Mixed colonies of two species of congeneric stingless bees (Hymenoptera: Apinae,Meliponini) display environmentally‐acquired and endogenously‐produced recognition signals

Nestmate recognition is fundamental for the maintenance of social organization in insect nests. It is becoming well recognized that cuticle hydrocarbons mediate the recognition process, although the origin of recognition cues in stingless bees remains poorly explored. The present study investigates the effects of endogenously‐produced and environmentally‐acquired components in cuticular hydrocarbons in stingless bees. The tests are conducted using colonies of Plebeia droryana Friese and Plebeia remota Holmberg. Recognition tests are performed with four different groups: conspecific nestmates, conspecific non‐nestmates, heterospecifics and conspecific, genetically‐related individuals that emerge in a heterospecific nest. This last group is produced by introducing brood cells of P. droryana into a P. remota colony, and the resulting adult bees are tested for acceptance 10 days after emergence. For all groups, 15 individuals are sampled for chemical analysis. The results show the acceptance of all conspecific nestmates, and the rejection of almost every conspecific non‐nestmate and every heterospecific bee. Genetically‐related individuals emerging from heterospecific nests present intermediate rejection (66.7% rejection). Chemical analysis shows that P. droryana individuals emerging in a P. remota nest have small amounts of alkene and diene isomers found in P. remota cuticle that are not found in workers from the natal nest. The data clearly show that the majority of the compounds present in P. droryana cuticle are endogenously produced, although a few unsaturated compounds are acquired from the environment, increasing the chemical differences and, consequently, the rejection percentages.     

Behavioral suites mediate group-level foraging dynamics in communities of tropical stingless bees

Competition for floral resources is a key force shaping pollinator communities, particularly among social bees. The ability of social bees to recruit nestmates for group foraging is hypothesized to be a major factor in their ability to dominate rich resources such as mass-flowering trees. We tested the role of group foraging in attaining dominance by stingless bees, eusocial tropical pollinators that exhibit high diversity in foraging strategies. We provide the first experimental evidence that meliponine group foraging strategies, large colony sizes and aggressive behavior form a suite of traits that enable colonies to improve dominance of rich resources. Using a diverse assemblage of Brazilian stingless bee species and an array of artificial “flowers” that provided a sucrose reward, we compared species’ dominance and visitation under unrestricted foraging conditions and with experimental removal of group-foraging species. Dominance does not vary with individual body size, but rather with foraging group size. Species that recruit larger numbers of nestmates (Scaptotrigona aff. depilis, Trigona hyalinata, Trigona spinipes) dominated both numerically (high local abundance) and behaviorally (controlling feeders). Removal of group-foraging species increased feeding opportunities for solitary foragers (Frieseomelitta varia, Melipona quadrifasciata and Nannotrigona testaceicornis). Trigona hyalinata always dominated under unrestricted conditions. When this species was removed, T. spinipes or S. aff. depilis controlled feeders and limited visitation by solitary-foraging species. Because bee foraging patterns determine plant pollination success, understanding the forces that shape these patterns is crucial to ensuring pollination of both crops and natural areas in the face of current pollinator declines.     

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. We dedicate this review to Martin Lindauer and Warwick Kerr who pioneered research on the communication and recruitment in stingless bees by studies reported in a seminal paper published in this Journal half a century ago in 1958.     

Visual and chemical cues provide redundant information in the multimodal recruitment system of the stingless bee <Emphasis Type="Italic">Scaptotrigona mexicana</Emphasis> (Apidae,Meliponini)

Multimodal communication plays an important role in pollination biology. Bees have evolved multimodal communication to recruit nestmates to rewarding food sources. Highly social bees can use visual and chemical information to recruit nestmates to rich food sources. However, no studies have determined if this information is redundant or has an additive effect such that multimodal information is more attractive than either modality presented by itself to free-flying bees. We tested the effect of two modalities, forager-deposited odor marks and the visual presence of foragers, on the orientation of stingless bee (Scaptotrigona mexicana) recruits. Our results show that odor marks alone were significantly more attractive than multimodal information, and that multimodal information was significantly more attractive than visual forager presence alone. Given the high olfactory sensitivity and limited visual acuity of insects, odor marks likely attracted recruits over a greater distance than the visual presence of nestmates. Thus, multimodal information in S. mexicana is redundant, not additive, in terms of orientation to food sources.     

Olfactory learning in the stingless bee Tetragonisca angustula (Hymenoptera, Apidae, Meliponini)

Tetragonisca angustula stingless bees are considered as solitary foragers that lack specific communication strategies. In their orientation towards a food source, these social bees use chemical cues left by co-specifics and the information obtained in previous foraging trips by the association of visual stimuli with the food reward. Here, we investigated their ability to learn the association between odors and reward (sugar solution) and the effect on learning of previous encounters with scented food either inside the hive or during foraging. During food choice experiments, when the odor associated with the food was encountered at the feeding site, the bees’ choice is biased to the same odor afterwards. The same was not the case when scented food was placed inside the nest. We also performed a differential olfactory conditioning of proboscis extension response with this species for the first time. Inexperienced bees did not show significant discrimination levels. However, when they had had already interacted with scented food inside the hive, they were able to learn the association with a specific odor. Possible olfactory information circulation inside the hive and its use in their foraging strategies is discussed.     

Pheromone paths attached to the substrate in meliponine bees: helpful but not obligatory for recruitment success

In contrast to marking of the location of resources or sexual partners using single-spot pheromone sources, pheromone paths attached to the substrate and assisting orientation are rarely found among flying organisms. However, they do exist in meliponine bees (Apidae, Apinae, Meliponini), commonly known as stingless bees, which represent a group of important pollinators in tropical forests. Worker bees of several Neotropical meliponine species, especially in the genus Scaptotrigona Moure 1942, deposit pheromone paths on substrates between highly profitable resources and their nest. In contrast to past results and claims, we find that these pheromone paths are not an indispensable condition for successful recruitment but rather a means to increase the success of recruiters in persuading their nestmates to forage food at a particular location. Our results are relevant to a speciation theory in scent path-laying meliponine bees, such as Scaptotrigona. In addition, the finding that pheromone path-laying bees are able to recruit to food locations even across barriers such as large bodies of water affects tropical pollination ecology and theories on the evolution of resource communication in insect societies with a flying worker caste.     

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 andM. bicolor , to 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 andM. 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.     

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

Summary We 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 recursa Smith, T. hypogea Silvestri, Scaptotrigona depilis Moure), (ii) in solitary foraging species with possible but still doubtful communication of food location inside the nest (Melipona seminigra Friese, M. favosa orbignyi Guérin), and (iii) in species with a less precise (Nannotrigona testaceicornis Lep., Tetragona clavipes Fab.) or no communication (Frieseomelitta varia Lep.). 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.     

An exploration of the relationship between recruitment communication and foraging in stingless bees

Social information is widely used in the animal kingdom and can be highly adaptive. In social insects, foragers can use social information to find food, avoid danger, or choose a new nest site. Copying others allows individuals to obtain information without having to sample the environment. When foragers communicate information they will often only advertise high-quality food sources, thereby filtering out less adaptive information. Stingless bees, a large pantropical group of highly eusocial bees, face intense inter- and intra-specific competition for limited resources, yet display disparate foraging strategies. Within the same environment there are species that communicate the location of food resources to nest-mates and species that do not. Our current understanding of why some species communicate foraging sites while others do not is limited. Studying freely foraging colonies of several co-existing stingless bee species in Brazil, we investigated if recruitment to specific food locations is linked to 1) the sugar content of forage, 2) the duration of foraging trips, and 3) the variation in activity of a colony from 1 day to another and the variation in activity in a species over a day. We found that, contrary to our expectations, species with recruitment communication did not return with higher quality forage than species that do not recruit nestmates. Furthermore, foragers from recruiting species did not have shorter foraging trip durations than those from weakly recruiting species. Given the intense inter- and intraspecific competition for resources in these environments, it may be that recruiting species favor food resources that can be monopolized by the colony rather than food sources that offer high-quality rewards.     

Bumble bee olfactory information flow and contact-based foraging activation

Nestmate foraging activation and interspecific variation in foraging activation is poorly understood in bumble bees, as compared to honey bees and stingless bees. We therefore investigated olfactory information flow and foraging activation in the New World bumble bee species, Bombus impatiens. We (1) tested the ability of foragers to associate forager-deposited odor marks with rewarding food, (2) determined whether potential foragers will seek out the food odor brought back by a successful forager, and (3) examined the role of intranidal tactile contacts in foraging activation. Bees learned to associate forager-deposited odor marks with rewarding food. They were significantly more attracted to an empty previously rewarding feeder presented at a random position within an array of eight previously non-rewarding feeders. However, foragers did not exhibit overall odor specificity for short-term, daily floral shifts. For two out of three tested scents, activated foragers did not significantly prefer the feeder providing the same scent as that brought back by a successful forager. Finally, bees contacted by the successful forager inside the nest were significantly more likely to leave the nest to forage (38.6% increase in attempts to feed from empty feeders) than were non-contacted bees. This is the first demonstration that tactile contact, a hypothesized evolutionary basal communication mechanism in the social corbiculate bees, is involved in bumble bee foraging activation. Received 4 September 2007; revised 30 May 2008; accepted 15 July 2008.     

Allocation of Colony‐Level Foraging Effort in Vespula germanica in Response to Food Resource Quantity,Quality, and Associated Olfactory Cues

In social insects, selection takes place primarily at the level of the colony. Therefore, unlike solitary insects, social species are expected to forage at rates that maximize colony fitness rather than individual fitness. Workers can increase the net benefit of foraging by responding to increased resource availability, by responding more strongly to higher‐quality resources, and by decreasing the uncertainty with which nestmates find resources. Unlike many ants and social bees, no social wasp is known to utilize a nest‐based recruitment signal to inform nestmates of food location. On the other hand, wasps do learn the odor of food brought to the nest and use this cue to locate the food source outside the nest. Here, we quantify the effects of three food‐associated variables on the allocation of foraging effort in the yellowjacket Vespula germanica. We used an experimental approach to assess whether resource quantity, quality, or associated olfactory information affect the probability that a forager will leave the nest on a foraging trip. We addressed these questions by inserting a known amount of sucrose solution directly into nests and recording foraging effort (departure rate) over the subsequent hour‐long observation period. No differences were found in foraging effort because of the presence/absence of olfactory cues, but there was strong evidence that foraging effort increased in response to resource influx and resource quality. Thus, while olfactory cues are learned in the nest, only resource quality and the cue of increased amount of food in the nest factor into a forager's decision of whether or not to depart on a foraging trip. However, as prior work has shown, once a wasp forager leaves the nest, it uses the learned olfactory cues to aid in finding resources.     

Monitoring Flower Visitation Networks and Interactions between Pairs of Bumble Bees in a Large Outdoor Flight Cage

Pollinators, such as bees, often develop multi-location routes (traplines) to exploit subsets of flower patches within larger plant populations. How individuals establish such foraging areas in the presence of other foragers is poorly explored. Here we investigated the foraging patterns of pairs of bumble bees (Bombus terrestris) released sequentially into an 880m² outdoor flight cage containing 10 feeding stations (artificial flowers). Using motion-sensitive video cameras mounted on flowers, we mapped the flower visitation networks of both foragers, quantified their interactions and compared their foraging success over an entire day. Overall, bees that were released first (residents) travelled 37% faster and collected 77% more nectar, thereby reaching a net energy intake rate 64% higher than bees released second (newcomers). However, this prior-experience advantage decreased as newcomers became familiar with the spatial configuration of the flower array. When both bees visited the same flower simultaneously, the most frequent outcome was for the resident to evict the newcomer. On the rare occasions when newcomers evicted residents, the two bees increased their frequency of return visits to that flower. These competitive interactions led to a significant (if only partial) spatial overlap between the foraging patterns of pairs of bees. While newcomers may initially use social cues (such as olfactory footprints) to exploit flowers used by residents, either because such cues indicate higher rewards and/or safety from predation, residents may attempt to preserve their monopoly over familiar resources through exploitation and interference. We discuss how these interactions may favour spatial partitioning, thereby maximising the foraging efficiency of individuals and colonies.     

Pollination efficiency and foraging behaviour of honey bees and non‐Apis bees to sweet cherry

1. Crop pollination generally increases with pollinator diversity and wild pollinator visitation. To optimize crop pollination, it is necessary to investigate the pollination contribution of different pollinator species. In the present study, we examined this contribution of honey bees and non‐Apis bees (bumble bees, mason bees and other solitary bees) in sweet cherry.
2. We assessed the pollination efficiency (fruit set of flowers receiving only one visit) and foraging behaviour (flower visitation rate, probability of tree change, probability of row change and contact with the stigma) of honey bees and different types of non‐Apis bees.
3. Single visit pollination efficiency on sweet cherry was higher for both mason bees and solitary bees compared with bumble bees and honey bees. The different measures of foraging behaviour were variable among non‐Apis bees and honey bees. Adding to their high single visit efficiency, mason bees also visited significantly more flower per minute, and they had a high probability of tree change and a high probability to contact the stigma.
4. The results of the present study highlight the higher pollination performance of solitary bees and especially mason bees compared with bumble bees and honey bees. Management to support species with high pollination efficiency and effective foraging behaviour will promote crop pollination.

     

Influence of visual targets and landmarks on honey bee foraging and waggle dancing

Animals use diverse sensory stimuli to navigate their environment and to recognize rewarding food sources.Honey bees use visual atributes of the targeted food source,such as its color,shape,size,direction and distance from the hive,and the landmarks around it to navigate during foraging.They transmit the location information of the food source to other bees if it is highly rewarding.To investigate the relative importance of these attributes,we trained bees to feeders in two different experiments.In the first experiment,we asked whether bees prefer to land on(a)a similar feeder at a different distance on the same heading or on(b)a visually distinct feeder located at the exact same location.We found that,within a short foraging range,bees relied heavily on the color and the shape of the food source and to a lesser extent on its distance from the hive.In the second experiment,we asked if moving the main landmark or the feeder(visual target)influenced recruitment dancing for the feeder.We found that foragers took longer to land and danced fewer circuits when the location of the food source,or a major landmark associated with it,changed.These results demonstrate that prominent visual atributes of food sources and landmarks are evidently more reliable than distance information and that foraging bees heavily utilize these visual cues at the later stages of their journey.     

Complex memories in honeybees: can there be more than two?

Foraging honeybees are likely to learn visual and chemical cues associated with many different food sources. Here, we explore how many such sources can be memorized and recalled. Marked bees were trained to visit two (or three) sugar feeders, each placed at a different outdoor location and carrying a different scent. We then tested the ability of the bees to recall these locations and fly to them, when the training scents were blown into the hive, and the scents and food at the feeders were removed. When trained on two feeder locations, each associated with a different scent, the bees could correctly recall the location associated with each scent. However, this ability broke down when the number of scents and feeder locations was increased to three. Performance was partially restored when each of the three training feeders was endowed with an additional cue, namely, a distinct colour. Our results suggest that bees can recall a maximum of two locations when each is associated with a different scent. However, this number can be increased if the scent cues are augmented by visual cues. These findings have implications for the ways in which associations are established and laid down in honeybee memory.     

Wildflower plantings on fruit farms provide pollen resources and increase nesting by stem nesting bees

1. Wildflower plantings on farms have been shown to attract foraging wild bees, however, whether these added floral resources increase nesting densities of bees remains largely untested.
2. We placed nest boxes containing natural reeds at 20 fruit farms in Michigan. We then compared nesting densities between farms with and without wildflower plantings and analysed nest provisions to evaluate use of wildflower plantings for brood provisioning.
3. We found significantly greater nesting at farms with wildflower plantings, with only one out of 236 completed nests at a farm without a planting. The majority of nests were completed by Megachile pugnata, with a portion of nests completed by Osmia caerulescens.
4. We found that nesting bees collected pollen from only a subset of the available flowers in the wildflower plantings, with a strong preference for Centaurea maculosa, and Rudbeckia type pollens. While these species were found growing in the plantings, only Rudbeckia type species were seeded in the plantings.
5. This study provides evidence that wildflower plantings (though not only seeded species) are filling a critical resource gap for stem-nesting bees in agricultural landscapes and likely support local populations.

     

Contrasting foraging related behaviours in two sympatric wasps (Vespula maculifrons and V. germanica)

ABSTRACT.

• 1 Using pinned freshly killed wasps (yellowjackets) to simulate feeding animals, it was found that V. germanica was socially facilitated, and concentrated its foraging activity on those feeders with the most pinned wasps (twenty). V. maculifrons foragers responded inversely, preferentially foraging at feeders with few or no pinned wasps.
• 2 Using hand-painted drawing pins (thumb tacks) as wasp models, similar results were found, indicating that visual, rather than olfactory, cues were responsible for the observed distribution.
• 3 Vespula maculifrons and V. germanica exhibit aggression while foraging at honey-baited feeders. Both species attack conspecifics at frequencies lower than would be expected under random encounter.

     

Geometric morphometrics of the forewing shape and size discriminate Plebeia species (Hymenoptera: Apidae) nesting in different substrates

Historically, studies evaluating morphological diversity in stingless bees (Hymenoptera, Apidae: Meliponini) by geometric morphometrics have been used to successfully discriminate taxa and/or populations. Moreover, the use of geometric morphometrics to evaluate phylogenetic morphological variation among stingless bee species has received less attention. Here, we used geometric morphometrics to assess taxonomic discrimination and putative phylogenetic signals for six diapausing stingless bee species (Plebeia) occurring in southern Brazil. In all, 12 landmarks were captured from forewings of P. droryana, P. saiqui, P. emerina, P. remota, P. nigriceps and P. wittmanni. Our data show that the centroid size of the forewings reliably discriminated, for example, between P. droryana and P. emerina from P. saiqui. Moreover, this trait does not have a significant phylogenetic signal. In turn, we found that the overall accuracy in discriminating between the six Plebeia species according to forewing shape was 84%, while the confusion matrix achieved 71%. Interestingly, our discriminant analysis separated Plebeia species nesting in tree cavities from those nesting under granitic rocks. The latter group has second cubital (landmarks = 5, 6, 7), first medial (landmarks = 2, 3, 8) and first submarginal cells (landmarks = 3, 4, 9, 10) that are larger than those of species nesting in trees. The forewing shape showed a strong phylogenetic signal, therefore suggesting that its variation may be due to an evolutionary history shared between Plebeia species studied here rather than to environmental features. This work sheds light on the value of forewing size and shape attributes in discriminating Plebeia species within same genus. We suggest that landmarks separating different taxonomic groups could be incorporated into dichotomous keys to help in identifying clades of complex resolution.     

Colony foraging allocation is finely tuned to food distance and sweetness even close to a bee colony

Social bee colonies can allocate their foraging resources over a large spatial scale, but how they allocate foraging on a small scale near the colony is unclear and can have implications for understanding colony decision‐making and the pollination services provided. Using a mass‐foraging stingless bee, Scaptotrigona pectoralis (Dalla Torre) (Hymenoptera: Apidae: Meliponini), we show that colonies will forage near their nests and allocate their foraging labor on a very fine spatial scale at an array of food sources placed close to the colony. We counted the foragers that a colony allocated to each of nine feeders containing 1.0, 1.5, or 2.0 M sucrose solution [31, 43, and 55% sucrose (wt/wt), respectively] at distances of 10, 15, and 20 m from the nest. A significantly greater number of foragers (2.6–5.3 fold greater) visited feeders placed 10 vs. 20 m away from the colony. Foraging allocation also corresponded to food quality. At the 10‐m feeders, 4.9‐fold more foragers visited 2.0 M as compared to 1.0 M sucrose feeders. Colony forager allocation thus responded to both differences in food distance and quality even when the travel cost was negligible compared to normal colony foraging distances (10 m vs. an estimated 800–1 710 m). For a nearby floral patch, this could result in unequal floral visitation and pollination.     

German Yellowjacket (Vespula germanica) Foragers Use Odors Inside the Nest to Find Carbohydrate Food Sources

Prior work has shown that yellowjacket waSPS remember food odors and use them as cues when foraging. There is also evidence they have mechanisms to recruit nest mates to highly rewarding food sources, as naïve individuals are more likely to go to food sources with scents similar to those visited by nest mates. We asked whether recruitment requires behavioral stimulation by returning foragers, as in honey bees, or if sampling the food source inside the nest is sufficient. We tested this by eliminating the behavior of returning foragers by inserting a scented sugar solution directly into a Vespula germanica nest. Exiting foragers were given a choice of the test scent and a control scent. WaSPS were more likely to choose the test scent. We conclude that behavioral interactions with returning foragers are not necessary to stimulate nest mates to associate an odor with a food source and search for a resource bearing that odor, and that experience with the scented reward inside the nest is sufficient to achieve this result.