Plant-attracted ants affect arthropod community structure but not necessarily herbivory

Abstract.  1. The effectiveness of ants as plant defenders is equivocal for plants that attract ants via extrafloral nectaries (EFNs).
2. This study focused on the myrmecophilic savannah tree Pseudocedrela kotschyi that attracts ants to EFNs and on the arthropod fauna associated with P. kotschyi . Herbivory and arthropod community composition were compared between trees that were dominated by one of three congeneric ant species, Camponotus acvapimensis , C. rufoglaucus , and C. sericeus , and between trees where ants were experimentally excluded and untreated control trees.
3. Short-term ant-exclusion experiments failed to demonstrate a consistent effect of ants on herbivory.
4. Plants dominated by different ant species differed significantly in leaf damage caused by herbivorous insects. The relative ranking of herbivory levels of the trees dominated by different ant species was persistent in three consecutive years.
5. Ants significantly reduced the abundance of different arthropod groups (Araneae, Blattodea, Coleoptera, Homoptera, non-ant Hymenoptera). Other groups, including important herbivores, seemed not to be affected (Lepidoptera, Orthoptera, Thysanoptera, Heteroptera).
6. The study suggests that the presence of ants only benefits plants when specific ant species are attracted, and protection by these ants is not counterbalanced by their negative effect on other beneficial arthropods.     

Plant defense, herbivory, and the growth of Cordia alliodora trees and their symbiotic Azteca ant colonies

The effects of herbivory on plant fitness are integrated over a plant??s lifetime, mediated by ontogenetic changes in plant defense, tolerance, and herbivore pressure. In symbiotic ant?Cplant mutualisms, plants provide nesting space and food for ants, and ants defend plants against herbivores. The benefit to the plant of sustaining the growth of symbiotic ant colonies depends on whether defense by the growing ant colony outpaces the plant??s growth in defendable area and associated herbivore pressure. These relationships were investigated in the symbiotic mutualism between Cordia alliodora trees and Azteca pittieri ants in a Mexican tropical dry forest. As ant colonies grew, worker production remained constant relative to ant-colony size. As trees grew, leaf production increased relative to tree size. Moreover, larger trees hosted lower densities of ants, suggesting that ant-colony growth did not keep pace with tree growth. On leaves with ants experimentally excluded, herbivory per unit leaf area increased exponentially with tree size, indicating that larger trees experienced higher herbivore pressure per leaf area than smaller trees. Even with ant defense, herbivory increased with tree size. Therefore, although larger trees had larger ant colonies, ant density was lower in larger trees, and the ant colonies did not provide sufficient defense to compensate for the higher herbivore pressure in larger trees. These results suggest that in this system the tree can decrease herbivory by promoting ant-colony growth, i.e., sustaining space and food investment in ants, as long as the tree continues to grow.     

Observations on the Ecology of Weaver Ants (Oecophylla smaragdina Fabricius) in a Thai Mangrove Ecosystem and Their Effect on Herbivory of Rhizophora mucronata Lam.

Ants of the genus Oecophylla are predators of other insects and are able to protect a variety of terrestrial plants against pest insects; however, observations on the ecology of these ants in mangrove forests are lacking. General observations on the ecology of Oecophylla smaragdina were carried out in a Thai mangrove forest to determine if these ants can protect their host plants in less favorable mangrove habitats. Leaf herbivory and the density of O. smaragdina ants were measured on Rhizophora mucronata trees at two sites. The results showed a negative correlation between ant density and herbivory. At both sites, the mean percent damaged leaf area was more than four times higher on trees without ants compared to “ant‐trees.” A significant negative correlation was found between tree mean percent leaf damage and the density of ants on the tree. Furthermore, on trees with ants, there was less herbivory on leaves close to ant nests compared to other leaves on the tree. Most damage was caused by chrysomelid beetles (62%) and sesarmid crabs (25%) and both types of herbivory were significantly reduced on ant‐trees.     

Top-down control of herbivory by birds and bats in the canopy of temperate broad-leaved oaks (Quercus robur)

The intensive foraging of insectivorous birds and bats is well known to reduce the density of arboreal herbivorous arthropods but quantification of collateral leaf damage remains limited for temperate forest canopies. We conducted exclusion experiments with nets in the crowns of young and mature oaks, Quercus robur, in south and central Germany to investigate the extent to which aerial vertebrates reduce herbivory through predation. We repeatedly estimated leaf damage throughout the vegetation period. Exclusion of birds and bats led to a distinct increase in arthropod herbivory, emphasizing the prominent role of vertebrate predators in controlling arthropods. Leaf damage (e.g., number of holes) differed strongly between sites and was 59% higher in south Germany, where species richness of vertebrate predators and relative oak density were lower compared with our other study site in central Germany. The effects of bird and bat exclusion on herbivory were 19% greater on young than on mature trees in south Germany. Our results support previous studies that have demonstrated clear effects of insectivorous vertebrates on leaf damage through the control of herbivorous arthropods. Moreover, our comparative approach on quantification of leaf damage highlights the importance of local attributes such as tree age, forest composition and species richness of vertebrate predators for control of arthropod herbivory.     

Do Herbivores Eavesdrop on Ant Chemical Communication to Avoid Predation?

Strong effects of predator chemical cues on prey are common in aquatic and marine ecosystems, but are thought to be rare in terrestrial systems and specifically for arthropods. For ants, herbivores are hypothesized to eavesdrop on ant chemical communication and thereby avoid predation or confrontation. Here I tested the effect of ant chemical cues on herbivore choice and herbivory. Using Margaridisa sp. flea beetles and leaves from the host tree (Conostegia xalapensis), I performed paired-leaf choice feeding experiments. Coating leaves with crushed ant liquids (Azteca instabilis), exposing leaves to ant patrolling prior to choice tests (A. instabilis and Camponotus textor) and comparing leaves from trees with and without A. instabilis nests resulted in more herbivores and herbivory on control (no ant-treatment) relative to ant-treatment leaves. In contrast to A. instabilis and C. textor, leaves previously patrolled by Solenopsis geminata had no difference in beetle number and damage compared to control leaves. Altering the time A. instabilis patrolled treatment leaves prior to choice tests (0-, 5-, 30-, 90-, 180-min.) revealed treatment effects were only statistically significant after 90- and 180-min. of prior leaf exposure. This study suggests, for two ecologically important and taxonomically diverse genera (Azteca and Camponotus), ant chemical cues have important effects on herbivores and that these effects may be widespread across the ant family. It suggests that the effect of chemical cues on herbivores may only appear after substantial previous ant activity has occurred on plant tissues. Furthermore, it supports the hypothesis that herbivores use ant chemical communication to avoid predation or confrontation with ants.     

Tree seedling responses to leaf-cutting ants herbivory in Atlantic Forest restoration sites

Leaf-cutting ants (LCA) are generalist herbivores capable of causing severe plant damage. Negative impacts of ant herbivory vary according to the density of nests and availability of palatable plants; however, it is not yet clear how these herbivores affect tropical forest restoration sites. To investigate how LCA preference affects plant species performance, we evaluated the herbivory of Atta sexdens rubropilosa on native tree species seedlings in Atlantic Forest restoration sites. We expected pioneer species to suffer higher herbivory by LCA when compared with non-pioneer species and that species with higher damage will have poorer growth and higher mortality. The experiment was conducted in three restoration sites in northern Paraná state, southern Brazil, with 1,500 seedlings of 5 pioneer and 5 non-pioneer species. Sites share similar age, stand size, tree species composition, and LCA nest density. The number of attacks, degree of leaf damage, number of leaves, plant height, and survival were recorded. Specific leaf area, leaf polyphenols, flavonoids, tannins, and nitrogen content were analyzed for each species. Plant damage was similar between pioneer and non-pioneer plant species. This could be explained by trait variability among species in each group and by LCA generalist foraging. Preferred species suffered decreases in growth and survival. Less preferred species suffered fewer ant attacks and no change in performance. Results suggest that ant herbivory can influence plant species establishment and thus species composition in restoration sites by reducing performance and increasing mortality of some, but not all species, making LCA an important ecological filter.     

Birds exploit herbivore‐induced plant volatiles to locate herbivorous prey

Arthropod herbivory induces plant volatiles that can be used by natural enemies of the herbivores to find their prey. This has been studied mainly for arthropods that prey upon or parasitise herbivorous arthropods but rarely for insectivorous birds, one of the main groups of predators of herbivorous insects such as lepidopteran larvae. Here, we show that great tits (Parus major) discriminate between caterpillar‐infested and uninfested trees. Birds were attracted to infested trees, even when they could not see the larvae or their feeding damage. We furthermore show that infested and uninfested trees differ in volatile emissions and visual characteristics. Finally, we show, for the first time, that birds smell which tree is infested with their prey based on differences in volatile profiles emitted by infested and uninfested trees. Volatiles emitted by plants in response to herbivory by lepidopteran larvae thus not only attract predatory insects but also vertebrate predators.     

Plant Ontogeny as a Conditionality Factor in the Protective Effect of Ants on a Neotropical Tree

The outcome of any interspecific interaction is often determined by the ecological context in which the interacting species are embedded. Plant ontogeny may represent an important source of variation in the outcome of ant–plant mutualisms, as the level of investment in ant rewards, in alternative (non‐biotic) defenses, or both, may be modulated by the plant's developmental stage. In addition, the abundance and identities of the ants involved in the interaction may change during ontogeny of the host‐plant. Here, we evaluated if plant ontogeny affects the interaction between ants and a savanna tree species (Caryocar brasiliense) that produces extrafloral nectar. We found fewer ants per branch and fewer species of ants per tree in juvenile than in reproductive trees of medium and large size. In addition, large‐sized reproductive trees were more likely to host more aggressive ants than were medium‐sized reproductive or juvenile trees. Such differences strongly affected the outcome of the interaction between ants and their host‐plants, as the magnitude of the effect of ants on herbivory was much stronger for large trees than for juvenile ones. The fact that we did not find significant ontogenetic variation in the concentration of leaf tannins suggests that the observed differences in herbivory did not result from a differential investment in chemical defenses among different‐sized plants. Overall, the results of our study indicate that the developmental stage of the host plant is an important factor of conditionality in the interaction between C. brasiliense and arboreal foraging ants.     

What determines conditionality in ant–Hemiptera interactions? Hemiptera habitat preference and the role of local ant activity

Abstract.  1. This paper describes spatial variation in density of a mutualist Hemiptera, and attempts to elucidate an understanding of the spatial variation in conditionality of its mutualism with ants.
2. Aggregations of the membracid treehopper, Campylenchia sp., occurred more frequently, and with higher number of individuals, in isolated trees as compared with their occurrence in the same tree species in wooded patches.
3. Using treehopper aggregations as the level of replication, there was a habitat × ant presence interaction associated with colony survival time. However, when the median survival time of all aggregations within each tree was used, only an additive effect of both habitat type and ant presence were apparent. This suggests that treehopper aggregations in some isolated trees experienced more benefit from ant presence than other trees.
4. The ant:treehopper ratio averaged over each tree was correlated with effect of ant presence on survivorship (survival time without ants/survival time with ants). Therefore, conditionality in the ant–membracid mutualism appears related to ant attendance level at the scale of individual trees.
5. Ant attendance at treehopper aggregations in isolated and matorral trees did not differ, and therefore there is no clear mechanism by which ants create the contrast in treehopper densities between the two habitat types.
6. The main force shaping initial treehopper densities in the two habitats is likely plant quality. Results suggest that growing situation (or more specifically plant health) is likely a good predictor of membracid density, while general ant activity within a tree is the best indicator of interaction strength.     

Fire Increases Insect Herbivory in a Neotropical Savanna

Fire is an important agent of disturbance in many tropical ecosystems that can potentially influence plant consumers. Nevertheless, there are few reports on whether levels of plant damage change as a result of fire. Here we present the results of a 1‐yr study evaluating the effects of fire on rates of herbivory and damage by pathogens in leaves of cerrado (Brazilian savanna) tree species. Damage by leaf chewers was over two times greater in burned than in unburned trees. Levels of damage by leaf miners, leaf scrapers, galling insects, and leaf pathogens were relatively low and increased, remained the same, or even decreased as a result of fire. Nevertheless, in all three plant species studied, total herbivore damage was significantly greater in burned than in unburned trees given the preponderance of damage caused by leaf chewers compared with the other types of damage. Leaf chewers, mainly leaf‐cutter ants, caterpillars, and grasshoppers, completely ate over 50 percent of the >2000 leaves we marked in burned trees. That our results were consistent among different plant species with contrasting leaf phenologies suggests that the observed increase in herbivory is a general phenomenon in our study system. Because herbivore pressure is augmented dramatically in recently burned areas, herbivory may act synergistically with fire in influencing the structure of cerrado vegetation.     

Benefits for plants in ant-plant protective mutualisms: a meta-analysis

Costs and benefits for partners in mutualistic interactions can vary greatly, but surprisingly little is known about the factors that drive this variation across systems. We conducted a meta-analysis of ant-plant protective mutualisms to quantify the effects of ant defenders on plant reproductive output, to evaluate if reproductive effects were predicted from reductions in herbivory and to identify characteristics of the plants, ants and environment that explained variation in ant protection. We also compared our approach with two other recent meta-analyses on ant-plant mutualisms, emphasizing differences in our methodology (using a weighted linear mixed effects model) and our focus on plant reproduction rather than herbivore damage. Based on 59 ant and plant species pairs, ant presence increased plant reproductive output by 49% and reduced herbivory by 62%. The effects on herbivory and reproduction within systems were positively correlated, but the slope of this relationship (0.75) indicated that tolerance to foliar herbivory may be a common plant response to absence of ant guards. Furthermore, the relationship between foliar damage and reproduction varied substantially among systems, suggesting that herbivore damage is not a reliable surrogate for fitness consequences of ant protection. Studies that experimentally excluded ants reported a smaller effect of ant protection on plant reproduction than studies that relied upon natural variation in ant presence, suggesting that study methods can affect results in these systems. Of the ecological variables included in our analysis, only plant life history (i.e., annual or perennial) explained variation in the protective benefit of mutualistic ants: presence of ants benefitted reproduction of perennials significantly more than that of annuals. These results contrast with other quantitative reviews of these relationships that did not include plant life history as an explanatory factor and raise several questions to guide future research on ant-plant protection mutualisms.     

Induced biotic responses to herbivory and associated cues in the Amazonian ant-plant Maieta poeppigii

Ants inhabiting ant‐plants can respond to cues of herbivory, such as the presence of herbivores, leaf damage, and plant sap, but experimental attempts to quantify the dynamic nature of biotic defenses have been restricted to a few associations between plants and ants. We studied the relationship between certain features of the ant‐shrub Maieta poeppigii Cogn. (Melastomataceae) and the presence or absence of ant patrolling on the leaf surface in plants occupied by the ant Pheidole minutula Mayr (Hymenoptera: Formicidae). We also carried out field experiments to examine ant behavior following plant damage, and the potential cues that induce ant recruitment. These experiments included clipping of the leaf apex, as well as the presentation of a potential herbivore (live termite worker) and a foliar extract from Maieta on treatment leaves. The presence of ants patrolling the leaves of M. poeppigii is influenced by the number of domatia on the plant. Ant patrolling on the leaves of M. poeppigii was constant throughout a 24 h cycle, but the mean number of patrolling ants decreased from young to mature leaves, and from leaves with domatia to those without domatia. There was an overall increase in the number of ants on experimental leaves following all treatments, compared to control leaves. Visual and chemical cues associated with herbivory are involved in the induction of ant recruitment in the Maieta–Pheidole system. The continuous patrolling behavior of ants, associated with their ability to respond rapidly to foliar damage, may result in the detection and repellence/capture of most insect herbivores before they can inflict significant damage to the leaves.     

Ant–aphid interactions on Asclepias syriaca are mediated by plant genotype and caterpillar damage

The means by which plant genotypes influence species interactions and arthropod community structure remain poorly understood. One potential, but largely unstudied mechanism is that occurring through plant genetic variation in induced responses to herbivory. Here we test whether induced responses to leaf damage and genotypic variation for induction in Asclepias syriaca influence interactions among Formica podzolica ants, the ant‐tended aphid Aphis asclepiadis, and the untended aphid Myzocallis asclepiadis. In so doing, we assess genetic variation in plant‐mediated interactions among different herbivore guilds. We conducted a three‐way factorial field experiment manipulating plant genotype, leaf damage by specialist monarch caterpillars Danaus plexippus, and ant presence, and documented effects on aphid and ant abundances. Leaf damage increased Aphis abundance in both the presence and absence of ants and Myzocallis abundance under ant exclusion. In the presence of ants, leaf damage decreased Myzocallis abundance, likely due to effects on ant–Myzocallis interactions; ants showed a positive association with Myzocallis, leaf damage increased the strength of this association (425% more ants per aphid), and this in turn fed back to suppress Myzocallis abundance. Yet, these aggregate effects of leaf damage on Myzocallis and ants were underlain by substantial variation among milkweed geno types, with leaf damage inducing lower aphid and ant abundances on some genotypes, but higher abundances on others. As a consequence, a substantial fraction of the variation in leaf damage effects on ants (R² =0.42) was explained by milkweed genetic variation in the strength and sign of leaf damage effects on Myzocallis. Although plant genetic variation influenced Aphis abundance, this did not translate into genetic variation in ant abundance, and leaf damage did not influence Aphis–ant interactions. Overall, we show that variation in induced responses to herbivory is a relevant condition by which plant genotype influences interactions in plant‐centered arthropod communities and provide novel results of effects on the third trophic level.     

Ant-plant-homopteran mutualism: how the third partner affects the interaction between a plant-specialist ant and its myrmecophyte host

By estimating relative costs and benefits, we explored the role of the homopteran partner in the protection mutualism between the myrmecophyte Leonardoxa africana T3, the ant Aphomomyrmex afer, and sap-sucking homopterans tended by ants in the tree''s swollen hollow twigs. The ants obtain nest sites and food from their host-plant (food is obtained either directly by extrafloral nectar or indirectly via homopterans). Aphomomyrmex workers patrol the young leaves of L. africana T3 and protect them against phytophagous insects. Because ants tended, either solely or primarily, coccids in some trees and pseudococcids in others, we were able to study whether the nature of the interaction was dependent on the identity of the third partner. First, the type of homopteran affects the benefits to the tree of maintaining a large ant colony. Larger colony size (relative to tree size) confers greater protection against herbivory; this relationship is more pronounced for trees whose ants tend pseudococcids than for those in which ants tend coccids. Second, for trees (and associated ant colonies) of comparable size, homopteran biomass was much larger in trees harbouring coccids than in trees with pseudococcids. Thus, the cost to the tree of maintaining ants may be greater when ants are associated with coccids. The net benefits to the plant of maintaining ants appear to be much greater with pseudococcids as the third partner. To explore how the type of homopteran affects functioning of the system, we attempted to determine which of the resources (nest sites, extrafloral nectar, and homopterans) is likely to limit ant colony size. In trees where ants tended coccids, ant-colony biomass was strongly dependent on the number of extrafloral nectaries. In contrast, in trees whose ants tended only pseudococcids, colony biomass was not related to the number of nectaries and was most strongly determined by the volume of available nest sites. We present hypotheses to explain how the type of homopteran affects functioning of this symbiosis, and discuss the implications of our study for the evolutionary ecology of ant–plant–homopteran relationships.     

<Emphasis Type="Italic">Catalpa bignonioides</Emphasis> alters extrafloral nectar production after herbivory and attracts ant bodyguards

Inducible anti-herbivore defenses are found within many plant taxa, but there are fewer examples of inducible indirect defenses that incorporate the third trophic level. This study links caterpillar foraging, herbivore-induced changes in extrafloral nectar production, and the attraction of ants to vulnerable leaves and plants. Catalpa bignonioides Walter (Bignoniaceae) uses extrafloral nectar to attract ant (Forelius pruinosus(Roger)) bodyguards in response to Ceratomia catalpae (Boisduval)(Lepidoptera: Sphingidae) herbivory. Ant density per leaf increased with the sugar content of extrafloral nectar excreted by sampled leaves, suggesting that increased nectar production could attract or retain beneficial arthropods. The masses of sucrose, fructose, glucose and all three sugars combined in the extrafloral nectar increased two- to three-fold on attacked leaves within 36 h of the experimental addition of caterpillars. Production rates for neighboring non-attacked leaves and non-attacked leaves on adjacent plants did not differ over the same time period. Ant attendance at caterpillar-attacked leaves increased two- to three-fold within 24 h of herbivory, relative to attendance at neighboring, undamaged leaves. These attacked leaves attracted the fewest ants prior to the onset of herbivory, suggesting the specialist caterpillar may avoid or be excluded from leaves with more bodyguards. The removal of leaf tissue with scissors did not alter ant attendance at damaged leaves. Mean ant attendance per leaf on attacked plants increased 6- to 10-fold after caterpillar introduction, relative to adjacent unattacked plants. The plant's biotic defense thus operates at two scales; the number of bodyguards (ant workers) on the plant increases after attack, and this increased workforce is biased towards attacked leaves within plants. Fewer caterpillars remained on plants that attracted greater numbers of ants, suggesting these bodyguards benefit the plant.     

The diversity of ant–plant interactions in the rainforest understorey tree, Ryparosa (Achariaceae): food bodies, domatia, prostomata, and hemipteran trophobionts

Ant–plant relationships, with variability in both intimacy and the trophic structure of associations, are described for the Austro-Malesian rainforest tree genus Ryparosa (Achariaceae). The range of associations involves opportunistic interactions between plants and foraging ants, mediated by food bodies, and tighter associations in which ant colonies, tending hemipteran trophobionts, reside permanently in plant structures with different degrees of adaptation to house ants. Our study provides strong baseline data to suggest that Ryparosa could become a new model system for examining the evolutionary radiation of ant-related traits. To define the diversity of ant–plant associations in Ryparosa , we first present a review of ant-plant terminology and an outline of its use in this study. Field studies of ant interactions with food bodies in myrmecotrophic R. kurrangii from Australia and the association between myrmecoxenic R. fasciculata and two Cladomyrma plant-ant species on the Malay Peninsula provide detailed examples of ant–plant interactions. An examination of herbarium material revealed a diverse range of ant–plant associations in other Ryparosa taxa. All 27 species had evidence of food body production, seven species had evidence of stem inhabitation by ants, five species had specialized stem domatia, and the domatia of R. amplifolia featured prostomata. Variation in the specificity of Ryparosa ant–plant interactions is discussed in relation to known ant partners and other ant–plant associations.  © 2007 The Linnean Society of London, Botanical Journal of the Linnean Society , 2007, 154 , 353–371.     

The role of ant-tended extrafloral nectaries in the protection and benefit of a Neotropical rainforest tree

One possible function of extrafloral nectaries is to attract insects, particularly ants, which defend plants from herbivores. We determined whether ants visiting saplings of the tree Stryphnodendronmicrostachyum (Leguminosae) provide protection (decreased plant damage due to ant molestation or killing of herbivores) and benefit (increased plant growth and reproduction associated with ant presence) to the plant. We compared ant and herbivore abundance, herbivore damage and growth of ant-visited plants and ant-excluded plants grown in sun and shade microhabitats of a 6-ha plantation in Costa Rica over a 7-month period. Results show that ants provided protection to plants not by reducing herbivore numbers but by molesting herbivores. Ants also reduced the incidence of pathogen attack on leaves. Protection was greater in the shade than in the sun, probably due to lower herbivore attack in the sun. Protection was also variable within sun and shade habitats, and this variability appeared to be related to variable ant visitation. Results also indicate that ant presence benefits the plant: ant-visited plants grew significantly more in height than ant-excluded plants. The cultivation of ants may serve as an important natural biological control in tropical forestry and agroforestry systems, where increased plant density can otherwise lead to increased herbivore attack. Received: 4 May 1998 / Accepted: 6 October 1998     

Mutualism between Maieta guianensis Aubl., a myrmecophytic melastome,and one of its ant inhabitants: ant protection against insect herbivores

Summary The hypothesis that ants (Pheidole minutula) associated with the myrmecophytic melastome Maieta guianensis defend their host-plant against herbivores was investigated in a site near Manaus, Amazonas, Brazil. M. guianensis is a small shrub that produces leaf pouches as ant domatia. Plants whose ants were experimentally removed suffered a significant increase in leaf damage compared with control plants (ants maintained). Ants patrol the young and mature leaves of Maieta with the same intensity, presumably since leaves of both ages are equally susceptible to herbivore attack. The elimination of the associated ant colony, and consequent increase in herbivory, resulted in reduced plant fitness. Fruit production was 45 times greater in plants with ants than in plants without ants 1 year after ant removal.     

Herbivore and pathogen effects on tree growth are additive,but mediated by tree diversity and plant traits

Herbivores and fungal pathogens are key drivers of plant community composition and functioning. The effects of herbivores and pathogens are mediated by the diversity and functional characteristics of their host plants. However, the combined effects of herbivory and pathogen damage, and their consequences for plant performance, have not yet been addressed in the context of biodiversity–ecosystem functioning research. We analyzed the relationships between herbivory, fungal pathogen damage and their effects on tree growth in a large‐scale forest‐biodiversity experiment. Moreover, we tested whether variation in leaf trait and climatic niche characteristics among tree species influenced these relationships. We found significant positive effects of herbivory on pathogen damage, and vice versa. These effects were attenuated by tree species richness—because herbivory increased and pathogen damage decreased with increasing richness—and were most pronounced for species with soft leaves and narrow climatic niches. However, herbivory and pathogens had contrasting, independent effects on tree growth, with pathogens decreasing and herbivory increasing growth. The positive herbivory effects indicate that trees might be able to (over‐)compensate for local damage at the level of the whole tree. Nevertheless, we found a dependence of these effects on richness, leaf traits and climatic niche characteristics of the tree species. This could mean that the ability for compensation is influenced by both biodiversity loss and tree species identity—including effects of larger‐scale climatic adaptations that have been rarely considered in this context. Our results suggest that herbivory and pathogens have additive but contrasting effects on tree growth. Considering effects of both herbivory and pathogens may thus help to better understand the net effects of damage on tree performance in communities differing in diversity. Moreover, our study shows how species richness and species characteristics (leaf traits and climatic niches) can modify tree growth responses to leaf damage under real‐world conditions.