Learning to anticipate mate presence shapes individual sex roles in the hermaphroditic pond snail, Lymnaea stagnalis.

Despite being simultaneously male and female, hermaphrodites may still need to assume the male or female sexual role in a mating encounter, with the option to swap roles afterwards. For the great pond snail, Lymnaea stagnalis, deciding which sexual role to perform has important consequences, since sperm transfer and male reproductive success can be decreased. We hypothesised that detecting cues that indicate a possible mating encounter could help them to adapt their mating behaviour. Therefore, we experimentally assessed whether signalling the presence of a conspecific with an odour can affect the sexual role of Lymnaea stagnalis. The results showed that learning resulted in either an increased ability to mate as a male or in faster mating compared to the control group. These findings reveal that learning shapes the mating dynamics of Lymnaea stagnalis, thus showing that cognitive processes not only affect mating in separate-sexed species but also in hermaphrodites.

Cause, development, function, and evolution: Toward a behavioral ecology of rescue behavior in ants.

In a species of Mediterranean desert-dwelling ant, Cataglyphis piliscapa (formerly, C. cursor), some individuals, mostly foragers, engage in highly orchestrated behavior to free a trapped nestmate. Their behavior, which we have labeled rescue, is a heritable trait in this species, and it appears fully formed within a few days of an ant's emergence as an adult. Not only is the rescue behavior by these ant specialists precisely targeted, but also it involves a complex, dynamic sequence of behavioral patterns. That is, each rescue operation is responsive both to the specific circumstances of the nestmate's entrapment and to the way in which that particular rescue operation unfolds, relying on the rescuer's short-term memory of its previous actions to increase efficiency and to decrease energy expenditure. Rescue appears in several other ant species as well, and, although the specific behavioral patterns and contexts vary across species, the outcome-namely, releasing a distressed nestmate-remains the same. Here, we describe research designed to address questions about the function, evolution, cause, and development of rescue behavior in C. piliscapa-a behavior ecological approach-drawing on research in other species, and by other researchers, both to highlight comparative similarities and differences and, importantly, to draw attention to still unanswered questions. In addition, by shedding light on the rescue behavior of ants, we also hope to engender increased attention to, and research on, this extraordinary form of helping behavior in multiple other taxa.

Rescue specialists in Cataglyphis piliscapa ants: The nature and development of ant first responders.

Previous research in our laboratories has demonstrated that, within each colony of Cataglyphis piliscapa (formerly C. cursor) ants, only some individuals are capable of performing a complex sequence of behavioral patterns to free trapped nestmates-a sequence that not only is memory-dependent but also is responsive to the particular circumstances of that entrapment and how the rescue operation unfolds. Additionally, this rescue behavior is inherited patrilineally from but a few of the many males that fertilize the eggs of the colony's single queen. Here, we describe three experiments to explore rescue behavior further-namely, whether rescuers are in any way selective about which nestmates they help, how the age of rescuers and the victims that they help affect the quantity and quality of the rescue operation, and when this complex behavior first emerges in an ant's development. Taken together with the previous heritability analysis, these behavioral experiments provide clear evidence that the ability to rescue nestmates in distress should be recognized as a specialization, which together with other specialized tasks in C. piliscapa, contributes to a division of labor that increases the efficiency of the colony as a whole and, thus increases its reproductive success.

Analysis of ants' rescue behavior reveals heritable specialization for first responders.

In colonies of Cataglyphis cursor ants, a single queen mates with multiple males, creating the foundation for heritable behavioral specializations. A novel and unique candidate for such specializations is rescue behavior, a precisely delivered form of altruism in which workers attempt to release trapped nestmates and which relies on short-term memory of previous actions to increase its efficiency. Consistent with task specialization, not all individuals participate; instead, some individuals move away from the victim, which gives rescuers unrestricted access. Using a bioassay to identify rescuers and non-rescuers, coupled with paternity assignment via polymorphic microsatellite markers, we not only show that rescue behavior is heritable, with 34% of the variation explained by paternity, but also establish that rescue, heretofore overlooked in analyses of division of labor, is a true specialization, an ant version of first responders. Moreover, this specialization emerges as early as 5 days of age, and the frequency of rescuers remains constant across ants' age ranges. The extremely broad range of these ants' heritable polyethism provides further support for the critical role of polyandry in increasing the efficiency of colony structure and, in turn, reproductive success.

Natural aversive learning in Tetramorium ants reveals ability to form a generalizable memory of predators' pit traps.

Many species of ants fall prey to pit-digging larval antlions (Myrmeleon spp.), extremely sedentary predators that wait, nearly motionless at the bottom of their pit traps, for prey to stumble inside. Previous research, both in the field and laboratory, has demonstrated a remarkable ability of these ants to rescue trapped nestmates, thus sabotaging antlions' attempts to capture them. Here we show that pavement ants, Tetramorium sp. E, an invasive species and a major threat to biodiversity, possess yet another, more effective, antipredator strategy, namely the ability to learn to avoid antlion traps following a single successful escape from a pit. More importantly, we show that this learned antipredator behavior, an example of natural aversive learning in insects, is more complicated than a single cue-to-consequence form of associative learning. That is, pavement ants were able to generalize, after one experience, from the learned characteristics of the pit and its specific location, to other pits and other contexts that differed in many features. Such generalization, often described as a lack of precise stimulus control, nonetheless would be especially adaptive in nature, enabling ants to negotiate antlions' pit fields, which contain a hundred or more pits within a few centimetres of one another. Indeed, the ability to generalize in exactly this way almost certainly is responsible for the sudden, and heretofore inexplicable, behavioural modifications of ants in response to an invasion of antlions in the vicinity of an ant colony.

Organization of rescue behaviour sequences in ants, Cataglyphis cursor, reflects goal-directedness, plasticity and memory.

The experimental study of rescue behaviour in ants, behaviour in which individuals help entrapped nestmates in distress, has revealed that rescuers respond to victims with very precisely targeted behaviour. In Cataglyphis cursor, several different components of rescue behaviour have been observed, demonstrating the complexity of this behaviour, including sand digging and sand transport to excavate the victim, followed by pulling on the victim's limbs as well as the object holding the victim in place, behaviour that serves to free the victim. Although previous work suggested that rescue was optimally organized, first to expose and then to extricate the victim under a variety of differing circumstances, experimental analysis of that organization has been lacking. Here, using experimental data, we characterize the pattern of individual rescue behaviour in C. cursor by analysing the probabilities of transitions from one behavioural component to another. The results show that the execution of each behavioural component is determined by the interplay of previous acts. In particular, we show not only that ants move sand away from the victim in an especially efficient sequence of behaviour that greatly minimizes energy expenditure, but also that ants appear to form some kind of memory of what they did in the past, a memory that directs their future behaviour.

Ants and antlions: The impact of ecology, coevolution and learning on an insect predator-prey relationship.

A behavioural ecological approach to the relationship between pit-digging larval antlions and their common prey, ants, provides yet another example of how the specific ecological niche that species inhabit imposes selection pressures leading to unique behavioural adaptations. Antlions rely on multiple strategies to capture prey with a minimal expenditure of energy and extraordinary efficiency while ants employ several different strategies for avoiding capture, including rescue of trapped nestmates. Importantly, both ants and antlions rely heavily on their capacity for learning, a tool that sometimes is overlooked in predator-prey relationships, leading to the implicit assumption that behavioural adaptations are the result of fixed, hard-wired responses. Nonetheless, like hard-wired responses, learned behaviour, too, is uniquely adapted to the ecological niche, a reminder that the expression of associative learning is species-specific. Beyond the study of ants and antlions, per se, this particular predator-prey relationship reveals the important role that the capacity to learn plays in coevolutionary arms races.

Rescue of newborn ants by older Cataglyphis cursor adult workers.

Cataglyphis cursor worker ants are capable of highly sophisticated rescue behaviour in which individuals are able to identify what has trapped a nestmate and to direct their behaviour towards that obstacle. Nonetheless, rescue behaviour is constrained by workers' subcaste: whereas foragers, the oldest workers, are able both to give and to receive the most help, the youngest workers, inactives, neither give nor receive any help whatsoever; nurses give and receive intermediate levels of aid, reflecting their intermediate age. Such differences in rescue behaviour across subcastes suggest that age and experience play a critical role. In this species, as in many others in which a sensitive period for nestmate recognition exists, newly enclosed ants, called callows, are adopted by ants belonging not only to different colonies but also to different species; foreign callows receive nearly the same special care provided to resident newborns. Because callows are younger than inactives, which are incapable of soliciting rescue, we wondered whether entrapped callows would receive such aid. In the present study, we artificially ensnared individual callows from their own colony (homocolonial), from a different colony (heterocolonial), and from a different species (heterospecific), and tested each one with groups of five potential C. cursor rescuers, either all foragers or all nurses. Our results show that all three types of callows are able to elicit rescue behaviour from both foragers and nurses. Nonetheless, nurse rescuers are better able to discriminate between the three types of callow victims than are foragers.

Toward a behavioral ecology of rescue behavior.

Although the study of helping behavior has revolutionized the field of behavioral ecology, scientific examination of rescue behavior remains extremely rare, except perhaps in ants, having been described as early as 1874. Nonetheless, recent work in our laboratories has revealed several new patterns of rescue behavior that appear to be much more complex than previously studied forms. This precisely-directed rescue behavior bears a remarkable resemblance to what has been labeled empathy in rats, and thus raises numerous philosophical and theoretical questions: How should rescue behavior (or empathy) be defined? What distinguishes rescue from other forms of altruism? In what ways is rescue behavior in ants different from, and similar to, rescue in other non-human animals? What selection pressures dictate its appearance? In this paper, we review our own experimental studies of rescue in both laboratory and field, which, taken together, begin to reveal some of the behavioral ecological conditions that likely have given rise to rescue behavior in ants. Against this background, we also address important theoretical questions involving rescue, including those outlined above. In this way, we hope not only to encourage further experimental analysis of rescue behavior, but also to highlight important similarities and differences in very distant taxa.

Division of labor regulates precision rescue behavior in sand-dwelling Cataglyphis cursor ants: to give is to receive.

Division of labor, an adaptation in which individuals specialize in performing tasks necessary to the colony, such as nest defense and foraging, is believed key to eusocial insects' remarkable ecological success. Here we report, for the first time, a completely novel specialization in a eusocial insect, namely the ability of Cataglyphis cursor ants to rescue a trapped nestmate using precisely targeted behavior. Labeled "precision rescue", this behavior involves the ability of rescuers not only to detect what, exactly, holds the victim in place, but also to direct specific actions to this obstacle. Individual ants, sampled from each of C. cursor's three castes, namely foragers, nurses and inactives, were experimentally ensnared (the "victim") and exposed to a caste-specific group of potential "rescuers." The data reveal that foragers were able to administer, and obtain, the most help while members of the youngest, inactive caste not only failed to respond to victims, but also received virtually no help from potential rescuers, regardless of caste. Nurses performed intermediate levels of aid, mirroring their intermediate caste status. Our results demonstrate that division of labor, which controls foraging, defense and brood care in C. cursor, also regulates a newly discovered behavior in this species, namely a sophisticated form of rescue, a highly adaptive specialization that is finely tuned to a caste member's probability of becoming, or encountering, a victim in need of rescue.

Specialized learning in antlions (Neuroptera: Myrmeleontidae), pit-digging predators, shortens vulnerable larval stage.

Unique in the insect world for their extremely sedentary predatory behavior, pit-dwelling larval antlions dig pits, and then sit at the bottom and wait, sometimes for months, for prey to fall inside. This sedentary predation strategy, combined with their seemingly innate ability to detect approaching prey, make antlions unlikely candidates for learning. That is, although scientists have demonstrated that many species of insects possess the capacity to learn, each of these species, which together represent multiple families from every major insect order, utilizes this ability as a means of navigating the environment, using learned cues to guide an active search for food and hosts, or to avoid noxious events. Nonetheless, we demonstrate not only that sedentary antlions can learn, but also, more importantly, that learning provides an important fitness benefit, namely decreasing the time to pupate, a benefit not yet demonstrated in any other species. Compared to a control group in which an environmental cue was presented randomly vis-à-vis daily prey arrival, antlions given the opportunity to associate the cue with prey were able to make more efficient use of prey and pupate significantly sooner, thus shortening their long, highly vulnerable larval stage. Whereas "median survival time," the point at which half of the animals in each group had pupated, was 46 days for antlions receiving the Learning treatment, that point never was reached in antlions receiving the Random treatment, even by the end of the experiment on Day 70. In addition, we demonstrate a novel manifestation of antlions' learned response to cues predicting prey arrival, behavior that does not match the typical "learning curve" but which is well-adapted to their sedentary predation strategy. Finally, we suggest that what has long appeared to be instinctive predatory behavior is likely to be highly modified and shaped by learning.

Rescue behavior: Distinguishing between rescue, cooperation and other forms of altruistic behavior.

Reports of rescue behavior in non-human animals are exceedingly rare, except in ants where rescue is well known, but has not been explored experimentally until recently. Although we predict that rescue behavior should be limited to circumstances in which the victim and the rescuer are highly related to one another, or in which unrelated individuals must cooperate very closely with one another, we also predict that it is likely to be far more common than the current literature would suggest. To address this oversight, we propose a rigorous definition of rescue behavior, one that helps researchers to focus on its necessary and sufficient components, at the same time that it helps to differentiate rescue behavior from cooperation and other forms of helping behavior. In this way we also hope to expand our understanding of altruism in particular and kin selection in general.

Ants, Cataglyphis cursor, use precisely directed rescue behavior to free entrapped relatives.

Although helping behavior is ubiquitous throughout the animal kingdom, actual rescue activity is particularly rare. Nonetheless, here we report the first experimental evidence that ants, Cataglyphis cursor, use precisely directed rescue behavior to free entrapped victims; equally important, they carefully discriminate between individuals in distress, offering aid only to nestmates. Our experiments simulate a natural situation, which we often observed in the field when collecting Catagyphis ants, causing sand to collapse in the process. Using a novel experimental technique that binds victims experimentally, we observed the behavior of separate, randomly chosen groups of 5 C. cursor nestmates under one of six conditions. In five of these conditions, a test stimulus (the "victim") was ensnared with nylon thread and held partially beneath the sand. The test stimulus was either (1) an individual from the same colony; (2) an individual from a different colony of C cursor; (3) an ant from a different ant species; (4) a common prey item; or, (5) a motionless (chilled) nestmate. In the final condition, the test stimulus (6) consisted of the empty snare apparatus. Our results demonstrate that ants are able to recognize what, exactly, holds their relative in place and direct their behavior to that object, the snare, in particular. They begin by excavating sand, which exposes the nylon snare, transporting sand away from it, and then biting at the snare itself. Snare biting, a behavior never before reported in the literature, demonstrates that rescue behavior is far more sophisticated, exact and complexly organized than the simple forms of helping behavior already known, namely limb pulling and sand digging. That is, limb pulling and sand digging could be released directly by a chemical call for help and thus result from a very simple mechanism. However, it's difficult to see how this same releasing mechanism could guide rescuers to the precise location of the nylon thread, and enable them to target their bites to the thread itself.

Learning in a sedentary insect predator: antlions (Neuroptera: Myrmeleontidae) anticipate a long wait.

Pit-building antlions, the larvae of a winged adult insect, capture food by digging funnel-shaped pits in sand and then lying in wait, buried at the vertex, for prey to fall inside. The sedentary nature of this sit-and-wait predatory behaviour and, especially, antlions' innate ability to detect prey arrival, do not fit the typical profile of insects that possess learning capabilities. However, we show, for the first time, that learning can play an important role in this unique form of predation. In three separate experiments, individual antlions received, once per training day, either a vibrational cue presented immediately before the arrival of food or that same cue presented independently of food arrival. Signalling of food not only produced a learned anticipatory behavioural response (Experiment 1), but also conferred a fitness advantage: Associative learning enabled antlions to dig better pits (Experiments 2 and 3), extract food more efficiently (Experiments 2 and 3), and, in turn, moult sooner (Experiment 3) than antlions not receiving the associative learning treatment.

The bitter truth: sensitivity to saccharin's bitterness predicts overactivity in highly arousable female dieters.

OBJECTIVE: The interaction between taste sensitivity and emotionality in rats provides a provocative view of hyperactivity. Rats that have been bred selectively for their reactivity to saccharin exhibit characteristic emotionality. When placed on restrictive diets, these rats exhibit excessive activity levels, relative to rats that are not sensitive to saccharin. Because humans who are highly arousable (i.e., reactive to environmental stimuli) also exhibit an increase in sensitivity to saccharin's bitterness, the current study evaluated whether women who are highly arousable, currently dieting, and sensitive to saccharin's bitterness engage in excessive exercise. METHOD: Participants completed a questionnaire packet, which assessed emotionality, eating patterns, and exercise patterns. On another occasion, they completed a body contour drawings handout, and their weight and height were measured. They also rated saccharin's bitterness and sweetness following a stressful event. RESULTS AND DISCUSSION: As hypothesized, sensitivity to saccharin's bitterness predicted overactivity in highly arousable female dieters, which reveals the multidimensionality of activity anorexia.