Effects of resource availability on tolerance of herbivory: a review and assessment of three opposing models

Although it is widely acknowledged that a plant's tolerance of herbivore damage depends on resource availability in the plant's environment, there is no consensus on whether higher resource levels lead to greater or to lower tolerance. The prevailing model, the compensatory continuum hypothesis (CCH), predicts that tolerance of herbivory should be greater in high-resource or low-competition conditions. The main rival hypothesis, the growth rate model (GRM), makes the opposite prediction: tolerance of herbivory should be greater in more stressful conditions. The tolerance predictions of a recently introduced model, the limiting resource model (LRM), are more flexible and depend on the type of resource and herbivore under consideration. We reviewed 48 studies (from 40 published articles) of plant tolerance of leaf damage in conditions differing in levels of light, inorganic nutrients, water stress, or competition. The results of 31%, 48%, and 95% of the studies were consistent with the predictions of the CCH, GRM, and LRM, respectively. Thus, by considering which resource is primarily affected by herbivory and which resource is limiting a plant's fitness, the LRM offers a substantial advance in predicting how tolerance will be affected by environmental differences in resource availability.     

Effects of mycorrhizal symbiosis on tallgrass prairie plant–herbivore interactions

Complex relationships occur among plants, mycorrhizal fungi, and herbivores. By altering plant nutrient status, mycorrhizas may alter herbivory or plant tolerance to herbivory via compensatory regrowth. We examined these interactions by assessing grasshopper preference and plant growth and fungal colonization responses to herbivory under mycorrhizal and non‐mycorrhizal conditions within tallgrass prairie microcosms. Mycorrhizal symbiosis increased plant regrowth following defoliation, and some strongly mycotrophic plant species showed overcompensation in response to herbivory when they were mycorrhizal. Although grasshoppers spent more time on mycorrhizal plants, herbivory intensity did not differ between mycorrhizal and non‐mycorrhizal plants. Aboveground herbivory by grasshoppers significantly increased mycorrhizal fungal colonization of plant roots. Thus mycorrhizas may greatly benefit plants subjected to herbivory by stimulating compensatory growth, and herbivores, in turn, may increase the development of the symbiosis. Our results also indicate strong interspecific differences among tallgrass prairie plant species in their responses to the interaction of aboveground herbivores and mycorrhizal symbionts.     

Herbivory and Stoichiometric Feedbacks to Primary Production

Established theory addresses the idea that herbivory can have positive feedbacks on nutrient flow to plants. Positive feedbacks likely emerge from a greater availability of organic carbon that primes the soil by supporting nutrient turnover through consumer and especially microbially-mediated metabolism in the detrital pool. We developed an entirely novel stoichiometric model that demonstrates the mechanism of a positive feedback. In particular, we show that sloppy or partial feeding by herbivores increases detrital carbon and nitrogen allowing for greater nitrogen mineralization and nutritive feedback to plants. The model consists of differential equations coupling flows among pools of: plants, herbivores, detrital carbon and nitrogen, and inorganic nitrogen. We test the effects of different levels of herbivore grazing completion and of the stoichiometric quality (carbon to nitrogen ratio, C:N) of the host plant. Our model analyses show that partial feeding and plant C:N interact because when herbivores are sloppy and plant biomass is diverted to the detrital pool, more mineral nitrogen is available to plants because of the stoichiometric difference between the organisms in the detrital pool and the herbivore. This model helps to identify how herbivory may feedback positively on primary production, and it mechanistically connects direct and indirect feedbacks from soil to plant production.     

The resource regulation hypothesis and positive feedback loops in plant–herbivore interactions

Resource regulation occurs when herbivory maintains or increases plant susceptibility to further herbivory by the same species. A review of the literature indicates it is a widespread plant–animal interaction involving a diverse array of herbivores. At least three mechanisms can produce this positive feedback cycle. First, phytophagous insect and mammalian herbivore damage can stimulate dormant buds to produce vigorous juvenile growth, which is preferred for further attack. Juvenilization cycles may have repeatedly evolved because herbivores are able to take advantage of a generalized plant compensatory response to any type of damage. Second, herbivores can manipulate plant source–sink relationships to attain more resources, and this alteration of plant growth may benefit subsequent herbivore generations. Third, herbivory can alter plant nutrition or defensive chemistry in a way that makes a plant susceptible to more herbivory. Resource regulation probably occurs because damage to resources preferred by the herbivores induces a generalized plant response that produces more preferred resources. Alternatively, manipulation of plant resources to induce resource regulation may have evolved in herbivores with a high degree of philopatry due to selection to alter plant resources to benefit their offspring. Resource regulation can stabilize insect population dynamics by maintaining a supply of high-quality plant resources. It can also increase the heterogeneity of host-plant resources for herbivores by altering the physiological age structure and the distribution of resources within plants. Resource regulation may have strong plant-mediated effects on other organisms that use that host plant, but these effects have not yet been explored.     

Herbivore‐induced plant responses in Brassica oleracea prevail over effects of constitutive resistance and result in enhanced herbivore attack

1. Plant responses to herbivore attack may have community‐wide effects on the composition of the plant‐associated insect community. Thereby, plant responses to an early‐season herbivore may have profound consequences for the amount and type of future attack. 2. Here we studied the effect of early‐season herbivory by caterpillars of Pieris rapae on the composition of the insect herbivore community on domesticated Brassica oleracea plants. We compared the effect of herbivory on two cultivars that differ in the degree of susceptibility to herbivores to analyse whether induced plant responses supersede differences caused by constitutive resistance. 3. Early‐season herbivory affected the herbivore community, having contrasting effects on different herbivore species, while these effects were similar on the two cultivars. Generalist insect herbivores avoided plants that had been induced, whereas these plants were colonised preferentially by specialist herbivores belonging to both leaf‐chewing and sap‐sucking guilds. 4. Our results show that community‐wide effects of early‐season herbivory may prevail over effects of constitutive plant resistance. Induced responses triggered by prior herbivory may lead to an increase in susceptibility to the dominant specialists in the herbivorous insect community. The outcome of the balance between contrasting responses of herbivorous community members to induced plants therefore determines whether induced plant responses result in enhanced plant resistance.     

Relative importance of drought,soil quality,and plant species in determining the strength of plant–herbivore interactions

1. Although studies on plant–herbivore interactions comparing different plant species are common, little is known about the importance of environmental conditions in determining variation in herbivory within single plant species. 2. This study assessed the effects of experimentally manipulated nutrient and water availability on plant palatability, and compared these differences with differences among species. The extent to which these patterns can be explained by leaf toughness and specific leaf area was also investigated. Six plant species from the subfamily Carduoideae and four free‐living leaf chewing invertebrates were used in the study. 3. Herbivore preferences were significantly affected by soil nutrients and water regime and varied among plant as well as herbivore species. Generally, herbivores preferred watered plants and plants from nutrient‐poor soil. The effects of soil nutrients and water regime differed between the plant and herbivore species. The differences between the plant species were greater than those between the environmental treatments. Differences at both levels could be partly explained by leaf toughness and specific leaf area. Leaf toughness, in particular, turned to be an important predictor indicating that herbivores preferred species with softer leaves, and species from wetter conditions with reduced leaf toughness. 4. The environmental conditions in which plants are growing have significant effects on plant palatability. Between‐species comparisons thus need to pay attention to this variation. Future studies may consider how the effects of current conditions interact with conditions of plant origin to predict possible effects of changes in environmental conditions on the intensity of plant–herbivore interactions.     

Effect of water availability on tolerance of leaf damage in tall morning glory,Ipomoea purpurea

Resource availability may limit plant tolerance of herbivory. To predict the effect of differential resource availability on plant tolerance, the limiting resource model (LRM) considers which resource limits plant fitness and which resource is mostly affected by herbivore damage. We tested the effect of experimental drought on tolerance of leaf damage in Ipomoea purpurea, which is naturally exposed to both leaf damage and summer drought. To seek mechanistic explanations, we also measured several morphological, allocation and gas exchange traits. In this case, LRM predicts that tolerance would be the same in both water treatments. Plants were assigned to a combination of two water treatments (control and low water) and two damage treatments (50% defoliation and undamaged). Plants showed tolerance of leaf damage, i.e., a similar number of fruits were produced by damaged and undamaged plants, only in control water. Whereas experimental drought affected all plant traits, leaf damage caused plants to show a greater leaf trichome density and reduced shoot biomass, but only in low water. It is suggested that the reduced fitness (number of fruits) of damaged plants in low water was mediated by the differential reduction of shoot biomass, because the number of fruits per shoot biomass was similar in damaged and undamaged plants. Alternative but less likely explanations include the opposing direction of functional responses to drought and defoliation, and resource costs of the damage-induced leaf trichome density. Our results somewhat challenge the LRM predictions, but further research including field experiments is needed to validate some of the preliminary conclusions drawn.     

Adaptive foraging of leaf‐cutter ants to spatiotemporal changes in resource availability in Neotropical savannas

1. Generalist herbivores feed on a wide and diverse set of species, but fine‐scale foraging patterns may be affected by the interplay between the quality, quantity and spatial distribution of host plants. 2. The foraging patterns of a prevalent Neotropical herbivore, the leaf‐cutter ant Atta laevigata, in the Brazilian Cerrado savannas were examined in order to determine if patterns observed are in concert with central‐place foraging predictions. 3. The results showed that A. laevigata acts as a polyphagous but highly selective herbivore, with ant attacks often resulting in partial defoliation of less‐preferred species and full defoliation of preferred ones. It was found, for the first time, that there is a strong and positive relationship between the relative attack frequency on plants from preferred species and foraging distance to the nest. This suggests a balance between the quality of plant resources harvested and costs involved in their transportation. It was also observed that colonies focused their harvest on preferred species in months with low availability of young leaves. Consequently, high herbivory rate was more frequent in plants attacked far away from the nest and in dry months. 4. These assessments highlight the fact that Atta colonies may become more selective as foraging distance to the nest increases and in response to fluctuations in the availability of palatable resources throughout the year. The results also show some dissimilarities in the foraging behaviours of A. laevigata when compared with other locations, suggesting that widely distributed herbivores may modify foraging strategies across their geographic range.     

Experimental Infection of Plants with an Herbivore-Associated Bacterial Endosymbiont Influences Herbivore Host Selection Behavior

Although bacterial endosymbioses are common among phloeophagous herbivores, little is known regarding the effects of symbionts on herbivore host selection and population dynamics. We tested the hypothesis that plant selection and reproductive performance by a phloem-feeding herbivore (potato psyllid, Bactericera cockerelli) is mediated by infection of plants with a bacterial endosymbiont. We controlled for the effects of herbivory and endosymbiont infection by exposing potato plants (Solanum tuberosum) to psyllids infected with “Candidatus Liberibacter solanacearum” or to uninfected psyllids. We used these treatments as a basis to experimentally test plant volatile emissions, herbivore settling and oviposition preferences, and herbivore population growth. Three important findings emerged: (1) plant volatile profiles differed with respect to both herbivory and herbivory plus endosymbiont infection when compared to undamaged control plants; (2) herbivores initially settled on plants exposed to endosymbiont-infected psyllids but later defected and oviposited primarily on plants exposed only to uninfected psyllids; and (3) plant infection status had little effect on herbivore reproduction, though plant flowering was associated with a 39% reduction in herbivore density on average. Our experiments support the hypothesis that plant infection with endosymbionts alters plant volatile profiles, and infected plants initially recruited herbivores but later repelled them. Also, our findings suggest that the endosymbiont may not place negative selection pressure on its host herbivore in this system, but plant flowering phenology appears correlated with psyllid population performance.     

Vertebrate herbivores and plants in the Arctic and subarctic: effects on individuals, populations, communities and ecosystems

Plants in the Arctic and subarctic face the problems posed by herbivory in addition to short growth seasons, low temperatures and low nutrient availability. Herbivores control plant performance by removing biomass, by altering resource availability, by altering the physical environment, and by changing the balance of competition. The main difference between effects of herbivores in the Arctic and at lower latitudes may be the relatively greater importance of changes in resource availability and the physical environment resulting from herbivore activity, and their consequences for plant competitive abilities.Species responses to defoliation depend primarily on growth form. Artificial defoliation of graminoids has negative effects on most species, but in the field total effects of herbivores are often neutral or even positive, resulting in increased nitrogen concentrations in shoots in many species. Shrubs are less able to respond positively to herbivory than graminoids, and although there is some evidence that deciduous shrubs recover faster than evergreen ones, the difference is not great. However, effects of herbivores on shrubs are little studied, despite their importance in the herbivore diet.Responses of individual species to increased nutrient availability vary greatly, even within a growth form. Some graminoids and shrubs show strong positive responses to fertilization while others show little or no response. These species-specific effects suggest that herbivores can alter interspecific relationships through differential responses to fertilization. Herbivores may alter plant population dynamics by altering flower or seed production, by consuming seedlings, or by altering the availability of microsites. However, no study has adequately examined this for any arctic species.Changes in community composition following removal of herbivores are the result not only of selective removal of some plant species, but also of changes in microsite availability, nutrient availability, litter accumulation, and soil characteristics. Thus, the view that abiotic factors are the overwhelming determinants of community structure in low-productivity environments is compatible with the view that herbivores exercise their influence to a large extent by altering abiotic factors.Arctic herbivores often increase total above-ground nitrogen availability (and therefore food quality) in the plant community, but increased productivity as a result of herbivores is rare. The increase in nutrient availability is probably due in part to changes in soil temperature and soil moisture following a reduction in litter accumulation.Although our knowledge of effects of herbivory on individual plants and on communities is extensive, we lack information on effects at the population level. We also do not have an adequate understanding of impacts of herbivores at different spatial and temporal scales, something which is needed to be able to make predictions about longer-term impact of herbivores in these systems.     

Consequences of sequential attack for resistance to herbivores when plants have specific induced responses

Plants in nature are attacked sequentially by herbivores, and theory predicts that herbivore-specific responses allow plants to tailor their defenses. We present a novel field test of this hypothesis, and find that specific responses of Solanum dulcamara lead to season-long consequences for two naturally colonizing herbivores, irrespective of the second herbivore to attack plants. This result indicates that responses induced by the initial herbivore made plants less responsive to subsequent attack. We show that initial herbivory by flea beetles and tortoise beetles induce distinct plant chemical responses. Initial herbivory by flea beetles lowered the occurrence of conspecifics and tortoise beetles relative to controls. Conversely, initial herbivory by tortoise beetles did not influence future herbivory. Remarkably, the experimentally imposed second herbivore to feed on plants did not modify consequences (induced resistance or lack thereof) of the first attacker. Induction of plant chemical responses was consistent with these ecological effects; i.e. the second herbivore did not modify the plant's initial induced response. Thus, canalization of the plant resistance phenotype may constrain defensive responses in a rapidly changing environment.     

Interactions between herbivory and resource availability on grazing tolerance of Leymus chinensis

Herbivory and resource interact to influence plant regrowth following grazing, but few detailed investigations on grazing tolerance at population levels are available. We conducted two pot experiments along a simulated grazing gradient (0%, 25%, 50% and 75% of shoot removal) at three water or nutrient levels to determine the interaction of resource and herbivory on Leymus chinensis, a perennial, dominant species in the eastern Eurasian steppes. Interactions between water availability and clipping intensity on the relative height growth rate (RHGR) and bud number were significant. Significant interactions between nutrient and clipping on RHGR, total biomass and specific leaf area (SLA) were also found. Total biomass and bud number, showing a unimodal curve along the clipping gradient in resource-rich environments, were highest at light clipping level, suggesting that this species has the plastic compensatory responses from under- to overcompensation. Interactions between herbivory and water or nutrient were opposite to each other. The “cooperative” interactions between water and herbivory magnified the difference in grazing tolerance of L. chinensis between high and low water treatments. The “antagonistic” interactions between nutrient and herbivory, on the other hand, were reflected in the lower tolerance to heavy clipping in the high nutrient than low nutrient treatments. Results partly support the limiting resource model (LRM). A modified and simplified graphic model of the LRM was proposed based on our results. The new LRM clearly demonstrated that “cooperative” interactions between varying water levels and clipping intensities aggravate the detrimental impacts of herbivores on plant growth and reproduction, whereas “antagonistic” interactions between nutrient and grazing alleviate the negative effects of herbivores. Biomass compensation and density compensation were identified as main mechanisms of herbivory tolerance in this clonal species.     

Can the evolution of plant defense lead to plant-herbivore mutualism?

Moderate rates of herbivory can enhance primary production. This hypothesis has led to a controversy as to whether such positive effects can result in mutualistic interactions between plants and herbivores. We present a model for the ecology and evolution of plant-herbivore systems to address this question. In this model, herbivores have a positive indirect effect on plants through recycling of a limiting nutrient. Plants can evolve but are constrained by a trade-off between growth and antiherbivore defense. Although evolution generally does not lead to optimal plant performance, our evolutionary analysis shows that, under certain conditions, the plant-herbivore interaction can be considered mutualistic. This requires in particular that herbivores efficiently recycle nutrients and that plant reproduction be positively correlated with primary production. We emphasize that two different definitions of mutualism need to be distinguished. A first ecological definition of mutualism is based on the short-term response of plants to herbivore removal, whereas a second evolutionary definition rests on the long-term response of plants to herbivore removal, allowing plants to adapt to the absence of herbivores. The conditions for an evolutionary mutualism are more stringent than those for an ecological mutualism. A particularly counterintuitive result is that higher herbivore recycling efficiency results both in increased plant benefits and in the evolution of increased plant defense. Thus, antagonistic evolution occurs within a mutualistic interaction.     

Variation in insect herbivory across a salt marsh tidal gradient influences plant survival and distribution

Herbivore damage and impact on plants often varies spatially across environmental gradients. Although such variation has been hypothesized to influence plant distribution, few quantitative evaluations exist. In this study I evaluated patterns of insect herbivory on an annual forb, Atriplex patula var. hastata, across a salt marsh tidal gradient, and performed experiments to examine potential causes and consequences of variation in herbivory. Damage to plants was generally twice as great at mid-tidal elevations, which are more frequently inundated, than at higher, less stressful, elevations at five of six surveyed sites. Field herbivore assays and herbivore preference experiments eliminated the hypothesis that plant damage was mediated by herbivore response to differences in host plants across the gradient. Alternately, greater herbivore densities in the mid-marsh, where densities of an alternate host plant (Salicornia europaea) were high, were associated with greater levels of herbivory on Atriplex, suggesting spillover effects. The effect of insect herbivores on host plant performance varied between the two sites studied more intensively. Where overall herbivore damage to plants was low, herbivory had no detectable effect on plant survival or seed production, and plant performance did not significantly differ between zones. However, where herbivore damage was high, herbivores dramatically reduced both plant survival (>50%) and fruit production (40-70%), and their effects were stronger in the harsher mid-marsh than the high marsh. Thus herbivores likely play a role in maintaining lower Atriplex densities in mid-marsh. Overall, these results suggest that variation in herbivore pressure can be an important determinant of patterns of plant abundance across environmental gradients.     

GRAZING OPTIMIZATION,NUTRIENT CYCLING,AND SPATIAL HETEROGENEITY OF PLANT‐HERBIVORE INTERACTIONS: SHOULD A PALATABLE PLANT EVOLVE?

Abstract.— Can the evolution of plant defense lead to an optimal primary production? In a general theoretical model, Loreau (1995) and de Mazancourt et al. (1998, 1999) have shown that herbivory could increase primary production up to a moderate rate of grazing intensity through recycling of a limiting nutrient, provided several conditions are fulfilled. In the present paper, we assume: (1) grazing intensity is controlled by plants through their level of palatability; and (2) plant fitness is determined by its productivity. We explore the conditions under which such an optimal production may be reached through natural selection. We model two competing plant types that differ only in palatability and are distributed in a patchy landscape determined by the plant‐herbivore interaction. Patch size is determined by herbivore behavior: herbivores recycle nutrient homogeneously within patches, but recycle nutrient proportionally to consumption between patches. The model shows that a strategy of intermediate palatability can be adaptive in response to a small herbivore that lives on and recycles nutrient around one or a few individual plants. For moderately small herbivores, plant palatability may evolve towards one of two local convergent strategies, depending on the initial conditions. For medium‐ to large‐sized herbivores, the nonpalatable strategy is always selected. We discuss the functional and evolutionary implications of these results, and suggest that the traditional dichotomy describing antagonistic and mutualistic interactions may be misleading.     

Invasive and native populations of common ragweed exhibit strong tolerance to foliar damage

Tolerance and resistance are defence strategies evolved by plants to cope with damage due to herbivores. The introduction of exotic species to a new biogeographical range may alter the plant–herbivore interactions and induce selection pressures for new plant defence strategies with a modified resource allocation. To detect evolution in tolerance to herbivory in common ragweed, we compared 3 native (North America) and 3 introduced (France) populations, grown in a common garden environment. We explored the effect of leaf herbivory on plant vegetative and reproductive traits. Plants were defoliated by hand, simulating different degrees of insect grazing by removing 0%, 50% or 90% of each leaf blade. Total and shoot dry biomasses were not affected by increasing defoliation, whereas root dry biomass and root:shoot ratio decreased significantly for native and introduced populations. Furthermore, defoliation treatments did not affect any of the plant reproductive traits measured. Hence, common ragweed displayed an efficient reallocation of resources in shoot biomass at the expense of roots following defoliation, which allows the species to tolerate herbivory without obvious costs for fitness. We did not detect any difference in herbivory tolerance between introduced and native populations, but significant differences were found in reproduction with invasive populations producing more seeds than native populations. As a result, tolerance to herbivory has been maintained in the introduced plant populations. We discuss some implications of these preliminary results for biological control strategies dedicated to common ragweed.     

Insect herbivory on water mint: you can't get there from here?

Aquatic plants are thought to have fewer herbivore species than their terrestinal counterparts, and possibly to suffer less herbivory I examined herbivory on water mint Mentha aquatica growing in and out of water and tested possible processes determining the observed pattern of leaf damage Plants growing on land had much more herbivore damage than those growing in water The most common herbivore of Mentha at the site (a chrysomelid beetle) showed no p reference for leaves from terrestrial plants over those from aquatic plants Caging aquatic plants to exclude moorhens suggested that these predators were not having a strong effect in removing insect herbivores (though this conclusion is tentative due to low insect numbers) Transplanting aquatic plants to a terrestrial location, while keeping their roots in water, resulted in marked increases in herbivore damage, relative to control aquatic plants The results suggest that the water barrier may prevent effective exploitation of emergent aquatic plants by terrestrial herbivores This may have consequences for observed patterns of herbivore richness on such plants, plant fitness, and a more speculative suggestion, for the mode of reproduction in aquatic plants     

Defence against vertebrate herbivores trades off into architectural and low nutrient strategies amongst savanna Fabaceae species

Herbivory contributes substantially to plant functional diversity and in ways that move far beyond direct defence trait patterns, as effective growth strategies under herbivory require modification of multiple functional traits that are indirectly related to defence. In order to understand how herbivory has shaped plant functional diversity, we need to consider the physiology and architecture of the herbivores and how this constrains effective defence strategies. Here we consider herbivory by mammals in savanna communities that range from semi‐arid to humid conditions. We posited that the saplings of savanna trees can be grouped into two contrasting defence strategies against mammals, namely architectural defence versus low nutrient defence. We provide a mechanistic explanation for these different strategies based on the fact that plants are under competing selection pressures to limit herbivore damage and outcompete neighbouring plants. Plant competitiveness depends on growth rate, itself a function of leaf mass fraction (LMF) and leaf nitrogen per unit mass (N_m). Architectural defence against vertebrates (which includes spinescence) limits herbivore access to plant leaf materials, and partly depends on leaf‐size reduction, thereby compromising LMF. Low nutrient defence requires that leaf material is of insufficient nutrient value to support vertebrate metabolic requirements, which depends on low N_m. Thus there is an enforced tradeoff between LMF and N_m, leading to distinct trait suites for each defence strategy. We demonstrate this tradeoff by showing that numerous traits can be distinguished between 28 spinescent (architectural defenders) and non‐spinescent (low nutrient defenders) Fabaceae tree species from savannas, where mammalian herbivory is an important constraint on plant growth. Distributions of the strategies along an LMF‐N_m tradeoff further provides a predictive and parsimonious explanation for the uneven distribution of spinescent and non‐spinescent species across water and nutrient gradients.     

Herbivores and plant defences affect selection on plant reproductive traits more strongly than pollinators

Pollinators and herbivores can both affect the evolutionary diversification of plant reproductive traits. However, plant defences frequently alter antagonistic and mutualistic interactions, and therefore, variation in plant defences may alter patterns of herbivore‐ and pollinator‐mediated selection on plant traits. We tested this hypothesis by conducting a common garden field experiment using 50 clonal genotypes of white clover (Trifolium repens) that varied in a Mendelian‐inherited chemical antiherbivore defence—the production of hydrogen cyanide (HCN). To evaluate whether plant defences alter herbivore‐ and/or pollinator‐mediated selection, we factorially crossed chemical defence (25 cyanogenic and 25 acyanogenic genotypes), herbivore damage (herbivore suppression) and pollination (hand pollination). We found that herbivores weakened selection for increased inflorescence production, suggesting that large displays are costly in the presence of herbivores. In addition, herbivores weakened selection on flower size but only among acyanogenic plants, suggesting that plant defences reduce the strength of herbivore‐mediated selection. Pollinators did not independently affect selection on any trait, although pollinators weakened selection for later flowering among cyanogenic plants. Overall, cyanogenic plant defences consistently increased the strength of positive directional selection on reproductive traits. Herbivores and pollinators both strengthened and weakened the strength of selection on reproductive traits, although herbivores imposed ~2.7× stronger selection than pollinators across all traits. Contrary to the view that pollinators are the most important agents of selection on reproductive traits, our data show that selection on reproductive traits is driven primarily by variation in herbivory and plant defences in this system.