Additive effects of herbivory,nectar robbing and seed predation on male and female fitness estimates of the host plant <Emphasis Type="Italic">Ipomopsis aggregata</Emphasis>

Many antagonistic species attack plants and consume specific plant parts. Understanding how these antagonists affect plant fitness individually and in combination is an important research focus in ecology and evolution. We examined the individual and combined effects of herbivory, nectar robbing, and pre-dispersal seed predation on male and female estimates of fitness in the host plant Ipomopsis aggregata. By examining the effects of antagonists on plant traits, we were able to tease apart the direct consumptive effects of antagonists versus the indirect effects mediated through changes in traits important to pollination. In a three-way factorial field experiment, we manipulated herbivory, nectar robbing, and seed predation. Herbivory and seed predation reduced some male and female fitness estimates, whereas plants tolerated the effects of robbing. The effects of herbivory, robbing, and seed predation were primarily additive, and we found little evidence for non-additive effects of multiple antagonists on plant reproduction. Herbivory affected plant reproduction through both direct consumptive effects and indirectly through changes in traits important to pollination (i.e., nectar and phenological traits). Conversely, seed predators primarily had direct consumptive effects on plants. Our results suggest that the effects of multiple antagonists on estimates of plant fitness can be additive, and investigating which traits respond to damage can provide insight into how antagonists shape plant performance.     

When resources don't rescue: flowering phenology and species interactions affect compensation to herbivory in Ipomopsis aggregata

The ability of plants to tolerate, or compensate for, herbivore damage is highly variable and has been the subject of much research. Although many plants can compensate for herbivore damage, and some even overcompensate, we cannot yet generalize about the conditions that promote a positive response to damage. Here, we asked how abiotic resources (i.e. plant nutrient status) coupled with biotic interactions – i.e. subsequent interactions with pollinators, seed predators and nectar robbing bumble bees – affect the compensatory ability of Ipomopsis aggregata, a monocarpic herb that has been the subject of much previous debate. We hypothesized that compensation to herbivore damage in I. aggregata (Polemoniaceae) would depend first on plants having an ample supply of resources and, second, on the outcome of subsequent interactions with mutualist pollinators and enemy pre‐dispersal seed predators and nectar robbing bumble bees. We used a fully‐factorial experiment in which plants were watered, fertilized or left as unmanipulated controls, crossed with clipping to simulate herbivore damage to the apical meristem. Resource addition enhanced both male and female components of fitness, but resource enhancement did not provide the means for plants to fully compensate for simulated herbivory. Clipped plants produced significantly more inflorescences, but at the expense of a delay in flowering and fewer total flowers. Clipping significantly reduced losses to dipteran pre‐dispersal seed predators by delaying flowering time, but early flowering plants produced higher numbers of seeds despite incurring higher rates of predation. Clipped plants incurred a higher risk to nectar robbers in one of two years. Overall, clipped plants suffered severe reductions (a nearly 50% reduction in total seed set) in female success, but clipping combined with nutrient addition enhanced male function through increases in per‐flower pollen production. However, because clipped plants produced significantly fewer flowers than unclipped plants, whole‐plant pollen production was significantly reduced by clipping. Pollinator visitation and nectar robbing were variable between clipping treatments and between years and (nectar robbing) among sites. Our results demonstrate that the variability in plant response to herbivory can, at least in part, be driven by plant interactions with mutualists and enemies. Thus, accounting for such interactions and their variability is important to fully understanding plant compensation for herbivore damage and will likely go far to explain variation in plant response that appears to be independent of resources.     

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.

     

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.     

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.     

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.     

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.     

Nectar robbing improves male reproductive success of the endangered Aconitum napellus ssp. lusitanicum

Nectar robbery is usually thought to impact negatively on the reproductive success of plants, but also neutral or even positive effects have been reported. Very few studies have investigated the effects of nectar robbing on the behaviour of legitimate pollinators so far. Such behavioural changes may lead to the reduction of geitonogamy or to increased pollen movement. We simulated nectar robbing in experimental sites as well as in natural populations of Aconitum napellus ssp. lusitanicum, a rare plant pollinated by long-tongued bumblebees. In an experimental setup, we removed the nectaries of 40 % of the flowers, which is similar to rates of robbing observed in wild populations. Patches of plants with experimentally robbed flowers were compared with control patches containing plants with untreated flowers. We observed pollinator behaviour, mimicked male reproductive success (pollen dispersal) using fluorescent dye, and measured female reproductive success (seed set). The main legitimate visitors were bumblebees while honeybees were often observed robbing nectar. They did so by “base working”, i.e. sliding between tepals. Bumblebees tended to visit fewer flowers per plant and spent less time per single flower when these had been experimentally robbed. This change in behaviour consequently increased the proportion of flowers visited by bumblebees in patches with robbed flowers. Fluorescent dye mimicking pollen flow was dispersed larger distances after pollinators had visited patches with robbed flowers compared to control patches. Average seed set per plant was not affected by nectar robbing. Our results demonstrated that A. napellus does not suffer from nectar robbery but may rather benefit via improved pollen dispersal and thus, male reproductive success. Knowledge on such combined effects of behavioural changes of pollinators due to nectar robbery is important to understand the evolutionary significance of exploiters of such mutualistic relationships between plants and their pollinators.     

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     

A positive association between oviposition and fruit set: female choice or manipulation?

The relationship between where a female chooses to oviposit and her larvae’s performance at those sites is critical to both the ecology and evolution of plant-insect interactions. For predispersal seed predators that do not themselves pollinate their host and whose larvae are sessile, females must be able to predict which flowers will ultimately be pollinated and set fruit, or be able to manipulate flowers in some way to ensure they set fruit. Otherwise, their offspring will perish. Here we describe the results of an experiment in which we tested if female Hylemya (Diptera: Anthomyiidae) are choosing oviposition sites wisely, or if they are manipulating flowers of their host, Ipomopsis aggregata (Polemoniaceae), in some way to ensure fruit set. Previous work in this system established a positive correlation between oviposition and fruit set. By bagging females on flowers, we removed their ability to choose flowers on which to oviposit. We found that flowers females oviposited on, whether bagged (”no choice”) or unbagged (”female choice”), had a significantly higher probability of setting fruit than ”control” flowers that we bagged but did not cage females on. In addition, we tested if Hylemya prefer particular architectural locations of flowers and if those locations correspond with higher than average fruit set. Although flowers at the distal end of the plant, and those most proximal to the main stem, were more likely to set fruit overall, Hylemya was no more likely to oviposit on those flowers than others on the plant. Taken together, our results suggest that Hylemya is somehow able to manipulate its host to ensure fruit set and thus the provisioning of their larvae. Received: 3 December 1999 / Accepted: 23 March 2000     

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 alkaloids decrease pollination and female reproduction in a native plant

The evolution of floral traits may be shaped by a community of floral visitors that affect plant fitness, including pollinators and floral antagonists. The role of nectar in attracting pollinators has been extensively studied, but its effects on floral antagonists are less understood. Furthermore, the composition of non-sugar nectar components, such as secondary compounds, may affect plant reproduction via changes in both pollinator and floral antagonist behavior. We manipulated the nectar alkaloid gelsemine in wild plants of the native perennial vine Gelsemium sempervirens. We crossed nectar gelsemine manipulations with a hand-pollination treatment, allowing us to determine the effect of both the trait and the interaction on plant female reproduction. We measured pollen deposition, pollen removal, and nectar robbing to assess whether gelsemine altered the behavior of mutualists and antagonists. High nectar gelsemine reduced conspecific pollen receipt by nearly half and also reduced the proportion of conspecific pollen grains received, but had no effect on nectar robbing. Although high nectar gelsemine reduced pollen removal, an estimate of male reproduction, by one-third, this effect was not statistically significant. Fruit set was limited by pollen receipt. However, this effect varied across sites such that the sites that were most pollen-limited were also the sites where nectar alkaloids had the least effect on pollen receipt, resulting in no significant effect of nectar alkaloids on fruit set. Finally, high nectar gelsemine significantly reduced seed weight; however, this effect was mediated by a mechanism other than pollen limitation. Taken together, our work suggests that nectar alkaloids are more costly than beneficial in our system, and that relatively small-scale spatial variation in trait effects and interactions could determine the selective impacts of traits such as nectar composition.     

Wise flies: a pre‐dispersal seed predator prefers hermaphrodites over females in the gynodioecious Polemonium foliosissimum

1. Oviposition choices can profoundly affect offspring performance. Oviposition decisions of the dipteran pre‐dispersal seed predator, Hylemya sp. (Diptera: Anthomyiidae), when choosing among sex morphs of their host‐plant—Polemonium foliosissimum Hook—were evaluated. Polemonium foliosissimum is gynodioecious, with female and hermaphrodite sex morphs that differ in flower size. 2. It was asked: Do female flies preferentially oviposit on hermaphrodite plants and, if so, are oviposition choices correlated with flower size? Is larval survivorship higher on hermaphrodite plants and, if so, is larval success correlated with flower size? Can the differences in oviposition and/or larval success be explained by slight differences in flowering phenology between the sexes? 3. Hermaphrodite flowers received 45% more Hylemya eggs than females. Although hermaphrodites had larger petals and sepals than females, egg loads were not correlated with petal or sepal size. Larval survival was 30% greater on hermaphrodites than females and higher on plants with larger sepals. However, the difference in sepal area between genders did not fully explain larval survival differences. Egg numbers declined over weeks, but differences in egg loads between the sex morphs were not attributable to a slight phenological delay of females. Larval survival declined over the season; however, larval survival differences between sex morphs were consistent. 4. Hylemya preferentially oviposited on hermaphrodites where their larvae had a significantly greater survival rate compared with females. The present results add to the knowledge that intra‐specific choices have consequences for phytophagous insects and that the relationship between antagonists and their gynodioecious host plants is complex.     

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.     

Differential effects of nectar robbing by the same bumble-bee species on three sympatric Corydalis species with varied mating systems

Background and Aims

Most research on the widespread phenomenon of nectar robbing has focused on the effect of the nectar robbers'' behaviour on host-plant fitness. However, attention also needs be paid to the characteristics of host plants, which can potentially influence the consequences of nectar robbing as well. A system of three sympatric Corydalis species sharing the same nectar-robbing bumble-bee was therefore studied over 3 years in order to investigate the effect of nectar robbing on host reproductive fitness.

Methods

Three perennial species of Corydalis were studied in the Shennongjia Mountain area, central China. Observations were conducted on visitor behaviour and visitation frequencies of nectar-robbers and legitimate pollinators.

Key Results

The results indicated that the effect of nectar robbing by Bombus pyrosoma varied among species, and the three species had different mating systems. Seed set was thus influenced differentially: there was no effect on seed set of the predominantly selfing C. tomentella; for the facultative outcrossing C. incisa, nectar robbing by B. pyrosoma had a positive effect; and nectar robbing had a significant negative effect on the seed set of outcrossing C. ternatifolia.

Conclusions

A hypothesis is proposed that the type of host-plant mating system could influence the consequences of nectar robbing on host reproductive fitness.Key words: Nectar robbing, Corydalis, reproductive fitness, bumble-bee, Bombus pyrosoma, mating systems     

Plant reproductive strategies vary under low and high pollinator densities

Long‐term variation in the population density of honey bees Apis mellifera across landscapes has been shown to correlate with variation in the floral traits of plant populations in these landscapes, suggesting that variations in pollinator population density and foraging rates can drive floral trait evolution of their host plants. However, it remained to be determined whether this variation in plant traits is associated with adaptive variation in plant reproductive strategies under conditions of high and low pollinator densities. Here we conducted a reciprocal transplant experiment to examine how this variation in floral traits, under conditions of either high and low pollinator density, impacted seed production in the Tibetan lotus Saussurea nigrescens. In 2014 and 2015, we recorded the floral traits, pollinator visitation rates, and seed production of S. nigrescens populations grown in both home sites and foreign sites, where sites varied in honey bee population density. Our results demonstrated that the floral traits reflected those of their original population, regardless of their current location. However, seed production varied with both population origin and transplant site. Seed number was positively correlated with flower abundance in the pollinator‐rich sites, but with nectar production in the pollinator‐poor sites. Pollinator visitation rate was also positively correlated with flower number at pollinator‐rich sites, and with nectar volume at pollinator‐poor sites. Overall, the local genotype had higher seed production than nonlocal genotypes in home sites. However, when pollen is hand‐supplemented, plants from pollinator‐rich populations had higher seed production than plants from pollinator‐poor populations, regardless of whether they were transplanted to pollinator‐rich or ‐poor sites. These results suggest that the plant genotypic differences primarily drive variation in pollinator attraction, and this ultimately drives variation in seed: ovule ratio. Thus, our results suggest that flowering plant species use different reproductive strategies to respond to high or low pollinator densities.     

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。     

Community-dependent foraging habits of flower visitors: cascading indirect interactions among five bumble bee species

Despite the ubiquity and the importance of interspecific interactions among flower visitors, few studies have examined their effects on the realized feeding niches of visitor species in a community context. To evaluate the community-wide effects of interactions among flower visitors, I have examined changes in the flower utilization patterns of each visitor species at several sites where the component of the visitor’s community differed. Specifically, I compared the flower preferences and foraging habits (legitimate foraging vs. primary nectar robbing vs. secondary nectar robbing) of five bumble bee species in flower patches consisting of Trifolium pratense L. (red clover) and T. repens L. (white clover) on Hokkaido Island, Japan. I also examined the nectar production and standing crops of each flower species to evaluate the exploitation competition based on nectar. The bumble bee species exhibited different flower utilization patterns among sites. At sites where the long-tongued Bombus diversus tersatus was common and the exotic short-tongued B. terrestris was rare, B. diversus tersatus visited red clover (long-tubed flowers) exclusively, whereas medium-tongued B. pseudobaicalensis and short-tongued B. hypocrita sapporoensis and B. hypnorum koropokkrus preferentially visited white clover (short-tubed flowers). Conversely, at sites where the long-tongued bee was rare, four other species frequently visited red clover in different modes: B. pseudobaicalensis visited legitimately, B. hypocrita sapporoensis and B. terrestris visited as primary nectar robbers, and B. hypnorum koropokkrus visited as a secondary nectar robber. The presence or absence of resource exploitation by the long-tongued species and the interaction between primary and secondary nectar robbers via robbing holes was the major ecological sources of these differences. Diverse effects of interactions among flower visitors played important roles in shaping pattern of plant and flower visitor interactions.     

Nectar robbing impacts pollinator behavior but not plant reproduction

Trait‐mediated indirect effects (TMIEs) refer to interactions in which the effect of one species on another is mediated by the behavior of a third species. A mechanistic approach that identifies the direction and impact of TMIEs can shed light on why different net outcomes are observed in the same general phenomena across systems. Nectar robbing has variable net effects through TMIEs on animal‐pollinated plants across systems, but the mechanistic steps underlying this range of outcomes are often unclear. To address this knowledge gap, we assessed linkages between nectar robbing, pollinator behavior and plant reproductive success in the Andean tree, Oreocallis grandiflora. We found that robbing in this system led to lower nectar volumes, higher nectar sucrose concentration, and higher nectar viscosity, which together negatively impact nectar quality. This drop in nectar quality was associated with decreased visitation rates by hummingbirds, which might be expected to impact plant reproduction negatively by pollen limitation. However, it was also associated with increased diversity (Shannon's) and evenness in the pollinator community due to reduced visitation by a territorial hummingbird, which might be expected to impact reproduction positively via enhanced genetic diversity of pollen as non‐territorial pollinators forage over greater areas. We measured seed set and mass to distinguish the relative intensity of these two possible outcomes, but found no detectable effect. We tentatively conclude that these two consequences of TMIEs may have balanced each other out to yield a neutral net effect of nectar robbing on plant reproduction, though other explanations are also possible. This study highlights ways in which ecologically important TMIEs may act in opposing directions to mask important ecological forces, and underscores the continued need for detailed study of the mechanisms through which TMIEs operate.     

Sugar landscapes and pollinator‐mediated interactions in plant communities

Pollinator‐mediated interactions between plants can play an important role for the dynamics of plant communities. Pollination services depend on the abundance and the foraging behaviour of pollinators, which in turn respond to the availability and distribution of floral resources (notably nectar sugar). However, it is still insufficiently understood how the ‘sugar landscapes’ provided by flowering plant communities shape pollinator‐mediated interactions between multiple plant species and across different spatial scales. A better understanding of pollinator‐mediated interactions requires an integrative approach that quantifies different aspects of sugar landscapes and investigates their relative importance for pollinator behaviour and plant reproductive success. In this study, we quantified such sugar landscapes from individual‐based maps of Protea shrub communities in the Cape Floristic Region, South Africa. The 27 study sites of 4 ha each jointly comprise 127 993 individuals of 19 species. We analysed how rates of visitation by key bird pollinators and the seed set of plants respond to different aspects of sugar landscapes: the distribution of nectar sugar amounts, as well as their quality, taxonomic purity and phenology. We found that pollinator visitation rates strongly depended on phenological variation of site‐scale sugar amounts. The seed set of focal plants increased with nectar sugar amounts of conspecific neighbours and with site‐scale sugar amounts. Seed set increased particularly strongly if site‐scale sugar amounts were provided by plants that offer less sugar per inflorescence. These combined effects of the amount, quality, purity and phenological variation of nectar sugar show that nectar sugar is a common interaction currency that determines how multiple plant species interact via shared pollinators. The responses of pollinator‐mediated interactions to different aspects of this interaction currency alter conditions for species coexistence in Protea communities and may cause community‐level Allee effects that promote extinction cascades.