Pigment pattern formation in larval ambystomatid salamanders: Ambystoma tigrinum tigrinum

We have begun a comparative study of pigment patterns and their mechanisms of formation in ambystomatid salamanders in an attempt to elucidate the evolution of these traits in this family. In Ambystoma t. tigrinum, the migration of the prospective pigment cells was followed by using scanning electron microscopy and light microscopy combined with markers (dopa incubation for detecting melanophores, ammonia-induced pterin fluorescence for detecting xanthophores). The pigment pattern resulting from the cell migration shares features both with the alternating vertical xanthophore and melanophore bars of A. mexicanum and the horizontal stripes of certain salamandrids and ambystomatids. The pigment pattern of A. t. tigrinum is interpreted here as an intermediate evolutionary step between a primitive horizontal stripe pattern and a derived vertical bar pattern. The initiation of pigment pattern formation resembles the situation in A. mexicanum, probably reflecting the close phylogenetic relationship between the two taxa.     

Pigment pattern formation in the larval salamander Ambystoma maculatum

As part of an ongoing comparative study of pigment patterns and their formation in embryos and larvae of ambystomatid salamanders, Ambystoma maculatum from two differnt populations, one in the northern (New York) and one in the central (Tennessee) United States, were investigated. Scanning electron microscopy was used to study early neural crest development. Light microscopy in combination with markers for the two pigment cell types (xanthophores and melanophores) made it possible to follow pigment cell migration before the pigment cells were fully differentiated. A bilateral pigment pattern consisting of two horizontal melanophore stripes surrounding an interstripe area populated by xanthophores formed in the larvae. In both populations, some variation was present in the form of a continuum ranging from clear horizontal stripes to extreme cases with a random pattern. Unlike the other ambystomatids that have been investigated, the neural crest cells in A. maculatum do not form aggregates and no vertical bars are formed. Instead, both the pattern and its formation are very similar to what has been reported for salamandrids. If pattern formation mechanisms can act as developmental constraints we would expect the A. maculatum pattern to be the primitive condition in the Ambystomatidae, using the Salamandridae as the outgroup. There is no strong support for this when aggregate formation is used as a character and mapped onto phylogenies for the group. The aggregate formation mechanism, and the pigment pattern that it leads to, have most likely been secondarily lost in A. maculatum. © 1993 Wiley-Liss, Inc.     

Shifty salamanders: transient trophic polymorphism and cannibalism within natural populations of larval ambystomatid salamanders

Introduction

Many species of ambystomatid salamanders are dependent upon highly variable temporary wetlands for larval development. High larval densities may prompt the expression of a distinct head morphology that may facilitate cannibalism. However, few studies have characterized structural cannibalism within natural populations of larval salamanders. In this study we used two species of larval salamanders, long-toed (Ambystoma macrodactylum) and ringed salamanders (A. annulatum). Head morphometrics and stable isotopic values of carbon (δ¹³C) and nitrogen (δ¹⁵N) were used to identify the presence or absence of structural cannibalism. Weather conditions were also analyzed as a potential factor associated with the expression of cannibalistic morphology.

Results

Populations of salamander larvae did not consistently exhibit cannibalistic morphologies throughout collection periods. Larval long-toed salamanders exhibited trophic polymorphisms when relatively lower precipitation amounts were observed. Larval ringed salamanders were observed to be cannibalistic but did not exhibit polymorphisms in this study.

Conclusions

Structural cannibalism may be transient in both species; however in long-toed salamanders this morphology is necessary for cannibalism. Ringed salamanders can be cannibalistic without morphological adaptations; however the cannibal morph may prolong the viable time period for cannibalism. Additionally, weather conditions may alter pond hydroperiod, subsequently influencing head morphology and cannibalism.

     

Influence of temperature on Ranavirus infection in larval salamanders Ambystoma tigrinum

Temperature strongly influenced percent mortality and time to death of salamanders exposed to the Ambystoma tigrinum virus (iridovirus) (ATV). Most salamanders survived when exposed at 26 degrees C, whereas all died at 18 degrees C and nearly all died at 10 degrees C. Some asymptomatic salamanders that survived 60 d at 10 or 26 degrees C were found to be carrying virus. Polymerase chain reaction (PCR) confirmed the presence of virus in ATV-exposed salamanders but was found to be less sensitive than cell culture in detecting ATV at low concentrations. PCR products were 100% identical to ATV in the major capsid protein sequence. Virus titer was higher in salamanders held at 10 degrees C than at 18 degrees C but little virus, if any, was present in the small number of salamanders that died at 26 degrees C. These results may help explain periodic viral epizootics in field populations of A. tigrinum where water temperatures fluctuate widely.     

Effect of microhabitat on fitness components of larval tiger salamanders,Ambystoma tigrinum nebulosum

Summary Survivorship and growth of larval tiger salamanders, Ambystoma tigrinum nebulosum, in the White Mountains of east-central Arizona were compared in six microhabitats using field enclosures during summers, 1983–85. Microhabitats were vegetated and nonvegetated shallows, surface, middle, and bottom horizontal layers of limnetic areas, and the vertical limnetic water column. Initial enclosure densities (0.025 larvae per 1) were identical among microhabitats. Three enclosures were placed in each microhabitat in two ponds. Larval survivorship and growth were usually greatest in vegetated shallows in lowest in middle and bottom limnetic enclosures, despite several population dieoffs. Lower fitness, as reflected in survivorship and growth, in these latter enclosures was correlated with lower food levels, temperatures, and oxygen concentrations in deeper limnetic areas. Relative fitness varied greatly between years while food levels, temperatures, and oxygen concentrations within microhabitats remained relatively constant indicating additional factors affected fitness. Disparities in fitness between microhabitats apparently affect habitat use patterns of larvae.     

Interaction of an insecticide with larval density in pond-breeding salamanders (Ambystoma)

1. Amphibian populations residing in or near agricultural areas are often susceptible to pesticide contamination. Recent evidence suggests that the effects of pesticides on amphibians often exceed those estimated in laboratory toxicity tests because other environmental factors (e.g. predators, resource abundance) can influence pesticide toxicity. 2. To examine the effects of an insecticide (carbaryl) on two species of Ambystoma salamanders experiencing the natural stress of competition, we manipulated chemical concentration (control, 3.5 and 7.0 mg L^?1) and larval density (low and high). We determined the effect of treatments on snout‐vent length (SVL), growth rate, lipid reserves, time to metamorphosis, per cent survival and per cent metamorphosis. 3. Carbaryl negatively affected all response variables of Ambystoma maculatum significantly, and significantly reduced survival and metamorphosis of A. opacum. Increased density significantly influenced SVL, lipid reserves, growth rate and metamorphosis of A. maculatum. 4. The effects of carbaryl and increased density on per cent metamorphosis were nearly additive, but were generally less than additive on other variables. 5. The negative effects of chemical contamination on salamanders were likely because of pesticide‐induced reductions of food resources, as zooplankton abundance decreased by as much as 97% following carbaryl application. 6. Our study demonstrates the importance of the interactive effects that chemical contamination and natural environmental factors have on salamanders.     

The effects of food level and conspecific density on biting and cannibalism in larval long-toed salamanders, Ambystoma macrodactylum

Previous studies have examined abiotic and biotic factors that facilitate agonistic behavior. For larval amphibians, food availability and conspecific density have been suggested as important factors influencing intraspecific aggression and cannibalism. In this study, we examined the separate and combined effects of food availability and density on the agonistic behavior and life history of larval long-toed salamanders, Ambystoma macrodactylum. We designed a 2Ƕ factorial experiment in which larvae were raised with either a high or low density of conspecifics and fed either a high or low level of food. For each treatment, we quantified the amount of group size variation, biting, and cannibalism occurring. Additionally, we examined survival to, time to and size at metamorphosis for all larvae. Results indicated that differences in both density and food level influenced all three life history traits measured. Moreover, differences in food level at which larvae were reared resulted in higher within-group size variation and heightened intraspecific biting while both density and food level contributed to increased cannibalism. We suggest that increased hunger levels and an uneven size structure promoted biting among larvae in the low food treatments. Moreover, these factors combined with a higher encounter rate with conspecifics in the high density treatments may have prompted larger individuals to seek an alternative food source in the form of smaller conspecifics.     

Filling ephemeral ponds affects development and phenotypic expression in Ambystoma talpoideum

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Aquatic prey capture in ambystomatid salamanders: patterns of variation in muscle activity

Functional morphologists commonly study feeding behavior in vertebrates by recording electrical activity from head muscles during unrestrained prey capture. Rarely are experiments designed to permit a partitioning variation in muscle electrical activity patterns. Analysis of muscle activity during aquatic prey capture in two morphologically distinct species of salamanders, Ambystoma dumerilii and A. mexicanum, is conducted to assess variation at four levels: between species, among individuals within species, among experiments conducted on different days, and among feedings. The results show that 1) mean correlations among the 11 electromyographic variables measured for each feeding are low and vary considerably among individuals, 2) many of the variables show significant differences among experimental days, 3) only one variable, the difference in timing between the depressor mandibulae and sternohyoideus muscles, showed significant variation between species, and 4) seven of the 11 variables showed significant variation among individuals within species. Overall, the variation between feedings (trials) was high, and there was some variation between days on which the experiments were conducted. Neither electrode position within the muscle nor satiation contributed to the high trial variance. The results suggest that functional analyses of feeding behavior should include an assessment of variation due to individuals, days, and trials, because the amount of variation at these levels may render differences between species nonsignificant.     

Ontogeny of the hyobranchial apparatus in the salamanders Ambystoma talpoideum (Ambystomatidae) and Notophthalmus viridescens (Salamandridae): The ecological morphology of two neotenic strategies

Comparison of metamorphosis of skull and hyobranchial system in two species of neotenic salamanders reveals two different types of neoteny. Ambystoma talpoideum is completely neotenic owing to delayed metamorphosis. Notophthalmus viridescens exhibits limited neoteny as a result of incomplete metamorphosis. Morphological details of neoteny are compared to life history in both species in order to discuss the ecological morphology of the two neotenic strategies. Comparisons to Taricha granulosa, Triturus vulgaris, and Ambystoma gracile indicate that these two strategies are widely employed and may represent familial patterns.     

Polymorphic microsatellite loci for tiger salamanders,Ambystoma tigrinum

Microsatellites have been developed for few amphibian species. However, developing genetic markers for population genetic studies in amphibians is critical because amphibians are declining globally. The tiger salamander, Ambystoma tigrinum, is widespread throughout the United States and includes the endangered subspecies, A. t. stebbinsi. We present primers and amplification conditions for 10 polymorphic microsatellite loci that have produced successful results in three subspecies of A. tigrinum. Number of alleles per locus ranged from one to 11 and heterozygosity ranged from 0 to 0.815 depending on the subspecies and locus analysed. These markers should prove useful for future studies of genetic diversity and population subdivision.     

Effects of retinoic acid on the muscle patterns produced during forelimb regeneration in larval salamanders (Ambystoma)

After systemic treatment with retinoic acid (RA), Ambystoma opacum and A. punctatum larvae regenerated forelimbs with a wide variety of skeletal and gross anatomical abnormalities. Yet the musculatures within the RA-treated limb regenerates were normal even in instances where the cartilages were deformed beyond recognition as components of the limb skeleton. RA is known to induce reduplication of limb structures, sometimes entire segments. When the latter condition occurred in the present study, the corresponding replicates exhibited limb musculatures which were perfect down to minute details, yet of opposite bilateral symmetry. The results attest, firstly, to the independence of myogenesis and chondrogenesis during limb regeneration. Secondly, RA treatment unmasked an otherwise hidden potential within postembryonic salamander limb tissue for the morphogenesis of the contralateral musculature.     

Predator-prey relationships among larval dragonflies,salamanders, and frogs

Summary Tadpoles of the barking tree frog, Hyla gratiosa, are abundant in spring and summer in some ponds and Carolina bays on the Savannah River Plant near Aiken, South Carolina. To determine how these tadpoles survive in the presence of predaceous salamander larvae, Ambystoma talpoideum, and larvae of an aeshnid dragonfly, Anax junius, we determined fields densities and sizes of the predators and the prey and conducted predation experiments in the laboratory. Tadpoles rapidly grow to a size not captured by Ambystoma, although Anax larvae can capture slightly larger tadpoles. Differing habitat preferences among the tadpoles and the two predator species probably aid in reducing predation pressure. Preliminary work indicates that the tadpoles may have an immobility response to an attack by a predator. In addition, the smallest, most vulnerable tadpoles have a distinctive color pattern which may function to disrupt the body outline and make them indiscernable to predators.     

Growth and the expression of alternative life cycles in the salamander Ambystoma talpoideum (Caudata: Ambystomatidae)

Complex life cycles (CLCs) contain larval and adult phases that are morphologically and ecologically distinct. Simple life cycles (SLCs) have evolved from CLCs repeatedly in a wide variety of lineages but the processes that may underlie the transition have rarely been identified or investigated experimentally. We examined the influence of larval growth rate on the facultative expression of alternative life cycles (metamorphosis or maturation as gill-bearing adults [= paedomorphosis]) in the salamander Ambystoma talpoideum. We manipulated growth rates by altering the amount of food individuals received throughout larval development. The expression of alternative life cycles in A. talpoideum is influenced by growth via food levels, but the same growth rates at different points in the larval period elicit different responses. Individuals were more likely to metamorphose (i.e. express a CLC) when food levels and growth rates were high later in development and more likely to mature without metamorphosing (SLC) when growth rates were comparatively low during the same point in development. Growth rates at particular points in development, rather than overall larval growth rate, may be an important proximate factor in salamander life-cycle evolution.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 80 , 639–646.