Michael Hrncir

Signals and cues in the recruitment behavior of stingless bees (Meliponini)

Since the seminal work of Lindauer and Kerr (1958), many stingless bees have been known to effectively recruit nestmates to food sources. Recent research clarified properties of several signals and cues used by stingless bees when exploiting food sources. Thus, the main source of the trail pheromone in Trigona are the labial, not however the mandibular glands. In T. recursa and T. spinipes, the first stingless bee trail pheromones were identified as hexyl decanoate and octyl decanoate, respectively. The attractant footprints left by foragers at the food source are secreted by glandular epithelia of the claw retractor tendon, not however by the tarsal gland. Regarding intranidal communication, the correlation between a forager’s jostling rate and recruitment success stresses the importance of agitated running and jostling. There is no evidence for a “dance” indicating food source location, however, whereas the jostling rate depends on food quality. Thoracic vibrations, another intranidal signal well known in Melipona, were analyzed using modern technology and distinguishing substrate vibrations from airborne sound. Quantitative data now permit estimates of signal and potential communication ranges. Airflow jets as described for the honeybee were not found, and thoracic vibrations do not “symbolically” encode visually measured distance in M. seminigra.

Food exploitation by social insects : ecological, behavioral, and theoretical approaches

Foraging is a complex task, particularly in a social animal. This chapter will focus on one critical aspect of social insect foraging, namely, navigation, without reiterating all the important aspects related to social insects’ communication and foraging behaviors. I will briey provide an overview of some important, but distinct, ways in which medium-range navigation in foraging insects have been modeled, with a particular focus on the effects of social interactions.Measuring the Adaptiveness of Social Insect Foraging Strategies: An Empirical Approach, N.E. Raine and L. Chittka Social Cues and Adaptive Foraging Strategies in Ants, C. Detrain and J.-L. Deneubourg Individual and Social Foraging in Social Wasps, R.L. Jeanne and B.J. Taylor Season-Dependent Foraging Patterns: Case Study of a Neotropical Forest-Dwelling Ant (Pachycondyla striata Ponerinae), F.N.S. Medeiros and P.S. Oliveira Foraging Range and the Spatial Distribution of Worker Bumble Bees, D. Goulson and J.L. Osborne How to Tell Your Mates: Costs and Benefits of Different Recruitment Mechanisms, M. Beekman and A. Dussutour Social Information Use in Foraging Insects, E. Leadbeater and L. Chittka Local Enhancement, Local Inhibition, Eavesdropping, and the Parasitism of Social Insect Communication, W.O.H. Hughes and E.J. Slaa The Role of Scents in Honey Bee Foraging and Recruitment, J. Reinhard and M.V. Srinivasan Trophallaxis: A Mechanism of Information Transfer, W.M. Farina and C. Gruter Mobilizing the Foraging Force: Mechanical Signals in Stingless Bee Recruitment, M. Hrncir Chemical Communication During Food Exploitation in Stingless Bees, S. Jarau The Use of Scent Marks by Foraging Bumble Bees, D. Goulson Information Transfer and the Organization of Foraging in Grass- and Leaf-Cutting Ants, F. Roces and M. Bollazzi An Evolutionary Simulation of the Origin of Pheromone Communication, Y. Nakamichi and T. Arita Mathematical and Neural Network Models of Medium-Range Navigation During Social Insect Foraging, A. Cheung Social Insects and the Exploitation of Food Sources: Concluding Thoughts, S. Jarau and M. Hrncir IndexScents play a crucial role in a honey bee’s life. Both in the darkness of the hive and in the outside environment bees encounter an overwhelming array of different scents, from which they retrieve information. The scents they come across are either produced by other bees (pheromones) or originate from the bees’ environment, such as the food processed inside the hive and the owering plants that bees use as food sources. The role of honey bee pheromones during social activities such as mating, reproduction, brood care, kin recognition, swarming, alarm, and defense has been researched and reviewed extensively (Free 1987). Here, we will focus on the role of pheromones as well as oral scents in honey bee foraging and recruitment. The rst section of this chapter introduces the honey bee’s sense of smell: it explains how odors are detected, goes on to describe the bee’s olfactory anatomy, how olfactory information is processed, and how bees learn and discriminate scents. The next section introduces scents that typically occur in the honey bee foraging environment and gives some background with respect to the scents’ origin and chemistry. In this section, we also briey discuss how honey bees might perceive and interpret the complex scents they encounter. The main section of this book chapter describes the ways that honey bees make use of scents during foraging and recruitment, and discusses the kind of information bees can obtain and transfer via scents.

Spitting out information: Trigona bees deposit saliva to signal resource locations

Stingless bees of the species Trigona spinipes (Fabricius 1793) use their saliva to lay scent trails communicating the location of profitable food sources. Extracts of the cephalic labial glands of the salivary system (not the mandibular glands, however) contain a large amount (approx. 74%) of octyl octanoate. This ester is also found on the scent-marked substrates at the feeding site. We demonstrate octyl octanoate to be a single compound pheromone which induces full trail following behaviour. The identification of the trail pheromone in this widely distributed bee makes it an ideal organism for studying the mechanism of trail following in a day flying insect.

Effectiveness of recruitment behavior in stingless bees (Apidae, Meliponini)

SummaryWe examined the ability of stingless bees to recruit nest mates to a food source (i) in group foraging species laying pheromone trails from the food to the nest (Trigona recursaSmith, T. hypogeaSilvestri, Scaptotrigona depilisMoure), (ii) in solitary foraging species with possible but still doubtful communication of food location inside the nest (Melipona seminigraFriese, M. favosa orbignyiGuérin), and (iii) in species with a less precise (Nannotrigona testaceicornisLep., Tetragona clavipesFab.) or no communication (Frieseomelitta variaLep.). The bees were allowed to collect food (sugar solution or liver in the necrophageous species) ad libitum and the forager number to accumulate, as it would do under normal unrestrained conditions. The median number of bees collecting differed considerably among the species (1.0–1436.5). It was highest in the species employing scent trails. The time course of recruitment was characteristic for most of the species and largely independent of the number of foragers involved. The two Melipona species recruited other bees significantly faster than T. recursa, S. depilis, and N. testaceicornis during the first 10 to 30 minutes of an experiment. In species laying a scent trail to guide nestmates to a food source the first recruits appeared with a delay of several minutes followed by a quick increase in forager number. The median time required to recruit all foragers available differed among the species between 95.0 and 240.0 min. These differences can at least partly be explained by differences in the recruitment mechanisms and do not simply follow from differences in colony biomass.

Hexyl Decanoate, the First Trail Pheromone Compound Identified in a Stingless Bee, Trigona recursa

Foragers of many species of stingless bees guide their nestmates to food sources by means of scent trails deposited on solid substrates between the food and the nest. The corresponding trail pheromones are generally believed to be produced in the mandibular glands, although definitive experimental proof has never been provided. We tested the trail following behavior of recruits of Trigona recursa in field experiments with artificial scent trails branching off from natural scent trails of this stingless bee. First-time recruits (newcomers) did not follow these trails when they were laid with pure solvent or mandibular gland extract. However, they did follow trails made with labial gland extract. Chemical analyses of labial gland secretions revealed that hexyl decanoate was the dominant component (72.4 ± 1.9% of all volatiles). Newcomers were significantly attracted to artificial trails made with synthetic hexyl decanoate, demonstrating its key function in eliciting scent-following behavior. According to our experiments with T. recursa, the trail pheromone is produced in the labial glands and not in the mandibular glands. Hexyl decanoate is the first component of a trail pheromone identified and proved to be behaviorally active in stingless bees.

A STINGLESS BEE (Melipona seminigra) MARKS FOOD SOURCES WITH A PHEROMONE FROM ITS CLAW RETRACTOR TENDONS

By depositing scent marks on flowers, bees reduce both the search time and the time spent with the handling of nonrewarding flowers. They thereby improve the efficiency of foraging. Whereas in honey bees the source of these scent marks is unknown, it is assumed to be the tarsal glands in bumble bees. According to histological studies, however, the tarsal glands lack any openings to the outside. Foragers of the stingless bee Melipona seminigra have previously been shown to deposit an attractant pheromone at sugar solution feeders, which is secreted at the tips of their tarsi. Here we show that the claw retractor tendons have specialized glandular epithelia within the femur and tibia of all legs that produce this pheromone. The secretion accumulates within the hollow tendon, which also serves as the duct to the outside, and is released from an opening at the base of the unguitractor plate. In choice experiments, M. seminigra was attracted by feeders baited with pentane extracts of the claw retractor tendons in the same way as it was attracted by feeders previously scent marked by foragers. Our results resolve the seeming contradiction between the importance of foot print secretions and the lack of openings of the tarsal glands.

Thorax vibrations of a stingless bee (Melipona seminigra). II. Dependence on sugar concentration

Using a laser vibrometer we studied the influence of the food’s sugar concentration on different parameters of the thorax vibrations produced by foragers of Melipona seminigra during trophallaxis in the nest. The concentrations tested (20–70% sugar w/w) were within the biologically relevant range. They substantially influenced different parameters of the thorax vibrations. An increase of energy gains at the food source due to an increased sugar concentration was followed by an increase of both the pulse duration and the duty cycle and by a decrease of the pause duration between two subsequent pulses. These findings further support the hypothesis that the temporal pattern of the thorax vibrations reflects the energy budget of a foraging trip rather than food source distance. Likewise, the steep increase of pulse duration variability with sugar concentration is hard to reconcile with the assumption that pulse duration conveys reliable information about food source distance when bees collect at high-quality food sources.

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.

Morphology and structure of the tarsal glands of the stingless bee Melipona seminigra

Footprint secretions deposited at the nest entrance or on food sources are used for chemical communication by honey bees, bumble bees, and stingless bees. The question of the glandular origin of the substances involved, however, has not been unequivocally answered yet. We investigated the morphology and structure of tarsal glands within the fifth tarsomeres of the legs of workers of Melipona seminigra in order to clarify their possible role in the secretion of footprints. The tarsal gland is a sac-like fold forming a reservoir. Its glandular tissue is composed of a unicellular layer of specialized epidermal cells, which cover the thin cuticular intima forming the reservoir. We found that the tarsal glands lack any openings to the outside and therefore conclude that they are not involved in the secretion of footprint substances. The secretion produced accumulates within the gland’s reservoir and reaches as far as into the arolium. Thus it is likely that it serves to fill and unfold the arolium during walking to increase adhesion on smooth surfaces, as is known for honey bees and weaver ants.

Thorax vibrations of a stingless bee (Melipona seminigra). I. No influence of visual flow

An important question in stingless bee communication is whether the thorax vibrations produced by foragers of the genus Melipona upon their return to the nest contain spatial information about food sources or not. As previously shown M. seminigra is able to use visual flow to estimate flight distances. The present study investigated whether foraging bees encode the visually measured distance in their thorax vibrations. Bees were trained to collect food in flight tunnels lined with a black-and-white pattern on their side walls and floor, which substantially influenced the image motion they experienced. When the bees had collected inside the tunnels the temporal pattern of their vibrations differed significantly from the pattern after collecting in a natural environment. These changes, however, were not associated with the visual flow experienced inside the tunnel. Bees collecting in tunnels offering little visual flow (stripes parallel to flight direction) modified their vibrations similarly to bees collecting in tunnels with high image motion (cross stripes). A higher energy expenditure due to drastically reduced flight velocities inside the tunnel is suggested to be responsible for changes in the thorax vibrations. The bees’ vibrations would thus reflect the overall energetic budget of a foraging trip.