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.     

Genetic architecture of the Tetragonula carbonaria species complex of Australian stingless bees (Hymenoptera: Apidae: Meliponini)

A species complex is a group of closely related species whose ecological or morphological boundaries are sufficiently vague that delimiting one species from another is difficult. In Australia, a group of four stingless bee species – Tetragonula carbonaria Smith, Tetragonula hockingsi Cockerell, Tetragonula mellipes Friese, and Tetragonula davenporti Franck – form a species complex in which gross morphology is clinal and overlapping. The species are most readily distinguished by the morphology of their brood combs. Here we genetically characterize bees sampled in areas where the species do and do not have contact. Our data corroborate previous evidence that T. hockingsi and T. carbonaria are genetically distinct and that there are two genetically distinct groups of T. hockingsi – one in the north and the other in the south of Queensland. Curiously, northern populations of T. hockingsi, which are allopatric to T. carbonaria, are genetically closer to T. carbonaria than are southern populations of T. hockingsi, which are in sympatry with T. carbonaria. We detected three hybrid colonies that appear to have arisen because of anthropogenic movement of T. hockingsi colonies from north to south of Queensland where males mated with local T. carbonaria queens. We discuss the status of T. davenporti, a recently described species cryptically similar to T. hockingsi from south‐east Queensland. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 149–161.     

Mitochondrial genome differences between the stingless bees Melipona rufiventris and Melipona mondury (Apidae: Meliponini)

Within the Meliponini, a widely distributed group of stingless bees, Melipona rufiventris has been considered as a single, cohesive species. Recently, analysis of morphological characters led to the splitting of this species into two species, M. mondury and M. rufiventris. The former occurs in the Atlantic Rain Forest ranging from Santa Catarina to Bahia States, while the latter is found in other parts of Brazil. We used PCR + RFLP to identify genetic marker patterns of the mtDNA between these species. Nine mtDNA regions were amplified and digested with four restriction enzymes (EcoRI, EcoRV, HindIII, and HinfI). Six species-specific restriction sites were identified for M. mondury and M. rufiventris with all enzymes, except for HindIII. The molecular data agree with the morphological classification.     

Pollinators of Bertholletia excelsa (Lecythidales: Lecythidaceae): interactions with stingless bees (Apidae: Meliponini) and trophic niche

This paper presents an analysis of the foraging behavior and interactions of Xylocopa frontalis Olivier (Apidae: Xylocopini) and Eulaema mocsaryi (Friese) (Apidae: Euglossini) in the presence of stingless bees (Apidae: Meliponini) in flowers of Bertholletia excelsa, the Brazilian nut. The palynological load carried by both species was also examined. This study was conducted in the farm Aruan?, Itacoatiara/ Amazonas state, Brazil, during the flowering peak of B. excelsa. The visitation by the main pollinators X. frontalis and E. mocsaryi were influenced by the presence and activities of stingless bees in the flowers of B. excelsa. Meliponini bees did not have any effect on the visits and collection of floral resources by X. frontalis, while negatively affecting the number of visits by E. mocsaryi. The stingless bees presented a variety of strategies to get access to pollen grains of B. excelsa, grouped into two categories: opportunism -Frieseomelitta trichocerata Moure, Tetragona goettei (Friese), and Tetragona kaieteurensis (Schwarz), and stealing -Trigona branneri Cockerell, Trigona fuscipennis Friese, and Trigona guianae Cockerell. The palynological analysis from X. frontalis showed that the bee collected pollen in a few species of plants, but mainly on B. excelsa. The pollen grains of B. excelsa were poorly represented in the pollen shipments of E. mocsaryi, due to its large trophic niche in the locality.     

Nonvolatile chemicals provide a nest defence mechanism for stingless bees Tetragonula carbonaria (Apidae,Meliponini)

Social insects construct nests that protect their brood and food resources from both the physical environment and natural enemies. Stingless bees use plant‐derived resins, mixed with wax to form propolis, in the construction of their nests, and these products can be effective sources of defense against natural enemies, including ants. However, it is not known whether this defense, in the form of deterring or repelling workers, derives from the physical properties or chemical compounds of these products. The nest entrance of Tetragonula carbonaria is constructed with propolis and Corymbia resins, and we ask whether nonvolatile chemicals present in these products act as a defense against ants. Our field experiments revealed that workers of Iridomyrmex mayri Forel were deterred from crossing a chemical barrier comprising nonvolatile, nonpolar (hexane) extracts of propolis and Corymbia tree resin. However, polar (ethanol) extracts did not have this effect. These data are the first to demonstrate that the chemical components alone of entrance propolis and resins can provide a nest‐defense function against ants.     

Descriptive attributes used in the characterization of stingless bees (Apidae: Meliponini) in rural populations of the Atlantic forest (Misiones-Argentina)

Background

We propose a new quantitative measure that enables the researcher to make decisions and test hypotheses about the distribution of knowledge in a community and estimate the richness and sharing of information among informants. In our study, this measure has two levels of analysis: intracultural and intrafamily.

Methods

Using data collected in northeastern Brazil, we evaluated how these new estimators of richness and sharing behave for different categories of use.

Results

We observed trends in the distribution of the characteristics of informants. We were also able to evaluate how outliers interfere with these analyses and how other analyses may be conducted using these indices, such as determining the distance between the knowledge of a community and that of experts, as well as exhibiting the importance of these individuals' communal information of biological resources. One of the primary applications of these indices is to supply the researcher with an objective tool to evaluate the scope and behavior of the collected data.     

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.     

Nestmate recognition in the stingless bee Melipona panamica (Apidae, Meliponini)

Summary: Nestmate recognition was studied in the Neotropical stingless bee Melipona panamica, a species in which workers "sneak" their own reproductive eggs into 1 % of brood cells. We manipulated four factors that could influence individual recognition cues: the mother queen, the environment during the immature stage, the environment during the early adult stage, and worker age. We also simulated the action of natural enemies on colonies tested for discrimination of such worker characteristics. All factors that we tested affected responses of the discriminating workers, which could recognize sisters, nieces and unrelated workers. Previous exposure of unrelated callow bees to the odor of the host nest greatly increased chances of acceptance by the host colony. Probability of acceptance decreased, however, with increasing age of introduced bees or increasing disturbance of the host colony. These complexities in patterns of nestmate recognition and nest defense are adequately explained from the standpoint of inclusive fitness of the discriminating workers. Differences in nestmate recognition and worker egg laying among Meliponini are also discussed.     

Alelle number and heterozigosity for microsatellite loci in different stingless bee species (Hymenoptera: Apidae, Meliponini)

In the present study we compare genetic characteristics (allele diversity and observed heterozygosity) of microsatellite loci, from three stingless bee species (Plebeia remota Holmberg, Partamona mulata Moure In Camargo and Partamona helleri Friese), amplified by using heterospecific primers originally designed for Melipona bicolor Lepeletier and Scaptotrigona postica Latreille. We analyzed 360 individuals of P. remota from 72 nests, 58 individuals of R. mulata from 58 nests, and 47 individuals of P. helleri from 47 nests. The three species studied showed low level of polymorphism for the loci amplified with primers derived from M. bicolor. However, for the loci amplified with primers derived from S. postica, only P. remota presented low level of polymorphism.     

A molecular phylogeny of the Old World stingless bees (Hymenoptera: Apidae: Meliponini) and the non-monophyly of the large genus Trigona

Abstract.  We examined the inter- and infrageneric relationships of Old World Meliponini with a near-complete sampling of supra-specific taxa. DNA sequences for the taxa were collected from four genes (mitochondrial 16S rRNA, nuclear long-wavelength rhodopsin copy 1 (opsin), elongation factor-1α copy F2 and arginine kinase). Additional sampling of New World taxa indicated that Trigona sensu lato is not monophyletic: Trigona from the Indo-Malayan/Australasian Regions forms a large clade distantly related to the Neotropical Trigona . A separate clade comprises the Afrotropical meliponines, and includes the 'minute' species found in the Afrotropical, Indo-Malayan and Australasian Regions. The Neotropical genus Melipona , by contrast with previous investigations, is not the sister lineage to the remaining stingless bees, but falls within the strongly supported Neotropical clade. These results constitute the framework for a revised classification and ongoing biological investigations of Meliponini. A single taxonomic change, Heterotrigona bakeri stat.n. , is proposed on the basis of sequence divergence.     

Chemical basis for inter-colonial aggression in the stingless bee Scaptotrigona bipunctata (Hymenoptera: Apidae)

Inter-colonial aggression was tested using three colonies of Scaptotrigona bipunctata in a natural setting when their nests were moved and by artificial contact between individuals. Examination of the cuticular lipids of individuals from two colonies kept under identical conditions showed clear differences in their cuticular hydrocarbon profiles. The cuticular lipids were a mixture of hydrocarbons (saturated and unsaturated alkanes and alkenes) within the range of C23-C29. The use of multivariate analysis (PCA and discriminant analysis) showed that seven of the identified surface compounds are enough to separate workers from colonies A and B from each other.     

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.     

Patterns of sexual size dimorphism in stingless bees: Testing Rensch’s rule and potential causes in highly eusocial bees (Hymenoptera: Apidae,Meliponini)

Eusocial insects offer a unique opportunity to analyze the evolution of body size differences between sexes in relation to social environment. The workers, being sterile females, are not subject to selection for reproductive function providing a natural control for parsing the effects of selection on reproductive function (i.e., sexual and fecundity selection) from other kinds of natural selection. Patterns of sexual size dimorphism (SSD) and testing of Rensch's rule controlling for phylogenetic effects were analyzed in the Meliponini or stingless bees. Theory predicts that queens may exhibit higher selection for fecundity in eusocial taxa, but contrary to this, we found mixed patterns of SSD in Meliponini. Non‐Melipona species generally have a female‐biased SSD, while all analyzed species of Melipona showed a male‐biased SSD, indicating that the direction and magnitude of the selective pressures do not operate in the same way for all members of this taxon. The phylogenetic regressions revealed that the rate of divergence has not differed between the two castes of females and the males, that is, stingless bees do not seem to follow Rensch's rule (a slope >1), adding this highly eusocial taxon to the various solitary insect taxa not conforming with it. Noteworthy, when Melipona was removed from the analysis, the phylogenetic regressions for the thorax width of males on queens had a slope significantly smaller than 1, suggesting that the evolutionary divergence has been larger in queens than males, and could be explained by stronger selection on female fecundity only in non‐Melipona species. Our results in the stingless bees question the classical explanation of female‐biased SSD via fecundity and provide a first evidence of a more complex determination of SSD in highly eusocial species. We suggest that in highly eusocial taxa, additional selection mechanisms, possibly related to individual and colonial interests, could influence the evolution of environmentally determined traits such as body size.     

Isolation and characterization of ten microsatellite loci in stingless bee Trigona spinipes (Apidae: Meliponini)

Stingless bees are the most abundant pollinators of Brazilian tropical flora. Trigona spinipes has some of the largest colonies of any stingless bee species found in several types of environment. This work describes the isolation and characterization of microsatellite loci for this species. A microsatellite‐enriched genomic library was constructed and ten primer pairs were designed for T. spinipes. The primers were tested in 20 unrelated individuals. The mean number of alleles was 8.10 and mean observed and expected heterozygosity were 0.655 and 0.680, respectively. Primers were also tested in cross‐species amplification and five loci were successfully amplified in Trigona chanchamayoensis, Trigona hyalinata, Tetragonisca angustula, Partamona mulata and Frieseomelitta varia. The microsatellite primers described herein will be useful for evaluating genetic variability and gaining a better understanding of the population structure of T. spinipes as well as other species of stingless bees.     

Temporal resource partitioning and climatological influences on colony flight and foraging of stingless bees (Apidae; Meliponini) in Ugandan tropical forests

We studied the flight activity of two stingless bee species (Meliponula ferruginea and Meliponula nebulata) and the environmental factors influencing their flight. Two morphs of M. ferruginea were studied: M. ferruginea (brown) in Budongo forest and M. ferruginea (black) in Bwindi Park. The two bee species exited their nests in characteristically distinct foraging bouts suggesting that the recruitment methods used may be direct leading or ‘piloting’. The number of individuals in a returning bout was less than that in an exiting bout suggesting recruits do not follow experienced foragers the whole distance to food source, a phenomenon referred to as ‘partial piloting’. Flight period of M. ferruginea (black) and M. nebulata in Bwindi was restricted to a few hours each day. Meliponula nebulata foraged in the drizzle; a survival strategy, which could promote its reproductive fitness. Nectar and pollen foraging took place throughout the day while the removal of debris was greater in the late hours of the morning. Increased temperature resulted in significant increase in number of exiting bees. There was increase in number of exiting bees with decrease in humidity up to an optimal of 78% thereafter, increase in humidity resulted in reduced number of exiting bees.