Alicia Mathis

Cultural transmission of predator recognition in fishes: intraspecific and interspecific learning

Individuals that live in groups may have the opportunity to learn to recognize unfamiliar predators by observing the fright responses of experienced individuals in the group. In intraspecific trials, naive fathead minnows, Pimephales promelas, gave fright responses to chemical stimuli from predatory northern pike, Esox lucius, when paired with pike-experienced conspecifics but not when paired with pike-naive conspecifics. These pike-conditioned minnows retained the fright responses to pike odour when tested alone, indicating that learning had occurred, and transmitted their fright responses to pike-naive minnows in subsequent trials. Brook stickleback, Culaea inconstans, are found in mixed-species aggregations with fathead minnows and are also vulnerable to predation by northern pike. In a series of interspecific tests, pike-naive brook stickleback gave fright responses to chemical stimuli from northern pike when paired with pike-experienced minnows but not when paired with pike-naive minnows. Pike-conditioned stickleback also retained the fright responses when tested alone and subsequently also transmitted the fright responses to pike-naive minnows. Individuals may benefit from observations of the fright responses of conspecifics or heterospecifics by (1) being alerted to the immediate presence of unfamiliar predators and (2) learning to recognize unfamiliar predators as a potential threat.

Territoriality in a terrestrial salamander: the influence of resource quality and body size

Intraspecific interference competition associated with territoriality has been documented in laboratory studies of the red-backed salamander, Plethodon cinereus. I used laboratory and field experiments to study the effect of resource quality and body size on such competition. In an experiment in southwestern Virginia, cover objects (e.g., logs) from which the resident salamanders were removed were invaded significantly more often than cover objects from which the resident salamander was not removed. These data provide the first direct test of territoriality for a salamander in a natural habitat. Newly invading salamanders were significantly smaller than the original territorial residents. Therefore, large body size is an advantage in territorial encounters. Because cover objects are important resources for terrestrial salamanders, characteristics of the cover object may contribute to territory quality. In an experiment conducted during warm summer weather at the Virginia site, soil temperatures under large cover objects were significantly cooler than those under small cover objects or under the leaf litter. Large cover objects may therefore benefit the salamanders by providing a buffer zone between the salamander and extreme environmental temperatures on the forest floor. In both laboratory and field experiments, when salamanders were offered a choice between large and small cover objects, both large and small salamanders exhibited a significant preference for large cover objects. Also I censused cover objects in a natural mixed hardwood forest habitat during courting and noncourting seasons and, for both seasons, I found a significant positive correlation between the body size of the salamander and the size of the cover object that it occupied. I conclude that, in this natural forest habitat, there is intraspecific competition for high quality cover objects and larger individuals are more successful competitors than smaller individuals.

Intraspecific and Cross‐Superorder Responses to Chemical Alarm Signals by Brook Stickleback

Fathead minnows (Pimephales promelas) and brook stickleback (Culaea inconstans) are often sympatric, occupy similar microhabitats, and share common predators. Therefore, individuals that detect alarm signals of both conspecifics and heterospecifics should gain antipredator benefits. We conducted a series of experiments to determine the extent to which these species respond to chemical alarm signals from conspecifics and heterospecifics. In laboratory experiments, brook stickleback responded to chemical stimuli from injured conspecifics with increased shoaling, but did not increase shoaling following exposure to chemical stimuli from injured swordtails (Xiphophorus helleri), an unfamiliar tropical fish that is not closely related to either stickleback or fathead minnows. These data are the first to document a chemical alarm signal for fishes in the order Gasterosteiformes. Brook stickleback also exhibited fright responses to extracts from injured fathead minnows in both laboratory and field tests. Stickleback did not exhibit a fright reaction following exposure to chemical stimuli from fathead minnows that had been treated with testosterone to decrease the concentration of alarm substance cells. This result suggests that the minnow alarm pheromone is the active component rather than some other constituent of the minnow skin extracts. In contrast to the response of the stickleback, fathead minnows did not respond to extracts from brook stickleback with a fright response. These data suggest that brook stickleback may benefit from close proximity with fathead minnows by gaining early warning of danger.

Territories of male and female terrestrial salamanders: costs, benefits, and intersexual spatial associations

SummaryI used a mark-recapture study to estimate home areas for 107 red-backed salamanders (Plethodon cinereus) in a natural forest habitat. Both males and females of this species defend feeding territories, but I presume that some individuals in this relatively highdensity population (approximately 2.8 salamanders per m2) are nonterritorial floaters. Although territorial salamanders exhibited greater numbers of tail autotomies, they had significantly longer relative tail lengths. This difference suggests that territorial individuals gain benefits from territorial ownership. From the observation that home area size was inversely correlated with body size, I infer that larger animals gained higher quality foraging areas. Home areas of adults were significantly more segregated intrasexually and more aggregated intersexually than would be expected from a random distribution. Furthermore, intersexual overlap of home areas was significantly greater than intrasexual home area overlap. Territorial defense of feeding areas by male and female red-backed salamanders therefore also may play a role in mating behavior.

Epidermal ‘alarm substance’ cells of fishes maintained by non-alarm functions: possible defence against pathogens, parasites and UVB radiation

Many fishes possess specialized epidermal cells that are ruptured by the teeth of predators, thus reliably indicating the presence of an actively foraging predator. Understanding the evolution of these cells has intrigued evolutionary ecologists because the release of these alarm chemicals is not voluntary. Here, we show that predation pressure does not influence alarm cell production in fishes. Alarm cell production is stimulated by exposure to skin-penetrating pathogens (water moulds: Saprolegnia ferax and Saprolegnia parasitica), skin-penetrating parasites (larval trematodes: Teleorchis sp. and Uvulifer sp.) and correlated with exposure to UV radiation. Suppression of the immune system with environmentally relevant levels of Cd inhibits alarm cell production of fishes challenged with Saprolegnia. These data are the first evidence that alarm substance cells have an immune function against ubiquitous environmental challenges to epidermal integrity. Our results indicate that these specialized cells arose and are maintained by natural selection owing to selfish benefits unrelated to predator–prey interactions. Cell contents released when these cells are damaged in predator attacks have secondarily acquired an ecological role as alarm cues because selection favours receivers to detect and respond adaptively to public information about predation.

Population declines of a long-lived salamander: a 20+-year study of hellbenders, Cryptobranchus alleganiensis

Accurate assessment of whether long-lived species are stable or declining is challenging. Life history characteristics such as delayed maturity result in relatively slow population responses to perturbations, so data should be collected across a relatively long time span. Because differential effects on age classes can be important, studies should also examine potential changes in the populations age structure. Moreover, multiple populations should be studied to indicate whether changes are regional or are restricted to local populations. We incorporated all three factors (long duration, multiple populations, age structure data) into our study of the conservation status of a long-lived aquatic salamander, the hellbender, Cryptobranchus alleganiensis. Over the 20+ years of this study, populations of hellbenders declined by an average of about 77%. This decline was characterized by a shift in size (age) structure, with a disproportionate decrease in numbers of young individuals. The change in density and age structure was consistent for populations in five rivers and for two subspecies (C. a. alleganiensis and C. a. bishopi), indicating that the decline is not restricted to one or two local populations. For the population with the most extensive data, the decline had clearly begun by the 1980s and there was a significant decrease in body condition over the period of the study. It is not known whether population declines for hellbenders have a single cause or whether each population has experienced independent declines.

Chemical labeling of northern pike (Esox lucius) by the alarm pheromone of fathead minnows (Pimephales promelas)

In previous experiments, chemical stimuli from northern pike (Esox lucius) elicited fright responses from pike-naive fathead minnows (Pimephales promelas) only if the pike had recently eaten conspecific minnows. We used a behavioral assay to determine if the fright response is the result of the incorporation of the minnow alarm pheromone into the chemical signature of the pike. Because the alarm substance cells (epidermal club cells) of fathead minnows are seasonally lost by males, we used chemical stimuli from pike that had eaten breeding male minnows as a control stimulus. In independent laboratory and field experiments, pike-naive minnows exhibited fright reactions (e.g., increased shelter use, avoidance) when exposed to water from tanks containing pike that had eaten nonbreeding fatheads (with alarm substance cells), but not to water from tanks containing pike that had eaten breeding male fatheads (without alarm substance cells). These data indicate that the fathead minnow alarm pheromone chemically labels northern pike as dangerous to pike-naive receivers.

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.

Acquired Recognition of Chemical Stimuli from an Unfamiliar Predator: Associative Learning by Adult Newts, Notophthalmus viridescens

Many vertebrates recognize potential predators using only chemical cues (Weldon, 1990). Chemical detection of predators is particularly important at night, in dark or murky habitats, in areas with dense vegetation, or with cryptic or ambush predators, all conditions that are common in aquatic environments (Dodson et al., 1994). Chemical recognition of some common predators may be innate (e.g., Elliot et al., 1993). Natural selection also may favor the ability to learn to associate unfamiliar predators with danger (e.g., Maloney and McLean, 1995; Chivers et al., 1996). Previous attempts to demonstrate associative learning by amphibians have been relatively unsuccessful (Suboski, 1992). Chemical alarm signals play an important role in the antipredator behavior of many aquatic vertebrates (e.g., Hews and Blaustein, 1985; Smith, 1992; Mathis and Smith, 1993a). For amphibians, response to chemical alarm signals has been documented for some anuran tad-

Territorial salamanders assess sexual and competitive information using chemical signals

Abstract Adult male and female red-backed salamanders, Plethodon cinereus , gain information about gender and body size of conspecifics through chemical signals. Responses to information about gender differed between the sexes: females produced faecal pellets (territorial pheromonal markers) fastest when exposed to their own pheromones while males produced faecal pellets fastest when exposed to pheromones of females. These data suggest that for females the primary pheromonal function of faecal pellets is advertisement (i.e. defence) of their own areas, and that faecal pellets produced by males are of primary importance in the attraction of mates. Two types of responses to information concerning body size were found. (1) Both male and female intruders exposed to the pheromones of resident males tended to produce larger faecal pellets when the intruder and resident were of similar body sizes. This phenomenon was not observed when the resident was female. (2) Male intruders were significantly more aggressive when exposed to the pheromones of individuals of similar body size and more submissive when exposed to pheromones of individuals that were larger. Therefore, information about body size (an indicator of competitive ability) of males may be transmitted via chemical signals and may cause changes in the behaviour of conspecifics.