Characterizing the Interaction Between the Bogus Yucca Moth and Yuccas: Do Bogus Yucca Moths Impact Yucca Reproductive Success?

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Characterizing the Interaction Between the Bogus Yucca Moth and Yuccas: Do Bogus Yucca Moths Impact Yucca Reproductive Success? Oecologia (2004) 140: 321–327 DOI 10.1007/s00442-004-1584-5 PLANT ANIMAL INTERACTIONS David M. Althoff . Kari A. Segraves . Jed P. Sparks Characterizing the interaction between the bogus yucca moth and yuccas: do bogus yucca moths impact yucca reproductive success? Received: 11 November 2003 / Accepted: 7 April 2004 / Published online: 29 May 2004 # Springer-Verlag 2004 Abstract Yucca moths are most well known for their within the inflorescence scape. Surveys of percent total obligate pollination mutualism with yuccas, where polli- nitrogen at three time periods during the flowering and nator moths provide yuccas with pollen and, in exchange, fruiting of Y. filamentosa also showed that larval feeding the moth larvae feed on a subset of the developing yucca decreased the amount of nitrogen in fruit tissue. Taken seeds. The pollinators, however, comprise only two of the together, the results suggest that although P. decipiens three genera of yucca moths. Members of the third genus, influences nitrogen distribution in Y. filamentosa, this Prodoxus, are the “bogus yucca moths” and are sister to physiological effect does not appear to impact the female the pollinator moths. Adult Prodoxus lack the specialized components of reproductive success. mouthparts used for pollination and the larvae feed on plant tissues other than seeds. Prodoxus larvae feed within Keywords Mutualism . Community context . Herbivory . the same plants as pollinator larvae and have the potential Plant physiology . Species interactions to influence yucca reproductive success directly by drawing resources away from flowers and fruit, or indirectly by modifying the costs of the mutualism with Introduction pollinators. We examined the interaction between the scape-feeding bogus yucca moth, Prodoxus decipiens, and Our understanding of mutualism has been based largely on one of its yucca hosts, Yucca filamentosa, by comparing studies of pairwise interactions between mutualists female reproductive success of plants with and without (Bacher and Friedli 2002; Bronstein and Barbosa 2002; moth larvae. We determined reproductive success by Stanton 2003). From these studies, we have learned that measuring a set of common reproductive traits such as the evolution and maintenance of mutualisms are depen- flowering characteristics, seed set, and seed germination. dent on the fitness benefits and costs of engaging in the In addition, we also quantified the percent total nitrogen in interaction. Mutualisms are viewed as balanced antag- the seeds to determine whether the presence of larvae onistic interactions in which the net outcome is beneficial could potentially reduce seed quality. Flowering charac- to both participants (Thompson 1982; Herre et al. 1999; teristics, seed set, and seed germination were not Bronstein 1994, 2001). This view has spurred research on significantly different between plants with and without identifying the benefits and costs across a wide range of bogus yucca moth larvae. In contrast, the percent total mutualisms and has also focused attention on model nitrogen content of seeds was significantly lower in plants systems such as the pairwise interactions in obligate with P. decipiens larvae, and nitrogen content was pollination mutualisms. For these interactions in particular, negatively correlated with the number of larvae feeding progress has been made in identifying, not only the benefits and costs, but also the mechanisms that balance D. M. Althoff (*) . K. A. Segraves these factors to prevent overexploitation by the mutualists Department of Biological Sciences, University of Idaho, themselves (Pellmyr and Huth 1994; West and Herre Rm 252 Life Sciences South, 1994; Nefdt and Compton 1996; Addicott 1998; Wilson Moscow, ID, 83844-3051, USA e-mail: [email protected] and Addicott 1998; Herre 1999; Weiblen et al. 2001; Tel.: +1-208-8858860 Segraves 2003). Although studies of these pairwise Fax: +1-208-8857905 interactions have been essential to our understanding of mutualism, we know, however, that mutualists are part of a J. P. Sparks Department of Ecology and Evolutionary Biology, Cornell greater community and must simultaneously interact with University, other species. Ithaca, NY, 14853, USA 322 Such interactions with other community members may Powell 1988; Powell 1992). Seven of the species feed directly or indirectly influence mutualisms by modifying within the inflorescence scape, three in the fruit wall, and their cost-benefit ratios (e.g., Gaume et al. 1998). To fully one as a leafminer. Unlike the wealth of information about understand the evolution and maintenance of mutualisms, the interactions between the true pollinator yucca moths we need to place them in the community context in which and yuccas, there are no studies that specifically examine they occur (Cushman and Whitham 1989; Cushman 1991; the interactions between bogus yucca moths and yuccas. Thompson and Pellmyr 1992; Thompson 1994; Bacher Characterizing these interactions is important for incorpor- and Friedli 2002; Bronstein and Barbosa 2002; Stanton ating a community context into the pollination mutualism 2003). Examining how mutualists interact with other between Tegeticula and yuccas, and for addressing community members is the first step in identifying the hypotheses about the diversification of yucca moths in direct and indirect effects third parties may have on general (Althoff et al. 2001). Moreover, recent theoretical mutualisms. models have shown that community members can influ- The specialized interactions between plants and their ence the temporal and spatial dynamics of mutualisms obligate pollinators represent good starting points for such as the one between yuccas and yucca moths incorporating a community context into studies of mutu- (Bronstein et al. 2003; Morris et al. 2003; Wilson et al. alism. The interaction between yuccas (Agavaceae) and 2003). yucca moths in the genus Tegeticula (Prodoxidae) is a In this study, we examined the interaction between a well-studied, classic example of an obligate pollination scape-feeding Prodoxus species, P. decipiens, and one of mutualism (Riley 1892; Powell 1992; Pellmyr 2003). This its hosts, Y. filamentosa. We chose this system because interaction is one of several that have formed the basis of there are already a number of studies on flowering and our knowledge about mutualisms in general, and many fruit production in Y. filamentosa (Huth and Pellmyr 1997; models of mutualism have been formulated with this Marr et al. 2000), on the costs and benefits of the interaction in mind (e.g., Bull and Rice 1991; Law et al. mutualism between Y. filamentosa and its pollinators 2001; Holland and DeAngelis 2001, 2002; Bronstein et al. (Pellmyr and Huth 1994; Huth and Pellmyr 2000; Marr 2003; Morris et al. 2003; Wilson et al. 2003). Pollinator and Pellmyr 2003), and on the impact of the cheater yucca yucca moth larvae feed exclusively on yuccas, and the moths on the mutualism (Marr et al. 2001). Specifically, female moths actively pollinate the flowers into which we asked whether P. decipiens feeding reduces the they lay eggs (Powell 1992; Pellmyr 2003). Because the reproductive success of Y. filamentosa. We addressed developing moth larvae only consume a portion of the this question in two ways. First, we compared commonly seeds within a fruit, the overall interaction is beneficial to measured components of female reproductive success such both partners. This mutualism is balanced by both intrinsic as flowering phenology, fruit set, and seed production plant factors and extrinsic mortality factors that reduce between plants in which P. decipiens was excluded and seed damage caused by moth larvae (Pellmyr and Huth those with naturally occurring densities of moth larvae. 1994; Addicott 1998; Wilson and Addicott 1998; Segraves For these plants, we also measured seed nitrogen content. 2003). The obligate nature of the interaction has made it Second, we quantified whether P. decipiens larvae repres- tractable for studying the evolution of mutualism because ent a drain on plant nutrients allocated to the entire there is usually only one or two pollinator species utilizing inflorescence, and the temporal component of this effect. a yucca species at a given locality (Pellmyr 2003). We harvested another subset of plants with naturally In addition to interacting with the pollinator moths, occurring densities of moth larvae and measured the yuccas are also utilized by other prodoxid moths that are percent nitrogen content of the scape, flower, and fruit not mutualists. Within the Tegeticula pollinator lineage, tissues. These plants were harvested at three time points two cheater species have evolved that do not pollinate, yet during the flowering and seed-provisioning periods for Y. feed on the developing seeds (Pellmyr and Leebens-Mack filamentosa. We chose to examine nitrogen content, 1999, 2000; Pellmyr 1999; Marr et al. 2001). Another because nitrogen is a key component in both seed genus of yucca specialists, Prodoxus, also does not provisioning (e.g., Parrish and Bazzaz 1985) and insect pollinate, but feeds on plant parts other than seeds larval development (Bernays and Chapman 1994; Schoon- (Davis 1967). This genus is widespread and species co- hoven et al. 1998). occur with the pollinator moths on almost every species of yucca with the possible exception of Yucca reverchoni (O. Pellmyr, personal communication). Adults rest in the Methods flowers during the day and mate within yucca flowers at night, but they lack the specialized
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