Adam L. Crane

Do gill parasites influence the foraging and antipredator behaviour of rainbow darters, Etheostoma caeruleum?

Parasites are known to affect an array of characteristics of their hosts, including morphology, physiology and behaviour. We examined the foraging and antipredator behaviour of rainbow darters, Etheostoma caeruleum, that were parasitized by glochidia larvae of freshwater mussels (Ptychobranchus occidentalis and Venustaconcha pleasii: Unionidae). Glochidia attach to the gills of the host and become encapsulated in host tissue. Over a period of days or weeks the larvae develop into free-living juveniles, which then leave the host. Parasitized darters increased ventilation rates (either early in the infestation or at the height of the infestation), were less active during foraging trials, lost more body size than nonparasitized darters and showed significantly weaker responses to predation risk (signalled by the presence of a chemical alarm cue). Therefore, even for a relatively short-term infection, parasitized darters may pay a cost in terms of decreased growth and decreased probability of survival.

THE EFFECT OF REPRODUCTIVE CONDITION ON THERMOREGULATION IN FEMALE AGKISTRODON PISCIVORUS NEAR THE NORTHWESTERN RANGE LIMIT

Females of some temperate-zone snake species appear to exhibit thermophilic behavior during gestation, resulting in differential habitat use between gravid and nongravid individuals. We investigated thermoregulation of 13 female cottonmouths (Agkistrodon piscivorus) near their northwestern range limit in southwestern Missouri during mid-summer. Mean preferred body temperature (23.4 C) and preferred body temperature range (Tset, 20.0–26.5 C) measured in a laboratory thermal gradient were lower than those reported for most snake species. Physical models demonstrated that Tset consistently was available to snakes during the study period, although the frequency of availability varied among habitats. The relatively high thermal quality of the environment (based on Tset availability) allowed snakes to achieve field body temperatures (Tb) closely matching laboratory preferences. Gravid females exploited the thermal environment more efficiently than nongravid females by preferentially occupying the most thermally favorable microhabitats. Accordingly, gravid females consistently maintained higher Tb than nongravid females, demonstrating a functional link between habitat use and thermoregulation. Differences in Tb between gravid and nongravid females were greatest at low ambient temperatures, highlighting their different thermoregulatory strategies. Maintenance of low Tb in nongravid females is consistent with an energy conservation strategy benefiting reproductive investment.

Getting ready for invasions: can background level of risk predict the ability of naive prey to survive novel predators?

Factors predicting the outcome of predator invasions on native prey communities are critical to our understanding of invasion ecology. Here, we tested whether background level of risk affected the survival of prey to novel predators, both native and invasive, predicting that high-risk environments would better prepare prey for invasions. We used naïve woodfrog as our prey and exposed them to a high or low risk regime either as embryos (prenatal exposure) or as larvae (recent exposure). Tadpoles were then tested for their survival in the presence of 4 novel predators: two dytiscid beetles, crayfish and trout. Survival was affected by both risk level and predator type. High risk was beneficial to prey exposed to the dytiscids larvae (ambush predators), but detrimental to prey exposed to crayfish or trout (pursuit predators). No effect of ontogeny of risk was found. We further documented that high-risk tadpoles were overall more active than their low-risk counterparts, explaining the patterns found with survival. Our results provide insights into the relationship between risk and resilience to predator invasions.

Certainty and the cognitive ecology of generalization of predator recognition

Prey exposed to unknown species have the ability to label them as predatory if they are closely related to a predator already known to the prey. This phenomenon is coined generalization of predator recognition. While increasing the threat level of the known predator widens the generalization window (i.e. prey respond to species that are more distantly related), nothing is known about whether or not certainty associated with the identity of the known predator affects the generalization window. Here, we compared the generalization of tadpoles that were conditioned once (low certainty) or five times (high certainty) to recognize the odour of a rainbow trout, Oncorhynchus mykiss, and subsequently tested them for their response to rainbow trout, brown trout, Salmo trutta (closely related), brook trout, Salvelinus fontinalis (more distantly related) or goldfish, Carassius auratus. We found that the window shifted in two opposite ways, with high-certainty tadpoles responding more to brown trout but less to brook trout, when compared to their low-certainty counterparts. Our results highlight the nonlinear nature of stimuli generalization. We discuss potential mechanisms for our results and provide directions for future research aimed at understanding the role of uncertainty in antipredator decision making.

Patterns of predator neophobia: a meta-analytic review

Neophobia, the fear of novel stimuli, plays a major role in animal ecology. Here, we review studies on predator neophobia and explore its underlying patterns within an ecological framework. Predator neophobia is typically assessed by observing behaviours in novel areas that bring potential risk from unknown predators, or by observing behaviours towards certain kinds of objects and odours that are novel. We conducted a literature review across taxa, surveying research on baseline and induced neophobia versus controls. We calculated effect sizes for the intensity of neophobic responses, and categorized data according to six factors (taxa, age class, background type, trophic position, test cue type and experimental treatment type). While accounting for each of the other factors, we found that baseline neophobia was stronger among birds and mammals, and towards novel areas, relative to other taxa and cue types. Baseline neophobia was lower for wild-caught animals and for those that were higher in trophic position, compared with those reared in captivity and from lower trophic levels. By contrast, induced neophobia was similar in intensity across taxa, background types and testing cue types, while again being lower among upper trophic-level members and among juvenile animals. Although induced neophobia occurred across all treatment types, brain lesions induced stronger neophobia than predation risk or social isolation. We discuss potential mechanisms underlying these results and highlight gaps in the literature.

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.

Social learning in a high-risk environment: incomplete disregard for the ‘minnow that cried pike’ results in culturally transmitted neophobia

Many prey species rely on conspecifics to gather information about unknown predation threats, but little is known about the role of varying environmental conditions on the efficacy of social learning. We examined predator-naive minnows that had the opportunity to learn about predators from experienced models that were raised in either a low- or high-risk environment. There were striking differences in behaviour among models; high-risk models showed a weaker response to the predator cue and became neophobic in response to the control cue (a novel odour, NO). Observers that were previously paired with low-risk models acquired a strong antipredator response only to the predator cue. However, observers that interacted with high-risk models, displayed a much weaker response to the predator odour and a weak neophobic response to the NO. This is the first study reporting such different outcomes of social learning under different environmental conditions, and suggests high-risk environments promote the cultural transmission of neophobia more so than social learning. If such a transfer can be considered similar to secondary traumatization in humans, culturally transmitted neophobia in minnows may provide a good model system for understanding more about the social ecology of fear disorders.

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.

Behavioral and Physiological Responses of Ozark Zigzag Salamanders to Stimuli from an Invasive Predator: The Armadillo

When new predators invade a habitat, either through range extensions or introductions, prey may be at a high risk because they do not recognize the predators as dangerous. The nine-banded armadillo (Dasypus novemcinctus) has recently expanded its range in North America. Armadillos forage by searching soil and leaf litter, consuming invertebrates and small vertebrates, including salamanders. We tested whether Ozark zigzag salamanders (Plethodon angusticlavius) from a population coexisting with armadillos for about 30 years exhibit antipredator behavior in the presence of armadillo chemical cues and whether they can discriminate between stimuli from armadillos and a nonpredatory sympatric mammal (white-tailed deer, Odocoileus virginianus). Salamanders appeared to recognize substrate cues from armadillos as a threat because they increased escape behaviors and oxygen consumption. When exposed to airborne cues from armadillos, salamanders also exhibited an antipredator response by spending more time in an inconspicuous posture. Additionally, individually consistent behaviors across treatments for some response variables suggest the potential for a behavioral syndrome in this species.

Learning about danger by young hellbenders (Cryptobranchus alleganiensis): are antipredator strategies ontogenetically plastic?

Some aquatic species are able to learn to recognize chemical cues from predators through classical conditioning. In previous tests, laboratory-reared larval hellbenders (Cryptobranchus alleganiensis) showed weak antipredator responses to introduced predators (trout) compared to responses to their native predators, such as bass and sculpin. However, hellbender larvae that were conditioned with conspecific alarm cues at six months of age learned to recognize trout odour, but the responses of younger larvae to alarm cues have not been tested and the ontogeny of learning abilities is not known. In this study, we successfully trained younger larval hellbenders (4 months old) to recognize trout. Moreover, we found that the learned responses of younger hellbenders (decreased activity) are different from those of the older hellbenders (increased activity) in the previous study. This ontogenetic shift in behaviour may result from larvae increasing locomotor and sensory abilities and becoming more visible during the 4-6 month time period.