Components Of Plant Fitness Research Articles

Integration of root phenes for soil resource acquisition

Suboptimal availability of water and nutrients is a primary limitation to plant growth in terrestrial ecosystems. The acquisition of soil resources by plant roots is therefore an important component of plant fitness and agricultural productivity. Plant root systems comprise a set of phenes, or traits, that interact. Phenes are the units of the plant phenotype, and phene states represent the variation in form and function a particular phene may take. Root phenes can be classified as affecting resource acquisition or utilization, influencing acquisition through exploration or exploitation, and in being metabolically influential or neutral. These classifications determine how one phene will interact with another phene, whether through foraging mechanisms or metabolic economics. Phenes that influence one another through foraging mechanisms are likely to operate within a phene module, a group of interacting phenes, that may be co-selected. Examples of root phene interactions discussed are: (1) root hair length × root hair density, (2) lateral branching × root cortical aerenchyma (RCA), (3) adventitious root number × adventitious root respiration and basal root growth angle (BRGA), (4) nodal root number × RCA, and (5) BRGA × root hair length and density. Progress in the study of phenes and phene interactions will be facilitated by employing simulation modeling and near-isophenic lines that allow the study of specific phenes and phene combinations within a common phenotypic background. Developing a robust understanding of the phenome at the organismal level will require new lines of inquiry into how phenotypic integration influences plant function in diverse environments. A better understanding of how root phenes interact to affect soil resource acquisition will be an important tool in the breeding of crops with superior stress tolerance and reduced dependence on intensive use of inputs.

Tracing impacts of partner abundance in facultative pollination mutualisms: from individuals to populations

Partner abundance affects costs and benefits in obligate mutualisms, but its role in facultative partnerships is less clear. We address this gap in a pollination web consisting of two clovers (Trifolium) that differ in specialization on a bumble bee pollinator Bombus balteatus. We examine how pollination niche breadth affects plant responses to pollinator abundance, comparing early-flowering (specialized) and late-flowering (generalized) cohorts of T. parryi and early T. parryi to T. dasyphyllum, a pollination generalist. Co-pollinators disrupt the link between B. halteatus visitation and pollination rate for both clovers. Only for early-flowering T. parryi do visitation, pollination, and seed set increase with density of B. balteatus. Bumble bee density also alters timing of seed germination in T. parryi, with seeds from plants receiving augmented B. balteatus germinating sooner than seeds of open-pollinated counterparts. Benefits saturate at intermediate bumble bee densities. Despite strong effects of B. balteatus density on individual plant fitness components, population models suggest little impact of B. balteatus density on lamda in T. parryi or T. dasyphyllum. Findings show that functional redundancy in a pollinator guild mediates host-plant responses to partner density. Unexpected effects of pollinator density on life history schedule have implications for recruitment under pollinator decline.

Molecular mechanisms of seed dormancy

Seed dormancy is an important component of plant fitness that causes a delay of germination until the arrival of a favourable growth season. Dormancy is a complex trait that is determined by genetic factors with a substantial environmental influence. Several of the tissues comprising a seed contribute to its final dormancy level. The roles of the plant hormones abscisic acid and gibberellin in the regulation of dormancy and germination have long been recognized. The last decade saw the identification of several additional factors that influence dormancy including dormancy-specific genes, chromatin factors and non-enzymatic processes. This review gives an overview of our present understanding of the mechanisms that control seed dormancy at the molecular level, with an emphasis on new insights. The various regulators that are involved in the induction and release of dormancy, the influence of environmental factors and the conservation of seed dormancy mechanisms between plant species are discussed. Finally, expected future directions in seed dormancy research are considered.

Simulation of environmental and genotypic variations of final leaf number and anthesis date for wheat

The rate of organ emergence and the duration of developmental phases are key components of plant fitness to its environment. Here, we describe a hybrid genetic algorithm for the estimation of the parameters of complex non-linear simulation models that we used to estimate the varietal parameters of a well-evaluated ecophysiological model (Sirius) of wheat phenology. The aim of this study was to analyze the correlations between the varietal parameters of Sirius and to determine the minimum number of parameters that need to be estimated in order to accurately simulate the effect of the genotype and environment on wheat anthesis date. A panel of 16 bread wheat cultivars was grown under controlled conditions with different vernalization and daylength treatments and in a field nursery with different sowing dates in order to characterize their vernalization and photoperiodic requirements and earliness per se. These cultivars were also grown in the field in two consecutive growing seasons in France and in the UK along a 800km latitude transect, where the dynamics of leaf appearance and anthesis date were determined. Variation in both final leaf number and anthesis date in response to the environment and the genotype was predicted with a mean error of 0.55 leaves and 3.94d, respectively, after estimation of only three of the seven varietal parameters of Sirius: the phyllochron, the response of vernalization rate to temperature, and the daylength response of leaf production. Among them, the phyllochron was reasonably well estimated and showed a positive association with earliness per se (Spearman's coefficient of rank correlation=0.59). This study showed that the number of varietal parameters in Sirius was overestimated and that considering only three varietal parameters reduced the correlations between the parameters and the root mean square error of prediction for final leaf number and anthesis date. We conclude that a phenomenogical model of wheat development can be used to estimate key phenological parameters that are difficult to determine in the field; offering the possibility to conduct large-scale quantitative genetic studies to understand better the genetic control of flowering time in cereals.

Floral Mimicry Enhances Pollen Export: The Evolution of Pollination by Sexual Deceit Outside of the Orchidaceae

Although the majority of flowering plants achieve pollination by exploiting the food‐seeking behavior of animals, some use alternative ploys that exploit their mate‐seeking behavior. Sexual deception is currently known only from the Orchidaceae and almost always involves pollination by male hymenoptera. An outstanding problem has been to identify the selective factors in plants that favor exploitation of mating versus feeding behaviors in pollinators. Here we show that the insectlike petal ornaments on inflorescences of the daisy Gorteria diffusa elicit copulation attempts from male bombyliid flies and that the intensity of the mating response varies across geographical floral morphotypes, suggesting a continuum in reliance on feeding through mating responses for pollination. Using pollen analogues applied to a morphotype with prominent insectlike petal ornaments, we demonstrate that mate‐seeking male flies are several‐fold more active and export significantly more pollen than females. These results suggest that selection for traits that exploit insect mating behavior can occur through the male component of plant fitness and conclusively demonstrates pollination by sexual deception in Gorteria, making this the first confirmed report of sexual deception outside of the Orchidaceae.

The seed dispersal catapult of Cardamine parviflora (Brassicaceae) is efficient but unreliable

Seed dispersal performance is an essential component of plant fitness. Despite their significance in shaping performance, the mechanical processes that drive dispersal are poorly understood. We have quantified seed dispersal mechanics in Cardamine parviflora (Brassicaceae), a ballistic disperser that launches seeds with specialized catapult-like structures. To determine which aspects of catapult function dictate interspecific dispersal differences, we compared this disperser with other ballistic dispersers. Comparison with brassicas that lack ballistic dispersal may also provide insight into the evolution of this mechanism. • Catapult performance was quantified using high-speed video analysis of dehiscence, ballistic modeling of seed trajectories, and measuring the mechanical energy storage capacity of the spring-like siliqua valve tissue that launched the seeds. • The siliquae valves coiled rapidly outward, launching the seeds in 4.7 ± 1.3 ms (mean ± SD, N = 11). Coiling was likely driven by the bilayered valve structure. The catapult was 21.3 ± 10.3% efficient (mean ± SD, N = 11) at transferring stored elastic energy to the seeds as kinetic energy. The majority of seeds (71.4%) were not launched effectively. • The efficiency of the C. parviflora catapult was high in comparison to that of a ballistic diplochore, a dispersal mode associated with poor ballistic performance, although the unreliability of the launch mechanism limited dispersal distance. Effective launching requires temporary seed-valve adhesion. The adhesion mechanism may be the source of the unreliability. Valve curvature is likely driven by the bilayered valve structure, a feature absent in nonballistic brassicas.

Plant glandular trichomes mediate protective mutualism in a spider–plant system

1. Although several species of Peucetia (Oxyopidae) live strictly in association with plants bearing glandular trichomes worldwide, to date little is known about whether these associations are mutualistic.2. In this study we manipulated the presence of Peucetia flava on the glandular plant Rhynchanthera dichotoma in the rainy and post‐rain season, to test the strength of its effects on leaf, bud, and flower damage and plant reproductive output. In addition, we ran independent field experiments to examine whether these sticky structures improve spider fidelity to plants.3. Peucetia suppressed some species of foliar phytophages, but not others. Although spiders have reduced levels of leaf herbivory, this phenomenon was temporally conditional, i.e. occurred only in the post‐rain but not in the rainy season. Floral herbivory was also reduced in the presence of spiders, but these predators did not affect plant fitness components.4. Plants that had their glandular trichomes removed retained fewer insects than those bearing such structures. Spiders remained longer on plants with glandular trichomes than on plants in which these structures had been removed. Isotopic analyses showed that spiders that fed on live and dead labelled flies adhered to the glandular hairs in similar proportions.5. Spiders incurred no costs to the plants, but can potentially increase individual plant fitness by reducing damage to reproductive tissues. Temporal conditionality probably occurred because plant productivity exceeded herbivore consumption, thus dampening top‐down effects. Specialisation to live on glandular plants may have favoured scavenging behaviour in Peucetia, possibly an adaptation to periods of food scarcity.

Cryptic bracts facilitate herbivore avoidance in the mycoheterotrophic plant Monotropsis odorata (Ericaceae)

Plant coloration, shown to play a dynamic role in animal attraction, has been proposed as a means of defense, although these reports lack experimental evidence. This study empirically assesses defensive coloration in the mycoheterotrophic plant, Monotropsis odorata, which produces stems and flowers covered by dried vegetative bracts. Field studies were conducted using an experimental group of plants with bracts removed and a control group to evaluate the frequency of and fitness impacts associated with herbivory. Additionally, we quantitatively assessed the reflectance spectra of bracts, stems, and flowers of M. odorata relative to an ambient leaf litter substrate. Across the 2-yr study, the experimental group experienced a 20-27% higher mean herbivory rate and 7-20% lower mean fruit production relative to the control group. Bracts were shown to strongly resemble ambient leaf litter in spectral analyses, with stems and flowers having more conspicuous coloration. Results show that the presence of dried bracts effectively camouflages conspicuous stem and floral tissues, significantly reducing the frequency of floral and stem herbivory, and thereby increasing fruit set, a component of plant fitness. This study supports the principal hypothesis that coloration can play a fundamental role in plant defense.

The sweet smell of success: floral scent affects pollinator attraction and seed fitness in Hesperis matronalis

Summary 1Patterns of floral scent are generally assumed to have been shaped by pollinator-mediated natural selection. However, while many studies document behavioural responses of pollinators to floral scent, few document the relationship between floral scent and fitness. 2In this study, we explore the effect of variation in floral scent emission in colour polymorphic Hesperis matronalis on both pollinator visitation and seed fitness. 3Using target inflorescences augmented with colour-specific floral scent extracts, we find that diurnal floral visitors significantly prefer night-scent extracts to non-augmented controls; inflorescences augmented with day-scent extracts receive an intermediate level of visits. Colour did not have a significant effect on visitation. 4We characterized the relationship between natural variation in floral scent emission rate and seed production for plants under two settings: in small experimental arrays exposed to either day- or night-flying pollinators, and in wild populations exposed to all pollinators. In arrays, we found greater emission rate led to higher seed production, but only in plants exposed to day-flying pollinators. In contrast, we found a significant positive relationship between night-time floral emission rate and seed fitness in wild populations. In neither setting did floral anthocycanin concentration (colour) affect fitness. 5This study reinforces the idea that scent-mediated pollinator visitation is an important component of plant fitness. Moreover, our results suggest that plants emitting more scent have higher fitness, although there is variation as to when this positive relationship occurs (i.e., at day or night). Research connecting floral scent and fitness is a necessary first step in understanding the evolution of floral scent.

TRAIT‐MEDIATED EFFECTS ON FLOWERS: ARTIFICIAL SPIDERS DECEIVE POLLINATORS AND DECREASE PLANT FITNESS

Although predators can affect foraging behaviors of floral visitors, rarely is it known if these top-down effects of predators may cascade to plant fitness through trait-mediated interactions. In this study we manipulated artificial crab spiders on flowers of Rubus rosifolius to test the effects of predation risk on flower-visiting insects and strength of trait-mediated indirect effects to plant fitness. In addition, we tested which predator traits (e.g., forelimbs, abdomen) are recognized and avoided by pollinators. Total visitation rate was higher for control flowers than for flowers with an artificial crab spider. In addition, flowers with a sphere (simulating a spider abdomen) were more frequently visited than those with forelimbs or the entire spider model. Furthermore, the presence of artificial spiders decreased individual seed set by 42% and fruit biomass by 50%. Our findings indicate that pollinators, mostly bees, recognize and avoid flowers with predation risk; forelimbs seem to be the predator trait recognized and avoided by hymenopterans. Additionally, predator avoidance by pollinators resulted in pollen limitation, thereby affecting some components of plant fitness (fruit biomass and seed number). Because most pollinator species that recognized predation risk visited many other plant species, trait-mediated indirect effects of spiders cascading down to plant fitness may be a common phenomenon in the Atlantic rainforest ecosystem.

The Relationship of Within-Host Multiplication and Virulence in a Plant-Virus System

BackgroundVirulence does not represent any obvious advantage to parasites. Most models of virulence evolution assume that virulence is an unavoidable consequence of within-host multiplication of parasites, resulting in trade-offs between within-host multiplication and between-host transmission fitness components. Experimental support for the central assumption of this hypothesis, i.e., for a positive correlation between within-host multiplication rates and virulence, is limited for plant-parasite systems.Methodology/Principal FindingsWe have addressed this issue in the system Arabidopsis thaliana-Cucumber mosaic virus (CMV). Virus multiplication and the effect of infection on plant growth and on viable seed production were quantified for 21 Arabidopsis wild genotypes infected by 3 CMV isolates. The effect of infection on plant growth and seed production depended of plant architecture and length of postembryonic life cycle, two genetically-determined traits, as well as on the time of infection in the plant's life cycle. A relationship between virus multiplication and virulence was not a general feature of this host-parasite system. This could be explained by tolerance mechanisms determined by the host genotype and operating differently on two components of plant fitness, biomass production and resource allocation to seeds. However, a positive relationship between virus multiplication and virulence was detected for some accessions with short life cycle and high seed weight to biomass ratio, which show lower levels of tolerance to infection.Conclusions/SignificanceThese results show that genotype-specific tolerance mechanisms may lead to the absence of a clear relationship between parasite multiplication and virulence. Furthermore, a positive correlation between parasite multiplication and virulence may occur only in some genotypes and/or environmental conditions for a given host-parasite system. Thus, our results challenge the general validity of the trade-off hypothesis for virulence evolution, and stress the need of considering the effect of both the host and parasite genotypes in analyses of host-parasite interactions.

Nitrogen cycling dynamics in the carnivorous northern pitcher plant, Sarracenia purpurea

Summary 1In nutrient-poor environments, plants employ many strategies to acquire and recycle scarce nutrients. Predictable relationships among a variety of leaf traits, including leaf nitrogen (N) suggest that how plants obtain, use, store and re-use N is a major component of plant fitness. The northern pitcher plant, Sarracenia purpurea, receives nitrogen from multiple sources: NH4 and NO3 dissolved in precipitation; N mineralized from captured prey; the scant N in saturated peat; and N remobilized from storage. In two greenhouse experiments, we examined N cycling in S. purpurea and consider how these dynamics relate to prior observations that this carnivorous plant has an unusually low photosynthetic rate for its tissue N content. 2In the first experiment we assessed assimilation, translocation, storage and remobilization of 15N supplied to pitchers and roots. In the second experiment, we examined how 15N assimilated by the first pitcher produced at the start of the growing season contributed to the production and maintenance of subsequent pitchers, roots and rhizomes. 3Patterns of N cycling were similar at the individual-leaf and whole-plant level. Pitchers assimilated 55%–69% of available 15N and served as both the largest sink for newly assimilated N (> 90% of the 15N assimilated during 2004) and the largest source of N remobilization the following spring. In contrast, N assimilated by roots was low and accounted for < 2·5% of the overall S. purpurea N budget. Sarracenia purpurea used both stored N and newly-acquired N throughout the growing season. The importance of stored N decreased throughout the growing season as newly assimilated N contributed more to later pitcher production. 4Our detailed mechanistic analysis of nitrogen cycling dynamics of S. purpurea suggests why this plant has a low photosynthetic rate for its tissue N content. Excess nitrogen is stored for future use, and production of new pitchers is primarily aimed at enhancing prey capture rather than increasing photosynthetic tissue.

Population-level Consequences of Herbivory Timing in Trillium Grandiflorum

The timing of herbivory may have important consequences to components of plant fitness as well as the growth rate and persistence of plant populations. Specifically, this study examines whether the timing of herbivory by white-tailed deer (Odocoileus virginianus) affects the population dynamics of the long-lived herb, Trillium grandiflorum. This study combines results from a clipping experiment with demographic matrix modeling in four different T. grandiflorum populations to determine how both the frequency and timing of herbivory alter the population growth rate. Herbivory early, but not late in the season, increased the probability that reproductive plants fail to reproduce in the next year. Both early and late season herbivory resulted in a complete loss of reproductive success in the current year. Because the growth rates of these populations were sensitive to changes in the fate of reproductive plants, but insensitive to changes in annual fecundity, early season herbivory was more detrimental to population growth rates than late season herbivory. Plant persistence may depend as much on the timing of herbivory as it does its frequency.

Limits to reproductive success of Sarracenia purpurea (Sarraceniaceae)

Plant biologists have an enduring interest in assessing components of plant fitness and determining limits to seed set. Consequently, the relative contributions of resource and pollinator availability have been documented for a large number of plant species. We experimentally examined the roles of resource and pollen availability on seed set by the northern pitcher plant Sarracenia purpurea. We were able to distinguish the relative contributions of carbon (photosynthate) and mineral nutrients (nitrogen) to reproductive success. We also determined potential pollinators of this species. The bees Bombus affinis and Augochlorella aurata and the fly Fletcherimyia fletcheri were the only floral visitors to S. purpurea that collected pollen. Supplemental pollination increased seed set by <10%, a much lower percentage than would be expected, given data from noncarnivorous, animal-pollinated taxa. Seed set was reduced by 14% in plants that could not capture prey and by another 23% in plants whose pitcher-shaped leaves were also prevented from photosynthesizing. We conclude that resources are more important than pollen availability in determining seed set by this pitcher plant and that reproductive output may be another "cost" of the carnivorous habit.

Population structure effect on reproduction of a rare plant: beyond population size effect

Several studies have evaluated the effect of population size on plant reproductive output, but there are few studies concerning the effect of other population structure variables on plant reproduction. In this study, we went beyond population size effect and we tested the effect of some population spatial variables such as plant density, plant aggregation, population structure, and population identity on plant reproductive success and fitness in large populations (&gt;1000 individuals) of Centaurea hyssopifolia Vahl., an endemic species of central Spain. We analysed the reproductive output (capitula, flowers, and seeds) and another two components of plant fitness (seed mass and germinability) in 350 individuals from seven populations in 2002 and 2003. All populations were similar in size but differed in other population spatial characteristics (density, plant aggregation pattern, population plant size structure). We used Morisita’s aggregation index to characterize the level of plant aggregation within populations. Population plant size structure variable determined the proportion of different sized plants in a population. We used generalized linear mixed models to model the contribution of these population spatial variables to several reproductive parameters. Our results showed that whereas the aggregation index exerted a positive control on plant seed set, plant density had a negative effect, and plant population size structure did not significantly influence any response variable. Density only exerted a negative effect on seed set. On the contrary, plant aggregation had a positive effect. Seed mass was also larger in more aggregated populations, although no differences in seed germinability were observed. We detected the effect of population attributes on reproduction in terms of seed set, but we did not detect any effect on other overall reproductive variables measured at plant level. To sum up, our results showed that if population fragments were large enough, spatial population attributes became crucial factors for plant reproductive output and fitness. These easily measurable population variables may improve the conservation management of rare plant species.

Size-dependent reproductive effort in Amaranthus retroflexus: the influence of planting density and sowing date

Size-dependent reproductive effort is an important component of plant fitness. The responses of reproductive effort to environmental factors in Amaranthus retroflexus L. were measured in two experiments. A wide range of selection pressures were generated by manipulating the sowing date (29 April, 23 May, 18 June, and 14 July) and planting density (13.4, 36, 121, and 441 plants·m–2). Allometric analysis between reproductive biomass and vegetative biomass across treatments showed that reproductive effort increased with size in response to different planting densities but decreased with size in sowing dates experiment. The allometric exponent between treatments was not influenced by planting densities but had significant variation with sowing date. Total branch length could explain most of the variation of reproductive accumulation and allocation in planting density experiments. For the plants with different sowing dates, total branch length was the main determinant of reproductive biomass, while reproductive effort mainly depended on the number of primary branches per unit stem mass. Architectural constraints with size result in size-dependent reproduction. Size-dependent reproduction in A. retroflexus was influenced by available resources and environmental conditions through the mechanisms of self-regulation of architectural traits.

Forest fragmentation and plant reproductive success: a case study in four perennial herbs

We assessed the effects of habitat fragmentation on reproductive success in natural populations of four forest herbs with differing life-history traits and whose distribution patterns appeared to be negatively affected by decreased habitat size and/or increased isolation: Carex sylvatica, Galium odoratum, Sanicula europaea and Veronica montana. Our aims were to test (1) whether habitat size and isolation are positively correlated with population size and isolation, respectively, (2) whether plant reproductive success, a major component of plant fitness, is reduced in small and/or isolated populations when also accounting for differences in habitat quality (edaphic conditions, light intensity) and the effects of plant size, and (3) whether species with different life histories are affected differently. There were significant positive relationships between habitat and population size and between habitat and population isolation in some, but not all of the species. We mostly found no negative effects of small population size or isolation on reproduction. However, reproductive success was reduced in small populations of Sanicula, and this effect was independent of differences in plant size and environmental conditions. The reduced fecundity in small populations may be a consequence of the Allee-effect, a possible mechanism being pollen limitation. Furthermore, the proportion of flowering ramets was reduced in small and isolated populations of Galium, which may have been caused by changes in population structure. Lastly, we found some evidence for largely outcrossing, non-clonal species to be more sensitive to reductions in population size, at least in terms of their reproductive success.

EARLY EMERGENCE ENHANCES PLANT FITNESS: A PHYLOGENETICALLY CONTROLLED META-ANALYSIS

The time at which a seedling emerges can determine its future success as a plant. Despite the large number of studies that have examined the effect of emergence time on different components of plant fitness (survival, growth, and/or fecundity), the potential evolutionary response to selection on seedling emergence date is still poorly known. In this study, we review 55 of those studies by a random-effects meta-analysis, considering the phylogenetic relatedness among taxa. We test the following hypotheses: (1) early emergence increases seedling survival, growth, and fecundity, (2) early emergence is more advantageous to large-seeded species than to small-seeded ones, as the former can compensate for the lower number of seeds by increasing seedling survival, (3) perennial plants benefit more than annuals from early emergence, as the iteroparity of the former allows them to risk seedling emergence to the best conditions each year, whereas the semelparity of the latter forces them to spread the risk of emergence over time, and (4) the effect of emergence time may depend upon the experimental conditions (field vs. controlled experiments in a greenhouse or laboratory). Our results show that early emergence differentially affects components of plant fitness, with no effect on seedling survival but large benefits to seedling growth and fecundity. Such effects vary depending upon intrinsic factors like seed size or life-form, and also upon methodology (census time and experimental conditions). Large-seeded species gain from emerging early by growing more during their first growing seasons, although they survive and reproduce similarly to small-seeded species. The survival benefit of early emergence is greater in perennial than in annual species, thus supporting hypothesis 3. The relationship between emergence time and seedling growth appears to be stronger under controlled conditions than in the field, probably as a result of the unlimited nutrient and water resources of the former. In field conditions, in contrast, limited resources probably decelerate the growth of early seedlings, precluding the detection of differences between these and late seedlings.

Crab spiders show mixed effects on flower-visiting bees and no effect on plant fitness components

:Predation on flower-visiting insects can potentially reduce pollination levels and hence plant fitness. We tested this prediction in a field experiment with 10 matched pairs of milkweed patches in which one patch in each pair contained crab spiders and the other patch was predator free. Significantly fewer honeybees were observed in the spider than no spider patches, but there was no spider effect on the two species of bumblebees. A possible explanation for this difference is that the honeybees suffered three times higher predation rates than the bumblebees. There were no spider effects on either the rate of pollinia removal from milkweed flowers or the number and mass of seeds produced. The results suggest that crab spiders may have only small effects on bees and plant fitness, at least where bees are abundant.

Herbivore effects on developmental instability and fecundity of holm oaks.

Plants are able to compensate for loss of tissue due to herbivores at a variety of spatial and temporal scales, masking detrimental effects of herbivory on plant fitness at these scales. The stressing effect of herbivory could also produce instability in the development of plant modules, and measures of such instability may reflect the fitness consequences of herbivory if instability is related to components of plant fitness. We analyse the relationships between herbivory, developmental instability and production of female flowers and fruits of holm oak Quercus ilex trees by means of herbivore removal experiments. Removal of leaf herbivores reduced herbivory rates at the tree level, but had no effect on mean production of female flowers or mature fruits, whereas herbivory tended to enhance flower production and had no effect on fruit abortion at the shoot level. Differences in herbivory levels between shoots of the same branch did not affect the size and fluctuating asymmetry of intact leaves. These results indicate compensation for herbivory at the tree level and over-compensation at the shoot level in terms of allocation of resources to female flower production. Removal of insect herbivores produced an increase in the mean developmental instability of leaves at the tree level in the year following the insecticide treatment, and there was a direct relationship between herbivory rates in the current year and leaf fluctuating asymmetry the following year irrespective of herbivore removal treatment. Finally, the production of pistillate flowers and fruits by trees was inversely related to the mean fluctuating asymmetry of leaves growing the same year. Leaf fluctuating asymmetry was thus an estimator of the stressing effects of herbivory on adult trees, an effect that was delayed to the following year. As leaf fluctuating asymmetry was also related to tree fecundity, asymmetry levels provided a sensitive measure of plant performance under conditions of compensatory responses to herbivory.