Bracken, ants and extrafloral nectaries. III. How insect herbivores avoid ant predation

Abstract. 1. Ants (Myrmica spp. and Formica lemani) visiting the extrafloral nectaries of bracken, Pteridium aquilinum, imposed heavy mortality on caterpillars of a novel moth species experimentally introduced onto bracken fronds. However, the exclusion of ants from bracken fronds had no significant effect on adapted bracken-feeding herbivores in Britain.
2. The feeding stages of British bracken-feeding insects are immune to, or can largely avoid, predation by ants in a variety of ways. Gall formers and miners cannot be attacked by these ants. Two other species hide, one inside tied leaves, the other in a mass of 'spittle'. Another group of species jumps away from, or falls off the plant when touched by ants. Sawfly caterpillars in the genera Strongylogaster, Aneugmenus and Tenthredo have viscous, distasteful haemolymph that repels ants.
3. No species of bracken herbivore has an absolute temporal refuge from ants; during their development they all overlap with ants to some degree.
4. Ant predation appears to have played a significant role in determining the contemporary structure of British bracken-feeding insect communities. Distasteful haemolymph in sawfly caterpillars may have evolved in response to selection from ant predation. Other species may fortuitously possess characteristics, evolved in response to a variety of selective forces, that also reduce the impact of ants; without such characteristics, however, we postulate that they would be unable to live on this plant. An absence of external, foliage feeding Lepidoptera early in the spring, a high proportion of sawfly species, and a high proportion of gall-formers and miners may all be characteristics of the bracken herbivore community which have been influenced by ant predation.     

Ant protection of the nectaried fern Polypodium plebeium in central Mexico

Nectaries on fronds of Polypodium spp. have been studied previously only in cultivated specimens. We conducted field observations in middle-elevation forests in Mexico and found five ant species associated with nectaries of Polypodium plebeium and P. lepidotrichum. To investigate whether nectaries promote protection against herbivores, we performed ant-exclusion experiments with nectary-bearing ferns (P. plebeium) and other ferns without nectaries (Polypodium plesiosorum, P. furfuraceum, and Phlebodium pseudoaureum). When ants were excluded from the developing fronds of Polypodium plebeium, damage from foliage-feeding sawfly and lepidopteran caterpillars was significantly greater than in control fronds. Ferns without nectaries did not show a difference in damage between ant-excluded and control fronds. Our results demonstrate that fern nectaries can support ant defense of the plant body as do the extrafloral nectaries of many angiosperms.     

Ant Defense Versus Induced Defense in Lafoensia pacari (Lythraceae), a Myrmecophilous Tree of the Brazilian Cerrado1

We compared the effects of ant presence at extrafloral nectaries of Lafoensia pacari St. Hil. on herbivore damage and silicon accumulation. Plants that were accessible to ants experienced lower herbivory levels over the first 3 mo of the experiment. After 3 mo, most leaves were fully expanded with inactive extrafloral nectaries; by 6 mo there was no effect of ant access on herbivore damage. Along with experiencing higher herbivory, plants in the ant‐exclusion treatment had significantly higher silicon levels in their leaves, suggesting that silicon serves as an induced defense in this ant–plant–herbivore interaction.     

The effect of nitrogen additions on bracken fern and its insect herbivores at sites with high and low atmospheric pollution

The impact of atmospheric pollution, including nitrogen deposition, on bracken fern herbivores has never been studied. Bracken fern is globally distributed and has a high potential to accumulate nitrogen in plant tissue. We examined the response of bracken fern and its herbivores to N fertilization at a high and low pollution site in forests downwind of Los Angeles, California. Foliage from the high pollution site had higher total N and nitrate than the low pollution site. Bracken fern biomass, foliar N and herbivore abundance were all affected by fertilization treatments. Biomass and herbivore responses were greatest during a year of high precipitation. N additions at the low pollution site were primarily associated with decreased fern biomass, and with transient impacts on herbivore abundance. N additions significantly affected bracken fern and its herbivores at the high pollution site where foliar N and nitrate decreased in response to N addition treatments, while biomass and herbivore abundance increased. High atmospheric deposition and fertilization were both associated with increased herbivore richness. Herbivore abundance was most impacted by fertilization during the early expansion of fern fronds. The most abundant chewing herbivore, a sawfly, was positively associated with plant nitrogen at the low pollution site, but negatively associated with plant nitrogen at the high pollution site, where concentrations of both total N and nitrate were high. While overall growth and herbivore impacts in this xeric location were limited, the variable response we observed associated with rainfall, may indicate impacts could be larger in more mesic environments.     

The effect of disturbance on an ant–plant mutualism

Protective ant–plant mutualisms—where plants provide food or shelter to ants and ants protect the plants from herbivores—are a common feature in many ecological communities, but few studies have examined the effect of disturbance on these interactions. Disturbance may affect the relationship between plants and their associated ant mutualists by increasing the plants’ susceptibility to herbivores, changing the amount of reward provided for the ants, and altering the abundance of ants and other predators. Pruning was used to simulate the damage to buttonwood mangrove (Conocarpus erectus) caused by hurricanes. Pruned plants grew faster than unpruned plants, produced lower levels of physical anti-herbivore defenses (trichomes, toughness), and higher levels of chemical defenses (tannins) and extrafloral nectaries. Thus, simulated hurricane damage increased plant growth and the amount of reward provided to ant mutualists, but did not have consistent effects on other anti-herbivore defenses. Both herbivores and ants increased in abundance on pruned plants, indicating that the effects of simulated hurricane damage on plant traits were propagated to higher trophic levels. Ant-exclusion led to higher leaf damage on both pruned and upruned plants. The effect of ant-exclusion did not differ between pruned and unpruned plants, despite the fact that pruned plants had higher ant and herbivore densities, produced more extrafloral nectaries, and had fewer physical defenses. Another common predator, clubionid spiders, increased in abundance on pruned plants from which ants had been excluded. I suggest that compensatory predation by these spiders diminished the effect of ant-exclusion on pruned plants.     

Deterrent effect of a guild of extrafloral nectary-visiting ant species on Raphidopalpa foveicollis, a major insect pest of sponge gourd, Luffa cylindrica

Among the 10 ant species visiting the extrafloral nectaries of sponge gourd plants [ Luffa cylindrica L. (Cucurbitaceae)], Camponotus compressus (Fabricius) (Hymenoptera: Formicidae) appears to be the ecologically dominant species, due to its abundance and the high frequency of deterrent encounters with the major insect herbivore, Raphidopalpa foveicollis Lucas (Coleoptera: Chrysomelidae). A significant positive linear correlation was found between the number of extrafloral nectaries per leaf, calyx, bract, and bracteole and the patrolling time of C. compressus , Camponotus paria (Emery), Pheidole spec., and Tetramorium spec. (all Hymenoptera: Formicidae) at the corresponding plant parts. Many one-to-one deterrent interactions between the ant visitors and adult R. foveicollis were recorded, with C. compressus being involved in most encounters on the calyx and bracts, Pheidole spec. on the leaves, and Pachycondyla tesserinoda (Emery) (Hymenoptera: Formicidae) on the bracteoles. Tapinoma melanocephalum (Fabr.) (Hymenoptera: Formicidae) exhibited significant deterrent effects on adult herbivores on the corolla when in groups larger than 15 ants. Ant exclusion and inclusion experiments revealed a significant reduction in the residence time, as well as dose- and time-dependent reduction in the frequency of visits of the herbivore on crop plants with C. compressus , C. paria , Pheidole spec., and T. melanocephalum ants, compared to the control. Results support the optimal defence hypothesis, as the plant structures most closely linked to plant fitness bear the extrafloral nectaries and are defended by the visiting ant species. This is a valuable, indirect plant-protection strategy of an annual crop plant.     

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     

Role of extrafloral nectaries of Vicia faba in attraction of ants and herbivore exclusion by ants

We directly evaluated the role of extrafloral nectaries (EFN) in ant attraction and herbivore exclusion by experimental removal of EFN in the laboratory. When EFN of Vicia faba Linnaeus (Leguminosae) were artificially removed, the number of workers of Tetramorium tsushimae Emery (Hymenoptera: Formicidae) visiting the plant decreased, and the efficiency of herbivore exclusion by ants also decreased. Herbivore exclusion by ants was mostly ineffective on a plant when less than four workers visited the plant, but when more than four workers visited, the time a herbivore resided on the plant decreased rapidly with increasing numbers of visiting ants. Therefore, the efficiency of herbivore exclusion from a plant is determined by the number of ants visiting, and EFN play an important role in ant attraction.     

Ants on plants: a meta-analysis of the role of ants as plant biotic defenses

We reviewed the evidence on the role of ants as plant biotic defenses, by conducting meta-analyses for the effects of experimental removal of ants on plant herbivory and fitness with data pooled from 81 studies. Effects reviewed were plant herbivory, herbivore abundance, hemipteran abundance, predator abundance, plant biomass and reproduction in studies where ants were experimentally removed (n = 273 independent comparisons). Ant removal exhibited strong effects on herbivory rates, as plants without ants suffered almost twice as much damage and exhibited 50% more herbivores than plants with ants. Ants also influenced several parameters of plant fitness, as plants without ants suffered a reduction in biomass (−23.7%), leaf production (−51.8%), and reproduction (−24.3%). Effects were much stronger in tropical regions compared to temperate ones. Tropical plants suffered almost threefold higher herbivore damage than plants from temperate regions and exhibited three times more herbivores. Ant removal in tropical plants resulted in a decrease in plant fitness of about 59%, whereas in temperate plants this reduction was not statistically significant. Ant removal effects were also more important in obligate ant–plants (=myrmecophytes) compared to plants exhibiting facultative relationships with hemiptera or those plants with extrafloral nectaries and food bodies. When only tropical plants were considered and the strength of the association between ants and plants taken into account, plants with obligate association with ants exhibited almost four times higher herbivory compared to plants with facultative associations with ants, but similar reductions in plant reproduction. The removal of a single ant species increased plant herbivory by almost three times compared to the removal of several ant species. Altogether, these results suggest that ants do act as plant biotic defenses, but the effects of their presence are more pronounced in tropical systems, especially in myrmecophytic plants. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users. N. P. de U. Barbosa, L. Diniz, Y. Oki and F. Pezzini contributed equally to this work and are listed in alphabetical order.     

Insights into a novel three-partner interaction between ants,coreids (Hemiptera: Coreidae) and extrafloral nectaries: implications for the study of protective mutualisms

Extrafloral nectar of plants and honeydew of hemipterans are the common mediators of facultative interactions that involve ants as a mobile strategy of defence. The outcome of these interactions can vary from mutualistic to commensalistic or even antagonistic, depending on the ecological context and the interacting species. Here, we explore a novel, three-partner interaction involving ants, the coreid Dersagrena subfoveolata (Hemiptera) and the extrafloral nectaries (EFNs) bearing plant Senna aphylla (Fabaceae) in semi-arid Northwest Argentina. We surveyed natural areas and conducted ant exclusion experiments, to understand how each pairwise interaction influences the overall outcome among the three interacting parts. The outcome of the interactions was assessed for experimental plants as the reproductive output and herbivore abundances and for coreids as predator abundances. We found that the coreids occurred exclusively on S. aphylla plants and that at least nine ant species interacted with the EFNs as well as with the coreids. Coreid occurrence and abundance depended on ant densities, which in turn, was determined by the presence of actively secreting EFNs. Coreid and ant presence did not influence plant reproductive success, and ants provided to coreids some biotic defence, mainly against vespid wasp predators, but had no effect on non-coreid herbivores. We conclude that the interaction outcome is commensalistic between ants and plants (assuming that EF nectar is not costly for the plant), antagonistic between coreids and plants, and mutualistic between coreids and ants. The sum of all outcomes is net positive effect for ants and coreids, and net slightly negative to neutral for plants.     

Florivorous myrmecophilous caterpillars exploit an ant–plant mutualism and distract ants from extrafloral nectaries

Females of myrmecophilous butterflies tend to oviposit in plants visited by ant species that engage in stable associations with its larvae. In Banisteriopsis malifolia, caterpillars are attended by the same ants that feed on extrafloral nectaries. A conflict may arise when both the plant and caterpillars compete for ant attention, and ants are assumed to forage on the highest quality resource. By attending caterpillars, ants can be indirectly detrimental to plant fitness because florivorous larvae feed intensively until pupation. In this study, we specifically investigated (i) whether the occurrence of facultative myrmecophilous Synargis calyce (Riodinidae) caterpillars in B. malifolia was based on ant species (Camponotus blandus or Ectatomma tuberculatum) and abundance; (ii) the monopolization of ants by the butterfly larvae and (iii) the florivory rates incurred by the caterpillars on inflorescences. The abundance of S. calyce was six‐fold greater in plants with C. blandus, compared to E. tuberculatum treatments. Caterpillars monopolized up to 50% of C. blandus on the plants, indicating that the resources offered by S. calyce were more attractive to ants than extrafloral nectaries. Florivory by riodinids incurred losses of almost 60% of flower buds. Myrmecophilous riodinids exploited an ant–plant mutualism by attracting aggressive ants that become larvae bodyguards. Thus, this ecological interaction is potentially detrimental to B. malifolia, since the ants, which can provide protection against herbivores, shift to provide defence for one of these herbivores.     

Ant Species Identity has a Greater Effect than Fire on the Outcome of an Ant Protection System in Brazilian Cerrado

Although fire‐ and ant–plant interactions influence the community structure and dynamics of Neotropical savannas, no previous studies have considered their simultaneous effects on target host plants. We monitored the effect of ant exclusion for 3 years on leaf area loss to leaf chewing insects, thrips abundance, and reproductive output of the extrafloral nectary‐bearing shrub, Peixotoa tomentosa (Malpighiaceae). We predicted that the impact of ants on herbivores and plants would depend on the ant species, and that fire would reduce the effect of ants. We deliberately chose control plants that differed in their occupant ant species. Fire occurred in the second year of the study, allowing us to determine its effect on the benefit afforded by ants. Ants reduced leaf area loss and thrips abundance, and increased fruit and seed production in all 3 years. Some ant species were more effective than others, while plants with multiple ant species suffered higher leaf area loss than plants with a single ant species. In the year following the fire, leaf damage was greater than in the other years, regardless of the ant species, and the proportional effect of ants in reducing damage was less. Interactions affecting thrips abundance did not change following fire, nor was the benefit to the plant proportionally reduced. Overall, the identity of the ant species had a greater effect than did the occurrence of fire on the ant–herbivore–plant interaction: the identity of the ant species influenced leaf area loss, thrips numbers, and bud and seed production, while fire only modified the impact of ants on the amount of leaf area consumed by insect herbivores.     

Ants have a negative rather than a positive effect on extrafloral nectaried Crotalaria pallida performance

Crotalaria pallida (Fabaceae) is a pantropical plant with extrafloral nectaries (EFNs) near the reproductive structures. EFN-visiting ants attack and remove arctiid moth Utetheisa ornatrix larvae, the main pre-dispersal seed predator, but the impact of ants on C. pallida fitness is unknown. To assess this impact, we controlled ant presence on plants and evaluated the reproductive output of C. pallida with and without ants. Predatory wasps also visit EFNs, prey upon U. ornatrix larvae, and may be driven out by ants during EFN feeding. Does this agonistic interaction affect the multitrophic interaction outcome? We found it difficult to evaluate the effect of both visitors because cages excluding wasps affect plant growth and do not allow U. ornatrix oviposition. Therefore, we verified whether ant presence inhibited wasp EFN visitation and predicted that (1) if ants confer a benefit for C. pallida, any negative effect of ants on wasps would be negligible for the plant because ants would be the best guardians, and (2) if ants are poor guardians, they would negatively affect wasps and negatively impact the fitness of C. pallida. Surprisingly, we found that the number of seeds/pods significantly increased, ca. 4.7 times, after ant removal. Additionally, we unexpectedly verified that controls showed a higher percentage of herbivore bored pods than ant-excluded plants. We found that wasps spent less time visiting EFNs patrolled by ants (ca. 299 s less). These results support our second prediction and suggest that the outcome of multitrophic interactions may vary with natural enemy actors.     

The influence of extrafloral nectaries on parasitism of an insect herbivore

The extrafloral nectaries of many plants promote ant defense against insect herbivores. We examined the influence of extrafloral nectaries on the levels of parasitism of a generalist insect herbivore, the gypsy moth (Lymantria dispar L.). Larvae and pupae of the moth were collected from trees with and without extrafloral nectaries growing in the same forests in South Korea and reared to evaluate parasitism. More parasitism occurred on plants with extrafloral nectaries in seven of the nine season-long collections at the six sites and in four out of five collecting periods. Parasitism was higher on the four main genera of plants with extrafloral nectaries than on any of five main genera of plants without extrafloral nectaries. There was no difference in parasitoid richness; nine species occurred in each group, eight of which were the same. There was a positive and almost significant correlation between the abundance of plants with extrafloral nectaries and the parasitism of gypsy moth at the sites. Extrafloral nectaries may reduce herbivory by inducing more parasitism of the insect herbivores that attack plants bearing the glands.     

No Defensive Role of Ants throughout a Broad Latitudinal and Elevational Range of a Cactus

Defensive mutualisms mediated by extrafloral nectaries are particularly variable; their net results may change with seasons, communities and environmental contexts. Particularly, an environmental factor that can promote changes in outcomes of ant‐plant interactions is elevation in mountainous regions. We tested whether (1) the interaction between the cactus Opuntia sulphurea and ant visitors of extrafloral nectaries is a defensive mutualism; and (2) ant‐plant interaction outcomes vary with elevation as a result of changes in herbivory rate and ant activity. To evaluate if the outcome of interactions was consistent at two extremes of the range distribution of O. sulphurea, we performed an ant‐exclusion experiment with plants at two growth conditions (natural or potted) in two sites with contrasting elevation (1235–1787 m asl) in a temperate region (Villavicencio Nature Reserve, Mendoza, Argentina), and in a tropical region (Huajchilla, La Paz, Bolivia). Although herbivory rate and ant visitation frequency increased with elevation, herbivore damage, plant reproductive success, and cladode growth rate were similar between plants excluded and non‐excluded from ants among sites, geographic regions and growth conditions. These results do not support the hypotheses that the interaction between O. sulphurea and ants is a defensive mutualism, and that elevation affects the net outcome of this ant‐plant interaction.     

Extrafloral nectaries: ants,herbivores and fecundity in Cassia fasciculata

Summary Extrafloral nectaries of Cassia fasciculata attract nectar feeding ants which protect the plant against leaf herbivores. High ant visitation in late July coincided with high herbivore densities at two sites in east central Iowa. The highest level of leaf herbivory occurred during the time of flowering and early fruit filling, just after the peak of herbivore and ant activity. Results of ant exclusion experiments at the two sites showed that ant visitation resulted in decreased herbivore numbers, decreased leaf area loss, increased growth, and at one site decreased plant mortality. However, this reduction in leaf area loss and increase in growth did not translate into seed set differences between plants with and without ants at either site. Initial plant size was more important than the presence or absence of ants in determining fecundity for this temperate annual during a year of summer drought.     

A selection mosaic in the facultative mutualism between ants and wild cotton

In protection mutualisms, one mutualist defends its partner against a natural enemy in exchange for a reward, usually food or shelter. For both partners, the costs and benefits of these interactions often vary considerably in space because the outcome (positive, negative or neutral) depends on the local abundance of at least three species: the protector, the beneficiary of protection and the beneficiary's natural enemy. In Gossypium thurberi (wild cotton), ants benefit nutritionally from the plant's extrafloral nectaries and guard plants from herbivores. Experimentally altering the availability of both ants and extrafloral nectar in three populations demonstrated that the mutualism is facultative, depending, in part, on the abundance of ants and the level of herbivore damage. The species composition of ants and a parasitic alga that clogs extrafloral nectaries were also implicated in altering the outcome of plant-ant interactions. Furthermore, experimental treatments that excluded ants (the putative selective agents) in combination with phenotypic selection analyses revealed that selection on extrafloral nectary traits was mediated by ants and, importantly, varied across populations. This work is some of the first to manipulate interactions experimentally across multiple sites and thereby document that geographically variable selection, mediated by a mutualist, can shape the evolution of plant traits.     

Foliage-dwelling ants in a neotropical savanna: effects of plant and insect exudates on ant communities

Ant dominance in tropical ecosystems can be explained by a capacity to exploit liquid foods such as extrafloral nectaries (EFNs) and secretions from honeydew-producing hemipterans (HPHs). Such nutritious exudates may determine ant distribution in space and shape specialization in ant–plant interactions. We provide a first assessment of how EFNs and HPHs mediate the structure of ant assemblages, ant visitation intensity, and characteristics of ant–plant interaction networks across space in Brazilian “cerrado” savanna. We used arboreal pitfall traps to sample visiting ants in four cerrado localities and recorded the presence of lepidopteran larvae to determine their possible response to ant visitation. Ant species composition and richness did not differ regardless of the presence of liquid rewards on plants, and most network patterns did not show consistent differences. However, in two of the four sites, ant densities were higher on plants with HPHs or EFNs due to increased activity by Camponotus and Pseudomyrmex ants. At these two sites, plants with liquid food sources had a more specific ant assemblage (higher specialization d′) than did plants without resources, and caterpillars were more frequently found on plants with fewer workers of Camponotus and Pseudomyrmex. Plants with HPHs had increased ant visitation and accumulated more ant species than did plants with EFNs or without liquid foods. Ant response to such food sources may thus depend on local conditions and identity of ant species, and may determine how ant assemblages are structured. Results highlight how different patterns of ant visitation to liquid resources can produce distinctive effects on herbivore infestation.     

When are ant-attractant devices a worthwhile investment? Vicia faba extrafloral nectaries and Lasius niger ants

Most studies aiming to determine the beneficial effect of ants on plants simply consider the effects of the presence or exclusion of ants on plant yield. This approach is often inadequate, however, as ants interact with both non-tended herbivores and tended Homoptera. Moreover, the interaction with these groups of organisms is dependent on ant density, and these functional relationships are likely to be non-linear. A model is presented here that segregates plant herbivores into two categories depending on the sign of their numerical response to ants (myrmecophiles increase with ants, non-tended herbivores decline). The changes in these two components of herbivores with increasing ant density and the resulting implications for ant-plant mutualisms are considered. It emerges that a wide range of ant densities needs to be considered as the interaction sign (mutualism or parasitism) and strength is likely to change with ant density. The model is used to interpret the results of an experimental study that varied levels of Aphis fabae infestation and Lasius niger ant attendance on Vicia faba bean plants. Increasing ant density consistently reduced plant fitness and thus, in this location, the interaction between the ants and the plant can be considered parasitic. In the Vicia faba system, these costs of ants are unlikely to be offset by other beneficial agents (e.g., parasitoids), which also visit extrafloral nectaries.     

The ontogeny of plant indirect defenses

Plants frequently attract natural enemies of their herbivores, resulting in a reduction in tissue damage and often in enhanced plant fitness. While such indirect defenses can dramatically change as plants develop, only recently have ecologists begun to explore such changes and evaluate their role in mediating plant–herbivore–natural enemy interactions. Here we review the literature documenting ontogenetic patterns in plant rewards (i.e. extrafloral nectaries (EFNs), food bodies (FBs) and domatia) and volatile organic compounds (VOCs), and identify links between ontogenetic patterns in such traits and the attraction of natural enemies (ants). In the case of reward traits we concentrate in ant–plant studies, which are the most numerous. We report that all indirect defensive traits commonly vary with plant age but ontogenetic trajectories differ among them. Myrmecophytic species, which provide both food and shelter to their defenders, do not produce rewarding traits until a minimum size is reached. Then, a pronounced increase in the abundance of food rewards and domatia often occurs as plants develop, which explains the temporal succession or colony size increase of mutualistic ant species and, in some cases, leads to a reduction in herbivore damage and enhanced fitness as plants age. In contrast, ontogenetic patterns were less consistent in plant species that rely on VOC emissions to attract natural enemies or those that provide only food rewards (EFNs) but not nesting sites to their associated ants, showing an overall decline or lack of trend with plant development, respectively. Future research should focus on uncovering: (i) the costs and mechanisms underlying ontogenetic variation in indirect defenses, (ii) the relative importance of environmental and genetic components shaping these ontogenetic trajectories, and (iii) the consequences of these ontogenetic trajectories on plant fitness. Advances in this area will shed light on the context dependency of bottom-up and top-down controls of herbivore populations and on how natural selection actually shapes the ontogenetic trajectories of these traits.