Social learning about egg-laying substrates in fruitflies

Social learning, defined as learning from other individuals, has had dramatic effects on some species, including humans, in whom it has generated a rich culture. As a first step in examining the evolution of and mechanisms underlying social learning in insects, we tested for social learning in fruitflies (Drosophila melanogaster). Focal females (observers) that experienced novel food together with mated females (models), who had laid eggs on that food, subsequently exhibited a stronger preference for laying eggs on that food over another novel food compared with focal females that experienced the food alone. We observed no social learning, however, when observers experienced food with potentially more ambiguous social information provided by the presence of either virgin models or aggregation pheromone. This first documentation of social learning about egg-laying substrates in fruitflies builds on recent data indicating intricate use of social information by fruitflies and opens up exciting avenues for research on the evolution and neurogenetics of social learning using biology''s major model system.     

Orientation of European corn borer first instar larvae to synthetic green leaf volatiles

European corn borer (ECB) neonate larvae are capable of orienting towards maize odours and of avoiding spinach odours. We previously reported that maize odours’ attraction was dependent on the stimulus regime. This led us to propose that maize odours could have a repellent or attractive effect depending on their concentration. In this work, we tested this hypothesis by evaluating attraction or avoidance of neonate ECB larvae to four concentrations of each of six single green leaf volatiles (GLVs); these are commonly found in maize and other plants. We found a dose‐dependent effect for all of these GLVs with the exception of 1‐hexyl acetate, which did not elicit any orientation behaviour over the range of concentrations tested. These five GLVs were repellent at high concentrations, while two of them were attractive at a lower concentration. These observations indicate for the first time that plant odours induce different behaviours in ECB neonate larvae depending not only on their chemical identity but also their concentration.     

Concurrent modulation of neuronal and behavioural olfactory responses to sex and host plant cues in a male moth

Mating has profound effects on animal physiology and behaviour, not only in females but also in males, which we show here for olfactory responses. In cotton leafworm moths, Spodoptera littoralis, odour-mediated attraction to sex pheromone and plant volatiles are modulated after mating, producing a behavioural response that matches the physiological condition of the male insect. Unmated males are attracted by upwind flight to sex pheromone released by calling females, as well as to volatiles of lilac flowers and green leaves of the host plant cotton, signalling adult food and mating sites, respectively. Mating temporarily abolishes male attraction to females and host plant odour, but does not diminish attraction to flowers. This behavioural modulation is correlated with a response modulation in the olfactory system, as shown by electro-physiological recordings from antennae and by functional imaging of the antennal lobe, using natural odours and synthetic compounds. An effect of mating on the olfactory responses to pheromone and cotton plant volatiles but not to lilac flowers indicates the presence of functionally independent neural circuits within the olfactory system. Our results indicate that these circuits interconnect and weigh perception of social and habitat odour signals to generate appropriate behavioural responses according to mating state.     

Social learning in a high-risk environment: incomplete disregard for the ‘minnow that cried pike’ results in culturally transmitted neophobia

Many prey species rely on conspecifics to gather information about unknown predation threats, but little is known about the role of varying environmental conditions on the efficacy of social learning. We examined predator-naive minnows that had the opportunity to learn about predators from experienced models that were raised in either a low- or high-risk environment. There were striking differences in behaviour among models; high-risk models showed a weaker response to the predator cue and became neophobic in response to the control cue (a novel odour, NO). Observers that were previously paired with low-risk models acquired a strong antipredator response only to the predator cue. However, observers that interacted with high-risk models, displayed a much weaker response to the predator odour and a weak neophobic response to the NO. This is the first study reporting such different outcomes of social learning under different environmental conditions, and suggests high-risk environments promote the cultural transmission of neophobia more so than social learning. If such a transfer can be considered similar to secondary traumatization in humans, culturally transmitted neophobia in minnows may provide a good model system for understanding more about the social ecology of fear disorders.     

Dietary salt levels affect salt preference and learning in larval Drosophila

Drosophila larvae change from exhibiting attraction to aversion as the concentration of salt in a substrate is increased. However, some aversive concentrations appear to act as positive reinforcers, increasing attraction to an odour with which they have been paired. We test whether this surprising dissociation between the unconditioned and conditioned response depends on the larvae's experience of salt concentration in their food. We find that although the point at which a NaCl concentration becomes aversive shifts with different rearing experience, the dissociation remains evident. Testing larvae using a substrate 0.025 M above the NaCl concentration on which the larvae were reared consistently results in aversive choice behaviour but appetitive reinforcement effects.     

Contrasting responses of bumble bees to feeding conspecifics on their familiar and unfamiliar flowers

Animals exploiting their familiar food items often avoid spatio-temporal aggregation with others by avoiding scents, less rewarding areas or visual contacts, thereby minimizing competition or interference when resources are replenished slowly in patches. When animals are searching or assessing available food sources, however, they may benefit from reducing sampling costs by following others at food sites. Therefore, animals may adjust their responses to others depending on their familiarity with foraging situations. Here, we conducted field experiments to test whether nectar-collecting bumble bees make this adjustment. We allowed free-foraging bees to choose between two inflorescences, one occupied by a conspecific bee and another unoccupied. When bees were presented with flowers of a familiar type, they avoided occupied inflorescences. In contrast, bees visited an occupied inflorescence when the flower type was unfamiliar. To our knowledge, this is the first report suggesting that animals adjust their responses to feeding conspecifics depending on their familiarity with food sources. Such behavioural flexibilities should allow foragers to both explore and exploit their environments efficiently.     

Effects of Early‐Life Experience on Learning Ability in Fruit Flies

Learning and memory require the development, modification and maintenance of brain tissue, which cost time and energy. It may be adaptive for developing animals to adjust such investments based on environmental cues indicating the future utility of learning. The optimal learning ability that maximizes fitness will vary with the degree of complexity or difficulty of the environment, and developing animals may show an adaptive plastic modification of the extent of their learning ability based on early‐life cues of environmental complexity. We tested whether fruit fly larvae reared in a ‘complex’ environment, where they had to search, sample and choose between three foods differing in flavour and bitterness subsequently possessed greater learning abilities than larvae reared in a simple environment with only one food type. We tested learning ability both at the larval stage and in young adults. Our results suggest that, despite theoretical and intuitive appeal, these environmental factors did not affect learning ability.     

Feeding while evading predators by a lotic mayfly: linking short-term foraging behaviours to long-term fitness consequences

Laboratory experiments were performed to quantify the combined effects of food abundance (low, high) and predation threat, imposed using a model fish (safe, risky) on fitness correlates (i.e. growth, time to emergence, adult body mass, fecundity, egg size) of the mayfly Baetis tricaudatus. These effects were determined by rearing larvae under different combinations of food abundance and predator threat. Fitness correlates were significantly affected by food abundance, predation threat or the interaction of these factors. High food abundance and the absence of predation threat significantly increased larval growth rates, adult body mass, fecundity, egg size, and decreased time to emergence. Long-term effects of predator threat and food abundance on fitness correlates of B. tricaudatus were compared to previously conducted short-term patch choice trials to test for concordance between short-term measures of patch choice and their potential longer-term fitness consequences. This comparison indicated that patches that were utilized the most were those that yielded the highest fitness benefits. These results suggest that behavioural costs of balancing mortality risk due to predation against food acquisition by B. tricaudatus can have strong fitness consequences.     

Social facilitation of learning in mixed-species schools of common carp Cyprinus carpio L. and Nile tilapia Oreochromis niloticus (L.)

The process of learning to associate a visual cue with food was studied in groups of common carp Cyprinus carpio and Nile tilapia Oreochromis niloticus by means of a classical conditioning paradigm. In the first phase of the study, fishes were conditioned in either single-species or mixed-species groups to associate a blinking blue light with food. In the second phase, group composition was altered so that only single species were reconditioned, composed of individuals previously paired with the same or the other species. In the first phase, in the single-species groups, Nile tilapia rapidly formed an association between the visual cue and food, whereas common carp failed to do so. In mixed-species groups, both Nile tilapia and common carp associated a visual cue with food. In the second phase of the study, Nile tilapia retained that ability irrespective of whether they had previously been trained in single-species or mixed-species groups, common carp previously trained with Nile tilapia, were not repelled by the blinking blue light and gradually approached it from a distance, whereas common carp previously trained in homogenous groups continued to be repelled by the blinking light. Fish arrivals and departures from the feeding zones as well as fish position in the testing apparatus were analysed and contrasted in single-species and mixed-species groups outside the training sessions, revealing mutual impacts of one species on the other in mixed-species groups. The findings of this study demonstrated interspecific social facilitation of learning to associate a visual cue with food.     

When to approach novel prey cues? Social learning strategies in frog-eating bats

Animals can use different sources of information when making decisions. Foraging animals often have access to both self-acquired and socially acquired information about prey. The fringe-lipped bat, Trachops cirrhosus, hunts frogs by approaching the calls that frogs produce to attract mates. We examined how the reliability of self-acquired prey cues affects social learning of novel prey cues. We trained bats to associate an artificial acoustic cue (mobile phone ringtone) with food rewards. Bats were assigned to treatments in which the trained cue was either an unreliable indicator of reward (rewarded 50% of the presentations) or a reliable indicator (rewarded 100% of the presentations), and they were exposed to a conspecific tutor foraging on a reliable (rewarded 100%) novel cue or to the novel cue with no tutor. Bats whose trained cue was unreliable and who had a tutor were significantly more likely to preferentially approach the novel cue when compared with bats whose trained cue was reliable, and to bats that had no tutor. Reliability of self-acquired prey cues therefore affects social learning of novel prey cues by frog-eating bats. Examining when animals use social information to learn about novel prey is key to understanding the social transmission of foraging innovations.     

Superparasitism in Cotesia glomerata does not benefit the host plant by reduction of herbivory caused by Pieris brassicae

Superparasitism occurs in Cotesia glomerata L. (Hymenoptera: Braconidae), a gregarious endoparasitoid of Pieris spp. (Lepidoptera: Pieridae). The responses of Pieris brassicae L. larvae to superparasitism were examined in order to elucidate the ecological significance of this behaviour. Models of tritrophic interactions often imply that attraction of herbivore natural enemies by the plant constitutes a defence. Parasitoid attack on herbivores is assumed to result in a reduction in herbivory and or an increase in plant fitness. Coupled with the active involvement of the plant in producing signals, this can be seen as an indirect mediation of wound induced defence. The results show that superparasitism of P. brassicae by the parasitoid C. glomerata reduced survivorship but increased food consumption and weight growth in P. brassicae larvae. The duration of host larval development was found prolonged as the number of oviposition increased and superparasitized larvae (three to five time parasitized) grew slower than unparasitized larvae or larvae parasitized one or two times.     

Attraction of Drosophila melanogaster males to food-related and fly odours

The fruit fly Drosophila melanogaster has become a model for olfaction and odour-mediated behaviour. In the wild, Drosophila flies aggregate on decaying fruit where they mate and oviposit and a strategy to find mates would be to locate fruit which has already been colonized by other flies. We therefore developed a bioassay to investigate attraction of males to food and fly odours. We showed that upwind flights are initiated by food odours. At shorter distances, males are attracted by volatiles produced by conspecifics. However, only odours produced by copulating flies attract males. This suggests either a synergistic effect of both male and female odours or changes in pheromone release during mating, that indicate the presence of sexually receptive females. Our findings demonstrate the essential role of food odours and pheromones for mate location in D. melanogaster.     

Bumblebees (Bombus terrestris) use social information as an indicator of safety in dangerous environments

Avoiding predation is one of the most important challenges that an animal faces. Several anti-predation behaviours can be employed, yet simply using the presence of conspecifics can be a good signal of safety in an environment with potential predation hazards. Here, we show, for the first time, that past experience of predation causes bumblebees (Bombus terrestris) to aggregate with conspecifics, facilitating the identification of safe foraging patches. Bees were trained to differentiate between flowers that harboured predators and flowers that were predator free. When test subjects were subsequently presented solely with the previously predator-infested flower species, there was a significant preference to only land on flowers occupied by other feeding conspecifics. Yet, when safe flowers were made available to subjects previously entrained to discriminate safe from predator-occupied flowers, subjects ignored other bees and the social information potentially provided by them, demonstrating that attraction towards conspecifics is confined to dangerous situations. Our findings demonstrate a previously unknown social interaction in pollinators which may have important implications for plant–pollinator interactions.     

Related male Drosophila melanogaster reared together as larvae fight less and sire longer lived daughters

Competition over access to reproductive opportunities can lead males to harm females. However, recent work has shown that, in Drosophila melanogaster, male competition and male harm of females are both reduced under conditions simulating male-specific population viscosity (i.e., in groups where males are related and reared with each other as larvae). Here, we seek to replicate these findings and investigate whether male population viscosity can have repercussions for the fitness of offspring in the next generation. We show that groups of unrelated-unfamiliar (i.e., unrelated individuals raised apart) males fight more intensely than groups of related-familiar males (i.e., full siblings raised together as larvae), supporting previous findings, and that exposure to a female is required to trigger these differential patterns of male–male competition. Importantly, we show that differences in male–male competition can be associated with transgenerational effects: the daughters of females exposed to unrelated-unfamiliar males suffered higher mortality than the daughters of females exposed to related-familiar males. Collectively, these results suggest that population structure (i.e., variation in the relatedness and/or larval familiarity of local male groups) can modulate male–male competition with important transgenerational consequences.     

Propagule vs. niche limitation: untangling the mechanisms behind plant species' distributions

Distinguishing the roles of propagule limitation and niche requirements in controlling plant species distributions is important for understanding community structure, invasion, and restoration. We used species distribution models based on plant and environmental survey data to assess the strength of species' affinities for particular environmental conditions. We hypothesized that species with statistically detectable environmental requirements were primarily niche-limited, while species with weak habitat affinities were primarily propagule-limited. We tested this hypothesis via a seeding experiment in which we compared species' reproductive fitness in occupied and unoccupied sites. Species that appeared to be niche-limited based on distribution models had lower fitness when planted in unoccupied sites, while species that models suggested were propagule-limited had equivalent fitness when planted in occupied and unoccupied sites. Our results demonstrate that within a single community, both species limited primarily by niche availability or primarily by propagule availability can be identified using observational data.     

Evolution of heterospecific attraction: using other species as cues in habitat selection

We analyzed the ecological conditions that may favor a habitat selection process in which later arriving individuals (colonists) use the presence of earlier established species (residents) as a cue to profitable breeding sites (heterospecific attraction). In our model, colonists assessing potential breeding patches could select between high-quality source and low-quality sink patches. A proportion of the source patches were occupied by residents. Colonists could either directly sample the relative quality of the patches (termed samplers) or, alternatively, they could also use residents as a cue of patch quality (cue-users). Cue-users gained benefit from lowered costs when assessing occupied source patches. The cue-using strategy is an efficient way to choose the best possible patch not only when interspecific competition is intense, but also when benefits from social aggregation exceed the effects of competition. High relative cost of sampling empty patches increases the fitness of the cue-using strategy relative to samplers. The strongest attraction to heterospecifics was predicted when the benefit from aggregating with residents exceeded the effects of competition, and approximately half of the landscape consisted of occupied, high-quality source patches.     

Poor Nutritional Conditions During the Early Larval Stage Reduce Risk‐Taking Activities of Fire Salamander Larvae (Salamandra salamandra)

Environmental conditions experienced early in life have been shown to significantly affect growth trajectories at later stages in many vertebrate species. Amphibians typically have a biphasic life history, with an aquatic larval phase during early development and a subsequent terrestrial adult phase after completed metamorphosis. Thus, the early conditions have an especially strong impact on the future survival and fitness of amphibians. We studied whether early nutritional conditions affect the behavioural reaction of fire salamander larvae (Salamandra salamandra) before completion of metamorphosis. Fire salamander larvae reared under rich nutritional conditions were heavier and larger, displayed better body condition overall throughout the first three month of life and metamorphosed earlier compared with larvae raised under poor nutritional conditions. Specifically, we tested whether larvae reared under these different conditions differed with respect to their risk‐taking behaviour and activity. We found no differences in the activity of larvae with respect to their experienced early food conditions. However, larvae reared under poor nutritional conditions hid significantly more often in a risk‐taking test than larvae reared under rich food conditions. This increase in shelter‐seeking behaviour might be an adaptation to reduce the risk of larval drift or an adaptation to compensate for physiological deficits in part by appropriate behavioural reactions. Our results indicate that environmental conditions, such as food availability, may lead to different behavioural strategies.     

The group-size paradox: effects of learning and patch departure rules

In many species, foraging in groups can enhance individual fitness.However, groups are often predicted to be larger than the sizethat maximizes individual fitness. This is because individualforagers are expected to continue joining a group until thefitness in the group falls to the level experienced by solitaryforagers. If such a process were pervasive, social foraging,paradoxically, would provide little evolutionary advantages.We propose a solution to the group-size paradox by allowingforagers to learn about habitat quality and leave food patcheswhen their current intake rate falls below that expected forthe whole habitat. By using a simulation model, we show thatunder a wide range of population sizes, foragers using suchrules abandon under- and overcrowded patches, ensuring thatgroup size remains close to the optimal value. The results holdin habitats with varying patch quality, but we note that thelack of food renewal in patches can disrupt the process of groupformation. We conclude that groups of optimal sizes can occurfrequently if fitness functions are peaked and resources patchilydistributed, without the need to invoke relatedness betweenjoiners and established group members, group defense againstjoiners, or other mechanisms that were proposed earlier to preventgroups from becoming too large.     

Socially synchronized circadian oscillators

Daily rhythms of physiology and behaviour are governed by an endogenous timekeeping mechanism (a circadian ‘clock’). The alternation of environmental light and darkness synchronizes (entrains) these rhythms to the natural day–night cycle, and underlying mechanisms have been investigated using singly housed animals in the laboratory. But, most species ordinarily would not live out their lives in such seclusion; in their natural habitats, they interact with other individuals, and some live in colonies with highly developed social structures requiring temporal synchronization. Social cues may thus be critical to the adaptive function of the circadian system, but elucidating their role and the responsible mechanisms has proven elusive. Here, we highlight three model systems that are now being applied to understanding the biology of socially synchronized circadian oscillators: the fruitfly, with its powerful array of molecular genetic tools; the honeybee, with its complex natural society and clear division of labour; and, at a different level of biological organization, the rodent suprachiasmatic nucleus, site of the brain''s circadian clock, with its network of mutually coupled single-cell oscillators. Analyses at the ‘group’ level of circadian organization will likely generate a more complex, but ultimately more comprehensive, view of clocks and rhythms and their contribution to fitness in nature.     

Social learning of floral odours inside the honeybee hive

A honeybee hive serves as an information centre in which communication among bees allows the colony to exploit the most profitable resources in a continuously changing environment. The best-studied communication behaviour in this context is the waggle dance performed by returning foragers, which encodes information about the distance and direction to the food source. It has been suggested that another information cue, floral scents transferred within the hive, is also important for recruitment to food sources, as bee recruits are more strongly attracted to odours previously brought back by foragers in both honeybees and bumble-bees. These observations suggested that honeybees learn the odour from successful foragers before leaving the hive. However, this has never been shown directly and the mechanisms and properties of the learning process remain obscure. We tested the learning and memory of recruited bees in the laboratory using the proboscis extension response (PER) paradigm, and show that recruits indeed learn the nectar odours brought back by foragers by associative learning and retrieve this memory in the PER paradigm. The associative nature of this learning reveals that information was gained during mouth-to-mouth contacts among bees (trophallaxis). Results further suggest that the information is transferred to long-term memory. Associative learning of food odours in a social context may help recruits to find a particular food source faster.