Pollination Biology of Lapeirousia subgenus Lapeirousia (Iridaceae) in southern Africa; floral divergence and adaptation for long-tongued fly-pollination Abstract | Materials and Methods | Results | Discussion | Literature RESULTS Inflorescence Architecture Most species of subgenus Lapeirousia have a simple or branched flowering stem, and each axis terminates in a spike of several to many flowers. In L. oreogena, L. montana, L. plicata, and L. odoratissima the inflorescence is a congested tuft of flowers borne at ground level. The number of flowers per plant varies considerably from year to year. Vigorous plants have as many as five spikes each and up to 20 flowers per tuft or spike. Floral Phenology and Life Span Flowering in southern African species of subgenus Lapeirousia in the study area ranges from late May until early November Figure 1. Populations of each species bloom for two to four weeks. Exact timing of flowering within a species varies seasonally, and to some extent locally, depending on elevation and aspect. The higher the elevation the later a population comes into bloom. Despite considerable overlap in flowering times Figure 1, species may be characterized generally as early (June to mid August), mid (late August and September), or late season (October and November) bloomers. The pattern of flower buds opening on an inflorescence is acropetal. In all species the perianth of a mature bud expands in the early to mid­morning. The rate at which buds open and the longevity of the expanded perianth are dependent on ambient temperatures. The perianth of an open flower lives a maximum of five days if daily temperatures remain below 20°C and soils remain wet. At sunset the tepals of most species contract, partly or sometimes completely enclosing the exserted anthers and stigmas. In L. exilis, tropical African L. odoratissima, and L. pyramidalis (both subspecies) the tepals remain open all night. The anthers of all species dehisce longitudinally within two to four hours after the tepals unfold. Pollen remains in the open thecae until contacted by insects or washed out by rain. The three stylar lobes do not normally expand to expose the receptive stigmas until the day after the anthers have dehisced. This suggests that all the species studied are weakly protandrous. Floral Morphology Figure 2 In most species of subgenus Lapeirousia the perianth tube is cylindric. In L. divaricata and L. spinosa, however, the tube is funnel-shaped Figure 2H. In sixteen species the perianth tube always exceeds 17 mm in length, with a maximum of 76 mm in L. anceps (Table 5). In L. divaricata, L. spinosa and L. tenuis the tube is less than 16 mm long. In L. exilis, L. montana, and L. plicata, however, the external length of the tube is misleading: the lower half of the tube is occluded by the style and intrusive ridges, decurrent on the filaments Figure 2K, so that the nectar is forced into the upper part of the tube. Functional tube length, in terms of accessibility of nectar to insects, is less than half what it appears to be (Table 5). Tube length is unusually variable in L. anceps, and may be as little as 20-30 mm in populations in the south of its range, and 45-76 mm in the west and north. Seventeen species have a zygomorphic flower and unilateral, arcuate stamens and style (Table 5, Figure 2A, E, H). In contrast L. oreogena, L. montana, L. plicata, and L. odoratissima have actinomorphic flowers Figure 2J, K in which the stamens and style are symmetricallybdisposed. Tepals of the fully open flower either spread horizontally and are thus patent, or the dorsal (adaxial) tepal is erect (Lapeirousia silenoides, L. pyramidalis, L. verecunda), or inclined over the stamens (L. divaricata, L. spinosa). In species with zygomorphic flowers the dorsal tepal is broader and sometimes longer than the five other tepals. Lapeirousia fabricii and L. barklyi are the only species in which the tepals are broadly cupped below and patent above, and thus include the filaments. In several species with zygomorphic flowers (e.g., L. divaricata, L. fabricii - Figure 2H), each of the three lower tepals bears a raised ridge or narrow tooth. These appendages are absent in species with actinomorphic flowers. In all species the stamens are equal in size and the filaments are erect, or sometimes slightly inclined. In zygomorphic­flowered species the anthers are parallel and face the center of the flower and the lower tepals and nectar guides, but in species with actinomorphic flowers the anthers are symmetrically disposed and face outward Figure 2J, K. The style branches of all species of subgenus Lapeirousia included in the study are divided for half their length. Although this is a generic characteristic, the style branches may be undivided in some species or populations of the genus (Goldblatt, 1972, 1990). The resulting six stylar arms, which spread outward and recurve, bear receptive stigmatic hairs that appear to be dry when observed under a 10x hand lens. The style arms are normally held between 1 and 3 mm above the anther apices, but in L. arenicola, L. jacquinii, L. simulans, and L. violacea the style arms become tangled in the anthers as the style lobes expand. Compatibility and Fruit Set We were unable to make a thorough study of compatibility in subgenus Lapeirousia, but present the following observations. In L. arenicola, L. jacquinii, L. simulans, and L. violacea, stems cut at bud stage, maintained in water, and excluded from insects for two weeks routinely set full capsules containing the normal number of seeds for that species. Furthermore, L. jacquinii and L. oreogena have been noted to set seed in greenhouses where insect activity was excluded. Lapeirousia barklyi, L. dolomitica subsp. dolomitica, L. pyramidalis, L. silenoides, and L. spinosa, did not set fruit when inflorescences were maintained in water as in the species above. In these taxa dehisced anthers and stigmatic surfaces are in contact in both field populations and laboratory specimens. Lapeirousia silenoides and L. pyramidalis subsp. regalis, in which the anthers and stigmas are not in contact, do not set fruit even when self-pollinated by hand either maintained in water or grown in pots. In field populations of L. dolomitica, L. pyramidalis, and L. silenoides individual plants were often observed to produce none, or only one or two mature capsules per spike after flowering. Floral Presentation, Attractants and Rewards Field observations of species of subgenus Lapeirousia indicate that they can be divided into three morphological types based on floral chracteristics (Tables 3, 4, 5), and that each of the floral types is associated with a different suite of pollinators. The three flower types are defined primarily by floral pigmentation and patterning in combination with perianth tube length. However, regardless of flower type, in zygomorphic flowers visible nectar guides are always confined to the three lower tepals Figure 2. In all species nectar is secreted at the base of the floral tube in volumes ranging from 20 to 76 ml (only 10-12 ml in L. divaricata and L. spinosa) (Table 4). In L. exilis, L. montana and L. plicata occlusion of the basal part of the tube results in the nectar being forced into the upper half. 1. The L. silenoides-type Figure 2A: tepal pigmentation dark blue to purple or dark red, darker than the nectar guides; visible nectar guides yellow to white streaks or blotches near the tepal bases and sometimes a zone of intense pigmentation in the center of each lower tepal; callus ridges absent; no scent discernable to the human nose except in L. dolomitica subsp. dolomitica, which has a faint sweet odor; floral tubes 33-70 mm long; flowers actinomorphic or zygomorphic; nectar sucrose rich to sucrose dominant. 2. The L. fabricii-type Figure 2E: tepal pigmentation white to cream or pale pink (but usually pink to red on the reverse), lighter than the nectar guides; visible nectar guides dark red to maroon oblong to acute patterns at the tepal bases; callus ridges usually present; no scent discernable to the human nose; floral tubes normally 30-76 mm long; flowers zygomorphic; nectar sucrose dominant or, in L. macrospatha, hexose rich. 3. The L. divaricata-type Figure 2H: tepal pigmentation white to cream or pale blue, lilac, or pink; visible nectar guides usually narrow to streaky, light purple sometimes grading to a yellow to cream-colored ridge at the base of the tepals or merely a white zone in the center of the flower (L. montana); scents present and variable, ranging from a cloyingly sweet heavy fragrance (L. exilis, L. pyramidalis subsp. pyramidalis) to a lightly sweet to mildly spicy scent reminiscent of Dianthus or Narcissus; callus ridges well-developed in L. divaricata, L. spinosa, rare and inconspicuous in L. pyramidalis subsp. pyramidalis; floral tubes never exceeding 55 mm, in 3 of the 5 species tubes less than 30 mm (functional tube length always less than 35 mm); flowers actinomorphic or zygomorphic; nectar usually sucrose dominant, or sucrose rich (L. montana), or hexose rich (L. barklyi). Pollination Mechanisms The three modes of floral presentation are accompanied by three different pollinator guilds. However, all floral foragers collected on Lapeirousia species had two foraging characters in common. First, pollen load analysis (Table 2) and observations of flight patterns indicate that all insects observed on Lapeirousia Figure 2, 3 forage actively on the flowers of some other co-blooming plants (Table 2). Second, no matter how elongated the mouth parts of the pollinator are, they are always somewhat shorter than the perianth tube (Table 5). In addition, an insect was rarely observed to probe anthers with its proboscis or actively collect pollen on any Lapeirousia species. 1. The Lapeirousia silenoides group. Nectar foraging in this flower type was dominated by long-tongued flies of the genus Prosoeca (Nemestrinidae) Figures 3A-B, 4A. Prosoeca peringueyi was observed foraging on the flowers of all species in this group (Tables 2, 5) excluding L. oreogena. Lapeirousia oreogena was visited by Prosoeca sp. nov. Figure 3B, and this fly species also visited L. jacquinii at two sites on the Nieuwoudtville Plateau (where P. peringueyi evidently does not occur). In both species of flies the insects hover while orienting and inserting their proboscis into the tube. When the proboscis has been fully inserted into a tube that is long enough to permit this, the insect grasps the tepals with its legs during the actual feeding process, but the wings remain in motion. By flexing the tibiae of the hind legs forward the fly can use all three pairs of legs for grasping, and this is done in plants with both vertical and horizontal flower presentation. In flowers with short tubes that are visited for nectar, the body does not contact the stamens or stigmas so that pollination is not effected, and the fly hovers without grasping the tepals. Prosoeca species are active on mild to warm days from mid­morning to early afternoon, and again in the late afternoon. These flies remain at each Lapeirousia flower for 3-5 seconds, and pollen adheres to the frons and thorax in L. oreogena and on the dorsum and upper frons in other species. Often pollen depositions are so heavy they are visible to the naked eye. In species with zygomorphic flowers, the fly always orients itself in the same way, approaching the flower from the front, thus facing the anthers as it forages. Density of visitors varies considerably, ranging from four to five flies present locally at the same time, or as few as one or two flies at sites over periods as long as an hour. At one site, the top of Botterkloof Pass, where L. jacquinii and L. violacea co-occur, individuals of P. peringueyi were observed to visit both species indiscriminately. Prosoeca species typically interrupted foraging on Lapeirousia species to collect nectar on other species growing nearby, including Pelargonium species (Geraniaceae), and taxa of Iridaceae including Babiana species, Sparaxis variegata subsp. metelerkampiae (L. Bolus) Goldblatt, Xenoscapa uliginosa Goldblatt & Manning, Hesperantha latifolia (Klatt) de Vos, and Geissorhiza kamiesmontana Goldblatt. Interestingly, the flowers of Pelargonium sericifolium van der Walt do not secrete nectar although they have long floral tubes and may mimic flowers of species that do produce nectar Figure 2, suggesting pollination by deceit, a phenomenon best known in Orchidaceae. Pollen deposition tends to be on the head and back part of the thorax (nototribic) in Lapeirousia except L. oreogena, but on the underside (sternotribic) in Pelargonium, a factor that reduces contamination of pollen loads and competition for vector sites on the insects' bodies. 2. The L. fabricii group. Nectar foraging in this group was limited to one species of fly in the Nemestrinidae (Moegistorhynchus longirostris - Figure 4B and one species of fly of the family Tabanidae (Philoliche gulosa - Figure 4C). Both fly taxa are long-tongued and have mouth parts as long as or longer than the Prosoeca species discussed above. Moegistorhynchus longirostris was observed actively foraging on L. fabricii only in the late afternoon, 4:00­6:00 PM, at one study site in northern Namaqualand. The same fly species was recorded visiting L. anceps at the study site near Ysterfontein during the late morning on a cool and cloudy day. Philoliche gulosa visited Lapeirousia fabricii at three sites between 11 AM and 3 PM. The foraging behavior of Moegistorhynchus longirostris and P. gulosa on Lapeirousia species was similar to the foraging behavior of Prosoeca species. Nemestrinid species fly with their mouth parts hanging downward, and forage for nectar by extending the fairly flexible proboscis either forward or downward depending on the characteristics of a particular flower. Philoliche gulosa flies with its proboscis extended forward, and its proboscis appears to be less flexible (S. Johnson, pers. comm.). Moegistorhynchus longirostris interrupted its foraging on Lapeirousia species to forage on the flowers of Pelargonium species, and species of two other Iridaceae, Geissorhiza exscapa (Thunb.) Goldblatt and Babiana tubulosa (Burm. f.) Ker-Gawl. We assume that B. brachystachys (Bak.) G. Lewis, Ixia paniculata Delaroche, Tritonia crispa (L. f.) Ker-Gawl., Geissorhiza confusa Goldblatt, and Gladiolus angustus L. (all Iridaceae) also belong to this guild, because their flowers are similarly constructed and colored. Moegistorhynchus was also observed attempting to forage on the spurred but nectarless terrestrial orchid, Disa draconis (L. f.) Sw. The foraging of the fly on the orchid suggests another example of pollination by deceit, as the orchid produces creamy white flowers with narrow purple nectar guides, similar to floral presentation in L. anceps. 3. The L. divaricata group. Species in this group were visited by various combinations of Lepidoptera, bees, and bombyliid flies (Table 2). Lapeirousia exilis and L. plicata appear to be pollinated by a combination of bombyliid flies and Hymenoptera, including the native Apis mellifera Apidae: Figure 3C and Tetraloniella karooensis (Anthophoridae). These insects were observed to contact anthers and stigmas while foraging, and pollen was brushed onto their bodies passively. All of the insects collected on flowers in this group have mouth parts shorter than Philoliche gulosa and the three taxa of nemestrinid flies (Table 5). Bees were active throughout most of the day, but were observed most frequently during the cooler periods before 11 AM or after 4 PM. The noctuid moth, Heliothis armigera Figure 3D, was observed in large numbers foraging on L. divaricata at two sites between 3.30 and 6 PM. Bombyliid flies, bees, H. armigera, and the butterfly, Cynthia cardui (Nymphalidae), did not usually forage by hovering. In zygomorphic flowers these insects always perched on the lower tepals before foraging for nectar. The only insect observed to feed while hovering was the sphinx moth, Hippotion celerio (L.), which was seen, but not captured in a population of Lapeirousia pyramidalis subsp. pyramidalis near de Wet (Worcester District). Pollen load analyses (Table 2) indicate that H. armigera and Cynthia cardui may be poor vectors of pollen compared to bees. All bees collected on the Lapeirousia divaricata group belonged to long-tongued families. With the exception of two specimens of Hoplitis similis (Megachilidae) and one specimen of Parafidelia (Fideliidae), bees collected on the L. divaricata group belong in the families Anthophoridae and Apidae. Two anthophorid bee individuals collected (Anthophora diversipes and Amegilla grisella) were males, and the remainder, female. Analyses of pollen washes of the hairs on the hind legs and ventral abdominal region show two characteristics. First, all female bees collected on the L. divaricata group are polylectic and polytrophic. Field observations as well as pollen-load analyses showed that these bees collected pollen actively on nectarless flowers including Cyanella alba L.f. (Tecophilaeaceae) and Hermannia sp. (Sterculiaceae). Hoplitis similis, collected on L. spinosa, interrupted its visits to this species to forage on similarly pigmented Moraea tortilis Goldblatt, the flower of which is also a meranthium of the gullet type "blossoms" (see discussion), similar to that of Iris. The flowers of M. tortilis produce small quantities of nectar. Pollen-load analyses showed that all bees foraged on a much broader selection of taxa than were recorded for fly or moth specimens. Although female bees do not collect pollen actively on Lapeirousia flowers, the pollen deposited passively on the bee's head and thorax is combed off by the bee and deposited in the scopae. Bee activity in species of the L. divaricata group differed during the season. Apis mellifera was collected most frequently in July and early August while the first anthophorids were not observed and netted until mid August. << BACK | TOP | NEXT >>