Neither insects nor wind: ambophily in dioecious Chamaedorea palms (Arecaceae)

Pollination of Neotropical dioecious trees is commonly related to generalist insects. Similar data for non‐tree species with separated genders are inconclusive. Recent studies on pollination of dioecious Chamaedorea palms (Arecaceae) suggest that species are either insect‐ or wind‐pollinated. However, the wide variety of inflorescence and floral attributes within the genus suggests mixed pollination mode involving entomophily and anemophily. To evaluate this hypothesis, we studied the pollination of Chamaedorea costaricana, C. macrospadix, C. pinnatifrons and C. tepejilote in two montane forests in Costa Rica. A complementary morphological analysis of floral traits was carried out to distinguish species groups within the genus according to their most probable pollination mechanism. We conducted pollinator exclusion experiments, field observations on visitors to pistillate and staminate inflorescences, and trapped airborne pollen. A cluster analysis using 18 floral traits selected for their association with wind and insect pollination syndromes was carried out using 52 Chamaedorea species. Exclusion experiments showed that both wind and insects, mostly thrips (Thysanoptera), pollinated the studied species. Thrips used staminate inflorescences as brood sites and pollinated pistillate flowers by deception. Insects caught on pistillate inflorescences transported pollen, while traps proved that pollen is wind‐borne. Our empirical findings clearly suggest that pollination of dioecious Chamaedorea palms is likely to involve both insects and wind. A cluster analysis showed that the majority of studied species have a combination of floral traits that allow for both pollination modes. Our pollination experiments and morphological analysis both suggest that while some species may be completely entomophilous or anemophilous, ambophily might be a common condition within Chamaedorea. Our results propose a higher diversity of pollination mechanisms of Neotropical dioecious species than previously suggested.     

Honeyeater (Meliphagidae) pollination and the floral biology of PolynesianHeliconia (Heliconiaceae)

The primary pollinator of Polynesian heliconias,Heliconia laufao andH. paka, is the Wattled Honeyeater,Foulehaio carunculata. This report is the first documentation of pollination by honeyeaters in the genusHeliconia and the first record ofF. carunculata as a pollinator of a plant species. The Polynesian heliconias bear inflorescences that produce 2–4 hermaphroditic flowers per day for a period of 2–3 months. Each flower secretes abundant nectar (125–184 l) with low sugar concentration (15–18% sucrose-equivalents, weight per weight basis) which is available at anthesis just before dawn. Ninety percent of flower visits occur between anthesis and mid-morning. The honeyeaters perch on inflorescence bracts, and probing of the flower results in pollen deposition on the head and bill from where pollen is transferred between flowers. No statements on compatibility can be made forHeliconia paka; however,Heliconia laufao appears to be self-compatible. Calculations of energetic values of nectar of the Polynesian heliconias and Daily Energy Expenditures ofF. carunculata suggest that populations ofH. laufao andH. paka serve as rich energy resources for their pollinators.     

Reproductive biology and pollination ecology of Triplaris gardneriana (Polygonaceae): a case of ambophily in the Brazilian Chaco

• Triplaris gardneriana (Polygonaceae) is a dioecious pioneer tree reported as insect‐pollinated, despite possessing traits related to anemophily. Here, we analyse the possible roles of insects and wind on the pollination of this species to establish whether the species is ambophilous.
• We carried out observations of floral biology, as well as on the frequency and behaviour of pollinators visiting flowers in a population of T. gardneriana in the Chaco vegetation of Brazil. We conducted experimental pollinations to determine the maternal fertility of female plants and whether they were pollen‐limited, and we also conducted aerobiological experiments to provide evidence of how environmental factors influence atmospheric pollen dispersal.
• The population comprised an area of approximately 152.000 m² and was composed of 603 female and 426 male plants (sex ratio = 0.59:0.41). We observed 48 species of insects visiting flowers of T. gardneriana, of which the bees Scaptotrigona depilis and Apis mellifera scutellata were the most effective pollinators. We recorded pollen grains dispersed by wind on 74% of the glass slides placed on females, located at different distances (1–10 m) from male plants.
• Airborne pollen concentration was negatively correlated with relative humidity and positively correlated with temperature. Our observations and experimental results provide the first evidence that T. gardneriana is an ambophilous species, with pollen dispersal resulting from both animal and wind pollination. This mixed pollination strategy may be adaptive in T. gardneriana providing reproductive assurance during colonisation of sites with different biotic and abiotic conditions.

     

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.     

Attalea phalerata and Bactris glaucescens (Arecaceae, Arecoideae): Phenology and pollination ecology in the Pantanal, Brazil

We compared the reproductive and vegetative phenology and pollination ecology of sympatric Attalea phalerata and Bactris glaucescens palms (Arecaceae) in the Pantanal, Brazil, in a riparian forest area subject to periodic flooding. Attalea phalerata has a solitary stem and produces staminate, pistillate and rarely bisexuals inflorescences that open during the day. Bactris glaucescens has multiple stems and has bisexual flowers with crepuscular/nocturnal anthesis. Both species present bud break and leaf-budding during the year. Attalea phalerata shows continual annual flowering with ripening of fruits during the dry season. For B. glaucescens flowering occurs simultaneously with fruiting for about seven months, and fruit production can be influenced by temperature and level of flooding. The difference in the timing of anthesis of the flowers ensures production of floral resources during both day and night when both species of palms are flowering. The floral structures of both species have morphological characteristics associated with pollination by insects (mainly beetles), such as the presence of odor, stigmatic secretion, heat production, and adhesive substances (“pollenkitt”) in the pollen. In A. phalerata, the main pollinators were Mystrops sp. (Nitidulidae) and Madarini (Curculionidae). Derelomus sp. (Curculionidae) and Paratenetus sp. (Tenebrionidae) beetles visited B. glaucescens during the day and could have pollinated the flowers at these occasions.     

Diurnal palm pollination by mystropine beetles: is it weather-related?

We studied pollination ecology of the sympatric palms Attalea allenii and Wettinia quinaria in a tropical rain forest in Colombia. Attalea has a subterranean stem and Wettinia is tall and arboreal. Both species have thermogenesis and short anthesis, and their floral scents differ in chemical composition. Inflorescences of both palms are visited by beetles, bees and flies. Pollination is diurnal, and is effected mostly by two species of Mystrops (Nitidulidae: Nitidulinae: Mystropini) each of them specific to one palm species. Both palms share few visitors and no pollinators. Differences in scent composition probably cause this isolation. We contrast their diurnal pollination with nocturnal pollination of other palms by mystropines in Amazonia and elsewhere, and relate it to precipitation regimes. The diurnal anthesis of A. allenii and W. quinaria and the diurnal activity of their specific mystropines probably coevolved as a response to the high, predominantly nocturnal rainfall in the Chocó.     

Effect of pollination intensity on fruit and seed set in cacao (Theobroma cacao L.)

We studied the functional relationship between pollination intensity and fruit survival as well as the number of seeds per pod in the tropical tree Theobroma cacao L. on a Forastero Upper-Amazon clone (UPA 409) in Ivory Coast. Cutting the style 24 h after pollination allowed for counting the number of pollen grains deposited on a stigma without affecting fruit set and seed development. Forty-three pollen grains were necessary to reach 50% of maximum fruit set 28 days after pollination. Above 115 pollen grains, the proportion of developing ovaries reached a maximum of 88% 28 days after pollination and 75% at maturity. With fewer than 238 pollen grains per stigma, there was a close relationship between pollination intensity and number of seeds per pod; the pollenseed ratio increased from 1.61 to 3.81 for PI increasing from 30 to 238 pollen grains. For higher pollination intensities, the average number of seeds per pod reached a maximum of 58. The relationship between pollination intensity and seed content was modelled. Results are consistent with the hypothesis that ovules attracted pollen tubes in a similar way regardless of whether or not they had already been reached by another pollen tube.     

Transfer of pollinaria on birds’ feet: a new pollination system in orchids

We report the discovery of a new mechanism of pollination in orchids: transfer of pollinaria on the feet of birds. Observations carried out in South Africa and Malawi showed that the orchids Disa chrysostachya Sw. and Disa satyriopsis Kraenzl. are pollinated by sunbirds. Pollinaria of these orchids become attached firmly to the birds toes when they perch on the tall narrow inflorescences which are packed tightly with numerous small orange flowers. Birds typically perch on the lower part of an inflorescence while reaching up to feed on nectar in flowers on the upper part, but occasionally reverse this position to probe the lower flowers. The nectar is contained within a short bulbous spur with a narrow entrance that permits entrance of a sunbirds slender tongue. Contrary to expectation, the pollination mechanism in D. chrysostachya is remarkably efficient with about 6.1% of pollen reaching stigmas on other plants and fruit set occurring in 95% of flowers at one site. Birds seldom move their feet once perched, thus minimizing the incidence of self-pollination, either within or between flowers on an inflorescence.     

Insect and wind pollination inUrginea maritima (Liliaceae)

Three co-existing pollination mechanisms are found inUrginea maritima: insect-, wind-, and self-pollination. The flowers exhibit a typical insect-pollination syndrome; they offer abundant exposed nectar as well as pollen. Out of the many different visitors only a few could be regarded as pollinators:Apis mellifera, Polistes gallicus, andVespa orientalis. Wind pollination also occurs and generally is responsible for self-pollination.It is argued that the development of extra wind-pollination accompanied by partial self-incompatibility is an adaptation to increase pollination in an unfavourable season (August–September), when insects are scarce.     

Effectiveness of buzz pollination in Pedicularis chamissonis: significance of multiple visits by bumblebees

Pollination success of plants is highly susceptible to the frequency of visits and foraging behavior of pollinators. Pollination of the nectarless flowers of Pedicularis species depends on bumblebee workers collecting pollen by vibrating the anthers (buzz pollination). However, little is known about the efficiency of the pollination system. Foraging behavior, pollen removal from anthers and pollen deposition on stigmas of P. chamissonis were studied to assess the effectiveness of buzz pollination in an alpine snowbed population of northern Japan. Although bumblebees tended to visit most of the flowers open at a given time within inflorescences during a single visit, pollen removal rate at the first visit was about 20%, and buzzing period decreased with increasing number of previous visits, resulting in a decreasing proportion of pollen removed per visit as the number of visits increased. These trends enable plants to provide pollen for more pollinators. The number of pollen grains deposited on stigmas was not saturated during the first visit and increased with additional visits. Irrespective of weak self-compatibility, evidence of interference between self and outcross pollen was lacking for seed production. Therefore, buzz pollination in P. chamissonis acts as a mechanism that improves the chance of cross-pollination upon multiple visits if pollinator visitation is frequent.     

“Ixoroid” secondary pollen presentation and pollination by small moths in the Malagasy treeletIxora platythyrsa (Rubiaceae)

The pollination biology ofIxora platythyrsa (Rubiaceae) was studied in NW. Madagascar. The plant displayed cream-yellow, nocturnally fragrant, nectariferous, tubular and strongly protandrous flowers. These had an ixoroid secondary pollen presentation mechanism: prior to anthesis, anthers exhausted their pollen onto unripe stylar heads. From this position pollen of male-stage flowers later adhered to primarily the probosces of small visiting nocturnal noctuid and geometrid moths. — Pollen was subsequently raked off moths' probosces by receptive, copiously papillose stigmas of female-stage flowers. Principal pollination adaptation was probably to the noctuid moth subfam.Sarrothripinae.     

Breeding system and spatial variation in the pollination biology of the heterocarpic Thymelaea velutina (Thymelaeaceae)

Thymelaea velutina (Thymelaeaceae) is a unique dioecious and heterocarpic shrub, each female producing both dry and fleshy fruits. It is endemic to the Balearic Islands (western Mediterranean) and has suffered an important regression in recent decades, especially due to habitat loss. It lives in coastal areas, mainly in dunes, but a few populations occur up to 1300 m in the mountains of Mallorca. In the present study, we examined its breeding system and pollen vectors, determined whether seed production is pollen-limited, and quantified the relative importance of different insect visitors at coastal and mountain sites. Selective exclusions showed no differences between populations in the relative importance of insects and wind as pollen vectors. Pollen was limiting at both populations, though not consistently in time. Flowers of T. velutina were visited mostly by generalist insects, and species composition and abundance of flower visitors varied both in space and time. The flowering period is about a month later in the mountain than in the dune, and this results in a higher frequency of insect visits to plants in the mountain due to the higher insect abundance; insects were also more diverse in the mountain, although they visited a proportionally lower number of flowers than in the dune. Despite this spatio-temporal variation in the frequency of insect visits and in the importance of a particular insect group, the ambophilous system in this species (previously described as anemophilous) ensures a relatively high fruit set at the two different sites.     

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.     

Pollen precedence and stigma closure: a mechanism of competition for pollination between Delphinium nelsonii and Ipomopsis aggregata

Summary Previous experiments showed that the sympatric herbs Delphinium nelsonii and Ipomopsis aggregata compete for hummingbird pollination and that deleterious effects of the former species on seed set of the latter involve interspecific pollen transfer. However, seed set was not reduced when pollen of both species was applied simultaneously to I. aggregata stigmas. Hence a competitive effect may require arrival of foreign pollen before conspecific pollen. To explore this possibility we subjected I. aggregata flowers to a competition treatment in which they received D. nelsonii pollen 6 h before I. aggregata pollen, or to a control in which they received only the conspecific pollen. Foreign pollen precedence decreased mean seed set by almost 50%, which is consistent with effects observed in previous experiments. Reduced seed set can be explained by the fact that foreign pollen often caused stigma lobes to close together within 1.5–6 h, reducing subsequent receptivity. Stigma closure was also elicited by conspecific pollen, but not by mechanical stimulation, and was influenced by size of the pollen load and identity of the plant being pollinated.     

The effectiveness of heterostyly in preventing illegitimate pollination in dish-shaped flowers

Heterostyly is thought to have evolved because it confers efficiency of cross-pollination. While it can be an alternative to an incompatibility mechanism in tube-shaped flowers, its effectiveness in dish-shaped flowers, such as those of Fagopyrum esculentum, has not been demonstrated. Stigmatic pollen loads were examined over the daily course of pollination in a planted field of this crop species. Natural pollination by bees resulted in 23% of the pollen on pin flowers and 69% on thrum flowers being legitimate. Both flower morphs therefore received the two pollen types in about the same proportions. Pin pollen constituted 74% of the pollen delivered to stigmata, even though the two morphs are present in equal numbers. Pin flowers collected about 75 pollen, and thrum flowers about 25 pollen by the end of the day of anthesis. The net result was about 15 compatible pollen per flower on both floral morphs. These results indicate that heterostyly is associated with excess pin-pollen delivery rather than excess legitimate-pollen delivery in F. esculentum.     

TheMoegistorhynchus longirostris (Diptera: Nemestrinidae) pollination guild: long-tubed flowers and a specialized long-proboscid fly pollination system in southern Africa

A guild of 20 late spring- and early summer-flowering species ofIridaceae, Geraniaceae andOrchidaceae is pollinated partly or exclusively by the long-proboscid flyMoegistorhynchus longirostris (Nemestrinidae). This large-bodied fly, active in late spring and early summer, has mouthparts 40–70 (90) mm long and forages for nectar from a variety of species. These plants share a suite of convergent floral features including a straight or weakly curved floral tube usually 50–70 mm long but sometimes to 90 mm, relatively short petals or tepal lobes coloured white, cream or salmon with reddish nectar guides, and often violet or red anthers and pollen. Flowers of most species with these characteristics are zygomorphic with the stamens either arcuate (mostIridaceae) or declinate (Geraniaceae and someIridaceae). The flowers are odourless and typically secrete large amounts of nectar of relatively constant sugar concentration, mostly 24–29%, with a high sucrose:hexose ratio. Guild members utilize five separate sites of pollen deposition on the body of the fly, typically utilizing different deposition sites when two or more co-occur, indicating strong selection to aviod pollen contamination.M. longirostris is restricted to the west coast of southern Africa and at least 8 species appear to depend exclusively on the insect for pollination. The remaining species in the guild are pollinated by one or both of the long-proboscid fliesPhiloliche gulosa andP. rostrata (Tabanidae) over other parts of their range. Species and races pollinated entirely byM. longirostris have longer floral tubes which makes nectar unavailable to other insects, including other species of long-proboscid fly. The only insect with mouthparts long enough to forage effectively on these long-tubed flowers isM. longirostris and this fly must be considered a keystone species in the ecosystems in which it occurs.Dedicated to emer. Univ.-Prof. DrFriedrich Ehrendorfer on the occasion of his 70th birthday     

A supplementary contribution of ants in the pollination of an orchid, Epipactis thunbergii, usually pollinated by hover flies

It has been controversial how extensively ants contribute to pollination, and we evaluated the contribution of the Japanese carpenter ant, Camponotus japonicus, to the pollination of an orchid, Epipactis thunbergii. Two-year field studies revealed that (1) the ant workers foraged even in cool/cloudy conditions and accordingly visited orchid flowers more frequently (about 40% of all the visitors) than hover flies, the principle pollinators (10–20%), and that (2) the flower-visiting ants occasionally removed pollinia from the anther and then delivered pollen onto the stigmatic surface of other flowers, although self-pollination might frequently occur in the consecutive visits of flowers within an inflorescence. An artificial pollination experiment with pollinia which had been transferred to the ant integument showed that (3) the treated flowers produced as many fruits and seeds as control flowers. We concluded that C. japonicus workers could actually pollinate E. thunbergii flowers and their relative importance as pollinators appeared to be largely dependent on the abundance of flower-visiting workers or weather conditions during the flowering period, which mainly determined the availability of hover flies.     

Reproductive biology of Alpinia blepharocalyx (Zingiberaceae): another example of flexistyly

The floral biology and breeding system of Alpinia blepharocalyx were studied in Yunnan province, southwest China. Our results indicate that populations of A. blepharocalyx have two floral morphs, which differ in flowering behaviour: the cataflexistylous morph in which the stigma is held erect above the dehiscent anther when anthesis begins in the morning and becomes curved under the anther at afternoon, and the anaflexistylous morph in which the receptive stigma is curved under the indehiscent anther first and moves into a reflexed superior position above the anther as it begins to shed pollen in the afternoon; the flowering period of both floral morphs is 12 hours; the stylar movements in the two floral morphs are synchronous, and they have similar traits to those found in other Alpinia species previously reported. Also, on average, cataflexistylous flowers are larger than anaflexistylous flowers, especially the labellum and corolla tube length; moreover, the P/O ratio of the two floral morphs is significantly different: the cataflexistylous morph has more pollen grains and fewer ovules than the anaflexistylous morph; the evolutionary significance of this comparison is discussed. Cataflexistylous flowers were observed to produce a lower concentration of nectar than that of anaflexistylous flowers before 11:00 a.m., but they then have higher nectar concentration; cataflexistylous flowers always have more nectar than anaflexistylous flowers. Flowers of A. blepharocalyx were visited by fewer insects at a lower frequency, including honey bees (Apis cerana cerana) and two species of carpenter bees (Xylocopa spp.). No significant differences were found in the fruit set among the hand-pollination treatments regardless of selfing (geitonogamy and autogamy) or crossing (intermorph and intramorph); but all hand-pollination treatments exhibited much higher fruit set than the controls; meanwhile, no fruit set occurred in the unpollinated bagged plants. Pollen tube growth was examined using fluorescence microscopy following self, intramorph, and intermorph hand pollinations at different times of the day; the pollen tubes of both floral morphs have the same growth rate and the capability to reach the ovary. Both the results of pollen tube growth and fruit sets under different pollination conditions show that A. blepharocalyx is self-compatible and dependent upon insects for pollination. The distinctive flexistyly mechanism of A. blepharocalyx is likely a floral mechanism that promotes effective intermorph pollen transfer.     

Floral sexual dimorphism and flower choice by pollinators in a nectarless monoecious vine Akebia quinata (Lardizabalaceae)

We investigated the pollination system and movement patterns of pollinators among flowers of the nectarless, monoecious vine Akebia quinata in natural populations and experimental floral arrays. Female flowers did not offer any rewards for pollinators and were larger than male flowers. Pollinators of A.quinata , such as small solitary bees and hoverflies, clearly discriminated between male and female flowers. Hoverflies always visited male flowers and rarely visited female flowers. In contrast, solitary bees tended to visit female flowers first when entering the array, but then switched to male flowers within the same foraging bout. This tendency disappeared when the sepal size of female flowers was experimentally reduced to the size of male flowers. Thus, observed non-randomness in flower choice by solitary bees may be caused by female>male sexual dimorphism and may increase the chance of cross-pollination and lower the probability of geitonogamous pollination in a single visit to a plant. Therefore, floral sexual dimorphism in A.quinata is considered to be an adaptation for deceptive pollination associated with discriminating pollinators.     

Notes on the floral morphology in Vivianiaceae (Geraniales)

The functional floral morphology of the three genera of Vivianiaceae (= Ledocarpaceae, Geraniales), Rhynchotheca, Viviania and Balbisia, is compared. Likely pollination mechanisms are inferred from morphology and field observations. The flowers of Viviania are nectariferous and apparently zoophilous with nectar as the (primary) pollinator reward. Balbisia has pollen flowers without nectaries, its showy corolla indicates that it is also zoophilous with pollen as sole pollinator reward; bees were observed as flower visitors. One taxon (B. gracilis) may be anemophilous. Rhynchotheca has flowers without petals, with large, pendulous anthers and lacks nectaries. It shows synchronous mass flowering in its natural populations and is evidently anemophilous. A comparison with other Geraniales shows that nectar flowers with small anthers are likely the ancestral condition in Vivianiaceae. This suggests that the pollen flowers with larger anthers of Balbisia and Rhynchotheca may represent an apomorphic condition. The documentation of pollen flowers and anemophily in Vivianiaceae expands the range of known floral and pollination syndromes in Geraniales.