Male Bees Research Articles

Seasonal changes in odour preferences by male euglossine bees (Hymenoptera: Apidae) and their ecological implications

Orchid bees are an important group of specialized insect pollinators in the Neotropics. Male orchid bees are attracted by a wide range of aromatic substances often produced by flowers. Previous studies found that in some species the males change their aromatic preferences between seasons. In our study we documented seasonal changes of aromatic preferences in five euglossine bee assemblages along a 380-km-long seasonality and precipitation gradient and related them to climatic factors. We found that the proportion of species per site showing changes in their aromatic preference between seasons increased with climatic seasonality towards the south. Those species mainly belong to the genus Euglossa, subgenus Euglossa. We conclude that climatic seasonality mainly affects the orchid bees via the turnover of the aromatic substances provided by the plants. Further, we suggest that the ability to change the aromatic preference between seasons could be interpreted as a phylogenetic pre-adaptation that enabled some species to colonize climatically strongly seasonal habitats.

Long-term male aggregations of Euglossa melanotricha moure (Hymenoptera: Apidae) on fern fronds Serpocaulon triseriale (Pteridophyta: Polypodiaceae)

A communal dormitory of male orchid bees, Euglossa melanotricha Moure, was monitored over a one-year period, when they passed the night in the fronds of a Serpocaulon triseriale (Polypodiaceae) fern. The bees used the same fronds continuously, moving to neighboring fronds as senescence set in. As many as 49 males were observed together on any one night, clinging to the midribs on the abaxial surface of up to five fern blades with their mandibles. A number of males returned to the same site to pass the night continuously over a number of months, and were observed making physical contact with one another without provoking agonistic behavior. Males of E. melanotricha appeared to prefer sleeping at sites close to nests and potential sources of odoriferous essences, such as orchids (Orchidaceae).

Enantioselective Preference and High Antennal Sensitivity for (−)-Ipsdienol in Scent-Collecting Male Orchid Bees, Euglossa cyanura

Male neotropical orchid bees (Euglossini) collect volatile chemicals from their environment, store them in tibial pouches, and later expose their "perfumes" during a courtship display. Here, we showed that enantiomeric selectivity plays an important role in the choice of volatiles by male Euglossa cyanura in southern Mexico, and that behavioral selectivity is linked to antennal sensitivity. In field bioassays with equal concentrations of (+)-ipsdienol, (-)-ipsdienol, and racemate, males preferred the (-)-isomer to the racemate, while neglecting the (+)-isomer. Correspondingly, antennae of male E. cyanura showed larger electroantennographic responses to the (-)-isomer than to the (+)-isomer. In comparison, antennae of male Euglossa mixta, which are not attracted to any form of ipsdienol, showed lower electroantennographic responses to (-)-ipsdienol than did antennae of E. cyanura, and also did not differ in sensitivity with respect to the (+)- or (-)-isomers. We suggest that (-)-ipsdienol is an important component of perfume signals in male E. cyanura, which have undergone selection in favor of increased antennal sensitivity to that enantiomer.

Comparative labellar micromorphology of Zygopetalinae (Orchidaceae)

Molecular evidence indicates that the Neotropical sub-tribe Zygopetalinae is sister to Maxillariinae. Most members of the latter sub-tribe have deceit pollination strategies, but some species produce rewards such as nectar, pseudopollen, resin and wax, and are pollinated by a range of pollinators that include stingless bees (Meliponini), wasps and hummingbirds. By contrast, relatively little is known about the pollination of Zygopetalinae species. However, some are pollinated by fragrance-gathering, male euglossine bees or employ nectar deceit strategies. The aim of this study is to describe the labellar micromorphology of Zygopetalinae and to compare it with that of Maxillariinae sensu lato (s.l.) as part of an ongoing project to record the range of labellar characters found within the tribe Maxillarieae, and to assess whether these characters represent synapomorphies or homoplasies resulting from similar pollination pressures. The labella of 31 species of Zygopetalinae, including Cryptarrhena R. Br. and representatives of the Zygopetalum, Huntleya and Warrea clades, were examined using light microscopy and scanning electron microscopy, and the range of labellar characters was recorded. These characters were subsequently compared with those of Maxillariinae s.l. which formed the subject of our previous investigations. The labellar micromorphology of Zygopetalinae is less diverse than that of Maxillariinae and does not reflect the currently accepted phylogeny of the former sub-tribe based on molecular studies. Instead, the relative uniformity in labellar micromorphology of Zygopetalinae is probably due to homoplasies resulting from similar pollinator pressures. Labellar trichomes are relatively uncommon in Zygopetalinae, but occur in certain members of both the Zygopetalum and Huntleya clades. Trichomes are unbranched, uniseriate and multicellular with rounded apices, or unbranched and unicellular, with tapering, pointed and flexuose apices. Hitherto, unicellular trichomes of this kind have been observed only for euglossophilous orchid taxa, and the adoption of a relatively limited range of pollination strategies by Zygopetalinae may have resulted in reduced investment in micromorphological labellar characters.

Study on some biological characteristics of Tetrastichus gallerucae (Hym. Eulophidae), important parasitoid of Elm leaf beetle eggs in Kerman, Iran

In this study, a number of biologic characteristics of Tetrastichus gallerucae, the most important natural enemy of Xanthogaleruca luteola (Col.: Chrysomellidae), were studied. Experiments were carried out in growth room with a temperature of 25°C±1°C, relative humidity of 60%±5% and light period of 16L:8D. The results demonstrated the following outcomes: without food and host egg, the longevity of male and female bees was respectively, 1.23 and 1.35 days. On the host egg, their longevities were 3.85 and 6.02 days, respectively. On rarefied honey their longevities were 14.04 and 24.74 days, respectively and on the host eggs together with rarefied honey, their longevities were 13.4 and 34.72 days, respectively. The average growth period times in the egg of elm leaf beetle of male and female bees were 12.97 and 12.63 days, respectively. The percentage of female bees decreases as the longevity of the insects increases. These bees lay eggs in the 1–9-day-old eggs of elm leaf beetle but 1-day-old eggs of the host are preferred by T. gallerucae.

Solitary and social bees as pollinators of Wahlenbergia (Campanulaceae): single-visit effectiveness, overnight sheltering and responses to flower colour

Solitary bees often form specialised mutualisms with particular plant species, while honeybees are considered to be relatively opportunistic foragers. Thus, it may be expected that solitary bees are more effective pollinators than honeybees when foraging on the same floral resource. To test this, we studied two Wahlenbergia species (Campanulaceae) in South Africa that are visited by both social honeybees and solitary bees, and which are shown here to be genetically self-incompatible and thus reliant on pollinator visits for seed production. Contrary to expectation, the solitary bee Lipotriches sp. (Halictidae) and social bee Apis mellifera (Apidae), which were the two most frequent visitors to flowers of the study species, were equally effective pollinators in terms of the consequences of single visits for fruit and seed set. Both bee species preferentially visited female phase flowers, which contain more nectar than male phase flowers. Male solitary bees of several genera frequently shelter overnight in flowers of both Wahlenbergia species, but temporal exclusion experiments showed that this behaviour makes little contribution to either seed production or pollen dispersal (estimated using a dye particle analogue). Manipulation of flower colour using a sunscreen that removed UV reflectance strongly reduced visits by both bee groups, while neither group responded to Wahlenbergia floral odour cues in choice tests. This study indicates that while flowers of Wahlenbergia cuspidata and W. krebsii are pollinated exclusively by bees, they are not under strong selection to specialise for pollination by any particular group of bees.

The Pollination Biology of an Annual Endemic Herb, Physaria filiformis (Brassicaceae), in the Missouri Ozarks Following Controlled Burns1

Physaria filiformis, a threatened species of calcareous glade communities, blooms profusely within the Rocky Barrens Conservation Area (Missouri) under a program of controlled burns. Flowers visited by insect foragers in 2008 and 2009 had a mean > 35 and > 50 germinating grains on their stigmas respectively and a mean of 1.96–2.0 pollen tubes entering their ovaries (mean of 4 ovules/ovary). Results of controlled hand-pollinations conducted in situ in 2009 showed that this species had a negligible rate of self-pollination (mechanical autogamy) and showed classic Brassica-type, early-acting self-incompatibility. Each dissected flower had nectar glands and each seasonal population was visited by insects representing four insect orders; Coleoptera, Diptera, Lepidoptera and Hymenoptera. The most commonly collected floral foragers found to carry the pollen of the host flower were male and female native bees representing 38 species in the Andrenidae, Apidae, Colletidae, Halictidae, Megachilidae and the naturalized Apis mellifera. Only four of these species (11%) were collected in all three years, but these four accounted for slightly more than a third of all individual bees collected. None of the bees were known specialists on flowers of the Brassicaceae and only two species were habitat (glade) specialists. As P. filiformis is an obligate out-breeder but a generalist entomophile we suggest that future management plans include conservation and management of adjacent non-glade habitats to sustain the diverse range of pollinators.

Pollination Value of Male Bees: The Specialist BeePeponapis pruinosa(Apidae) at Summer Squash (Cucurbita pepo)

Male bees can be abundant at flowers, particularly floral hosts of those bee species whose females are taxonomic pollen specialists (oligolecty). Contributions of male bees to host pollination are rarely studied directly despite their prevalence in a number of pollination guilds, including those of some crop plants. In this study, males of the oligolectic bee, Peponapis pruinosa Say, were shown to be effective pollinators of summer squash, Cucurbita pepo L. Seven sequential visits from male P. pruinosa maximized squash fruit set and growth. This number of male visits accumulated during the first hour of their foraging and mate searching at flowers soon after sunrise. Pollination efficacy of male P. pruinosa and their abundances at squash flowers were sufficient to account for most summer squash production at our study sites, and by extrapolation, to two-thirds of all 87 North American farms and market gardens growing squashes that were surveyed for pollinators by collaborators in the Squash Pollinators of the Americas Survey. We posit that the substantial pollination value of male Peponapis bees is a consequence of their species' oligolecty, their mate seeking strategy, and some extreme traits of Cucurbita flowers (massive rewards, flower size, phenology).

The ontogeny of immunity in the honey bee, Apis mellifera L. following an immune challenge

The honey bee, Apis mellifera, is an ideal system for investigating ontogenetic changes in the immune system, because it combines holometabolous development within a eusocial caste system. As adults, male and female bees are subject to differing selective pressures: worker bees (females) exhibit temporal polyethism, while the male drones invest in mating. They are further influenced by changes in the threat of pathogen infection at different life stages. We investigated the immune response of workers and drones at all developmental phases, from larvae through to late stage adults, assaying both a constitutive (phenoloxidase, PO activity) and induced (antimicrobial peptide, AMP) immune response. We found that larval bees have low levels of PO activity. Adult workers produced stronger immune responses than drones, and a greater plasticity in immune investment. Immune challenge resulted in lower levels of PO activity in adult workers, which may be due to the rapid utilisation and a subsequent failure to replenish the constitutive phenoloxidase. Both adult workers and drones responded to an immune challenge by producing higher titres of AMPs, suggesting that the cost of this response prohibits its constant maintenance. Both castes showed signs of senescence in immune investment in the AMP response. Different sexes and life stages therefore alter their immune system management based on the combined factors of disease risk and life history.

Seasonal change in a pollinator community and the maintenance of style length variation in Mertensia fusiformis (Boraginaceae)

In sub-alpine habitats, patchiness in snowpack produces marked, small-scale variation in flowering phenology. Plants in early- and late-melting patches are therefore likely to experience very different conditions during their flowering periods. Mertensia fusiformis is an early-flowering perennial that varies conspicuously in style length within and among populations. The hypothesis that style length represents an adaptation to local flowering time was tested. Specifically, it was hypothesized that lower air temperatures and higher frost risk would favour short-styled plants (with stigmas more shielded by corollas) in early-flowering patches, but that the pollen-collecting behaviour of flower visitors in late-flowering patches would favour long-styled plants. Floral morphology was measured, temperatures were monitored and pollinators were observed in several matched pairs of early and late populations. To evaluate effects of cold temperatures on plants of different style lengths, experimental pollinations were conducted during mornings (warm) and evenings (cool), and on flowers that either had or had not experienced a prior frost. The effectiveness of different pollinators was quantified as seed set following single visits to plants with relatively short or long styles. Late-flowering populations experienced warmer temperatures than early-flowering populations and a different suite of pollinators. Nectar-foraging bumble-bee queens and male solitary bees predominated in early populations, whereas pollen-collecting female solitary bees were more numerous in later sites. Pollinators differed significantly in their abilities to transfer pollen to stigmas at different heights, in accordance with our prediction. However, temperature and frost sensitivity did not differ between long- and short-styled plants. Although plants in late-flowering patches tended to have longer styles than those in early patches, this difference was not consistent. Seasonal change in pollinator-mediated selection on style length may help maintain variation in this trait in M. fusiformis, but adaptation to local flowering time is not apparent. The prevalence of short styles in these populations requires further explanation.

Ipomoea bahiensis pollinators: Bees or butterflies?

Ipomoea bahiensis presents many characters of a psychophilous nectar flower. At the investigated synanthropic site, it is, however, visited and pollinated primarily by pollen-foraging small to medium sized bees that leave the flowers well before the end of anthesis. The busy bees appear to intimidate, probably by their mere existence, butterflies that function as pollinators in early morning, but disappear from the scene after beginning of anthesis. The plant is allogamous. A higher fruit set in hand cross-pollinated flowers as compared to naturally pollinated controls indicates pollen limitation. For the first time, we observed male bees entering the closing flowers as an overnight accommodation even before noon.

Diversity of the euglossine bee community (Hymenoptera, Apidae) of an Atlantic Forest remnant in southeastern Brazil

Diversity of the euglossine bee community (Hymenoptera, Apidae) of an Atlantic Forest remnant in southeastern Brazil. Euglossine bees, attracted to scent baits of cineole, eugenol and vanillin, were collected with entomological nets, from December 1998 to November 1999. Samplings were carried out once a month simultaneously by two collectors positioned in two different sites in an Atlantic Forest remnant in northeastern São Paulo state, Brazil. A total of 859 male euglossine bees, belonging to 13 species and four Euglossini genera were collected. Of the total sample, 506 (12 species) males were captured at site A and 353 (10 species) were collected at site B.In both sites, Euglossa pleosticta Dressler, 1982 was the most abundant species (45.79%), followed by Eulaema nigrita Lepeletier, 1841 (20.79%). The results of this study supply new information about the diversity of orchid bee fauna in Atlantic Forest remnants as well as show that more than one site is needed to sample these bees in a fragmented landascape.

Nest site selection in the European wool-carder bee, Anthidium manicatum, with methods for an emerging model species

For many organisms, choosing an appropriate nest site is a critical component of reproductive fitness. Here we examine nest site selection in the solitary, resource defense polygynous bee, Anthidium manicatum. Using a wood-framed screen enclosure outfitted with food sources, nesting materials, and bamboo trap nests, we show that female bees prefer to initiate nests in sites located high above the ground. We also show that nest sites located at higher levels are less likely to contain spiderwebs, suggesting an adaptive explanation for nest site height preferences. We report size differences between this study’s source populations in Boston, Massachusetts and Brooklyn, New York; male bees collected in Boston have smaller mean head widths than males collected in Brooklyn. Finally, we argue that methods for studying captive populations of A. manicatum hold great promise for research into sexual selection, alternative phenotypes, recognition systems, and the evolution of nesting behavior.

The importance of male red mason bee (Osmia rufa L.) and male bufftailed bumblebee (Bombus terrestris L.) pollination in blackcurrant (Ribes nigrum L.)

SummaryMale wild bees visit flowers to feed and, despite their lack of specialised organs for carrying pollen, simultaneously pollinate them. We analysed the pollinating efficiency of the males of two bee species for blackcurrant (Ribes nigrum L.): red mason bee (Osmia rufa L.) and bufftailed bumblebee (Bombus terrestris terrestris L.). Both bee species are commercial pollinators and many males are produced during their rearing. Gauze sleeves were used to isolate the inflorescences and to keep the males inside (one per sleeve). In each experimental group, there were six shoots with four neighbouring inflorescences (n = 24). The sleeves were also used to prevent other bees from reaching the flowers, and to allow self-pollination. Non-isolated flowers were pollinated by free-range bees. The effect of male bee pollination was similar to that of free-range bee pollination. The percentages of flowers that developed into fruit were as follows: male bufftailed bumblebee pollination, 79.5%; free-range bee pollination, 71.1%; male red mason bee pollination, 65.1%; and self-pollination, 46.4%; while the mean numbers of fruit per raceme were 5.0, 4.4, 3.6, and 2.4, respectively. The number of non-pollinated flowers per raceme (ranging from 1.3 – 2.8) exhibited an inverse relationship to these numbers of fruit. Our observations showed that male wild bees can pollinate blackcurrant flowers successfully, and could potentially be useful in other crops.

Bees in the Balance

B ees in the B alance B S J Jessica Robbins Our grocery stores are packed with fresh fruits, vegetables, and nuts—but how do they get there? The answer is bees. Bees and bee-assisted pollination are responsible for almost one third of what we eat, as well as for the growth and reproduction of plant species across the globe (Kaplan, 2011; Shultz, 2007). We all might know what bees are, but few recognize the magnitude of the importance they play in food production, and the possible losses that could occur if these populations of pollinators were to decline. Three-fourths of all plants depend on some form of pollinator intervention in order to reproduce, and over 90 common food crops—including most fruits, vegetables, nuts, and fibers— depend on bees specifically for pollination (Shultz, 2007; Tenebaum, 2010). Bees play an important role in the agricultural economy as well—their pollination is responsible for 15-20 billion dollars’ worth of crops in the United States alone, and they are considered the most economically valuable pollinators worldwide (Johnson, 2010). This could mean that if the domesticated bees used in agriculture were suddenly to disappear, one could face a bleak scene at the grocery store and on the kitchen table. sized honeycombs in order to pollinate the nation’s plants. While this certainly is not the rustic vision that many of us may have of beekeeping, the fundamentals of bee biology have not changed—being a beekeeper still means being in charge of a highly structured and complex society. Bees’ bodies are fine-tuned to capture pollen, and the bee hive is engineered to make the production of honey as streamlined as possible (Shultz, 2007; University of Georgia, 2011). When bee hives are healthy, they are constant centers of activity. They are filled with workers, non-reproducing females who maintain the health, cleanliness, and structural stability of the hive; drones, male bees who fly from hive to hive in the spring and summertime in order to reproduce; and the queen, the female bee in charge of producing the next generation (University of Georgia, 2011). Most of the activity in the bee colony at any given time is directed towards producing enough honey to survive the winter—when the bees cluster together in the hive in order to conserve heat and energy (University of Georgia, 2011). Winter is the most vulnerable time for bee colonies, when the larvae have begun to hatch and feed, but the new pollination season has not yet begun. However, if all goes well, the bee colony is continually being replenished by new generations of pollinators and producers (Shultz, 2007). “Honey bee health has been declining since the 1980s” Figure 1. A bee in the process of pollination Like many aspects of modern agriculture, humans have harnessed the role that bees play in food production—adapting bee’s natural lifestyles and utilizing their efficiency as pollinators in order to maximize productivity. Bees are now trucked across the nation, shuffled from farm to farm in industrial- Farmers across the country could tell that something was amiss in the winter of 2006 when, instead of seeing fully-stocked hives ready for the next production season, they discovered that their bee populations had declined almost overnight, leaving no clues about where the bees went or what had caused their disappearance. This sudden and mysterious evaporation of the bees was dubbed Colony Collapse Disorder (CCD), and triggered an avalanche of research efforts across the country as scientists and beekeepers struggled to better understand 1 • B erkeley S cientific J ournal • S cience of F ood • V olume 16 • I ssue 1

Attraction to old nest cues during nest selection by the solitary bee Megachile rotundata (Hymenoptera: Megachilidae)

SummaryThe alfalfa leafcutting bee, Megachile rotundata F. (Hymenoptera: Megachilidae), is an important pollinator for the commercial production of alfalfa seed. Poor nest establishment is, however, an ongoing problem for bee managers. Megachile rotundata are solitary yet gregarious bees that nest in pre-existing cavities and are attracted to previously used nests. Nest cells contain several components that may serve as cues for nesting females. In the current study, we sought to: 1. determine if there is a preference for cells that previously held male or female conspecific bees; 2. verify attraction to conspecific whole nest cells; and 3. determine which individual nest components of a cell are attractive to nesting females. In a series of cage and open field experiments, M. rotundata females were allowed to initiate nests in blocks containing whole cells or individual cell components from old nests. Statistical analyses of results verified the attraction to conspecific nest cells, with no preference for male or female cells. Females were equally attracted to whole cells from conspecifics and from another megachilid bee, Osmia lignaria. In field cages, females were equally attracted to all cell components, but preferred some cell components over others in open field experiments. These results provide a foundation for future studies to identify potential chemical lures to aid in the retention of bee populations at commercial nest sites.

Selective preying of the sphecid wasp Trachypus boharti on the meliponine bee Scaptotrigona postica: potential involvement of caste‐specific cuticular hydrocarbons

The specialist digger wasp Trachypus boharti Rubio‐Espina preys exclusively on males of the stingless bee Scaptotrigona postica Latreille 1807, although the hunting attacks involve both male and worker bees of S. postica and members of its own species. To understand the mechanism of prey selection, the cuticular hydrocarbon patterns of workers and males of S. postica are analyzed in detail, and the mandibular secretion of males is examined. The cuticular profiles of males and workers are distinctively different. The major group of cuticular compounds, heptacosene isomers, is twice as abundant in workers as in males. There is no clear distinction between worker and male mandibular secretions. Such a distinct and straightforward caste‐specific difference in cuticular hydrocarbons could function as a recognition cue by which T. boharti distinguishes between workers and males of S. postica.

Parasitism of the carpenter bee, Xylocopa virginica (L.) (Hymenoptera: Apidae), by larval Dermacentor variabilis (Say) (Acari: Ixodidae)

Seven larval Dermacentor variabilis were found during April 2010 on a male carpenter bee, Xylocopa virginica , at Rayne, Louisiana, USA, while looking for chaetodactylid mites. One tick appeared to be partially engorged. Subsequently, 10 more carpenter bees (7 males, 3 females) were collected from the same location and examined for ticks. None were infested. The significance of this finding is discussed

Behavioural differences between male and female carpenter bees in nectar robbing and its effect on reproductive success in Glechoma longituba (Lamiaceae)

Male and female nectar robbers may show significantly different behaviour on host plants and thus have different impacts on reproductive fitness of the plants. A 4-year study in natural populations of Glechoma longituba has shown that male carpenter bees (Xylocopa sinensis) are responsible for most of the nectar robbing from these flowers, while female bees account for little nectar robbing, demonstrating distinct behavioural differentiation between male and female bees in visiting flowers. The smaller male bee spends less time visiting a single flower than the larger female bee, consequently, the male bee is capable of visiting more flowers per unit time and has a higher foraging efficiency. Moreover, the robbing behaviour of female carpenter bees is more destructive and affects flower structures (ovules and nectaries) and floral life-span more than that of the male bee. According to the energy trade-off hypothesis, the net energy gain for male bees during nectar robbing greatly surpasses energy payout (17.72 versus 2.43 J), while the female bee net energy gain is barely adequate to meet energy payout per unit time (3.78 versus 2.39 J). The differences in net energy gain for male and female bees per unit time in nectar robbing are the likely cause of observed behavioural differences between the sexes. The differences in food resource preference between male and female bees constitute an optimal resource allocation pattern that enables the visitors to utilise floral resources more efficiently.

(6R, 10R)-6,10,14-Trimethylpentadecan-2-one, a Dominant and Behaviorally Active Component in Male Orchid Bee Fragrances

6,10,14-Trimethylpentadecan-2-one (Hexahydrofarnesyl acetone; HHA) previously has been found to be a major component in tibial fragrances of male orchid bees, Euglossa spp. HHA is a chiral molecule with four possible stereoisomers, (6R, 10R)-, (6R, 10S)-, (6S, 10R)-, and (6S, 10S)-6,10,14-trimethylpentadecan-2-one. In the present study, we characterized HHA extracted from Euglossa as the pure enantiomer (6R, 10R)-6,10,14-trimethylpentadecan-2-one. During bioassays in Mexico and Panama, the synthetic RR-isomer attracted males of six species of orchid bees, including three that were known to contain HHA in their tibial fragrances. Possible sources of HHA for wild bees are flowers of euglossophilous orchids and aroids. With a molecular weight of 268, HHA is the largest natural molecule known to attract male orchid bees in pure form. Its attractiveness to males suggests that low-volatility compounds have a function in male signals, e.g., serve as a "base note" in complex odor bouquets.