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190 Shifts Between Pollinators Are Often Associated with Evolution- Ary American Journal of Botany 101(1): 190–200. 2014. S HIFT FROM BIRD TO BUTTERFLY POLLINATION IN C LIVIA (AMARYLLIDACEAE) 1 I AN K IEPIEL AND S TEVEN D. JOHNSON 2 School of Life Sciences, University of KwaZulu-Natal, P Bag X01, Scottsville, Pietermaritzburg, 3209, South Africa • Premise of the study: Pollinator shifts have been implicated as a driver of divergence in angiosperms. We tested the hypothesis that there was a transition from bird- to butterfl y pollination in the African genus Clivia (Amaryllidaceae) and investigated how fl oral traits may have been either modifi ed or retained during this transition. • Methods: We identifi ed pollinators using fi eld observations, correlations between lepidopteran wing scales and pollen on stig- mas, and single-visit and selective exclusion experiments. We also quantifi ed fl oral rewards and advertising traits. • Key results: The upright trumpet-shaped fl owers of C. miniata were found to be pollinated effectively by swallowtail butterfl ies during both nectar-feeding and brush visits. These butterfl ies transfer pollen on their wings, as evidenced by positive correla- tions between wing scales and pollen loads on stigmas. All other Clivia species have narrow pendulous fl owers that are visited by sunbirds. Selective exclusion of birds and large butterfl ies from fl owers of two Clivia species resulted in a signifi cant decline in seed production. • Conclusions: From the distribution of pollination systems on available phylogenies, it is apparent that a shift took place from bird- to butterfl y pollination in Clivia . This shift was accompanied by the evolution of trumpet-shaped fl owers, smaller nectar volume, and emission of scent, while fl ower color and nectar chemistry do not appear to have been substantially modifi ed. These results are consistent with the idea that pollinator shifts can explain major fl oral modifi cations during plant diversifi cation. Key words: Bird pollination; butterfl y pollination; fl oral scent; nectar chemistry; pollen; pollination syndrome; pollinator shift; scent; spectral refl ectance. Shifts between pollinators are often associated with evolution- Studies of several plant lineages have provided evidence for ary modifi cation of fl oral traits and are thought to be a major driver shifts between bird and lepidopteran pollination ( Perret et al., of diversifi cation in angiosperms ( Stebbins, 1970 ; Harder and 2007 ; Whittall and Hodges, 2007 ; Tripp and Manos, 2008 ; Gübitz Johnson, 2009 ; van der Niet and Johnson, 2012 ). Other macroevo- et al., 2009 ). The shared utility of long corolla tubes in both bird lutionary evidence for the role of pollinators in shaping fl oral form and lepidopteran pollination systems may facilitate these shifts. In is that unrelated taxa pollinated by similar pollinator assemblages Aquilegia , for example, hawkmoth pollination evolved from hum- often display convergent suites of fl oral traits known as fl oral syn- mingbird pollination ( Whittall and Hodges, 2007 ), while in Petu- dromes ( Faegri and van der Pijl, 1979 ; Fenster et al., 2004 ). The nia there is at least one case of hummingbird pollination evolving shifts that produce these patterns of diversifi cation within clades, from hawkmoth-pollinated ancestors ( Gübitz et al., 2009 ). A recent and convergence among them, are believed to be infl uenced by literature survey ( van der Niet and Johnson, 2012 ) indicated that availability, behavior, and per-visit effectiveness of pollinators at shifts involving butterfl y pollination are poorly documented relative the local population level ( Stebbins, 1970 ), as well as intrinsic evo- to those involving other Lepidoptera. Studies of the irid genera lutionary constraints and opportunities (Stebbin’s “lines of least Gladiolus and Tritoniopsis indicate that butterfl y pollination in resistance”). There is still much that is unknown about which trait these lineages evolved mostly from long-tongued bee and long- modifi cations are critical for inducing pollinator shifts ( Schemske proboscid fl y pollination systems ( Manning and Goldblatt, 2005 ; and Bradshaw, 1999 ; Shuttleworth and Johnson, 2010 ), and Valente et al., 2012 ). Although not previously documented to our whether shifts are more likely to occur between pollination sys- knowledge, shifts between bird and butterfl y pollination systems tems that share many traits in common than between pollination seem plausible because of their shared associations with unscented systems that have few traits in common ( Aigner, 2001 ). To address tubular red or orange fl owers ( Faegri and van der Pijl, 1979 ). these questions, it is necessary to have data not only on the identity C livia (Amaryllidaceae) is one of the best-known ornamental and effectiveness of pollinators, but also the fl oral reward and ad- plant groups worldwide ( Koopowitz, 2002 ), yet the reproductive vertising traits of plant species with known phylogenetic relation- biology of Clivia species has not previously been investigated in ships ( van der Niet and Johnson, 2012 ). the wild. Four of the species ( C. nobilis Lindl., C. gardenii Hook., C. caulescens R. A. Dyer, and C. mirabilis Rourke) have tubular- pendulous flowers that conform to the syndrome of bird- 1 Manuscript received 9 October 2013; revision accepted 19 November 2013. pollination, while a fi fth species C. miniata (Lindl.) Bosse has The authors thank R. Wolter, J. Abbot, N. Abbot, T. Abbot, R. Rawson, upright, trumpet-shaped fl owers consistent with the syndrome of A. Solomon, T. Odendaal, and S. Steenhuisen for their assistance, and butterfl y pollination ( Manning, 2005 ). Phylogenetic studies of Clivia H. Grebe for permission to use his C. mirabilis image in the illustration of phylogenetic relationships. Funding was provided by the Natal Society suggest that C. miniata , with its unique trumpet-shaped fl owers, Foundation and National Research Foundation grant number 46372 (SDJ ). occupies a relatively derived position, sister to that of the C. gardenii 2 Author for correspondence (e-mail: [email protected]) species complex, with the remaining pendulous fl owered species occupying more basal lineages ( Conrad, 2008 ) ( Fig. 1 ) . It was doi:10.3732/ajb.1300363 therefore hypothesized that a shift took place from sunbird- to American Journal of Botany 101(1): 190–200, 2014 ; http://www.amjbot.org/ © 2014 Botanical Society of America 190 January 2014] KIEPIEL AND JOHNSON—POLLINATOR SHIFT IN CLIVIA Q1 191 Fig. 1. Distribution of Clivia species in southern Africa and their phylogenetic relationships according to Conrad (2008) . Butterfl y pollination in C. miniata represents a unique and most recent evolutionary modifi cation in the genus, while bird pollination represents the ancestral condition. Infl orescence and pollinator images are not to the same scale. butterfl y pollination in the genus. The aims of this study were (1) sometimes succeed in producing Clivia seeds from hand-selfi ng ( Swanevelder to determine whether pendulous and trumpet-fl owered Clivia and Fisher, 2009 ), our studies indicate that Clivia species have a late-acting species are, as hypothesized, pollinated by sunbirds and butter- self-incompatibility system, and are therefore fully reliant on pollinator visits for seed production (I. Kiepiel, unpublished data). Clivia fl owers are protogy- fl ies, respectively; and, (2) to determine whether fl oral traits such nous and remain open for up to three weeks if not pollinated. as morphology, spectral refl ectance, nectar and scent emissions This study focuses on C. miniata , the only member of the genus with upright were modifi ed during the putative pollinator shift. trumpet-shaped fl owers, and C. gardenii , a pendulous fl owered form. The two spe- cies have a similar habitat and geographical distribution, overlapping along the eastern coast of South Africa ( Fig. 1 ). Accordingly, any differences in their pollina- MATERIALS AND METHODS tor spectrum should refl ect interactions between pollinators and fl oral features, rather than geographical differences in pollinator distribution. Clivia robusta B. G. Species and Study sites — Clivia Lindl. (Amaryllidaceae) is a horticulturally Murray, Ran, de Lange, Hammett, Truter, Swanev. ( Murray et al., 2004 ) has been important taxon of long-lived evergreen perennials within the African tribe distinguished from other forms of C. gardenii by the large size of plants, their Haemantheae ( Meerow et al., 1999 ; Rourke, 2002 ). The genus consists of fi ve swamp habitat, anther exsertion, and unusual karyology ( Murray et al., 2004 ), but species that are endemic to southern Africa. With the exception of the semixeric this taxonomic arrangement is controversial because of the absence of any consistent C. mirabilis, which is adapted to a Mediterranean type climate ( Rourke, 2002 ), DNA sequence differences or quantitative studies of morphological discontinuities Clivia species do not tolerate full sun and favor cool, shady, moist, coastal, and in wild populations. We have, therefore. followed local taxonomic authorities ( Conrad, Afromontane forest habitats ( Swanevelder, 2003 ). Although horticulturists 2008 ; Rourke, 2012 ) in treating C. robusta as a “robust” form of C. gardenii. 192 AMERICAN JOURNAL OF BOTANY [Vol. 101 The taxa examined in this paper are listed as vulnerable ( Raimondo et al., to be used as controls. To determine whether small insects contribute to pollina- 2009 ); consequently we do not provide detailed plant localities, beyond the tion of the study species, 13 C. miniata plants and 14 C. gardenii plants were
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