Larvae

The majority of amphibian species have free-living larvae that are temporary residents in aquatic habitats. Although direct development of terrestrial eggs has evolved many times among modern amphibians, most species still retain a larval stage and for good reason. In parts of the world where the seasons change and ponds vary in their longevity and productivity, there are clear benefits in having an aquatic stage of development. Most amphibians lay their eggs at a time of year (spring in the temperate world and the rainy season in the tropics) when food is abundant for the larvae. The larvae then metamorphose later in the season, when competition, predation, or physical degradation of the environment (e.g., drying up of ponds) makes those habitats unsafe. Amphibian species that have lost the larval stage tend to live in tropical environments with little seasonality. Indeed, the majority of caecilians (approximately 75%) are viviparous (born alive) without a free-living larval stage. Most of the remaining caecilian species, which are oviparous (egg laying), have direct development of terrestrial eggs.

Morphologic characteristics

Among the caecilians, free-living larvae are found in some species of Caeciliidae, Rhinatrematridae, and Ichthyophiidae. These larvae are morphologically similar to the adults but have open gill slits and relatively long, filamentous, external gills. They also have a vertical tail fin and thin skin and lack scales. They are carnivorous, feeding largely on small aquatic invertebrates. Caecilian larvae are secretive, nocturnal, and little is known about their behavior and ecology.

There are free-living larvae in all salamander families, though they are absent in most plethodontid genera. Common external features that distinguish larval salamanders from adult salamanders are open gill slits and external gills, a tail fin, and specialized dentition. In certain taxa (e.g., Ambystoma), flaps of skin at the corners of the mouth help make the mouth rounder when it is open. This facilitates suction feeding, which is important in catching active prey.

At metamorphosis both caecilian and salamander larvae lose their gills, gill slits, and tail fins. There are also changes in the bones of the skull. The alimentary tract, however, alters little relative to the changes seen at metamorphosis in frogs and toads. The caecilian and salamander larvae, like the adults, are predators, feeding on aquatic invertebrates and other amphibian larvae, including in certain circumstances members of their own species.

The larvae of frogs and toads are known as tadpoles. Tadpoles differ far more from adults than do the larvae of caecilians or salamanders. The most conspicuous features that tadpoles share with adult anurans are a wide head, a short vertebral column, and no neck. As a result, tadpoles have a round combined head and body, with a laterally compressed tail appended to it. This "lollipop" shape, as seen from above, distinguishes tadpoles not only from other amphibian larvae but also from virtually all fishes. Tadpoles also differ from other amphibian larvae in that their gills and forelimbs develop under a fold of skin, the opercular fold. This fold may not cover the gills fully at hatching, but the external gills shrink, and the opercular fold grows quickly backward from the throat region to cover the gills by the time the tadpoles are freely swimming and feeding.

Compared with frogs, tadpoles have small mouths externally. This mouth is directed ventrally (downward) or anteroventrally (forward and downward) in the majority of tadpoles, which are bottom feeders. A few tadpoles graze on particles floating at the water's surface, and their mouths are directed dorsally (upward). Tadpoles in the families Microhylidae (with the exception of the Peret' toad, Otophryne), Pipidae, and Rhinophrynidae lack keratinized structures (hard tissue such as human nails) surrounding their mouths. Keratinized mouthparts are also absent in a few species with obligatorily carnivorous tadpoles that feed only on large prey (including other tadpoles of their own species, e.g., Lepidobatrachus) as well as some genera with nonfeeding larvae that survive until metamorphosis solely on yolk reserves.

Free-living tadpoles in all the other families have complex external oral features surrounding their mouths. The most prominent are the jaw sheaths (or beaks), formed of hard, darkly pigmented, keratinized tissue. The margins of these sheaths commonly are embellished with fine serrations, which make the jaws efficient at scraping and biting into soft material during feeding. In some carnivorous tadpoles (e.g., Ceratophrys), the jaw sheaths are sharply pointed. In certain stream-associated tadpoles from Southeast Asia, the sheaths are divided on the midline and are peglike in structure. This

shape presumably is an aid to holding on to irregular rocky surfaces. In some other stream-associated species, many keratinized spikes replace the sheaths. Most pond-and stream-dwelling tadpoles have a fleshy oral disc surrounding the jaw sheaths. The free border of this disc may be partly or fully covered with tiny finger-like projections (papillae). Between the marginal papillae and the jaw sheaths run transverse rows of labial teeth (also called denticles or keradonts). These teeth are formed of the same keratin that stiffens the jaw sheaths. Seen under the microscope, the individual teeth may end in a blunt point, or they can be multi-cusped, depending on the species. In the majority of tadpoles, which feed by scraping food off surfaces, the labial teeth are multi-cusped.

Tadpoles of most species from around the world have two rows of labial teeth in front of (rostral to) the upper jaw sheath and three rows of denticles behind (caudal to) the lower jaw sheath. The number of labial tooth rows ranges greatly from species to species, even among closely related taxa. For example, tadpoles of the Central American treefrog Hyla microcephala, which feed on large food particles in ponds, have small jaws set back in an oral tube and no labial teeth. Tadpoles of a certain tropical stream-dwelling Hyla, in contrast, have the most number of rows known: 17 upper and 21 lower rows.

Variations in the size and shape of the oral disc, the papillae at the margins of the oral disc, the shape of the jaws, the numbers of denticle rows, and any gaps in those rows are all important features in identifying tadpoles of different species. The ways in which these structures actually function has received little study, however. It is clear that large oral discs with many denticle rows are common among stream-dwelling tadpoles exposed to currents. The larvae use these structures to hold on to surfaces and resist being swept downstream. Jaw sheaths that have sharp edges characterize many tadpoles that feed on active prey.

High-speed video of feeding North American bullfrog (Rana catesbeiana) larvae, which have the common pattern of two upper and three lower tooth rows, show that tadpoles use their labial teeth to anchor the oral disc to surfaces while their jaws bite at the substrate. When grazing on algae, the mouth can open and close rapidly, more than six times per second at room temperature. As the jaws close, the labial teeth release their grip and then rake the surface toward the mouth. This action produces a suspension of fine material that can be sucked into the mouth. The sucking itself is achieved by the pulsatile raising and lowering of cartilaginous plates that lie under the front, or the buccal region, of the oral cavity. Pulsations of the buccal floor draw water into the mouth, aiding both feeding and aquatic breathing (i.e., gill irrigation).

Although the mouths of tadpoles are externally small, inside they are relatively large and structurally complex. Typical pond and stream tadpoles have sensory papillae near the front of the buccal cavity and additional rows of papillae on the buccal floor and roof that are used to trap larger food particles and funnel them toward the esophagus. Most tadpoles have a flap of skin that acts as a valve and separates the buccal cavity anteriorly from the pharynx region posteriorly. This valve ensures that flow through the mouth is one way, that is, backward into the pharynx. In the pharynx there are mucus-secreting organs that trap finer particles that get past the papillae of the buccal cavity. They work in conjunction with ruffled gill filters, which extend inward and upward from gill bars to catch the smaller particles that the tadpoles draw into their mouths.

These internal oral features of tadpoles vary among taxa and can be correlated with their diets. Most stream-dwelling tadpoles, for example, feed on a rather coarse suspension of material that they generate by scraping their food off of algal-covered surfaces. Such tadpoles tend to have many large papillae on the buccal floor and roof, for coarse sieving of food particles, but smaller and less dense gill filters in the pharynx. Pond tadpoles that live midwater and feed largely on single-cell organisms already in suspension (i.e., microphagous tadpoles) have few or no papillae in their mouths but comparatively large, dense gill filters. Obligatorily macrophagous tadpoles—ones that feed solely on big items, like frogs' eggs or other tadpoles—have neither elaborate buccal papillation nor large and dense gill filters. They also lack the mucus-secreting food traps. The muscles that depress the buccal floor are massive, however, which is consistent with the powerful sucking forces they must generate during feeding to capture active prey.

Water that passes the gill filters of tadpoles washes through the gill slits and around the gill filaments that lie on the superficial side of the gill bars. This water must exit the gill chamber, which is covered by an opercular fold. There may be one or two openings, called spiracles, for expelling water from the opercular cavity. The pattern of these openings has been important in the superfamilial taxonomy of anurans. Tadpoles of Ascaphidae, Leiopelmatidae, Discoglossidae, Bombinatoridae, and Microhylidae (with the exception of Otophryne) have a single, midline spiracle. Those of Pipidae and Rhinophrynidae (plus the carnivorous leptodactylid tadpole Lepidobatrachus) have two spiracles, one on each side of the tadpole. By far the most common pattern, found in the free-living ectotrophic tadpoles of all other anuran families, is a single sinistral spiracle.

In most tadpoles this single spiracle lies halfway between the ventral (front) and dorsal (back) surfaces of the tadpole, about halfway between the snout and the end of the head/body. For tadpoles of the leaf frogs (phyllomedusine hylids), which are largely midwater feeders, the otherwise sinistral spiracle lies close to the midline of the belly. In some microhylid tadpoles the branchial chamber extends all the way to the end of the body, and thus the spiracle opens near the vent. In Otophryne the sinistral spiracle is at the end of a long, flexible, free tube that extends caudally halfway to the tip of the tadpole's tail. This strange appendage is believed to help these tadpoles expel water when they are buried below the surface in the sandy bottoms of streams in northern South America.

The body cavity of tadpoles is filled mostly with an elongated and coiled intestine. Except in a few carnivorous tadpoles, the foregut of tadpoles is undeveloped, and the region of the gut tube that later becomes the stomach does not expand into a sac, as in most vertebrates, and does not secrete acid. The intestines of many tadpoles can be more than 10 times the length of the tadpole's head and body, though it is shorter in strictly carnivorous species. Most tadpoles are omnivorous grazers and at the same time suspension feeders. One typically finds silt and fragments of plant matter packed in the intestines of bottom-dwelling pond tadpoles. The microscopic animals living within that material may be disproportionately important as a source of protein for these larvae. Tadpoles of the clawed frogs (genus Xenopus) and the microhylid tadpoles are obligatory midwater suspension feeders, which is consistent with their lack of hard mouthparts for grazing on surfaces. Their guts are filled with a mixture of the various planktonic organisms that live with them in the water column.

Tadpoles vary in the timing of lung development. Most tadpoles that live in lentic (still) water fill their lungs for the first time shortly after hatching. From then on, they supplement aquatic respiration with aerial respiration. For some tadpoles that live in turbid (muddy) water, such as those of Xenopus, occasional air breaths are essential for normal growth and development. At the other extreme, tadpoles that live in lotic (flowing) water tend to be negatively buoyant and do not inflate

flate their lungs until shortly before metamorphosis. Most, if not all, bufonid tadpoles fill their lungs just before metamorphosis.

As tadpoles grow in size, their head/body and tail change little in shape, but conspicuous hind limbs develop. The limbs start as simple rounded protuberances or limb buds at the junction of the body with the tail. By the time the tadpole is ready to metamorphose, those limbs are large and functional, assisting the tadpole in locomotion. The forelimbs develop at the same time as the hind limbs, but they do so under the opercular cover and thus are not seen externally until the moment of metamorphosis, when within a day or so they erupt through the operculum.

Behavior and ecology

Where a tadpole lives is determined largely by where its mother lays her eggs. Indeed, there is evidence that adult frogs can sense the presence of potential aquatic predators and even the intermediate hosts of some parasites that might harm their tadpoles, and, given a choice, they avoid depositing their eggs in those dangerous places. Once the eggs hatch, most tadpoles in ponds and streams are on their own. The most common defense that tadpoles have against predators is their cryptic coloration and secretiveness. Most tadpoles that live in ponds hide among vegetation. Those that live in streams may hang on to rocks in torrents, where they are similarly difficult to see. Other stream-dwelling tadpoles may sequester themselves between rocks at the bottom of streams or in vegetation at the stream margins. The daily activity cycles of tadpoles have not been well studied, but pond-dwelling tadpoles of species such as the green frog, Rana clamitans, change their location throughout the day. Temperature, oxygen concentration, and predation risk all may be factors affecting the microhabitat selection of tadpoles at any hour on any day.

When tadpoles swim rapidly, they produce high-amplitude waves in their tails, and their snouts oscillate accordingly from side to side. This wobbly swimming may appear grossly inefficient. Indeed, a computer simulation of tadpole swimming has shown that tadpoles are less efficient than more streamlined fishes of similar sizes when swimming in a straight line. Those same simulations also show that the tadpole's kinematics and shape work in concert to produce a region behind the body where the hind limbs can develop without handicapping their swimming. Thus, although the shape and swimming style of tadpoles are not graceful compared with those of fish, they allow tadpoles to grow hind limbs in preparation for metamorphosis with far less loss of efficiency than a fish-shaped animal would experience. In that regard, the tadpole shape and swimming style may not be ideal for the aquatic environment, but it fits well with tadpoles' ability to transform into something quite different—a frog or a toad.

Because of their highly flexible tails, tadpoles can turn rapidly; that is, they have high angular acceleration, with a short turning radius. Those features, rather than simple speed or endurance, may be most important in terms of escaping predatory insects, fish, and wading birds. In general, though, tadpoles do not do well in large, open bodies of water, particularly if large predatory fishes are present. Most tadpoles live in temporary ponds or isolated lakes that, in the absence of active stocking programs, would not have resident populations of large fishes. Those tadpoles that live in larger and more permanent waters are found most often in the grassy margins or shallow reaches. A few tadpoles that live in the open in permanent ponds with fishes (e.g., Rana catesbeiana) that are unpalatable to some predators.

Toad tadpoles (genus Bufo) from around the world are black and particularly toxic. They form large schools with hundreds to thousands of individuals. Bufo tadpoles can distinguish siblings from nonsiblings, suggesting that school structure may be influenced by the genetic relationships of the individual tadpoles. Schooling is seen in other anuran larvae from diverse genera around the world. In a few species (e.g., the genus Leptodactylus), schooling tadpoles may even follow an adult frog, which is presumed to be guarding them, around the pools where they live.

There is increasing evidence that amphibian larvae are cognizant of other animals in their environment besides conspecifics. Salamander larvae (Ambystoma) in ponds with fish, for example, avoid the open water much more than those in similar ponds without fish. Tadpoles of many species minimize their activity and stay near the bottom when housed in aquariums with fish or predatory insects, even when the predators are screened off and thus pose no real risk to the tadpoles. Tadpoles also can exhibit phenotypic plasticity and change their form in subtle ways in response to environmental stresses. These changes are best documented in the shape of their tails, which become more efficient for swimming when the tadpoles are raised in the presence of potential predators. There are, however, trade-offs in these situations. If tadpoles change their behavior and morphologic features in response to predators, they pay for it in the time that they can spend feeding and in the morphologic characteristics they have dedicated to food capture. As a result, the threat of predation can reduce the growth rates of tadpoles. The way tadpoles sense other species is not well studied. Schooling species respond to the visual presence of other tadpoles, but for sensing nearby predators olfaction appears to be most important.

Ecomorphological types

The feature of salamander larvae that varies most with habitat is gill size. Species that live in lotic environments have proportionately smaller gills than those species that live in lentic environments. Various researchers have divided tadpoles into a wealth of categories based on ecomorphologic factors, but there is clearly a continuous spectrum of tadpole types. Anuran larval diversity is greatest in the tropics, whereas salamander larval diversity is highest among temperate taxa (most tropical salamanders, in fact, are direct developers). In the wet tropics, one can find tadpoles in aquatic habitats that are as meager as the axil bases of bromeliads or cattle footprints or as vast as a torrential stream.

In general, tadpoles that live in still water and off the bottom have tall tail fins, compared with similar species of bottom-dwelling tadpoles. Tadpoles in several families that are midwater specialists have tails that terminate in an elongated filament that can oscillate rapidly. This allows the tadpoles to hold their positions or move slowly through the water without the whole-body movements that occur when tadpoles use the entire tail for locomotion. Tadpoles that live in flowing water have proportionately longer tails with more axial musculature. The few semiterrestrial tadpoles that live on wet, rocky surfaces have long, thin tails with reduced fins. Fossorial tadpoles—whether they live in wet leaves along the edge of tropical streams or among the axils of bromeliads—also tend to have long, thin tails.

Metamorphosis

Tadpoles vary greatly in their size at metamorphosis. The tadpoles of some small treefrogs (genus Hyla) leave their aquatic environment when they are less than 0.79 in (20 mm) in length, whereas tadpoles of the paradox frog, Pseudis paradoxa, can grow to 9.8 in (25 cm) before they transform. How close a tadpole's size at metamorphosis is to the size of the mature adult varies from family to family. Thus, for example, in the Ranidae and Leptodactylidae, tadpoles that transform at a large size typically become large frogs. In the family Bufonidae, however, the tadpoles always transform at a small size regardless of whether the adult is the 1.2-in-long (30-mm-long) oak toad (Bufo quercicus) or the 9-in-long (23-cm-long) marine toad (Bufo marinus).

Metamorphosis for anurans is very rapid compared with the length of their larval life. Whereas some temperate tadpoles may take more than two years to reach metamorphosis (e.g., Ascaphus truei and Rana catesbeiana), most tadpoles can go from emergence of the forelimbs to complete loss of the tail in just a few days. At metamorphosis the forelimbs emerge, the tail is resorbed, and the head changes shape. The rapid loss of the tail is facilitated by the absence of vertebrae, except at the base. Those few caudal vertebrae fuse at the end of metamorphosis to form the urostyle, which is a long thin bone that extends backward between the hip bones of the frog and provides surfaces for the attachment of muscles used in jumping. The major change in the head is associated with the shift from a small-mouthed tadpole to a big-mouthed adult. The oral disc, labial teeth, and jaw sheaths are lost. The corners of the mouth move backward as the jaws themselves elongate. The tongue develops, except in the tongueless frogs (family Pipidae). All the internal oral features involved in the capture of food particles are lost, as are the gill filaments and gill slits. The foregut expands into a stomach, and the intestines shorten greatly as the gut prepares for a strictly carnivorous diet. All these changes testify to the great difference in the way of life of a tadpole versus an adult anuran.

Resources

Books

Anstis, Marion, ed. Tadpoles of South-eastern Australia: A Guide with Keys. Sydney, Australia: New Holland Publishers, 2002.

McDiarmid, Roy W., and Ronald Altig, eds. Tadpoles: The Biology of Anuran Larvae. Chicago: University of Chicago Press, 1999.

Sanderson, S. Laurie, and Sarah J. Kupferberg. "Development and Evolution of Aquatic Larval Feeding Mechanisms." In The Origin and Evolution of Larval Forms, edited by Brian K. Hall and Marvalee H. Wake. San Diego: Academic Press, 1999.

Wassersug, Richard J. "Assessing and Controlling Amphibian Populations from the Larval Perspective." In Amphibians in Decline: Canadian Studies of a Global Problem, edited by David Green. Herpetological Conservation, Vol. 1. St. Louis: Society for the Study of Amphibians and Reptiles Publications, 1997.

Zug, George R., Laurie J. Vitt, and Janalee P. Caldwell, eds. Herpetology: An Introductory Biology of Amphibians and Reptiles. 2nd edition. San Diego: Academic Press, 2001.

Periodicals

Liu, Hao, Richard J. Wassersug, and Keiji Kawachi. "The Three Dimensional Hydrodynamics of Tadpole Locomotion." Journal of Experimental Biology 200, no. 20 (1997): 2807–2819.

Liu, Hao, Richard J. Wassersug, Keiji Kawachi, and Masamichi Yamashita. "Plasticity and Constraints on Feeding Kinematics in Anuran Larvae." Comparative Biochemistry and Physiology A: Molecular Integrative Physiology 131, no. 1 (2001): 183–195.

Relyea, Rick A. "Morphological and Behavioral Plasticity of Larval Anurans in Response to Different Predators." Ecology 82, no. 2 (2001): 523–540.

Van Buskirk, J., and S. A. McCollum. "Functional Mechanisms of an Inducible Defence in Tadpoles: Morphology and Behavior Influence Mortality Risk from Predation." Journal of Evolutionary Biology 13 (2000): 336–347.

Richard J. Wassersug, PhD