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Review
, 97 (3), 317-44

Radiation of Pollination Systems in the Iridaceae of sub-Saharan Africa

Affiliations
Review

Radiation of Pollination Systems in the Iridaceae of sub-Saharan Africa

Peter Goldblatt et al. Ann Bot.

Abstract

Background: Seventeen distinct pollination systems are known for genera of sub-Saharan African Iridaceae and recurrent shifts in pollination system have evolved in those with ten or more species. Pollination by long-tongued anthophorine bees foraging for nectar and coincidentally acquiring pollen on some part of their bodies is the inferred ancestral pollination strategy for most genera of the large subfamilies Iridoideae and Crocoideae and may be ancestral for the latter. Derived strategies include pollination by long-proboscid flies, large butterflies, night-flying hovering and settling moths, hopliine beetles and sunbirds. Bee pollination is diverse, with active pollen collection by female bees occurring in several genera, vibratile systems in a few and non-volatile oil as a reward in one species. Long-proboscid fly pollination, which is apparently restricted to southern Africa, includes four separate syndromes using different sets of flies and plant species in different parts of the subcontinent. Small numbers of species use bibionid flies, short-proboscid flies or wasps for their pollination; only about 2 % of species use multiple pollinators and can be described as generalists.

Scope: Using pollination observations for 375 species and based on repeated patterns of floral attractants and rewards, we infer pollination mechanisms for an additional 610 species. Matching pollination system to phylogeny or what is known about species relationships based on shared derived features, we infer repeated shifts in pollination system in some genera, as frequently as one shift for every five or six species of southern African Babiana or Gladiolus. Specialized systems using pollinators of one pollination group, or even a single pollinator species are the rule in the family. Shifts in pollination system are more frequent in genera of Crocoideae that have bilaterally symmetric flowers and a perianth tube, features that promote adaptive radiation by facilitating precise shifts in pollen placement, in conjunction with changes in flower colour, scent and tube length.

Conclusions: Diversity of pollination systems explains in part the huge species diversity of Iridaceae in sub-Saharan Africa, and permits species packing locally. Pollination shifts are, however, seen as playing a secondary role in speciation by promoting reproductive isolation in peripheral, ecologically distinct populations in areas of diverse topography, climate and soils. Pollination of Iridaceae in Eurasia and the New World, where the family is also well represented, is poorly studied but appears less diverse, although pollination by both pollen- and oil-collecting bees is frequent and bird pollination rare.

Figures

F<sc>ig</sc>. 1.
Fig. 1.
Flowers pollinated by bees, using either the large anthophorine system (A–F) or the pollen-collecting female bee system (G–J). (A) Gladiolus papilio, with arched dorsal tepal concealing the stamens and style branches. (B) G. alatus, arrows indicate flowers in male phase (style branches folded together and style not extended) or female phase (style extended, style branches unfolded and stigmatic tips expanded). (C) G. uysiae. (D) Tritonia watermeyeri, with tooth-like ridges on lower three tepals. (E) Moraea tripetala. (F) M. papilionacea. (G) Gladiolus stellatus. (H) G. quadrangulus. (I) Moraea bifida. (J) M. marlothii. I and J with the staminal column enlarged to show anthers in close proximity to stigmatic surfaces. Scale bar = 10 mm.
F<sc>ig</sc>. 2.
Fig. 2.
Lateral and frontal views of flowers pollinated by long-proboscid flies and the fly Moegistorhynchus longirostris. (A) Ixia paniculata. (B) Geissorhiza exscapa. (C) Lapeirousia anceps. (D) Gladiolus angustus. (E) Tritonia crispa. (F) Pelargonium moniliforme (Geraniaeae), to show similarity of flower form in another family belonging to this guild. Scale bar = 10 mm.
F<sc>ig</sc>. 3.
Fig. 3.
Differential pollen placement indicated by arrows and hatching on fly's body by different plant species of the Moegistorhynchus longirostris pollination guild. (A) Ixia paniculata (frons and base of proboscis). (B) Tritonia crispa (dorsal part of head). (C) Lapeirousia anceps (dorsal part of thorax). (D) Pelargonium appendiculatum (ventral part of head and thorax). (E) Geissorhiza exscapa (ventral part of abdomen). Scale bar = 1 cm.
F<sc>ig</sc>. 4.
Fig. 4.
Pollination systems in Iridaceae I. Bee pollination. Apis mellifera (Apidae) on Moraea ciliata (top row, left); Rediviva sp. (Melittidae) on Moraea inclinata (top row, right). Long-proboscid fly pollination. Moegistorhynchus longirostris (Nemestrinidae) visiting Lapeirouisa anceps (middle row, left); Prosoeca sp. (Nemestrinidae) visiting Lapeirousia oreogena (middle row, centre); Prosoeca peringueyi (Nemestrinidae) visiting Lapeirousia pyramidalis subsp. regalis (middle row, right). Butterfly pollination. Aeropetes tulbaghia (Satyridae) on Tritoniopsis burchellii (bottom row, left). Bird pollination. Lesser double-collared sunbird, Nectarinia chalybea on Chasmanthe aethiopica (bottom row, right) (photographer: Colin Paterson-Jones).
F<sc>ig</sc>. 5.
Fig. 5.
Flowers pollinated by large butterflies, with vertical sections of some flowers, and the satyrid butterfly Aeropetes tulbaghia at same scale. (A) Hesperantha coccinea. (B) Tritoniopsis lesliei, lateral and dorsal views. (C) Crocosmia aurea. (D) Freesia laxa. (E) Gladiolus saundersii. (F) G. stefaniae. (G) G. nerineoides; a brush flower in contrast to the previous two flag flowers of the same genus. Scale bar = 10 mm.
F<sc>ig</sc>. 6.
Fig. 6.
Flowers pollinated by moths: (A–D), sphinxmoth flowers; (E–H) settling moth flowers. (A) Lapeirousia odoratissima. (B) Gladiolus longicollis subsp. praelongitubus. (C) Gladiolus hyalinus. (D) Tritoniopsis nervosa with the moth Hyles lineata. (E) Gladiolus emiliae. (F) Hesperantha falcata. (G) Hesperantha radiata. (H) Freesia viridis. Scale bar = 10 mm.
F<sc>ig</sc>. 7.
Fig. 7.
Lateral views of flowers pollinated by sunbirds, with vertical sections of some flowers, and the sunbird Nectarinia famosa at the same scale. (A) Gladiolus watsonius (section Homoglossum). (B) G. abyssinicus (section Ophiolyza). (C) G. cunonius (section Hebea). (D) Tritoniopsis caffra. (E) T. burchellii. (F) Witsenia maura (radially symmetric flower). Note the different floral form in the different species of Gladiolus. Scale bar = 10 mm.
F<sc>ig</sc>. 8.
Fig. 8.
Flowers pollinated by hopliine beetles. (A) Babiana papyracea; whole plant and single flower—note the narrow perianth tube that serves only to raise the flower above the ground. (B) Hesperantha vaginata, with prominent ‘beetle marks’ in centre of flower and at tips of outer tepals. (C) Ixia superba; flowering branch and lateral view of single flower. (D) Ixia maculata; dorsal and lateral views. (E) Moraea insolens. (F) Moraea elegans. Scale bar = 10 mm.
F<sc>ig</sc>. 9.
Fig. 9.
Pollination systems in Iridaceae. Beetle pollination. Anisonyx ursus on Moraea villosa (top row, left); Clania macgregorii on Romulea monadelpha (top row, right). Short-proboscid fly pollination. Muscid fly on Moraea ochroleuca (middle row, left); Muscid fly on Ferraria densepunctulata (middle row, right). Generalist pollination. Belenois aurata (Pieridae) on Micranthus junceus (bottom row, left); Cynthia cardui (Nymphalidae) on Nivenia parviflora (bottom row, centre). Polistes sp. (Vespidae) on Moraea inconspicua (bottom row, right).
F<sc>ig</sc>. 10.
Fig. 10.
Relationship between number of species and number of pollination systems per genus in ancestrally actinomorphic (open circles, broken curve) and ancestrally zygomorphic (closed circles, solid curve) genera of African Iridaceae. (A) Untransformed data; (B) logarithmically transformed data, with the two curves tested for between-group effects using the general linear model (F = 92·135, P < 0·001). A, Aristea; B, Babiana; Ch, Chasmanthe; Cr, Crocosmia; D, Duthiastrum; Fe, Ferraria; Fr, Freesia; Ge, Geissorhiza; Gl, Gladiolus; H, Hesperantha; I, Ixia; K, Klattia; L, Lapeirousia; Me, Melaspherula; Mi, Micranthus; Mo, Moraea; N, Nivenia; P, Pillansia; Ra, Radinosiphon; Ro, Romulea; Sa, Savannosiphon; Sp, Sparaxis; Th, Thereianthus; Tr, Tritonia; Ts, Tritoniopsis; Wa, Watsonia; Wi, Witsenia; X, Xenoscapa.

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