Response of pollinators to the tradeoff between resource acquisition and predator avoidance

Although the behaviour of animals facing the conflicting demands of increasing foraging success and decreasing predation risk has been studied in many taxa, the response of pollinators to variations in both factors has only been studied in isolation. We compared visit rates of two pollinator species, hoverflies and honeybees, to 40 Chrysanthemum segetum patches in which we manipulated predation risk (patches with and without crab spiders) and nectar availability (rich and poor patches) using a full factorial design. Pollinators responded differently to the tradeoff between maximising intake rate and minimising predation risk: honeybees preferred rich safe patches and avoided poor risky patches while the number of hoverflies was highest at poor risky patches. Because honeybees were more susceptible to predation than hoverflies, our results suggest that, in the presence of competition for resources, less susceptible pollinators concentrate their foraging effort on riskier resources, where competition is less severe. Crab spiders had a negative effect on the rate at which inflorescences were visited by honeybees. This effect was mediated through changes in the foraging strategy of honeybees, and could, in principle, be reversed by increasing nectar productivity of inflorescences. Our study shows that both pollinator species responded simultaneously and differently to variations in food reward and predation risk, and highlights the importance of studying the foraging strategies of pollinators in order to fully understand how plant–pollinator interactions are established.     

Spider movement, UV reflectance and size, but not spider crypsis, affect the response of honeybees to Australian crab spiders

According to the crypsis hypothesis, the ability of female crab spiders to change body colour and match the colour of flowers has been selected because flower visitors are less likely to detect spiders that match the colour of the flowers used as hunting platform. However, recent findings suggest that spider crypsis plays a minor role in predator detection and some studies even showed that pollinators can become attracted to flowers harbouring Australian crab spider when the UV contrast between spider and flower increases. Here we studied the response of Apis mellifera honeybees to the presence of white or yellow Thomisus spectabilis Australian crab spiders sitting on Bidens alba inflorescences and also the response of honeybees to crab spiders that we made easily detectable painting blue their forelimbs or abdomen. To account for the visual systems of crab spider's prey, we measured the reflectance properties of the spiders and inflorescences used for the experiments. We found that honeybees did not respond to the degree of matching between spiders and inflorescences (either chromatic or achromatic contrast): they responded similarly to white and yellow spiders, to control and painted spiders. However spider UV reflection, spider size and spider movement determined honeybee behaviour: the probability that honeybees landed on spider-harbouring inflorescences was greatest when the spiders were large and had high UV reflectance or when spiders were small and reflected little UV, and honeybees were more likely to reject inflorescences if spiders moved as the bee approached the inflorescence. Our study suggests that only the large, but not the small Australian crab spiders deceive their preys by reflecting UV light, and highlights the importance of other cues that elicited an anti-predator response in honeybees.     

Crab spiders (Thomisidae) attract insect flower‐visitors without UV signalling

1. Crab spiders (Thomisidae) indirectly affect insect flower‐visitor and flowering plant interactions by consuming and altering the behaviour of insects. 2. Although one expects insect flower‐visitors to avoid crab spiders actively, some crab spider species are known to attract flower‐visitors. Crab spiders may use UV signalling to lure potential prey to the flowers they occupy. 3. In the present study, a field experiment was conducted to examine the effects of crab spiders occupying three prairie plant species for the insect flower‐visitor community. Pollinating insects were significantly attracted to inflorescences with crab spiders compared to inflorescences without crab spiders for two plant species, and herbivorous insects were attracted to inflorescences with crab spiders for one of these plant species. The two flowering plant species with increased pollinator visitation showed increased seed weights for plants with crab spiders, indicating crab spider presence indirectly increased pollination. 4. To test the UV signalling hypothesis, inflorescences with crab spiders of one plant species were observed under both a UV‐blocking plastic and a clear plastic control. Contrary to our prediction, flower‐visitors were not more likely to land on inflorescences under the clear plastic; the UV signalling hypothesis was not supported. Other unknown explanations underlie prey attraction to inflorescences with crab spiders.     

Evidence for UV-based sensory exploitation in Australian but not European crab spiders

Some crab spiders reflect UV-light, thereby creating a deceptive signal that attracts prey to the flowers that they sit on. We conducted a survey of several Australian and European species of crab spiders and found that UV-reflection is common in Australian species but absent from European species. Furthermore, honeybees are attracted to UV-reflecting Australian spiders while they are either indifferent to or repelled by European crab spiders. We do not know if UV-reflection evolved once or several times independently in crab spiders endemic to Australia or whether UV-reflective spiders arrived in Australia more recently.     

Predator crypsis enhances behaviourally mediated indirect effects on plants by altering bumblebee foraging preferences

Predators of pollinators can influence pollination services and plant fitness via both consumptive (reducing pollinator density) and non-consumptive (altering pollinator behaviour) effects. However, a better knowledge of the mechanisms underlying behaviourally mediated indirect effects of predators is necessary to properly understand their role in community dynamics. We used the tripartite relationship between bumblebees, predatory crab spiders and flowers to ask whether behaviourally mediated effects are localized to flowers harbouring predators, or whether bees extend their avoidance to entire plant species. In a tightly controlled laboratory environment, bumblebees (Bombus terrestris) were exposed to a random mixture of equally rewarding yellow and white artificial flowers, but foraging on yellow flowers was very risky: bees had a 25 per cent chance of receiving a simulated predation attempt by ‘robotic’ crab spiders. As bees learnt to avoid ‘dangerous’ flowers, their foraging preferences changed and they began to visit fewer yellow flowers than expected by chance. Bees avoided spider-free yellow flowers as well as dangerous yellow flowers when spiders were more difficult to detect (the colour of yellow spiders was indistinguishable from that of yellow flowers). Therefore, this interaction between bee learning and predator crypsis could lead flower species harbouring cryptic predators to suffer from reduced reproductive success.     

Crab spiders deter insect visitations to slickspot peppergrass flowers

Insects visiting the flowers of slickspot peppergrass, Lepidium papilliferum (Brassicaceae), risk predation by crab spiders, Misumena vatia (Thomisidae). In a field study conducted at two sites in southwestern Idaho, 7.5±2.7% of L. papilliferum plants (range 0–30%, N=16 surveys of up to 40 randomly selected plants) harbored a crab spider. However, through 205 minutes of observations at plants with a spider, only 15 predation attempts were observed, with only 3 of those being successful. Despite the relatively low incidence of predation by crab spiders, an experiment revealed that the number of insects visiting L. papilliferum flowers was significantly lower at plants that harbored a crab spider than at plants free of spiders. In another experiment, floral visits increased significantly following the removal of crab spiders from individual plants. The deterrent effect of spiders was not due to a disproportionate avoidance response by certain types of insects; all insect families included in our analysis showed decreases in visitations to flowers when spiders were present, although none of these differences were statistically significant at the individual level. We found no significant change in the duration of visits to plants harboring a spider, implying either that the visitors were oblivious to the predator's presence, or that they were aware of the predator but kept their distance. Our study is one of a growing number to find a decrease in floral visits in response to predators, suggesting that the phenomenon is more widespread than was previously recognized.     

Honeybees enhance reproduction without affecting the outcrossing rate in endemic Pedicularis densispica (Orobanchaceae)

There has been substantial debate in recent years surrounding the impact of introduced honeybees on native biota. This study reports on an investigation of Pedicularis densispica, a subalpine annual herb endemic to Southwest China, in an attempt to determine the impact of introduced domestic honeybees on pollen dispersal and thus on their reproductive success and mating system. Honeybees were introduced into the study site in 2004, and a sudden seasonal pollinator shift from bumblebees to honeybees was observed. Intra- and inter-plant visits by different pollinators were recorded in the field in 2003 and 2004. Fruit and seed sets prior to and after the pollinator shift were measured. Experimental pollinations were performed to characterize the breeding system. Outcrossing rates at the seed stage were estimated for both years using RAPD markers. Our results indicated that honeybees foraged between plants more frequently than bumblebees did. Our results also revealed that the introduction of honeybees significantly enhanced reproductive success. However, no significant difference was detected between the outcrossing rates due to bumblebee and honeybee pollination. P. densispica was almost completely outcrossing ( T(m) = 0.956 and 0.967, respectively in 2003 and 2004) but partially self-compatible. This study presents the first report of the outcrossing rate in the genus pedicularis and reveals a limited influence of pollination on the mating system in P. densispica. The pollinator shift did not reduce reproductive success of the plants and honeybees may be used to augment pollinator services for nectariferous P. densispica.     

A meta-analysis of predation risk effects on pollinator behaviour

Flower-visiting animals are constantly under predation risk when foraging and hence might be expected to evolve behavioural adaptations to avoid predators. We reviewed the available published and unpublished data to assess the overall effects of predators on pollinator behaviour and to examine sources of variation in these effects. The results of our meta-analysis showed that predation risk significantly decreased flower visitation rates (by 36%) and time spent on flowers (by 51%) by pollinators. The strength of the predator effects depended neither on predator taxa and foraging mode (sit-and-wait or active hunters) nor on pollinator lifestyle (social vs. solitary). However, predator effects differed among pollinator taxa: predator presence reduced flower visitation rates and time spent on flowers by Squamata, Lepidoptera and Hymenoptera, but not by Diptera. Furthermore, larger pollinators showed weaker responses to predation risk, probably because they are more difficult to capture. Presence of live crab spiders on flowers had weaker effects on pollinator behaviour than presence of dead or artificial crab spiders or other objects (e.g. dead bees, spheres), suggesting that predator crypsis may be effective to some extent. These results add to a growing consensus on the importance of considering both predator and pollinator characteristics from a community perspective.     

Impact of flower-dwelling crab spiders on plant-pollinator mutualisms

Indirect effects in interactions occur when a species influences a third species by modifying the behaviour of a second one. It has been suggested that indirect effects of crab spiders (Thomisidae) on pollinator behaviour can cascade down the food web and negatively affect plant fitness. However, it is poorly understood how different pollinator groups react to crab spiders and, thus, when a reduction in plant fitness is likely to occur. Using continuous video surveillance, we recorded the behaviour of pollinators on two flower species and the pollinators’ responses to three crab spider treatments: inflorescences (1) with a pinned dried spider, (2) with a spider model made of paper, and (3) without spiders (control). We found that pollinators avoided inflorescences with dried spiders only on one plant species (Anthemis tinctoria). Pollinators showed no significant avoidance of paper spiders. Honeybees and bumblebees did not react to dried spiders, but solitary bees and syrphid flies showed a strong avoidance. Finally, we found no evidence that inflorescences with dried spiders suffered from a decrease in fitness in terms of a reduced seed set. We hypothesise that top-down effects of predators on plants via pollinators depend on the degree of specialisation of pollinators and their tendency to avoid spiders.     

Do ambush predators prefer rewarding or non‐rewarding orchid inflorescences?

Previous research has shown that the presence of a reward on average doubles reproductive success in orchids by correspondingly increasing the frequency of pollinator visitations. We examined whether such reward-induced increases have a downstream effect on the behaviour of ambush predators concealed in orchid inflorescences, extending observations begun at Downe by Charles Darwin. Specifically, we studied three orchid-rich sites in southern England, in order to compare the occurrence of crab spiders on three coexisting species of terrestrial orchids: the nectariferous Gymnadenia conopsea versus the nectar-less Dactylorhiza fuchsii and Anacamptis pyramidalis . No significant difference was observed between rewarding and non-rewarding inflorescences at Risborough, whereas at Aston Clinton the nectar-less species supported significantly more crab spiders, albeit mainly in relatively short grass. Comparison of the two non-rewarding species present at Downe approximated a significant preference by the spiders for Anacamptis , which more closely resembles the rewarding Gymnadenia . The presence of a floral reward does not result in a higher frequency of crab spiders. We speculate that concealment quality of the inflorescence, the nature of the dominant pollinator(s), and/or ease of movement of spiders between inflorescences may be more important than frequency of visits by potential prey, particularly when no other form of concealment is readily available.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 763–771.     

Flower Symmetry Preferences in Honeybees and their Crab Spider Predators

Flowers exhibit symmetrical patterns, and innate preferences for symmetry in pollinators like honeybees are documented. Most previous studies of symmetry preferences in honeybees, Apis mellifera, tested levels of asymmetry using artificial flowers or stimuli. Here we investigated the effect of flower asymmetry on flower preferences of honeybees in a novel approach using real flowers, incorporating their spectral properties and how the receivers process the visual signals. Importantly, we also tested the response of an ‘eavesdropping’ predator, the crab spider Thomisus spectabilis, that also utilizes the same flower to prey on honeybees. Flowers (Chrysanthemum frutescens) were manipulated to contain asymmetrical and symmetrical patterns, excluding olfactory cues. Both crab spiders and honeybees exhibited a significant preference for symmetrical flowers. Moreover, honeybees exhibited a significant preference for radial symmetry over bilateral symmetry, but no corresponding effect was recorded in crab spiders. Further analyses demonstrated that flower reflectance and orientation of the axis of symmetry did not affect crab spider decisions. Field observations on T. spectabilis revealed that the natural variation in C. frutescens symmetry had no effect on the choice of crab spiders. This indicates that spiders and honeybees may use other flower characteristics, for example, olfactory cues, together with flower symmetry, to make their foraging decisions.     

Pollinator community responses to the spatial population structure of wild plants: A pan-European approach

Land-use changes can alter the spatial population structure of plant species, which may in turn affect the attractiveness of flower aggregations to different groups of pollinators at different spatial scales. To assess how pollinators respond to spatial heterogeneity of plant distributions and whether honeybees affect visitation by other pollinators we used an extensive data set comprising ten plant species and their flower visitors from five European countries. In particular we tested the hypothesis that the composition of the flower visitor community in terms of visitation frequencies by different pollinator groups were affected by the spatial plant population structure, viz. area and density measures, at a within-population (‘patch’) and among-population (‘population’) scale. We found that patch area and population density were the spatial variables that best explained the variation in visitation frequencies within the pollinator community. Honeybees had higher visitation frequencies in larger patches, while bumblebees and hoverflies had higher visitation frequencies in sparser populations. Solitary bees had higher visitation frequencies in sparser populations and smaller patches. We also tested the hypothesis that honeybees affect the composition of the pollinator community by altering the visitation frequencies of other groups of pollinators. There was a positive relationship between visitation frequencies of honeybees and bumblebees, while the relationship with hoverflies and solitary bees varied (positive, negative and no relationship) depending on the plant species under study. The overall conclusion is that the spatial structure of plant populations affects different groups of pollinators in contrasting ways at both the local (‘patch’) and the larger (‘population’) scales and, that honeybees affect the flower visitation by other pollinator groups in various ways, depending on the plant species under study. These contrasting responses emphasize the need to investigate the entire pollinator community when the effects of landscape change on plant–pollinator interactions are studied.     

Seasonal variation in exploitative competition between honeybees and bumblebees

Honeybees (Apis mellifera) and bumblebees (Bombus spp.) often undergo exploitative competition for shared floral resources, which can alter their foraging behaviour and flower choice, even causing competitive exclusion. This may be strongest in summer, when foraging conditions are most challenging for bees, compared to other times of the year. However, the seasonal dynamics of competition between these major pollinator groups are not well understood. Here, we investigate whether the strength of exploitative competition for nectar between honeybees and bumblebees varies seasonally, and whether competitive pressure is greatest in summer months. We carried out experimental bee exclusion trials from May to late September, using experimental patches of lavender, variety Grosso, in full bloom. In each trial, we compared the numbers of honeybees (HB) foraging on patches from which bumblebees had been manually excluded (bumblebee excluded, BBE) versus control (CON) patches, HB(BBE-CON). This measure of exploitative competition varied significantly with season. As expected, mean HB(BBE-CON) was significantly greater in summer trials than in spring or autumn trials. This was despite high nectar standing crop volumes in BBE patch flowers in spring and autumn trials. Mean HB(BBE-CON) was not different between spring and autumn trials. Our results show that nectar competition between honeybees and bumblebees varies seasonally and is stronger in summer than spring or autumn, adding to current understanding of the seasonality of resource demand and competition between bee species. This information may also help to inform conservation programs aiming to increase floral resources for bees by showing when these resources are most needed.     

Evidence for competition between honeybees and bumblebees; effects on bumblebee worker size

Numerous studies suggest that honeybees may compete with native pollinators where introduced as non-native insects. Here we examine evidence for competition between honeybees and four bumblebee species in Scotland, a region that may be within the natural range of honeybees, but where domestication greatly increases the honeybee population. We examined mean thorax widths (a reliable measure of body size) of workers of Bombus pascuorum, B. lucorum, B. lapidarius and B. terrestris at sites with and without honeybees. Workers of all four species were significantly smaller in areas with honeybees. We suggest that reduced worker size is likely to have implications for bumblebee colony success. These results imply that, for conservation purposes, some restrictions should be considered with regard to placing honeybee hives in or near areas where populations of rare bumblebee species persist.     

Increased bumblebee abundance along the margins of a mass flowering crop: evidence for pollinator spill‐over

Although the practice of cultivating mass flowering crops (MFCs) is seen as a means of counteracting the widespread decline of insect pollinators, no study to‐date has evaluated whether the increased pollinator abundance associated with MFCs influences pollinator visits to assemblages of adjacent native, non‐crop plant species (pollinator ‘spill‐over’). In this study we quantified bumblebee abundance along hedgerow transects in MFC (field bean) vs non‐MFC (wheat) margins. Surveys were conducted on east and west‐facing margins twice daily (morning and afternoon) for three or four days during the main MFC flowering period (June) over four years involving paired bean and wheat fields in Devon and Cornwall, southwest England. Although no single bumblebee species showed any consistent change in relative frequency, when taken across all years and bumblebee species combined, we observed twice as many bumblebees visiting flowers adjacent to the MFC. However, when we compared bumblebee activity along hedgerow transects two weeks after bean flowering, there was no difference between crops. We thus conclude that although there is evidence for pollinator spill‐over from the bean MFC to nearby semi‐natural habitat, the effect is comparatively short lived and not specific to any single bumblebee species. We also suggest that while pollinator services to native plant species might be briefly enhanced by MFC cultivation, the possible repercussions of bumblebee spill‐over from MFCs to semi‐natural habitats and the other pollinator groups they support should be evaluated before MFC cultivation is considered as a means of conserving declining bumblebee populations.     

Foraging habitats and foraging distances of bumblebees, Bombus spp. (Hym., Apidae), in an agricultural landscape

Abstract: In selected foraging habitats of an agricultural landscape flower visits of bumblebees and community structure of foraging bumblebees were studied, with special regard to the role of crops as super-abundant resources. Most crops represent temporal foraging habitats with high abundance of bumblebees but mainly with low diversity in the bumblebee forage community, in contrast to permanent foraging habitats such as, for example, a hedgerow. The high numbers of bumblebees in the monoculture of crop plantations consisted mainly of short-tongued bumblebee species. The role of foraging distances for the visitation rate of foraging habitats was studied by performing capture–recapture experiments with natural nests of Bombus terrestris , Bombus lapidarius and Bombus muscorum . Differences were found on the species as well as the individual level. The foraging distances of B. muscorum were more restricted to the neighbourhood of the nesting habitat than the foraging activity of B. terrestris and B. lapidarius . High percentages of B. terrestris workers were recaptured while foraging on super-abundant resources in distances up to 1750 m from the nest. Isolated patches of highly rewarding forage crops, in agricultural landscapes, are probably only accessed by bumblebee species with large mean foraging distances, such as the short-tongued B. terrestris . Species like the rare, long-tongued B. muscorum depend on a close connection between nesting and foraging habitat. A restricted foraging radius might be one important factor of bumblebee species loss and potential pollinator limitation in modern agricultural landscapes. Furthermore, long-distance flights of bumblebee pollinators have to be considered in the present discussion on gene flow from transgenic plant species on a landscape scale.     

Exploitation of floral signals by crab spiders (Thomisus spectabilis, Thomisidae)

Flowers exhibit characteristics through which they exploit thesensory biases of pollinating insects, and both signaler andreceiver benefit from this interaction, either through reproductiveservice or food reward. However, the preferences of pollinatorsfor certain flower traits such as color or odor might be exploitedby predators that target pollinating insects. Crab spiders,Thomisus spectabilis, position themselves on flowers to preyon pollinators such as honeybees, Apis mellifera. We gave bothhoneybees and crab spiders the choice between two randomly chosenwhite Chrysanthemum frutescens, including olfactory signalsin one experiment and excluding odor in a second experiment.When olfactory signals were included, crab spiders and honeybeesclearly preferred the same flower out of a pair. However, agreementlevel was at chance in the absence of olfactory signals. Wealso analyzed the visual flower characteristics that might influencethe decision of the animals. Neither the size of flowers (diameterof flower and diameter of reproductive flower center) nor thereflectance properties (receptor excitation values in ultraviolet,blue, and green; overall brightness) influenced the choicesof crab spiders and honeybees. Therefore, odor seems to be thefloral signal that bees use to identify high-quality flowersand that crab spiders exploit to encounter honeybees.     

The making of eusociality: insights from two bumblebee genomes

The genomes of two bumblebee species characterized by a lower level of sociality than ants and honeybees provide new insights into the origin and evolution of insect societies.     

The effect of colour variation in predators on the behaviour of pollinators: Australian crab spiders and native bees

1. Australian crab spiders exploit the plant–pollinator mutualism by reflecting UV light that attracts pollinators to the flowers where they sit. However, spider UV reflection seems to vary broadly within and between individuals and species, and we are still lacking any comparative studies of prey and/or predator behaviour towards spider colour variation. 2. Here we looked at the natural variation in the coloration of two species of Australian crab spiders, Thomisus spectabilis and Diaea evanida, collected from the field. Furthermore, we examined how two species of native bees responded to variation in colour contrast generated by spiders sitting in flowers compared with vacant flowers. We used data from a bee choice experiment with D. evanida spiders and Trigona carbonaria bees and also published data on T. spectabilis spiders and Austroplebeia australis bees. 3. In the field both spider species were always achromatically (from a distance) undetectable but chromatically (at closer range) detectable for bees. Experimentally, we showed species‐specific differences in bee behaviour towards particular spider colour variation: T. carbonaria bees did not show any preference for any colour contrasts generated by D. evanida spiders but A. australis bees were more likely to reject flowers with more contrasting T. spectabilis spiders. 4. Our study suggests that some of the spider colour variation that we encounter in the field may be partly explained by the spider's ability to adjust the reflectance properties of its colour relative to the behaviour of the species of prey available.     

The effects of predation risk from crab spiders on bee foraging behavior

Recent studies have suggested that top–down effects ofpredation on plant–pollinator interactions may not be,as previously thought, rare and/or weak. In this paper, we explorethe effects of crab spiders (Araneae: Thomisidae) on the behaviorof 2 species of bee (Hymenoptera: Apidae) foraging for nectarand pollen on 3 different plant species in central Portugal.In 2 experiments, we found that the eusocial bee Apis melliferawas significantly less likely to inspect and accept a floweror inflorescence if it harbored a spider. In contrast, we foundno such effects of spiders on the behavior of the solitary beeEucera notata. Further experiments showed that the effects ofenvironmental cues associated with predators on flower visitationby A. mellifera were detectable even when no spider was presentat the moment a flower was encountered. Such indirect effectswere only identified, however, in bees foraging on 1 of 2 plantspecies studied. In a final experiment, A. mellifera was shownto respond negatively to the presence of the corpses of conspecificsglued to flowers. This suggests that prey corpses left exposedon petals or bracts by spiders provide an obvious cue that beescan use to avoid predators. These results add to a growing bodyof evidence that plant–pollinator interactions are notimmune to the effects of predation and suggest that the strengthof such effects vary both between and within species.