Nectar Robbers Research Articles

Impacts of nectar robbing on the foraging ecology of a territorial hummingbird

While the effects of nectar robbing on plants are relatively well-studied, its impacts from the perspective of the pollinators of robbed plants is not. Numerous studies do consider the impacts of robbing on pollinator visitation to robbed plants, but rarely do they focus on its scaled-up impacts on individual pollinator behavior. We used radio telemetry to track the spatial and behavioral responses of the territorial hummingbird Aglaeactis cupripennis to experimental nectar robbing over a period of several days. Simulated nectar robbing impacted foraging behavior by increasing territory area, distance flown, and reliance on novel food resources, especially small-bodied flying insects. We did not observe any impact on the amount of time individuals spent foraging, nor did we observe territory abandonment. These findings indicate that nectar robbing may impose a significant energetic cost on pollinators via increased flight distances and shifts towards potentially less profitable food resources, and demonstrate the importance of quantifying the indirect effects of nectar robbing on pollinators in addition to plants.

Differential Outcomes of Nectar Robbing on the Reproductive Success of a Melittophilous and an Ornithophilous Species

Premise of research. Nectar robbers can affect pollinator behavior and indirectly affect plant fitness. The signal of such effects (positive, neutral, or negative) may depend on how the primary pollinators of a given plant species respond to robbed flowers. Comparative studies are important to give insight on which factors are linked to these differential outcomes of nectar robbing on plant reproductive success. Here, we investigated the effect of a common Neotropical nectar robber, the stingless bee, Trigona spinipes (Apidae), on the reproductive success of the bee-pollinated Crotalaria vitellina (Fabaceae) and the hummingbird-pollinated Besleria longimucronata (Gesneriaceae).Methodology. We compared the robbing rate (number of flowers robbed relative to total flower display) between species and evaluated the effect of robbing on plant reproductive success by comparing the seed number per fruit of robbed fruits (identified by the presence of scars in the calyx, caused by the robber) with that of intact f...

Ornithophily for the nonspecialist: Differential pollination efficiency of the Macaronesian island paleoendemic Navaea phoenicea (Malvaceae) by generalist passerines.

A bird pollination syndrome exists in the Canary Islands archipelago across independent plant lineages despite the absence of specialist birds. The pollination efficiency of current floral visitors remains unknown for many plant species despite this being a fundamental factor in testing hypotheses about the origin of the syndrome. Here, we studied the components of pollination efficiency in the paleoendemic Navaea phoenicea, a species exhibiting conspicuous anatomical modifications associated with bird pollination. We measured the components of the pollination efficiency (PE) of species foraging on flowers. The measured quantitative components were visitation frequency patterns to plants and individual flowers. The qualitative components were the contributions to the fitness of male and female functions (pollen removal and deposition and fruit set). Pollination by warbler species was highly efficient, but visit frequency was low; conversely, Canarian chiffchaffs had high visit frequency and low efficiency. Overall PE was almost 0 for blue tits due to disruptive behavior. We also found insects acting as nectar robbers. Pollination efficiency of three of the four bird species visiting flowers of Navaea phoenicea may be high enough to maintain selective pressure on floral traits of a relict pollination syndrome. The behavior of these birds plays a crucial role in their pollination efficiency. Perching, by generalist passerines when visiting N. phoenicea flowers, is the most efficient habit. The frequency and PE of insect visits calls into question their role as legitimate visitors.

Anti-adhesive effects of plant wax coverage on insect attachment.

The long period of reciprocal antagonistic coevolution between some insect and plant species has led to the development of plant surface attributes that reduce insect attachment. These features serve as a defence against herbivores, sap-sucking insects and nectar robbers, contribute to a temporary capture of insect pollinators, and prevent the escape of insects from traps of carnivorous plants. This review summarises the literature on attachment-mediated insect-plant interactions. A short introduction to attachment systems of insects is presented and the effect of three-dimensional epicuticular waxes on insect attachment is illustrated by many examples. Special attention is given to the mechanisms of the anti-attachment properties of plant wax structures (the roughness hypothesis, the contamination hypothesis, the fluid-adsorption hypothesis, and the wax-dissolving hypothesis) and their ecological implications.

Distasteful Nectar Deters Floral Robbery

Toxic nectar is an ecological paradox [1, 2]. Plants divert substantial resources to produce nectar thatattracts pollinators [3], but toxins in this rewardcould disrupt the mutualism and reduce plant fitness [4]. Alternatively, such compounds could protect nectar from robbers [2], provided that they do not significantly alter pollinator visitation to the detriment of plant fitness [1, 5-8]. Indeed, very few studies have investigated the role of plant toxins in nectar for defense against nectar robbers [4, 9, 10]. Here, we compared two Aconitum species (A.napellus and A.lycoctonum) that have flowers specialized for long-tongued bumblebee pollinators (Bombus hortorum) but are occasionally robbed by short-tongued bumblebees (B.terrestris) [6, 11-13]. Pollinator visits to flowers were much more frequent than by robbers, but visits correlated negatively with nectar alkaloid concentration and declined sharply between 200 and 380 ppm. However, alkaloid concentrations of>20 ppm were deterrent to B.terrestris, suggesting that robbers were less tolerant of nectar alkaloids. Nectar of both plant species contained similar concentrations of carbohydrates and toxic alkaloids, but A.lycoctonum was more likely to secrete nectar in each flower and was also visited more frequently by pollinators and robbers. We conclude that alkaloids in Aconitum spp. nectar affect rates ofboth pollinator visitation and robbery but may have co-evolved with nectar availability to maintain the fitness benefits of specialized plant-pollinator relationships. Chemical defense of nectar is, however, ultimately constrained by pollinator gustatory sensitivity.

Pin-monomorphism in Palicourea crocea (SW.) Roem. & Schult. (Rubiaceae): reproductive traits and role of floral visitors

Although heterostyly frequently occurs in Rubiaceae, there are cases of distylous species with populations that have variations in their reproductive systems. For example, in the typically distylous genus Palicourea, P. crocea showed a pin-monomorphism. Considering this, the questions addressed in the present study were: (1) Are there other pin-monomorphic Palicourea crocea populations? (2) How important are flower visitors to the pollination of this species? (3) What is the compatibility system in P. crocea? In addition, we tested the hypothesis that P. crocea is self-compatible and autogamous that can be a result of a variation in the distylous pattern. To answer the questions, we verified the position of anthers and stigmas in flowers of other populations of Palicourea crocea using voucher specimens. Furthermore, we made focal observations to analyze the role of flower visitors and we made field experiments to verify the compatibility system in P. crocea. Among seven flower visitors species observed—four bees, one wasp, one butterfly and one hummingbird—the latter was considered the main pollinator due to its high frequency of visits at all times analyzed. However, the small size of the population in the study area, the territorial behavior of hummingbirds, and the activity of nectar robbers may contribute to a low pollen flow. In this situation, traits as self-compatibility and autogamy observed in Palicourea crocea are beneficial, since they maintain species fertility. This could represent a new evolutionary path for the reproduction of this population, different from that of P. crocea populations that display distinct floral morphs.

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.

Pollination ecology of Clerodendrum indicum (Lamiaceae): first report of deceit pollination by anther-mimicking stigma in a bisexual flower

Clerodendrum indicum (Lamiaceae) is a medicinally important shrub. We have studied the details of its pollination ecology which was hitherto unknown. The work was done during three consecutive years 2012-2014, based on 118 plants occurring in three widely separated wild populations in West Bengal, India, together with 25 individuals grown in an experimental plot. Details of flower structure and dynamics of floral events, pollen production and pollen dispersal, visitors and pollinators, floral attractants and floral rewards and pollen transfer mechanism have been worked out by standard methodologies with a 10x high resolution hand lens (IRL), a Leica WILD M3B Stereo-binocular microscope (Switzerland) and a Leica DMLB compound bright field light microscope (Germany). The tubular flower of four-day longevity attracts its visitors by visual cues. Flowers are visited regularly by ten species of insects. On the basis of the visitor behaviour, these can be classified into three distinct categories, viz., visitors belonging to Category-I act on cushion and trichome nectaries of calyx and corolla respectively, those of Category-II act on the dehisced anthers and trichome nectaries of corolla while those of Category-III act on dehisced anthers as well as receptive stigma. Majority of the visitors belong to either Category-I or Category-II. They visit only the 2nd day flowers and never visit a 3rd day flower when the stigma assumes receptivity. Therefore, they are not regarded as pollinators but, act as pollen and/or nectar robbers. Those are discriminated by offering secretions from extra-nuptial nectaries of the flower. Visitor species of Category-III, represented by a species of Trigona, constitute the legitimate pollinator of the plant and thereby, making the plant monophilic. Pollen presentation from the bisexual, dichogamous and protandrous flower takes place on the 2nd day, while the stigma assumes its receptivity on the 3rd day of flower opening. Pollen transfer to the body of the pollinator by a 2nd day flower in its male phase is achieved by offering edible pollen grains. On the other hand, a 3rd day flower at its female phase is devoid of the reward (pollen grain). The yellow shiny receptive stigma of such a flower strikingly mimics the freshly dehisced anthers and the pollinators being lured by such a stigma inadvertently transfer pollen onto it. C. indicum is so far the only known species of flowering plants where deceit pollination occurs by anther-mimicking stigma in a bisexual flower.

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 replenishment maintains the neutral effects of nectar robbing on female reproductive success of Salvia przewalskii (Lamiaceae), a plant pollinated and robbed by bumble bees.

It has been suggested that the dynamics of nectar replenishment could differ for flowers after being nectar robbed or visited legitimately, but further experimental work is needed to investigate this hypothesis. This study aimed to assess the role of nectar replenishment in mediating the effects of nectar robbing on pollinator behaviour and plant reproduction. Plant-robber-pollinator interactions in an alpine plant, Salvia przewalskii , were studied. It is pollinated by long-tongued Bombus religiosus and short-tongued B. friseanus , but robbed by B. friseanus . Nectar production rates for flowers after they were either robbed or legitimately visited were compared, and three levels of nectar robbing were created to detect the effects of nectar robbing on pollinator behaviour and plant reproduction. Nectar replenishment did not differ between flowers that had been robbed or legitimately visited. Neither fruit set nor seed set was significantly affected by nectar robbing. In addition, nectar robbing did not significantly affect visitation rate, flowers visited within a plant per foraging bout, or flower handling time of the legitimate pollinators. However, a tendency for a decrease in relative abundance of the pollinator B. religiosus with an increase of nectar robbing was found. Nectar robbing did not affect female reproductive success because nectar replenishment ensures that pollinators maintain their visiting activity to nectar-robbed flowers. Nectar replenishment might be a defence mechanism against nectar robbing to enhance reproductive fitness by maintaining attractiveness to pollinators. Further studies are needed to reveal the potential for interference competition among bumble bees foraging as robbers and legitimate visitors, and to investigate variation of nectar robbing in communities with different bumble bee species composition.

Nectar Robbing Behavior of the Horned Sungem Hummingbird (Heliactin bilophus) (Birds: Trochilidae) in Two Species Plant the Genus Amphilophium kunth (Bignoniaceae) and Sinningia Nees (Gesneriaceae)

The Horned Sungem Hummingbird ( Heliactin bilophus ) is a typical savannah hummingbird inhabiting opened phytophysiognomies in areas of Cerrado, Caatinga, highlands and plains with low vegetation. There are few studies about its feeding habits and little known about its behavior patterns. Here we report the bird feed behavior on two plant species Amphilophium elongatum and Sinningia sp. Trough illegitimate visits to the floral nectary, H. bilophus obtained food acting as a nectar robber. This foraging strategy included new sources of food for the hummingbird and could represent negative effects to the related plant species. Keywords: bird-flower interactions; food resources; floral visitor.

Species interactions in an Andean bird-flowering plant network: phenology is more important than abundance or morphology.

Biological constraints and neutral processes have been proposed to explain the properties of plant–pollinator networks. Using interactions between nectarivorous birds (hummingbirds and flowerpiercers) and flowering plants in high elevation forests (i.e., “elfin” forests) of the Andes, we explore the importance of biological constraints and neutral processes (random interactions) to explain the observed species interactions and network metrics, such as connectance, specialization, nestedness and asymmetry. In cold environments of elfin forests, which are located at the top of the tropical montane forest zone, many plants are adapted for pollination by birds, making this an ideal system to study plant–pollinator networks. To build the network of interactions between birds and plants, we used direct field observations. We measured abundance of birds using mist-nets and flower abundance using transects, and phenology by scoring presence of birds and flowers over time. We compared the length of birds’ bills to flower length to identify “forbidden interactions”—those interactions that could not result in legitimate floral visits based on mis-match in morphology. Diglossa flowerpiercers, which are characterized as “illegitimate” flower visitors, were relatively abundant. We found that the elfin forest network was nested with phenology being the factor that best explained interaction frequencies and nestedness, providing support for biological constraints hypothesis. We did not find morphological constraints to be important in explaining observed interaction frequencies and network metrics. Other network metrics (connectance, evenness and asymmetry), however, were better predicted by abundance (neutral process) models. Flowerpiercers, which cut holes and access flowers at their base and, consequently, facilitate nectar access for other hummingbirds, explain why morphological mis-matches were relatively unimportant in this system. Future work should focus on how changes in abundance and phenology, likely results of climate change and habitat fragmentation, and the role of nectar robbers impact ecological and evolutionary dynamics of plant–pollinator (or flower-visitor) interactions.

Native Bee Diversity and Pollen Foraging Specificity in Cultivated Highbush Blueberry (Ericaceae: Vaccinium corymbosum) in Rhode Island.

We identified 41 species of native bees from a total of 1,083 specimens collected at cultivated highbush blueberry plantings throughout Rhode Island in 2014 and 2015. Andrena spp., Bombus spp., and Xylocopa virginica (L.) were collected most often. Bombus griseocollis (DeGeer), B. impatiens Cresson, B. bimaculatus Cresson, B. perplexus Cresson, and Andrena vicina Smith collected the largest mean numbers of blueberry pollen tetrads. The largest mean percent blueberry pollen loads were carried by the miner bees Andrena bradleyi Viereck (91%), A. carolina Viereck (90%), and Colletes validus Cresson (87%). The largest mean total pollen grain loads were carried by B. griseocollis (549,844), B. impatiens (389,558), X. virginica (233,500), and B. bimaculatus (193,132). Xylocopa virginica was the fourth and fifth most commonly collected bee species in 2014 and 2015, respectively. They exhibit nectar robbing and females carried relatively low blueberry pollen loads (mean 33%). Overall, we found 10 species of bees to be the primary pollinators of blueberries in Rhode Island.

Geographic distribution and trait-mediated causes of nectar robbing by the European bumblebee Bombus terrestris on the Patagonian shrub Fuchsia magellanica

Invasive floral visitors may obtain nectar rewards from native plants exerting nectar robbing. Nevertheless, the probability of a plant to be robbed will ultimately depend upon the accessibility constraints imposed by the phenotypes of flowers and animals, and putatively upon the abundance of animals. The alien bumblebee B. terrestris is widely distributed in the temperate forests of Chile, where it is exerting nectar robbing on flowers of F. magellanica. Its geographic distribution and the causes of nectar robbing, however, are currently unknown. The aim of this study is to evaluate the distribution of nectar robbing in a wide range of distribution of plants and animals, and the causes of nectar robbing in terms of floral and animal phenotypes, and in terms of animal abundances. The primary nectar robbing did not correlate with the latitude, longitude or altitude of populations, thus indicating an absence of cline variation in the causes of nectar robbing. The variability of primary nectar robbing seemingly showed a bimodal distribution, since the most represented categories were the low and high incidence of primary nectar robbing. Petal length, rather than other flora traits, coupled to the glossa length of animals, played a pivotal role in the probability of flowers to experience nectar robbing. The putative negative consequences upon the population persistence and the evolution and maintenance of floral phenotypes of hummingbird-pollinated plants strongly encourage new assessments.

Facilitated exploitation of pollination mutualisms: fitness consequences for plants

Summary Mutualisms are only rarely one‐to‐one interactions: each species generally interacts with multiple mutualists. Exploitation is ubiquitous in mutualisms, and we would therefore expect that each mutualist interacts with multiple exploiters as well. Exploiter species may also interact with one another. For example, the action of one exploiter species might open the opportunity for exploitation by a second species. Exploitation is common in many plant–pollinator mutualisms: ‘primary’ nectar robbers feed through holes they make in flowers, which can be subsequently used by ‘secondary’ nectar robbers unable to create holes themselves. The overall effect of nectar robbing on plant fitness is often (although not always) negative. No study has separated the effects of interacting with primary vs. secondary robbers. Here, we examine the effects of primary vs. secondary nectar robbing on pollinator visitation rate and female fitness in Ipomopsis aggregata. Manipulating the type of nectar robbing that flowers experienced, we found that secondary nectar robbing inflicted fitness costs to plants beyond that inflicted by primary robbing alone. Secondary nectar robbing significantly reduced pollen receipt to flowers, as well as fruit and seed production. Although the causes are elusive, the effect may be attributed to changes in pollinator behaviour at these plants. Synthesis. Our findings provide evidence that interacting with multiple exploiters can lead to increased negative effects for mutualists, and highlight the importance of incorporating multiple exploiters into the conceptual framework of mutualism.

Geographic variation in resistance to nectar robbing and consequences for pollination

Floral evolution is frequently ascribed to selection by pollinators, but may also be shaped by antagonists. However, remarkably few studies have examined geographic mosaics in resistance to floral antagonists or the consequences for other floral interactions. Gelsemium sempervirens experiences frequent nectar robbing in northern Georgia, but rarely in southern Georgia. We conducted common-garden experiments in both locations using genotypes from each region and measured robbing, pollinator attraction, floral attractive and defensive traits, and plant reproduction. Nectar robbing was more than four times higher in the north vs. south, and pollinator visits did not differ between gardens. Across both gardens, northern genotypes were half as likely to be nectar-robbed but received half as many pollinator visits as southern genotypes, suggesting evolution of resistance to robbing at a cost of reduced pollinator attraction. Plant-level traits, such as height and number of flowers, were more closely associated with resistance to robbing than floral size, shape, or chemistry. Northern genotypes had lower female and estimated male reproduction compared to southern genotypes at both locations, which could be due to costs of resistance to nectar robbing, or costs of adaptations to other biotic or abiotic differences between regions. Our study indicates that geographic variation can play a strong role structuring interactions with floral antagonists and mutualists and provides evidence consistent with the hypothesis that local resistance to nectar robbing imposes costs in terms of decreased pollinator attraction and reproduction.

Floral Variation, Nectar Production, and Reproductive Success of Two Drymonia (Gesneriaceae) Species with Mixed Pollination Syndromes

Premise of research. Pollination syndromes are suites of correlated characters that reflect selection by most frequent and effective pollinators. However, the floral phenotypes of some angiosperm species combine traits from different pollination syndromes. The aim of this study was to assess the correspondence between floral traits and floral visitors, considering the breeding systems of two co-occurring Drymonia species with mixed floral phenotypes.Methodology. We assessed floral morphology, nectar production patterns, frequency of floral visitation, breeding systems, and natural fruit set in Drymonia strigosa and Drymonia oinochrophylla species at Los Tuxtlas, Veracruz, Mexico, during 2011–2014. We also conducted a field test of reproductive assurance in D. strigosa, the only species with a high potential for autonomous self-pollination.Pivotal results. In D. strigosa, morphology and nectar production patterns correspond to the ornithophilous syndrome; however, anthers have poricidal dehiscence, a trait associated with bee pollination. Hummingbirds were the most frequent floral visitors, and stingless bees were less frequent visitors acting mostly as nectar robbers. The species has a high autofertility potential, but autonomous self-pollination contributed little to fruit set during the study years. In D. oinochrophylla, most floral traits correspond to the melittophilous syndrome; however, high nectar production and large flower size resemble traits of chiropterophilous flowers. Primary pollinators were bees with less frequent visits by butterflies and moths; bats were not observed during the study period. Drymonia oinochrophylla is self-compatible, but it has little potential for autonomous self-pollination; therefore, seed production is highly dependent on pollinators.Conclusions. Our results suggest that mixed floral phenotypes in the two Drymonia species are not likely a consequence of visitation by multiple pollinator functional groups. Instead, incomplete correspondence of floral traits with classic pollination syndromes may represent undetected floral visitors in disturbed environments or plesiomorphies retained throughout the evolutionary history of the genus Drymonia.

Pollination ecology of Clerodendrum inerme (L.) Gaertn. (Lamiaceae) in Coringa mangrove ecosystem, Andhra Pradesh, India

Clerodendrum inerme (L.) Gaertn. (Lamiaceae) is bisexual, self-compatible and has a vector-dependent mixed breeding system. They are dichogamous and herkogamous; the day 1 flowers are staminate while the day 2 and 3 flowers are pistillate. The plant blooms in the evening, possesses a white long corolla with a hairy interior to exclude other insects and strong fragrance are adaptations for pollination by the hawk-moth Macroglossum gyrans. The 2nd and 3rd day flowers are nectar-rich and attract hawk-moths during the dawn and dusk hours. The plant is also visited by bees and butterflies. The bees Xylocopa and Anthophora are primary nectar robbers which collect nectar without effecting pollination. In C. inerme, three forms of flowers can be distinguished based on the position of sex organs. The first form is characterized by elongated stamens and a style which occur in close proximity to each other just after anthesis facilitating contact between the stamens and stigma. The second form is characterized by the scattered position of stamens and style. In the third form, the stamens are fully extended while the style is curved away from them, either to the left or to the right; subsequently the stamens curl inward and the style elongates. Interestingly, the three flower forms can be found within a cyme also. These forms of flowers with strong protandry prevent autonomous selfing but not geitonogamy. The fruit is a capsule and breaks open to disperse nutlets. Birds such as Acridotheres tristis, Corvus splendens, Corvus macrorhynchos and Turdoides caudatus disperse nutlets during the early winter season. Seeds germinate in June and seedlings grow gradually to produce new plants.

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

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

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.