Students hard at work on the "Mangrove Challenge"! (Sierpe River, SW Costa Rica)
12 May 2005
Amphibians are extremely sensitive indicators of environmental changes- uptake of oxygen and water through their skin can increase concentrations of pollutants, and the life cycle of frogs and toads exposes them to water and airborne contaminants. Amphibians are so sensitive to changes in the environment that scientists have likened them to a canary in a coalmine.
Nearly 400 species of amphibians and reptiles are known to inhabit Costa Rica, which is a very large number for such a small country ( Osterhaus, 2004). The variety of habitats in Costa Rica, as well as its location as a land bridge between North and South America, accounts for the striking species diversity. A 30 square mile area of the Monteverde Cloud Forest Preserve harbored 50 species of amphibians in 1987; since then, 20 species have vanished (Kirby, 1999). One of the most well-known of these extinct species is the Golden Toad.
Golden Toads- Background
Discovered in 1964, the golden toad is renowned for its brilliant color- it is the only known species of toad that is not gray or brown. Otherwise known as elsapo dorado (the namesake for a hotel in the Monteverde preserve) the golden toad displays extreme sexual dimorphism. Males are golden in color, while females range from yellow to dark brown or black, spotted with scarlet. Males were found to outnumber females by as much as 8 to 1.
For a week in April every year, thousands of these brilliant toads gathered in temporary water pools in an explosive breeding orgy (Fogden, 1984). In 1987, more than 1500 golden toads were observed during the breeding period (Pounds, 1994). Unable to differentiate gender, male toads would clasp anything that moved. The male golden toads possessed a special vibration signal to relay gender, and disengage other males. Inadvertent coupling with other species of frogs that did not possess this vibration signal could occur, lasting for days.
When a male sapo dorado successfully located a toad of the right sex and species, he would remain attached to the female in amplexus until the female laid eggs . Females would lay approx. 200 to 400 eggs. After hatching, larvae would remain in water for five weeks before metamorphosing into their terrestrial form. The breeding pools frequented by golden toads were so small that a few days without rain could dry them out, causing the tadpoles to die of desiccation.
The golden toad occupied a few square miles in the Monteverde Cloud Forest Reserve in northern Costa Rica (Fogden, 1984). Habitat was restricted to about 2000 m ASL. Golden toads were thought to live under fallen leaves and moss. Sightings of golden toads were limited to the week of breeding in April.
Decline and Extinction
The April breeding frenzy was the only time that the toads were ever observed, and around 1500 golden toads were observed in 1987 (Pounds, 1994). However, only one solitary male was observed in 1988 and 1989, and no golden toads have been seen since this time. The Monteverde Cloud Forest Preserve had several toads in captivity; they also died in the mid-1980’s of unknown causes. In 1992, experts pronounced the golden toad almost certainly extinct. It is obvious that the population of golden toads declined, but no one is certain as to the cause of the extinction. At least four theories have been postulated as to the reason for the decline and extinction of golden toads: climatic change, pollution, ultraviolet radiation, and fungal skin infections.
At the same time that the Golden Toad populations experienced rapid decline, members of six other families of amphibians in the Monteverde Cloud Forest became scarce. One species of frog- the Harlequin frog ( Atelopus varius )- became very scarce and apparently became extinct in 1996-. However, an undergraduate from the University of Delaware came across several Harlequins during a trip to Costa Rica in 2004 ( Young UD scientist finds frog thought to be extinct, 2004).
In 1986 and 1987, El Nino resulted in the lowest rainfall on record at Monteverde. Rainfall was the lowest recorded for each of the four “seasons” as defined by Pounds and Crump (1994): the late wet season, transition into dry season, dry season, and the post-dry season (early wet season). Temperatures during this period also reached record highs.
The shift in climate during an El Nino event is due to northeasterly trade winds, caused by increasing atmospheric pressure in the Atlantic and decreasing pressure in the Pacific. These winds decrease the amount of convective rains on Pacific-facing slopes. Additionally, temperatures in the dry season are warmer than usual (Pounds, 1994).
This warm, dry climate caused by an El Nino event in 1986-1987 could have caused decline of golden toads through several possible mechanisms. Direct decline of golden toad populations could have been caused through dessication. Golden toad tadpoles require approximately five weeks of maturation on puddles- if these puddles dry up, the tadpoles die of dessication.
It is possible that the warmer, drier climate could have increased the susceptibility of the golden toads to disease. Another hypothesis states that atmospheric contaminants reach critical concentrations when conditions are especially warm and dry (Pounds, 1994).
Although golden toads occurred in an environment that appeared largely untouched by humans, it is possible that pollution caused harm to golden toad populations. Recent research has proved that atrazine, the most common pesticide, has serious effects on the sexual development of frogs. One study conducted by Dr. Hayes at UC-Berkeley in 2002 showed that low concentrations (0.1 part per billion) of atrazine in pond water can cause sexual dimorphism in leopard frogs, rendering them sterile (Hayes, 2002). This result is shocking when one considers that the EPA minimum contaminant level ( mcl) for atrazine in drinking water is 3 parts per billion! Costa Rica has pesticide control laws, but in 1993 about 18% of all pesticide imports (by volume) were in the World Health Organisation toxicity classification categories Ia, extremely hazardous, or Ib, highly hazardous(2). Pesticides in Costa Rica are also exempt from taxes and duties ( Agne, 1997). Large amounts of pesticides are used in Costa Rican agriculture.
It is possible that pesticides entered the atmosphere from one of three methods. These pesticides could have become airborne as a function of application- pesticides sprayed onto crops could drift from intended crops and end up in clouds. Pesticide-carrying dust particles, in the form of soil eroding from fields, could enter the atmosphere. Finally, It is possible that the contaminants entered the atmosphere through evaporation ( Seiber, 1989). Under normal conditions, these are methods for contaminants to become concentrated only over long periods, and an immediate population crash isn’t likely due to these factors alone. However, the warm weather conditions in 1986-1987 could have increased contaminant evaporation from fields, and little precipitation during this time could have caused excessive concentrations to build in the atmosphere. This climate-linked contaminant pulse hypothesis, described by Pounds (1994) could have poisoned golden toad populations as the dehydrated amphibians rehydrated with precipitation high in concentrations of toxic contaminants.
Solar ultraviolet (UV) radiation of wavelength 280-320 nm has been responsible for declines in populations of of R. cascadae and B. boreas boreas in Oregon. Blaustein and Wake (1995) have suggested that UV exposure impairs immune function, making the larvae more susceptible to infection by the fungus Saprolegnia, which naturally occurs in lakes and ponds. It is unlikely that an increase in ultraviolet radiation had a dramatic effect on populations of golden toads, as the golden toad spends almost all of its time in shade. However, ultraviolet radiation could be another stress on golden toads that, when combined with other factors, led to a population crash.
The underlying cause of the decline of many amphibians could be due to a fungal disease known as chytridiomycosis. The result of this type of infection is skin damage, leading to skin thickening and eventual suffocation and/or dehydration. Field diagnosis of this condition is difficult, as external symptoms such as ulcers or lesions are rare. Diagnosis is usually only possible through examination of a freshly preserved carcass under an electron microscope ( Daszak, 2000).
There are also numerous bacterial pathogens that can cause amphibian mortality. Pounds (1994) suggests that the climate in 1986-1987 could have increased susceptibility of golden toads to infection in two ways. First, the stress of the warm conditions and low moisture could have made the toads more susceptible to disease. Second, the decreased moisture could have led to decreased habitat for the toads. This could have led to crowding as the toads competed for optimal space. In turn, this could have made it easier for disease to spread from one toad to another.
Extinction is a natural process- approx. 2% to 4% of the species that have ever lived survive today. However, the extinction rate today is estimated to be between 1000 and 10,000 times higher than the natural extinction rate (Chanson, 2004) especially hard-hit by the recent wave of global extinctions- around 122 species of amphibians have gone extinct since 1980, and one-third of the remaining 6000 species are threatened with extinction (Stuart, 2004). Only 12 percent of birds and 23 percent of mammals are in the same position. This statistic is sobering enough; it is even more startling when one considers that scientists have only named about 1.75 million species of plant and animal life out of the 13-14 million species that are believed to exist (Hilton-Taylor, 2000). Pollution is not the only factor threatening wildlife- a team of researchers concluded that if climate warming proceeds unchecked, 15% to 37% of the 1103 plant and animal species they examined will disappear by 2050 ( Sreenivasan, 2004).
It is likely that no one factor alone is responsible for the extinction of the golden toad; rather, a combination of factors has probably led to its decline. The disappearance of this species was most likely due to a combination of unfavorable climate, pollution, and disease. Due to their sensitivity to environmental changes, amphibians can provide an early warning of impending environmental problems. The extinction of the golden toad, and the disappearance of amphibians worldwide at rates much higher than normal, is an indication that human activity is taking a toll on ecosystems worldwide.
2000 IUCN Red LIst of Threatened Species. Comp. C. Hilton-Taylor. May 2001. World Conservation Union. 15 Apr. 2005. Accessed via the web address http://www.iucn.org/redlist/2000/news.html.
Agne , S. and Waibel, H. (1997). “Pesticide Policy in Costa Rica.”Pesticides News 36, 8-10.
Blaustein A., Wake D., & Sousa W.. (1994). Amphibian declines: judging stability, persistence, and susceptibility of populations to local and global extinctions. Conservation Biology, 8, 60-71.
Daszak , P., Cunningham, A.A. & Hyatt, A.D. “Amphibian Chytridiomycosis and Emerging Infectious Diseases of Wildlife.” Accessed via the web address http://www.vet.uga.edu/ivcvm/2000/Daszak/Daszak.htm. Viewed March 25, 2005.
Fogden , M., and Fogden, P. (1984). "All that glitters may be toads." Natural History, 5/84: 46-50.
Hayes, T., Haston, K., Tsui, M., Hoang, C.H., and Vonk, A. (2002). “ Atrazine-induced hermaphroditism at 0.1 ppb in American leopard frogs ( Rana pipiens): laboratory and field evidence.” Environmental Health Perspectives , 111 (4).
Kirby, Alex. "Climate claims the golden toad ." BBC News 26 Apr. 1999. Accessed via the web address http:// news.bbc.co.uk . Viewed April 15, 2005.
Osterhaus , Eron. “Research, diversity and prospects for herpetological survival in Costa Rica and the rest of the world.” 24 Apr. 2002. Accessed via the web address http://www.wisemonkeynews.com. Viewed April 15, 2005.
Pounds JA, Crump ML. (1994). Amphibian declines and climate disturbance: the case of the golden toad and the harlequin frog. Conservation Biology, 8, 72-85.
Seiber , J., McChesney, M., and Woodrow, J. (1989). “Airborne residues resulting from use of methyl parathion, molinate, and thiobencarb on rice in the Sacramento Valley, CA.”Environmental Toxicology and Chemistry 8 (577-588).
Sreenivasan , Aparna. "Biodiversity getting baked."Science Now (1/7/2004): 2-4.
Stuart, S., et al. "Status and trends of amphibian declines and extinctions worldwide." Science 306 (2004): 1783-1787.
“Young UD scientist finds frog thought to be extinct.” 02 June 2004. University of Delaware . Accessed via the web address http://http://www.udel.edu/PR/UDaily/2005/jul/frog070204.html. Viewed May 7, 2005.
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