Newt Larvae Research Articles

Competitive and predatory interactions between invasive mosquitofish and native larval newts

Invasive fish have a high disruptive potential in aquatic ecosystems, in which amphibians may be highly impacted due to intense competition and/or predation on their eggs and larvae. Most studies have focused on the effect of large invasive fishes such as salmonids, whereas the effect of smaller fish on amphibians has been seldom investigated. We experimentally studied effects of the invasive Eastern mosquitofish (Gambusia holbrooki) on pygmy newts (Triturus pygmaeus), a species endemic to the Iberian Peninsula. We set up outdoor mesocosms in Donana National Park with native aquatic flora and invertebrate fauna, and containing larval newts at two experimental densities. Density of larval newts was also crossed with presence or absence of mosquitofish, either free-swimming or caged, in order to distinguish consumptive and non-consumptive effects. Increased density of coexisting larval newts did not reduce their survival, but reduced their growth and development. Newt survival and size at metamorphosis were dramatically reduced in the presence of free-swimming mosquitofish, whether at low or high fish densities. Caged mosquitofish, however, had no effect on larval newts. In laboratory trials, mosquitofish preyed more efficiently on insect larvae than did larval pygmy newts, highlighting the high competitive potential of mosquitofish. This was confirmed by the depletion of zooplankton that free fish caused in the experimental outdoor mesocosms. Our study suggests that invasive mosquitofish exert a high negative impact on coexisting newt populations. Such effects can be explained by a combination of direct predation, injuries caused by predation attempts, and intense competitive exploitation of common food resources.

Differences in the mechanism of muscle regeneration between the larval and metamorphosed newts.

The newt switches the cellular mechanism for limb regeneration from a stem/progenitor-based mechanism(larval mode)to a dedifferentiation-based one(adult mode)as it grows beyond metamorphosis. When it comes to muscle, larval newts regenerate muscle from muscle stem/progenitor cells such as satellite cells, but after metamorphosis the animals recruit muscle fibers for the same purpose by means of dedifferentiation in which muscle fibers(multinucleated cell)at the stump are fragmented to produce mononucleated cells, the primary cell source for new muscle. Dedifferentiation of muscle fibers may have been advantageous for the newt, during its evolution, to quickly regenerate the limbs by supplementing satellite cells whose number and potency become restricted by metamorphosis(transformation to adapt to terrestrial environments)or aging. The ability of dedifferentiation may have been invented in this animal through modifications of the molecular mechanism(or program)which runs in dying or degenerating muscle fibers.

Pigmentation plasticity enhances crypsis in larval newts: associated metabolic cost and background choice behaviour

In heterogeneous environments, the capacity for colour change can be a valuable adaptation enhancing crypsis against predators. Alternatively, organisms might achieve concealment by evolving preferences for backgrounds that match their visual traits, thus avoiding the costs of plasticity. Here we examined the degree of plasticity in pigmentation of newt larvae (Lissotriton boscai) in relation to predation risk. Furthermore, we tested for associated metabolic costs and pigmentation-dependent background choice behaviour. Newt larvae expressed substantial changes in pigmentation so that light, high-reflecting environment induced depigmentation whereas dark, low-reflecting environment induced pigmentation in just three days of exposure. Induced pigmentation was completely reversible upon switching microhabitats. Predator cues, however, did not enhance cryptic phenotypes, suggesting that environmental albedo induces changes in pigmentation improving concealment regardless of the perceived predation risk. Metabolic rate was higher in heavily pigmented individuals from dark environments, indicating a high energetic requirement of pigmentation that could impose a constraint to larval camouflage in dim habitats. Finally, we found partial evidence for larvae selecting backgrounds matching their induced phenotypes. However, in the presence of predator cues, larvae increased the time spent in light environments, which may reflect a escape response towards shallow waters rather than an attempt at increasing crypsis.

On the identification of paedomorphic and overwintering larval newts based on cloacal shape: review and guidelines.

Paedomorphosis is an alternative process to metamorphosis in which adults retain larval traits at the adult stage. It is frequent in newts and salamanders, where larvae reach sexual maturity without losing their gills. However, in some populations, larvae overwinter in water, while remaining immature. These alternative ontogenetic processes are of particular interest in various research fields, but have different causes and consequences, as only paedomorphosis allows metamorphosis to be bypassed before maturity. It is thus relevant to efficiently identify paedomorphs versus overwintering larvae. In this context, the aim of this article was 3-fold: firstly, to perform a meta-analysis of the identification procedures carried out in the literature; secondly, to determine the effectiveness of body size to make inferences about adulthood by surveying natural newt populations of Lissotriton helveticus and Ichthyosaura alpestris, and thirdly, to propose easy guidelines for an accurate distinction between large larvae and paedomorphs based on an external sexual trait, which is essential for reproduction—the cloaca. More than half of the studies in the literature do not mention the diagnostic criteria used for determining adulthood. The criteria mentioned were the presence of mature gonads (10%), eggs laid (4%), courtship behavior (10%), and external morphological sexual traits (39%) including the cloaca (24%). Body-size thresholds should not be used as a proxy for paedomorphosis, because overwintering larvae can reach a larger size than paedomorphs within the same populations. In contrast, diagnosis based on cloacal external morphology is recommended, as it can be processed by the rapid visual assessment of all caught specimens, thus providing straightforward data at the individual level for both sexes.

A developmentally regulated switch from stem cells to dedifferentiation for limb muscle regeneration in newts.

The newt, a urodele amphibian, is able to repeatedly regenerate its limbs throughout its lifespan, whereas other amphibians deteriorate or lose their ability to regenerate limbs after metamorphosis. It remains to be determined whether such an exceptional ability of the newt is either attributed to a strategy, which controls regeneration in larvae, or on a novel one invented by the newt after metamorphosis. Here we report that the newt switches the cellular mechanism for limb regeneration from a stem/progenitor-based mechanism (larval mode) to a dedifferentiation-based one (adult mode) as it transits beyond metamorphosis. We demonstrate that larval newts use stem/progenitor cells such as satellite cells for new muscle in a regenerated limb, whereas metamorphosed newts recruit muscle fibre cells in the stump for the same purpose. We conclude that the newt has evolved novel strategies to secure its regenerative ability of the limbs after metamorphosis.

UV wavelengths experienced during development affect larval newt visual sensitivity and predation efficiency.

We experimentally investigated the influence of developmental plasticity of ultraviolet (UV) visual sensitivity on predation efficiency of the larval smooth newt, Lissotriton vulgaris. We quantified expression of SWS1 opsin gene (UV-sensitive protein of photoreceptor cells) in the retinas of individuals who had developed in the presence (UV+) or absence (UV-) of UV light (developmental treatments), and tested their predation efficiency under UV+ and UV- light (testing treatments). We found that both SWS1 opsin expression and predation efficiency were significantly reduced in the UV- developmental group. Larvae in the UV- testing environment displayed consistently lower predation efficiency regardless of their developmental treatment. These results prove for the first time, we believe, functional UV vision and developmental plasticity of UV sensitivity in an amphibian at the larval stage. They also demonstrate that UV wavelengths enhance predation efficiency and suggest that the magnitude of the behavioural response depends on retinal properties induced by the developmental lighting environment.

Body size, swimming speed, or thermal sensitivity? Predator-imposed selection on amphibian larvae.

BackgroundMany animals rely on their escape performance during predator encounters. Because of its dependence on body size and temperature, escape velocity is fully characterized by three measures, absolute value, size-corrected value, and its response to temperature (thermal sensitivity). The primary target of the selection imposed by predators is poorly understood. We examined predator (dragonfly larva)-imposed selection on prey (newt larvae) body size and characteristics of escape velocity using replicated and controlled predation experiments under seminatural conditions. Specifically, because these species experience a wide range of temperatures throughout their larval phases, we predict that larvae achieving high swimming velocities across temperatures will have a selective advantage over more thermally sensitive individuals.ResultsNonzero selection differentials indicated that predators selected for prey body size and both absolute and size-corrected maximum swimming velocity. Comparison of selection differentials with control confirmed selection only on body size, i.e., dragonfly larvae preferably preyed on small newt larvae. Maximum swimming velocity and its thermal sensitivity showed low group repeatability, which contributed to non-detectable selection on both characteristics of escape performance.ConclusionsIn the newt-dragonfly larvae interaction, body size plays a more important role than maximum values and thermal sensitivity of swimming velocity during predator escape. This corroborates the general importance of body size in predator–prey interactions. The absence of an appropriate control in predation experiments may lead to potentially misleading conclusions about the primary target of predator-imposed selection. Insights from predation experiments contribute to our understanding of the link between performance and fitness, and further improve mechanistic models of predator–prey interactions and food web dynamics.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0522-y) contains supplementary material, which is available to authorized users.

An orphan gene is necessary for preaxial digit formation during salamander limb development.

Limb development in salamanders differs from other tetrapods in that the first digits to form are the two most anterior (preaxial dominance). This has been proposed as a salamander novelty and its mechanistic basis is unknown. Salamanders are the only adult tetrapods able to regenerate the limb, and the contribution of preaxial dominance to limb regeneration is unclear. Here we show that during early outgrowth of the limb bud, a small cohort of cells express the orphan gene Prod1 together with Bmp2, a critical player in digit condensation in amniotes. Disruption of Prod1 with a gene-editing nuclease abrogates these cells, and blocks formation of the radius and ulna, and outgrowth of the anterior digits. Preaxial dominance is a notable feature of limb regeneration in the larval newt, but this changes abruptly after metamorphosis so that the formation of anterior and posterior digits occurs together within the autopodium resembling an amniote-like pattern.

Effects of temperature on embryonic and early larval growth and development in the rough-skinned newt (Taricha granulosa)

We investigated the effects of temperature on the growth and development of embryonic and early larval stages of a western North American amphibian, the rough-skinned newt (Taricha granulosa). We assigned newt eggs to different temperatures (7, 14, or 21°C); after hatching, we re-assigned the newt larvae into the three different temperatures. Over the course of three to four weeks, we measured total length and developmental stage of the larvae. Our results indicated a strong positive relationship over time between temperature and both length and developmental stage. Importantly, individuals assigned to cooler embryonic temperatures did not achieve the larval sizes of individuals from the warmer embryonic treatments, regardless of larval temperature. Our investigation of growth and development at different temperatures demonstrates carry-over effects and provides a more comprehensive understanding of how organisms respond to temperature changes during early development.

Fire salamander (Salamandra salamandra) in Larzac plateau: low occurrence, pond-breeding and cohabitation of larvae with paedomorphic palmate newts (Lissotriton helveticus)

th November; revised on 2014, 18 th January; accepted on 2014, 31 st January Abstract. Alternative reproductive strategies are widespread in caudate amphibians. Among them, fire salamanders (Salamandra salamandra) usually rely on streams to give birth to aquatic larvae but also use ponds, whereas palmate newt larvae (Lissotriton helveticus ) typically metamorphose into terrestrial juveniles, but can also reproduce in retain- ing their gills, a process known as paedomorphosis. Here we report repeated observations of an unusual case of coex- istence of these two alternative traits in the same pond (Larzac, France). The prevalence of fire salamanders in South- ern Larzac was very low (pond occupancy: 0.36%). The observed abundance of fire salamander larvae and paedo- morphic newts was also low in the studied pond. On one hand, the rarity of this coexistence pattern may suggest that habitat characteristics may not be optimal or that competition or predation processes might be operating. However, these hypotheses remain to be tested. On the other hand, as this is the only known case of breeding in Southern Lar - zac, it could be considered to be at a high risk of extirpation.

Developmental and evolutionary history affect survival in stressful environments.

The world is increasingly impacted by a variety of stressors that have the potential to differentially influence life history stages of organisms. Organisms have evolved to cope with some stressors, while with others they have little capacity. It is thus important to understand the effects of both developmental and evolutionary history on survival in stressful environments. We present evidence of the effects of both developmental and evolutionary history on survival of a freshwater vertebrate, the rough-skinned newt (Taricha granulosa) in an osmotically stressful environment. We compared the survival of larvae in either NaCl or MgCl2 that were exposed to salinity either as larvae only or as embryos as well. Embryonic exposure to salinity led to greater mortality of newt larvae than larval exposure alone, and this reduced survival probability was strongly linked to the carry-over effect of stunted embryonic growth in salts. Larval survival was also dependent on the type of salt (NaCl or MgCl2) the larvae were exposed to, and was lowest in MgCl2, a widely-used chemical deicer that, unlike NaCl, amphibian larvae do not have an evolutionary history of regulating at high levels. Both developmental and evolutionary history are critical factors in determining survival in this stressful environment, a pattern that may have widespread implications for the survival of animals increasingly impacted by substances with which they have little evolutionary history.

Stem stiffness plays a role in determining the foraging success of predators

The presence of macrophytes in the littoral zone provide prey animals with protection from predators. Two macrophyte characters, stem density and branching, are known to hinder predator foraging in macrophyte beds. Stem stiffness is a character that allows the macrophyte to withstand current power in the intertidal zone, but its effect on predator movements in macrophyte beds has not been studied to date. In this study I examined whether the foraging success of predators is constrained by stem stiffness, as well as stem density and the presence of branches. Artificial macrophytes were constructed using two types of rubber that differed in stiffness. The newt Cynops ensicauda popei and larvae of the damselfly Paracercion melanotum were used as predator and prey, respectively, in this model system. The results revealed that all three plant characters studied influenced the survival rate of prey. Stiff stems consistently increased the survival rate compared with flexible stems. Stem density had the highest positive influence on survival rate. The direct effect of branches was negative and minute, but it altered the dependency on stem density. Although stiffness did have an effect on the survival rate of prey, its magnitude was relatively low. The effect of stiffness in other settings should be examined in future studies.

Eastern Newt (Notophthalmus viridescens) larvae alter morphological but not chemical defenses in response to predator cues

Prey traits are often modified in response to exposure to predators, a phenomenon known as predator-induced phenotypic plasticity. Morphological plasticity in response to predator cues is well documented in amphibians; however, predator-induced chemical defenses have received relatively little attention. The Eastern Newt (Notophthalmus viridescens (Rafinesque, 1820)), which possesses tetrodotoxin—a toxin for chemical defense, is most vulnerable to predation during its larval stage. We assessed whether exposing Eastern Newt larvae to predator scent cues (from dragonfly larvae) would elicit change in their morphological and chemical defenses. Newt larvae exposed to scent cues of predatory dragonfly larvae exhibited significantly greater tail depths, which should increase survival of attempted predation by allowing them to swim faster, but did not differ in mass, snout–vent length, or tail length. Toxin concentrations in newt larvae were not significantly affected by exposure to these predator cues. Larval toxicity may be derived maternally or environmentally and is inflexible, or induced toxicity may only be detectable later in development. Predator-induced phenotypic plasticity, especially of chemical defenses, warrants greater attention, as potentially important outcomes of species interactions remain unclear.

Disentangling prey-handling efficiency of larval newts through multivariate prey trait analysis

Multivariate prey trait analysis is a functional approach to understand predator–prey relationships. In the present study, six prey macroinvertebrate ecological traits were used to identify several key factors in the handling efficiency of seven predatory larval newt species. The results revealed a remarkable similarity in the feeding behaviour among species, suggesting a foraging behaviour convergence among species in the prey-handling efficiency of larval newts. Nevertheless, larvae of some newt species showed clear preferences for particular categories of ecological trait; for example, Lissotriton vulgaris tended to feed on macroinvertebrate taxa with random trajectory, and Calotriton asper fed on macroinvertebrate taxa with high agility. In contrast, Mesotriton alpestris showed a clear ability to feed on prey with movable accessories (cases/tubes) and patterned concealment. This study shows how multivariate approaches can complement traditional diet analyses, and the method has wide applicability across life-stages and species.

Effect of temperature extremes on the spatial dynamics of predator–prey interactions: A case study with dragonfly nymphs and newt larvae

Theory predicts that predators are more vulnerable to increasing temperature than prey. Despite huge variations in the magnitude and duration of thermally-extreme episodes in nature, most empirical studies on predator–prey interactions consider conditions induced by a climatic shift in mean temperature. We asked whether the increased vulnerability of predators holds under daily thermal extremes occurring during heat waves, using dragonfly nymphs and newt larvae as the predator–prey model system. Direct exposure of predator to prey in heated and non-heated aquaria under semi-natural conditions revealed that predator movements increased with rising temperature, whereas prey activity decreased. In contrast to the theory of predator–prey space use, the spatial co-occurrence of predator and prey individuals increased with temperature, while predation rates diminished. We conclude that daily thermal extremes affect trophic interactions in the same way, i.e. through the increased vulnerability of predators, as do long-term shifts in mean environmental temperature. Our results highlight the importance of behavioral studies for understanding mechanisms mediating the effect of extreme thermal events on species interactions.

Predator-Prey Interactions Shape Thermal Patch Use in a Newt Larvae-Dragonfly Nymph Model

Thermal quality and predation risk are considered important factors influencing habitat patch use in ectothermic prey. However, how the predator’s food requirement and the prey’s necessity to avoid predation interact with their respective thermoregulatory strategies remains poorly understood. The recently developed ‘thermal game model’ predicts that in the face of imminent predation, prey should divide their time equally among a range of thermal patches. In contrast, predators should concentrate their hunting activities towards warmer patches. In this study, we test these predictions in a laboratory setup and an artificial environment that mimics more natural conditions. In both cases, we scored thermal patch use of newt larvae (prey) and free-ranging dragonfly nymphs (predators). Similar effects were seen in both settings. The newt larvae spent less time in the warm patch if dragonfly nymphs were present. The patch use of the dragonfly nymphs did not change as a function of prey availability, even when the nymphs were starved prior to the experiment. Our behavioral observations partially corroborate predictions of the thermal game model. In line with asymmetric fitness pay-offs in predator-prey interactions (the ‘life-dinner’ principle), the prey’s thermal strategy is more sensitive to the presence of predators than vice versa.

Pleurodeles waltl Newt Larvae Diet Regarding Available Prey: Choice or Mere Coincidence?

Vernal pools are preferred breeding habitats for numerous amphibian species. The analysis of prey composition during the amphibian larval stages is necessary to understand diet composition and food choice in aquatic communities. We studied the diet of larvae of Pleurodeles waltl when exogenous feeding begins and throughout the flooding period in an episodic Mediterranean pond. The stomach contents were analyzed and the diet was compared to the availability of prey in the pond. The diet analysis revealed an ample diversity of prey, the most abundant being cyclopoid and calanoid copepods and podocopid ostracods. Changes in the composition of the diet corresponded principally to the variations in the availability of different prey as a consequence of the succession of the zooplankton community throughout the flooding period. However, certain taxa such as large anostracans, small anomopods, and turbellarias were not consumed although they were available and abundant. In contrast, prey scarcely represented in the pond such as coleopteran, dipteran, and hemipteran larvae were efficiently captured, suggesting their accessibility to newt larvae. The proportion of prey found in stomachs with respect to their abundance in the pond increased with larval size, coinciding with a reduction in number and bio-volume of available prey. The results suggest that newt larvae are opportunistic feeders and that breeding success of newts may be highly dependent on early egg-laying to match the abundant food supply found at early flooding stages of vernal pools.

Does developmental acclimatization reduce the susceptibility to predation in newt larvae?

Many organisms respond to the heterogeneity of abiotic environmental conditions by plastic modifications of their phenotypes (acclimation or acclimatization). Despite considerable research efforts in this area, the beneficial (adaptive) effect of acclimation or acclimatization is still debated. We examined whether the development of newt larvae (Ichthyosaura alpestris) under different natural light and thermal conditions subsequently altered their susceptibility to predation in sun-exposed versus shaded tanks in nature. During predation trials in various light and temperature conditions, newt larvae that developed in sun-exposed warmer tanks consistently suffered from higher predation by dragonfly nymphs (Aeshna cyanea) compared to larvae from shaded or colder tanks. We conclude that higher sun exposure during embryonic and larval development negatively affects antipredator performance even in sun-exposed tanks: this result is inconsistent with the beneficial acclimation hypothesis. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, , –.

Parasite transmission in complex communities: Predators and alternative hosts alter pathogenic infections in amphibians

While often studied in isolation, host-parasite interactions are typically embedded within complex communities. Other community members, including predators and alternative hosts, can therefore alter parasite transmission (e.g., the dilution effect), yet few studies have experimentally evaluated more than one such mechanism. Here, we used data from natural wetlands to design experiments investigating how alternative hosts and predators of parasites mediate trematode (Ribeiroia ondatrae) infection in a focal amphibian host (Pseudacris regilla). In short-term predation bioassays involving mollusks, zooplankton, fish, larval insects, or newts, four of seven tested species removed 62-93% of infectious stages. In transmission experiments, damselfly nymphs (predators) and newt larvae (alternative hosts) reduced infection in P. regilla tadpoles by -50%, whereas mosquitofish (potential predators and alternative hosts) did not significantly influence transmission. Additional bioassays indicated that predators consumed parasites even in the presence of alternative prey. In natural wetlands, newts had similar infection intensities as P. regilla, suggesting that they commonly function as alternative hosts despite their unpalatability to downstream hosts, whereas mosquitofish had substantially lower infection intensities and are unlikely to function as hosts. These results underscore the importance of studying host-parasite interactions in complex communities and of broadly linking research on predation, biodiversity loss, and infectious diseases.

Conspecific alarm cues, but not predator cues alone, determine antipredator behavior of larval southern marbled newts, Triturus pygmaeus

Predation imposes selection on the ability of prey to recognize and respond to potential threats. Many prey species detect predators via chemoreception, particularly in aquatic environments. Also, chemical cues from injured prey are often perceived as an indication of predation risk. However, because antipredatory behavior can be costly, prey responses should depend on the current level of risk that each predator poses, which may depend on the type of chemical cues detected. We exposed larval newts, Triturus pygmaeus, to chemical cues from predator larval beetles or to alarm cues from conspecific larval newts and examined the behavioral changes of larval newts. Results showed that larval newts reduced activity levels when conspecific alarm cues were present but not when the predator cues alone were present. These results might suggest that larval newts are unable to recognize predator chemicals. To avoid costs of unnecessary antipredatory behaviors, larval newts may benefit by avoiding only predators that represent a current high level of threat, showing only antipredatory responses when they detect conspecific alarm cues indicating that an actual predatory attack has occurred.