Reproduction

An essential attribute of any species or population is the ability to produce a succeeding generation. As the first vertebrates to set foot on land, amphibians were faced with new reproductive challenges. The primitive reproductive behavior involves terrestrial adults moving to water. There the eggs are deposited, fertilized externally, and develop into larvae that obtain necessary nutrients from the aquatic environment; the larvae grow and change into adults with a body form adapted for life on land—a process known as metamorphosis. Early European naturalists observed this kind of reproductive behavior in local frogs, toads, and newts, and for more than a century, amphibians were characterized as having a biphasic (two-stage) life cycle (as implied by the name Amphibia).

One of the most fascinating aspects of amphibians is that their successful exploitation of a great variety of habitats necessitated the evolution of diverse reproductive modes; these modes made use of existing environmental resources in mixed climatic conditions and enhanced the survival of their young. It generally is conceded that the ancestral reproductive mode is the deposition of eggs that are fertilized externally and that development takes place in water or in a moist terrestrial or arboreal (tree) environment; this mode is known as oviparous. During their nearly 300 million years of reproductive experimentation, different groups of amphibians independently evolved terrestrial eggs, many of which undergo direct development into miniatures of the adults and bypass the free-living aquatic larval stage. Various amphibians exhibited different degrees of parental care, not only attending eggs or larvae or both but in some cases also transporting them; others evolved ways to fertilize eggs internally. In the latter case, the result is that embryos derive nutrients from the yolk for development (ovoviparous) or obtain nutrients from maternal tissues (viviparous) in a manner reminiscent of placental mammals. Both ovoviviparity and viviparity result in the birth of living young that are miniatures of the adults; again, there are no intermediate aquatic larval stages.

Within these general evolutionary trends, there are many specializations restricted to a few species (e.g., stomach-brooding and carrying larvae in pouches) and some deviations that are counter to general trends (e.g., nonfeeding larvae in terrestrial nests in humid regions). However, the overall pattern clearly is toward increased terrestriality. Thus, the existence among amphibians of manifold ways to reproduce is an example of multiple evolutionary success stories—amphibians have adopted disparate life-history strategies to cope with a variety of environmental regimes. The diversity of these strategies within the group as a whole and their flexibility within species and even within populations reflect the evolutionary and ecological diversity of amphibians, the vertebrate pioneers of the terrestrial environment.

There are costs and benefits associated with different reproductive strategies in amphibians. The presumed primitive strategy is to produce many small eggs with a small amount of yolk and deposit them in water; these eggs hatch into small larvae that obtain nutrients from the environment (exogenous larvae). Parental investment (energetic expenditure) per offspring is minimal, but survivorship is low. The large numbers of potential offspring maintain populations; this is the strategy common to ambystomatid salamanders and many families of frogs, (e.g., bufonids, hylids, and ranids). Chances of survivorship improve when larger eggs with more nutrients are produced; the embryos hatch as more advanced larvae. These larvae can survive in more strenuous environments, such as mountain streams (e.g., salamanders, such as Dicamptodon and Rhyacotriton, and anurans, such as Atelopus, Ptychohyla, and Scutiger), or require less time to complete metamorphosis (e.g., some species of marsupial frogs). This strategy requires greater investment per offspring by the female. The next step is production of fewer eggs with sufficient nutrients for the completion of development as nonfeeding larvae or as miniatures of the adults. Maternal investment per offspring and survivorship are high. Survivorship is enhanced by many kinds of parental care, but in many of these species fecundity is low.

Direct development not only has evolved independently in different lineages of anurans, but it also has taken place in distinct ways. In most direct-developing anurans, the early larval stages are absent; thyroid hormones that are essential to triggering metamorphosis in tadpoles also influence later developmental stages in frogs, such as Eleutherodactylus coqui, and bring about the metamorphic climax shortly before hatching. In contrast, in hemiphractine hylids, the usual larval stages are present within the egg capsules of those species with direct development. Possibly, the production of tadpoles in some species of marsupial frogs (Gastrotheca) is an example of

arrested development or simply suggests that there are insufficient amounts of nutrients in the eggs to complete development.

Courtship and mating

With the possible exception of some poison frogs of the genus Dendrobates, in which pairs apparently are bonded throughout a breeding season, amphibians are polygamous. Most salamanders reach sexual maturity during their second year, with females usually maturing later than males. Females of the aquatic cryptobranchids and proteiids do not breed before six years; in contrast, both sexes of the aquatic plethodontid Eurycea multiplicata reach sexual maturity shortly after metamorphosis at an age of five to eight months. Most anurans reach sexual maturity in six months to one year, but species inhabiting cool climates require much longer, up to four years in Ascaphus and many Rana. The limited data on caecilians suggest that sexual maturity is reached in two to three years.

Reproductive cycles are controlled by hormones, the actions of which are correlated with environmental variables as well as constraints of habitat, size, reproductive mode, and parental care. Caecilians reproduce biennially, and salamanders reproduce annually or biennially. In the wet tropics, anurans commonly reproduce continually and may deposit several clutches of eggs per year, but in seasonally dry or cold regions, the number of clutches may be limited to one per year or one every other year. In temperate regions, breeding coincides with higher temperatures and spring rains, whereas in semiarid regions and deserts, breeding activity is initiated by rains that result in the formation of temporary ponds. Thus,

breeding activities may be limited to only a few days or weeks in any given year.

In many amphibians, especially those laying terrestrial eggs, courtship and mating take place within their normal home ranges, but most of those species that deposit their eggs in water migrate to breeding sites, and large numbers of individuals often congregate at these sites. Several species of anurans and salamanders are known to return to the same breeding sites in successive years; in some cases, this is the site where they developed as larvae. Olfaction seems to be the primary method used by salamanders and some frogs to locate breeding sites, but vocalization plays the dominant role among most frogs. Calling by aggregations of anurans attracts not only females but also other males to the breeding site. Little is known about courtship in the secretive, subterranean caecilians; it is thought that olfaction is important for the location of mates in burrows.

Release of hormones (principally gonadotropin) during early phases of the reproductive cycle results in the development of many secondary sexual characters that can persist throughout adult life or might be transitory during the reproductive season. Among the former features are body size and skin texture. Females usually are larger than males. Males of some salamanders, especially newts (Salamandridae), develop

more intense coloration, and in many kinds of male frogs, vocal sacs become more brightly colored during the breeding season. Courtship glands develop on the chins of males of many kinds of salamanders, especially plethodontids, and on the chins and bellies of various kinds of frogs. The most conspicuous secondary sexual characteristics are horny growths known as nuptial pads or excrescences in males. Males use these growths to better grip the female during breeding. Most male anurans clasp females from above (amplexus); the clasp is around the waist (inguinal amplexus) in some frogs, but more often it is just behind the arms (axillary amplexus). Nuptial excrescences are present at the base of the thumb and sometimes on the fingers and the chest; typically, the excrescence is a roughened pad, but in some species it takes the form of one to many spines. Nuptial excrescences also develop on the insides of the arms or legs of some salamanders that breed in water.

Fecundity and egg deposition

Generally, larger species deposit more eggs than smaller species, and eggs placed in water are smaller and more numerous than those laid on land or carried by a parent. For example, the oviparous caecilian Ichthyophis glutinosus may lay as many as 54 eggs in a clutch, but the viviparous Geotrypetes seraphini gives birth to only one to four young. Fecundity is higher in salamanders; again, clutches deposited in water are the largest. The tiger salamander (Ambystoma tigrinum) can lay as many as 500 eggs, and the hellbender (Cryptobranchus alleganiensis) and the greater siren (Siren lacertina) deposit clutches of about 450 and 500 eggs, respectively. In contrast, clutches of the Olympic torrent salamander (Rhyacotriton olympicus) contain as few as eight relatively large eggs laid in mountain streams. Many plethodontid salamanders lay their eggs on land; clutches may contain as few as nine and as many as 40 eggs. The live-bearing salamander (Salamandra atra) gives birth to only two young at a time.

Fecundity in anurans varies much more widely than in other groups of living amphibians. Many species, especially large species of Bufo and Rana, that deposit eggs in water have extremely large clutches containing thousands of eggs. Many small and medium-size species in the humid tropics lay clutches of only a few hundred eggs, but females return to

breeding ponds in a matter of a week or two to deposit another clutch. Species (e.g., phyllomedusine hylids and hyperoliids of the genera Afrixalus and Hyperolius) that deposit their eggs on vegetation above water have smaller clutches, commonly fewer than 400 eggs, and the small glass frogs (Centrolenidae) usually deposit fewer than 40 eggs. Many kinds of frogs deposit clutches of six to 67 eggs on land; in some cases the eggs are deposited in chambers excavated by the parents. A few kinds of frogs give birth to no more than eight living young at a time.

Anurans deposit eggs in places other than in water or on land. Several kinds of hylids and microhylids lay their eggs in water-holding leaf axils, tree holes, or bromeliads; such clutches usually contain fewer than 60 eggs. Amplectant pairs of some leptodactylids and limnodynastids kick the eggs with their feet into a mixture of water, air, and secretions that form a foamlike mass floating on the water; the outer part of the foam nest hardens and protects the moist interior in which the eggs develop. Rhacophorid frogs also build foam nests on leaves or branches over water, and some leptodactylids (Adenomera) deposit eggs in terrestrial foam nests, where the eggs and embryos obtain all their nutrients for development from the yolk. Fecundity decreases from as many as 1,000 eggs in aquatic foam nests to as few as 25 in terrestrial foam nests.

Fertilization

The eggs, which consist of an ovum within one or more gelatinous capsules, are fertilized externally in nearly all anurans and in salamanders of the families Cryptobranchidae, Hynobiidae, and, presumably, Sirenidae. Eggs are deposited in water (on land in the case of many anurans), and males exude sperm over them. However, in all caecilians and in most salamanders, success is enhanced by internal fertilization. In caecilians, males have a penis-like intromittent organ, the phallodeum, which is inserted into the female's cloaca. This unique structure in amphibians is a portion of the cloaca that is eversible (able to turn inside out). An analogous, but not

homologous, "tail" (a posterior extension of the cloaca) in frogs of the genus Ascaphus (Ascaphidae), which breed in fast-flowing streams, conducts sperm from the male into the female's cloaca. Internal fertilization in salamanders is accomplished by another unique feature, the spermatophore, which is a conical, gelatinous structure with a cap of sperm. During courtship, males deposit spermatophores on the substrate; females pick up spermatophores in their cloacas, and the sperm are stored in a small pouch, the spermatheca, off the cloaca. Subsequently, often many months later, the eggs are fertilized as they pass through the cloaca. Aside from Ascaphus, internal fertilization is known in a few other anurans, namely, African toads (Nectophrynoides) and some West Indian species of the leptodactylid genus Eleutherodactylus. Internal fertilization also is suspected in the African bufonid Mertensophryne micranotis and an East Indian ranid of the genus Limnonectes, because of modifications of the cloacal regions of males.

Development and hatching

Most aquatic eggs hatch as small larvae, whereas many terrestrial eggs undergo direct development and hatch as miniatures of the adults. In direct-developing eggs, the larval stages are completed within the egg capsules, or the larval stage is suppressed. There is a positive correlation between ovum size and stage of hatching. The ova of salamanders that have aquatic larvae usually are 0.06–0.12 in (1.5–3.0 mm) in diameter, and anuran ova deposited in water are even smaller, 0.04–0.08 in (1.0–2.0 mm) in diameter. Such eggs contain small amounts of yolk that provide sufficient nutrients for only partial development. The larvae obtain nutrients from the environment for the rest of their development.

In those salamanders and frogs that undergo direct development, the ova contain all the nutrients necessary for growth into a small salamander or frog. Consequently, the ova are much larger—0.12–0.5 in (3.0–5.0 mm) in salamanders and 0.08–0.40 in (2.0–10.0 mm) in anurans—than eggs that hatch as tadpoles. A negative correlation exists between temperature and developmental rate. Aquatic eggs of salamanders develop in relatively cold water, and the duration of development ranges from 20 days in some newts (Triturus) to about nine months for the eggs of Dicamptodon in cold mountain streams. Likewise, most salamanders laying terrestrial eggs live in cool or temperate conditions; their eggs require 56–165 days to complete their growth to miniatures of the adults. The small aquatic eggs of many anurans hatch within one day of deposition, but those laid in cold water may require more than

40 days to hatch. Direct-developing eggs of anurans need longer, usually about a month, but those of the small leptodactylid Eleutherodactylus planirostris complete their development in as few as 15 days. In a few salamanders (e.g., the plethodontid Desmognathus aeneus) and several frogs (e.g., the myobatrachid Crinia nimbus, limnodynastids of the genera Kyarranus and Philoria, leptodactylids of the genus Adenomera, bufonids of the genus Pelophryne, and some dendrobatids of the genus Colostethus), terrestrial eggs hatch as nonfeeding larvae that obtain the nutrients necessary to complete growth from yolk encased in their body cavities.

Parental care

Parental care in the form of protection and feeding typifies birds and mammals; although they are less universal, diverse kinds of parental care exist among amphibians as well. Parental care can be defined as any behavior exhibited by a parent toward its offspring that increases the offspring's chances of survival; this behavior, however, can reduce the parent's ability to invest in additional offspring. Among amphibians, parental care includes attendance of eggs, transportation of eggs or larvae, and feeding of larvae. Parental care occurs only in those species that deposit their eggs in single clusters, never among species that scatter their eggs in aquatic situations. Nest construction and retention of eggs in the oviducts are not considered to be parental care.

Egg attendance

Egg attendance is the most common and taxonomically widespread type of parental care. In most cases, the eggs simply are guarded against potential predators, but some species of salamanders have been observed to rotate and possibly aid in aeration of aquatic eggs by creating water currents with their gills or tails. Guarding seems to be the principal function of terrestrial salamanders that coil about their clutches, but by osmotic transfer of moisture they also may help prevent desiccation of the eggs; some species also have been seen to rotate the eggs, which aids in the elimination of pathogenic fungi. A few anurans attend clutches of aquatic eggs, but many attend terrestrial or arboreal clutches.

Stream-inhabiting salamanders of five families are known to attend egg clutches attached to objects in streams; attendance is by males in Andrias, Cryptobranchus (Cryptobranchidae), and several species of Hynobius (Hynobiidae) but by females in two species of Dicamptodon (Dicamptodontidae), several species of plethodontids (Desmognathus, Eurycea, Gyrinophilus, and Pseudotriton), and Necturus maculosus (Proteiidae). Attendance is by either parent in the subterranean proteiid Proteus anguinus. Generally, the adults remain with the eggs from the time of deposition until hatching; the duration of this attendance varies from about six weeks in Necturus maculosus to about 13 weeks in Desmognathus marmoratus.

Attendance by females at terrestrial nests is known among many salamanders—the ambystomatid Ambystoma opacum and several genera of plethodontids (e.g., Batrachoseps, Bolitoglossa, Ensatina, Desmognathus, Hemidactylium, and Plethodon). Because egg deposition may occur many months after insemination by spermatophores, males of these salamanders may no longer be in the vicinity and do not attend nests. The duration of female attendance varies from about six weeks in Ambystoma opacum to nearly six months in Bolitoglossa rostrata. Females of some caecilians (Ichthyophis and Idiocranium) and one salamander (Amphiuma) are known to coil around subterranean clutches of eggs, presumably to minimize desiccation, or loss of moisture.

With the exception of males of the hairy frogs (Arthroleptidae: Trichobatrachus robustus), which sit on eggs in streams, and males of the moustache toads (Megophryidae: Vibrissaphora), which guard eggs under boulders at the edges of streams, attendance of aquatic eggs among anurans is known only in species that lay eggs in foam nests (Limnodynastidae: Adelotus) or in basins constructed by males (Bufonidae: Nectophryne; Hylidae: Hyla rosenbergi). In these cases, the eggs are in territories defended by males, who secondarily guard eggs. Eggs are not attended very long in these species—two to three days in Hyla rosenbergi, six days in Adelotus brevis, and 35 days in Nectophryne afra. Females of some species of Leptodactylus guard aquatic foam nests and subsequently remain with the schools of tadpoles, defending them from potential predators.

Male attendance of egg clutches on vegetation over water is common among territorial centrolenids, but it is unknown in the arboreal-nesting phyllomedusine hylids. Centrolenids not only guard the eggs from potential parasitic insects but also keep the eggs moist by perching on top of them by day. Species in three genera of microhylids (Anodonthyla, Platypelis, and Plethodontohyla) in Madagascar deposit their eggs in water-filled leaf axils; males attend the eggs for 26–35 days, until hatching. Females of the African ranid Phrynodon attend arboreal eggs, as do females of at least two hyperoliids (Alexteroon obstetricans and Hyperolius spinigularis), who not only guard their arboreal egg clutches but also moisten them by eliminating water from their bladders on the eggs.

Attendance of eggs is common among species that deposit their eggs on the ground and in burrows. The eggs of African Hemisus (Hemisotidae) and Breviceps (Microhylidae) are deposited in subterranean burrows and attended by females, who presumably moisten the eggs. Females of the former genus burrow headfirst from the chamber to a nearby pond, thereby releasing tadpoles into the water.

Several species of frogs in different families and one salamander, the plethodontid Desmognathus aeneus, have terrestrial eggs that hatch as nonfeeding larvae and derive all their nutrients from the yolk encased in their bodies. Attendance is by females in the salamander and in the leptodactylid frog

Zachaenus parvulus, but the eggs are attended by males in the leptodactylid Thoropa petropolitana, the bufonid Nectophrynoides malcolmi, three species of the ranid genus Petropedetes, and at least two microhylids (Breviceps adspersus and Synapturanus salseri).

Clutches of terrestrial eggs undergo direct development into froglets in many different lineages of anurans. This mode of development is characteristic of all arthroleptines and brachycephalids, three species of Leiopelma, two genera of myobatrachids (Arenophryne and Myobatrachus), a few bufonids and ranids, and leptodactylids of the genus Eleutherodactylus (and relatives). The mode also characterizes about 50% of the Microhylidae (all asterophryines, brevicipines, and genyophrynines and at least one microhyline, Myersiella microps). In some cases females attend the clutches, but in others attendance is by males, especially territorial species, such as some Eleutherodactylus. The known duration of attendance is 17–100 days.

Transportation of eggs and larvae

Adults of diverse species of anurans that attend developing clutches of eggs subsequently transport eggs, larvae, or

both. The European midwife toads of the genus Alytes exhibit the simplest form of this type of parental care. As the strings of eggs are deposited and fertilized in shallow water, they adhere to the hind limbs of the male; he carries them with him and enters water when the eggs are ready to hatch, at which time the egg membranes disintegrate, and the tadpoles swim away.

Most instances of larval transport are associated with terrestrial eggs. In all dendrobatids except Aromobates, an adult sits in the disintegrating gelatinous material, and the hatchling tadpoles wriggle up the legs and onto the back of the adult. The larvae do not hold on to the adult with their mouths; instead, their bellies adhere to the skin on the dorsum of the parent by means of a gluelike substance (mucopolysaccharide) that dissolves in water once the parent transports them to a stream, small pond, or water-holding plant. In some Dendrobates, adults transport tadpoles from terrestrial nests to arboreal bromeliads that may be as high as 100 ft (30 m) above the ground. Similar transportation of larvae from terrestrial nests to aquatic sites for tadpole development is known in two genera (Aphantophryne and Liophryne) of genyophrynine microhylids and in some species of the ranid genus Limnonectes. Terrestrial eggs of the sooglossid Sooglossus sechellensis hatch as nonfeeding larvae that wriggle onto the back of the attending female, where they complete their growth. Transportation of hatchling froglets occurs in three of the four species of Leiopelma in New Zealand; the hatchlings climb on the back of attendant males.

Males of the small myobatrachid frog in Australia (Assa darlingtoni) have an inguinal pocket on each side of the body. The male sits in a clutch of 10 or 11 terrestrial eggs; upon hatching, the nonfeeding tadpoles wriggle onto the male and into the inguinal pockets, where they complete their development and emerge as froglets about two months later. Males of the southern South American mouth-brooding frogs of the family Rhinodermatidae attend terrestrial clutches of eggs. Male Rhinoderma rufum transport the tadpoles in the mouth to water, where they complete their development. Male Rhinoderma darwinii pick up hatchling tadpoles in the mouth; the tadpoles enter the vocal sac via the vocal slits in the floor of the mouth. The male carries the tadpoles in his vocal sac for 50–70 days, at which time fully developed young crawl through the vocal slits and emerge from the mouth. Some evidence suggests that nutrients are provided by the epithelial lining of the vocal sac.

Two groups of anurans exhibit highly specialized modes of transport of eggs and developing embryos under entirely different environmental conditions. During inguinal amplexus in aquatic frogs of the genus Pipa (Pipidae), females exude eggs into the water, and males sweep them with the feet onto the backs of the females, where the eggs become imbedded in the females' skin. In all species the eggs hatch as tadpoles. In some species (e.g., Pipa carvalhoi and P. myersi), the tadpoles leave the chambers and complete development as free-swimming tadpoles. In other species (e.g., Pipa aspera and P. pipa), the tadpoles complete their growth within the chambers and emerge as froglets. Females of the terrestrial and arboreal hemiphractine hylid frogs transport eggs or

tadpoles on the dorsum (back) or in a dorsal pouch; the eggs are enclosed at least partially in bell-shaped external gills. The eggs adhere to the dorsum in Cryptobatrachus, Stefania, and Hemiphractus and hatch as froglets.

In Flectonotus, the eggs reside in a basinlike structure (which may be open or closed by lateral folds of skin) on the female's back; the eggs develop into nonfeeding tadpoles that are deposited in water in bromeliads or tree holes, where they complete their development in a few days. During amplexus, male marsupial frogs of the genus Gastrotheca push eggs into the opening of a pouch on the back of the female. In most species (e.g., Gastrotheca ceratophrys, G. guentheri, and G. plumbea), the large eggs develop directly into froglets that emerge from the pouch. In several species inhabiting high elevations of the Andes, the eggs hatch as tadpoles, at which time the females sit in shallow ponds and spread out the pouch opening with their toes to allow the tadpoles to escape into the water, where they feed and complete their growth.

Perhaps the most unusual mode of transport was in two species of Australian gastric-brooding frogs (Myobatrachidae: Rheobatrachus) that lived in mountain streams in northeastern Australia and are now presumed to be extinct. The female swallowed the fertilized eggs; the eggs or embryos secreted a hormone, prostaglandin E₂, that inhibited the usual production of digestive enzymes and acids by the epithelial tissue of the stomach. Thus, for a period of six to seven weeks, the female did not feed, because her digestive system had been shut down and her stomach converted to a gestation chamber. The tadpoles obtained all nutrients for development from the large amount of yolk contained in the eggs. Young were expelled from the mouth by the mother's propulsive vomiting. Within a few days after giving birth, the female's stomach resumed its digestive function, and the female began to feed.

Feeding of tadpoles

Females of frogs in four families are known to provide eggs as nutrients for developing tadpoles; all examples of this kind

of maternal behavior occur in cases in which the tadpoles are in confined or constrained situations, such as water in bromeliads or tree holes or in foam nests. After deposition of eggs or transportation of tadpoles, the female returns to the site and deposits eggs on which the tadpoles feed. Insofar as is known, tadpoles of some species are obligatorily oophagous (egg eating), whereas those of other species also feed on detritus or insect larvae, which may be present in the water in bromeliads or tree holes.

The simplest expression of this type of parental behavior is seen in a species of Leptodactylus (L. fallax) in the Lesser Antilles and several species of hylid frogs in Jamaica and Central and South America. The eggs of L. fallax are deposited as a foam nest in a shallow basin; the hatchlings remain in a disintegrating foam nest and produce secretions that mix with moisture to create additional foam in which they develop. The female periodically inserts her cloaca into the foam and exudes eggs, on which the tadpoles feed.

Likewise, females of several hylids that deposit eggs in bromeliads or tree holes provide eggs for their larvae; these species include Anotheca spinosa, Hyla picadoi, and H. zeteki in Central America; Osteocephalus oophagus and some species of Phyllodytes in South America; and Osteopilus brunneus in Jamaica. Because presumably conspecific (i.e. of the same species) frog eggs have been found in the stomachs of some other tadpoles, the females of those species are thought to provide eggs as nutrients for their tadpoles. These species include the microhylid Hoplophryne rogersi in Africa, a species of Philautus (Rhacophoridae) in Asia, Phrynohyas resinifictrix in South America, and Calyptahyla crucialis, Hyla marianae, and H. wilderi in Jamaica. With additional studies in the field, we should expect to find many more examples of this kind of parental care.

In some species of Dendrobates, females transport tadpoles individually from the terrestrial nest to an aquatic microhabitat (bromeliad, tree hole, or the husk of a Brazil nut). Subsequently, the female returns to each of the sites of tadpole development and deposits unfertilized eggs for the tadpoles to eat. In some other species of Dendrobates (e.g., D. vanzolinii), however, the male transports the tadpoles and subsequently leads the female to each deposition site so that she can feed the tadpoles.

Live birth

Ovoviviparity (in which all nutrients during development are provided by yolk) occurs facultatively (i.e. in some conditions but not others) in two salamanders (Mertensiella caucasica and Salamandra salamandra) and two frogs (Nectophrynoides tornieri and N. viviparus). True viviparity (maternal provision of nutrients during development in the oviducts) is known in several caecilians of three different families and in two salamanders (some populations of Mertensiella luschani and Salamandra atra) and one anuran (Nectophrynoides occidentalis). During their development, fetuses of the caecilians quickly exhaust their yolk supply, escape from the embryonic membranes, and obtain nourishment from the female by ingesting secretions and epithelial tissue from the lining of the oviducts; fetal caecilians have deciduous teeth that are specialized for scraping the lining of the oviduct. Maternal nutrients also are supplied from the walls of the oviduct in Salamandra atra and by epithelial secretions in the oviducts of Nectophrynoides occidentalis.