Anura

(Frogs and toads)

Class Amphibia

Order Anura

Number of families 28

Number of genera, species 352 genera; 4,837 species

Evolution and systematics

Anurans (frogs and toads) usually are divided into two informal groups. Of these groups, the archaeobatrachians include the basal living families Ascaphidae, Leiopelmatidae, Bombinatoridae, Discoglossidae, Pipidae, Rhinophrynidae, Megophryidae, Pelobatidae, and Pelodytidae as well as the fossil family Paleobatrachidae. Some authors consider Megophryidae, Pelobatidae, Pelodytidae, Pipidae, and Rhinophrynidae to constitute an "intermediate" group, the mesobatrachians; all other families are placed among the neobatrachians.

Even the most experienced herpetologists can have difficulty ascertaining the family to which a frog belongs by examining only the external features, because many species closely resemble other species in unrelated families. The most important morphological characters are features of the internal anatomy, especially the skeleton. In the nineteenth century, biologists discovered that some frogs lacked tongues and so divided the Anura into two suborders—tongued frogs (Phaneroglossa) and tongueless frogs (Aglossa). Subsequently, two basic types of pectoral girdles were recognized—two halves overlapped ventrally (arciferal condition) and two halves fused midventrally (firmisternal condition).

Early in the twentieth century many additional suites of characters were discovered, including different kinds of vertebral articulations, presence of free ribs, dentition, and thigh musculature. By the middle of the twentieth century, classification of anurans commonly consisted of five suborders (Amphicoela, Anomocoela, Diplasiocoela, Opisthocoela, and Procoela) based on the nature of the articulating surfaces of the vertebrae and the intervertebral elements, but contemporary herpetologists no longer accept this arrangement. Later in the century, larval characters, developmental patterns, nature of the mating embrace (amplexus), and pupil shape were added to the growing number of characters used in classification. By the end of the twentieth century, molecular data sets provided support for some but not all arrangements based on morphological features; also, by this time, rigorous analyses were used to propose testable hypotheses of phylogenetic relationships of both living and extinct anurans.

The resulting phylogenies and classifications place the Triassic Triadobatrachus as the sister taxon to anurans and establishes the monophyly (descendents of a single ancestor) of Anura, within which the basal familes Ascaphidae, Leiopelmatidae, Bombinatoridae, and Discoglossidae form a grade. The assumed sister relationships of Pipoidea (Pipidae and Rhinophrynidae) and Pelobatoidea (Megophryidae, Pelobatidae, and Pelodytidae) are the subject of controversy. Many unresolved problems exist within the neobatrachians, but most evidence supports a clade (all descended from one ancestor) usually referred to as the ranoids (Arthroleptidae, Hemisotidae, Hyperoliidae, Microhylidae, Ranidae, Rhacophoridae, and Scaphiophrynidae). A group of Madagascar frogs recognized by some workers as Mantellidae has been placed in the Rhacophoridae or Ranidae by various researchers (covered here in Rhacophoridae).

The remaining neobatrachians, sometimes referred to as bufonoids, may be viewed as a grade between archaeobatrachians and ranoids. Among the bufonoids, no evidence supports the monophyly of Leptodactylidae; morphological and molecular data support the monophyly of one group of families—Allophrynidae, Centrolenidae, and Hylidae (including Pseudidae). Morphological data associate Sooglossidae, endemic to the Seychelles Islands group, with the Australo-Papuan Limnodynastidae and Myobatrachidae, but molecular evidence places Sooglossidae as the sister taxon to ranoids. Also, Dendrobatidae has been placed in the ranoids by some authors, but molecular evidence does not support that arrangement. Relationships of Bufonidae, Brachycephalidae, Heleophrynidae, Limnodynastidae, Myobatrachidae, and Rhinodermatidae have

yet to be determined with any degree of certainty, but some molecular evidence supports the relationships of Bufonidae and Rhinodermatidae and of Heleophrynidae and Myobatrachidae.

Physical characteristics

Anurans are unique among amphibians and all other vertebrates in having a broad head, large mouth, large protuberant eyes, short body, and no tail. The hind limbs are long and modified for jumping by having an extra segment composed of elongated "ankle" bones—fibulare and tibiale (astragalus and calcaneum, respectively). The vertebral column is short and consists of no more than nine (usually eight, but 10 in the Jurassic Notobatrachus) presacral vertebrae; the presacral vertebrae are articulated firmly so as to allow only slight lateral and dorsoventral flexure, and the postsacral vertebrae are fused into a bony rod, the urostyle (coccyx).

Although most anurans have snout-vent lengths of about 1.5–3.0 in (35–75 mm), many are much smaller, and a few are much larger. The smallest frogs are the Brazilian two-toed toadlet (Psyllophryne didactyla) and the Cuban Iberian rain frog (Eleutherodactylus iberia), which have lengths of 0.42 in (10.2 mm) and 0.43 in (10.5 mm), respectively. By far the largest anuran is the West African ranid, the Goliath frog (Conraua goliath), which reaches a length of 13 in (32 cm).

Larval anurans (tadpoles) are unlike the aquatic larvae of other amphibians. Tadpoles have short, globular bodies and long tails. The mouth is a unique structure usually containing keratinized rows of labial teeth and jaw sheaths supported by cartilaginous elements. During metamorphosis the tail is absorbed, and the mouthparts and their support structures change dramatically to produce the adult condition.

Distribution and habitat

Frogs and toads are nearly worldwide in distribution, except for Antarctica, Greenland, Arctic regions of North America and Eurasia, and some oceanic islands. In desert regions, such as the Sahara, they are restricted to oases. Few species live at high latitudes. The ranges of only three species extend north of the Arctic Circle; these are the brown frog (Rana temporaria) and the moor frog (Rana arvalis) in Eurasia and the wood frog (Rana sylvatica) in North America. The southernmost frog is the gray four-eyed frog (Pleurodema bufonina), which reaches the Straits of Magellan. Most frogs and toads live at low to moderate elevations, but a few are found at high elevations. The highest known record is for the Pakistani toad (Bufo siachinensis) at an elevation of 16,971 ft (5,238 m) in the Himalaya Mountains of Pakistan. In South America, the range

of the puna frog (Pleurodema marmorata) extends to 16,200 ft (5,000 m) in the Andes of Peru.

Far more anurans live in the tropical parts of the world than in the northern temperate climates. Only 90 species live in North America and 116 species in temperate Eurasia. The greatest diversity of anurans is in the neotropical region (Central America, South America, and the West Indies), which is home to about 2,200 species. This number is about three times those in tropical Asia or tropical Africa and about five times that in the Australo-Papuan region.

Different historical patterns are evident among anurans. The basal living families Ascaphidae (northwestern North America) and Leiopelmatidae (New Zealand) apparently are relics of former widespread Pangaean distributions and presumably are related to Notobatrachus from the Middle to Upper Jurassic boundary in Argentina. With the breakup of Pangaea in the Triassic, the ancestors of the archaeobatrachian families Bombinatoridae, Discoglossidae, Megophryidae, Pelobatidae, and Pelodytidae were in Laurasia, whereas the ancestors of the other families of archaeobatrachians and the neobatrachians were in Gondwana.

Behavior

Because of their thin skin, through which water is lost, most frogs live in humid regions or are active only during rainy seasons of the year. During dry times of the year, anurans estivate, usually below ground. Likewise, in temperate regions, anurans hibernate below the frost line. Despite these physiological limitations, anurans display a wide variety of activity, mostly at night, when they feed and breed. Most respiration is cutaneous (through the skin) and is facilitated by dermal mucous glands that secrete a moist coating.

The long hind limbs facilitate a saltatorial (jumping) locomotion; most frogs can leap two to 10 times their body length, and a few can approach 30 times their body length. A few anurans (e.g., species in the Andean bufonid genus Osornophryne) have relatively short hind limbs and slowly walk instead of jumping. Because of their saltatorial locomotion, anurans do not leave a scent trail, and females do not locate males by chemosensory means. Instead, male frogs vocalize; air is forced from the lungs over the vocal cords and is resonated by a single or paired vocal sacs. Acute hearing allows females (and other males) not only to recognize the unique vocalization of their species but also to locate the calling males.

Predation of anurans

Throughout all stages of their life cycle anurans are preyed upon by a great variety of animals, and small frogs even fall prey to a carnivorous plant—the Venus flytrap. Aquatic eggs are eaten by fish and various aquatic invertebrates; the arboreal eggs of centrolenids are consumed by various orthopterns and parasitized by wasps and flies, and the arboreal eggs of phyllomedusines are eaten by noctural colubrid snakes of the genus Leptodeira. Tadpoles are eaten by fishes, snakes, wading birds, and aquatic insects, such as diving beetles, water bugs, water scorpions, and dragonfly larvae. Some salamander larvae also feed on tadpoles, and the large tadpoles of species of Ceratophrys and Leptodactylus pentadactylus consume the smaller tadpoles of other species. Adult African clawed frogs (Xenopus laevis) also feed on tadpoles. Practically anything will eat anurans, especially newly metamorphosed individuals. Frogs are consumed by a variety of birds and mammals. Many snakes feed almost exclusively on frogs, and several species of carnivorous frogs include anurans in their diets. When in water, anurans fall prey to fishes, turtles, and crocodilians. Spiders are the major invertebrate predators on small anurans.

Anurans have evolved a variety of defense mechanisms to escape predation. The most obvious of these methods is the jumping ability of most anurans; by leaping away, anurans leave no scent trail that can be followed by a potential predator using chemosensation in tracking its prey. This kind of escape behavior may involve a long leap to shelter (e.g., from land to water, as employed by many species of Rana); a single leap and subsequent immobility, with the anuran depending on cryptic coloration to avoid subsequent discovery (e.g., many cryptically colored terrestrial frogs, such as some species of Eleutherodactylus); a leap from one branch to another, as is characteristic of most treefrogs; a series of long leaps that carry the frog a sufficient distance from the predator (e.g., the rocket frog, Litoria nasuta, in Australia); or a series of multidirectional hops, such as are employed by cricket frogs of the genus Acris and dendrobatid frogs of the genus Colostethus.

Many anurans have cryptic or disruptive coloration, so that they are difficult to detect visually by potential predators. Other anurans are structured cryptically so that they blend into the substrate. This is a common feature of "dead-leaf mimics" that live on the forest floor. Examples are species of Bufo, Ceratobatrachus, Edalorhina, Hemiphractus, and Megophrys, all of which have disruptive structures, such as projecting snouts or posterolateral corners of their skulls, dermal flaps, or dermal ridges.

Many anurans exhibit defensive behavior when faced by a potential predator. Some treefrogs (Hylidae) feign death by tucking the limbs close to the body and remaining motionless on their backs. A common defensive behavior among heavy-bodied anurans is the inflation of the lungs, thereby puffing up the body and presenting a larger image to a potential predator. Other species modify their posture to display aspects of

their coloration. Some leptodactylid frogs of the genera Physalaemus and Pleurodema have large, elevated inguinal glands, which are displayed prominently in a defensive posture when the head is lowered and the pelvic region is elevated, thereby emphasizing the glands to a potential predator. The markings on the glands have been interpreted as "eyespots," with the suggestion that the broad pelvic region with elevated "eyes" gives an image of a much larger frog.

Some anurans avoid predation by being unpalatable to potential predators. Granular (or poison) glands may be distributed throughout the integument or concentrated in certain areas, such as the parotoid glands behind the eyes in toads of the genus Bufo, and secrete substances that are noxious or even toxic. Consequently, potential predators soon learn to avoid grabbing such anurans. Poison frogs of the genera Dendrobates, Epipedobates, and especially Phyllobates have extremely toxic steroidal alkaloids in the skin; these frogs also have bright aposematic (warning) coloration and usually are avoided by predators. Defensive postures may be assumed to direct poison glands toward a potential predator. This is obvious in toads of the genus Bufo when they elevate the posterior part of the body and lower the head directly at the

predator. Some frogs (e.g., Bombina and Melanophryniscus) display their brightly colored venters in an unken reflex consisting of arching the back and elevating the head and posterior part of the body while remaining motionless. Even the eggs of some species of bufonids of the genera Atelopus and Bufo have noxious properties, as do the larger tadpoles of other anurans, such as Rana chalconota and Gastrophryne carolinensis.

Feeding ecology and diet

Most anurans adopt the sit-and-wait foraging strategy; that is, they perch in one place and wait for suitable prey to appear. In most anurans, vision is important in detecting potential prey, and anurans respond positively to movement of prey. Anurans can distinguish different colors, and visual cues are used to identify different kinds of prey, such as those that may be optimal in energy content or those that are distasteful. Some frogs, such as Bufo boreas, B. marinus, and Rana pipiens, are capable of locating prey solely by olfaction, and some species of Bufo are known to be able to locate prey by auditory

detection. The aquatic Pipidae, however, have poor vision and detect prey by olfaction; they also can detect movements of potential prey by the sensitive lateral-line organs.

Prey are captured with the tongue, which is equipped with glands that produce a sticky substance. Prey capture involves a lingual flip, during which the posterodorsal surface of the retracted tongue becomes the anteroventral surface of the extended tongue; adhesion to the prey permits retraction of the prey into the mouth. Food is not chewed but swallowed whole. In this manner, anurans feed on a great variety of insects, spiders, and other small invertebrates. It seems that most anurans feed on a variety of prey, determined by the animal's gape and corresponding size of the prey. Several small frogs specialize on small prey, especially ants (e.g., dendrobatids and many microhylids) and termites (e.g., members of the leptodactylid genus Physalaemus and fossorial frogs of the genera Hemisus and Rhinophrynus). Some large frogs, such as the African ranid (Pyxicephalus) and the South American leptodactylid (Ceratophrys) feed on small vertebrates, including other frogs, snakes, lizards, rodents, and birds. But some anurans feed in other ways. The diurnal dendrobatids use the same mechanism for feeding, but they are active foragers on the ground, where they feed on small prey, such as ants and small beetles. A few frogs feed on ants and termites underground; at least one of these frogs, the Mesoamerican burrowing toad, Rhinophrynus dorsalis, does not flip its tongue but protrudes it forward from the small mouth. Pipid frogs are completely aquatic and lack tongues; feeding is accomplished by transportation of food into the mouth with water currents produced by pumping movements of the throat, but larger prey are pushed into the mouth by the fingers.

Reproductive biology

Except for Dendrobatidae and a few Ranidae, mating typically takes place by males grasping females from above (amplexus). In archaeobatrachians, Myobatrachidae, Sooglossidae, and a few Leptodactylidae, the male grasps the female around the waist (inguinal amplexus), whereas males of most neobatrachians grasp the female just behind the forelimbs (axillary amplexus). In the globular-bodied microhylids (e.g., Breviceps,), the small males are "glued" by dermal secretions of the male to the posterior part of the body of the much larger females. In a few Ranidae (e.g., Nyctibatrachus and some species of Mantidactylus), males simply straddle females. In some Dendrobatidae, amplexus is cephalic, other dendrobatids and some Eleutherodactylus do not amplex but solely juxtapose their cloacas. In these various positions, the female deposits eggs that are fertilized externally.

Most species deposit their eggs in water, but many Leptodactylidae (Eleutherodactylus and relatives), some Arthroleptidae, Microhylidae, and Ranidae, among others, deposit eggs in moist places on the ground, and these eggs undergo development directly into froglets; the aquatic tadpole stage is bypassed. Internal fertilization is known for a few anurans. Males of the stream-dwelling Ascaphus have a "tail," an extension of the cloaca, that during inguinal amplexus is inserted into the cloaca of the female. Fertilization is internal and accomplished by cloacal apposition in Eleutherodactylus jasperi and some species of Nectophrynoides.

Resources

Books

Duellman, William E., ed. Patterns of Distribution of Amphibians: A Global Perspective. Baltimore: Johns Hopkins University Press, 1999.

Duellman, William E., and Linda Trueb. Biology of Amphibians. Baltimore: Johns Hopkins University Press, 1994.

Lynch, John D. "The Transition from Archaic to Advanced Frogs." In Evolutionary Biology of Anurans, edited by James L. Vial. Columbia: University of Missouri Press, 1973.

Savage, Jay M. "The Geographic Distribution of Frogs: Patterns and Predictions." In Evolutionary Biology of Anurans, edited by James L. Vial. Columbia: University of Missouri Press, 1973.

Tyler, Michael J. Frogs. Sydney, Australia: Collins, 1976.

Periodicals

Bossuyt, Franky, and Michel C. Milinkovitch. "Convergent Adaptive Radiations in Madagascan and Asian Ranid Frogs Reveal Co-variation Between Larval and Adult Traits."

Proceedings of the National Academy of Sciences of the United States of America 97 (2000): 6585–6590.

——. "Amphibians as Indicators of Early Tertiary 'Out-of-India' Dispersal of Vertebrates." Science 292 (2001): 93–95.

Ford, Linda S., and David C. Cannatella. "The Major Clades of Frogs." Herpetological Monographs 7 (1993): 94–117.

Hay, Jennifer M., et al. "Phylogenetic Relationships of Amphibian Families Inferred from DNA Sequences of Mitochondial 12S and 16S ribosomal RNA genes." Molecular Biology and Evolution 12 (1995): 928–937.

Maglia, Anne S., L. Analía Pugener, and Linda Trueb. "Comparative Development of Anurans: Using Phylogeny to Understand Ontogeny." American Zoologist 41 (2001): 538–551.

Orton, Grace L. "The Systematics of Vertebrate Larvae." Systematic Zoology 2 (1953): 63–75.

William E. Duellman, PhD