Differences in pollinator effectiveness of birds and insects visiting Banksia menziesii (Proteaceae)

Summary The effectiveness of nectarivorous birds, introduced honey bees and staphylined beetles as pollinators of Banksia menziesii was assessed. Staphylinids removed substantial amounts of pollen but did not deposit any onto stigmata. Abundance of beetles on inflorescences was related to the mean number of florets opening per day. Honey bees collecting pollen were more likely to effect pollination than those collecting nectar which only contacted stigmata when arriving or leaving an inflorescence. Nectar-foraging birds probed between florets 10.2±0.8 (±SE) times, contacting 8–16 stigmata during each probe. Bees visited inflorescences ten times more frequently than birds although they deposited only 25% of the pollen that birds did on stigmata. Fruit set was ten times greater on inflorescences visited by birds than on inflorescences visited by bees. Bees were capable of removing as much pollen as birds but, because of direct pollen transfer to birds when florets opened during foraging, actual removal was probably much less. Selection for floret opening during nectar foraging by birds may have resulted from pollen removal by non-pollinating animals, such as staphylinids.     

The pollination biology ofHibbertia stricta (Dilleniaceae)

The exines of pollen grains ofHibbertia stricta (DC.)R. Br. exF. Muell. (Sect.Pleurandra) wear an oily, yellow pollen coat that stains positively for lipids. The pollen is collected by asocial bees, exclusively. The most common floral foragers are members of the genusLasioglossum (subgenusChilalictus;Halictidae) and they harvest pollen via thoracic vibration. As these bees cling to the inflated anthers their pollen smeared bodies come in contact with either of the two wet, nonpapillate stigmas. The stigmas respond positively to cytochemical tests for the presence of esterase immediately following expansion of the corolla, indicating the effective pollination period. The foraging patterns of the bees are narrowly to broadly polylectic. AsH. stricta flowers are nectarless, it is not surprising that bees bearing mixed pollen loads always carry the pollen of at least one nectariferous, coblooming plant. The pollination biology ofH. stricta is compared with otherHibbertia spp. and with pollen flowers in general.     

Notes on the pollination mechanisms ofMoraea inclinata andM. brevistyla (Iridaceae)

Individual flowers ofMoraea inclinata are nectariferous and last about six hours. They appear to be pollinated largely by bees in the familyHalictidae (Lasioglossum spp.,Nomia spp.,Zonalictus) and to a lesser extent by bees in the familyAnthophoridae (Amegilla). The mechanism of bee-pollination inM. inclinata is the Iris type; i.e., each flower consists of three pollination units (an outer tepal, a partly exserted anther, and the opposed style branch which terminates in a pair of petal-like crests). Bees rarely visit more than one pollination unit per flower. Transferral of pollen to the bee is passive and nototribic although all bees collected on the flowers were female and 55% of the bees carried pollen loads with 2–5 pollen taxa in their scopae.Moraea brevistyla flowers are nectariferous but lack scent and last two days. They are visited infrequently by bees and only one femaleLasioglossum spec. carried the pollen ofM. brevistyla. Unlike flowers ofM. inclinata those ofM. brevistyla deposit pollen only on the head and thorax. Bee-mediated autogamy in both species is avoided due to the erratic foraging patterns of the bees and the flexibility of each stigma lobe as the bee backs out of the flower. Approximately 2–4 flowers in the inflorescences of both species (6–8 flowers/infloresence) develop into capsules.     

Flower choice by honey bees (Apis mellifera L.): sex-phase of flowers and preferences among nectar and pollen foragers

Bees foraging for nectar should choose different inflorescences from those foraging for both pollen and nectar, if inflorescences consist of differing proportions of male and female flowers, particularly if the sex phases of the flowers differ in nectar content as well as the occurrence of pollen. This study tested this prediction using worker honey bees (Apis mellifera L.) foraging on inflorescences of Lavandula stoechas. Female flowers contained about twice the volume of nectar of male flowers. As one would predict, bees foraging for nectar only chose inflorescences with disproportionately more female flowers: time spent on the inflorescence was correlated with the number of female flowers, but not with the number of male flowers. Inflorescence size was inversely correlated with the number of female flowers, and could be used as a morphological cue by these bees. Also as predicted, workers foraging for both pollen and nectar chose inflorescences with relatively greater numbers of both male and female flowers: time spent on these inflorescences was correlated with the number of male flowers, but not with the number of females flowers. A morphological cue inversely associated with such inflorescences is the size of the bract display. Choice of flowers within inflorescences was also influenced predictably, but preferences appeared to be based upon corolla size rather than directly on sex phase.     

Influence of resource topography on pollinator flight directionality of two species of bees

Analyses of the search patterns of ApisMellifera workers foraging on artificial inflorescences and Bombus Pennsylvanicusqueens foraging on inflorescences of red clover are used to identify a general rule specifying intrapatch search patterns. Bees land, move about the inflorescences in search of nectar, and come to a last-faced position from which takeoff occurs. Last-faced directions are generated by a forward-moving tendency while probing artificial inflorescences or real florets. This tendency is modulated by restricted bee locomotion, caused by the size and shape of the visited inflorescence and the spatial distribution of florets within such inflorescences. The result is that bees tend to circle inflorescences. The process is terminated with an undefined stopping rule, whereupon bees usually depart in the direction they last face. The last-faced direction is a by-product of intrafloral search and becomes less associated with arrival directions as intrafloral search continues. Pollinator flight directionality is usually represented as a frequency distribution of angular changes in direction which typically has a mean near 0° and a variance that increases with increases in energy gain. We show that these characteristics are artifacts of pooling mirror-image movement data sets;a mean of 0° is the result of canceling the means of the left- and right-hand turns. The putative increased variance associated with energy gain is the result of adding the variances associated with left- and right-handed turns. These computational artifacts may be avoided by changing the sign of the left-handed turns prior to pooling with the right-handed turns (or vice versa). Pooling bee visits based only on the number of florets probed can destroy information relevant to studies examining behavioral mechanisms of flight directionality. Analytical problems encountered when turns exceed 360° are also addressed.     

Behavioral responses by bumble bees to variation in pollen availability

Summary Pollen-collecting bumble bees (Bombus spp.) detect differences between individual flowers in pollen availability and alter their behavior to capitalize on rewarding flowers. Specific responses by bees to increased pollen availability included: longer visits to flowers; visits to more flowers within an inflorescence, including an increased frequency of revisits; an increased likelihood of grooming while the bee flow between flowers within the inflorescence; and more protracted inter-flower flights, probably because of longer grooming bouts. The particular suite of responses that a bee adopted depended on the pollen-dispensing mechanism of the plant species involved. Bees buzzed previously-unvisited Dode-catheon flowers longer than empty flowers. In contrast, pollen availability did not significantly affect the duration of visits to Lupinus flowers, which control the amount of pollen that can be removed during a single visit. Simulation results indicate that the observed movement patterns of bumble bees on Lupinus inflorescences would return the most pollen per unit of expended energy. The increased foraging efficiency resulting from facultative responses by bees to variation in pollen availability, especially changes in the frequency and intensity of grooming, could correspondingly decrease pollen dispersal between plants.     

Floral mimesis inThelymitra nuda (Orchidaceae)

Insect pollination occurred inThelymitra nuda R. Br. on sunny days when the ambient temperature exceeded 20 °C. The flower buds on a raceme opened subsynchronously displaying the brightly-colored, actinomorphic perianth and exposed the contrastingly-colored, scented and ornamented column. InT. nuda the staminodes and the filament of the fertile stamen are fused to one another producing an inflated hood over the anther. This staminodal hood is terminated in two non-ornamental, but brightly-colored, central lobes and two terete lateral lobes bearing approximately 400 white trichomes. Each trichome bears a double chain of 30–40 spherical, rugulose cells. Female bees, in the genusLasioglossum (Halictidae), were observed to land directly on the hood and curled their bodies around the four lobed tip of the staminodal complex. The bees attempted to forage on the lobes as if they were collecting pollen from fertile, poricidal stamens. These bees applied thoracic vibration to the yellowish central lobes and actively scraped the trichome clusters (Pseudopollen) with their forelegs. Bees carried the pollinaria ofT. nuda dorsally on their abdomens. Abdominal contact with the rostellum appeared to occur when the female bee disengaged herself from the staminodal hood. Observations made of bees on co-blooming flowers, and analyses of pollen loads collected by bees suggested that the orchid flower mimics the guild of blue-purple flowers that lack floral nectar but offer pollen in poricidal anthers. The models ofT. nuda are co-bloomingLiliaceae in the generaDichopogon andThysanotus. However, nectarless, buzz-pollinated flowers are also extensively distributed over the orchid’s range. More than 30% of the flowers in theT. nuda population had their pollinaria removed, suggesting a high capacity for cross-pollination in an orchid genus usually considered to be self-pollinated via mechanical autogamy. This study confirmed previous predictions that column modifications represented a trend towards pseudanthery.     

Bee-pollination inHibbertia fasciculata (Dilleniaceae)

In direct contrast to mostHibbertia spp., the flowers ofH. fasciculata R. Br. ex D. C. bear only a single whorl of stamens and these stamens are arranged separately (not in typical bundles). The short filaments are appressed to the three carpels so that the inflated, porose and introrsive anthers form a centralized cluster obscuring the three ovaries. The three slender styles emerge at right angles from between the filaments. These styles curve upward and the stigmas form the three points of a triangle; each stigma is approximately one millimeter outside the centralized cluster of anthers. The flowers are nectarless and bear a bright yellow corolla. A pungent and unpleasant fragrance appears to be concentrated within the pollenkitt. When native bees attempt to forage for the pollen, within the cluster of anthers, the ventrally deposited loads of pollen, on the bees' abdomens, contact the outer triangle of stigmas. The major pollinators ofH. fasciculata are female bees in the polylectic genera,Lasioglossum (subgenusChilalictus, Halictidae) andLeioproctus (Colletidae). These bees carry an average of more than two pollen taxa when they are caught foraging onH. fasciculata. 78% of the 47 bees, captured onH. fasciculata carried the pollen from at least one sympatric taxon bearing nectariferous flowers (e.g., genera in theMyrtaceae, Compositae, andEpacridaceae). The pollination biology ofH. fasciculata is assessed in relation to the known radiation of bee-pollinated flowers in the genusHibbertia, and within theDilleniaceae s. l.     

The movement patterns of carpenter beesXylocopa micans and bumblebeesBombus pennsylvanicus onPontederia cordata inflorescences

The movement patterns of carpenter bees (Xylocopa micans) and bumblebees (Bombus pennsylvanicus) foraging for nectar on vertical inflorescences ofPontederia cordata were studied near Miami, Florida. The floral biology ofP. cordata is unique in several ways: (a) many short-lived flowers per inflorescence, (b) constant nectar production throughout the life span of each flower, and (c) abscence of vertical patterning of nectar and age of flowers. Inflorescences ranged between 3.5 and 15.8 cm long and had between 9 and 55 open flowers. Both carpenter bees and bumblebees arrived mostly on the bottom third of the inflorescence and left after visiting flowers on the top third of the inflorescence. The departure position from the inflorescence was higher up than observed in studies of other insect pollinators foraging on other speces of plants. This pattern of departure probably occurs in the absence of a vertical gradient of nectar or floral morphology.     

Pollination ecology ofOxalis violacea (Oxalidaceae) following a controlled grass fire

Vernal grass fires may encourage profuse flowering in clonal, colonies ofOxalis violacea. Long-styled colonies appear to be more floriferous than short-styled colonies and set a greater number of capsules. Individual flowers of both morphs live one or two days, change position on their respective pedicels and advertise nectar concealed at the base of the floral throat. AlthoughDiptera, Hymenoptera, andLepidoptera forage for nectar, bees (Andrenidae,Anthophoridae, Halictidae, andMegachilidae) probably make the only effective pollen transfers between the two morphs. Both male and female bees may transport pollen of both morphs and short-tongued bees (e.g.,Augochlorella spp.,Dialictus spp.) may be more common but as effective as pollinators as long-tongued bees (e.g.,Calliopsis andreniformis andHoplitis spp.). The conversion rate of flowers into capsules is only 13–17%. The spreading style in the short-styled morph is interpreted as an adaptation restricting insect-mediated, self-pollination but encouraging bee-stigma contact during nectar foraging.     

An exception to Darwin's syndrome: floral position,protogyny, and insect visitation in Besseya bullii (Scrophulariaceae)

Darwin pointed out that plants with vertical inflorescences are likely to be outcrossed if the inflorescence is acropetalous (flowers from the bottom up), the flowers are protandrous (pollen is dispersed before stigmas are receptive), and pollinators move upward on the inflorescence. This syndrome is common in species pollinated by bees and flies, and very few exceptions are known. We investigated flowering phenology and pollinator behavior in Besseya bullii (Scrophulariaceae) and found that it did not fit Darwin's syndrome. The vertical inflorescence was acropetalous but the flowers were distinctly protogynous, so flowers with newly receptive stigmas appeared on the inflorescence above those with dehiscing anthers. A number of small insects visited B. bullii; bees in the family Halictidae (Augochlorella striata and Dialictus spp.) were most common. When insects moved between gender phases within inflorescences, they moved up more often than down (61% versus 39% of observations, respectively) but this difference was only marginally significant. Most visits were to male-phase flowers only, and this preference was more pronounced for pollen-foraging insects than for nectar-foraging insects. B. bullii was self-compatible, so its flowering characteristics potentially could result in considerable self-pollination. However, an average of 38% of the lowermost flowers opened before any pollen was available on the same inflorescence; these solo females had a high probability of outcrossing (though fruit set was relatively low in the bottom portion of the inflorescence). Upper flowers may also be outcrossed because downward insect movement was not uncommon. Therefore protogyny in B. bullii may not necessarily lead to more selfing than would protandry.     

Pollinator visitation in populations of tristylous Eichhornia paniculata in northeastern Brazil

Summary The frequencies of floral morphs in populations of tristylous Eichhornia paniculata often deviate from the theoretical expectation of equality. This variation is associated with the breakdown of tristyly and the evolution of self-fertilization. Differences in morph frequencies could result from selection pressures due to variable levels of insect visitation to populations and contrasting foraging behavior among the floral morphs. We estimated pollinator densities in 16 populations and quantified visitation sequences to morphs in five populations of E. paniculata in northeastern Brazil. Foraging behavior among floral morphs was measured as the frequency of visits to morphs relative to their frequency in the population (preference) and number of flights between inflorescences of the same versus different morphs (constancy). Pollinator density (number/m²/minute) was not correlated with population size, plant density or morph diversity. Pollinator densities varied most among populations of less than 200 plants. Whether pollinators discriminated among the morphs, depended on whether they primarily collected nectar or pollen. In four populations, nectar-feeding bees (Ancyloscelis and Florilegus spp.) and butterflies showed no consistent preference or constancy among the morphs. In contrast, pollen-collecting bees (Trigona sp.) visited a lower proportion of longstyled inflorescences than expected and tended to visit more mid-and short-styled inflorescences in succession, once they were encountered. Pollinator constancy for morphs did not result from differences in inflorescence production or spatial patchiness among the morphs. Although non-random pollinator visitation to morphs in heterostylous populations could potentially affect mating and hence morph frequencies, the observed visitation patterns in this study do not provide evidence that pollinators play a major role in influencing floral morph frequencies.     

Pollen foraging by bumblebees: Foraging patterns and efficiency on Lupinus polyphyllus

Summary Bumblebees foraging on vertical inflorescences start near the bottom and work upward, behavior commonly interpreted as a response to the greater amounts of nectar available in lower flowers. Lupinus polyphyllus, which produces no nectar, has more pollen available in upper flowers. Although bees are probably unable to detect this gradient, since pollen is hidden from their view, they still start low and forage upward. Therefore, we concluded that the bees' tendency to forage upward on vertical inflorescences is not tied to a reward gradient. In addition, bees use only about 15% of the flowers per inflorescence, although they could be much more efficient by visiting and revisiting every flower systematically. In general, revisits would not be penalized because most flowers contain enough pollen for several visits. Optimal foraging theory may not offer an adequate explanation for such gross inefficiency.     

Effects of variation in inflorescence size and floral rewards on the visitation rates of traplining pollinators ofAralia hispida

Summary In field experiments withAralia hispida inflorescences, the following variables were manipulated: number of umbels per inflorescence, number of flowers per umbel, and amounts of pollen and nectar per flower. Visitation rates by bumble bees, the principal pollinators, were then observed. In the reward-variation experiments, bees appeared to learn the positions of nectar-rich shoots, and visited them significantly more often than nectar-poor shoots. They did not respond to similar variation in pollen production. The nectar preferences developed slowly after the treatments were imposed, and bees continued to favor sites that had been occupied by nectar-rich shoots even after the treatments were discontinued. Visitation rate was approximately proportional to flower number, making it unlikely that increases in inflorescence size produced a disproportionate gain in male reproductive success (a necessary condition in certain models for the evolution of dioecy). For a fixed number of flowers per inflorescence, bees preferred inflorescences with more umbels. In pairwise choice tests of male-phase and female-phase umbels of various sizes, bees preferred male-phase umbels and larger umbels; the preference for male-phase umbels is stronger in bees that had previously fed on male-phase umbels.     

Pollination disruption by European honeybees in the Australian bird-pollinated shrubGrevillea barklyana (Proteaceae)

European honeybees (Apis mellifera) were less efficient pollinators ofGrevillea barklyana than nectar-feeding birds. Nectar-collecting honeybees did not contact reproductive parts of flowers. Pollen-collecting honeybees preferentially visited malestage flowers but rarely visited female-stage flowers. Fruit set on caged inflorescences that allowed access to honeybees but excluded birds was reduced by more than 50% compared to inflorescences that were visited by both types of visitors. Further, fruit set on caged inflorescences was less than on bagged inflorescences that excluded both birds and honeybees, indicating that pollen removal by bees decreased opportunities for delayed autonomous selfing in the absence of birds. Although fruit set was not pollen-limited at the study site, pollen removal by honeybees would decrease fruit set in small populations where birds are scarce. In addition, pollen removal by honeybees would reduce opportunities for outcrossing and reproductive success through male function. Although honeybees have been in Australia for insufficient time to have exerted selection on floral traits, evolutionary shifts in response to these animals are likely to occur in the future.     

Foraging by honeybees on Carduus acanthoides: pattern and efficiency

Abstract.

• 1 The relationship between the fluctuation in total quantity of sugar available in the nectar of Carduus acanthoides inflorescences and the foraging behaviour of honeybees Apis mellifera ligustica was studied in a patch under natural conditions.
• 2 Every day, three inflorescence populations coexisted, one for each day of the inflorescence life-span. The maximum availability of sugar occurred in second-day capitula from 12.00 to 15.00 hours.
• 3 Bee arrivals at the patch were positively correlated with the total availability of sugar as determined by sampling.
• 4 Bees responded to variation in the availability of sugar by visiting the inflorescence stage that was most rewarding at that time of day. Early in the morning, when the frequency of visits was low, the bees worked the third-day capitula, which were the best available choice at that time. Similarly, beginning at 12.00 hours, bees switched to second-day capitula. At the end of the day, some bees switched to third-day capitula where a slightly superior quantity of sugar could be obtained from a small number of florets although other bees continued to work the second-day capitula.
• 5 Individual bees switched to another inflorescence stage after a high proportion of their visits to a small number of capitula of one kind had provided a low reward.
• 6 The number of florets visited per minute per bee varied throughout the day and was positively correlated with the availability of sugar.

     

The branching of the inflorescence and vegetative shoot and taxonomy of the genusKummerowia (Leguminosae)

A study of the branching of the inflorescence and the vegetative shoot of the genusKummerowia, consisting ofK. stipulacea (Maxim.) Makino andK. striata (Thunb.) Schindler, has led to the following conclusions: (1) the inflorescences of both species are reduced compound cymes, (2) the branching system of the inflorescence ofKummerowia is not clearly different from that of the vegetative shoot and there are some transitional forms between both systems, and (3) the inflorescence ofKummerowia is different from the racemose inflorescences ofLespedeza andCampylotropis. Based on the differences found in the branching system of the inflorescence,Kummerowia is distinctly separated fromLespedeza andCampylotropis and is more correctly treated as a distinct genus from the latter two.     

The pollination ofStenorrhynchos lanceolatus (Aublet) L. C. Rich. (Orchidaceae: Spiranthinae) by hummingbirds in southeastern Brazil

Hummingbird pollination is documented for a natural population ofStenorrhynchos lanceolatus Aublet. L. C. Rich. occurring in Rio de Janeiro State, southeastern Brazil. At the study site the plants are pollinated byPhaethornis eurynome (Phaethorninae),Thalurania glaucopis (females only) andLeucochloris albicollis (Trochilinae). The plants offer nectar as a reward and the pollinaria become stuck to the surface of the hummingbird's bill while it is probing the flowers. The orchid population received a few (0–4) hummingbird visits per day, with about 83% of the flowers being pollinated. In spite of the low frequency of visits, the granular structure of the pollinarium plus the behaviour of the most frequent pollinators, which tend to visit all the fresh-looking flowers of each inflorescence, a very high fruiting success was promoted. Experimental evidence suggests that the pollinaria may remain up to 6.30 hours on the hummingbird's bill, enhancing the chances of cross-pollination and long-distance pollen flow.     

The effect of nectar abundance on foraging patterns of bumble bees

Abstract.

• 1 Bumble bees (Bombus spp.) fed more on previously screened, nectar-rich plots of cow vetch (Vicia cracca) and white clover (Trifolium repens), and remained longer on inflorescences there, than on continually-exploited plots of these flowers. No significant differences between previously screened and continually available plots occurred in the number of individuals visiting these two areas, the number of inflorescences per visit, the number of florets visited per inflorescence, and the percentage of inflorescences rejected.
• 2 Individual bees were analysed in greater detail. They visited more inflorescences and spent longer times on cow vetch in the previously-screened plots, whether moving from previously-screened to continually available areas, or vice versa. On white clover the same pattern held for bees moving from previously screened to continually available plots, but not for those moving from continually available to previously-screened areas.

     

Male-biased sex ratio and promiscuous pollination in the dioecious island treeLaurus azorica (Lauraceae)

Pollination ofLaurus azorica (Lauraceae), a dioecious Macaronesian tree, was studied. Male and female trees had the same size distribution. The population had 2.5 times as many male trees as females. In addition, males produced more flowers, and their inflorescences lasted longer. Individual flower lifetime and length of flowering season were the same in both sexes. Between the years of observation, one tree changed sex. Pollinators wereHalictinae bees and the flyTachina canariensis. The bees collected pollen and nectar and the fly collected nectar from both sexes. Both species visited other plants as well. The evolution of breeding systems inLauraceae is discussed.