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Use the link below to share a full-text version of this article with your friends and colleagues. Learn more. The galls are functionally similar to extrafloral nectaries, plant structures well known for their role in ant—plant mutualisms. The family Cynipidae Hymenoptera , known commonly as gall wasps or gallflies, is a family of parasitoid wasps that induce superficial growths galls on plants, inside which their larvae develop and feed. Gall structures are made entirely of plant tissue, but are controlled and induced by the gall wasp Shorthouse and Rohfritsch Some species within the Cynipidae have taken this structural defense one step further, by recruiting ants to defend against their enemies.

The tending ants deter predators, parasitoids, and inquilines of the gall wasps, thereby increasing the chance of successful emergence. Though they have received relatively little attention, several novel experiments have investigated the impact that tending ants have on the developing gall wasps, and it is generally agreed that ants are a beneficial and sometimes necessary partner. He found that preventing ants from tending galls resulted in much higher levels of parasitism of the gall wasp, and a much lower rate of emergence.

Furthermore, Abe showed that gall clustering enhances the benefit from ants. Multiple evolutions of nectar secretion and a lack of subsequent loss both suggest a significant benefit to the wasp, and the transition to gall clustering demonstrates that the benefit is additive; more nectar leads to more ants, and more ants lead to fewer enemies. For instance, in the tripartite interaction between wasp, plant, and ant, only the benefit to the wasp has been addressed.

The potential benefits for tending ants and plant hosts have been suggested, but not investigated. Finally, while the potential importance of gall nectar as a food source for other organisms has been suggested, it has not been demonstrated experimentally. The relationships they form with ants and other insects are evocative of other, functionally related plant structures, and they may have a deep evolutionary significance. Extrafloral nectaries have evolved independently at least times, occurring globally across a wide range of climates and habitats Weber and Keeler Seibert demonstrated that on Quercus gambellii oak trees where the ant F.

With few exceptions e. Moreover, benefits from reduced herbivory may result in selective pressure for developing plant traits that encourage greater ant attendance, especially in seasonal times of gall absence, or during periods when the gall wasp population is suppressed. The ant—plant mutualism that extrafloral nectaries facilitate cuts both ways. It has even been proposed that extrafloral nectaries have contributed to the ecological success and dominance of ants as a group Davidson This demonstrates that even a transient food resource can be significant for tending ants, and might allow for increased brood production when available.

Early observations of the importance of gall nectar to the iconic Honeypot ant Myrmecocystus mexicanus exemplify this idea. McCook observed that M. Resulting discussion suggested that nectar secretion by galls is widespread throughout the Rocky Mountain region and the Mississippi valley and common among other galls Mann Furthermore, Wheeler posits that the development of replete workers by ants from arid regions of North America, South Africa, and Australia is likely due to the temporary abundance of nectar, including gall nectar, and the long periods of unavailability of other food sources.

The relative importance of gall nectar for other groups has mostly been overlooked, but it has been suggested for some groups. Although most evidence is anecdotal, originating from field observations, the diversity of insect groups observed feeding on gall nectar suggests that it might be more relevant than currently understood, a promising area for future research.

One recent study from the forest canopy underscored the potential importance of gall nectar as a food resource and exemplifies the false assumptions that can result from observational bias. Satyrium favonius ontario , also called the northern oak hairstreak, is among the rarest butterfly species in eastern North America. The authors suggest that its rarity is mostly observational, and results from the fact that adults reside mostly in the canopy, feeding on gall nectar and honeydew. Understanding of the ecological importance of the forest canopy is rapidly growing, and similar patterns may yet be uncovered elsewhere.

Of course, any organisms exploiting this space may become prey for the ants themselves.

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Further, even if consumed as prey, the net benefit might still be positive if the mortality rate from ant predation was less than that induced by parasitoids Johnstone and Bshary Previous work suggests that extrafloral nectar can in fact mediate a mutualistic relationship between ants and other insects.

They can vary from symmetrical to asymmetrical, generalized to specialized, and facultative to obligate Bronstein a. Asymmetrical relationships, including predatory and parasitic relationships, can over time transition to mutualisms Johnstone and Bshary In both cases, the plants provide housing and food to their ant partners, which in turn aggressively defend the plant from herbivores.

For example, defensive mutualisms facilitated by extrafloral nectaries led to an increase in the diversification rate of certain plant groups Weber and Agrawal Hypothesized scenarios can be constrained by assumptions about factors that favor mutualism, using commonly observed themes. These include 1 a historical ecological context that brings a mobile partner into contact with a sedentary partner e.

More generally, mutualisms are likely to arise from the gradual increased interdependence of two or more species, as a result of selective forces acting on morphological or behavioral traits, facilitated by overlapping ecological niches. This review examines the evidence for VOCs in galler attraction to host plants, potential VOC suppression by gallers, increased emission from galls and neighboring tissues, attraction of galler enemies, and the role of galler symbionts in VOC production.

Leaf Galls

It suggests a research focus and ways in which studies on galler-associated VOCs can progress from a philatelic approach involving VOC listing toward a more predictive and evolutionary perspective. Galls are a classic example of niche construction Gilbert, and partly of the extended phenotype of the galling organism Stone and Cook, Galls are constructed by gallers in concert with plant tissue that is coerced into gall formation Favery et al. These hypertrophied tissues provide protection and nutrition for one or more galler generations Wool and Burstein, Diverse organisms including viruses, bacteria, fungi, and invertebrates induce galls on plants Mani, ; Raman, ; Fernandes and Santos, Of invertebrates, galling insects are possibly the most diverse and most studied and include gall midges Diptera: Cecidomyiidae , gall wasps Hymenoptera: Cynipidae , and aphids Hemiptera: Aphididae ; nematodes and mites are also important.

Thrips and galls - Thrips Wiki

Most galls are an infestation; to be sustained, gallers must suppress or cope with plant defenses such as herbivore-induced plant volatiles HIPVs or manipulate them to their own advantage Figure 1. This review is restricted to invertebrate-induced galls, and focuses on the less-examined role of volatiles in galler—plant—galler enemy interactions Figure 1.

Beneficial galls occur in some brood-site pollination mutualisms when gallers themselves are pollinators, e. Here the interests of the host-plant and the gallers are aligned, and plants actively signal to their galler pollinators. Interactions between gallers and plants by means of volatiles. Arrows point toward the affected interactant from the volatile source. Volatiles may attract gallers to plants; the galler may suppress plant volatile production, or plants may increase volatile production to attract galler enemies or to up-regulate defenses.

Symbionts within galls or gallers may affect volatile production. Interactions of plants with beneficial and parasitic gallers. Examples are from the cluster fig Ficus racemosa A seeds and pollinator galls in a syconium. Note remnants of stigma and single developing pollinator in each galled uniovulate flower. B Large galls of an early-arriving parasitic galler Sycophaga stratheni in a syconium; these gallers target tissues of the syconium lumen.

C Aggregations of parasitic gallers Sycophaga fusca on a syconium; these gallers are attracted by the syconium volatile blend emitted at pollen-receptive stage. D The weaver ant Oecophylla smaragdina preying upon pollinator gallers Ceratosolen fusciceps entering a syconium through the ostiole; ants are attracted by syconial volatiles at pollen-receptive phase.

E Oviposition by parasitoid Apocrypta sp. Plant tissues rich in meristems are likely most suitable for gall initiation Carneiro et al. In the fig pollination mutualism, where gallers are pollinators and gall individual flowers at the expense of seeds, a diverse volatile organic compound VOC blend attracts agaonid wasp pollinators Hossaert-McKey et al.

These are likely produced by glandular cells in the outer wall of fig syconia enclosed globular inflorescences or in bracts surrounding the syconium opening at the pollen-receptive stage Souza et al. These blends comprise mostly terpenoids, with some benzenoids and aliphatic compounds Borges, In one study, 4-methylanisole was proposed as the major pollinator attractant Chen et al. Another study determined that enantiomeric mixtures of some dominant monoterpenes were more attractive to pollinators than others Chen and Song, Besides pollinating gallers, most fig syconia also harbor non-pollinating, parasitic galler wasp species Herre et al.

Sometimes floral VOCs serves as cues for leaf gallers. Floral volatiles in Salix are long-distance attractants for leaf-galling sawflies Pontania proxima Kehl et al. Although the target galling sites are leaves, flowering twigs produce 90 times more VOC quantities than non-flowering twigs suggesting that using floral volatiles as a proxy for leaves may be an efficient host-finding strategy; more flowering than non-flowering plants were galled. Interestingly, the antennae also responded to green leaf volatiles GLVs. Considering the voluminous research on cecidomyiid and cynipid galls, very little work exists on host volatiles as attractants.

The ecological and evolutionary importance of nectar‐secreting galls

Volatiles of flowering stems of the herbaceous perennial Silphium Asteraceae attracted the cynipid gall wasp Antistrophus rufus Tooker et al. The compound ratios in the blend must be crucial since these monoterpenes are present in sympatric Silphium species to which the cynipids are not attracted. Male cynipid wasps use parts of this same blend to locate females within galled stems indicating that host volatiles are employed as mate location cues Tooker et al.

The cynipid chestnut gall wasp Dryocosmus kuriphilus was attracted to a GLV blend from Castanea stems 60— min after damage, and failed to be attracted to intact stems Germinara et al. All these compounds were detected by wasp antennae.

The ecological and evolutionary importance of nectar‐secreting galls

C6 volatiles from young apple leaves were major attractants, eliciting EAD responses in the apple cecidomyiid midge Dasineura mali Anfora et al. Female orange wheat blossom cecidomyiid midges Sitodiplosis mosellana were attracted by key compounds, e. For root-knot nematodes, CO 2 seems to be the most important attractant released by actively respiring roots Rasmann et al. Low concentrations of lauric or dodecanoic acid attract root-knot nematodes while this VOC is repellent at high levels Dong et al.

A successful galling strategy may require that gall makers suppress the induction of plant defenses Kant et al. Since many plant-induced defenses involve activation of the jasmonic acid JA pathway, which also often results in volatile release, it is therefore not surprising that VOC production is often suppressed during galling.

A meta-analysis of secondary metabolites that are up-regulated on gall induction found that, unlike other metabolites, volatiles were usually unaffected Hall et al. For example, goldenrod plants Solidago altissima showed no increase in VOC emission after attack by galling flies Eurosta solidagnis or galling moths Gnorimoschema gallaesolidaginis Tooker et al.

Furthermore, infestation by E. Tooker and De Moraes speculate that gallers are adapted to suppress JA, since JA inhibits plant growth hormones such as auxin and also cytokinins, both of which must be locally up-regulated in gall formation Tooker and Helms, Whether gallers can suppress ethylene production which could impact VOC production Broekgaarden et al.

Some insect gallers may synthesize phytohormones, e. Gallers may succeed in suppressing plant defenses by deploying effector molecules Zhao et al. Five non-mutually exclusive mechanisms have been suggested for the absence of increased VOC emission after galling Tooker et al. Besides the SA up-regulation mentioned above, they include a avoidance of galler detection, b targetting relatively non-reactive tissues, e. In flower galls produced by the dipteran Myopites stylatus on the woody fleabane Dittrichia viscosa Asteraceae , emission of the phenylpropene compound estragole, an isomer of anethole, increased six times compared to ungalled flowers Santos et al.

A moderate increase in anethole was also evident. The terpene eucalyptol 1,8-cineole was emitted in large quantities only from galls, and was absent from floral scents. Eucalyptol emitted by another Asteraceae plant was a repellent and oviposition-deterrent to mosquitoes Klocke et al.

Gall insect-host plant relationships—An ecological perspective

Many interesting questions arise from these observations on the fleabane—fly interaction. First, the concentrations of the VOCs within the gall are unknown; therefore, whether high concentrations of estragole and anethole are also present within gall tissues is not known. If so, are they being produced by the galler by hijacking plant biochemical machinery to their advantage, so that non-resistant galler enemies such as parasitoids are also deterred? It is also possible that gallers are unable to manipulate VOC release and that VOC emission is under multifactorial control resulting in unexpected VOC emission patterns.

In another example, the aphid Baizongia pistaciae induces galls on the terminal buds of the pistachio Pistacia palaestina Anacardiaceae. The high terpene levels resulted from increased biosynthetic activity within the galls rather than accumulation from surrounding tissue Rand et al.

Concentrations of three terpenes, i. The principal galler enemies in this study were mammalian herbivores, i. While the authors speculate that terpenes were largely responsible for the feeding deterrence, they admit that the high gall tannin concentrations may also have deterrent effects.