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Drought and Leaf Herbivory Influence Floral Volatiles and Pollinator Attraction

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Drought and Leaf Herbivory Influence Floral Volatiles and Pollinator Attraction Global Change Biology (2016) 22, 1644–1654, doi: 10.1111/gcb.13149 Drought and leaf herbivory influence floral volatiles and pollinator attraction LAURA A. BURKLE1 and JUSTIN B. RUNYON 2 1Department of Ecology, Montana State University, Bozeman, MT 59717, USA, 2Rocky Mountain Research Station, USDA Forest Service, 1648 S. 7th Avenue, Bozeman, MT 59717, USA Abstract The effects of climate change on species interactions are poorly understood. Investigating the mechanisms by which species interactions may shift under altered environmental conditions will help form a more predictive understand- ing of such shifts. In particular, components of climate change have the potential to strongly influence floral volatile organic compounds (VOCs) and, in turn, plant–pollinator interactions. In this study, we experimentally manipulated drought and herbivory for four forb species to determine effects of these treatments and their interactions on (1) visual plant traits traditionally associated with pollinator attraction, (2) floral VOCs, and (3) the visitation rates and community composition of pollinators. For all forbs tested, experimental drought universally reduced flower size and floral display, but there were species-specific effects of drought on volatile emissions per flower, the composition of compounds produced, and subsequent pollinator visitation rates. Moreover, the community of pollinating visitors was influenced by drought across forb species (i.e. some pollinator species were deterred by drought while others were attracted). Together, these results indicate that VOCs may provide more nuanced information to potential floral visitors and may be relatively more important than visual traits for pollinator attraction, particularly under shifting environmental conditions. Keywords: Campanula rotundifolia, climate change, floral display, floral scent, Heterotheca villosa, Phacelia hastata, plant–pollinator interactions, pollinator community, Potentilla recta, volatile organic compounds Received 28 July 2015; revised version received 11 October 2015 and accepted 21 October 2015 2015). To date, pollination biology has focused largely Introduction on the role of visual cues for pollinator attraction One of the main challenges facing ecologists today is to (Raguso, 2008a), which contribute to community-level gain a better understanding of how climate change is patterns in plant–pollinator interaction networks (Vaz- affecting ecological interactions among species so that quez et al., 2009). The importance of floral odors for we may maintain and restore the essential ecosystem pollination is increasingly appreciated (e.g. Kessler services they provide, like pollination. To better under- et al., 2008; Raguso, 2008a,b; Morse et al., 2012; Riffell stand the mechanisms by which shifts in species inter- et al., 2013), yet how they structure plant–pollinator actions could occur, ecologists quantify traits interactions, particularly in the context of climate potentially involved in mediating these interactions. change, is relatively poorly studied. Given their crucial Volatile organic compounds (VOCs) are traits that can roles in directing other plant–insect interactions (e.g. in be influenced by climate change and strongly mediate a the context of herbivory), plant VOCs likely exert wide array of interactions between plants and insects, important influences on plant–pollinator interactions either in an attractive or repellant manner. VOCs have and community dynamics. been most extensively studied in the context of tri- Components of climate change, including increasing – – trophic (plant herbivore natural enemy) interactions temperatures and CO2 levels and altered precipitation where they play important roles in plant defense (e.g. patterns, can affect plant traits important for pollinator De Moraes et al., 2001; Kessler & Baldwin, 2001; Xiao attraction (e.g. Jablonski et al., 2002; Scaven & Rafferty, et al., 2012). Although less studied, VOCs emitted from 2013). For instance, elevated temperatures can influence flowers can mediate mutualistic interactions between flower production, flower size, floral phenology, plant plants and their pollinators (Dudareva et al., 2006). For height, and the production and composition of nectar example, pollinators use these airborne chemical sig- and pollen (e.g. Delph et al., 1997; Wahid et al., 2007; nals while searching for nectar and pollen (Schiestl, Liu et al., 2012). Importantly, studying the effects of cli- mate change on these traits of plants has done little to Correspondence: Laura A. Burkle, tel. +1 406 994 7223, fax advance our understanding of how plant–pollinator +1 406 994 3190, e-mail: [email protected] interactions and community dynamics may shift 1644 © 2015 John Wiley & Sons Ltd DROUGHT AFFECTS VOLATILES AND POLLINATORS 1645 because (1) plant species often respond similarly to the (Bidart-Bouzat & Imeh-Nathaniel, 2008). Thus, it will be same environmental cue (i.e. community-wide reduc- important to not only investigate the effects of multiple tions in flower production due to drought, or advance- climate change factors and their interactions (e.g. ment of flowering phenology due to warmer spring Schweiger et al., 2010; Hoover et al., 2012), but also temperatures); (2) when species-specific responses multiple types of species interactions (Tylianakis et al., occur, it has proved difficult to leverage this informa- 2008; Fontaine et al., 2011). tion in a predictive way, and (3) a slow recognition that Environmental conditions that induce stress in plants pollinator foraging behavior is not static (i.e. interac- (e.g. drought and herbivory) have the potential to tions within a community are flexible consequences of change floral VOCs and affect pollination attraction, context-dependent pollinator choices) hinders our but this remains poorly understood. Here, we experi- understanding of how cascades of shifts in foraging mentally manipulated drought and herbivory for four patterns may occur in communities altered by climate species of forbs in a fully factorial design to investigate change. Thus, studying floral VOCs – information-rich effects on (1) traditional measures of pollinator attrac- signals that are highly responsive to the environment – tion (i.e. plant size, floral display, and flower size), (2) and plant–pollinator interactions in the context of cli- floral VOC quantity (i.e. total volatile production per mate change will likely enhance our ability to form a flower) and quality (i.e. shifts in VOC composition and more predictive understanding of how plant–pollinator dispersion of compounds), and (3) subsequent rates interactions will change. In fact, increasing tempera- and composition of pollinator visitors. Our results sug- tures have been found to increase the quantity of floral gest that floral VOCs represent a strong, consistent link VOCs and alter the quality (i.e. shift ratios of com- between plant physiological responses to drought and pounds in floral bouquets) with potentially important, information-rich signals by which pollinators make for- but unknown, effects on pollinators (Farre-Armengol aging choices. We also show that herbivory can modify et al., 2014). the effects of drought on plant traits including floral Reduced precipitation resulting in drought is occur- VOCs, at least in some species. ring as a result of anthropogenic climate change, and drought is predicted to become more severe in many Materials and methods places across the globe (e.g. Pederson et al., 2010; Dai, 2013; Cook et al., 2015). Water availability can have Plant material and growth conditions strong effects on plant growth as well as plant traits important for pollination and other species interactions. We used three species of widespread native forbs: Campanula For example, drought stress reduced flower size and rotundifolia L., harebell; Heterotheca villosa (Pursh) Shinners, nectar volume in fireweed (Epilobium angustifolium) hairy false goldenaster; and Phacelia hastata Douglas ex Lehm., (Carroll et al., 2001) and the wild tobacco species Nico- silverleaf phacelia as well as one invasive forb: Potentilla recta L., sulphur cinquefoil; native to Eurasia. Sixty individuals of tiana quadrivalvis (Halpern et al., 2010). Given shifts in each species were grown from seed in a greenhouse with a plant quality under drought conditions, the amount day/night temperature regime of 26 °C/15 °C and a 16 h and consequences of herbivory are also likely to be photoperiod with supplemental lighting provided by metal altered (Huberty & Denno, 2004). In fact, drought may halide lamps. Seeds were collected locally at the Mt. Ellis field have the strongest effects on herbivory compared to site (see below). Plants were grown in 6.5 cm wide by 25 cm other components of climate change (Scherber et al., tall plastic cone-tainers using Sunshine Mix #1 soil (Sun Gro 2013). Moreover, herbivory and pollination do not Horticulture, Agawam, MA, USA) with added fertilizer (1 tea- occur in isolation (i.e. plants are simultaneously spoon or ca. 5 mL of Osmocote per pot; The Scotts Company, exposed to herbivores and pollinators). Plant herbivory Marysville, OH, USA). Seeds were planted in the fall (Octo- is ubiquitous, predicted to increase as the climate ber), allowed to grow and establish for 6 weeks, and then ver- ° warms (Currano et al., 2010), and herbivore feeding has nalized in a climate-controlled chamber at approximately 4 C with a 12 h photoperiod for 100–130 days. Plants removed recently been shown to affect flower volatile emissions from
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