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Generalised Pollination Systems for Three Invasive Milkweeds in Australia M

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Generalised Pollination Systems for Three Invasive Milkweeds in Australia M Plant Biology ISSN 1435-8603 RESEARCH PAPER Generalised pollination systems for three invasive milkweeds in Australia M. Ward1 & S. D. Johnson2 1 School of Biological Sciences, The University of Queensland, St Lucia, Qld, Australia 2 DST-NRF Centre for Invasion Biology, School of Biological and Conservation Sciences, University of KwaZulu-Natal, Pietermaritzburg, South Africa Keywords ABSTRACT Asclepiadoideae; floral rewards; generalisation; invasive plants; pollination. Because most plants require pollinator visits for seed production, the ability of an introduced plant species to establish pollinator relationships in a new ecosystem may Correspondence have a central role in determining its success or failure as an invader. We investigated M. Ward, University of Queensland, School of the pollination ecology of three milkweed species – Asclepias curassavica, Gomphocar- Biological Sciences, St Lucia, Qld 4072, pus fruticosus and G. physocarpus – in their invaded range in southeast Queensland, Australia. Australia. The complex floral morphology of milkweeds has often been interpreted as E-mail: [email protected] a general trend towards specialised pollination requirements. Based on this interpreta- tion, invasion by milkweeds contradicts the expectation than plant species with spec- Editor ialised pollination systems are less likely to become invasive that those with more J. Arroyo generalised pollination requirements. However, observations of flower visitors in nat- ural populations of the three study species revealed that their pollination systems are Received: 22 April 2012; Accepted: 10 Octo- essentially specialised at the taxonomic level of the order, but generalised at the spe- ber 2012 cies level. Specifically, pollinators of the two Gomphocarpus species included various species of Hymenoptera (particularly vespid wasps), while pollinators of A. curassav- doi:10.1111/j.1438-8677.2012.00700.x ica were primarily Lepidoptera (particularly nymphalid butterflies). Pollinators of all three species are rewarded with copious amounts of highly concentrated nectar. It is likely that successful invasion by these three milkweed species is attributable, at least in part, to their generalised pollinator requirements. The results of this study are dis- cussed in terms of how data from the native range may be useful in predicting pollina- tion success of species in a new environment. genetically self-compatible, are dependent on pollinators for INTRODUCTION reproductive output (e.g. van Kleunen & Johnson 2005; Jesse Invasive plant species are of critical concern on a worldwide et al. 2006; Liu et al. 2006; Hong et al. 2007; Lafuma & Maurice scale, and have consequently become the subject of intensive 2007; Gross et al. 2010; Ward et al. 2012). Furthermore, it has research (e.g. Henderson et al. 2006). However, a central ques- been documented that a lack of pollinator visitation can restrain tion that remains unanswered is: why do some introduced the rate of spread of invasive plant species (Parker 1997). plant species become successful invaders, whereas other species Introduced plant species generally arrive in a new ecosystem do not (e.g. Pysˇek & Richardson 2007)? In an attempt to without the pollinator species that serve them in their native understand factors that control the process of biological plant range, and consequently require formation of new relationships invasions, researchers have mostly focused on antagonistic with pollinator species that are already established in the local interactions between introduced plant species and organisms ecosystem (Richardson et al. 2000). Therefore, it is logical to in their new ecosystem, such as competition (e.g. Blossey & predict that introduced plant species with specialised pollina- No¨tzold 1995) and herbivory (e.g. Keane & Crawley 2002; tion systems are less likely to become invasive due to difficulties Wolfe 2002). However, data on positive interactions such as in establishment of pollinator relationships in their invaded reproductive mutualisms may be critical to provide insight into ecosystem, whereas introduced plant species that can be served how biological plant invasions are facilitated (Richardson et al. by numerous pollinator species have a greater chance of suc- 2000). Indeed, an introduced plant species will not be able to cessful reproduction (Baker 1974; Richardson et al. 2000). colonise new habitats unless reproductive barriers are over- Indeed, recent studies have shown that a number of invasive come. Therefore, an understanding of pollination ecology is plant species achieve reproduction through visits by a broad important for assessing the invasive potential of plant species. assemblage of pollinator species (e.g. Memmott & Waser 2002; Plant species that rely on sexual reproduction generally Jesse et al. 2006; Stout et al. 2006). Furthermore, other studies require pollinators, or are wind-pollinated or autonomously have demonstrated that pollinators may increase seed-set even self-fertilising. Although a large proportion of invasive plants in autonomously self-pollinating invasive species, thereby were originally expected to be autonomously self-fertilising enhancing the invasive ability of these species, despite their (Baker 1955, 1967, 1974; Stebbins 1957), there is growing evi- ability to set some seed in the absence of pollinators (e.g. Jacobi dence that many invasive plant species, even those that are et al. 2005; Bartomeus & Vila 2009; Rodger et al. 2010). 566 Plant Biology 15 (2013) 566–572 © 2012 German Botanical Society and The Royal Botanical Society of the Netherlands Ward & Johnson Pollination of invasive milkweeds Production of abundant floral rewards is likely to enhance natural populations over peak flowering season from Decem- the ability of an invasive plant species to attract pollinators ber 2005 to April 2006. Study populations encompassed a vari- (Ghazoul 2002). It has been observed that invasive plant species ety of habitat types and population sizes, with six populations achieve this through characteristics such as prolific production surveyed for each of A. curassavica and G. physocarpus, and of flowers (Ghazoul 2002; van Kleunen & Johnson 2005), eight populations surveyed for G. fruticosus (see Table S1). secreting profuse volumes of nectar (Chittka & Schurkens Flower visitor observations involved recording the presence 2001) and making floral resources available over a prolonged of all visitors foraging on flowers during a standardised time period of time (Memmott & Waser 2002). When examining period of 30 min per observation event. Where possible, indi- pollination systems, it is relevant to note that different species vidual insects were closely observed in order to determine of pollinator often display variation in their importance for whether they deposited a pollinium into a stigmatic chamber pollination of a given plant species (e.g. see O’Brien 1980; Lind- of the visited flower. Insect visitors were then captured with a say 1984; Jennersten & Morse 1991; Ivey et al. 2003). The butterfly net and placed in ethyl acetate killing jars. Stigmatic importance of particular pollinators is determined by their rel- chambers of the visited flowers were subsequently inspected to ative abundance (i.e. common pollinator species may contrib- confirm the presence of deposited pollinia, as newly deposited ute more towards pollination than less common pollinator pollinia can generally be differentiated from old pollinia by species), as well as factors that influence their per-visit pollina- their brighter colour (M. Ward, personal observation). Insects tion effectiveness, such as pollen load. were later pinned and identified to species where possible, but Three milkweed species – Asclepias curassavica L., Gompho- otherwise to genus or family, and the number and position of carpus fruticosus (L.) W.T. Aiton and Gomphocarpus physocar- pollinia attached to the body of each insect recorded. Insects pus E. Mey. – have become invasive in Australia. All three were examined under magnification to determine whether any species are non-clonal, self-compatible and dependent on poll- residual corpuscula (i.e. corpuscula without pollinia) were inators for seed-set, and the two Gomphocarpus species have present. Voucher specimens of each insect species have been shown potential for hybridisation (Ward et al. 2012). Due to deposited in the University of Queensland Insect Collection. the characteristically highly evolved floral morphology of milk- Flower visitor observations were repeated at the various weeds, these species form an interesting case study of the polli- study populations at different times of the day throughout the nation systems of invasive plants. Pollen grains of milkweeds flowering season. Overall, 18 diurnal observation periods were are aggregated in discrete packages termed pollinia, which are conducted for A. curassavica (total of 540 min), 25 diurnal joined pair-wise to form a pollinarium. Each milkweed flower observation periods were conducted for G. fruticosus (total of holds five pollinaria, and a single pollinium contains enough 750 min) and 17 diurnal observation periods were conducted pollen grains to ensure full seed-set (Wyatt et al. 2000). Polli- for G. physocarpus (total of 510 min). The distribution of sam- nation is typically achieved when a pollinarium is removed by pling effort across populations is indicated in Table S1. Addi- a pollinator from the anther sac of the donor flower and, after tionally, two evening flower visitor observation
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