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Home , Allobates, Allobates zaparo, Archaeobatrachia, Hemiphractidae, Iberian ribbed newt, Pelobatoidea

Current Biology Magazine

Primer Leiopelmatoidea (6) Discoglossoidea (21) Pipoidea (42) a (228) } David B. Wake* and Michelle S. Koo

Since the dawn of history, amphibians b have been a part of human culture. Western Europeans built fi res for (6682) cooking and warmth, adding large c logs as needed. What occasionally emerged was astounding: large black (which had found shelter in the logs) with four legs and a tail, jet d black with striking bright yellow spots. Cryptobranchoidea (72) These fi re were variously Sirenoidea (4) thought to be the product of the fi re e

itself, or, as Aristotle reported, capable Caudata Anura of extinguishing fi re. Pliny the Elder (490) f is said to have tested this idea by Salamandroidea throwing a into fl ames — g the salamander died! — nevertheless (156) the association with fi re persisted. Pliny perpetuated other fantastical claims, which spread; even Leonardo da Vinci Rhinatrematidae (11) contributed to the legend, and myths Ichythyophiidae (57) from different regions merged — at h one point, asbestos was claimed to Crown Group be salamander wool. Salamanders (141) were attributed great powers; a single salamander upstream was thought Current Biology to be suffi cient to kill an army. King Francis I. of France chose a salamander Figure 1. The tree of life. as his emblem — a powerful symbol, The three orders of amphibians differ greatly in numbers, morphology, and reproductive modes. born of fi re, fi lled with poison, immune Generalized phylogeny is shown with the number of for major clades in parentheses. Amphibians shown include: (a) Xenopus leavis (), a fully aquatic species from burning, and even able to douse (photo: B. Gratwicke); (b) tricolor (Dendrobatidae), a toxic species that sequesters fl ames. Before the emergence of great toxins from its diet (photo: D. Cannatella); (c) Rana aurora (Ranidae) has a ‘typical’ life history cities and conurbations, people grew with eggs laid in a pond where they hatch and grow as until metamorphosis into an adult up surrounded by nature. Salamanders form (photo: B. Freiermuth); (d) females of the frog johnsoni () carry and , and were all developing eggs on their backs, where they hatch into fully formed miniatures of adults (photo: D. part of normal human experience. Wake); (e) Ensatina eschscholtzii (Plethodontidae) females guard their eggs, which hatch into fully formed miniatures of adults (photo: H. Greene); (f) Salamandra salamandra (), the Myths such as those surrounding the Fire Salamander of European folklore (photo: A. Noellert); (g) Ambystoma andersonii (Ambysto- fi re salamanders were commonplace. midae), a critically endangered permanently larval form closely related to the model organism A. Shakespeare’s witches brewed with an mexicanum, the Axolotl (photo: L. Fehlandt); (h) annulatus (), a eye of and tail of frog. As a child, whose females stay with their eggs until they hatch into miniatures of adults and feed on a lipid we raised tadpoles and were taught to secretion produced by the skin (photo: C. Jared). shudder at the appearance of a tiger salamander in a root cellar. In general, at high risk of extinction, and by 2008, taxa are early Mesozoic in origin. The amphibians are seen as benign and the decline of amphibians was seen as earliest known frog (Triadobatrachus) harmless, even helpful as creatures evidence of an impending sixth mass lived about 250 million years ago that devour harmful insects and serve extinction. (early ). They are survivors, as an alternative food source. Thus, it with several modern families dating came as a shock to most biologists and Amphibian and anatomy to mid- (110–120 million to the public at large in the 1980s that Amphibians constitute three major year ago); amphibians appear to have amphibians around the world were in taxa: anurans, the frogs and toads; passed through the mass extinction decline and that they were at greater caudates or urodeles, the salamanders at the end of the Cretaceous relatively risk of extinction as a taxon than any and newts; and gymnophiones, the unscathed. Salamanders and frogs are other group. A study of every limbless caecilians. Amphibians are an well-known and broadly distributed, but amphibian species known in 2004 ancient group, representing remnants caecilians remain poorly known even showed that on the order of 40% were of the fi rst land . Modern to professionals. Caecilians are mainly

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islands in the temperate and tropical A regions (for example, they are abundant on Madagascar, the Philippines, Borneo and New Guinea), but absent from all but a very few oceanic islands. They are especially abundant in the tropics. In contrast, salamanders are distributed mainly in northern regions (although they reach below the equator in ). Salamanders are absent even from most large continental islands (all those mentioned above) and all oceanic islands. Most restricted of all, caecilians are limited to the tropics. The three groups of amphibians are so distinct in appearance that they never are mistaken for one another. B What they most notably share is a moist skin, which serves as the main respiratory organ and produces diverse secretions, many of them poisonous to other organisms. The frog body plan is highly conserved and they are unmistakable for any other vertebrate. Frogs have very short trunks, with nine or fewer vertebrae in front of the sacrum. Their bodies are made larger by the elongated pelvic girdle. All adult frogs lack tails. Forelimbs are relatively short, but hind limbs are long. Frogs have four digits on the forelimb and fi ve on the hind limb, but sometimes one or two are very small. The hind limbs C contain four well-defi ned segments and can be very long, enabling some species to make prodigious leaps. Leaps exceeding two meters have been recorded. However, many species that live mainly underground have short legs and walk or hop, or burrow, rather than leap. Heads of frogs are large relative to body size. Salamanders typically have the body type of a prototypical, generalized land vertebrate, with well-proportioned heads, limbs of roughly similar length, and a tail about as long as the head Current Biology plus body. Trunks are of moderate length with between 12 and 22 Figure 2. Global distribution of the three orders of amphibians. presacral vertebrae and the tail is The three orders of amphibians differ in distribution with frogs (A) commoner to the south, sala- sometimes much longer then the manders (B) to the north, and caecilians (C) restricted to the tropics. Darker colors toward blue body. Limbs are of moderate size and indicate higher species richness. Based on data for 7,011 species from AmphibiaWeb and IUCN usually overlap when pressed against 2018. the trunk; the limbs have three major burrowers (fossorial) that rarely are seen salamanders are more closely related segments. Salamanders are like frogs on the surface; little is known of their to each other than either is to caecilians in having no more than four digits on life history. Today nearly 8,000 living (Figure 1). These three groups are the forelimb, while fi ve typically are amphibian species are known, of which distributed very differently around the found on the hind limb. Because of 88% (~7000) are frogs (anurans), about world (Figure 2). Frogs are found on their appearance, people may mistake 9% (~700) are salamanders, and about all continents except Antarctica and salamanders for lizards and vice versa. 3% (>200) are caecilians. Frogs and on most large and small continental A few exceptions include aquatic

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amphiumas and sirens, salamanders that have become elongate and eel-like with reduced or absent limbs. Aptly called giant salamanders of China and Japan can exceed 1.5 meters in length. Other salamanders have retained aquatic larval morphology, usually with feathery external gills and keeled tails, throughout life. Caecilians differ sharply from other amphibians. They are superfi cially worm-like, with bodies marked by rings. Most are terrestrial burrowers, but a few are aquatic. The head is small and much the same width as the anterior trunk. The very elongated trunk often contains well over 100 vertebrae. The tail is typically absent, but some species have a very short tail. The cloacal opening is usually at the very end of the . Eyes are Figure 3. Amphibian warning colors. Aposematic (warning) coloration has evolved many times in amphibians, and mimicry is wide- reduced to nearly but never completely spread. Top: these poison dart frogs live together in Ecuadorian and northern Peruvian rainforests: absent. The mouth is large with Ameerega bilinguis (left) is toxic and distasteful to predators, which the harmless Batesian mimic many teeth. The head has a unique zaparo (right) uses to its advantage. Bottom: the polymorphic salamander Ensatina chemosensory organ, the tentacle, eschscholtzii (right; Plethodontidae) mimics the highly toxic Rough-skinned newt Taricha granu- which lies between the external nostril losa (left; Salamandridae) in parts of its range where the two species overlap, and only here does it and the mouth and fl icks in and out closely resemble the newt. Pictured specimens are displaying their bright eye and ventral colora- tion (photos: D. Cannatella (top); A. Schusteff (bottom left), H. Rockney (bottom right)). like a snake’s tongue. Limbs or limb rudiments are completely absent, even Thousands of species of frogs, Their skin distinguishes amphibians during development. hundreds of salamanders, and from other vertebrates. It is well nearly all caecilians diverge from vascularized and serves as the main Amphibian biology the typical life history. The most respiratory organ. It is richly supplied Water governs the lives of all common difference is loss of the larval with diverse glands that produce an amphibians, although a few frogs and stage; eggs that develop directly amazing array of secretions, some salamanders have gone to extremes into miniatures of the adults are laid of which help moisten the skin while of specialization to live in places on land. A stark contrast is found others produce a broad array of where water is scarce. Many frogs and in some salamanders that remain poisons and toxins. Chromatophores especially the tropical salamanders live in a larval state (usually with gills in the skin produce the often dramatic on trees. and fi ns) throughout life, a condition colors that characterize many species What is often presented as a often termed paedomorphosis or (Figure 3). typical amphibian life history is neoteny. In many caecilians, eggs Several amphibians qualify as strongly biased by the fact that are retained in modifi ed oviducts ‘model organisms’, which are used early biologists who first described and nourished before — sometimes in experimental biology. The most amphibians resided in temperate very large — miniatures of adults famous are the Axolotl (Ambystoma zones, where the ‘typical’ amphibian emerge; this is true viviparity. Both mexicanum; especially important in life history dominates: land-dwelling frogs and salamanders have a few studies of limb and tail ) adults gather at ponds or streams in viviparous species that give birth to and the tetraploid African clawed frog spring to meet, mate and reproduce. metamorphosed young that have been (Xenopus laevis) and its diploid relative Females lay eggs in water, which are nourished, but they are uncommon. X. tropicalis, both widely used in studies then fertilized by males. Tadpoles Instead, especially in frogs, almost of developmental and cell biology. A (in the case of frogs) or larvae endless variations are found on the few additional frog and salamander (salamanders) are produced that grow theme: stay out of water, where danger species are widely used, including the and metamorphose into tiny juveniles, lurks. Eggs are laid in bromeliads Iberian ribbed newt ( waltl). which return to land. Europeans on tree branches, placed in vocal There are two major impediments knew about some alternative life sacs of males, in compartments on with amphibians as model organisms: histories; the midwife toads (Alytes) the backs of females, even in the husbandry (which explains why there is lay a few large eggs in water, which stomach! Larvae in bromeliads are no caecilian model organism as there are collected by males and draped fed nutritive eggs, or they have many is no captive breeding protocol) and around their hind limbs until they specializations for living in unusual lack of complete sequenced genomes. are ready to hatch, when they were places. Reproductive diversity is one Genomes of the two Xenopus have returned to ponds. of the hallmarks of amphibians. been available for a few years, but two

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as destruction, the clearing of forests for timber and replacement with agricultural land, expansion of urbanization and drainage of wetlands. Other factors include the widespread use of pesticides and fertilizers and the infl uence of increasing environmental temperatures and droughts associated with climate change. What has attracted the greatest attention, however, is a pathogenic chytrid fungus of very wide distribution that has had a demonstrated devastating impact on amphibians worldwide (Figure 4). The pathogen, Batrachochytrium dendrobatidis (or Bd), was discovered only at the end of the last century and since then has become a major focus of investigation. The microscopic organism invades the permeable skin and disrupts the osmotic balance of the infected individual, ultimately killing it by inducing heart failure. Bd Figure 4. Amphibian threats. was fi rst detected in outbreaks of Amphibians are being hit hard by pathogenic fungi. Top: the blue-tailed fi rebellied newt (left; Cyn- extreme mortality in amphibian-rich ops cyanurus) and oriental fi rebellied (right; Bombina orientalis) are Asian species suspected environments of the Australian wet to be agents in the spread of chytrid fungus worldwide, in part due to their popularity in the pet tropics and upland cloud forests in trade (photos: T. Pierson, T. Leenders). Bottom: the harlequin frog (left; Atelopus varius) from Costa Rica and Panama. Massive Central America through , and salamandra chica (right; Bolitoglossa chica) from north- western have experienced precipitous declines attributed mainly to chytridiomycosis mortality also occurred in formerly outbreaks (photos: B. Gratwicke, S. Ron). abundant mountain yellow-legged frogs in the high Sierra Nevada in salamander genomes have become Nature (IUCN) published in 2004 found the iconic national parks (Yosemite, available only now. Few other complete an astounding 43% of species to be Sequoia Kings Canyon) of California. genomes have been obtained because experiencing population decreases; Subsequently, outbreaks have been the very large genomes of many 7.4% were in the highest category traced to the early 1970s in Mexico, frogs and all salamanders are a major of risk. This is the highest level of and there is circumstantial evidence impediment. Genome sizes range as endangerment of any major vertebrate of even earlier events elsewhere. The high as nearly 15 Gb for frogs and taxon and is especially worrisome fungus is likely to have arisen in eastern well over 100 Gb for salamanders. because 22.5% of the then-known Asia, where it is endemic and seems to Species with very large genomes species (5743) were so poorly known cause little harm, and to have spread experience greatly reduced cell cycle that they could not be assessed. These out, possibly from Korea, near the times, slow development and long species are also likely to be in high-risk middle of the 20th century. Mitigation of generation times, as well as very low categories. In the intervening years, the effects of the chytrid has included basal metabolic rates. These factors the situation has only worsened and promising studies of the skin microbial would seem to be highly detrimental the proportion of insuffi ciently known community to enhance the frog’s and one would expect natural selection species has increased. own immune system. In some areas, to have weeded out the extraordinarily While amphibians might appear Australia for example, there has been abundant and highly repetitive DNA to be vulnerable to environmental recovery from the initial outbreaks. At were it not for some compensating challenges because of their moist present, however, Bd constitutes the factor. The nature of that compensation, skins and life history traits, they are, major threat to large numbers of frog however, remains unknown and in fact, examples of resilience, having species and communities. constitutes a major research challenge survived previous mass extinction Returning to the Fire Salamander because for the species with the events and being successful in diverse of European legend, it is deeply largest genomes the costs are great from lowland rainforests to ironic that being the epitome of a (e.g., increased developmental time, deserts and extreme high elevations. survivor, even of fi re, they are suffering extended age at fi rst reproduction). Their resilience makes it all the more a steep decline in one of their last challenging to explain some of the redoubts in The Netherlands, a small Threats to amphibians current declines. forested area just north of Maastricht. The fi rst worldwide assessment The known causes for amphibian In this area, researchers recently of the status of amphibians by the declines are many and complex and discovered another new, highly International Union for Conservation of include such widely understood factors virulent, single-celled chytrid fungus,

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Batrachochytrium salamandrivorans twice as large. Salamanders are more Correspondence (Bsal). In addition to the chaos caused northern in distribution, with United by Bd, an even more deadly pathogen States having almost 200 species. Orangutan is now wreaking havoc. Fortunately, the While salamanders in the Old World new chytrid fungus is largely restricted barely enter the tropics, the lungless populations are to the immediate site of discovery, salamanders, Plethodontidae, have but in the time since discovery, it has undergone an adaptive radiation in the certainly not been found in nearby parts of Belgium New World tropics (over 40% of all increasing in the and Germany and the threat of spread salamanders), where they extend south to other species and areas is high. It of the 20th parallel in . Caecilians wild seems to be endemic and enzootic in occur only in tropical countries. species of the Family Salamandridae Perhaps the most surprising center Erik Meijaard1,2,9,*, Julie Sherman3, in eastern Asia and it is likely to have of caecilian diversity is the Seychelles Marc Ancrenaz1,4, Serge A. Wich5,6, been introduced to Europe through the islands (with eight species) in the Indian Truly Santika2, and Maria Voigt7,8 pet trade. In both Europe and North Ocean; India has the most caecilians America, new restrictions have brought (nearly 40 species). A recent report, published by the importation nearly to a halt. Whereas Amphibians are key components Government of Indonesia with support Bd can kill individual amphibians, of ecosystems throughout the world, from the Food and Agricultural some recover, and some immunity has and they may be the most abundant Organization and Norway’s International been detected, so far as is known, vertebrate in many local communities Climate and Forest Initiative, states outside its native range, Bsal is lethal. despite escaping notice by most people. that orangutan populations (Pongo Other infectious diseases also affect They are often the top predator of spp.) have increased by more than amphibians. While most are relatively invertebrates in ecosystems, and the 10% in Indonesia from 2015 to 2017, poorly known and not associated with most abundant vertebrates by biomass. exceeding the government target of an any mass mortality events, ranaviruses Frogs and salamanders are a critical annual 2% population increase [1]. This have been known for decades and food source for other vertebrates. assessment is in strong contrast with they can be a signifi cant factor in local They are richly represented in tropical recent publications that showed that populations. regions where they have radiated the Bornean orangutan (P. pygmaeus) especially along mountain slopes. Frogs lost more than 100,000 individuals in Amphibian diversity and distribution and salamanders are familiar animals, the past 16 years [2] and declined by Paradoxically, in this era of great concern enjoyed by the public, studied by many at least 25% over the past 10 years for amphibian survival, more and more scientists, and the focus of biomedical [3]. Furthermore, recent work has also new species are being discovered. and environmental research. Today demonstrated that both Sumatran Some of these are not new discoveries amphibians are in crisis, often victims orangutans (P. abelii) and the recently but rather subdivision of long-known of anthropogenic factors and novel described Tapanuli orangutan (P. species detected through the use of pathogens, but they are long-term tapanuliensis) lost more than 60% of molecular markers. The majority are survivors and many species continue their key habitats between 1985 and new discoveries. The numbers are to thrive. Frogs, salamanders and 2007, and ongoing land use changes impressive. As of August 2018, 7900 caecilians promise to be with us for the are expected to result in an 11–27% species of amphibians are known, long term. decline in their populations by 2020 about twice the species known in 1985. [4,5]. Most scientifi c data indicate Roughly three new species are being that the survival of these species described per week! Many of the new FURTHER READING continues to be seriously threatened by species refl ect the greatly increased deforestation and killing [4,6,7] and thus focus on the study of amphibians and Altig, R., and McDiarmid, R.W. (2015). Handbook of all three are Critically Endangered under Larval Amphibians of United States and Canada. the numbers of scientists being recruited. (Ithaca, NY: Cornell University Press). the International Union for Conservation Field biologists are probing ever deeper, Collins, J.P., and Crump, M.L. (2009). Extinction In of Nature’s Red List. Our Times: Global Amphibian Decline. (Oxford: into the last unexplored places on this Oxford University Press). We applaud the Indonesian planet. Areas that are particularly rich in Halliday, T. (2016). The Book of Frogs: A Life-size conservation authorities for providing new species include Madagascar, Papua Guide to Six Hundred Species from Around the publicly available documentation on World. (Lewes, UK: Ivy Press). New Guinea and several South American Sparreboom, M. (2014). Salamanders of the forest management impacts, and for countries. It is not just unexplored areas Old World. (Zeist, The Netherlands: KNNV their use of quantitative measures Publishing). that are producing new species; in 2017 Wells, K.D. (2007). The Ecology and Behavior of of wildlife conservation progress and 2018, new species were recorded Amphibians. (Chicago: University of Chicago [1]. Based on the above-mentioned from the United States and many new Press). discrepancy, however, we question http://amphibiaweb.org species were found in urban areas of http://research.amnh.org/vz/herpetology/amphibia/ whether appropriate methods and India and China. efforts were employed to assess South America is the richest area management impacts on wildlife trends. Museum of Vertebrate Zoology and for frogs, with having over 1000; Department of Integrative Biology, University For orangutan impact monitoring, the Ecuador has 586 frogs, which contrasts of California, Berkeley, CA 94720-3160, USA. Indonesian government reported on with 28 for , a country nearly *E-mail: [email protected] nine monitoring sites, including national

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