The pollination efficiency of a pollinator depends on its foraging strategy,flowering phenology,and the flower characteristics of a plant species

Honey bees and stingless bees are generalist visitors of several wild and cultivated plants. They forage with a high degree of floral fidelity and thereby help in the pollination services of those plants. We hypothesized that pollination efficiency might be influenced by flowering phenology, floral characteristics, and resource collection modes of the worker bees. In this paper, we surveyed the foraging strategies of honey bees (Apis cerana, Apis dorsata, and Apis florea) and stingless bees (Tetragonula iridipennis) concerning their pollination efficiencies. Bees showed different resource gathering strategies, including legitimate (helping in pollination as mixed foragers and specialized foragers) and illegitimate (serving as nectar robbers and pollen thieves) types of flower visitation patterns. Foraging strategies are influenced by the shape of flowers, the timing of the visitation, floral richness, and bee species. Honey bees and stingless bees mainly acted as legitimate visitors in most plants studied. Sometimes honey bees served as nectar robbers in tubular flowers and stingless bees as pollen thieves in large-sized flowers. Among the legitimate categories, mixed foragers have a comparatively lower flower visitation rate than the specialized nectar and pollen foragers. However, mixed foragers have greater abundance and higher values of the single-visit pollination efficiency index (PEi) than nectar and pollen foragers. The value of the combined parameter ‘importance in pollination (PI)’ was thus higher in mixed foragers than in nectar and pollen foragers.     

Pollination of strawberry by the stingless bee,Trigona minangkabau,and the honey bee,Apis mellifera: An experimental study of fertilization efficiency

To know basic information about the stingless bee, Trigona minangkabau, and the European honey bee, Apis mellifera, as pollinator of strawberry, we set three greenhouse areas: the honey bee introduced area, the stingless bee introduced area and the control area. Foraging and pollination efficiencies of the two bee species were studied comparatively. During the experimental period (10 days), the stingless bee foraged well and the nest weight did not change, though the honey bee often foraged inefficiently and the nest weight decreased by 2 kg. The average nectar volume of a flower was lower in the honey bee area (0.02 μl) and nearly the same in the other two areas (0.1 μl). We make a numerical model to describe pollination and fertilization process. This model shows that one visit of the honey bee pollinated 11% of achenes and one visit of the stingless bee did 4.7% on average and that 11 visits of the honey bee or 30 visits of the stingless bee are required per flower to attain normal berry (fertilization rate, 87%). In this study, the rate of deformed berries in the stingless bee area (73%) was lower than that of the control area (90%), but higher than that of the honey bee area (51%). From our numerical model, we conclude the stingless bee could pollinate strawberry as well as the honey bee if we introduced 1.8 times of bees used in this experiment.     

Flowers morphology and nectar concentration determine the preferred food source of stingless bee,Heterotrigona itama

Heterotrigona itama is a stingless bee species from Meliponini tribe. The bee collects nectar, pollen and resin to produce honey, bee bread, and propolis. The bee is also known to visit and collect nectar from various types of flowers but there are limited studies on why this species of bee prefers to visit certain types of flowers. This study was conducted to identify the nectar concentration in selected flowers favoured by H. itama and the relationship between the bee and the morphology of the flowers. Nectar was obtained from different species of flowers and the concentrations were measured using a digital refractometer. The tube length of each flower species and the tongue length of the bees were also measured. The results revealed that flowers preferred by H. itama have high nectar concentrations. The tube lengths of the preferred flowers were between 2.0 and 4.0 mm, which is compatible with the tongue length of the bee. This study revealed that both nectar concentration and flower morphology are important factors for the bees in choosing their food sources. The results from this study will benefit the beekeepers in the identification of flowers that should be planted in their farms to improve stingless bee beekeeping activities. Understanding the relationship between the bees and their flower preferences could also help us to understand the importance of conserving both the bee colonies and the various species of flowering plants to ensure the sustainability of flora and fauna in the ecosystem.     

Floral Preference of Melipona eburnea Friese (Hymenoptera: Apidae) in a Colombian Andean Region

Melipona eburnea Friese is a stingless bee kept in some regions of Colombia, where it is reported to be vulnerable to extinction due to habitat disturbance. To contribute to raising conservation strategies, the aim of this study was to identify the floral preferences of this species using melissopalynological analysis. A total of 31 pollen pot samples and 37 honey samples were taken from March 2009 through March 2010 from four colonies in Fusagasuga, Colombia. We found 92 pollen types: 17 from pollen pot samples, 39 from honey samples (indicating the sources of nectar), and 36 in both types of samples. The most frequent pollen types in the pollen pot samples were Myrcia type (100%), Eucalyptus globulus (96.9%), and Fraxinus uhdei (96.9%). The most frequent pollen types in honey samples were E. globulus (97.4%) and Myrcia type (94.9%). The pollen types corresponded mainly to native plants (68%), trees (44.5%), plants whose sexual system is hermaphroditic (56.5%), and plants with inflorescences (76.2%). The most frequent shapes of the flowers were brush-like (type Myrtaceae) and dish-like (type Asteraceae), and the preferred flower colors were white or cream (52.2%). In general, we found that M. eburnea showed a strong preference for trees of the family Myrtaceae to obtain nectar and pollen, including native and introduced species. Some other families are contributing significantly, such as Melastomataceae for pollen collection and Asteraceae for nectar. These results highlight the key plant species for the diet of M. eburnea.     

Influence of environmental and colony factors on the initial commodity choice of foragers of the stingless bee Plebeia tobagoensis (Hymenoptera, Meliponini)

Novice foragers of social bees have to decide what food commodity to collect when they start foraging for the first time. In this decision making process two types of factors are involved: internal factors (the response threshold) and external factors (environmental and colony conditions). In this study we will focus on the importance of two external factors, pollen storage level and information from experienced foragers about food availability in the field, on the initial commodity choice of foragers of the stingless bee species Plebeia tobagoensis. We also studied the effect of the initial choice of individuals on their subsequent foraging career. This study was performed in a closed greenhouse compartment, where food availability and colony condition could be controlled. Information on food availability in the field from experienced foragers and pollen storage level both greatly influenced the initial commodity choice of individuals, with more choices for the commodity communicated by experienced foragers or lacking in storage. The initial choice of foragers is of importance for their future foraging career, although a substantial proportion of foragers did switch between food commodities. Because of the ability of novice foragers to become flexibly distributed over foraging tasks, social bees are able to react to changes in their environment without directly having to decrease foraging effort devoted to other foraging tasks. This, in combination with individual flexibility during foraging careers makes it possible for colonies of P. tobagoensis to forage efficiently in an ever-changing environment. Received 7 November 2005; revised 12 January 2006; accepted 16 February 2006.     

Resource Partitioning between Highly Eusocial Bees and Possible Impact of the Introduced Africanized Honey Bee on Native Stingless Bees in the Brazilian Atlantic Rainforest

The highly eusocial bee community of the neotropical Atlantic Rainforest was studied at Boracéia Biological Station in the state of São Paulo, Brazil. In this reserve, 17 species of stingless bees and the introduced Africanized honey bee were found, the latter being the most abundant flower visitor. Of all flowering plants, Asteraceae and Myrtaceae were particularly important as resources for bees. Trophic niche overlap between the various species of stingless bees is evident, and it was generally larger within the tribes Meliponini and Trigonini than between members of different tribes. Nevertheless, in the stingless bee community the competitive pressure is rather uniformly spread. The trophic niche of the Africanized honey bee can be positioned between those of Meliponini and Trigonini. Today this introduced species represents the main competitor in this bee community. However, its impact on native stingless bee populations is apparently buffered by mass-flowering trees which are the most important food plants of the indigenous highly eusocial bees.     

Bees and Other Insects Recorded on Flowering Trees in a Subtropical Araucaria Forest in Southern Brazil

Flower visiting insects were monitored on angiosperm trees in an Araucaria forest in Rio Grande do Sul, Brazil. The most abundant flower visitors were workers of the introduced honey bee, Apis mellifera, followed by stingless bees which were represented by 8 species. Together with other bees, they provide the main guild of foragers on flowering trees. The stingless bee fauna of the study area is similar to that of other regions of the Mata Atlântica, especially of former Araucaria forests, but also of montane coastal rain forests.     

Networks and dominance hierarchies: does interspecific aggression explain flower partitioning among stingless bees?

1. The distribution of consumers among resources (trophic interaction network) may be shaped by asymmetric competition. Dominance hierarchy models predict that asymmetric interference competition leads to a domination of high quality resources by hierarchically superior species. 2. In order to determine the competitive dominance hierarchy and its effect on flower partitioning in a local stingless bee community in Borneo, interspecific aggressions were tested among eight species in arena experiments. 3. All species tested were strongly mutually aggressive in the arena, and the observed interactions were often lethal for one or both opponents. Aggression significantly increased with body size differences between fighting pairs and was asymmetric: larger aggressors were superior over smaller species. Additional aggression tests involved dummies with surface extracts, and results suggest that species‐ and colony‐specific surface profiles are important in triggering the aggressive behaviour. 4. Sixteen stingless bee species were observed foraging on 41 species of flowering plants. The resulting bee–flower interaction network showed a high degree of generalisation (network‐level specialisation H₂’ = 0.11), corresponding to a random, opportunistic distribution of bee species among available flower species. 5. Aggressions on flowers were rare and only occurred at a low level. The dominance hierarchy obtained in the arena experiments did not correlate significantly with plant quality, estimated as the number of flowers per plant or as total bee visitation rate. 6. Our findings suggest that asymmetries in interference competition do not necessarily translate into actual resource partitioning in the context of complex interacting communities.     

Foraging by Male and Female Solitary Bees with Implications for Pollination

Both male and female solitary bees visit flowers for rewards. Sex related differences in foraging efficiency may also affect their probability to act as pollinators. In some major genera of solitary bees, males can be identified from a distance enabling a comparative foraging-behavior study. We have simultaneously examined nectar foraging of males and females of three bee species on five plant species in northern Israel. Males and females harvested equal nectar amounts but males spent less time in each flower increasing their foraging efficiency at this scale. The overall average visit frequencies of females and males was 27.2 and 21.6 visits per flower per minute respectively. Females flew shorter distances increasing their visit frequency, relative foraging efficiency and their probability to pollinate. The proportion of conspecific pollen was higher on females, indicating higher floral constancy and pollination probability. The longer flights of males increase their probability to cross-pollinate. Our results indicate that female solitary bees are more efficient foragers; females seem also to be more efficient pollinators but males contribute more to long-distance pollen flow.     

Food Recruitment Information can Spatially Redirect Employed Stingless Bee Foragers

Within a rewarding floral patch, eusocial bee foragers frequently switch sites, going from one flower to another. However, site switching between patches tends to occur with low frequency while a given patch is still rewarding, thus reducing pollen dispersal and gene flow between patches. In principle, forager switching and gene flow between patches could be higher when close patches offer similar rewards. We investigated site switching during food recruitment in the stingless bee Scaptotrigona mexicana . Thus, we trained three groups of foragers to three feeders in different locations, one group per location. These groups did not interact each other during the training phase. Next, interaction among trained foragers was allowed. We found that roughly half of the foragers switched sites, the other half remaining faithful to its training feeder. Switching is influenced by the presence of recruitment information. In the absence of recruitment information (bees visiting and recruiting for feeders), employed foragers were site specific. Foragers only switched among feeders that were being visited and recruited to. Switching was not caused by learned aversion to experimental handling. Switching in response to recruitment could provide a fitness benefit to the colony by facilitating rapid switching among exploited patches and provide a benefit of increasing plant gene flow between patches.     

The use of field–based social information in eusocial foragers: local enhancement among nestmates and heterospecifics in stingless bees

Abstract. 1. Foragers of social insects can be guided to profitable food sources by social information transfer within the nest. This study showed that in addition to such an information-centre strategy, social information in the field also plays an important role in individual foraging decisions. The effect of the presence of a nestmate on individual decision-making on where to forage was investigated in six species of stingless bee that differ in their recruitment system. Some species preferred to feed close to a nestmate (local enhancement) whereas other species actively avoided landing close to a nestmate. The term local inhibition is introduced for this avoidance behaviour.
2. Local enhancement and local inhibition were species specific but were not related to the species' recruitment system.
3. Local enhancement and local inhibition were affected by the individual's experience with the food source. Newly recruited foragers of Trigona amalthea showed local enhancement whereas experienced foragers showed local inhibition.
4. These individual decision-making rules explained accurately the spatial distribution of recruited nestmates: foraging groups of T. amalthea , which shows local inhibition, were more dispersed than foraging groups of Oxytrigona mellicolor , which shows local enhancement.
5. The effect of heterospecifics on stingless bee flower choice was investigated for 18 species combinations. Landing decisions were influenced significantly by the aggressiveness and the body size of the resident bee. Larger and more aggressive heterospecifics were avoided, whereas in some cases less aggressive bees acted as an attraction cue.     

POLLINATION ADAPTATION IN PEDICULARIS GROENLANDICA

Cinematographic and stereophotographic records indicate that Pedicularis groenlandica is pollinated in the Colorado Front Range by seven species of pollen-foraging bumblebees (Bombus sp.) to which the nectarless flower is intricately adapted functionally and structurally. Removing pollen by wing vibrations of an oscilloscopically identified frequency significantly distinct from flight vibration frequency, foragers carried pollen loads with up to three foreign pollen types in addition to Pedicularis pollen, which was found in all loads. No direct correlation was evident between flight vibration frequency and combined body-pollen load weight, ambient air temperature, or forager species. The flower is phenologically and morphologically adapted to the worker caste of apparently any Bombus species available to it throughout the plant's montane-alpine zone vertical-distribution range. The evolutionary position of the pollination mechanism is considered in relation to the floral morphology of other species in the genus Pedicularis.     

Effect of Biotic Factors on the Spatial Distribution of Stingless Bees (Hymenoptera: Apidae, Meliponini) in Fragmented Neotropical Habitats

We recorded stingless bee colony abundance and nesting habits in three sites with different anthropogenic activities in the Soconusco region of Chiapas, Mexico: (1) agroforestry (7 hacacao crop), (2) grassland (12?ha), and (3) urban area (3?ha). A total of 67 nests were found, representing five stingless bee species, Tetragonisca angustula angustula (Lepeletier), Trigona fulviventris (Guérin), Scaptotrigona mexicana (Guérin), Scaptotrigona pectoralis (Dalla Torre), and Oxytrigona mediorufa (Cockerell). The most abundant stingless bee in each site was T. angustula angustula (>50%). The primary tree species used by the bees were Ficus spp. (Moraceae, 37.8%) and Cordia alliodora (Boraginaceae, 13.5%). The nest entrance height of T. angustula angustula (96?±?19?cm) was different than the other species, and this bee was the only one that used all different nesting sites. Volatiles analyzed by gas chromatography from pollen collected by the stingless bees differed between bee species, but were highly similar in respect to the fragrances of the pollen collected by the same species at any site. Our data indicate that T. angustula angustula experienced low heterospecific and high intraspecific foraging overlap especially in the urban site. We observed cluster spatial distribution in grassland and in agroforestry sites. In the urban site, T. angustula angustula presented random distribution tended to disperse. Trigona fulviventris was the only overdispersed and solitary species.     

Environmental influences on flight activity of USDA-ARS Russian and Italian stocks of honey bees (Hymenoptera: Apidae) during almond pollination

Differences in flight activity and in the percentages of pollen foragers between commercially managed honey bees, Apis mellifera L. (Hymenoptera: Apidae), of two stocks (USDA-ARS Russian, n = 41 colonies; and Italian, n = 43 colonies) were evaluated in an almond, Prunus dulcis (Miller) D. A. Webb, orchard in Kern Co., CA, during February and March 2002. Flight activity was measured by taking 1-min counts of bees exiting colonies on each of 9 d. Flight activity was best predicted with a model containing the effects of colony size (populations of adult bees and sealed brood), temperature, time of day, the interaction of adult bee population with temperature, and the interaction of adult bee population with time of day. Flight increased linearly with adult bee and brood population, had a quadratic relationship with temperature (increasing, but less so at higher temperatures), and had a quadratic relationship with time of day (decreasing, but less so at later times). Larger colonies had more response to changing temperatures and less response to different times of day than small colonies. Bee type had no direct influence on flight activity at any given colony size, temperature, or time of observation or when evaluated using a reduced data set retaining 34 Italian colonies and 32 Russian colonies whose mean sizes were equal. Overall, however, Russian colonies were less populous by about one-fourth and so fielded on average 71% of the foragers that Italian colonies did. Pollen collection was measured by capturing returning foragers on 4 d. The percentages of foragers with pollen were not different for the bee types.     

Inflorescence Height Affects Visitation Behavior of Bees–A Case Study of an Aquatic Plant Community in Bolivia1

We studied the bee fauna visiting a plant community of 10 species of flowering aquatic plants in an inundated savanna region in Bolivia. In total we observed 36 bee species in 17 genera at the flowers. Cluster analysis of the similarities among the plant species in terms of their visitor spectra showed a division into two groups: plants with inflorescence heights shorter than the grass height and plants with inflorescences projecting out of the surrounding vegetation. Larger bees of the genera Apis, Melipona, Bombus, and Xylocopa were observed only at flowers above the surrounding vegetation. Smaller, mainly solitary bees (e.g., Augochlorella, Ancyloscelis) visited flowers in the dense vegetation near the water surface. Analyses of the pollen loads revealed that most individuals were highly flower constant. When bees carried different pollen types, it was generally pollen from flowers within a single stratum. We discuss specialization, flower constancy, competition, and different foraging strategies as possible reasons for stratum fidelity.     

西方蜜蜂和兰州熊蜂在设施桃园的访花偏好性比较

【目的】为了比较西方蜜蜂 Apis mellifera 和兰州熊蜂 Bombus lantschouensis 在设施桃园内对不同时期桃花的访花偏好性、以及这种偏好性与花粉活力和采集花粉花蜜之间的关系。【方法】记录2种蜂在温室桃园内访问早期花、中期花和晚期花的比例,测定桃花不同时期的花粉活力以及2种蜂携带的花粉活力,观察2种蜂采集花蜜和采集花粉的成功率,统计2种蜂访花过程中桃花所处的枝条数及植株数。【结果】桃花不同时期的花粉活力差异显著,早期花花药未开裂,花粉未释放,中期花花粉活力（58.3%）显著高于晚期花花粉活力（34.2%）（P<0.01）;西方蜜蜂更加偏好访问中期花,对中期花的访问率高达75.3%,显著高于兰州熊蜂对中期花的访问率（49.2%）（P<0.01）;西方蜜蜂携带的花粉活力（92.1%）显著高于兰州熊蜂携带的花粉活力（72.9%）,但是西方蜜蜂采集花粉和采集花蜜的成功率均低于兰州熊蜂（P<0.01）;在访问一定数量的桃花过程中,兰州熊蜂在设施桃园内访问的枝条数和植株数较多,分布范围较广（P<0.01）。【结论】和兰州熊蜂相比,西方蜜蜂对活力花粉的辨别能力更强,更加偏好访问花粉活力较高的花朵,这种偏好性导致其采集花粉花蜜的成功率降低。     

Cover Caption

Tomato flowers are pollinated by bees that vibrate their thorax for pollen collecting, behavior known as buzz‐pollination. The phenomenon is common and a specimen of the Neotropical stingless bee Melipona quadrifasciata is here depicted visiting a tomato flower for pollen collecting. While testing whether flower anthers exhibit optimal frequency for pollen release and whether flower bees tune their buzzes to match these frequencies, we recognized that neither bees nor plants are tuned to optimal pollen release frequencies (see pages 133–142). Photo provided José Lino‐Neto.     

Influence of functional traits on foraging behaviour and pollination efficiency of wild social and solitary bees visiting coffee (Coffea canephora) flowers in Uganda

An on-farm pollination experiment was conducted during the June–August and November–February blooming seasons of 2007 to 2008, in 30 small-scale coffee fields characterised by different habitat and vegetation types. The study was conducted in order to determine the best pollinator groups for coffee in Uganda and to collect relevant field information and determine the pollination efficiency of different bee species. Results indicate that across blooming seasons, coffee flowers were visited by 24–36 bee species. Hypotrigona gribodoi was the most frequent flower visitor, comprising over 60% of 5941 bee-visits recorded. Foraging rate and pollination speed varied among bee species. Solitary bees foraged on more flowers than social bees, but they spent less time per flower visited. Solitary bees visited more coffee trees and fields, but deposited less pollen, whereas social bees visited less trees and coffee fields in the landscape, but deposited more pollen on flowers. Fruit set was of 87%, 64% and 0.9%, respectively, in hand-cross pollination, open pollination and controlled-pollination treatments. Fruit abortion due to self-pollination was insignificant in this study. There was variability in pollination efficiency of different bee species. Pollination efficiency varied more significantly with sociality than with other bee functional traits and was not significantly influenced by tongue length and bee body size. Single-flower visits by social and solitary bees resulted in 89.7% and 68.14% fruit set, respectively. The most efficient bee species was Meliponula ferruginea (98.3%) followed by Meliponula nebulata (97.1%). Thus, very good pollinator species were wild social bees (mainly stingless bees) as opposed to honeybees and solitary bees that were previously reported to be the best pollinators of coffee in Panama and Indonesia. Morphological and anatomical characteristics of the bee pollen storage features may explain the difference in foraging behaviour activities and in pollination efficiency of social and solitary afrotropical bee species visiting lowland coffee in Uganda. In addition, pollination efficiency was influenced by land-use intensity, field management systems and habitat types found in the immediate surroundings of coffee fields, but not by coffee field size, coffee genotypes and mass blooming wild vegetation. It is recommended to farmers to adopt pollinator-friendly conservation and farming practices such as keeping an uncultivated portion (25%–30%) of their farms as pollinator reservoirs, protecting semi-natural habitats found in the vicinity of coffee fields, as well as promoting high on-farm tree cover to benefit a functionally diverse pollinator community.     

Color and Shape Discrimination in the Stingless Bee Scaptotrigona mexicana Guérin (Hymenoptera, Apidae)

To increase our understanding in bee vision ecology, we investigated the color and shape discrimination performance of the stingless bee Scaptotrigona mexicana Guérin. Our main goal was to describe the choice behavior of experienced foragers over time, trying to understand to what extent color and shape stimuli (separately tested) aid them to choose the rewarding option, in the presence of distracting, unrewarding stimuli. Single foragers were trained to collect sucrose solution from a target plate. Afterwards, one distracting, unrewarding plate was placed besides the target plate and eight choices were recorded. Our results showed that both color and shape stimuli assisted efficiently the trained foragers in locating the target plate. However, foragers chose significantly more often the target plate in the color experiments than in the shape experiments. In conclusion, in our experimental setup, color was of better assistance to the foragers of S. mexicana than shape to choose their rewards. This is the first study in which it is demonstrated that the choice performance over time in a stingless bee depends upon the characteristics of the resource, such as shape and color.     

Initial floral visitor identity and foraging time strongly influence blueberry reproductive success

Priority effects occur when the order of species arrival affects subsequent ecological processes. The order that pollinator species visit flowers may affect pollination through a priority effect, whereby the first visitor reduces or modifies the contribution of subsequent visits. We observed floral visitation to blueberry flowers from honeybees, stingless bees or a mixture of both species and investigated how (i) initial visits differed in duration to later visits; and (ii) how visit sequences from different pollinator taxa influenced fruit weight. Stingless bees visited blueberry flowers for significantly longer than honeybees and maintained their floral visit duration, irrespective of the number of preceding visits. In contrast, honeybee visit duration declined significantly with an increasing number of preceding visits. Fruit weight was positively associated with longer floral visit duration by honeybees but not from stingless bee or mixed species visitation. Fruit from mixed species visits were heavier overall than single species visits, because of a strong priority effect. An initial visit by a stingless bee fully pollinated the flower, limiting the pollination contribution of future visitors. However, after an initial honeybee visit, flowers were not fully pollinated and additional visitation had an additive effect upon fruit weight. Blueberries from flowers visited first by stingless bees were 60% heavier than those visited first by honeybees when total floral visitation was short (∼1 min). However, when total visitation time was long (∼ 8 min), blueberry fruit were 24% heavier when initial visits were from honeybees. Our findings highlight that the initial floral visit can have a disproportionate effect on pollination outcomes. Considering priority effects alongside traditional measures of pollinator effectiveness will provide a greater mechanistic understanding of how pollinator communities influence plant reproductive success.