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

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South African Journal of Botany

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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 taxonomy 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

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). Observer data for the four localities are: 1. Leipodtville: two than 25 plants. observers on warm days over the period 11:00 to 13:00 (Sep 2012) The species has not been collected from any additional localities in and 10:30 to 12:00 (Sep 2013) scanned over 100 plants in flower for vis- more than a century and is thus evidently a highly localized endemic. iting insects, and sampled beetles from ± 50 plants; 2. Doringbaai: two Conservation notes: The species is known from a single ridge in a re- observers on warm days over the period 10:30 to 12:30 (Oct 2008) and gion that has been highly transformed by agriculture. Grazing by cattle 11:30 to 13:30 (Sep 2013) scanned ± 60 plants in flower for visiting in- and sheep on farms along the ridge and agriculture have already nega- sects, and sampled beetles from ± 20 plants; 3. Aurora: two observers tively affected the population and will likely continue to do so. on a warm day over the period 12:00 to 14:00 scanned ± 20 plants in Diagnosis: Wahlenbergia melanops is an annual with alternate leaves flower, all with beetles; 4. Orange Kloof: three observers on a warm not clustered basally in a rosette and 5-merous flowers with a glabrous, day over the period 09:30 to 12:30 scanned ± 50 plants in flower for 3-locular ovary and three broad stigma lobes, each bearing a gland at visiting insects, and sampled beetles from ± 15 plants. the base. The blue-mauve flowers are shallowly bowl-shaped with a

Table 1 Study sites, all in Western Cape, with pollinator and host plant information (less frequent hopliine visitors in parentheses). P. (Peritrichia), L. (Lepithrix), W. (Wahlenbergia). Plant vouchers deposited at MO and NBG).

Study site Hopliine species Plant host with voucher data

1. Leipoldtville (32°13.39S 18°28.713E); sandy ground; P. pseudopistrinaria (L. longitarsis, Pachynema crassipes) W. androsacea (Goldblatt & Porter 13983). Sep 2012, Sep 2013 2. Doringbaai, Farm Kliphoek (31°45.61S 18°20.91E); P. pseudopistrinaria, L. longitarsis W. melanops (Goldblatt & Porter 13997). sandveld; Oct 2008, Sep 2013 3. 1.5 km N of Aurora (32°41.58S 18°28.93E); rocky P. pseudopistrinaria (L. lineata) W. capensis (Goldblatt & Porter s.n., no voucher) sandy slope; Sept. 2012; Sep 2013 4. Cape Peninsula, Orange Kloof (34° 00'24.83S 18°24'05.10E), P. bipilosa sp. nov. W. capensis (Colville s.n., no voucher) 267 m; fynbos; 16 Nov 2013 60 J.C. Manning et al. / South African Journal of Botany 100 (2015) 58–62

conspicuous grey cup, and the slender calyx lobes enlarge from 3 mm long in the open flower to 5 mm in fruit. The mature capsules are glabrous, 7–9 mm long and ± twice as long as wide. Wahlenbergia melanops is a distinctive species that might only be confused with W. capensis and collections of the species (Hall 3182, Van Breda 1270) were generally referred to that species. The two species share an annual habit, cauline foliage, similar open, mauve-blue flowers with a large grey eye but W. capensis is unique in the genus in its hispid, 5-locular ovary with five enlarged stigma lobes fertile only along the margins. W. capensis was segregated by von Brehmer (1915) as the monotypic sect. Capenses Brehmer but phylogenetic analyses by Prebble et al. (2011) and Cupido et al. (2013) place it as sister to W. cernua (Thunb.) A.DC. (sect. Cernuae Brehmer). Other annual species with relatively large bowl-shaped flowers, such as W. androsacea A.DC. and W. annularis A.DC., have the leaves clustered at the base of the stems and flowers either unmarked or with a ring of small markings around the edge of the cup. The species appears to have been first collected by Carl Zeyher, some- time in the first half of the nineteenth century [Zeyher s.n. (SAM)]. This collection was misidentified as W. arenaria A. DC., now treated as a synonym of W. androsacea A. DC., and was evidently overlooked by von Brehmer (1915) in his revision of the genus. The immediate relationships of W. melanops are difficult to assess and it does not key to section satisfactorily in Brehmer's monograph of the African species (von Brehmer, 1915). We initially keyed W. melanops to sect. Dichotomae Brehmer on the basis of its oblanceolate, alternate leaves, pedunculate flowers, and 5-locular ovary with well-developed stylar glands but it does not have the slender, elongate stigma lobes of the other species in the section. Alternatively, W. melanops keys to the Fig. 1. Wahlenbergia melanops. A. Flowering stem; B. calyx; C. single detached stamen; monotypic sect. Annuliformes Brehmer, defined by three transverse D. filament at time of anther dehiscence in bud; E. filament after flower has expanded; glands forming an almost a complete ring at the base of the stigma and F. style and stigma showing ring of three stylar glands at base of stigma lobes; H, capsule. short stigma lobes. The only species in the section, W. annuliformis Scale bars: A, G. 10 mm; B, 2.5 mm; C. 2 mm; D, E, 1 mm; F, 4 mm; H. 2.5 mm.

Fig. 2. Distribution of Wahlenbergia melanops. J.C. Manning et al. / South African Journal of Botany 100 (2015) 58–62 61

Brehmer, has white to pale blue petals with a white throat, and is said to have sparsely hairy capsules.

3.1.1. Additional specimens SouthAfrica,WesternCape,3118 (Vanrhynsdorp):roadfromLam- berts Bay to Vredendal, red sand dunes, (–CD), 2 Sept. 1961, Van Breda 1270 (PRE); Farm Kliphoek, 12 km inland from Doringbaai, (–CD), 29 Aug. 1970, Hall 3798 (NBG, PRE); 6 Sept. 1970, Hall 3812 (PRE); 11 Sept. 2008, Goldblatt & Porter 13107 (MO, NBG, PRE); 13 Sept. 2008. Cupido 371 (NBG); east of Vredendal, Fonteintjie, 15 km SE of Doringbaai, (–CD), 25 Aug. 2006, Helme 4292 (NBG). Without precise locality: In region trans Olifantsrivier, Zeyher SAM40417 (SAM).

3.2. Nomenclature of Wahlenbergia annuliformis

We have located and examined one of the two syntypes cited for W. annuliformis (von Brehmer, 1915), viz. Bachmann 1729 (Z). This collection closely matches W. androsacea (sect. Rosulatae Brehmer) in the subrosulate, narrowly oblanceolate leaves, sparsely branched stems, bowl-shaped corolla of comparable size, and three broad stigma lobes with prominent stylar glands at the base. The essential difference between sects. Annuliformes and Rosulatae thus resides in whether the Fig. 3. Hopliine pollination in Wahlenbergia. A. Pollination of W. capensis by male glands form an annular collar around the style (sect. Annuliformes)or Peritrichia bipilosa sp. nov. (Dombrow, in prep.) (body length = 7.24 mm) at Orange remain as three discrete glands (sect. Rosulatae) (sect. Rosulatae). We Kloof (Photo: Annalie Melin). B. Pollination of W. capensis by two male Dicranocnemus have examined numerous specimens of both W. annularis and sulcicollis (body length = 5.10 mm) at Rondevlei on the Cape Peninsula (Photo: Sarah- fi Leigh Hutchinson). C. Pollination of W. annularis by male Peritrichia pseudopistrinaria W. androsacea and nd all grades from a ring of three discrete stigma (body length = 7.59 mm), near Leipoldtville, on the west coast (Photo: Lendon Porter). glands to a more or less continuous annulus (see also Manning and D. Pollination of W. capensis by female Lepithrix lineata Fabricius (brown beetle, left: Goldblatt, 2012). We therefore place W. annuliformis in synonymy body length = 9.38 mm) and female P. pseudopistrinaria (grey beetle, right; body under W. androsacea. length = 7.42 mm) near Aurora, on the west coast (Photo: Lendon Porter). Wahlenbergia androsacea A. DC., Monogr. Camp.: 150, t. 19, f. I. Wahlenbergia annuliformis Brehmer in Bot. Jahrb. 53: 118 (1915), We have also observed and captured hopliines on Wahlenbergia ‘ fi ’ syn. nov. Type: South Africa, [Western Cape], umgegend von Hope eld , annularis at Leipoldtville (Goldblatt and Porter 13983)(Fig. 3C), notably Oct. 1885, Bachmann 1729 (Z, lecto.!, designated here). [Paratype: South Peritrichia pseudopistrinaria but also individuals of Lepithrix longitarsis ‘ ’ Africa, [Western Cape], Troe Troe , Oct. 1883, Bachmann 343 (not and Pachynema crassipes Fabricius. The beetles behaved as described by located)] Goldblatt et al. (1998), using the flowers as a platform to assemble, en- gage in agonistic behavior and copulation, and not infrequently flying 3.3. Hopliine pollination in Wahlenbergia from flowers of one plant to another. Their behavior, matched in hopliines visiting W. melanops flowers, results in their becoming visibly covered in The observations on hopliine pollination in the shrubby pollen which they passively transport to other flowers. The flowers of Prismatocarpus pedunculatus (P.J.Bergius) A. DC. and the annual W. annularis are moderately sized, 15–20 mm in diameter, and pale Wahlenbergia capensis by Goldblatt et al. (1998) evidently constitute blue with dark longitudinal marks or streaks around the edge of the the first report of this pollination strategy in the family but since then bowl. We also recorded visits to flowers of W. annularis (but never to we have regularly noted hopliines on W. capensis (see also Gess and those of W. melanops) by worker honey bees which collected pollen but Gess, 2010). More recently, hopliine pollination was also reported also acquired dorsal deposits of Wahlenbergia pollen. Gess (1996) noted for Roella ciliata L. by Cupido and Nelson (2012). honeybeesasopportunistic visitors of several Wahlenbergia species and Our observations on hopliine pollination in annual Wahlenbergia considered them as unreliable pollinators. This was not supported by ob- species confirm the association of this pollination system with dark flo- servations on two Wahlenbergia species in the KwaZulu-Natal Drakens- ral markings documented by Van Kleunen et al. (2007). The unique, berg, in which solitary halictid bees and social honey bees were large grey stigma lobes in Wahlenbergia capensis appear to mimic the frequent and effective pollinators (Welsford and Johnson, 2012). color and texture of visiting hopliine species, suggesting co-adaptation We observed that the beetles landed on the flower and then imme- between plant and pollinators in this species. Beetle species recorded diately crawled to the base of the style with their heads downward, visiting W. capensis include Peritrichia pseudursa Schein (Gess and sometimes proceeding to move around the base of the style. This sug- Gess, 2010), to which we now add observations of visits by P. bipilosa gests to us that the beetles were feeding on the nectar held at the base sp. nov. (Dombrow, in prep.) and Dicranocnemus sulcicollis Wiedem., of the style but we are unable to confirm this. We saw no evidence of de- from the Cape Peninsula (Fig. 3A, see also Fig. 3B), and by Lepithrix structive feeding by the beetles, nor were they observed to feed on the lineata Fabricius and P. pseudopistrinaria (Fig. 3D) near Aurora pollen during the male phase of the flowers. (Table 1). These beetles were observed carrying a dense covering of Two pollination systems were documented among southwestern the grey-blue pollen of W. capensis, which adheres to the hairs on the Cape Wahlenbergia species by Gess (1996). Species with deeply cam- beetle’s prothorax and elytra during feeding and mating. Species of panulate flowers, including W. paniculata A.DC., were pollinated by Peritrichia and Lepithrix are typically attracted to blue and white flowers, masarine wasps (Vespidae: Celonites)(Gess, 1996), and those with shal- where they have been observed to feed on pollen and nectar (Picker and lowly campanulate flowers, e.g., W. annularis and W. namaquana Sond., Midgely, 1996). Examination of gut contents and mouthpart morpholo- were visited by as many as 19 species of bees and wasps but pollinated gy has confirmed the feeding preferences of these species for pollen and primarily by melittid bees (Melittidae: Capicola). We conclude that the nectar (Hansal, 2014; Johnson and Nicolson, 2001). pollination strategy of W. capensis and W. melanops represents a third 62 J.C. Manning et al. / South African Journal of Botany 100 (2015) 58–62 pollination type that conforms to the specialized hopliine system in Germishuizen, G., Meyer, N.L., 2003. 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