Mandibular arch musculature of anuran tadpoles, with comments on homologies of amphibian jaw muscles

This study analyzes the structure of the mandibular arch musculature in larval, metamorphic, and postmetamorphic anurans of 26 species and makes comparisons with larvae of three caudate and one gymnophione species. Major transformations in early evolution of anuran larvae comprise, for example, the powering of the larval upper jaw cartilages by relocating insertion sites of mandibular arch levators; splitting of some larval muscles into two muscles or muscle heads (m. intermandibularis, m. lev. mand. externus, m. lev. mand. longus); evolution of a muscle invading the lower lip of the oral disk (m. mandibulolabialis), and shift of origin of the internus and longus muscles from dorsal on the cranium to sites on the ventral otic capsule and palatoquadrate, respectively. In all these characters, Ascaphus truei shares the plesiomorphic conditions with caudates. The larva of Xenopus laevis is remarkable because the insertion pattern of three larval mandibular muscles anticipates the postmetamorphic condition of frogs in general and also resembles the caudate condition. Discoglossids, bombinatorids, pelobatids, and neobatrachians are largely similar in their muscle arrangements. The filter-feeding microhylids, however, have most clearly modified the general neobatrachian pattern. Past conflicts in the interpretation and naming of muscles can be attributed to the implicit or explicit homology assumptions used. In particular, the muscles' relations to the branches of the trigeminal nerve have been the dominant criteria for inferring homology and has led to inconsistencies. This concept is questioned herein. It is observed that the relative position of the ramus mandibularis (V(3)) is more variable interspecifically in anuran larvae than previously thought. The relations of the nerve branches and muscles in larvae are maintained during metamorphosis. Considering the muscle pattern to be more conserved in interspecific comparisons than the position of the nerve branches results in a new interpretation of muscle homologies and a hypothesis of jaw muscle evolution in amphibians that is more parsimonious than earlier views. A new, simplified terminology for the jaw musculature is proposed that is applicable for larvae and adults. It maximizes information content and reflects the hypothesized homologies of amphibian jaw muscles.     

Ammonia as a pheromone in anuran tadpoles

In laboratory experiments, conspecific excretions and ammonia solutions evoked avoidance reactions in tadpoles of three anuran species, Bufo bufo, Rana temporaria, and Rana arvalis. A differential sensitivity of ammonia chemoreception was determined for two anuran species. For Bufo bufo tadpoles, these characteristics at ammonia background concentration of 0.2 mg/l lied in the range 150 % < dI/I < 500 %, and for background of 0.4 mg/l the value lied in the range 400 % < dI/I < 500 %. For Rana temporaria tadpoles, differential threshold against ammonia background concentration of 0.15 mg/l was close to 200 % and against background ammonia concentration of 1.1 mg/l was close to 100 %. These results suggest that such sensitivity of both anurans is sufficient for using ammonia in intra- and interspecies communication.     

Configurations of the rectus abdominis muscle of anuran tadpoles

Configurations of the rectus abdominis in tadpoles of 60 anuran species in 13 families were examined. This muscle is present by Gosner stage 25 and does not change until late in metamorphosis. The anterior terminus of the r. abdominis usually is a straight, transverse front or fan-shaped array only loosely associated with the rectus cervicis. In some suspension feeders (Rhinophrynus, Xenopus, but not microhylids), macrophagous suction feeders (Lepidobatrachus) and bromeliad inhabitants (Hyla bromeliacia) the r. abdominis is contigous with the r. cervicis which continues anterolaterally and dorsally from the wall of the spiracular cavity. Suctorial forms (Scutiger), those that live in confined spaces (burrowers, Centrolenella; bromeliad inhabitants, Hyla bromeliacia), and the taxa that have the r. cervicis and r. abdominis contiguous all have closed myosepta; the myosepta of other taxa; except for ones with large tadpoles (e.g., Rana catesbeiana), have large gaps between at least anterior myotomes. These initial data suggest that the configurations of the r. abdominis have responded to selection based on ecomorphological function and convergence among lineages are noted. © 1992 Wiley-Liss, Inc.     

Selective predation on tadpoles of three tailless anuran species]

In laboratory experiments an introduced fish Perccottus glenii consumed selectively tadpoles of three numerous anuran amphibian species of Moscow Province. Perccottus glenii actively consumed all seized tadpoles of the Rana arvalis and R. temporaria. These predators consumed significantly lesser number of Bufo bufo tadpoles and frequently rejected them after seizing without considerable damages. Observations showed that P. glenii rejects B. bufo after intraoral testing. Larvae of dragonfly Aeschna cyanea also actively consumed almost all seized R. arvalis tadpoles, while usually rejected B. bufo after attacking and damaging them. Larvae of diving beetle Dytiscus marginalis sucking out captured prey, intensively consumed tadpoles of R. arvalis and B. bufo and did not reject them.     

Keratodont formulae in anuran tadpoles: proposals for a standardization

The various systems proposed to describe concisely, in the form of a formula, the number and arrangement of keratodont rows in the oral disk of anuran tadpoles, are reviewed and classified. A distinction is made between individual and collective keratodont formulae. The different systems are compared and evaluated, and proposals are made to standardize the use of various signs, numerals and letters in keratodont formulae. Nine standardized systems (seven all-cardinal and two cardinal-ordinal systems) are finally retained: these should cover all needs according to the kind of use and the level of precision required.     

Effects of light intensity on activity in four sympatric anuran tadpoles

Though light conditions are known to affect the development and anti-predation strategies of several aquatic species, relatively little is known about how different species react to light, or how light can affect these species during different points in their life-cycle. In this study, we used four sympatric anuran tadpoles(Bufo gargarizans, B. melanostictus, Pelophylax nigromaculatus and Microhyla fissipes) as animal system to examine species-specific activities of the underdoing different light intensity treatments, so as to better understand how they respond to light. We exposed four different species of tadpoles to 1660 and 14 lux light intensity treatments and then measured several parameters including development stage, body length and tail length, and as well as their basic activities. The results of this observation and analysis showed that the activities of tadpoles were significantly greater in B. gargarizans and B. melanostictus than in P. nigromaculatus and M. fissipes; and were also significantly greater during times of high light intensity as compared to during low light intensity. Moreover, the observed relationship between species and light intensity was significant. The activities of B. gargarizans and B. melanostictus tadpoles were greater in high light, while the activity of P. nigromaculatus tadpoles was greater in low light intensity, while M. fissipes tadpoles showed no differences in either low or high intensity light. Furthermore, the activities of B. gargarizans, B. melanostictus and M. fissipes tadpoles in terms of developmental stage, body size or tail length did not seem to differ with light intensity, but during early larval developmental period of P. nigromaculatus, the activity of tadpoles was negatively correlated with development stage, but irrelevant to either body size or tail length in different light intensities. These results lead us to conclude the observed activities of the four sympatric anuran tadpoles are closely correlated with their specific anti-predation strategies.     

Keratodont formulae in anuran tadpoles: proposals for a standardization1

The various systems proposed to describe concisely, in the form of a formula, the number and arrangement of keratodont rows in the oral disk of anuran tadpoles, are reviewed and classified. A distinction is made between individual and collective keratodont formulae. The different systems are compared and evaluated, and proposals are made to standardize the use of various signs, numerals and letters in keratodont formulae. Nine standardized systems (seven all-cardinal and two cardinal-ordinal systems) are finally retained: these should cover all needs according to the kind of use and the level of precision required.     

Food availability determines the response to pond desiccation in anuran tadpoles

Food availability and pond desiccation are two of the most studied factors that condition amphibian metamorphosis. It is well known that, when food is abundant, organisms undergo metamorphosis early and when they are relatively large. The capability of anurans to accelerate their developmental rate in response to desiccation is also common knowledge. These two variables must act together in nature, since we know that, as a pond dries, the per capita resources decrease. We conduct an experiment to evaluate the effects of desiccation and food availability separately and in combination in tadpoles of the painted frog (Discoglossus pictus). We demonstrate that food deprivation leads to slow growth rates, which delay metamorphosis and produce smaller size and weight. The capability to accelerate metamorphosis when facing a drying pond is also confirmed, but, nevertheless, with factor interaction (when the pool is drying and resources are scarce) the capacity to respond to desiccation is lost. In addition, slow drying rates are shown to be stressful situations, but not enough to provoke a shortening of the larval period; in fact, the larval period becomes longer. We also demonstrate that the interaction of these factors changes the allometric relationship of different parts of the hind limb, which has implications for the biomechanics of jumping. Due to low mortality rates and an adequate response to both environmental factors, we expect D. pictus to have a great invasive potential in its new Mediterranean distribution area, where lots of temporary and ephemeral ponds are present.     

Osmoregulatory-like mitochondria-rich cells in the developing pancreatic ducts of young anuran tadpoles

Pancreatic ducts of young posthatching Rana temporaria tadpoles are the main component of the developing pancreas. At this stage (free-swimming tadpoles with internal gills), duct cells display a high degree of development of basal and lateral outfoldings of the cell membrane with extensive interdigitation, and numerous mitochondria are present throughout the cytoplasm. Wide intercellular spaces also exist, sometimes forming canaliculi-like structures. Since these traits are characteristic of cells engaged in osmotic regulation, we suggest the possibility that this temporary duct system participates in such control. Duct cells in tadpoles with well-developed hindlegs have diminished interdigitation, and mitochondria are localized apically. © 1993 Wiley-Liss, Inc.     

Responses to competition effects of two anuran tadpoles according to life-history traits

Experimental manipulations of the densities of two larval anurans, Pelodytes punctatus and Bufo bufo , showed that these species compete asymmetrically in semi-natural conditions. Growth, mass at metamorphosis, date of metamorphosis, and survival were used as measures of response to interspecific competition. A mechanistic approach was used to collect information on the behaviour of the two species in different conditions. The competitive superiority of Pelodytes at individual level was correlated with a larger body, faster growth rate, increased per capita competitive impact on conspecifics, and greater reduction in the availability of trophic and spatial resources. In the presence of Pelodytes, Bufo showed slower growth, smaller size at metamorphosis and reduced survival. In the interspecific treatments Bufo individuals modified their behaviour by increasing activity and use of the water column while Pelodytes did not change their foraging activity or space use in the aquaria. However, the presence of Bufo resulted in a reduced larval period and smaller size at metamorphosis. We hypothesise that the presence of Bufo act as a signal of environmental degradation and shorten the larval period of Pelodytes, a typical temporal pond breeder . The smaller Bufo tadpoles are potentially stronger competitors at population level because they use relatively large amounts of energy (greater densities and higher metabolic rates). Consequently, they use larger proportions of the shared resources than their larger competitor. A possible evolutionary response for larger tadpoles is the development of interference mechanisms or "escaping" from ephemeral ponds where mortality by drying represent a high risk.     

Agropastoral activities increase fluctuating asymmetry in tadpoles of two neotropical anuran species

Agriculture and pasture activities are the main drivers for habitat reduction, directly affecting amphibian assemblages. In the Cerrado, the progress of agricultural and pasture areas negatively affects aquatic environments and their organisms, once the suppression of marginal vegetation reduces the natural protection against allochtone stressors. One possible way to measure the stress level is the Fluctuating Asymmetry (FA), which is calculated based on the deviations in the development of bilateral morphological traits of the organism. Herein, we evaluated whether environments with a higher degree of agropastoral influence and reduced marginal vegetation can increase FA levels in tadpoles of two common and widely distributed anuran species in the Cerrado (Physalaemus cuvieri and Scinax fuscomarginatus). We sampled and classified water bodies according to the percentage of agropastoral land use and marginal vegetation, and measured four morphological traits of tadpoles to evaluate the degree of FA. We found that in environments with intensive agropastoral land use, tadpoles of P. cuvieri and S. fuscomarginatus had higher FA in nostril‐snout distance (NSD). In environments with reduced marginal vegetation, tadpoles of S. fuscomarginatus had higher FA in eye width (EW), but no effect was detected for tadpoles of P. cuvieri. These morphological traits (i.e. nostrils and eyes) are associated to individual fitness of tadpoles. Thus, these developmental deviations can affect species fitness and population homeostasis over time, contributing to generate stochastic population dynamics and increasing the vulnerability of native species to local extinctions. The use of FA as a tool to measure environmental impact on species with potential to be used as bioindicators can contribute to generate and test hypothesis when integrated with long‐term studies.     

Autolysis in the tail muscles of metamorphosing tadpoles

Degradation of muscle homogenate from the metamorphosing tadpole tail of bullfrog, Rana catesbeiana, was examined at acid and neutral pHs. More rapid and complete degradation was observed at acid pH. Proteinases working at acid pH were not inhibited by pepstatin but were inhibited by leupeptin. However, the inhibition by leupeptin was enhanced by pepstatin. These results show that lysosomal proteinases, a thiol proteinase(s) rather than cathepsin D, are involved in the degradation of tail muscle proteins.     

Stage-dependent restoration of sensory dorsal columns following spinal cord transection in anuran tadpoles

In frogs sensory axons from the lumbar dorsal roots ascend in the dorsal column of the spinal cord to terminate in the medulla and cerebellum. The response of these axons to complete transection of the thoracic spinal cord has been analysed in Rana temporaria tadpoles at different stages of development. The presence and position of dorsal column axons were assessed by using the anterograde transport of horseradish peroxidase or by electrophysiological methods. Before developmental stage VIII, dorsal column axons can grow across the transection and reach their normal areas of termination in the brainstem. Axons that do cross the transection follow their normal pathways. From stage VIII onwards this capacity for growth is largely lost. These results are discussed in terms of the relation between neurogenesis, axon growth and axonal regeneration.     

Sequence of ontogenetic development and atrophy of the oral apparatus of six anuran tadpoles

The development of the oral structures of six species of anuran tadpoles with four different types of mouth parts and the metamorphic atrophy of these structures in two species with different mouth parts are described. The oral labia of typical tadpoles, oral flaps of microhylids, and lateral oral folds of Rhinophrynus are assumed to be homologous. We also suggest that the barbels of the tadpoles of Rhinophrynus are homologs of the marginal papillae of species with an oral disc. Developmental patterns and sequences of the oral structures of all tadpoles examined follow a common pattern: stomodeal invagination, oral pad development, jaw sheeth delimitation, tooth row ridge development, jaw sheath keratinization, and labial tooth keratinization. Developmental patterns remain constant, while interspecific differences are apparent because of truncations of ontogeny at specific stages. Metamorphic atrophy of oral structures occurs roughly in the reverse order of development, although the procedure is rapid and more haphazard than development.     

Predator-avoidance behavior in anuran tadpoles: a new bioassay for characterization of water-soluble cues

Most surveys of large wood in streams are conducted by counting and measuring every piece of large wood within a reach, a technique that is effective but time-consuming. In this study we evaluated an alternative method that takes less time and can be employed in studies in which an estimate of total large wood volume along a stream reach is the primary metric of interest. In first- through third-order streams we estimated in-stream large wood volume and large wood frequency, comparing large wood census estimates to those from a modified a line-intercept technique that has been commonly used in terrestrial forest surveys. Estimates of large wood volume from line transects located in the geographic center of the stream (parallel to stream axis and equidistant from bankfull margins) were highly correlated with those from the wood census (P < 0.001, r ² = 0.88, Pearson’s r = 0.935), but produced slightly greater estimates of large wood volume (regression slope = 1.28, SE = 0.16). Line-intercept estimates of large wood frequency (number per 100 m of stream) were significantly correlated to the wood census counts, but the line-intercept method underestimated frequency by about 50% (P = 0.016). Differences in the estimated large wood volume between line-intercept and wood census surveys were associated with variability in the diameter of the large wood, but unrelated to stream bankfull width, for the range of stream sizes evaluated in this study (≈ 2 to 11 m). Our results suggest that in small constrained streams, line-intercept surveys are an effective method for estimating in-stream large wood volume and that these estimates better approximate results from whole-stream census techniques where the diameter of in-stream wood is relatively consistent. Handling editor: K. Martens