Michael E. Fraker

Characterization of an alarm pheromone secreted by amphibian tadpoles that induces behavioral inhibition and suppression of the neuroendocrine stress axis.

Many species assess predation risk through chemical cues, but the tissue source, chemical nature, and mechanisms of production or action of these cues are often unknown. Amphibian tadpoles show rapid and sustained behavioral inhibition when exposed to chemical cues of predation. Here we show that an alarm pheromone is produced by ranid tadpole skin cells, is released into the medium via an active secretory process upon predator attack, and signals predator presence to conspecifics. The pheromone is composed of two components with distinct biophysical properties that must be combined to elicit the behavioral response. In addition to the behavioral response, exposure to the alarm pheromone caused rapid and strong suppression of the hypothalamo-pituitary-adrenal (HPA) axis, as evidenced by a time and dose-dependent decrease in whole body corticosterone content. Reversing the decline in endogenous corticosterone caused by exposure to the alarm pheromone through addition of corticosterone to the aquarium water (50 nM) partially blocked the anti-predator behavior, suggesting that the suppression of the HPA axis promotes the expression and maintenance of a behaviorally quiescent state. To our knowledge this is the first evidence for aquatic vertebrate prey actively secreting an alarm pheromone in response to predator attack. We also provide a neuroendocrine mechanism by which the behavioral inhibition caused by exposure to the alarm pheromone is maintained until the threat subsides.

The effect of hunger on the strength and duration of the antipredator behavioral response of green frog (Rana clamitans) tadpoles

The activity level of prey reflects a trade-off between predation risk and foraging gain. A number of theoretical and empirical studies have shown that a preys energetic state or the level of its resource should influence this trade-off (i.e., what the optimal activity level at a level of predation risk is). Here, I show that the energetic state of prey may also influence the duration of their antipredator behavioral response. Green frog tadpoles (Rana clamitans) reduced their activity level for a shorter time during exposure to the chemical cue of predatory larval dragonflies (Anax spp.) as their time since last feeding increased (i.e., as their energetic state decreased). Interestingly, the tadpoles strongly reduced their activity level upon cue exposure in all treatments. Thus, the relative activity level of tadpoles at different energetic states varied over time.

Predation risk assessment by green frog (Rana clamitans) tadpoles through chemical cues produced by multiple prey

Many prey assess predation risk through predator chemical cues. Numerous studies have shown that (1) prey sometimes respond to chemical cues produced by heterospecifics and (2) that many species are capable of associative learning. This study extends this research by focusing on predation risk assessment and antipredator behavior in environments containing chemical cues produced by multiple prey species. The results show that green frog (Rana clamitans) tadpoles (1) assess risk from the chemical cue produced during predation by a heterospecific (gray tree frog, Hyla versicolor, tadpoles) and (2) can exhibit similarly strong behavioral responses to a mix of conspecific and heterospecific cues compared to conspecific cue alone, depending on their conditioning environment. I then discuss how the prey choice of the predators and the relative abundances of the prey species should influence the informational value of heterospecific cues.

The effect of prior experience on a prey’s current perceived risk

The prior experience of prey may influence how they assess the level of predation risk associated with an information source. Here, I present the results from a set of experiments that demonstrate how the prior experience of green frog (Rana clamitans) tadpoles can influence their risk assessment during exposure to the chemical cue of predatory larval dragonflies (Anax spp.) consuming conspecific tadpoles. At the short-term scale, green frog tadpoles perceived a higher level of risk when consecutive cue exposures overlapped, but only when the total chemical cue concentration was weak. Weaker chemical cue concentrations may be less reliable than stronger cue concentrations, and overlapping cue exposures may increase the degree of certainty that tadpoles have in their perceived risk. When consecutive cue exposures did not overlap, tadpoles assessed the risk associated with each cue exposure independently. Predator-conditioned tadpoles responded longer during exposure to the Anax chemical cue than nonconditioned tadpoles, which suggests that a tadpole’s long-term experience eventually does influence its risk assessment. In general, the results suggest that a prey’s prior experience may influence its current perceived risk by influencing either the degree of certainty in or the level of its perceived risk. Understanding how the prior experience of prey influences their current risk assessment requires that the rate of decay of the value of prior experience should be identified at two timescales as an indicator of the current level of predation risk.

Differences in Growth and Maturation of Blacknose Dace (Rhinichthys atratulus) across an Urban-Rural Gradient

Abstract To investigate changes in the biology of blacknose dace (Rhinichthys atratulus) populations accompanying watershed urbanization, we sampled dace from four watersheds in the Baltimore, Maryland area, representing a gradient from urbanized to rural conditions. Dace from the most urbanized watershed grew to greater standard lengths during their first year of life when compared to dace from other watersheds but grew little during their second year. Dace from the other watersheds showed slower growth during their first year but continued to grow through age II. Approximately 90% of age I dace from the most urbanized watershed were mature at age I, whereas only 25% of age I dace from the other watersheds were mature. Dace from the most urbanized watershed also reached maturity at shorter standard lengths than dace from the other watersheds. Growth and maturation of dace from the most rural watershed were similar to those reported for dace from other regions. We conclude that watershed urbanization results in increased growth rates of young blacknose dace, and in heavily urbanized (> 90% urban land use) watersheds, decreased age and size at maturity.

Risk Assessment and Anti-Predator Behavior of Wood Frog (Rana sylvatica) Tadpoles: A Comparison with Green Frog (Rana clamitans) Tadpoles

Abstract This study combines three experiments that identify how Wood Frog (Rana sylvatica) tadpoles assess risk from chemical cues produced by larval dragonflies (Anax junius) preying on conspecifics. I also compare the results to previous studies using Green Frog (Rana clamitans) tadpoles. The results suggest that Wood Frog tadpoles largely assess predation risk through Anax chemical cues similarly to Green Frog tadpoles. This is to be expected because the tadpoles are congeneric and both face predation from Anax in the field. However, their behavioral response to a particular level of perceived risk differs. Wood Frog tadpoles reduced their total activity (swimming and feeding) for a shorter time than Green Frog tadpoles. Wood Frog tadpoles also reduced their feeding activity more strongly than their swimming activity during cue exposure. I relate the differences between the behavioral responses of Wood Frog and Green Frog tadpoles to differences in their life-history strategies.

The Influence of the Circadian Rhythm of Green Frog (Rana clamitans) Tadpoles on Their Antipredator Behavior and the Strength of the Nonlethal Effects of Predators

Prey trade off predation risk and foraging gain in their activity level. Their response to this trade‐off mediates direct and indirect interactions between predators and the community (i.e., nonlethal effects). A prey’s activity level may also vary independently because of circadian rhythms. I tested how the antipredator behavior of green frog (Rana clamitans) tadpoles can be influenced by their circadian rhythm (primarily nocturnal feeding) and how the strengths of nonlethal effects vary in turn. Tadpoles exhibited stronger activity reductions when under predation risk during the day (which may result in stronger resource depression). However, when predation risk was high and persistent, tadpoles remained inactive during both day and night. Consequently, the nonlethal effect on tadpoles (growth rate reduction) was more negative at night. Predicting prey behavior and its effects requires identifying how their perceived risk interacts with and is limited by all factors that can influence their response.

Portfolio theory as a management tool to guide conservation and restoration of multi‐stock fish populations

Habitat degradation and harvest have upset the natural buffering mechanism (i.e., portfolio effects) of many large-scale multi-stock fisheries by reducing spawning stock diversity that is vital for generating population stability and resilience. The application of portfolio theory offers a means to guide management activities by quantifying the importance of multi-stock dynamics and suggesting conservation and restoration strategies to improve naturally occurring portfolio effects. Our application of portfolio theory to Lake Erie Sander vitreus (walleye), a large population that is supported by riverine and open-lake reef spawning stocks, has shown that portfolio effects generated by annual inter-stock larval fish production are currently suboptimal when compared to potential buffering capacity. Reduced production from riverine stocks has resulted in a single open-lake reef stock dominating larval production, and in turn, high inter-annual recruitment variability during recent years. Our analyses have shown (1) a weak average correlation between annual river and reef larval production (ρ = 0.24), suggesting that a natural buffering capacity exists in the population, and (2) expanded annual production of larvae (potential recruits) from riverine stocks could stabilize the fishery by dampening inter-annual recruitment variation. Ultimately, our results demonstrate how portfolio theory can be used to quantify the importance of spawning stock diversity and guide management on ecologically relevant scales (i.e., spawning stocks) leading to greater stability and resilience of multi-stock populations and fisheries.

Perceptual limits to predation risk assessment in green frog ( Rana clamitans ) tadpoles

Summary Many prey assess predation risk through information sources that decline in reliability over time (i.e., the information sources indicate a wider range of potential predation risk levels over time until they provide no information about the current predation risk). However, prey may lack the perceptual ability to accurately assess the reliability of ageing information sources. Here, evidence is provided that suggests that green frog {Rana clamitans) tadpoles are unable to assess the age of the chemical cue of predatory larval dragonflies (Anax junius) upon exposure to cue up to 48 h old (but can at 72 h). As a result, tadpoles may overestimate the level of risk when they encounter aged Anax chemical cue, resulting in a disproportionately strong behavioural response. In general, the results suggest that the predation risk assessment of prey depends not only on the objective characteristics of the information source, but also on the perceptual limitations of the prey. Prey may lack the context to accurately assess information sources and may consequently misestimate the actual level of predation risk.

Particle Backtracking Improves Breeding Subpopulation Discrimination and Natal-Source Identification in Mixed Populations

We provide a novel method to improve the use of natural tagging approaches for subpopulation discrimination and source-origin identification in aquatic and terrestrial animals with a passive dispersive phase. Our method integrates observed site-referenced biological information on individuals in mixed populations with a particle-tracking model to retrace likely dispersal histories prior to capture (i.e., particle backtracking). To illustrate and test our approach, we focus on western Lake Erie’s yellow perch (Perca flavescens) population during 2006–2007, using microsatellite DNA and otolith microchemistry from larvae and juveniles as natural tags. Particle backtracking showed that not all larvae collected near a presumed hatching location may have originated there, owing to passive drift during the larval stage that was influenced by strong river- and wind-driven water circulation. Re-assigning larvae to their most probable hatching site (based on probabilistic dispersal trajectories from the particle backtracking model) improved the use of genetics and otolith microchemistry to discriminate among local breeding subpopulations. This enhancement, in turn, altered (and likely improved) the estimated contributions of each breeding subpopulation to the mixed population of juvenile recruits. Our findings indicate that particle backtracking can complement existing tools used to identify the origin of individuals in mixed populations, especially in flow-dominated systems.