|Male golden toad|
The golden toad (Incilius periglenes) was a small true toad that was once abundant in a small, high-altitude region about 4 square kilometres (1.5 sq mi) in area north of the city of Monteverde, Costa Rica. It is also called the golden toad of Monteverde or the Monte Verde toad, and is commonly considered to be the "poster child" for the amphibian decline crisis. Other common English names include Alajuela toad and orange toad. This toad was first described in 1966 by herpetologist Jay Savage. On 15 May 1989, a single male golden toad was found, but no sightings of B. periglenes have been reported since that time, so it is classified by the International Union for Conservation of Nature (IUCN) as an extinct species. Its sudden extinction may have been caused by a chytrid fungus and extensive habitat loss.
The golden toad was one of more than 500 species in the family Bufonidae—the "true toads". It inhabited northern Costa Rica’s Monteverde Cloud Forest Reserve, distributed over an area of roughly 4 square kilometres (1.5 sq mi) at an average elevation of 1,500 metres (4,900 ft). These toads lived in areas where the land area decreased with increasing elevation[clarification needed], meaning golden toads were less likely to be found as the elevation increased. The average lifespan of the golden toad is still unknown, but other amphibian species in the Bufonidae family have an average lifespan of 10–12 years.
Adult males measured up to 5 centimetres (2.0 in) long. Males have been described as being "DayGlo golden orange", and, unlike most toads, their skin was shiny and bright. Jay Savage was so surprised upon first seeing them that he did not believe they could be real; he is quoted as saying, "I must confess that my initial response when I saw them was one of disbelief and suspicion that someone had dipped the examples in enamel paint." The toads exhibited sexual dimorphism; female toads were slightly larger than the males, and instead of being bright orange, were dark olive to black with scarlet spots encircled by yellow. The females also had enlarged cranial crests above the level of the orbit (eye socket), while in males the crests were much lower.
The golden toad's main habitat was on one cold, wet ridge called Brillante, where they would emerge in the springtime for five to ten days at a time to mate in rainwater that pooled against tree roots. The last documented breeding episode occurred from April–May 1987.
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. 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.
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 Jay Savage described as a "writhing masses of toad balls". 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.
SK Jacobson and JJ Vandenberg discovered that golden toads bred explosively when it rained heavily from March to June. During the 1977 and 1982 seasons, males outnumbered females by over 8 to 1 at breeding pools. Single males attacked pairs twice as often as they attacked individual males, but no males were displaced. Male body size was not linked with mating success, but size assortative mating occurred in 1977, according to Jacobson and Vandenberg. Life history characteristics like clutch size and large egg size were similar to other tropical montane toads. Yearly breeding activity was observed in B. periglenes from at least 1977 until cessation during 1988–1990.
The golden toad, like most frog species, was very dependent on water for breeding. Their porous, permeable skin made them very sensitive to moisture and temperature. Thus, when an especially dry year hit in 1987, the toads had a very difficult time breeding. The increase in temperature in their habitat caused the frequency of mists to decline. The decline began to dramatically change in the mid-1970s because of the warming of the oceans and the atmosphere. The cloud formations in Costa Rica began to form at higher altitudes than before and researchers believe that changes of this sort lead to disease outbreaks. The air could only become saturated and create mist through the cooling of the air to its dew point temperature or evaporating moisture into the air and increasing the water vapor content. This did not occur because of the great increase in temperature of the surrounding environments. The dew point temperature is the temperature at which a parcel of air must be cooled at constant pressure and humidity mixing ratio until it reaches saturation and at which condensation of water vapor forms either as dew, cloud droplets, ice crystals, mist, or fog. In the case of the golden toads, the mist levels decreased, so with the warmer air more water vapor is retained and there is less mist where the golden toads can continue with their reproduction process. In addition, El Niño and the Southern Oscillation left behind warm breeding pools which led to unsuitable conditions for reproduction, as well as heavy rainfall and a high pH balance in the water, all which disturbed the toads’ breeding patterns. After the storm hit, many breeding pools dried up and thousands of eggs and tadpoles were subsequently left to die.
In 1987, an American ecologist and herpetologist, Martha Crump, was fortunate enough to see the 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.
Jay Savage first discovered the toads in 1964. From their discovery in 1964 for about 17 years, and from April to July in 1987, over 1500 adult toads were seen. Only ten or eleven toads were seen in 1988, including one seen by Martha Crump, and none have been seen since May 15, 1989, when Nicholas Carter saw the last two males toads, believed to be from the group that Crump had seen the year before.
In the period between its discovery and disappearance, the golden toad was commonly featured on posters promoting the biodiversity of Costa Rica. There is a single anecdotal report from the 1970s of a golden toad in the mountains of Guatemala near the village of Chichicastenango, but this sighting has not been confirmed. Holdridge's toad, which was declared extinct in 2008 but has since been rediscovered, lives in the same forest in Costa Rica.
In the spring of 1987, an American biologist who had come to the cloud forest specifically to study the toads counted 1500 of them in temporary breeding pools. That spring was unusually warm and dry and most of the pools evaporated before the tadpoles had time to mature. The following year, only one male was seen at what previously had been the major breeding site. Seven males and two females were seen at a second site a few miles away. The year after, on May 15, 1989, the last sighting of only two males occurred. No golden toad has been seen since then.
The Global Amphibian Assessment (GAA) listed 427 species as “critically endangered” in its extensive analysis, including 122 species that could be “possibly extinct”. A majority of species, including the golden toad, have declined in numbers even in seemingly undisturbed environments. As late as 1994, five years after the last sighting, researchers still hoped that B. periglenes continued to live in underground burrows, as similar toad species have lifespans of up to twelve years. 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. In August 2010 a search organised by the Amphibian Specialist Group of the International Union for Conservation of Nature set out to look for various species of frogs thought to be extinct in the wild, including the golden toad.
In Costa Rica’s Monteverde cloud forest the frequency of mist in warm years and the fungi is associated with the disappearance of the golden toad. The cloudy weather favors the chytrids which grows best between 17 to 25 °C and peaking at 23 °C. They stop growing at 28 °C and die at 30 °C. These temperatures shield from excessive warmth and welcome moist conditions, The chytrid then grows on amphibian skin and produces aquatic zoospores. The infections of the chytrid fungus occur in the cells of the outer skin layers that contain large amounts of the protein keratin. Chytridiomycosis causes the skin to become thick, a change that is deadly to amphibians because unlike most other animals, amphibians absorb water and salts through their skin. These skin lesions deter oxygen from entering the body, eventually suffocating them. The golden toads who contract chytridiomycosis display a variety of symptoms. These symptoms include reddened or discolored skin, shedding of the skin more than usual, and even exhibiting abnormal behaviors such as seizures or nocturnal behavior. If amphibians seek warmth to combat the infection, increasing cloudiness might hamper their defences. In any case, local or microscale cooling should often beneﬁt the chytrids.
IUCN gave numerous possible reasons for the species' extinction, including its "restricted range, global warming, chytridiomycosis and airborne pollution". 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. 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. The underground hypothesis also has flaws. While the average lifespan of golden toads is still unknown, evidence suggest that it might be somewhere around 10–12 years. If this is the case, it is highly unlikely that the toads are still underground as they have not been seen in close to 30 years. Furthermore, there have been many mating seasons since 1987 with very favorable conditions and we have not had a reappearance of the species. However, Crump et al. (1992) concluded that conditions after 1987 were warmer than in 1987 after studying the temperatures of the golden toad breeding pools. J. Alan Pounds and Martha L Crump discovered that Crump et al. (1992) did not take into consideration that there was a cold front in early April 1987 when they came up with their conclusion. Pounds and Crump’s data prove that 1987 conditions were in fact warmer than conditions after 1987 using anomalies of daytime air temperatures at Monteverde.
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. This unpredictable environment and sudden changes in weather such as global warming and pollution lead to the untimely extinction of this interesting creature.
A more recent study supports the El Niño hypothesis in conjunction with the chytrid fungus, stating that "...Monteverde was the driest it had been in a hundred years following the 1986–1987 El Niño, but that those dry conditions were still within the range of normal climate variability". The new study has shown that the chytrid fungus has spread because of the dry conditions caused by El Niño. An estimated 67% of the 110 or so species of amphibians endemic to the American tropics, have become extinct or endangered, and a pathogenic chytrid fungus (Batrachochytrium dendrobatidis) is implicated.
Three hypotheses of how the chytrid fungus could have caused the extinction of the golden toad were reviewed by Jason R. Rohr et al. 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. 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. This theory is controversial.
Kevin J. Anchukaitis and Michael N. Evans, authors of “Tropical cloud forest climate variability and the demise of the Monteverde golden toad”, also proposed the chytrid thermal optimum hypothesis. They presented the earlier study by Pounds and Crump based on the El Niño event in 1986–1987. After observing the dry conditions from higher temperatures and lower seasonal rainfall, they concluded that this could potentially have caused the extinction. After that, Chytridiomycosis caused by B. dendrobatidis was eventually identified as a major cause of the amphibian extinction throughout the world. To test it, they used radiocarbon and chronology validation to test the amount of δ18O or (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.
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. In "Widespread amphibian extinctions from epidemic disease driven by global warming" J. Alan Pounds et al. established that global climate change is a direct link to species extinctions. Taking the results and recent findings that tie the golden toad's population crash to disease, Pounds 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. There is then the case of the "climate-chytrid" paradox. Chytridiomycosis, caused by the fungus Batrachochytrium dendrobatidis, grows on amphibian skin and produces aquatic zoospores. The chytrid 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.
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.
However, the last three collected and preserved specimens of B. periglenes were found to be negative for B. dendrobatidis. 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 still is not enough data to conclusively tie the pathogen with the now extinct species.
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