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Reproductive Biology |
Department of Botany and Zoology, Stellenbosch University, Private Bag X1, Matieland, 7602 South Africa
Received for publication February 11, 2005. Accepted for publication August 6, 2005.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: distyly • enantiostyly • evolution of selfing • Hemimeris sabulosa • heterostyly • mating system • morph ratio • reproductive biology
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Jesson and Barrett, 2002a
).
Darwin's (1877)
pioneering work on stylar polymorphism has blossomed into a rich literature (reviewed in Barrett, 1992
; Barrett et al., 2000
; Barrett, 2002
), which describes five principal types. Populations of distylous and tristylous species (together referred to as heterostylous) are composed, respectively, of two and three floral morphs that differ in style and stamen lengths. Stigma height dimorphism is a less common condition in which populations consist of two morphs that differ only in the length of the style, but not in the length of the anthers. Enantiostyly is a form of floral asymmetry in which the style is deflected away from the central axis of the flower either to the left or right side. Lastly, populations of flexistylous plants consist of two morphs that differ in the timing of male and female functions. The style curls out of the way during pollen release, which occurs either in the morning or in the afternoon depending on the morph.
In this study, I describe a new type of stylar polymorphism, provisionally referred to as inversostyly. The polymorphism occurs in most populations of Hemimeris racemosa (Scrophulariaceae), a common annual herb from the Cape region, which is specialized for pollination by female oil-collecting bees. The aims of the study were to (1) describe the phenomenon of inversostyly in H. racemosa and to make comparisons with homostylous populations of H. racemosa and other species in the genus, (2) describe the unusually specialized mode of pollination, (3) document patterns of morph ratio variation among inversostylous populations and to explore reasons for this variation, (4) investigate the breeding system of inversostylous and homostylous populations of Hemimeris, and (5) explore factors that contribute to the breakdown of inversostyly and the evolution of homostyly.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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. Frequent comparisons are made with H. sabulosa L. f., as well as with the remaining two species in the genus. Detailed studies were conducted on 23 populations of H. racemosa and four populations of H. sabulosa in an area bound by Nieuwoudville, Tulbagh, Botrivier, and the Cape Peninsula of South Africa.
Functional floral morphology
I examined and photographed H. racemosa and H. sabulosa populations in the field and collected specimens into an FAA (formalin, acetic acid and alcohol) solution to compare three-dimensional morphologies. Scanning electron micrographs of liquid-preserved material were taken using a LEO S440 scanning electron microscope (LEO Electron Microscopy, Thornwood, New York, USA). Before viewing, flowers were critical-point dried and splutter-coated with Au/Pd. At all sites, I collected voucher specimens and placed them in the Bolus Herbarium, University of Cape Town.
The Sudan IV test was used to test for the presence of floral oil in the study species. The crystals dissolve in oil, which then turns red; the crystals do not dissolve in aqueous solutions, which remain unstained. Crystals were sprinkled onto the floral parts and the reaction examined with a Leica MZ8 dissecting microscope (Leica Microscopy and Scientific Instruments Group, Heerburg, Switzerland). The swollen trichomes inside the flower were mechanically agitated before testing.
Flower visitors and pollinator behavior
I observed pollinators at flowering populations of Hemimeris racemosa and H. sabulosa on 35 days between mid August and mid October of 1998–2004. Flower visitors were captured and identified according to Whitehead and Steiner (2001)
. I described pollinator behavior in detail from photographic series.
Pollinator visitation rate was quantified at 22 of the populations of H. racemosa and at all four populations of H. sabulosa by observing 
5-m2 patches of flowering plants for two 15-min intervals from a distance of 1.5 m. These observations were restricted to warm (>20°C), windless hours between 1030 and 1530 hours. I calculated visitation rate as visits per flower per hour.
Frequency of style morphs
To determine the relative frequencies of style-up and style-down morphs in inversostylous populations of H. racemosa, I surveyed 12 populations by checking the style position on 71–244 plants along a random, wandering transect (median = 95.5 plants). Biased selection of individuals is unlikely, because the style position can only be determined at very close range. I sampled plants at 4-m intervals, because a pilot study revealed spatial clustering of same style morphs within small neighborhoods (<4 m). Replicated goodness-of-fit tests (G statistics) were calculated as in Sokal and Rohlf (1995)
to determine whether (1) populations deviated from the 1 : 1 expectation of morph ratios, (2) morph ratios were homogeneous across populations, and (3) the pooled data from all populations deviated from the expected 1 : 1 frequency.
To explore reasons for deviations from the expected 1 : 1 morph ration, I correlated interpopulation variation in morph ratio with variation in pollinator visitation rate. To investigate the possibility that deviations in morph ratio result from morph-specific differences in the autogamous self-pollination rate, I excluded pollinators from style-down and style-up plants at Chapman's Peak by enclosing budding plants in wire cages covered with fine gauze bags. The edges of the bags were pinned to the ground. There was no contact between gauze and flowers. I recorded capsule set as the dependent variable because seeds in Hemimeris are minute and numerous. Capsules mature and dehisce sequentially over a prolonged period, both during and after flowering, but remain attached to the plant after the seeds are released. The withered remains of undeveloped ovaries, along with their peduncles and calyxes, also remain attached to the plant after flowering, indicating failed capsule set. I evaluated differences in capsule set between morphs using the Mann-Whitney U test.
Variation in self-fertility and capsule set
I used the same pollinator exclusion bags to compare autogamous pollination rate between homostylous and inversostylous populations of H. racemosa and between species of Hemimeris. Control plants were marked with adhesive jewelry tags and left unbagged to receive pollinator visits. Sites and sample sizes are listed in Table 1. The Mann-Whitney U test was used to determine the statistical significance of differences in capsule set between treatments.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Five of 23 populations of H. racemosa were homostylous. Plants in these populations differ from both of the two morphs in the inversostylous populations in having the two stamens and the style clustered together in the down position (Figs. 1d, 2c). Thus, plants in homostylous populations are not herkogamous, and there is direct contact between the anthers and stigma. Plants in homostylous populations are smaller and have fewer, considerably smaller flowers (Fig. 1f vs. e). In other details of floral and vegetative morphology, the homostylous form of H. racemosa resembles the typical inversostylous form.
In contrast with H. racemosa, all examined populations of H. sabulosa were homostylous, with the two stamens and the style clustered together in the down position (Figs. 1c, 2d). In this respect, the flowers of H. sabulosa resemble the flowers of the homostylous, autogamous form of H. racemosa. The dish shaped flowers and vegetative features (Grant, 1938
) nevertheless distinguish this species from the autogamous form of H. racemosa. There was considerable variation in plant and flower size among populations of H. sabulosa. The remaining two species in the genus, H. gracilis and H. centrodes, were also found to be homostylous, with direct contact between the anthers and stigma.
Flower visitors and pollinator behavior
During visitor censuses at the flowers of inversostylous Hemimeris racemosa, 177 visits by small beetles and 3088 visits by oil-collecting bees in the genus Rediviva were observed. Rediviva species were present at 15 of the 18 populations of inversostylous H. racemosa. In contrast, Rediviva species were absent from all five homostylous populations of H. racemosa and present at only one of four populations of H. sabulosa.
Insects captured on the flowers of inversostylous Hemimeris racemosa were three species (20 individuals) of small pollen-eating beetle (Nitidulidae, Melyridae, and Scarabaeidae) and five species (57 individuals) of Rediviva. The maximum number of Rediviva species captured on H. racemosa at one site was three (five sites). R. parva was captured at nine sites, R. bicava at six sites, R. intermixta at four, R. peringueyi at four, and R. albifasciata at one. R. parva was the only species captured on H. sabulosa. All captured Rediviva were female.
Beetles were most often observed to be resting inside the flowers of H. racemosa. Occasionally, mating and pollen feeding were observed (Fig. 3c). Because beetles seldom moved between flowers, low levels of beetle visitation were recorded during censusing (0.03 ± 0.02 visits · flower–1 · h–1, range = 0–0.31, 17 sites). In contrast, the average visitation rate by Rediviva was 0.78 ± 0.22 visits per flower per hour (range = 0–3.60, 17 sites). All Rediviva were actively engaged in collecting oil from H. racemosa flowers (Fig. 3a, b). They did so by hinging the dorsal petal lobe open and probing inside the pouches with their front legs. The tibia of the middle legs typically rested on the entrances to the pouches. The hind tibia hooked onto the edges of the bilobed lower lip of the corolla. In this position, the stigma and anthers were brought into contact with the bases of the legs (coxa) and the underside of the head and thorax (mesosoma). In some photographs, the bees are holding on to the anthers or style (whichever is vertical) with their front tarsi and/or jaws, while the middle legs and/ or front legs are inside the pouches. Individual R. parva visited 17–19 flowers per minute. A maximum of 84 flowers were visited during one foraging bout by an individual bee.
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Pollen loads
The beetles carried little or no H. racemosa pollen on their bodies. The Rediviva spp. carried large quantities of H. racemosa pollen on the sternum (underside) of the mesosoma (thorax) and the coxae (bases of the legs), as well as smaller quantities on the post genial area (underside of the head) (Fig. 3d). Some individuals carried unidentified pollen in their scopae (pollen baskets). Large quantities of yellow oil could be drawn from the pollen masses in the scopae using filter paper.
Preliminary observations suggest that the two morphs of H. racemosa deposit pollen on separate locations on the body of the bee. Pollen, apparently derived from the style-down morph, forms a cluster anterior to the coxa of the front legs on the sternum of the mesosoma; pollen, apparently derived from the style-up morph, forms a cluster posterior to the coxa of the front legs on the sternum of the mesosoma (Fig. 3d). In contrast, pollen was clustered in only one area (posterior to the front legs) on individuals of R. parva captured on the monomorphic H. sabulosa.
Frequency of style morphs
Most inversostylous populations had a slight bias in favor of the style-down morph (Fig. 4). The deviation from the expectation of equal ratios was significant in only one of 12 populations (Paradyskloof site, G = 6.8, df = 1, P < 0.01) . When the data from all 12 populations were pooled, the ratio of style-up to style-down plants in the total sample deviated significantly from the 1 : 1 expectation (Table 2). The significant deviation did not result from heterogeneity among populations, but rather from the increase in power obtained by pooling samples (Table 2). The bias in favor of the style-down morph was greatest where pollinators were scarce (Fig. 5), suggesting morph-specific differences in selfing rate; however, a preliminary pollinator exclusion experiment did not detect a significant difference in autogamous pollination rate between the two morphs (Capsule set: Style-down = 17%, SE = 7, N = 9; Style-up = 15%, SE = 4, N = 9; Z = 0.37).
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Average capsule set in unmanipulated plants varied from 18–81% in inversostylous populations of H. racemosa. In homostylous populations of H. racemosa, capsule set varied from 48–92%. In two populations of H. sabulosa, capsule set was 84%–86%. In inversostylous populations of H. racemosa, relatively low levels of capsule set are associated with low pollinator visitation rates (Fig. 6). In contrast, consistently high levels of capsule set were observed in homostylous populations of H. racemosa and H. sabulosa, even where pollinators were absent (Fig. 6).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Inversostyly is distinct from heterostyly (distyly and tristyly) in which floral morphs differ in style and stamen length, rather than orientation. Also, unlike typical heterostylous systems, Hemimeris lacks an associated heteromorphic self-incompatibility system (Table 1). Inversostyly is distinct from enantiostyly (mirror-image flowers) in which flowers are asymmetrical, with the style deflected either to the left or right (Barrett et al., 2000
). A further difference with enantiostyly is the complete reciprocity of all the sex organs; in enantiostylous species, the style alternates with, at most, one of the stamens, while the position of the remainder of stamens does not differ between morphs (Jesson and Barrett, 2003
). Stylar polymorphisms are particularly well represented in the South African flora (Ornduff, 1974
; Steiner, 1987
), but have not been reported for Hemimeris, and are not known from other Scrophulariaceae (Barrett et al., 2000
).
Five of 17 populations of H. racemosa were monomorphic for style and stamen position. In these homostylous populations of H. racemosa, the dissolution of the stylar polymorphism occurs through the formation of a third morph in which the two stamens and the style are clustered together in the down position (Figs. 1d, 2c). Plants in homostylous populations are not herkogamous—there is direct contact between the anthers and stigma. In this respect, homostylous populations of H. racemosa resemble the widespread Hemimeris sabulosa (Figs. 1c, 2d), as well as H. gracilis and H. centrodes.
Pollination by oil-collecting bees
Hemimeris racemosa is unusual among plants with stylar polymorphism in having a specialized pollination system. In the southwestern Cape, where this study was conducted, H. racemosa was found to be pollinated by five species of oil-collecting bee in the genus Rediviva, while a maximum of three Rediviva species served as the pollinators at any one site (Fig. 3). In other parts of its range, additional species of Rediviva are known to visit H. racemosa (Whitehead and Steiner, 2001
). The flowers of H. racemosa offer only oil as a reward to pollinators. The oil is secreted by trichome elaiophores, which are concentrated inside and around twin pouches (Fig. 2e, f). In their structure, the elaiophores superficially resemble those of several other members of the Scrophulariaceae (Vogel, 1974
; Steiner and Whitehead, 2002
; Kornhall, 2004
).
Female Rediviva enter the flowers of H. racemosa by forcing open the hinged dorsal petal lobe and inserting their front (and sometimes middle) legs into the twin pouches. There are plumose oil-collecting hairs on the tarsi of these legs, as well as blade-like scraper hairs (Whitehead and Steiner, 2001
), which may play a role in rupturing the swollen elaiophores. Floral oil is not known to be used as an adult food by oil-collecting bees, but is used by female bees primarily as a larval food (Vogel, 1974
; Cane et al., 1983
; Vinson et al., 1997
). Thus, the fact that only female bees were caught on the flowers of the study species confirms the finding that the reward is oil rather than nectar. The presence of large quantities of oil in the scopae (pollen baskets) of female bees indicates that the reward was collected successfully by Rediviva. The placement of the oil-secreting pouches on either side of the anthers and style is very similar to the arrangement in the Rediviva-pollinated Diascia (Scrophulariaceae) (Steiner and Whitehead, 1988
) and necessitates contact between the reproductive parts and the underside of the foraging bee.
The distribution of pollen on the underside of captured Rediviva suggests anterior/posterior segregation of the pollen load from style-up and style-down morphs of H. racemosa. Pollen from the style-down morph appeared to be clustered anterior to the first pair of legs; pollen from the style-up morph appeared to be clustered posterior to the first pair of legs (Fig. 3d). The styles alternate with the stamens, so the morph that places pollen anteriorly will collect pollen posteriorly and vice versa. Because all flowers on a plant are of the same morph, inversostyly is likely to promote cross-pollination by limiting geitonogamy and geitonogamous pollen loss. Thus, inversostyly is suggested to be functionally analogous to dimorphic reciprocal enantiostyly (Jesson and Barrett, 2002a
, 2003
). The precise positioning of the bee on the flower is critical to the functioning of inversostyly, because mispositioning of the bee by only 3 mm will result in intramorph pollen transfer.
Morph ratios in inversostylous populations
Equal morph ratios are expected in plants with polymorphic sexual systems because frequency dependent selection will favor the rarer morph (Fisher, 1941
; Charlesworth and Charlesworth, 1979
). In this light, the subtle bias in favor of the style-down morphs in most inversostylous populations of H. racemosa is interesting (Fig. 4). In heterostylous and enantiostylous species, unequal morph ratios have been suggested to result from founder effects and genetic drift, clonal propagation, and morph-specific differences in selfing or assortative mating (Eckert and Barrett, 1992
; Husband and Barrett, 1992
; Barrett et al., 1997
; Jesson and Barrett, 2002b
). Morph-specific differences in selfing rate are a possible explanation for morph ratio deviation in H. racemosa because pollen movement by gravity is likely to result in more frequent self-fertilization in the style-down morph. The observation that the proportion of style-down plants in a population tends to increase as pollinator visitation rate decreases favors this explanation (Fig. 5). However, the style-down morph did not set significantly more capsules than the style-up morph under artificial conditions of pollinator exclusion. An alternative hypothesis focuses on morph-specific differences in the male component of fitness. The style-up morph is likely to suffer greater pollen losses to pollen-feeding beetles and the elements, because the anthers in this morph are not protected under the hooded dorsal petal lobe (Fig. 3c). The observed relationship with pollination rate (Fig. 5) also makes sense in this scenario: when the pollination rate is low, the pollen of the style-up morph will remain exposed for longer periods. Central to both hypotheses is the observation that pollination rate is spatially variable and frequently very low in Hemimeris as a result of its specialized pollination system.
The maintenance of inversostyly in a specialized pollination system
Self-pollinating populations or taxa that have originated through the breakdown of stylar polymorphism are commonly observed in heterostylous and enantiostylous clades (Darwin, 1877
; Ernst, 1955
; Baker, 1966
; Ornduff, 1972
; Barrett and Shore, 1987
; Barrett, 1989
; Washitani et al., 1994
; Jesson and Barrett, 2002b
). This seems also to be the case in inversostyly. Homostyly in H. racemosa and H. sabulosa allows direct contact between the anthers and stigma and is associated with autogamous self-pollination (Table 1).
It is interesting to note that homostylous populations of H. racemosa and most populations of H. sabulosa occurred in areas where their specialized pollinators are rare or absent. During censuses, Rediviva were not observed at any of five homostylous populations of H. racemosa and were present at only one of four populations of H. sabulosa. At these sites, few other insects were observed on the flowers, presumably because the specialized reward (floral oil) is attractive only to Rediviva. Despite low visitation rates, capsule set was nevertheless high in homostylous populations (Fig. 6), so the adaptive value of homostyly is apparently to provide reproductive assurance through self-pollination.
Unique among stylar polymorphisms, inversostyly occurs in a species with a specialized pollination system. This specialization ensures an exact fit between flower and pollinator and is likely to have promoted the evolution of the polymorphism. On the other hand, this specialized oil-bee pollination system is spatially and temporally variable—pollination rate drops from high to zero over short distances (Pauw, 2004
). This variability sets up strong selection differentials, which, coupled with the annual nature of the plant, create unique opportunities for the study of the evolution of stylar polymorphisms.
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FOOTNOTES |
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The author thanks William Bond, Spencer Barrett, and two anonymous reviewers for valuable comments; Vin Whitehead for help with Rediviva identification; John Rourke for help with terminology; Gabriela Demergasso, Tilla Raimondo, and Anthony Roberts for help in the field; Lize Agenbag for line drawings; and the National Geographic Society and the NRF (South Africa) for funding. 
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Barrett S. C. H. 1989 The dissolution of a complex genetic polymorphism: the evolution of self-fertilization in tristylous Eichhornia paniculata (Pontederiaceae). Evolution 43: 1398-1416[CrossRef][ISI]
Barrett S. C. H. 1992 Evolution and function of heterostyly. Springer Verlag, Berlin, Germany
Barrett S. C. H. 2002 The evolution of plant sexual diversity. Nature Reviews Genetics 3: 274-284[CrossRef][ISI][Medline]
Barrett S. C. H. J. S. Shore 1987 Variation and evolution of breeding systems in the Turnera ulmifolia L. complex (Turneraceae). Evolution 41: 340-354[CrossRef][ISI]
Barrett S. C. H. L. K. Jesson A. M. Baker 2000 The evolution and function of stylar polymorphisms in flowering plants. Annals of Botany 85: 253-265
Barrett S. C. H. W. W. Cole J. Arroyo M. B. Cruzan D. G. Lloyd 1997 Sexual polymorphisms in Narcissus triandrus (Amaryllidaceae): is this species tristylous?. Heredity 78: 135-145[CrossRef][ISI]
Cane J. H. G. C. Eickwort F. R. Wesley J. Speilholz 1983 Foraging, grooming and mate-seeking behaviors of Macropis nuda (Hymenoptera, Melittidae) and use of Lysimachia (Primulaceae) oils in larval provisions and cell linings. American Midland Naturalist 110: 257-264[CrossRef][ISI]
Charlesworth B. D. Charlesworth 1979 A model for the evolution of distyly. American Naturalist 114: 467-498[CrossRef][ISI]
Darwin C. 1877 The different forms of flowers on plants of the same species. Murray, London, UK
Eckert C. G. S. C. H. Barrett 1992 Stochastic loss of style morphs from populations of tristylous Lythrum salicaria and Decodon verticillatus (Lythraceae). Evolution 46: 1014-1029[CrossRef][ISI]
Ernst A. 1955 Self-fertility in monomorphic primulas. Genetica 27: 91-148
Fisher R. A. 1941 The theoretical consequences of polyploid inheritance for the mid style form in Lythrum salicaria. Annals of Eugenics 11: 31-38
Grant A. L. 1938 A monograph of the genus Hemimeris. Annals of the Missouri Botanical Garden 25: 435-453[CrossRef]
Husband B. C. S. C. H. Barrett 1992 Genetic drift and the maintenance of the style length polymorphism in tristylous populations of Eichhornia paniculata (Pontederiaceae). Heredity 69: 440-449[ISI]
Jesson L. K. S. C. H. Barrett 2002a Enantiostyly: solving the puzzle of mirror-image flowers. Nature 417: 707[CrossRef][Medline]
Jesson L. K. S. C. H. Barrett 2002b Enantiostyly in Wachendorfia (Haemodoraceae): the influence of reproductive systems on the maintenance of the polymorphism. American Journal of Botany 89: 253-262
Jesson L. K. S. C. H. Barrett 2003 The comparative biology of mirror-image flowers. International Journal of Plant Sciences 164: S237-S249[CrossRef][ISI]
Kornhall P. 2004 Phylogenetic studies in the Lamiales with special focus on the Scrophulariaceae and Stilbaceae. Ph.D. dissertation, Uppsala University, Uppsala, Sweden
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Ornduff R. 1972 The breakdown of trimorphic incompatibility in Oxalis section Corniculatae. Evolution 25: 52-65
Ornduff R. 1974 Heterostyly in South African flowering plants: a conspectus. South African Journal of Botany 40: 169-187
Pauw A. 2004 Variation in pollination across a fragmented landscape at the Cape of Africa. Ph.D. dissertation, University of Cape Town, Cape Town, South Africa
Sokal R. R. F. J. Rohlf 1995 Biometry. Freeman, New York, New York, USA
Steiner K. E. 1987 Breeding systems in the Cape flora. In A. G. Rebelo [ed.], A preliminary synthesis of pollination biology in the Cape flora, 22–51. CSIR, Pretoria, South Africa
Steiner K. E. V. B. Whitehead 1988 The association between oil-producing flowers and oil-collecting bees in the Drakensberg of southern Africa. Monographs in Systematic Botany from the Missouri Botanic Gardens 25: 259-277
Steiner K. E. V. B. Whitehead 2002 Oil secretion and the pollination of Colpias mollis (Scrophulariaceae). Plant Systematics and Evolution 235: 53-66[CrossRef][ISI]
Vinson S. B. H. J. Williams G. W. Frankie G. Shrum 1997 Floral lipid chemistry of Byrsonima crassifolia (Malpigheaceae) and a use of floral lipids by Centris bees (Hymenoptera: Apidae). Biotropica 29: 76-83[CrossRef][ISI]
Vogel S. 1974 Ölblumen und ölsammelnde Bienen. Tropische und subtropische Pflanzenwelt 7: 285-547
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