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Hopliine Beetle Pollination in Annual Wahlenbergia Species (Campanulaceae) from Western South Africa, and the New Species W

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Hopliine Beetle Pollination in Annual Wahlenbergia Species (Campanulaceae) from Western South Africa, and the New Species W South African Journal of Botany 100 (2015) 58–62 Contents lists available at ScienceDirect South African Journal of Botany journal homepage: www.elsevier.com/locate/sajb Hopliine beetle pollination in annual Wahlenbergia species (Campanulaceae) from western South Africa, and the new species W. melanops J.C. Manning a,c,⁎, P. Goldblatt b,c,J.F.Colvilled,e,C.N.Cupidoa,f a Compton Herbarium, South African National Biodiversity Institute, Private Bag X7, Claremont 7735, South Africa b B.A. Krukoff Curator of African Botany, Missouri Botanical Garden, P.O. Box 299, St. Louis, MO 63166, USA. c Research Centre for Plant Growth and Development, School of Life Sciences, University of KwaZulu-Natal, Pietermaritzburg, Private Bag X01, Scottsville 3209, South Africa d Kirstenbosch Research Centre, South African National Biodiversity Institute, Private Bag X7, Claremont 7735, South Africa e Statistics in Ecology, Environment and Conservation, Department of Statistical Sciences, University of Cape Town, Rondebosch 7701, South Africa. f Department of Biodiversity and Conservation Biology 7535, University of the Western Cape, Private Bag X17, Bellville, South Africa article info abstract Article history: Field exploration in western South Africa over the past 10 years has revealed the existence of an unnamed annual Received 20 January 2015 species of Wahlenbergia Schrad. ex Roth that we describe here as W. melanops Goldblatt and J. C. Manning for the Received in revised form 13 April 2015 dark grey center of the flower. Plants have alternate leaves scattered along the stem and are otherwise distinguished Accepted 27 April 2015 in part by narrow calyx lobes and the presence of stylar glands at the base of the stigma lobes. Flowers of Available online 7 June 2015 W. androsacea, W. capensis,andW. melanops conform to a specialized hopliine pollination system and we present fi Edited by GV Goodman-Cron observations documenting hopliine pollination for these three species. This now con rms a third pollination system in western South African Wahlenbergia species that includes one other specialized pollination system utilizing Keywords: masarine (pollen) wasps and another possibly more generalist system using melittid bees. W. annuliformis Brehmer New species is treated as a synonym of W. androsacea A. DC. Nomenclature © 2015 SAAB. Published by Elsevier B.V. All rights reserved. Pollination biology Taxonomy 1. Introduction Cape has since been described by Cupido (2011). Although the taxono- my of the genus in southern Africa is much in need of revision, a prelim- The genus Wahlenbergia Schrad. ex Roth (Campanulaceae), with inary list of species recognized from the Cape Floristic Region was some 260 species listed (Lammers, 2007), is by far the largest genus in provided by Manning and Goldblatt (2012). This list includes just a the family in the southern Hemisphere. Essentially pan-austral in distri- half-dozen annual species with three to five locules and stigma lobes. bution, it includes minor incursions into the Mediterranean region, Campanulaceae are characterized by a secondary pollination presen- Macaronesia, Arabia, and SE Asia. tation system involving transfer of pollen from the anthers to the present- Over 180 species are currently recorded from southern Africa er region of the immature style, where it is held in place by special hairs. (Germishuizen and Meyer, 2003), with some 65 species in the Cape Flo- This takes place in bud before the perianth expands. At expansion of the ristic Region (Manning and Goldblatt, 2012). Recent phylogenetic anal- perianth, the flower is said to be in the male phase and the stigma lobes yses of DNA sequence data confirm that the genus is not monophyletic are not displayed and are not receptive. When most pollen is removed as currently circumscribed (Cupido et al., 2013; Prebble et al., 2011)but from the presenter region, the flower enters the female phase and the an alternative classification has yet to be proposed. stigma lobes open and become receptive. The nectar at the base of the co- Wahlenbergia is distinguished from related genera by a more or less rolla is covered by the accrescent bases of the stamens, which form a inferior ovary and mostly turbinate to subglobose capsules that dehisce dome-like structure, and nectar can only be accessed by insects strong regularly through three to five terminal valves (Manning and Goldblatt, enough to force the filament bases apart. 2012). The African species were last comprehensively revised by von Campanulaceae appear to be predominantly adapted to pollination Brehmer (1915), with more recent regional or partial revisions by by bees, with many species evidently specialized for pollination by sol- Adamson (1955) and Thulin (1975). One new species from Western itary bees (Gess, 1996, 1999; Welsford and Johnson, 2012). This is likely to be true in Wahlenbergia, in which most species have unmarked, pale fl ⁎ Corresponding author. to deep blue owers, sometimes with small dark markings around the E-mail address: [email protected] (J.C. Manning). edge of the floral cup. In only two species, W. capensis and the new http://dx.doi.org/10.1016/j.sajb.2015.04.014 0254-6299/© 2015 SAAB. Published by Elsevier B.V. All rights reserved. J.C. Manning et al. / South African Journal of Botany 100 (2015) 58–62 59 W. melanops,dotheflowers have prominent dark markings that are Beetles were hand-collected and killed by freezing or in 80% ethanol consistent with ‘beetle-flowers.’ before pinning. Voucher specimens are housed in the Kirstenbosch Re- Although barely known in southern Africa until the late twentieth century, search Centre. specialization for hopliine beetle (Scarabaeidae:Melolonthinae:Hopliini) pollination has now been documented in well over 70 species in several plant families, primarily in the Greater Cape Floristic Region (Goldblatt 3. Results and Manning, 2011), the center of diversity for the hopliines (Colville et al., 2014). Typical floral adaptations to hopliine pollination include 3.1. Taxonomy shallow or open flowers with relatively large, dark markings (beetle marks). Among Campanulaceae, only a few species of Wahlenbergia Wahlenbergia melanops Goldblatt and J. C. Manning, sp. nov. Type: were identified by Goldblatt and Manning (2011) in their review of South Africa, Western Cape, 3118 (Vanrhynsdorp): sandveld east of the system as potential members of this pollination guild, notably Doringbaai at Farm Kliphoek, 61 m, (–CD), 11 Oct. 2013, Goldblatt & Por- W. capensis (L.) DC. plus a second, as yet unnamed species that we ter 13997 (NBG, holo.; K, MO, PRE, iso.). describe here. Annual from slender taproot, to 600 mm high. Stem branching from This distinctive annual species with three locular ovaries, which base and above, sparsely scabrid-papillose. Leaves alternate, ±narrowly we describe as Wahlenbergia melanops Goldblatt and J. C. Manning, elliptic, 30–90 × 3–9 mm, margins shallowly toothed to lightly dentate, is a narrow endemic of the Atlantic coast east of Doringbaai. It is sparsely ciliate at base, upper leaves becoming scale-like. Inflorescence one of just two species of Wahlenbergia with shallow flowers with lax, pedicels 30–70 mm long, smooth. Flowers blue-mauve with conspic- a dark central eye. This distinctive floral morphology is part of the uous grey cup edged with white. Hypanthium obconic, ± 2 mm long, 10- syndrome associated with a specialized pollination system utilizing nerved. Calyx lobes narrowly triangular, 3–4 mm long, ascending, tips hopliine beetles. slightly recurved, enlarging to 5 mm in fruit. Corolla up to 24 mm long Atthetypelocality,theflowers of Wahlenbergia melanops were visit- (much shorter late in season), lobes united below for 2.5–3.0 mm in ed by two species of hopliine beetle, Peritrichia pseudopistrinaria Schein shallow, basin-like cup, cup densely puberulous. Stamens 5, filaments ± and Lepithrix longitarsis Schein, individuals of which were present on nu- 1.5 mm long at dehiscence, bases deltoid, ± 1 mm long, orange with merous open flowers. Hopliine pollination has been documented in only black flecks, ciliate on margins, filiform distally for 0.5 mm, bases enlarg- asinglespeciesofWahlenbergia, W. capensis (Goldblattetal.,1998;see ing after dehiscence and to 2 mm long at anthesis and then conspicuously also Picker and Midgley, 1996; Gess and Gess, 2010) although it is likely lobed at base with upper part of filament recurved and thickened; anthers in a few other species as well. Here we present observations on hopliine linear, 2 mm long, Ovary inferior, 3-locular; style ± slender throughout, pollination in W. capensis and W. annularis A. DC., the last also visited by ± 4 mm long, hirsute in upper half, with 3 transverse glands alternating worker honey bees carrying Wahlenbergia-type pollen. with stigma lobes; stigma lobes ± ovate, ± 1.7 × 1.2 mm, obtuse, spread- ing horizontally, upper surface papillate. Capsules obconic, 7–9mmlong, ± 6 wide at apex, domed in center, glabrous. seeds ellipsoid, smooth, 2. Materials and methods 0.6–0.8 mm long. Flowering time September to mid October (Fig.1). Distribution and ecology: Wahlenbergia melanops has been collected The new species was described and illustrated from living plants col- several times over the past 50 years but all collections are from essen- lected in the wild. No additional herbarium material was located at BOL, tially the same locality, and it is evidently restricted to the crest of the NBG, or SAM. Several plants were collected and pressed for documenta- ridge inland of Doringbaai on the Atlantic coast of Western Cape and tion, and duplicate specimens have been distributed to multiple south of Vredendal (Fig. 2), where it occurs on sandy flats and gentle herbaria as listed below. sandstone slopes. Population sizes vary from season to season and we Pollinator observations were made on plants in the field at four dif- have seen hundreds of plants along the road verges and inside farm ferent localities along the west coast of Western Cape, South Africa fences in some seasons but in dry years we struggled to find more (Table 1).
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