Costs and benefits for phytophagous myrmecophiles: when ants are not always available

Costs and benefits in mutualistic associations between ants and phytophagous myrmecophiles are context dependent. We collected information from the literature on costs and benefits of myrmecophily in aphids, coccids, membracids and lycaenids. A key result of the literature survey is that investment in mutualism with ants entails costs paid not only when ants are present (direct costs) but also when they are absent (indirect costs). We incorporated such a trade-off in a model that investigates the fitness consequences of the decision of a potential myrmecophile whether or not to invest in cooperation with ants. The model shows that whether myrmecophily should be favoured depends on the rate of increase of the population, and, if there are indirect costs, on the frequency of habitats with ants. Both direct and indirect costs can limit or prevent the evolution of myrmecophily even when ants are abundant. To understand the patterns of associations in the field we therefore need to measure the benefits and costs of myrmecophily both in the presence and in the absence of ants.     

Molecular substitution rate increases in myrmecophilous lycaenid butterflies (Lepidoptera)

Pellissier, L., Litsios, G., Guisan, A. & Alvarez, N. (2012). Molecular substitution rate increases in myrmecophilous lycaenid butterflies (Lepidoptera). —Zoologica Scripta, 41, 651–658. Is species diversification driven by neutral‐ or niche‐based processes? Butterflies of the Lycaenidae family have developed mutualistic interactions with ants. This biotic requirement increased the spatial fragmentation of populations of lower effective population size (Ne) compared with autonomous species. The nearly neutral theory predicts that species with smaller Ne should fix more mutations because of the increased strength of drift. Taking into account the phylogenetic relatedness among species, this study shows that species with a stronger dependence on ants displayed more intra‐specific Single Nucleotide Polymorphisms compared with species with low or no myrmecophily. This phenomenon can cause more pronounced genetic differentiation between populations and could ultimately promote speciation in a similar manner as on physical islands. The large species diversity observed in this family could be the consequence of this neutral process enhancing the diversification of lineages.     

Mutualistic ants and parasitoid communities associated with a facultative myrmecophilous lycaenid,Arhopala japonica,and the effects of ant attendance on the avoidance of parasitism

Herbivorous insects have evolved various defensive strategies to avoid their primary enemies, parasitoids. Many species of Lycaenidae (Lepidoptera) have food‐for‐protection mutualism with ants in their larval stages, where larvae produce nectar for ants and in return ants exclude parasitoids as well as predators. Myrmecophilous relationships are divided into two categories, obligate and facultative, by degrees of myrmecophily. Although parasitoids attacking obligate lycaenids always encounter lycaenid‐specific ant species, parasitoids that use facultative lycaenids are likely to encounter diverse ant species showing various defense systems. However, we know little about the parasitoid community of facultative lycaenid larvae. In this study, we investigated the mutualistic ant and parasitoid communities of a facultative myrmecophilous species, Arhopala japonica, in seven localities in Japan. The present field observation newly recorded four ant species attending A. japonica larvae, and combined with the previous data, the number of attending ant species reached 16, which is nearly the maximum number of reported attending ant species among myrmecophilous lycaenids. However, the present study revealed that almost all parasitized A. japonica larvae were attacked by a single braconid species, Cotesia sp. near inducta. We also assessed the efficiency of facultative ant defense against the parasitoid in the laboratory and revealed that oviposition by Cotesia sp. near inducta females was almost completely hindered when A. japonica larvae were attended by ants. This suggests that the dominant parasitoid does not have effective traits to overcome defensive behavior of ants and that the female wasps oviposit mainly in A. japonica larvae without intensive attendance.     

Myrmecophilous butterflies utilise ant–treehopper associations as visual cues for oviposition

1. Selection of a safe oviposition site is important for herbivorous insects whose immature stages have limited mobility. Female herbivores rely on environmental cues for this choice, and presence of natural enemies or mutualistic partners may be important in this process. 2. Some butterflies have mutualistic interactions with ants (myrmecophily), in which caterpillars offer a nutritional liquid and gain protection against natural enemies. Participants in butterfly–ant mutualisms may utilise signals to initiate interactions, but the use of visual cues by ovipositing myrmecophilous butterflies remains uncertain. 3. Larvae of facultatively myrmecophilous Parrhasius polibetes (Lycaenidae) feed on Schefflera vinosa, and females prefer to oviposit near aggregations of the ant‐tended treehopper Guayaquila xiphias, where caterpillars survive better due to increased ant attendance. Given the conspicuousness of ant–treehopper associations, it was investigated whether butterflies use them as visual cues for oviposition and, if so, which participants of the association are used as cues: ants, treehoppers, or both. 4. Experiments using dried insects on paired branches revealed that females visually recognise ants and ant–treehopper associations, using them for egg‐laying decisions. However, presence of a treehopper aggregation alone had no effect on oviposition choices. 5. This is a first insight into the importance of visual discrimination for ovipositing myrmecophilous butterflies. The results show that facultative mutualisms can be important enough to promote a behavioural adaptation (visual detection of ants) reinforcing the interaction. Our research highlights the importance of the behavioural interface within complex multispecies systems.     

High host‐plant nitrogen content: a prerequisite for the evolution of ant–caterpillar mutualism?

The amount of nitrogen required to complete an insect's life cycle may vary greatly among species that have evolved distinct life history traits. Myrmecophilous caterpillars in the Lycaenidae family produce nitrogen-rich exudates from their dorsal glands to attract ants for protection, and this phenomenon has been postulated to shape the caterpillar's host-plant choice. Accordingly, it was postulated that evolution towards myrmecophily in Lycaenidae is correlated with the utilization of nitrogen-rich host plants. Although our results were consistent with the evolutionary shifts towards high-nutrient host plants serving as exaptation for the evolution of myrmecophily in lycaenids, the selection of nitrogen-rich host plants was not confined to lycaenids. Butterfly species in the nonmyrmecophilous family Pieridae also preferred nitrogen-rich host plants. Thus, we conclude that nitrogen is an overall important component in the caterpillar diet, independent of the level of myrmecophily, as nitrogen can enhance the overall insect fitness and survival. However, when nitrogen can be obtained through alternative means, as in socially parasitic lycaenid species feeding on ant brood, the selective pressure for maintaining the use of nutrient-rich host plants is relaxed, enabling the colonization of nitrogen-poor host plants.     

保护性的蚂蚁-植物相互作用及其调节机制研究综述

蚂蚁-植物互利关系是生态和进化研究中的模式系统之一。该文分析总结了近年来有关蚂蚁对植物的保护作用及其调节机制的研究进展。植物通过给蚂蚁提供食物体、蚁菌穴和蜜露吸引蚂蚁, 通过自身的物理、化学方式调节与蚂蚁的互利关系, 使蚂蚁能有效地保护自已, 防止欺骗和寄生的发生。反过来, 蚂蚁可以减少植食性动物对植物的伤害和取食, 减少叶片损伤, 提高种子产量和质量, 提高植物的竞争优势等。虽然蚂蚁对植物的保护作用的强度受到多种生物与非生物因素的影响, 变异性较大, 但在大多数情况下, 蚂蚁-植物之间仍呈显著的正相互作用。同时, 蚂蚁-植物的相互作用还具有广泛的生态影响, 尤其会大大降低林冠上节肢动物群落的物种多样性和多度。未来的研究需要加强蚂蚁-植物互利关系的起源与维持机制、对蚂蚁自身的影响、与生物入侵的关系, 以及进化生态学等方面的研究。     

Mutualisms in a changing world: an evolutionary perspective

Ecology Letters (2010) 13: 1459-1474 ABSTRACT: There is growing concern that rapid environmental degradation threatens mutualistic interactions. Because mutualisms can bind species to a common fate, mutualism breakdown has the potential to expand and accelerate effects of global change on biodiversity loss and ecosystem disruption. The current focus on the ecological dynamics of mutualism under global change has skirted fundamental evolutionary issues. Here, we develop an evolutionary perspective on mutualism breakdown to complement the ecological perspective, by focusing on three processes: (1) shifts from mutualism to antagonism, (2) switches to novel partners and (3) mutualism abandonment. We then identify the evolutionary factors that may make particular classes of mutualisms especially susceptible or resistant to breakdown and discuss how communities harbouring mutualisms may be affected by these evolutionary responses. We propose a template for evolutionary research on mutualism resilience and identify conservation approaches that may help conserve targeted mutualisms in the face of environmental change.     

Tolerance traits and the stability of mutualism

Identifying factors which allow the evolution and persistence of cooperative interactions between species is a fundamental issue in evolutionary ecology. Various hypotheses have been suggested which generally focus on mechanisms that allow cooperative genotypes in different species to maintain interactions over space and time. Here, we emphasise the fact that even within mutualisms (interactions with net positive fitness effects for both partners), there may still be inherent costs, such as the occasional predation by ants upon aphids. Individuals engaged in mutualisms benefit from minimising these costs as long as it is not at the expense of breaking the interspecific interaction, which offers a net positive benefit. The most common and obvious defence traits to minimise interspecific interaction costs are resistance traits, which act to reduce encounter rate between two organisms. Tolerance traits, in contrast, minimise fitness costs to the actor, but without reducing encounter rate. Given that, by definition, it is beneficial to remain in mutualistic interactions, the only viable traits to minimise costs are tolerance-based 'defence' strategies. Thus, we propose that tolerance traits are an important factor promoting stability in mutualisms. Furthermore, because resistance traits tend to propagate coevolutionary arms races between antagonists, whilst tolerance traits do not, we also suggest that tolerance-based defence strategies may be important in facilitating the transition from antagonistic interactions into mutualisms. For example, the mutualism between ants and aphids has been suggested to have evolved from parasitism. We describe how phenotypic plasticity in honeydew production may be a tolerance trait that has prevented escalation into an antagonistic arms race and instead led to mutualistic coevolution.     

Chemical convergence between a guild of facultative myrmecophilous caterpillars and host plants

1. Ants exert strong selective pressure on herbivorous insects, although some caterpillars can live in symbiosis with them using chemical defensive strategies.
2. We investigated the adaptive resemblance of cuticular hydrocarbons (CHCs) in multitrophic systems involving a guild of facultative myrmecophilous caterpillar species (Lepidoptera: Lycaenidae), tending ants (Hymenoptera: Formicidae), and host plants from three families. We hypothesised that the CHCs of the caterpillars would resemble those of their host plants (chemical camouflage).
3. We analysed CHCs using gas chromatography/mass spectrometry. Morisita's similarity index (SI) was used to compare CHC profiles of caterpillar species with different types of ant associations (commensal or mutualistic), ants, and host plants.
4. We found strong convergence between caterpillars' CHCs and plants, especially for commensal species that do not provide secretion rewards for ants. Moreover, we found unexpected chemical convergence among mutualistic (trophobiotic) caterpillar species that offer caloric reward secretions to ants.
5. These results show that the studied caterpillars acquire CHCs through their diet and that they vary according to host plant species and type of ant association (commensalism or mutualism). This ‘chemical camouflage’ of myrmecophilous caterpillars may have arisen as a defensive strategy allowing coexistence with ants on plants, whereas ‘chemical conspicuousness’ may have evolved in the context of honest signalling between mutualistic partners.
6. We suggest the existence of chemical mimicry among myrmecophilous species, especially between mutualistic caterpillars. Cuticular chemical mixtures can play a key adaptive role in decreasing ant attacks and increasing caterpillar survival in multimodal sensory systems.

     

Temperature cues phenological synchrony in ant‐mediated seed dispersal

Species‐specific climate responses within ecological communities may disrupt the synchrony of co‐evolved mutualisms that are based on the shared timing of seasonal events, such as seed dispersal by ants (myrmecochory). The spring phenology of plants and ants coincides with marked changes in temperature, light and moisture. We investigate how these environmental drivers influence both seed release by early and late spring woodland herb species, and initiation of spring foraging by seed‐dispersing ants. We pair experimental herbaceous transplants with artificial ant bait stations across north‐ and south‐facing slopes at two contrasting geographic locations. This use of space enables robust identification of plant fruiting and ant foraging cues, and the use of transplants permits us to assess plasticity in plant phenology. We find that warming temperatures act as the primary phenological cue for plant fruiting and ant foraging. Moreover, the plasticity in plant response across locations, despite transplants being from the same source, suggests a high degree of portability in the seed‐dispersing mutualism. However, we also find evidence for potential climate‐driven facilitative failure that may lead to phenological asynchrony. Specifically, at the location where the early flowering species (Hepatica nobilis) is decreasing in abundance and distribution, we find far fewer seed‐dispersing ants foraging during its fruit set than during that of the later flowering Hexastylis arifolia. Notably, the key seed disperser, Aphaenogaster rudis, fails to emerge during early fruit set at this location. At the second location, A. picea forages equally during early and late seed release. These results indicate that climate‐driven changes might shift species‐specific interactions in a plant–ant mutualism resulting in winners and losers within the myrmecochorous plant guild.     

Reversal of mutualism in a leafflower–leafflower moth association: the possible driving role of a third‐party partner

A major goal in the study of mutualism is to understand how co‐operation is maintained when mutualism may potentially turn into parasitism. Although certain mechanisms facilitate the persistence of mutualism, parasitic species have repeatedly evolved from mutualistic ancestors. However, documented examples of mutualism reversals are still rare. Leafflowers (Phyllantheae; Phyllanthaceae) include approximately 500 species that engage in obligate mutualism with leafflower moths (Epicephala; Gracillariidae), which actively pollinate flowers, and whose larvae feed on the resulting seeds. We found that the Taiwanese population of the Phyllanthus reticulatus species complex was associated with six sympatric Epicephala species, of which three were derived parasites that induced gall formation on flowers/buds and produced no seeds. Notably, two parasitic species have retained mutualistic pollination behaviour, suggesting that the parasitism was likely not selected for to reduce the cost of mutualism. We propose that the galling habit evolved as an adaptation to escape parasitism by a specialized braconid wasp. The tough gall produced by one species was almost free of braconid parasitism, and the swollen gall induced by the other species probably prevents attack as a result of the larger airspace inside the gall. Our findings suggest that the presence of a third‐party partner can greatly influence the evolutionary fate of mutualisms, regardless of whether the pairwise interaction continues to favour co‐operation.     

Genetic diversity of termite-egg mimicking fungi “termite balls” within the nests of termites

Antagonistic or mutualistic interactions between insects and fungi are well-known, and the mutualistic interactions of fungus-growing ants, fungus-growing termites, and fungus-gardening beetles with their respective fungal mutualists are model examples of coevolution. However, our understanding of coevolutionary interactions between insects and fungi has been based on a few model systems. Fungal mimicry of termite eggs is one of the most striking evolutionary consequences of insect–fungus associations. This novel termite–fungus interaction is a good model system to compare with the relatively well-studied systems of fungus-growing ants and termites because termite egg-mimicking fungi are protected in the nests of social insects, as are fungi cultivated by fungus-growing ants and termites. Recently, among systems of fungus-growing ants and termites, much attention has been focused on common factors including monoculture system for the ultimate evolutionary stability of mutualism. We examined the genetic diversity of termite egg-mimicking fungi within host termite nests. RFLP analysis demonstrated that termite nests were often infected by multiple strains of termite egg-mimicking fungi, in contrast to single-strain monocultures in fungus combs of fungus-growing ants and termites. Additionally, phylogenetic analyses indicated the existence of a free-living stage of the termite egg-mimicking fungus as well as frequent long-distance gene flow by spores and subsequent horizontal transmission. Comparisons of these results with previous studies of fungus-growing ants and termites suggest that the level of genetic diversity of fungal symbionts within social insect nests may be important in shaping the outcome of the coevolutionary interaction, despite the fact that the mechanism for achieving genetic diversity varies with the evolutionary histories of the component species.     

Perturbed partners: opposite responses of plant and animal mutualist guilds to inundation disturbances

Mutualists have been suggested to play an important role in the assembly of many plant and animal communities, but it is not clear how this depends on environmental factors. Do, for instance, natural disturbances increase or decrease the role of mutualism? We focused on entire guilds of mutualists, studying seed‐dispersing ants and ant‐dispersed plants along gradients of inundation disturbances. We first studied how abundance and richness of the mutualists, relative to non‐mutualists, change along 35 small‐scale gradients of inundation disturbances. We found that at disturbed sites, mutualistic plant species, those that reproduce by seeds dispersed by ants, increased in abundance and in consequences in richness, relative to other herbaceous plants. In contrast, we found that among the epigeic arthropods the abundance of mutualists declined, even more so than other arthropods. Correspondingly, distributions of plant and animal mutualists became increasingly discordant at disturbed sites: most plant mutualists were spatially separated from most animal mutualists. We finally found that high abundances of plant mutualists did not translate into a high nutrition service rendered to ants: at disturbed sites, many of the plants of ant‐dispersed species did not produce seeds, which coincided with a decline in seed dispersal by ants and a changing searching behavior of the ants. Overall, the small‐scale natural disturbances we studied were correlated to a major change in the assembly of mutualist guilds. However, the correlation was often opposite between interacting plant and animal mutualist guilds and may thus reduce the potential interaction between them.     

The network structure of myrmecophilic interactions

1. Ants establish mutualistic interactions involving a wide range of protective relationships (myrmecophily), in which they provide defence against enemies and partners provide food rewards and/or refuge. Although similar in the general outcome, myrmecophilic interactions differ in some characteristics such as quantity and quality of rewards offered by partners which may lead to different specialisation levels and, consequently, to different network properties. 2. The aim of this study was to identify structural patterns in myrmecophilic interaction networks, focusing on aspects related to specialisation: network modularity, nestedness and taxonomic relatedness of interaction ranges. To achieve this, a database of networks was compiled, including the following interactions: ants and domatia‐bearing plants (myrmecophytes); ants and extrafloral nectary‐bearing plants (EFNs); ants and floral nectary‐bearing plants (FNs); ants and Lepidoptera caterpillars; and ants and Hemiptera. 3. Myrmecophilic networks differed in their topology, with ant–myrmecophyte and ant–Lepidoptera networks being similar in their structural properties. A continuum was found, ranging from highly modular networks and phylogenetically structured interaction ranges in ant–myrmecophyte followed by ant–Lepidoptera networks to low modularity and taxonomically unrelated interaction ranges in ant–Hemiptera, EFN and FN networks. 4. These results suggest that different network topologies may be found across communities of species with similar interaction types, but also, that similar network topologies can be achieved through different mechanisms such as those between ants and myrmecophytes or Lepidoptera larvae. This study contributes to a generalisation of myrmecophilic network patterns and a better understanding of the relationship between specialisation and network topology.     

The origin of a mutualism: a morphological trait promoting the evolution of ant-aphid mutualisms

Mutualisms are mutually beneficial interactions between species and are fundamentally important at all levels of biological organization. It is not clear, however, why one species participates in a particular mutualism whereas another does not. Here we show that pre-existing traits can dispose particular species to evolve a mutualistic interaction. Combining morphological, ecological, and behavioral data in a comparative analysis, we show that resource use in Chaitophorus aphids (Hemiptera: Aphididae) modulates the origin of their mutualism with ants. We demonstrate that aphid species that feed on deeper phloem elements have longer mouthparts, that this inhibits their ability to withdraw their mouthparts and escape predators and that, consequently, this increases their need for protection by mutualist ants.     

Host-plant relationships of lycaenid butterflies: large-scale patterns, interactions with plant chemistry, and mutualism with ants

The Lycaenidae are the second-largest family of butterflies. From host-plant data collated for more than 1200 species worldwide, large-scale taxonomic, geographical and ecological patterns emerge which suggest that phytochemical similarities and barriers, coupled with phylogenetic conservatism and constraints are key factors governing hostplant use. More than two thirds of the lycaenid species are restricted to one plant family or genus. Affiliations with toxic plants are rare in the Lycaenidae, and excretion rather than sequestration of plant toxins appears to be their usual way of detoxifying host-plant compounds. Flavonoids are frequently sequestered by lycaenid larvae and are subsequently concentrated as pigments in the adults' wings, where they might play a role in visual communication. Mutualistic associations with ants occur in the larvae of more than 50% of the extant Lycaenidae species. Because of a conflict between the nutrient demands of the larvae and the proportion of plant-derived resources allocated to maintain the mutualism with ants, variation in resource quality often translates into variation of mutualistic capacities of the caterpillars, in particular under nutrient stress.     

Joint evolution of interspecific mutualism and regulation of variation of interaction under directional selection in trait space

The present study theoretically examines the process by which interspecific mutualism is established with trait matching. The mathematical model includes joint evolution of the mutualistic relationship between two species and regulation of variation of interaction in one-dimensional trait space, assuming abiotic directional selection. The model considers three types of regulation: homeostasis against environmental variation, developmental stability, and acceptability of dissimilar mutualism partners (mutualism kernel). Mainly focusing on the developmental stability, the analysis indicates that the mutualism can evolve when (1) higher levels of developmental stability are more intensively degenerated by deleterious mutations, (2) the basal rate of deleterious mutation is low, (3) trait expression is less influenced by environmental factors, and (4) the specificity of mutualism is high. It also shows that the evolution of developmental stability can promote the evolution of mutualism with trait matching when the deleterious mutation bias disappears at a certain level of developmental instability. Evolution of homeostasis and mutualism kernel can be discussed in the similar way because of formal similarities in the model. In plant–pollinator interactions, it has recently been proposed that evolutionary increments of developmental stability in mutualistic traits might promote plant diversification. The present results partly support this hypothesis with respect to the evolutionary relationship between mutualism and developmental stability.     

Evolution of obligate pollination mutualism in the tribe Phyllantheae (Phyllanthaceae)

The landmark discovery of obligate pollination mutualism between Glochidion plants and Epicephala moths has sparked increased interest in the pollination systems of Phyllantheae plants. In this paper I review current information on the natural history and evolutionary history of obligate pollination mutualism in Phyllantheae. Currently, an estimated >500 species are mutualistic with Epicephala moths that actively pollinate flowers and whose progeny feed on the resulting seeds. The Phyllantheae also includes species that are not mutualistic with Epicephala moths and are instead pollinated by bees and/or flies or ants. Phylogenetic analyses indicate that the mutualism evolved independently five times within Phyllantheae, whereas active pollination behavior, a key innovation in this mutualism, evolved once in Epicephala . Reversal of mutualism has occurred at least once in both partner lineages, involving a Breynia species that evolved an alternative pollination system and a derived clade of Epicephala that colonized ant-pollinated Phyllantheae hosts and thereby lost the pollinating habit. The plant–moth association is highly species specific, although a strict one-to-one assumption is not perfectly met. A comparison of plant and moth phylogenies suggests signs of parallel speciation, but partner switches have occurred repeatedly at a range of taxonomic levels. Overall, the remarkable species diversity and multiple originations of the mutualism provide excellent opportunities to address many important questions on mutualism and the coevolutionary process. Although research on the biology of the mutualism is still in its infancy, the Phyllantheae– Epicephala association holds promise as a new model system in ecology and evolutionary biology.     

Interaction intimacy affects structure and coevolutionary dynamics in mutualistic networks

The structure of mutualistic networks provides clues to processes shaping biodiversity [1-10]. Among them, interaction intimacy, the degree of biological association between partners, leads to differences in specialization patterns [4, 11] and might affect network organization [12]. Here, we investigated potential consequences of interaction intimacy for the structure and coevolution of mutualistic networks. From observed processes of selection on mutualistic interactions, it is expected that symbiotic interactions (high-interaction intimacy) will form species-poor networks characterized by compartmentalization [12, 13], whereas nonsymbiotic interactions (low intimacy) will lead to species-rich, nested networks in which there is a core of generalists and specialists often interact with generalists [3, 5, 7, 12, 14]. We demonstrated an association between interaction intimacy and structure in 19 ant-plant mutualistic networks. Through numerical simulations, we found that network structure of different forms of mutualism affects evolutionary change in distinct ways. Change in one species affects primarily one mutualistic partner in symbiotic interactions but might affect multiple partners in nonsymbiotic interactions. We hypothesize that coevolution in symbiotic interactions is characterized by frequent reciprocal changes between few partners, but coevolution in nonsymbiotic networks might show rare bursts of changes in which many species respond to evolutionary changes in a single species.     

Tree diversity alters the structure of a tri‐trophic network in a biodiversity experiment

Species and processes in ecosystems are part of multi‐trophic interaction networks. Plants represent the lowest trophic level in terrestrial ecosystems, and experiments have shown a stabilizing effect of plant diversity on higher trophic levels. Such evidence has been mainly collected in experimental grasslands. Forests are structurally more complex than grasslands and support the majority of the global biodiversity, but studies on multi‐trophic interaction networks are missing in experimental tree diversity gradients. In a forest diversity experiment in southeast China, we examined how tree diversity affects the structure of trophobiotic networks. Trophobioses are tri‐trophic interactions between plants, sap‐sucking Hemiptera and honeydew‐collecting ants that can be subdivided into a largely mutualistic Hemiptera–ant and an antagonistic plant–Hemiptera network. We inspected almost 7000 trees in 146 plots ranging from monocultures to 16 tree species mixtures and found 194 trophobioses consisting of 15 tree, 33 Hemiptera and 18 ant species. We found that tree diversity increased the proportion of trees harboring trophobioses. Consistent with the prediction that mutualistic and antagonistic networks respond differently to changing environments, we found that the generality index of the mutualistic Hemiptera–ant but not the antagonistic plant–Hemiptera network increased with tree diversity. High generality, maintained by high tree diversity, might correspond to higher functional stability. Hence, our results indicate that tree diversity could increase via bottom–up processes the robustness of ant–Hemiptera associations against changing environmental conditions. In turn, the plant–Hemiptera network was highly complementary, suggesting that host‐specific Hemiptera species may be vulnerable to co‐extinction if their host plants disappear. Based on our results, we provide possible future research directions to further disentangle the bottom–up effect of tree diversity on the structure of trophobiotic networks. Synthesis It is now widely accepted that plant diversity promotes ecosystem functionality and stability. However, it is still largely unknown how plant diversity affects interactions between trophic levels and if different interaction types are affected differently. Using a tri‐trophic study system consisting of plants, sap‐sucking Hemiptera, and ants we provide evidence that increasing local plant diversity stabilizes the mutualistic Hemiptera–ant but not the antagonistic plant–Hemiptera networks. Our results suggest that bottom–up effects of plant diversity on trophic interactions might generally depend on the type of interaction (mutualistic versus antagonistic) considered.