Ambystoma Annulatum Research Articles

Agonistic Behavior and Resource Defense among Sympatric Juvenile Pond-Breeding Salamanders

Abstract Interference competition is frequently observed in sexually mature adults as they defend breeding territories. However, it remains unclear in many taxa whether juveniles respond aggressively to other juveniles or if they defend resources. To test whether postmetamorphic juveniles of a pond-breeding amphibian were aggressive towards other juveniles or were defending resources, we staged terrestrial encounters between three species of sympatric Ambystoma salamanders. We observed biting and other aggressive behaviors by juvenile Spotted (Ambystoma maculatum) and Marbled Salamanders (Ambystoma opacum). However, we did not observe aggressive behaviors by Ringed Salamanders (Ambystoma annulatum). In addition to species-level variations in aggression, these three species also differed in whether aggression was targeted primarily intra- or interspecifically. This study suggests that juveniles of pond-breeding amphibians of some species may defend essential habitat with agonistic behavior.

Predator recognition learning in rainbow darters Etheostoma caeruleum: specific learning and neophobia.

This study investigated whether rainbow darters Etheostoma caeruleum can learn to recognize unfamiliar predators through the process of classical conditioning. Etheostoma caeruleum were conditioned by exposing them simultaneously to their chemical alarm cues (a known fright stimulus) and either chemical cues from larval ringed salamanders Ambystoma annulatum (unfamiliar predator) or to a blank water cue (control). Conditioning could result in either specific learning of the A. annulatum cue or increased wariness in response to any novel cue (neophobia). To distinguish between these possibilities, E. caeruleum in both groups were exposed to either A. annulatum cues alone or to chemical cues from western rat snakes Pantherophis obsoletus (novel cue) 2 days after conditioning. Treatment (A. annulatum-conditioned) E. caeruleum, but not control E. caeruleum, showed a fright response when they were exposed to both the conditioned (A. annulatum) and novel (P. obsoletus) cues, indicating increased sensitivity to new stimuli. When E. caeruleum were retested after an additional 32 days, however, the fright response occurred only following exposure to the conditioned (A. annulatum) stimulus, indicating that specific learning of the A. annulatum cue had been retained whereas the neophobia to novel stimuli was temporary.

Assessing modularity in genetic networks to manage spatially structured metapopulations

AbstractAs habitats and landscapes are becoming increasingly fragmented, it is more important than ever that the conservationists understand how organisms move across the landscape and to assess connectivity. Functional connectivity is necessary to maintain metapopulation dynamics, minimize genetic drift, maintain genetic diversity on the landscape, and ultimately for the preservation of future evolutionary potential. Graph theory and network analyses have proven to be exceptional tools for assessing functional connections among habitat patches. Ecological studies have recently begun incorporating modularity into analyses of networks. Modularity arises in networks when nodes (habitat patches) form clusters or modules wherein patches within a module interact extensively with each other, but rarely interact with patches from different modules. The goals of this study were to assess modularity in a genetic network, determine the critical scales that functional connections occur among populations, assess the contributions of populations to connectivity, and to identify habitat and landscape connectivity variables affecting network modularity. We constructed a network of genetic covariance to determine functional connections among breeding populations of Ambystoma annulatum (Ringed Salamander) at Fort Leonard Wood, Missouri, United States. From this network, we tested for the presence of modularity after accounting for the effects of distance between each breeding population, assessed the relative importance of each breeding population in contributing to within‐ and among‐module movements, and tested the effects of habitat and landscape connectivity on network parameters using linear models. The genetic network consisted of four modules, and modularity was significant after accounting for distance. Individual populations generally contributed to within‐ or among‐module movements, but not both. As within‐module strength decreased, among‐module connectivity increased. Habitat and connectivity parameters were generally poor predictor network parameters, suggesting that modularity may be a result of biotic or abiotic factors that affect successful recruitment from local populations. Our study highlights the importance of fully understanding the functional connections among populations on the landscape. The scale at which connections occur and the role of each population in contributing to connectivity are invaluable to making effective management and conservation decisions. Ultimately, analyses of network modularity have tremendous potential to inform these decisions.

Variability in functional response curves among larval salamanders: comparisons across species and size classes

Predator species and body size represent critical factors that have differential effects on prey populations, as well as overall community structure. However, investigations of how morphologically-similar predator species, simultaneous to variation in predator body size, influence lower trophic levels are infrequently performed. We tested whether predator species and body size influenced the functional response curve of three larval ambystomatid salamanders (Ringed Salamander, Ambystoma annulatum Cope, 1886; Spotted Salamander, Ambystoma maculatum (Shaw, 1802); Marbled Salamander, Ambystoma opacum (Gravenhorst, 1807)) while eating congeneric prey. We combined larval salamanders of varying body sizes with up to six prey densities within experimental microcosms. We tested for the shape of the functional response curve and obtained parameter estimates for attack rate and handling time for each predator size – species combination. We found variability among both species and size classes, with a combination of type I and type II functional response curves. Large size classes of predators had higher attack rates than smaller size classes, but equivalently-sized larvae of different species exhibited differences in attack rates and handling time. Our study shows that predation risk varies depending on the size structure and diversity of predators present in a food web, and that grouping predators by either species or size class may reduce the ability to predict changes in community structure resulting from such interactions.

Non-additive response of larval ringed salamanders to intraspecific density

Conditions experienced in early developmental stages can have long-term consequences for individual fitness. High intraspecific density during the natal period can affect juvenile and eventually adult growth rates, metabolism, immune function, survival, and fecundity. Despite the important ecological and evolutionary effects of early developmental density, the form of the relationship between natal density and resulting juvenile phenotype is poorly understood. To test competing hypotheses explaining responses to intraspecific density, we experimentally manipulated the initial larval density of ringed salamanders (Ambystoma annulatum), a pond-breeding amphibian, over 11 densities. We modeled the functional form of the relationship between natal density and juvenile traits, and compared the relative support for the various hypotheses based on their goodness of fit. These functional form models were then used to parameterize a simple simulation model of population growth. Our data support non-additive density dependence and presents an alternate hypothesis to additive density dependence, self-thinning and Allee effects in larval amphibians. We posit that ringed salamander larvae may be under selective pressure for tolerance to high density and increased efficiency in resource utilization. Additionally, we demonstrate that models of population dynamics are sensitive to assumptions of the functional form of density dependence.

Top predators and habitat complexity alter an intraguild predation module in pond communities.

Predator diversity and habitat complexity frequently influence species interactions at lower trophic levels, yet their joint investigation has been performed infrequently despite the demonstrated importance of each individual factor. We investigated how different top predators and varying habitat complexity influence the function of an intraguild predation module consisting of two larval salamanders, intraguild predator Ambystoma annulatum and intraguild prey A. maculatum. We manipulated predator food webs and habitat complexity in outdoor mesocosms. Top predators significantly influenced body condition and survival of A. annulatum, but habitat complexity had minimal effects on either response. A three-way interaction among the covariates top predator identity, habitat complexity and A. annulatum survival influenced body condition and survival of A. maculatum via a density-mediated indirect effect. Different top predator combinations had variable effects in different habitat complexity treatments on intraguild predator (A. annulatum) survival that subsequently influenced intraguild prey (A. maculatum) body condition and survival. Future work should consider how different top predators influence other food web components, which should vary due to predator attributes and the physical environments in which they co-occur.

Predation of Eggs and Recently Hatched Larvae of Endemic Ringed Salamanders (Ambystoma annulatum) by Native and Introduced Aquatic Predators

Predation is a key determinant of pond community structure, yet not all predators are equally effective and not all life stages of potential prey are similarly susceptible. Understanding the effects of native and introduced species is essential to informing management strategies, especially for endemic and species of conservation concern. We examined the effects of five common predators (three native: Central Newts [Notophthalmus viridescens louisianensis], aeshnid dragonfly naiads [Aeshnidae], and Southern Leopard Frog tadpoles [Lithobates sphenocephalus]; and two introduced: Fathead Minnows [Pimephales promelas] and Mosquitofish [Gambusia affinis]) on survival of eggs and recently hatched larvae of Ringed Salamanders (Ambystoma annulatum). We also examined the effect of supplemental food or cover availability on survival at each stage. Predators primarily showed a binary response to eggs, consuming all or none of them. Supplemental food did not influence whether eggs or larvae were consumed. Larvae were consumed by all predator species although the effect varied. The presence of cover did not reduce the impacts of the other predators on larval survival. Overall, the two introduced fish species had a greater impact on survival of the early stages of Ringed Salamanders than did the native predators. Further inquiries into the susceptibility of different life stages and survival will improve conservation strategies for rare and endemic species such as Ringed Salamanders.

Abundance and phenology patterns of two pond-breeding salamanders determine species interactions in natural populations.

Phenology often determines the outcome of interspecific interactions, where early-arriving species often dominate interactions over those arriving later. The effects of phenology on species interactions are especially pronounced in aquatic systems, but the evidence is largely derived from experimental studies. We examined whether differences in breeding phenology between two pond-breeding salamanders (Ambystoma annulatum and A. maculatum) affected metamorph recruitment and demographic traits within natural populations, with the expectation that the fall-breeding A. annulatum would negatively affect the spring-breeding A. maculatum. We monitored populations of each species at five ponds over 4years using drift fences. Metamorph abundance and survival of A. annulatum were affected by intra- and interspecific processes, whereas metamorph size and date of emigration were primarily influenced by intraspecific effects. Metamorph abundance, snout-vent length, date of emigration and survival for A. maculatum were all predicted by combinations of intra- and interspecific effects, but often showed negative relationships with A. annulatum metamorph traits and abundance. Size and date of metamorphosis were strongly correlated within each species, but in opposite patterns (negative for A. annulatum and positive for A. maculatum), suggesting that the two species use alternative strategies to enhance terrestrial survival and that these factors may influence their interactions. Our results match predictions from experimental studies that suggest recruitment is influenced by intra- and interspecific processes which are determined by phenological differences between species. Incorporating spatiotemporal variability when modeling population dynamics is necessary to understand the importance of phenology in species interactions, especially as shifts in phenology occur under climate change.

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

IntroductionMany 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.ResultsPopulations 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.ConclusionsStructural 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.

Differential dispersal shapes population structure and patterns of genetic differentiation in two sympatric pond breeding salamanders

Understanding patterns of dispersal, gene flow, and population differentiation are critical to making informed management and conservation decisions. By assessing these processes in multiple sympatric species, we can increase the generality and applicability of management plans. In this study, we assess patterns of genetic differentiation and pop- ulation structure in two ecologically similar ambystomatid salamanders in Missouri, USA. Ambystoma annulatum (rin- ged salamander) and A. maculatum (spotted salamander) are both dependent upon forested habitats and fishless ponds for reproduction, but differ in their breeding phenology. In comparing these species, we assessed the support for five different processes that we hypothesized to affect genetic differentiation: (1) resistance of landscape features to move- ment, (2) distribution of breeding habitat, (3) dispersal pro- pensity, (4) dispersal ability, and (5) breeding habitat quality. Of these hypotheses, we found support for differences in dispersal ability and propensity. In both species, there was a strong pattern of isolation-by-distance. However, A. annula- tum exhibited greater overall differentiation (F 0 ¼ 0:31 ), had a greater rate of differentiation increase with distance, and were grouped into three spatially congruent genetic clusters. In contrast, A. maculatum consisted of a single population cluster and overall F 0 ST was 0.047. We estimated the mean genetic dispersal distance of A. annulatum and A. maculatum to be 1,693 m and 2,050 m, respectively. Our results under- score the importance of considering multiple species when developing management criteria to better account for differ- ences in dispersal ability.

Structure and Dynamics of Ringed Salamander (Ambystoma annulatum) Populations in Missouri

We report a detailed account of the structure and dynamics of five populations of Ringed Salamanders (Ambystoma annulatumCope, 1886) in Missouri, USA, studied over a 4-yr period. The average date of capture for breeding males varied from 30 August to 2 October, and average date of capture for breeding females varied from 9 September to 7 October. The sex ratio was consistently male biased and averaged 2.05 males to each female. The smallest breeding female was 77 mm snout–vent length ([SVL]; mean = 96.3 mm) and the smallest breeding male was 66 mm SVL (mean = 94.2 mm). Eggs and larvae were present in September and October each year, and the larval period varied from 7 to 9 mo. Juveniles metamorphosed in all years in every pond, albeit in low numbers (6–631). The mean SVL of metamorphosing juveniles among all years and ponds was 39.2 mm. Intra-annual body size of emerging juveniles declined over time; juveniles that metamorphosed early were larger in body size than those metamorphosing later in the summer. Production of juveniles per female averaged 0.76 (range, 0.056–2.929), and survival of juveniles from egg to metamorphosis averaged 0.2% (range, 0.01%–0.75%). Both females and males can reach reproductive maturity at 1 yr of age, but most return at 2–3 yr of age. Management of the Ringed Salamander must focus on all life-history stages; protecting the aquatic stage to maximize the number and fitness of metamorphosing juveniles, managing the terrestrial habitat to maximize survival to first reproduction, and monitoring connectivity to promote metapopulation dynamics.

High intraguild predator density induces thinning effects on and increases temporal overlap with prey populations

AbstractIntraguild (IG) predator density can alter its effects on intraguild prey populations through several mechanisms, including density‐dependent processes that affect IG predator traits such as size or growth that enhance or limit its predatory abilities. We examined whether intraspecific density‐dependence altered IG predator traits, as well as the subsequent interspecific effects among its intraguild prey within a larval salamander guild. Four densities of ringed salamanders (Ambystoma annulatum), the IG predator, were combined with the presence/absence of spotted salamanders (A. maculatum), the IG prey, within experimental mesocosms. We modeled the effects of A. annulatum density on both conspecific and heterospecific responses that would be indicative of density‐dependent competition and predation, respectively. We also modeled the reciprocal interspecific effects of A. maculatum on A. annulatum. We found that increasing intraspecific density negatively affected morphological traits but not survival of A. annulatum. No interspecific effects of A. maculatum on A. annulatum were observed. Alternatively, traits of A. maculatum showed nonlinear relationships with increasing A. annulatum density. Thinning effects of A. annulatum on A. maculatum were observed, as survival was positively and size negatively related for A. maculatum with IG predator density. The temporal overlap of the IG predator and prey also increased nonlinearly with IG predator density, intensifying the potential encounter rate of the two species. Overall, this study shows that density‐dependent processes in IG predators can significantly affect traits of both themselves, as well as IG prey, which could ultimately change whether competition or predation occurs between the two groups.

Identification of Polymorphic Loci in Ambystoma annulatum and Review of Cross-species Microsatellite Use in the Genus Ambystoma

We screened 74 published microsatellite primers in Ambystoma annulatum, a species for which no microsatellite markers have been developed. Overall, we had a moderate success rate, identifying 11 polymorphic microsatellites previously developed in four different species of Ambystoma. We also conducted a review of the literature, collecting all published cross-species applications of microsatellite markers within the genus Ambystoma. From this, we identified 20 loci that have amplified in three or more species. Our synthesis of microsatellite use within the genus Ambystoma should prove valuable to future molecular research, especially in species without developed markers and for studies in species that may already have microsatellites, but are being conducted far from the region where individuals were collected for original development of species-specific loci.

Socially facilitated antipredator behavior by ringed salamanders (Ambystoma annulatum)

Many aspects of animal behavior can be socially facilitated, including foraging behavior, exploration behavior, and antipredator behavior. Although larvae of the ringed salamander (Ambystoma annulatum) are not gregarious, they can live in high densities and face intense predation pressure during a short period following hatching. In a predator-recognition experiment, we found that these salamanders responded to chemical cues from dragonfly nymphs (Family: Libellulidae) with appropriate antipredator behavior (decreased activity), and this response was absent when salamanders were exposed to chemical cues from nonpredatory mayfly nymphs (Family: Heptageniidae). In a second experiment, we tested whether antipredator behavior in response to chemical cues of dragonflies could be socially facilitated by larval ringed salamanders. We placed an “observer” salamander into a central arena with four “demonstrator” salamanders behind clear barriers around an arena. The barriers ensured that chemical cues would not be detected by the observer. When demonstrators were exposed to chemical cues from dragonflies, the data were consistent with the hypothesis that both demonstrators and observers decreased activity relative to a blank control. Our results provide evidence that social facilitation can occur in larval ringed salamanders, a nonsocial species.

Learning by embryos and the ghost of predation future

Most research on the effects of exposure to stressful stimuli during embryonic development has focused on post-embryonic behaviour that appears to be abnormal or maladaptive. Here, we tested whether exposure to some stressful stimuli (predatory cues) can lead to post-embryonic behaviour that is adaptive. When eggs of ringed salamanders (Ambystoma annulatum) were exposed to chemical cues from predators, post-hatching larvae showed reduced activity and greater shelter-seeking behaviour; larvae that had been exposed to control cues did not show these behaviours. In addition, wood frog (Rana sylvatica)tadpoles learned to respond to chemical cues from unfamiliar predators with danger based on embryonic conditioning. Therefore, if embryonic experience is a good predictor of future risk, learning associated with exposure to negative stimuli during development may be adaptive.

Breeding and Recruitment Phenology of Amphibians in Missouri Oak-Hickory Forests

ABSTRACT Knowing the phenologies of species in a region helps guide management and conservation activities in breeding ponds and surrounding terrestrial habitats. We examined the phenology of pond-breeding amphibians in central Missouri oak-hickory forests. Two ponds were monitored for 4 y from 2000–2003 and five other ponds were monitored for 1 y during 2004 using drift fences with pitfall traps. We found 15 species of pond-breeding amphibians, nine of which we captured in sufficient abundance to evaluate breeding phenology. Among the nine species, breeding migrations occur from Feb. to Nov., while subsequent metamorph emigration occurred primarily from May to Oct.. Our ponds were nearly permanent, resulting in salamander-dominated communities in these oak-hickory forests. Pond-use was partitioned by species that differed in their timing of reproduction and post-metamorphic emergence. For example, breeding in the fall gives larval ringed salamanders a potential size advantage over the spring-breeding spo...

EFFECTS OF TIMBER HARVESTING ON POND-BREEDING AMPHIBIAN PERSISTENCE: TESTING THE EVACUATION HYPOTHESIS

Numerous studies have documented the decline of amphibians following timber harvest. However, direct evidence concerning the mechanisms of population decline is lacking and hinders attempts to develop conservation or recovery plans and solutions for forest species. We summarized the mechanisms by which abundance of amphibians may initially decline following timber harvest into three testable hypotheses: (1) mortality, (2) retreat, and (3) evacuation. Here, we tested the evacuation hypothesis within a large-scale, replicated experiment. We used drift fences with pitfall traps to capture pond-breeding amphibians moving out of experimental clearcut quadrants and into control quadrants at four replicate arrays located within the Daniel Boone Conservation Area on the upper Ozark Plateau in Warren County, Missouri, USA. During the preharvest year of 2004, only 51.6% of the 312 individuals captured were moving out of pre-clearcut quadrants, and movement did not differ from random. In contrast, during both postharvest years of 2005 and 2006, the number of captures along the quadrant edge increased, and a higher proportion of individuals (59.9% and 56.6%, respectively, by year) were moving out of clearcut quadrants than entering. Salamanders moved out of clearcuts in large percentages (Ambystoma annulatum, 78.2% in 2005, 78.2% in 2006; A. maculatum, 64.0% in 2005, 57.1% in 2006). Frogs and toads also moved out of clearcut quadrants, but in lower percentages (Bufo americanus, 59.6% in 2005, 53.3% in 2006; Rana clamitans, 52.7% in 2006). Salamanders moved out of clearcuts with low-wood treatments more than out of clearcuts with high-wood treatments. Movement of salamanders out of clearcuts was independent of sex. Estimated movement out of clearcuts represented between 8.7% and 35.0% of the total breeding adults captured for two species of salamanders. Although we recognize that some portion of the amphibian population may retreat underground for short periods and others may not survive the effects of timber harvest, these data are the first direct evidence showing that individuals are capable of leaving clearcuts and shifting habitat use.

DEMOGRAPHICS OF A RINGED SALAMANDER (AMBYSTOMA ANNULATUM) BREEDING MIGRATION

Breeding migrations of the ringed salamander (Ambystoma annulatum) occur in autumn during rainy nights, when adults move in phalanxes toward small, fishless ponds. We intercepted ringed salamanders on their breeding migration in 1997 and 1998 as they crossed a paved road close to their 0.11-ha breeding pond. In 1997, we measured over 100 salamanders and found larger individuals of both sexes moved earlier in the migration, and females averaged larger than males in both weight and length. In 1998, we counted 1,096 salamanders moving towards the pond and 135 post-breeding animals as they emigrated back to their woodland habitat. Males dominated the first migration event of the 1998 season (73%) and females the last major phalanx (72%), but by the end of the migration season sex ratios were equal. A model predicted 9,848 ringed salamanders crossed the road to breed in this pond in 1998. Our sampling accounted for only 12% of post-breeding salamanders moving away from the pond, suggesting emigration is less directed than immigration. We found 61 ringed salamanders dead on the highway in 1998, indicating a 0.62% mortality due to vehicles.

Do Experience and Body Size Play a Role in Responses of Larval Ringed Salamanders, Ambystoma annulatum, to Predator Kairomones? Laboratory and Field Assays

AbstractPrey may experience ontogenetic changes in vulnerability to some predators, either because of changes in morphology or experience. If prey match their level of antipredator behavior to the level of predatory threat, prey responses to predators should reflect the appropriate level of threat for their stage of development. For larval salamanders, responses to predators may change with body size because larger larvae are less vulnerable to predation by gape‐limited predators or because fleeing responses by large salamanders may be more effective than for smaller salamanders. In a field experiment, small larval ringed salamanders, Ambystoma annulatum, responded to chemical stimuli (‘kairomones’) from predatory newts, Notophthalmus viridescens, with an antipredator response (decreased activity). Laboratory‐reared larvae decreased their activity following exposure to newt kairomones, indicating that larval ringed salamanders do not require experience with newts to recognize them as predators. In both experiments, larvae distinguished between chemical stimuli from newts and stimuli from tadpoles (non‐predators) and a blank control. In a third experiment, field‐caught (experienced) larvae showed a graded response to newt kairomones based on their body size: small larvae tended to decrease their activity while larger larvae showed no change or an increase in activity. This graded response was not observed for neutral stimuli, indicating that it is predator‐specific. Therefore, ringed salamander larvae exhibit threat‐sensitive ontogenetic changes in their response to chemical stimuli from predatory newts.

Effects of hypoxia on egg capsule conductance in Ambystoma (Class Amphibia, Order Caudata).

Aquatic amphibian eggs frequently encounter hypoxic conditions that have the potential to limit oxygen uptake and thereby slow embryonic development and hatching. Oxygen limitation might be avoided if egg capsule surface area and oxygen conductance increased in response to hypoxia. We investigated this possibility in two salamander species, Ambystoma annulatum and Ambystoma talpoideum. The effective surface area of egg capsules increased in response to hypoxia, which increased the conductance for oxygen and enhanced oxygen transport. The ability of amphibian eggs to adjust their conductance in response to oxygen availability may increase survival in hypoxic environments.