Araujia Sericifera Brot.; Asclepiadoideae) Co-Opts Native Honeybees As Its Primary Pollinator in South Africa
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AoB PLANTS http://aobplants.oxfordjournals.org/ Open access – Research article The invasive ‘mothcatcher’ (Araujia sericifera Brot.; Asclepiadoideae) co-opts native honeybees as its primary pollinator in South Africa Gareth Coombs* and Craig I. Peter Department of Botany, Rhodes University, PO Box 94, Grahamstown 6140, South Africa Received: 29 July 2010; Returned for revision: 5 September 2010; Accepted: 30 November 2010; Published: 9 December 2010 Citation details: Coombs G, Peter CI. 2010. The invasive ‘mothcatcher’ (Araujia sericifera Brot.; Asclepiadoideae) co-opts native honeybees as its primary pollinator in South Africa. AoB PLANTS 2010: plq021, doi:10.1093/aobpla/plq021 Abstract Background Successful invasive plants such as Araujia sericifera usually either are capable of automatic and aims self-pollination or maintain pollinator services by having generalized pollination systems to make use of local pollinators in the invaded range. Alternatively, plants must co-opt new pol- linators with similar morphology to native pollinators or reproduce asexually. We aimed to document the pollination biology of A. sericifera in South Africa. Given the success of this species as an invader, we predicted that sexual reproduction occurs either through self-polli- nation or because A. sericifera has successfully co-opted native insect pollinators. Methodology We examined the pollination biology of the South American A. sericifera in South Africa. We documented the effective pollinators including a comparison of the efficacy of nocturnal versus diurnal pollinators as well as the breeding system and long-term natural levels of the pollination success of this species. Principal results We found that native honeybees (Apis mellifera) were the main pollinators of A. sericifera in South Africa. Visiting moths are unimportant pollinators despite being attracted by the pale colour and nocturnal scent of the flowers. Plants from the Grahamstown population were incapable of autonomous self-pollination but pollinator-mediated self-pollination does occur. However, the highest fruit initiation resulted from out-crossed pollination treatments. The high pollen transfer efficiency of this species was comparable to other hymenopteran- pollinated exotic and native milkweeds, suggesting that A. sericifera maintains pollinator ser- vices at levels experienced by indigenous asclepiad species. Conclusions Araujia sericifera reproduces successfully in South Africa due to a combined ability of this species to attract and exploit native honeybees as its pollinators and of individual plants to set fruit from pollinator-mediated self-pollination. Introduction pollination failure if they cannot shift to new pollinators Invasive species introduced into new environments in (Parker 1997; Larson et al. 2002; Parker and Haubensak small numbers could experience pollen limitation or 2002). However, pollination failure (lack of seed set due * Corresponding author’s e-mail address: [email protected] AoB PLANTS Vol. 2010, plq021, doi:10.1093/aobpla/plq021, available online at www.aobplants.oxfordjournals.org & The Authors 2010. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.5/uk/) which permits unrestricted non- commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. AoB PLANTS Vol. 2010, plq021, doi:10.1093/aobpla/plq021 & The Authors 2010 1 Coombs and Peter — Invasive milkweed co-opts native honeybee pollinators to pollinator absence) rarely occurs in invasive species rise to common names of ‘mothcatcher’ or ‘cruelplant’ and is more likely to prevent species with highly special- (Hicken 1928; Forster and Bruyns 1992). Smaller ized pollination systems and intricate flower mor- insects may also be trapped in the corpusculum and phologies (e.g. figs and orchids) from becoming are incapable of escaping as these insects are too invasive (Richardson et al. 2000), although exceptions small to remove pollinaria. Araujia sericifera is polli- occur (e.g. Ficus spp.: Nadel et al. 1992; Gardner and nated by honeybees in Australia (Coleman 1935) and Early 1996; orchids: Liu and Pemberton 2010). Many bumble bees (Bombus spp.) and Scoliid wasps (Scolia invasive species typically either have generalized pollina- spp.—Scoliidae) in Europe (Romeo 1933). Several tion systems and flowers with open accessible rewards notes and papers have enumerated insects that visit (Richardson et al. 2000; Bjerknes et al. 2007) or over- the flowers of A. sericifera in other countries (see come pollinator limitation through autonomous or Romeo 1933 and references therein; Hicken 1928; pollinator-mediated self-pollination (Baker 1974; van Coleman 1935), although records from the native Kleunen et al. 2008). range are limited to a single observation (Morong The mechanism of pollination in milkweeds (Asclepia- 1889). doideae-Apocynaceae) is mechanically complex and Given the success of this species as an invader in requires the accurate re-insertion of pollinia (aggregated South Africa and the rarity of autonomous self- compact pollen masses) that are removed as pairs and pollination in the Asclepiadoideae, we hypothesized deposited individually into a snugly fitting stigmatic that A. sericifera successfully utilizes native pollinators groove (Wyatt and Broyles 1994; Ollerton et al. 2003; to maintain pollination success. We therefore set out Fig. 1C). Two pollinia are suspended off a clam-like mech- to (i) determine the reliance of A. sericifera on anical clip (the corpusculum) that attaches to the pollina- pollinators by documenting its breeding system, (ii) tor, and constitute a single structure, the pollinarium, that determine the functional pollinators of A. sericifera in is removed by pollinators. Pollinia are deposited when the South Africa, (iii) quantify the consistency of pollination insect that is already bearing a pollinarium drags a polli- success in this species for several consecutive nium through one of the five specialized stigmatic flowering seasons, (iv) determine the relative contri- grooves where it may become lodged, breaking off to bution of diurnal and nocturnal pollinators to pollina- effect pollination (Wyatt 1976; Wyatt and Broyles 1994). tion success and (v) compare whether the levels of This relatively specialized floral morphology translates pollination success in A. sericifera are similar to those into specialized interactions with pollinators in 70 % of of a native milkweed with similar growth form and examined asclepiads that have less than five species of pollination biology. pollinators, while 38 % have only a single pollinator (Ollerton and Liede 1997). Nevertheless, several milk- weeds, including the well-known North American Materials and methods species in the genus Asclepias, have highly generalized pollination systems (Ollerton and Liede 1997). Despite Study species such generalizations, many of these are functionally Araujia sericifera (Apocynaceae-Asclepiadoideae) is specialized (sensu Fenster et al. 2004) to a group or indigenous to tropical (including Peru, Argentina, Para- family of pollinators with the right morphology and be- guay and Brazil) and temperate (Uruguay) regions of haviour (Wolff et al. 2008). South America, and has become invasive in several Ten of the 94 species of milkweed occurring in Austra- countries in Europe (France, Greece, Italy, Portugal lia are naturalized invasive species (Forster 1994). In and Spain), Australia, New Zealand, North America, North America at least two species of Vincetoxicum are Israel and South Africa (Forster and Bruyns 1992; invasive (Daehler 1998; Cappuccino 2004), while there EMPPO 2008). In South Africa, it commonly grows in are two naturalized Asclepiadoideae in South Africa abandoned fields and on fences in urban environ- (Victor et al. 2000). Invasive milkweeds are likely to ments (Fig. 1A; Henderson and Anderson 1966). depend largely on co-opting new pollinators as few Flowers are white, streaked with light purple, and species can set seed through autonomous self- scented day and night. Flowers are borne on peduncu- pollination (Wyatt and Broyles 1994). late axillary inflorescences (sensu Henderson and Araujia sericifera (Brot.) is an invasive tropical vine Anderson 1966). In South Africa, flowering begins in that is famous for catching both diurnal and nocturnal late November and ends in May, with the mid-season Lepidopteran flower visitors. This results from the long peak occurring in December (pers. obs.). proboscides of these insects becoming wedged Cynanchum ellipticum (Apocynaceae-Asclepiadoideae) between the rigid anther wings of its flowers, giving is a common milkweed, endemic to southern Africa 2 AoB PLANTS Vol. 2010, plq021, doi:10.1093/aobpla/plq021 & The Authors 2010 Coombs and Peter — Invasive milkweed co-opts native honeybee pollinators (Liede 1993). Both species share broad similarities, total of 5 days in 2007 and 1 day in 2008. Bees were nor- including growth form and pollination biology. Cynan- mally caught between 0800 and 1030 h, with most chum ellipticum also grows on fences in urban environ- sampling periods not exceeding 1 h, for a total of 8h ments, forming large, dense floral displays. Cynanchum observation time. For all insects we counted the ellipticum flowers semi-continuously throughout the number of full pollinaria (pollinaria with no pollinia year whereas A. sericifera only flowers