The interaction of plants and their herbivorous opponents has shaped the evolution of an intricate network of defences and counter-defences for millions of years. The result is an astounding diversity of phytochemicals and plant strategies to fight and survive. Trees are specifically challenged to resist the plethora of abiotic and biotic stresses due to their dimension and longevity. Here, we review the recent literature on the consequences of phytochemical variation in trees on insect–tree–herbivore interactions. We discuss the importance of genotypic and phenotypic variation in tree defence against insects and suggest some molecular mechanisms that might bring about phytochemical diversity in crowns of individual trees.
Plants and insects coevolved since more than 350 million years (Whitney and Glover 2013) and during this time plants have developed an enormous diversity of chemical defence compounds. An arms race between insects and plants is thought to be the main driver of diversification in plant defence chemistry (Ehrlich and Raven 1964). Trees, as long-lived woody perennials, are dominant components of terrestrial ecosystems and they host an enormous diversity of insects (Basset et al. 2012). Their longevity, their size, their architecture and the formation of wood make the appearance of trees very different from herbaceous plant species. A survey of leaf herbivory across all major plant lineages revealed that compared to herbaceous plants, woody species experience 60% more herbivory (Turcotte et al. 2014). How can individual trees withstand these loads of herbivores and the amount of concomitant damage throughout their lifetime of sometimes hundreds of years? They have evolved physical barriers such as spines and thorns as well as tough, lignified leaves and on top of this they produce a large diversity of carbon-based phytochemicals such as phenolics and terpenoids as defences against their attackers. Additionally, there are vertical and horizontal gradients in abiotic conditions in treetops that can promote variation in tree defence chemistry which in turn can affect insect herbivore performance. In the eye of a tiny herbivorous insect, the treetop of a single tree is not just a homogenous predictable habitat but rather a heterogeneous and often inhospitable environment. Phytochemical diversity in treetops has the potential to shape insect community diversity and population structure as recent studies in woody species within the tropical genus Piper convincingly showed (Glassmire et al. 2016; Richards et al. 2015). In the light of this, it seems surprising that both the differences in the phytochemical composition within a tree crown, as well as the elucidation of potential mechanism maintaining phytochemical variation, has received little attention (Table 1).
Here, we review the recent literature of the last 15 years on causes and consequences of intra-specific variation in tree defence chemistry against insect herbivores aboveground. Recent findings on the role of abiotic conditions, tree genotype, spatial and temporal patterns, ontogeny and herbivore feeding for tree phytochemical variation are summarized (Fig. 1). In this manuscript, we want to specifically emphasize the phytochemical variation within treetops of old-growth trees, and the consequences for insect herbivores, as the vertical dimension of trees has so far almost been neglected in studies on tree defence chemistry (Table 1). In the second part of this review, we outline different molecular mechanisms that contribute to the maintenance of phytochemical variation in plants (Fig. 1). The recent literature from mostly herbaceous species is used to suggest molecular mechanisms responsible for the variation in tree defence chemistry against insect herbivores. In a final chapter, we point out the lack of knowledge in the mechanistic understanding of tree defence against insect herbivores under natural conditions and suggest an interdisciplinary research approach to study the ecology of tree-insect interactions in the future.
The tree genotype determines intra-specific variation in phytochemistry
Intra-specific genotypic variation in trees is known to be a major driver of phenotypic plasticity that can also shape arthropod community structures via genotypic effects on variation in tree defence chemistry (Donaldson and Lindroth 2007; Whitham et al. 2006, Bernhardsson et al. 2013). Studies in poplar trees have shown that intra-specific genotypic variation has strong effects on the concentration of compounds in the two major groups of phenolic defences, condensed tannins and salicinoids (e.g., Donaldson and Lindroth 2007). Genotypic effects on tree phytochemistry were, e.g., also shown in studies on willow (Barbour et al. 2015), Eucalyptus (Barbour et al. 2009; Gosney et al. 2017) and birch (Haviola et al. 2012). The phytochemistry of trees has been suggested to be the intermediate link between tree genes and the arthropods associated with trees by the genetic similarity rule (Bangert et al. 2006). However, empirical studies have shown that the tree genotype is not always the best predictor for arthropod community composition and insect herbivore feeding patterns. In a study by Maldonado-Lopez et al. (2015) on the relationship between red oak genetics, phytochemistry and damage patterns by two herbivorous feeding guilds, leaf chewers and leaf miners, only damage by the latter was explained by genetics and tree chemistry. In Norway spruce galling aphid communities were not related to tree phytochemical profiles and tree genetics only affected the abundance of galls within one taxonomic group but not the other (Axelsson et al. 2015). A recent study comparing 100 naturally growing adult oak trees (Quercus robur, Q. petraea) found no evidence for genotype effects on arthropod communities but chemical traits as potential links between tree genetics and arthropod community structure were not explicitly investigates in this study (Gossner et al. 2015).
Abiotic conditions affect the tree defence chemistry
Certainly a main driver of phytochemical variation in trees is the abiotic environment which in itself can vary dramatically throughout the lifetime of a tree and even through the course of 1 day. A number of recent common garden and laboratory studies investigated the impact of abiotic conditions such as rainfall, humidity, nutrient availability and temperature on tree defence chemistry (e.g., Jamieson et al. 2015; Vallat et al. 2005). Together with studies looking at phytochemical variation in trees in response to climate change scenarios with, e.g., increases in temperature, O3, CO2, as well as more frequent drought and frost periods [recently reviewed by Lindroth (2010) and Jamieson et al. (2012)], a picture emerges where the phytochemical composition is heavily influenced not only by the genetic make-up of a given species, but also by these non-intrinsic abiotic factors (Blande et al. 2007; Copolovici et al. 2014; Couture et al. 2017; Gutbrodt et al. 2012; Hale et al. 2005). The phytochemistry of young Populus tremuloides trees substantially changed in response to experimental vernal freezing (Rubert-Nason et al. 2017) with decreased concentrations of condensed tannins and slightly increased levels of phenolic glycosides in the foliage of frost-stressed trees as compared to control trees. In naturally growing mature P. tremuloides trees, however, vernal freezing induced only changes in phenolic glycoside levels (St Clair et al. 2009). A recent study by Abdala-Roberts et al. (2016) suggests that temperature is the most important factor explaining variation in the defence chemistry of mature pedunculated oak (Q. robur) trees occurring at different altitudes in Northern Spain. In this study, the foliar concentrations of phenolic compounds (rutin, gallic acid and catechin) significantly increased with decreasing mean annual temperatures of 4 °C across an elevation gradient of around 800 m.
There are strong temporal and ontogenetic patterns in tree defence chemistry
The phytochemical composition in trees can also strongly vary over time (Yamasaki and Kikuzawa 2003) and diurnal rhythms of, e.g., tree volatile emission (Clavijo McCormick et al. 2014a; Giacomuzzi et al. 2017; Trowbridge et al. 2014) as well as seasonal changes in carbon-based defence compounds were documented (Gripenberg et al. 2007; Holeski et al. 2012). The chronologically oldest branches in a tree, i.e., closest to the root crown will exhibit the youngest phenotype whereas the most distant shoots at the outer rim of the tree crown display the more mature phenotype. Kearsley and Whitham (1998) termed this counterintuitive phenomenon of within-tree phenotypic plasticity the “developmental stream”. Ramets within the crown of one tree genotype can, thus, vary significantly in their phytochemical profiles (Rehill et al. 2006; Smith et al. 2011) and even within these ramets an ontogenetic gradient in phytochemistry can occur (Boeckler et al. 2013).
Insect herbivory is a major source of phytochemical variation in trees
One of the main reasons for the observed phytochemical variation within tree species might very well be explained by differences in individual biotic interactions with pathogens and herbivores (vertebrates and invertebrates). Unlike simplified single species interactions studied in the greenhouse and in the lab, naturally growing trees of all age classes are simultaneously attacked by numerous insects and pathogens. This induces variable levels of damage, ranging from losses of a few leaves to complete defoliation. Attack by an insect herbivore induces rapid local and systemic responses by de novo synthesis and relocation of defence compounds such as phenolics or terpenoids. Phenolics in tree leaves can make up to a quarter of the leaf dry weight as in the case of condensed tannins and salicinoids in aspen (Donaldson and Lindroth 2008; Donaldson et al. 2006). These compounds are constantly present in tree tissues and thus termed constitutive defences just like terpenoids in coniferous resins are. Insect feeding, however, can induce an increase in the concentration of these phytochemicals. The induction of phenolics in trees is dependent on the tree species, the genotype and the attacking insect herbivore species. In poplar for instance, only a few studies have shown the induction of salicinoids (phenolic glycosides), a major group of phenolic defences (Rubert-Nason et al. 2015), whereas other studies did not see induction after herbivore attack at all (Boeckler et al. 2013). Insect herbivory also induces a change in the composition of volatile organic compounds (VOCs) released from trees. Upon gypsy moth (Lymantria dispar) caterpillar feeding young black poplar (Populus nigra) trees increase their emission of VOCs by more than 20-fold and the herbivore-induced blend qualitatively differs from the volatiles released from non-damaged control trees. Minor nitrogenous compounds (aldoximes and nitriles) are only emitted by the trees when they are attacked by herbivores (Clavijo McCormick et al. 2014b) and the composition of herbivore-induced black poplar VOCs also varies in response to different herbivore species (Unsicker et al. 2015). Variation in tree VOC emission due to insect herbivore feeding has been reported in a number of tree species such as pine (Heijari et al. 2011; Trowbridge et al. 2014), oak (Copolovici et al. 2017; Staudt and Lhoutellier 2007), alder (Copolovici et al. 2014), beech (Gossner et al. 2014), apple (Suckling et al. 2012) and willow (Yoneya et al. 2010). Changes in VOC emission upon insect herbivore damage are not restricted to the locally damaged sites but also occur in non-damaged adjacent foliage in apical direction (Clavijo McCormick et al. 2014b). Under field conditions in old-growth black poplar trees, however, this systemic induction of herbivore-induced VOCs was not significant (Unsicker unpublished data). Besides producing defence chemicals immediately upon insect herbivore damage, trees are also able to respond to severe defoliation by increasing their defence in the next growing season. This phenomenon termed “delayed-inducible resistance” has been shown for a number of mainly deciduous tree species (e.g., Haukioja 1991; Kaitaniemi et al. 1998; Martemyanov et al. 2012) but also conifers with inconsistent results (Lombardero et al. 2016; Roitto et al. 2009).
Phytochemical variation in treetops: the overlooked vertical dimension
It may seem trivial to specifically point out here that all abiotic and biotic variables influencing intra-specific variation in tree phytochemistry can also cause phytochemical variation within the treetop of a single tree. Under natural conditions, the abiotic conditions in treetops can vary drastically along the vertical and horizontal axis. The outer part of the tree crowns experiences very different levels or irradiation, wind speed, temperature and humidity than the innermost crown areas. As a consequence, microclimatic conditions within trees can be highly variable. Additionally, spatial variation in arthropod abundance and insect herbivore feeding in tree crowns have been observed (Robinson et al. 2012, Basset et al. 2003; Rowe and Potter 1996; Unsicker and Mody 2005; Yamasaki and Kikuzawa 2003) and thus it seems intuitively logical, that there must also be a large spatial component in the variation of tree defence chemistry within the treetop of a single tree. Unfortunately, most studies on tree defence chemistry, specifically the ones with experimental approaches, have been performed in small, immature trees likely due to the difficulties in accessing large old-growth trees (Barker and Pinard 2001). To our knowledge, there is hardly any study that focused specifically on phytochemical variation in different layers of large, mature trees (Table 1).
Molecular mechanisms of phytochemical variation in tree species and individual treetops
The diversification of defence compounds and defence strategies within tree species is largely based on genetic variation. The mechanisms creating the substrate for this evolutionary change are diverse and a detailed review of these is beyond the scope of this article (for a review, see, e.g., Chen et al. 2013). One prominent mechanism for creating genetic diversity is the duplication of genes or, more prominent in plants, whole genome duplications (Panchy et al. 2016). Most duplicated genes are lost in the course of evolution (Lynch and Conery 2003) but when they are retained, they can acquire new functions. One illustrative example for this is the massive diversification of compounds within the group of terpenoids. Currently, more than 30.000 different terpenes are known (Keeling and Bohlmann 2006). Here, different terpene synthases (mono-, sesqui-, and diterpene synthases), which apparently evolved through repeated duplication followed by functional diversification, produce an amazingly diverse array of terpene backbones (Zapata and Fine 2013). Interestingly, the diversification in the group of terpenoids might be due to different mechanisms in mono- and dicot species (Boutanaev et al. 2015). Species hybridization can furthermore increase the phytochemical diversity in trees (Caseys et al. 2015) in a local context as could be envisioned for the local accumulation of advantageous single nucleotide polymorphisms (SNPs) (Bernhardsson and Ingvarsson, 2012). In trees, the above-mentioned mechanisms do not only lead to a diversification of compounds, but also ultimately, and possibly more importantly from an ecological perspective, shape community compositions of a given habitat (Whitham et al. 2006) and additionally provide the basis for new species interactions at the ecosystem level (Benfey and Mitchell-Olds 2008).
The importance of the above-described mechanisms in creating species diversity on an evolutionary time scale cannot be overestimated. For a single tree, faced with the challenge of responding to myriads of attackers throughout its lifetime, however, the phytochemical diversity created in the past is a mere platform to act and survive in the present, using the arsenal provided by its (lifetime-wise) largely invariant genome (Sarkar et al. 2017). However, somatic mutations (alterations in the genetic information that is not transmitted to the next generation) might, in specific cases, play a role for phenotypic diversity within an individual tree as in the case of mosaic trees within the genus Eucalyptus (Padovan et al. 2012, 2015).
Given the vertical and horizontal dimension of mature tree crowns, the challenges one crown area faces might be very different to what another crown area tackles at the same time. Consequently, the heterogeneity of influential variables may lead to local adaptations in different parts of the treetop.
In the following, we will review potential mechanisms leading to intra-crown (treetop) diversity in phytochemistry. The sensing of a local challenge (e.g., insect herbivory) provides informational value for the tree that might be relevant for other parts of the tree as well. Transmission of this information requires efficient and fast means of communication between both the affected, as well as the (yet) unaffected tissues, which can be realized, e.g., by VOC emission (Heil and Karban 2010). As mentioned earlier, trees emit specific blends of VOCs upon herbivore attack but interestingly, this signal is only emitted as long as there is actual feeding (Clavijo Mc Cormick et al. 2014a). Herbivore-induced VOCs, thus, signal a potential threat in the future and prime non-damaged tissues for a faster and stronger response, e.g., upon a second herbivory event (Frost et al. 2008). This raises the question how this perceived information is stored and then only transferred into a chemical defence response when, e.g., insect herbivore attack happens. Mechanistically, this requires several steps: the information needs to be spread to receivers and be decoded (e.g., VOCs emitted upon herbivory need to be sensed and linked to a response). After decoding the information, some kind of memory of this information needs to be established and this memory then alters the response when a specific stress (e.g., herbivory) recurs. Here, different (and certainly nonexclusive) mechanisms to store information locally have been proposed. These range from an increase in inactive signalling compounds like signalling kinases (Beckers et al. 2009), which, once activated by a specific stimulus, lead to a massive amplification of signalling and hence a potentially quicker and stronger response. Another possibility is the accumulation of specific metabolites (Navarova et al. 2012), which are either directly involved in defence or which serve as signalling molecules that can be released once stress recurs. A widely observed pattern in primed plant responses are alterations in transcriptional activity, where a primed transcriptional response is different from the transcriptional response when stress is encountered for the first time (Hilker et al. 2016). When altered transcriptional responses are observed, chromatin modifications offer a mechanistically intuitive way of modulation. In the nucleus, DNA is organized in a structure called chromatin (all nuclear DNA and associated proteins like histones); modifications to histones or DNA either directly or indirectly regulate the accessibility of genomic loci and either facilitate or restrict transcriptional activity. Indeed, chromatin was long viewed as an interface between the environment and the genome. In genetically identical ramets of poplar, for example, globally altered DNA-methylation patterns depending on growth history were described (Raj et al. 2011). In herbaceous plants, recurring stress lead to altered levels of histone modifications at stress relevant loci, which correlated with altered transcriptional responses when stress recurred (Ding et al. 2012; Jaskiewicz et al. 2011; Lämke et al. 2016). These works established histone 3, lysine 4 hypermethylation as a potential memory mark that might be instructive for altered transcriptional activity when loci are re-activated upon a second stress. Of note, this chromatin modification persisted long after the initial transcriptional activity ceased and hence might store the perceived information (Conrath et al. 2015; Lämke and Baurle 2017). In case of priming within the tree crown, this scenario suggests that priming might lead to different chromatin states within the crown, which then allow for the modulation of (transcriptional) responses when a stress either spreads or recurs, leading to locally different phytochemical responses to the same challenge. Indeed, alterations in transcriptional responses are observed upon priming by volatiles and subsequent challenge (Frost et al. 2008). It seems reasonable to assume that trees use chromatin-based mechanisms extensively to store perceived information within the tree crown to allow for an adapted response. We are currently lacking a clear picture of both the extent as well as the duration of chromatin based memory in trees. Given the very long life span and sheer size of a tree, resulting both in the constant need to adapt to the changing local environment and the highly informative value of previous stress exposure, it seems very plausible that trees use chromatin-based means extensively to constantly adapt and be prepared for future challenges (Bräutigam et al. 2013).
Critical remarks and future directions
In this article, we outlined different sources of phytochemical variation within tree species and individual treetops and suggested mechanisms at the molecular level to maintain this variation.
An obvious drawback in the studies on tree defence chemistry and the consequences for insect herbivores is that they are limited to a narrow range of tree species or genera (i.e., oak, poplar, willow, pine, eucalyptus, birch) and within those only a few or single tree genotypes. Furthermore, most experimental studies investigating tree defence mechanisms are performed under controlled greenhouse or laboratory conditions with immature trees, raising the question whether the results from these studies allow us to deduce generalities and make predictions also for mature trees under natural conditions. Experimentally applied abiotic and biotic stresses are mostly inflicted singly and only rarely are trees under laboratory conditions exposed to real-world scenarios with, e.g., simultaneously occurring biotic and abiotic stresses. Even under field conditions, the majority of studies on tree defences investigate younger trees of reasonable height, as it is certainly challenging, if not impossible, to obtain samples for phytochemical analysis representing the entire treetop of a large old-growth trees. Furthermore, field studies are mostly descriptive and rarely imply experimental approaches with modern molecular methods. Well-replicated experimental approaches within treetops of old-growth trees are very demanding and likely restricted to sites with canopy cranes, canopy walkways or trees accessible with, e.g., the single rope climbing technique. Despite these difficulties, we urgently need the synthesis of field based experiments in old-growth trees with experimental approaches using modern molecular techniques to reveal the causes and consequences of phytochemical variation in trees for tree-insect-herbivore interactions. Here, “genome-enabled field biologists” (Baldwin 2012) with a fascination for climbing trees should step up to the plate.
Abdala-Roberts L, Rasmann S, Berny-Mier YTJC, Covelo F, Glauser G, Moreira X (2016) Biotic and abiotic factors associated with altitudinal variation in plant traits and herbivory in a dominant oak species. Am J Bot 103:2070–2078. https://doi.org/10.3732/ajb.1600310
Agrawal AA, Weber MG (2015) On the study of plant defence and herbivory using comparative approaches: how important are secondary plant compounds. Ecol Lett 18:985–991. https://doi.org/10.1111/ele.12482
Axelsson EP, Iason GR, Julkunen-Tiitto R, Whitham TG (2015) Host genetics and environment drive divergent responses of two resource sharing gall-formers on Norway Spruce: a common garden analysis. PLoS One 10:e0142257. https://doi.org/10.1371/journal.pone.0142257
Baldwin IT (2012) Training a new generation of biologists: the genome-enabled field biologists. Proc Am Philos Soc 156:204–2014
Bangert RK et al (2006) A genetic similarity rule determines arthropod community structure. Mol Ecol 15:1379–1391. https://doi.org/10.1111/j.1365-294X.2005.02749.x
Barbour RC et al (2009) A geographic mosaic of genetic variation within a foundation tree species and its community-level consequences. Ecology 90:1762–1772. https://doi.org/10.1890/08-0951.1
Barbour MA et al (2015) Multiple plant traits shape the genetic basis of herbivore community assembly. Funct Ecol 29:995–1006. https://doi.org/10.1111/1365-2435.12409
Barker MG, Pinard MA (2001) Forest canopy research: sampling problems, and some solutions. Plant Ecol 153:23–38
Basset Y, Hammond PM, Barrios H, Holloway JD, Miller SE (2003) Vertical stratification of arthropd assemblages. In: Basset Y, Novotny V, Miller SE, Kitching RL (eds) Arthropods of tropical forests. Cambridge University Press, Cambridge
Basset Y et al (2012) Arthropod diversity in a tropical forest. Science 338:1481–1484. https://doi.org/10.1126/science.1226727
Beckers GJM et al (2009) Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 21:944–953. https://doi.org/10.1105/tpc.108.062158
Benfey PN, Mitchell-Olds T (2008) From genotype to phenotype: systems biology meets natural variation. Science 320:495–497. https://doi.org/10.1126/science.1153716
Bernhardsson C, Ingvarsson PK (2012) Geographical structure and adaptive population differentiation in herbivore defence genes in European aspen (Populus tremula L., Salicaceae). Mol Ecol 21:2197–2207. https://doi.org/10.1111/j.1365-294X.2012.05524.x
Bernhardsson C, Robinson KM, Abreu IN, Jansson S, Albrectsen BR, Ingvarsson PK (2013) Geographic structure in metabolome and herbivore community co-occurs with genetic structure in plant defence genes. Ecol Lett 16:791–798. https://doi.org/10.1111/ele.12114
Blande JD, Tiiva P, Oksanen E, Holopainen JK (2007) Emission of herbivore-induced volatile terpenoids from two hybrid aspen (Populus tremula × tremuloides) clones under ambient and elevated ozone concentrations in the field. Glob Change Biol 13:2538–2550
Boeckler GA, Gershenzon J, Unsicker SB (2011) Phenolic glycosides of the Salicaceae and their role as anti-herbivore defences. Phytochemistry 72:1497–1509. https://doi.org/10.1016/j.phytochem.2011.01.038
Boeckler GA, Gershenzon J, Unsicker SB (2013) Gypsy moth caterpillar feeding has only a marginal impact on phenolic compounds in old-growth black poplar. J Chem Ecol 39:1301–1312. https://doi.org/10.1007/s10886-013-0350-8
Boutanaev AM et al (2015) Investigation of terpene diversification across multiple sequenced plant genomes. PNAS 112:E81–E88. https://doi.org/10.1073/pnas.1419547112
Bräutigam K et al (2013) Epigenetic regulation of adaptive responses of forest tree species to the environment. Ecol Evol 3:399–415. https://doi.org/10.1002/ece3.461
Caseys C, Stritt C, Glauser G, Blanchard T, Lexer C (2015) Effects of hybridization and evolutionary constraints on secondary metabolites: the genetic architecture of phenylpropanoids in European Populus species. PLoS One 10:e0128200. https://doi.org/10.1371/journal.pone.0128200
Chen SD, Krinsky BH, Long MY (2013) New genes as drivers of phenotypic evolution. Nat Rev Genet 14:645–660. https://doi.org/10.1038/nrg3521
Clavijo McCormick A, Boeckler G, Köllner TG, Gershenzon J, Unsicker SB (2014a) The timing of herbivore-induced volatile emission in black poplar (Populus nigra) and the influence of herbivore age and identity affect the value of individual volatiles as cues for herbivore enemies. BMC Plant Biol 14:304. https://doi.org/10.1186/s12870-014-0304-5
Clavijo McCormick A et al (2014b) Herbivore-induced volatile emission in black poplar: regulation and role in attracting herbivore enemies. Plant Cell Environ 37:1909–1923. https://doi.org/10.1111/pce.12287
Conrath U, Beckers GJM, Langenbach CJG, Jaskiewicz MR (2015) Priming for enhanced defence. In: Van Alfen NK (ed) Annual review of phytopathology, vol 53, pp 97–119. https://doi.org/10.1146/annurev-phyto-080614-120132
Copolovici L, Kannaste A, Remmel T, Niinemets U (2014) Volatile organic compound emissions from Alnus glutinosa under interacting drought and herbivory stresses. Environ Exp Bot 100:55–63. https://doi.org/10.1016/j.envexpbot.2013.12.011
Copolovici L et al (2017) Disproportionate photosynthetic decline and inverse relationship between constitutive and induced volatile emissions upon feeding of Quercus robur leaves by large larvae of gypsy moth (Lymantria dispar). Environ Exp Bot 138:184–192. https://doi.org/10.1016/j.envexpbot.2017.03.014
Couture JJ, Meehan TD, Rubert-Nason KF, Lindroth RL (2017) Effects of elevated atmospheric carbon dioxide and tropospheric ozone on phytochemical composition of trembling aspen (Populus tremuloides) and paper birch (Betula papyrifera). J Chem Ecol 43:26–38. https://doi.org/10.1007/s10886-016-0798-4
Ding Y, Fromm M, Avramova Z (2012) Multiple exposures to drought ‘train’ transcriptional responses in Arabidopsis. Nat Communications 3:740. https://doi.org/10.1038/ncomms1732
Donaldson JR, Lindroth RL (2007) Genetics, environment, and their interaction determine efficacy of chemical defence in trembling aspen. Ecology 88:729–739
Donaldson JR, Lindroth RL (2008) Effects of variable phytochemistry and budbreak phenology on defoliation of aspen during a forest tent caterpillar outbreak. Agric For Entomol 10:399–410. https://doi.org/10.1111/j.1461-9563.2008.00392.x
Donaldson JR, Stevens MT, Barnhill HR, Lindroth RL (2006) Age-related shifts in leaf chemistry of clonal aspen (Populus tremuloides). J Chem Ecol 32:1415–1429. https://doi.org/10.1007/s10886-006-9059-2
Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608
Frost CJ, Mescher MC, Dervinis C, Davis JM, Carlson JE, De Moraes CM (2008) Priming defence genes and metabolites in hybrid poplar by the green leaf volatile cis-3-hexenyl acetate. New Phytol 180:722–733. https://doi.org/10.1111/j.1469-8137.2008.02599.x
Giacomuzzi V et al (2017) Diel rhythms in the volatile emission of apple and grape foliage. Phytochemistry 138:104–115. https://doi.org/10.1016/j.phytochem.2017.03.001
Glassmire AE et al (2016) Intraspecific phytochemical variation shapes community and population structure for specialist caterpillars. New Phytol 212:208–219. https://doi.org/10.1111/nph.14038
Gosney B, O’Reilly-Wapstra J, Forster L, Whiteley C, Potts B (2017) The extended community-level effects of genetic variation in foliar wax chemistry in the forest tree Eucalyptus globulus. J Chem Ecol 43:532–542. https://doi.org/10.1007/s10886-017-0849-5
Gossner MM, Weisser WW, Gershenzon J, Unsicker SB (2014) Insect attraction to herbivore-induced beech volatiles under different forest management regimes. Oecologia 176:569–580. https://doi.org/10.1007/s00442-014-3025-4
Gossner MM, Brandle M, Brandl R, Bail J, Muller J, Opgenoorth L (2015) Where is the extended phenotype in the wild? The community composition of arthropods on mature oak trees does not depend on the oak genotype. PLoS One 10:e0115733. https://doi.org/10.1371/journal.pone.0115733
Gripenberg S, Salminen JP, Roslin T (2007) A tree in the eyes of a moth - temporal variation in oak leaf quality and leaf-miner performance. Oikos 116:592–600. https://doi.org/10.1111/j.2007.0030-1299.15415.x
Gutbrodt B, Dorn S, Mody K (2012) Drought stress affects constitutive but not induced herbivore resistance in apple plants. Arthropod Plant Interact 6:171–179. https://doi.org/10.1007/s11829-011-9173-0
Hale BK, Herms DA, Hansen RC, Clausen TP, Arnold D (2005) Effects of drought stress and nutrient availability on dry matter allocation, phenolic glycosides, and rapid induced resistance of poplar to two lymantriid defoliators. J Chem Ecol 31:2601–2620
Haukioja E (1991) Induction of defences in trees. Annu Rev Entomol 36:25–42
Haviola S et al (2012) Genetic and environmental factors behind foliar chemistry of the mature mountain birch. J Chem Ecol 38:902–913. https://doi.org/10.1007/s10886-012-0148-0
Heijari J, Blande JD, Holopainen JK (2011) Feeding of large pine weevil on Scots pine stem triggers localised bark and systemic shoot emission of volatile organic compounds. Environ Exp Bot 71:390–398. https://doi.org/10.1016/j.envexpbot.2011.02.008
Heil M, Karban R (2010) Explaining evolution of plant communication by airborne signals. Trends Ecol Evol 25:137–144. https://doi.org/10.1016/j.tree.2009.09.010
Hilker M et al (2016) Priming and memory of stress responses in organisms lacking a nervous system. Biol Rev 91:1118–1133. https://doi.org/10.1111/brv.12215
Holeski LM, Hillstrom ML, Whitham TG, Lindroth RL (2012) Relative importance of genetic, ontogenetic, induction, and seasonal variation in producing a multivariate defence phenotype in a foundation tree species. Oecologia 170:695–707. https://doi.org/10.1007/s00442-012-2344-6
Jamieson MA, Trowbridge AM, Raffa KF, Lindroth RL (2012) Consequences of climate warming and altered precipitation patterns for plant-insect and multitrophic interactions. Plant Physiol 160:1719–1727. https://doi.org/10.1104/pp.112.206524
Jamieson MA, Schwartzberg EG, Raffa KF, Reich PB, Lindroth RL (2015) Experimental climate warming alters aspen and birch phytochemistry and performance traits for an outbreak insect herbivore. Glob Change Biol 21:2698–2710. https://doi.org/10.1111/gcb.12842
Jaskiewicz M, Conrath U, Peterhansel C (2011) Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep 12:50–55. https://doi.org/10.1038/embor.2010.186
Kaitaniemi P, Ruohomaki K, Ossipov V, Haukioja E, Pihlaja K (1998) Delayed induced changes in the biochemical composition of host plant leaves during an insect outbreak. Oecologia 116:182–190. https://doi.org/10.1007/s004420050578
Kearsley MJC, Whitham TG (1998) The developmental stream of cottonwoods affects ramet growth and resistance to galling aphids. Ecology 79:178–191
Keeling CI, Bohlmann J (2006) Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens. New Phytol 170:657–675. https://doi.org/10.1111/j.1469-8137.2006.01716.x
Lämke J, Bäurle I (2017) Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biol 18:124. https://doi.org/10.1186/s13059-017-1263-6
Lämke J, Brzezinka K, Altmann S, Bäurle I (2016) A hit-and-run heat shock factor governs sustained histone methylation and transcriptional stress memory. EMBO J 35:162–175. https://doi.org/10.15252/embj.201592593
Lindroth RL (2010) Impacts of elevated atmospheric CO2 and O3 on forests: phytochemistry, trophic interactions, and ecosystem dynamics. J Chem Ecol 36:2–21. https://doi.org/10.1007/s10886-009-9731-4
Lombardero MJ, Ayres MP, Bonello P, Cipollini D, Herms DA (2016) Effects of defoliation and site quality on growth and defences of Pinus pinaster and P. radiata. For Ecol Manag 382:39–50. https://doi.org/10.1016/j.foreco.2016.10.003
Lynch M, Conery JS (2003) The evolutionary demography of duplicate genes. J Struct Funct Genom 3:35–44
Maldonado-Lopez Y, Cuevas-Reyes P, Gonzalez-Rodriguez A, Perez-Lopez G, Acosta-Gomez C, Oyama K (2015) Relationships among plant genetics, phytochemistry and herbivory patterns in Quercus castanea across a fragmented landscape. Ecol Res 30:133–143. https://doi.org/10.1007/s11284-014-1218-2
Martemyanov VV et al (2012) The effects of defoliation-induced delayed changes in silver birch foliar chemistry on gypsy moth fitness, immune response, and resistance to baculovirus infection. J Chem Ecol 38:295–305. https://doi.org/10.1007/s10886-012-0090-1
Navarova H, Bernsdorff F, Doring AC, Zeier J (2012) Pipecolic acid, an endogenous mediator of defense amplification and priming, is a critical regulator of inducible plant immunity. Plant Cell 24:5123–5141. https://doi.org/10.1105/tpc.112.103564
Padovan A, Keszei A, Wallis IR, Foley WJ (2012) Mosaic eucalypt trees suggest genetic control at a point that influences several metabolic pathways. J Chem Ecol 38:914–923. https://doi.org/10.1007/s10886-012-0149-z
Padovan A et al (2015) Transcriptome sequencing of two phenotypic mosaic Eucalyptus trees reveals large scale transcriptome re-modelling. Plos One 10:e0123226. https://doi.org/10.1371/journal.pone.0123226
Panchy N, Lehti-Shiu M, Shiu SH (2016) Evolution of gene duplication in plants. Plant Physiol 171:2294–2316. https://doi.org/10.1104/pp.16.00523
Raj S et al (2011) Clone history shapes Populus drought responses. PNAS 108:12521–12526. https://doi.org/10.1073/pnas.1103341108
Rehill BJ, Whitham TG, Martinsen GD, Schweitzer JA, Bailey JK, Lindroth RL (2006) Developmental trajectories in cottonwood phytochemistry. J Chem Ecol 32:2269–2285. https://doi.org/10.1007/s10886-006-9141-9
Richards LA et al (2015) Phytochemical diversity drives plant-insect community diversity. PNAS 112:10973–10978. https://doi.org/10.1073/pnas.1504977112
Robinson KM, Hauzy C, Loeuille N, Albrectsen BR (2015) Relative impacts of environmental variation and evolutionary history on the nestedness and modularity of tree-herbivore networks. Ecol Evol 5:2898–2915. https://doi.org/10.1002/ece3.1559
Robinson KM, Ingvarsson PK, Jansson S, Albrectsen BR (2012) Genetic variation in functional traits influences arthropod community composition in aspen (Populus tremula L.). PLos One 7:e37679. https://doi.org/10.1371/journal.pone.0037679
Roitto M et al (2009) Induced accumulation of phenolics and sawfly performance in Scots pine in response to previous defoliation. Tree Physiol 29:207–216. https://doi.org/10.1093/treephys/tpn017
Rowe WJ, Potter DA (1996) Vertical stratification of feeding by Japanese beetles within linden tree canopies: selective foraging or height per se? Oecologia 108:459–466. https://doi.org/10.1007/bf00333722
Rubert-Nason KF, Couture JJ, Major IT, Constabel CP, Lindroth RL (2015) Influence of genotype, environment, and gypsy moth herbivory on local and systemic chemical defences in trembling aspen (Populus tremuloides). J Chem Ecol 41:651–661. https://doi.org/10.1007/s10886-015-0600-z
Rubert-Nason KF, Couture JJ, Gryzmala EA, Townsend PA, Lindroth RL (2017) Vernal freeze damage and genetic variation alter tree growth, chemistry, and insect interactions. Plant Cell Environ. https://doi.org/10.1111/pce.13042
Sarkar N et al (2017) Low rate of somatic mutations in a long-lived oak tree. https://doi.org/10.1101/149203
Smith EA et al (2011) Developmental contributions to phenotypic variation in functional leaf traits within quaking aspen clones. Tree Physiol 31:68–77. https://doi.org/10.1093/treephys/tpq100
St Clair SB, Monson SD, Smith EA, Cahill DG, Calder WJ (2009) Altered leaf morphology, leaf resource dilution and defence chemistry induction in frost-defoliated aspen (Populus tremuloides). Tree Physiol 29:1259–1268. https://doi.org/10.1093/treephys/tpp058
Staudt M, Lhoutellier L (2007) Volatile organic compound emission from hohn oak infested by gypsy moth larvae: evidence for distinct responses in damaged and undamaged leaves. Tree Physiol 27:1433–1440
Suckling DM et al (2012) Volatiles from apple trees Infested with light brown apple moth larvae attract the parasitoid Dolichogenidia tasmanica. J Agric Food Chem 60:9562–9566. https://doi.org/10.1021/jf302874g
Trowbridge AM, Daly RW, Helmig D, Stoy PC, Monson RK (2014) Herbivory and climate interact serially to control monoterpene emissions from pinyon pine forests. Ecology 95:1591–1603
Turcotte MM, Davies TJ, Thomsen CJM, Johnson MTJ (2014) Macroecological and macroevolutionary patterns of leaf herbivory across vascular plants. Proc R Soc Lond Ser B-Biol Sci 281(1787):20140555. https://doi.org/10.1098/rspb.2014.0555
Unsicker SB, Mody K (2005) Influence of tree species and compass bearing on insect folivory of nine common tree species in the West African savanna. J Trop Ecol 21:227–231
Unsicker SB, Gershenzon J, Köllner TG (2015) Beetle feeding induces a different volatile emission pattern from black poplar foliage than caterpillar herbivory. Plant Signal Behav 10:e987522. https://doi.org/10.4161/15592324.2014.987522
Vallat A, Gu HN, Dorn S (2005) How rainfall, relative humidity and temperature influence volatile emissions from apple trees in situ. Phytochemistry 66:1540–1550
Whitham TG et al (2006) A framework for community and ecosystem genetics: from genes to ecosystems. Nat Rev Genet 7:510–523. https://doi.org/10.1038/nrg1877
Whitney HM, Glover BJ (2013) Coevolution: plant-insect eLS. Wiley, Chichester
Yamasaki M, Kikuzawa K (2003) Temporal and spatial variations in leaf herbivory within a canopy of Fagus crenata. Oecologia 137:226–232. https://doi.org/10.1007/s00442-003-1337-x
Yoneya K, Ozawa R, Takabayashi J (2010) Specialist leaf beetle larvae use volatiles from willow leaves infested by conspecifics for reaggregation in a tree. J Chem Ecol 36:671–679. https://doi.org/10.1007/s10886-010-9808-0
Zapata F, Fine PVA (2013) Diversification of the monoterpene synthase gene family (TPSb) in Protium, a highly diverse genus of tropical trees. Mol Phylogenet Evol 68:432–442. https://doi.org/10.1016/j.ympev.2013.04.024
Open access funding provided by Max Planck Society. We thank Caroline Müller and two anonymous reviewers for their helpful comments on earlier versions of this manuscript. SBU was funded by the Max Planck Society while preparing this manuscript.
Communicated by Caroline Müller.
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Lämke, J.S., Unsicker, S.B. Phytochemical variation in treetops: causes and consequences for tree-insect herbivore interactions. Oecologia 187, 377–388 (2018). https://doi.org/10.1007/s00442-018-4087-5
- Chromatin-based mechanisms
- Genotypic variation
- Insect herbivore
- Phenotypic plasticity
- Tree defence