AMPHIBIANS, BIODIVERSITY OF

n w z Ross A. Alford , Stephenw J. Richards ,andKeithR.McDonald n James Cook University, South Australian Museum, and z Queensland Parks and Wildlife Service

I. The Evolutionary History of Amphibians tetrapods The terrestrial vertebrate classes amphib- II. Historical Biogeography and Current Diversity ians, reptiles, birds, and mammals, so named be- of Modern Amphibians cause they primitively possess four legs. III. Basic Morphology and Functional Anatomy of Modern Amphibians IV. Reproductive Biology and Life Histories of Modern Amphibians AMPHIBIANS ARE TETRAPOD VERTEBRATES. They V. Ecology and Functional Morphology of Larval differ from the other tetrapods (reptiles, birds, and Amphibians mammals) in that their eggs are anamniotic; they are VI. Behavior and Ecology of Postlarval Amphibians relatively simple and are enclosed in a jelly capsule. VII. Amphibian Conservation VIII. Conclusion: The Amphibian Success Story and Its Future I. THE EVOLUTIONARY HISTORY OF AMPHIBIANS

GLOSSARY Amphibians first appeared during the Late Devonian, about 360 million years ago (Ma). There is a general anamniotic Eggs are not surrounded by the complex consensus that all amphibians shared a common an- membranes that distinguish the amniotic eggs of cestor, a sarcopterygian (fleshy finned) bony fish of the reptiles, birds, and mammals. class Osteichthyes. All sarcopterygians have paired fins cloaca The common chamber in which the reprod- with limblike bones, and many exhibit other anatom- uctive, excretory, and digestive tracts of amphibians ical features, such as lungs, that ally them with the unite before exiting the body. tetrapods. It is not likely that either of the extant metapopulation A group of local populations among groups of sarcopterygians, the dipnoans (lungfishes) which individuals migrate relatively frequently; and crossopterygians (lobe-finned fishes), contained however, the rate of migration is slow enough that the ancestor of the amphibians. The earliest major the populations fluctuate independently. radiation of terrestrial vertebrates occurred during the pedomorphosis Reproduction while retaining at Carboniferous Period (ca. 335 Ma). By the end of the least some larval characteristics. Triassic, about 200 Ma, nearly all the large ancestral

Encyclopedia of Biodiversity Copyright & 2007 Elsevier Inc. All rights of reproduction in any form reserved. 1 2 ______AMPHIBIANS, BIODIVERSITY OF______amphibians were extinct. The subclass Lissamphibia, TABLE I the modern amphibians, appeared during the Triassic Richness of modern amphibian taxa and is the only group that has survived to the present. Taxon Families Genera Species The ancestry of modern amphibians is poorly un- derstood because there is a sparse fossil record linking Anura 33 354 5067 primitive amphibians to the three modern orders. The Caudata 10 59 508 Gymnophiona 5 33 168 earliest fossil Lissamphibian is Triadobatrachus massi- noti from the Early Triassic, about 230 Ma. Triado- Total 48 446 5743 is similar to the modern frogs but is not batrachus Based on Stuart et al. (2004) and Frost (2004). considered to belong to the order Anura. The Anura (frogs) and Gymnophiona (caecilians) appeared dur- ing the Early Jurassic (about 190 Ma), whereas the the Laurasian continents and many groups of frogs on Caudata (salamanders) appeared in the Middle Juras- the Gondwanan continents, several clades of frogs sic, 170–150 Ma. Although the fossil evidence is have dispersed to all continents and frogs are now sparse, phylogenetic analyses of shared derived absent only in Antarctica. morphological characters and of molecular characters There are now more described species of amphib- strongly suggest that the Lissamphibia share a com- ians than there are of mammals (Stuart et al., 2004; mon early amphibian ancestor and that the Lis- Table I). More than 500 salamander species are cur- samphibia and the amniote tetrapods (reptiles, birds, rently known in 10 families, with the highest diversity and mammals) originated from different early am- found in North America. One family, the Plethodonti- phibians. It is possible, however, that the Lissamphibia dae of North and South America, contains more than is a polyphyletic group, with one or more of the mod- half of the known salamander species. ern orders having an independent origin from the The frogs are placed in 25 families, and more than subclasses Temnospondylii or Microsauria. 5000 species are known, ~80% of which are in tropical regions. Recent estimates suggest that over a 1000 species remain to be described. The greatest diversity II. HISTORICAL BIOGEOGRAPHY AND of frogs occurs in South America, but other tropical areas such as Southeast Asia, New Guinea, Madagas- CURRENT DIVERSITY OF MODERN car, and Central Africa also have highly diverse frog AMPHIBIANS faunas. Four of the five most diverse frog families, the Modern amphibians are found in all continents except Hylidae, Ranidae, Bufonidae, and Microhylidae, are Antarctica. However, the three modern orders show each found across several continents—distributions disparate patterns of fossil and recent diversity that are that reflect successful dispersal. The most speciose associated with their different histories on the land- family is the Leptodactylidae, which is restricted to mass of Pangaea and subsequently on landmasses as- South and Central America and contains 22% of living sociated with Gondwana and Laurasia. The evolution frogs. It contains the genus Eleutherodactylus, which is of salamanders is linked closely with landmasses the most diverse vertebrate genus with more than 550 derived from Laurasia. All fossil and living species oc- species. cur in the Northern Hemisphere, with the exception of the lungless salamanders (family Plethodontidae), which invaded South America relatively recently. In III. BASIC MORPHOLOGY AND contrast, the caecilians and most frogs are associated predominantly with the southern Gondwanan land- FUNCTIONAL ANATOMY OF MODERN masses. The caecilians occur throughout the tropics, AMPHIBIANS except in Madagascar and to the east of Wallace’s Line in Australasia. They are the least diverse group of All modern amphibians have complex glandular skins living amphibians, with five families and 168 species. and all but caecilians lack scales. Their skins are kept The greatest diversity of species occurs in northern moist by the secretions of mucous glands, whereas South America and Central America. Frogs are the granular glands produce a variety of toxins that serve most widespread of the three orders. Although the to deter predation and also produce a variety of anti- breakup of Pangaea probably isolated salamanders on microbial peptides that deter microbial infections. ______AMPHIBIANS, BIODIVERSITY OF______3

They shed their skins periodically and usually accomplished by active or passive transport of water consume them as they are shed. Their color patterns across the skin. are produced by xanthophores, iridophores, and Amphibians are ectotherms, relying on the external melanophores. Many species are able to alter the environment as a source of body heat. All aquatic shape of pigment cells and the distribution of pigments forms and many terrestrial forms are also poikilo- within them and can rapidly change color. therms or thermoconformers, with body temperatures The eyes of most species contain photoreceptors of that do not differ from their environments. Some spe- several types, probably giving at least limited color cies control their body temperatures to some extent by vision, can be covered by moveable eyelids, and focus selecting microhabitats that provide appropriate tem- by moving the lens using ciliary muscles. Many frogs peratures, and some species of frogs periodically in- and salamanders have a wide binocular field of vision crease their body temperatures by basking in sunlight. and have good depth perception. Many species use The ability of most terrestrial amphibians to thermo- olfaction in the detection and capture of prey and have regulate by basking is limited by their need to conserve well-developed olfactory systems and Jacobson’s or- water while maintaining a moist skin. Some species of gans. Larval amphibians and the adults of many frogs and salamanders can be active at temperatures aquatic species have lateral line systems. Amphibians approaching 01C, whereas others can tolerate body have no external ears; their tympanum (when present) temperatures well above 401C. Some temperate species is at the surface of the body. The middle ears have a can survive exposure to temperatures o01C by su- columella bone (also found in reptiles and birds and percooling. A few species can survive partial freezing modified in mammals) that transmits vibrations from by a combination of ice nucleating proteins that enc- the tympanum to the inner ear. In anurans, there is a ourage freezing of extracellular fluids and high intra- second bony element in the middle ear, the oper- cellular glucose concentrations that prevent culum, which can be engaged by muscular contrac- intracellular water from freezing and keep cells from tions, and modifies hearing to increase the reception of dehydrating. low-frequency sounds. Most terrestrial amphibians respire (in part) with lungs and have largely separate pulmonary and sys- A. Special Features of Caecilians temic blood circulations. Their hearts typically have Caecilians are aquatic and burrowing animals that su- three chambers—two atria that receive blood from the perficially resemble large earthworms. Adults range body and the lungs and one ventricle that serves to from ~10 to 150 cm in length. They have elongated pump blood to the lungs and the body. Although the bodies with distinct annuli, which are grooves delinea- ventricle is usually single, a combination of partial ting their body segments. They are limbless, and their septa and the high viscosity of blood reduce mixing of tails are reduced or absent. Their eyes are reduced and the blood streams flowing to the lungs and the re- are covered by skin. They are unique among the Liss- mainder of the body. Many species carry out a con- amphibia in possessing dermal scales, which occur in siderable fraction of gas exchange across the moist the annuli of some species. Their skulls are heavily skin; for the lungless salamanders (family Plethodon- ossified and completely roofed. Caecilians possess a tidae) this is the primary mode of respiration. unique chemosensory organ, the tentacle, which ex- The kidneys of amphibians function in maintaining tends a short distance from the surface of the head, water and ionic balance. In species with aquatic larval emerging from a skull opening between the eyes and stages, most water and ion balance needs are reversed the nostrils. at metamorphosis; the freshwater larvae must cope with a hypo-osmotic environment, to which they lose ions and from which they gain water, whereas the B. Special Features of Salamanders terrestrial stages must cope with rates of evaporative water loss that are typically high because of their Salamanders are typically four-limbed animals with moist skins. Aquatic individuals tend to excrete dilute relatively long tails. They superficially resemble lizards solutions of ammonia, whereas terrestrial animals but lack epidermal scales and claws. Salamanders excrete more concentrated solutions of urea, although range from ~30 mm to 2 m in total length. Their limbs no amphibian excretes fluid urine that is more con- are relatively small and are reduced or lost in some centrated than the blood plasma. Water uptake in terrestrial and aquatic species. Their skulls typically most amphibians does not involve drinking but is show the loss of many bony elements. Salamanders 4 ______AMPHIBIANS, BIODIVERSITY OF______lack external ears and, with the exception of weak Frogs have a variety of adaptations to structures distress calls in some species, do not vocalize. The other than the skin for maintaining water balance. most diverse group of salamanders, the Plethodontidae Most species store copious quantities of dilute urine in of the Americas, is lungless. Salamanders of many the bladder when water is available and withdraw groups exhibit various degrees of pedomorphosis, water from this pool to replace evaporative losses. which in some species is facultative, allowing them to Desert species and species that inhabit brackish water exploit high-quality aquatic environments while re- can allow high concentrations of urea to accumulate in taining the option of a terrestrial stage. Salamander the body fluids. A few species can excrete nitrogenous larvae are carnivorous and usually have well-devel- wastes as uric acid, which minimizes the water lost oped external gills. when they are excreted.

C. Special Features of Anurans IV. REPRODUCTIVE BIOLOGY AND LIFE Anurans are invariably four-limbed, and terrestrial HISTORIES OF MODERN AMPHIBIANS juveniles and adults completely lack true tails. Adults range from about 1 to 30 cm in length. Their The ‘‘typical’’ life history of the Lissamphibia includes a hindlimbs and feet are greatly elongated. The radius complex life cycle in which eggs are deposited in fresh- and ulna of the forelimb and the tibia and fibula of the water habitats, where larvae grow and develop, eventu- hindlimb are usually fused. There are not more than ally metamorphosing into terrestrial juveniles and nine trunk vertebrae, and most modern frogs lack free leaving the water. Although this is a common pattern ribs. The caudal vertebrae are fused into a rod-shaped found in all three modern orders, it is far from univer- urostyle that is associated with the elongated pelvis. sal. One of the major feature that sets amphibians apart Most of these features are probably the result of ad- from the remainder of terrestrial vertebrates is their aptation for light weight and strength for jumping and extremely wide range of life histories and modes of re- show interesting convergences with similar adapta- production, many of which occur in all three extant tions in birds. The lightweight skulls of frogs are large orders (Duellman and Trueb, 1986). The presence of a relatively to their body size and lack many bones. All wide range of life histories and reproductive modes but one species lack teeth on the dentary bone of the suggests that the ‘‘typical’’ amphibian life cycle does not lower jaw. The tongue is attached at the front of the reflect a failure to adapt to the terrestrial environment mouth in most species and is flipped forward rapidly but rather serves as an adaptation that allows female to capture the prey. The ears of frogs often have ex- amphibians to produce very large numbers of eggs with ternal tympanic membranes. a small investment in each and to exploit freshwater The skins of frogs depart from the usual amphibian habitats for larval growth and development. pattern in several ways. Some species have additional types of glands: lipid glands which secrete lipids that A. Caecilians reduce rates of evaporative water loss or breeding glands that produce sticky secretions, which adhere Limited observations have been made on the reprod- the male to the female during amplexus. Skin lipids uctive biology of caecilians and very little information and other as yet poorly understood modifications of on their courtship behavior is available. It appears that the skin allow some tree frogs to achieve rates of fertilization is internal via protrusion of the male evaporative water loss as low as those of some lizards. cloacal wall. Although vocalizations have been re- Frogs also have distinct differences between their dor- ported for some species, it is not known if they are sal and ventral skins. The ventral skin usually has linked to reproduction. fewer granular and mucous glands, and many terres- Caecilians are oviparous or viviparous. In vivipa- trial species have an area called the pelvic patch in rous species, gestation may take up to a year with which thin and highly vascularized skin can be ex- reproduction occurring every 2 years only, and nutri- posed. Water uptake from substrates via the pelvic tion can be supplied to the young within the oviduct. patch is the primary means by which almost all species Oviparous species lay terrestrial eggs but the larvae of frogs obtain water. Burrowing desert frogs of several can be aquatic or can complete development within lineages form cocoons by repeatedly shedding their the egg. Oviparous caecilians produce more offspring skins and retaining the shed layers to reduce evapo- than viviparous species. In oviparous species, parental rative water loss while they are buried. care of eggs is common. ______AMPHIBIANS, BIODIVERSITY OF______5

B. Salamanders mostly by terrestrial breeders and may serve to protect the eggs from predation, fungus infection, and dessic- Many salamanders conform to the ‘‘typical’’ amphibian cation. Adults attend clutches for up to 9 months. In a complex life cycle. Most produce aquatic eggs and few species, communal clutches are attended by larvae, which metamorphose into terrestrial juveniles. aggregations of females, and eggs are fertilized by As in the frogs, there is a great deal of variation beyond many different males. this basic mode. Larval salamanders are relatively sim- ilar to adults; this has allowed species belonging to several groups to evolve the ability to reproduce while C. Anurans retaining larval characters, either facultatively or obligately. The most common reproductive strategy in frogs An example of the complexity and variability of involves a complex life cycle with externally fertilized salamander life histories is the life history of red-spot- aquatic eggs, which produce highly specialized lar- ted newts (Notophthalmus viridescens, family Sal- vae—tadpoles. The tadpoles grow and develop for amandridae). Their life history begins with aquatic some period in the water and then undergo a radical eggs that hatch into aquatic larvae. The larvae typically metamorphosis and emerge as terrestrial juvenile develop within one summer and metamorphose into a frogs. However, frogs have evolved a remarkable morphologically distinct terrestrial juvenile stage, the variety of reproductive strategies, most involving a eft. The eft stage lasts from 1 to 8 years, depending on trend toward removal of eggs and larvae from the temperature and food availability. Efts undergo a sec- aquatic environment. Pough et al. (1998) described 29 ond transformation into adults, which then return an- combinations of egg-deposition sites, including still nually to water to breed. Larvae that encounter very water and fast-flowing water, terrestrial nests, and on favorable conditions and grow rapidly can retain some or in the body of the male or the female, and they also larval morphological characteristics, remain perma- described tadpole development, ranging from the typ- nently aquatic, and reproduce as pedomorphic adults. ical free-swimming feeding larva to direct develop- Larvae that encounter slightly less-favorable condi- ment inside the oviduct. Because amphibian eggs lack tions can bypass the eft stage and metamorphose di- a water-resistant shell, the greatest diversity of reprod- rectly into the adult morphology. uctive modes occurs in the humid tropics where eggs Courtship in salamanders can be quite elaborate, can survive for long periods in the permanently moist incorporating chemical, visual, and tactile cues. terrestrial environment. Complex behaviors including During the breeding season, males of aquatic species egg guarding and embryo transport (on the dorsum, in can develop enlarged fins and become more brightly specialized pockets or pouches, in the mouth, and in colored. There may be other morphological changes to Rheobatrachus species in the stomach), and unusual the head glands, tooth structure, musculature, and morphological structures such as skin pockets to skin during the breeding season. Many salamanders provide protection for developing embryos, are asso- have specialized glands that secrete compounds used ciated with many reproductive modes. Many separate as olfactory signals during courtship. lineages of anurans have evolved direct development, Salamanders have internal or external fertilization. bypassing the aquatic larval stage. Most direct External fertilization involves deposition of the sperm developers have some form of parental care of the on the egg mass. Salamanders with internal fertiliza- eggs. Several species bear live young, and at least one tion either transfer sperm directly from male to female of these, Nectophrynoides occidentalis, actually provides or exhibit a unique form of sperm transfer in which a oviductal nutrition to its developing embryos. bundle of sperm (the spermatophore) is deposited by In tropical regions where conditions for reproduc- males. The spermatophore is picked up in the female tion are favorable throughout the year, breeding can be cloaca and stored in a special structure in the cloaca, aseasonal, and females may lay multiple clutches in the spermatheca. The stored sperm can remain viable 1 year. In more temperate or high-altitude regions, until ovulation, which may occur from a few days to breeding is typically strongly seasonal, occurring only 2.5 years later. In live-bearing salamanders the sperm during short periods of the year when temperature and enters the oviduct, in which the eggs are internally rainfall reach critical levels. Under these conditions fertilized. females generally lay only one clutch of eggs each year. Both male and female salamanders of some species Male frogs vocalize mainly to attract mates (Fig. 1b) exhibit parental care (Fig. 1a), although it is practiced and to advertise their presence and sometimes their 6 ______AMPHIBIANS, BIODIVERSITY OF______

FIGURE 1 (a) A black-bellied salamander Desmognathus quadromaculatus guards its eggs (removed from (and replaced in) a small stream, Appalachian Mountains). (b) A male Australian desert tree frog, Litoria rubella, produces an ear-splitting call with the aid of its balloon-like vocal sac. (c) Spike-nosed frogs, Litoria prora, from New Guinea, in amplexus. The function of the rostral (nose) spine is unknown. (d) A suctorial tadpole of the Australian treefrog Litoria nyakalensis. The upper and lower jaw sheaths, surrounded by keratinized ‘‘teeth’’ and oral papillae set in an oral disc, are clearly visible. These tadpoles use their large ventral oral discs as suckers to attach to rocks in fast-flowing rain forest streams. See also color Plate 9 (this volume). All photographs taken and copyright by Stephen J. Richards. status to other males. Calls are species-specific and location. Females of many species use these charac- females typically respond only to males of their own teristics to choose their mates from among competing species. Males of most species possess a single or dou- males. Males vocalize from species-specific locations ble vocal sac which serves as a resonator and in at least which can be in water, on or beneath the ground, in some species as a sound radiator. Vocal sacs also cons- vegetation from near ground level to high in trees, and erve energy by allowing passive reinflation of the lungs even under water (several species including African as the vocal sac contracts after a call. Some male frogs, clawed frogs, Xenopus). such as the Australian torrent frog (Litoria nannotis), Female frogs do not have a vocal sac and very few lack a vocal sac but can still produce a surprisingly vocalize. Some female frogs produce a scream when loud call. Environmental conditions such as temper- distressed, and reproductively active females of some ature affect vocalizations. At colder temperatures notes species call in response to male advertisement calls. and pulses are produced at slower rates, but the length Females of a few species call in other contexts, such as of the call increases. The dominant frequencies in the territoriality and during mating. calls of most frogs are lower than 5000 Hz, although The posture of frogs during the fertilization of eggs those of some small species are higher. Within species, is called amplexus; in most species this involves the variation in the dominant frequencies, pulse rates, and male grasping the female from above (Fig. 1c). The durations of calls often reflects male body size; there- exact posture adopted depends on the morphology fore, the call may indicate male quality as well as male and relative size of the male and female. The two most ______AMPHIBIANS, BIODIVERSITY OF______7 common positions involve the male grasping the fe- carnivore, but when conditions are favorable some male in front of the back legs (inguinal amplexus) or individuals develop relatively larger heads and more the front legs (axillary amplexus). Amplexus is aided powerful jaws, adopting a ‘‘cannibal’’ morphology that in many species by specialized patches of skin called allows them to prey on small vertebrates, including nuptial pads on the forelimbs of males. Pairs remain in their siblings. amplexus while the male sheds sperm onto the eggs as As in larval frogs, there is considerable variation they are released by the female. Fertilization in nearly among and within species in rates of larval growth and all frogs is external but several species accomplish in- development. Both the minimum and the maximum ternal fertilization by cloacal apposition. The frog As- development rates for salamanders are slower than caphus truei, commonly called the tailed frog, breeds in those for frogs. Salamanders can take from 6 weeks to fast-flowing streams of the northwest of North Amer- 5 years to complete larval development. Within spe- ica and carries out internal fertilization using the ‘‘tail,’’ cies, rates respond to both temperature and food which is actually an intromittent organ formed from availability, and salamanders have the additional op- an extension of the male’s cloaca. tion, apparently not available to frogs, of changing the relative rates of development of somatic and reprod- uctive structures so that they mature sexually without V. ECOLOGY AND FUNCTIONAL losing all larval characters. MORPHOLOGY OF LARVAL AMPHIBIANS A. Caecilians C. Anurans The tadpole larvae of frogs are highly specialized for Relatively little is known about the larvae of caecilians. growth and development in the aquatic environment They are more similar to adults than are those of frogs (McDiarmid and Altig, 1999). They have an oval or salamanders. Externally, they closely resemble head–body region and a long tail, which is laterally adults but have gill slits and fins. Free-living caecil- compressed and includes a central area of musculature ian larvae have long external gills and a lateral line and dorsal and ventral fins of thin, lightly vascularized system. Their mouth and dentition resemble those of tissue. The tail is supported only by a notochord. De- adults. They lack the tentacle organ that appears on spite their very different body form, they swim and the head of adults; this appears at metamorphosis. turn as rapidly and efficiently as fishes of similar body sizes. They feed using an elaborate pumping mecha- B. Salamanders nism that is very different from the oral and branchial morphology of adults. This mechanism transports Salamander larvae are much more similar to adults water though the mouth and pharyngeal cavity, where than are the tadpoles of frogs. Larval salamanders have food particles are removed by branchial filters and external gills that are not completely covered by an entrapment in strands of mucus. Some tadpoles can operculum. Some embryonic salamanders have paired remove particles as small as 0.126 mm from the water. lateral projections from the head called balancers; in Water is ejected through the nostrils of most species some species, these persist for a short period following and through the spiracle, which is usually a single, hatching. Most species possess well-developed tubular structure leading out of the opercular chamber fore- and hindlimbs through most of the larval period. that can be located midventrally or on the left side of Their bodies are laterally compressed compared with the body. The unique mouthparts of tadpoles typically those of adults, and their tails are also relatively thinner include an oral disc with transverse rows of keratini- and deeper. Their skins contain lateral line organs zed ‘‘teeth’’ that are used to scrape particles into sus- (neuromasts) and are thinner and less glandular than pension. Keratinized sheaths on the jaws provide those of adults. Their dentition is different from adults, cutting and biting surfaces. The oral apparatus is var- and their tongues are rudimentary. Their eyes lack lids. iously modified and sometimes allows attachment to Almost all larval salamanders are carnivorous, usually the substrate via suction (Fig. 1d). The relatively long, feeding on zooplankton and larval insects. The larvae coiled intestine fills most of the body cavity. Tadpoles of larger species can also feed on small vertebrates. The are typically thought of as microphagous herbivores larvae of some species have alternative morphologies; that feed on algae and small parts of higher plants, but the typical morphology is usually a planktivorous most species will feed on animal material when it is 8 ______AMPHIBIANS, BIODIVERSITY OF______available. Tadpoles often scavenge on dead animals in serve its new function of conserving water and excre- the water and frequently prey on amphibian eggs. ting urea. The gonads differentiate at about the time of They typically feed at high rates, retain food in their metamorphosis. guts for relatively short periods, and extract only a Rates of growth and development of tadpoles are small fraction of the energy from ingested food. This typically highly variable within species, responding to makes them an important source of the fine particulate environmental temperature, food availability, and the organic matter that many aquatic invertebrates depend density of tadpoles of their own and other species. upon for food. Many species that inhabit unpredictable environments, Tadpoles often hatch with external gills, which are such as temporary ponds, can have larval periods from quickly covered over by a fold of epithelium, forming 2 weeks or less up to months. Some species regularly the opercular chamber. Before the opercular chamber spend 1 year or more (maximum 3 years) as larvae. forms, many species do not swim but attach to a The interaction between rates of growth and substrate using adhesive organs located posterior to development in tadpoles has produced a rich litera- the mouth. Tadpoles lack limbs at hatching. The rear ture that examines how and why this interaction is legs usually develop slowly, starting as limb buds at the controlled. In general, it appears that rates of growth posterior end of the body and developing over a long control rates of development during the earlier part of period. The forelimbs develop within the opercular the free-living tadpole stage (Wilbur and Collins, chamber and are visible only after they erupt fully 1973). Larvae that are growing slowly develop more formed through the opercular wall at the onset of slowly than fast growers, and changes in growth rate metamorphosis. caused by changes in environmental conditions are A typical pattern of tadpole growth and develop- mirrored by alterations in developmental rate. Fast- ment would include one to a few days as a nonswim- growing tadpoles tend to metamorphose both earlier ming hatchling with exposed gills followed by several and at larger sizes than slower-growing individuals. weeks to months as a swimming and feeding larva. Very slow growers appear to regulate their develop- During this period, the tadpole grows dramatically; mental rate so that they metamorphose near a many species increase their body mass by hundreds of species-specific minimum size after a larval period that times and some by thousands. During this period, the may vary greatly in length. This flexibility in relative hindlimbs begin to grow and slowly develop through rates of growth and development is lost late in the the remainder of larval life. larval period at a point that may vary among taxa. Metamorphosis begins with the eruption of the Theory suggests that the regulation of these rates forelimbs and involves drastic changes to all elements ultimately responds to natural selection acting in a of the structure and function of the body. Reorgan- way that depends on the relative rates of growth and ization of the mouth and digestive tract allows a survival in aquatic and terrestrial environments. These switch from larval filter feeding to adult carnivory. The ideas have been applied to life-history transitions in tail fins and musculature are broken down and re- many nonamphibian taxa, including fishes, insects, absorbed. Most elements of the chondrocranium are and plants. reshaped and realigned, and the branchial apparatus Because frogs typically deposit large numbers of ceases to be a support for gills and takes on a role as eggs during relatively short breeding seasons, densities support for the adult tongue. The external and middle of tadpoles are often high. The success or failure of a ears form, and in all but a few aquatic species the cohort of tadpoles in a typical temporary freshwater lateral line system disappears. The eye changes in size habitat depends on a highly complex and unpredict- and structure, the photopigments of the rods change able set of factors, including the density of tadpoles of from porphyropsin to rhodopsin, and eyelids appear. their own species and other species, which control the The axial skeleton is reorganized and many elements degree of intraspecific and interspecific competition are ossified. The lungs, which begin to develop and for food and space, the number and species of pred- function during the larval period of many species, ators present, and the duration of the aquatic phase of enlarge and take on their role as a major respiratory the habitat. Competition and predation are both con- structure. The complexity of the skin increases, with trolled by the choice of time and place of breeding by the epidermis increasing from two layers of cells to five adult frogs and to some extent by microhabitat selec- or six, many with specialized functions. The kidney, tion within habitats by tadpoles. The outcomes of which in tadpoles is relatively simple and excretes ex- species interactions involving tadpoles can be altered cess water and ammonia, becomes more complex to by changes in the timing of breeding, and microhabitat ______AMPHIBIANS, BIODIVERSITY OF______9 selection by tadpoles can depend on the species and salamanders usually feed by extending their large, sizes of other tadpoles present. fleshy tongues, which adhere to prey and pull it into Tadpoles are preyed on by a wide variety of ver- their mouths. The tongue of salamanders is attached at tebrate and invertebrate predators, for whom they the base and is protruded and elongated by muscles constitute a valuable resource. Major predators in- and fluid tension. The degree of attachment of the clude fishes, salamanders and salamander larvae, and tongue and the length to which it is protruded vary the aquatic larvae of insects such as dragonflies, dam- among taxa. Captured prey are ingested whole. Ter- selflies, and beetles. Vulnerability of tadpoles to pred- restrial anurans also capture prey by protruding their ators typically decreases as the tadpoles grow and tongues. These are usually attached near the front of develop, and many tadpoles exhibit short-term beha- the lower jaw and are protruded by literally flipping vioral responses to predators, such as decreasing their them forward and downward. Prey that adhere to the levels of activity or switching from midwater feeding tongue are drawn into the mouth and swallowed to substrate feeding, that appear to decrease their whole. vulnerability. Most of these responses also decrease the Amphibians generally appear to grow throughout tadpoles’ rates of growth and development, leading to their lives, but rates of growth decline drastically after trade-offs that have been explored by behavioral reproductive maturity is attained. In captivity, many ecologists. species can live for decades, and even in nature some species live for extended periods. In general, amphib- ian life spans appear to be limited more by environ- mental hazards than by aging and senescence. VI. BEHAVIOR AND ECOLOGY OF Many species of frogs and salamanders occupy re- POSTLARVAL AMPHIBIANS latively small home ranges during the nonbreeding sea- son and migrate to breeding habitats for reproduction. The ecological breadths of the three classes of modern The nonbreeding home range is aggressively defended amphibians are reflected in their geographical distri- by some species. Some species return to their natal butions (Savage, 1973). The caecilians are restricted ponds to breed, whereas others may simply migrate to a by both thermal and water requirements to relatively suitable body of water. In temperate regions, some spe- low latitudes and elevations, and they do not occur cies may also regularly migrate to overwintering sites. where mean annual temperatures are t121C or total Amphibians use celestial navigation, light polarization, annual precipitation is t1000–2000 mm. The sala- and the Earth’s magnetic field as means of orientation manders have less-restrictive ecological requirements during migrations. There is considerable movement and are distributed across a broader range of habitats, among local populations in many species, particularly occurring from low to high latitudes and elevations. by anurans. Some of this movement is dispersal by Their major limitation is clearly moisture; they do not juveniles, but some is due to longer range movements occur in areas that have prolonged dry seasons and by terrestrial adults. At least one species of frog, Bufo only rarely in areas with total rainfalls o1000 mm per marinus, can move great distances over relatively short annum. The anurans as a group can tolerate wide periods. The range of the introduced Australian pop- ranges of both temperature and water availability, and ulations of this species has expanded by ~30 km/yr for they occur at all but the highest latitudes and elevat- an extended period, and the animals that arrive first in ions and in all but the driest deserts. new habitat are adults. Detailed studies of the local Almost all adult amphibians are relatively non- movements of adult B. marinus suggest that they are selective carnivores that ingest invertebrate and ver- nomadic. Many mark-recapture studies of frogs have tebrate prey small enough to be swallowed whole. found high rates of disappearance of marked frogs and Amphibians are either sit-and-wait predators or of the appearance of unmarked animals, suggesting that active foragers, but do not engage in cursorial pursuit adults of many species may at least occasionally dis- of prey. Sit-and-wait predators locate their prey pri- perse to new areas. marily using vision, whereas active foragers often use The relatively high rates of migration between local olfaction. populations found in many amphibian species suggest Salamanders use a variety of methods for prey cap- that groups of local populations often form meta- ture. Many larvae, and adults of aquatic taxa, are suc- populations. It is important to recognize this because tion feeders, using rapid depression of the floor of the the dynamics of metapopulations are governed by dif- mouth and throat to pull in water and prey. Terrestrial ferent factors than those of local populations, and the 10 ______AMPHIBIANS, BIODIVERSITY OF______conservation of metapopulations requires a different exceptionally toxic skin compounds and one species, approach than the conservation of local populations. Phyllobates terribilis, contains sufficient toxin in a Because amphibians typically produce relatively single frog to kill several adult humans. This toxin is large numbers of relatively small eggs, their popula- smeared on darts used by the Choco Indians of west- tions can increase rapidly in size when reproduction is ern Colombia for hunting monkeys and other large successful. It is likely that populations of most am- game. There are connections between frog diets and phibians normally fluctuate fairly widely over time the presence of skin toxins; some dendrobatid frogs (Alford and Richards, 1999). It may be common for with high toxin levels in the wild gradually lose their local populations of many species to fluctuate to ex- toxicity when held in captivity. Although indigenous tinction, followed by relatively rapid recolonization by cultures have recognized the toxic and medicinal immigrants from adjacent local populations belonging properties of frog skin for centuries, their potential for to the same metapopulation. It is likely that for many development as medicines using scientific methods species the persistence of most local populations has has only recently emerged as a significant field of re- little bearing on whether the regional metapopulation search, which has already yielded many compounds will persist. However, there may be a few critical local that may be of great use in combating a variety of populations that either serve as reliable sources of illnesses, including the HIV virus. colonists or serve as stepping stones for migration be- tween more widely distributed local populations. Identifying these local populations and conserving B. Amphibians as Components of Ecosystems them, and ensuring that migration among local pop- Amphibians form a vital link in many food chains. ulations remains possible, will be crucial for ensuring They consititute the highest vertebrate biomass in the long-term persistence of many species. some ecosystems and occupy an intermediate position in the food chain. Aquatic larval amphibians are herbivorous to omnivorous (Anura) or carnivorous VII. AMPHIBIAN CONSERVATION (Caudata and Apoda) and are significant prey items for a wide variety of vertebrate and invertebrate predators. A. Human Uses of Amphibians Tadpoles in lakes and ponds often reach extremely high densities and can have a significant impact on Amphibians have featured prominently in many hu- nutrient cycling within these aquatic habitats. Because man cultures through stories, songs, and poetry. In anuran larvae feed on algae and other aquatic material, urban areas, they are frequently found coexisting suc- they play an important role in the transfer of plant cessfully with humans in parks and garden ponds. By energy to predators of tadpoles, and facilitate the consuming large numbers of insects, they are impor- breakdown of plant biomass into plant nutrients. tant in controlling agricultural pests and reducing dis- Adult amphibians feed on a wide variety of live food. ease transmission. Frogs are an important source of Most are generalists that consume any living creature protein in some subsistence cultures. In affluent coun- smaller than their gape size. However, some have spe- tries, frogs are imported for consumption in gourmet cialized to feed exclusively on narrow ranges of food restaurants. Hundreds of millions of frogs have been items, such as worms, ants, and even snails. Predators exported from Southeast Asia and the Indian subcon- of amphibian eggs, tadpoles, and adults include other tinent, resulting in increased insect pest populations. amphibians, spiders, insects, mammals, birds, and Frogs have also become model organisms in ecologi- reptiles (especially snakes). Because of their important cal, embryological, physiological, and genetic re- role in ecosystems, population declines or extinctions search. of amphibians may have significant impacts beyond Amphibian skin contains a wide variety of chem- the amphibian species affected. icals, including complex amines, alkaloids, and poly- peptides, some of which have pharmacological properties. Many skin secretions are effective against C. Amphibian Diversity and Levels of Threat amphibian bacterial and fungal infections. Secretions of the South American frog Epipedobates tricolor con- There are almost 6000 recognized amphibian species tains a constituent, epibatidine, that blocks pain 200 (Table I), and new species are being discovered every times more effectively than morphine. Poison dart year. It has been estimated that the eventual number of frogs of the family Dendrobatidae harbor many species will be between 8000 and 10,000. Amphibians ______AMPHIBIANS, BIODIVERSITY OF______11 occupy all continents except Antarctica, and they are Many causes have been postulated for amphibian found in habitats ranging from arid deserts and saline declines, including habitat loss and modification, pre- mangrove swamps to tropical rain forests and moun- dation, environmental toxicity, disease, immuno- tain peaks more than 4000 m high. More than 80% of suppression, ultraviolet radiation, changes in climate or amphibians are found in the tropics, with an estimated weather patterns, and combinations of these. It is likely 44% of the world’s amphibians in the tropical Amer- thatmanyofthesehavecausedsomeofthedeclines icas. Many tropical regions, including New Guinea, that have occurred (Alford and Richards, 1999). The South-East Asia, and parts of northern South America, GAA identified three major likely causes of declines in have been inadequately surveyed, and there is no the 435 species whose conservation status had wors- doubt that many previously unknown species will be ened since 1980. Overexploitation by humans ap- discovered in these areas. peared to be affecting 12% of these species, habitat loss The conservation status of amphibians has deteri- 42%, and ‘‘enigmatic decline,’’ which was defined as orated rapidly in recent years. The 1996 International declines occurring where there is suitable habitat, was Union for the Conservation of Nature (IUCN) Red identified for the remaining 46%. Many of the enigma- Data Book listed five amphibian species as extinct and tic declines have involved rapid crashes of populations 124 as threatened, which represented 25% of the spe- in relatively pristine habitats, such as montane rain cies for which assessment of conservation status had forests. Lips et al. (2006) monitored a species-rich been undertaken at that time. Concern over the status community in Panama before and during such a crash, of amphibians led the IUCN to conduct the Global and determined that it was caused by an outbreak of Amphibian Assessment (GAA; Stuart et al., 2004), chytridiomycosis, caused by the amphibian chytrid which enlisted the aid of scientists throughout the skin fungus, Batrachochytrium dendrobatidis.Thisre- world in determining the status of amphibians in their cently discovered disease appears likely to be the country or region. The results of this are frightening. proximate cause of many ‘‘enigmatic’’ amphibian In 2004, 1856 species, 32% of all known amphibians, declines. It infects the outer layer of amphibian skin were listed as threatened by the IUCN, with 427 listed via motile zoospores, which can be transmitted as critically endangered. Thirty-four species were through contact or shared water. The host–pathogen identified as being extinct, with nine having become ecology of this disease is complex; its prevalence extinct since 1980, and 122 as being possibly extinct, and virulence are strongly affected by environmental with 113 possible extinctions since 1980. In all, the temperature and humidity, and the timing of outbreaks GAA estimated that the conservation satus of 435 spe- of chytridiomycosis is probably affected by weather, cies had become worse since 1980. All of these are and perhaps by changes in weather patterns related probably underestimates; although the GAA used the to global climate change. It is a very unusual disease knowledge of over 500 amphibian specialists, insuffi- in that it infects a very wide range of host species cient information was available on 1294 species and can drive many of them to extinction, probably (22.5%) to determine their conservation status, and because it also has alternative hosts or persists in many of the thousands of undescribed species that the environment. It is likely that the pathogen has probably exist may also be under threat. recently increased its geographic range, and it may even have spread globally from a single place of origin, possibly aided by human activities such as the D. The Problem of Amphibian Population extensive trade in amphibians for food, medical and Declines scientific purposes, and as pets. In case this hypothesis is correct, it would be prudent to conduct surveys to All amphibian populations fluctuate, and assessing the determine the present range of the pathogen, and significance of downward trends in amphibian popu- institute quarantine measures to reduce its possible lations has been difficult. However, well-documented spread. declines and disappearances of amphibian species and A major hindrance to our understanding of am- entire suites of species occurred over wide areas in the phibian population declines is a general lack of 1980s and 1990s. These widespread losses of species information about amphibian autecology and host– and populations in a relatively short time frame, in- pathogen interactions, about how amphibian popula- cluding dramatic extinctions of previously abundant tions normally fluctuate, and about the extent to species in protected areas such as national parks, are which they operate as metapopulations (Heyer et al., evidence that declines are real. 1994). In the short term, a great deal of research aimed 12 ______AMPHIBIANS, BIODIVERSITY OF______at increasing our knowledge in these areas and testing many amphibians may be an early manifestation of a hypotheses about population declines will be vital for general crisis in biodiversity, and unless they are halted identifying causal factors and determining how to it seems likely that future generations will be denied a eliminate or mitigate them. full appreciation of the remarkable extent of amphib- ian diversity. It also seems likely, though, that as long as terrestrial habitats continue to accommodate ver- VIII. CONCLUSION: THE AMPHIBIAN tebrate life, amphibians will persist. SUCCESS STORY AND ITS FUTURE

Contrary to popular opinion, modern amphibians are See Also the Following Articles not a relictual remnant of the ancestors of other tetra- BIRDS, BIODIVERSITY OF FISH, BIODIVERSITY OF pods but are a highly successful group in their own MAMMALS, BIODIVERSITY OF REPTILES, BIODIVERSITY OF right. There are more species of amphibians than there are of mammals. Modern amphibians occur in nearly all of the Earth’s terrestrial habitats, from within the Bibliography Arctic Circle to tropical deserts. Groups of modern amphibians that need to conserve water have evolved Alford, R. A., and Richards, S. J. (1999). Global amphibian declines: A problem in applied ecology. 30, 133–165. impermeable skins, cocoons, and the ability to excrete Annu. Rev. Ecol. Syst. Duellman, W. E., and Trueb, L. (1986). Biology of Amphibians. Johns uric acid. Groups that need to breed outside water Hopkins University Press, Baltimore. have evolved a startling array of reproductive adapta- Frost, D. R. (2004). Amphibian species of the world: An online tions; amphibians have the widest range of reprod- reference. Version 3.0 (22 August). Electronic Database acces- uctive modes of any tetrapods. These include aquatic sible at http://research.amnh.org/herpetology/amphibia/index. html (accessed July 2006). American Museum of Natural eggs and larvae, many species with terrestrial eggs, and History, New York, USA. truly viviparous species in which the mother provides Heyer, W. R., Donnelly, M. A., McDiarmid, R. W., Hayek, L. C., and nutrition in addition to the yolk during development. Foster, M. S. (1994). Measuring and Monitoring Biological Diver- This diversity indicates that the typical reproductive sity: Standard Methods for Amphibians. Smithsonian Institution pattern, with aquatic eggs and larvae, must not rep- Press, Washington, DC. Lips, K. R., Brem, F., Brenes, R., et al. (2006). Emerging infectious resent a constraint that has limited their success. It disease and the loss of biodiversity in a neotropical amphibian probably represents a successful adaptation that allows community. Proc. Natl. Acad. Sci. USA 103, 3165–3170. the exploitation of aquatic habitats by terrestrial spe- McDiarmid, R. W., and Altig, R. (1999). Tadpoles: The Biology of cies and allows a much higher fecundity than is avail- Anuran Larvae. University of Chicago Press, Chicago. able to species that must provision their eggs with Pough, F.H., Andrews, R. M., Cadle, J. E., Crump, M. L., Savitzky, A. H., and Wells, K. D. (1998). Herpetology. Prentice-Hall, Engle- enough yolk for complete development. wood Cliffs, NJ. The ability to respond to environmental challenges Savage, J. M. (1973). The geographic distribution of frogs patterns has allowed the modern amphibians to persist and and predictions. In Evolutionary Biology of the Anurans Contem- flourish during and through periods of dominance of porary Research on Major Problems (J. L. Vial, Ed.), pp. 315–445. terrestrial habitats by other tetrapod groups. They University of Missouri Press, Columbia. Stuart, S. N., Chanson, J. S., Cox, N. A., et al. (2004). Status and have outlived the early dominant amphibians, several trends of amphibian declines and extinctions worldwide. Science waves of dominance by reptiles including the dino- 306, 1783–1786. saurs, and many radiations and extinctions of mam- Wilbur, H. M., and Collins, J. P. (1973). Ecological aspects of mals. The current declines and disappearances of amphibian metamorphosis. Science 182, 1305–1314.