Pollination of Cyphomandra endopogon var. endopogon (Solanaceae) by Eufriesea spp. (Euglossini) in French Guiana

The pollination systems of two closely related genera.Cyphomandra andSolanum, differ in rewards offered and pollinator activity. I suggest that the anther differences which define these two genera have evolved in response to the different pollination systems. Male euglossine bees of the genusEufriesea were observed to pollinate the flowers ofCyphomandra endopogon var.endopogon while gathering aromatic compounds from the anther connectives. Samples of the compound collected from the flowers and the bees were tentatively identified as ocimene, a terpene.     

Floral biology of two Vanilloideae (Orchidaceae) primarily adapted to pollination by euglossine bees

Vanilloideae comprises 15 genera distributed worldwide, among which are Vanilla and Epistephium (tribe Vanilleae). Based on field and laboratory investigations, the pollination biology of V. dubia and E. sclerophyllum was analysed. The former was surveyed in a semi‐deciduous mesophytic forest at the biological reserve of Serra do Japi and in a marshy forest at the city of Pradópolis, southeastern Brazil. The latter was examined in rocky outcrop vegetation in the Chapada Diamantina, northeastern Brazil. In the studied populations, the tubular flowers of V. dubia and E. sclerophyllum were pollinated by bees. Pollen was deposited on either their scutellum (V. dubia) or scutum (E. sclerophyllum). The mentum region of V. dubia is dry, whereas that of E. sclerophyllum presents a small quantity of dilute nectar. Flowers of E. sclerophyllum are scentless, while those of V. dubia are odoriferous. Although V. dubia is self‐compatible, it needs a pollinator to produce fruit. In contrast, E. sclerophyllum sets fruit through spontaneous self‐pollination, but biotic pollination also occurs. Both species are primarily adapted to pollination by euglossine bees. Pollination by Euglossina seems to have occurred at least twice during the evolution of Vanilleae. Furthermore, shifts between rewarding and reward‐free flowers and between autogamous and allogamous species have been reported among vanillas.     

EUGLOSSINE BEE POLLINATION OF THE ORCHID,COCHLEANTHES LIPSCOMBIAE: A FOOD SOURCE MIMIC

Cochleanthes lipscombiae is pollinated by large male and female euglossine bees. The flowers lack pollinator rewards, but attract bees searching for nectar. The euglossines extend their long tongues and crawl into the gullet-flower. The bees probe the back-swept lateral sepals for nectar. Pollination occurs as a pollinarium laden bee backs out, deposits pollinia on the stigma, and obtains a new pollinarium load by dislodging the anther. Some related orchid species have similar morphological characteristics as those essential to the pollination mechanism of C. lipscombiae. These features may have taxonomic significance at the generic level. Cochleanthes lipscombiae may be a floral mimic of a sympatric legume, but may also receive exploratory visits by bees searching for food resources. The latter may be young, recently emerged naive bees, or individuals seeking new nectar hosts during a period of rapid host species turnover.     

Severe outbreeding and inbreeding depression maintain mating system differentiation in Epipactis (Orchidaceae)

In hermaphroditic plants, theory for mating system evolution predicts that populations will evolve to either complete autonomous selfing (AS) or complete outcrossing, depending on the balance between automatic selection favouring self‐fertilization and costs resulting from inbreeding depression (ID). Theory also predicts that selection for selfing can occur rapidly and is driven by purging of genetic load and the loss of ID. Therefore, selfing species are predicted to have low levels of ID or even to suffer from outbreeding depression (OD), whereas predominantly outcrossing species are expected to have high levels of ID. To test these predictions, we related the capacity of AS to the magnitude of early‐acting inbreeding or OD in both allogamous and autogamous species of the orchid genus Epipactis. For each species, the level of AS was assessed under controlled greenhouse conditions, whereas hand‐pollinations were performed to quantify early costs of inbreeding or OD acting at the level of fruit and seed production. In the autogamous species, the capacity of AS was high (> 0.72), whereas in the allogamous species AS was virtually absent (< 0.10). Consistent with our hypothesis, allogamous Epipactis species had significantly higher total ID (average: 0.46) than autogamous species, which showed severe costs of OD (average: ?0.45). Overall, our findings indicate that strong early‐acting ID represents an important mechanism that contributes to allogamy in Epipactis, whereas OD may maintain selfing in species that have evolved to complete selfing.     

Exine micromorphology and ultrastructure in Neottieae (Epidendroideae,Orchidaceae)

The diverse epidendroid orchid tribe Neottieae is characterized by multiple transitions between autotrophy and mycoheterotrophy, allogamous and autogamous mating systems, pollen released as tetrads or monads, and pollen exine tectate or semitectate. We use transmission and scanning electron microscopy on pollen of ten species of Neottieae to investigate whether the differences in pollen aggregation and exine micromorphology and ultrastructure reflect phylogenetic relationships, or whether this variation is subject to ecological constraints. Our results showed that differences in exine micromorphology are mostly concordant with phylogenetic relationships in Neottieae, i.e. an ascending tendency of pollen ornamentation from tectate (Cephalanthera) to semitectate (e.g. Neottia). In contrast, pollen aggregation, when plotted on the most recent phylogeny, shows repeated transitions between monads and tetrads that could be related to ecological constraints. Tetrads are present in species that are nectar rewarding, whereas monads are common in deceptive species. Cephalanthera is characterized by recalcitrant pollen, including the frequent occurrence of collapsed pollen. In this genus, the observed shifts from allogamous to autogamous or cleistogamous mating systems could help to reduce pollen damage caused by exposure to dry habitats.     

RELATIVE POLLINATOR EFFECTIVENESS AND EVOLUTION OF FLORAL TRAITS IN SPATHIPHYLLUM FRIEDRICHSTHALII (ARACEAE)

We studied the relative effectiveness of different pollinators of Spathiphyllum friedrichsthalii Schott for 15 months on Barro Colorado Island, Panama. Pollen-foraging stingless bees (Apidae: Trigona) made 87% of floral visits. Experiments showed that these bees pollinate flowers, and correlations of fruit- and seed-set with visitation frequencies and floral contact times suggested that they were responsible for the majority of seeds produced. Fifteen species of fragrance-foraging, male euglossine bees (Apidae: Euglossini) collectively accounted for a small portion of seed-set in fewer than 27% of the inflorescences. Neocorynura (Halictidae) were pollen thieves and were unimportant as pollinators. We propose that euglossine and stingless bees differentially influence outcrossing rates and the evolution of floral traits of S. friedrichsthalii. Foraging behavior of male euglossines should allow for more long-distance pollen flow whereas stingless bees are likely to promote near-neighbor and geitonogamous pollinations. We discuss why the prolonged male phase of anthesis in this protogynous species may be maintained through pollination by stingless bees rather than male euglossines. Furthermore, although the floral fragrance is attractive to many species of male euglossines, it attracts few individuals. This condition may represent an intermediate step in the evolution of predominant pollination by male euglossines.     

POLLINATION ECOLOGY OF FOUR DALECHAMPIA SPECIES (EUPHORBIACEAE) IN NORTHERN NATAL,SOUTH AFRICA

The pollination ecology of four Dalechampia species was studied in three areas in northern Natal, South Africa. All species were pollinated by resin- and/or pollen-collecting megachilid bees (Hymenoptera: Megachilidae). The most common of these at all study sites was Heriades sp. (Megachilini), which collected both pollen and resin. This bee was the primary pollinator of D. galpinii and D. volubilis, and a secondary pollinator of D. aff. parvifolia and D. capensis. The primary pollinators of these latter two Dalechampia were Pachyanthidium near cucullatum and P. cordatum (Anthididiini), respectively. These are larger bees that collected mainly resin. Other visitors varied among Dalechampia species and among sites. Pairs of Dalechampia species were often found in sympatry (within 30 m of each other) and shared pollinators to varying extents. “Transfer experiments,” in which we placed inflorescences of two Dalechampia species together, reinforced observations of flower discrimination by bees foraging among naturally occurring sympatric pairs. Heriades sp. showed no obvious discrimination between Dalechampia species, but Pachyanthidium spp. “preferred” the Dalechampia species with the greater resin reward. Occasionally, however, Pachyanthidium would visit less rewarding species. Thus, although sympatric African Dalechampia species showed some pollinator partitioning, it was much weaker than found among New World species, and cannot alone explain the general absence of Dalechampia hybrids in northern Natal.     

Plant–pollinator interactions in the understory of a lowland mixed dipterocarp forest in Sarawak

Pollination biology of 41 plants species of 21 families blooming in the forest understory was investigated in a lowland mixed diplerocarp forest in Lambir Hills National Park, Sarawak. Among these species, 29 species (71%) were pollinated by bees, four (10%) by nectariniid birds, three by small dipterans, and others by moths, butterflies, syrphid flies, wasps, and beetles. The 29 bee-pollinated species consisted of five distinct pollination guilds: ten species pollinated by medium traplining bees (two Amegilla species), nine by small traplining bees (three halictid and a xylocopine species), two by stingless bees and beetles, seven by stingless bees, and one by megachilid bees. The bees constituting the first two guilds were shade-loving, swiftly flying, long-tongued trapliners. Proboscis lengths of these pollinators correlated with flower depth of the host plant. Pollination systems in the forest understory were distinguished from that in the canopy by the prevalence of specific interactions, the number of traplining solitary bees, and lack of pollination systems by mass-recruiting eusocial bees, large Xylocopa bees, thrips, bats, and wind. These characteristics are largely similar between the Palaeotropics and the Neotropics through convergence of nectarivorous birds (spiderhunters vs. hummingbirds) and traplining bees (Amegilla vs. euglossine bees).     

Notes on pollination ecology and floral scent chemistry of the rare neotropical orchid Catasetum galeritum Rchb.f.

The neotropical orchid genus Catasetum embraces about 180 species that produce perfume as reward for pollinators (i.e. male euglossine bees). Among the ca. 1000 perfume‐rewarding plants, Catasetum species are the best studied with respect to their natural history. Nevertheless, the pollination ecology of most species (> 80%) remains unknown. Here, we investigated the pollination ecology and floral scent chemistry of C. galeritum, a rare species endemic to the poorly investigated Brazilian Amazon. Flowers of C. galeritum were visited only by male bees of Eufriesea superba. Its perfume bouquet was composed of six volatiles, with 1,4‐dimethoxybenzene accounting for about 85% of the total scent discharge. Curiously, this compound is a potent attractant of more than 40 euglossine species. The absence of euglossine species other than Ef. superba on flowers of C. galeritum might be, therefore, be mediated by a modifier effect of another compound(s) in its floral scent bouquet.     

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.     

ENTOMOPHILOUS,INTRAFLORAL POLLINATION IN PHYLA INCISA

Experimental pollination studies indicate that probing into the corolla tube by insects is a requirement for autogamous reproduction in Phyla incisa. Insect-mediated self-fertilization combines the anthecology of allogamous reproduction with the genetic consequences of autogamy.     

Ancestral deceit and labile evolution of nectar production in the African orchid genus Disa

An outstanding feature of the orchid family is that approximately 30–40% of the species have non-rewarding flowers and deploy various modes of deception to attract pollinators, whereas the remaining species engage in pollination mutualisms based on provision of floral rewards. Here, we explore the direction, frequency and reversibility of transitions between deceptive and rewarding pollination systems in the radiation of the large African genus Disa, and test whether these transitions had consequences for diversification. By optimizing nectar production data for 111 species on a well-resolved phylogeny, we confirmed that floral deception was the ancestral condition and that nectar production evolved at least nine times and was lost at least once. Transitions to nectar production first occurred ca 17 million years ago but did not significantly affect either speciation or extinction rates. Nectar evolved independently of a spur, which was lost and gained multiple times. These results show that nectar production can be a highly labile trait and highlight the need for further studies of the genetic architecture of nectar production and the selective factors underlying transitions between deception and mutualism.     

Specialized pollination by carpenter bees in Calanthe striata (Orchidaceae), with a review of carpenter bee pollination in orchids

Calanthe striata has nectarless flowers that are self‐compatible, but pollinator dependent. Field observations showed that the flowers were pollinated exclusively by the carpenter bee Xylocopa appendiculata circumvolans, although the bees occasionally wasted pollen by delivering to the stigmatic surface pollinaria that retained their anther caps. Fruit set ratios at the population level varied spatiotemporally, but were generally low (8.3–17.3%). Calanthe striata blooms in spring when post‐overwintering carpenter bees have not yet started foraging for brood production. It can therefore exploit an abundance of opportunistic/naïve foragers. This timing may also increase the possibility of pollinator visits, because no rewarding co‐flowering plants are available in the orchid habitats. A literature review of Orchidaceae pollinated by carpenter bees revealed that at least 14 species of Orchidoideae and Epidendroideae have evolved flowers specialized for carpenter bee pollination. They typically have shallow pink/magenta flowers with a foothold for pollinators; pollinaria are attached to the head, ventral thorax or base of the middle legs of carpenter bees when they insert their heads and/or proboscises into flowers; pollination success is generally low, a probable consequence of the deceptive pollination systems. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013 , 171 , 730–743.     

Are pollination "syndromes" predictive? Asian dalechampia fit neotropical models

Using pollination syndrome parameters and pollinator correlations with floral phenotype from the Neotropics, we predicted that Dalechampia bidentata Blume (Euphorbiaceae) in southern China would be pollinated by female resin-collecting bees between 12 and 20 mm in length. Observations in southwestern Yunnan Province, China, revealed pollination primarily by resin-collecting female Megachile (Callomegachile) faceta Bingham (Hymenoptera: Megachilidae). These bees, at 14 mm in length, were in the predicted size range, confirming the utility of syndromes and models developed in distant regions. Phenotypic selection analyses and estimation of adaptive surfaces and adaptive accuracies together suggest that the blossoms of D. bidentata are well adapted to pollination by their most common floral visitors.     

Pollination ecology of the Neotropical gesneriad Gloxinia perennis: chemical composition and temporal fluctuation of floral perfume

• Although common among orchids, pollination by perfume‐gathering male euglossine bees is quite rare in other Neotropical families. In Gesneriaceae, for example, it is reported in two genera only, Drymonia and Gloxinia. Flowers of G. perennis are known to emit perfume, thereby attracting male euglossine bees as pollinators. However, detailed reports on the pollination ecology, as well as on chemistry of floral perfume of individuals in natural populations, are still missing. In this study, we report on the pollination ecology of G. perennis, focusing on the ecological significance of its floral perfume.
• In natural populations in Peru, we documented the floral biology and breeding system of G. perennis, as well as its interaction with flower visitors. We also characterised the chemical composition of floral perfume, as well as its timing of emission.
• Gloxinia perennis is self‐compatible and natural pollination success is high. Spontaneous self‐pollination occurs as a ‘just in case strategy’ when pollinators are scarce. Perfume‐collecting males of Eulaema cingulata and El. meriana were identified as pollinators. The perfume bouquet of G. perennis consists of 16 compounds. (E)‐Carvone epoxide (41%) and limonene (23%) are the major constituents. Perfume emission is higher at 09:00 h, matching the activity peak of Eulaema pollinators.
• Flowers of G. perennis have evolved a mixed strategy to ensure pollination (i.e. self‐ and cross‐pollination), but cross‐pollination is favoured. The size and behaviour of Eulaema males enables only these bees to successfully cross‐pollinate G. perennis. Furthermore, G. perennis floral perfume traits (i.e. chemistry and timing of emission) have evolved to optimise the attraction of these bees.

     

Long Tongues and Loose Niches: Evolution of Euglossine Bees and Their Nectar Flowers1

I examined relationships between tongue length of orchid bees (Apidae: Euglossini) and nectar spur length of their flowers in the genera Calathea, Costus, and Dimerocostus using phylogenetically independent contrasts. Long‐tubed flowers have specialized on one or several species of long‐tongued euglossine bees, but long‐tongued bees have not specialized on long‐tubed flowers. Whereas long tongues may have evolved to provide access to a wider variety of nectar resources, long nectar spurs may be a mechanism for flowers to conserve nectar resources while remaining attractive to traplining bee visitors.     

Abundance and Diversity of Euglossine Bees in the Fragmented Landscape of the Brazilian Atlantic Forest1

Male euglossine bees were sampled with chemical baits every two months from September 1997 to July 1999 at nine sites in the Desengano mountain range, Rio de Janeiro State, Brazil. Four sites were located in Atlantic Forest mature second growth, two sites in disturbed forest, and three sites in forest fragments of 200, 156, and 14 ha, respectively. We collected 3653 male euglossine bees from at least 21 species. Analyses of variance indicated no differences among the three habitat types for total number of bees, and 5 of the 6 dominant species. Bootstrapping indicated significant variation in species richness and diversity for some sites, but there was no clear indication of differences among habitats. Similarity as measured with the Morisita–Horn index was inversely related to distance between sites, but relatively high for most site combinations. These results suggest that the euglossine bee community in the three habitats was essentially the same. Although some species were associated with each habitat type, most appeared to respond to temporal local conditions. Our results do not support the hypothesis that forest fragmentation or habitat alteration reduces abundance and diversity of euglossine bees.     

Pollination Biology of Hosta sieboldiana (Lodd.) Engler and H. sieboldii (Paxton) J. Ingram (Liliaceae)

Abstract The pollination biology of Hosta sieboldiana and H. sieboldii is investigated comparatively in Central Japan. Both species have homogamous, one-day flowers pollinated by bumblebees. The abdomens of the bees touch the stigma on the extended style when they land on the anthers inside the herkogamous flower, and autogamy is effectively prevented. However, the flowers are fairly self-compatible, and geitonogamy may occur rather frequently because two or more flowers on a scape very often bloom at the same time and many ramets are contiguous. The pollen/ovule ratios suggest that these species are facultative outbreeders. The flower of H. sieboldii seems completely suited to bumblebee pollination. In H. sieboldiana the stigma of the flower, whose style strongly protrudes, is not always touched by bumblebees, but frequent visitation of bumblebees results in pollination of almost all the flowers. Both species have similar pollination systems but seem reproductively isolated by blooming times and habitats. Their common pollinators, however, may sometimes cause introgressive hybridization in contiguous populations.     

Generalized food deception: colour signals and efficient pollen transfer in bee‐pollinated species of Eulophia (Orchidaceae)

Non‐rewarding plants use a variety of ruses to attract their pollinators. One of the least understood of these is generalized food deception, in which flowers exploit non‐specific food‐seeking responses in their pollinators. Available evidence suggests that colour signals, scent and phenology may all play key roles in this form of deception. Here we investigate the pollination systems of five Eulophia spp. (Orchidaceae) lacking floral rewards. These species are pollinated by bees, notably Xylocopa (Anthophorinae, Apidae) or Megachile (Megachilidae) for the large‐flowered species and anthophorid (Anthophorinae, Apidae) or halictid (Halictidae) bees for the small‐flowered species. Spectra of the lateral petals and ultraviolet‐absorbing patches on the labella are strongly contrasting in a bee visual system, which may falsely signal the presence of pollen to bees. All five species possess pollinarium‐bending mechanisms that are likely to limit pollinator‐mediated self‐pollination. Flowering times extend over 3–4 months and the onset of flowering was not associated with the emergence of pollinators, some of which fly year round. Despite sharing pollinators with other plants and lacking rewards that would encourage fidelity, the Eulophia spp. exhibited relatively high levels of pollen transfer efficiency compared with other rewarding and deceptive orchids. We conclude that the study species employ generalized food deception and exploit food‐seeking bees. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013 , 171 , 713–729.