family Pelodryadidae that occurs in the Wet Tropics of Australia.

<i>Calyptocephalella</i> species of amphibian

Calyptocephalella is a genus of frogs in the family Calyptocephalellidae. It is represented by a single living species, Calyptocephalella gayi, commonly known as the helmeted water toad, Chilean helmeted bull frog or wide-mouth toad. Additionally, there are a few extinct species that only are known from Late Cretaceous and Paleogene fossil remains from Patagonia in South America and in the Antarctic Peninsula. The helmeted water toad living today is aquatic to semi-aquatic, and found in deep ponds and reservoirs in central Chile and possibly adjacent west-central Argentina.

<i>Batrachochytrium salamandrivorans</i> Species of pathogenic chytrid fungus that infects amphibian species

Batrachochytrium salamandrivorans (Bsal) is a pathogenic chytrid fungus that infects amphibian species. salamanders and newts seem to be the most susceptible, however some anuran species are susceptible. Bsal has emerged recently and poses a major threat to species in Europe and North America.

Karen Lips US herpetologist

Karen R. Lips is a Professor of Biology at University of Maryland, College Park. Lips' work more than 20 years ago eventually contributed to the identification of the chytrid fungus as the primary cause of frog decline worldwide.

Lee Berger, is an Australian biologist and veterinarian, who discovered during her Ph.D that the fungus Batrachochytrium dendrobatidis was responsible for the decline and extinction of hundreds of amphibian species.


  1. 1 2 3 4 5 Savage, J., Pounds, J. & Bolaños, F. (2008). Incilius periglenes. The IUCN Red List of Threatened Species doi:10.2305/IUCN.UK.2008.RLTS.T3172A9654595.en
  2. 1 2 3 4 Jay Savage (1965). "An extraordinary new toad from Costa Rica". Revista de Biología Tropical. 14: 153–167. Archived from the original on 2015-06-26. Retrieved 2009-01-13.
  3. 1 2 3 4 Pounds, J. Alan; Crump, Martha L. (1994). "Amphibian declines and climate disturbance: The case of the golden toad and the harlequin frog". Conservation Biology. 8 (1): 72–85. doi:10.1046/j.1523-1739.1994.08010072.x. JSTOR   2386722.
  4. 1 2 Richards-Hrdlicka, K. L. (2013). "Preserved specimens of the extinct golden toad of Monteverde (Cranopsis periglenes) tested negative for the amphibian chytrid fungus (Batrachochytrium dendrobatidis)". Journal of Herpetology. 47 (3): 456–458. doi:10.1670/11-243.
  5. "Reproductive Ecology of the Endangered Golden Toad (Bufo periglenes)". September 23, 2018.
  6. "Recently Extinct Animals – Species Info – Golden Toad". October 28, 2015. Archived from the original on March 4, 2016.
  7. 1 2 3 4 5 6 Alan Pounds, J.; Bustamante, M. N. R.; Coloma, L. A.; Consuegra, J. A.; Fogden, M. P. L.; Foster, P. N.; La Marca, E.; Masters, K. L.; Merino-Viteri, A. S.; Puschendorf, R.; Ron, S. R.; Sánchez-Azofeifa, G. A.; Still, C. J.; Young, B. E. (2006). "Widespread amphibian extinctions from epidemic disease driven by global warming". Nature. 439 (7073): 161–167. Bibcode:2006Natur.439..161A. doi:10.1038/nature04246. PMID   16407945.
  8. Blaustein, A.B. (1994). "Chicken little or nero's fiddle? A perspective on declining amphibian populations" (PDF). Herpetologica. 50 (1): 85–97. JSTOR   3892877. Archived from the original (PDF) on 2019-06-14.
  9. 1 2 Crump, M. L.; Hensley, F. R.; Clark, K. L. (1992). "Apparent Decline of the Golden Toad: Underground or Extinct?" (PDF). Copeia. 1992 (2): 413–420. doi:10.2307/1446201. JSTOR   1446201. Archived from the original (PDF) on 2014-05-05.
  10. Mattoon, Ashley (July–August 2000). "Amphibia fading". World Watch. 13 (4): 12–23. Archived from the original on 2013-10-29. Retrieved 2013-10-24.
  11. Sarkar, Sahotra (March 1996). "Ecological Theory and Anuran Declines". BioScience. 46 (3): 199–207. doi: 10.2307/1312741 . JSTOR   1312741. Lock-green.svg
  12. Jacobson, S. K.; Vandenberg, J. J. (September 1991). "Reproductive Ecology of the Endangered Golden Toad (Bufo periglenes)". Journal of Herpetology. 25 (3): 321–327. doi:10.2307/1564591. JSTOR   1564591.
  13. 1 2 "The Extinction of the Golden Toad FINAL". Retrieved 2015-10-29.
  14. 1 2 Flannery, Tim (2005). The Weather Makers . Toronto, Ontario: HarperCollins. pp.  114–119. ISBN   978-0-87113-935-1.
  15. Crump, Marty (1998). In Search of the Golden Frog quoted in Flannery.
  16. 1 2 3 4 5 6 Neville, Jennifer J. (2003). "The Case of the Golden Toad: Weather Patterns Lead to Decline". North Ohio Association of Herpetologists. Archived from the original on October 10, 2004. Retrieved July 27, 2006.
  17. 1 2 Ochoa-Ochoa, Leticia (October 29, 2015). "The Demise of the Golden Toad and the Creation of a Climate Change Icon Species". Conservation and Society. 11 (3): 291. doi: 10.4103/0972-4923.121034 . Lock-green.svg
  18. Phillips, K. 1994. Tracking the vanishing frogs. New York: Penguin. 244 p. Cited in Neville.
  19. "Reconsidering Extinction: Rediscovery of Incilius holdridgei (Anura: Bufonidae) in Costa Rica After 25 Years". ResearchGate. Retrieved 2015-12-27.
  20. Black, Richard (2010-08-09). "Global hunt begins for 'extinct' species of frogs". BBC News . Retrieved 2010-08-09.
  21. 1 2 Anchukaitis, Kevin J.; Evans, Michael N. (2010-03-16). "Tropical cloud forest climate variability and the demise of the Monteverde golden toad". Proceedings of the National Academy of Sciences. 107 (11): 5036–5040. Bibcode:2010PNAS..107.5036A. doi:10.1073/pnas.0908572107. ISSN   0027-8424. PMC   2841931 . PMID   20194772.
  22. 1 2 Rohr, J. R.; Raffel, T. R.; Romansic, J. M.; McCallum, H.; Hudson, P. J. (2008). "Evaluating the links between climate, disease spread, and amphibian declines". Proceedings of the National Academy of Sciences. 105 (45): 17436–17441. Bibcode:2008PNAS..10517436R. doi:10.1073/pnas.0806368105. PMC   2582253 . PMID   18987318.
  23. Berger, L; Speare, R; Hines, HB; Marantelli, G; Hyatt, AD; McDonald, KR; Skerratt, LF; Olsen, V; Clarke, JM; Gillespie, G; Mahony, M; Sheppard, N; Williams, C; Tyler, MJ (July 2004). "Effect of season and temperature on mortality in amphibians due to chytridiomycosis". Australian Veterinary Journal. 82 (7): 434–439. CiteSeerX . doi:10.1111/j.1751-0813.2004.tb11137.x. PMID   15354853.
  24. Alford, Ross A.; Bradfield, K. S.; Richards, S. J. (31 May 2007). "Ecology – Global warming and amphibian losses" (PDF). Nature. 447 (7144): E3–E6. Bibcode:2007Natur.447....3A. doi:10.1038/nature05940. PMID   17538571.
  25. "El Niño and a Pathogen Killed Costa Rican Toad, Study Finds". The Earth Institute – Columbia University. 2010-03-01. Retrieved 2012-08-16.
  26. 1 2 Anchukaitis, K. J.; Evans, M. N. (2010). "Tropical cloud forest climate variability and the demise of the Monteverde golden toad". Proceedings of the National Academy of Sciences. 107 (11): 5036–5040. Bibcode:2010PNAS..107.5036A. doi:10.1073/pnas.0908572107. PMC   2841931 . PMID   20194772.
  27. Cheng, T. L.; Rovito, S. M.; Wake, D. B.; Vredenburg, V. T. (2011). "Coincident mass extirpation of neotropical amphibians with the emergence of the infectious fungal pathogen Batrachochytrium dendrobatidis". Proceedings of the National Academy of Sciences. 108 (23): 9502–9507. Bibcode:2011PNAS..108.9502C. doi:10.1073/pnas.1105538108. PMC   3111304 . PMID   21543713.

Further reading