The ringed salamander (Ambystoma annulatum) is a species of mole salamander native to hardwood and mixed hardwood-pine forested areas in and around the Ozark Plateau and Ouachita Mountains of Arkansas, Oklahoma, and Missouri. This species of salamander has slender body, small head, and long tail. They are usually found to have various dorsal color from dark gray to dark brown. Various close relatives are found such as marbled salamander (A. opacum) and spotted salamander (A. maculatum). This species of salamander has cannibal behavior especially those in large body size.
It is found in damp, forested areas, usually under leaves, rotting logs, or in abandoned ground holes of other organisms, near shallow ponds. Highly fossorial (adapted to digging), adults are often found in subterranean refuges. This salamander is increasingly rare and perhaps endangered. This is likely a result of its restricted range and specific breeding habit needs. The world population is thought to be around 100,000 animals. Its conservation status is assessed as Least Concern by the IUCN. This salamander can perform embryotic learning and social-facilitated learning.Crane, Adam L., et al. "Learning to find food: evidence for embryonic sensitization and juvenile social learning in a salamander." Animal Behaviour 142 (2018): 199-206.Mathis, Alicia, Kevin L. Murray, and Caleb R. Hickman. "Do experience and body size play a role in responses of larval ringed salamanders, Ambystoma annulatum, to predator kairomones? Laboratory and field assays." Ethology 109.2 (2003): 159-170.
Description The Ringed Salamander has a slender body shape with a small head and a long tail. This species has 15 costal (along the ribs) grooves and a depressed round snout. There are two arrays of vomerine teeth—teeth along a thin bone that form the inferior and posterior part of the nasal septum and divide the nostrils. Each series contains 7 - 11 teeth. Each of their hind feet has five toes. The dorsal color of adults can range from dark gray to blackish brown decorated with white to yellowish bands and light-colored dots. Ventral sides are generally grayish-yellow. Newly metamorphosed juveniles have black backs and white bellies. A row of light spots extended from their forelimbs to the tails. Soon after metamorphosis yellow bands started to appear, and complete adult colorations form within two months after metamorphosis.
Habitat and distribution
Habitat Ringed salamander is strictly terrestrial and has been found in hardwood and mixed hardwood-pine forests. During non-breeding seasons, adults hide under leaves, rotting logs, or abandoned holes on the ground in damp forest areas. Larvae and juveniles exist in small, fishless semi-permanent ponds. Most ringed salamanders are found in the vicinity of Hot Springs, Arkansas, and the Missouri portion of the Ozark Plateau. Small populations have also been found in eastern Oklahoma.
Geographic distribution Ringed salamander is endemic to the Ozark plateau and the Ouachita Mountains of southern Missouri, Arkansas, and eastern Oklahoma. This is a much more restricted range of distribution compared to other species in the same genus, such as A. maculatum and A. opacum.
Conservation
Habitat loss While drying of ponds during late summer has significant impacts on spring breeding species such as spotted salamanders, it does not affect ringed salamanders much. However, a reduction of rain and numbers of filling ponds during September and October can cause a great decrease in ringed salamander's breeding efforts and egg depositions. Although average canopy cover and leaf litter depth do not significantly relate to ringed salamander's occupancy, continuous forests are highly associated with its breeding wetlands. Clear-cut timber harvest also has a negative effect on ringed salamander distribution. Forest sites after a clear-cut harvest have more open canopies, which results in higher ground temperatures. In order to survive, ringed salamanders either retreat underground into burrows or move to other places. Thus, juveniles and adults with small body sizes are more vulnerable as they have lower dispersal abilities.
Conservation efforts There are two major areas of focus for maximizing the proliferation of ringed salamanders, which concentrate on minimizing the local extinction of both juveniles and adults and maintaining metapopulation dynamics respectively. Protecting permanent fishless ponds is crucial for the survival of metamorphosing juveniles. Maintaining terrestrial habitat around the breeding ponds is important for reproducing adults. A study has shown that a core terrestrial habitat with a radius of 200-500m from the pond edge must be established to provide enough space for the survival of breeding adults, especially during their first reproduction. Connectivity between ponds is critical for keeping sufficient gene flows among multiple populations. A suitable habitat should have breeding ponds no more than 300m from each other, and rescue-recolonization management is recommended.
Population structure
Close relatives Ringed salamander (A. annulatum), marbled salamander (A. opacum), and spotted salamander (A. maculatum) are sympatric close relatives, and they are all terrestrial. They all belong to a famous genus of salamanders called mole salamanders (Ambystoma). Spotted salamanders and marbled salamanders have much larger distributions and are more well-studied than ringed salamanders. Similar to ringed salamanders, marbled salamanders also breed in fall, while the other species spotted salamander breeds in spring.
Genetic population structure Molecular evidence from nuclear microsatellites and mitochondrial DNA analysis shows that populations of ringed salamanders in the Central Interior Highlands ecoregion are separated into two.Burkhart, Jacob Jonathon. Genetic diversity and distribution of the ringed salamander (Ambystoma annulatum) across multiple spatial scales. Diss. University of Missouri--Columbia, 2018. One population lives on the Ozark plateau in the north, while the other population lives in the Ouachita Mountain in the south.McAllister, Chris T., Stanley E. Trauth, and Betty G. Cochran. "Endoparasites of the ringed salamander, Ambystoma annulatum (Caudata: Ambystomatidae), from Arkansas." The Southwestern Naturalist 40.3 (1995): 327-330. The separation first occurred during the Cretaceous to mid-Miocene and was further bisected by the development of the Arkansas River system during the Pleistocene. Genetic differentiation is also largely influenced by human-induced habitat fragmentation since European settlement.
Diet Common preys for ringed salamander larvae include microcrustaceans, dipteran larvae, larval chironimids, and many larval and adult insects such as beetles, snails, earthworms, and eggs of other salamanders and frogs.Nyman, Stephen, Robert F. Wilkinson, and Jackie E. Hutcherson. "Cannibalism and size relations in a cohort of larval ringed salamanders (Ambystoma annulatum)." Journal of Herpetology (1993): 78-84. Ringed salamanders usually serve as the top predator in their breeding ponds. This is likely due to the fall breeding timing of ringed salamanders, which allows them to prey on individuals of other spring breeding species that are still in their early life stages such as spotted salamanders, marbled salamanders, red-spotted newts, and many other anuran species, thus decreases their abundances.
Cannibalism Although larvae of all sizes eat other prey species, those with larger body sizes can be cannibalistic. Cannibalism can be beneficial as conspecific preys are large, might contain growth-promoting hormones, and lack toxic substances in heterospecific preys. However, there is also a risk of pathogen and endoparasite transmissions. The cannibals differ from their conspecific prey by having twice longer mean body lengths and slightly broader heads. The long breeding season leads to increasing larvae size variation, which contributes to the possibility of cannibalism. Larvae hatched later in the season have smaller sizes, so early spawn breeders may gain a selective advantage by producing large offspring with higher fitness, but this advantage may be offset by more unpredictable pond conditions. The cannibalism of ringed salamanders is an opportunistic behavior that is more likely to occur in conditions of high larvae density, the coexistence of larvae of various sizes, or insufficient alternate food choice. Larvae that commit cannibalism have been shown to have wider mouths and a larger size than their noncannibal counterparts. This adds to the evidence that cannibalism is an opportunistic enterprise based no having an advantageous size. Ringed salamander larvae have intermediate-level cannibalism compared to other species in the same genus. Spotted salamanders only show cannibalism in extreme conditions, while tiger salamanders (A. tigrinum) have really high tendencies of cannibalism.
Reproduction and life cycle
Breeding migration and oviposition Ringed salamander is an autumn breeding species. Males and females both reach their reproductive maturity at 1 year old, but most individuals return for breeding at 2–3 years old. Migration to breeding ponds usually started at night after or during rain in mid-September, and individuals tend to stick with specific ponds every year. Annual cycle of air and soil temperatures ensures that adults enter reproductive conditions in time, but autumn rainfall is the major factor that triggers breeding migration, and the precipitation threshold must be at least 1.27 cm. A huge variation of breeding population size exists across ponds and years, which is positively correlated with the amount of rainfall during migration season. Males start to migrate to breeding ponds as early as August, which is earlier than females with the earliest record in September. The end date of migration is in early November, which is similar for both sexes.
After mating, egg laying begins on the night of courtship or the next day and is completed within two days. The female extends her rear legs laterally and arches their backs to get the cloacae onto a substrate. She stays motionless after climbing onto a suitable object until muscular contractions start. The contraction spread posteriorly from a point 2.5 from the front to the rear legs, depositing eggs from the cloaca one at a time in a row. Shapes of egg masses can be strings, clumps, or large clusters, which largely depend on what are the available supporting materials, such as sticks, for oviposition. Adults leave the pond right after breeding but could remain active above-ground for several days before getting back to their resting places.
Larval and juvenile development Larvae start to present in ponds in September and October. Based on eggs hatched in the laboratory environment, the average total length of larvae just hatched is 11.5mm. Unlike spring breeding species, ringed salamander larvae overwinter under the ice in their birth ponds. The larval period ranges from 7 to 9 months, which is similar to that of marbled salamanders. Larvae mortality can be caused by freezing, drying, low pH, predation including cannibalism, and disease. Premetamorphic mortality can be as high as 99.9% and peaks during the first two months post-hatching and during metamorphic periods.Peterson, Chris L., et al. "Premetamorphic survival of Ambystoma annulatum." Herpetologica (1991): 96-100.