Morphology and feeding in tadpoles of Ceratophrys cranwelli (Anura: Leptodactylidae)

This paper provides data on the skeleton, musculature, buccal apparatus, buccopharyngeal cavity and diet of Ceratophrys cranwelli tadpoles, and attempts to contribute to the knowledge of relations between morphology and ecology in anuran larvae. Both in morphological characters and feeding habits, these tadpoles are very similar to other species within the genus. They possess many of the structural features usually found in predaceous tadpoles: strong, keratinized jaw sheaths and keratodonts, reduced buccal papillation, high values of in‐lever arm proportion and buccal floor area, well‐developed ceratohyals, and hypertrophied jaw muscles. Food sources consist of other tadpoles, microcrustaceans, larvae of insects, plant fragments, as well as rotifers and microalgae. As facultative carnivores, they are likely to play an important role in regulating the aquatic communities of the ephemeral ponds where they develop.     

Functional response of suspension feeding anuran larvae to different particle sizes at low concentrations (Amphibia)

The influence of particle size, initial particle concentration and larval stage on the ingestion rate, ‘retention efficiency’, and filtering rate of anuran larvae with varying filter apparatus anatomy and different life histories was investigated for four species. Larvae of premetamorphic Stages 28 and 32 and prometamorphic Stage 40 were selected for filtering experiments on the basis of their different growth rates. Three different sizes of silica gel particles were offered as mock food. Particle concentration was measured photometrically. The Michaelis-Menten model was used to describe the dependency of ingestion rate, filtering rate, and ‘retention efficiency’ upon initial particle concentration, and to calculate maximum ingestion rate, threshold concentration, and the half-saturation constant. (1) The highest ingestion rates, filtering rates and ‘retention efficiencies’ were achieved by Xenopus laevis larvae, followed by Bufo calamita larvae. Bufo bufo larvae lay at the opposite end of the scale. Rana temporaria larvae were placed between B. calamita and B. bufo larvae. This order is attributed to differences in life histories, especially the different breeding environments in which these larvae occur. (2) The larger the particle size and the older the stage, the greater the tendency toward saturation of the ingestion rate, filtering rate and ‘retention efficiency’. These filtration parameters are graded according to particle size. The ingestion rate (number of particles), filtration rate and ‘retention efficiency’ are greatest for PS3. Ingestion volume is greatest for PS 1. The difference between PS3 and PS2 on the one hand, and PS1 on the other, is often great; for Stage 28 X. laevis it is very great. This shows that larvae ingest large particles more effectively, and that the most effective ingestion takes place at Stages 28 and 32, owing to the growth function of these stages. The ability of larvae to ingest large particles effectively is possibly a very basic phylogenetic characteristic. (3) The threshold concentration is lowest when the particles are at their largest. In accordance with conclusions drawn by other authors, threshold feeding is attributed to regulation by buccal pumping and mucus production. Considerable importance is attributed to threshold feeding with respect to larval adaptation to oligotrophic environments.     

Functional morphology of feeding and gill irrigation in the anuran tadpole: electromyography and muscle function in larval Rana catesbeiana

This study provides the first data on muscle activity patterns during active feeding in a larval anuran. Data regarding muscle function during gill irrigation and hyperexpiration are also provided. Electromyographic and kinematic data were recorded from six mandibular and hyoid muscles in unanesthetized, unrestrained larvae of Rana catesbeiana. Only three (hyoangularis, orbitohyoideus, anterior interhyoideus) of the six muscles examined are active during gill irrigation. Feeding cycles are characterized by the recruitment of three additional muscles: intermandibularis, suspensorioangularis, and levator mandibulae longus superficialis. The latter two contribute, respectively, to wide opening and forceful closing of the mouth during feeding. Hyperexpiration is characterized by a reversal of water flow anteriorly out of the mouth. This hydrodynamic change occurs due to modulation of the timing of firing of the anterior interhyoideus, as well as recruitment of the posterior interhyoideus, which is only active during hyperexpiration. Both regions of the interhyoideus, which are responsible for evacuation of the buccal cavity, are active during the opening phase of hyperexpiration. Kinematically, transitioning from gill irrigation to feeding involves both an overall shortening of the gape cycle and a shift in the relative length of opening phase vs. closing phase. Our results corroborate many of the findings of Gradwell ([1972] Can J Zool 50:501-521) regarding muscle function during gill irrigation and hyperexpiration. Furthermore, we demonstrate that in larval anurans the transition from gill irrigation to feeding involves modulation of gape cycle kinematics, changes in the level of activity of muscles, and recruitment of muscles that are not active during irrigation. In light of new data presented here, a review of muscle function in tadpoles is also provided.     

Visual cues contribute to predator detection in anuran larvae

The ability of prey to detect predators directly affects their probability of survival. Chemical cues are known to be important for predator detection in aquatic environments, but the role of other potential cues is controversial. We tested for changes in behaviour of Rana temporaria tadpoles in response to chemical, visual, acoustic, and hydraulic cues originating from dragonfly larvae (Aeshna cyanea) and fish (Gasterosteus aculeatus). The greatest reduction in tadpole activity occurred when all cues were available, but activity was also significantly reduced by visual cues only. We did not find evidence for tadpoles lowering their activity in response to acoustic and hydraulic cues. There was no spatial avoidance of predators in our small experimental containers. The results show that anuran larvae indeed use vision for predator detection, while acoustic and hydraulic cues may be less important. Future studies of predator‐induced responses of tadpoles should not only concentrate on chemical cues but also consider visual stimuli. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ??, ??–??.     

Morphological and biomechanical changes of the feeding apparatus in developing southern flounder,Paralichthys lethostigma

The feeding biomechanics of premetamorphic, metamorphic, and postmetamorphic southern flounder, Paralichthys lethostigma, were investigated to better understand the origin and design of adult pleuronectiform feeding mechanisms. Larval P. lethostigma were sampled from culture tanks every day from first feeding through metamorphosis. Fish were then fixed, cleared, and double stained for cartilage and bone. Postmetamorphic juvenile and adult fish were obtained from aquaculture facilities, fixed, and the muscles and bones of the head dissected. All fish were digitally photographed from both sides of the head. Measurements from digital images included head depth, head length, and quadratal angle (a measure of articular‐quadrate position). Measurements were also made of closing in‐lever, opening in‐lever, and out‐lever moment arm lengths for the determination of lower jaw opening and closing mechanical advantage. In premetamorphic larvae, quadratal angle increased from 40° to 80°, opening lever ratio increased from 0.10 to 0.37, and closing lever ratio increased from 0.06 to 0.40. From these measurements and observations of cleared and double‐stained specimens, it was determined that lower jaw depression and elevation changed from a hyoid‐based to an opercular‐based mechanism prior to the onset of metamorphosis. With migration of the right eye to the left side of the head, quadratal angle remained relatively unchanged at 72° to 84°, opening lever ratio decreased from a high of 0.32 to a low of 0.14, and closing lever ratio decreased to as low as 0.17. Postmetamorphic fish exhibited little change with a quadratal angle of 83° to 84°, an opening lever ratio of 0.19, and a closing lever ratio of 0.17 to 0.19. Paired measurements made on the left (ocular) and right (blind) sides of the head indicated that quadratal angle was asymmetrical during metamorphosis (P = 0.003, α = 0.017). Mechanical advantage for lower jaw elevation was also bilaterally asymmetrical following metamorphosis (P = 0.002, α = 0.013). Because mechanical advantage for lower jaw depression was not directionally asymmetrical in metamorphic or postmetamorphic P. lethostigma, functional asymmetry (lateral jaw flexion) is not predicted for jaw opening. These results suggest differences in the design and function of feeding mechanisms for premetamorphic, metamorphic, and postmetamorphic P. lethostigma. J. Morphol., 2008. © 2008 Wiley‐Liss, Inc.     

Suspension feeding of anuran larvae at low concentrations of Chlorella algae (Amphibia,Anura)

Summary Ingestion and filtering rates in larval Xenopus laevis, Bufo calamita, Rana temporia and Bufo bufo fed suspensions of Chlorella fusca were investigated. Concentrations were measured with a Coulter Counter. (1) For all species, filtration occurred at concentrations far below those reported by other authors for Rana sylvatica feeding on Chlorella pyrenoidosa. For Bufo bufo, only larvae near metamorphosis showed ingestion at low particle concentrations. Since buccopharyngeal ventilation continues even in the absence of food particles, this threshold feeding behaviour in the younger larvae must be due to different mechanisms to those found in Daphnia and Calanus studied by other authors: probably reduction of the buccal pumping rate and the mucus production of the filter apparatus. (2) For B. calamita, R. temporaria and X. laevis the highest suspension feeding efficiency was at early tadpole stages, corresponding with the high growth rate of these stages. (3) The life histories of the species provide the basis for understanding their different retention efficiencies and functional responses.Supported by the Deutsche Forschungsgemeinschaft-DFG     

Carnivory and resource-based niche differentiation in anuran larvae: implications for food web and experimental ecology

1.  Food webs represent the paths of material and energy flow through organisms in an ecosystem. Anuran larvae are important components of pond food webs: they are abundant, consume large quantities of food and serve as prey for many organisms. However, there are very basic uncertainties about the feeding ecology of anuran larvae; for instance, as to which trophic level they belong and whether species differ in resource use. Because anuran larvae have been employed in model systems in experimental ecology for decades, these uncertainties could lead to misinterpretation of published experiments, or inadequate designs of experiments directed at general, conceptual issues in ecology.
2.  Using ¹³C and ¹⁵N stable isotope and gut content analyses of free-ranging and enclosed tadpoles of four ranid species ( Lithobates sylvaticus , L. pipiens , L. clamitans , L. catesbeianus ) in the food webs of six wetlands, we tested the following null hypotheses: (i) that anuran larvae are strict primary consumers; (ii) that they are non-selective feeders and therefore exhibit little feeding niche differentiation; (iii) that they are opportunistic consumers and (iv) that their diet remains unchanged through ontogeny.
3.  All four species consumed and assimilated substantial amounts of animal food; bullfrog larvae, in particular, appear to be predatory. Significant feeding niche differentiation among species occurred with respect to the sources of carbon, consumption of animal matter and nutritional quality of food ingested. We further documented opportunistic feeding habits and ontogenetic shifts in diet.
4.  Collectively, these studies revealed complex trophic relationships that might require a reconsideration of the role of anuran larvae in pond food webs, as well as a reinterpretation of results of previous studies employing anuran larvae in model experimental systems.     

Neotropical tadpoles influence stream benthos: evidence for the ecological consequences of decline in amphibian populations

1. Few studies have assessed the role of tadpoles in tropical streams, although they are often abundant and conspicuous components of these systems. Moreover, amphibian populations are declining around the globe, particularly stream‐dwelling species in tropical uplands, and the ecological consequences of these losses are not understood. 2. We chose a stream in the central Panamanian highlands, which has an intact fauna of stream‐breeding anurans, to examine the ecological consequences of amphibian losses. This site differs dramatically from sites in nearby western Panama and Costa Rica where anuran diversity and abundance have declined greatly in the last two decades. 3. We used an underwater electric field to create tadpole exclosures in runs, so that we could evaluate their influence on sediment dynamics and the abundance and community structure of algae and aquatic insects. Tadpoles reduced total sediments and both organic and inorganic fractions on substrata. Tadpoles also reduced algal abundance on substrata by approximately 50% and decreased algal biovolume. Gut content analyses showed that tadpoles consumed algae and sediments and we could see that algae and sediments were also displaced through bioturbation. 4. Atelopus zeteki, Rana warszewitschii, and Hyla spp. were the dominant larval anurans responsible for the effects observed. Visual surveys indicated that the densities of these taxa ranged from 23 (R. warszewitschii and Hyla spp. combined) to 43 m^?2 (A. zeteki) in runs. 5. The abundance of baetid mayflies was lower in tadpole exclosures compared with controls, and this was attributed to tadpoles facilitating mayfly feeding by removing sediments and exposing underlying periphyton. 6. Tadpoles affect the abundance and diversity of basal resources and other primary consumers, and thus influence food web dynamics and energy flow in these tropical streams. Catastrophic decline in stream‐breeding anuran populations will influence the structure and function of neotropical stream ecosystems.     

Prey detection of aquatic predators: Assessing the identity of chemical cues eliciting prey behavioral plasticity

Chemical cues transmitted through the environment are thought to underlie many prey responses to predation risk, but despite the known ecological and evolutionary significance of such cues, their basic composition are poorly understood. Using anuran tadpoles (prey) and dragonfly larvae (predators), we identified chemical cues associated with predation risk via solid phase extraction and mass spectrometry of the extracts. We found that dragonfly larvae predators consistently produced a negative ion, m/z 501.3, when they fed on bullfrog (Rana catesbeiana) and mink frog (Rana septentrionalis) tadpoles, but this ion was absent when dragonflies were fasted or fed invertebrate prey. When tadpole behavioral responses to dragonfly chemical cues were examined, tadpoles reduced their activity, particularly in response to dragonflies feeding on tadpoles. Furthermore, a negative correlation was noted between the level of tadpole activity and the concentration of the m/z 501.3 compound in dragonfly feeding trials, indicating that this ion was possibly responsible for tadpole anti-predator behavior.     

昆嵛林蛙蝌蚪口器结构的研究

本文对昆嵛林蛙(Rana kunyuensis)的蝌蚪口部外形和口咽腔形态结构进行了观察,并与长肢林蛙进行了比较。结果表明它们有着基本相似的形态特征,但也存在明显的差别:昆嵛林蛙蝌蚪的上唇齿比长肢林蛙少一行;昆嵛林蛙蝌蚪口腔内突起数量明显少于长肢林蛙;昆嵛林蛙腺区不明显,而长肢林蛙腺区明显。     

Quantitative comparative analysis of the nasal chemosensory organs of anurans during larval development and metamorphosis highlights the relative importance of chemosensory subsystems in the group

The anuran peripheral olfactory system is composed of a number of subsystems, represented by distinct neuroepithelia. These include the main olfactory epithelium and vomeronasal organ (found in most tetrapods) and three specialized epithelia of anurans: the buccal‐exposed olfactory epithelium of larvae, and the olfactory recess and middle chamber epithelium of postmetamorphic animals. To better characterize the developmental changes in these subsystems across the life cycle, morphometric changes of the nasal chemosensory organs during larval development and metamorphosis were analyzed in three different anuran species (Rhinella arenarum , Hypsiboas pulchellus , and Xenopus laevis ). We calculated the volume of the nasal chemosensory organs by measuring the neuroepithelial area from serial histological sections at four different stages. In larvae, the vomeronasal organ was relatively reduced in R. arenarum compared with the other two species; the buccal‐exposed olfactory epithelium was absent in X. laevis , and best developed in H. pulchellus . In postmetamorphic animals, the olfactory epithelium (air‐sensitive organ) was relatively bigger in terrestrial species (R. arenarum and H. pulchellus ), whereas the vomeronasal and the middle chamber epithelia (water‐sensitive organs) was best developed in X. laevis . A small olfactory recess (likely homologous with the middle chamber epithelium) was found in R. arenarum juveniles, but not in H. pulchellus . These results support the association of the vomeronasal and middle chamber epithelia with aquatic olfaction, as seen by their enhanced development in the secondarily aquatic juveniles of X. laevis . They also support a role for the larval buccal‐exposed olfactory epithelium in assessment of oral contents: it was absent in X. laevis , an obligate suspension feeder, while present in the two grazing species. These initial quantitative results give, for the first time, insight into the functional importance of the peripheral olfactory subsystems across the anuran life cycle.     

The mechanism of breathing in the South Asmerican lungfish, Lepidosiren paradoxa; radiological study

In filling the lungs by means of the buccal "force-pump", air drawn into the buccal cavity by the lowering of the floor of the mouth is forced into the lungs when the mouth is firmly closed and the buccal floor raised. This mechanism depends on the ability of the fish to prevent air being forced out of the mouth through the lips and it is shown that the tongue is pressed against the roof of the mouth to form a seal. Radiologically it has been shown that the hyoid apparatus ("ceratohyal" of some authors) plays a large part in the movements necessary to draw air into the mouth, seal it in and force it into the lungs. Another skeletal element involved is the pectoral girdle which makes considerable movements in association with the filling of the lungs. Expiration of the air from the lungs, which as shown by radiographs may be remarkably complete, is brought about by the elasticity of the lung tissue.     

Toxicity of an Anionic Detergent to the Spawn and Larvae of Anurans (Amphibia)

Several experiments were performed to test the toxicity of FIT, a washing-up and general cleaning liquid containing about 10 % sodiumalkanemonosulfonate (industrial name E 30) to spawn and larvae of anura. The LC₅₀ values for spawn were between 1.62 × 10⁻³ % (Rana dalmatina) and 4.97 × 10⁻³ % (Rana temporaria). The sensitivity of anuran larvae depends on the concentration and duration of exposure to the detergent as well as on the developmental and differentiation stage of the organisms. The toxicity of FIT is not due solely to the alkanesulfonate it contains, but results from the joint action of the surfactant, polyphosphates and solvents. The results indicate that detergents may be harmful to the amphibian fauna of Central Europe.     

Comparative and developmental functional morphology of the jaws of living and fossil gars (Actinopterygii: Lepisosteidae)

The feeding mechanism of gars (Ginglymodi : Lepisosteidae) is characterized by cranial elevation and lower jaw rotation but minimal cranial kinesis. Gar jaws have numerous, sharply pointed, elongate teeth for capture of evasive prey. Their mandibles range from relatively short to extremely long depending on the species. Jaw length and lever dimensions were hypothesized to affect the biomechanics of force and motion during feeding, according to simple mechanical models of muscles exerting force through first- or third-order levers. A morphometric protocol was used to measure the jaw structure of seven living and five fossil species of gar and these data were used to calculate the mechanical advantage (a measure of force transmission) for both opening and closing of the mandible. Gars were found to possess low mechanical advantage (MA) and high transmission of motion, although gars occupy a range of biomechanical states across the continuum of force vs. velocity transmission. The long-nose gar, Lepisosteus osseus, has one of the lowest jaw closing MAs (0.05) ever measured in fishes. Intraspecific lever mechanics were also calculated for a developmental series (from feeding larvae to adults) of L. osseus and Atractosteus spatula. A characteristic ontogenetic curve in MA of the lower jaw was obtained, with a large decrease in MA between larva and juvenile, followed by a steady increase during adult growth. This curve correlates with a change in prey type, with the small, robust-jawed individuals feeding mainly on crustaceans and insects and the large, long-jawed individuals of all species becoming mainly piscivorous. Principal components analysis of functionally important morphometrics shows that several gar species occupy different regions of functional morphospace. Some fossil gar species are also placed within functional morphospace using this approach.     

A tadpole-induced polyphenism in the salamander Hynobius retardatus

Abstract.— Larvae of the salamander Hynobius retardatus have two distinct morphs: normal and broad-headed, cannibal morphs. We performed three experiments to differentiate among the following hypotheses: The broad-headed morph is induced to allow: (1) feeding on nutritious conspecifics; (2) exclusion of strong competitors for food or space; or (3) feeding on large, tough prey when smaller prey items are unavailable. When newly hatched larvae were reared with a heterospecific, Rana pirica (an anuran amphibian) tadpoles, the broad-headed morph was induced more frequently compared with those reared with conspecifics. The phenotype expressed depended on the size of the tadpoles: The broad-headed morph occurred more frequently with small and the normal morph with large tadpoles. Metamorphosis occurred sooner in larvae fed conspecifics compared with those fed heterospecific tadpoles, and the mean growth rate of larvae fed conspecifics was significantly faster than that of those fed tadpoles, suggesting that the heterospecific tadpoles were less nutritive than the conspecifics. These results do not support the hypotheses that the broad-headed morph evolved for consuming conspecifics because of their better balance of nutrients or for excluding strong competitors for food or space. We tentatively conclude that the morph evolved to eat large, tough prey, including both conspecifics and heterospecific tadpoles. Because H. retardatus usually spawns very early in the spring in small ponds partially covered with ice and snow, newly hatched larvae may starve from the lack of proper food owing to extremely low water temperatures. Thus, the broad-headed morph of H. retardatus may represent a cold-habitat adaptation to overcome the severe circumstance when the only food items available are relatively large conspecifics or heterospecific tadpoles.     

Lateralized Turning Biases in Two Neotropical Tadpoles

Lateralized turning behavior in startle responses and upon descent after surfacing for a breath of air has been documented for tadpoles in several anuran species. A left‐handed preference is most common and was previously thought to be linked to the asymmetry in spiracle location. Here, we investigate the presence of behavioral asymmetries in tadpoles of Agalychnis callidryas and Leptodactylus melanonotus in explosive turns after air‐breathing. Data were also collected on lateralized posture in the orientation of tails of embryonic A. callidryas within the egg case, as well as the startle response of free‐swimming tadpoles exposed to mechanical stimulation. A left‐curled tail bias was found among several clutches from Costa Rica, but this was not the case among clutches examined from Panama. Free‐living tadpoles of L. melanonotus displayed a distinct right‐handed preference during explosive turns. While some tadpoles of A. callidryas were at stages too early to detect any explosive turns when breathing, later‐staged individuals did display a left‐handed bias in startle response to mechanical stimulation. Additionally, it appears that the expression of behavioral lateralization of larvae (but not embryos) may predict whether or not the adults exhibit similar lateralization. Findings herein provide insight into the ontogeny and evolutionary origins of lateralized behavior in anurans.     

The morphology of amphibian skin vascularization before and after metamorphosis

Summary The skin vascularization was investigated troughout the ontogenetic development and in adults of two anurans, Rana temporaria and Bufo bufo, and two urodeles, Triturus vulgaris and Triturus cristatus. It was found that, contrary to the urodele larvae, the anuran tadpoles have a very sparse skin vascularization. During the early stages of anuran metamorphosis the skin capillary network becomes dense; later, during skin metamorphosis, a second, venous, network is formed as anastomoses between the subcutaneous vein ramifications. In the urodeles, metamorphosis is not accompanied by any significant morphological changes in the skin vascularization, and a subcutaneous network is not formed. It is suggested that the reduced skin vascularization in anuran tadpoles is an advanced larval character relative to the rich vascularization of the skin in urodele larvae. It is further suggested that anuran tadpoles have a reduced ability to utilize gaseous exchange through the skin. The function of the subcutaneous venous network found in anurans after metamorphosis is obscure; experiments indicate a vasomotor regulation which is neither adrenergic nor cholinergic.Abbreviations a arteriole - A artery - an anastomosis between the subepidermal capillary network and the subcutaneous venous network - C stratum compactum - E epidermis - ec subepidermal capillaries - S stratum spongiosum - sv subcutaneous venous network - v venule - V vein - vc venae comitantes