Nectar yeasts enhance the interaction between Clematis akebioides and its bumblebee pollinator

• It has been hypothesised that intense metabolism of nectar‐inhabiting yeasts (NIY) may change nectar chemistry, including volatile profile, which may affect pollinator foraging behaviours and consequently plant fitness. However, empirical evidence for the plant–microbe–pollinator interactions remains little known.
• To test this hypothesis, we use a bumblebee‐pollinated vine Clematis akebioides endemic to southwest China as an experimental model plant. To quantify the incidence and density of Metschnikowia reukaufii, a cosmopolitan NIY in floral nectar, a combination of yeast cultivation and microscopic cell‐counting method was used. To examine the effects of NIY on plant–pollinator interactions, we used real flowers filled with artificial nectar with or without yeast cells. Then the volatile metabolites produced in the yeast‐inoculated nectar were analysed with coupled gas chromatography and mass spectrometry (GC‐MS).
• On average 79.3% of the C. akebioides flowers harboured M. reukaufii, and cell density of NIY was high to 7.4 × 10⁴ cells mm^?3. In the field population, the presence of NIY in flowers of C. akebioides increased bumblebee (Bombus friseanus) pollinator visitation rate and consequently seed set per flower. A variety of fatty acid derivatives produced by M. reukaufii may be responsible for the above beneficial interactions.
• The volatiles produced by the metabolism of M. reukaufii may serve as an honest signal to attract bumblebee pollinators and indirectly promote the female reproductive fitness of C. akebioides, forming a potentially tripartite plant–microbe–pollinator mutualism.

     

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.     

Florivory indirectly decreases the plant reproductive output through changes in pollinator attraction

Species often interact indirectly with each other via their traits. There is increasing appreciation of trait‐mediated indirect effects linking multiple interactions. Flowers interact with both pollinators and floral herbivores, and the flower‐pollinator interaction may be modified by indirect effects of floral herbivores (i.e., florivores) on flower traits such as flower size attracting pollinators. To explore whether flower size affects the flower‐pollinator interaction, we used Eurya japonica flowers. We examined whether artificial florivory decreased fruit and seed production, and also whether flower size affected florivory and the number of floral visitors. The petal removal treatment (i.e., artificial florivory) showed approximately 50% reduction in both fruit and seed set in natural pollination but not in artificial pollination. Furthermore, flower size increased the number of floral visitors, although it did not affect the frequency of florivory. Our results demonstrate that petal removal indirectly decreased 75% of female reproductive output via decreased flower visits by pollinators and that flower size mediated indirect interactions between florivory and floral visitors.     

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.     

Can short‐billed nectar thieving sunbirds replace long‐billed sunbird pollinators in transformed landscapes?

• Pollinator specialisation through exploitation barriers (such as long floral tubes) does not necessarily mean a lack of pollination when the favoured pollinator is rare or absent. Theory predicts that suboptimal visitors will contribute to plant reproduction in the absence of the most effective pollinator. Here I address these questions with Chasmanthe floribunda a long‐tubed plant species in the Cape Floristic Region, which is reliant on one species of pollinator, the long‐billed Malachite Sunbird. In contrast to short‐billed sunbirds, the Malachite Sunbird occurs in lower abundance or is absent in transformed landscapes. Short‐billed sunbirds rob and thieve nectar from long‐tubed flowers, but their potential contribution towards pollination is unknown.
• Experiments assessing seed set after single flower visits were performed to determine whether thieving short‐billed sunbirds can act as substitute pollinators. To determine whether short‐billed sunbirds reduce pollen limitation in transformed areas, pollen supplementation was done by hand and compared to natural fruit set.
• Short billed sunbirds are unable to act as substitute pollinators, and seed set is significantly lower in the flowers that they visited, compared to flowers visited by long‐billed sunbirds. This is substantiated on a landscape scale, where fruit production in Chasmanthe floribunda could artificially be increased by 35% in transformed landscapes, but not so in natural areas.
• These findings have important consequences for the management and conservation of long‐tubed bird‐pollinated plant species that exist in recently transformed landscapes. The potential vulnerability of specialised plant species in transformed landscapes is highlighted.

     

Florivores decrease pollinator visitation in a self-incompatible plant

Different biotic interactions may influence one another to produce complex patterns of direct and indirect effects, which together influence plant reproductive success. However, so far most studies on plant-animal interactions have focused on single interactions in isolation. In this study, we studied the effect of florivory by the weevil Cionus nigritarsis on pollinator visitation rate in the self-incompatible perennial herb Verbascum nigrum by combining observations of florivory and pollination in natural populations with records of pollinator visitation to plants with different levels of experimentally inflicted damage.Increasing levels of damage through either natural or simulated florivory resulted in fewer pollinator visits per plant and per flower. As expected, the magnitude of the indirect effect of florivory on pollinator visitation was proportional to the intensity of florivory. Our results indicate that biotic non-pollinating agents, such as florivores, may induce substantial changes in pollinator availability. Therefore, studies addressing different plant-animal interactions in parallel are necessary to better comprehend the factors influencing the reproductive performance and demography of flowering plants.     

Relative pollination effectiveness of floral visitors of Pitcairnia angustifolia (Bromeliaceae)

The effectiveness of flower visitors as pollinators will determine their potential role as selective agents on flower traits. Pitcairnia angustifolia has floral characters that would fit pollination by long-billed hummingbirds, and they should be the most effective pollinators for this plant. To test this prediction, we characterized the behavior of visitors toward flowers and their pollination effectiveness. Coereba flaveola (bananaquits) was the most frequent flower visitor and acted as a primary nectar robber; however, they pollinated incidentally and deposited pollen on stigmas. The endemic short-billed hummingbird Chlorostilbon maugaeus behaved as a secondary robber and did not pollinate flowers. As expected, the long-billed hummingbird, Anthracothorax viridis, was the most efficient visitor in terms of pollen deposition; however, it was the least frequent flower visitor. Introduced Apis mellifera (honeybees) were second in efficiency at depositing pollen and performed one third of the flower visits. Estimates of the expected rate of pollen deposition by each pollinator did not identify a single most effective pollinator. For P. angustifolia at least three flower visitors including an exotic bee and a nectar robber may be equally important to reproductive success. While these results limit our ability to make predictions on the role of hummingbird-pollination on current flower evolution, they do suggest the potential for pollination redundancy among flower visitors for P. angustifolia populations.     

Reproductive biology of a hummingbird‐pollinated Billbergia: light influence on pollinator behaviour and specificity in a Brazilian semi‐deciduous forest

• Ornithophily has evolved in parallel several times during evolution of angiosperms. Bird pollination is reported for 65 families, including Bromeliaceae. One of the most diverse bromeliad is Billbergia, which comprises species pollinated mainly by hummingbirds.
• Based on investigations on flowering phenology, morpho‐anatomy, volume and concentration of nectar, pollinators and breeding system, this paper explores the reproductive biology and pollinator specificity of B. distachia in a mesophytic semi‐deciduous forest of southeastern Brazil.
• The results have show that B. distachia is pollinated by a single species of hermit hummingbird, Phaethornis eurynome, which search for nectar produced by a septal nectary, where the secretory tissue is located above the placenta. The species is self‐incompatible. The combination of pollinator specificity, due to long corolla tubes that exclude visitation of short‐billed hummingbirds, complete self‐incompatibility and non‐territorial behaviour of pollinators, it is very important to reduce pollen loss and increase gene flow within population.
• Our results indicate that studies on pollination biology and reproduction are essential to understand the evolutionary history of pollination systems of plants since, at least in Billbergia, variation in the pollinator spectrum has been recorded for different habitats among Brazilian forests. Furthermore, according to our data, foraging of Phaethornis on flowers is independent of air temperature and humidity, while the main factor influencing hummingbird visitation is daylight. Considering current knowledge on climatic parameters influencing hummingbird foraging, pollination and reproductive biology of Neotropical flora and environment of the hermit hummingbird in tropical forests, new insights on plant–pollinator interaction are provided.

     

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 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.     

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.     

Cheater or mutualist? Novel florivory interaction between nectar‐rich Crotalaria cunninghamii and small mammals

Animals visit flowers to access resources and by moving pollen to conspecific individuals act as pollinators. While biotic pollinators can increase the seed set of plants, other flower visitors can reduce seed set directly by damaging vital reproductive organs and indirectly by affecting the way the plant interacts with subsequent flower visitors. It is, therefore, vital to understand the varied effects of all visitors and not only pollinators on plant fitness, including those visitors that are temporally or spatially rare. We document the first known case of flower visitation by small mammals to Crotalaria cunninghamii (Fabaceae), a plant species morphologically suited to bird pollination. During a rain‐driven resource pulse in the Simpson Desert in 2011, the rodents Mus musculus (Muridae) and Pseudomys hermannsburgensis (Muridae) visited flowers to remove nectar by puncturing the calyx. We investigated the effects of this novel interaction on the reproductive output of C. cunninghamii. Compared with another recent resource pulse in 2007, plants flowering during mammal visitation had five times as many inflorescences per plant, 90% more flowers per inflorescence, and two to three times more nectar per flower, but this nectar was 30% less sugar rich. Concurrently, rodent plagues were up to three times larger during this rain‐driven resource pulse than during a previous pulse in 2007. Up to 75% of flowers had evidence of small mammal florivory, but this was not necessarily destructive, as up to 90% of fruit had the remains of florivory. Through a series of exclusion experiments, we found that small mammal florivory did not directly reduce seed set. We conclude that rain‐driven resource pulses led to a unique combination of events that facilitated the novel florivory interaction. Our findings emphasize the dynamic nature of biotic interactions and the importance of testing the role of all visitors to pollination services.     

Small but attractive: female‐biased nectar production and floral visitors in a dimorphic shrub

• In sexually dimorphic species, hermaphrodite flowers in gynodioecious species or male flowers in dioecious species are often larger and produce more nectar than their conspecific female flowers. As a consequence, hermaphrodite or male flowers frequently receive more pollinator visits.
• Sex ratio, flower size, floral display, nectar production and floral visits were evaluated in two natural populations of Fuchsia thymifolia, a morphologically gynodioecious but functionally subdioecious insect‐pollinated shrub.
• Sex ratio did not differ from the expected 1:1 in the two studied populations. As expected, hermaphrodite flowers were larger than female flowers, but in contrast to the general pattern, hermaphrodite flowers did not produce nectar or produced much less than female flowers. Flower visitors were flies (68%) and bumblebees (24%), both of which showed a preference for female flowers. No sex difference was detected in either flower longevity or floral display across the flowering season.
• Higher nectar production by females may attract more pollinators, and may be a strategy to enhance female reproductive success in this species. Finally, floral dimorphism and insect preferences did not seem to hamper the maintenance of sub‐dioecy or prevent the evolution of dioecy in F. thymifolia.

     

Nectar sugar composition of European Caryophylloideae (Caryophyllaceae) in relation to flower length,pollination biology and phylogeny

Floral nectar composition has been explained as an adaptation to factors that are either directly or indirectly related to pollinator attraction. However, it is often unclear whether the sugar composition is a direct adaptation to pollinator preferences. Firstly, the lower osmolality of sucrose solutions means that they evaporate more rapidly than hexose solutions, which might be one reason why sucrose‐rich nectar is typically found in flowers with long tubes (adapted to long‐tongued pollinators), where it is better protected from evaporation than in open or short‐tubed flowers. Secondly, it can be assumed that temperature‐dependent evaporation is generally lower during the night than during the day so that selection pressure to secrete nectar with high osmolality (i.e. hexose‐rich solutions) is relaxed for night‐active flowers pollinated at night. Thirdly, the breeding system may affect selection pressure on nectar traits; that is, for pollinator‐independent, self‐pollinated plants, a lower selective pressure on nectar traits can be assumed, leading to a higher variability of nectar sugar composition independent of pollinator preferences, nectar accessibility and nectar protection. To analyse the relations between flower tube length, day vs. night pollination and self‐pollination, the nectar sugar composition was investigated in 78 European Caryophylloideae (Caryophyllaceae) with different pollination modes (diurnal, nocturnal, self‐pollination) using high‐performance liquid chromatography (HPLC). All Caryophylleae species (Dianthus and relatives) were found to have nectar with more than 50% sucrose, whereas the sugar composition of Sileneae species (Silene and relatives) ranged from 0% to 98.2%. In the genus Silene, a clear dichotomous distribution of sucrose‐ and hexose‐dominant nectars is evident. We found a positive correlation between the flower tube length and sucrose content in Caryophylloideae, particularly in day‐flowering species, using both conventional analyses and phylogenetically independent contrasts.     

Seasonal and annual variations in the pollination efficiency of a pollinator community of Dictamnus albus L.

The interplay between insect and plant traits outlines the patterns of pollen transfer and the subsequent plant reproductive fitness. We studied the factors that affect the pollination efficiency of a pollinator community of Dictamnus albus L. by evaluating insect behaviour and morphological characteristics in relation to flowering phenology. In order to extrapolate the pollinator importance of single taxa and of the whole pollinator guild, we calculated an index distinguishing between potential (PPI) and realized (RPI) pollinator importance. Although the pollinator species spectrum appeared rather constant, we found high intra‐ and inter‐annual variability of pollinator frequency and importance within the insect community. Flower visitation rate strictly depended on insect abundance and on the overlap between their flying period and flower blooming. All the pollinators visited flowers from the bottom to the top of the racemes, excluding intra‐plant geitonogamous pollination, and most of them showed high pollen fidelity. Only medium large‐sized bees could contact the upward bending stiles while feeding on nectar, highlighting a specialisation of the plant towards bigger pollinators. Moreover, we found evidence of functional specialisation, since all pollinators were restricted to a single taxonomic group (order: Hymenoptera; superfamily: Apoidea). Both the PPI and RPI indices indicate Habropoda tarsata as the most important pollinator of D. albus. Following hand cross‐pollination experiments we revealed the presence of pollination limitation in 1 of the 3 years of field study. We discuss this result in relation to flowering abundance and to possible mismatches of phenological periods between plants and insects.     

Spatio‐temporal patterns in pollination of deceptive Aristolochia rotunda L. (Aristolochiaceae)

• Pollination success of highly specialised flowers is susceptible to fluctuations of the pollinator fauna. Mediterranean Aristolochia rotunda has deceptive trap flowers exhibiting a highly specialised pollination system. The sole pollinators are kleptoparasitic flies in search of food. This study investigates these pollinators on a spatio‐temporal scale and the impact of weather conditions on their availability. Two potential strategies of the plants to cope with pollinator limitation, i.e. autonomous selfing and an increased floral life span, were tested.
• A total of 6156 flowers were investigated for entrapped pollinators in 10 Croatian populations. Availability of the main pollinator was correlated to meteorological data. Artificial pollination experiments were conducted and the floral life span was recorded in two populations according to pollinator availability.
• Trachysiphonella ruficeps (Chloropidae) was identified as dominant pollinator, along with less abundant species of Chloropidae, Ceratopogonidae and Milichiidae. Pollinator compositions varied among populations. Weather conditions 15–30 days before pollination had a significant effect on availability of the main pollinator. Flowers were not autonomously selfing, and the floral life span exhibited considerable plasticity depending on pollinator availability.
• A. rotunda flowers rely on insect pollen vectors. Plants are specialised on a guild of kleptoparasitic flies, rather than on a single species. Pollinator variability may result in differing selection pressures among populations. The availability/abundance of pollinators depends on weather conditions during their larval development. Flowers show a prolonged trapping flower stage that likely increases outcrossing success during periods of pollinator limitation.

     

A trade-off between the frequency and duration of bumblebee visits to flowers

Pollinator behavior influences plant reproduction in many ways. A traditional measure of pollination, the number of visits received, may be a poor predictor of plant reproductive success, particularly when there are trade-offs between visit quantity and components of visit quality. For example, the duration of pollinator visits may be negatively correlated with the number of visits received by a flower. We tested for a trade-off between the number of bumblebee visits and the duration of those visits in an experimental population of snapdragons (Antirrhinummajus: Scrophulariaceae). The duration of a bumblebee visit to a flower increased significantly with the time interval since the flower had last been visited. Over the lifetime of a flower the correlation between the total number and average duration of visits received by a flower was weakly negative. However, at the whole-plant level the correlation was positive: plants whose flowers received more visits also received visits of longer duration. Factors affecting the relationship between quantity and duration of pollinator visits to flowers also were investigated. Two factors weakened the negative dependence of average visit duration on number of visits received by individual snapdragon flowers: (1) the correlation between the total number of visits to a flower and the average interval between visits was only −0.53, as visits to individual flowers were not very evenly spaced over time, and (2) newly opened flowers received fewer and shorter visits than older flowers. Comparing whole plants, nectar production per flower varied dramatically across individuals, a probable explanation for the positive correlation between visit number and average duration per flower observed at the plant level. The potential for a trade-off between these two components of pollinator service exists when visit duration depends on reward quantity; whether the trade-off is realized will depend on variation in nectar production and on whether pollinators forage systematically. Received: 3 October 1997 / Accepted: 16 June 1998     

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.     

Effects of nectar-robbing on plant reproduction and evolution

The relationship between plant and pollinator is considered as the mutualism because plant benefits from the pollinator’s transport of male gametes and pollinator benefits from plant’s reward. Nectar robbers are frequently described as cheaters in the plant-pollinator mutualism, because it is assumed that they obtain a reward (nectar) without providing a service (pollination). Nectar robbers are birds, insects, or other flower visitors that remove nectar from flowers through a hole pierced or bitten in the corolla. Nectar robbing represents a complex relationship between animals and plants. Whether plants benefit from the relationship is always a controversial issue in earlier studies. This paper is a review of the recent literatures on nectar robbing and attempts to acquire an expanded understanding of the ecological and evolutionary roles that robbers play. Understanding the effects of nectar robbers on the plants that they visited and other flower visitors is especially important when one considers the high rates of robbing that a plant population may experience and the high percentage of all flower visitors that nectar robbers make to some species. There are two standpoints in explaining why animals forage on flowers and steal nectar in an illegitimate behavior. One is that animals can only get food in illegitimate way because of the mismatch of the morphologies of animals’ mouthparts and floral structure. The other point of view argues that nectar robbing is a relatively more efficient, thus more energy-saving way for animals to get nectar from flowers. This is probably associated with the difficulty of changing attitudes that have been held for a long time. In the case of positive effect, the bodies of nectar robbers frequently touch the sex organs of plants during their visiting to the flowers and causing pollination. The neutral effect, nectar robbers’ behavior may destruct the corollas of flowers, but they neither touch the sex organs nor destroy the ovules. Their behavior does not affect the fruit sets or seed sets of the hosting plant. Besides the direct impacts on plants, nectar robbers may also have an indirect effect on the behavior of the legitimate pollinators. Under some circumstances, the change in pollinator behavior could result in improved reproductive fitness of plants through increased pollen flow and out-crossing. __________ Translated from Acta phytoecologiaca Sinica, 2006, 30(4): 695–702 [译自: 植物生态学报]     

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

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