Cari-Ann M. Hickerson

Territorial Behavior and Ecological Divergence in a Polymorphic Salamander

Polymorphic species provide an opportunity to examine the process of sympatric divergence as it occurs. The Eastern Red-backed Salamander, Plethodon cinereus, is a polymorphic species that has served as a model organism in behavioral and ecological studies. Recent work suggests that the two most common color phenotypes (striped and unstriped) exhibit weak assortative mating and are diverging along a number of niche dimensions including temperature optima, diet, and response to predators. Males and females of P. cinereus are territorial and this behavior is thought to function in the context of prey and mate acquisition. Striped males have been shown to gain access to larger, and presumably more fecund, females. We posited that this pattern emerges through differential territorial behavior between the two phenotypes. We predicted that striped and unstriped salamanders would differ in their use of cover objects in the field, and in their aggressive responses to intruders in the laboratory. We examined salamander cover use and movement by placing artificial cover objects (ACOs) on the forest floor and monitoring them for 3.5 years. We compared residency time, number of recaptures, and number of ACOs occupied between the two phenotypes. The proportion of striped salamanders that were territorial residents was significantly greater than the proportion of unstriped salamanders that were territorial residents. Striped salamanders also exhibited significantly longer territorial residency, were recaptured more often, and were more often found under multiple, adjacent cover objects than unstriped salamanders. In the laboratory, we examined territorial behavior of the two morphs. As residents, striped salamanders were more aggressive and less submissive than were unstriped residents. When compared to intruders, resident salamanders of both morphs behaved more aggressively, but significant differences between resident and intruder behavior were only detected for the striped phenotype. These differences in aggression and cover object use may help to explain how striped males gain access to larger females and may be important in the interpretation of sympatric niche divergence and assortative mating by color in this species.

Interactions among Forest-floor Guild Members in Structurally Simple Microhabitats

Abstract Intraguild predation in structurally complex habitats is thought to weaken trophic cascades and increase food web stability. However, many predators commonly found in leaf litter become restricted to simple microhabitat beneath rocks and logs during periods between rains. It is within this structurally simple microhabitat that some predators defend rich prey resources and are likely to interact strongly as the surrounding forest becomes too dry to forage broadly in space. We conducted a 4-y press experiment where we removed focal predators from unfenced field plots. To evaluate the effects of predators on one another we removed either salamanders or centipedes from beneath artificially placed cover objects and compared abundances of these and other intraguild predators to those in non-removal controls. We predicted that salamanders and centipedes would have strong negative effects on each other and on carabid beetles and spiders. We removed a total of 1288 salamanders and 1056 centipedes over 98 sampling dates. In salamander removal plots spider abundance increased by 34%, and carabid beetles decreased by 15% relative to the control. In centipede removal plots salamanders increased by 18% and carabid beetles increased by 29%, but spider abundance decreased by 15%. Interaction strengths were strongest in the drier summer months when territorial predators were confined in spatially fixed microhabitats. It is during these periods that predators may strongly regulate the abundances of guild members. In territorial species that defend areas beneath natural cover, the effect of intraguild predators may be an important mechanism that regulates distribution and abundance of forest floor predators.

Assortative Mating in a Polymorphic Salamander

Reproductive isolation due to divergent selection is thought to be one of the mechanisms that promote speciation in sympatry. A key element of reproductive isolation is assortative mating. We examined a polymorphic population of Eastern Red-backed Salamanders (Plethodon cinereus) for evidence of reproductive isolation through assortative mating. Our study population was made up of two common color morphs, striped and unstriped. In the field, we turned over natural cover objects to find male–female pairs of P. cinereus during peak mating season. We recorded sex, color morphology, and snout–vent length of 112 pairs of salamanders. Estimates of sexual isolation indicated weak assortative pairing in the field with more same-color pairs than expected by chance. Striped females paired with striped males were significantly larger in size than those paired with unstriped males. Intermorph pairs were observed and such pairings, if successful, would interfere with the potential for divergence. Laboratory experiments were conducted to assess the ability of females of each color morph to distinguish between the two phenotypes through fecal odors and male scent. Additionally, mating trials were conducted to examine assortative mating in the laboratory. We found no evidence that scent or natural diet cues (fecal odors) of males contributed to assortative pairing, but females of both phenotypes were more likely to be associated with striped males during mating trials. Our study provides additional evidence that striped males of P. cinereus may be more attractive to females and this may contribute to positive assortative mating in the field. Territoriality and diet may be important factors that influence this pattern.

Selective Foraging on Ants by a Terrestrial Polymorphic Salamander

Abstract Numerous authors have studied the diet of the Eastern Red-backed Salamander (Plethodon cinereus) and have described this species as a generalist predator of invertebrates. In most studies, prey taxa are identified to the family or order level. Additionally, few studies have directly assessed dietary preference by comparing diet to available prey. We chose an important component of the diet of red-backed salamanders (ants) to test whether salamanders altered their diets temporally and to determine if salamanders preyed on a subset of available ant prey. We identified ant species in salamander diets over a 13 mo period. In the fall season we also compared ants in stomach contents to those available in the surrounding leaf litter to determine if territorial residents of P. cinereus selectively forage on different ant species. We found significant temporal differences in ant species incorporated in the diet of P. cinereus that were consistent with our detailed examination of salamander ant preference in the fall. Our estimates of prey diversity and richness indicate that salamanders consumed a subset of available ant species. Aphaenogaster picea, an abundant species that prefers similar microhabitat characteristics to P. cinereus, made up a majority of the ants in the diet. However, our results indicate that P. cinereus avoids foraging on Myrmica punctiventris, Myrmecina americana, and Lasius alienus, ants that are among the most abundant species in the forested areas of northeastern Ohio where the study was conducted. These species are potentially aggressive and/or chemically defended, reducing their profitability as prey. The striped and unstriped morphs of red-backed salamanders foraged similarly on ant taxa, but the striped morph consumed significantly more ants and was found within territories that contained more ants. Our findings suggest selective foraging may be more common among generalist predators than previously considered, and we propose striped and unstriped morphs may represent a trophic polymorphism in P. cinereus.

Niche partitioning along the diet axis in a colour polymorphic population of Eastern Red-backed Salamanders, Plethodon cinereus

Eastern Red-backed Salamanders are colour polymorphic and have become a model system for examining ecological separation and the mechanisms for potential divergence in sympatry. Morphs of this species are differentiated along several niche axes including temperature optima, territorial behaviour, and response to predators. We were interested in whether temporal variation in ecological conditions would affect foraging behavior and ultimately diet. The goal of our study was to compare the diets of striped and unstriped P. cinereus over a range of seasonal conditions to better understand if the reported differences observed in the fall season at our field site remain consistent through the active season of this species. Diet differences between the two morphs were greatest during spring and fall when salamanders are most abundant at the surface. These diet differences were driven largely by two prey categories. In the spring, striped salamanders ate more oribatid mites and in the fall they consumed more entomobryomorph Collembola. Trade-offs associated with territory acquisition coupled with physiological and morphological differences may explain the observed seasonal niche partitioning related to the diet in this population.

Invasive Asian Earthworms Negatively Impact Keystone Terrestrial Salamanders.

Asian pheretimoid earthworms (e.g. Amynthas and Metaphire spp.) are invading North American forests and consuming the vital detrital layer that forest floor biota [including the keystone species Plethodon cinereus (Eastern Red-backed Salamander)], rely on for protection, food, and habitat. Plethodon cinereus population declines have been associated with leaf litter loss following the invasion of several exotic earthworm species, but there have been few studies on the specific interactions between pheretimoid earthworms and P. cinereus. Since some species of large and active pheretimoids spatially overlap with salamanders beneath natural cover objects and in detritus, they may distinctively compound the negative consequences of earthworm-mediated resource degradation by physically disturbing important salamander activities (foraging, mating, and egg brooding). We predicted that earthworms would exclude salamanders from high quality microhabitat, reduce foraging efficiency, and negatively affect salamander fitness. In laboratory trials, salamanders used lower quality microhabitat and consumed fewer flies in the presence of earthworms. In a natural field experiment, conducted on salamander populations from “non-invaded” and “pheretimoid invaded” sites in Ohio, salamanders and earthworms shared cover objects ~60% less than expected. Earthworm abundance was negatively associated with juvenile and male salamander abundance, but had no relationship with female salamander abundance. There was no effect of pheretimoid invasion on salamander body condition. Juvenile and non-resident male salamanders do not hold stable territories centered beneath cover objects such as rocks or logs, which results in reduced access to prey, greater risk of desiccation, and dispersal pressure. Habitat degradation and physical exclusion of salamanders from cover objects may hinder juvenile and male salamander performance, ultimately reducing recruitment and salamander abundance following Asian earthworm invasion.

Eastern Red-backed Salamanders Regulate Top-Down Effects in a Temperate Forest-Floor Community

Abstract Understanding the role of species interactions as regulatory mechanisms for ecosystem processes presents a challenge to ecologists working in systems with high species diversity and habitat complexity. Recent studies suggest that interactions among intraguild predators, such as terrestrial salamanders and large arthropods, might be important for the regulation of detritivores, fungivores, and perhaps detritus within terrestrial webs. A key prediction is that interactions among predators weaken trophic cascades. Our research examined this prediction by removing predators for 4 yr from unfenced field plots to investigate the effects on litter arthropods, the microbial community, and rates of leaf litter decomposition. We manipulated predator abundance in three treatments (salamander removal, centipede removal, and multiple predator removal) compared to a control in which no predators were removed. Despite difficulties in suppressing centipede numbers, we observed increases in salamanders, millipedes, isopods, slugs, numbers of ant colonies, and gamasid mites in the centipede removal plots. Additionally, several phospholipid fatty acid markers for bacteria were suppressed in plots where salamanders were most abundant. Finally, we detected treatment effects on the rate of litter disappearance from leaf bags in our field plots: those with the most salamanders had the lowest levels of litter decomposition. Overall, we found some evidence for top-down effects of predators in a temperate forest-floor web. Our study is one of few that have employed an unfenced field design and the only study examining the effects of salamanders on forest soil microbes. The results contribute to a growing body of evidence indicating that territorial predators, such as terrestrial salamanders, can be strong regulators of species composition at lower trophic levels in a system that is commonly thought to be regulated primarily through bottom-up effects of organic matter supply.

Plethodon cinereus (Eastern Red-Backed Salamander) Not Affected by Long-Term Exposure to Soil Liming

Abstract The recovery of ecosystems affected by anthropogenic acidification is often a slow process, and one that is not always achievable through natural means. Application of carbonate materials to forest soils is being used more frequently to aid in the recovery of acidified ecosystems. However, few studies have addressed how the application of carbonate materials affects amphibians. We sampled field sites undergoing long-term application of high-calcium lime to investigate the effects of increases in soil pH on body condition and population demography of Plethodon cinereus (Eastern Red-backed Salamander). We found no effect of soil liming on body condition, population demographics, or density of surface-active Eastern Red-backed Salamanders. Our results are consistent with previous studies regarding the response of this species to soil liming, but unique in that they arise from an investigation of the long-term effects of liming exposure on density and demography in a wild population of Eastern Red-backed Salamander.

Behavioral interactions between terrestrial salamanders and spiders: competition or intraguild predation?

Several studies suggest that small terrestrial salamanders are important regulators of leaf litter arthropod communities, and likely contribute to ecosystem processes such as decomposition and nutrient cycling. Despite the recognition that salamanders have the potential to strongly affect ecosystem function through both direct and indirect pathways, little is known regarding the nature of interactions between small vertebrates and the large, predatory arthropods with which they share both microhabitat and prey. Our study was designed to explore interactions between Eastern Red-backed Salamanders, Plethodon cinereus, and spiders in the genus Wadotes in an eastern North American temperate forest ecosystem. We were particularly interested in teasing apart behaviors such as territoriality and intraguild predation in an attempt to determine specifically which interaction is most likely responsible for the observed negative relationship between salamander and spider abundance at our field site. Field data indicate that P. cinereus and large syntopic spiders exhibit negative spatial associations in the microhabitat beneath cover objects, a possible indication of interspecific territoriality. In our laboratory experiments, resident salamanders displayed agonistic postures similarly toward both intruding conspecifics and spiders, suggesting that salamanders may perceive large intruding spiders as competitors. Finally, we observed no injuries to individual P. cinereus or adult spiders even though occasional chases and bites by both were recorded during the behavioral trials. We found no evidence that adults or juveniles of P. cinereus were envenomated by adult Wadotes spp., and there were no instances of intraguild predation in this study. Multiple lines of evidence from this study, and others, suggest that the primary interaction between individuals of P. cinereus and large spiders is competitive in nature rather than predatory. We suggest that the cost associated with intraguild predation on salamanders with noxious skin secretions may preclude them from being preyed upon by spiders.

Male mate preference as an agent of fecundity selection in a polymorphic salamander

Abstract Color polymorphisms are associated with variation in other traits which may affect individual fitness, and these color‐trait associations are expected to contribute to nonrandom mating in polymorphic species. The red‐backed salamander (Plethodon cinereus) exhibits a polymorphism in dorsal pattern: striped and unstriped, and previous studies have suggested that they may mate nonrandomly. However, the mechanism(s) contributing to this behavior remain unclear. Here we consider the role that male preference may have in driving mating behavior in P. cinereus. We limit our focus to striped individuals because this morph is most likely to be choosy given their dominant, aggressive behavioral profiles relative to unstriped males. Specifically, we evaluated (a) whether striped males preferentially associate with females with respect to her dorsum color, size, and body condition and (b) if so, whether female traits are evaluated via visual or chemical cues. We also considered whether the frequency of another male social behavior, nose taps, was associated with mate preferences. We found that striped male P. cinereus nose tapped more often to preferred females. However, males only assessed potential mates via chemical cues, preferring larger females overall. Reproductive phenology data on a sample of gravid females drawn from the same population indicated that the color morphs do not differ in reproductive traits, but larger females have greater fecundity. Given our findings, we conclude that female P. cinereus are under fecundity selection, mediated by male preference. In this manner, male mating behavior contributes to observations of nonrandom mate associations in this population of P. cinereus.