ArticlePDF Available

Foraging behaviour of honey bees (Apis mellifera L.) on staghorn sumac [Rhus hirta Sudworth (ex-typhina L.)]: Differences and dioecy

Authors:

Abstract and Figures

The foraging behaviour of honey bees (Apis mellifera L.) on inflorescences of staghorn sumac [Rhus hirta Sudworth (ex-typhina L.)] was studied using a “choice table” placed in natural stands of this plant. The choice table consisted of a wooden grid with alternated male and female inflorescences of sumac. Honey bee activity was recorded also on inflorescences of naturally growing plants in which the secretion of nectar was measured and the anther dehiscence recorded. Honey bees were the only common pollinators observed on sumac in the study area. During the morning, both plant sexes secreted little nectar, and pollen was available after the dehiscence of the anthers which took place between 1000 and 1100 hours. Female inflorescences secreted great amounts of nectar during the afternoon, but in male inflorescences there was little secretion. Honey bees seemed to forage according to the circadian availability of resources. Most of their activity concentrated on male inflorescences in the morning and on female ones during the afternoon. Both the occurrence of bees with pollen loads in their corbiculae and the length of the visits to each sex also seemed to be in accordance to the kind of resource exploited at particular times of the day. Most of the bees with pollen loads were observed during the morning and the longest visits to any inflorescences were registered on female ones during the afternoon (by bees foraging for nectar). Despite our results suggesting that the pollination success of staghorn sumac would be impaired by the foraging pattern of honey bees, an explanation is proposed for its reproductive success.
Content may be subject to copyright.
A preview of the PDF is not available
... In these cases, generalist pollinators are also expected to visit male flowers first, and females later in the day (Bawa 1980, Beach 1981. Detailed assessment of the nectar and pollen resources provided by R. michauxii remains for future studies, but insect behavior and the large, visible nectaries of female flowers suggest that they do provide substantial resources-a feature that may be typical of the genus Rhus (Young 1972, Greco et al. 1996, Matsuyama et al. 2009). Other Rhus species, however, appear to vary in the extent of pollinator preference for male flowers. ...
... Matsuyama et al. (2009) documented male preference in many, but not all, of the diverse visitors to Rhus trichocarpa in Japan. And Greco et al. (1996) showed that male Rhus hirta flowers provide pollen in the morning but secrete little nectar, whereas female flowers of the same species secrete nectar in the afternoon. Honey bees, the sole visitor in that study, were thus attracted to males in the morning, but occasionally dropped pollen on female plants during pollen-foraging bouts. ...
Article
Dioecy is rare among flowering plants, and is associated with a high frequency of threatened species. Dioecious plants are often pollinated by wind or insects, but are susceptible to pollination failure should male and female plants become spatially separated, or should pollinator abundance decline. Here we characterize the plant–pollinator interactions of Rhus michauxii Sarg (Sapindales: Anacardiaceae), an endangered dioecious shrub endemic to the southeastern United States. Working in the sandhills region of North Carolina, we detected a diverse community of arthropods visiting R. michauxii flowers, including 55 species or morphospecies, with moderate niche overlap between male and female flowers. Although most visitors acquired pollen from male flowers, pollen loads were greatly reduced or diluted on visitors to female flowers; conspecific pollen was completely absent at all-female sites. Bees in the genus Megachile appear to be the most important pollen vectors in this system because of their abundance and pollen load composition. We constructed a regional pollen transport network involving 73 arthropod species and 46 pollen species/morphotypes, in which R. michauxii participated in 10% of links and attracted 38% of individual visitors, suggesting that it competes successfully with other plants for visitation. Finally, time-lapse videography revealed that female inflorescences were visited about six times less often than male inflorescences, but at similar times of day. Despite overall high rates of bee visitation, pollen movement from male to female plants was uncommon, and restoration of sexual reproduction in this species may require hand pollination or translocation of suitable mates to single-sex sites.
... Davila and Wardle (2007) One reward type becomes temporally available Rhus hirta Sudworth Greco, Holland, and Kevan (1996) Aralia hispida Thomson, McKenna, and Cruzan (1989) Lavandula latifolia Herrera (1990) The majority of research on bee cognition approximates the 'nectar only' reward scenario. ...
Article
Keywords: Bombus impatiens bumblebee learning memory multitasking nectar pollen pollination In their natural environments, most animals must learn about multiple kinds of rewards, both within and across contexts. Despite this, the majority of research on animal learning involves a single reward type. For example, bees are an important model system for the study of cognition and its ecological consequences , but nearly all research to date on their learning concerns a single reward, nectar (carbohy-drates), even though foragers often simultaneously collect pollen (protein). Features of learning under more ecologically realistic conditions involving multiple reward types are thus largely unexplored. To address this gap, we compared performance on a colour-learning task when floral surrogates offered bumblebees, Bombus impatiens, a single type of floral reward versus multiple, nutritionally distinct rewards. In one experiment, bees learned a floral association with nectar either alone or while simultaneously collecting pollen. In a reciprocal experiment, bees learned a floral association with pollen either alone or while simultaneously collecting nectar. Bees that collected pollen while learning about nectar did not suffer any detriment to learning which flower colour offered nectar. However, this was not the case for the reciprocal task: collecting nectar impaired bees' ability to learn and remember associations between floral colour and pollen. Our findings offer new insight into how bees learn in relation to ecologically realistic rewards and how cognitive constraints may shape their behaviour under ecologically realistic foraging scenarios.
... Nectar composition may differ in male and female flowers of monoecious and dioecious species. That produced by female flowers of Cucurbita pepo, Euterpe precatoria and Rhus hirta is more abundant and more concentrated than that of male flowers (Greco et al. 1996, Ku¨chmeister et al. 1997). On the other hand, in the three species of the genus Silene, Witt et al. (1999) found more concentrated nectar in male flowers. ...
Article
Full-text available
Nectaries differ in many aspects but a common feature is some kind of advantage for the plant conferred by foraging of consumers which may defend the plant from predators in the case of extrafloral nectaries, or be agents of pollination in the case of floral nectaries. This minireview is concerned mainly with floral nectaries and examines the following characteristics: position in flower; nectary structure; origin of carbohydrates, aminoacids and proteins; manner of exposure of nectar; site of nectar presentation; volume and production of nectar in time; sexual expression of flower and nectary morphology; nectar composition and floral sexual expression; variability of nectar composition; fate of nectar; energy cost of nectar production. The species of certain large families, such as Brassicaceae, Lamiaceae and Asteraceae, resemble each other in nectary organisation; other families, such as Cucurbitaceae and Ranunculaceae, have various types of organisation. A scheme is presented to illustrate factors influencing nectary and nectar biodiversity.
... In contrast to Charlesworth's (1993) hypothesis, Ashman (2000) found that pollinators distinguish between female and hermaphroditic flowers, visiting hermaphrodites more frequently than females. These results agree with findings of previous studies of florally dimorphic plant species, which also reported that pollinators distinguish between male and female or hermaphroditic flowers (Bell et al. 1984;Agren et al. 1986;Bierzychudek 1987;Kevan et al. 1990;Ashman and Stanton 1991;Delph and Lively 1992;Eckhart 1992;Greco et al. 1996). Given these results, Ashman (2000) suggested that the association of dioecy and generalist pollinators results from the diversity of generalist pollinators, which reduces variance in pollination success by reducing dependence on any one pollinator species. ...
Article
Full-text available
We consider the role of generalist Diptera in the pollination of two dioecious plant species, Clematis ligusticifolia Nutt. (Ranunculaceae) and Shepherdia canadensis (L.) Nutt. (Elaeagnaceae). In particular, we assess (i) whether or not generalist pollinators are unable to distinguish between the sexes of dioecious species and so visit the sexes at equivalent rates, and (ii) the number of flowers that generalist flies visit and revisit during a foraging bout, which would affect self-pollination if plants were hermaphroditic. We determined the visitation rate to each plant species during 10 min periods and recorded the number of flowers that individual pollinators visited and revisited per foraging bout. Diptera were the main pollinators, visiting both sexes at similar rates for both plant species. The main visitors to C. ligusticifolia were muscoid flies (small and large), Culicidae, and halictid bees. The number of flowers visited in this species varied with pollinator group, but groups did not differ in the frequency of revisits. Visitors to S. canadensis were primarily Syrphidae and Empididae. Neither the number of flowers visited nor the number of revisits differed between these two pollinator groups. The results for each plant species are discussed and contrasted, particularly with other studies of the behaviour of generalist and specialist pollinators. We compare the observed pollinator behaviours, and their implications for plant mating, with the various theories of the role of pollinators in the evolution of the dioecious breeding system in plants.
... Nectar composition may differ in male and female flowers of monoecious and dioecious species. That produced by female flowers of Cucurbita pepo, Euterpe precatoria and Rhus hirta is more abundant and more concentrated than that of male flowers (Greco et al. 1996, Ku¨chmeister et al. 1997). On the other hand, in the three species of the genus Silene, Witt et al. (1999) found more concentrated nectar in male flowers. ...
Article
Full-text available
Nectaries differ in many aspects but a common feature is some kind of advantage for the plant conferred by foraging of consumers which may defend the plant from predators in the case of extrafloral nectaries, or be agents of pollination in the case of floral nectaries. This minireview is concerned mainly with floral nectaries and examines the following characteristics: position in flower; nectary structure; origin of carbohydrates, amino-acids and proteins; manner of exposure of nectar; site of nectar presentation; volume and production of nectar in time; sexual expression of flower and nectary morphology; nectar composition and floral sexual expression; variability of nectar composition; fate of nectar; energy cost of nectar production. The species of certain large families, such as Brassicaceae, Lamiaceae and Asteraceae, resemble each other in nectary organisation; other families, such as Cucur-bitaceae and Ranunculaceae, have various types of organisation. A scheme is presented to illustrate factors influencing nectary and nectar biodiversity.
... Der Essigbaum ist zweihäusig und wird ausschließlich durch Insekten bestäubt. Die Art ist besonders bei Imkern beliebt (Greco et al. 1996). Ältere Exemplare produzieren viele Samen, die allerdings einer ausgeprägten Keimhemmung unterliegen, die auch künstlich nur schwer zu überwinden ist. ...
Book
Full-text available
Eine nachhaltige, multifunktionale Forstwirtschaft hat den Anspruch, Wälder so zu pflegen und zu nutzen, dass deren Produktivität, Verjüngungsfähigkeit, Vitalität und biologische Vielfalt erhalten bleiben. In der Vergangenheit hat sich gezeigt, dass weder im Kielwasser der Rohholzerzeugung noch in jenem des Naturschutzes alle Waldfunktionen angemessen erfüllt werden. Die Integration eingeführter Baumarten in einen Waldbau auf ökologischen Grundlagen erfordert daher Kompromisse, die sich auf der Basis wissenschaftlicher Erkenntnisse in der Regel auch finden lassen. Konkret bedeutet dies, dass der Anbau nicht invasiver eingeführter Baumarten in gewissem Umfang vom Naturschutz ebenso akzeptiert wird, wie seitens der Forstwirtschaft naturschutzfachliche Interessen berücksichtigt werden, indem bei ihrem Anbau auf eine räumliche Ordnung geachtet wird und bestehende Vorkommen invasiver Baumarten zurückgedrängt werden. Ziel dieser Ausarbeitung ist es vor diesem Hintergrund, die Potenziale und Risiken von 15 eingeführten Baumarten auf der Grundlage wissenschaftlicher Literatur und langjähriger Forschungsarbeiten auf Versuchsflächen der verschiedenen Forschungseinrichtungen und Anbauflächen der Forstbetriebe aufzuzeigen, um die zwischen Naturschutz und Forstwirtschaft aufgekommene Diskussion zu versachlichen.
... In contrast to Charlesworth's (1993) hypothesis, Ashman (2000) found that pollinators distinguish between female and hermaphroditic flowers, visiting hermaphrodites more frequently than females. These results agree with findings of previous studies of florally dimorphic plant species, which also reported that pollinators distinguish between male and female or hermaphroditic flowers (Bell et al. 1984;Agren et al. 1986;Bierzychudek 1987;Kevan et al. 1990;Ashman and Stanton 1991;Delph and Lively 1992;Eckhart 1992;Greco et al. 1996). Given these results, Ashman (2000) suggested that the association of dioecy and generalist pollinators results from the diversity of generalist pollinators, which reduces variance in pollination success by reducing dependence on any one pollinator species. ...
Article
In dioecious, bee‐pollinated tree species, male and female flowers offer different resources. It is unclear how this unbalanced quantity and quality of floral resources affects flower visits and pollen transfer to female flowers. We asked, what characteristics of flowering and dynamics of resource production by trees favour flights of bees between male and female trees. We quantified the floral resources produced by individual flowers and entire trees of Myracrodruon urundeuva (Anacardiaceae), measured pollen flow to female flowers, fruit set of naturally pollinated flowers and determined the effective pollinators. Crown volume of male trees was four‐fold, flower number 15‐fold and nectar volume 60 times higher than in female trees. While ~70% of male flowers opened in the morning, ~70% of female flowers opened in the afternoon. Fruit set was 27%. Stingless bee species were the main pollinators, while honeybees were common only on male flowers. Strongly unbalanced production of floral resources, high potential lifespan of female flowers and anticipated opening of male flowers favour pollinator movement and pollen deposition on female flowers, albeit low (0.003% of pollen that reached stigmas), but sufficient to produce thousands of fruits per tree. Besides being an astonishing pollen and nectar source for numerous social bee species, only a few of them were effective pollinators. Our quantitative approach to floral resource production of each gender provides new insights, such as the proportion of resources allocated to each gender and the corresponding behaviour of flower visitors, for understanding the reproductive strategy of dioecious tropical mass‐flowering trees. Male biased flower attractiveness, higher lifespan of female flowers, staggered flowering, and anticipated anthesis of male flowers favor the flights of stingless bee pollinators among trees in a dioecious mass‐flowering species.
Article
Full-text available
Our objective was to examine how bee foraging preferences on dioecious willows are influenced by plant sex, time of day, by sampling date on multiple sites and across different willow species. In a common garden experiment examining diurnal pollinator visitation patterns of Andrena bees (andrenids), there was a strong preference for male willow plants: 87% of visitations on male plants of Salix eriocephala (ERI) and 71% on males of S. interior (INT). The significant plant sex × time of day interaction was not a result of a change in bee preference for a certain plant sex during a certain part of the day but rather the result of diurnal changes in the magnitude of the preference of andrenid bees for male willow plants. Visits to male flower catkins were highest in the morning and early afternoon, peaking at midday. Visits to female catkins showed a more uniform, lower frequency visitation pattern throughout the day. In a larger field test at a reclaimed former coal mine site, which included S. cordata (COR) as well as ERI and INT, there were no sampling date × plant sex or sampling date × plant sex × willow species interactions. This indicates no plant sex switching behaviour by sampling date for the three willow species. Preference for male plants was greatest on the first sampling day and the proportion of male preference continued to decline until the fourth and final sampling day. On the mine site, 17 of the 25 Apoidea bee species identified were andrenids, and they represented 92% of the 744 individual bees collected while foraging on willow catkins. In addition, the overall number of observed and collected Apoidea bees visiting available flowering willow plants showed that the preference for male plants was 83%, 72% and 91%, for ERI, INT and COR, respectively. We discuss possibilities for promoting populations of native bees to increase commercial fruit and berry crop pollination by using willows as natural sources of pollen and nectar, thereby reducing costs of production associated with the annual importation of commercial bees. This article is protected by copyright. All rights reserved.
Article
The family Anacardiaceae Lindl. (cashew family, sumac family) is one of the nine families of the order Sapindales Dumortier. It consists of about 600 species classified in 70 genera. Members of the family are shrubs, trees and lianas with pantropical distribution; however, a few species occur in the North Temperate Zone. Some species are used for the production of fruit (mango, mombin), some species are cultivated for edible seeds (pistachio, cashew nuts). Many species are of toxicological importance, especially members of the genus Toxicodendron P. Mill., other species are widely used in folk medicines. This review introduces the most widely cultivated species of the Anacardiaceae family in the Czech Republic and concurrentlyinvasive plant Staghorn Sumac - Rhus hirta (L.) Sudw. The secondary metabolites, their pharmacological properties and pharmaceutical importance of the species are discussed.
Article
Full-text available
The hypothesis that male-biased sex ratios result from the great costs of reproduction for females was examined at various modular levels in a study of staghorn sumac. Study suggests the importance in a clonal species of defining the modular level at which costs are assessed. The hypothesis that females suffer greater reproductive costs as a consequence of fruit production is supported by the finding of diminished survivorship of daughter trunks in female clones, but it is not supported by data on annual trunk diameter increments. Reproductive costs in sumac are shown at the level of the clone (ramet survivorship) or the branch, rather than at the level of the flowering trunk module. -from Authors
Article
Rhus hirta (L.) Sudworth is based on Datisca hirta L., a name long rejected as a monstrosity but which has priority over Rhus typhina L. (1756). Three formae of the North American staghorn-sumac are recognized: Two cultivated, f. hirta (including R. typhina f. laciniata (Wood) Rehder) and f. dissecta (Rehder) Reveal; one wild, R. hirta f. typhina (L.) Reveal (here lectotypified).
Article
(1) Three foraging ecology models (optimal diet; minimal uncertainty; individual constancy) were studied by using honey bees in an artificial patch of yellow, blue, and white flowers. Reward quality, quantity and frequency were varied. (2) When rewards were identical in all flower morphs some bees were constant to yellow flowers, while others randomly visited only blue and white flowers. (3) Foraging patterns did not change when any one flower morph was given a higher quantity of reward. (4) However, foraging patterns of some bees did change when reward quality or frequency differed between flower types. When blue flowers had a higher quality or frequency of reward than white, bees randomly visiting blue flowers and white flowers became constant to blue flowers. Bees visiting yellow flowers remained constant even though they offered a poorer reward. The same type of response was observed when white flowers had a higher quality or frequency of reward than blue. When yellow flowers had the better reward, bees visiting blue flowers and white flowers did not switch to yellow. (5) Although bees are capable of distinguishing our blue flowers from the white morph, they behaviourally displayed this capacity only under some circumstances when benefits of doing so were high. (6) Individually constant foraging in honey bees appears to be a `superstructure,' within which the subclassifications `optimal diet' and `minimal uncertainty' foraging may occur. Thus, in the experiments herein reported, foraging ecology is more complex than could be predicted by any one of the models tested.
Article
1. The numbers of honey and solitary bees visiting five varieties of apple growing in the same orchard were correlated with the abundance of their flowers. The relative attractiveness of each variety depended on the stage of flowering. 2. Honeybees distinguished between at least some of the varieties and, when the variety they were visiting remained relatively attractive, they tended to remain constant to it. When this variety became less attractive, they tended to move to another. 3. The foraging areas of individual honeybees on attractive varieties remained quite small over consecutive trips. 4. The implications of these results on the efficient planting of orchards for cross-pollination are discussed.
Article
The reproductive biology of five populations of Rhus integrifolia and R. ovata was studied. The breeding system of the two species is better described as gynodioecious rather than polygamodioecious. Hybridization between the two species was discovered in one population where they were sympatric. The presence of less than 50% male steriles in each population suggests that gynodioecism is inherited via the nucleus in both taxa. Increased seed set of male steriles, compared to hermaphrodites, appears to be the mechanism by which gynodioecism is maintained in natural populations of the two species, and is presented as another example supporting the model of Ross and Shaw (1971). Self-incompatibility appears to be the mechanism reducing seed production in hermaphrodites. Seed parasitism by small wasps (Eurytomidae and Torymidae) was discovered in both species, and involved approximately 50% of all seeds produced. The gradual evolution from hermaphrodite to male-sterile was evident, and it is suggested that gynodioecism, in itself, is an effective out-breeding mechanism in the two species.
Article
Pollen is transferred between bees as they brush against each other inside the hive, so that much of the pollen on the bodies of bees leaving to forage comes from species other than the crop on which they are working. The pollen being collected most abundantly by a colony occurs on most of its bees. Many foraging bees still carry some 'foreign' pollen on their bodies, but because it is more diluted with pollen from the crop being worked, pollen-gatherers have proportionally less 'foreign' pollen than nectar-gatherers.