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Floral Volatiles Structure Plant-Pollinator Interactions in a Diverse Community Across the Growing Season

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Floral Volatiles Structure Plant-Pollinator Interactions in a Diverse Community Across the Growing Season Received: 8 April 2019 | Accepted: 26 July 2019 DOI: 10.1111/1365-2435.13424 RESEARCH ARTICLE Floral volatiles structure plant–pollinator interactions in a diverse community across the growing season Laura A. Burkle1 | Justin B. Runyon2 1Department of Ecology, Montana State University, Bozeman, Montana Abstract 2Rocky Mountain Research Station, USDA 1. While the importance of floral odours for pollinator attraction relative to visual Forest Service, Bozeman, Montana cues is increasingly appreciated, how they structure community‐level plant–pol- Correspondence linator interactions is poorly understood. Elucidating the functional roles of flow- Laura A. Burkle ering plant species with respect to their floral volatile organic compounds (VOCs) Email: [email protected] and how those roles vary over the growing season is an initial step towards under- Funding information standing the contribution of floral VOCs to plant–pollinator interaction structure. USDA Forest Service; Montana State University 2. We sampled the floral VOCs, phenologies and bee visitors of naturally growing plants in a montane meadow in the Northern Rocky Mountains of USA in order Handling Editor: Jessamyn Manson to acquire a base understanding of how floral VOCs and other plant traits may structure plant–pollinator interactions across the growing season. We expected forb species with floral VOCs that were original (far from the community mean) and unique (far from the nearest neighbour) would have few pollinating partners (i.e. specialists), while forbs with non‐original or highly variable floral VOCs would form the generalist core of interactors, thereby contributing to network nested- ness (specialists interacting with nested subsets of generalists). Network modu- larity (patterns of distinct, highly connected subnetworks) could be influenced by groups of pollinators that are attracted to or repelled by certain floral bouquets. 3. Species blooming in early spring emitted similar floral VOC blends containing gen- eralist attractants, whereas floral VOC complexity was highest in mid to late sum- mer. Forb species varied in the originality, uniqueness, and intraspecific variation (i.e. dispersion) of their floral VOCs, indicating the potential for different func- tional roles in plant–pollinator networks. Specifically, the originality, uniqueness and dispersion of forb species’ floral VOCs increased across the growing season. 4. Floral VOCs influenced forb interactions with pollinators. Floral VOCs contributed to the nested structure, but not modular structure, of community‐level plant–pol- linator network structure. Forb species with more original floral VOCs were less connected, while forb species emitting more compounds and with higher intraspe- cific variation in floral VOCs were more connected to pollinators. 5. These findings show that floral scent plays important roles in structuring bee–forb interactions and guiding seasonal patterns in complex communities. Understanding seasonal patterns in floral VOCs may have important implications for plant–pollinator interactions among communities differing in species composi- tion, or as shifts occur in suites of co‐flowering species due to climate change. 2116 | © 2019 The Authors. Functional Ecology wileyonlinelibrary.com/journal/fec Functional Ecology. 2019;33:2116–2129. © 2019 British Ecological Society BURKLE ET AL. Functional Ecolo gy | 2117 KEYWORDS floral scent, floral traits, functional diversity, interspecific trait variation, intraspecific trait variation, native bees, plant–pollinator network structure, pollination services 1 | INTRODUCTION that emit similar, specific suites of floral VOCs that are nested sub- sets of generalist bouquets. To date, pollination biology has largely focused on the role of vi- Though not as well‐studied as the nested structure of plant–pol- sual cues for pollinator attraction (Raguso, 2008a), including floral linator interactions, these interaction networks can also be mod- colour, size and shape, and these traits are known to contribute to ular (contain compartments; e.g. Olesen, Bascompte, Dupont, & community‐level patterns in plant–pollinator interaction networks Jordano, 2007). Pollination systems (i.e. floral syndromes and the (e.g. Vazquez, Chacoff, & Cagnolo, 2009). The importance of floral pollinator functional groups that visit them; Faegri & Van Der Pijl, odours for pollination is increasingly appreciated (Raguso, 2008b; 1979; Fenster, Armbruster, Wilson, Dudash, & Thomson, 2004) Schiestl, 2015), yet how they structure plant–pollinator interac- have been found to be associated with the modular structure of tions is less well understood (Larue, Raguso, & Junker, 2016). Floral plant–pollinator interaction networks (e.g. Carstensen, Sabatino, & odours are predicted to be important determinants of interaction Morellato, 2016; Danieli‐Silva et al., 2012; Dicks, Corbet, & Pywell, network structure because they are among the most important cues 2002). While floral scent is often mentioned in a general sense as a used by pollinators to locate pollen and nectar rewards. For exam- contributor to pollination syndromes and has been tested in some ple, the odour plume emitted by flowers can function over long dis- groups (e.g. Dobson, 2006; Knudsen & Tollsten, 1993; Knudsen, tances to attractant or repel pollinators and at short distances can Tollsten, Groth, Bergström, & Raguso, 2004; Kantsa et al., 2019), the stimulate landing and feeding (Dötterl & Vereecken, 2010; Junker, degree to which floral VOCs contribute to the modular structure of 2016; Raguso, 2008b). Although bees are known to possess innate plant–pollinator interactions is unknown. If certain pollinator groups preferences for some floral scents, they can quickly learn odours as- are attracted to (or repelled by) specific floral bouquets, then we sociated with flowers containing the most abundant and nutritious would expect to observe these groups associating within modules, rewards (Milet‐Pinheiro et al., 2013; Raguso, 2008b). However, floral thereby influencing the structure of interaction networks. While volatiles are not expected to fully explain network structure since these previous studies have considered widely divergent pollinator they usually function in tandem with other floral cues (e.g. flower groups, including butterflies, bees and flies, where a strong signal of colour; e.g. Junker & Parachnowitsch, 2015; Kantsa et al., 2017). floral scent syndromes may be expected among these groups, it is Two ways that we can approach the structure of plant–pollinator not known whether finer‐scale, within‐group (e.g. bees only) mod- interactions in order to better understand the role of floral volatile ules are related to bouquets of floral VOCs. organic compounds (VOCs) is (a) community‐level structural proper- Within plant–pollinator interaction networks, each plant species ties (nestedness and modularity) and (b) the roles of species within has traits that influence the roles of that species in its interactions these networks. with pollinators. Floral bouquets can signal to pollinators in several Across systems, plant–pollinator interactions are very often ob- ways. First, the floral VOCs of an individual or a species may be served to have a nested structure, meaning that specialists interact unique if no other individuals or species in the community have a sim- with subsets of increasingly more generalist species (Bascompte, ilar scent profile (i.e. no near neighbours in floral scent trait space; Jordano, Melian, & Olesen, 2003). This nested structure is thought sensu Buisson, Grenouillet, Villéger, Canal, & Laffaille, 2013; Coux, to be important because it can confer robustness to perturbations Rader, Bartomeus, & Tylianakis, 2016; Walker, 1992). Second, the like extinctions, invasions and disturbances (e.g. Memmott, Waser, floral VOCs of an individual or species may be original if its scent pro- & Price, 2004). Numerous factors are known to contribute to nest- file is distinct compared to the scent of the average member of the edness, including morphology and size‐related traits, phenology community (sensu Buisson et al., 2013; Coux et al., 2016; Laliberté & and abundance (e.g. Stang, Klinkhamer, & van der Meijden, 2006; Legendre, 2010). Likewise, if the flowers of an individual or species Vazquez, Bluthgen, Cagnolo, & Chacoff, 2009; Vazquez, Chacoff, et emit compounds that are similar to many other species in the com- al., 2009). One factor that has received insufficient investigation as a munity, its floral VOCs would be unoriginal. Third, the floral VOC contributor to network nestedness is the VOCs emitted by flowers. profiles of the individuals of a species in the community may be con- Pollinators are known to exhibit preferences for certain combina- sistent (low dispersion and intraspecific variability) or highly variable tions, or ‘bouquets’, of volatile compounds (Dobson, 2006; Wright, (high dispersion) (sensu, e.g. Bolnick et al., 2011; Kuppler, Höfers, Lutmerding, Dudareva, & Smith, 2005), and these preferences can Wiesmann, & Junker, 2016; Siefert, 2012). These metrics are not correlate with patterns of visitation (Junker, Hocherl, & Bluthgen, static properties of the individual or species because they depend 2010; Kantsa et al., 2018). We might expect generalist pollinators on community context (i.e. the composition of the other individu- to be attracted, in part, to many forb species with a range of floral als and species in the community and their floral VOCs). Therefore, VOCs, and
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