Scaling of fast-start performance and its thermal dependence in mummichog Fundulus heteroclitus.

Fast-start predator-escape performance and its sensitivity to temperature (24, 30, and 36°C) were evaluated in mummichog Fundulus heteroclitus across a range of body sizes spanning YOY to adult (35-68 mm standard length). Mummichogs exhibit isometry of body dimensions and areas of the dorsal and anal fins but negative allometry of the caudal fin area. These scaling relationships are consistent with observed decreases in fast-start angular velocities with increasing body size. Linear velocity, on the contrary, does not vary with size, and both large and small mummichogs are capable of traversing similar distances in a given amount of time. In addition, temperature influences fast-start performance in similar ways over the size range, though the magnitude of the effect varies with size for some performance measures. In general, fast-start performance increases with test temperature, but mummichogs acclimated to warmer temperatures exhibit lower performance at each test temperature. Altogether, our results suggest that mummichogs across the adult size range may suffer decreases in their predator-escape performance as increasing sea temperatures combine with short-term temperature fluctuations in the estuaries these fish occupy.

Gene expression underlying variation in the survival skills of red drum larvae (Sciaenops ocellatus).

Mortality rates of marine fish larvae are incredibly high and can determine year-class strength. The major causes of larval mortality are predation and starvation, and the performance of larvae in survival skills that can mitigate this mortality (predator evasion, foraging) varies among individuals and cohorts, but the causes of the variation are not known. Transcriptomics can link gene expression variation to phenotypic variation at the whole-system level to investigate the molecular basis of behavioural variation. We used tag-based RNA-sequencing to examine the molecular basis of variation in predator evasion and routine swimming (trait related to foraging efficiency) in the larval red drum, Sciaenops ocellatus. We looked for functional gene networks in which interindividual variation would explain variation in larval behavioural performance. We identified co-expressed gene groups ("modules") associated with predator evasion traits and found enrichment of motor, neural and energy metabolism pathways. These functional associations and pattern of correlations between modules and traits suggest that energy availability and allocation were responsible for the magnitude of startle responses, while differential neural and motor activation were associated with differences in response latency.

Behavioural responses of threespine stickleback with lateral line asymmetries to experimental mechanosensory stimuli.

Behavioural asymmetry, typically referred to as laterality, is widespread among bilaterians and is often associated with asymmetry in brain structure. However, the influence of sensory receptor asymmetry on laterality has undergone limited investigation. Here we used threespine stickleback (Gasterosteus aculeatus) to investigate the influence of lateral line asymmetry on laterality during lab simulations of three mechanosensation-dependent behaviours: predator evasion, prey localization and rheotaxis. We recorded the response of stickleback to impacts at the water surface and water flow in photic conditions and low-frequency oscillations in the dark, across four repeat trials. We then compared individuals' laterality with asymmetry in the number of neuromasts on either side of their body. Stickleback hovered with their right side against the arena wall 57% of the time (P<0.001) in illuminated surface impact trials and 56% of the time (P=0.085) in dark low-frequency stimulation trials. Light regime modulated the effect of neuromast count on laterality, as fish with more neuromasts were more likely to hover with the wall on their right during illumination (P=0.007) but were less likely to do so in darkness (P=0.025). Population-level laterality diminished in later trials across multiple behaviours and individuals did not show a consistent side bias in any behaviours. Our results demonstrate a complex relationship between sensory structure asymmetry and laterality, suggesting that laterality is modulated by multiple sensory modalities and is temporally dynamic.

Behavioural and physiological responses to low- and high-intensity locomotion in Chinese shrimp Fenneropenaeus chinensis.

We explored stroke behaviour, energy sources, and their related metabolic enzymes during multi-intensity swimming and tail-flipping at low- and high-intensity modes in Chinese shrimp Fenneropenaeus chinensis. In swimming, shrimp were encouraged to swim at velocities of 3, 6, 9 cm s-1 for 200 min (low-intensity), and at 12, 15, 18 cm s-1 until fatigue (high-intensity). In tail-flipping, shrimp were encouraged to tail-flip by tapping cephalothorax at frequencies of 0.020, 0.040, 0.063 Hz (one tap every 50, 25, 16 s) for 5 min (low-intensity), and at 0.083, 0,100, 0.125 Hz (one tap every 12, 10, 8 s) until no response (high-intensity). Results showed that shrimp increased stroke rates of pleopods and uropods to elevate swimming and tail-flipping ability. For low-intensity locomotion, glycogen was burned in aerobic pathway due to low pleopods beat frequency in swimming; however, glycogen was anaerobically burned due to high uropods beat amplitude in tail-flipping. Anaerobic metabolism occurred in high-intensity locomotion in either swimming or tail-flipping. Critical contents of muscle lactate causing locomotion fatigue might be around threefold of rest condition. Shrimp reduced locomotive time to avoid glycogen exhaustion and lactate accumulation during high-intensity locomotion. These findings highlight our understanding of physiological mechanisms of locomotion activities in shrimp.

Resolving tradeoffs among crypsis, escape behavior, and microhabitat use in sexually dichromatic species.

Variation in color pattern between populations of cryptic animals is common and typically attributed to selection pressures from visual predators combined with variation in substrate composition. However, little is known about how cryptic color pattern relates to varied rates of predation, and few studies simultaneously analyze patterns of escape behavior and microhabitat use along with variation in color pattern, even though these traits evolve in tandem. Here, we use a combination of calibrated photographs and spectrometry to examine the influence of spatial heterogeneity in rates of predation on dorsal brightness in the Florida scrub lizard (Sceloporus woodi), a cryptic and sexually dimorphic species. Simultaneously, we analyze patterns of escape behavior and microhabitat use measured in the field. The results of this study indicate that populations inhabiting environments of increased predation have less color variation and more closely match the color of local substrate than populations sampled in environments of relaxed predation. Populations exposed to increased predation also show more pronounced escape behavior and are more selective in their use of microhabitat. Interestingly, geographic variation of dorsal brightness, escape behavior, and microhabitat use were greater for females than for males. Our results not only provide empirical evidence for theories of adaptive coloration, but suggest that sexual dichromatism can be maintained by selection pressures related to predation.

Thermal modulation of anthropogenic estrogen exposure on a freshwater fish at two life stages.

Human-mediated environmental change can induce changes in the expression of complex behaviors within individuals and alter the outcomes of interactions between individuals. Although the independent effects of numerous stressors on aquatic biota are well documented (e.g., exposure to environmental contaminants), fewer studies have examined how natural variation in the ambient environment modulates these effects. In this study, we exposed reproductively mature and larval fathead minnows (Pimephales promelas) to three environmentally relevant concentrations (14, 22, and 65ng/L) of a common environmental estrogen, estrone (E1), at four water temperatures (15, 18, 21, and 24°C) reflecting natural spring and summer variation. We then conducted a series of behavioral experiments to assess the independent and interactive effects of temperature and estrogen exposure on intra- and interspecific interactions in three contexts with important fitness consequences; reproduction, foraging, and predator evasion. Our data demonstrated significant independent effects of temperature and/or estrogen exposure on the physiology, survival, and behavior of larval and adult fish. We also found evidence suggesting that thermal regime can modulate the effects of exposure on larval survival and predator-prey interactions, even within a relatively narrow range of seasonally fluctuating temperatures. These findings improve our understanding of the outcomes of interactions between anthropogenic stressors and natural abiotic environmental factors, and suggest that such interactions can have ecological and evolutionary implications for freshwater populations and communities.

Effects of developmental exposure to neurotoxic algal metabolites on predator-prey interactions in larval Pimephales promelas.

Harmful algal blooms are a growing environmental concern in aquatic systems. Although it is known that some of the secondary metabolites produced by cyanobacteria can alter predator-prey dynamics in aquatic communities by reducing foraging and/or predator evasion success, the mechanisms underpinning such responses are largely unknown. In this study, we examined the effects of a potent algal neurotoxin, ß-N-methylamino-L-alanine (BMAA), on the development and behavior of larval Fathead Minnows, Pimephales promelas, during predator-prey interactions. We exposed eggs and larvae to environmentally relevant concentrations of BMAA for 21 days, then tested subjects in prey-capture and predator-evasion assays designed to isolate the effects of exposure at sequential points of the stimulus-response pathway. Exposure was associated with changes in the ability of larvae to detect and respond to environmental stimuli (i.e., a live prey item and a simulated vibrational predator), as well as changes in behavior and locomotor performance during the response. Our findings suggest that chronic exposure to neurodegenerative cyanotoxins could alter the outcomes of predator-prey interactions in natural systems by impairing an animal's ability to perceive, process, and respond to relevant biotic stimuli.

Multiple preferred escape trajectories are explained by a geometric model incorporating prey's turn and predator attack endpoint.

The escape trajectory (ET) of prey - measured as the angle relative to the predator's approach path - plays a major role in avoiding predation. Previous geometric models predict a single ET; however, many species show highly variable ETs with multiple preferred directions. Although such a high ET variability may confer unpredictability to avoid predation, the reasons why animals prefer specific multiple ETs remain unclear. Here, we constructed a novel geometric model that incorporates the time required for prey to turn and the predator's position at the end of its attack. The optimal ET was determined by maximizing the time difference of arrival at the edge of the safety zone between the prey and predator. By fitting the model to the experimental data of fish Pagrus major, we show that the model can clearly explain the observed multiple preferred ETs. By changing the parameters of the same model within a realistic range, we were able to produce various patterns of ETs empirically observed in other species (e.g., insects and frogs): a single preferred ET and multiple preferred ETs at small (20-50°) and large (150-180°) angles from the predator. Our results open new avenues of investigation for understanding how animals choose their ETs from behavioral and neurosensory perspectives.

When a prey spots a predator about to pounce, it turns swiftly and accelerates away to avoid being captured. The initial direction the prey chooses to take ­ known as its escape trajectory ­ can greatly impact their chance of survival. Previous models were able to predict the optimal direction an animal should take to maximize its chances of evading the predator. However, experimental data suggest that prey actually tend to escape via multiple specific directions, although why animals use this approach has not been clarified. To investigate this puzzle, Kawabata et al. built a new mathematical model that better represents how prey and predators interact with one another in the real world. Unlike past models, Kawabata et al. incorporated the time required for prey to change direction and only allowed the predators to move toward the prey for a limited distance. By including these two factors, they were able to reproduce the escape trajectories of real animals, including a species of fish, as well as species from other taxa such as frogs and insects. The new model suggests that prey escape along one of two directions: either by moving directly away from the predator in order to outrun its attack, or by dodging sideways to avoid being captured. Which strategy the prey chooses has some elements of unpredictability, which makes it more difficult for predators to adjust their capturing method. These findings shed light on why escaping in multiple specific directions makes prey harder to catch. The model could also be extended to test the escape trajectories of a wider variety of predator and prey species, which may avoid capture via different routes. This could help researchers better understand how predators and prey interact with one another. The findings could also reveal how sensory information (such as sound and sight) associated with the threat of an approaching predator is processed and stimulates the muscle activity required to escape in multiple different directions.

The effects of familiarity on escape responses in the Trinidadian guppy (Poecilia reticulata).

Predation is the main cause of mortality during early life stages. The ability to avoid and evade potential threats is, therefore, favoured to evolve during the early stages of life. It is also during these early stages that the process of familiarization occurs. It has long been recognized that associating with familiar individuals confers antipredator benefits. Yet gaps in our knowledge remain about how predator evasion is affected by social experience during early stages. In this study, we test the hypothesis that familiarization acquired during early life stages improves escape responses. Using the guppy Poecilia reticulata, we examine the effect of different recent social conditions in the three main components of predator evasion. Using high-speed motion analysis, we compared the number of individuals in each test group that responded to a visual stimulus, their reactive distance and magnitude of their response (maximum speed, maximum acceleration and distance) in groups composed either of familiar or non-familiar individuals. Contrary to the prediction, groups composed of familiar individuals were less responsive than groups of unfamiliar individuals. Reactive distance and magnitude of response were more dependent on individual size rather than on familiarity. Larger individuals reached higher maximum speeds and total distances in their escape response. Our result indicates that familiarity is likely to affect behaviour earlier in a predator-prey interaction, which then affects the behavioural component of the response. Taken together, our study contributes to previous ones by distinguishing which components of an escape response are modulated by familiarity.

Mixed flocks and polyspecific associations: Costs and benefits of mixed groups to birds and monkeys.

This review examines the diversity of avian mixed foraging flocks with the goal of relating the conclusions to primate polyspecific associations. Mixed associations are considered as adaptations for achieving an optimal balance between predator protection and feeding efficiency. In open habitat, predator and prey are able to detect each other at a distance and feeding competition is low, especially in species that subsist on a homogeneously distributed food supply. These conditions favor large groups of variable composition. In closed habitats, predators attack at close range, so early warning alarm systems are at a premium. Feeding competition is often intense because food resources such as fruit, flushing leaves, and nectar are spatially concentrated. Since feeding competition is generally less between than within species, these conditions favor mixed associations composed of small numbers of several to many species, and the evolution of elaborate early warning systems to thwart predators. The primate polyspecific associations that have been studied to date share characteristics with the closed habitat model while exhibiting some important distinctions. Primate associations are made up of integral troops, not individuals, implying high incremental costs of joining. These costs, plus a paucity of ecologically compatible combinations of species, seem to limit primate polyspecific associations geographically to regions in which the presence of monkey-eating raptors provides a strong incentive for aggregation.