Ecology Letters, (2006) 9: 1351–1365 doi: 10.1111/j.1461-0248.2006.00975.x REVIEW AND SYNTHESIS Florivory: the intersection of pollination and herbivory Abstract Andrew C. McCall1,2* and Plants interact with many visitors who consume a variety of plant tissues. While the Rebecca E. Irwin3 consequences of herbivory to leaves and shoots are well known, the implications of 1Center for Population Biology, florivory, the consumption of flowers prior to seed coat formation, have received less University of California, One attention. Herbivory and florivory can yield different plant, population and community Shields Avenue, Davis, CA outcomes; thus, it is critical to distinguish between these two types of consumption. 95616, USA Here, we consider the ecological and evolutionary consequences of florivory. A growing 2Department of Biology, number of studies recognize that florivory is common in natural systems and in some Denison University, Granville, cases surpasses leaf herbivory in magnitude and impact. Florivores can affect male and OH 43023, USA 3Department of Biology, female plant fitness via direct trophic effects and through altered pathways of species Dartmouth College, Hanover, interactions. In particular, florivory can affect pollination and have consequences for NH 03755, USA plant mating and floral sexual system evolution. Plants are not defenceless against *Correspondence: E-mail: florivore damage. Concepts of resistance and tolerance can be applied to plant–florivore [email protected] interactions. Moreover, extant theories of plant chemical defence, including optimal defence theory, growth rate hypothesis and growth differentiation–balance hypothesis, can be used to make testable predictions about when and how plants should defend flowers against florivores. The majority of the predictions remain untested, but they provide a theoretical foundation on which to base future experiments. The approaches to studying florivory that we outline may yield novel insights into floral and defence traits not illuminated by studies of pollination or herbivory alone. Keywords Floral herbivory, florivory, growth differentiation–balance hypothesis, growth rate hypothesis, optimal defence theory, plant mating system, pollination, resistance, tolerance. Ecology Letters (2006) 9: 1351–1365 herbivory and pollination, as damage to flowers or other INTRODUCTION reproductive tissues can have direct consumptive effects on As much as 18% of terrestrial plant biomass and 51% of gamete production or maturation (Krupnick & Weis 1999) aquatic plant biomass is consumed by herbivores, making as well as non-consumptive effects through changes in herbivory an important biotic interaction (Cyr & Pace 1993). pollination service (Krupnick et al. 1999). These direct and While significant effects of leaf herbivory on plant biomass indirect effects may affect individual plant fitness, popula- and fitness are well documented (e.g. Marquis 1984), the tions, and communities. Nonetheless, many studies have effects of florivory have been less studied. This is surprising failed to distinguish among damage to leaves and seeds vs. considering that the evolution and radiation of flowering floral tissues. Despite the recognition that floral damage can plants and insects is intertwined with opportunistic and decrease plant fitness to degrees comparable with or obligatory feeding on flowers and reproductive structures surpassing leaf damage (Strauss et al. 2004), few predictions (Ehrlich & Raven 1964). Thus, floral feeders may be exist concerning the effects of florivores on floral trait important enough to drive adaptations in plant and floral evolution and in current theories of plant defence (but see traits (Frame 2003). Florivory combines the forces of Euler & Baldwin 1996; Ashman 2002). Ó 2006 Blackwell Publishing Ltd/CNRS 1352 A. C. McCall and R. E. Irwin Review and Synthesis In this review, we outline patterns of florivory and then damage to seeds is often not visible externally, while consider how different types of floral damage can affect damage to petals or sepals may affect a plant’s overall plant fitness. Second, given that florivores damage flowers reproductive display, and may be evident to pollinators and can influence pollination, we explain how the causes (Krupnick et al. 1999) that are essential to the reproduction and consequences of florivory are linked to plant mating of many flowering species (Buchmann & Nabhan 1996). system and floral gender. Third, because florivores can Conversely, damage to seeds may be more costly for plant decrease plant fitness, we consider the mechanisms by fitness than florivory, as fertilized ovules are presumably which plants defend against florivores, including both more valuable than the unfertilized ovules found in a new resistance and tolerance, and we apply theories of chemical flower. Second, florivory is generally associated with the defence against herbivores and pathogens to make predic- removal of resource sinks, but leaf herbivory is often tions about how plants may defend flowers against associated with the removal of plant biomass important for florivores. Finally, we suggest future areas of research in photosynthate production (but see Aschan & Pfanz 2003). this field and ways in which emerging technologies can help Thus, while florivory may alter source–sink resource determine the origin and expression of defence in repro- relationships within a plant and may increase resource ductive tissues. Throughout this review, rather than formu- availability per surviving flower (Krupnick & Weis 1999), lating new theory, we extend ideas from established models leaf herbivory generally changes resource acquisition and to make testable predictions about the causes and conse- overall plant resource status and may decrease resource quences of florivory. Our findings suggest that the study of availability per surviving flower. Third, florivory and florivory may yield novel insights regarding not only herbivory can sometimes have different effects on plant ecological interactions but also may help explain the population dynamics as population growth rates can be evolution and persistence of floral traits not explained by differentially sensitive to changes at different life-history pollination pressure alone and floral defences not explained stages. For example, in annual or monocarpic species that by herbivory alone. rely on successful seed production, damage to floral or seed tissues often is more strongly linked to changes in demographic rates than damage to vegetative structures DEFINITIONS AND PATTERNS OF FLORAL (Rose et al. 2005). In some perennial plant species, similar DAMAGE trends are observed; for example, flower removal Florivory is any type of consumer-caused damage to decreased population growth rate by 20% in Primula veris developing floral buds or mature flowers before the whereas the effects of leaf tissue removal were weaker development of the seed coat and includes damage to (Garcia & Ehrlen 2002). One caveat is that any interaction bracts, sepals, petals, stamens, and pistils, as well as pollen that effects fecundity (i.e. florivory, herbivory or seed and ovules (Burgess 1991). We limit our review of damage predation) may similarly affect population growth, and the patterns to those that do not break apical dominance, and demographic consequences of florivory vs. other species we do not include nectar robbers, low-efficiency pollinators, interactions will ultimately depend on plant life history, bees that primarily consume pollen or obligate seed-eating spatial and temporal variation in attack, and the current pollination mutualists; some of these other types of plant– demographic state of the population. animal interactions have been recently reviewed (e.g. Maloof Quantifying florivory is not as straightforward as meas- & Inouye 2000; Irwin et al. 2001). Within insects, florivores uring leaf herbivory. First, because flowers are often are found in many orders with organisms displaying a variety ephemeral structures that are produced throughout the of life-history strategies and food preferences, ranging from blooming season and do not persist over the lifetime of the pollenivores (Kirk et al. 1995), to gall-makers (A. C. McCall, plant, florivory in the field can be difficult to assess unless personal observation), to generalist herbivores that eat many sampling occurs at frequent intervals throughout the other plant tissues in addition to flowers (McCall & Karban flowering season (Breadmore & Kirk 1998) or on long- 2006). lived flowers. Even though other structures like leaves and The distinguishing characteristics of florivory vs. other roots are also ephemeral over the lifetime of a plant, flowers types of plant damage are subtle, but important. First, often are only open for a few days, and often no clear record florivory is associated with damage to structures related to of damage is visible for flowers when the corolla senesces. potential reproductive output. In contrast, seed predation, Second, separating the effects of florivores vs. other both pre- and post-dispersal, is associated with the antagonists, such as seed predators, in the field and in the consumption of already-fertilized ovules at later life-history literature can be challenging. Researchers usually do not stages. Damage to seeds that have already developed can distinguish between consumption of developing seeds vs. result in different plant reproductive outcomes than other reproductive tissue, or are unable to manipulate either damage to pre-seed reproductive structures. For example, seed damage