Discrimination of Unrewarding Flowers by Bees; Direct Detection of Rewards and Use of Repellent Scent Marks

Bumblebees and honeybees deposit short-lived scent marks on flowers that they visit when foraging. Conspecifics use these marks to distinguish those flowers that have recently been emptied and, so, avoid them. The aim of this study was to assess how widespread this behavior is. Evidence for direct detection of reward levels was found in two bee species: Agapostemon nasutus was able to detect directly pollen availability in flowers with exposed anthers, while Apis mellifera appeared to be able to detect nectar levels of tubular flowers. A third species, Trigona fulviventris, avoided flowers that had recently been visited by conspecifies, regardless of reward levels, probably by using scent marks. Three further bee/flower systems were examined in which there was no detectable discrimination among flowers. We argue that bees probably rely on direct detection of rewards where this is allowed by the structure of the flower and on scent marks when feeding on flowers where the rewards are hidden. However, discrimination does not always occur. We suggest that discrimination may not always make economic sense; when visiting flowers with a low handling time, or flowers that are scarce, it may be more efficient to visit every flower that is encountered.     

Why do honeybees reject certain flowers?

Summary Honeybees often approach flowers of Lotus corniculatus and then fly away without attempting to extract nectar. These rejected flowers contained 41% less nectar than my random sample. The accepted flowers contained 24% more nectar than my random sample. The differences among these three flower-groups were due to differences in the percent of empty flowers in each group rather than the differences in the absolute amount of nectar. Honeybees increased their foraging efficiency by accepting less empty flowers and rejecting more empty flowers than would be expected if they foraged randomly. There are two possible mechanisms for this discrimination-behavior: either the bees are smelling nectar odor or they are smelling bee scent left by previous visitors to the flower. My results are inconsistent with the hypothesis that bees are basing their decision on nectar smell and suggest that they are using bee scent as a means of identifying empty flowers.     

Do foraging bumblebees scent-mark food sources and does it matter?

Summary The foraging of worker bees of Bombus terrestris visiting artificial feeders in a climatic test chamber was investigated. The behaviour of worker bees visiting rewarding and unrewarding feeders is completely different. Of all flower visits to rewarding feeders 94% are probing-visits, i.e. the bees land on the flower and probe for nectar. In contrast, only 0.3% of all visits to unrewarding feeders are probing-visits, whereas 47% are approach-visits, i.e., the bees approach the feeders without landing. Exchanging feeder discs proves that the signal used for discrimination must be associated with the plastic disc used as landing platform. Most probably it involves scent-marking of the rewarding feeders with components of high and low volatility. The mean foraging efficiency of bees in a scent-marked foraging arena is 5.7 mg sugar/min and drops to 2.8 mg sugar/min after the scent marked discs are replaced by clean ones. Three components generate this drop in foraging efficiency: (1) the between-flower flight time increases, i.e. the bees search for a longer time before landing on flowers, (2) the bees no longer discriminate between rewarding and unrewarding feeders, and (3) the bees probe empty feeders longer than necessary; obviously they expect to find nectar.     

The repellent scent-mark of the honeybeeApis mellifera tigustica and its role as communication cue during foraging

Summary Experimental evidence for flower-marking in honeybees (Apis mellifera ligustica), using pairs of workers from the same colony foraging on an artificial patch of flowers, is reported. Workers marked artificial flowers with scent and strongly rejected all flowers they had recently visited. The same rejection behavior, in a lower although significant proportion, was observed when bees visited flowers just abandoned by the other individual of the pair. The repellent nature of this scent-mark was demonstrated with the use of an air extractor connected to the patch of artificial flowers. When the apparatus was turned on, the rejection behavior disappeared and bees accepted both flowers just abandoned by themselves and flowers just abandoned by the other bee. Differences in the response level of bees to their own marks or to the partner's marks suggest that the repellent scent-mark applied by a bee during foraging would basically be a self-use signal, although it certainly has value in communicating with other workers.     

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.     

Recognition of scent marks in solitary bees to avoid previously visited flowers

Knowing how floral visitors forage efficiently among flowers is important to understanding plant-pollinator interactions. When bees search for rewarding flowers, they use several visual cues to detect the available floral resources. In addition to these cues, bees can recognize scent marks, which are olfactory cues left on flowers foraged by previous visitors. This behavior is well known in social bees, such as honeybees and bumblebees. Although solitary bees do not need to give information about which flowers were foraged to conspecifics, several pieces of evidence have indicated the use of scent marks. However, it is unknown whether the behavior is widely used in many different bee species. We investigated whether four different solitary bees, Colletes patellatus (Colletidae), Andrena prostomias (Andrenidae), Osmia orientalis (Megachilidae), and Tetralonia mitsukurii (Apidae), can recognize flowers that have been foraged previously by visitors within 3 min. All four bees showed rejection responses to flowers foraged by conspecifics. However, our results showed that responses to foraged flowers varied among bee species. The tendency of A. prostomias and T. mitsukurii to reject the foraged flowers was pronounced, while in C. patellatus and O. orientalis it was weak. In both A. prostomias and T. mitsukurii, the rejection rate of flowers foraged by conspecifics decreased as the time lag after the last visit increased. Both bees visited the flowers from which pollen or nectar had been artificially removed. We suggest that A. prostomias and T. mitsukurii would recognize scent marks left by previous visitors, while the other two bees would not recognize them so strongly. It is likely that the decision to use scent marks is dependent either on the richness of resources or on the complexity of floral structure.     

Flower choice by honey bees (Apis mellifera L.): sex-phase of flowers and preferences among nectar and pollen foragers

Bees foraging for nectar should choose different inflorescences from those foraging for both pollen and nectar, if inflorescences consist of differing proportions of male and female flowers, particularly if the sex phases of the flowers differ in nectar content as well as the occurrence of pollen. This study tested this prediction using worker honey bees (Apis mellifera L.) foraging on inflorescences of Lavandula stoechas. Female flowers contained about twice the volume of nectar of male flowers. As one would predict, bees foraging for nectar only chose inflorescences with disproportionately more female flowers: time spent on the inflorescence was correlated with the number of female flowers, but not with the number of male flowers. Inflorescence size was inversely correlated with the number of female flowers, and could be used as a morphological cue by these bees. Also as predicted, workers foraging for both pollen and nectar chose inflorescences with relatively greater numbers of both male and female flowers: time spent on these inflorescences was correlated with the number of male flowers, but not with the number of females flowers. A morphological cue inversely associated with such inflorescences is the size of the bract display. Choice of flowers within inflorescences was also influenced predictably, but preferences appeared to be based upon corolla size rather than directly on sex phase.     

Bees use honest floral signals as indicators of reward when visiting flowers

Pollinators visit flowers for rewards and should therefore have a preference for floral signals that indicate reward status, so called ‘honest signals’. We investigated honest signalling in Brassica rapa L. and its relevance for the attraction of a generalised pollinator, the bumble bee Bombus terrestris (L.). We found a positive association between reward amount (nectar sugar and pollen) and the floral scent compound phenylacetaldehyde. Bumble bees developed a preference for phenylacetaldehyde over other scent compounds after foraging on B. rapa. When foraging on artificial flowers scented with synthetic volatiles, bumble bees developed a preference for those specific compounds that honestly indicated reward status. These results show that the honesty of floral signals can play a key role in their attractiveness to pollinators. In plants, a genetic constraint, resource limitation in reward and signal production, and sanctions against cheaters may contribute to the evolution and maintenance of honest signalling.     

Nectar utilization and pollination by Australian honeyeaters and insects visiting Calothamnus quadrifidus (Myrtaceae)

Nectar availability in Calothamnus quadrifidus flowers was studied at Wongamine Nature Reserve in late spring (November). Despite some overnight depletion by moths and other invertebrates, more nectar was present in flowers at dawn than at the preceding dusk. Significant nectar depletion occurred within a few hours after dawn, mainly due to foraging by two honeyeater species. Lichmera indistincta and Phylidonyris nigra. Thereafter, nectar availability was maintained at relatively low levels, principally because of foraging by honeyeaters and honey bees. Apis mellifera, that became active during the warmer part of the day. Although individual honeyeaters consumed more nectar than A. mellifera, honey bees were so abundant that their total impact was greater than that of either honeyeater species for much of the day. Transfer of C. quadrifidus pollen between flowers is necessary in order to achieve a high level of seed set, as the flowers appear to be protandrous. Honeyeaters appeared to be considerably more significant pollen vectors than A. mellifera.     

The evolution of floral scent: the influence of olfactory learning by insect pollinators on the honest signalling of floral rewards

1.  The evolution of flowering plants has undoubtedly been influenced by a pollinator's ability to learn to associate floral signals with food. Here, we address the question of 'why' flowers produce scent by examining the ways in which olfactory learning by insect pollinators could influence how floral scent emission evolves in plant populations.
2.  Being provided with a floral scent signal allows pollinators to learn to be specific in their foraging habits, which could, in turn, produce a selective advantage for plants if sexual reproduction is limited by the income of compatible gametes. Learning studies with honeybees predict that pollinator-mediated selection for floral scent production should favour signals which are distinctive and exhibit low variation within species because these signals are learned faster. Social bees quickly learn to associate scent with the presence of nectar, and their ability to do this is generally faster and more reliable than their ability to learn visual cues.
3.  Pollinators rely on floral scent as a means of distinguishing honestly signalling flowers from deceptive ones. Furthermore, a pollinator's sensitivity to differences in nectar rewards can bias the way that it responds to floral scent. This mechanism may select for flowers that provide olfactory signals as an honest indicator of the presence of nectar or which select against the production of a detectable scent signal when no nectar is present.
4.  We expect that an important yet commonly overlooked function of floral scent is an improvement in short-term pollinator specificity which provides an advantage to both pollinator and plant over the use of a visual signal alone. This, in turn, impacts the evolution of plant mating systems via its influence on the species-specific patterns of floral visitation by pollinators.     

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.     

Invasive ant (<Emphasis Type="Italic">Anoplolepis gracilipes</Emphasis>) disrupts pollination in pumpkin

Yellow crazy ant (Anoplolepis gracilipes (F. Smith); “YCA”) is known for its aggressive predatory ability and ability to exert exploitation competition on both native and other invasive ants via floral nectar. We argue that YCA invasion can exert both interference and exploitation competition on legitimate pollinators. In pumpkin fields (Cucurbita maxima L.) of south India, YCA infested the flowers, particularly the pistillate flowers, for nectar foraging. Pumpkin is a honey bee-mediated cross-pollinated monoecious plant that produces disproportionately very few pistillate flowers. We hypothesize that YCA presence in the flowers can affect the visitation rate and foraging time of honey bees in the flowers, the fruit set in pumpkins, and can exert predatory pressure on the honey bees if the bees linger in ant-colonized flowers. Both YCA and honey bees preferred to forage on the limited pistillate flowers in the plants. After colonizing the flowers, YCA did not retreat for hours, even upon disturbance by competitors, such as honey bees. Both the visitation frequency and the foraging time of honey bees were drastically reduced in ant-colonized flowers, and none of the ant-colonized flowers developed into fruits, suggesting that the YCA exert both an ecological and evolutionary pressure on pumpkin. The ants preyed upon about 17% of the honey bees that lingered in ant-colonized flowers, and the time the bees spent foraging predicted the fate of the bees. Exploitation competition exerted by the YCA on pumpkin may have far-reaching consequences for the pollination and productivity of this cash crop.     

Traplining in bumblebees (Bombus impatiens): a foraging strategy’s ontogeny and the importance of spatial reference memory in short-range foraging

To test the relative importance of long-term and working spatial memories in short-range foraging in bumblebees, we compared the performance of two groups of bees. One group foraged in a stable array of six flowers for 40 foraging bouts, thereby enabling it to establish a long-term memory of the array, and adjust its spatial movements accordingly. The other group was faced with an array that changed between (but not within) foraging bouts, and thus had only access to a working memory of the flowers that had been visited. Bees in the stable array started out sampling a variety of routes, but their tendency to visit flowers in a repeatable, stable order (“traplining”) increased drastically with experience. These bees used shorter routes and converged on four popular paths. However, these routes were mainly formed through linking pairs of flowers by near-neighbour movements, rather than attempting to minimize overall travel distance. Individuals had variations to a primary sequence, where some bees used a major sequence most often, followed by a minor less used route, and others used two different routes with equal frequency. Even though bees foraging in the spatially randomized array had access to both spatial working memory and scent marks, this manipulation greatly disrupted foraging efficiency, mainly via an increase in revisitation to previously emptied flowers and substantially longer search times. Hence, a stable reference frame greatly improves foraging even for bees in relatively small arrays of flowers.     

Scent-marking behaviour of the honey badger, Mellivora capensis (Mustelidae), in the southern Kalahari

We investigated sexual and seasonal patterns in scent-marking behaviour of the honey badger, by direct observations of habituated individuals (five females, four adult males, two young males). Four categories of scent-marking behaviour were identified: (1) scent marking at latrines; (2) token urination in holes along the foraging path; (3) squat marking at single-use sites; and (4) functional excretion. Females and young males used all four types of scent marking, but adult males were not observed to use token urination. A strategy of hinterland scent marking was used, as was predicted from the large home ranges of both male and female honey badgers. There were significant sexual differences in marking rate: adult males primarily used latrines and adult females favoured token urination. Latrine scent marking in adult male honey badgers provides support for the ‘scent-matching’ hypothesis. Females visited latrines when they were in oestrus. However, the low level of marking activity during a visit and the intensive smelling suggested a scent-matching function rather than reproductive advertisement. Token urination appeared to be related to the maintenance of spatiotemporal separation in females, although we also observed token urination in young males. While the placement of urine in foraging holes and its relation with successful digging attempts offer some support for the foraging efficiency hypothesis, we consider this unlikely, because we did not observe it in adult males and there was no seasonal pattern. Squat marking occurred under a wide range of conditions in both males and females and may be related to marking valuable resources. It is likely that scent marking in honey badgers has many functions.     

Remote perception of floral nectar by bumblebees

Summary On both artificial flowers in the laboratory and certain plant species in the field, bumblebees often closely approached flowers and then departed without probing for nectar. In laboratory experiments where nectar rewards were associated with subtle visual or olfactory cues, bumblebees approached and avoided non-rewarding flowers. Flowers that bees entered and probed for nectar contained rewards much more frequently than predicted by chance alone. When there were no external cues associated with nectar content, bees visited rewarding flowers by chance alone, provided rewarding flowers were not spatially clumped. In the field, bumblebees approached and rejected a large proportion of dogbane flowers and red clover inflorescences. On both species, flowers or inflorescences probed by bees contained more nectar than those rejected by bees or those that I chose at random. On fireweed and monkshood, bees rarely or never approached and rejected healthy-looking flowers. Predictions generated by an optimal foraging model were tested on data from four bumblebee species foraging on red clover. The model was highly successful in qualitatively predicting the relationship between handling time and proportion of inflorescences rejected by individual bees, and the relationship between threshold nectar content for acceptance by bees and average resource availability. Thus, bees appeared to use remotely perceived cues to maximize their rates of nectar intake.     

Trapline foraging by bumble bees: IV. Optimization of route geometry in the absence of competition

Foraging on resources that are fixed in space but that replenishover time, such as floral nectar and pollen, presents animalswith the problem of selecting a foraging route. What can flowervisitors such as bees do to optimize their foraging routes,that is, reduce return time or route distance? Some repeatedlyvisit a set of plants in a significantly predictable sequence(so-called "trapline foraging"), which may also enhance theirforaging efficiency. A moderate level of optimization and repetitionof foraging routes can be reached by following simple movementrules for choosing the distances and turning angles of successiveflights, without the use of spatial memory. If pollinators canlearn the locations of patches and choose among possible foragingroutes or paths, however, even better performance may be achieved.We tested whether and how bumble bees can optimize and repeattheir foraging routes in laboratory experiments with artificialflowers that secreted nectar at a constant rate. With increasingexperience, foraging routes of bees became more repeatable andefficient than expected from a combination of simple movementrules between successive flowers. We suggest that trapline foragingis a more sophisticated pattern of spatial use than searchingand is based on memory. On the other hand, certain spatial configurationsof flowers hampered optimization by the bees; bees preferredto choose short distances over straight moves and showed littleplasticity in this regard. Developing an efficient trapline,therefore, may require prior selection of a set of plants withan appropriate spatial configuration.     

Competition for nectar resources does not affect bee foraging tactic constancy

1. Competition alters animal foraging, including promoting the use of alternative resources. It may also impact how animals feed when they are able to handle the same food with more than one tactic. Competition likely impacts both consumers and their resources through its effects on food handling, but this topic has received little attention. 2. Bees often use two tactics for extracting nectar from flowers: they can visit at the flower opening, or rob nectar from holes at the base of flowers. Exploitative competition for nectar is thought to promote nectar robbing. If so, higher competition among floral visitors should reduce constancy to a single foraging tactic as foragers will seek food using all possible tactics. To test this prediction, field observations and two experiments involving bumble bees visiting three montane Colorado plant species (Mertensia ciliata, Linaria vulgaris, Corydalis caseana) were used under various levels of inter- and intra-specific competition for nectar. 3. In general, individual bumble bees remained constant to a single foraging tactic, independent of competition levels. However, bees that visited M. ciliata in field observations decreased their constancy and increased nectar robbing rates as visitation rates by co-visitors increased. 4. While tactic constancy was high overall regardless of competition intensity, this study highlights some intriguing instances in which competition and tactic constancy may be linked. Further studies investigating the cognitive underpinnings of tactic constancy should provide insight on the ways in which animals use alternative foraging tactics to exploit resources.     

Effects of nectar robbing on nectar dynamics and bumblebee foraging strategies in Linaria vulgaris (Scrophulariaceae)

Differences in morphology among bumblebee species sharing a nectar resource may lead to variation in foraging behaviour and efficiency. Less efficient bumblebees might opportunistically switch foraging strategies from legitimate visitation to secondary robbing when hole-biting primary robbers are present. We observed various aspects of pollination and nectar robbing ecology of Linaria vulgaris in the Colorado Rocky Mountains, with emphasis on the role of bumblebee proboscis length. Bees can extract nectar from a nectar spur legitimately, by entering the front of the flower, or illegitimately, by biting or reusing holes in the spur. Although L. vulgaris flowers are apparently adapted for pollination by long-tongued bees, short-tongued bees visited them legitimately for trace amounts of nectar but switched to secondary robbing in the presence of primary robbers. Longer-tongued bees removed more nectar in less time than did shorter-tongued bees, and were less likely to switch to secondary robbing even when ∼100% of flowers had been pierced. As the proportion of robbed flowers in the population increased, the relative number of legitimate visits decreased while the relative number of robbing visits increased. Robbing decreased nectar standing crop and increased the proportion of empty flowers per inflorescence. Despite these potentially detrimental effects of robbers, differences in inflorescence use among robbers and pollinators, and the placement of holes made by primary robbers, may mitigate negative effects of nectar robbing in L. vulgaris . We discuss some of the reasons that L. vulgaris pollination ecology and growth form might temper the potentially negative effect of nectar robbing.     

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.     

Forage quality and quantity affect red mason bees and honeybees differently in flowers of strawberry varieties

Nectar is a vital source of energy for bees and other pollinators and pollen represents the only source of protein in the diet of bees. Nectar and pollen quality and quantity can therefore affect foraging choices. Strawberry, Fragaria × ananassa (Rosaceae), is a flowering crop that requires insect pollination for the berries to develop optimally. The solitary red mason bee, Osmia bicornis L. (Hymenoptera: Megachilidae), occurs naturally but like the eusocial western honeybee, Apis mellifera mellifera L. (Hymenoptera: Apidae), it is also a commercially reared pollinator used in strawberry production. We hypothesized that strawberry nectar and pollen quality would affect the foraging choice of these two types of bees. In this study nectar and pollen quality is represented by various levels of sugar and protein content, respectively, as well as the number of open strawberry flowers in the experimental field, would affect the foraging choice of these two types of bees. Consistent with previous studies, we found significant and major differences between strawberry varieties in proportions of sucrose in the nectar sugar and in pollen viability – a proxy for pollen protein content. All measured parameters had a significant effect on red mason bee visitation frequency. Contrary to expectations, honeybee foraging behavior was only affected by the number of open flowers and not by any of the quality parameters measured. Our findings indicate that red mason bees were capable of assessing nectar and pollen quality and prioritize accordingly. The pattern observed indicates that individual red mason bees changed foraging focus between strawberry varieties depending on whether nectar or pollen was collected. Our results suggest that targeted breeding of varieties toward high levels of nectar sugar and sucrose concentrations and high pollen protein content may increase pollination success from red mason bees and possibly other solitary bees.