L. G. KAWAGUCHI, K. OHASHI and Y. TOQUENAGA

Transcription

1 Functional Ecology 2006 Do bumble bees save time when choosing novel flowers by Blackwell Publishing Ltd following conspecifics? L. G. KAWAGUCHI, K. OHASHI and Y. TOQUENAGA Integrative Environmental Sciences, Graduate School of Life and Environmental Sciences, University of Tsukuba, 1-1-1, Tennodai, Tsukuba City, Ibaraki , Japan Summary 1. Spatio-temporal variation in resource availability is often large and unpredictable. When animals need to find and sample novel foods, therefore they may prefer to choose food sources with feeding conspecifics or odour left by the conspecifics. This behaviour (local enhancement) would be favoured, especially if it decreases the time spent on food-finding and subsequent decision-making. In laboratory experiments we tested if naive bumble bees use local enhancement, and to what degree it could reduce the time spent on finding and sampling novel flowers. 2. When naive bees were presented with a pair of equally rewarded artificial or real flowers in a flight cage, they preferred to land and feed on the flower where a dead conspecific was attached. The presence of conspecifics reduced the time spent on detecting floral reward, which was significant only when bees chose between real flowers. In a similar pairwise choice, bees landed on artificial flowers with a dead conspecific wrapped in plastic more frequently than on flowers with the same-sized plastic wrap including no bees, which suggests that visual cues have important influences on the bees flower choice. 3. Effects of conspecifics on flower choice and food detection time were most evident when they were attached to real flowers, and least evident when they were wrapped in plastic. These results suggest that the presence of conspecifics on flowers has stronger effects on bees decision-making as the attractiveness of flowers increases, and that bees use both visual and non-visual cues to recognize conspecifics on flowers. 4. If the benefit of saving time were universal, the use of local enhancement would also be advantageous when bees switch between focal flower species or sites in response to temporal changes in resource availability. Key-words: Bombus terrestris, foraging behaviour, information transfer, local enhancement, plant animal interactions Functional Ecology (2006) doi /j x Ecological Society Introduction Time is honey Heinrich (1996) Many animals face considerable variability in food abundance, quality and appearance at various spatial and temporal scales. Because such variation is often unpredictable, animals have to make choices as to when, where and what they should forage to gain sufficient energy for growth, survival and reproduction (Pyke et al. 1977; Pyke 1978). The efficiency of food-finding will therefore greatly affect the fitness of these animals (White 1978; Bell 1990). A well known example of resources with spatio-temporal variability is nectar or Author to whom correspondence should be addressed. kawa@pe.ies.life.tsukuba.ac.jp pollen for flower visitors; individual plants and plant species, which grow in discrete patches, open their flowers at different times of day and different times of year (Pleasants 1983; Waser 1983; Hunter & Price 1992). Other food resources, such as fruits, seeds, foliage (reviewed by Hunter & Price 1992), carrion (Heinrich 1989) and many prey organisms (reviewed by White 1978), are also known to exhibit great variability in time and space. To locate and choose novel foods, animals may use social information perceived from other foragers, in addition to personal information that they can obtain through their own locomotory and sensory abilities. For example, honeybees and ants can rapidly locate newly discovered food sources, depending on directional information provided by successful foragers in their nests (von Frisch 1967; Seeley 1998; Hölldobler 239

2 240 L. G. Kawaguchi et al. 1999). This type of information transfer is called recruitment, which will increase foraging efficiency of the whole colony that is comprised of closely related kin. Recruitment would be beneficial even among nonrelated individuals if group foraging can sufficiently reduce their predation risk or prevent exclusive resource consumption by dominant individuals. Juvenile ravens are known to yell and recruit other non-related juveniles when they discover a new carcass to prevent exclusive food consumption by a few dominant adults (Heinrich 1989). Alternatively, animals can approach feeding conspecifics at food sites without any recruitment behaviour, which is called local enhancement (Thorpe 1956; Heyes 1994; Galef & Giraldeau 2001). Local enhancement was originally defined by Thorpe (1956) as an apparent imitation resulting from directing an animal s attention to a particular object or to a particular part of the environment, but the term is currently used to refer to cases where foraging animals prefer to visit food sources with feeding conspecifics or odour left by the conspecifics (Heyes et al. 2000). The use of local enhancement may be beneficial to animals despite the apparent costs of increased competition. Possible benefits will include (1) a reduction in the time used for food-finding and subsequent decisionmaking; (2) guaranteed food profitability in terms of energetic value and security; (3) a reduction of predation risk through facilitation of feeding-group formation (Giraldeau & Caraco 2000). Although local enhancement has mostly been studied in vertebrates that forage in groups (Thorpe 1956; Galef & Giraldeau 2001; Brown & Laland 2003), there have also been a few reports in social insects such as wasps and stingless bees (Raveret Richter & Tisch 1999; D Adamo et al. 2000, 2003; Slaa et al. 2003), and even in solitary insects such as flies (Collins & Bell 1996; Prokopy et al. 2000). Moreover, Slaa et al. (2003) found that the use of local enhancement during food-finding in six species of stingless bee is not related to the species strategy of foraging in groups, nor to their recruitment system. In addition, they found that newly recruited foragers showed local enhancement, but gradually shifted to local inhibition (avoidance of other feeding individuals) as they became experienced with the food patches. Thus previous studies on insects strongly suggest that a reduction of time spent on finding novel foods, rather than the benefits of group formation, is the main benefit of local enhancement. In this study we conducted laboratory experiments with Bombus terrestris L. to test whether, and to what degree, the use of local enhancement could reduce the time spent on finding and sampling novel foods. We allowed each test bee to choose between two equally rewarded artificial or real flowers: one with a resident bee on its petal (occupied flower) and the other without any bees (unoccupied flower). To focus on bees responses during food-finding and subsequent decision-making, we minimized the possible effects of previous foraging experience (Slaa et al. 2003) by using naive bees for each trial in the experiments. To rule out the possibilities of nest-based information transfer, nest-mates were never allowed to forage outside nest boxes, and each test bee was isolated from its nest 60 h before the experiment. In addition, to minimize possible effects of physical interference between resident and incoming bees, we used fresh dead bees as residents on occupied flowers. We addressed the following specific questions: (1) whether a bee prefers to visit occupied flowers than unoccupied ones when she does not have any prior information; and (2) whether, and to what degree, the preference for occupied flowers reduces the time spent on finding and sampling food. Materials and methods We used worker B. terrestris reared in nine commercial nests (API Co. Ltd, Gifu, Japan). Each colony was fed ad libitum, with fresh pollen added directly to the nest and 65% sucrose solution (g/g) exuding from a white cotton stick inside the nest, with its lower end inserted into a tank placed at the bottom of the nest box. The nest box was equipped with a cardboard lid on its top, which was closed to prevent light from entering except when necessary. Thus we kept bees naive to both artificial flowers and the mesh cage used for the experiments. To prepare the test bees, we picked up workers from the colonies, choosing average-sized ones with body length 20 mm, and placed each one in a plastic container (6 cm diameter) with a piece of cotton soaked with 200 µl diluted honey (50% sucrose equivalent). The cotton pieces were replaced with fresh ones every 24 h. This procedure was intended to help bees associate honey scent with the presence of food. After h, experiments were carried out in a mesh cage ( cm) as described below. The cage was placed near a large glass window in a laboratory that was illuminated with normal fluorescent light bulbs at the ceiling and sunlight entering through the window. Two artificial flowers were hung on an inside wall of the cage, which were 20 cm distant from the bottom and 18 5 cm apart from one another (Fig. 1). A green background (30 30 cm acrylic board) was attached to the wall from outside. Each artificial flower consisted of a centrifuge tube (tube micro I- 050C, AS One Corporation, Osaka, Japan) filled with 750 µl diluted honey (50% sucrose equivalent) and a round piece of yellow drawing paper (3 cm diameter) as the petal. We attached a dead bee to the petal with a piece of wire and used it as an occupied flower. Dead bees were chosen randomly from the same nest with the test bees and had been starved to death in a plastic container within 24 h before the experiments. The same artificial flowers without attaching dead bees were unoccupied. We also prepared visually occupied flowers by attaching dead bees wrapped tightly in plastic so as to preclude bees from perceiving the odour of conspecifics. The flowers attached with the same-sized plastic wrap including no bees were called

3 241 Local enhancement in bumble-bees Fig. 1. Top view of the flight cage. unoccupied wrap. All these flowers were rewarded equally, as described above. We also conducted an experiment with real flowers that already have structures and designs attractive to pollinators, to see whether these flower advertisements change bees responses to other conspecifics on flowers. We used capitula (flower heads) of a common Asteraceae species (Chrysanthemum morifolium Ramat.) as the real flowers. Each head has small, tubular disc florets in the middle and ray florets round the edge. Both types of floret are yellow, and ray florets are largely responsible for the conspicuousness of the head. In each test, we used a pair of heads of similar size ( 3 cm diameter), and put equal amounts of 50% diluted honey (5 10 µl) on disc florets of each head with a micropipette, to check whether bees that landed on heads fed or not. We prepared occupied and unoccupied real flowers as in the experiments with artificial flowers. In each trial, a test bee was placed in the cage in a plastic container 30 cm distant from the flowers (Fig. 1). Then the lid of the container was gently removed, and the bee was allowed to fly freely in the cage and choose between two flowers. We recorded the first flower she landed on as first landing and the first flower she probed as first feeding. We also recorded the time elapsed since the bee started flying in the cage until she landed on either of two flowers as flower detection time, and the time to first feeding as reward detection time. After each trial, the bee and the two flowers were removed from the cage and replaced with new ones for the next trial. Thus each bee and flower was used only once. First, we performed a choice test with a pair of unoccupied flowers (UU treatment) for each of 37 bees, to test whether they had a preference for visiting either right- or left-hand flowers. Second, we used a pair of an occupied and an unoccupied flower (OU treatment) and made 70 bees choose between them. Third, we used a pair of a visually occupied and an unoccupied wrap flower (VW treatment) for 51 bees. Fourth, we used a pair of an occupied and an unoccupied real flower (OU real treatment) for 73 bees. In each trial of these treatments, each flower was randomly assigned to either the right or left position. We compared frequency of choice between rightand left-hand flowers in UU treatments using a binomial test (H 0, right : left = 1 : 1). If the null hypothesis was not rejected bees had no preference for right or left flowers when they were identical we performed a binomial test for the other treatments to examine if the bees preferred to visit either of occupied (visually occupied) or unoccupied (unoccupied wrap) flowers. We also compared flower and reward detection time between right- and left-hand flowers in UU treatments. If we found no difference in detection time between the two positions, then we examined if detection time differed between cases where occupied (visually occupied) flowers were chosen and cases where unoccupied (unoccupied wrap) flowers were chosen. We also tested if detection time, irrespective of which flower was chosen, was reduced by the presence of resident bees by comparing between UU and OU treatments. Because the observed distribution of detection time lacks normality in most cases, and the variation in detection time often varies greatly between alternative flowers, we performed a sampled randomization test using a computer (Sokal & Rolf 1995). For each treatment we calculated the median of detection time for each alternative flower, and compared the difference of the median with its null equivalents calculated from random divisions of the pooled data between the alternatives. We then calculated the probabilities for all computed differences of medians, and summed probabilities that were smaller or equal to the probability that the observed difference of medians was produced when the null hypothesis was true (two-tailed probability). Results In UU treatments, bees showed no preference for either the right- or left-hand flower (first landing L : R = 18 : 19, P = 1; first feeding L : R = 20 : 17, P = 0 74). Also, detection time did not differ between the two positions (the sampled randomization test: P = 0 87 for flower detection time; P = 0 49 for reward detection time). In OU treatments, we found that bees preferred to land and feed on occupied flowers (Table 1). We found that a bee sometimes fed on the occupied flower after she made a first landing on the unoccupied flower, and vice versa. The probability of acceptance after first landing was therefore 45/55 (= 0 82) for occupied flowers, and 13/15 (= 0 87) for unoccupied flowers. This difference was not statistically significant (two-tailed Fisher s exact test, P = 1). The flower detection time for cases where bees chose occupied flowers was

4 242 L. G. Kawaguchi et al. Table 1. Number of first choices made by bumble bees in each treatment (OU; VW; OU real ) Treatment Unoccupied Occupied P* OU First landing <0 001 First feeding VW First landing First feeding OU real First landing 5 69 <0 001 First feeding <0 001 *P values are obtained from two-tailed binomial tests. OU, pair of occupied and unoccupied flowers; VW, pair of visually occupied and unoccupied wrap flowers; OU real, pair of occupied and unoccupied real flowers. significantly shorter than for unoccupied flowers (Table 2). The reward detection time for occupied flowers was also shorter than for unoccupied flowers, although the difference was not significant (Table 2). Because the detection time for unoccupied flowers did not differ between UU and OU treatments (the sampled randomization test: P = 0 98 for flower detection time; P = 0 83 for reward detection time), we performed another sampled randomization test when we pooled the detection time for unoccupied flowers in the UU and OU treatments, which balanced the sample size between occupied and unoccupied flowers. The pooled data showed a trend similar to the unpooled data (P < for flower detection time; P = for reward detection time). We also compared flower and reward detection time between UU and OU treatments, irrespective of flowers chosen, to test if the presence of a conspecific forager reduced the time for food-finding and subsequent decision-making (Table 2). The trend was similar to the above comparisons, but the reduction in detection time was not statistically significant. In VW treatments, bees preferred to choose the visually occupied flowers, but the trend was significant only for the frequency of first landing (Table 1). The detection time for visually occupied flowers was shorter than for unoccupied wrap flowers, although neither case was statistically significant (Table 2). In OU real treatments, bees preferred to choose occupied flowers more significantly than in OU and VW treatments (Table 1). While flower detection time did not differ significantly between occupied and unoccupied flowers (Table 2), reward detection time for occupied flowers was significantly shorter than for unoccupied flowers (Table 2). Discussion Throughout our experiments, naive bumble bees chose flowers with resident bees on their petals more frequently than unoccupied flowers (Table 1). Similar behaviour has also been observed in vertebrates such as mammals, birds and fish (Thorpe 1956; Heyes 1994; Galef & Giraldeau 2001; Brown & Laland 2003), as well as in insects (Collins & Bell 1996; Raveret Richter & Tisch 1999; D Adamo et al. 2000, 2003; Prokopy et al. 2000; Slaa et al. 2003; Leadbeater & Chittka 2005). Most of these studies, however, have not completely ruled out the possibility that the discoverer actively recruited others to the food source by conveying information through signals such as motion, sounds or pheromonal chemicals (Heinrich 1989). Even in cases where the effects of recruitment were carefully excluded, information transfer about the food source may have occurred in other places such as communal roosts, breeding colonies of birds, or colonies of social insects (Raveret Richter & Tisch 1999). We used dead bees or those wrapped in plastic as residents, which would have excluded the chances of recruitment. Also, it is improbable that test bees had obtained prior information about food sources in their nests because their nest-mates were never allowed to go outside or see the artificial flowers. Thus our results show clear evidence that naive bumble bees follow conspecifics when choosing novel flowers; in other words, they use local enhancement at food sites. Note, however, that bee choices might have been motivated by the dead conspecific emulating a nectar guide, a visual pattern on some flowers that is often used by pollinators for short-range orientation to the nectar (Kevan 1983). Also, tested individuals in our experiments had been entirely separated from the nest for a while beforehand. Thus our efforts to exclude possible information flow among nest-mates might have affected different aspects of bee behaviour, for example, the bees might have approached to residents to re-establish contact with nest-mates. Furthermore, we found that naive bees could often decrease the time spent on finding food by following Table 2. Comparisons of time elapsed before bees detected flowers and reward between UU and OU treatments ; and between occupied (visually occupied, V) and unoccupied (unoccupied wrap, W) flowers in each treatment Treatments Flower detection time (s) P* Reward detection time (s) P* UU : OU ( ) : ( ) ( ) : ( ) 0 14 U : O ( ) : ( ) ( ) : ( ) 0 33 W 2006 : V The Authors ( ) : ( ) ( ) : ( ) 0 38 U real : O real 8 00 ( ) : ( ) ( ) : ( ) Median Ecological (interquantile Society, range; 25 75% point). *Two-tailed probability obtained from the sampled randomization test (see text). UU, pair of unoccupied flowers; OU, pair of occupied and unoccupied flowers.

5 243 Local enhancement in bumble-bees conspecifics (Table 2). The difference in median of reward detection time between occupied and unoccupied flowers reached up to several minutes, which was significant when bees chose between real flowers. The trend was similar, but not significant, when bees chose between artificial flowers, suggesting that the presence of conspecifics has stronger effects on the decisionmaking of incoming bees as the flowers provide more attractive visual or olfactory signals. Because bumble bees usually visit hundreds of flowers during a short period (Harder 1983), even a minute of decrease in time for decision-making could greatly improve their foraging efficiency. Hence our results suggest that the primary benefit of following conspecifics at food sites, or local enhancement, is a reduction of time used for food-finding and subsequent decision-making. When the presence of residents indicates that the food is sufficiently rewarding and secure, the incomings could receive secondary benefits through local enhancement (Leadbeater & Chittka 2005). The need to make fast decisions when choosing novel foods would be a common requirement for naive foragers in nature. It is highly likely, therefore, that many other animals receive the same benefit from local enhancement as we observed in bumble bees. How often an animal actually uses local enhancement may be related to various aspects, including the animal s sensory abilities, learning abilities, energy requirements, diet breadth, residents aggressiveness, or changes in food availability and its spatial distribution. The use of local enhancement may also be beneficial for experienced bees when they need to switch between food species or sites. Because floral resources are often variable in time and space (Pleasants 1983; Waser 1983; Hunter & Price 1992), it would be crucial for bees and colonies to update their focal species or sites rapidly, especially before competitors show up, the weather changes, the sun sets, or the flowers wither. Thus experienced bees could improve their foraging efficiency by adopting local enhancement. Although bumble bees do not possess such a sophisticated language as that of honeybees, they are actually able to shift their focal species or patches within a day in response to a decrease in reward levels or flower densities (Heinrich 1979; Thomson 1981). Such rapid responses may be, at least partly, explained by the use of local enhancement. It should be noted, however, that experienced foragers may also learn to avoid occupied flowers so as to minimize competition from others (local inhibition), while foraging on the same flower species or site (Goulson et al. 1998; Slaa et al. 2003). The cues that the bees might use to recognize residents are still open to question. As we can see in the results from VW treatments, it is certain that a significant portion of recognition could be explained by visual cues (Table 1). Note, however, that the observed trends in preference and detection time were consistently weaker in VW than in OU treatments (Tables 1 and 2). This finding indicates that some non-visual cues may have been involved in the perception of resident bees. First, bees are known to recognize scent marks left on flowers (Schmitt & Bertsch 1990; Giurfa & Nüñez 1992; Goulson et al. 1998; Gilbert et al. 2001) or electrostatic charges modified by previous visitors (Erickson & Buchmann 1983), and use them to avoid or approach recently visited flowers. Second, movements of residents may generate air vibrations that incoming bees can perceive. In addition, it is known that honeybees are spontaneously attracted to small moving targets (Zhang & Srinivasan 1990; Lehrer & Srinivasan 1992). As bees eyes have acute temporal resolution (Lehrer 1998), incoming bees may exhibit more pronounced preference and shorter detection time if motion cues are added to the still image of residents. Further experiments will be needed to clarify how these perceptual cues contribute to local enhancement in bees. In summary, our laboratory experiments demonstrated that bumble bees use vision-based local enhancement when choosing novel flowers. Although local enhancement has been studied mostly in vertebrates, our results show that bumble bees posses enough ability to perform this behaviour innately. Another important finding is that local enhancement yields a substantial benefit in terms of reduced time spent finding and sampling unfamiliar foods. This primary benefit of local enhancement appears to be applicable to a wide range of animals other than flower visitors, especially when their food availability is variable in time and space (White 1978; Heinrich 1989; Hunter & Price 1992). From the plant s perspective, rapid responses of pollinators to reductions in flower density or reward level would affect the pollination services provided to earlyand late-blooming plants within a population. Further studies on whether and how animals use local enhancement in changing environments, as well as the benefits they obtain from it, will give new insights into our understanding of animal foraging strategies and plant animal interactions. Acknowledgements We are grateful to Dr K. Goka for providing us with B. terrestris colonies; two anonymous reviewers for critical reading of the manuscript; and Dr K. Fujii and many other colleagues for their helpful suggestions. This work was supported in part by grants from the Ministry of Education, Japan ( ) to Y.T. and from the Development Project of Prevention and Control for Ecological Risks of Commercial Bumble bees (Project Chief: Dr K. Goka, National Institute of Environmental Studies) to Y.T. References Bell, W.J. (1990) Searching behavior patterns in insects. Annual Review of Entomology 35, Brown, C. & Laland, K.N. (2003) Social learning in fishes: a review. Fish and Fisheries 4,

6 244 L. G. Kawaguchi et al. Collins, R.D. & Bell, W.J. (1996) Enhancement of resource finding efficiency by visual stimuli in Musca domestica (Diptera: Muscidae). Journal of the Kansas Entomological Society 69, D Adamo, P., Corley, J., Sackmann, P. & Lozada, M. (2000) Local enhancement in the wasp Vespula germanica: are visual cues all that matter? Insectes Sociaux 47, D Adamo, P., Lozada, M. & Corley, J. (2003) Conspecifics enhance attraction of Vespula germanica (Hymenoptera: Vespidae) foragers to food baits. Annals of the Entomological Society of America 96, Erickson, E.H. & Buchmann, S.L. (1983) Electrostatics and pollination. Handbook of Experimental Pollination Biology (eds C.E. Jones & R.J. Little), pp Van Nostrand Reinhold, New York. von Frisch, K. (1967) The Dance Language and Orientation of Bees. Harvard University. Press, Cambridge, MA, USA. Galef, B.G. Jr & Giraldeau, L.-A. (2001) Social influences on foraging in vertebrates: causal mechanisms and adaptive functions. Animal Behaviour 61, Gilbert, F., Azmeh, S., Barnard, C., Behnke, J., Collins, S.A. & Hurst, J. (2001) Individually recognizable scent marks on flowers made by a solitary bee. Animal. Behaviour 61, Giraldeau, L.-A. & Caraco, T. (2000) Social Foraging Theory. Princeton University Press, Princeton, NJ, USA. Giurfa, M. & Nüñez, J.A. (1992) Honeybees mark with scent and reject recently visited flowers. Oecologia 89, Goulson, D., Hawshon, S.A. & Stout, J.C. (1998) Foraging bumble bees avoid flowers already visited by conspecifics or by other bumble bee species. Animal Behaviour 55, Harder, L.D. (1983) Flower handling efficiency of bumble bees: morphological aspects of probing time. Oecologia 57, Heinrich, B. (1979) Majoring and minoring by foraging bumble bees, Bombus vagans: an experimental analysis. Ecology 60, Heinrich, B. (1989) Ravens in Winter. Summit Books, New York. Heinrich, B. (1996) The Thermal Warriors. Harvard University Press, Cambridge, MA, USA. Heyes, C.M. (1994) Social learning in animals: categories and mechanisms. Biological Reviews 69, Heyes, C.M., Ray, E.D. & Nokes, T. (2000) Stimulus enhancement: controls for social facilitation and local enhancement. Learning and Motivation 31, Hölldobler, B. (1999) Multimodal signals in ant communication. Journal of Comparative Physiology A 184, Hunter, M.D. & Price, P.W. (1992) Natural variability in plants and animals. Effects of Resource Distribution on Animal Plant Interactions (eds M.D. Hunter, T. Ohgushi & P.W. Price), pp Academic Press, San Diego, CA, USA. Kevan, P.G. (1983) Floral colors through the insect eye: what they are and what they mean. Handbook of Experimental Pollination Biology (eds C.E. Jones & R.J. Little), pp Van Nostrand Reinhold, New York. Leadbeater, E. & Chittka, L. (2005) A new mode of information transfer in foraging bumble bees? Current Biology 15, Lehrer, M. (1998) Looking all around: honeybees use different cues in different eye regions. Journal of Experimental Biology 201, Lehrer, M. & Srinivasan, M.V. (1992) Freely flying bees can discriminate between moving and stationary objects: performance and possible mechanisms. Journal of Comparative Physiology A 171, Pleasants, J.M. (1983) Structure of plant and pollinator communities. Handbook of Experimental Pollination Biology (eds C.E. Jones & R.J. Little), pp Van Nostrand Reinhold, New York. Prokopy, R.J., Miller, N.W., Duan, J.J. & Vargas, R.I. (2000) Local enhancement of arrivals of Ceratitis capitata females on fruit mimics. Entomologia Experimentalis et Applicata 97, Pyke, G.H. (1978) Optimal foraging: movement patterns of bumble bees between inflorescences. Theoretical Population Biology 13, Pyke, G.H., Pulliam, H.R. & Charnov, E.L. (1977) Optimal foraging: a selective review of theory and tests. Quarterly Review of Biology 52, Raveret Richter, M. & Tisch, V.L. (1999) Resource choice of social wasps: influence of presence, size and species of resident wasps. Insectes Sociaux 46, Schmitt, U. & Bertsch, A. (1990) Do foraging bumble bees scent-mark food sources and does it matter? Oecologia 82, Seeley, T.D. (1998) Thoughts on information and integration in honey bee colonies. Apidologie 29, Slaa, E.J., Wassenberg, J. & Biesmeijer, J.C. (2003) The use of field-based social information in eusocial foragers: local enhancement among nestmates and heterospecifics in stingless bees. Ecological Entomology 28, Sokal, R.R. & Rolf, F.J. (1995) Biometry. The Principles and Practice of Statistics in Biological Research, 3rd edn. W.H. Freeman, New York. Thomson, J.D. (1981) Spatial and temporal components of resource assessment by flower-feeding insects. Journal of Animal Ecology 50, Thorpe, W.H. (1956) Learning and Instinct in Animals. Hazell Watson and Viney, London. Waser, N.M. (1983) The adaptive nature of floral traits: ideas and evidence. Pollination Biology (ed. L. Real), pp Academic Press, Orlando, FL, USA. White, T.C.R. (1978) The importance of a relative shortage of food in animal ecology. Oecologia 33, Zhang, S.W. & Srinivasan, M.V. (1990) Visual tracking of moving targets by freely flying honeybees. Visual Neuroscience 4, Received 31 October 2005; revised 11 November 2005; accepted 14 November 2005 Editor: James E. Cresswell