Nectar robbing of a carpenter bee and its effects on the reproductive fitness of Glechoma longituba (Lamiaceae)

The floral biology and pollination process of Glechoma longituba (Nakai) Kuprian, a clonal gynodioecious, perennial herb that is widely distributed in China was investigated in natural populations. During visits to the flowers of G. longituba, the carpenter bee—Xylocopa sinensis mainly displayed nectar-robbing behavior with minimal pollination. Nectar robbing behavior began at the onset of flowering and continued for about 3 weeks ending at about the middle of the flowering period. A total of 18.6% floral visits in this period were by nectar robbers, with about 90% of the flowers in the study populations being subjected to two or two nectar-robbing episodes. During controlled experiments, lower pollination efficiency was recorded for X. sinensis compared to legitimate pollinators. Pollination by the robber-like pollinator X. sinensis during the early-mid phase of the flowering season yielded seeds of 16.16%. Although nectar robbing by the carpenter bee seemed to have a slight enhancing effect on seed set in G. longituba, this effect was effectively masked by the more pronounced detrimental effect of nectar robbing. Experiments indicated that nectar robbing by the carpenter bee reduced seed production by more than 26%, largely owing to the consequent shortening of the life span of robbed flowers. Furthermore, 10.43% of the ovules and 13.04% of the nectaries in the robbed flowers were damaged, thus causing a decrease or entire loss of reproductive opportunity in the robbed flowers. In addition, a higher number of pollen grains remained on the androecia of robbed flowers indicating that nectar robbing may have a lowering effect on male fitness in G. longituba.     

Sexual differences in reproductive characters and pollinator attractiveness in gynodioecious Glechoma longituba (Lamiaceae)

We quantified the differences in floral characters and attractiveness to flower visitors under natural conditions between the sexual types in the gynodioecious plant Glechoma longituba. We also manipulated flowers by altering corolla size or nectar volume, or by removing anthers, to examine the effect of these primary and secondary attractants (i.e. rewards and advertisements) on attractiveness. A change in corolla size and shape reduced visiting frequency and pollen load. Removal of anthers did not affect visiting rates, but significantly reduced pollination rates and stigmatic pollen load. A decrease in the nectar volume of a flower was associated with a reduction in handling time and pollen loads on stigmas. These results show that corolla size is an important advertisement to pollinators (particularly at greater distance), which associate hermaphrodite flowers with a larger corolla and a larger volume of nectar than female flowers. We found that artificial changes in population structure affected the behavior of pollinators as well as the pollination rates of flowers. We suggest that the pattern of distribution of hermaphrodite and female clones in a population may serve to avoid pollen limitation in a female clone or patch. This effect may ensure female reproductive success and allow for the maintenance of female individuals in natural populations of this gynodioecious plant.     

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.     

连钱草愈伤组织诱导及增殖研究

对连钱草Glechoma longituba (Nakai) Kupr.愈伤组织培养作了初步的探索,以不同的培养条件,利用连钱草的顶芽、叶、叶柄为外植体,研究了连钱草愈伤组织的培养。结果表明：在以MS培养基和LS培养基为基本培养基附加不同外源激素2,4-D、NAA、KT、BA条件下,连钱草在一个较宽的生长范围内,均可诱导产生连钱草的愈伤组织,但不同外植体、不同类型植物激素及其不同浓度对愈伤组织发生均有一定影响：作为外植体,连钱草叶柄和叶都可顺利诱导出愈伤组织;生长素2,4-D对连钱草外植体的脱分化起促进作用,但NAA却抑制愈伤组织的形成;细胞分裂素KT和BA均能与2,4-D组合促进愈伤组织的诱导。MS+2,4-D在光暗交替条件下和LS+2,4-D在黑暗条件下有利于连钱草愈伤组织的诱导,最佳诱导和增殖条件是MS+2,4-D（1.5 mg·L^-1）+BA（1.0 mg·L^-1）光、暗交替（光照14 h·d^-1）。在此条件下, 30 d后,叶的诱导率达91.38%,叶柄的诱导率达100%;愈伤组织继代培养14 d后,平均增殖率达202.2%。     

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.     

Variability of nectar production and composition in Linaria vulgaris (L.) Mill. (Scrophulariaceae)

 We studied nectar characteristics during the long flowering period (late June to end of November) in two populations of Linaria vulgaris (L.) Mill. spontaneously growing in the Botanical Gardens of Siena University (Tuscany, central Italy). The two populations were close to each other but they differed in blooming period. Plants of population 1 sprouted in May and flowered from the end of June to the end of September. Population 2 sprouted at the end of August and flowered from September to the end of November. Differences in nectar production and composition were found between and within populations. Flowers of population 1 produced a very small amount of nectar (not collectable) that remained on the nectary surface. The quantity of nectar increased in late September, when each flower produced 2–3 μl of nectar that flowed into the spur. Total sugar concentration was 175.8 mg/ml in young flowers. Flowers of population 2 produced 5–8 μl of nectar with a total sugar concentration of 200.9 mg/ml in the young stage. In bagged senescent flowers nectar volume decreased in both populations and nectar sugar concentration decreased down to 11.6 mg/ml in population 2 and increased up to 289.6 mg/ml in population 1. For both populations, the decrease in nectar volume in bagged flowers may have been due to water loss by evaporation. In population 2, the decrease in sugar concentration may have been due to nectar reabsorption that was never observed in population 1. Nectar variability is discussed in relation to insect visits and seed set. Received August 14, 2002; accepted December 17, 2002 Published online: June 2, 2003     

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.     

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。     

Differential effects of anthropogenic edges and gaps on the reproduction of a forest‐dwelling plant: The role of plant reproductive effort and nectar robbing by bumblebees

Forest fragmentation produces sharp changes in the spatial configuration of remnant forest patches, which include the increasing influence of patch edges on the interior of forest patches (‘edge effects’). Human activities responsible for forest fragmentation tend also to change the internal characteristics of remnant patches, for example, through the creation of gaps by selective logging. While edges and gaps can be expected to cause comparable changes in the micro‐environmental conditions of the forest, their effects on forest‐dwelling species and their interactions are not necessarily comparable. This study compares the effect of forest edges and anthropogenic gaps on the reproductive success of a self‐incompatible epiphytic plant (Mitraria coccinea), mediated by changes in its relationship with mutualists (pollinators) and antagonists (flower larcenists). Mitraria coccinea's flowers are pollinated by hummingbirds and robbed by the bumblebee Bombus dahlbomii. Edges and gaps had comparable positive effects on flower production and fruit set; however, nectar robbing was up to sevenfold higher in patches with numerous gaps and resulted in lower reproductive success (fruit set and total fruit crop). Forest fragmentation studies should therefore avoid treating forest remnants as homogeneous units (i.e. focusing exclusively on their characteristics and connectivity), without taking into account the internal heterogeneity caused by anthropogenic pressures (e.g. gaps and edge effects).     

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.     

Relationship between floral tube length and nectar robbing in Duranta erecta L. (Verbenaceae)

Although nectar robbing is a common phenomenon in plant species with tubular flowers or flowers with nectar spurs, the potential effect of this illegitimate interaction on plant reproductive success has not received the deserved attention. In the present study, we analysed the functional relationship between flower morphology and nectar robbing, and examined the reproductive consequences of the interaction in a population of Duranta erecta (Verbenaceae) on the island of Cuba. The results show that nectar robbing is conducted by the carpenter bees Xylocopa cubaecola and affects up to 44% of flowers in the studied population. However, not all the flowers have the same probability of being robbed. The chance of flowers being robbed increases with flower length and flower diameter. Moreover, nectar robbing significantly decreases the chance that flowers will set fruit. Also, the impact of nectar robbing on the probability of flowers to set fruits is dependent on the plant. We suggest that nectar robbing may represent an opposite selective force that balances the selection for longer corollas often imposed by pollinators specializing in visiting tubular flowers. Such a relationship with nectar robbers would have obvious implications for the evolution of tubular or closed flowers. This preliminary finding deserves further research in light of the ecological and evolutionary consequences of nectar robbing in tubular flowers.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 392–398.     

洛阳地区黄胸木蜂访花植物种类及访花行为

【目的】明确黄胸木蜂Xylocopa appendiculata的访花植物种类和访花行为, 为进一步开发和利用木蜂资源奠定基础。【方法】 2009-2011年连续3年, 在洛阳地区黄胸木蜂的活动期3-10月, 采用目测、 拍照等方法记录其访花植物及访花行为, 记录和统计访花植物的生物学特征; 测量访花植物种类被盗蜜后盗蜜口的大小。【结果】在洛阳地区黄胸木蜂访花植物种类为27科52种, 主要的访花植物有25种。采访的植物种类中, 忍冬科和豆科植物最多, 分别为9种和8种, 占采访植物种类的17.31%和15.38%; 其中黄胸木蜂盗蜜的植物有16种, 占其采访植物种类的30.77%。在采访的植物种类中, 黄胸木蜂喜欢采访中等花型、 两侧对称的紫色、 黄色和白色花。在不同植物上, 黄胸木蜂的盗蜜口大小和访花频率不同, 黄胸木蜂在臭牡丹上的盗蜜口最大, 为9.43±1.91 mm, 蝟实上的盗蜜口最小, 为3.46±0.98 mm; 在紫薇上的访花速度最快, 访花频率为25.71±2.36朵/min; 在蜀葵上的单花停留时间和访花间隔时间均最长, 单花停留时间5.89±3.34 s, 访花间隔时间为2.63±2.04 s。【结论】在洛阳地区黄胸木蜂访花植物种类多、 访花时间长。对于不同的植物种类, 黄胸木蜂的访花行为和访花频率有差异。     

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.

     

Postpollination nectar reabsorption in the African epiphyte Aerangis verdickii (Orchidaceae)

Nectar reabsorption in flowering plants seems to be a rare phenomenon and to our knowledge it has not been reported previously in the Orchidaceae. In this study we present data that show statistically significant differences in nectar sugar concentrations before and after pollination. Virgin flowers of the African epiphytic orchid Aerangis verdickii showed mean sugar concentrations in the nectar of 14.4 and of 18.3% in 1994 and 1995, respectively (sucrose mass by mass equivalent). Sugar concentration in nectar from naturally pollinated flowers had a mean of 3.2 and of 8.7% for the same period. In an experiment in the wild 60 flowers were protected against nectar theft by the ants. Half of those flowers were hand-pollinated. Control (virgin) flowers had nectar with a mean value of 13.8%, while flowers measured 48 h after pollination had a mean sugar concentration of 4.3%. The mean volume of nectar based on measurements of 23 virgin flowers from nine different plants was 19 uL. We estimated an average energy value for the nectar produced of 684 J per plant per season. At the study site, over 60% of the unmanipulated flowers were robbed of all their nectar by arboreal ants, Polyrachis spp. (Formicinae). The adaptive significance of nectar reabsorption for A. verdickii is probably a function of the environmental stresses to which it has been exposed and the relative costs of nectar production.     

Sex expression,female frequency,and reproductive output in a gynodioecious clonal herb, <Emphasis Type="Italic">Glechoma longituba</Emphasis> (Lamiaceae)

We investigated the sex morphs and frequency of females in 24 natural populations of the clonal, gynodioecious species Glechoma longituba. In addition to the presence of hermaphrodites and females, there were some individuals with intermediate sex expression that could not be categorized as either morph. The majority of populations contained a predominance of hermaphrodites, although female frequency varied from 0 to 100%. The sexual expression of individual ramets did not change over three consecutive years or when ramets were transplanted to different populations, but it did change over the course of a flowering season. Seeds from females weighed more than those from hermaphrodites. The seed set of hermaphrodites was relatively constant across populations; the seed set of females was higher than that of hermaphrodites in most populations, but lower in populations in which females occurred at a very high frequency because of pollen limitation. This led to a negative correlation being detected between the seed set of females and the frequency of females in a population. We postulated that the adjustment of sex expression within seasons could be an adaptive mechanism of reproductive assurance in this system.     

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.     

The dynamics of pollen removal and deposition,and its effects on sexual phases in a protandrous plant: Glechoma longituba (Lamiaceae)

The duration of sexual phases in dichogamous plants are affected by many factors. Using both experimental and observational studies, we investigated natural patterns of pollen removal and deposition, visiting frequency of pollinators, patterns of nectar secretion, and effects of pollen removal and stigmatic pollen deposition on the duration of sexual phases in a protandrous plant, Glechoma longituba. We found that visiting frequency of pollinators correlated with the nectar secretion pattern. The nectar volume during the male phase was higher than during the female phase. In the morning, the main pollinator, the bee Anthophora plumipes, mainly foraged for nectar and showed no preference for flowers in male or female phase, despite male phase flowers producing higher amounts of nectar. However, in the afternoon, they changed their behavior and foraged mainly for pollen, and then showed a preference for flowers in male phase. Furthermore, the rates of pollen removal and stigmatic pollen deposition can affect the starting time and the duration of the female phase. When pollen removal and pollination rates are low due to scarcity of pollinator services, the sexual phase can be prolonged, leading to an overlap, and thereby enhance the chance for sexual reproduction through pollinator‐facilitated self‐pollination. We consider the variation of sexual phases in Glechoma longituba an adaptive mechanism prepared for both cross‐pollination enhancement and reproductive assurance depending on the available pollination services.