David W. Roubik

Ecology and natural history of tropical bees

Preface Acknowledgments Part I. Introduction: 1. Approaches to tropical bee biology 2. Diversity of tropical bees Part II. Foraging and Pollination: 3. Resources gathered by bees 4. Mechanisms of resource collection 5. Foraging and flight activity 6. Pollination ecology Part III. Nesting and Reproduction Biology: 7. Bee nests 8. Nest predators, associates and defense 9. Mating and brood production Part IV. Community Ecology: 10. Seasonality, abundance and flower preference 11. Composition of bee assemblages 12. Roles of bees in communities References Index Appendices.

Arthropod diversity in a tropical forest

Assessing Creepy Crawlies Arthropods are the most diverse group of terrestrial animal species, yet estimates of the total number of arthropod species have varied widely, especially for tropical forests. Basset et al. (p. 1481, see the cover) now provide more reliable estimates of total arthropod species richness in a tropical rainforest in Panama. Intensive sampling of a half hectare of forest yielded just over 6000 arthropod species. Scaling up this result to the whole forest suggests that the total species diversity lies between 17,000 and 40,000 species. Total arthropod species richness in a tropical rainforest can be best predicted by plant diversity. Most eukaryotic organisms are arthropods. Yet, their diversity in rich terrestrial ecosystems is still unknown. Here we produce tangible estimates of the total species richness of arthropods in a tropical rainforest. Using a comprehensive range of structured protocols, we sampled the phylogenetic breadth of arthropod taxa from the soil to the forest canopy in the San Lorenzo forest, Panama. We collected 6144 arthropod species from 0.48 hectare and extrapolated total species richness to larger areas on the basis of competing models. The whole 6000-hectare forest reserve most likely sustains 25,000 arthropod species. Notably, just 1 hectare of rainforest yields >60% of the arthropod biodiversity held in the wider landscape. Models based on plant diversity fitted the accumulated species richness of both herbivore and nonherbivore taxa exceptionally well. This lends credence to global estimates of arthropod biodiversity developed from plant models.

Mate number, kin selection and social conflicts in stingless bees and honeybees

Microsatellite genotyping of workers from 13 species (ten genera) of stingless bees shows that genetic relatedness is very high. Workers are usually daughters of a single, singly mated queen. This observation, coupled with the multiple mating of honeybee queens, permits kin selection theory to account for many differences in the social biology of the two taxa. First, in contrast to honeybees, where workers are predicted to and do police each others male production, stingless bee workers are predicted to compete directly with the queen for rights to produce males. This leads to behavioural and reproductive conflict during oviposition. Second, the risk that a daughter queen will attack the mother queen is higher in honeybees, as is the cost of such an attack to workers. This explains why stingless bees commonly have virgin queens in the nest, but honeybees do not. It also explains why in honeybees the mother queen leaves to found a new nest, while in stingless bees it is the daughter queen who leaves.

THE ECOLOGICAL IMPACT OF NECTAR-ROBBING BEES AND POLLINATING HUMMINGBIRDS ON A TROPICAL SHRUB'

The consequences of nectar robbing by highly social bees were studied at 71 patches of the forest-edge shrub, Pavonia dasypetala (Malvaceae) at two tropical moist forest habitats in central Panama. Groups of Trigona (Trigona) ferricauda (Apidae: Meliponinae) arrived at flowers in early morning; each bee dominated a single flower that it perforated to rob nectar (Fig. 1). Robbers in each patch aggressively defended their feeding sites from the sole pollinator of the plant, the Hermit Hummingbird Phaethornis supercilious (Trochilidae: Phaethorninae). Less visitation by humming- birds and reduced seed production resulted from nectar robbing. Flower number in patches was not associated with visitation per flower by pollinators, but patches having the most flowers were entered more often by P. superciliosus. In contrast, thieving P. longuemareus and robbing T. ferricauda showed no patch preference related to total flower number. Seed production per flower was not related to the total number of flowers presented in patches at one time. The average proportion of robbed flowers through the entire flowering episode of P. dasypetala was 36% among 66 patches at one site and 35% among 5 patches at a second site. Reduced seed production was not caused directly by robber damage to flowers, but indirectly through successful deterrence of birds via joint attacks by bees on and near the flower visited by a hummingbird. Further, although fewer seeds were pro- duced by robbed flowers overall, robbed and unrobbed flowers in patches that were heavily robbed did not differ in seed production. Thus robbing primarily influenced reproductive success at the level of the flower patch. P. dasypetala was self-pollinating, yet unrobbed flowers that were not bagged produced 67% more seeds than those not visited by P. superciliosus. Persistent robbing by Trigona may result in selective advantage for autogamous or apomictic P. dasypetala.

Competitive interactions between neotropical pollinators and africanized honey bees.

The Africanized honey bee, a hybrid of European and African honey bees, is thought to displace native pollinators. After experimental introduction of Africanized honey bee hives near flowers, stingless bees became less abundant or harvested-less resource as visitation by Africanized honey bees increased. Shifts in resource use caused by colonizing Africanized honey bees may lead to population decline of Neotropical pollinators.

Ups and Downs in Pollinator Populations: When is there a Decline?

Introduction Methods Biological background Variability measures Trends and perturbations Euglossine census techniques and evaluation Results Community comparisons Long-term trends Simultaneous sampling and evaluation of census techniques Discussion Bee communities over time ENSO and the bees Euglossine sampling techniques and long-term sampling strategies Responses to this Article Acknowledgments Literature Cited Appendix 1 Appendix 2 Appendix 3 Appendix 4

Nectar selection by Melipona and Apis mellifera (Hymenoptera: Apidae) and the ecology of nectar intake by bee colonies in a tropical forest

SummaryColony foraging activity of four Melipona species (Apidae: Meliponinae, tribe Meliponini) was studied during the dry season, when many plants flower in central Panama. The efficiency of sucrose solution uptake by Melipona was compared to that of domesticated European Apis mellifera. Dynamics of nectar foraging were also recorded for 3 of the Melipona visiting the forest shrub, Hybanthus prunifolius (Violaceae).1.Sugar concentration in nectar brought to nests averaged from 21 to 60% sugar for 15 colonies of M. fasciata, M. compressipes triplaridis, M. fuliginosa and M. marginata micheneri. Concentrations ranged from 19 to 72%, and all species collected nectars ranging at least between 24 and 63% sugar. However, M. compressipes and M. marginata preferred higher concentrations and foraged less on dilute nectars. Peak colony nectar harvest occured in late morning or early afternoon; peak pollen harvest was in early morning.2.Imbibing rates of bees given 20, 30, 45, 60 or 70% sucrose solutions were highest at ≦45% sucrose, but caloric intake was most rapid at 60% sucrose for all species. All but M. marginata displayed greater net intake rates than domesticated European Apis mellifera. A foraging choice model incorporating caloric reward and imbibing rates of bees suggests M. compressipes and M. marginata should specialize on richer nectars. Rate of caloric intake per forager weight was higher for all Melipona (0.03–0.13g) than for A. mellifera (0.10 g).3.The nectar of Hybanthus prunifolius (Violaceae), a shrub pollinated exclusively by Melipona, progressed from 35 to 60% sugar during the day. Bees foraged most when nectar was below 60% concentration, a pattern best explained as the result of intercolony competition and greater availability of lower quality nectar.4.Sugar concentration in nectar harvested by colonies rose from lower to higher values through the day for Melipona. The increasing caloric reward of nectar is adaptive in exploiting foraging preferences of such bees. As standing nectar crop is depleted by competing bees, a gradual shift to more rewarding nectar should promote increased bee foraging range, more flower visits during a foraging trip, floral constancy, and genetic outcrossing.5.The nectar load capacity of A. mellifera is greater than that of Melipona. Other factors being equal, Africanized A. mellifera, now a permanent resident of neotropical forests, should visit more flowers during a foraging trip. Additional species differences in foraging behavior are analyzed.

Long-term ecology of euglossine orchid-bees (Apidae : Euglossini) in Panama

SummaryAbundance patterns during 6–7 years and orchid visitation were determined for 51 species of the 57 local euglossine bees. Male bees were counted at 3 chemical attractants presented in the same manner each month. Sites were separated by 75 km but included wet Atlantic forest at 500 m elevation, moist forest at 180 m near Barro Colorado Island, and cloud forest at 900 m near the Pacific ocean. 1. From 15 to 30 euglossine species of 4 genera were active in each month and site; monthly species number and general bee abundance were positively correlated. Many species had 3 annual abundance peaks (range 1–4) and were active throughout the year, but peak annual abundances rarely occurred during late wet or early dry seasons. In contrast, Eufriesea generally were present as adults only 1–2 months in a year. 2. Euglossine populations were exceptionally stable. Species at each site were more stable than any known insect population, and stability and abundance were positively associated. However, year-to-year population stability and the degree of seasonality were not correlated. Among the three sites, the more diverse (species rich) bee assemblages displayed lower stability; these were the wetter and upland sites. 3. The most abundant bees visited more orchid species. Eg. and El. each visited and average of 4 orchid species (range 0–13); Ex. and Ef. visited 0–3. Stable populations did not visit more or fewer orchid species than did unstable populations. 4. Less than 68% of species at each site visited orchid flowers; less than a few dozen of the 100–800 bees counted in a day carried orchid pollinaria. Over 20% of the euglossine species never were seen with pollinaria at any site and probably seldom visit orchids in central Panama. 5. Most bee species visited 1 or no fragrance orchids in a given habitat. Orchids tended to utilize common pollinators that seldom included more than 1 species, and they utilized stable or unstable, seasonal or aseasonal bees. However, the most stable and abundant bee, Eg. imperialis, rarely pollinated orchids; fewer than 10 of ca. 20000 bees carried pollinaria. 6. Orchids may interact primarily with discrete seasonal bee population peaks-probably the emerging adults. Although specialized orchid preferences are implicated for species that visit few or no local orchids but pollinate other species and carry pollinaria in other areas, euglossine bees do not need orchids to survive or reproduce.

Sporadic food competition with the African honey bee: projected impact on neotropical social bees

Bee colonies in lowland forest in Panama were monitored for pollen and nectar harvest, pollen species utilization and nectar quality and quantity per returning forager. Despite sharing most pollen resources and nectar of the same quality with 20 introduced colonies of the African honey bee (Apis mellifera), native stingless bees of 12 species were largely unaffected by its activity. Pollen and nectar harvested by the honey bees were 10-200 times that pro- cured by 17 stingless bee colonies. This discrepancy in total harvest and general lack of com- petitive effect is explained by a honey bee foraging area over 10 times that of the native bees, and apparent foraging shifts to escape competition with honey bees, thus reduced potential overlap in foraging sites. Seven cases of direct resource competition for pollen or nectar were documented, out of 31 tests. Rare periods of intensive harvest were diminished by competing African honey bees. Such harvest peaks lasted for only a few hours in 13 days of observation. Despite average dura- tion of 4%o foraging time for each species, peaks included as much as 51% total harvest. Calcu- lations based upon colony populations, food stores and flight range show that if African honey bees persist at a density of 1 colony per km2, colonies of some stingless bee species may dis- appear after 10 years. Their chances of escaping food competition by taxonomic specialization on flowers seem slight.

FRAGRANCE COLLECTION, STORAGE, AND ACCUMULATION BY INDIVIDUAL MALE ORCHID BEES

Individually marked males of two species of Euglossa were sighted repeatedly and over considerable periods of time (up to 44 days) at artificial fragrance baits exposed on Barro Colorado Island (BCI), Panama. Individuals switched between different bait chemicals that are attractive for the respective species, and no bait preferences or individual bait constancy was observed. GC-MS analyses of 153 males of three species showed that individual hind tibiae contain highly variable quantities of a complex and species-specific blend of fragrance compounds, mainly terpenoids and aromatics. In all three species, frequency distributions of individual quantities were strongly skewed towards individuals with small amounts, and individual amount and complexity were positively correlated. Tibial contents of male Euglossa imperialis that were kept alive in a flight cage for 0, 5, 10, or 15 days showed no qualitative or quantitative change over time, suggesting that the fragrances are very efficiently stored in the hind legs. In Euglossa cognata wing wear, an established age correlate of the species, was positively correlated with individual fragrance quantity. Our results suggest that male euglossines forage continuously for a variety of volatiles, store them, and finally acquire large quantities of a complex and specific fragrance bouquet. Both qualitative and quantitative aspects of individual contents are likely to contain information on male phenotypic and genotypic quality.