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1.  Pollination function transferred: modified tepals of Albuca (Hyacinthaceae) serve as secondary stigmas 
Annals of Botany  2012;110(3):565-572.
Background and Aims
The stigma, a structure which serves as a site for pollen receipt and germination, has been assumed to have evolved once, as a modification of carpels, in early angiosperms. Here it is shown that a functional stigma has evolved secondarily from modified tepals in some Albuca species (Hyacinthaceae).
Deposition of pollen on Albuca floral organs by bees was recorded. Pollen germination and fruit set was measured in flowers that had pollen deposited solely on their tepals or had their tepal tips experimentally isolated or removed after pollination.
Key Results
Leafcutter bees deposit pollen onto the papillate apices of the inner tepals of Albuca flowers. Pollen germinates in tepal-derived fluid secreted 2 or 3 d after anthesis and pollen tubes subsequently penetrate the style during flower wilting. Application of cross-pollen to the inner tepal apices of A. setosa flowers led to high fruit set. No fruits were produced in pollinated flowers in which the inner tepals were mechanically isolated or removed.
Pollen capture by tepals in the Albuca clade probably evolved in response to selection for floral morphology that maximizes the accuracy of pollen transfer. These findings show how pollination function can be transferred among floral organs, and shed light on how the original angiosperm stigma developed from sporophylls.
PMCID: PMC3400444  PMID: 22652419
Hyacinthaceae; Ornithogaloideae; pollen; pollen germination; pollen receipt; pollen tube; pollination; sexual interference
2.  Floral traits mediate the vulnerability of aloes to pollen theft and inefficient pollination by bees 
Annals of Botany  2012;109(4):761-772.
Background and Aims
Pollen-collecting bees are among the most important pollinators globally, but are also the most common pollen thieves and can significantly reduce plant reproduction. The pollination efficiency of pollen collectors depends on the frequency of their visits to female(-phase) flowers, contact with stigmas and deposition of pollen of sufficient quantity and quality to fertilize ovules. Here we investigate the relative importance of these components, and the hypothesis that floral and inflorescence characteristics mediate the pollination role of pollen collection by bees.
For ten Aloe species that differ extensively in floral and inflorescence traits, we experimentally excluded potential bird pollinators to quantify the contributions of insect visitors to pollen removal, pollen deposition and seed production. We measured corolla width and depth to determine nectar accessibility, and the phenology of anther dehiscence and stigma receptivity to quantify herkogamy and dichogamy. Further, we compiled all published bird-exclusion studies of aloes, and compared insect pollination success with floral morphology.
Key Results
Species varied from exclusively insect pollinated, to exclusively bird pollinated but subject to extensive pollen theft by insects. Nectar inaccessibility and strong dichogamy inhibited pollination by pollen-collecting bees by discouraging visits to female-phase (i.e. pollenless) flowers. For species with large inflorescences of pollen-rich flowers, pollen collectors successfully deposited pollen, but of such low quality (probably self-pollen) that they made almost no contribution to seed set. Indeed, considering all published bird-exclusion studies (17 species in total), insect pollination efficiency varied significantly with floral shape.
Species-specific floral and inflorescence characteristics, especially nectar accessibility and dichogamy, control the efficiency of pollen-collecting bees as pollinators of aloes.
PMCID: PMC3286288  PMID: 22278414
Pollen theft; pollination efficiency; dichogamy; floral morphology; Aloe; Alooideae; Xanthorrhoeaceae; Asphodeloideae
3.  Carrion mimicry in a South African orchid: flowers attract a narrow subset of the fly assemblage on animal carcasses 
Annals of Botany  2011;107(6):981-992.
Background and Aims
Although pollination of plants that attract flies by resembling their carrion brood and food sites has been reported in several angiosperm families, there has been very little work done on the level of specificity in carrion mimicry systems and the importance of plant cues in mediating such specialization. Specificity may be expected, as carrion-frequenting flies often exploit different niches, which has been interpreted as avoidance of interspecific competition. Interactions between the orchid Satyrium pumilum and a local assemblage of carrion flies were investigated, and the functional significance of floral traits, especially scent, tested. Pollination success and the incidence of pollinator-mediated self-pollination were measured and these were compared with values for orchids with sexual- and food-deceptive pollination systems.
Methods and Key Results
Observations of insect visitation to animal carcasses and to flowers showed that the local assemblage of carrion flies was dominated by blow flies (Calliphoridae), house flies (Muscidae) and flesh flies (Sarcophagidae), but flowers of the orchid were pollinated exclusively by flesh flies, with a strong bias towards females that sometimes deposited live larvae on flowers. A trend towards similar partitioning of fly taxa was found in an experiment that tested the effect of large versus small carrion quantities on fly attraction. GC-MS analysis showed that floral scent is dominated by oligosulfides, 2-heptanone, p-cresol and indole, compounds that also dominate carrion scent. Flesh flies did not distinguish between floral and carrion scent in a choice experiment using olfactory cues only, which also showed that scent alone is responsible for fly attraction. Pollination success was relatively high (31·5 % of flowers), but tracking of stained pollinia also revealed that a relatively high percentage (46 %) of pollen deposited on stigmas originates from the same plant.
Satyrium pumilum selectively attracts flesh flies, probably because its relatively weak scent resembles that of the small carrion on which these flies predominate. In this way, the plants exploit a specific subset of the insect assemblage associated with carrion. Pollination rates and levels of self-pollination were high compared with those in other deceptive orchids and it is therefore unlikely that this mimicry system evolved to promote outcrossing.
PMCID: PMC3080630  PMID: 21402538
Calliphoridae; deception; floral scent; indole; oligosulfides; osmophore; outcrossing; p-cresol; Sarcophagidae; Satyrium pumilum; specialization
4.  Pollination and late-acting self-incompatibility in Cyrtanthus breviflorus (Amaryllidaceae): implications for seed production 
Annals of Botany  2010;106(4):547-555.
Background and Aims
Animal pollination is typically an uncertain process that interacts with self-incompatibility status to determine reproductive success. Seed set is often pollen-limited, but species with late-acting self-incompatibility (SI) may be particularly vulnerable, if self-pollen deposition results in ovule discounting. Pollination is examined and the occurrence of late-acting SI and ovule discounting assessed in Cyrtanthus breviflorus.
The pollination system was characterized by observing floral visitors and assessing nectar production and spectral reflectance of flowers. To assess late-acting SI and ovule discounting, growth of self- and cross-pollen tubes, and seed set following open pollination or hand pollination with varying proportions of self- and cross-pollen, were examined.
Key Results
Native honeybees Apis mellifera scutellata pollinated flowers as they actively collected pollen. Most flowers (≥70 %) did not contain nectar, while the rest produced minute volumes of dilute nectar. The flowers which are yellow to humans are visually conspicuous to bees with a strong contrast between UV-reflecting tepals and UV-absorbing anthers and pollen. Plants were self-incompatible, but self-rejection was late-acting and both self- and cross-pollen tubes penetrated ovules. Seed set of open-pollinated flowers was pollen-limited, despite pollen deposition exceeding ovule number by 6-fold. Open-pollinated seed set was similar to that of the cross + self-pollen treatment, but was less than that of the cross-pollen-only treatment.
Flowers of C. breviflorus are pollinated primarily by pollen-collecting bees and possess a late-acting SI system, previously unknown in this clade of the Amaryllidaceae. Pollinators of C. breviflorus deposit mixtures of cross- and self-pollen and, because SI is late-acting, self-pollen disables ovules, reducing female fertility. This study thus contributes to growing evidence that seed production in plants with late-acting SI systems is frequently limited by pollen quality, even when pollinators are abundant.
PMCID: PMC2944973  PMID: 20647225
Amarydillaceae; Cyrtanthus breviflorus; honeybee pollination; late-acting self-incompatibility; ovule discounting; pollen limitation; pollen quantity and quality
5.  Reproductive biology of Acrolophia cochlearis (Orchidaceae): estimating rates of cross-pollination in epidendroid orchids 
Annals of Botany  2008;104(3):573-581.
Background and Aims
Pollen fates strongly influence mating success in plants but are difficult to quantify. By promoting foraging constancy in pollinators, floral rewards such as nectar may enhance the overall efficiency of pollen transfer. However, this can also lead to high levels of geitonogamy. Pollen fates were studied in Acrolophia cochlearis, a member of a terrestrial epidendroid orchid genus that includes both rewarding and deceptive species.
Pollinator observations were conducted. Pollen transfer efficiency (PTE), the proportion of removed pollinia deposited on stigmas, was measured in a large population at regular intervals throughout the 5-month flowering season. The level of cross-pollination in two populations was estimated from the percentage of seeds with embryos in naturally pollinated fruits.
Key Results
Acrolophia cochlearis (and a congener A. micrantha) produce minute but concentrated nectar rewards. Observations showed that A. cochlearis is pollinated exclusively by a solitary bee species, Colletes claripes. Although both sexes visited flowers, only males carried pollinaria. Overall levels of pollination and PTE of the rewarding A. cochlearis were much higher than in a deceptive congener, A. capensis. Seeds resulting from self-fertilization had a significantly lower probability of containing viable embryos than did those from cross-fertilization. This dichotomy in fruit quality was used to estimate that cross-pollination occurred in approx. 66 % of A. cochlearis flowers in a large dense population and approx. 10 % in a small sparse population. Traits of A. cochlearis that limit geitonogamy include pollinarium reconfiguration that exceeds the visit time of pollinators and rapid flower senescence following visitation.
Presence of a nectar reward in Acrolophia cochlearis results in high levels of PTE. It is estimated that approx. 33–90 % of fruits in natural populations arise from self-pollination in this species.
PMCID: PMC2720661  PMID: 19001427
Reward; deception; pollen transfer efficiency; pollen tracking; geitonogamy; Acrolophia cochlearis; epidendroid orchid; Cape floral region
6.  Pollination Systems of Colchicum (Colchicaceae) in Southern Africa: Evidence for Rodent Pollination 
Annals of Botany  2008;102(5):747-755.
Background and Aims
Plants adapted for pollination by rodents tend to exhibit a distinct floral syndrome that includes dull coloured and geoflorous inflorescences and nocturnal anthesis and nectar production. On the basis of their floral traits, it was predicted that two African Colchicum species (C. scabromarginatum and C. coloratum) are rodent-pollinated.
Field studies were carried out in the semi-arid Succulent Karoo region of South Africa. Live trapping of rodents was conducted and pollen loads on the rodents were quantified. The daily periodicity of nectar production was determined. Selective exclusion and controlled pollination experiments were also conducted.
Key Results
Live-trapped rodents were found to carry large amounts of Colchicum pollen on the fur of their snouts, and in their faeces. Birds were occasional pollinators of flowers of C. coloratum. During the evening, nectar volume and concentration increased for both species. When vertebrates were excluded from C. scabromarginatum and C. coloratum plants, there was a significant decrease in seed set compared with open control plants. By contrast, vertebrate exclusion did not significantly affect seed production of a congener, C. hantamense, which has floral traits associated with insect pollination. Breeding system experiments revealed that both C. scabromarginatum and C. coloratum require pollinators for seed production. Colchicum scabromarginatum is strictly self-incompatible, whereas C. coloratum is partially self-compatible.
Pollination by rodents occurs in two African Colchicum species. C. scabromarginatum appears to depend exclusively on rodents for seed production, while birds and autonomous selfing may contribute to seed production in C. coloratum. These are the first records of rodent pollination in the Colchicaceae.
PMCID: PMC2712380  PMID: 18723860
Convergent evolution; floral syndrome; pollination; rodents; birds; insects; Colchicum scabromarginatum; Colchicum coloratum; Succulent Karoo; southern Africa
7.  Is Eucalyptus Cryptically Self-incompatible? 
Annals of Botany  2007;100(6):1373-1378.
Background and Aims
The probability that seeds will be fertilized from self- versus cross-pollen depends strongly on whether plants have self-incompatibility systems, and how these systems influence the fate of pollen tubes.
In this study of breeding systems in Eucalyptus urophylla and Eucalyptus grandis, epifluorescence microscopy was used to study pollen tube growth in styles following self- and cross-pollinations.
Key Results
Pollen tubes from self-pollen took significantly longer than those from cross-pollen to grow to the base of the style in both E. urophylla (120 h vs. 96 h) and E. grandis (96 h vs. 72 h). In addition, both species exhibited reduced seed yields following self-pollination compared with cross-pollination.
The present observations suggest that, in addition to a late-acting self-incompatibility barrier, cryptic self-incompatibility could be a mechanism responsible for the preferential out-crossing system in these two eucalypt species.
PMCID: PMC2759262  PMID: 17881341
Eucalyptus urophylla; Eucalyptus grandis; epifluorescence microscopy; cryptic self-incompatibility

Results 1-7 (7)