Nutrient compensatory foraging in a free-living social insect

The geometric framework model predicts that animal foraging decisions are influenced by their dietary history, with animals targeting a combination of essential nutrients through compensatory foraging. We provide experimental confirmation of nutrient-specific compensatory foraging in a natural, free-living population of social insects by supplementing their diet with sources of protein- or carbohydrate-rich food. Colonies of the ant Iridomyrmex suchieri were provided with feeders containing food rich in either carbohydrate or protein for 6 days, and were then provided with a feeder containing the same or different diet. The patterns of recruitment were consistent with the geometric framework: while feeders with a carbohydrate diet typically attracted more workers than did feeders with protein diet, the difference in recruitment between the two nutrients was smaller if the colonies had had prior access to carbohydrate than protein. Further, fewer ants visited feeders if the colony had had prior access to protein than to carbohydrates, suggesting that the larvae play a role in worker foraging behaviour.     

Experience,but not distance,influences the recruitment precision in the stingless bee <Emphasis Type="Italic">Scaptotrigona mexicana</Emphasis>

Recruitment precision, i.e. the proportion of recruits that reach an advertised food source, is a crucial adaptation of social bees to their environment. Studies with honeybees showed that recruitment precision is not a fixed feature, but it may be enhanced by factors like experience and distance. However, little is known regarding the recruitment precision of stingless bees. Hence, in this study, we examined the effects of experience and spatial distance on the precision of the food communication system of the stingless bee Scaptotrigona mexicana. We conducted the experiments by training bees to a three-dimensional artificial patch at several distances from the colony. We recorded the choices of individual recruited foragers, either being newcomers (foragers without experience with the advertised food source) or experienced (foragers that had previously visited the feeder). We found that the average precision of newcomers (95.6 ± 2.61%) was significantly higher than that of experienced bees (80.2 ± 1.12%). While this might seem counter-intuitive on first sight, this “loss” of precision can be explained by the tendency of experienced recruits to explore nearby areas to find new rewarding food sources after they had initially learned the exact location of the food source. Increasing the distance from the colony had no significant effect on the precision of the foraging bees. Thus, our data show that experience, but not the distance of the food source, affected the patch precision of S. mexicana foragers.     

Parasitoids and competitors influence colony-level responses in the red imported fire ant,<Emphasis Type="Italic"> Solenopsis invicta</Emphasis>

Social insect colonies respond to challenges set by a variable environment by reallocating work among colony members. In many social insects, such colony-level task allocation strategies are achieved through individual decisions that produce a self-organized adapting group. We investigated colony responses to parasitoids and native ant competitors in the red imported fire ant (Solenopsis invicta). Parasitoid flies affected fire ants by decreasing the proportion of workers engaged in foraging. Competitors also altered colony-level behaviours by reducing the proportion of foraging ants and by increasing the proportion of roaming majors, whose role is colony defence. Interestingly, the presence of both parasitism and competition almost always had similar effects on task allocation in comparison to each of the biotic factors on its own. Thus, our study uniquely demonstrates that the interactive effect of both parasitism and competition is not necessarily additive, implying that these biotic factors alter colony behaviour in distinct ways. More generally, our work demonstrates the importance of studying the dynamics of species interactions in a broader context.     

Chemical compounds of the foraging recruitment pheromone in bumblebees

When the frenzied and irregular food-recruitment dances of bumblebees were first discovered, it was thought that they might represent an evolutionary prototype to the honeybee waggle dance. It later emerged that the primary function of the bumblebee dance was the distribution of an alerting pheromone. Here, we identify the chemical compounds of the bumblebee recruitment pheromone and their behaviour effects. The presence of two monoterpenes and one sesquiterpene (eucalyptol, ocimene and farnesol) in the nest airspace and in the tergal glands increases strongly during foraging. Of these, eucalyptol has the strongest recruitment effect when a bee nest is experimentally exposed to it. Since honeybees use terpenes for marking food sources rather than recruiting foragers inside the nest, this suggests independent evolutionary roots of food recruitment in these two groups of bees.     

Behavioral genomics of honeybee foraging and nest defense

The honeybee has been the most important insect species for study of social behavior. The recently released draft genomic sequence for the bee will accelerate honeybee behavioral genetics. Although we lack sufficient tools to manipulate this genome easily, quantitative trait loci (QTLs) that influence natural variation in behavior have been identified and tested for their effects on correlated behavioral traits. We review what is known about the genetics and physiology of two behavioral traits in honeybees, foraging specialization (pollen versus nectar), and defensive behavior, and present evidence that map-based cloning of genes is more feasible in the bee than in other metazoans. We also present bioinformatic analyses of candidate genes within QTL confidence intervals (CIs). The high recombination rate of the bee made it possible to narrow the search to regions containing only 17–61 predicted peptides for each QTL, although CIs covered large genetic distances. Knowledge of correlated behavioral traits, comparative bioinformatics, and expression assays facilitated evaluation of candidate genes. An overrepresentation of genes involved in ovarian development and insulin-like signaling components within pollen foraging QTL regions suggests that an ancestral reproductive gene network was co-opted during the evolution of foraging specialization. The major QTL influencing defensive/aggressive behavior contains orthologs of genes involved in central nervous system activity and neurogenesis. Candidates at the other two defensive-behavior QTLs include modulators of sensory signaling (Am5HT ₇ serotonin receptor, AmArr4 arrestin, and GABA-B-R1 receptor). These studies are the first step in linking natural variation in honeybee social behavior to the identification of underlying genes.     

Temperature limits trail following behaviour through pheromone decay in ants

In Mediterranean habitats, temperature affects both ant foraging behaviour and community structure. Many studies have shown that dominant species often forage at lower temperature than subordinates. Yet, the factors that constrain dominant species foraging activity in hot environments are still elusive. We used the dominant ant Tapinoma nigerrimum as a model species to test the hypothesis that high temperatures hinder trail following behaviour by accelerating pheromone degradation. First, field observations showed that high temperatures (> 30°C) reduce the foraging activity of T. nigerrimum independently of the daily and seasonal rhythms of this species. Second, we isolated the effect of high temperatures on pheromone trail efficacy from its effect on worker physiology. A marked substrate was heated during 10 min (five temperature treatments from 25°C to 60°C), cooled down to 25°C, and offered in a test choice to workers. At hot temperature treatments (>40°C), workers did not discriminate the previously marked substrate. High temperatures appeared therefore to accelerate pheromone degradation. Third, we assessed the pheromone decay dynamics by a mechanistic model fitted with Bayesian inference. The model predicted ant choice through the evolution of pheromone concentration on trails as a function of both temperature and time since pheromone deposition. Overall, our results highlighted that the effect of high temperatures on recruitment intensity was partly due to pheromone evaporation. In the Mediterranean ant communities, this might affect dominant species relying on chemical recruitment, more than subordinate ant species, less dependent on chemical communication and less sensitive to high temperatures.     

The emergence of collective foraging in the arboreal<Emphasis Type="Italic"> Gnamptogenys menadensis</Emphasis> (Hymenoptera: Formicidae)

Gnamptogenys menadensis is an arboreal nester that forages opportunistically almost exclusively on vegetation, sometimes recruiting others to participate in prey retrieval. The three-dimensional characteristics of vegetation suggest that functions describing recruitment decision thresholds or the pattern of recruitment in arboreal species may differ from those predicted by optimal foraging theory. To examine the effects of prey abundance and distance on the recruitment dynamics of G. menadensis, we baited nests with one termite, five termites or a number of termites between 20 and 40 either near to or far from the entrance and observed the ensuing behaviors. G. menadensis recruited others when encountering multiple termites regardless of the termite pile's distance from the nest, although a few individuals remained at the site and defended the resource. The pattern of arrivals at the site indicates that the majority and sometimes all arrivals were recruited from the branch trails. In combination, these results suggest that the architecture of the foraging habitat, which limits available return routes to the nest and thus increases encounter probabilities with potential recruits, shaped the process of information transfer and generated a collective pattern of foraging and prey retrieval.     

Social familiarity modulates group living and foraging behaviour of juvenile predatory mites

Environmental stressors during early life may have persistent consequences for phenotypic development and fitness. In group-living species, an important stressor during juvenile development is the presence and familiarity status of conspecific individuals. To alleviate intraspecific conflicts during juvenile development, many animals evolved the ability to discriminate familiar and unfamiliar individuals based on prior association and use this ability to preferentially associate with familiar individuals. Assuming that familiar neighbours require less attention than unfamiliar ones, as predicted by limited attention theory, assorting with familiar individuals should increase the efficiency in other tasks. We assessed the influence of social familiarity on within-group association behaviour, development and foraging of juvenile life stages of the group-living, plant-inhabiting predatory mite Phytoseiulus persimilis. The observed groups consisted either of mixed-age familiar and unfamiliar juvenile mites or of age-synchronized familiar or unfamiliar juvenile mites or of pairs of familiar or unfamiliar larvae. Overall, familiar mites preferentially grouped together and foraged more efficiently, i.e. needed less prey at similar developmental speed and body size at maturity, than unfamiliar mites. Preferential association of familiar mites was also apparent in the inter-exuviae distances. Social familiarity was established by imprinting in the larval stage, was not cancelled or overridden by later conspecific contacts and persisted into adulthood. Life stage had an effect on grouping with larvae being closer together than nymphal stages. Ultimately, optimized foraging during the developmental phase may relax within-group competition, enhance current and future food supply needed for optimal development and optimize patch exploitation and leaving under limited food.     

Yellowjackets use nest-based cues to differentially exploit higher-quality resources

While foraging, social insects encounter a dynamic array of food resources of varying quality and profitability. Because food acquisition influences colony growth and fitness, natural selection can be expected to favor colonies that allocate their overall foraging effort so as to maximize their intake of high-quality nutrients. Social wasps lack recruitment communication, but previous studies of vespine wasps have shown that olfactory cues influence foraging decisions. Odors associated with food brought into the nest by successful foragers prompt naive foragers to leave the nest and search for the source of those odors. Left unanswered, however, is the question of whether naive foragers take food quality into account in making their decisions about whether or not to search. In this study, two different concentrations of sucrose solutions, scented differently, were inserted directly into each of three Vespula germanica nests. At a feeder away from the nest, arriving foragers were given a choice between two 1.5 M sucrose solutions with the same scents as those in the nest. We show that wasps chose higher-quality resources in the field using information in the form of intranidal food-associated odor cues. By this simple mechanism, the colony can bias the allocation of its foraging effort toward higher-quality resources in the environment.     

Transient division of labor and behavioral specialization in the ant Formica schaufussi

Cooperative prey retrieval in the monomorphic ant Formica schaufussi is carried out by workers that perform functionally distinct roles which persist only for the duration of a single retrieval event. A forager (scout) that locates prey too large to retrieve individually organizes cooperative prey transport by recruiting nestmates (recruits) to assist in retrieval. The scout and recruit roles appear to be determined by whether a worker activates recruitment or is recruited from the nest. Scouts organize recruitment and play a key role in maintaining the cohesion of the retrieval group. If a scout that has initiated group transport is experimentally removed, the recruited workers composing the retrieval group typically abandon the prey and cooperative foraging is terminated. In this context, recruits are unable to function as scouts and reorganize group transport. Individuals marked as recruits in one prey retrieval, however, can switch and act as scouts in subsequent retrievals. Because the roles of individuals persist within but not between retrieval events, the specialization involved in cooperative prey retrieval cannot easily be explained as a response associated with age-related or genetic predispositions. This transient division-of-labor, in which individual roles may persist only for the duration of a single group action, represents a novel type of short-term individual specialization.     

Worker honey bee pheromone regulation of foraging ontogeny

The evolution of sociality has configured communication chemicals, called primer pheromones, which play key roles in regulating the organization of social life. Primer pheromones exert relatively slow effects that fundamentally alter developmental, physiological, and neural systems. Here, I demonstrate how substances extracted from the surface of foraging and young pre-foraging worker bees regulated age at onset of foraging, a developmental process. Hexane-extractable compounds washed from foraging workers increased foraging age compared with controls, whereas extracts of young pre-foraging workers decreased foraging age. This represents the first known direct demonstration of primer pheromone activity derived from adult worker bees.     

Social learning of an associative foraging task in zebrafish

The zebrafish (Danio rerio) is increasingly becoming an important model species for studies on the genetic and neural mechanisms controlling behaviour and cognition. Here, we utilized a conditioned place preference (CPP) paradigm to study social learning in zebrafish. We tested whether social interactions with conditioned demonstrators enhance the ability of focal naïve individuals to learn an associative foraging task. We found that the presence of conditioned demonstrators improved focal fish foraging behaviour through the process of social transmission, whereas the presence of inexperienced demonstrators interfered with the learning of the control focal fish. Our results indicate that zebrafish use social learning for finding food and that this CPP paradigm is an efficient assay to study social learning and memory in zebrafish.     

How floral odours are learned inside the bumblebee (Bombus terrestris) nest

Recruitment in social insects often involves not only inducing nestmates to leave the nest, but also communicating crucial information about finding profitable food sources. Although bumblebees transmit chemosensory information (floral scent), the transmission mechanism is unknown as mouth-to-mouth fluid transfer (as in honeybees) does not occur. Because recruiting bumblebees release a pheromone in the nest that triggers foraging in previously inactive workers, we tested whether this pheromone helps workers learn currently rewarding floral odours, as found in food social learning in rats. We exposed colonies to artificial recruitment pheromone, paired with anise scent. The pheromone did not facilitate learning of floral scent. However, we found that releasing floral scent in the air of the colony was sufficient to trigger learning and that learning performance was improved when the chemosensory cue was provided in the nectar in honeypots; probably because it guarantees a tighter link between scent and reward, and possibly because gustatory cues are involved in addition to olfaction. Scent learning was maximal when anise-scented nectar was brought into the nest by demonstrator foragers, suggesting that previously unidentified cues provided by successful foragers play an important role in nestmates learning new floral odours.     

Variation of foraging rate and wing loading, but not resting metabolic rate scaling, of insect pollinators

Morphological, physiological and behavioural variation with body size (i.e. scaling) may affect costs of living in a particular environment for insects and, ultimately, pollination or foraging success. However, few studies have directly assessed the scaling of these traits at the species level. Using two similar-sized pollinator species (the hawkmoth Macroglossum trochilus and the fly Moegistorhynchus longirostrus), we compare intraspecific scaling relationships of resting metabolic rate (RMR), foraging rate (FR) and wing loading (WL) to address this paucity of data. Scaling of RMR was similar for both taxa although the intercepts for the relationships differed. However, these two species showed variation in WL scaling relationships and fundamentally different FR scaling. For M. longirostrus, FR scaling was positive but non-significantly related to body mass while for M. trochilus FR scaling was negative. This suggests that variation in FR and WL, but not RMR scaling, among these flies and hawkmoths may impose significant energetic costs which could affect animal–plant interactions in the wild.     

Coming out of the woods: do termites need a specialized worker caste to search for new food sources?

Most small-colony termites live confined within a single piece of wood on which they feed and do not possess permanent workers: Tasks are done by developmentally flexible immatures (pseudergates). By contrast, large-colony termites possess a specialized (true) worker caste and forage outside their nest for food. To shed light on possible transitional steps between these contrasting patterns of social organization, we studied an atypical Rhinotermitidae, Prorhinotermes inopinatus. In this species, despite the absence of a true worker caste, soldiers, pseudergates, and neotenic reproductives may leave the nest and explore their surroundings. Although evidence presented in this study indicates that termites recognize unknown areas, there is no directional recruitment toward them. The discovery of a food source, i.e., a piece of wood, is followed by the establishment of a long-lasting trail between the nest and the food source. A large fraction of the colony, including neotenic reproductives, ultimately migrates into the piece of wood. Our results thus demonstrate that multiple features of external foraging behavior can evolve independently of the existence of a true worker caste in termites. We suggest that large colonies with true workers, like those of most Rhinotermitidae, may easily have evolved from a Prorhinotermes-like pattern if submitted to increasing selective pressures for worker efficiency in a stable environment.     

Recruits of the stingless bee Scaptotrigona pectoralis learn food odors from the nest atmosphere

The ability to learn food odors inside the nest and to associate them with food sources in the field is of essential importance for the recruitment of nestmates in social bees. We investigated odor learning by workers within the hive and the influence of these odors on their food choice in the field in the stingless bee Scaptotrigona pectoralis. During the experiments, recruited bees had to choose between two feeders, one with an odor that was present inside the nest during the recruitment process, and one with an unknown odor. In all experiments with different odor combinations (linalool/phenylacetaldehyde, geraniol/eugenol) a significant majority of bees visited the feeder with the odor they had experienced in their nest (χ ²-tests; p?<?0.05). By contrast, the bees showed no preference for one of two feeders when they were either baited with the same odor (linalool) or contained no odor. Our results clearly show that naïve workers of S. pectoralis can learn the odor of a food source during the recruitment process from the nest atmosphere and that their subsequent food search in the field is influenced by the learned odor.     

Reverse positional orientation in a neotropical orb-web spider, <Emphasis Type="Italic">Verrucosa arenata</Emphasis>

Most orb-web spiders face downwards in the web. A downward orientation has been proposed to be the optimal strategy because spiders run faster downwards and thus can catch prey quicker. Consequently, orb-web spiders also extend their web in the lower part, leading to top-down web asymmetry. Since the majority of orb-web spiders face downwards, it has been difficult to test the effect of orientation on prey capture and web asymmetry. In this study, we explored the influence of reverse orientation on foraging efficiency and web asymmetry in Verrucosa arenata, a neotropical orb-web spider that faces upwards in the web. We show that reverse orientation does not imply reverse web asymmetry in this species. V. arenata spiders captured more prey in the lower part of the web but more prey per area on the upper part. The average running speeds of spiders did not differ between upward and downward running, but heavier spiders took longer to capture prey while running upwards. We discuss these findings in the context of foraging efficiency and web asymmetry.     

Indirect defense in a highly specific ant–plant mutualism

Although associations between myrmecophytes and their plant ants are recognized as a particularly effective form of protective mutualism, their functioning remains incompletely understood. This field study examined the ant-plant Hirtella physophora and its obligate ant associate Allomerus decemarticulatus. We formulated two hypotheses on the highly specific nature of this association: (1) Ant presence should be correlated with a marked reduction in the amount of herbivory on the plant foliage; (2) ant activity should be consistent with the "optimal defense" theory predicting that the most vulnerable and valuable parts of the plant are the best defended. We validated the first hypothesis by demonstrating that for ant-excluded plants, expanding leaves, but also newly matured ones in the long term, suffered significantly more herbivore damage than ant-inhabited plants. We showed that A. decemarticulatus workers represent both constitutive and inducible defenses for their host, by patrolling its foliage and rapidly recruiting nestmates to foliar wounds. On examining how these activities change according to the leaves’ developmental stage, we found that the number of patrolling ants dramatically decreased as the leaves matured, while leaf wounds induced ant recruitment regardless of the leaf’s age. The resulting level of these indirect defenses was roughly proportional to leaf vulnerability and value during its development, thus validating our second hypothesis predicting optimal protection. This led us to discuss the factors influencing ant activity on the plant’s surface. Our study emphasizes the importance of studying both the constitutive and inducible components of indirect defense when evaluating its efficacy and optimality.     

Winged queens replaced by reproductives smaller than workers in <Emphasis Type="Italic">Mystrium</Emphasis> ants

In ants, winged queens that are specialized for independent colony foundation can be replaced by wingless reproductives better adapted for colony fission. We studied this shift in reproductive strategy by comparing two Mystrium species from Madagascar using morphometry, allometry and dissections. Mystrium rogeri has a single dealate queen in each colony with a larger thorax than workers and similar mandibles that allow these queens to hunt during non-claustral foundation. In contrast, Mystrium ‘red’ lacks winged queens and half of the female adults belong to a wingless ‘intermorph’ caste smaller and allometrically distinct from the workers. Intermorphs have functional ovaries and spermatheca while those of workers are degenerate. Intermorphs care for brood and a few mate and reproduce making them an all-purpose caste that takes charge of both work and reproduction. However, their mandibles are reduced and inappropriate for hunting centipedes, unlike the workers’ mandibles. This together with their small thorax disallow them to perform independent colony foundation, and colonies reproduce by fission. M. rogeri workers have mandibles polymorphic in size and shape, which allow for all tasks from brood care to hunting. In M. ‘red’, colonial investment in reproduction has shifted from producing expensive winged queens to more numerous helpers. M. ‘red’ intermorphs are the first case of reproductives smaller than workers in ants and illustrate their potential to diversify their caste system for better colonial economy.     

High precision during food recruitment of experienced (reactivated) foragers in the stingless bee<Emphasis Type="Italic"> Scaptotrigona mexicana</Emphasis> (Apidae,Meliponini)

Several studies have examined the existence of recruitment communication mechanisms in stingless bees. However, the spatial accuracy of location-specific recruitment has not been examined. Moreover, the location-specific recruitment of reactivated foragers, i.e., foragers that have previously experienced the same food source at a different location and time, has not been explicitly examined. However, such foragers may also play a significant role in colony foraging, particularly in small colonies. Here we report that reactivated Scaptotrigona mexicana foragers can recruit with high precision to a specific food location. The recruitment precision of reactivated foragers was evaluated by placing control feeders to the left and the right of the training feeder (direction-precision tests) and between the nest and the training feeder and beyond it (distance-precision tests). Reactivated foragers arrived at the correct location with high precision: 98.44% arrived at the training feeder in the direction trials (five-feeder fan-shaped array, accuracy of at least ±6° of azimuth at 50 m from the nest), and 88.62% arrived at the training feeder in the distance trials (five-feeder linear array, accuracy of at least ±5 m or ±10% at 50 m from the nest). Thus, S. mexicana reactivated foragers can find the indicated food source at a specific distance and direction with high precision, higher than that shown by honeybees, Apis mellifera, which do not communicate food location at such close distances to the nest.