AMPHIBIANS, BIODIVERSITY OF Ross A. Alford,* Stephen J. Richards,† and Keith R. McDonald† *James Cook University; † Queensland Parks and Wildlife Service

I. The Evolutionary History of Amphibians II. Historical Biogeography and Current Diversity of Modern Amphibians III. Basic Morphology and Functional Anatomy of Modern Amphibians IV. Reproductive Biology and Life Histories of Modern Amphibians V. Ecology and Functional Morphology of Larval Amphibians VI. Behavior and Ecology of Postlarval Amphibians VII. Amphibian Conservation VIII. Conclusion: The Amphibian Success Story and Its Future

GLOSSARY anamniotic Eggs are not surrounded by the complex membranes that distinguish the amniotic eggs of reptiles, birds, and mammals. cloaca The common chamber in which the reproductive, excretory, and digestive tracts of amphibians unite before exiting the body. metapopulation A group of local populations among which individuals migrate relatively frequently; however, the rate of migration is slow enough that the populations fluctuate independently. paedomorphosis Reproduction while retaining at least some larval characteristics. tetrapods The terrestrial vertebrate classes amphibi-

ans, reptiles, birds, and mammals, so named because they primitively possess four legs.

AMPHIBIANS ARE TETRAPOD VERTEBRATES. They differ from the other tetrapods (the reptiles, birds, and mammals) in that their eggs are anamniotic; they are relatively simple and are enclosed in a jelly capsule.

I. THE EVOLUTIONARY HISTORY OF AMPHIBIANS Amphibians first appeared during the Late Devonian, about 360 million years ago (Ma). There is a general consensus that all amphibians shared a common ancestor, a sarcopterygian (fleshy-finned) bony fish in the class Osteichthyes. All sarcopterygians have paired fins with limb-like bones, and many exhibit other anatomical features, such as lungs, that ally them with the tetrapods. It is not likely that either of the extant groups of sarcopterygians, the dipnoans (lungfishes) and crossopterygians (lobe-finned fishes), contained the ancestor of the amphibians. The earliest major radiation of terrestrial vertebrates occurred during the Carboniferous Period (ca. 335 Ma). By the end of the Triassic, about 200 Ma, nearly all of the large ancestral amphibians were extinct. The subclass Lissamphibia, the modern amphibians, appeared during the Triassic and is the only group that has survived to the present.

Encyclopedia of Biodiversity, Volume 1 Copyright  2001 by Academic Press. All rights of reproduction in any form reserved.

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The ancestry of modern amphibians is poorly understood because there is a sparse fossil record linking primitive amphibians to the three modern orders. The earliest fossil Lissamphibian is Triadobatrachus massinoti from the early Triassic, about 230 Ma. Triadobatrachus is similar to the modern frogs but is not considered to belong to the order Anura. The Anura (frogs) and Gymnophiona (caecilians) appeared during the Early Jurassic (about 190 Ma), whereas the Caudata (salamanders) appeared in the Middle Jurassic, 170– 150 Ma. Although the fossil evidence is sparse, phylogenetic analyses of shared derived morphological characters and of molecular characters strongly suggest that the Lissamphibia share a common early amphibian ancestor and that the Lissamphibia and the amniote tetrapods (reptiles, birds, and mammals) originated from different early amphibians. It is possible, however, that the Lissamphibia is a polyphyletic group, with one or more of the modern orders having an independent origin from the subclasses Temnospondylii or Microsauria.

II. HISTORICAL BIOGEOGRAPHY AND CURRENT DIVERSITY OF MODERN AMPHIBIANS Modern amphibians are found in all continents except Antarctica. However, the three modern orders show disparate patterns of fossil and recent diversity that are associated with their different histories on the landmass of Pangaea and subsequently on landmasses associated with Gondwana and Laurasia. The evolution of salamanders is linked closely with landmasses derived from Laurasia. All fossil and living species occur in the Northern Hemisphere, with the exception of the lungless salamanders (family Plethodontidae) which invaded South America relatively recently. In contrast, the caecilians and most frogs are associated predominantly with the southern Gondwanan landmasses. The caecilians occur throughout the tropics, except in Madagascar and to the east of Wallace’s Line in Australasia. They are the least diverse group of living amphibians, with five families and 165 species. The greatest diversity of species occurs in northern South America and central America. Frogs are the most widespread of the three orders. Although the breakup of Pangaea probably isolated salamanders on the Laurasian continents and many groups of frogs on the Gondwanan continents, several clades of frogs have dispersed to all continents and frogs are now absent only from Antarctica. There are now more described species of amphibians than there are of mammals (Glaw and Kohler, 1998;

TABLE I Richness of Modern Amphibian Taxa* Taxon

Families

Genera

Species

Anura Caudata

25 10

334 61

4204 411

Gymnophiona Total

6 41

33 428

165 4780

* Based on Duellman 1993, Glaw and Kohler 1998.

Table I). More than 400 salamander species are currently known in 10 families, with the highest diversity found in North America. One family, the Plethodontidae of North and South America, contains more than half the known salamander species. The frogs are placed in 25 families, and more than 4200 species are known, 80% of which are in tropical regions. It is likely that at least several hundred species remain to be described. The greatest diversity of frogs occurs in South America, but other tropical areas such as Southeast Asia, New Guinea, Madagascar, and central Africa also have highly diverse frog faunas. Four of the five most diverse frog families, the Hylidae, Ranidae, Bufonidae, and Microhylidae, are each found across several continents—distributions that reflect successful dispersal. The most diverse family is the Leptodactylidae, which is restricted to South and Central America and contains 22% of living frogs. It contains the genus Eleutherodactylus, which is the most diverse vertebrate genus with more than 550 species.

III. BASIC MORPHOLOGY AND FUNCTIONAL ANATOMY OF MODERN AMPHIBIANS All modern amphibians have complex glandular skins and most lack scales. Their skins are kept moist by the secretions of mucous glands, whereas granular glands produce a variety of toxins that serve to deter predation and may also help to protect from microbial infections. They shed their skins periodically and usually consume them as they are shed. Their color patterns are produced by xanthophores, iridophores, and melanophores. Many species are able to alter the shape of pigment cells and the distribution of pigments within them and can rapidly change color. The eyes of most species contain photoreceptors of several types, probably giving at least limited color vision, they can be covered by moveable eyelids, and they

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focus by moving the lens using ciliary muscles. Many frogs and salamanders have a wide binocular field of vision and have good depth perception. Many species use olfaction in the detection and capture of prey and have well-developed olfactory systems and Jacobson’s organs. Larval amphibians and adults of aquatic species have lateral line systems. The amphibian auditory apparatus differs from those of other terrestrial vertebrates. Their middle ears have a columella bone (also found in reptiles and birds and modified in mammals) which functions in the reception of high-frequency sounds. A second bony element in the middle ear, the operculum, receives low-frequency vibrations from the air and substrate via a muscular connection to the pectoral girdle. Most terrestrial amphibians respire (in part) with lungs and have largely separate pulmonary and systemic blood circulations. Their hearts typically have three chambers—two atria that receive blood from the body and the lungs and one ventricle that serves to pump blood to the lungs and the body. Although the ventricle is usually single, a combination of partial septa and the high viscosity of blood reduce mixing of the blood streams flowing to the lungs and the remainder of the body. Many species carry out a considerable fraction of gas exchange across the moist skin; for the lungless salamanders (family Plethodontidae) this is the primary mode of respiration. The kidneys of amphibians function in maintaining water and ionic balance. In species with aquatic larval stages, most water and ion balance needs are reversed 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 terrestrial stages must cope with rates of evaporative water loss that are typically high because of their moist skins. Aquatic individuals tend to excrete dilute solutions of ammonia, whereas terrestrial animals excrete more concentrated solutions of urea, although no amphibian excretes fluid urine that is more concentrated than the blood plasma. Water uptake in almost all amphibians does not involve drinking but is accomplished by active or passive transport of water across the skin. Amphibians are ectotherms, relying on the external environment as a source of body heat. All aquatic forms and many terrestrial forms are also poikilotherms or thermoconformers, with body temperatures that do not differ from their environments. Some species may control their body temperatures to some extent by selecting microhabitats that provide appropriate temperatures, and a few species of frogs periodically increase their body temperatures by basking in sunlight. The ability of most terrestrial amphibians to thermoregulate by basking is limited by their need to conserve water while

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maintaining a moist skin. Some species of frogs and salamanders can be active at temperatures approaching 0⬚C, whereas others can tolerate body temperatures well above 40⬚C. Some temperate species can survive exposure to temperatures below 0⬚C by supercooling. A few species can survive partial freezing by a combination of ice nucleating proteins that encourage freezing of extracellular fluids and high intracellular glucose concentrations that prevent intracellular water from freezing and keep cells from dehydrating.

A. Special Features of Caecilians Caecilians are aquatic and burrowing animals that superficially resemble large earthworms. Adults range from approximately 10 to 150 cm in length. They have elongate bodies with distinct annuli, which are grooves delineating their body segments. They are limbless, and their tails are reduced or absent. Their eyes are reduced and are covered by skin. They are unique among the Lissamphibia in possessing dermal scales, which occur in the annuli of some species. Their skulls are heavily ossified and completely roofed. Caecilians possess a unique chemosensory organ, the tentacle, which extends a short distance from the surface of the head, emerging from a skull opening between the eyes and the nostrils.

B. Special Features of Salamanders Salamanders are typically four-limbed animals with relatively long tails that superficially resemble lizards but lack epidermal scales and claws. Salamanders range from about 30 mm to 2 m in total length. Their limbs are relatively small and are reduced or lost in some terrestrial and aquatic species. Their skulls typically show the loss of many bony elements. Salamanders lack external ears and, with the exception of weak distress calls in some species, do not vocalize. The most diverse group of salamanders, the Plethodontidae of the Americas, is lungless. Salamanders of many groups exhibit various degrees of paedomorphosis. Salamander larvae are carnivorous and usually have well-developed external gills.

C. Special Features of Anurans Anurans are invariably four-limbed, and terrestrial juveniles and adults completely lack true tails. Adults range from about 1 to 30 cm in length. Their hindlimbs and feet are greatly elongated. The radius and ulna of the forelimb and the tibia and fibula of the hindlimb are fused. There are no more than nine trunk

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vertebrae, and most modern frogs lack free ribs. The caudal vertebrae are fused into a rod-shaped urostyle that is associated with the elongate pelvis. Most of these features are probably the result of adaptation for light weight and strength for jumping and show interesting convergences with similar adaptations in birds. The lightweight skulls of frogs are large relative to their body size and lack many bones. All but one species lack teeth on the dentary bone of the lower jaw. The tongue is attached at the front of the mouth in most species and is flipped forward rapidly to capture prey. The ears of frogs follow the general amphibian model, with the addition of an external tympanic membrane in many species. The skins of frogs depart from the usual amphibian pattern in several ways. Some species have additional types of glands: lipid glands that secrete lipids which reduce rates of evaporative water loss or breeding glands that produce sticky secretions which adhere the male to the female during amplexus. Skin lipids and other as yet poorly understood modifications of the skin allow some treefrogs to achieve rates of evaporative water loss as low as those of some lizards. Frogs also have distinct differences between their dorsal and ventral skins. The ventral skin usually has fewer mucous glands, and many terrestrial species have an area called the pelvic patch in which the skin is unusually thin and highly vascularized. Frogs sit with the pelvic patch in contact with moist substrates to increase the rate of water uptake. Burrowing desert frogs of several lineages form cocoons by repeatedly shedding their skins and retaining the shed layers to reduce evaporative water loss while they are buried. Frogs have a variety of adaptations to structures other than the skin for maintaining water balance. Most species store copious quantities of dilute urine in the bladder when water is available and withdraw water from this pool to replace evaporative losses. Desert species and species that inhabit brackish water can allow high concentrations of urea to accumulate in the body fluids. A few species can excrete nitrogenous wastes as uric acid, which minimizes the water lost when they are excreted.

IV. REPRODUCTIVE BIOLOGY AND LIFE HISTORIES OF MODERN AMPHIBIANS The ‘‘typical’’ life history of the Lissamphibia includes a complex life cycle in which eggs are deposited in freshwater habitats, where larvae grow and develop,

eventually metamorphosing into terrestrial juveniles and leaving the water. Although this is a common pattern found in all three modern orders, it is far from universal. One of the major features that sets amphibians apart from the remainder of terrestrial vertebrates is their extremely wide range of life histories and modes of reproduction, many of which occur in all three extant orders. The presence of a wide range of life histories and reproductive modes suggests that the ‘‘typical’’ amphibian life cycle does not reflect a failure to adapt to the terrestrial environment but rather serves as an adaptation that allows female amphibians to produce very large numbers of eggs with a small investment in each and to exploit freshwater habitats for larval growth and development.

A. Caecilians Limited observations have been made on the reproductive biology of caecilians and no information on courtship behavior is available. It appears that fertilization is internal via protrusion of the male cloacal wall. Although vocalizations have been reported for some species, it is not known if they are linked to reproduction. Caecilians are oviparous or viviparous. In viviparous species gestation may take up to a year with reproduction occurring only every 2 years, and nutrition can be supplied to the young within the oviduct. Oviparous species lay terrestrial eggs but the larvae can be aquatic or can complete development within the egg. Oviparous caecilians produce more offspring than viviparous species. In oviparous species, parental care of eggs is common.

B. Salamanders Many salamanders conform to the ‘‘typical’’ amphibian complex life cycle. Most produce aquatic eggs and larvae, which metamorphose into terrestrial juveniles. As in the frogs, there is a great deal of variation beyond this basic mode. Larval salamanders are relatively similar to adults; this has allowed species belonging to several groups to evolve the ability to reproduce while retaining larval characters, either facultatively or obligately. An example of the complexity and variability of salamander life histories is the life history of red-spotted newts (Notophthalmus viridescens, family Salamandridae). Their life history begins with aquatic eggs which hatch into aquatic larvae. The larvae typically develop within one summer and metamorphose into a morphologically distinct terrestrial juvenile stage, the eft. The eft stage lasts from 1 to 8 years, depending on temperature and food availability. Efts undergo a second trans-

AMPHIBIANS, BIODIVERSITY OF

formation into adults, which then return annually to water to breed. Larvae that encounter very favorable conditions and grow rapidly can retain some larval morphological characteristics, remain permanently aquatic, and reproduce as paedomorphic adults. Larvae that encounter slightly less favorable conditions can bypass the eft stage and metamorphose directly into the adult morphology. Courtship in salamanders can be quite elaborate, incorporating chemical, visual, and tactile cues. During the breeding season males of aquatic species can develop enlarged fins and become more brightly colored. There may be other morphological changes to the head glands, tooth structure, musculature, and skin during the breeding season. Many salamanders have specialized glands that secrete compounds used as olfactory signals during courtship. Salamanders have internal or external fertilization.

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External fertilization involves deposition of the sperm on the egg mass. Salamanders with internal fertilization either transfer sperm directly from male to female or exhibit a unique form of sperm transfer in which a bundle of sperm (the spermatophore) is deposited by males. The spermatophore is picked up in the female cloaca and stored in a special structure in the cloaca, the spermatheca. The stored sperm can remain viable until ovulation, which may occur from a few days to 2.5 years later. In live-bearing salamanders the sperm enters the oviduct, in which the eggs are internally fertilized. Both male and female salamanders of some species exhibit parental care (Fig. 1A), although it is practiced mostly by terrestrial breeders and may serve to protect the eggs from predation, fungus infection, and desiccation. Adults attend clutches for up to 9 months. In a few species communal clutches are attended by aggrega-

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 treefrog, 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 (all photographs taken by and copyright by Stephen J. Richards). See also color insert, this volume.

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AMPHIBIANS, BIODIVERSITY OF

tions of females, and eggs are fertilized by many different males.

C. Anurans The most common reproductive strategy in frogs involves a complex life cycle with externally fertilized aquatic eggs which produce highly specialized larvae— tadpoles. The tadpoles grow and develop for some period in the water and then undergo a radical metamorphosis and emerge as terrestrial juvenile frogs. However, frogs have evolved a remarkable variety of reproductive strategies, most involving a trend toward removal of eggs and larvae from the aquatic environment. Pough et al. (1998) described 29 combinations of egg deposition sites, including still water and fastflowing water, terrestrial nests, and on or in the body of the male or the female, and they also described tadpole development, ranging from the typical free-swimming feeding larva to direct development inside the oviduct. Because amphibian eggs lack a water-resistant shell, the greatest diversity of reproductive modes occurs in the humid tropics where eggs can survive for long periods in the permanently moist terrestrial environment. Complex behaviors including egg guarding and embryo transport (on the dorsum, in the mouth, and in Rheobatrachus species in the stomach), and unusual morphological structures such as skin pockets to provide protection for developing embryos, are associated with many reproductive modes. Several species bear live young, and at least one of these, Nectophrynoides occidentalis, actually provides oviductal nutrition to its developing embryos. In tropical regions where conditions for reproduction are favorable throughout the year, breeding can be aseasonal, and females may lay multiple clutches in one year. In more temperate or high-altitude regions breeding is typically strongly seasonal, occurring only during short periods of the year when temperature and rainfall reach critical levels. Under these conditions females generally lay only one clutch of eggs each year. Male frogs vocalize mainly to attract mates (Fig. 1B) and to advertise their presence and sometimes their status to other males. Calls are species-specific and each female’s brain is tuned to respond only to males of her own species. In most frogs, males possess a single or double vocal sac which serves as a resonator and in at least some species as a sound radiator. Vocal sacs also conserve energy by allowing passive reinflation of the lungs as the vocal sac contracts after a call. Some male frogs, such as the Australian torrent frog (Litoria nannotis), lack a vocal sac but can still produce a surpris-

ingly loud call. Environmental conditions such as temperature affect vocalizations. At colder temperatures notes and pulses are produced at slower rates, but the length of the call increases. The dominant frequencies in the calls of most frogs are lower than 5000 Hz, although those of some small species are higher. Within species, variation in the dominant frequencies, pulse rates, and durations of calls often reflects male body size; therefore, the call may indicate male quality as well as male location. Females of many species use these characteristics to choose their mates from among competing males. Males vocalize from species-specific locations which can be in water, on or beneath the ground, in vegetation from near ground level to high in trees, and even under water (several species including African clawed frogs, Xenopus). Female frogs do not have a vocal sac and very few vocalize. Some female frogs produce a scream when distressed, and reproductively active females of some species call softly in response to male advertisement calls. The posture of frogs during the fertilization of eggs is called amplexus; in most species this involves the male grasping the female from above (Fig. 1C). The exact posture adopted depends on the morphology and relative size of the male and female. The two most common positions involve the male grasping the female in front of the back legs (inguinal amplexus) or the front legs (axillary amplexus). Amplexus is aided in many species by specialized patches of skin called nuptial pads on the forelimbs of males. Pairs remain in amplexus while the male sheds sperm onto the eggs as they are released by the female. Fertilization in nearly all frogs is external but several species accomplish internal fertilization by cloacal apposition. The frog Ascaphus truei, commonly called the tailed frog, breeds in fastflowing streams of the Northwest of North America and carries out internal fertilization using the ‘‘tail,’’ which is actually an intromittent organ formed from an extension of the male’s cloaca.

V. ECOLOGY AND FUNCTIONAL MORPHOLOGY OF LARVAL AMPHIBIANS A. Caecilians Relatively little is known about the larvae of caecilians. They are more similar to adults than are those of frogs or salamanders. Externally they closely resemble adults

AMPHIBIANS, BIODIVERSITY OF

but have gill slits and fins. Free-living caecilian larvae have long external gills and a lateral line system. Their mouth and dentition resemble those of adults. They lack the tentacle organ that appears on the head of adults; this appears at metamorphosis.

B. Salamanders Salamander larvae are much more similar to adults than are the tadpoles of frogs. Larval salamanders have external gills that are not completely covered by an operculum. Some embryonic salamanders have paired lateral projections from the head called balancers; in some species these persist for a short period following hatching. Most species possess well-developed fore- and hindlimbs through most of the larval period. Their bodies are laterally compressed compared to those of adults, and their tails are also relatively thinner and deeper. Their skins contain lateral line organs (neuromasts) and are thinner and less glandular than those of adults. Their dentition is different from adults, and their tongues are rudimentary. Their eyes lack lids. Larval salamanders are almost all carnivorous, usually feeding on zooplankton and larval insects. The larvae of larger species can also feed on small vertebrates. The larvae of some species have alternative morphologies; the typical morphology is usually a planktivorous carnivore, but when conditions are favorable some individuals develop relatively larger heads and more powerful jaws, adopting a ‘‘cannibal’’ morphology that allows them to prey on small vertebrates, including their siblings. As in larval frogs, there is considerable variation among and within species in rates of larval growth and development. Both the minimum and the maximum rates for salamanders are slower than those for frogs. Salamanders can take from 6 weeks to 5 years to complete larval development. Within species, rates respond to both temperature and food availability, and salamanders have the additional option, apparently not available to frogs, of changing the relative rates of development of somatic and reproductive structures so that they mature sexually without losing all larval characters.

C. Anurans The tadpole larvae of frogs are highly specialized for growth and development in the aquatic environment. They have an oval head–body region and a long tail, which is laterally compressed and includes a central area of musculature and dorsal and ventral fins of thin, lightly vascularized tissue. The tail is supported only

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by a notochord. Despite their very different body form, they swim and turn as rapidly and efficiently as fishes of similar body sizes. They feed using an elaborate pumping mechanism that is very different from the oral and branchial morphology of adults. This mechanism transports water though the mouth and pharyngeal cavity, where food particles are removed by branchial filters and entrapment in strands of mucus. Some tadpoles can remove particles as small as 0.126 애m from the water. Water is ejected through the nostrils of most species and through the spiracle, which is usually a single, tubular structure leading out of the opercular chamber and can be located midventrally or on the left side of the body. The unique mouthparts of tadpoles typically include an oral disc with transverse rows of keratinized ‘‘teeth’’ that are used to scrape particles into suspension. Keratinized sheaths on the jaws provide cutting and biting surfaces. The oral apparatus is variously modified and sometimes allows attachment to the substrate via suction (Fig. 1D). The relatively long, coiled intestine fills most of the body cavity. Tadpoles are typically thought of as microphagous herbivores that feed on algae and small parts of higher plants, but most species will feed on animal material when it is available. Tadpoles often scavenge on dead animals in the water and frequently prey on amphibian eggs. Tadpoles often hatch with external gills, which are quickly covered over by a fold of epithelium, forming the opercular chamber. Before the opercular chamber forms, many species do not swim but attach to a substrate using adhesive organs located posterior to the mouth. Tadpoles lack limbs at hatching. The rear legs usually develop slowly, starting as limb buds at the posterior end of the body and developing over a long period. The forelimbs develop within the opercular chamber and are visible only after they erupt fully formed through the opercular wall at the onset of metamorphosis. A typical pattern of tadpole growth and development would include 1 to a few days as a nonswimming hatchling with exposed gills followed by several weeks to months as a swimming and feeding larva. During this period, the tadpole grows dramatically; many species increase their body mass by hundreds of times and some by thousands. During this period, the hind-limbs begin to grow and slowly develop through the remainder of larval life. Metamorphosis begins with the eruption of the forelimbs and involves drastic changes to all elements of the structure and function of the body. Reorganization of the mouth and digestive tract allows a switch from

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larval filter feeding to adult carnivory. The tail fins and musculature are broken down and reabsorbed. Most elements of the chondrocranium are reshaped and realigned, and the branchial apparatus ceases to be a support for gills and takes on a role as support for the adult tongue. The external and middle ears form, and in all but the aquatic frogs of the family Pipidae the lateral line system disappears. The eye changes in size and structure, the photopigments of the rods change from porphyropsin to rhodopsin, and eyelids appear. The axial skeleton is reorganized and many elements are ossified. The lungs, which develop and begin to function during the larval period of many species, enlarge and take on their role as a major respiratory structure. The complexity of the skin increases, with the epidermis increasing from two layers of cells to five or six, many with specialized functions. The kidney, which in tadpoles is relatively simple and excretes excess water and ammonia, becomes more complex to serve its new function of conserving water and excreting urea. The gonads differentiate at about the time of metamorphosis. Rates of growth and development of tadpoles are typically highly variable within species, responding to environmental temperature, food availability, and the density of tadpoles of their own and other species. Many species that inhabit unpredictable environments, such as temporary ponds, can have larval periods from 2 weeks or less up to months. Some species regularly spend 1 year or more (maximum 3 years) as larvae. The interaction between rates of growth and development in tadpoles has produced a rich literature that examines how and why this interaction is controlled. In general, it appears that rates of growth control rates of development during the earlier part of the free-living tadpole stage (Wilbur and Collins, 1973). Larvae that are growing slowly develop more slowly than fast growers, and changes in growth rate caused by changes in environmental conditions are mirrored by alterations in developmental rate. Fast-growing tadpoles tend to metamorphose both earlier and at larger sizes than slower growing individuals. Very slow growers appear to regulate their developmental rate so that they metamorphose near a species-specific minimum size after a larval period that may vary greatly in length. This flexibility in relative rates of growth and development is lost late in the larval period at a point that may vary among taxa. Theory suggests that the regulation of these rates ultimately responds to natural selection acting in a way that depends on the relative rates of growth and survival in aquatic and terrestrial environments. These ideas

have been applied to life-history transitions in many nonamphibian taxa, including fishes, insects, and plants. Because frogs typically deposit large numbers of eggs during relatively short breeding seasons, densities of tadpoles are often high. The success or failure of a cohort of tadpoles in a typical temporary freshwater habitat depends on a highly complex and unpredictable set of factors, including the density of tadpoles of their own species and other species, which control the degree of intraspecific and interspecific competition for food and space; the number and species of predators present; and the duration of the aquatic phase of the habitat. Competition and predation are both controlled by the choice of time and place of breeding by adult frogs and to some extent by microhabitat selection within habitats by tadpoles. The outcomes of species interactions involving tadpoles can be altered by changes in the timing of breeding, and microhabitat selection by tadpoles can depend on the species and sizes of other tadpoles present. Tadpoles are preyed on by a wide variety of vertebrate and invertebrate predators, for whom they constitute a valuable resource. Major predators include fishes, salamanders and salamander larvae, and the aquatic larvae of insects such as dragonflies, damselflies, and beetles. Vulnerability of tadpoles to predators typically decreases as the tadpoles grow and develop, and many tadpoles exhibit short-term behavioral responses to predators, such as decreasing their levels of activity or switching from midwater feeding to substrate feeding, that appear to decrease their vulnerability. Most of these responses also decrease the tadpoles’ rates of growth and development, leading to trade-offs that have been explored by behavioral ecologists.

VI. BEHAVIOR AND ECOLOGY OF POSTLARVAL AMPHIBIANS The ecological breadth of the three classes of modern amphibians is reflected in their geographical distributions (Savage, 1973). The caecilians are restricted by both thermal and water requirements to relatively low latitudes and elevations, and they do not occur where mean annual temperatures are less than about 12⬚C or total annual precipitation is less than about 1000–2000 mm. The salamanders have less restrictive ecological requirements and are distributed across a broader range of habitats, occurring from low to high latitudes and

AMPHIBIANS, BIODIVERSITY OF

elevations. Their major limitation is clearly moisture; they do not occur in areas that have prolonged dry seasons and only rarely in areas with total rainfalls less than 1000 mm per annum. The anurans as a group can tolerate wide ranges of both temperature and water availability, and they occur at all but the highest latitudes and elevations and in all but the driest deserts. Almost all adult amphibians are carnivores that ingest invertebrate and vertebrate prey small enough to be swallowed whole. Amphibians are mostly either sitand-wait predators or active foragers, but none engage in cursorial pursuit of prey. Sit-and-wait predators locate their prey primarily using vision, whereas active foragers often use olfaction. Salamanders use a variety of methods for prey capture. Many larvae, and adults of aquatic taxa, are suction feeders, using rapid depression of the floor of the throat to pull in water and prey. Terrestrial salamanders usually feed by extending their large, fleshy tongues, which adhere to prey and pull it into their mouths. The tongue of salamanders is attached at the base and is protruded and elongated by muscles and fluid tension. The degree of attachment of the tongue and the length to which it is protruded vary among taxa. Captured prey are ingested whole. Terrestrial anurans also capture prey by protruding their tongues. These are usually attached near the front of the lower jaw and are protruded by literally flipping them forward and downward. Prey that adhere to the tongue are drawn into the mouth and swallowed whole. Amphibians generally appear to grow throughout their lives, but rates of growth decline drastically after reproductive maturity is attained. In captivity, many species can live for decades, and even in nature some species live for extended periods. In general, amphibian life spans appear to be limited more by environmental hazards than by aging and senescence. Many species of frogs and salamanders occupy relatively small home ranges during the nonbreeding season and migrate to breeding habitats for reproduction. The nonbreeding home range is aggressively defended by some species. Some species return to their natal ponds to breed, whereas others may simply migrate to a suitable body of water. In temperate regions, some species may also regularly migrate to overwintering sites. Amphibians use celestial navigation, light polarization, and the earth’s magnetic field as means of orientation during migrations. There is considerable movement among local populations in many species, particularly by anurans. Some of this movement is dispersal by juveniles, but some is due to longer range movements by terres-

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trial adults. At least one species of frog, Bufo marinus, can move great distances over relatively short periods. The range of the introduced Australian populations of this species has expanded by approximately 30 km per year for an extended period, and the animals that arrive first in new habitat are adults. Detailed studies of the local movements of adult B. marinus suggest that they are nomadic. Many mark-recapture studies of frogs have found high rates of disappearance of marked frogs and of the appearance of unmarked animals, suggesting that adults of many species may at least occasionally disperse to new areas. The relatively high rates of migration between local populations found in many amphibian species suggest that groups of local populations often form metapopulations. It is important to recognize this because the dynamics of metapopulations are governed by different factors than those of local populations, and the conservation of metapopulations requires a different approach than the conservation of local populations. Because amphibians typically produce relatively large numbers of relatively small eggs, their populations can increase rapidly in size when reproduction is successful. It is likely that populations of most amphibians normally fluctuate fairly widely over time (Alford and Richards, 1999). These normal fluctuations may include fluctuations of local populations to extinction, followed by relatively rapid recolonization by immigrants from adjacent local populations belonging to the same metapopulation. It is likely that for many species the persistence of most local populations has little bearing on whether the regional metapopulation will persist. However, there may be a few critical local populations that either serve as reliable sources of colonists or serve as stepping stones for migration between more widely distributed local populations. Identifying these local populations and conserving them will be crucial for ensuring the long-term persistence of many species.

VII. AMPHIBIAN CONSERVATION A. Human Uses of Amphibians Amphibians have featured prominently in many human cultures through stories, song, and poetry. In urban areas they are frequently found coexisting successfully with humans in parks and garden ponds. Frogs are an important source of protein in some subsistence cultures. In affluent countries, frogs are imported for consumption in gourmet restaurants. Hundreds of mil-

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lions of frogs have been exported from Southeast Asia and the Indian sub-continent, resulting in increasing insect pest populations. Frogs have also become model organisms in ecological, embryological, physiological, and genetic research. Amphibian skin contains a wide variety of chemicals, including complex amines, alkaloids, and polypeptides, some of which have pharmacological properties. Some skin toxins are effective against amphibian bacterial and fungal infections, and the skin of the South American frog Epipedobates tricolor contains a constituent, epibatidine, that blocks pain 200 times more effectively than morphine. Poison dart frogs of the family Dendrobatidae harbor many exceptionally toxic skin compounds and one species, Phyllobates terribilis, contains sufficient toxin in a single frog to kill several adult humans. This toxin is smeared on darts used by the Choco Indians of western Colombia for hunting monkeys and other large game. There are connections between frog diets and the presence of skin toxins; some dendrobatid frogs with high toxin levels in the wild gradually lose their toxicity when held in captivity. Although indigenous cultures have recognized the toxic and medicinal properties of frog skin for centuries, their potential for development as medicines using scientific methods has only recently emerged as a significant field of research.

B. Amphibians as Components of Ecosystems Amphibians form a vital link in many food chains. They represent the highest vertebrate biomass in some ecosystems and occupy an intermediate position in the food chain. Aquatic larval amphibians are herbivorous to omnivorous (Anura) or carnivorous (Caudata and Apoda) and are significant prey items for a wide variety of vertebrate and invertebrate predators. Tadpoles in lakes and ponds often reach extremely high densities and can have a significant impact on nutrient cycling within these aquatic habitats. Because anuran larvae feed on algae and other aquatic material, they play an important role in the transfer of plant energy to predators of tadpoles. Adult amphibians feed on a wide variety of live food. Most are generalists that consume any living creature smaller than their gape size. However, some have specialized to feed exclusively on narrow ranges of food items, such as worms, ants, and even snails. Predators of amphibian eggs, tadpoles, and adults include other amphibians, spiders, insects, mammals, birds, and reptiles (especially snakes). Because of their important role in ecosystems, population declines or

extinctions of amphibians may have significant impacts beyond the amphibian species affected.

C. Amphibian Diversity and Levels of Threat There are approximately 5000 amphibian species (Table I), and new species are being discovered every year. Amphibians occupy all continents except Antarctica, and they are found in habitats ranging from arid deserts and saline mangrove swamps to tropical rain forests and mountain peaks more than 4000 m high. More than 80% of amphibians are found in the tropics, with an estimated 44% of the world’s amphibians in the tropical Americas. Many tropical regions, including New Guinea, South-east Asia, and parts of northern South America, have been inadequately surveyed, and there is no doubt that many previously unknown species will be discovered in these areas. The 1996 International Union for the Conservation of Nature (IUCN) Red Data Book lists 5 amphibian species as extinct and 124 as threatened, which represents 25% of the species for which assessment of conservation status has been undertaken. However, this information is influenced to some degree by the research and assessment focus in affluent countries and may change substantially when comparable research is undertaken in other geographic regions. There is little doubt that extensive habitat loss in tropical regions is causing the extinction of poorly known and undiscovered species.

D. The Problem of Amphibian Population Declines Well-documented declines and disappearances of amphibian species and entire suites of species occurred over wide areas in the 1980s and 1990s. All amphibian populations fluctuate, and assessing the significance of downward trends in amphibian populations has been difficult. However, the widespread loss of species and populations in a relatively short time frame, including dramatic extinctions of previously abundant species in protected areas such as national parks, is evidence that declines are real. Many causes have been postulated for amphibian declines, including habitat loss and modification, predation, environmental toxicity, disease, immunosuppression, ultraviolet radiation, changes in climate or weather patterns, and combinations of these. No single cause

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has been identified and declines need to be assessed case by case. In some areas populations of a suite of species have declined while other ecologically similar species have not been affected. Populations of some species have declined at high altitudes but remained unaffected at low altitudes. Elucidating the causes of these declines remains a difficult and complex problem. Determining the causes of declines can be difficult. In areas of extensive urbanization, such as Europe and North America, declines or extinction of amphibian populations or species through habitat loss have clearly occurred. However, understanding rapid population declines in relatively pristine montane rain forests is a more challenging problem. A major hindrance to our understanding of population declines is the lack of information about amphibian autecology; how populations behave, and the extent to which they operate as metapopulations. Experimental ecology aimed at testing hypotheses about population declines will be vital for identifying causal factors. The role of diseases in amphibians is poorly understood, and many diseases have only recently been documented. Although monitoring of populations over time is essential to understand population behavior, it will not identify the causes of amphibian population declines. The amphibian decline problem is currently the focus of much research effort, as reviewed by Alford and Richards (1999).

VIII. CONCLUSION: THE AMPHIBIAN SUCCESS STORY AND ITS FUTURE Contrary to popular opinion, modern amphibians are not a relictual remnant of the ancestors of other tetrapods but are a highly successful group in their own right. There are more species of amphibians than there are of mammals. Modern amphibians occur in nearly all of Earth’s terrestrial habitats, from within the Arctic Circle to tropical deserts. Groups of modern amphibians that need to conserve water have evolved impermeable skins, cocoons, and the ability to excrete uric acid. Groups that need to breed outside water have evolved a startling array of reproductive adaptations; amphibians have the widest range of reproductive modes of any tetrapods. These include aquatic eggs and larvae, many species with terrestrial eggs, and truly viviparous species in which the mother provides nutrition in addition to the yolk during development. This diversity indicates that the typical reproductive pattern, with aquatic eggs and larvae, must not represent a constraint that has

limited their success. It probably represents a successful adaptation that allows the exploitation of aquatic habitats by terrestrial species and allows a much higher fecundity than is available to species that must provision their eggs with enough yolk for complete development. The ability to respond to environmental challenges has allowed the modern amphibians to persist and flourish during and through periods of dominance of terrestrial habitats by other tetrapod groups. They have outlived the early dominant amphibians, several waves of dominance by reptiles including the dinosaurs, and many radiations and extinctions of mammals. The current concern regarding declines and disappearances of many amphibians is justified because it may be an early manifestation of a general crisis in biodiversity. It seems likely, though, that as long as terrestrial habitats continue to accommodate vertebrate life, some amphibians will persist.

See Also the Following Articles BIRDS, BIODIVERSITY OF • FISH, BIODIVERSITY OF • MAMMALS, BIODIVERSITY OF • REPTILES, BIODIVERSITY OF

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