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Diversity's Disease

An Epidemic Is Wiping Out Amphibian Species Faster Than Researchers Can Count Them

In 1998 Karen Lips began an eight-year stakeout under the humid canopy of the El Copé cloud forest in central Panama. She awaited the arrival of a disease that scourged amphibian populations in neighboring Costa Rica, sending some species to extinction. The disease was moving like a wave east, at about 30 km per year.

While they waited, Lips and her team sampled the streams, woods, ponds, and puddles of El Copé, cataloguing the frogs and salamanders they found. They swabbed the amphibians' skin to determine if the disease agent, a fungus, was present. Seven and a half years passed with no sign of the disease.

Then in September 2004, it hit. Within four months of finding the first diseased frog, half of the species and over 70 percent of the total numbers of frogs disappeared from the study site. "Four months! We used to say one to two years and everything crashes," said Lips, a zoologist from Southern Illinois University in Carbondale. "It's incredibly dramatic, the impacts are phenomenal."

Lips is part of a larger group of researchers studying the declines of frog populations over the past two decades. According to the Global Amphibian Assessment, conducted in 2004, one third of all amphibian species are threatened.

These animals are in such peril that fifty of the leading researchers in the field recently called for the formation of an Amphibian Survival Alliance, to be led by the World Conservation Union (IUCN). In the plan, published in July in Science , the authors request $400 million to develop conservation programs to prevent further declines.

While habitat loss is to blame for the decline of many species, amphibians continue to die out in undisturbed habitats. These more mysterious losses vexed scientists, who asked: Why would highly protected populations die out?

A massive detective effort now underway suggests a disease-causing fungus named Batrachochytrium dendrobatidis, or chytrid for short, lies at the center of this mystery. Found in Asia, Europe, Australia, the Americas and Africa, the disease is most devastating to amphibian populations in mountainous areas, where it thrives on moist cool conditions. Chytrid is implicated in the disappearance of many regional populations of frogs, and it has driven some endemic species to extinction. Many of the die-offs are undocumented, due to remoteness of the regions where the disease flourishes.

The total loss of amphibians in the most devastated zones will fundamentally alter the affected ecosystem, says Andrew Blaustein, a professor of zoology at Oregon State University in Corvallis who studies the chytrid phenomenon. Frogs prey on insects such as mosquitoes, many of which are vectors of human disease. The larger frogs of South America eat rodents and so are an important component of pest control there. Amphibians, in turn, are the prey of snakes, birds, and mammals.

Although many scientists focus their research on understanding chytrid disease, the field is riddled with questions. Thus, while the origins, movement, and overall impact of chytrid are debated, amphibians continue to disappear in droves. Other researchers, hearing a call to action, are collecting the species in greatest peril to rear the last remaining hold-outs. Their hope: the disease will burn out and the animals can be returned to the wild to begin where they left off.

For Lips, the saga began in the early 1990s while she was working on her dissertation at Las Tablas in the Talamancan Mountains of Costa Rica. After spending several years documenting the life history of a stream-breeding tree frog Lips returned to the States to do some teaching. When she got back to Las Tablas in 1993, the frogs of her study were no where to be found. "Things were very murky at that point," recalls Lips, because the disease and the fungus that causes it hadn't been described. Thus, the effort to explain these disappearances began, a quest that has defined Lips' career.

A few years earlier, researchers documented a major decline in frogs northwest of Las Tablas, in the Monteverde region of Costa Rica. Lips thought, "and it was only a guess at this point," the declines in both regions might be related. Whatever was killing the frogs appeared to be moving northwest to southeast, across the volcanic spine stretching from Costa Rica into Panama.

So in 1997, Lips picked up and moved east to Fortuna, a mountainous region of western Panama, to see if the same thing would happen to amphibian populations there. After a couple years of monitoring there was a breakthrough. Lips found 50 dead frogs over a period of three weeks. "That was basically the end of a big die-off. Most of the frogs had already disappeared at that point, and I was just catching the tail end of it." Lips shipped these dead frogs to pathologists to see what had killed them. They found an as-yet undescribed fungus in their skin.

"The picture got out in the New York Times, when they wrote about the die-off, and the Australians saw it and said ‘Oh, they've got it too,'" says Lips. This prompted a meeting between the two groups, which included Joyce Longcore, a fungus specialist from the University of Maine in Orono. Longcore suggested they were dealing with a chytrid fungus: a new species, but a chytrid nonetheless.

Chytrid fungi serve as nutrient recyclers in the natural environment, digesting proteins from insect exoskeletons, breaking down cellulose from plants and keratin from skin and hair. Although they are known pathogens of insects and plants, no one knew they could parasitize a vertebrate animal.

Batrachochytrium operates by colonizing and feeding upon the outer layer a frog's skin. The actual means by which the fungus kills amphibians, however, is not yet proven. One hypothesis is that the fungus interferes with the animal's ability to breathe through their normally porous skin. Chytrid may also impair its host by secreting a toxic substance, basically poisoning the frog.

The fungus produces a sort of swimming infectious agent, called a zoospore, that transmits chytrid to amphibians when they inhabit infected streams or ponds. Frogs can then transmit the disease to each other when healthy animals share aquatic habitats with diseased individuals. Frog-to-frog contact out of the water can also spread the disease.

In the early disease stages, infected frogs are not easy to visually identify. "Once they get to the point where they are almost dead, or very very sick, it's pretty obvious," says Lips. "The frog can't move, it just sits there. It might jump once, but then it can't jump again. It has faded color." To confirm the presence of the disease researchers swab the skin of the animals, and analyze the sample for chytrid DNA.

"After Fortuna crashed, I moved to El Copé and said ‘this is the next protected area where I can go back and reliably, year after year, still find forest. We're going to sit here and do this right,'" says Lips.

Over the seven and a half years they waited for the disease to arrive, Lips' team surveyed nearly 30,000 amphibians. All of this work eventually paid off, providing the most comprehensively documented chytrid outbreak to date.

The factors that influence the spread of chytrid disease are strongly debated. One researcher, Alan Pounds, of the Monteverde Cloud Forest Preserve and Tropical Science Center, believes that climate change is altering the local environment in the mid-elevations of Central America, resulting in temperatures that promote outbreaks of the disease there.

Pounds data is correlative; he matches a decline in harlequin frog species in Central and South America to a change in temperature regimes at his study site in Monteverde, as well as a broader change in the regional climate of the tropics. One of the main criticisms of Pounds hypothesis is that he has no data that supports a direct connection between climate change and occurrence of the disease. Most of the disappearances in this region occurred before anyone was documenting them. Without that record it is difficult to explicitly link the climate to the disease, and the disease to the harlequin declines.

Lips' believes that chytrid disease moves like a classic epidemic wave, with frog-to-frog transmission accounting for its spread across Central America. "We have no data that suggests that climate change is involved," says Lips. "We don't need to talk about climate change. The epidemic disease theory is sufficient. This is an exotic introduced disease, the frogs are naïve to this disease, so none of them have any evolved immunity to it. It gets in there and spreads."

While Lips' study provides compelling evidence that the disease is new to Panama, infected frogs have been found in Australian and North American museum specimens from as early as 1974. This raises a basic question. Is the disease really new, or is this a pre-existing disease that some environmental change triggered to become worse? "People go both ways on this," says Blaustein.

The earliest known host of the chytrid is the African clawed frog ( Xenopus ), found in museum specimens dating back to 1938. The global transport of Xenopus frogs for use in pregnancy testing in the 1950s is the most popular explanation for the spread of the disease. Tissue of this species was injected with female urine, and if the frog produced eggs the test was considered positive.

Chytrid's ability to drive host populations and even species to extinction also perplexes researchers. "This is unusual because most diseases follow a density dependent process. What happens, basically, is the hosts get so dispersed that transmission goes to zero, and the disease burns itself out if it is too virulent," says Andrew Storfer, a zoology professor from Washington State University in Pullman who studies amphibian diseases.

This is another peculiar facet of the disease. It has little host-selectivity: that is, it can infect just about any amphibian. Thus, it doesn't depend on any one host species for its own fate. Further, the disease appears to infect, but not kill, certain species of amphibians. These animals may serve as reservoirs to keep the disease going.

Amphibian diversity declines throughout the world have signaled the call to action for Joe Mendelson of the Zoo Atlanta and Ron Gagliardo of the Atlanta Botanical Garden. Together, they have spearheaded a massive effort to develop emergency captive breeding programs for frogs threatened by the fungus. Their hope is that these animals might some day be reintroduced into the wild.

The problem is that, despite these efforts, the frogs' environment seems to remain infected. "You can bring all the frogs you want into captivity and cure them of this disease, but then what do you do?" asks Lips. Researchers hope to find a way to clean the environment of the fungus or develop a method to vaccinate frogs against the disease.

"Most of us are motivated to not sit idly-by and watch amphibians go extinct," says Storfer. "I think we all would like to do something about it but it's going to take some time to figure out what we can do and how can we do it responsibly and not make the situation worse."

Lips has now moved to a site just west of the Panama Canal and is waiting for the disease there, and so her quest to understand the disease continues. "Time is running out. We've lost so much already that we're really concerned about what we are going to have left," says Lips.

David Lawrence is a biologist at the University of Washington and has studied science writing in the UW Department of Technical Communication.

Images

Top: The Columbia spotted frog, Rana luteiventris. Photo: Brome McCreary, USGS.

Middle: The Columbia spotted frog. Photo: Wendy Wente, USGS.


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