Predator Avoidance Responses Research Articles

Fluoxetine inhibits predator avoidance behavior in tadpoles

Fluoxetine is a selective serotonin re-uptake inhibitor used to treat anxiety and depression in humans. It has been detected as a contaminant in the surface waters in many countries. The effects of fluoxetine (0, 0.03, 0.3, and 3 μg L−1) on the swimming and behavioral responses of Bufo arabicus tadpoles to alarm chemicals from predatory dragonfly larvae (Anax imperator) were measured. Fluoxetine significantly reduced swimming speed at 0.3 and 3 μg L−1 in the absence of predator alarm chemicals but had no effect in their presence. Tadpoles exposed to predator alarm chemicals avoided open water and preferred to hide. Exposure to fluoxetine at 3 μg L−1 completely eliminated this predator avoidance response, making the tadpoles more vulnerable to predation.

Personality and the response to predation risk: effects of information quantity and quality

Within aquatic ecosystems, chemosensory cues provide valuable public information regarding the form and degree of risk, allowing prey to make informed behavioural decisions. Such cues, however, may vary in both relative concentration detected (i.e. 'quantity') and reliability of the information available (i.e. 'quality'), leading to varying response patterns. Moreover, prey species are also known to exhibit consistent behavioural tactics towards managing risk (i.e. personality), possibly shaping their use of public information. Here, we present two experiments examining the potential interacting effects of personality and the quantity (Experiment 1) or quality (Experiment 2) of public information on the short-term predator avoidance responses of wild-caught Trinidadian guppies under semi-natural conditions. Our first experiment demonstrated that personality shaped responses to a high concentration of alarm cues (high risk), with shyer guppies exhibiting stronger antipredator responses than bolder guppies. When exposed to either low risk or stream water controls, personality had no effect on the intensity of response. Our second experiment demonstrated that personality again shaped the response to high concentrations of alarm cues (a known risk) but not to a novel chemosensory cue (tilapia odour). When exposed to the unknown novel cue, guppies exhibited a relatively high intensity antipredator response, regardless of personality. Combined, our results suggest that individual risk-taking tactics shape the use of public information in a context-dependent fashion.

Local adaptation and the potential effects of a contaminant on predator avoidance and antipredator responses under global warming: a space‐for‐time substitution approach

The ability to deal with temperature-induced changes in interactions with contaminants and predators under global warming is one of the outstanding, applied evolutionary questions. For this, it is crucial to understand how contaminants will affect activity levels, predator avoidance and antipredator responses under global warming and to what extent gradual thermal evolution may mitigate these effects. Using a space-for-time substitution approach, we assessed the potential for gradual thermal evolution shaping activity (mobility and foraging), predator avoidance and antipredator responses when Ischnura elegans damselfly larvae were exposed to zinc in a common-garden warming experiment at the mean summer water temperatures of shallow water bodies at southern and northern latitudes (24 and 20°C, respectively). Zinc reduced mobility and foraging, predator avoidance and escape swimming speed. Importantly, high-latitude populations showed stronger zinc-induced reductions in escape swimming speed at both temperatures, and in activity levels at the high temperature. The latter indicates that local thermal adaptation may strongly change the ecological impact of contaminants under global warming. Our study underscores the critical importance of considering local adaptation along natural gradients when integrating biotic interactions in ecological risk assessment, and the potential of gradual thermal evolution mitigating the effects of warming on the vulnerability to contaminants.

Effects of visual and chemical cues on orientation behavior of the Red Sea hermit crab Clibanarius signatus

Directional orientation of Clibanarius signatus toward different targets of gastropod shells was studied in a circular arena upon exposure to background seawater, calcium concentrations and predatory odor. Directional orientation was absent when crabs were presented with the white background alone. Each shell was tested in different positions (e.g., anterior, posterior, upside-down, lateral). Adult crabs were tested without their gastropod shells, and orientation varied with concentration and chemical cue. With calcium, orientation increased as concentration increased up to a maximum attraction percentage and then attraction became stable. In the case of predator cues, some individuals swim away from the target toward the opposite direction representing a predator avoidance response. Whenever, the blind hermit crab C. signatus was exposed to a shell target combined with calcium or predator cues, the majority of them stop moving or move in circles around the arena center. The others exhibited uniform orientation distribution. The responsiveness was higher with calcium cues than predator cues. Thus in the absence of vision, individual hermit crabs were able to detect both calcium and predator cues and have different response regarding them.

Flicker is part of a multi-cue response criterion in fiddler crab predator avoidance

Predator avoidance behaviour costs time, energy and opportunities, and prey animals need to balance these costs with the risk of predation. The decisions necessary to strike this balance are often based on information that is inherently imperfect and incomplete because of the limited sensory capabilities of prey animals. Our knowledge, however, about how prey animals solve the challenging task of restricting their responses to the most dangerous stimuli in their environment is very limited. Using dummy predators, we examined the contribution of visual flicker to the predator avoidance response of the fiddler crab Uca vomeris. The results illustrate that crabs let purely black or purely white dummies approach significantly closer than black-and-white flickering dummies. We show that this effect complements other factors that modulate escape timing such as retinal speed and the crab's distance to its burrow, and is therefore not due exclusively to an earlier detection of the flickering signal. By combining and adjusting a range of imperfect response criteria in a way that relates to actual threats in their natural environment, prey animals may be able to measure risk and adjust their responses more efficiently, even under difficult or noisy sensory conditions.

Continuous neurogenesis in the adult forebrain is required for innate olfactory responses

Although the functional significance of adult neurogenesis in hippocampal-dependent learning and memory has been well documented, the role of such neurogenesis in olfactory activity is rather obscure. To understand the significance of adult neurogenesis in olfactory functions, we genetically ablated newly born neurons by using tamoxifen-treated Nestin-CreER(T2);neuron-specific enolase-diphtheria toxin fragment A (NSE-DTA) mice. In these mice, tamoxifen-inducible Cre recombinase allows the NSE (Eno2) gene to drive DTA expression in differentiating neurons, leading to the efficient ablation of newly born neurons in the forebrain. These mutant mice were capable of discriminating odors as competently as control mice. Strikingly, although control and mutant mice frequently showed freezing behaviors to a fox scent, a predator odor, mutant mice approached this odor when they were conditioned to associate the odor with a reward, whereas control mice did not approach the odor. Furthermore, although mutant males and females showed normal social recognition behaviors to other mice of a different sex, mutant males displayed deficits in male-male aggression and male sexual behaviors toward females, whereas mutant females displayed deficits in fertility and nurturing, indicating that sex-specific activities, which are known to depend on olfaction, are impaired. These results suggest that continuous neurogenesis is required for predator avoidance and sex-specific responses that are olfaction dependent and innately programmed.

Natural visual cues eliciting predator avoidance in fiddler crabs

To efficiently provide an animal with relevant information, the design of its visual system should reflect the distribution of natural signals and the animal's tasks. In many behavioural contexts, however, we know comparatively little about the moment-to-moment information-processing challenges animals face in their daily lives. In predator avoidance, for instance, we lack an accurate description of the natural signal stream and its value for risk assessment throughout the prey's defensive behaviour. We characterized the visual signals generated by real, potentially predatory events by video-recording bird approaches towards an Uca vomeris colony. Using four synchronized cameras allowed us to simultaneously monitor predator avoidance responses of crabs. We reconstructed the signals generated by dangerous and non-dangerous flying animals, identified the cues that triggered escape responses and compared them with those triggering responses to dummy predators. Fiddler crabs responded to a combination of multiple visual cues (including retinal speed, elevation and visual flicker) that reflect the visual signatures of distinct bird and insect behaviours. This allowed crabs to discriminate between dangerous and non-dangerous events. The results demonstrate the importance of measuring natural sensory signatures of biologically relevant events in order to understand biological information processing and its effects on behavioural organization.

Animal personality

Animal personality

Predator avoidance performance of larval fathead minnows ( Pimephales promelas) following short-term exposure to estrogen mixtures

Aquatic organisms exposed to endocrine disrupting compounds (EDCs) at early life-stages may have reduced reproductive fitness via disruption of reproductive and non-reproductive behavioral and physiological pathways. Survival to reproductive age relies upon optimal non-reproductive trait expression, such as adequate predator avoidance responses, which may be impacted through EDC exposure. During a predator–prey confrontation, larval fish use an innate C-start escape behavior to rapidly move away from an approaching threat. We tested the hypotheses that (1) larval fathead minnows exposed to estrogens, a primary class of EDCs, singularly or in mixture, suffer a reduced ability to perform an innate C-start behavior when faced with a threat stimulus; (2) additive effects will cause greater reductions in C-start behavior; and (3) effects will differ among developmental stages. In this study, embryos (post-fertilization until hatching) were exposed for 5 days to environmentally relevant concentrations of estrone (E1), 17β-estradiol (E2), and 17α-ethinylestradiol (EE2) singularly and in mixture. Exposed embryos were allowed to hatch and grow in control well water until 12 days old. Similarly, post-hatch fathead minnows were exposed for 12 days to these compounds. High-speed (1000 frames/s) video recordings of escape behavior were collected and transferred to National Institutes of Health Image for frame-by-frame analysis of latency period, escape velocity, and total escape response (combination of latency period and escape velocity). When tested 12 days post-hatch, only E1 adversely affected C-start performance of larvae exposed as embryos. Conversely, larvae exposed for 12 days post-hatch did not exhibit altered escape responses when exposed to E1, while adverse responses were seen in E2 and the estrogen mixture. Ethinylestradiol exposure did not elicit changes in escape behaviors at either developmental stage. The direct impact of reduced C-start performance on survival, and ultimately, reproductive fitness provides an avenue to assess the ecological relevance of exposure in an assay of relatively short duration.

Response of small rodents to manipulations of vegetation height in agro‐ecosystems

Some small mammal populations require human interference to conserve rare or threatened species or to minimize adverse effects in plant production. Without a thorough understanding about how small rodents behave in their environment and consideration of how they react to management efforts, management will not be optimal. Social behavior, spatial and temporal activity patterns, predator avoidance and other behavioral responses can affect pest rodent management. Some of these behavioral patterns and their causes have been well studied. However, their impact on pest rodent management, especially for novel management approaches, is not always clear. Habitat manipulation occurs necessarily through land use and intentionally to reduce shelter and food availability and to increase predation pressure on rodents. Rodents often respond to decreased vegetation height with reduced movements and increased risk sensitivity in their feeding behavior. This seems to result mainly from an elevated perceived predation risk. Behavioral responses may lessen the efficacy of the management because the desired effects of predators might be mediated. It remains largely unknown to what extent such responses can compensate at the population level for the expected consequences of habitat manipulation and how population size and crop damage are affected. It is advantageous to understand how target and non-target species react to habitat manipulation to maximize the management effects by appropriate techniques, timing and spatial scale without causing unwanted effects at the system level.

Using an individual-based model to examine the roles of habitat fragmentation and behavior on predator–prey relationships in seagrass landscapes

Seagrasses, which form critical subtidal habitats for marine organisms worldwide, are fragmented via natural processes but are increasingly being fragmented and degraded by boating, fishing, and coastal development. We constructed an individual-based model to test how habitat fragmentation and loss influenced predator–prey interactions and cohort size for a group of settling juvenile blue crabs (Callinectes sapidus Rathbun) in seagrass landscapes. Using results from field studies suggesting that strong top-down processes influence the relationship between cannibalistic blue crab populations and seagrass landscape structure, we constructed a model in which prey (juvenile blue crabs) are eaten by mesopredators (larger blue crabs) which in turn are eaten by top-level predators (e.g., large fishes). In our model, we varied the following parameters within four increasingly fragmented seagrass landscapes to test for their relative effects on cohort size: juvenile blue crab (prey) predator avoidance response, hunting ability of mesopredators and predators, the presence of a top-level predator, and prey settlement routines. Generally, prey cohort size was maximized in the presence of top-level predators and when mesopredators and predators exhibited random searching behavior vs. directed hunting. Cohort size for stationary (tethered) prey was maximized in fragmented landscapes, which corresponds to results from field experiments, whereas mobile prey able to detect and avoid predators had higher survival in continuous landscapes. Prey settlement patterns had relatively small influences on cohort size. We conclude that the effects of seagrass fragmentation and loss on organisms such as blue crabs will depend heavily on behaviors of prey and predatory organisms and how these behaviors change with landscape structure.

Learning, memory and predator avoidance by freshwater snails: effects of experience on predator recognition and defensive strategy

Learning may allow animals to fine-tune predator avoidance responses to specific environments, but the degree to which predator avoidance behaviour depends on experience is not known for most taxa. We assessed whether perception of predation risk and choice of defensive strategies by the snail Physa acuta is influenced by experience by performing three experiments in which we manipulated exposure to predators and then assayed behavioural responses to predator cues. We first assessed the scope for learned avoidance behaviour by comparing the antipredator response of wild snails (exposed to predators) and captive-reared snails (not exposed to predators). Wild-caught snails showed a stronger response than did captive-reared snails to predators feeding on insect prey, predators feeding on snails and crushed-snail cues. A second experiment in which snails were reared with and without exposure to crayfish predators showed that snails from both rearing treatments responded to fish and crayfish, but the choice of defensive strategy depended on experience. Snails reared without exposure to predators responded to fish cues by moving under cover, whereas snails reared with crayfish responded to fish by moving to the water's surface. The final experiment also manipulated exposure to predators and showed that although snails from a fish-free pond responded to both fish and crayfish, their responses did not depend on experience. Overall, the effects of experience were significant but small relative to the overall effects of predator cues on snail habitat use, showing that the antipredator responses of P. acuta are largely innate.

Factors controlling the tentacle and polyp expansion behaviour of selected temperate Anthozoa

Although the factors influencing patterns of expansion and contraction of polyps and tentacles for tropical anthozoans has been well described there is still little information for temperate species. This study investigated the patterns of tentacle and polyp expansion behaviour of nine species of temperate Anthozoa in response to current flow, turbulence, food availability and time of day (light) at Lough Hyne Marine Nature Reserve (Ireland). In the absence of current flow, Metridium senile, Caryophyllia smithii, Alcyonium hibernicum and Corynactis viridis exhibited nocturnal expansion of polyps or tentacles with contraction occurring in the daytime, while Alcyonium digitatum, Actinia equina and Cerianthus lloydii showed no differences between light and dark periods. The symbiont containing species Anthopleura ballii and Anemonia viridis expanded or raised their tentacles during daylight hours (tentacle contraction is not possible for A. viridis), although in shallow waters (3 m) Anthopleura ballii tentacles were contracted at midday (highest light levels) presumably to prevent damage from ultraviolet radiation. The contraction of tentacles during light periods was considered a predator avoidance response since zooplankton availability did not vary between light and dark periods, while predator abundance (particularly fish) is greater during daylight. Even though M. senile, Alcyonium hibernicum and Corynactis viridis showed little expansion during daylight periods in the absence of current flow, tentacles and polyps were expanded at midday during periods of high current flow. A greater number of expanded polyps and tentacles were also recorded for A. digitatum, Anemonia viridis and Cerianthus lloydii during high flow conditions compared with periods of low/no flow (Caryophyllia smithii not examined). Actinia equina only exhibited tentacle expansion in response to the creation of a turbulent flow regime, which was determined from laboratory observations. Since species demonstrating contraction during daylight in the absence of current flow expanded their tentacles and polyps when subjected to high current flow, the need for feeding appears to be more important than predator avoidance in controlling expansion behaviour.

Wetland Restoration for Amphibians: Should Local Sites Be Designed to Support Metapopulations or Patchy Populations?

Abstract Pond‐breeding amphibians have been characterized as having metapopulation structure, and a goal of many local restoration projects is to establish viable metapopulations. However, recent studies suggest that metapopulation organization is unlikely at the local level because of high dispersal rates between neighboring ponds. Although many amphibians avoid ovipositing in habitats that pose high predation risk to their offspring, the spatial scale of avoidance is poorly resolved for natural systems and could involve wholesale movements between ponds. To determine the scale of avoidance, we monitored annual habitat use by the Wood frog (Rana sylvatica), American toad (Bufo americanus), and Spotted salamander (Ambystoma maculatum) at a restoration site in western North Carolina, U.S.A. Wood frogs consistently used most fish‐free ponds, but rapidly curtailed use following fish invasions. American toads rarely used the same breeding site from year to year, and adults strongly avoided ovipositing in habitats with predatory Wood frog tadpoles. Spotted salamanders exhibited a predator avoidance response to fish that was weaker than the predator avoidance response of anurans. Our data indicate that the spatial scale of predator avoidance by ovipositing amphibians often exceeds that of an individual pond and that the focal species at this site are organized as patchy populations rather than as metapopulations. At local restoration sites, ponds that are placed in spatial arrays to create metapopulations may not accomplish their goal and may limit the extent to which ovipositing adults can express an adaptive antipredator behavior. We discuss an alternative design that is more likely to enhance the long‐term persistence of local populations.

EFFECTS OF WIND ON THE BEHAVIOR AND CALL TRANSMISSION OF PIKAS (OCHOTONA PRINCEPS)

It has been suggested that pikas are less active during inclement weather. We hypothesized that this decrease in activity is a predator-avoidance response to wind conditions that decrease the effectiveness of the alarm calls of pikas. We examined this hypothesis by broadcasting and rerecording the prominent frequencies (900–5,500 Hz) of pikas’ calls and by observing behavior of focal pikas during varying weather conditions. Both attenuation of pure tones and the amount of wind noise increased significantly as wind speed increased. Additionally, wind direction created asymmetrical patterns of attenuation of pure tones, potentially distorting and degrading the call. Further, pikas spent significantly more time inactive at higher wind speeds, with nonvigilant active behaviors decreasing at a higher rate than vigilant active behaviors. Examination of these data supports the hypothesis and suggests that wind influences the behavior of animals that rely on alarm calls.

Predator avoidance in fiddler crabs: 2. The visual cues

The efficiency of predator avoidance strategies depends on the availability and accuracy of sensory information. Although vision can in principle provide instant information on a predator's position, direction of approach and identity, prey animals that face fast predators have to respond so early (close to the limits of detection) that visual cues are unreliable predictors of actual risk. This is a major problem for prey animals that have to balance predation risk with the cost of antipredator action. I investigated the visual cues fiddler crabs Uca vomeris use to decide when to run towards their burrow in response to an approaching (dummy) predator by running towards their burrow. The crabs did not always escape immediately when they first detected the dummy, but continued to monitor and assess its approach. The crabs relied on retinal image speed to trigger a home run. Retinal speed did not correlate well with the actual risk of predation because it confounded a predator's direction of approach with its speed and proximity. In an attempt to reconcile what is known about predator avoidance in semiterrestrial crabs, I propose a two-tier antipredator response system and discuss the crabs' multistage response strategy in the context of the associated costs and the availability of information. Multistage predator avoidance, which is common among prey animals, appears to be designed to improve the quality of information in an attempt to minimize the costs associated with predator avoidance responses.

Effects of Microphallus turgidus (Trematoda: Microphallidae) on the predation, behavior, and swimming stamina of the grass shrimp Palaemonetes pugio.

The effect of the trematode Microphallus turgidus on its second intermediate host, the grass shrimp, Palaemonetes pugio, was tested. To do so, we measured the susceptibility of infected and uninfected shrimp to predation by the mummichog, Fundulus heteroclitus. Shrimp behavior was compared in the presence and absence of a fish predator, and the swimming stamina and backthrust escape responses of infected and uninfected shrimp were measured. Infected shrimp were more likely to be eaten by a predator than uninfected shrimp, had lower swimming stamina, and spent more time swimming and less time motionless in the presence of a predator. There was no difference between backthrust distances traveled in response to a stimulus by either infected or uninfected shrimp. Thus, M. turgidus may increase the predation of P. pugio in the wild, possibly by affecting the swimming stamina and predator avoidance responses of the shrimp.

Habitat–predator association and avoidance in rainbowfish (Melanotaeniaspp.)

Abstract – The ability to recall the location of a predator and later avoid it was tested in nine populations of rainbowfish (Melanotaeniaspp.), representing three species from a variety of environments. Following the introduction of a model predator into a particular microhabitat, the model was removed, the arena rotated and the distribution of the fish recorded again. In this manner it could be determined what cues the fish relied on in order to recall the previous location of the predator model. Fish from all populations but one (Dirran Creek) were capable of avoiding the predator by remembering either the location and/or the microhabitat in which the predator was recently observed. Reliance on different types of visual cues appears to vary between populations but the reason for this variation remains elusive. Of the ecological variables tested (flow variability, predator density and habitat complexity), only the level of predation appeared to be correlated with the orientation technique employed by each population. There was no effect of species identity, which suggests that the habitat that each population occupies plays a strong role in the development of both predator avoidance responses and the cues used to track predators in the wild.

Predator-induced behavioral and morphological plasticity in the tropical marine Gastropod Strombus gigas.

Florida queen conch stocks once supported a significant fishery, but overfishing prompted the state of Florida to institute a harvest moratorium in 1985. Despite the closure of the fishery, the queen conch population has been slow to recover. One method used in the efforts to restore the Florida conch population has been to release hatchery-reared juvenile conch into the wild; however, suboptimal predator avoidance responses and lighter shell weights relative to their wild counterparts have been implicated in the high mortality rates of released hatchery juveniles. We conducted a series of experiments in which hatchery-reared juvenile conch were exposed to a predator, the spiny lobster (Panulirus argus), to determine whether they could develop behavioral and morphological characteristics that would improve survival. Experiments were conducted in tanks with a calcareous sand substrate to simulate a natural environment. Conditioned conch were exposed to caged lobsters while conch in the control tanks were exposed to empty cages. Conditioned conch moved significantly less and buried themselves more frequently than the naive control conch. Morphometric data indicated that the conditioned conch grew at a significantly slower rate than the naive conch, but the shell weights of the two groups were not significantly different. This implies that the conditioned conch had thicker or denser shells than the control group. As a result, the conditioned conch had significantly higher survival than naive conch in a subsequent predation experiment in which a lobster was allowed to roam free in each tank for 24 hours. In the future, the conditioning protocols documented in this study will be used to increase the survival of hatchery-reared conch in the wild.

Lateralisation of predator avoidance responses in three species of toads

Lateralisation of responses to presentation of a simulated predator was investigated in three species of toads: two European species (the common toad, Bufo bufo, and the green toad, Bufo viridis) and one species introduced to Australia from South America, the cane toad Bufo marinus. First a simulated snake was presented moving rapidly towards the toad in the frontal field of vision and the toad's escape responses, including jumps to the right and to the left, were recorded. No significant bias in left or right side jumping was apparent in this test. Next the simulated snake was presented in the left or right lateral field of vision in random order. Escape and defensive responses were elicited more strongly, in all three species, when the stimulus was on the toad's left side compared to its right side. Reaction times scored in the experiments with B. marinus, alone, did not differ from left to right. There were, however, species differences in the types of escape responses with respect to the laterality: B. viridis and B. marinus showed similar patterns of more sideways jumps with left presentation and more frontal jumps with right presentation. Sideways jumps were not lateralised in B. bufo, but this species showed more frontal jumps when the presentation was on the left side. These findings suggest that the selective involvement of structures located in the right side of the brain (left monocular visual field) in emotional responses (particularly fear responses) could be a phylogenetic ancient trait.