SOLUTIONS | 07.26.16

The Devourer

A new and deadly fungus could wreak havoc on America’s salamanders if—or when—it arrives on U.S. shores.

Story by Geoffrey Giller

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Squirming at the bottom of the Ziploc bag is a small salamander, its olive-hued back dotted with rust-colored spots. Evan Grant peers closely at the captured creature, his bearded face just a few inches away from its bright peach belly, as he checks for any abnormalities. In particular, he's looking for skin lesions: possible omens of a coming salamander apocalypse.

After the visual check, Grant, a wildlife biologist with the United States Geological Survey, swabs the animal's legs, belly, and tail, five swipes in each spot with a sterile cotton swab, and then again with a second swab. The salamander, a red-spotted newt (

Notophthalmus viridescens

) common across much of the eastern United States, protests silently in Grant’s gloved hand, its small limbs pushing against his firm grip. After he's done, Grant dumps the newt gently back into this western Massachusetts roadside pond; the swabs will go to the USGS's National Wildlife Health Center in Wisconsin, where they'll be tested to see if a deadly fungus is lurking on the skin of American amphibians.

That fungus is what’s brought Grant out on this overcast mid-April afternoon. Its name is

Batrachochytrium salamandrivorans

: the devourer of salamanders. Called

Bsal

for short, it was first identified in 2013 in the Netherlands. Its discovery jolted herpetologists around the globe—because its close relative, the fungus

Batrachochytrium dendrobatidis

, or

Bd

, played a large role in making amphibians the most threatened group of organisms worldwide.

Bd

is directly responsible for the decimation or extinction of many frog and toad species. While

Bd

has mostly spared salamanders,

Bsal

is coming for them.

For now,

Bsal

has killed salamanders only in a few European countries. It has also since been found in Asia, where scientists suspect it originated, but it doesn't appear to kill Asian salamanders. Besides the Netherlands, where unexplained deaths of chunky, black-and-yellow fire salamanders first tipped off researchers in 2010, it has also struck wild salamanders in Belgium and captive ones in Germany and the U.K. (

Bsal

doesn’t seem to affect frogs or toads.) But Grant and other members of a national task force aren't sitting around waiting for it to start killing salamanders here, too. Wildlife biologists and managers don't want to be caught flat-footed like they were with

Bd

. Step one in that effort: Make sure

Bsal

hasn’t already arrived in America, which is what Grant is helping to determine with his swabs.

Grant, who’s sporting a well-worn green cap emblazoned with the USGS’s slogan, “Science for a changing world,” doesn’t know whether

Bsal

has already crossed the ocean. But considering the 200,000 wild-caught and captive-bred salamanders imported into the States via the pet trade every year, before an import ban on some species went into effect in January, he and many other scientists think that if it's not here yet, it will be soon. "The big question," Grant says, "is, What do you do with that time between now and when you actually find it?"

If

Bsal

does end up in the States—or if it's already here—the ramifications are frightening. The U.S. has the highest salamander biodiversity of anywhere in the world, with about 200 different species. These range in size from barely two-inch long creatures with no lungs that hide under damp leaf litter to two-foot-long hellbenders, prehistoric-looking beasts that live in cold streams. Appalachian states are home to a plurality of our salamanders, with California a distant second. But salamanders are native to almost every state in the union. And despite their relatively small size and seemingly docile behavior, they're actually top predators in many ecosystems—like in the forest pools where many salamanders breed and where some, like Grant’s newts, spend their adult lives as well. Aquatic bugs no doubt cower in fear of these small amphibians.

Salamanders are a strange, squishy, wonderful amalgam of colors vibrant to dull, textures slimy to rough. America's salamander collection is the best in the world—as much a part of our natural heritage as a bald eagle or a bison.

As with any ecosystem, the predators at the top of the food web are especially important to the system's overall function. In many American forests, there are more salamanders than all other vertebrates—birds, deer, mice, shrews, and the like—combined. Hiding in ponds or under logs, salamanders are much less visible than birds or mammals. But their sheer numbers make them not just integral parts of forest ecosystems but drivers of many unseen natural processes. Salamanders eat untold numbers of insects and insect larvae, including mosquito larvae. Without them, says Vance Vredenburg, a professor of biology at San Francisco State University who studies

Bd

and

Bsal

, our world would be “a much buggier place. Insect populations would no longer have these incredibly important predators holding them down.” Not only might that be unpleasant for us humans, he says, but it’s possible that we could see extreme changes in the composition of the forests themselves—with out-of-control insect populations overwhelming trees or spreading diseases.

While it’s impossible to predict exactly what the end result of widespread salamander die-offs would be, it’s hard to overstate their importance. Subtler, long-term effects would also spread through the landscape in the absence of these tailed amphibians: Salamanders help carbon and nutrients cycle from ponds to terrestrial ecosystems. Vredenburg compares them to salmon, which bring crucial nutrients from their ocean-faring lives back to their natal rivers when they return to breed and die. “Salamanders probably serve very similar roles, and the effects may be just as dramatic,” he says.

To salamander researchers, the idea of losing vast numbers of salamanders if

Bsal

rampages through North America would be like going into the Metropolitan Museum of Art and finding that all the vivid, vibrant Romantic paintings had been ripped from the walls and burned. Such a deprivation might hit Romanticism fans harder than others, but for all visitors the museum would be far less rich for their absence.

Across the United States, researchers like Grant are scrambling to avoid such a catastrophe. The National

Bsal

Task Force, which consists of representatives from universities, federal agencies, and NGOs, came together last summer in Fort Collins, CO, with a mission to protect our salamanders and prevent a repeat of the first fungus (

Bd

)—which wiped out frogs and toads in the Americas and Australia before scientists even knew what was happening.

Bsal

Risk in the U.S.

Estimated

Bsal

threat to salamanders across the United States, based on both relative numbers of salamander species across the region and

Bsal

habitat suitability. Black dots indicate major ports of entry for salamander imports, despite the fact that the U.S. Fish and Wildlife Service has recently banned the import of most salamander species for the pet trade.

Adapted with permission from

Yap et. al. (2015).

Threat Level

High

Low

Port of entry

Back in September 1989, Martha Crump, then a zoologist at the University of Florida (and now a professor of behavioral ecology at the University of Utah), was attending the first ever World Congress of Herpetology, in Canterbury, England. There was a buzzing energy among the 1,400 attendees; for many of them, this was the first time they'd been surrounded by so many fellow amphibian and reptile lovers. But Crump was distracted by the disconcerting field season she’d just finished. For the second year in a row, at sites in Costa Rica where there used to be hundreds of golden toads, she had found only a single individual.

"As we were having a beer, or passing in the hall," Crump recounts of her colleagues at the Congress, "they would ask, 'So, how are the golden toads?'" When she told them of the missing amphibians, she was met with looks of horror. Consistently, other herpetologists from around the world would have eerily similar stories from their field sites, or else they knew someone whose amphibians were also missing. Slowly, they began to wonder whether there was some connection among all these disappearances.

David Wake, who was also at the meeting, recalls the discussions of vanished amphibians. Afterwards, he took his conference book and marked all the presentation summaries that mentioned missing or shrinking populations. Soon, dozens of Post-It notes were sticking out from the book. He organized a conference a few months later to figure out what was going on. Not everyone was convinced that there was really a global pattern, though—including Wake himself, now an emeritus professor of integrative biology at UC Berkeley. "I was cautious," he says, having experienced enough of the "vagaries of fieldwork" to know that amphibian populations regularly go through periods of highs and lows. In fact, a widely read paper published in

Science

a year after the conference argued that it was premature to declare that widespread, human-caused amphibian declines were in fact occurring, presenting as a counterpoint dramatic drought-caused highs and lows in healthy populations of three types of frog and one salamander in North Carolina.

Rather than trying to find what was killing amphibians, scientists spent several years just trying to figure out if there was even a problem. "It took a long time to recover from that article," says Vredenburg. But by the mid-90s, it was clear that amphibians truly were in trouble.

The question, however, was why? What was causing amphibians around the world to die, in spots as far apart as Central American mountains and Australian rainforests? In some cases, a major cause was obvious: habitat loss. But what about the frogs in seemingly pristine sites?

As is often the case in science, a combination of accidental circumstances and keen observations led to an answer. A team of scientists was studying an unexplained die-off of frogs in Australia in the early 1990s. All of the frogs seemed to have the same microscopic parasite on their skin, although the team couldn't figure out what exactly it was. A few years later, Karen Lips, now a professor at the University of Maryland and one of the leading experts on the

Bd

fungus, witnessed tree frogs inexplicably dying in Panama. In 1997, the

New York Times

published an article about her dying frogs. When the Australian team read the article, they were struck by the similarities.

Soon the two groups, with others that had seen similar deaths elsewhere, met in Illinois. The next year, several of those at the meeting published the first paper identifying a fungus as the cause of widespread die-offs. They knew it was a type of chytrid fungus, a ubiquitous and well-known group with more than 1,000 known species, but this one was unusual: It was the first case of a chytrid fungus infecting a vertebrate. (Plankton are their typical hosts). In 1999, researchers at the University of Maine isolated the fungus and identified it as a new species.

This discovery set off a new round of scientific debate. Herpetologists around the world grappled with the idea that a single species of fungus was killing multiple species of vertebrates—mostly because this was the first documented example. "Back in the early days, there was no disease that could kill hundreds of different species and that was globally distributed and that could cause extinction," says Lips. "All these things were thought to be basically impossible."

Of course, amphibians faced other problems, too. "It's a mistake to think that this is a chytrid-specific problem," Wake says of the declines, citing habitat destruction and pesticides as other major factors. "It's a death by a thousand cuts—with a very big cut being chytrid.”

By about 2004, though, most herpetologists had come to see

Bd

for what it was and still is: one of the gravest threats to amphibian biodiversity. And that acceptance reveals a thin silver lining to the

Bd

crisis. There's little chance the current response to

Bsal

would have been as urgent, says Vredenburg, if scientists didn't already know that a fungus could cause an amphibian holocaust.

The first shipment of dead fire salamanders (

Salamandra salamandra

) that arrived in 2010 at An Martel's lab at the University of Ghent, in Belgium, sealed in plastic bags, caused little stir. "We frequently get dead amphibians," says Martel, who studies wildlife population health. She had been working with amphibians and on the

Bd

fungus for years, and conservation groups would often send her dead salamanders and frogs found in the wild, to test for pathogens. The salamanders in this 2010 batch were too decomposed for a necropsy, but Martel and her colleagues checked for the usual suspects, including

Bd

and several amphibian viruses. All negative.

The shipment had come from the Netherlands, where there are—rather, were—only three known populations of the large amphibians. Over the next year, the salamanders from the largest population kept turning up dead. Alarmed, members of a conservation group collected three-dozen healthy-looking salamanders to set up a captive breeding program at Martel's lab, an attempt to save the population. Soon half of those salamanders were dying, too. But now Martel could actually observe them as they succumbed.

Martel put thin slices of skin from the deceased salamanders under the microscope and saw something seemingly familiar: chytrid fungus, with its distinctive round, brown spores. But these dead salamanders also had lesions covering their bodies like lepers, something she had never seen with

Bd

. That fungus typically causes thickening of the skin of infected animals, interfering with a number of vital processes. "This fungus really eats the skin," Martel says of the new fungus. "And so at the moment that the animals are dying, they almost have no skin anymore."

A genetic analysis of the new fungus confirmed what Martel had observed: it was another chytrid fungus, related to

B. dendrobatidis

, but definitely a new species.

“This fungus really eats the skin, and so at the moment that the animals are dying they almost have no skin anymore."

—An Martel

Martel wasn't yet ready to declare the new fungus as the killer, however. Just because you find a new organism on a dying animal, she notes, doesn't necessarily mean that it's the culprit. Maybe the fungus was just at the wrong place at the wrong time. Experimental infections of captive-bred salamanders with the fungus soon followed. When those salamanders also died gruesome deaths, Martel and her colleagues wrote up a paper announcing the existence of

Bsal

, the salamander-devouring fungus, to the world.

As soon as the paper was published in 2013, Martel says, "everyone understood immediately that it was important, because they had seen the story with

Bd

." But perhaps the more alarming finding appeared a year later in the journal

Science

. After they discovered

Bsal

, Martel and her colleagues tested dozens of other salamander species to see if the new fungus would kill them, too. It did. Of the 157 salamanders tested, a third died when exposed to the fungus. And newts fared the worst against

Bsal

. Forty-four newts of nine European and North American species were exposed to

Bsal

in the lab. All forty-four died. A news article published along with Martel’s paper in the same journal presaged “the coming salamander plague.”

Martel's findings spurred the meeting last summer in Colorado to launch the National

Bsal

Task Force. Priya Nanjappa, a program manager for amphibians and reptiles with the non-profit Association of Fish and Wildlife Agencies, describes the feeling of urgency at the meeting: “We gotta do something, and we’ve got to act as quickly as possible.” Vredenburg encapsulates the feeling of herpetologists starkly: “We are freaked out,” he says. “People realize, ‘Oh my god... This could be really bad.’”

Vredenburg wasn’t at the Colorado meeting, but he’s deeply involved in

Bsal

research efforts, including sampling West Coast newts for

Bsal

to complement Grant’s efforts back east. On a foggy May morning, Vredenburg leads a crew of students along a rocky trail in the Point Reyes National Seashore, across the Golden Gate Bridge and about an hour's drive from his San Francisco lab. The trail winds past sheer cliffs, with the Pacific Ocean nudging against the beach below. Vredenburg has a quick grin and an infectious enthusiasm for all things natural, constantly interrupting himself on the hike to point out unique plants, or shouting at his students to keep an eye out for whales.

A brisk two miles in, we arrive at a swampy basin, four ponds separated by narrow strips of land covered mostly in evergreens and poison oak. The steep path down from the trail is almost non-existent. The target: rough-skinned newts (

Taricha granulosa

), similar in many ways to the East Coast’s red-spotted newts. Vredenburg estimates that tens of thousands of them breed in these small ponds.

He sends pairs of students off to each pond to seek out amphibians. Soon, he nets the first newt of the day. It has a bright belly, the color and texture of a blood orange's skin. It shows off its coloration by arching its head and tail, a behavior that lets would-be predators know it's toxic. Another indicator is its smell: The poison these newts produce gives off a strong metallic scent. According to Vredenburg, each newt contains enough toxin to kill 50 people. (A popular, possibly apocryphal tale among herpetologists is that of three hunters found dead at their campsite in an Oregon forest with no signs of injury; they had accidentally boiled a rough-skinned newt along with their coffee and died after drinking the laced brew.)

After the first newt, though, the minutes drag on without another capture. "That's the way fieldwork goes," Vredenburg says. It's easy to see why it took scientists so long to conclude that amphibians were in fact disappearing; even at a spot like this, where Vredenburg knows there are usually lots of newts, their apparent absence doesn't ring any alarm bells.

Gradually, though, his students start finding and catching newts. As a light drizzle falls, Vredenburg sets up on the shore of one pond, swabbing each newt on its colorful stomach, throat, and limbs. He talks gently to one, which squirms and whips its tail back and forth as he swabs it. "That didn't hurt, buddy," he says gently, like he's talking to one of his kids at the doctor's office.

Back at Vredenburg's lab, a few dozen salamanders collected on earlier field outings sit in plastic enclosures, kept damp by moist paper towels and with ceramic pot saucers to hide under. They await potential sacrifice: exposure to

Bsal

to test their susceptibility.

This is the next stage of the

Bsal

effort. Martel only tested a few North American species, and only a few individuals of each. Vredenburg wants to verify the susceptibility of some species, like the rough-skinned newts, and test others that Martel didn't include in her study. That information will help scientists know where to focus their resources for

Bsal

monitoring. It may also help scientists choose species for so-called “captive assurance populations,” animals raised in captivity to prevent their complete extinction and provide a source for possible reintroduction into the wild, should it come to that.

Some of Vredenburg's captive newts are survivors from a previous experiment in which they were exposed to

Bd

. He’s curious whether prior exposure to

Bd

might change how amphibians deal with

Bsal

. Perhaps, he says, prior exposure and survival actually improves their ability to fight off

Bsal

as well. Or it could weaken them, making them more susceptible.

Down the hall in a locked room, Vredenburg is growing

Bsal

itself. For all the consternation that it has caused, it's remarkably mundane-looking: just a few pale specks on plates of agar. But Vredenburg knows the havoc that each tiny colony could wreak on American salamanders.

The best bet for stopping

Bsal

is already in place. In January, the U.S. Fish and Wildlife Service banned the import and interstate transport of 201 salamander species, in response to requests for action from conservation NGOs. Vredenburg and others working on

Bsal

praised the relatively quick action. But the ban is controversial. Some in the salamander pet trade complained the restrictions were too broad, while some conservation managers asked why more species weren’t included. The agency is now taking nearly 300 comments into consideration as it prepares a final ruling.

Part of the problem, says Nanjappa, who has been working on

Bsal

since news of the fungus reached the U.S., is that the agency is constrained in its ability to act. To pass the ban, it had to designate those 201 species as "injurious wildlife" under the Lacey Act, the federal law that bans the import or interstate transport of endangered or invasive species. That designation is normally used for invasive species that pose a threat to local ecosystems—not for species that are themselves at risk. "It's clunky at best," Nanjappa says of the Lacey Act, which was initially passed in 1900. "It's not set up to handle pathogens."

If a pathogen—be it fungus, bacteria, or virus—poses any sort of threat to

human

health, then there's no regulation problem. The CDC has full authority to act as it sees fit. Likewise, anything that threatens livestock or crops falls under the purview of the USDA. But there’s a gaping hole when it comes to wildlife. No law or agency is charged with addressing diseases that are passed only among wild species. That puts wildlife—including salamanders—at grave risk.

Instead of simply targeting

Bsal

itself—which might have led to the quarantine and testing of imported salamanders, or bans on salamanders from places known to have

Bsal

, or rules for decontamination when moving between areas vulnerable to

Bsal

infection in the U.S.—the agency was forced to enact a blanket ban on the import and transport of salamanders.

Nanjappa is helping draft a bill that would give the Department of the Interior (which includes the Fish and Wildlife Service) authority to deal with pathogens like

Bsal

. The Lacey Act is a blunt tool; Nanjappa is hoping to introduce some finer instruments, including the ability to target particular pathogens and respond quickly when wildlife diseases emerge. She's optimistic about its prospects, in part due to interest she's seen from Congress, including many Republicans. They recognize that such a bill might, in the long term, help keep species off of the Endangered Species List, avoiding the headaches and regulations that listed species engender.

Should

Bsal

manage to slip past the import ban, the story of

Bd

does not bode well. Despite years of research, there are few success stories about combatting it. In one case study, in Mallorca, researchers successfully eliminated

Bd

by removing all the tadpoles from some ponds, treating them with an anti-fungal drug, draining the ponds, dousing the dried basins with fungicide, and then returning the tadpoles after rain had refilled the ponds. But this approach is incredibly costly, not to mention time- and energy-intensive, and it might only work in certain environments. Containment, assuming rapid detection, is another possibility, through culling of infected and nearby salamanders. But containment may ultimately just slow the progress of

Bsal

, rather than stop it.

One promising research area involves probiotics. Countless microorganisms live on salamanders’ skin, apparently unbothered by the toxins many secrete. These microorganisms include bacteria that produce anti-fungal compounds, some of which inhibit

Bd

growth. Vredenburg and his students are planning trials to see if those same compounds can also inhibit

Bsal

. The benefit of using naturally occurring bacteria to fight

Bsal

is that they're already present on salamanders and in ecosystems; using them in the wild wouldn’t mean adding new organisms to the mix. But scientists don’t yet know enough about the potential ramifications of spraying bacteria in and around a pond. There’s some promising evidence that probiotics helped frogs in the Sierra Nevada fight off

Bd

. But safety tests are needed, says Douglas Woodhams, who studies microbiomes and disease ecology at UMass Boston—much like pesticides are tested for their impacts on other creatures. Every management action has risks, Woodhams notes, but those risks “must always be balanced by the risk of losing endangered amphibians if no action is taken.”

Bringing salamanders from the wild into captivity to ride out

Bsal

’s storm, or for probiotic treatment, is another option. But inevitably, hard choices would have to be made about which species we save. Knowing which ones are likely to be most susceptible to

Bsal

will certainly help inform those choices. But "we can't just rescue critters, and bring them into captivity, and hope for the best eventually," says Nanjappa. She thinks scientists should be considering more aggressive, proactive approaches, like trying to breed

Bsal

-resistant salamanders in captivity that could then be released into the wild, or even genetically engineering such resistance. "If we don't try and think a little bit bigger about these possibilities, then we're potentially just agreeing to lose all of it," she says.

Conservation biologists and wildlife managers have long struggled to justify the costs and efforts needed to preserve biodiversity and protect threatened species. When I asked Nanjappa why it was important to protect salamanders, she struggled a bit at first. She mentioned their ecological importance, their impressive biomass, and even the possibility that compounds found in salamander skin might someday yield medical treatments. But when I asked her how she, personally, felt about salamanders, she opened up. "You can just stumble on one by flipping a log or a rock, and pick it up, and hold it in your hand," she says. "Most salamanders are very docile, they're smiley, they've got those big, gorgeous eyes, and they're just cute!"

Cuteness aside, we need salamanders, whether we know it or not. The red-spotted newts, enormous hellbenders, eel-like sirens, and ubiquitous red-backed salamanders that make their homes in ephemeral pools, in cold streams, and under rotting logs can’t be replaced in the complex, vibrating webs of life and nutrients that keep our forests alive and beautiful. If we lose salamanders, says Vredenburg, “we’re switching towards the cockroach economy of the world.”

Back at the roadside pond in Massachusetts, the sun has broken through the clouds as Grant and his assistant wrap up their sampling. Total haul: 28 swabs from 14 lesion-free newts. In the next few days, they'll sample sites in eastern Massachusetts; other teams are sampling sites further south, down through Appalachia. Grant doesn't expect to get results back from the swabs until the end of the summer. With luck, they'll be negative, and the window to save America's salamanders will stay open a little longer.

Map by James Davidson

Yellow-eyed Ensatina (

Ensatina eschscholtzii xanthoptica

) salamander near creek photo by Sebastian Kennerknecht.
Red-Bellied Newt (

Taricha rivularis

) on white photo by Emanuele Biggi.

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ABOUT THE Author

Geoffrey Giller is a freelance science writer and photographer based in Ithaca, New York. He has a Master’s degree in environmental science and a special love for amphibians. His writing has also appeared in

Scientific American

,

Audubon

, and

Hakai Magazine

, among other outlets. You can follow him on Twitter @GeoffreyGiller and see more of his photography and writing on his website.

Geoffrey Giller

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