Ranid Tadpoles Research Articles

Stress hormone-mediated antipredator morphology improves escape performance in amphibian tadpoles

Complete functional descriptions of the induction sequences of phenotypically plastic traits (perception to physiological regulation to response to outcome) should help us to clarify how plastic responses develop and operate. Ranid tadpoles express several plastic antipredator traits mediated by the stress hormone corticosterone, but how they influence outcomes remains uncertain. We investigated how predator-induced changes in the tail morphology of wood frog (Rana sylvatica) tadpoles influenced their escape performance over a sequence of time points when attacked by larval dragonflies (Anax junius). Tadpoles were raised with no predator exposure, chemical cues of dragonflies added once per day, or constant exposure to caged dragonflies crossed with no exogenous hormone added (vehicle control only), exogenous corticosterone, or metyrapone (a corticosteroid synthesis inhibitor). During predation trials, we detected no differences after four days, but after eight days, tadpoles exposed to larval dragonflies and exogenous corticosterone had developed deeper tail muscles and exhibited improved escape performance compared to controls. Treatment with metyrapone blocked the development of a deeper tail muscle and resulted in no difference in escape success. Our findings further link the predator-induced physiological stress response of ranid tadpoles to the development of an antipredator tail morphology that confers performance benefits.

Consumption of the eggs, hatchlings, and tadpoles of Green Frogs (Lithobates clamitans) by native and non-native predators

Abstract Predation by native and non-native predators on the eggs, embryos, and early stage tadpoles can affect the recruitment of offspring into a population. We examined the effects of native (Little Brown Mudbugs, Cambarus thomai; overwintered Rana tadpoles; Common Green Darner, Anax junius, larvae) and non-native (Western Mosquitofish, Gambusia affinis) potential predators on the eggs, hatchlings, and early tadpoles of the Green Frog (Lithobates clamitans). The predators had no effect on survivorship or hatching of L. clamitans eggs. However, tadpole survivorship was significantly reduced by dragonfly larvae and crayfish, but not G. affinis or the overwintered ranid tadpoles. Our observation that invertebrates consumed Green Frog tadpoles while vertebrates did not is consistent with palatability contributing to the tadpoles’ susceptibility to different predators. Our results therefore suggest Green Frog tadpoles, but not eggs or embryos, from some populations may be subject to differential predation by invertebrate and vertebrate predators.

Seasonal and plant specific vulnerability of amphibian tadpoles to the invasion of a novel cyanobacteria

Aetokthonos hydrillicola (Ah) is a newly described cyanobacteria that forms dense colonies on aquatic macrophytes, primarily invasive Hydrilla verticillata, and is associated with mortality of freshwater wildlife. Prior research shows that Ah growing on Hydrilla is potently toxic to waterbirds, turtles, and fish, suggesting potentially broad sensitivity among vertebrates. We tested whether amphibian tadpole species were affected by ingestion of Ah-positive Hydrilla, and whether season, host plant, or tadpole age/size affected tadpole vulnerability. For trials involving ranid tadpoles (Bullfrogs, Rana catesbeiana; Green frogs, R. clamitans; and Southern leopard frogs, R. sphenocephala), feeding on Ah-positive Hydrilla collected during October–November resulted in the development of lesions within brain tissue and significant mortality. Ranid tadpole sensitivity to Ah toxin did not vary with age or size, but vulnerability from ingestion of Ah-positive Hydrilla varied seasonally and between two syntopic host plants. An unexpected result of our study was the apparent insensitivity of Green treefrog tadpoles (Hyla cinerea) fed toxic, Ah-positive Hydrilla. In conjunction with other studies, our results confirm wide but variable sensitivity among major vertebrate lineages to the Ah toxin. Differential sensitivity among species means that the introduction of Ah could alter interactions and structure within aquatic communities.

The frog inner ear: picture perfect?

Many recent accounts of the frog peripheral auditory system have reproduced Wever's (1973) schematic cross-section of the ear of a leopard frog. We sought to investigate to what extent this diagram is an accurate and representative depiction of the anuran inner ear, using three-dimensional reconstructions made from serial sections of Rana pipiens, Eleutherodactylus limbatus and Xenopus laevis. In Rana, three discrete contact membranes were found to separate the posterior otic (=endolymphatic) labyrinth from the periotic (=perilymphatic) system: those of the amphibian and basilar recesses and the contact membrane of the saccule. The amphibian 'tegmentum vasculosum' was distinguishable as a thickened epithelial lining within a posterior recess of the superior saccular chamber. These features were also identified in Eleutherodactylus, but in this tiny frog the relative proportions of the semicircular canals and saccule resemble those of ranid tadpoles. There appeared to be a complete fluid pathway between the right and left periotic labyrinths in this species, crossing the cranial cavity. Xenopus lacks a tegmentum vasculosum and a contact membrane of the saccule; the Xenopus ear is further distinguished by a lateral passage separating stapes from periotic cistern and a more direct connection between periotic cistern and basilar recess. The basilar and lagenar recesses are conjoined in this species. Wever's diagram of the inner ear of Rana retains its value for diagrammatic purposes, but it is not anatomically accurate or representative of all frogs. Although Wever identified the contact membrane of the saccule, most recent studies of frog inner ear anatomy have overlooked both this and the amphibian tegmentum vasculosum. These structures deserve further attention.

Common reed (Phragmites australis) invasion and amphibian distribution in freshwater wetlands

Invasive plants can substantially modify wetland structure and animal distribution patterns. In eastern North America, a Eurasian haplotype of the common reed (Phragmites australis, haplotype M) is invading wetlands. We studied the invasion of common reed in freshwater wetlands of an urbanized landscape and its effects on the distribution of amphibians at different life stages. Specifically, we hypothesized that the probability of reed invasion would be greatest in wetlands near anthropic disturbances. We predicted that the probability of desiccation at sampling stations increases with reed cover. Furthermore, we expected that wetlands invaded by common reed would have lower amphibian abundances, apparent survival, and rates of recruitment. We conducted trapping surveys to compare anuran assemblages of tadpoles, juveniles, and adults in 50 wetlands during two field seasons. The probability of reed invasion in wetlands increased with the cover of heavily-managed areas within 1,000 m and the distance to the nearest forest, but decreased with the length of roads within 1,000 m. The probability of station desiccation increased with reed cover. We found no evidence of a negative effect of reed presence on anuran population parameters, at any life stage. Landscape variables, such as the percent cover of forest or heavily-managed areas within a given radius from each wetland, influenced the abundance or the apparent survival of juvenile frogs and the abundance of ranid tadpoles. Our results show that amphibian patterns depend more strongly on the structure of the landscape surrounding wetlands than on exotic reed invasion in wetlands.

Fish Influences on Amphibian Presence and Abundance in Prairie and Parkland Landscapes of Minnesota, USA

Many amphibian populations are declining, and increased understanding of the drivers of amphibian presence and abundance will help in their conservation. In 2005 and 2006 we estimated relative abundance of larvae of two common amphibian taxa, Tiger Salamanders (Ambystoma tigrinum) and ranid tadpoles (Northern Leopard Frog Lithobates pipiens and Wood Frog Lithobates sylvaticus), in 75 shallow lakes in prairie and parkland areas in Minnesota. We used a two-step procedure in which we first modeled presence-absence with data from all lakes and then modeled abundance only in lakes where the amphibian taxa were present. For the two amphibian taxa, a generalized linear mixed effects model was used to examine the effects of dynamic factors like fish abundance and static (timeframe of study) variables like fish community type, depth, and adjacent land cover. Fish variables had the greatest influence but differed for the presence and abundance models. Salamander and tadpole presence was inversely correlated to the abundance of benthivorous fish, while salamander abundance was best explained by total fish abundance and tadpole abundance by fish community type. We did not detect influences of land cover types on the amphibian taxa we surveyed. Our findings are important because they complement previous studies documenting that negative correlations with fish extend beyond piscivores to include both planktivores and benthivores. Hydrological changes in our study landscape (e.g., installation of drainage networks, wetland consolidation) associated with agriculture and other land uses have likely increased the distribution and abundance of fish populations, thus dampening amphibian breeding success.

Distribution and Reproductive Strategies of Gyrinicola batrachiensis (Oxyuroidea: Pharyngodonidae) in Larvae of Eight Species of Amphibians From Nebraska

In total, 462 tadpoles and salamander larvae of 8 species were examined for the presence of Gyrinicola batrachiensis from 5 locations in Nebraska. Infection by G. batrachiensis occurred in tadpoles of Rana blairi , Rana catesbeiana, Rana pipiens, and Bufo woodhousii. Tadpoles of Hyla chrysoscelis , Spea bombifrons, and Pseudacris maculata and larvae of Ambystoma mavortium were not infected with G. batrachiensis. Population structure, defined as prevalence, mean abundance, and mean intensity of G. batrachiensis, varied among tadpoles of different amphibian species and was determined by collection locality, developmental period of tadpole hosts, amphibian species co-occurrence, and different reproductive strategies of G. batrachiensis , or a combination. Gyrinicola batrachiensis observed in all ranid tadpoles and B. woodhousii tadpoles from where bufonids were the only anuran species present, confirmed to the didelphic haplodiploidy and monodelphic parthenogenetic reproductive strategies, respectively. However, tadpoles of B. woodhousii that co-occurred with tadpoles of R. pipiens at Cedar Creek were inconsistent with these predictions and contained both male and didelphic female nematodes, but at a low mean intensity (1.61 ± 0.70). Didelphic female nematodes from B. woodhousii tadpoles at Cedar Creek only produced thick-shelled eggs, whereas nematodes in R. pipiens tadpoles had a high mean intensity (14.88 ± 23.83) from this location and contained both thick-shelled and thin-shelled eggs in their respective uteri. More importantly, adult female nematodes from tadpoles of R. pipiens and B. woodhousii from Cedar Creek were morphologically more similar to each other than to female nematodes recovered from tadpoles of other anuran species, other locations, or both. These data suggest that when strains of G. batrachiensis are shared by tadpoles of different amphibian species that differ in developmental period, the nematodes have an intermediate reproductive strategy in amphibian species, with tadpoles having short development.

Characterization of chemical defenses in ranid tadpoles against a fish predator

Tadpoles of some ranid species appear to possess chemical defenses against fish predators, but the chemicals have not been characterized. Here, we evaluated the vulnerability of three Japanese anuran tadpole species (Glandirana rugosa, Pelophylax nigromaculatus, and Hyla japonica) to a fish (Gnathopogon elongatus elongatus) and analyzed the defensive chemicals extracted from the unpalatable tadpoles. Additionally, we examined the defensive behavior of unpalatable tadpoles in response to fish chemical cues. The fish rejected both G. rugosa (83%) and P. nigromaculatus (48%), but not H. japonica (0%). Many of the rejected tadpoles survived (60–80%). Possible defensive chemicals were extracted by methanol from the skin of G. rugosa, but were not identifiable by gas chromatography–mass spectrometry because of small quantities. The chemicals have high polarity and non-volatility. When exposed to fish chemical cues, P. nigromaculatus decreased activity presumably as a defensive behavior, but G. rugosa did not. We demonstrated the presence of chemical defenses in at least two of these species and revealed that G. rugosa releases more effective or greater amounts of defense chemicals than P. nigromaculatus with respect to this fish predator. The increased efficacy of chemical defenses may correlate with decreasing defensive behavior.

Effects of malathion on embryonic development and latent susceptibility to trematode parasites in ranid tadpoles

We investigated the effects of embryonic exposure to the widely used organophosphate malathion (15-600 micro/L) on the early development and latent susceptibility of pickerel frog (Rana palustris) tadpoles to the trematode parasite Echinostoma trivolvis. The latent effects of contaminant exposure are rarely examined but could have important implications for individual survival and population viability. Malathion decreased hatching success by 6.5% and viability rates by 17% at 600 microg/L, which is a lower concentration than previously documented for anuran embryos. Incidence of malformations increased from 0.5% in controls to 11.2% in the 600-microg/L malathion treatment. The primary malformations documented in the two highest pesticide concentrations were ventralization and axial shortening. After seven weeks of development in water with no malathion, tadpoles previously exposed as embryos for only 96 h to 60 and 600 microg/L malathion suffered increased parasite encystment rates when compared to controls. Our research identifies embryonic development as a sensitive window for establishing latent susceptibility to infection in later developmental stages.

Dynamic visualization of the developing nervous system of the bullfrog, Rana catesbeiana

Anuran amphibians undergo a rapid and dramatic process of metamorphosis featuring widespread structural reorganization of the central nervous system. Although morphological changes during embryonic stages of anuran development have been well documented, much less information is available describing structural changes in the brain during larval (tadpole) stages. Using still images from cresyl-violet-stained material, we present an adaptation of the digital image and video manipulation technique of morphing that allows these images to be compiled in such a manner as to highlight key periods in tadpole brain development in a dynamic fashion. We present three morphed video data sets from ranid tadpoles that facilitate the identification of developmental changes in nuclear boundaries at different levels of the neuraxis. The use of animation allows dynamic examination of anatomical changes across long developmental spans without requiring additional anatomical preparations or specialized expensive equipment.

Exposure to the herbicide acetochlor alters thyroid hormone-dependent gene expression and metamorphosis in Xenopus Laevis.

A growing number of substances released into the environment disrupt normal endocrine mechanisms in a wide range of vertebrates. Little is known about the effects and identities of endocrine-disrupting chemicals (EDCs) that target thyroid hormone (TH) action, particularly at the cellular level. Frog tadpole metamorphosis depends completely on TH, which has led to the suggestion of a metamorphosis-based assay for screening potential EDCs. A major mechanism of TH action is the alteration of gene expression via hormone-bound nuclear receptors. To assess the gene expression profiles in the frog model, we designed a novel multispecies frog cDNA microarray. Recently, the preemergent herbicide acetochlor was shown to accelerate 3,5,3 -triiodothyronine (T3)-induced forelimb emergence and increase mRNA expression of thyroid hormone ss receptors in ranid tadpoles. Here we show that T3-induced metamorphosis of Xenopus laevis, a species commonly used in the laboratory, is accelerated upon acute exposure to an environmentally relevant level of acetochlor. The morphologic changes observed are preceded by alterations in gene expression profiles detected in the tadpole tail, and the nature of these profiles suggest a novel mechanism of action for acetochlor.

Turning Bias in Tadpoles

Turning Bias in Tadpoles

Field Response of Tadpoles to Conspecific and Heterospecific Alarm

AbstractMany organisms use chemical cues from a variety of sources to mediate predator avoidance. Response to heterospecific alarm cues has been demonstrated for tadpoles within but not among taxa and alarm response behavior has seldom been examined under field conditions. This study examined the response of three sympatric amphibian larvae and predaceous larval Dytiscus sp. (diving beetle) to damage‐release signals in natural ponds by using capture rates from treated funnel traps as an index of larval behavior. Hyla regilla (Pacific tree frog) tadpoles avoided traps treated with either crushed conspecifics or with Rana aurora (red‐legged frog) tadpoles but the larger ranids and Ambystoma macrodactylum (long‐toed salamander) did not respond to either treatment. H. regilla tadpoles were likely susceptible to any potential predators of ranid tadpoles in these ponds and this result is consistent with the hypothesis that a response to heterospecific alarm occurs in sympatric prey with shared predators.

Uptake of arsenic and metals by tadpoles at an historically contaminated Texas site

On 14 May 1994, tadpoles were collected from Lateral Pond and Municipal Lake in Bryan, Texas. These waters are immediately downstream from Finfeather Lake which was directly contaminated during 53 years of industrial production of arsenic (As)-based cotton defoliants. The tadpoles contained elevated levels of arsenic, chromium (Cr) and zinc (Zn). As far as it is known, the mean concentrations of As (6.87 p.p.m. wet weight) and Cr (6.91 p.p.m. wet weight) in cricket frog (Acris crepitans) tadpoles were the highest ever reported in tadpoles. The Zn in the tadpoles exceeded the levels found in sediments by six to 11 times. The concentrations of As, Cr and Zn in Finfeather Lake in 1994 may have been toxic because tadpoles could not be found there. Ranid tadpoles and a newly transformed ranid frog found dead in Lateral Pond and Municipal Lake in 1994 may indicate that the elements reached toxic levels in some individual amphibians. The concentrations of As, Cr and Zn found in the tadpoles in this study might be toxic to predators. Mortality of turtles showing symptoms linked to chronic exposure to As was reported in Finfeather Lake in 1973. Turtles were not reported in Finfeather Lake again until 1996. Observations at Municipal Lake in 1994–1996 showed abundant tadpoles and turtles but no snakes, which also have not been seen at Finfeather Lake. This absence of snakes may indicate that their sensitivity or exposure to the existing contaminants is greater than that of frogs and turtles.

Solitary chemosensory cells ? taste, common chemical sense or what?

Secondary solitary chemosensory cells (SCCs) occur scattered within the epidermis of lampreys, teleosts and ranid tadpoles. Counts in representative telost species revealed that SCC's outnumber chemosensory cells organized in taste buds. Therefore, SCCs may be considered the structural substrate of a basic and probably important vertebrate chemosense. However, detailed information on structure, innervation and function is only available from specialized fins in a few teleost species, where SCCs are sufficiently concentrated. The foremost research model has been the anterior dorsal fin (ADF) in rocklings, which contains millions of SCCs but no other specialized chemosensory elements. It has been shown that these ADF-SCCs are innervated from the recurrent facial nerve. Electrophysiological recordings revealed that there is virtually no overlap in stimulus spectrum between the ADF-SCCs and pelvic fin taste buds; SCC responses could only be triggered by dilutions of heterospecific fish body mucus. Results of behavioural experiments indicate that fish mucus is indeed a relevant stimulus. Therefore it is hypothesized that the biological role of the ADF-SCCs is predator avoidance rather than search for food. Whether these findings are valid for rockings only, or can be generalized for the scattered SCC systems in more than 20000 species of fish and in some amphibians, remains an open question. Further investigations on the function and biological roles of the SCC chemosense will be crucially important to improve our understanding of sensory perception and its evolution in aquatic vertebrates.

A New Frog Genus and Species from the Mountains of the Southwestern Cape, South Africa (Anura: Ranidae)

A new ranid frog is described from the mountains of the southwestern Cape Province, South Africa. It is placed in the Petropedetinae, but cannot be assigned to any existing genus. We erect the genus Poyntonia to accommodate it and name the new frog Poyntonia paludicola. Poyntonia may be separated from the other genera of petropedetine ranids by the absence of a tympanum, the lack of digital discs, a tarsal tubercle, and lingual papilla, and the presence of webbing and an ossified omosternum. Populations of Poyntonia paludicola are known from five localities, all marshy habitats at high elevations in the southwestern Cape mountains. Adults are of moderate size (SVL 30 mm) and are very warty. The tadpoles are distinguishable from other ranid tadpoles by their small mouth, long tail, and presence of minute sharp tubercles in areas corresponding to positions of adult warts. The diploid chromosome number is 2N = 24. A sonagram of the male advertisement call is presented.

Tadpole erythrocytes: Luminescent properties with dark field microscopy

To characterize and classify erythrocytes of ranid tadpoles, alcohol-fixed blood smears were studied with dark field illumination. All preclimax stage (limb bud-foot) Rana castesbeiana tadpoles from ponds in Massachusetts had red blood cells that were polymorphic. The majority of cells (88%) showed a bright, granular luminescence varying from white to blue-grey, whereas, cytoplasm of the other cells was smooth, black, and nonluminescent. On the other hand, tadpoles in similar stages from other species (Rana clamitans, Mass. and Rana pipens, Vermont) and from R. catesbeiana tadpoles from other locations (Wisconsin and North Carolina) had no observable cytoplasmic luminescence in any of their red blood cells. Moreover, as Mass. R. catesbeiana underwent metamorphic climax their luminescent cells disappeared and were replaced by small, round, dark, nonluminescent cells, precursors of the oval, nonluminescent erythrocytes characteristic of adult frogs. Cells with black nonluminescent cytoplasm generally contained nuclei which were luminescent. In conclusion, two main types of red blood cells-those with and those without cytoplasmic luminescence-are distinguishable with dark field microscopy. Luminescence of the cells varies with species, geographic location, and developmental stage of the tadpoles.

Field and Laboratory Studies of Ion Balance and Growth Rates of Ranid Tadpoles Chronically Exposed to Low pH

The effect of sublethal, chronic exposure of tadpoles to low environmental pH under natural conditions was investigated by making weekly measurements of various physiological variables. Rana sylvatica tadpoles from a low pH pond (pH 4.05-4.90) had lower body sodium, chloride and water concentrations in comparison with tadpoles from a nearby high pH pond (pH 5.74-6.37). Tadpoles from both ponds placed in the low pH pond also underwent higher sodium efflux than when placed in the high pH pond. These observations parallel similar studies on fish and demonstrate the effects of low environmental pH on larval anuran ionic regulatory mechanisms. Survival times of field-collected R. sylvatica tadpoles placed at pH 3.0 (H2SO4) did not change with age nor were there any differences between tadpoles from high and low pH ponds. However, survival times of laboratory raised R. pipiens tadpoles did increase with age, and animals raised at pH 4.4 grew slower than siblings at pH 5.8.

Curvilinearities in the Competition Equations: An Experiment with Ranid Tadpoles

Experiments were performed to determine the existence and significance of higher-order and cross-product terms in the traditional Lotka-Volterra competition equations. The effects of conspecific and heterospecific density on parameters of development were investigated in laboratory experiments with two species of frogs, Rana sylvatica and R. pipiens. A wide variety of complex density effects were observed, and they included positive as well as negative interactions. The data presented here, in combination with those of Wilbur (1972), Neill (1974), and Ayala et al. (1973) strongly support the conclusion that hills and valleys in the competitive landscape are highly significant and that linear approximations of competition coefficients are probably insufficient and misleading. The usefulness of community matrix theory based on simple linear approximations is dubious. We also conclude that the competition coefficients are themselves density dependent and that the structure of density functions may differ even among closely related species. We suggest that the studies of the underlying biological mechanisms of species interactions serve as the only legitimate basis of constructing potentially useful models of density functions and interspecific competition.

Effects of light and darkness on the visual pigments of amphibian tadpoles

The effects of light and darkness on the visual pigment composition in the eyes of tadpoles of Rana clamitans, Rana catesbeiana, Ambystoma maculatum and Xenopus laevis have been investigated. Ranid tadpoles have mainly porphyropsin in the light, but in darkness the proportion of rhodopsin gradually increases over a period of several weeks. The process is reversible over several light-dark cycles. The light effect is extremely rapid: exposure to illumination of 85–150 ft-c. can return the system to nearly pure porphyropsin after 24–48 hr. The reaction appears to be the same at all developmental stages examined, i.e. from Taylor-Kollros stage IV–XV (early prometamorphosis). Illumination retards but does not prevent the switch to rhodopsin at natural or thyroxine-induced metamorphic climax (i.e. forelimb emergence). The dark increase of rhodopsin is not prevented by 0.04% thiourea. If tadpoles which have been permitted to increase their rhodopsin in the dark are illuminated after one eye in each specimen has been covered with black vaseline, the exposed eyes synthesize more porphyropsin. The difference is not observed if normal, clear vaseline is used instead, and it is therefore concluded that the light-stimulated formation of porphyropsin is a local response of the ocular tissues and is not mediated by hormones (such as thyroxine) or extraocular receptors (such as the stirnorgan). The quantities of visual pigment molecules appear to be the same in tadpoles kept in light and darkness, irrespective of the composition of the mixture. Like their adult forms, bullfrog tadpoles at or approaching metamorphic climax always had more porphyropsin in the dorsal retina. The premetamorphic tadpoles kept in the light did not show any significant differences between dorsal and ventral retinal areas, but those kept in darkness sometimes did. No porphyropsin was detectable in any part of the retinas of adult R. clamitans, R. pipiens, R. palustris, R. sylvatica, Hyla crucifer and H. versicolor. No dorsoventral gradient of visual pigment composition was found in R. clamitans tadpoles or Xenopus laevis adults. Unlike Rana, Ambystoma tadpoles have pure rhodopsin like the adults. Xenopus tadpoles (stages 58–59) have virtually pure porphyropsin, like the adults. Neither species changes its visual pigments when kept for several weeks in light or darkness. It is suggested that the increase of rhodopsin in the dark occurs because rhodopsin is the major pigment that is incorporated into the outer segment during the renewal process. On the other hand, the rise of porphyropsin in the light is partly a consequence of the interchange of retinol and 3-dehydroretinol between retinal visual pigment and stores in the pigment epithelium, which are composed predominantly of 3-dehydroretinol even in tadpoles kept in the dark. However, ultimately there is total disappearance of retinol and rhodopsin from the eyes of tadpoles kept in continuous light, so it is believed that a further light-driven reaction must be implicated.