Drought stress affects constitutive but not induced herbivore resistance in apple plants

Plant-herbivore interactions are influenced by chemical plant traits, which can vary depending on the plants' abiotic and biotic environment. Drought events, which are predicted to become more frequent and prolonged due to climate change, may affect primary and secondary plant metabolites contributing to constitutive resistance. Furthermore, the ability of plants to respond to herbivore attack in terms of induced resistance may be altered under drought conditions. We assessed the effects of drought stress on constitutive and induced apple plant resistance to a generalist insect herbivore by quantifying plant and herbivore responses in concert. Plants were exposed to different drought stress intensities (constitutive resistance) and subsequently to herbivore damage treatments that included different damage durations (induced resistance). As drought stress intensified, plant growth and concentrations of the leaf phenolic phloridzin decreased, whereas leaf glucose concentrations increased. Changes in fructose concentrations and in herbivore feeding preferences indicated a non-monotonic shift in constitutive resistance. Moderately stressed plants showed reduced fructose concentrations and were consumed least, while severely stressed plants were fructose-enriched and consumed most compared to well-watered control plants showing intermediate fructose concentrations and palatability. We found no evidence for effects of drought stress on induced resistance, as herbivore feeding preferences for undamaged over damaged plants were independent of drought intensity. Our results suggest a strong role of primary metabolites for drought-dependent variation in constitutive plant resistance and offer novel experimental insights into the effects of drought stress on induced plant resistance across a gradient of water deprivatio

Diversity and composition of arboreal beetle assemblages in tropical pasture afforestations: effects of planting schemes and tree species identity

Timber tree plantations are considered for rehabilitating forest biodiversity in the tropics, but knowledge on determinants of faunal diversity patterns in such human-modified forest landscapes is scarce. We quantified the composition of beetle assemblages on three native timber species (Anacardium excelsum, Cedrela odorata and Tabebuia rosea) planted on former pasture to assess effects of tree species identity, tree species diversity, and insecticide treatment on a speciose group of animals in tropical plantations. The beetle assemblage parameters ‘abundance', ‘species richness', ‘Chao1 estimated species richness' and ‘Shannon diversity' were significantly reduced by insecticide treatment for each tree species. Shannon diversity increased with stand diversification for T. rosea but not for A. excelsum and C. odorata. Species similarity was highest (lowest species turnover) between beetle assemblages on T. rosea, and it was lowest (highest species turnover) for assemblages on insecticide-treated trees of all timber species. Considering trophic guilds, herbivorous beetles dominated on all tree species and in all planting schemes. Herbivores were significantly more dominant on T. rosea and C. odorata than on A. excelsum, suggesting that tree species identity affects beetle guild structure on plantation trees. Insecticide-treated stands harbored less herbivores than untreated stands, but exhibited a high abundance of predator beetle species. Our study revealed that even young pasture-afforestations can host diverse beetle assemblages and thus contribute to biodiversity conservation in the tropics. The magnitude of this contribution, however, may strongly depend on management measures and on the selected tree specie

Do multipurpose companion trees affect high value timber trees in a silvopastoral plantation system?

Establishment of native timber trees on deforested land may contribute to the livelihood of farmers, to improved ecosystem services and to increased greenhouse gas uptake. Here, we present a new silvopastoral planting design to assess species performance and interspecific competition or facilitation effects among native timber and multipurpose trees in Central America. Two timber species, Tabebuia rosea and Cedrela odorata, were established in three low-density planting regimes allowing combined tree and future livestock production: (1) solitary planting, (2) companion planting with Guazuma ulmifolia, and (3) companion planting with the nitrogen-fixing Gliricidia sepium. We quantified survival, growth and reforestation potential of the two timber species subjected to the different planting regimes for the first 2years after establishment. Nitrogen concentration as well as stable nitrogen and carbon isotope composition (δ15N, δ13C) of leaves of the timber saplings were determined. T. rosea showed higher survival and better growth than C. odorata under varying environmental conditions (soil, concomitant vegetation). Performance of the timber saplings was unaffected by either companion species. Planting regimes had no effect on foliar nitrogen concentration and δ15N of the two timber species, although δ15N values indicated nitrogen fixation activity in G. sepium trees. Planting regimes affected foliar δ13C values in T. rosea. δ13C values were significantly higher in solitarily growing individuals, suggesting lower exposition to water stress conditions in saplings surrounded by companion species. As we found positively correlated growth traits among timber and multipurpose trees, a combined planting may benefit farmers by providing additional goods and service

Species-specific responses of herbivores to within-plant and environmentally mediated between-plant variability in plant chemistry

Allocation of resources to growth and defense against herbivores crucially affects plant competitiveness and survival, resulting in a specific distribution of assimilates and defense compounds within plant individuals. Additionally, plants rarely experience stable environmental conditions, and adaptations to abiotic and biotic stresses may involve shifts in resistance to herbivores. We studied the allocation of phytochemicals in Brassica oleracea (Brussels sprouts) due to leaf age, drought stress and herbivore damage and assessed effects on two lepidopteran herbivores differing in diet breadth: the generalist Spodoptera littoralis and the specialist Pieris brassicae. Glucosinolates as secondary defense compounds and total nitrogen and carbon were quantified and linked to plant palatability, i.e., herbivore feeding preference. Herbivore responses were highly species-specific and partially related to changes in phytochemicals. Spodoptera littoralis preferred middle-aged leaves with intermediate levels of glucosinolates and nitrogen over young, glucosinolate and nitrogen rich leaves, as well as over old leaves, poor in glucosinolates and nitrogen. In contrast, P. brassicae preferred young leaves. Both species preferred severely drought-stressed plants to the well-watered control, although analyzed glucosinolate concentrations did not differ. Both S. littoralis and P. brassicae feeding induced an increase of indole glucosinolate levels, which may explain a reduced consumption of damaged plants detected for S. littoralis but not for P. brassicae. By revealing distinct, sometimes contrasting responses of two insect herbivores to within-plant and stress-mediated intraspecific variation in phytochemistry of B. oleracea, this study emphasizes the need to consider specific herbivore responses to understand and predict the interactions between herbivores and variable plant

Within-plant distribution of induced resistance in apple seedlings: rapid acropetal and delayed basipetal responses

Induction of plant resistance by herbivory is a complex process, which follows a temporal dynamic and varies spatially at the within-plant scale. This study aimed at improving the understanding of the induction process in terms of time scale and within-plant allocation, using apple tree seedlings (Malus×domestica) as plant model. Feeding preferences of a leaf-chewing insect (Spodoptera littoralis) for previously damaged and undamaged plants were assessed for six different time intervals with respect to the herbivore damage treatment and for three leaf positions. In addition, main secondary defense compounds were quantified and linked to herbivore feeding preferences. Significant herbivore preference for undamaged plants (induced resistance) was first observed 3days after herbivore damage in the most apical leaf. Responses were delayed in the other leaf positions, and induced resistance decreased within 10days after herbivore damage simultaneously in all tested leaf positions. Chemical analysis revealed higher concentrations of the flavonoid phloridzin in damaged plants as compared to undamaged plants. This indicates that herbivore preference for undamaged apple plants may be linked to phloridzin, which is the main secondary metabolite of apple leaves. The observed time course and distribution of resistance responses within plants contribute to the understanding of induction processes and patterns, and support the optimal defense theory stating young tissue to be prioritized. Moreover, induced resistance responses occurred also basipetally in leaves below the damage site, which suggests that signaling pathways involved in resistance responses are not unidirectiona

Growth, herbivore distribution, and herbivore damage of timber trees in a tropical silvopastoral reforestation system

Context: The reforestation of degraded tropical pastures requires innovative tree planting systems that consider land user needs. Aim: We established a silvopastoral reforestation system and assessed the effects of companion trees on the native timber tree Tabebuia rosea in Panama. Timber tree individuals were established in (1) solitary plantings (TSol) or in companion plantings with (2) Guazuma ulmifolia (TGua) or (3) the nitrogen-fixing Gliricidia sepium (TGli). Methods: We quantified growth characteristics and herbivory of T. rosea, and analyzed leaf chemistry (including the stable isotopes δ15N and δ13C) and structure (leaf mass per area). Results: Companion trees significantly affected stem diameter growth of T. rosea. Stem diameter growth was as high in TGli trees as in TSol trees but was reduced in TGua trees. Furthermore, TGua trees had higher leaf water content, and lower δ13C and lower leaf mass-to-area ratio than TGli trees, suggesting there were effects of shading by G. ulmifolia on T. rosea. Herbivory was high but not affected by planting regimes. Leafing phenology did not differ between planting regimes and G. sepium did not increase nitrogen content in T. rosea leaves. Conclusion: Companion tree planting can support timber tree growth in silvopastoral reforestations, but adequate species selection is crucial for successful implementation of this planting system. Tree-tree interactions seem to be more relevant for timber tree growth than herbivory in the studied syste

Morphological and olfactory tree traits influence the susceptibility and suitability of the apple species Malus domestica and M. sylvestris to the florivorous weevil Anthonomus pomorum (Coleoptera: Curculionidae)

The florivorous apple blossom weevil, Anthonomus pomorum (Coleoptera: Curculionidae), is the most economically relevant insect pest of European apple orchards in early spring. Neither efficient monitoring nor ecologically sustainable management of this insect pest has yet been implemented. To identify heritable traits of apple trees that might influence the host selection of A. pomorum, we compared the susceptibility of apple tree species using infestation rates of the domesticated apple, Malus domestica (Rosaceae: Pyreae), and the European crab apple, M. sylvestris. We evaluated the suitability of the two apple species for A. pomorum by quantifying the mass of weevil offspring. Because volatile organic compounds (VOCs) emitted from flower buds of the domesticated apple have previously been suggested to mediate female weevil preference via olfactory cues, we conducted bioassay experiments with blossom buds of both apple species to explore the olfactory preference of adult weevils and, furthermore, identified the headspace VOCs of blossom buds of both apple species through GC-MS analysis. The infestation analysis showed that A. pomorum infested the native European crab apple more prevalently than the domesticated apple, which originated from Central Asia. The European crab apple also appeared to be better suited for weevil larval development than the domesticated apple, as weevils emerging from M. sylvestris had a higher body mass than those emerging from M. domestica. These field observations were supported by olfactory bioassays, which showed that A. pomorum significantly preferred the odor of M. sylvestris buds compared to the odor of M. domestica buds. The analysis of headspace VOCs indicated differences in the blossom bud volatiles separating several M. domestica individuals from M. sylvestris individuals. This knowledge might be employed in further studies to repel A. pomorum from M. domestica blossom buds

Rust mite resistance in apple assessed by quantitative trait loci analysis

The aim of this study was to assess the genetic basis of rust mite (Aculus schlechtendali) resistance in apple (Malus × domestica). A. schlechtendali infestation of apple trees has increased as a consequence of reduced side effects of modern fungicides on rust mites. An analysis of quantitative trait loci (QTLs) was carried out using linkage map data available for F1 progeny plants of the cultivars ‘Fiesta' × ‘Discovery'. Apple trees representing 160 different genotypes were surveyed for rust mite infestation, each at three different sites in two consecutive years. The distribution of rust mites on the individual apple genotypes was aggregated and significantly affected by apple genotype and site. We identified two QTLs for A. schlechtendali resistance on linkage group 7 of ‘Fiesta'. The AFLP marker E35M42-0146 (20.2cM) and the RAPD marker AE10-400 (45.8cM) were closest positioned to the QTLs and explained between 11.0% and 16.6% of the phenotypic variability. Additionally, putative QTLs on the ‘Discovery' chromosomes 4, 5 and 8 were detected. The SSR marker Hi03a10 identified to be associated to one of the QTLs (AFLP marker E35M42-0146) was traced back in the ‘Fiesta' pedigree to the apple cultivar ‘Wagener'. This marker may facilitate the breeding of resistant apple cultivars by marker assisted selection. Furthermore, the genetic background of rust mite resistance in existing cultivars can be evaluated by testing them for the identified SSR marke

Associational resistance and associational susceptibility: specialist herbivores show contrasting responses to tree stand diversification

Heterospecific neighbors may reduce damage to a focal plant by lowering specialist herbivore loads (associational resistance hypothesis), or enhance damage by increasing generalist herbivore loads (associational susceptibility hypothesis). We tested the associational effects of tree diversity on herbivory patterns of the tropical focal tree Tabebuia rosea in an experimental plantation setup, which contained tree monocultures and mixed stands. We found higher herbivore damage to T. rosea at higher tree diversity, indicating that T. rosea did not benefit from associational resistance but rather experienced associational susceptibility. The specific consideration of the two dominant insect herbivore species of T. rosea, the specialist chrysomelid Walterianella inscripta and the specialist pyralid Eulepte gastralis, facilitated understanding of the detected damage patterns. Tree diversity exerted opposite effects on tree infestation by the two herbivores. These findings point to resource concentration effects for the chrysomelid beetle (favored by tree monoculture) and to resource dilution effects for the pyralid caterpillar (favored by tree mixture) as underlying mechanisms of herbivore distribution. A strong contribution of the pyralid to overall damage patterns in diversified stands suggests that associational susceptibility may not necessarily be related to higher abundances of generalist herbivores but may also result from specialized herbivores affected by resource dilution effects. Thus, the identity and biology of herbivore species has to be taken into account when attempting to predict damage patterns in forest ecosystem

QTL analysis for aphid resistance and growth traits in apple

The rosy apple aphid (Dysaphis plantaginea), the leaf-curling aphid (Dysaphis cf. devecta) and the green apple aphid (Aphis pomi) are widespread pest insects that reduce growth of leaves, fruits and shoots in apple (Malus × domestica). Aphid control in apple orchards is generally achieved by insecticides, but alternative management options like growing resistant cultivars are needed for a more sustainable integrated pest management (IPM). A linkage map available for a segregating F1-cross of the apple cultivars ‘Fiesta' and ‘Discovery' was used to investigate the genetic basis of resistance to aphids. Aphid infestation and plant growth characteristics were repeatedly assessed for the same 160 apple genotypes in three different environments and 2 consecutive years. We identified amplified fragment length polymorphism (AFLP) markers linked to quantitative trait loci (QTLs) for resistance to D. plantaginea (‘Fiesta' linkage group 17, locus 57.7, marker E33M35-0269; heritability: 28.3%), and to D. cf. devecta (‘Fiesta' linkage group 7, locus 4.5, marker E32M39-0195; heritability: 50.2%). Interactions between aphid species, differences in climatic conditions and the spatial distribution of aphid infestation were identified as possible factors impeding the detection of QTLs. A pedigree analysis of simple sequence repeat (SSR) marker alleles closely associated with the QTL markers revealed the presence of the alleles in other apple cultivars with reported aphid resistance (‘Wagener', ‘Cox's Orange Pippin'), highlighting the genetic basis and also the potential for gene pyramiding of aphid resistance in apple. Finally, significant QTLs for shoot length and stem diameter were identified, while there was no relationship between aphid resistance and plant trait QTL