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.     

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.

     

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.     

Are nectar-robbers mutualists or antagonists?

As exploiters of plant-pollinator mutualisms, nectar-robbers remove rewards (nectar) without providing pollination services. Though one might expect nectar-robbing to be costly to plants, it may instead benefit plants by indirectly increasing pollen dispersal. I investigated the direct effects of nectar-robbing bees (Xylocopa californica) on floral rewards and behaviors of pollinators visiting desert willow (Chilopsis linearis) and indirect effects of robbing on the reproductive success of the plant. Nectar-robbers reduced nectar; while unrobbed and robbed flowers were equally likely to contain nectar, nectar volumes were smaller in robbed flowers with nectar. Apis mellifera (honeybees), ineffective pollinators in terms of pollen deposition, avoided robbed flowers. In contrast, Bombus sonorus (bumblebees), effective pollinators, did not avoid robbed flowers. While bumblebees tended to spend less time in robbed flowers, the time that they spent in flowers was not correlated with pollen deposition. Using powder mimicking pollen, I found that on some days, powder was dispersed farther or to more flowers from robbed flowers, indicating that robbing may sometimes benefit plants by increasing male reproductive success. Powder movement suggested that the effect of robbing on male reproductive success ranged from costly to beneficial. The outcome for flowers that were marked early each morning was a function of prevalence of robbing and abundances of effective pollinators, but not a function of spatial variability among trees in prevalence of robbing or the abundance of ineffective honeybees. Unlike powder dispersal, female reproductive success, measured by fruit set and the number of pollen tubes growing in styles, was not affected by robbing. Thus, robbers did not reduce plants female reproductive success either directly by damaging flowers or indirectly by reducing pollen deposition by pollinators. Overall, this study indicates that nectar-robbers were not often costly to plants, and sometimes even benefited plants.     

Testing non-additive effects of nectar-robbing ants and hummingbird pollination on the reproductive success of a parasitic plant

Nectar robbing may have an indirect negative effect on plant reproduction by discouraging legitimate pollinator species from visiting robbed flowers. In this study, we set up a 2 × 2 factorial design with nectar-robbing ants and hummingbird pollination to test for non-additive effects on fruit set, seed mass, and seed germination of the leafless mistletoe Tristerix aphyllus (Loranthaceae). Even though ants caused conspicuous damage at the base of the floral tubes, nectar availability was reduced by only 8 % in the presence of ants. The green-backed firecrown Sephanoides sephaniodes was insensitive to the presence of ants. Rather, the bird responded to flower number and the presence or the absence of damage, but not to the extent of damage within inflorescences. As hummingbirds were largely insensitive to variation in nectar robbing, the interaction ant × hummingbird had no effect on plant-reproductive success. Thus, the factorial experiment did not provide evidence for indirect negative effects of nectar robbing on plant reproduction. These results suggest that indirect effects of nectar robbers on pollinator behaviour may occur under a more restricted set of conditions than those previously considered. We suggest that the low amount of nectar removed by nectar-robbing ants was insufficient for hummingbirds to avoid robbed flowers, which restricted the potential for non-additive 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.     

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.     

Direct and Indirect Effects of Nectar Robbing on the Pollinating Behavior of Patagona gigas (Trochilidae)1

In central Chile, nectar robbing of Puya coerulea (Bromeliaceae) flowers by the austral blackbird, Curaeus curaeus, had a direct impact on the plant via removal of floral resources and, in some cases, damage or even destruction of flowers. These robbing visits also likely had an indirect impact on plant fitness due to the decreased rate of legitimate visits by the hummingbird Patagona gigas to inflorescences with many robbed flowers. The proportion of flowers within an inflorescence visited by P. gigas was inversely proportional to the ratio of robbed flowers.     

Impact of Striped-Squirrel Nectar-Robbing Behaviour on Gender Fitness in Alpinia roxburghii Sweet (Zingiberaceae)

Nectar-robbing has the potential to strongly affect male and female reproductive fitness of plants. One example of nectar theft is that shown by striped-squirrels (Tamiops swinhoei) on a number of ginger species, including Alpinia roxburghii and A. kwangsiensis (Zingiberaceae). In this study, we used a fluorescent dye as a pollen analogue, and measured fruit and seed output, to test the effect of squirrel nectar-robbing on A. roxburghii reproductive fitness. Pollen transfer between robbed and unrobbed flowers was assessed by comparing 60 randomly established plots containing robbed and unrobbed flowers. The frequency of squirrel robbing visits and broken styles were recorded from a number of flowers for five consecutive days. Two bee species (Bombus eximius and Apis cerana), were the primary pollinators, and their visitation frequency was recorded for six consecutive days. The results showed that fluorescent powder from unrobbed flowers was dispersed further, and to a greater number of flowers than that placed on robbed flowers. Additionally, robbing flowers caused significant damage to reproductive organs, resulting in lower fruit and seed sets in robbed than in unrobbed flowers and influencing both male and female fitness. The frequency of the primary pollinator visits (B. eximius) was significantly higher for unrobbed plants than for robbed plants. The present study clearly shows the negative impact of squirrel robbing on A. roxburghii male reproductive fitness and neutral impact on female reproductive fitness.     

Selective nectar robbing in a gynodioecious plant (Glechoma longituba) enhances female advantage

Nectar robbing not only affects the reproductive fitness of the plant but it may also potentially affect the pollination dynamics of the associated coflowering individuals. In this study, we established that the nectar robber Xylocopa sinensis robs nectar only from the hermaphrodite ramets of the gynodioecious plant Glechoma longituba but not from the female ramets. In populations with high rates of nectar robbing, this results in hermaphrodite ramets having reduced seed set whereas the female ramets have a slightly increased seed set. We hypothesize that selective nectar robbing confers an advantage to female individuals and thus ensures their maintenance in gynodioecious populations. Results of controlled experiments indicated that the reduction in the amounts of nectar available occasioned by nectar robbing resulted in some legitimate pollinators switching to visiting flowers on female rather than hermaphrodite ramets. This resulted in lower pollination rates and seed set for hermaphrodites and higher pollination rates and seed set for females. This study presents a previously unreported mechanism causing female advantage in gynodioecious plants.     

Nectar robbers deter legitimate pollinators by mutilating flowers

Nectar robbing – harvesting nectar illegitimately – can have a variety of outcomes for plant sexual reproduction and for the pollinator community. Nectar robbers can damage flowers while robbing nectar, which could affect the behavior of subsequent flower visitors and, consequently, plant reproduction. However, only nectar manipulation by nectar robbers has so far received attention. We found a short-tongued bee, Hoplonomia sp. (Halictidae), mutilating the conspicuous lower petal of the zygomorphic flowers of Leucas aspera (Lamiaceae) while robbing nectar. We hypothesized that the mutilation of the conspicuous lower petal deters legitimate pollinators on L. aspera flowers, which, in turn, might affect plant reproduction. We first assessed the proportion of naturally-robbed flowers in plant populations for three years to confirm that it was not a purely local phenomenon due to a few individual bees. We then studied diversity, community and visitation characteristics of pollinators, nectar dynamics and fruit set in unrobbed and robbed open flowers in naturally-robbed populations. The proportion of robbed flowers varied significantly across sites and years. Robbing did not affect nectar dynamics in flowers, but it did alter flower morphology, so much so that it reduced pollinator visitation and altered the pollinator community on robbed flowers. However, the maternal function of plant reproduction was not affected by nectar robbing. This study for the first time shows that a nectar robber can have an ecologically significant impact on floral morphology.     

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.     

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.     

Consequences of nectar robbing for the fitness of a threatened plant species

The effect of nectar robbing on plant fitness is poorly understood and restricted to a few plant species. Furthermore, the available studies generally evaluate the effects of nectar robbing on female fitness, disregarding the male component. Here we measured the effects of the nectar-robbing bumblebees on male (measured as pollen analogue flow distance) and female (measured as seed production) reproductive success in the insect-dependent Polygala vayredae, a narrow endemic species from the pre-Pyrenees (Spain). Intense nectar robbing by bumblebees significantly reduced the nectar available to legitimate pollinators in the studied population, and this reduction affected both male and female fitness. Significant differences were observed in fluorescent dye dispersion between robbed and non-robbed flowers within the population. Fluorescent dyes from non-robbed flowers were dispersed to larger distances and over a larger number of flowers when compared with robbed ones. Moreover, significant differences were observed in both fruit set and seed ovule ratios between the two groups, with non-robbed flowers presenting higher reproductive outcomes. However, no effect on seed weight was detected among treatments. The data obtained suggest that in this species, nectar robbing has important indirect and negative effects on plant fecundity, through both male and female functions, due to a modification in the foraging behaviour of legitimate visitors.     

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.     

Nectar robbing in Ipomopsis aggregata : effects on pollinator behavior and plant fitness

Hummingbirds foraging in alpine meadows of central Colorado, United States, face a heterogeneous distribution of nectar rewards. This study investigated how variability in nectar resources caused by nectar-robbing bumblebees affected the foraging behavior of hummingbird pollinators and, subsequently, the reproductive success of a host plant (Ipomopsis aggregata). We presented hummingbirds with experimental arrays of I. aggregata and measured hummingbird foraging behavior as a function of known levels of nectar robbing. Hummingbirds visited significantly fewer plants with heavy nectar robbing (over 80% of available flowers robbed) and visited fewer flowers on those plants. These changes in hummingbird foraging behavior resulted in decreased percent fruit set as well as decreased total seed set in heavily robbed plants. These results indicate that hummingbird avoidance of nectar-robbed plants and flowers reduces plant fitness components. In addition, our results suggest that the mutualisms between pollinators and host plants may be affected by other species, such as nectar robbers. Received: 22 April 1998 / Accepted: 12 May 1998     

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.     

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.     

Nectar robbery by a hermit hummingbird: association to floral phenotype and its influence on flowers and network structure

Interactions between flowers and their visitors span the spectrum from mutualism to antagonism. The literature is rich in studies focusing on mutualism, but nectar robbery has mostly been investigated using phytocentric approaches focused on only a few plant species. To fill this gap, we studied the interactions between a nectar-robbing hermit hummingbird, Phaethornis ruber, and the array of flowers it visits. First, based on a literature review of the interactions involving  P. ruber, we characterized the association of floral larceny to floral phenotype. We then experimentally examined the effects of nectar robbing on nectar standing crop and number of visits of the pollinators to the flowers of Canna paniculata. Finally, we asked whether the incorporation of illegitimate interactions into the analysis affects plant–hummingbird network structure. We identified 97 plant species visited by P. ruber and found that P. ruber engaged in floral larceny in almost 30 % of these species. Nectar robbery was especially common in flowers with longer corolla. In terms of the effect on C. paniculata, the depletion of nectar due to robbery by P. ruber was associated with decreased visitation rates of legitimate pollinators. At the community level, the inclusion of the illegitimate visits of P. ruber resulted in modifications of how modules within the network were organized, notably giving rise to a new module consisting of P. ruber and mostly robbed flowers. However, although illegitimate visits constituted approximately 9 % of all interactions in the network, changes in nestedness, modularity, and network-level specialization were minor. Our results indicate that although a flower robber may have a strong effect on the pollination of a particular plant species, the inclusion of its illegitimate interactions has limited capacity to change overall network structure.     

Realized tolerance to nectar robbing: compensation to floral enemies in Ipomopsis aggregata

Background and Aims

Although the ecological and evolutionary consequences of foliar herbivory are well understood, how plants cope with floral damage is less well explored. Here the concept of tolerance, typically studied within the context of plant defence to foliar herbivores and pathogens, is extended to floral damage. Variation in tolerance to floral damage is examined, together with some of the mechanisms involved.

Methods

The study was conducted on Ipomopsis aggregata, which experiences floral damage and nectar removal by nectar-robbing bees. High levels of robbing can reduce seeds sired and produced by up to 50 %, an indirect effect mediated through pollinator avoidance of robbed plants. Using an experimental common garden with groups of I. aggregata, realized tolerance to robbing was measured. Realized tolerance included both genetic and environmental components of tolerance. It was hypothesized that both resource acquisition and storage traits, and traits involved in pollination would mitigate the negative effects of robbers.

Key Results

Groups of I. aggregata varied in their ability to tolerate nectar robbing. Realized tolerance was observed only through a component of male plant reproduction (pollen donation) and not through components of female plant reproduction. Some groups fully compensated for robbing while others under- or overcompensated. Evidence was found only for a pollination-related trait, flower production, associated with realized tolerance. Plants that produced more flowers and that had a higher inducibility of flower production following robbing were more able to compensate through male function.

Conclusions

Variation in realized tolerance to nectar robbing was found in I. aggregata, but only through an estimate of male reproduction, and traits associated with pollination may confer realized tolerance to robbing. By linking concepts and techniques from studies of plant–pollinator and plant–herbivore interactions, this work provides insight into the role of floral traits in pollinator attraction as well as plant defence.Key words: Compensation, herbivory, indirect effects, Ipomopsis aggregata, male reproductive success, nectar robbing, pollen donation, pollination, resistance, tolerance