Effects of acephate and glyphosate-based agrochemicals on the survival and flight of Plebeia lucii Moure, 2004 (Apidae: Meliponini).

The conservation of terrestrial ecosystems depends largely on the preservation of pollinators, mainly bees. Stingless bees are among the main pollinators of native plants and crops in tropical regions, where they can be exposed to agrochemicals while foraging on contaminated flowers. In the present study, we investigated the effects on stingless bees of both a commonly used insecticide and herbicide in Brazil. Plebeia lucii Moure, 2004 (Apidae: Meliponini) foragers were orally chronically exposed to food contaminated with different concentrations of commercial formulations of the insecticide acephate or the herbicide glyphosate. Bee mortality increased with increasing agrochemical concentrations. Depending on its concentration, the acephate-based formulation reduced the lifespan and impaired the flight ability of bees. The glyphosate-based formulation was toxic only under unrealistic concentrations. Our results demonstrate that realistic concentrations of acephate-based insecticides harm the survival and alter the mobility of stingless bees. The ingestion of glyphosate-based herbicides was safe for forager bees under realistic concentrations.

Diverse communication strategies in bees as a window into adaptations to an unpredictable world.

Communication is a fundamental feature of animal societies and helps their members to solve the challenges they encounter, from exploiting food sources to fighting enemies or finding a new home. Eusocial bees inhabit a wide range of environments and they have evolved a multitude of communication signals that help them exploit resources in their environment efficiently. We highlight recent advances in our understanding of bee communication strategies and discuss how variation in social biology, such as colony size or nesting habits, and ecological conditions are important drivers of variation in communication strategies. Anthropogenic factors, such as habitat conversion, climate change, or the use of agrochemicals, are changing the world bees inhabit, and it is becoming clear that this affects communication both directly and indirectly, for example by affecting food source availability, social interactions among nestmates, and cognitive functions. Whether and how bees adapt their foraging and communication strategies to these changes represents a new frontier in bee behavioral and conservation research.

Pollinator conservation: Where will bees go in the Anthropocene future?

For pollinator conservation in human-transformed landscapes, it is crucial to know whether species can overcome gaps between fragments of natural habitat. A new study reveals why colony size, recruitment communication, and flower constancy increase the foraging ranges in social bees.

Data standardization of plant-pollinator interactions.

BACKGROUND: Animal pollination is an important ecosystem function and service, ensuring both the integrity of natural systems and human well-being. Although many knowledge shortfalls remain, some high-quality data sets on biological interactions are now available. The development and adoption of standards for biodiversity data and metadata has promoted great advances in biological data sharing and aggregation, supporting large-scale studies and science-based public policies. However, these standards are currently not suitable to fully support interaction data sharing. RESULTS: Here we present a vocabulary of terms and a data model for sharing plant-pollinator interactions data based on the Darwin Core standard. The vocabulary introduces 48 new terms targeting several aspects of plant-pollinator interactions and can be used to capture information from different approaches and scales. Additionally, we provide solutions for data serialization using RDF, XML, and DwC-Archives and recommendations of existing controlled vocabularies for some of the terms. Our contribution supports open access to standardized data on plant-pollinator interactions. CONCLUSIONS: The adoption of the vocabulary would facilitate data sharing to support studies ranging from the spatial and temporal distribution of interactions to the taxonomic, phenological, functional, and phylogenetic aspects of plant-pollinator interactions. We expect to fill data and knowledge gaps, thus further enabling scientific research on the ecology and evolution of plant-pollinator communities, biodiversity conservation, ecosystem services, and the development of public policies. The proposed data model is flexible and can be adapted for sharing other types of interactions data by developing discipline-specific vocabularies of terms.

Linking body condition and thermal physiology in limping crickets: Does limb autotomy incur costs concerning behavioral thermal tolerance?

Many ectotherms have the ability to voluntarily detach a body part, known as autotomy, usually in response to predator attacks. Autotomy can have an immediate benefit for survival, but it can also involve costs related to the individual's body condition. Even though the effects of autotomy have been studied in many ecophysiological aspects, its short-term costs on the ability to tolerate high environmental temperatures are still unexplored. Herein, we evaluated the effects of autotomy on the behavioral thermal tolerance (VTMax ) in the cricket Gryllus assimilis. We hypothesized that, due to the increased energetic costs to maintain homeostasis, autotomized crickets have a lower VTMax than intact ones. Additionally, we investigated differences in VTMax between sexes, as well as the effects of heating rates and body mass on their VTMax . Contrary to our hypothesis, we found no differences between VTMax of autotomized and intact individuals. However, we observed that females have a higher VTMax than males, regardless of their condition (i.e., autotomized and intact). Moreover, we detected significant effects of body mass and heating rate on behavioral thermal tolerances. The results of our study indicate that costs associated with limb autotomy at high environmental temperatures might be intricate and not immediately impactful. Furthermore, important aspects of reproduction and ecology might be responsible for differences in VTMax between males and females. Our results contribute to understanding the ecological and physiological aspects of ectotherms and how they respond to changing climatic conditions.

Increasing thermal stress with flight distance in stingless bees (Melipona subnitida) in the Brazilian tropical dry forest: Implications for constraint on foraging range.

The thoracic temperature (TTX) of foraging bees usually exceeds ambient air temperatures (TAIR) by several degrees. In hot tropical climate zones, therefore, individuals may reach body temperatures close to their critical thermal maxima, which might constrain their activity. In the present study, we tested the hypothesis that thermal stress increases with flight distance in nectar foragers of M. subnitida, a stingless bee species native to the hottest regions of the Brazilian tropical dry forest. Using infrared thermography, we recorded the body surface temperature of individuals foraging at distances of 15, 50, and 100 m. Closest to the nests, foragers stabilized TTX at 40 °C when collecting sugar solution at TAIR > 30 °C. The simultaneous decrease of the temperature excess ratio of head and abdomen suggests evaporative cooling at these body parts. With increasing foraging distance, foragers increased heat dissipation to the head and abdomen. Thus, despite more intensive heating of the thorax due to faster and longer flights, the bees maintained similar TTX as foragers at close feeding sites. However, at TAIR > 30 °C, bees could no longer compensate the elevated heat gain at the head (50 m) and abdomen (50, 100 m), which caused an increasing temperature excess in these body parts. Thus, foragers of M. subnitida suffer overheating of the head and abdomen instead of the thorax when foraging in high temperatures at far feeding sites. Consequently, to avoid heat stress in the Brazilian tropical dry forest, the bees should forage close to the nest.

A Comparative Study of Food Source Selection in Stingless Bees and Honeybees: Scent Marks, Location, or Color.

In social bees, the choice of food sources is based on several factors, including scent marks, color, and location of flowers. Here, we used similar setups, in which two stingless bee species, Melipona subnitida and Plebeia flavocincta, and the Western honeybee, Apis mellifera, were tested regarding the importance of chemical cues, color cues, and location-dependent cues for foraging behavior. It was determined whether workers chose food sources according to (1) scent marks deposited by conspecifics, (2) the color hue of a food source, (3) the trained location or the proximity of a food source to the hive. All three species preferred the scent-marked over an unmarked feeder that was presented simultaneously, but M. subnitida showed a weaker preference compared to the other species. When trained to blue feeders all three bee species preferred blue, but A. mellifera showed the strongest fidelity. The training to yellow feeders led to less distinct color choices. Only workers of M. subnitida mostly orientated at the training position and the close proximity to the nest. Whether the distance of a feeding site influenced the choice was dependent on the tested parameter (color or scent marks) and the species. Workers of M. subnitida preferably visited the feeder closer to the nest during the scent mark trials, but choose randomly when tested for color learning. Worker honeybees preferred the closer feeding site if trained to yellow, but not if trained to blue, and preferred the more distant feeder during the scent mark trials. Workers of P. flavocincta preferred the closer feeder if trained to blue or yellow, and preferred the more distant feeder during the scent mark trials. The disparity among the species corresponds to differences in body size. Smaller bees are known for reduced visual capabilities and might rely less on visual parameters of the target such as color hue, saturation, or brightness but use scent cues instead. Moreover, the dim-light conditions in forest habitats might reduce the reliability of visual orientation as compared to olfactory orientation. Honeybees showed the most pronounced orientation at floral color cues.

Adjustment of fuel loads in stingless bees (Melipona subnitida).

Eusocial bee foragers leave their nest with nectar as flight fuel, therewith reducing the risk of starvation during a foraging trip. Yet, the extra mass results in an increase of energetic expenditure for flight. Thus, bees should tune their fuel loads to the respective foraging situation. In the present study, we investigated the fuel adjustment in the Brazilian stingless bee Melipona subnitida (Apidae, Meliponini). Specifically, we examined whether foragers of this species increase their fuel loads when they have low expectation for nectar collection during a foraging trip. Crop load measurements revealed that nectar foragers carried significantly less fuel on departing the nest than foragers collecting either pollen, clay, or resin. Surprisingly, 75% of nectar foragers left the nest without any detectable amount of nectar, which suggests that the majority of bees collected at nearby nectar sources and avoided an increase in foraging costs. Moreover, foragers increased their fuel loading when repeatedly experiencing empty food sources that had previously been rewarding. These results support our hypothesis and demonstrate that the capability of fuel adjustment is not restricted to honey bees.

Landscape genomics to the rescue of a tropical bee threatened by habitat loss and climate change.

Habitat degradation and climate change are currently threatening wild pollinators, compromising their ability to provide pollination services to wild and cultivated plants. Landscape genomics offers powerful tools to assess the influence of landscape modifications on genetic diversity and functional connectivity, and to identify adaptations to local environmental conditions that could facilitate future bee survival. Here, we assessed range-wide patterns of genetic structure, genetic diversity, gene flow, and local adaptation in the stingless bee Melipona subnitida, a tropical pollinator of key biological and economic importance inhabiting one of the driest and hottest regions of South America. Our results reveal four genetic clusters across the species' full distribution range. All populations were found to be under a mutation-drift equilibrium, and genetic diversity was not influenced by the amount of reminiscent natural habitats. However, genetic relatedness was spatially autocorrelated and isolation by landscape resistance explained range-wide relatedness patterns better than isolation by geographic distance, contradicting earlier findings for stingless bees. Specifically, gene flow was enhanced by increased thermal stability, higher forest cover, lower elevations, and less corrugated terrains. Finally, we detected genomic signatures of adaptation to temperature, precipitation, and forest cover, spatially distributed in latitudinal and altitudinal patterns. Taken together, our findings shed important light on the life history of M. subnitida and highlight the role of regions with large thermal fluctuations, deforested areas, and mountain ranges as dispersal barriers. Conservation actions such as restricting long-distance colony transportation, preserving local adaptations, and improving the connectivity between highlands and lowlands are likely to assure future pollination services.

Stingless bees and their adaptations to extreme environments.

Nearly half of all terrestrial tropical ecosystems around the globe comprise dry forests, characterised through elevated temperatures all year round, and short rainy seasons at irregular intervals. The consequent water deficit over several consecutive months limits the availability of floral resources to often very brief and unpredictable periods, which poses a challenge to the maintenance of perennial colonies in highly eusocial bees. Thus, only few highly eusocial bees occur permanently in tropical dry forests, among them some highly adapted species of stingless bees (Apidae, Meliponini). In the present review, we discuss the current knowledge on the adaptations to such extreme environments in Melipona subnitida, a stingless bee native to the Brazilian tropical dry forest. Key to the success of this species is not so much heat resistance of foragers, as it is the ability to maintain perennial colonies despite extended dearth periods. After several months of drought, M. subnitida colonies are capable of re-establishing fully functional colonies from nests containing only few dozens of workers. This surprising resilience is based on a quick reaction to precipitation-driven increase in floral resource availability, mainly owing to selective foraging at high-profit resources and an immediate up-regulation of brood production once food storage conditions improve.

Honey bee workers generate low-frequency vibrations that are reliable indicators of their activity level.

In social insects, the tuning of activity levels among different worker task groups, which constitutes a fundamental basis of colony organization, relies on the exchange of reliable information on the activity level of individuals. The underlying stimuli, however, have remained largely unexplored so far. In the present study, we describe low-frequency thoracic vibrations generated by honey bee workers (Apis mellifera) within the colony, whose velocity amplitudes and main frequency components significantly increased with the level of an individual's activity. The characteristics of these vibrations segregated three main activity level-groups: foragers, active hive bees, and inactive hive bees. Nectar foragers, moreover, modulated their low-frequency vibrations during trophallactic food unloading to nestmates according to the quality of the collected food. Owing to their clear association with the activity level of an individual and their potential perceptibility during direct contacts, these low-frequency thoracic vibrations are candidate stimuli for providing unambiguous local information on the motivational status of honey bee workers.

Stingless bees (Meliponini): senses and behavior.

Stingless bees (Hymenoptera, Apidae, Meliponini) are by far the largest group of eusocial bees on Earth. Due to the diversity of evolutionary responses to specific ecological challenges, the Meliponini are well suited for comparative studies of the various adaptations to the environment found in highly eusocial bees. Of particular interest are the physiological mechanisms underlying the sophisticated cooperative and collective actions of entire colonies, which form the basis of the ecological success of the different bee species under the particular conditions prevailing in their respective environment. The present Special Issue of the Journal of Comparative Physiology A provides a sample of the exciting diversity of sensorial and behavioral adaptations in stingless bees, particularly concerning (1) the sensory bases for foraging, (2) chemical communication, and (3) the behavioral ecology of foraging.

Stingless bees (Melipona scutellaris) learn to associate footprint cues at food sources with a specific reward context.

Foraging insects leave chemical footprints on flowers that subsequent foragers may use as indicators for recent flower visits and, thus, potential resource depletion. Accordingly, foragers should reject food sources presenting these chemical cues. Contrasting this assumption, experimental studies in stingless bees (Apidae, Meliponini), so far, demonstrated an attractive effect of footprints. These findings lead to doubts about the meaning of these chemical cues in natural foraging contexts. Here, we asked whether foragers of stingless bees (Melipona scutellaris) use footprints according to the previously experienced reward level of visited food sources. Bees were trained to artificial flower patches, at which the reward of a flower either decreased or, alternatively, increased after a visit by a forager. Individuals were allowed a total of nine foraging bouts to the patch, after which their preference for visited or unvisited flowers was tested. In the choice tests, bees trained under the decreasing reward context preferred unvisited flowers, whereas individuals trained under the increasing reward context preferred visited flowers. Foragers without experience chose randomly between visited and unvisited flowers. These results demonstrate that M. scutellaris learns to associate unspecific footprint cues at food sources with differential, specific reward contexts, and uses these chemical cues accordingly for their foraging decisions.

Nectar profitability, not empty honey stores, stimulate recruitment and foraging in Melipona scutellaris (Apidae, Meliponini).

In stingless bees (Meliponini) like in many other eusocial insect colonies food hoarding plays an important role in colony survival. However, very little is known on how Meliponini, a taxon restricted to tropical and subtropical regions, respond to different store conditions. We studied the impact of honey removal on nectar foraging activity and recruitment behaviour in Melipona scutellaris and compared our results with studies of the honey bee Apis mellifera. As expected, foraging activity increased significantly during abundance of artificial nectar and when increasing its profitability. Foraging activity on colony level could thereby frequently increase by an order of magnitude. Intriguingly, however, poor honey store conditions did not induce increased nectar foraging or recruitment activity. We discuss possible reasons explaining why increasing recruitment and foraging activity are not used by meliponines to compensate for poor food conditions in the nest. Among these are meliponine specific adaptations to climatic and environmental conditions, as well as physiology and brood rearing, such as mass provisioning of the brood.

Stingless bees (Melipona subnitida) adjust brood production rather than foraging activity in response to changes in pollen stores.

Highly eusocial bees (honey bees and stingless bees) sustain their colonies through periods of resource scarcity by food stored within the nest. The protein supply necessary for successful brood production is ensured through adjustments of the colonies' pollen foraging according to the availability of this resource in the environment. In honey bees Apis mellifera, in addition, pollen foraging is regulated through the broods' demand for this resource. Here, we investigated the influence of the colony's pollen store level on pollen foraging and brood production in stingless bees (Melipona subnitida). When pollen was added to the nests, colonies increased their brood production and reduced their pollen foraging within 24 h. On the other hand, when pollen reserves were removed, colonies significantly reduced their brood production. In strong contrast to A. mellifera; however, M. subnitida did not significantly increase its pollen foraging activity under poor pollen store conditions. This difference concerning the regulation of pollen foraging may be due to differences regarding the mechanism of brood provisioning. Honey bees progressively feed young larvae and, consequently, require a constant pollen supply. Stingless bees, by contrast, mass-provision their brood cells and temporary absence of pollen storage will not immediately result in substantial brood loss.

Sexual dimorphism and phenotypic plasticity in the antennal lobe of a stingless bee, Melipona scutellaris.

Among social insects, the stingless bees (Apidae, Meliponini), a mainly tropical group of highly eusocial bees, present an intriguing variety of well-described olfactory-dependent behaviors showing both caste- and sex-specific adaptations. By contrast, little is known about the neural structures underlying such behavioral richness or the olfactory detection and processing abilities of this insect group. This study therefore aimed to provide the first detailed description and comparison of the brains and primary olfactory centers, the antennal lobes, of the different members of a colony of the stingless bee Melipona scutellaris. Global neutral red staining, confocal laser scanning microscopy, and 3D reconstructions were used to compare the brain structures of males, workers, and virgin queens with a special emphasis on the antennal lobe. We found significant differences between both sexes and castes with regard to the relative volumes of olfactory and visual neuropils in the brain and also in the number and volume of the olfactory glomeruli. In addition, we identified one (workers, queens) and three or four (males) macroglomeruli in the antennal lobe. In both sexes and all castes, the largest glomerulus (G1) was located at a similar position relative to four identified landmark glomeruli, close to the entrance of the antennal nerve. This similarity in position suggests that G1s of workers, virgin queens, and males of M. scutellaris may correspond to the same glomerular entity, possibly tuned to queen-emitted volatiles since all colony members need this information.

Out with the garbage: the parasitic strategy of the mantisfly Plega hagenella mass-infesting colonies of the eusocial bee Melipona subnitida in northeastern Brazil.

Between April and June of 2012 mantisflies (Plega hagenella) were found to be extensively parasitizing the nests of two groups of managed colonzies of eusocial stingless bees (Melipona subnitida) in the semi-arid region of northeastern Brazil. The mantisfly larvae developed inside closed brood cells of the bee comb, where each mantispid larva fed on the bee larva or pupa present in a single brood cell. Mature mantispid larvae pupated inside silken cocoons spun in place within their hosts' brood cells then emerged as pharate adults inside the bee colony. Pharate adults were never attacked and killed by host colony workers. Instead, colony workers picked up the pharates and removed them from the nest unharmed, treating them similar to the way that the general refuse is removed from the nest. Adult mantispids subsequently eclosed from their pupal exuviae outside the nest. Manipulative experiments showed that post-eclosion adult mantispids placed back within active bee colonies were quickly attacked and killed. These observations demonstrate that pharate and post-eclosion adults of P. hagenella are perceived differently by colony workers and that delayed adult eclosion is an important functional element in the parasitic life strategy of P. hagenella, allowing adults to escape without injury from the bee colonies they parasitize.

The recruiter's excitement--features of thoracic vibrations during the honey bee's waggle dance related to food source profitability.

The honey bee's waggle dance constitutes a remarkable example of an efficient code allowing social exploitation of available feeding sites. In addition to indicating the position (distance, direction) of a food patch, both the occurrence and frequency of the dances depend on the profitability of the exploited resource (sugar concentration, solution flow rate). During the waggle dance, successful foragers generate pulsed thoracic vibrations that putatively serve as a source of different kinds of information for hive bees, who cannot visually decode dances in the darkness of the hive. In the present study, we asked whether these vibrations are a reliable estimator of the excitement of the dancer when food profitability changes in terms of both sugar concentration and solution flow rate. The probability of producing thoracic vibrations as well as several features related to their intensity during the waggle phase (pulse duration, velocity amplitude, duty cycle) increased with both these profitability variables. The number of vibratory pulses, however, was independent of sugar concentration and reward rate exploited. Thus, pulse number could indeed be used by dance followers as reliable information about food source distance, as suggested in previous studies. The variability of the dancer's thoracic vibrations in relation to changes in food profitability suggests their role as an indicator of the recruiter's motivational state. Hence, the vibrations could make an important contribution to forager reactivation and, consequently, to the organisation of collective foraging processes in honey bees.

Olfactory eavesdropping between two competing stingless bee species.

Foragers can improve search efficiency, and ultimately fitness, by using social information: cues and signals produced by other animals that indicate food location or quality. Social information use has been well studied in predator-prey systems, but its functioning within a trophic level remains poorly understood. Eavesdropping, use of signals by unintended recipients, is of particular interest because eavesdroppers may exert selective pressure on signaling systems. We provide the most complete study to date of eavesdropping between two competing social insect species by determining the glandular source and composition of a recruitment pheromone, and by examining reciprocal heterospecific responses to this signal. We tested eavesdropping between Trigona hyalinata and Trigona spinipes, two stingless bee species that compete for floral resources, exhibit a clear dominance hierarchy and recruit nestmates to high-quality food sources via pheromone trails. Gas chromatography-mass spectrometry of T. hyalinata recruitment pheromone revealed six carboxylic esters, the most common of which is octyl octanoate, the major component of T. spinipes recruitment pheromone. We demonstrate heterospecific detection of recruitment pheromones, which can influence heterospecific and conspecific scout orientation. Unexpectedly, the dominant T. hyalinata avoided T. spinipes pheromone in preference tests, while the subordinate T. spinipes showed neither attraction to nor avoidance of T. hyalinata pheromone. We suggest that stingless bees may seek to avoid conflict through their eavesdropping behavior, incorporating expected costs associated with a choice into the decision-making process. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1007/s00265-010-1080-3) contains supplementary material, which is available to authorized users.