Diverse pollination systems of the twin-spurred orchid genus Satyrium in African grasslands

The large terrestrial orchid genus Satyrium underwent evolutionary radiations in the Cape floral region and the grasslands of southern and eastern Africa. These radiations were accompanied by tremendous diversification of the unusual twin-spurred flowers that characterize the genus, but pollination data required to interpret these patterns of floral evolution have been lacking for grassland species in the genus. Here we document pollinators, nectar properties, and levels of pollination success for 11 grassland Satyrium species in southern and south-central Africa. Pollinators of these species include bees, beetles, butterflies, hawkmoths, noctuid moths, long-proboscid flies, and sunbirds. Most species appear to be specialized for pollination by one functional pollinator group. Long-proboscid fly pollination systems are reported for the first time in Satyrium (in S. macrophyllum and a high-altitude form of S. neglectum). Floral morphology, especially spur length and rostellum structure, differs markedly among plants with different pollinators, while nectar volume, concentration, and sugar composition are fairly uniform across species. Most taxa exhibited high levels of pollination success (>50% of flowers pollinated), a trend that can be attributed to the presence of nectar in the twin spurs.     

Bird pollination in South African species ofSatyrium (Orchidaceae)

Field observations showed that three South African orchid species,Satyrium carneum, S. coriifolium andS. princeps, are pollinated by sunbirds. Foraging sunbirds insert their bills into the labellum chamber of the flowers and suck nectar from the labellum spurs with their tongues. The column overarches the entrance to the labellum and pollinaria become affixed to the upper mandible of the bill. Birds often attempt to remove pollinaria by rubbing their bills against a branch, but are mostly unsuccessful due to the large plate-like viscidia which attach the pollinaria very firmly to the bill. Other modifications for bird pollination in theseSatyrium species may include the red, carmine or orange colour of the flowers, sturdy inflorescence stems used for perching and large amounts of dilute nectar in the spurs. EachSatyrium species was pollinated by several species of sunbird, and despite some differences in flowering time, occasional hybrids occur at a site whereS. carneum andS. coriifolium share the same sunbird pollinators.     

Nectar flow and pollinators' efficiency in two co-occurring species ofCapparis (Capparaceae) in Israel

Two closely related species ofCapparis, C. ovata andC. spinosa, which are exposed to the same pollination environment were studied. The nectar volume and concentration ofC. ovata are higher than inC. spinosa. Both species have similar pollination efficiency, but the relative contribution of each pollinator is different.C. ovata is pollinated mainly hy hawkmoths while the principal pollinators inC. spinosa are bees.     

Contrasting breeding systems in twoEriotheca (Bombacaceae) species of the Brazilian cerrados

The pollination biology and breeding systems ofEriotheca pubescens andE. gracilipes have been studied. These two species occur as trees in cerrado vegetation, the neotropical savannas of Central Brazil, with partially sympatric distributions. They have similar phenology and floral structure, although the flowers ofE. pubescens are larger. Both species have nectar flowers pollinated by largeAnthophoridae bees but the main pollinators of each species differ in size. The species have markedly different breeding systems: late-acting self-incompatibility inE. gracilipes and apomixis stimulated by pollination inE. pubescens.     

Pollination ofNuphar (Nymphaeaceae) in Europe: Flies and bees rather thanDonacia beetles

Nuphar (Nymphaeaceae) comprises a small holarctic group of aquatic perennials whose flowers are pollinated by flies, bees, and beetles. We studied pollination in different populations of the two European speciesN. lutea andN. pumila in Norway and in Germany. Flowers are self-compatible and protogynous, preventing automatic selfing, and insect pollination is required for seed production. Sympatric populations were studied in Vest-Agder county in Norway to determine whetherN. lutea andN. pumila have the same or different pollinators. Allopatric populations ofN. lutea in Germany and Norway were then compared to determine whether their pollinator spectra differ as would be expected in an open flower with seemingly easily accessible pollen and nectar. Results of the present as well as previous studies of the pollination ofN. lutea andN. pumila show that both species are mainly pollinated by flies, including apparentNuphar specialists, such as the scatophagidHydromyza livens and the ephydridsHydrellia andNotiphila, the last also a long-known pollinator ofN. advena in Florida. Pollinator overlap between sympatric heterospecific populations was small, while allopatric conspecific populations had similar visitor and pollinator spectra. We found no evidence of pollination byDonacia beetles as reported from some North American populations ofNuphar. Dedicated to Univ.-Prof. DrF. Ehrendorfer on the occasion of his 70th birthday     

Floral specialization for different pollinators and divergent use of the same pollinator among co‐occurring Impatiens species (Balsaminaceae) from Southeast Asia

Floral variation among closely related species is thought to often reflect differences in pollination systems. Flowers of the large genus Impatiens are characterized by extensive variation in colour, shape and size and in anther and stigma positioning, but studies of their pollination ecology are scarce and most lack a comparative context. Consequently, the function of floral diversity in Impatiens remains enigmatic. This study documents floral variation and pollination of seven co‐occurring Impatiens spp. in the Southeast Asian diversity hotspot. To assess whether floral trait variation reflects specialization for different pollination systems, we tested whether species depend on pollinators for reproduction, identified animals that visit flowers, determined whether these visitors play a role in pollination and quantified and compared key floral traits, including floral dimensions and nectar characteristics. Experimental exclusion of insects decreased fruit and seed set significantly for all species except I. muscicola, which also received almost no visits from animals. Most species received visits from several animals, including bees, birds, butterflies and hawkmoths, only a subset of which were effective pollinators. Impatiens psittacina, I. kerriae, I. racemosa and I. daraneenae were pollinated by bees, primarily Bombus haemorrhoidalis. Impatiens chiangdaoensis and I. santisukii had bimodal pollination systems which combined bee and lepidopteran pollination. Floral traits differed significantly among species with different pollination systems. Autogamous flowers were small and spurless, and did not produce nectar; bee‐pollinated flowers had short spurs and large floral chambers with a wide entrance; and bimodally bee‐ and lepidopteran‐pollinated species had long spurs and a small floral chamber with a narrow entrance. Nectar‐producing species with different pollination systems did not differ in nectar volume and sugar concentration. Despite the high frequency of bee pollination in co‐occurring species, individuals with a morphology suggestive of hybrid origin were rare. Variation in floral architecture, including various forms of corolla asymmetry, facilitates distinct, species‐specific pollen‐placement on visiting bees. Our results show that floral morphological diversity among Impatiens spp. is associated with both differences in functional pollinator groups and divergent use of the same pollinator. Non‐homologous mechanisms of floral asymmetry are consistent with repeated independent evolution, suggesting that competitive interactions among species with the same pollination system have been an important driver of floral variation among Impatiens spp.     

Pollination biology ofSymphonia globulifera (Clusiaceae)

The pollination biology ofSymphonia globulifera was studied in Central Amazonia, Brazil. As suggested by the bird syndrome of the flowers, these are mainly pollinated by hummingbirds. Occasional visits by other birds, butterflies and more rarely bees, as well as tamarin monkeys were also observed.Trigona bees partly destroy the flower tube to rob nectar. The possibility thatS. globulifera may not be primarily adapted to hummingbird pollination is discussed. The pollen is intermixed in an oily fluid secreted by the anthers (antheroil). Each of the five stigmas consists of a pore-like opening at the apex and a small chamber behind it. The antheroil mixed with pollen is absorbed by capillarity into the chamber when deposited on the pore. the pollen germinates inside the stigma. The presence of antheroil and pore-like stigmas in the flowers of the closely relatedPlatonia insignis indicate a similar mode of pollination. The results of this study are compared with observations in some otherClusiaceae (Caraipa, Clusia, Garcinia, Mahurea), where floral oils or floral resin occur. The role of these substances in the pollination process and their relation to the evolution of flower biology inClusiaceae are briefly discussed.     

Pollination by hummingbirds and bees in eight syntopic species and a putative hybrid of Ericaceae in Southeastern Brazil

We report on flowering phenology, floral morphology, pollinators, and nectar for eight species and a putative natural hybrid belonging to Agarista, Gaultheria and Gaylussacia that occur syntopically in a montane area. The campanulate to tubular flowers of eight out of nine Ericaceae taxa are primarily pollinated by either hummingbirds or bees. Flowering overlaps in all species but slight differences of floral shape, colour, and nectar characterize pollination by each pollinator group. Differences in floral traits are not large enough to exclude secondary pollinators. Thus, either the main pollinators of a species belonging to its syndrome, or secondary pollinators of a species belonging to different syndromes, may allow for inter-specific crosses.     

Is the timing of scent emission correlated with insect visitor activity and pollination in long‐spurred Satyrium species?

Plants are expected to emit floral scent when their pollinators are most active. In the case of long‐tubed flowers specialised for pollination by crepuscular or nocturnal moths, scent emissions would be expected to peak during dawn. Although this classic idea has existed for decades, it has rarely been tested quantitatively. We investigated the timing of flower visitation, pollination and floral scent emissions in six long‐spurred Satyrium species (Orchidaceae). We observed multiple evening visits by pollinaria‐bearing moths on flowers of all study species, but rarely any diurnal visits. The assemblages of moth pollinators differed among Satyrium species, even those that co‐flowered, and the lengths of moth tongues and floral nectar spurs were strongly correlated, suggesting that the available moth pollinator fauna is partitioned by floral traits. Pollinarium removal occurred more frequently during the night than during the day in four of the six species. Scent emission, however, was only significantly higher at dusk than midday in two species. Analysis of floral volatiles using gas chromatography coupled with mass spectrometry yielded 168 scent compounds, of which 112 were species‐specific. The scent blends emitted by each species occupy discrete clusters in two‐dimensional phenotype space, based on multivariate analysis. We conclude that these long‐spurred Satyrium species are ecologically specialised for moth pollination, yet the timing of their scent emission is not closely correlated with moth pollination activity. Scent composition was also more variable than expected from a group of closely related plants sharing the same pollinator functional group. These findings reveal a need for greater understanding of mechanisms of scent production and their constraints, as well as the underlying reasons for divergent scent chemistry among closely related plants.     

Differentiation of floral color and odor in two fly pollinated species ofMetrodorea (Rutaceae) from Brazil

We investigated if differences in morphological characters in two species ofMetrodorea (Rutaceae) from Brazilian semideciduous forests correspond to some pollination divergence.M. nigra andM. stipularis are sympatric species, display a similar floral morphology, are protandrous, self-incompatible, their flower periods overlap, and both are pollinated by flies.M. nigra main pollinators arePseudoptiloleps nigripoda (Muscidae) andFannia sp. (Fanniidae);M. stipularis major pollinators arePhaenicia eximia (Calliphoridae),Palpada sp. andOrnidia obesa (Syrphidae). The distinct floral odor (disagreeable inM. nigra and sweet inM. stipularis) and color (brownish violet vs. pale yellow) determine the differences on type and number of floral visitors observed. Several species from semideciduous forests initially considered to be pollinated by diverse insects, present flies as main pollinators, stressing the importance of fly pollination in such habitats.     

Do pollinators determine hybridization patterns in sympatricSatyrium (Orchidaceae) species?

The breakdown of species integrity was studied in three sympatricSatyrium (Orchidaceae) species at a site in the Western Cape province of South Africa. Hybrids with intermediate morphology were identified using multivariate analysis.Satyrium erectum ×S. bicorne andS. erectum ×S. coriifolium hybrids were common, while only oneS. bicorne ×S. coriifolium hybrid was found (a new record). Reciprocal artificial crossing experiments confirmed that genetic compatibility exists between all three species. However, the species have different pollinators: moths inS. bicorne, bees inS. erectum and sunbirds inS. coriifolium. Pollinators, rather than genetic factors, therefore, appear to be responsible for reproductive isolation between these species. Breakdown in pollinator specificity results in interspecific pollen transfer and the formation of hybrids. Overlap in floral signals, including nocturnal scent in bothS. erectum andS. bicorne, and bright coloration in bothS. erectum andS. coriifolium, facilitates the formation of hybrids between these species pairs. The brown, scented flowers ofS. bicorne, on the other hand, share no obvious floral signals with the bright orange, unscented flowers ofS. coriifolium, accounting for the rarity of hybrids between this species pair. Differences in floral morphology also result in mechanical isolation between these two species. Since the three species are sympatric in a very small part of their geographic ranges, it is unlikely that avoidance of hybridization has been an important selective factor in the evolution of specialized pollination systems.     

Pollination ecotypes of Satyrium hallackii (Orchidaceae) in South Africa

Intraspecific variation in floral traits may reflect adaptive shifts in the pollination system of a plant. This idea was tested by examining the pollination biology of Satyrium hallackii H. Bolus., an orchid which has spurs varying from 8 to 36 mm among populations in southern Africa. Field observations showed that the short-spurred form ( S. hallackii subsp. hallackii ) in coastal fynbos habitats is pollinated by bees, while the long-spurred form ( S. hallackii subsp. ocellatum ) in grassland habitats is pollinated primarily by hawkmoths and, secondarily, by long-tongued flies. The shift between hawkmoths and bees as pollinators may have been promoted by an ecological gradient in South Africa: carpenter bees are common in coastal fynbos habitats, but rare in grassland habitats where there are few available nesting sites. On the other hand, hawkmoths are common in grassland habitats, but rare in fynbos where there are few palatable host-plants. The formation of pollination ecotypes across pollinator gradients has probably been a major factor in the diversification of South African plants with specialized pollination systems.     

Chrysophyllum marginatum (Sapotaceae): Generalist pollination and cryptic gynomonoecious

Chrysophyllum (Chrysophylloideae, Chrysophylleae) is the second largest genus in the Sapotaceae. Studies of pollination ecology in this genus are non-existent, although there are records of entomophily for this family. Considering the lack of detailed studies on pollination ecology and sexual systems in Chrysophyllum species, we investigate the floral morphology and biology and floral visitors of Chrysophyllum marginatum to verify which sexual system is present in the studied population and whether flowers of this species are visited and pollinated by different insect groups. The population of C. marginatum has weak and cryptic gynomonoecy because the plants produce a low percentage of functionally pistillate flowers (4.2%) and these flowers appear to be perfect flowers (hermaphrode). Flowers of C. marginatum are phenotypically, ecologically and functionally generalist because: (a) they are actinomorphic, open and not restrictive in terms of access to floral resources; (b) they are visited by 26 species of insects that are potential pollinators; and (c) among these species several groups can be effective pollinators, mainly bees and flies, according to the most effective pollinator principle. We consider bees and flies to be the main pollinator group of C. marginatum, due to their high visitation rate, richness and intrafloral visiting behavior, and because they especially forage among plant individuals and are able to promote xenogamy. Nectaries were found in the ovary base and osmophores in the petal margins, as floral attractants. For Chrysophyllum, this is the first record of gynomonoecy and for the family this is considered the second record. Chrysophyllum marginatum has generalist and entomophilous pollination, as recorded in other Sapotaceae Neotropical species.     

Anthecology ofSchrankia nuttallii (Mimosaceae) on the tallgrass prairie

Schrankia nuttalii flowers through late spring on the tallgrass prairie. Although each stem produces an average of 26 capitate inflorescences only 12% of those inflorescences will open each day to disperse and receive polyads. Each inflorescence may live up to 48 hours but anthers abscise by late afternoon on the first day and the filaments change color and lose their scent. The 78–93 florets comprising each inflorescence open synchronously before dawn or during early morning hours. First day inflorescences ofS. nuttallii are herkogamous and fragrant. They are nectarless. Bombyliid flies and male bees are infrequent floral foragers so the major pollinators include female bees representing five families;Anthophoridae, Apidae, Colletidae, Halictidae, andMegachilidae. All foraging insects ignore second day inflorescences although stigmas are still receptive. Although 97% of all bees collected onS. nuttallii carrySchrankia polyads in their scopae or corbiculae 59% also carry the pollen/pollinaria of one or more coblooming angiosperms. At least 98% of all bees carrying mixed pollen loads incorporate the pollen/pollinaria of one or more nectariferous taxa (e.g.Asclepias spp.,Asteraceae, Convolvulaceae, Delphinium spec., etc.). Species of halictid bees are more likely to carry pure loads ofS. nuttallii polyads (70%) than bees of the four remaining families. Due to the nectarless florets and high degree of polylectic foraging bee-pollination inS. nuttallii converges more closely with the pollination systems of some AustralianAcacia spp. than with most other xeric/tropical genera of mimosoids studied in the western hemisphere.     

Pollination syndromes in a specialised plant‐pollinator interaction: does floral morphology predict pollinators in Calceolaria?

Pollination syndromes are defined as suites of floral traits evolved in response to selection imposed by a particular group of pollinators (e.g., butterflies, hummingbirds, bats). Although numerous studies demonstrated their occurrence in plants pollinated by radically different pollinators, it is less known whether it is possible to identify them within species pollinated by one functional pollinator group. In such a framework, we expect floral traits to evolve also in response to pollinator subgroups (e.g., species, genera) within that unique functional group. On this, specialised pollination systems represent appropriate case studies to test such expectations. Calceolaria is a highly diversified plant genus pollinated by oil‐collecting bees in genera Centris and Chalepogenus. Variation in floral traits in Calceolaria has recently been suggested to reflect adaptations to pollinator types. However, to date no study has explicitly tested that observation. In this paper, we quantitatively test that hypothesis by evaluating the presence of pollination syndromes within the specialised pollination system formed by several Calceolaria and their insect pollinators. To do so, we use multivariate approaches and explore the structural matching between the morphology of 10 Calceolaria taxa and that of their principal pollinators. Our results identify morphological matching between floral traits related to access to the reward and insect traits involved in oil collection, confirming the presence of pollinator syndromes in Calceolaria. From a general perspective, our findings indicate that the pollination syndrome concept can be also extended to the intra‐pollinator group level.     

Pollination mechanism in southern Brazilian orchids which are exclusively or mainly pollinated by halictid bees

The pollination process is documented in three sympatric orchids found in Curitiba, Paraná State, southern Brazil. InCampylocentrum aromaticum (Epidendroideae: Angraeciinae) andPrescottia densiflora (Spiranthoideae: Prescotiinae) halictid bees act as main pollinators with minor contributions from other insects, such as Syrphid flies. Because of the pollinarium and column structure inCyclopogon diversifolius. (Spiranthoideae, Spiranthinae), halictid bees are the only insects capable of performing pollination. In the three studied species pollinarium removal and deposition are achieved by interaction between the column and bee's mouth parts. Morphological and ecological flower features in agreement with this pollination mode are discussed and pollination by halictid bees is suggested to occur in a number of South American orchids.     

Preference of cabbage white butterflies and honey bees for nectar that contains amino acids

Summary Amino acids occur in most floral nectars but their role in pollinator attraction is relatively unstudied. Nectars of butterfly-pollinated flower tend to have higher concentrations of amino acids than do flowers pollinated by bees and many other animals, suggesting that amino acids are important attractants of butterflies to flowers. In order to determine whether amino acids are important in attracting butterflies and bees, we tested the preference of cabbage white butterflies (Pieris rapae) and honey bees (Apis mellifera) by allowing them to feed from artificial flowers containing sugar-only or sugar-amino acid mimics ofLantana camara nectar. Honey bees and female cabbage white butterflies consumed more sugar-amino acid nectar than sugar-only nectar. In addition, female cabbage white butterflies visited artificial flowers containing sugar-amino acid nectars more frequently than flowers containing sugar-only nectars; honey bees spent more time consuming the sugar-amino acid nectar. Male cabbage white butterflies did not discriminate between the two nectars. These results support the hypothesis that the amino acids of nectar contribute to pollinator attraction and/or feeding.     

Dioecy inHonkenya peploides var.major (Caryophyllaceae)

Sexual difference and pollination system inHonkenya peploides var.major were investigated. The present analyses indicate that sex expression of this plant is functionally dioecious, rather than androdioecious, as described previously. Its flowers are largely pollinated by small bees, hover-flies, flies, and ants. Female flowers were morphologically characterized by conspicuously longer styles and smaller petals, and had no pollen grains, while male flowers had shorter styles, larger petals, and longer filaments, and produced viable pollen grains. Although the male flowers possess many ovules in an ovary, they set fruits at a very low frequency in natural conditions and did not produce fruits by pollination experiments. We suggest that the dioecy of this species has been derived from hermaphrodite through gynodioecy, and not directly from hermaphrodite.     

The effect of wild radish floral morphology on pollination efficiency by four taxa of pollinators

The effects of floral morphology on rates of pollen removal and deposition by different pollinators in generalist plant species are not well known. We studied pollination dynamics in wild radish, Raphanus raphanistrum, a plant visited by four groups of pollinators: honey bees, small native bees, butterflies, and syrphyd flies. The effects of anther position and other factors on pollen removal during single visits by all four pollinator taxa were measured. Flowers with high anther exsertion (i.e., anthers placed higher above the opening of the corolla tube) tended to have the highest numbers of pollen grains removed, but this effect was strongest for honey bees and butterflies. For all pollinator taxa, pollen removal increased with the number of pollen grains available on a flower and whowed a positive, decelerating relationship with the duration of the visit. The effects of stigma position and other factors on pollen deposition during single visits by honey bees and butterflies were also studied. The nectar-feeding butterflies had a higher pollination efficiency (percentage of pollen grains removed from anthers that were subsequently deposited on a stigma) than the nectar- and pollen-feeding honey bees. Flowers with intermediate stigma exsertion had the highest numbers of pollen grains deposited on their stigmas by butterflies, but stigma exsertion had no effect on deposition by honey bees. For both butterflies and honey bees, pollen deposition on the recipient flower increased with the amount of pollen removed from the donor flower, and there was a positive, decelerating relationship between deposition and time spent at the flower; these results are analogous to those for pollen removal. The effects of anther and stigma exsertion on pollen removal and denosition did not fit predictions based on patterns of floral correlations, but results for morphology, pollen availability, time spent per visit, and pollinator efficiency are in broad agreement with previous studies, suggesting the possible emergence of some general rules of pollen transfer.