Optimal foraging: Random movement by pollen collecting bumblebees

Summary Two bumblebee species, Bombus bifarius and B. flavifrons, forage randomly with respect to direction when gathering pollen on Potentilla gracilis. Bees avoid revisiting flowers by being able to differentiate recently visited from unvisited flowers. This recognition occurs while bees are flying over open flowers and appears to be a response to the amount of available pollen within flowers. Random foraging with respect to direction is the optimal strategy when the probability of flower revisitation is low. Bumblebees appear to be moving preferentially between nearest neighbors, again as predicted by foraging theory. This behavior causes the establishment of pollen patches in the P. gracilis population. Unlike other pollinators studied in similar situations, bumblebees on P. gracilis do not forage utilizing an area-restricted searching behavior. Because floral reward quality can be assessed at low cost by bees foraging on P. gracilis, their tendency to move to nearby flowers even after encountering a poor quality blossom apparently yields a higher rate of net energy intake than does area-restricted searching. The data indicate that bumblebees exhibit great plasticity in foraging behavior and that they are able to forage efficiently under a wide range of environmental conditions.     

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.     

Honeybee (Apis mellifera ligustica) Response to Differences in Handling Time, Rewards and Flower Colours

Free flying honeybees were tested outdoors on blue–white and blue–yellow dimorphic artificial flower patches to examine the influence of reward difference, flower handling‐time difference and flower colour choice on foraging decisions. We employed different flower‐well depths to vary handling times (costs), and differences in sucrose molarity to vary reward quality. Tests were performed with 2 and 6 μl rewards to vary quantity. We show that when handling time is correlated with flower‐colour morphs on a pedicellate artificial flower patch, a honeybee's foraging behaviour is dependent on the flower colours used in the choice tests. This supports a honeybee foraging model where constraints are a significant factor in decision making. Bees visiting blue–yellow flower patches exhibited flower constancy to colour, where they restricted most visits to a single flower colour, some bees to blue and others to yellow, irrespective of handing time differences. When offered a choice of equally rewarding blue or white flowers, bees were not constrained by flower colour and chose to visit flowers with a lower handling time. When reward molarity varied with well depth between blue and white flowers, foragers chose shallow‐well flowers (short‐handling time) with a smaller net harvest rate over deep‐well flowers (long‐handling time) with a greater net harvest rate. Results using the blue–white dimorphic flower patch suggest that when foraging options simultaneously involve reward and handling‐time choices, honeybee forager behaviour is inconsistent with an absolute method of evaluating profit.     

Intra‐floral resource partitioning between endemic and invasive flower visitors: consequences for pollinator effectiveness

1. Sympatric flower visitor species often partition nectar and pollen and thus affect each other's foraging pattern. Consequently, their pollination service may also be influenced by the presence of other flower visiting species. Ants are solely interested in nectar and frequent flower visitors of some plant species but usually provide no pollination service. Obligate flower visitors such as bees depend on both nectar and pollen and are often more effective pollinators. 2. In Hawaii, we studied the complex interactions between flowers of the endemic tree Metrosideros polymorpha (Myrtaceae) and both, endemic and introduced flower‐visiting insects. The former main‐pollinators of M. polymorpha were birds, which, however, became rare. We evaluated the pollinator effectiveness of endemic and invasive bees and whether it is affected by the type of resource collected and the presence of ants on flowers. 3. Ants were dominant nectar‐consumers that mostly depleted the nectar of visited inflorescences. Accordingly, the visitation frequency, duration, and consequently the pollinator effectiveness of nectar‐foraging honeybees (Apis mellifera) strongly decreased on ant‐visited flowers, whereas pollen‐collecting bees remained largely unaffected by ants. Overall, endemic bees (Hylaeus spp.) were ineffective pollinators. 4. The average net effect of ants on pollination of M. polymorpha was neutral, corresponding to a similar fruit set of ant‐visited and ant‐free inflorescences. 5. Our results suggest that invasive social hymenopterans that often have negative impacts on the Hawaiian flora and fauna may occasionally provide neutral (ants) or even beneficial net effects (honeybees), especially in the absence of native birds.     

Foraging at a safe distance: crab spider effects on pollinators

1. The ability of pollinating insects to discover and evade their predators can affect plant–pollinator mutualisms and have cascading ecosystem effects. Pollinators will avoid flowers with predators, but it is not clear how far away they will move to continue foraging. If these distances are relatively small, the impact of predators on the plant–pollinator mutualism may be lessened. The plant could continue to receive some pollination, and pollinators would reduce the time and energy needed to search for another patch. 2. A native crab spider, Xysticus elegans, was placed on one cluster in a small array of Baccharis pilularis inflorescence clusters, and the preferred short‐range foraging distances of naturally visiting pollinators was determined. 3. Nearly all pollinator taxa (honey bees, wasps, other Hymenoptera, and non‐bombyliid flies) spent less time foraging on the predator cluster. 4. The key result of this study is that inflorescences within 90 mm of the crab spider were avoided by visiting honey bees and wasps, which spent three‐ and 18‐fold more time, respectively, foraging on more distant flower clusters. 5. Whether honey bees can use olfaction to detect spiders was then tested, and this study provides the first demonstration that honey bees will avoid crab spider odour alone at a food source.     

The effect of nectar production on neighborhood size

Summary Bumblebee foraging behavior was observed on two plant species with similar floral and inflorescence structures. One species produces nectar while the other does not. Bees, upon visiting nectar producing flowers tend to empty them of nectar and by frequently moving between close neighbors, create a patchily distributed resource base. Bees maximize their foraging efficiency in such an environment by using an area-restricted searching behavior and flying distances inversely correlated with the quality of reward received. Pollen collecting bumblebees do not create a patchy environment and maximize their foraging efficiency by more consistently moving shorter distances. Pollen collecting bumblebees are significantly more likely to revisit flowers and to visit more flowers per inflorescence than are nectar gathering bumblebees. These differences in foraging behavior increase the neighborhood size for nectar producing species and make it increasingly unlikely that random drift will be a dominant mode of evolution in populations of these species.     

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

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

The influence of relative plant density and floral morphological complexity on the behaviour of bumblebees

We assessed the combined effects of varying the relative density and the relative floral morphological complexity of plant species on the behaviour of their bumblebee pollinators. Three species of bumblebee (Bombus pascuorum, B. terrestris and B. hortorum) were observed foraging on experimental arrays consisting of pair-wise combinations of four plant species: Borago officinalis, Phacelia tanacetifolia (both with simple flowers), Antirrhinum majus and Linaria vulgaris (both with complex flowers). Plant arrangements consisted of either two simple-flower species, a simple with a complex species or two complex species. The number of plants in each array was constant, while the frequency of each species was manipulated so that it was either rare, equal or common compared with its competitor. Contrary to predictions, rare plants were actually at an advantage in terms of the number of bees attracted per plant. However, rare plants were at a disadvantage in terms of pollen wastage because foragers more often went to a flower of another species after visiting a rare plant. The behaviour of bees on each plant species was further affected by plant floral complexity and the identity of the other species in the array. The three bumblebee species were markedly different in their foraging behaviour and in their responses to varying floral density and complexity. Each species preferred particular flower species. The results are discussed with reference to resource partitioning among bumblebee species. Received: 29 July 1998 / Accepted: 5 October 1998     

Floral visitors and ant scent marks: noticed but not used?

1. Bee behaviour when visiting flowers is mediated by diverse chemical cues and signals, from the flower itself and from previous visitors to the flower. Flowers recently visited by bees and hoverflies may be rejected for a period of time by subsequent bee visitors. 2. Nectar‐thieving ants also commonly visit flowers and could potentially influence the foraging decisions of bees, through the detection of ant trail pheromones or footprint hydrocarbons. 3. Here we demonstrate that, while naÏve bumblebees in laboratory trials are not inherently repelled by ant scent marks, they can learn to use them as informative signals while foraging on artificial flowers. 4. To test for similar activity in the wild, visitor behaviours at the flowers of Digitalis purpurea Linnaeus, Bupleurum fruticosum Linnaeus, and Brassica juncea (Linnaeus) Czernajew were compared between flowers that had been in contact with ants and those that had not. No differences were found between the two treatments. 5. The use of chemical foraging cues by bees would appear to be strongly dependent on previous experience and in the context of these plant species bees did not associate ant scent mark cues with foraging costs.     

黄猄蚁对大蜜蜂的捕食行为及其潜在影响

捕食作用会对访花昆虫的种群、行为以及植物适合度产生影响,是植物与传粉者相互关系研究中常被忽视的因素.本文报道了黄猄蚁对大蜜蜂的捕食行为,并模拟捕食的关键环节研究了捕食过程对重要访花昆虫行为的影响.结果表明,黄猄蚁能够利用局部环境主动攻击猎物,利用群体合作捕获采集过程中的体型较大的大蜜蜂,捕食威胁是其影响植物-访花者关系的重要机制.大蜜蜂具有感知花上危险的能力,模拟处理的个体会逃离危险的花或植株并在花上留下标记,将危险信息传递给其它个体.其它拜访者对具有危险信号花的采集频次明显减少,采集时间缩短;模拟处理的影响会随时间推移而较快地消失.此外,该实验没有发现大蜜蜂在花上停留采集过程中具有明显的防御行为.     

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.     

Departure rules used by bees foraging for nectar: A field test

Summary Departure rules used by solitary long-tongued bees (Anthophora spp. andEucera spp.) collecting nectar from flowers ofAnchusa strigosa (Boraginaceae) were studied. The amount of nectar a bee receives from an individual flower was estimated by measuring the time elapsed since the previous bee visit to that flower. Measurements of nectar accumulation in experimentally emptied flowers indicated that this time interval is an accurate predictor of nectar volumes in flowers. We found that nectar rewards influence the probability of departure from individual plants, as well as distances of movements within plants. The probability of departure from individual plants was negatively related to the amount of reward received at the two lastvisited flowers. This result indicates that the bees used a probabllistic departure rule, rather than a simple threshold departure rule, and that rewards from both the current and the previously visited flower were important in determining departure points. Distances of inter-flower movements within plants were negatively related to the amount of reward received at the current flower. The overall results suggest that the pollinators ofA. strigosa make two types of departure decisions-departures from the whole plant and departures from the neighbourhood of individual flowers-and that they use different departure rules for each scale. Factors influencing the decision-making processes of the observed foraging behaviour are discussed.     

Assessment of pollen reward and pollen availability in Solanum stramoniifolium and Solanum paniculatum for buzz‐pollinating carpenter bees

The two widespread tropical Solanum species S. paniculatum and S. stramoniifolium are highly dependent on the visits of large bees that pollinate the flowers while buzzing them. Both Solanum species do not offer nectar reward; the rewarding of bees is thus solely dependent on the availability of pollen. Flower visitors are unable to visually assess the amount of pollen, because the pollen is hidden in poricidal anthers. In this study we ask whether and how the amount of pollen determines the attractiveness of flowers for bees. The number of pollen grains in anthers of S. stramoniifolium was seven times higher than in S. paniculatum. By contrast, the handling time per five flowers for carpenter bees visiting S. paniculatum was 3.5 times shorter than of those visiting S. stramoniifolium. As a result foraging carpenter bees collected a similar number of pollen grains per unit time on flowers of both species. Experimental manipulation of pollen availability by gluing the anther pores showed that the carpenter bees were unable to detect the availability of pollen by means of chemical cues before landing and without buzzing. Our study shows that the efficiency of pollen collecting on S. paniculatum is based on large inflorescences with short between‐flower search times and short handling time of individual flowers, whereas that of S. stramoniifolium relies on a large amount of pollen per flower. Interestingly, large carpenter bees are able to adjust their foraging behaviour to drastically different strategies of pollen reward in otherwise very similar plant species.     

A comparison of distances flown by different visitors to flowers of the same species

Summary The morphologically complex flowers of Delphinium nelsonii, D. barbeyi, and Ipomopsis aggregata are visited by a wide variety of animals. Visitors to each species range from small insects, such as worker bumblebees and solitary bees, to hummingbirds, and thus span roughly an order of magnitude in body mass and metabolic rate while flying; they also differ in type of food collected and in their efficacy as pollinators. Despite these differences, all the visitors to a given plant species fly similar, short distances between successively visited flowers and plants. There are no significant relationships between mean flight distance and metabolic rate or body mass among the visitors to any plant species. Thus there is no evidence that flight characteristics depend on anything as straightforward as whether flower visitors have high or low energetic requirements.     

Nectarivore foraging ecology: rewards differing in sugar types

Abstract.

• 1 Honey bees, visiting artificial flower patches, were used as a model system to study the effects of sugar type (sucrose, glucose, fructose, and mixed monosaccharide), caloric reward, and floral colour on nectarivore foraging behaviour. Observed behaviour was compared to the predictions of various (sometimes contradictory) foraging models.
• 2 Bees drank indiscriminately from flowers in patches with a blue-white flower dimorphism when caloric values of rewards were equal (e.g. 1M sucrose in both colours; 1 M sucrose versus 2 M monosaccharide of either type), but when nectar caloric rewards were unequal, they switched to the flower colour with the calorically greater reward.
• 3 In yellow-blue dimorphic flower patches, on the other hand, bees did not maximize caloric reward. Rather, bees were individually constant, some to blue, others to yellow, regardless of the sugar types or energy content of the rewards provided in the two flower morphs.
• 4 The results suggest that optimal foraging theory (maximization of net caloric gain per unit time) is a robust predictor of behaviour with regard to the sugar types common to nectars; such optimal foraging is, however, limited by a superstructure of individual constancy.

     

Pollen foraging by bumblebees: Foraging patterns and efficiency on Lupinus polyphyllus

Summary Bumblebees foraging on vertical inflorescences start near the bottom and work upward, behavior commonly interpreted as a response to the greater amounts of nectar available in lower flowers. Lupinus polyphyllus, which produces no nectar, has more pollen available in upper flowers. Although bees are probably unable to detect this gradient, since pollen is hidden from their view, they still start low and forage upward. Therefore, we concluded that the bees' tendency to forage upward on vertical inflorescences is not tied to a reward gradient. In addition, bees use only about 15% of the flowers per inflorescence, although they could be much more efficient by visiting and revisiting every flower systematically. In general, revisits would not be penalized because most flowers contain enough pollen for several visits. Optimal foraging theory may not offer an adequate explanation for such gross inefficiency.     

Pollinator flight directionality and the assessment of pollen returns

Summary Nectar-foraging pollinators often exhibit a directional pattern of movement between plants when the energetic costs of revisiting previously utilized areas can significantly reduce foraging efficiency. However, bumblebees (Bombus spp.) foraging for pollen on flowers of Aquilegia caerulea rarely moved in a straight line among successively visited plants. Most flights from plants visited were either to closely neighboring plants or were longer and involved bypassing near neighbor plants. Bees biased their flights toward plants with relatively large numbers of flowers yet visited only a small fraction of the flowers on each plant. Such foraging tactics might result when the energetic costs of revisiting plants are minor. Alternatively we suggest that bumblebees foraging for pollen may not perceive revisitations and their associated costs because they do not assess pollen returns on a per plant basis. In this case energetic-efficiency arguments predicting the pattern of foraging movements among plants may be inappropriate. A better level of analysis would be where the bees assess net energy returns, perhaps between bouts of pollen-combing and corbiculae-packing.     

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.     

The movement patterns of carpenter beesXylocopa micans and bumblebeesBombus pennsylvanicus onPontederia cordata inflorescences

The movement patterns of carpenter bees (Xylocopa micans) and bumblebees (Bombus pennsylvanicus) foraging for nectar on vertical inflorescences ofPontederia cordata were studied near Miami, Florida. The floral biology ofP. cordata is unique in several ways: (a) many short-lived flowers per inflorescence, (b) constant nectar production throughout the life span of each flower, and (c) abscence of vertical patterning of nectar and age of flowers. Inflorescences ranged between 3.5 and 15.8 cm long and had between 9 and 55 open flowers. Both carpenter bees and bumblebees arrived mostly on the bottom third of the inflorescence and left after visiting flowers on the top third of the inflorescence. The departure position from the inflorescence was higher up than observed in studies of other insect pollinators foraging on other speces of plants. This pattern of departure probably occurs in the absence of a vertical gradient of nectar or floral morphology.     

谁是腊梅的主要传粉者:昆虫行为与传粉作用

访花昆虫不同的访花与飞行行为导致其访花频率小同,进而对植物传粉产生不同的影响.意大利蜜蜂(Apis mellifera ligustica)、苍蝇和食蚜蝇是腊梅(Chimonanthus praecox)最常见的访花类群(或种类),但是它们的访花行为却有很大不同.意大利蜜蜂主要以快速飞行为主,偶见爬行,苍蝇访花时主要以快速飞行、爬行和跳跃为主,而食蚜蝇以长时间单花访问和悬空飞行以及间歇性休息为主.根据访花类群(或种类)在一朵花上的访花时间和花间飞行时间进行推算,每只意大利蜜蜂、苍蝇和食蚜蝇每分钟分别可以访问4.57、2.65和0.53朵花.结合每种(类)昆虫的访花数量推算出意大利蜜蜂、苍蝇和食蚜蝇每分钟分别可以访问498.19、1,089.74和99.78朵花.传粉效力(相同条件下单位时间内相同数目访花者能够授粉的花朵数)实验结果证明苍蝇和意大利蜜蜂分别是93％、100％(n=30),而食蚜蝇只有13％(n=30).苍蝇和意大利蜜蜂可携带大量花粉且具有很高的传粉效力,因此,访花速度的快慢是二者访花能力强弱的主要限制因素.由此,我们认为苍蝇可能是腊梅最主要的传粉者,意大利蜜蜂次之(数量偏少),食蚜蝇再次(访花与飞行行为的影响以及访花效力较低是限制其访花能力的主要因素).