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Florivore Impacts on Plant Reproductive Success and Pollinator Mortality in an Obligate Pollination Mutualism

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Florivore Impacts on Plant Reproductive Success and Pollinator Mortality in an Obligate Pollination Mutualism Oecologia (2013) 173:1345–1354 DOI 10.1007/s00442-013-2694-8 PLANT-MICROBE-ANIMAL INTERACTIONS - ORIGINAL RESEARCH Florivore impacts on plant reproductive success and pollinator mortality in an obligate pollination mutualism David M. Althoff · Wei Xiao · Sarah Sumoski · Kari A. Segraves Received: 25 October 2012 / Accepted: 23 May 2013 / Published online: 9 July 2013 © Springer-Verlag Berlin Heidelberg 2013 Abstract Florivores are present in many pollination analyses of phenotypic selection based on surveys of natu- systems and can have direct and indirect effects on both rally occurring plants revealed temporal variation in the plants and pollinators. Although the impact of florivores plant traits important to plant fitness and the effects of the are commonly examined in facultative pollination mutual- florivores on fitness. Leaf-footed bugs negatively impacted isms, their effects on obligate mutualism remain relatively fitness when fewer plants were flowering and leaf-footed unstudied. Here, we used experimental manipulations and bug density was high, whereas beetles had a positive effect surveys of naturally occurring plants to assess the effect on fitness when there were many plants flowering and their of florivory on the obligate pollination mutualism between densities were low. This positive effect was likely due to yuccas and yucca moths. Yucca filamentosa (Agavaceae) is adult beetles consuming yucca moth eggs while having a pollinated by the moth Tegeticula cassandra (Lepidoptera: negligible effect on floral abscission.T ogether, the actions Prodoxidae), and the mutualism also attracts two florivores: of both florivores either augmented the relationship of a generalist, the leaf-footed bug Leptoglossus phyllopus plant traits and fitness or slightly weakened the relation- (Hemiptera: Coreidae), and a specialist, the beetle Hyme- ship. Overall, the results suggest that, although florivores norus densus (Coleoptera: Tenebrionidae). Experimental are always present during flowering, the impact of floriv- manipulations of leaf-footed bug densities on side branches ores on phenotypic selection in yuccas is strongly mitigated of Y. filamentosa inflorescences demonstrated that feeding by changes in their densities on plants from year to year. causes floral abscission but does not reduce pollen or seed In contrast, both florivores consistently influenced pollina- production in the remaining flowers. Similar to the leaf- tor larval mortality through floral abscission, and H. densus footed bugs, experimental manipulations of beetle densities beetles additionally via the consumption of pollinator eggs. within individual flowers demonstrated that beetle feeding also causes floral abscission, but, in addition, the beetles Keywords Yucca · Florivory · Leptoglossus · Floral also cause a significant reduction in pollen availability. Path abscission · Community context Communicated by Christina Caruso. Introduction D. M. Althoff (*) · K. A. Segraves Department of Biology, Syracuse University, Syracuse, Pollination mutualisms are an important component of ter- NY 13244, USA restrial communities and strongly impact plant diversity e-mail: [email protected] and fitness (Pellmyr 1992). Although pollinators can exert W. Xiao strong selection on plants (e.g., Campbell et al. 1997; Con- Department of Environmental and Forest Biology, SUNY-ESF, ner 1997; Fenster et al. 2004; Parachnowitsch and Kessler Syracuse, NY 13210, USA 2010) and have often been assumed to be the main selec- tive agent on floral traits, plants also exist within a larger S. Sumoski College of William and Mary–Virginia Institute of Marine community of interacting organisms. Plants associate with Science, Gloucester Point, VA 23062, USA a suite of other species such as herbivores, seed predators, 1 3 1346 Oecologia (2013) 173:1345–1354 nectar robbers, and pathogens, and these other interactions The pollinating seed–parasite mutualism between yuc- can also contribute to plant evolution. As such, we would cas and yucca moths is a classic example of obligate mutu- expect plant traits to be shaped by the combined effects of alism (Powell 1992; Pellmyr 2003). Yuccas require yucca these different types of interactions (Brody 1997; Strauss moths for pollination and the moth larvae feed exclusively 1997; Pilson 2000; Adler 2008; Caruso et al. 2010). Pollina- on yucca seeds. In a correlative study examining the influ- tors will favor suites of traits that enhance pollination ser- ence of florivores on this mutualism,A lthoff et al. (2005) vices, while at the same time herbivores or nectar robbers used a combination of flowering traits, insect surveys, and may select for traits that deter their attraction. Consequently, structural equation modeling to examine the effects of two the evolution of floral traits may be limited by the additive florivore species and the yucca moth pollinator Tegeticula and non-additive effects of the set of interactions occurring cassandra (Lepidoptera: Prodoxidae) on fruit set in Yucca within plant populations (e.g., Herrera et al. 2002; Caruso filamentosa (Agavaceae). The effect of florivores on fruit et al. 2003; Adler and Bronstein 2004; Cariveau et al. 2004; set yielded mixed results: the generalist florivore Lepto- Ornelas et al. 2007; Parachnowitsch and Caruso 2008). glossus phyllopus (Hemiptera: Coreidae), the leaf-footed Florivores, in particular, may be more likely to impact bug, decreased fruit production, whereas the specialist plant–pollinator interactions through selection on floral beetle Hymenorus densus (Coleoptera: Tenebrionidae) had traits because they feed directly on floral tissue. Florivores no effect. Both florivores’ peak abundance coincided with have direct negative effects on pollination mutualisms by peak plant flowering; however, peak pollinator moth abun- causing loss of floral tissue (Mothershead and Marquis dance occurred earlier than peak flowering.A lthoff et al. 2000; Cascante-Marin et al. 2009; Oguro and Sakai 2009; (2005) suggested that, because pollinator larvae develop Rodriguez-Rodriguez and Valido 2011), a reduction of pol- within flowers and fruits, pollinators may be under selec- len (Weiss 1996; Krupnick and Weis 1999; McCall 2010), tion to emerge early in order to avoid increased larval mor- and reduced seed set due to florivore feeding (Louda and tality caused by florivory, primarily through floral abscis- Potvin 1995; Krupnick and Weis 1999). In addition, flori- sion. Later, Segraves (2008) demonstrated that the beetle vores may create indirect negative effects due to changes H. densus consumes pollinator moth eggs while feeding on in nectar production (Irwin and Brody 1998, 2011), flower style tissue in Y. filamentosa flowers. attractiveness, and inflorescence attractiveness (Leav- In this study, we used two approaches to examine the itt and Robertson 2006; McCall 2008; Cardel and Koptur direct effects of the leaf-footed bugs and beetles on plants 2010; Sober et al. 2010) that cause pollinators to reduce and moth pollinators. First, we examined the mechanistic time spent foraging within flowers and patches, while, in basis by which each of these florivore species may affect some cases, pollinators may avoid damaged flowers/inflo- seed set and pollen availability in Y. filamentosa. Specifi- rescences altogether (Irwin 2000; Leavitt and Robertson cally, we used independent experimental manipulations 2006; Botto-Mahan et al. 2011). These direct and indirect of adult leaf-footed bug and beetle densities on naturally effects have been shown to constrain the evolution of plant occurring plants to test if feeding increased floral abscis- traits associated with pollinator attraction, especially when sion and decreased pollen availability. Because leaf-footed florivores use the same cues to find flowers as pollinators bugs feed on xylem and phloem in buds, flowers, and fruit, (Theis 2006; Theis et al. 2007; Kessler et al. 2008; Galen we additionally tested whether this florivore reduced seed et al. 2011; Lay et al. 2011; Theis and Adler 2011). set in retained flowers. Second, we performed daily surveys Given that florivores are a common component of plant– of the florivores and measurements of flowering traits and pollinator communities, they have the potential to influence seed set from flowering periods in each of 3 years. Based the ecological and evolutionary dynamics of many plant– on these surveys, we used path analysis to elucidate the pollinator interactions (McCall and Irwin 2006). Although pattern of phenotypic selection on flowering traits and the the impact of florivores has been studied widely in a num- role of florivores in influencing this pattern. We also exam- ber of facultative mutualisms, their effects on obligate ined the effect of florivores on the pollinator larval loads mutualism remain relatively unstudied. This is somewhat within Y. filamentosa fruit. surprising as obligate mutualisms are used frequently in theoretical treatments of mutualism because these interac- tions are simple, often involving only a pair of mutualist Materials and methods species. From this perspective, obligate mutualisms are an excellent starting point for examining the influence of flo- Study species rivores and other antagonists on mutualism, and a strong theoretical framework in which to place these additional Yucca filamentosa (Agavaceae) is a native perennial interactors already exists (e.g., Bronstein et al. 2003; Mor- growing in disturbed areas throughout the southeastern ris et al. 2003; Jones et al. 2009).
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