Classic research on elevational gradients in plant–herbivore interactions holds that insect herbivore pressure is stronger under warmer, less seasonal climates characteristic of low elevations, and ...that this in turn selects for increased defence in low‐ (relative to high‐) elevation plants. However, recent work has questioned this paradigm, arguing that it overly simplifies the ecological complexity in which plant–insect herbivore interactions are embedded along elevational gradients. Numerous biotic and abiotic factors vary with elevation, and their simultaneous influences are the focus of current work on elevational gradients in insect herbivory and plant defences. The present review 1) synthesizes current knowledge on elevational gradients in plant–insect herbivore interactions; 2) critically analyses research gaps and highlights recent advances that contribute to filling these gaps; and 3) outlines new research opportunities to uncover underlying mechanisms and build towards a unified theory on elevational gradients. We conclude that the next generation of studies should embrace community complexity – including multi‐trophic dynamics and the multivariate nature of plant defence – and to do so by combining observational data, manipulative experiments and emerging analytical tools.
Plants defend themselves against herbivore attack by constitutively producing toxic secondary metabolites, as well as by inducing them in response to herbivore feeding. Induction of secondary ...metabolites can cross plant tissue boundaries, such as from root to shoot. However, whether the potential for plants to systemically induce secondary metabolites from roots to shoots shows genetic variability, and thus, potentially, is under selection conferring fitness benefits to the plants is an open question. To address this question, we induced 26 maternal plant families of the wild species
Cardamine hirsuta
belowground (BG) using the wound-mimicking phytohormone jasmonic acid (JA). We measured resistance against a generalist (
Spodoptera littoralis
) and a specialist (
Pieris brassicae
) herbivore species, as well as the production of glucosinolates (GSLs) in plants. We showed that BG induction increased AG resistance against the generalist but not against the specialist, and found substantial plant family-level variation for resistance and GSL induction. We further found that the systemic induction of several GSLs tempered the negative effects of herbivory on total seed set production. Using a widespread natural system, we thus confirm that BG to AG induction has a strong genetic component, and can be under positive selection by increasing plant fitness. We suggest that natural variation in systemic induction is in part dictated by allocation trade-offs between constitutive and inducible GSL production, as well as natural variation in AG and BG herbivore attack in nature.
It has been estimated that between 40 and 60 % of the assimilated carbon is diverted to the roots and released in the rhizosphere in form of root exudates. Root exudates thus define a complex mixture ...of low and high molecular weight compounds, including carbohydrates, amino acids, organic, and proteins, but also a broad spectrum of specialized molecules, such as flavonoids, glucosinolates, terpenoids, or alkaloids. Root exudates favour soil mineral nutrition, can bind to soil aggregate and in turn modify soil physico-chemical properties, but also mediate plant-plant, plant-microbe, and plant-animal interactions belowground. With this review, we aim to highlight how chemical ecologists have approached the study of root exudates-mediated interactions between plants and their biotic and abiotic surroundings. We do so by presenting a series of study cases for, on one hand, showcasing different methodologies that have been developed to test the activity of different root exudates, and, on the other hand, to show the broad array of interactions mediated by root exudates. Ultimately, we aim to spur further research and collaborations between chemists and ecologists studying belowground chemically-mediated interactions, so as to tackle essential challenges in terms of food security and climate change in the near future.
Global warming is predicted to dramatically alter communities' composition through differential colonization abilities, such as between sessile plants and their mobile herbivores. Novel interactions ...between previously non‐overlapping species may, however, also be mediated by altered plants' responses to herbivore attack. Syndromes of plant defences and tolerance are driven by inherited functional traits, biotic and abiotic conditions, and the geographical and historical contingencies affecting the community. Therefore, understanding climate change‐driven herbivore responses and evolution towards a particular plant defence syndrome is key to forecasting species interactions in the near future. In this paper, we first document variations in herbivory, and plant defences along altitudinal gradients that act as ‘natural experiments’. We then use an empirical model to predict how specialist herbivore abundance may shift with respect to elevation in the near future. Our field surveys and field experiment showed a decrease in herbivory with elevation. However, contrary to expectations, our meta‐regression analyses showed that plant defences, particularly leaf toughness and flavonoid compounds, tend to be higher at high elevations, while secondary metabolites showed no clear trend with elevation. Based on those results, we discuss how plant communities and species‐specific plant defence syndromes will change in response to the climate‐driven herbivore colonization of higher altitudes. Particularly, plant from high elevation, due to high protection against abiotic stress may be already ecologically fitted to resist the sudden increase in herbivory pressure that they will likely experience during global change.
Cardenolides are remarkable steroidal toxins that have become model systems, critical in the development of theories for chemical ecology and coevolution. Because cardenolides inhibit the ubiquitous ...and essential animal enzyme Na+/K+-ATPase, most insects that feed on cardenolidecontaining plants are highly specialized. With a huge diversity of chemical forms, these secondary metabolites are sporadically distributed across 12 botanical families, but dominate the Apocynaceae where they are found in > 30 genera. Studies over the past decade have demonstrated patterns in the distribution of cardenolides among plant organs, including all tissue types, and across broad geographic gradients within and across species. Cardenolide production has a genetic basis and is subject to natural selection by herbivores. In addition, there is strong evidence for phenotypic plasticity, with the biotic and abiotic environment predictably impacting cardenolide production. Mounting evidence indicates a high degree of specificity in herbivore-induced cardenolides in Asclepias. While herbivores of cardenolide-containing plants often sequester the toxins, are aposematic, and possess several physiological adaptations (including target site insensitivity), there is strong evidence that these specialists are nonetheless negatively impacted by cardenolides. While reviewing both the mechanisms and evolutionary ecology of cardenolide-mediated interactions, we advance novel hypotheses and suggest directions for future work.
Traits that mediate species interactions are evolutionarily shaped by biotic and abiotic drivers, yet we know relatively little about the relative importance of these factors. Herbivore pressure, ...along with resource availability and ‘third‐party’ mutualists, are hypothesized to play a major role in the evolution of plant defence traits. Here, we used the model system Plantago lanceolata, which grows along steep elevation gradients in the Swiss Alps, to investigate the effect of elevation, herbivore pressure, mycorrhizal inoculation and temperature on plant resistance. Over a 1200 m elevation gradient, the levels of herbivory and iridoid glycosides (IGs) declined with increasing elevation. By planting seedlings at three different elevations, we further showed that both low‐elevation growing conditions and mycorrhizal inoculation resulted in increased plant resistance to herbivores. Finally, using a temperature‐controlled experiment comparing high‐ and low‐elevation ecotypes, we showed that high‐elevation ecotypes are less resistant to herbivory, and that lower temperatures impair IGs deployment after herbivore attack. We thus propose that both lower herbivore pressure, and colder temperatures relax the defense syndrome of high elevation plants.
Inducible defenses, which provide enhanced resistance after initial attack, are nearly universal in plants. This defense signaling cascade is mediated by the synthesis, movement, and perception of ...jasmonic acid and related plant metabolites. To characterize the long-term persistence of plant immunity, we challenged Arabidopsis (Arabidopsis thaliana) and tomato (Solanum lycopersicum) with caterpillar herbivory, application of methyl jasmonate, or mechanical damage during vegetative growth and assessed plant resistance in subsequent generations. Here, we show that induced resistance was associated with transgenerational priming of jasmonic acid-dependent defense responses in both species, caused caterpillars to grow up to 50% smaller than on control plants, and persisted for two generations in Arabidopsis. Arabidopsis mutants that are deficient in jasmonate perception (coronatine insensitive1) or in the biogenesis of small interfering RNA (dicer-like2 dicer-like3 dicer-like4 and RNA polymerase d2a nuclear RNA polymerase d2b) do not exhibit inherited resistance. The observation of inherited resistance both the Brassicaceae and Solanaceae suggests that this trait may be more widely distributed in plants. Epigenetic resistance to herbivory thus represents a phenotypically plastic mechanism for enhanced defense across generations.
It is well known that plant damage by leaf-chewing herbivores can induce resistance in neighbouring plants. It is unknown whether such communication occurs in response to sap-feeding herbivores, ...whether communication is specific to herbivore identity, and the chemical basis of communication, including specificity.
We carried out glasshouse experiments using the California-native shrub Baccharis salicifolia and two ecologically distinct aphid species (one a dietary generalist and the other a specialist) to test for specificity of plant–plant communication and to document the underlying volatile organic compounds (VOCs).
We show specificity of plant–plant communication to herbivore identity, as each aphid-damaged plant only induced resistance in neighbours against the same aphid species. The amount and composition of induced VOCs were markedly different between plants attacked by the two aphid species, providing a putative chemical mechanism for this specificity. Furthermore, a synthetic blend of the five major aphid-induced VOCs (ethanone, limonene, methyl salicylate, myrcene, ocimene) triggered resistance in receiving plants of comparable magnitude to aphid damage of neighbours, and the effects of the blend exceeded those of individual compounds.
This study significantly advances our understanding of plant–plant communication by demonstrating the importance of sap-feeding herbivores and herbivore identity, as well as the chemical basis for such effects.
Costs of plant defense are a key assumption in evolutionary ecology, yet their detection has remained challenging. Here we introduce a novel method for quantifying plant growth using the common ...milkweed Asclepias syriaca and repeated non‐destructive size measurements to experimentally test for costs of defensive traits. We estimated mechanistic components of plant growth (relative growth rate, net assimilation rate, specific leaf area and leaf‐mass ratio) at two levels of fertilization (high and low), and related them to production of toxic cardenolides and exudation of sticky latex. We found negative genetic correlations between cardenolides and growth (most strongly with net assimilation rate) at both nutrient levels. Additionally, plants varied in their cardenolide response to low nutrients, and genetic families maintaining higher cardenolide production at low nutrient availability suffered proportionally larger reductions in growth. In contrast, the amount of latex was positively correlated with plant growth. Because latex is instantly deployed from a plant‐wide system of pressurized laticifers, larger plants may simply exude proportionally more latex when damaged and thus plant size is likely to mask potential costs of latex synthesis. Unbiased quantification of mechanistic growth processes, coupled with the manipulation of nutrient or stress levels, is thus an effective approach to demonstrate allocation to defense and tradeoffs with growth, especially in long‐lived plant species.
Soil nematodes are a foremost component of terrestrial biodiversity; they display a whole gamut of trophic guilds and life strategies, and by their activity, affect major ecosystem process, such as ...organic matter degradation and carbon cycling. Based on nematodes' functional types, nematode community indices have been developed, and can be used to link variation in nematodes community composition and ecosystem processes. Yet, the use of these indices has been mainly restricted to anthropogenic stresses. In this study, we propose to expand the use of nematodes' derived ecological indices to link soil and climate properties with soil food webs, and ecosystem processes that all vary along steep elevation gradients. For this purpose, we explored how elevation affects the trophic and functional diversity of nematode communities sampled every 300 m, from about 1,000 m to 3,700 m above sea level, across four transects in the lesser Himalayan range of Jammu and Kashmir. We found that (a) the trophic and functional diversity of nematodes increases with elevation; (b) differences in nematodes communities generate habitat‐specific functional diversity; (c) the maturity index (ΣMI) increases with elevation, while the enrichment index decreases, indicating less mature and less productive ecosystems, enhanced fungal‐based energy flow, and a predominant role of nematodes in generating carbon influxes at high‐elevation sites. We thus confirm that the functional contribution of soil nematodes to belowground ecosystem processes, including carbon and energy flow, is stronger at high elevation. Overall, this study highlights the central importance of nematodes in sustaining soil ecosystems and brings insights into their functional role, particularly in alpine and arctic soils.
Soil nematodes trophic and functional diversity increases with elevation. Therefore, soil nematodes in alpine and arctic soil contribute mostly to ecosystem functioning.
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