Lessons of the Lost
Amphibians are all but gone, bequeathing us lessons that must not be squandered
I learned great and terrible lessons in my first year of graduate work in 1989—more than I expected and more than I realized at the time. My advisor at the University of Texas at Arlington, Jonathan Campbell, arranged for me to spend a field season in Guatemala surveying the amphibians and reptiles in the environs of a coffee plantation near Pueblo Viejo, in the Department of Alta Verapaz. I was going it alone with no Spanish language skills in the midst of a brutal civil war. But there had never been any herpetological work done in this particular part of the country, so I balanced my apprehension with a vision of myself following in the footsteps of the intrepid tropical natural historians and explorers whose monographs I was intensely studying.
During that summer I assembled a good collection of reptiles from Pueblo Viejo, but only a poor collection of amphibians. We all assumed at the time that the paltry representation of amphibian specimens was due to my incomplete skills; where I come from in southern California, reptiles are common and amphibians are scarce. Twenty years later, it is clear to all herpetologists that I had arrived on the scene of a massacre. That field trip launched my research career as an amphibian taxonomist and, indeed, I discovered my first species of frog new to science at Pueblo Viejo. Since then I have had the pleasure of discovering and naming dozens of new species, but some of them I “discovered” on museum shelves and not in the field. My finds had become extinct before they were even named. I chose to become a herpetologist, not a paleontologist, because I enjoy working afield with live animals. Recent reflection has forced me to reconsider my academic title. I am a forensic taxonomist.
Dead on Arrival
It is a bittersweet experience to formally name a new species of animal, knowing that it is probably already extinct. Even more unsettling is the saga of Rabbs’ fringe-limbed treefrog (Ecnomiohyla rabborum), a spectacular new species that my colleagues and I discovered in central Panama in 2005. The publication formally naming it appeared in 2008 in the Journal of Herpetology, but the last individual in the wild was noted in 2007. At this writing, there are two individuals safe in captivity; both of them are males. The species is evidently extinct, even if those remnant males are yet unaware. Have you seen the iconic film clip of the last thylacine—the Tasmanian tiger—in its zoo enclosure? There is now a companion clip on YouTube of the second-to-last Rabbs' treefrog.
The crisis of global amphibian extinctions is profound, it is changing ecological systems in ways that we barely understand, and it is teaching us painful lessons about research and conservation. Amid all of the horrible environmental insults we inflict upon the planet’s biodiversity, Rabbs’ fringe-limbed treefrog did not disappear in the wild because of overharvest for food, pets, or science, and we cannot lay the blame on familiar threats such as deforestation, climate change or environmental pollution. The culprit was emerging infectious disease. Amphibian chytridiomycosis is capable of directly eradicating otherwise large and stable populations and directly causing extinction of species that are otherwise unthreatened.
Amphibian chytridiomycosis is a disease caused by the recently discovered chytrid fungus Batrachochytrium dendrobatidis. In the thallus phase of its life cycle, when fungi colonize to form vegetative masses, this chytrid forms a vase-shaped structure that embeds in the superficial epidermis of amphibians, allowing the fungus to harvest energy from the keratin in the host’s skin.* It then produces motile flagellate zoospores that disperse aquatically. Ironically, the zoospores resemble microscopic tadpoles. Chytrid fungi are generally decomposers or parasites of invertebrates or plants. This is the first taxon in that large group known to be parasitic on vertebrates.**
Batrachochytrium dendrobatidis likely is capable of infecting every species of amphibian on Earth (nearly 7,000 species), representing the broadest host-range of any known pathogen. Host responses vary from complete tolerance to rapid death, with death resulting from cardiac arrest stemming from osmotic imbalance. (Among its roles, keratin is a water-proofing protein). Tolerant host species, such as American bullfrogs (Lithobates catesbeianus), can act as disease vectors as they disperse naturally or are transported globally by humans. Tolerant species in any ecosystem may also act as reservoirs, ensuring that the pathogen remains on site and thereby reducing the probability that vanquished amphibian populations may recover, recolonize or be reintroduced. At some sites, such as the upland areas of Central America, the Andes, eastern Australia or western North America, the arrival of the pathogen into a new area promptly eliminates some amphibian populations, severely reduces others (with little evident recovery even after decades), yet leaves a subset of species infected but otherwise unaffected. At lower elevations, or at other sites such as upland areas of eastern North America, the disease is present but seems to have little effect on local species. Considerable research has been done in an effort to elucidate the synergistic influences that underlie these variable effects among sites and species, but the general answers remain frustratingly unclear. Batrachochytrium dendrobatidis is behaving as an emerging infectious disease and an invasive species on every continent (except perhaps Asia, and of course Antarctica, where no amphibians currently exist). Its native distribution (and naturally coevolved host species) remains unknown.
Herpetologists and wildlife biologists began observing inexplicable disappearances of amphibians around the globe in the mid-1970s and especially by the mid-1980s but were at a complete loss to explain them. Finally, in the late 1990s, an insightful team of pathologists at the U.S. National Zoo, led by Don Nichols, collaborated with one of the few chytrid fungus scholars in the world, Joyce Longcore, and identified this quite unusual new genus and species. Conservationists and disease ecologists were unprepared for the reality of a pathogen capable of directly and rapidly—mere months!—causing the elimination of a population or an entire species that was otherwise robust. Classical host-pathogen theory held that such dramatic consequences to the host population or species were only realized when the host population was already drastically reduced in size or otherwise compromised. The concept of a lightning extinction was foreign to researchers and conservationists, and we argued vehemently about it throughout the 1990s at symposia worldwide. In retrospect, the scenario of a spreading pathogen is parsimonious and clear, but in the midst of the massacre we were entangled in logical quagmires along these lines: “The disappearances cannot be the result of disease; diseases are not capable of such.” Not to mention the fact that the smoking gun, the pathogen itself, was not described until 1999. While we were debating the issue, a terrible lesson was playing out for us around the world as an unknown disease decimated amphibian populations. This lesson has led to an overdue focus on other neglected amphibian diseases, such as those caused by ranaviruses. I highly recommend the recent and quite readable book Extinction in Our Times: Global Amphibian Decline by James P. Collins, Martha L. Crump and Thomas E. Lovejoy III, which offers a complete history of the phenomenon and the desperate plight of the global stakeholders.
*Due to an editing error, this sentence has been corrected in the
online version of the essay. The original sentence began, "In the thallus or mycelium phase of its life cycle. . . ." 10/13/2011
**Due to an editing error, this sentence has been corrected in the online version of the essay. The original sentence read "Chytrid fungi are generally decomposers, and this is the first taxon in that large group known to be parasitic." 10/13/2011
Death in the Family
The scope and scale of these declines is truly difficult to grasp. Up until about the late 1980s there were at least 97 species of harlequin frog (Atelopus) in the Neotropics (several of them now known only because of the forensic taxonomy skills of my colleague Luis Coloma in Ecuador); only about 10 species can now be located. Perhaps 38 species of northern rain frogs (Craugastor rugulosus group) were distributed along montane streams in Central America; only four or five are still extant. I personally found the last known individual of one of these species in southern Mexico in 2000. The concept of “endangered species” does not apply here. We are witnessing the nearly complete elimination of entire clades of species. This is another lesson learned, as we were all trained that such things are only to be observed in the fossil record. This precedent from the amphibians forces us to address the serious implications for possible disease-driven losses among other major clades. Consider for a moment the potential consequences of clade-level extinctions among monocot plants (corn, rice, wheat), pollinating insects, salmonids or scombrid fishes (mackerel, tuna), mammals or birds.
Amphibians are the typically uncredited vertebrate basis of almost all ecosystems on the planet, by virtue of the astounding biomass and population densities they can achieve despite their typically small body size. However, they are secretive and often nocturnal, so their reign is a well-kept secret, even among most ecologists. In light of this, a couple of qualifications about extinction are required. First, extinction is difficult to demonstrate unequivocally (as it is based on negative evidence), so organizations such as the International Union for the Conservation of Nature (IUCN) justifiably are quite conservative in their assignment of the term, and we sometimes get it wrong. Second, extinction is simply defined by zero living representatives, but we are in need of a conceptually clear categorization of “functionally extinct” to account for the many hundreds of species of amphibians that swirl in the so-called extinction vortex, no longer able to provide the important goods and services they once contributed to ecosystems. They are only nearly extinct, which may make us feel better (or worse), but they don’t really exist in a functional sense. The typical biomass of amphibians and the sheer magnitude of their declines and extinctions requires me to make bold statements, such as “There no longer exists a natural upland ecosystem in Mesoamerica” despite many fully protected reserves. I published that statement recently in Herpetological Review, and I note that no one has argued with it. In fact, my colleague Larry David Wilson extended the concept to suggest that virtually all publications of field-based research should bear a label: “Warning: this study was conducted in a disturbed ecosystem.” The point is that the baseline of amphibian diversity and populations has shifted dramatically in many areas and no one—not even amphibian biologists—is adequately addressing that reality.
Amphibian declines must affect any ecological studies at famously “pristine” sites like La Selva Biological Station in Costa Rica, and they also affect evolutionary studies, taxonomic reviews and biotic inventories. In the latter case, we will never know the true biodiversity of some areas that are yet unsurveyed, and thus we will never be able to fully understand the interdependencies of those ecosystems in their fully evolved complexity. With my colleague Martin Bustamante, I recently learned this lesson the hard way in southern Ecuador, when cumulative months of field work revealed only a handful of amphibian species (several of them new to science) in a “pristine” upland cloudforest reserve that should have harbored dozens of amphibian species. Local ranchers described in wonderful detail a species of harlequin frog they had not seen in years. Quite possibly it represented a species unknown to science, but we will never know because Martin and I arrived after the massacre, too late even to accomplish a decent forensic taxonomic survey of the region. My graduate-school experience in Guatemala in 1989 taught me not to assume that we had simply failed to find the regional amphibians.
Planning for Posterity
Conservationists have been overwhelmed by the amphibian crisis. In the atmosphere of ongoing declines, we realized that there was no framework to address a challenge of this magnitude or rapidity. Even worse than problems of scope and scale is the reality that conservationists, collectively, are stymied by the central problem of not knowing what to do. We have decades of experience as first responders in aid of species threatened by the familiar challenges of habitat loss, pollution and overharvesting. In many of these cases the solution is straightforward (often, stop eating that species), even if the sociopolitical and economic challenges can be formidable. The appropriate conservation response for amphibians perishing from disease must await a real breakthrough in disease control. There is no vaccine for any fungal disease known to affect humans or livestock, despite the high value we place on those species. Breakthroughs in research take time, and the amphibians are teaching us that time is tragically correlated with functional and actual extinctions. Climate change is another difficult conservation challenge for amphibians, but the threat of climate change is shared by all species, so at least amphibians will benefit from global programs conservationists are now battling to enact worldwide.
The IUCN has produced an Amphibian Conservation Action Plan to outline the basic endeavors necessary to confront the global amphibian crisis. The plan outlines important programs to protect habitat, reduce pollution, control commercial harvest, understand the consequences of climate change, and expand efforts toward population monitoring and taxonomic studies. Two major elements of the plan focus on the understanding and control of emerging infectious diseases and on the conundrum of what to do in the case of epidemics. The IUCN has charged the Amphibian Specialist Group (http://www.amphibians.org) and the newly organized Amphibian Survival Alliance with monitoring amphibian status worldwide and implementing an action plan. Meanwhile, awaiting the necessary breakthroughs in research and disease control, IUCN has charged Amphibian Ark (http://www.amphibianark.org) with the difficult task of organizing a global network of captive survival-assurance colonies of those species that can no longer be safeguarded in the wild. Nobody prefers a future in which amphibians on this planet are to be found only in safe-house aquaria at zoos and other institutions, but that is the best hope for some species right now.
Amphibians are teaching us lessons about the state of our planet. Waves of unstoppable fungal epidemics have all but silenced the wonderful frog choruses, all but eliminated the massive hidden biomass of invertebrate-consuming salamanders, and they have done so in some of the most remote and pristine areas left on our planet, including national parks. Those remote and fully protected areas may end up little more than ghosts of epidemics past. We remain pitifully ignorant of the basic biology, and the fates, of the ever-mysterious earthworm-like caecilians. Jonathan Campbell’s work at Reserva del Quetzal in Guatemala indicates that it has lost about 70 percent of its amphibian species. Karen Lips’s site in the Parque Nacional G. D. Omar Torrijos H., near El Copé, Panama, lost at least 30 species of amphibians (41 percent of the total) in the span of a few months during 2004 and 2005.
I am by profession an amphibian taxonomist, if nowadays a part-time forensic taxonomist, and I am by necessity an amphibian conservationist. The thrill of discovering and naming new species never gets old, but documenting the disappearance of any species—especially ones that I discovered and named—feels like a personal blow every time it happens. I never anticipated that my career as a neontologist in the life sciences would so closely resemble paleontology. There is a parallel between what amphibian taxonomists do these days and what homicide detectives do. Both arrive at scenes of mayhem. Maybe they solve the crime, but they are powerless to undo it. Yet the difficulty of demonstrating actual extinction gives me a flicker of hope. I hope that I am wrong in some of my scientific endeavors—a posture I never anticipated as a graduate student.
Our powerlessness in this terrible crisis must be balanced by increased efforts in realms that we can control, such as reducing carbon emissions to protect what habitat remains from chemical and physical disruption. We can go further and restore what has been wounded but can still be salvaged. We need to inspire and fund truly innovative research on pathogens in order to better predict and thwart emerging infectious diseases. The lessons we learn here will extend far beyond the amphibians. We must support funding for programs such as the Amphibian Ark and the Amphibian Survival Alliance. We must keep looking for species gone missing, and continue biodiversity surveys, despite the sometimes paralyzing depression that both activities can induce in this era. But especially, we need to pay close attention to the lessons that legions of dead amphibians are teaching us. I note with some satisfaction that our colleagues in bat research and conservation did not spend a decade arguing whether the fungus that causes white-nose syndrome could possibly eliminate entire colonies of bats in a single season. Our colleagues assumed that it was possible and reacted quickly. We can thank the amphibians for leaving us that lesson, but at such cost.
- Cheng, T. L., S. M. Rovito, D. B. Wake and V. T. Vredenburg. 2011. Coincident mass extirpation of neotropical amphibians with the emergence of the infectious fungal pathogen Batrachochytrium dendrobatidis. Proceedings of the National Academy of Sciences (USA). doi: 10.1073/pnas.1105538108.
- Collins, J. P., and M. L. Crump. 2009. Extinction in our Times: Global Amphibian Decline. Oxford University Press.
- Crump, M. L. 2000. In Search of the Golden Frog. Chicago: University of Chicago Press.
- Fisher, M. C., T. W. J. Garner, and S. F. Walker. 2009. Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. Annual Review of Microbiology 63:291–310.
- Gascon, C. J., P. Collins, R. D. Moore, D. R. Church, J. E. McKay and J. R. Mendelson III (eds.). 2007. Amphibian Conservation Action Plan. IUCN/SSC Amphibian Specialist Group. Gland, Switzerland, and Cambridge, UK.
- La Marca, E., et al. 2005. Catastrophic population declines and extinctions in Neotropical Harlequin frogs (Bufonidae: Atelopus). Biotropica 37:190–201.
- Lannoo, M. (ed.). 2005. Amphibian Declines: The Conservation Status of United States Species. Berkeley: University of California Press.
- Lannoo, M. 2008. Malformed Frogs: The Collapse of Aquatic Ecosystems. Berkeley: University of California Press.
- Lips, K. R., et al. 2006. Infectious disease and global biodiversity loss: pathogens and enigmatic amphibian extinctions. Proceedings of the National Academy of Science (USA) 103:3165–3170.
- Mendelson, J. R., III, et al. 2006. Policy Forum: Confronting amphibian declines and extinctions. Science 313:48.
- Mendelson, J. R., III, and R. Donnelly. 2011. The Crisis of Global Amphibian Declines: Causes, Consequences, and Solutions. Network for Conservation Educators and Practitioners. New York: American Museum of Natural History. http://research.amnh.org/biodiversity/ncep
- Nichols, D. K. 2003. Tracking down the killer chytrid of amphibians. Herpetological Review 34:101–104.
- Rosenblum, E. B., J. Voyles, T. J. Poorten and J. E. Stajich. 2009. The deadly chytrid fungus: a story of an emerging pathogen. Public Library of Science Pathogens 6:e1000550.
- Skerratt, L. F, et al. 2007. Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4:125–134.
- Stuart, S. N, et al. 2004. Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786.
- Voyles, J., et al. 2009. Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science 326:582–585.
- Vredenberg, V. T., R. A. Knapp, T. S. Tunstall and C. J. Briggs. 2010. Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proceedings of the National Academy of Sciences (USA). doi/10.1037/pnas.0914111107.
- Whitfield, S. M., et al. 2007. Amphibian and reptile declines over 35 years at La Selva, Costa Rica. Proceedings of the National Academy of Sciences (USA) 104:8352–8356.