Phylogenetics of swimming behaviour in Medusozoa: the role of giant axons and their possible evolutionary origin.

Although neural tissues in cnidarian hydroids have a nerve net structure, some cnidarian medusae contain well-defined nerve tracts. As an example, the hydrozoan medusa Aglantha digitale has neural feeding circuits that show an alignment and condensation, which is absent in its relatives Aequorea victoria and Clytia hemisphaerica. In some cases, neural condensations take the form of fast propagating giant axons concerned with escape or evasion. Such giant axons appear to have developed from the fusion of many, much finer units. Ribosomal DNA analysis has identified the lineage leading to giant axon-based escape swimming in Aglantha and other members of the Aglaura clade of trachymedusan jellyfish. The Aglaura, along with sister subclades that include species such as Colobonema sericeum, have the distinctive ability to perform dual swimming, i.e. to swim at either high or low speeds. However, the form of dual swimming exhibited by Colobonema differs both biomechanically and physiologically from that in Aglantha and is not giant axon based. Comparisons between the genomes of such closely related species might provide a means to determine the molecular basis of giant axon formation and other neural condensations. The molecular mechanism responsible may involve 'fusogens', small molecules possibly derived from viruses, which draw membranes together prior to fusion. Identifying these fusogen-based mechanisms using genome analysis may be hindered by the many changes in anatomy and physiology that followed giant axon evolution, but the genomic signal-to-noise ratio may be improved by examining the convergent evolution of giant axons in other hydrozoa, such as the subclass Siphonophora.

Fearless distasteful butterflies and timid mimetic butterflies: comparison of flight initiation distances in Papilioninae.

Prey are expected to flee from an approaching predator when the cost of remaining (i.e. being captured) exceeds the cost of fleeing. In species where individuals experience less predation pressure, delayed escape responses to predatory threats are predicted. Therefore, non-chalant behaviour should be observed in unpalatable and Batesian mimetic prey while rapid escape behaviour may be displayed in palatable and non-mimetic prey from closely related species. This study compared the flight initiation distances (FIDs; the distances at which a prey starts to flee during a standardized human approach) of several sympatric swallowtail butterflies (Papilionidae) in two areas with different temperate zones. As predicted, it was found that unpalatable species had significantly shorter FIDs than palatable species in both areas. By contrast, FIDs of Batesian mimic species were significantly longer than those of unpalatable model species and were not significantly different from those of palatable species. FIDs were not significantly different between mimetic and non-mimetic forms of the intraspecific polymorphic species Papilio polytes. The mimetic species or form may reduce the risk of revealing their identity (i.e. palatability) through early escape behaviour. These findings have implications for the selective forces that affect the escape tendency of prey.

(Eye-)tracking the escape from the self: guilt proneness moderates the effect of failure on self-avoidance.

Failure increases the motivation to escape self-awareness. To date, however, the role of self-conscious emotions (shame and guilt) in triggering escape responses after failure has not been sufficiently addressed. In this pre-registered study (N = 156 undergraduates), we adapted a classic paradigm (avoidance of one's image in a mirror) to a modern eye-tracking technology to test the hypothesis that shame proneness moderates the effect of failure on self-awareness avoidance. Individual differences in guilt and shame proneness were assessed before priming thoughts of failure or success. Then, an eye-tracking paradigm was used to monitor gaze avoidance of one's screen-reflected face during a neutral, unrelated task. Unexpectedly, results showed that guilt but not shame proneness exacerbated self-avoidance after failure. The present findings challenge the dominant view that shame fosters avoidance more so than guilt.

Evidence of predictive selective attention in fiddler crabs during escape in the natural environment.

Selective attention is of fundamental relevance to animals for performing a diversity of tasks such as mating, feeding, predation and avoiding predators. Within natural environments, prey animals are often exposed to multiple, simultaneous threats, which significantly complicates the decision-making process. However, selective attention is rarely studied in complex, natural environments or in the context of escape responses. We therefore asked how relatively simple animals integrate the information from multiple, concurrent threatening events. Do they identify and respond only to what they perceive as the most dangerous threat, or do they respond to multiple stimuli at the same time? Do simultaneous threats evoke an earlier or stronger response than single threats? We investigated these questions by conducting field experiments and compared escape responses of the fiddler crab Gelasimus dampieri when faced with either a single or two simultaneously approaching dummy predators. We used the dummies' approach trajectories to manipulate the threat level; a directly approaching dummy indicated higher risk while a tangentially approaching dummy that passed the crabs at a distance represented a lower risk. The crabs responded later, but on average more often, when approached more directly. However, when confronted with the two dummies simultaneously, the crabs responded as if approached only by the directly approaching dummy. This suggests that the crabs are able to predict how close the dummy's trajectory is to a collision course and selectively suppress their normally earlier response to the less dangerous dummy. We thus provide evidence of predictive selective attention within a natural environment.

Context-dependent behavioural lateralization in the European pond turtle, Emys orbicularis (Testudines, Emydidae).

Lateralization presents clear advantages in ecological contexts as the dominance of one brain side prevents the simultaneous activation of contrasting responses in organisms with laterally located eyes. This is crucial in selecting a safe refuge during a predatory attack and may strongly affect predator-prey interactions. We explored the possible presence of lateralization in the anti-predatory behaviour of European pond turtles, considering their escape facing a possible predatory attack. Thirty individuals (17 males, 13 females) were exposed to three different environmental situations of gradually increasing predatory threat: escape underwater from an unsafe shelter, diving into the water from a basking site and righting after being overturned. All turtles were tested 20 times for each of the three experiments (60 trials per individual; 1800 overall trials). We recorded multiple behavioural responses in the general context of predation risk. This was done in order to assess both the existence of lateralization and possible correlations among different behaviours as function of lateralization. The number of significant responses to the left side was always prevalent in each of the three simulated anti-predatory situations, suggesting the existence of a lateralized behaviour in this species. At the individual level, the differences we found in the three experiments could be related to different ecological contexts and consequent risk of predation. Our findings, among the few on chelonians, support the possible involvement of right hemisphere activity and, most importantly, reveal how the complexity of a general predatory context can affect the laterality of escape behaviour.

Escape path complexity and its context dependency in Pacific blue-eyes (Pseudomugil signifer).

The escape paths prey animals take following a predatory attack appear to be highly unpredictable - a property that has been described as 'protean behaviour'. Here, we present a method of quantifying the escape paths of individual animals using a path complexity approach. When individual fish (Pseudomugil signifer) were attacked, we found that a fish's movement path rapidly increased in complexity following the attack. This path complexity remained elevated (indicating a more unpredictable path) for a sustained period (at least 10 s) after the attack. The complexity of the path was context dependent: paths were more complex when attacks were made closer to the fish, suggesting that these responses are tailored to the perceived level of threat. We separated out the components of speed and turning rate changes to determine which of these components contributed to the overall increase in path complexity following an attack. We found that both speed and turning rate measures contributed similarly to an individual's path complexity in absolute terms. Overall, our work highlights the context-dependent escape responses that animals use to avoid predators, and also provides a method for quantifying the escape paths of animals.

Differences in the escape response of a grapsid crab in the field and in the laboratory.

Escape behaviours of prey animals are frequently used to study the neural control of behaviour. Escape responses are robust and fast, and can be reliably evoked under both field and laboratory conditions. Many escape responses are not as simple as previously suggested, however, and are often modulated by a range of contextual factors. To date it has been unclear to what extent behaviours studied in controlled laboratory experiments are actually representative of the behaviours that occur under more natural conditions. Here, we have used the model species Neohelice granulata, a grapsid crab, to show that there are significant differences between the crabs' escape responses in the field compared with those previously documented in laboratory experiments. These differences are consistent with contextual adjustments such as the availability of a refuge and have clear consequences for understanding the crabs' neural control of behaviour. Furthermore, the methodology used in this study mirrors the methodology previously used in fiddler crab research, allowing us to show that the previously documented differences in escape responses between these grapsid species are real and substantial. Neohelice granulata's responses are delayed and more controlled. Overall, the results highlight the adaptability and flexibility of escape behaviours and provide further evidence that the neural control of behaviour needs to be addressed in both the laboratory and field context.

Island tameness: living on islands reduces flight initiation distance.

One of Darwin's most widely known conjectures is that prey are tame on remote islands, where mammalian predators are absent. Many species appear to permit close approach on such islands, but no comparative studies have demonstrated reduced wariness quantified as flight initiation distance (FID; i.e. predator-prey distance when the prey begins to flee) in comparison with mainland relatives. We used the phylogenetic comparative method to assess influence of distance from the mainland and island area on FID of 66 lizard species. Because body size and predator approach speed affect predation risk, we included these as independent variables. Multiple regression showed that FID decreases as distance from mainland increases and is shorter in island than mainland populations. Although FID increased as area increased in some models, collinearity made it difficult to separate effects of area from distance and island occupancy. FID increases as SVL increases and approach speed increases; these effects are statistically independent of effects of distance to mainland and island occupancy. Ordinary least-squares models fit the data better than phylogenetic regressions, indicating little or no phylogenetic signal in residual FID after accounting for the independent variables. Our results demonstrate that island tameness is a real phenomenon in lizards.

Use of a behavioural response method to assess the risk of collision between migrating humpback whales and vessels.

With the substantial increase in many large whale populations, paired with the rise in global shipping and recreational vessel activity, it is not surprising that negative interactions between whales and vessels are increasing. Here, the collision risk between migrating groups of humpback whales (Megaptera novaeangliae) and vessels was assessed by determining if changes in their movement trajectories in response to an oncoming vessel translated to vessel avoidance. It was assumed groups would implement an escape response strategy, using cues such as the vessel speed, trajectory, proximity, and received level of noise to inform their response magnitude. However, many groups were unresponsive to an approaching vessel such that the vessel had to take evasive action. This study shows that humpback whales are not likely to take sufficient avoidance action when there is a potential for a vessel and whale to collide. Therefore, when developing a risk management strategy, mitigation measures that reduce the encounter rate between whales and vessels are likely to be the most effective.

A method for studying escape behavior to terrestrial threats in rodents.

BACKGROUND: Escape is one of the most essential behaviors for an animal's survival because it could be a matter of life and death. Much of our current understanding of the neural mechanisms underlying escape is derived from the looming paradigm, which mimics a diving aerial predator. Yet, the idea of the looming paradigm does not account for all types of threats like lions hunting antelopes or cats stalking mice. Escape responses to such terrestrial threats may require different strategies and neural mechanisms. NEW METHODS: Here, we developed a real-time interactive platform to study escape behavior to terrestrial threats in mice. A closed-loop controlled robot was magnetically pulled to mimic a terrestrial threat that chases a mouse. By using strong magnets and high-precision servo motors, the robot is capable of moving precisely with a high spatial-temporal resolution. Different algorithms can be used to achieve single approach or persistent approach. RESULTS: Animal experiments showed that mice exhibited consistent escape behavior when exposed to an approaching robotic predator. When presented with a persistently approaching predator, the mice were able to rapidly adapt their behavior, as evidenced by a decrease in startle responses and changes in movement patterns. COMPARISON WITH EXISTING METHODS: In comparison to existing methods for studying escape behavior, such as the looming paradigm, this approach is more suitable for investigating animal behavior in response to sustained threats. CONCLUSION: In conclusion, we have developed a flexible platform to study escape behavior to terrestrial threats in mice.

Sustained predation pressure may prevent the loss of anti-predator traits from havened populations.

Conservation havens free of invasive predators are increasingly relied upon for fauna conservation, although havened populations can lose anti-predator traits, likely making them less suitable for life 'beyond the fence'. Sustaining low levels of mammalian predator pressure inside havens may prevent the loss of anti-predator traits from havened populations. We opportunistically compared behavioural and morphological anti-predator traits between four woylie (Bettongia penicillata ogilbyi) populations- one haven isolated from all mammalian predators, one haven containing a native mammalian predator (chuditch; Dasyurus geoffroii), and their respective non-havened counterparts (each containing both chuditch and invasive predators). Havened woylies existing without mammalian predators were smaller (shorter hindfeet, smaller body weight) and less reactive (consumed more food from fox-treated and control feeding stations, less agitated during human handling) than a non-havened reference population. However, in the haven containing chuditch, we found no difference in behaviour or morphology compared to the adjacent non-havened population. Across populations, anti-predator responses tended to appear stronger at sites with higher predator activity, suggestive of an adaptive response across a gradient of predation pressure. Our findings suggest that maintaining mammalian predation pressure in conservation havens could be effective for preventing or slowing the loss of anti-predator traits from these populations.

Nitric oxide-signalling affects panic-like defensive behaviour and defensive antinociception neuromodulation in the prelimbic cerebral cortex.

RATIONALE: The prelimbic division (PrL) of the medial prefrontal cortex (mPFC) is a key structure in panic. OBJECTIVES: To evaluate the role of nitric oxide (NO) in defensive behaviour and antinociception. METHODS: Either Nω-propyl-L-arginine (NPLA) or Carboxy-PTIO was microinjected in the PrL cortex, followed by hypothalamic treatment with bicuculline. The exploratory behaviours, defensive reactions and defensive antinociception were recorded. Encephalic c-Fos protein was immunolabelled after escape behaviour. RESULTS: NPLA (an inhibition of nNOs) decreased panic-like responses and innate fear-induced antinociception. The c-PTIO (a membrane-impermeable NO scavenger) decreased the escape behaviour. PrL cortex pre-treatment with c-PTIO at all doses decreased defensive antinociception. c-Fos protein was labelled in neocortical areas, limbic system, and mesencephalic structures. CONCLUSION: The NPLA and c-PTIO in the PrL/mPFC decreased the escape behaviour and defensive antinociception organised by medial hypothalamic nuclei. The oriented escape behaviour recruits neocortical areas, limbic system, and mesencephalic structures. These findings suggest that the organisation of defensive antinociception recruits NO-signalling mechanisms within the PrL cortex. Furthermore, the present findings also support the role of NO as a retrograde messenger in the PrL cortex during panic-like emotional reactions.

Are birds more afraid in urban parks or cemeteries? A Latin American study contrasts with results from Europe.

The escape behaviour, measured as flight initiation distance (FID; the distance at which individuals take flight when approached by a potential predator, usually a human in the study systems), is a measure widely used to study fearfulness and risk-taking in animals. Previous studies have shown significant differences in the escape behaviour of birds inhabiting cemeteries and urban parks in European cities, where birds seem to be shyer in the latter. We collected a regional dataset of the FID of birds inhabiting cemeteries and parks across Latin America in peri-urban, suburban and urban parks and cemeteries. FIDs were recorded for eighty-one bird species. Mean species-specific FIDs ranged from 1.9 to 19.7 m for species with at least two observations (fifty-seven species). Using Bayesian regression modelling and controlling for the phylogenetic relatedness of the FID among bird species and city and country, we found that, in contrast to a recent publication from Europe, birds escape earlier in cemeteries than parks in the studied Latin American cities. FIDs were also significantly shorter in urban areas than in peri-urban areas and in areas with higher human density. Our results indicate that some idiosyncratic patterns in animal fearfulness towards humans may emerge among different geographic regions, highlighting difficulties with scaling up and application of regional findings to other ecosystems and world regions. Such differences could be associated with intrinsic differences between the pool of bird species from temperate European and mostly tropical Latin American cities, characterized by different evolutionary histories, but also with differences in the historical process of urbanization.

Temperatures leading to heat escape responses in Antarctic marine ectotherms match acute thermal limits.

Thermal tolerance windows are key indicators of the range of temperatures tolerated by animals and therefore, a measure of resilience to climate change. In the ocean, where ectotherms are immersed, body temperatures are tightly coupled to environmental temperature and species have few options for thermoregulation. However, mobile species do have the ability to orientate towards optimal temperatures and move away from sub-optimal or dangerous temperatures. Escape responses are one such locomotory behavior, which typically manifests as a series of violent flicking movements that move individuals out of dangerous environments. We tested 11 species of Antarctic marine ectotherms, from one of the most stable shallow water marine environments, with an annual temperature range of -2°C to +2°C, that are vulnerable to small degrees of warming. Three species, the clam Laternula elliptica, the sea cucumber Cucumaria georgiana, and the brittlestar Ophionotus victoriae, showed no, or virtually no, escape response to temperature. Escape responses from a further eight species had a median response temperature of 11.2 (interquartile range, 10°C-15.7°C), which is well above current environmental temperatures but close to the range for acute lethal limits of Antarctic marine ectotherms (CTmax range, 17.2°C-26.6°C). This highlights that both acute tolerance limits and escape responses, fall outside current environmental temperatures, but also those predicted for 100s of years in the Southern Ocean. In a warmer Southern Ocean Antarctic fauna may not have the capacity to use temperature to select optimal thermal conditions, which leaves adaptation as a primary mechanism for their persistence.

Flight initiation distance and refuge in urban birds.

Risk-taking in birds is often measured as the flight initiation distance (FID), the distance at which individuals take flight when approached by a potential predator (typically a human). The ecological factors that affect avian FID have received great attention over the past decades and meta-analyses and comparative analyses have shown that FID is correlated with body mass, flock size, starting distance of the approaching human, density of potential predators, as well as varying along rural to urban gradients. However, surprisingly, only few studies (mainly on reptiles and mammals) have explored effects of different types of refugia and their availability on animal escape decisions. We used Bayesian regression models (controlling for the phylogenetic relatedness of bird species) to explore changes in escape behaviour recorded in European cities in relationship to the birds' distance to the nearest refuge and distance fled to the refuge. In our analyses, we also included information on the type of refuge, built-up and vegetation cover, starting distance, flock size, urbanization level, and type of urban habitat. We found that birds preferred tree refuges over artificial and bush refuges. Birds escaped earlier if the distance to the nearest refuge of any type was longer and if birds fled longer distances to the refuge. FID was shorter when birds used bushes as refugia or landed on the ground after flushing compared to using artificial refugia. Similarly, the distance fled to a refuge was shortest when using bushes, and increased when escaping to artificial substrates and trees. Birds were more timid in suburban than core areas of cities, cemeteries than parks, and in areas with higher bush cover but lower cover of built-up areas and trees. Our findings provide novel information regarding the importance of refuge proximity and type as factors affecting the escape behaviour of urban birds.

Temperament, Plasticity, and Emotions in Defensive Behaviour of Paca (Mammalia, Hystricognatha).

Within a species, some individuals are better able to cope with threatening environments than others. Paca (Cuniculus paca) appear resilient to over-hunting by humans, which may be related to the behavioural plasticity shown by this species. To investigate this, we submitted captive pacas to temperament tests designed to assess individual responses to short challenges and judgement bias tests (JBT) to evaluate individuals' affective states. Results indicated across-time and context stability in closely correlated "agitated", "fearful" and "tense" responses; this temperament dimension was labelled "restless". Individual "restless" scores predicted responses to novelty, although not to simulated chasing and capture by humans in a separate modified defence test battery (MDTB). Restless animals were more likely to show a greater proportion of positive responses to an ambiguous cue during JBT after the MDTB. Plasticity in defensive behaviour was inferred from changes in behavioural responses and apparently rapid adaptation to challenge in the different phases of the MDTB. The results indicate that both temperament and behavioural plasticity may play a role in influencing paca responses to risky situations. Therefore, our study highlights the importance of understanding the role of individual temperament traits and behavioural plasticity in order to better interpret the animals' conservation status and vulnerabilities.

Corvids exhibit dynamic risk assessment during escape.

It is widely accepted that stationary prey are able to carefully assess the risk levels associated with an approaching predator to make informative decisions on when to escape. However, little is known about subsequent decision-making process. We set out to compare whether escape durations of three species of corvids differ depending on how a human observer (in the role of a predator) behaves after the escape has begun. When birds were being followed during escape, escape durations were the longest, escape trajectory was modified the most during escape, and a larger proportion of individuals changed from terrestrial to aerial escape strategy compared to observations where birds were not followed. Mean horizontal escape angle of ca 120° was also a potential indication that monitoring the threat is taken into account when deciding on the escape trajectory. While there were some differences between the behaviour of these three closely related species, the general patterns supported the notion that birds dynamically assess risk during escape to find an optimal balance between getting caught and spending too much time and energy on escaping. Further research using different predator-prey combinations or making comparisons between habitats could help understand the generality of our results.

Motile behaviour of the free-living planktonic ciliate Zoothamnium pelagicum (Ciliophora, Peritrichia).

Zoothamnium pelagicum is the only free-floating species among ∼1000 peritrich ciliates that develops its complete life cycle in the open ocean. In the NW Mediterranean Sea, Z. pelagicum was usually associated with ectobiotic bacteria, while in the South Atlantic Ocean was sometimes fouled by the diatom Licmophora. Each colony constituted a radial branch that joined at its base with other colonies to form a lens-shaped pseudocolony of up to 400 zooids. The cilia beat slowly, propelling the expanded pseudocolony in the direction of the concave face. Contraction was triggered by external stimuli (threat) or occurred spontaneously. Frame-by-frame analyses of high-speed camera sequences revealed that during contraction the pseudocolony reduced its diameter 70-75% in 3-3.2ms with peak velocity up to 350mms-1. The contraction induced a forward jump of 1-2mm that attained a peak speed of 110mms-1 (∼250pseudocolony lengthss-1) in 5ms after onset. This medusa-like locomotion at low Reynolds numbers allowed the pseudocolony to exploit new patches of food resources, as well as to escape from predators. Zoothamnium pelagicum has been able to proliferate in the oligotrophic open ocean, while its sessile counterparts are restricted to eutrophic environments.

Fifty years of chasing lizards: new insights advance optimal escape theory.

Systematic reviews and meta-analyses often examine data from diverse taxa to identify general patterns of effect sizes. Meta-analyses that focus on identifying generalisations in a single taxon are also valuable because species in a taxon are more likely to share similar unique constraints. We conducted a comprehensive phylogenetic meta-analysis of flight initiation distance in lizards. Flight initiation distance (FID) is a common metric used to quantify risk-taking and has previously been shown to reflect adaptive decision-making. The past decade has seen an explosion of studies focused on quantifying FID in lizards, and, because lizards occur in a wide range of habitats, are ecologically diverse, and are typically smaller and differ physiologically from the better studied mammals and birds, they are worthy of detailed examination. We found that variables that reflect the costs or benefits of flight (being engaged in social interactions, having food available) as well as certain predator effects (predator size and approach speed) had large effects on FID in the directions predicted by optimal escape theory. Variables that were associated with morphology (with the exception of crypsis) and physiology had relatively small effects, whereas habitat selection factors typically had moderate to large effect sizes. Lizards, like other taxa, are very sensitive to the costs of flight.

Influence of boat noises on escape behaviour of white-spotted eagle ray Aetobatus ocellatus at Moorea Island (French Polynesia).

The present study tested different sounds that could disturb eagle rays (Aetobatus ocellatus) during their foraging activities at Moorea, French Polynesia. Results showed that artificial white sound and single-frequency tones (40 Hz, 600 Hz or 1 kHz) did not have an effect on rays (at least 90% of rays continued to forage over sand), while playbacks of boat motor sound significantly disturbed rays during foraging activity (60% exhibited an escape behaviour). Overall, our study highlighted the negative effect of boat noises on the foraging activity of eagle rays. These noises produced by boat traffic could, however, have some positive effects for marine aquaculture if they could be used as a deterrent to repel the eagle rays, main predators of the pearl oysters.