Felipe A. L. Contrera

Olfactory eavesdropping by a competitively foraging stingless bee, Trigona spinipes.

Signals that are perceived over long distances or leave extended spatial traces are subject to eavesdropping. Eavesdropping has therefore acted as a selective pressure in the evolution of diverse animal communication systems, perhaps even in the evolution of functionally referential communication. Early work suggested that some species of stingless bees (Hymenoptera, Apidae, Meliponini) may use interceptive olfactory eavesdropping to discover food sources being exploited by competitors, but it is not clear if any stingless bee can be attracted to the odour marks deposited by an interspecific competitor. We show that foragers of the aggressive meliponine bee, Trigona spinipes, can detect and orient towards odour marks deposited by a competitor, Melipona rufiventris, and then rapidly take over the food source, driving away or killing their competitors. When searching for food sources at new locations that they are not already exploiting, T. spinipes foragers strongly prefer M. rufiventris odour marks to odour marks deposited by their own nest–mates, whereas they prefer nest–mate odour marks over M. rufiventris odour marks at a location already occupied by T. spinipes nest–mates. Melipona rufiventris foragers flee from T. spinipes odour marks. This olfactory eavesdropping may have played a role in the evolution of potentially cryptic communication mechanisms such as shortened odour trails, point–source only odour marking and functionally referential communication concealed at the nest.

Clustered male production by workers in the stingless bee Melipona subnitida Ducke (Apidae, Meliponinae)

Summary: In stingless bees brood cells are sequentially filled with liquid larval food (mass-provisioning), upon which the queen lays an egg. Thereafter the cell is closed by a worker. This study showed that during these processes workers of Melipona subnitida regularly laid eggs that served as food for the queen. Occasionally cells were oviposited in and immediately closed by a worker. These cells always rendered males. Some of these reproductive workers were seen to lay a trophic egg as well. Cells which were exclusively oviposited in by the physogastric queen gave rise to workers and queens only. In one colony it could be verified that three workers alone, which differed in age by one day, laid 15 male-producing eggs within a period of two successive weeks. Among them the number of ovipositions was positively related to the order in which workers eclosed - the oldest worker laying most eggs - and inversely related to the number of times they closed cells oviposited in exclusively by the queen. Apparently the physogastric queen was not able to stop certain workers from reproducing. We therefore conclude that some workers in M. subnitida temporarily dominated their queens in egg-laying.

Pulsed mass recruitment by a stingless bee, Trigona hyalinata

Research on bee communication has focused on the ability of the highly social bees, stingless bees (Hymenoptera, Apidae, Meliponini) and honeybees (Apidae, Apini), to communicate food location to nest–mates. Honeybees can communicate food location through the famous waggle dance. Stingless bees are closely related to honeybees and communicate food location through a variety of different mechanisms, many of which are poorly understood. We show that a stingless bee, Trigona hyalinata, uses a pulsed mass–recruitment system that is highly focused in time and space. Foragers produced an ephemeral, polarized, odour trail consisting of mandibular gland secretions. Surprisingly, the odour trail extended only a short distance away from the food source, instead of providing a complete trail between the nest and the food source (as has been described for other stingless bees). This abbreviated trail may represent an intermediate strategy between full–trail marking, found in some stingless bees, and odour marking of the food alone, found in stingless bees and honeybees.

Long distance foraging and recruitment by a stingless bee, Melipona mandacaia

Body size is hypothesized to play a major role in animal foraging, particularly in pollinators. In general, species with larger bodies forage over greater distances. Studies have found support for this body size-foraging range hypothesis across a wide variety of pollinator species, but have not investigated the possibility that this effect also applies within a pollinator species. We trained foragers of the stingless bee Melipona mandacaia to feeders in their native habitat under natural conditions, and found that larger foragers forage at and recruit to significantly greater distances than smaller foragers. The maximum foraging and recruitment distances are significantly greater (by 24% and 48% respectively) for larger as compared to smaller foragers. We also provide the first direct evidence that stingless bees can forage in their native habitat at distances up to 2.1 km and recruit over 1 km from their nest, recruiting more than 230% farther than previously reported for any stingless bee feeder experiments. Natural size variation among colonies within the same species may play a role in foraging range, and could thus influence plant gene flow and population structure.ZusammenfassungBei vielen Tierarten geht man davon aus, dass die individuelle Körpergrösse eine wichtige Rolle spielt in der Frage, in welcher Entfernung Futterquellen noch ausgebeutet werden. Bei Bienen fliegen grössere Arten in der Regel weiter enfernte Futterquellen an als kleinere Arten. Die Körpergrösse sollte damit von Bedeutung sein sowohl für die Definition der ökologischen Nische von Bienenarten, sowie auch für den Genfluss bei Pflanzen, die von ihnen bestäubt werden. Der Frage, ob die intraspezifische Variation in der Körpergrösse einen Einfluss auf den Sammelradius von Koloniemitgliedern bei sozialen Arten hat, wurde jedoch noch nicht nachgegangen. Wir untersuchten dies an einer Stachellosen Bienen, Melipona mandacaia, die in Brasilien in trockenen Caatinga-Habitaten vorkommt, wo Nahrungsquellen jahreszeitlich stark beschränkt sein können. Angesichts dieser Beschränkung an Futterquellen gingen wir davon aus, dass diese Bienen weit entfernte Futterquellen anfliegen und zu diesen auch rekrutieren könnten. Diese Untersuchungen führten wir an drei Völkern während der Trockensaison in Bahia durch. Wir bestimmten die maximalen Sammeldistanzen und die Rekturierdistanzen für Bienen, die auf den Besuch einer künstlichen Futterquellen mit 60 % v/v Sacharose trainiert worden waren. Dabei markierten wir individuell alle an der Futterquelle ankommenden Bienen, um bestimmen zu können zu welchem Volk sie zurückkehrten und wo sie dort rekrutiert worden waren. Am Ende der Versuche sammelten wir Sammlerinnen von den Völkern ab und bestimmten ihre Körpergrösse (Kopfbreite, Distanz zwischen den Augen und Thoraxbreite); Unsere Ergebnisse sind ein erster Hinweis darauf, dass Stachellose Bienen in ihrem natürlichen Habitat bis zu 2,1 km weit entfernte Futterquellen anfliegen und bis zu 1 km vom Nest entfernt auch rekrutieren können. Diese Werte liegen um 230 % über den Werten, die bisher mittels künstlicher Futterquellen für Stachellose Bienen ermittelt worden waren. Des weiteren konnten wir eine beachtliche und signifikante Variation in der Körpergrösse der Sammlerinnen feststellen. Die Sammel- und die Rekrutierdistanzen für grosse Arbeiterinnen waren signifikant um 24 %, bzw. 48 % weiter als die kleiner Arbeiterinnen.Diese Ergebnisse weisen darauf hin, dass innerartliche Unterschiede in der Körpergrösse auch bei einer sozialen Bienenart den Sammelradius beeinflussen können. Völker mit grösseren Arbeiterinnen sammelten und rekrutierten über signifikant weitere Entfernungen als Völker mit kleineren Sammlerinnen. Die maximale Sammeldistanz grosser Arbeiterinnen lag bei 2100 m, während die kleiner Sammlerinnen 1700 m betrug. Das gleiche galt für die Rekrutierdistanzen, mit Werten von 1220 m für grosse und 820 m für kleine Sammlerinnen. Die natürliche Variation der Körpergrösse zwischen Völkern der gleichen Art könnte damit das Sammelverhalten und in diesem Zusammenhang auch den Genfluss und die Poplationsstruktur von Pflanzenarten beeinflussen. Ähnliche intrakoloniale Unterschiede in der Körpergrösse sind bereits für andere soziale Insekten bekannt, insbesondere für Ameisen und Hummeln. Für Stachellose Bienen verstehen wir jedoch noch nicht im vollen Umfang die Bedeutung dieser Grössenunterschiede.

How queen and workers share in male production in the stingless bee Melipona subnitida Ducke (Apidae, Meliponini)

Summary.Potential conflict between the queen and workers over the production of males is expected in stingless bees as a result of the higher relatedness of workers with their sons than with their brothers. This conflict was studied in Melipona subnitida by observing how the queen and the workers share in male production. The oviposition of individual cells was observed in two colonies with individually marked workers for a period of 51 and 40 days respectively. The gender that developed from these cells was then determined. The results revealed that most male production was concentrated in a 2–3-week period, during which laying workers were present. During these weeks, the queens produced twice as many males as all laying workers together. Outside this distinct period, the queens produced an occasional male. A reproductive worker either oviposited before the queen did, in which case she immediately proceeded to close the cell and thus prevented the queen from oviposition, or oviposited and sealed the cell after the queen had laid an egg. When cell construction and oviposition occured on several combs simultaneously, the workers preferentially laid male eggs on the newest combs. We discuss the proximate mechanism and ultimate cause of the way in which queen-worker male production occurred. In conclusion, we argue that overt behavioural conflict, occasionally displayed by reproductive workers of this species, can be of great cost to the colony.

Effect of group size on the aggression strategy of an extirpating stingless bee‚ Trigona spinipes

Summary.Group aggression influences communication and defense strategies in many social insect communities. Such aggression plays a particularly significant role in the lives of stingless bees, important native Neotropical pollinators, in which the battle for food resources can be deadly and critical to colony survival. However, the effects of group size on individual aggression levels and the spatio-temporal aggression strategy of communal aggressors have not been fully explored. We therefore investigated how group size affects the aggression levels and the spatio-temporal attack strategy (which body parts, and the amount of time spent in attacking each part) in close combats between Trigona spinipes foragers and a natural competitor, Melipona rufiventris. In all trials, T. spinipes foragers competitively excluded M. rufiventris foragers from nearby feeders, exhibiting four levels of aggressive behavior ranging from threat displays to prolonged grappling and decapitation. Surprisingly, aggression levels and spatial strategy corresponded to the size of group attacks. Larger groups of attackers used individually lower aggression levels than small groups of attackers. Smaller groups also attacked appendages linked to escape (legs and wings) with greater frequency than larger groups, which focused on vital central body areas (abdomen, thorax, and head). Increased aggression corresponded to increased risks for attackers and the attacked. All combatants engaging at the highest level of aggression died (100% mortality). Thus the dominance style of T. spinipes may minimize attack risk and maximize victim harm with finely tuned hostility.

Variation in the ability to communicate three-dimensional resource location by stingless bees from different habitats

We evaluated the ability of two Brazilian stingless bee species, Melipona mandacaia and M. bicolor ,t o recruit nestmates to a specific three-dimensional location. We used experimental feeder arrays and provide the first detailed evidence demonstrating that recruitment communication in Melipona can lead to large, rapid and highly significant increases in the number of nestmates visiting a specific location. Melipona bicolor and M. mandacaia foragers both recruited nestmates to the correct distance and direction, but differed in their ability to recruit nestmates to the correct height. These differences may relate to their respective habitats. Melipona mandacaia inhabits semi-arid areas of Caatinga where most food sources occur close to the ground, and its foragers evidently cannot recruit nestmates to the correct height. Melipona bicolor, an Atlantic rainforest species, evidently does not communicate height when the food source is at ground level, but can communicate height when the food source is at the forest canopy level (12 m high), where major food sources occur. Species-specific variation in three-dimensional location communication is intriguing because it suggests that Melipona may be a good model for studying the evolution of recruitment communication systems in highly social bees.  2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.

Effect of forager-deposited odors on the intra-patch accuracy of recruitment of the stingless bees Melipona panamica and Partamona peckolti (Apidae, Meliponini)

We show that the stingless bees Melipona panamica and Partamona peckolti have a high precision of intra-patch recruitment that is influenced by forager-deposited odor marks in the field. We trained foragers to a 2.5 M sucrose feeder in the center of an array of five identical feeders (20 cm between feeders) at different distances and directions from the nest and measured the distribution of recruit visitations. In the free-foraging phase foragers could odor mark a filter paper around the experimental feeder, and in the odor-removal phase we substituted it each five minutes by a clean one. Significantly more recruits in both species chose the experimental feeder over the controls in the distance and directional arrays (P ⩽ 0.034) and odor removal significantly decreased precision of recruitment in both species (P ⩽ 0.034). Scent marks in both species thus play a significant role in orienting recruits to already known profitable food sources.ZusammenfassungWir zeigen, dass die neotropischen Stachellosen Bienen Melipona panamica und Partamona peckolti eine hohe räumliche Genauigkeit bei der Sammlerinnenrekrutierung innerhalb von Blütenansammlungen aufweisen, und dass diese stark von durch die Sammlerinnen abgegebenen Duftmarkierungen beeinflusst wird. Wir trainierten Sammlerinnen auf einen mit 2,5 M Zuckerlösung versehenen Fütterer in der Mitte einer fächerförmigen Reihung von 5 identischen Fütterern (20 cm Abstand zwischen den Fütterern) in unterschiedlichen Abständen und Richtungen vom Nest und ermittelten die Verteilung von Besuchen durch Neuankömmlinge (Bienen, die nie zuvor einen der Fütterer besucht hatten). Trainierte Sammlerinnen wurden nur zu der mittleren Futterstelle zugelassen. Die Richtungs- und Entfernungsgenauigkeit innerhalb der Ansammlungen wurde durch verschiedene Reihen von Fütterern untersucht. Jedes Experiment wurde in zwei Phasen unterteilt: freies Sammeln, wobei die Sammlerinnen ein Filterpapier um den Fütterer herum mit Duft markieren konnten, und Duft entfernen, wobei wir das Filterpapier alle 5 Minuten entfernten und durch ein neues, sauberes Papier ersetzten. Insgesamt bevorzugten sowohl bei den Versuchen zur Entfernungsgenauigkeit als auch zur Richtungsgenauigkeit bei beiden Arten signifikant mehr Rekruten die experimentellen Fütterer gegenüber Kontrollfütterern. (72 % bis 87 % an den experimentellen Fütterern, P ⩽ 0,034, Abb. 1a, c, 2a, c, 3a und 3c). Die Entfernung der von den Sammlerinnen abgegebenen Duftmarken verminderte die Genauigkeit der Rekrutierung bei M. panamica signifikant (−23 % bzw. −25 % weniger Neuankömmlinge bei dem Experiment mit einer Richtungsreihung, −46 % bzw. −18 % bei einer Entfernungsreihung; bei 25 m: Abb. 2b, d, und bei 75 m: Abb, 3b, d, P ⩽ 0,024) und bei P. peckolti (−41 % bei der Richtungsreihung, keine Änderung bei der Entfernungsreihung; bei 45 m, P ⩽ 0,034, Abb. 1b, d). Diese Ergebnisse zeigen zum ersten Mal, dass Sammlerinnen von P. peckolti Duftmarken abgeben, die auf Nestgenossen anziehend wirken. Bei beiden Arten scheinen Duftmarken daher wichtig zu sein, um die Rekruten auf den Besuch von bereits bekannten profitablen Futterstellen hin zu orientieren und eine rasche Ausnutzung dieser Futterstellen zu ermöglichen.

Trophallaxis and reproductive conflicts in social bees

In the eusocial Hymenoptera, reproductive division of labour is a key aspect of colony organisation. In most of its species, workers are sterile and are unable to reproduce, while the queen monopolises reproduction. When workers are able to reproduce, a conflict with the queen or with other workers over male production is predicted. Because this reproduction may involve costs for the colony, the potential conflict over male parentage gives rise to important questions, such as what are the proximate mechanisms that allow a queen to control the reproductive potential of its workers, and which factors make some workers fertile and others not. In the groups where it occurs, an important mechanism for the regulation of reproduction is trophallaxis (the process of mutual feeding through regurgitation that occurs in several species of social insects). Trophallaxis gives dominant individuals a trophic advantage by taking nutrients from submissive individuals. In advanced eusocial species of bees, trophallaxis may also serve as an alternative hierarchical interaction in the absence of agonistic conflicts. In this way, trophallaxis not only represents an alternative path for hierarchical interactions, but it may be evolutionary linked to intracolonial conflict among workers.

The effect of ambient temperature on forager sound production and thoracic temperature in the stingless bee, Melipona panamica

Foragers of the stingless bees genus Melipona may produce intranidal sounds that are correlated with food location and quality. In this study, we provide the first detailed analysis of pulsed sounds produced by Melipona panamica foragers while feeding on a carbohydrate food source. We trained foragers to a 2.5-M sucrose feeder under normal, ambient temperature (23–33°C) and lower temperature (11–25°C) conditions. We recorded forager sounds under both conditions and tested the effect of temperature of the thorax, feeder plate, and air on sound temporal characteristics. Forager energetic expenditure and the number of pulses per visit were significantly higher in the cold condition than in the normal condition. Foragers spent a longer time at the feeder under the cold condition than during the normal condition. Interpulse durations were significantly shorter in the cold condition than in the normal condition and became progressively and significantly shorter at the end of each performance. Thus, pulse production increased before departure. Foragers increased their thoracic temperatures above ambient at all experimental air temperatures. Under chilled conditions, foragers had a significantly greater difference between thorax temperature and ambient air temperature than under normal conditions. Foragers must achieve a minimum flight muscle temperature before take-off, and thus forager sounds may be linked to muscle warm-up.