THE ROLE OF RESIN IN ANGIOSPERM POLLINATION: ECOLOGICAL AND CHEMICAL CONSIDERATIONS

Members of at least two unrelated genera of plants, Dalechampia (Euphorbiaceae) and Clusia (Guttiferae), attract pollinators by secreting resins from floral structures. Bees that pollinate these flowers collect and use the resin in nest construction; these include Euglossa, Eulaema, Eufriesea, Trígona and, Hypanthidium in the neotropics, and Heriades in Africa. Floral resins are slow in hardening as compared with many other plant resins; this facilitates collection and storage by bees, hence probably enhancing the attractiveness of the flowers. Floral resins are probably of great utility and dependability and may be an especially important resource to certain bees, which in turn are major pollinators of many species of tropical plants. Bees appear to forage floral resin using a “strategy” of energy efficiency; large bees collect resin only from copious sources, smaller bees collect resin from sources with small amounts as well as from sources with large amounts of resin. Resin secretion in flowers may have originated as defense against herbivores and secondarily assumed the role of pollinator reward.     

Dioecious <Emphasis Type="Italic">Clusia nemorosa</Emphasis> achieves pollination by combining specialized and generalized floral rewards

Plants often combine multiple strategies to achieve pollen transfer. The dioecious Clusia nemorosa (Clusiaceae) produces floral resin, a specialized reward for resin-collecting bees. It also exhibits floral automimicry with female flowers mimicking male flowers in order to attract pollen-collecting insects. We observed the hourly visitation frequency and behaviour of bee visitors on two rock savanna sites in French Guiana. The major strategy in pollen transfer and the variation in visitation rates among visitor species were examined. We hypothesized that the visitation rate will vary between the floral sexes and degree of this variation will differ between the two-reward systems. We found no evidence for visits being exclusively related to resin collection, which we expected to be the principal strategy in pollen transfer. Deceit pollination appeared to have minor importance and seemed to be locally associated with the site, where demand for pollen was greater. Flower visits that probably facilitated most pollen transfer, combined resin and pollen. The pollinators involved in this system collected pollen from male flowers and resin from female flowers. The fruit set was not particularly low (44.19%) so offering different rewards by different flower genders has not constrained reproductive success in this system. Pronounced variation in visitation rates between sexes was not related to the pollination mechanisms but to the demand for the two rewards. Overall demand for pollen was greater than demand for resin. Female flowers were visited much less frequently than male flowers. Peak pollen collection occurred in the morning, i.e., as soon as the resource was available, while resin was collected throughout the day. There was a local variability in demand for the two resources because both the visitation rate and the behaviour of foraging bees varied between the two observation sites.     

Pollinator responses to variation in floral display and flower size in dioecious Sagittaria latifolia (Alismataceae)

In animal-pollinated plants with unisexual flowers, sexual dimorphism in floral traits may be the consequence of pollinator-mediated selection. Experimental investigations of the effects of variation in flower size and floral display on pollinator visitation can provide insights into the evolution of floral dimorphism in dioecious plants. Here, we investigated pollinator responses to experimental arrays of dioecious Sagittaria latifolia in which we manipulated floral display and flower size. We also examined whether there were changes in pollinator visitation with increasing dimorphism in flower size. In S. latifolia, males have larger flowers and smaller floral displays than females. Visitation by pollinators, mainly flies and bees, was more frequent for male than for female inflorescences and increased with increasing flower size, regardless of sex. The number of insect visits per flower decreased with increasing floral display in males but remained constant in females. Greater sexual dimorphism in flower size increased visits to male inflorescences but had no influence on the number of visits to female inflorescences. These results suggest that larger flower sizes would be advantageous to both females and males, and no evidence was found that females suffer from increased flower-size dimorphism. Small daily floral displays may benefit males by allowing extended flowering periods and greater opportunities for effective pollen dispersal.     

Understanding the basis of pollinator selectivity in sexually dimorphic Fragaria virginiana

Pollinators of gender dimorphic (e.g., gynodioecious or dioecious) species often show a preference for hermaphrodite or male flowers over conspecific females, and such pollinator selectivity can have implications for the evolution of sexual dimorphism. However, because the sex morphs differ in several floral features, it is not readily apparent which specific traits generate differential pollinator service. In this study, we sought to understand the basis of pollinator preferences for hermaphrodites to females of gynodioecious Fragaria virginiana . We extend a previous study that revealed that lack of pollen-filled anthers and shorter petals were not solely responsible for small bee and fly discrimination against females, by investigating the roles of other morphological features, reward characters, and floral context in bringing about pollinator discrimination. Using floral manipulations we revealed that small bees preferentially visit flowers with wide petals, more nectar, intact stamens, as well as flowers located in hermaphrodite-dominated patches. Specifically, bees were able to remotely detect nectar presence. In addition, bees were attracted to both the anther sac and the filament regions of the stamen, indicating that not only anthers, but also filaments may function as visual or olfactory cues to pollen reward. Furthermore, pollinator preference for flowers in hermaphrodite-dominated patches serves to intensify their discrimination against female flowers which occur predominantly in female-dominated patches. For the most part, preferences of flies mirrored those of the bees with the exception that flies also showed a significant preference for flowers held high over those held closer to the ground. These results indicate that a suite of character differences contributes to pollinators' preferences for hermaphrodite to female flowers. Furthermore, they suggest pollinators could mediate selection on both floral morphology and reward in this species.     

Floral biology and reproductive ecology ofClusia nemorosa (Clusiaceae) in northeastern Brazil

Between March 1993 and May 1995 the floral biology and the phenology ofClusia nemorosa G. Mey. (Clusiaceae) were studied in two dioecious populations in Pernambuco State, and some observations were made in gynodioecious populations, that were encountered only in Bahia State. The species flowers from June to January/February. The flowers are bowl shaped, and last only one day. The floral reward is resin which is produced by staminodia in all types of flowers. The sex ratio was 1:1 for the studied populations. The pollen viability was approximately 98%. Apomixis was not observed. The rate of fruit set, in hermaphrodite individuals, under natural conditions and the sex ratio of the gynodioecious populations studied suggest that the hermaphrodite individuals may behave as males.Clusia nemorosa is melittophilous and was visited by 16 species of bees. The main pollinators wereEuplusia mussitans, E. iopyhrra, Eulaema cingulata, E. nigrita, Euglossa cordata andEuglossa sp.     

Two polyisoprenylated benzophenones from the trunk latex of Clusia grandiflora (Clusiaceae)

The polyisoprenylated benzophenones, chamones I and II, were isolated from the trunk latex of Clusia grandiflora (Clusiaceae) growing in southeastern Venezuela. A third benzophenone, nemorosone II, was isolated from the pollinator reward resin of the female flowers of the same plant. Chamone I and nemorosone II are structurally similar, differing only in the degree of prenylation. Bioassays of chamone I and nemorosone II using the honeybee pathogens, Paenibacillus larvae and Paenibacillus alvei, demonstrate that both have potent antibacterial activity, and that their structural differences affect both their bactericidal efficacies and their aqueous mobilities.     

Behavioral responses of the small hive beetle,Aethina tumida,to odors of three meliponine bee species and honey bees,Apis mellifera scutellata

Recent studies have shown that honey bees, bumble bees, and some meliponine bee species of the genera Trigona, Meliponula, and Dactylurina are hosts of the small hive beetle (SHB) Aethina tumidaMurray (Coleoptera: Nitidulidae), a pest of honey bee colonies in various regions of the world. Olfaction has been implicated in SHB infestations of honey bee and bumble bee colonies. We used olfactometer bioassays to investigate responses of adult male and female SHBs to odors from intact colonies and separate hive components (pot honey, pot pollen, cerumen, and propolis) of three African meliponine bee species, Meliponula ferruginea (Lepeletier) (black morphospecies), M. ferruginea (reddish brown morphospecies), and Meliponula bocandei (Spinola) (Hymenoptera: Apidae). Although both sexes of the beetle strongly preferred intact colony, pot honey, and pot pollen odors, there was no evidence of attraction to propolis and cerumen odors from the three meliponine bee species. Both sexes of SHB also strongly preferred odors from honey bees, Apis mellifera L. (Hymenoptera: Apidae), over odors from the three meliponine bee species. Our results provide substantial evidence of the host potential of African meliponine bees for the SHB, and we discuss this complex association of the SHB with species within the Apidae family.     

Pollination in Geonoma macrostachys and Three Congeners,G. acaulis,G. gracilis,and G. interrupta

A continuous 15 month study of the floral ecology of four syntopic understorey palm species of Genoma was conducted in Amazonian Peru lowland rainforest. The spicate inflorescences of G. macrostachys, G. acaulis and G. gracilis are strictly protandrous and the plants are functionally dioecious. Data suggest that in G. macrostachys and G. acaulis pollination is based on a mimicry system, the pistillate flowers mimicking the staminate ones in colour, shape and scent. Pollen-collecting meliponine bees (Hymenoptera, Apidae, Meliponinae) and pollen-feeding syrphid flies (Diptera, Syrphidae) which visit inflorescences during both sexual stages are the pollinators of G. macrostachys. Geonoma acaulis is pollinated by small pollen-feeding weevils (Coleoptera, Curculionidae, Derelomini) that visit male and female spikes. Additionally, in G. macrostachys another pollinator type, viz. euglossine bees (Hymenoptera, Apidae, Euglossinae), which are attracted and rewarded by both types of flowers may account for long-distance pollination. The palm G. gracilis shows a very distinct pollination system. Although opportunistic insect visitors are attracted to the inflorescences of this species it seems to be mainly anemophilous because pollen becomes powdery during an thesis. The branched inflorescences of G. interrupta are also protandrous, but unlike the other species of Geonoma observed, staminate and pistillate anthesis of individual flowers are, for the most, overlapping. A broad spectrum of visitors is attracted (bees, wasps, flies, and beetles), which all may act as pollinators. Outcrossing is especially encouraged during the purely female phase at the end of the flowering cycle when there are no more staminate flowers in the inflorescence. Effects on the reproductive biology and population structure of different pollination systems and breeding system are discussed.     

Floral reward presentation favored the expression of male function in the pollen‐only flower Melastoma malabathricum

Abstract Animal‐pollinated plant species modulate the presentation of pollinator rewards to maximize reproductive success. In plants providing pollen as the only reward for pollinators, it is usually difficult to unravel the dual roles of reward presentation and the realization of male and female functions (pollen removal and deposition). Exploiting the two types of anther in the androecia of Melastoma malabathricum L., we examined whether the removal of pollen for reward is regulated primarily to favor male function or female function. Pollen removal by carpenter bees from the feeding and pollination anthers, as well as pollen deposition on the stigmas, were quantified during anthesis of M. malabathricum. There was no significant difference in pollen removal rates from the feeding and pollination anthers of M. malabathricum between the onset of anthesis and flower wilting. The stigmatic pollen loads exceeded the ovule number after three sonication bouts, and female function was satisfied earlier than male function. The results support the hypothesis that the presentation of pollination reward in this species is regulated primarily to favor the expression of male function, rather than female function, in agreement with the pollen‐donation hypothesis. A cooperative relationship between the feeding and pollination anthers was demonstrated in heterantherous flowers, which optimizes the balance in investments between pollinator rewards and “functional pollen” for gene transfer.     

Fine-scale temporal dynamics of flower visitors sheds light on insect-assemblage overlap between sexes in a dioecious Ecuadorian palm

Dioecious plants generally display sexual dimorphism in male and female floral traits, potentially attracting slightly different pollinator communities. The sharing of common floral visitors between male and female flowers and their timing of visits to both sexes is of critical importance to ensure plant's reproductive success. Palm inflorescences are visited by abundant and diverse insect communities, yet the temporal patterns of insect visits on both sexes remain poorly known. We characterized the composition of a community of flower-visiting arthropods associated with the dioecious ivory palm (Phytelephas aequatorialis, Spruce) in a pre-montane forest of Ecuador. We monitored the temporal variations in insect visits along the flowering of 12 inflorescences (eight female and four male) using interception traps recovered every 4 h. We report 59 morphospecies in the arthropod community, dominated by three beetle families: Staphylinidae, Nitidulidae, and Curculionidae. Male inflorescences were more abundantly visited than female, but visitors of the later were taxonomically more diverse. Among the 16 pollinator candidates identified, nine visited both inflorescence sexes synchronously at dusk /night whereas the others did so asynchronously during the day. Our study provides new insights into the pollination mechanism of P. aequatorialis. We found evidence of differential pollinator attraction between floral sexes, which may be explained by the sexual dimorphism of both flowers. Synchronicity in dusk/night visits of both inflorescence sexes suggests a sexual synchronization of the signal used to attract pollinators.     

Isolation of polymorphic microsatellite loci in the genus Clusia (Clusiaceae)

Microsatellite flanking region sequences may provide phylogenetically useful information. We isolated 13 polymorphic microsatellite loci from two species, Clusia minor (five loci) and Clusia nemorosa (eight loci), to aid in the determination of phylogenetic relationships within the genus Clusia. Eleven loci amplified across all 17 Clusia species tested, while two loci amplified in 10 out of 17 species. The extensive cross‐species amplification suggests that these loci may be useful for an examination of phylogenetic relationships in this genus.     

Naturalized Orchid Bee Pollinates Resin‐reward Flowers in Florida: Novel and Known Mutualisms

Females of an orchid bee, Euglossa viridissima, recently naturalized in southern Florida, routinely collect resin to construct their brood cells from the flowers of two Clusia (Clusiaceae) and two Dalechampia (Euphorbiaceae) species. We demonstrated that the bee pollinates three of these species including: (1) the newly naturalized D. scandens, which it pollinates in Mexico; (2) the ornamental D. aristolochiifolia native to Peru; and (3) the ornamental C. lanceolata native to Brazil, but not the apomictic Clusia rosea native to Florida. Field observations indicated that the bee promotes outcrossing in a naturalized D. scandens population. Comparisons of fruit set between unmanipulated control flowers and flowers supplemented with additional pollen indicated that the presence of bee eliminates pollen limitation for cultivated C. lanceolata. The orchid bee's pollination of ornamental resin‐reward plants may promote their naturalization.     

Phenotypic divergence and inter-specific trait correlation in a plant-pollinator/seed predator mutualism

Plant-pollinator interactions have been suggested as key drivers of morphological divergence and speciation of the involved taxa. These interactions can also promote sexual dimorphism in both the plant and pollinator, particularly if the pollinator is also a seed-eater and/or exerts different selection pressures on male and female plants. Here we tested the hypotheses that plant-pollinator interactions can be reflected in trait variation and sexual dimorphism in both organisms within and across populations. Across nine European populations, we examined intraspecific variation and sexual dimorphism in phenotypic traits potentially involved in the plant–insect interaction of the dioecious white campion Silene latifolia (Caryophyllaceae) and its specialist pollinator Hadena bicruris (Noctuidae). This interaction is expected to entail sex-specific selective pressures, as female moths lay eggs on female plants and the larvae predate on the seeds during their development. We compared divergence in phenotypic traits among populations and between sexes within populations, examined correlations between plant and pollinator traits, and between phenotypic distances and genetic distances among co-occurring populations for both plants and insects. We found key differences in phenotypic traits across populations of both the plant and moth, though only in the moth were these differences correlated with geographic distances. We also found evidence for sexual dimorphism in the plant but not in the pollinator. Evolution of floral sexual dimorphism in S. latifolia most likely results from the joint contribution of different selective forces, including biotic interactions with H. bicruris moths.     

Flower development and anatomy of Clusia valerioi,a Central American species of Clusiaceae offering floral resin

The present paper is part of a study dealing with various aspects of reproduction of two Costa Rican Clusia species offering resin as a floral reward. It provides data on the floral development and flower (especially stamen and staminode) anatomy of one of the species, Clusia valerioi. In the early stages, both male and female flowers develop in the same manner. The bracts are distinguished by a decussate arrangement from the five sepals and five petals, which emerge in a spiral manner. In the male flowers the apical meristem forms five meristematic mounds (common stamen primordia) that are pentagonally arranged around the apical meristem in epipetalous position. From these mounds, the primordia of the proper stamina emerge in 3–5 whorls. Direction is centrifugal. In the centre, five hemispherical bulges arise which develop into carpel primordia. These, however, cease growth, stay rudimentary and are hidden by the stamens in the mature male flower. The adult stamens consist mainly of a thick angular filament column, while the two anthers situated at the flattened top are very small. One anther is annular and surrounds a second, hemispherical one right in the centre. At the periphery, these two pollen sacs (provided with a distinct wall of customary anatomy) are surrounded by a ring-like protuberance of the filament. The resin canals are situated at the periphery of the filament. Their schizogenous development is documented in cross sections. At anthesis, the resin is released from the ring-like filament protuberance by burst of the single-layered epidermis. In the female flower, the five meristematic mounds produce two whorls of staminode primordia. The development of the staminodes does not essentially differ from that of the fertile stamens, but some staminodes lack the central pollen sac and the other tissues do not develop into pollen grains. An attempt is made to derive the peculiar stamen morphology of Clusia valerioi and similar species from conventional stamens. Three hypotheses are proposed and discussed.     

Impacts of floral gender and whole-plant gender on floral evolution in Ecballium elaterium (Cucurbitaceae)

Investigation of gender specialization in plants has led to several theories on the evolution of sexual dimorphism: reproductive compensation, based on enhanced reproductive efficiency with gender specialization (flowers should be larger on dioecious plants); Bateman's Principle, based on sex-specific selection (display for pollinator attraction in males and seed set in females); and intersexual floral mimicry, based on mimicry of a reward-providing gender by a non-reward providing gender (reduced dimorphism in dioecious plants due to increased spatial separation of male and female flowers). These theories were evaluated in Ecballium elaterium, which contains two subspecies, elaterium (monoecious) and dioicum (dioecious). Our results show that flowers of the dioecious subspecies are larger and allocate more to reproductive organs than do flowers of the monoecious subspecies. Both subspecies are sexually dimorphic (male flowers larger than female flowers). Variance in flower size among populations is greater in the dioecious subspecies. Finally, there is sufficient genetic variation to enable ongoing response to selection; genetic correlation constraints on independent response of female and male flowers may be stronger in the monoecious subspecies. Our findings provide support for aspects of all three theories, suggesting that the evolution of floral dimorphism is based on a complex interplay of factors.     

Behavioral suites mediate group-level foraging dynamics in communities of tropical stingless bees

Competition for floral resources is a key force shaping pollinator communities, particularly among social bees. The ability of social bees to recruit nestmates for group foraging is hypothesized to be a major factor in their ability to dominate rich resources such as mass-flowering trees. We tested the role of group foraging in attaining dominance by stingless bees, eusocial tropical pollinators that exhibit high diversity in foraging strategies. We provide the first experimental evidence that meliponine group foraging strategies, large colony sizes and aggressive behavior form a suite of traits that enable colonies to improve dominance of rich resources. Using a diverse assemblage of Brazilian stingless bee species and an array of artificial “flowers” that provided a sucrose reward, we compared species’ dominance and visitation under unrestricted foraging conditions and with experimental removal of group-foraging species. Dominance does not vary with individual body size, but rather with foraging group size. Species that recruit larger numbers of nestmates (Scaptotrigona aff. depilis, Trigona hyalinata, Trigona spinipes) dominated both numerically (high local abundance) and behaviorally (controlling feeders). Removal of group-foraging species increased feeding opportunities for solitary foragers (Frieseomelitta varia, Melipona quadrifasciata and Nannotrigona testaceicornis). Trigona hyalinata always dominated under unrestricted conditions. When this species was removed, T. spinipes or S. aff. depilis controlled feeders and limited visitation by solitary-foraging species. Because bee foraging patterns determine plant pollination success, understanding the forces that shape these patterns is crucial to ensuring pollination of both crops and natural areas in the face of current pollinator declines.     

Pollen morphology and functional dioecy inSolanum (Solanaceae)

Dioecy has evolved independently several times in the large, mostly tropical genusSolanum. In all cases of dioecy inSolanum functionally male flowers have normal anthers, normal pollen and reduced stigmas while functionally female flowers have stigmas and anthers that appear normal but contain non-functional, usually inaperturate pollen. The inaperturate pollen has living cytoplasm, but apparently never germinates and it has been hypothesised that the pollen in these functionally female flowers is retained as a pollinator reward. Pollen morphology is compared in twelve of the thirteen known dioecious species ofSolanum, and some stages in the the development of inaperturate pollen in the anthers of functionally female flowers ofSolanum confertiseriatum of Western Ecuador are examined. Observations on the development and morphology of inaperturate pollen in functionally female flowers ofSolanum are related to hypotheses about the evolution of dioecy in the genus.     

Polyploidization and sexual dimorphism of floral traits in a subdioecious population of Dasiphora glabra

银露梅亚雌雄异株种群的多倍化和花特征性二态 性二态是性别分离植物的常见性状,对植物的雌性和雄性功能可能产生不同的影响。本文以青藏高原特有植物银露梅(Dasiphora glabra)为研究对象,利用银露梅同时存在两性、雌性和雄性植株的种群,探讨银露梅与传粉相关的花特征性二态现象及其对传粉者访问、花粉流和结实的影响。另外,本文还利用流式细胞仪检查了两性植株、雄性植株和雌性植株之间基因组大小的差异。研究结果表明：银露梅雌性植株和雄性植株数量约占种群中植株总数量的40%,表明银露梅两性植株数量多于雄性和雌性的植株数量。两性植株的花数量显著多于雄性和雌性植株的花数量。雄花的花大小显著大于雌花和两性花的花大小。雄花的花粉数量与两性花的花粉数量没有差异,但是雌花的胚珠数量显著高于两性花的胚珠数量。双翅目的蝇类是银露梅最主要的访花者,尽管访花者偏好访问更大的花,但是在花间连续访问对大花没有表现出偏好。模拟花粉流实验表明,两性植株和雄性植株的有效花粉转移都很低,从而导致较低的结实率。雌性植株和雄性植株的DNA含量约为两性植株的4倍,并且单性植株和两性植株之间相互授粉不能结实。以上结果表明,与两性花相比,雌花和雄花在与传粉相关的花特征二态性上分别在雌性和雄性功能上表现出优势,但这种优势在很大程度上被低效的花粉转移所掩盖。银露梅的雌性植株和雄性植株经历了多倍化事件,导致与两性植株之间存在繁殖隔离,从而维持了3种性别植株的共存。     

Pollinators entering female dioecious figs: why commit suicide?

In the dioecious fig/pollinator mutualism, the female wasps that pollinate figs on female trees die without reproducing, whereas wasps that pollinate figs on male trees produce offspring. Selection should strongly favour wasps that avoid female figs and enter only male figs. Consequently, fig trees would not be pollinated and fig seed production would ultimately cease, leading to extinction of both wasp and fig. We experimentally presented pollinators in the wild (southern India) with a choice between male and female figs of a dioecious fig species, Ficus hispida L. Our results show that wasps do not systematically discriminate between sexes of F. hispida. We propose four hypotheses to explain why wasp choice has not evolved, and how a mutualism is thus maintained in which all wasps that pollinate female figs have zero fitness.     

Relative importance of diurnal and nocturnal pollinators for reproduction in the early spring flowering shrub Stachyurus praecox (Stachyuraceae)

Generalized pollination systems may be favored in early spring flowering plants, as during this period pollinator activity is unpredictable. Many previous studies have concentrated on the importance of diurnal visitors in pollination, and consequently, information on the contribution of nocturnal visitors to pollination in early spring is limited. This study was conducted to evaluate the relative importance of diurnal and nocturnal pollinators in the early spring flowering dioecious shrub Stachyurus praecox (Stachyuraceae), in two temperate forests in central Japan. Visitors to the female and male flowers were observed during day and night, and their relative contributions to seed set were compared. The pollinator observations revealed that the diurnal and nocturnal insects visited both male and female flowers, and that the main flower visitors were diurnal small bees and flies as well as nocturnal settling moths. The diurnal and nocturnal flower visitors also acted as pollinators, as the pollen grains of S. praecox were attached to the insects collected from the female flowers. Pollination experiments demonstrated that the contributions of diurnal pollinators to the seed set were higher than those of the nocturnal pollinators. The results of this study indicate that S. praecox has a generalized pollination system, comprising both diurnal insects and nocturnal settling moths. Although the roles of diurnal insects are more important in the pollination of S. praecox, nocturnal settling moths may have a complementary role in early spring.