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

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

KRISTINE MOTHERSHEAD [1]

University of Missouri, 8001 Natural Bridge Road, St. Louis, Missouri 63121-4499 USA

Abstract. The negative impacts of herbivores on plant fitness may include both direct and indirect effects. Direct effects on female plant fitness occur when decreased seed production is due to decreased resource availability from loss of leaf area and its attendant photosynthesis or through consumption of reproductive structures. Indirect effects occur when folivore- and florivore-mediated changes in floral traits influence pollinator preference and/or pollinator efficiency, thus reducing pollen receipt. We examined the effects of both leaf and floral herbivory (bud damage) and determined the relative contribution of direct and indirect effects of damage on female fitness through changes in floral traits for Oenothera macrocarpa (Onagraceae). The experiment was a two-factorial design that manipulated both leaf damage ([tilde]25% leaf area removed by hand) and pollen receipt (supplemental hand pollination). We then measured effects of leaf damage on floral traits (corolla diameter, floral tube length, and fl ower number) and fruit and seed set. Because herbivores damaged corollas in the bud stage in this experiment, we were also able to determine the effect of florivores on subsequent female reproduction.

Plants in the increased leaf damage treatment (33.4% leaf area loss) produced fewer flowers than natural leaf damage plants (6.5% leaf area loss), and their flowers had smaller corolla diameters and shorter floral tube lengths. Experimentally damaged plants also had 18% lower fruit set and produced 33% fewer seeds compared with natural leaf damage plants. Hand pollination increased fruit set by 60% and total seed number by 38% above that of naturally pollinated plants, demonstrating that female fitness was pollen-limited. Bud damage significantly decreased corolla diameter and floral tube length, and it led to a 68% reduction in fruit set. Hawk moths were observed preferentially visiting flowers with larger corollas, and study flowers with larger corollas had significantly increased probability of setting fruit. Additionally, seed number per fruit was positively related to floral tube length. In path analysis, we found no significant path between percentage leaf damage and female reproduction, suggesting tha t herbivores did not reduce seed production directly through decreased resource availability. Instead, we found a significant indirect path from percentage leaf damage to seed number through corolla diameter. We conclude that decreased female reproduction was due to changes in floral traits from both leaf and floral bud damage, which affected hawk moth preference (flowers with smaller corollas received fewer visits) and hawk moth efficiency of pollen delivery (flowers with shorter floral tubes had fewer seeds). This study demonstrates that herbivores can mitigate the mutualistic relationship between plants and pollinators through their effects on floral traits.

Key words: direct and indirect effects; floral herbivory; hawk moths; herbivory; leaf herbivory; Missouri Ozark glade communities; Oenothera macrocarpa; path analysis; plant-pollinator interactions; pollen limitation; pollinator efficiency; pollinator preference.

INTRODUCTION

Both herbivores and pollinators have the potential to select for changes in plant traits. Herbivores do so by decreasing plant growth (Kinsman and Platt 1984, Marquis 1984, Strauss 1991), and both female (Stephenson 1982, Marquis 1984, Edwards 1985, Meyer and Root 1993, Wise and Sacchi 1996, Juenger and Bergelson 1997) and male reproduction (Allison 1990, Quesada et al. 1995, Mutikainen and Delph 1996, Strauss et al. 1996). The plant traits that mediate a plant's interactions with its herbivores are those that confer defense (i.e., leaf trichomes, secondary chemicals, and extra-floral nectaries) and tolerance (the ability to grow, survive, and reproduce in the presence of herbivore damage). In turn, pollinators influence plant traits that mediate pollen removal and receipt within and among plants. These traits include flower shape, size, color, scent, and reward (e.g., Schemske and Horvitz 1984, Nilsson 1988, Young and Stanton 1990, Herrera 1993b, Campbell et al. 1996, Conner et al. 1996, Galen 1996, Johnson and Steiner 1997). Perhaps because separate traits are involved, as well as different animal species (in most cases), plant herbivore ecology and pollination ecology traditionally have developed as separate disciplines.

The negative impacts of herbivores on plant fitness are likely to include both the direct effects of folivory on seed production through decreased resource availability and indirect effects on mating success. Most studies of herbivore impacts on plant fitness have implicitly assumed that decreases in seed production are due to decreases in resource availability for seed production resulting from loss of photosynthetic leaf area. However, because folivores and florivores can affect floral traits and flowering phenology, some of these presumed direct effects may be due to the indirect effects of herbivory on plant--pollinator interactions. To date little attention has been paid to these potential indirect effects of leaf and floral damage (but see Karban and Strauss 1993, Lohman et al. 1996, Strauss et al. 1996, Strauss 1997).