Competition, Herbivory, and Reproduction of Trichome Phenotypes of Datura Wrightii

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Competition, Herbivory, and Reproduction of Trichome Phenotypes of Datura Wrightii Ecology, 86(2), 2005, pp. 334±339 q 2005 by the Ecological Society of America COMPETITION, HERBIVORY, AND REPRODUCTION OF TRICHOME PHENOTYPES OF DATURA WRIGHTII J. DANIEL HARE1 AND JAMES L. SMITH II Department of Entomology, University of California, Riverside, California 92521 USA Abstract. The trichome dimorphism of Datura wrightii is intriguing because glandular trichome production has a high ®tness cost. Plants producing glandular trichomes (``sticky'' plants) are resistant to many insect herbivores that attack plants producing nonglandular trichomes (``velvety'' plants). When protected from herbivores, sticky plants initially pro- duce fewer seeds than velvety plants but grow to a larger size. In a three-year ®eld ex- periment, we tested the hypothesis that sticky plants acquire a competitive advantage through greater vegetative growth. In the absence of herbivores, sticky and velvety plants grew to similar sizes in their ®rst year, but sticky plants grew larger in the second and third years. Seed production of sticky plants was 46±60% less than velvety plants in their ®rst year, and this caused a 13% reduction in their ®nite rate of increase overall, even though sticky plants produced more seeds than velvety plants did in later years. The impact of herbivory varied with plant density, and herbivores reduced plant ®tness more at low plant density than at high plant density. The differences in growth associated with trichome morphology occurred too late to provide a competitive advantage to sticky plants and probably contribute little to the maintenance of D. wrightii's trichome dimorphism. Key words: competition; Datura wrightii; herbivory; polymorphism; resistance; trichomes. INTRODUCTION synergistic interactions are expected when resistance It has been dif®cult to develop generalizations con- and competitive ability are positively associated (Sie- cerning the combined effects of competition and her- mens et al. 2002). When resistance occurs at the ex- bivory on plant ®tness despite extensive research on pense of competitive ability, a number of outcomes are each factor individually. One hypothesis is that com- possible; competition may either amplify the costs of Reports petition and herbivory should affect plant performance resistance, especially on early growth under asymmet- independently (Reader and Bonser 1998), and many ric competition with low levels of damage, or amplify studies indeed ®nd such independence (Parker and the bene®ts of resistance under symmetric competition Salzman 1985, Rees and Brown 1992, Karban 1993, at high plant density and high levels of damage to Maron 2001). Independence is not universal, and dam- susceptible plants (Weis and Hochberg 2000). age by herbivores also can exacerbate (Lee and Bazzaz We studied competition and herbivory using Datura 1980) or mitigate the effects of competition (Parmesan wrightii Regel (Solanaceae). In this species, herbivore 2000, Haag et al. 2004). resistance is costly and is correlated with plant growth The lack of pattern may be in¯uenced by details of traits that may be bene®cial in a competitive environ- the experimental design. The effect of herbivory on ment. All plants produce leaf trichomes, and two phe- competition will depend upon how herbivory is dis- notypes occur (van Dam et al. 1999). ``Velvety'' plants tributed over the superior and inferior competitors. If are densely covered with short, nonglandular trichomes damage were concentrated on the inferior competitor, while ``sticky'' plants are less densely covered with then herbivory should increase the asymmetry of com- glandular trichomes. Glandular trichomes secrete acyl- petition favoring the superior competitor. If damage sugars (van Dam and Hare 1998) that confer resistance were concentrated on the superior competitor, then her- to many of D. wrightii's insect herbivores (Hare and bivory should reduce the superior competitor's advan- Elle 2002). Trichome phenotype is controlled by a sin- tage. If herbivores attack superior and inferior com- gle Mendelian gene, the sticky condition is dominant petitors similarly, then herbivory may mitigate the ef- (van Dam et al. 1999), and the frequency of sticky fects of competition overall (Gurevitch et al. 2000). plants ranges from 0 to 93% among populations (Hare Similarly, no interaction is expected between compe- and Elle 2001). tition and herbivory if competition and resistance The production of glandular trichomes is correlated mechanisms are independent (Uriarte et al. 2002), and with increased vegetative growth at the expense of ear- ly seed production (Hare et al. 2003). Although sticky Manuscript received 15 June 2004; revised 13 September plants initially produce fewer seeds than velvety plants, 2004; accepted 15 September 2004. Corresponding Editor: A. R. Zangerl. sticky plants may accrue a competitive advantage over 1 E-mail: [email protected] velvety plants by virtue of greater size at high densities. 334 February 2005 PLANT COMPETITION AND INSECT HERBIVORY 335 The cost of producing glandular trichomes might be reduced or eliminated when sticky and velvety plants are grown under suf®ciently high competition. We carried out a competition experiment in the ®eld over three years where sticky and velvety plants were grown in pure or mixed stands at three different densities (Marshall and Jain 1969, Gurevitch et al. 1990, Goldberg and Scheiner 1993), and exposed to, or protected from herbivores to test the following hypotheses: 1) Because sticky plants eventually grow larger than velvety plants, the sticky type may be the better competitor, and the advantage that velvety plants have over sticky plants should decline when plants are grown at increasing densities. FIG. 1. Distribution of nearest-neighbor distances be- 2) If the sticky type is the superior competitor, then tween individual Datura wrightii plants. Data were obtained from four populations (two sites from University of Califor- the seed production of sticky plants should be nia, Riverside, California, USA: Pictograph Trail and Mill relatively greater, and that of velvety plants should Creek; see van Dam et al. [1999] and Hare and Elle [2004] be relatively less, when grown in mixed than in for more detailed population descriptions). pure stands. 3) Herbivory and competition will act independently upon plant ®tness. competitors. Each data plant was in direct competition with six adjacent plants: the center plant, two adjacent METHODS data plants, and three nondata competitors in the out- The life history of D. wrightii in southern California side ring. We used three stand types: pure velvety, pure has been described previously (Elle et al. 1999). In sticky, and mixed. The mixed stand utilized three data brief, plants are found in sandy or gravelly disturbed plants of each type, each of which was surrounded by Reports sites in the southwestern United States and Mexico three sticky and three velvety competitors. To deter- (Avery et al. 1959). Seeds germinate during the winter mine relevant plant densities for our experiment, we rainy season, and plants ¯ower and produce seeds from surveyed 131 plants from four local populations. The April through December. The large white ¯owers are nearest-neighbor distances between plants yielded a open for one night, and, despite obvious characteristics skewed distribution ranging from 0.5 m to 12 m with favoring pollination by hawk moths (Grant and Grant a mean of 2.9 m but a mode of 1.0 m (Fig. 1). On the 1983), outcrossing averaged only 29% in previous ex- basis of this information, we replicated our stands at periments (Elle and Hare 2002). Leaves and stems se- three plant spacings: 3 m, 1 m, and 0.5 m between nesce during the winter, and new foliage is produced plants. from a storage root each spring. Plant leaf canopies We also included an herbivory treatment in which often reach 1±2 m in diameter and1minheight (Mira half of the plots were exposed to herbivorous insects and Bernays 2002, Hare et al. 2003). and the other half were protected from herbivory by Experimental conditions were similar to those used twice-monthly applications of acephate (0.63 kg/ha ac- previously (Hare et al. 2003), except that plants were tive ingredient), an insecticide that does not affect plant never irrigated after establishment. Seedlings were uti- growth (Elle et al. 1999). Applications were made be- lized from three randomly selected families originating tween 24 May and 27 September 2001, 3 April and 13 from crosses between a randomly selected velvety pol- October 2002, and 3 April and 16 October 2003. Weeds len donor and heterozygous sticky pollen acceptor from were controlled by hoeing and treatment with gly- two local populations. Because the sticky phenotype is phosate when needed. inherited as a dominant Mendelian character, the ex- There were a total of 54 plots (three densities 3 three pected ratio of sticky and velvety offspring from these stand types 3 three families 3 two herbivore treat- crosses is 1:1. Seedlings were germinated in the green- ments), 324 data plants, and 1026 plants in total. Plots house in the winter of 2000±2001 and reared until adult were separated by at least 5 m of bare soil and the trichome type could be assessed. Plants were trans- whole ®eld site was 0.6 ha in size. planted to a ®eld at Agricultural Operations, University A fully expanded leaf from each data plant protected of California, Riverside, on 19 and 20 April 2001, after from herbivores was collected in July 2001. The num- the ®eld had been furrow irrigated for 20 h. bers of glandular and nonglandular trichomes on the Plants were arrayed in hexagonal plots of 19 plants abaxial midrib of each leaf were tallied under a dis- (Harper 1977: Fig. 8/1). The center plant was surround- secting microscope using standard procedures (van ed by a hexagon of six data, or focal, plants and the Dam et al. 1999). Densities of glandular and nonglan- data plants were surrounded by an outer hexagon of 12 dular trichomes were analyzed by analyses of variance 336 J.
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