Karen Lips, Sabin Award Winner 2012

Karen Lips, Sabin Award Winner 2012

Dr Karen Lips, currently based at the University of Maryland, is a ground breaker. Much of our understanding of the underlying causes of amphibian declines and extinctions can be attributed to her work. Add to this her considerable effort in basic tropical ecology and systematics, and you have a broad-based world leader in tropical biology, a ground-breaking leader on research into amphibian declines, and also a leader in conservation policy making.

Building on her early efforts to determine the underlying causes of amphibian declines, Dr Lips is now involved in some truly cutting-edge collaborative work to investigate the genetic basis of amphibian responses to chytrid infections and the genetics of the chytrid fungi themselves.

In addition to her research Karen has co-led efforts to conceptualize, fund and realize the RANA network – a network of Neotropical amphibian specialists that has been extraordinarily influential and successful cross-disciplinary and international framework of collaboration and data sharing.

Dr Lips was accepted as a Fellow into the rather exclusive Aldo Leopold Leadership Program and continues to be an inspirational leader.

Seeing the Before and After

By Dr Karen Lips

I grew up in Jensen Beach, Florida, a small beach town where the Indian River Lagoon and the St. Lucie River empty into the Atlantic Ocean. I was lucky having grown up in subtropical Florida ñ a place rich with unusual plants and animals, unique habitats, and rare species.   I grew up watching the sea turtles come up to breed on beaches during the summer, and I remember watching the House of Refuge staff release boxes of head-started turtles in the fall.  I spent a lot of time snorkeling in the Florida Keys where I learned about marine biology, I stomped through the marshes and swamps, and explored the scrub habitat where we saw gopher tortoises, indigo snakes and rattlesnakes. But I also grew up at a time when South Florida was entering a building boom where development was rapidly expanding along the beaches, the upland areas, and along the marshy headwaters of the Everglades.

After I graduated from the University of South Florida (USF)with a B.S., I spent a year as an intern at Archbold Biological Station (ABS) in Lake Placid, Florida.  At ABS I learned more in one year than I had in all four years of college and still consider this one of the most influential periods of my career.  I discovered the excitement of field biology, I learned how to study vertebrate ecology, and I did an independent project that exposed me to the trials and tribulations of field research.  I did an independent research project where I compared the numbers and kinds of small animals that lived in gopher tortoise burrows in different kinds of habitat. Out in the hot, dry scrub of South Florida, tortoises create underground burrows that provide a cool moist habitat for delicate amphibians, endemic invertebrates, and cool mammals and reptiles. Many of these species only occupy gopher burrows that are kept clean and open by a resident tortoise.  Amazingly, the most abundant vertebrate in these burrows was the tiny, exotic Cuban greenhouse frog (Eleutherodactylus planirostris).  Growing up in South Florida, I was familiar with the growing numbers of exotic species which would become a major problem over the years.  The other lesson I learned was that where tortoise populations were being lost to development and habitat fragmentation, we were also losing a large number of endemic or endangered animals.

As amazing as my experience at ABS was, I was intrigued by the exciting organisms and exotic locations my fellow interns described. I especially remember a talk by my friend Nancy who had studied in Costa Rica and who had seen the golden toad in Monteverde.  I remembered from my Herpetology class at USF how diverse and interesting those tropical frogs were, and also how little was known about them.  I decided to apply to grad schools where I would be able to study tropical herpetology.  In 1988 I started graduate school at the University of Miami, in the lab of Dr Jay Savage, where I eventually designed a project on stream frogs in the Reserva Protectora Las Tablas, adjacent to the Amistad Biosphere Reserve.  Amistad is located in the Talamancan Mountains on the border with Panama, and is one of the most remote, biologically diverse, and unexplored areas of Costa Rica.  In 1991 I moved into a 4 x 4 m shack without electricity or running water located at the top of a mountain in the cloud forest.  I lived there alone for two years, while I studied the population ecology of Isthmohyla calypsa, a spiny, green, iridescent treefrog known only from this mountain. I saw Quetzals every day as they floated across the open pasture, showing off their long, green iridescent tails.  I was stalked by jaguars and mountain lions, and collected many new species of amphibians and reptiles.  It seemed like everything was new, and that even for the species that had names, there was little ecological information. There was so much to do – I felt overwhelmed by the sheer amount of the unknown, but I also figured I had enough projects and species to study for decades.

But things were about to change.  I went home for Christmas in 1992, and when I returned in 1993, I had trouble finding enough frogs. It was a mystery.  At first I blamed it on the weather, the rains were delayed that year and I couldn’t imagine what else could have such a sudden and widespread loss.  I figured that as soon as the rainy season started I would be back in business. A few years later, after I graduated with my PhD and had taken a job, I would return to the site and still find no frogs under perfect conditions.  While I still did not know what caused the disappearance, I had undeniable evidence that a large and diverse mix of species had disappeared quickly and completely from one of the most remote, protected, and pristine sites in all of Central America.

I had not planned on studying amphibian declines – I was a first year graduate student, and even the experts did not know what was happening, or the causes of these declines, where or when they might occur, or how to recognize them, much less how to study them!  But I happened to be in the right place at the right time, and had the right kind of data to piece it all together.  But now I had a new problem ñ the site where I expected to work for years no longer had any frogs, and I needed to develop a new research program.  I decided I would move to Fortuna, a nearby site in western Panama where I had spent a few days searching for my study species.  I did not find that species, but had found over 36 species in two days, so I knew amphibians would be plentiful for study. Fortuna was a Forest Reserve, and was administered by a Panamanian electric company as a new hydroelectric project.  While not as pristine, nor as remote as Las Tablas, the site was easily accessible by road and had a diverse  amphibian fauna.  I remember thinking how lucky I was to have found such a perfect site for long-term research and in 1995 I started to run transects and collect tadpoles. With a full time job, I wasnít able to spend years at Fortuna, but I used summer and winter breaks to escape to the tropics and gather baseline data on amphibian populations.

About this time I remember telling Dr Stan Rand, the resident herpetologist at the Smithsonian Tropical Research Institute (STRI) that I had a hunch that whatever happened in Monteverde ñ where the golden toad had disappeared 10 years earlier ñ was the same thing that happened at Las Tablas, and that if the trend continued, I expected it to show up in western Panama. But nobody was more surprised than I when in December 1996 I returned to Fortuna and found dead and dying frogs along every transect.  In three weeks we collected 50 frogs and sent them to Dr. David Green, a vet pathologist at the U.S. National Wildlife Health Center to determine what caused their death.  Meanwhile, just as I had done for Las Tablas, I described all the evidence for what might have caused such a rapid decline and die-off of the Fortuna amphibians.  I had seen many of the same trends, which was consistent with a disease moving in an epidemic-like wave.  Dr Green wrote to say that the dead frogs all had some unusual skin infection, although he did not know what this was.  I was surprised and told him about some unpublished findings from seven dead frogs I had collected from Las Tablas in 1992.  Dr Rebecca Papendick had g how lucky I was to have found such a perfect site for long-term research and in 1995 I started to run transects and collect tadpoles. With a full time job, I wasnít able to spend years at Fortuna, but I used summer and winter breaks to escape to the tropics and gather baseline data on amphibian populations.

About this time I remember telling Dr Stan Rand, the resident herpetologist at the Smithsonian Tropical Research Institute (STRI) that I had a hunch that whatever happened in Monteverde – where the golden toad had disappeared 10 years earlier – was the same thing that happened at Las Tablas, and that if the trend continued, I expected it to show up in western Panama. But nobody was more surprised than I when in December 1996 I returned to Fortuna and found dead and dying frogs along every transect.  In three weeks we collected 50 frogs and sent them to Dr. David Green, a vet pathologist at the U.S. National Wildlife Health Center to determine what caused their death.  Meanwhile, just as I had done for Las Tablas, I described all the evidence for what might have caused such a rapid decline and die-off of the Fortuna amphibians.  I had seen many of the same trends, which was consistent with a disease moving in an epidemic-like wave.  Dr Green wrote to say that the dead frogs all had some unusual skin infection, although he did not know what this was.  I was surprised and told him about some unpublished findings from seven dead frogs I had collected from Las Tablas in 1992.  Dr Rebecca Papendick had examined them in 1994 but other than an odd skin infection, none of the usual amphibian pathogens were present at lethal levels. But now that we had dead frogs from two declining sites, and both had the same kind of skin infection, we began to wonder if we had found the smoking gun!

Our results were picked up by the New York Times, who published a photo of the odd skin infection.  That photo grabbed the attention of a team of scientists at the National Zoo who had been trying to identify a skin fungus that was killing frogs in their captive populations.  The article was also seen by a team in Australia who had an organism infecting the skin of dead frogs in the field and in the lab.  Behind the scenes, Dr George Rabb worked to bring these three groups together at the University of Illinois in late 1997 to compare samples and exchange information.  It was there that we all realized for the first time that we had evidence for a novel pathogen that seemed to be responsible for the global decline of amphibians.  We also learned that it had a name, Batrachochytrium dendrobatidis, or Bd.

It was time again to find another new field site.  This time I had more than a hunch that it was moving along the Cordilleras that run through Central America.  This time I knew what I was doing, and I was going to stake out a place and wait for this thing to arrive so that I could see what it did, and hopefully figure out how it moved and where it occurred, so that we could figure out how to stop it. Finding a protected area at higher elevations and with road access was more difficult ñ east of Fortuna was an extensive area of Indigenous Reserves, and areas of heavily grazed grasslands.  I spent many days driving into the mountains only to end in small towns surrounded by pastures and see the forest far off in the distance.  Some places, like the mountain streams above the town of Santa FÈ, I would continue to visit every year, but this was not yet an official park, and there was no lodging close to the forest.

So I set up research transects in Parque Nacional Omar TorrÌjos, a national park just above the town of El CopÈ in Central Panama.  After the old growth oak forests of montane Costa Rica and western Panama, I was not impressed by the relatively low elevation cloud forest at El CopÈ.  The forest had of the large mammals.  The road sucked.  It was hot.  And boy, those trails were steep!  Wherever you went, you had to climb up eventually.   But there was a small house where we could sleep and store our gear.  Living right on the Continental Divide meant we could see both the Atlantic and the Pacific Oceans on clear days.  Not only did the park straddle the Continental Divide, but it was also located at the eastern end of the Cordillera Talamanca, and the beginning of the Cordillera Central, so it was a biogeographic crossroads between the North and South American faunas, and also between those from the Atlantic and Pacific slopes.  The longer we surveyed, the more species we found ñ eventually reaching 74 species of amphibians and over 90 species of reptiles.  I was back to thinking that if Bd did not appear, I would have decades of research to do on all these amazing species.    But of course one day in 2004 Bd arrived at the site, and within a week we found our first dead frog. We collected 400 dead and dying animals in the next three months, until there was nothing left to collect.  In the end, the dead frogs represented almost all of the species known from the site, all possible life styles, and all possible habitats of tropical frogs. This unfortunately, was the proof we were looking for that Bd was an invasive pathogen, spreading through naive populations of amphibians from southern Mexico to Central America.  I would explore this idea further by studying the history of population declines in South America and showing that the timing of population declines of harlequin frogs (Atelopus) in the 1970’s and 1980’s was consistent with the spread of Bd through the Cordilleras of the Andes, and that this pattern had no relationship to changes in climate over that period.

For the past few years I have been working in the eastern-most region of Panama, all the way up to the Colombian border.  These sites are a diverse mix ñ all are in the mountains, but some are quite low in elevation, or are on the drier Pacific slope, while others are the equal of any site in the Talamancas of Costa Rica.  I no longer spend years at one site, but visit several sites every year.  Access is more difficult ñ sometimes we use horses to survive the five-hour hike up the hill, or we charter small planes to fly us in between the mountains and onto tiny grassy landing strips in the middle of the jungle where jaguars still roam.  We are quantifying changes in the abundance and species richness ofthese sites, swabbing frogs to determine their disease load, and marking animals to figure out whether their demography has been affected by disease.  We are also looking for evidence that survivors are evolving resistance to disease by comparing the genetic composition of frogs sampled ahead of the wave to those sampled after the wave has passed through.  For a while, I had hoped that some of these sites might be uninfected, and allow us to watch the epidemic again.  But this time we arrived too late ñ all these sites were Bd-positive during our first visit, and have already declined.  How much they have declined will never be known ñ most of these sites were unexplored, and we had no list of species collected.

A few years ago I took a job at the University of Maryland.  The proximity of the Appalachian Mountains was just too tempting, and I quickly developed a project that would allow us to work close to home, but in yet another amphibian biodiversity hotspot!  For the past two years we have been surveying populations of woodland salamanders across the Appalachians, searching for evidence of population declines and disease.  It is a joy to work with the species-rich, well-studied, and ecologically important group of woodland salamanders. Best of all, we have access to extensive historical records of weather, land use, and salamander populations from generations of ecologists and collectors working in the area.  After all those years of working with limited background information on species distribution and ecology, it is a welcome change to be able to ask different kinds of questions that build off a solid ecological and evolutionary foundation.  Already we will be able to show that Appalachian salamander populations have declined across their range, that losses were species-specific, and that Bd was involved – many of the same patterns described in the loss of tropical frogs.

What is surprising is that in the heavily populated East Coast, in the backyard of our Nationís Capitol, and in some of our most visited parks, few people thought this was anything other than natural population fluctuations.  Of course, these are small, brownish animals that spend most of their lives underground, and many have very large populations and very large distributions that would make extinction very unlikely so itís more difficult to show that populations have really declined.  Ironically, for me the good news is that Bd has already passed through, and although abundances are down compared to historical times, there are still lots of salamanders; best of all, it seems that no species were lost.  These populations are evolving and have likely developed genetic, physiological or ecological defenses to coexist with Bd.  I am happy to think that I will probably not witness a mass die-off here.

But it’s a Bd world now, and the kinds of questions we need to ask and the kinds of research we do are different.  There arenít many places left on the planet where Bd doesnít yet occur, so while the chance of catching another epidemic are low, so is the number of future extinctions. Still, I dread the day when I hear that an infected frog has been found on Madagascar or Papua New Guinea where amphibian biodiversity and endemism are the highest in the world.  That is going to be a very bad day.

I have been put in a unique position, to have seen the Before, and to have seen the After, and to know that hundreds of amphibian species have gone extinct while I watched.  It is bittersweet to know enough to predict what will happen next, but not be able to stop it.  But I also know that Mother Nature is resilient, and that evolution happens, and that one day some amphibian populations will increase in abundance, as they evolve various ways to combat or tolerate Bd.  I hope I get to see that too.