Fitness Impacts Of Herbivory Through Indirect Effects On Plant-Pollinator Interactions In Oenothera Macrocarpa

Ecology, Jan, 2000 by Kristine Mothershead, Robert J. Marquis

Results from studies that have measured effects of natural and experimental leaf damage on floral traits suggest the potential for indirect effects through delays in flowering time (Marquis 1988, Meyer and Root 1993, Frazee and Marquis 1994, Juenger and Bergelson 1997), reduced flower number (Karban and Strauss 1993, Quesada et al. 1995, Juenger and Bergelson 1997), decreased flower size (Michaud 1991, Frazee and Marquis 1994, Strauss et al. 1996, Strauss 1997), and a reduction in quality or quantity of pollinator reward (Quesada et al. 1995, Mutikianen and Delph 1996, Strauss et al. 1996). Similarly, floral herbivores can indirectly affect plant fitness by changing floral morphology (petal or inflorescence damage), and in so doing influence the probability of pollination (Karban and Strauss 1993, Cunningham 1995, Lohman et al. 1996).

These indirect effects of both floral and foliar herbivory come through changes in pollinator behavior, and can be manifested in two ways: (1) changes in pollinator preference (i.e., whether a flower receives a visit) and (2) changes in pollinator efficiency (i.e., during a visit, how much pollen is transferred). First, decreased attractiveness of the flower to pollinators may decrease the number of visits. Several studies have shown that pollinator visitation is affected by variation in specific plant and floral traits, including inflorescence height and corolla size (Campbell 1989, Young and Stanton 1990, Johnston 1991, Johnson et al. 1995, Strauss et al. 1996). Second, during a visit, changes in floral characters may decrease effective pollen receipt and/or removal (pollinator efficiency). Here, traits such as floral tube length may determine whether the pollinator contacts sexual parts effectively (Nilsson 1988, Johnson and Steiner 1997), and variation in pollinator rewards (nectar and/or pollen) may inf luence the duration of each visit (Heinrich and Raven 1972, Galen and Plowright 1984). One study has linked herbivore-induced changes in floral morphology to pollinator preference and efficiency: in Raphanus raphanistrum, leaf damage by Pieris rapae larvae decreased flower size and pollen and nectar production, and in so doing, reduced the number of visits to the plant and the time spent on the plant during visitation (Strauss et al. 1996).

The potential for herbivores to indirectly influence female fitness depends on seed production being pollen-limited at some stage of reproduction. If pollen is not limiting, then additional pollen delivery is not likely to influence seed production. For leaf and floral herbivores to influence female reproduction indirectly via pollinators, three conditions should be met: (1) some aspect of reproduction must be pollen-limited, (2) damage must affect floral traits, and (3) pollinators must discriminate against flowers on damaged plants (pollinator preference), or be less effective pollinators during visitation (pollinator efficiency) to those flowers.

We investigated the reproductive consequences of herbivore damage on female (and not male) fitness in the hawk moth pollinated species Oenothera macrocarpa (Onagraceae) by manipulating both the level of leaf damage and the amount of pollen to the plant. Additionally, the existence of natural floral herbivory (bud damage) allowed us to examine the indirect effects of leaf and floral damage through their impact on pollinator performance and pollinator efficiency. We are not aware of previous studies that have manipulated leaf damage and pollen receipt and measured changes in floral traits to determine the relative contribution of direct and indirect effects of damage to female plant fitness. Specifically, this study addressed the following questions: (1) Is plant female fitness (fruit and seed number) limited by pollen availability in O. macrocarpa? (2) What are the effects of increased leaf damage and natural florivory on O. macrocarpa floral traits and plant female fitness? (3) How does variation in floral t raits affect pollinator preference and efficiency and plant female fitness?