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The Ecology and Evolution of Plant Volatiles: Introduction

Edited by Robert. A. Raguso
JULY 2010

In the last decade, tantalizing glimpses of the invisible world of plant volatiles have been revealed through studies that have probed the functional ecology and evolutionary dynamics of chemical phenotypes. This hard-won progress comes largely through the growing realization among researchers that plants routinely use volatile organic compounds (VOCs) to communicate with friends, enemies, neighbors and, indeed, themselves. Once considered a heretical idea, “plant communication” is now the subject of edited volumes, special features and review articles, international symposia and university level courses world-wide. A consensus among these many voices is that VOCs constitute a primary medium of plant communication.

In this virtual special feature, we have supplemented the 6 original papers and introductory essay published in the October 2009 special feature entitled “Floral scent in a whole-plant context” with 8 additional papers of topical relevance published in Functional Ecology from 2005-2010. This expanded roster is now organized into three thematic categories that encompass a more modern view of how VOCs contribute to plant reproduction and defense.

The first grouping explores the consequences of variation in VOC composition for plants and their animal mutualists alike. Majetic et al. (2009) experimentally manipulated the VOC emission rates of colour-polymorphic flowers of Hesperis matronalis using floral extracts, while controlling for flower colour and size. Surprisingly, significant increases in seed fitness and floral visitation by syrphid fly pollinators were associated with floral scent emission rate but not with visual display. This study provides some of the best evidence to date of the impact of floral VOC variation on seed production, through enhanced pollinator visitation. Borges et al. (2008) examine the obligate fig-fig wasp system and ask what becomes of fig VOCs when pollinator-receptive syconia mature to the stage of fruit dispersal in species that differ either in dispersal agent (birds vs. mammals) or in gender expression (monoecy vs. gynodioecy). This study provides several lines of evidence for the functional importance of fig VOCs, including changes in chemical composition when mammals are the primary dispersal agents (but not birds, which don’t use odours to find figs), and the presence of repellent VOCs in gall syconia that contain developing pollinators and should not be consumed by birds or mammals.

The second grouping canvases the two primary mechanisms by which floral volatiles mediate pollinator specialization, through unique attractants (private channels) perceived only or primarily by specialized mutualists, and through repellent chemical components of flowers (floral filters) that screen or restrict the visitor spectrum of otherwise accessible flowers. Schiestl and Peakall (2005) describe two sexually deceptive Chiloglottis orchid species that maintain reproductive isolation, despite producing the same, unique floral odour (chiloglottone), due to temporal, geographic and micro-spatial differences in flowering that track the biology of their wasp pollinators. This study emphasizes the importance of context in further modifying the specificity of a private channel. Chen et al. (2009) document a different class of specialization (nursery pollination) between a dioecious fig (Ficus semicordata) and its obligate wasp pollinator, mediated by another private VOC channel (methyl anisol). The dominance of this compound in male and female receptive figs, its absence in two sympatric fig species, and the nearly dose-independent responses of fig wasps to methyl anisol in choice tests all lend support to private channel hypothesis. In contrast, Shuttleworth and Johnson (2009) present support for a competing view that pollinator specialization, by comparison with directed fruit dispersal, is a net result of the attraction of effective pollinators and the repellence of poor pollinators or enemies. Thus, apparent specialization in Pachycarpus grandiflorus and similar South African flowers can result when cryptic colouration, unpalatable nectar and attractive odours combine to form a “floral filter” that winnows the spectrum of potential floral visitors, in this case, to spider hunting wasps.

The third grouping extends beyond the floral functions of VOCs to document how many of the same compounds, presented in different organs and contexts, mediate diverse aspects of plant politics. In their careful study of extra-floral nectar (EFN) in cotton plants, Röse et al. (2006) present evidence that parasitic wasps can utilize EFN as a primary source of sugar, enhancing their retention as a “standing army” on these plants. Their finding that wasps use the odour of EFN to find the inconspicuous nectaries beneath cotton leaves identifies a valuable example of an “honest” volatile signal associated with sugar rewards that target plant mutualists. On a similar theme, Poelman et al. (2009) show that specific herbivore-induced VOC blends favoured by parasitic wasps in laboratory choice assays (using cultivars of Brassica oleracea) are correlated with higher parasitism rates of Pieris butterfly larvae on B. oleracea plants that emit such blends in field settings. These VOC blends include familiar components of floral scents, including methyl salicylate. Finally, the original feature’s article by Kessler and Halitschke (2009) documented the direct consequences of herbivore-induced plant responses for pollinator attraction through changes in floral and vegetative VOCs and phenolic defense compounds. In a more recent paper, Kiers et al. (2010) explore this potential conflict between plant defense and reproduction by examining the context dependence of jasmonate-induced cucumber plant responses in the presence or absence of arbuscular mycorrhizae and variable soil phosphorus levels. Although these authors did not explicitly track VOC emissions, exogenous jasmonate treatments (approximating endogenous herbivore-induced signals) reduced mean flower size, nectar and pollen quality only in mycorrhizal plants, suggesting that apparent tradeoffs between plant reproduction and induced defense are contingent upon belowground interactions with microbial symbionts.

When taken together, this larger sample of papers highlights a growing list of fitness-related functions for plant volatiles, and the need to better incorporate chemical phenotypes into experimental studies of plant communication, within a whole plant context.

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