Foraging strategy predicts foraging economy in a facultative secondary nectar robber

In mutualistic interactions, the decision whether to cooperate or cheat depends on the relative costs and benefits of each strategy. In pollination mutualisms, secondary nectar robbing is a facultative behavior employed by a diverse array of nectar‐feeding organisms, and is thought to be a form of cheating. Primary robbers create holes in floral tissue through which they feed on nectar, whereas secondary robbers, which often lack chewing mouthparts, feed on nectar through existing holes. Because primary robbers make nectar more readily available to secondary robbers, primary robbers facilitate the behaviors of secondary robbers. However, the net effect of facilitation on secondary robber fitness has not been empirically tested: it is unknown whether the benefit secondary robbers receive is strong enough to overcome the cost of competing with primary robbers for a shared resource. We conducted foraging experiments using the bumble bee Bombus bifarius, which can alternatively forage ‘legitimately’ (from the floral opening) or secondary‐rob. We measured the relative foraging efficiencies (handling time per flower, flowers visited per minute, proportion of foraging bout spent consuming nectar) of these alternative behaviors, and tested whether the frequency of primary robbing and nectar standing crop in primary‐robbed flowers of Linaria vulgaris (Plantaginaceae) affected foraging efficiency. Surprisingly, there was no effect of primary robbing frequency on the foraging efficiency of secondary‐robbing B. bifarius. Instead, foraging strategy was a major predictor of foraging efficiency, with legitimate foraging being significantly more efficient than secondary robbing. Legitimate foraging was the more common strategy used by B. bifarius in our study; however, it is rarely used by B. bifarius foraging on L. vulgaris in nature, despite indications that it is more efficient. Our results suggest the need for deeper investigations into why bees adopt secondary robbing as a foraging strategy, specifically, the environmental contexts that promote the behavior.     

Pollination ecology of Anthyllis vulneraria subsp. vulgaris (Fabaceae): nectar robbers as pollinators

This paper examines the hypothesis that nectar robbing can affect plant reproductive success either positively or negatively. To this end, I investigated various aspects of the pollination ecology of a population of the herb Anthyllis vulneraria subsp. vulgaris in northwest Spain over 5 yr. By observing floral visitors, I found that the most important pollinator species was the long-tongued bee Anthophora acervorum, which accounted for ～45% of recorded insect visits. However, just over 45% of visits were by the nectar-robbing bumble bees Bombus terrestris and B. jonellus. Although the incidence of robbing differed considerably over 5 yr of study, the frequency in every season was very high (66.4-76.5% of robbing) except for 1997 (0% robbing). Despite this high frequency of robbing, robbed flowers had a higher probability of setting fruit than nonrobbed flowers in all years of the study (mean: 82.0 vs. 51.0%; excluding 1997). This increased fruit set in robbed flowers is directly related to bumble bee behavior because the robbers' bodies came into contact with both the anthers and stigmas while robbing. Thus, the robbers effect pollination. These results suggest that the effect of nectar robbers on plant reproductive success is dependent both on the robbers' behavior and on flower/inflorescence structure. The importance of nectar-robbing bumble bees on the reproductive success of A. vulneraria and its yearly high frequency suggest that the relationship between robbers and this plant is part of a successful long-term mutualism.     

大和切叶蜂对其蜜源植物披针叶黄华的盗蜜行为

【目的】调查和观测内蒙古毛乌素沙地大和切叶蜂Megachile (Xanthosaurus) japonica Alfken对其蜜源植物披针叶黄华Thermopsis lupinoides (L.)的盗蜜行为。【方法】在披针叶黄华花期内, 设置样方观测披针叶黄华的主要访花昆虫。采用目测, 拍照等方法对大和切叶蜂盗蜜行为进行观测, 记录和统计花被盗蜜后留下的盗蜜孔的数量和在花上的位置。【结果】大和切叶蜂在披针叶黄华传粉蜂中数量上占有绝对的优势。作为初级盗蜜者时, 用上颚在花基部切割出一个纵向裂口, 将口器伸入孔内吸取花蜜。作为次级盗蜜者时, 利用已有的孔洞来吸蜜。在盗蜜时没有表现出寻找已经存在的盗蜜孔来吸蜜的现象, 同时其个体在盗蜜时表现出“偏好”花基部一侧的行为。在13个样地, 已开放花朵被盗蜜率最低为95.4%, 最高达到100%, 而未开放花朵的被盗蜜率最高则达到64.7%。【结论】在毛乌素沙地大和切叶蜂既是披针叶黄华的主要传粉者, 也是其初级盗蜜者和次级盗蜜者。     

Pollinators shift to nectar robbers when florivory occurs,with effects on reproductive success in Iris bulleyana (Iridaceae)

• Studies have indicated that florivory and nectar robbing may reduce reproductive success of host plants. However, whether and how these effects might interact when plants are simultaneously attacked by both florivores and nectar robbers still needs further investigation.
• We used Iris bulleyana to detect the interactions among florivory, nectar robbing and pollination, and moreover, their effects on plant reproductive success. Field investigations and hand‐pollination treatments were conducted on two experimental plots from a natural population, in which Experimental plot was protected from florivores and Control plot was not manipulated.
• The flower calyx was bitten by sawflies to consume the nectary, and three bumblebee species were pollinators. In addition, the short‐tongued pollinator, Bombus friseanus, was the only robber when there was a hole made by a sawfly. The bumblebee had significantly shortened flower handling time when robbing, as compared to legitimate visits. Pollinator visitation and seed production decreased significantly in damaged flowers. However, seed production per flower after supplementary hand‐pollination did not differ significantly between damaged and undamaged flowers. Compared to the Experimental plot, bumblebees visited fewer flowers per plant in a foraging bout in the Control plot.
• The flowers damaged by florivory allowed B. friseanus to shift to a nectar robber. Florivory and nectar robbing collectively decreased plant reproductive success by consuming nectar resources, which may reduce attractiveness to pollinators of the damaged flowers. However, the changes in pollinator behaviour might be beneficial to the plant by reducing the risk of geitonogamous mating.

     

Pollinators and nectar robbers cause directional selection for large spur circle in Impatiens oxyanthera (Balsaminaceae)

Nectar spurs have an important role in floral evolution and plant–pollinator coadaptation. The flowers of some species possess spurs curving into a circle. However, it is unclear whether spur circle diameter is under direct selection pressure from different sources, such as pollinators and nectar robbers. In this study, we quantified selection on some floral traits, such as spur circle diameter in Impatiens oxyanthera (Balsaminaceae) using phenotypic selection analysis and compared the relative importance of pollinators and nectar robbers as selective agents using mediation analysis. The study showed that pollinators caused significant selection on corolla length, spur curvature and spur circle diameter while nectar robbers only imposed strong selection on spur circle diameter. Pollinators favored flowers with large corolla, curly spurs and large spur circle while nectar robbers preferred flowers with small spur circle. More pollinator visits resulted in higher female reproductive success, while robbery reduced female fitness. Conflicting selection on spur traits from pollinators and nectar robbers was not found. Mediation analysis showed that selection on floral traits through nectar robbing was stronger than selection through pollination. The results suggested that pollinators and nectar robbers jointly mediated the directional selection for large spur circle, and nectar robbers caused stronger selection than pollinators on floral traits.     

Pollination in Jacaranda rugosa (Bignoniaceae): euglossine pollinators, nectar robbers and low fruit set

Nectar robbers access floral nectar in illegitimate flower visits without, in general, performing a pollination service. Nevertheless, their effect on fruit set can be indirectly positive if the nectar removal causes an incremental increase in the frequency of legitimate flower visits of effective pollinators, especially in obligate outcrossers. We studied pollination and the effect of nectar robbers on the reproductive fitness of Jacaranda rugosa , an endemic shrub of the National Park of Catimbau, in the Caatinga of Pernambuco, Brazil. Xenogamous J . rugosa flowers continuously produced nectar during the day at a rate of 1 μl·h⁻¹. Female and male Euglossa melanotricha were the main pollinators. Early morning flower visits substantially contributed to fruit set because stigmas with open lobes were almost absent in the afternoon. Ninety-nine per cent of the flowers showed damage caused by nectar robbers. Artificial addition of sugar water prolonged the duration of flower visits of legitimate flower visitors. Removal of nectar, simulating the impact of nectar robbers, resulted in shorter flower visits of euglossine bees. While flower visits of nectar-robbing carpenter bees ( Xylocopa frontalis , X . grisescens, X . ordinaria) produced only a longitudinal slit in the corolla tube in the region of the nectar chamber, worker bees of Trigona spinipes damaged the gynoecium in 92% of the flowers. This explains the outstandingly low fruit set (1.5%) of J. rugosa in the National Park of Catimbau.     

Variation in composition of two bumble bee species across communities affects nectar robbing but maintains pollinator visitation rate to an alpine plant,Salvia przewalskii

1. In many flowering plants, bumble bees may forage as both pollinators and nectar robbers. This mixed foraging behaviour may be influenced by community context and consequently, potentially affect pollination of the focal plant. 2. Salvia przewalskii is both pollinated and robbed exclusively by bumble bees. In the present study area, it was legitimately visited by two species of bumble bees with different tongue length, Bombus friseanus and Bombus religiosus, but it was only robbed by Bombus friseanus, the shorter‐tongued bumble bee. The intensity of nectar robbing and pollinator visitation rate to the plant were investigated across 26 communities in the Hengduan Mountains in East Himalaya during a 2‐year project. For each of these communities, the floral diversity, and the population size and floral resource of S. przewalskii were quantified. The abundances of the two bumble bee species were also recorded. 3. Both nectar robbing and pollinator visitation rate were influenced by floral diversity. However, pollinator visitation rate was not affected by nectar robbing. The results revealed that relative abundance of the two bumble bee species significantly influenced the incidence of nectar robbing but not the pollinator visitation rate. Increased abundance of B. religiosus, the legitimate visitors, exacerbated nectar robbing, possibly by causing B. friseanus to shift to robbing; however, pollinator visitation remained at a relatively high level. 4. The results may help to explain the persistence of both nectar robbing and pollination, and suggest that, in comparison to pollination, nectar robbing is a more unstable event in a community.     

Nectar robbery by bees Xylocopa virginica and Apis mellifera contributes to the pollination of rabbiteye blueberry

Honey bees, Apis mellifera L., probe for nectar from robbery slits previously made by male carpenter bees, Xylocopa virginica (L.), at the flowers of rabbiteye blueberry, Vaccinium ashei Reade. This relationship between primary nectar robbers (carpenter bees) and secondary nectar thieves (honey bees) is poorly understood but seemingly unfavorable for V. ashei pollination. We designed two studies to measure the impact of nectar robbers on V. ashei pollination. First, counting the amount of pollen on stigmas (stigmatic pollen loading) showed that nectar robbers delivered fewer blueberry tetrads per stigma after single floral visits than did our benchmark pollinator, the southeastern blueberry bee, Habropoda laboriosa (F.), a recognized effective pollinator of blueberries. Increasing numbers of floral visits by carpenter bee and honey bee robbers yielded larger stigmatic loads. As few as three robbery visits were equivalent to one legitimate visit by a pollen-collecting H. laboriosa female. More than three robbery visits per flower slightly depressed stigmatic pollen loads. In our second study, a survey of 10 commercial blueberry farms demonstrated that corolla slitting by carpenter bees (i.e., robbery) has no appreciable affect on overall V. ashei fruit set. Our observations demonstrate male carpenter bees are benign or even potentially beneficial floral visitors of V ashei. Their robbery of blueberry flowers in the southeast may attract more honey bee pollinators to the crop.     

Visual signalling of nectar‐offering flowers and specific morphological traits favour robust bee pollinators in the mass‐flowering tree Handroanthus impetiginosus (Bignoniaceae)

Mass flowering is a widespread blooming strategy among Neotropical trees that has been frequently suggested to increase geitonogamous pollination. We investigated the pollination ecology of the mass‐flowering tree Handroanthus impetiginosus, addressing its breeding system, the role in pollination of different visitors, the impact of nectar robbers on fruit set and the function of colour changes in nectar guides. This xenogamous species is mainly pollinated by Centris and Euglossa bees (Apidae) seeking nectar, which are known to fly long distances. The flowers favour these bees by having: (1) a closed entrance in newly opened flowers which provides access only to strong bees capable of deforming the flower tube; and (2) a nectar chamber that is accessible only to long‐tongued bees. Only first‐day flowers with yellow nectar guides produce nectar. Pollinators prefer these flowers over second‐ and third‐day flowers with orange and red nectar guides, respectively. Nectar robbers damage two‐thirds of the flowers and this robbing activity decreases fruit set by half. We attribute the low fruit set of H. impetiginosus to the intense nectar robbing and hypothesize that visual signalling of nectar presence in newly opened (receptive) flowers reduces geitonogamy by minimizing bee visits to unrewarding (non‐receptive) flowers. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 176 , 396–407.     

Novel nectar robbing negatively affects reproduction in Digitalis purpurea

With many plant–pollinator interactions undergoing change as species’ distributions shift, we require a better understanding of how the addition of new interacting partners can affect plant reproduction. One such group of floral visitors, nectar robbers, can deplete plants of nectar rewards without contributing to pollination. The addition of nectar robbing to the floral visitor assemblage could therefore have costs to the plant´s reproductive output. We focus on a recent plant colonist, Digitalis purpurea, a plant that in its native range is rarely robbed, but experiences intense nectar robbing in areas it has been introduced to. Here, we test the costs to reproduction following experimental nectar robbing. To identify any changes in the behavior of the principal pollinators in response to nectar robbing, we measured visitation rates, visit duration, proportion of flowers visited, and rate of rejection of inflorescences. To find the effects of robbing on fitness, we used proxies for female and male components of reproductive output, by measuring the seeds produced per fruit and the pollen export, respectively. Nectar robbing significantly reduced the rate of visitation and lengths of visits by bumblebees. Additionally, bumblebees visited a lower proportion of flowers on an inflorescence that had robbed flowers. We found that flowers in the robbed treatment produced significantly fewer seeds per fruit on average but did not export fewer pollen grains. Our finding that robbing leads to reduced seed production could be due to fewer and shorter visits to flowers leading to less effective pollination. We discuss the potential consequences of new pollinator environments, such as exposure to nectar robbing, for plant reproduction.     

Pollination Ecology and Effect of Nectar Removal in Macleania bullata (Ericaceae)1

The floral syndrome of Macleania bullataYeo (Ericaceae) reflects its adaptation to hummingbird pollination. Its flowers, however, are subject to high levels of nectar robbing. I examined the floral visitor assemblage of M. bullata in a tropical montane wet forest in southwestern Colombia, focusing on the behavior of the visitors. I also tested for the presence of nocturnal pollination and the effects of nectar removal on new nectar production. The principal floral visitors were the nectar robbing hummingbirds Ocreatus underwoodii (19.1% of visits) and Chlorostilbon mellisugus (18.9%). Only two species of long–billed hummingbirds visited the flowers of M. bullata as “legitimate” pollinators: Coeligena torquata (14.7% of visits) and Doryfera ludoviciae (14.3%). The remaining visits constituted nectar robbing by bees, butterflies, and other species of hummingbirds. Nocturnal pollination took place, although fruit set levels were 2.4 times higher when only diurnal pollination was allowed as opposed to exclusively nocturnal pollination. Nectar robbers removed floral nectar without pollinating the flower. Treatments of experimental nectar removal were carried out to examine if flowers synthesize more nectar after nectar removal. Nectar removal increased the total volume of nectar produced by each flower without affecting sugar concentration. Thus, nectar robbing can impose a high cost to the plants by forcing them to replace lost nectar.     

Visitation rate of pollinators and nectar robbers to the flowers and inflorescences of Tabebuia aurea (Bignoniaceae): effects of floral display size and habitat fragmentation

Large floral displays favour pollinator attraction and the import and export of pollen. However, large floral displays also have negative effects, such as increased geitonogamy, pollen discounting and nectar/pollen robber attraction. The size of the floral display can be measured at different scales (e.g. the flower, inflorescence or entire plant) and variations in one of these scales may affect the behaviour of flower visitors in different ways. Moreover, the fragmentation of natural forests may affect flower visitation rates and flower visitor behaviour. In the present study, video recordings of the inflorescences of a tree species (Tabebuia aurea) from the tropical savannah of central Brazil were used to examine the effect of floral display size at the inflorescence and tree scales on the visitation rate of pollinators and nectar robbers to the inflorescence, the number of flowers approached per visit, the number of visits per flower of potential pollinators and nectar robbers, and the interaction of these variables with the degree of landscape disturbance. Nectar production was quantified with respect to flower age. Although large bees are responsible for most of the pollination, a great diversity of flower insects visit the inflorescences of T. aurea. Other bee and hummingbird species are highly active nectar robbers. Increases in inflorescence size increase the visitation rate of pollinators to inflorescences, whereas increases in the number of inflorescences on the tree decrease visitation rates to inflorescences and flowers. This effect has been strongly correlated with urban environments in which trees with the largest floral displays are observed. Pollinating bees (and nectar robbers) visit few flowers per inflorescence and concentrate visits to a fraction of available flowers, generating an overdispersed distribution of the number of visits per inflorescence and per flower. This behaviour reflects preferential visits to young flowers (including flower buds) with a greater nectar supply.     

盗蜜对角蒿传粉者行为和生殖成功的影响

一些研究显示盗蜜对自交植物的结实和结籽没有显著影响。然而, 对于既有传粉者为其传粉实现异交又能通过自交实现生殖保障的兼性自交植物来说, 盗蜜对其生殖的影响还知之甚少。由于兼性自交植物可以自交, 盗蜜对其总体结实可能不会有显著影响, 但可能会通过影响传粉者行为而影响传粉者介导的结实。为了验证这一假说, 本研究以兼性自交的一年生角蒿(Invarvillea sinensis var. sinensis)为研究材料, 通过野外调查和控制实验, 探讨了盗蜜对传粉者介导的结实(传粉者行为)和总体结实率的影响。结果表明: 角蒿的盗蜜者和主要传粉者相同, 均为密林熊蜂(Bombus patagiatus)。熊蜂盗蜜频率平均为20.24% (范围为0-51.43%)。盗蜜对角蒿总体结实率、每果结籽数和每果种子重量没有显著影响。然而, 被盗蜜花的柱头闭合比率显著高于未被盗蜜花, 说明盗蜜影响传粉者的访花行为和传粉者介导的结实率。另外, 被盗蜜花的高度显著高于未被盗蜜花, 说明盗蜜者倾向于从较大较高的花上盗蜜。这些结果为全面认识盗蜜对植物生殖的影响提供了新的信息。     

Predicting the effects of nectar robbing on plant reproduction: implications of pollen limitation and plant mating system

The outcome of species interactions is often difficult to predict, depending on the organisms involved and the ecological context. Nectar robbers remove nectar from flowers, often without providing pollination service, and their effects on plant reproduction vary in strength and direction. In two case studies and a meta-analysis, we tested the importance of pollen limitation and plant mating system in predicting the impacts of nectar robbing on female plant reproduction. We predicted that nectar robbing would have the strongest effects on species requiring pollinators to set seed and pollen limited for seed production. Our predictions were partially supported. In the first study, natural nectar robbing was associated with lower seed production in Delphinium nuttallianum, a self-compatible but non-autogamously selfing, pollen-limited perennial, and experimental nectar robbing reduced seed set relative to unrobbed plants. The second study involved Linaria vulgaris, a self-incompatible perennial that is generally not pollen limited. Natural levels of nectar robbing generally had little effect on estimates of female reproduction in L. vulgaris, while experimental nectar robbing reduced seed set per fruit but not percentage of fruit set. A meta-analysis revealed that nectar robbing had strong negative effects on pollen-limited and self-incompatible plants, as predicted. Our results suggest that pollination biology and plant mating system must be considered to understand and predict the ecological outcome of both mutualistic and antagonistic plant-animal interactions.     

Effects of nectar robbing on pollinator behavior and plant reproductive success of Pitcairnia angustifolia (Bromeliaceae)

Nectar robbers may have direct and indirect effects on plant reproductive success but the presence of nectar robbing is not proof of negative fitness effects. We combined census data and field experiments to disentangle the complex effects of nectar robbing on nectar production rates, pollinator behavior, pollen export, and female reproductive success of Pitcairnia angustifolia. Under natural conditions flowers were visited by four different animal species including a robber‐like pollinator and a secondary robber. Natural levels of nectar robbing ranged from 40 to 100%. Natural variation in nectar robbing was not associated with fruit set in any year whereas seed set was weakly positively associated for 1 year only. Artificial nectar robbing did not increase nectar production or concentration, did not affect the behavior of long‐billed hummingbirds, and when faced with artificially robbed flowers, these visitors behaved as secondary nectar robbers. The number of stigmas within a patch that received pollen dye analogs and the average distance traveled by these analogs were not significantly different between robbing treatments (robbed flowers versus unrobbed flowers), but the maximum distance traveled by these pollen analogs was higher when nectar robbing was not prevented. Overall, the proportion of robbed flowers on an inflorescence had a neutral effect to a weak positive effect on the reproduction of individual plants (i.e. positive association between nectar robbing and fruit set in 2002) even when it clearly changed the behavior of its most efficient pollinator potentially increasing the frequency of nectar robbing within a plant.     

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

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

Behavioural differences between male and female carpenter bees in nectar robbing and its effect on reproductive success in Glechoma longituba (Lamiaceae)

Male and female nectar robbers may show significantly different behaviour on host plants and thus have different impacts on reproductive fitness of the plants. A 4-year study in natural populations of Glechoma longituba has shown that male carpenter bees (Xylocopa sinensis) are responsible for most of the nectar robbing from these flowers, while female bees account for little nectar robbing, demonstrating distinct behavioural differentiation between male and female bees in visiting flowers. The smaller male bee spends less time visiting a single flower than the larger female bee, consequently, the male bee is capable of visiting more flowers per unit time and has a higher foraging efficiency. Moreover, the robbing behaviour of female carpenter bees is more destructive and affects flower structures (ovules and nectaries) and floral life-span more than that of the male bee. According to the energy trade-off hypothesis, the net energy gain for male bees during nectar robbing greatly surpasses energy payout (17.72 versus 2.43 J), while the female bee net energy gain is barely adequate to meet energy payout per unit time (3.78 versus 2.39 J). The differences in net energy gain for male and female bees per unit time in nectar robbing are the likely cause of observed behavioural differences between the sexes. The differences in food resource preference between male and female bees constitute an optimal resource allocation pattern that enables the visitors to utilise floral resources more efficiently.     

Roles of nectar robbers in reproduction of the tropical treelet Quassia amara (Simaroubaceae)

Summary Different subsets of mainland nectarivores visited Quassia amara (Simaroubaceae), a self-compatible, predominately bird-pollinated treelet, at three islands and the mainland in Panamá. Factors correlated with reproductive success, defined as seed to ovule ratio, included the species pollinating and robbing flowers, visitor activity, pollinator response to nectar robbing, and internal regulation of fruit production. The absence of robbers and former pollinators on an island separated from the mainland during the holocene was associated with shifts in flower size, nectar production, and 3–4fold increases in population reproductive success and pollinator efficiency (=seeds produced per visit). Exclusion of robbers at three sites resulted in seed production 4–12 times greater than control flowers, at which robbers accounted for 52–98% of all visits. Although 36% of buds and over 83% of all flowers were robbed, this had no direct influence on the recorded 36–61% respective abortion rates of buds and flowers. Opportunistic avian robbers appeared where normal robbers were absent; three avian robbers extensively used floral perforations made by Trigona bees, and all ancillary pollinators also robbed. Selection pressures from nectar robbers are discussed that may relate to plant reproductive fitness.     

Primary nectar robbing by Apis mellifera (Apidae) on Pyrostegia venusta (Bignoniaceae): behavior,pillaging rate,and its consequences

The interactions between plants and their pollinators are the result of convergent evolution of floral attributes reflecting pressure exerted by pollinators. Nonetheless, the strategies employed by floral visitors to collect floral resources are extremely complex, and commonly involve theft or robbery in addition to pollination. We describe here the behavioral repertory of Apis mellifera during the collection of the floral resources, and evaluated the robbing rates of A. mellifera on the buds and flowers of Pyrostegia venusta during periods of intense and sparse flowering. We recorded the behaviors exhibited by foraging bees while collecting floral resources, quantified the numbers of floral buds and flowers with perforations in their corolla tissues, and determined whether that damage reduced nectar production. The evaluations were conducted during two distinct periods: during the period of intense flowering of P. venusta, and during the period of sparse flowering. Nectar robbing was observed during 93.4% of the visits of foraging A. mellifera bees, while nectar theft was observed during only 0.7% of the visits, and pollen theft during 5.9%. The robbing of floral buds and flowers was most intense during the period of heavy flowering. Flowers that had been intensely robbed secreted significantly less nectar than those non-robbed. The unusual nectar robbing activities of A. mellifera, especially during the period of intense flowering indicates an optimization of access to larger volumes of food resources. Our results therefore point to a major limitation of nectar per floral unit during the intense flowering period of P. venusta due to the high activity of nectar robbing by A. mellifera bees.

     

Causes and consequences of floral damage in Aconitum lycoctonum at high and low elevations in Switzerland

The outcomes of interactions among plants and the insects that use their flowers are likely to vary among the physical environments and the communities in which they grow. In this study we quantified floral damage of Aconitum lycoctonum in high (>2000 m) and low (c. 500 m) elevation populations in Switzerland. At high elevation, floral damage was frequent and was caused by nectar-robbing short-tongued bumblebees. Nectar robbers make a hole in the flower when they collect nectar. A nectar robber exclusion experiment showed that nectar robbery by short-tongued bumblebees had no effect on the female reproductive success of plants; robbing bees rarely damaged the nectaries, and damage to the petals probably does not decrease flower longevity. In addition, nectar robbers tended to collect pollen during about 10% of their visits. Thus, these bees may act as low-efficiency pollinators and may, at times, be mutualistic associates. At low elevation, the holes in the flowers were caused by beetles (Meligethes viridescens) and not by short-tongued bumblebees. The beetles eat pollen and might also consume nectar. Since the beetles gain access to pollen and nectar by entering the flower through its opening, and later chew holes while foraging on floral tissue, the beetles are pollen eaters rather than nectar robbers. Overall, our results show that not all floral damage is caused by nectar robbers and that there can be strong altitudinal variation in the causes and consequences of floral damage.