The Long-Tongued Hawkmoth Pollinator Niche for Native and Invasive Plants in Africa

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The Long-Tongued Hawkmoth Pollinator Niche for Native and Invasive Plants in Africa Annals of Botany 117: 25–36, 2016 doi:10.1093/aob/mcv137, available online at www.aob.oxfordjournals.org The long-tongued hawkmoth pollinator niche for native and invasive plants in Africa Steven D. Johnson1,* and Robert A. Raguso2 1School of Life Sciences, University of KwaZulu-Natal, P Bag X01, Scottsville, Pietermaritzburg, 3209, 2 South Africa and Department of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853, USA Downloaded from https://academic.oup.com/aob/article-abstract/117/1/25/2195680 by guest on 11 June 2020 *For correspondence. E-mail [email protected] Received: 22 May 2015 Returned for revision: 25 June 2015 Accepted: 28 July 2015 Published electronically: 7 September 2015 Background and Aims Unrelated organisms that share similar niches often exhibit patterns of convergent evolu- tion in functional traits. Based on bimodal distributions of hawkmoth tongue lengths and tubular white flowers in Africa, this study hypothesized that long-tongued hawkmoths comprise a pollination niche (ecological opportunity) that is distinct from that of shorter-tongued hawkmoths. Methods Field observations, light trapping, camera surveillance and pollen load analysis were used to identify pollinators of plant species with very long-tubed (>8 cm) flowers. The nectar properties and spectral reflectance of these flowers were also measured. The frequency distributions of proboscis length for all captured hawkmoths and floral tube length for a representative sample of night-blooming plant species were determined. The geographical distributions of both native and introduced plant species with very long floral tubes were mapped. Key Results The convolvulus hawkmoth Agrius convolvuli is identified as the most important pollinator of African plants with very long-tubed flowers. Plants pollinated by this hawkmoth species tend to have a very long (approx. 10 cm) and narrow flower tube or spur, white flowers and large volumes of dilute nectar. It is estimated that >70 grassland and savanna plant species in Africa belong to the Agrius pollination guild. In South Africa, at least 23 native species have very long floral tubes, and pollination by A. convolvuli or, rarely, by the closely related hawkmoth Coelonia fulvinotata, has been confirmed for 11 of these species. The guild is strikingly absent from the species-rich Cape floral region and now includes at least four non-native invasive species with long-tubed flowers that are pre-adapted for pollination by A. convolvuli. Conclusions This study highlights the value of a niche perspective on pollination, which provides a framework for making predictions about the ecological importance of keystone pollinators, and for understanding patterns of convergent evolution and the role of floral traits in plant colonization. Key words: Agrius convolvuli, biological invasions, ecological opportunity, flower colour, functional traits, long-tongued hawkmoth, moth pollination, mutualism, nectar, plant–pollinator interactions, pollination ecology, proboscis length, regeneration niche, specialization. INTRODUCTION arguably as compelling as those in Galapagos finches and The concept of the niche as an ecological opportunity has had a Caribbean lizards (Schluter, 2000). Pollinator niches can be de- major influence on evolutionary biology and ecology (Schluter, fined according to axes of pollinator morphology such as pro- 2000; Chase and Leibold, 2003; Devictor et al.,2010; Losos, boscis length, as well as phenology and perception of colour 2010). Pollinators are niches in that they represent ecological and scent. As examples, evolutionary shifts between bird and opportunities for plants, but the niche concept has historically bee pollinators will typically involve floral modifications along been focused on competition and thus has been slow to infil- several of these niche axes (Bradshaw and Schemske, 2003), trate the study of mutualisms. This is surprising because plant shifts between different hummingbird species may involve flo- floral traits can readily be linked to pollinator niches (Johnson, ral adjustment to both the length and curvature of bills 2010), while the relationships of other plant functional traits (McDade, 1992; Maglianesi et al.,2014), while shifts between such as height, leaf dimensions and seed size to particular envi- short- and long-tongued moths may involve adjustments only ronmental niches often are much harder to establish. As a com- of the floral tube length and nectar volume (Boberg et al., ponent of the regeneration niche (Grubb, 1977), pollinators can 2014). be likened to canopy gaps and other ecological opportunities For an outbreeding plant with a highly specialized pollination that plants exploit under selection for enhanced reproduction. system, a particular pollinator may be considered part of its fun- Shifts between pollinator niches have been a key driver of damental niche requirement. However, in most cases interac- adaptive radiation in angiosperms (Whittall and Hodges, 2007; tions among species will shape a more complex realized van der Niet and Johnson, 2012). These ecological niche shifts pollination niche. For example, the colour preference of provide examples of evolutionary diversification that are pollinators may be altered by the dominant nectar plants in a VC The Author 2015. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: [email protected] 26 Johnson & Raguso — Long-tongued hawkmoths form a pollination niche community, such that the floral colour traits that a plant re- hawkmoths in southern Africa; and (4) to determine the biogeo- quires to attract pollinators may vary among communities graphical distribution of long-tongued hawkmoth pollination (Newman et al., 2012). For generalist plants, there is no single systems in South Africa. pollinator niche, and floral trait combinations will be selected according to the composition of local assemblages of pollina- tors (Gomez et al., 2015). In both specialized and generalized MATERIALS AND METHODS plants, floral adaptation to pollinators can be mitigated or constrained by opposing selective pressures provided by floral Trait measurements enemies (Theis et al., 2007; Galen et al., 2011). Interactions between hawkmoths and plants with long-tubed The identification of proboscis length as a key niche dimen- flowers (Fig. 1) were studied by us between 2002 and 2015 at sion and floral tube length as a key functional floral trait stems 16 sites distributed across the eastern half of South Africa back to Darwin and his famous prediction of a very long- (Supplementary Data Table S1). Hawkmoths were recorded by Downloaded from https://academic.oup.com/aob/article-abstract/117/1/25/2195680 by guest on 11 June 2020 tongued species of hawkmoth in Madagascar, based on the flo- light trapping, direct observations at flowers and through use of ral dimensions of an orchid flower (Darwin, 1877). Subsequent motion-activated cameras. Data from a further eight sites de- work has confirmed the importance of pollinator proboscis scribed by Anderson et al. (2010) were used for analyses of the length for floral tube length evolution (Nilsson, 1988; morphometrics of light-trapped hawkmoths. To estimate the Alexandersson and Johnson, 2002), although the role of coevo- frequency distribution of proboscis lengths in the general hawk- lution in the evolution of the pollinator niche itself (Nilsson moth fauna, measurements to the nearest 1 mm using a steel et al.,1987; Anderson and Johnson, 2008; Pauw et al., 2009) ruler or digital calipers were taken of the proboscides of 1199 vs. shifts between pre-existing pollinator niches (Wasserthal, hawkmoths captured by light trapping. 1997; Whittall and Hodges, 2007) is still much debated. To estimate the frequency distribution of floral tube length in In this study we examine the niche axis of hawkmoth probos- moth-pollinated plants in eastern South Africa, we used botani- cis length in Africa. Previous studies in Madagascar (Nilsson cal descriptions in guides to wildflowers and trees of the region et al.,1987) and Costa Rica (Haber and Frankie, 1989; Agosta (Pooley, 1998; Boon, 2010). Plants were considered likely to be and Janzen, 2005) suggest that the distribution of hawkmoth moth pollinated if they have flowers that are long-tubed, white, tongue lengths in these regions is multimodal, reflecting the scented and night blooming. If the tube length was given as a rich diversity of hawkmoths in these regions, and also right- range, we used midpoint values. To identify the entire set of skewed, reflecting dominance of shorter-tongued hawkmoths, plants in southern Africa that have long-tubed flowers, we con- while recent studies indicated that there may be a simple bi- tacted taxonomic authorities and consulted descriptions in gen- modal distribution of both tongue lengths of hawkmoths and eral taxonomic accounts of the flora. Data for Kenya were tube lengths of flowers on the African mainland (Anderson obtained from Martins and Johnson (2013). et al.,2010; Martins and Johnson, 2013). On the basis of this bi- For each of 18 plant species, we measured, to the nearest modal distribution, we hypothesized that there is a distinct 1 mm using a steel ruler, the tube length and distance from the niche of long-tongued hawkmoths to which African plants have stigma to the base of the nectar column of 3–289 flowers (me- become adapted. Our interest here is the classical macroevolu- dian ¼ 9 flowers per species),
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