Herbivore-induced plant volatiles mediate behavioral interactions between a leaf-chewing and a phloem-feeding herbivore

Plants respond adaptively to herbivore stress in order to maintain fitness. Upon herbivore attack, plants emit blends of volatile organic compounds (VOCs) that differ from those that are constitutively emitted. These defense responses are typically specific to the identity of the attacking herbivore and often linked to the herbivore's feeding guild (e.g. chewing, phloem-feeding). Herbivores use plant volatiles to locate suitable host plants and changes in volatile emissions can affect host-plant location. Therefore, herbivores from separate feeding guilds can interact indirectly through the modulation of plant responses. In this study we tested how damage by an herbivore from one feeding guild affected the host-plant choice of an herbivore from a separate feeding guild, and vice versa. A chewing herbivore, the Colorado potato beetle (Leptinotarsa decemlineata), and a phloem feeding herbivore, the green peach aphid (Myzus persicae), were assayed in olfactometers to assess behavioral responses to odors emitted by potato plants (Solanum tuberosum) that were damaged by herbivores from the other feeding guild. Leptinotarsa decemlineata oriented more frequently towards undamaged plants compared to M. persicae damaged plants. Surprisingly, M. persicae preferred plants that were damaged by L. decemlineata, although previous studies had shown that they perform worse on these plants. Distinct differences were detected in the volatile profiles of herbivore-damaged and undamaged plants. Leptinotarsa decemlineata induced stronger volatile emissions compared to undamaged control plants, while M. persicae tended to suppress volatile emissions. These herbivores demonstrate contrasting induction of plant volatiles and behavioral responses. Exploring the nature of co-occurring herbivores and how they perceive potential hosts can play a significant role in understanding the ecological functions and community dynamics of plant plasticity and interactions with a variety of herbivores.     

Herbivore‐induced plant responses in Brassica oleracea prevail over effects of constitutive resistance and result in enhanced herbivore attack

1. Plant responses to herbivore attack may have community‐wide effects on the composition of the plant‐associated insect community. Thereby, plant responses to an early‐season herbivore may have profound consequences for the amount and type of future attack. 2. Here we studied the effect of early‐season herbivory by caterpillars of Pieris rapae on the composition of the insect herbivore community on domesticated Brassica oleracea plants. We compared the effect of herbivory on two cultivars that differ in the degree of susceptibility to herbivores to analyse whether induced plant responses supersede differences caused by constitutive resistance. 3. Early‐season herbivory affected the herbivore community, having contrasting effects on different herbivore species, while these effects were similar on the two cultivars. Generalist insect herbivores avoided plants that had been induced, whereas these plants were colonised preferentially by specialist herbivores belonging to both leaf‐chewing and sap‐sucking guilds. 4. Our results show that community‐wide effects of early‐season herbivory may prevail over effects of constitutive plant resistance. Induced responses triggered by prior herbivory may lead to an increase in susceptibility to the dominant specialists in the herbivorous insect community. The outcome of the balance between contrasting responses of herbivorous community members to induced plants therefore determines whether induced plant responses result in enhanced plant resistance.     

Order of herbivore arrival on wild cabbage populations influences subsequent arthropod community development

In plant–arthropod associations, the first herbivores to colonise a plant may directly or indirectly affect community assembly on that particular plant. Whether the order of arrival of different arthropod species further modulates community assembly and affects plant fitness remains unclear. Using wild Brassica oleracea plants in the field, we manipulated the order of arrival of early‐season herbivores that belong to different feeding guilds, namely the aphid Brevicoryne brassicae and caterpillars of Plutella xylostella. We investigated the effect of herbivore identity and order of arrival on community assembly on two B. oleracea plant populations during two growth seasons. For this perennial plant, we evaluated whether foliar herbivory also affected herbivore communities on the flowers and if these interactions affected plant seed production. Aphid infestation caused an increase in parasitoid abundance, but caterpillars modulated these effects, depending on the order of herbivore infestation and plant population. In the second growth season, when plants flowered, the order of infestation of leaves with aphids and caterpillars more strongly affected abundance of herbivores feeding on the flowers than those feeding on leaves. Infestation with caterpillars followed by aphids caused an increase in flower‐feeding herbivores compared to the reversed order of infestation in one plant population, whereas the opposite effects were observed for the other plant population. The impact on plant seed set in the first reproductive year was limited. Our work shows that the identity and arrival order of early season herbivores may have long‐term consequences for community composition on individual plants and that these patterns may vary among plant populations. We discuss how these community processes may affect plant fitness and speculate on the implications for evolution of plant defences.     

Field evidence for indirect interactions between foliar‐feeding insect and root‐feeding nematode communities on Nicotiana tabacum

Abstract 1. As herbivory often elicits systemic changes in plant traits, indirect interactions via induced plant responses may be a pervasive feature structuring herbivore communities. Although the importance of this phenomenon has been emphasised for herbivorous insects, it is unknown if and how induced responses contribute to the organisation of other major phytoparasitic taxa. 2. Survey and experimental field studies were used to investigate the role of plants in linking the dynamics of foliar‐feeding insects and root‐feeding nematodes on tobacco, Nicotiana tabacum. 3. Plant‐mediated interactions between insects and nematodes could largely be differentiated by insect feeding guild, with positive insect–nematode interactions predominating with leaf‐chewing insects (caterpillars) and negative interactions occurring with sap‐feeding insects (aphids). For example, insect defoliation was positively correlated with the abundance of root‐feeding nematodes, but aphids and nematodes were negatively correlated. Experimental field manipulations of foliar insect and nematode root herbivory also tended to support this outcome. 4. Overall, these results suggest that plants indirectly link the dynamics of divergent consumer taxa in spatially distinct ecosystems. This lends support to the growing perception that plants play a critical role in propagating indirect effects among a diverse assemblage of consumers.     

Plant genotype and induced responses affect resistance to herbivores on evening primrose (Oenothera biennis)

Abstract. 1. Although both genotype and induced responses affect a plant's resistance to herbivores, little is known about their relative and interactive effects. This study examined how plant genotype of a native plant (Oenothera biennis) and induced plant responses to herbivory affect resistance to, and interactions among, several herbivores. 2. In a field experiment, genetic and environmental variation among habitats led to variation in the amount of early season damage and plant quality. The pattern of variation in early season infestation by spittlebugs (Philaenus spumarius, a piercing–sucking herbivore) negatively correlated with oviposition preference by a later feeding specialist weevil (Tyloderma foveolatum, a leaf‐chewer). 3. To determine if plant genotype and induced responses to herbivory might be responsible for these field patterns, we performed no‐choice and choice bioassays using four genotypes of O. biennis that varied in resistance. Plants were induced by either spittlebugs or weevils and assays measured the responses of the same specialist weevil as well as a generalist caterpillar (Spodoptera exigua). 4. Resistance to adult weevils was largely unaffected by plant genotype, while they experienced induced resistance following damage by conspecific weevils in no‐choice assays. Caterpillars were more strongly affected by plant genotype than induced responses in both no‐choice and choice assays, but they also fed less and experienced higher mortality on plants previously damaged by weevils. In contrast to the pattern suggested by the field experiment, spittlebugs did consistently induce resistance against either weevils or caterpillars in the bioassay experiment. 5. These results support recent findings that show herbivore species can compete via induced plant responses. Additionally, a quantitative review of the literature demonstrates that plant genotype tends to be more important than interspecific competition among herbivores (plant‐mediated or otherwise) in affecting herbivore preference and performance.     

Jasmonate-mediated induced plant resistance affects a community of herbivores

1. The negative effect of induced plant resistance on the preference and performance of herbivores is a well‐documented ecological phenomenon that is thought to be important for both plants and herbivores. This study links the well‐developed mechanistic understanding of the biochemistry of induced plant resistance in the tomato system with an examination of how these mechanisms affect the community of herbivores in the field. 2. Several proteins that are induced in tomato foliage following herbivore damage have been linked causally to reductions in herbivore performance under laboratory conditions. Application of jasmonic acid, a natural elicitor of these defensive proteins, to tomato foliage stimulates induced responses to herbivory. 3. Jasmonic acid was sprayed on plants in three doses to generate plants with varying levels of induced responses, which were measured as increases in the activities of proteinase inhibitors and polyphenol oxidase. 4. Field experiments conducted over 3 years indicated that induction of these defensive proteins is associated with decreases in the abundance of all four naturally abundant herbivores, including insects in three feeding guilds, caterpillars, flea beetles, aphids, and thrips. Induced resistance killed early instars of noctuid caterpillars. Adult flea beetles strongly preferred control plants over induced plants, and this effect on host plant preference probably contributed to differences in the natural abundance of flea beetles. 5. The general nature of the effects observed in this study suggests that induced resistance will suppress many members of the herbivore community. By linking plant biochemistry, insect preference, performance, and abundance, tools can be developed to manipulate plant resistance sensibly and to predict its outcome under field conditions.     

Plant‐mediated interactions between two herbivores differentially affect a subsequently arriving third herbivore in populations of wild cabbage

• Plants are part of biodiverse communities and frequently suffer from attack by multiple herbivorous insects. Plant responses to these herbivores are specific for insect feeding guilds: aphids and caterpillars induce different plant phenotypes. Moreover, plants respond differentially to single or dual herbivory, which may cascade into a chain of interactions in terms of resistance to other community members. Whether differential responses to single or dual herbivory have consequences for plant resistance to yet a third herbivore is unknown.
• We assessed the effects of single or dual herbivory by Brevicoryne brassicae aphids and/or Plutella xylostella caterpillars on resistance of plants from three natural populations of wild cabbage to feeding by caterpillars of Mamestra brassicae. We measured plant gene expression and phytohormone concentrations to illustrate mechanisms involved in induced responses.
• Performance of both B. brassicae and P. xylostella was reduced when feeding simultaneously with the other herbivore, compared to feeding alone. Gene expression and phytohormone concentrations in plants exposed to dual herbivory were different from those found in plants exposed to herbivory by either insect alone. Plants previously induced by both P. xylostella and B. brassicae negatively affected growth of the subsequently arriving M. brassicae. Furthermore, induced responses varied between wild cabbage populations.
• Feeding by multiple herbivores differentially activates plant defences, which has plant‐mediated negative consequences for a subsequently arriving herbivore. Plant population‐specific responses suggest that plant populations adapt to the specific communities of insect herbivores. Our study contributes to the understanding of plant defence plasticity in response to multiple insect attacks.

     

Response of Brassica oleracea to temporal variation in attack by two herbivores affects preference and performance of a third herbivore

1. Plants are frequently under attack by multiple insect herbivores, which may interact indirectly through herbivore‐induced changes in the plant's phenotype. The identity, order, and timing of herbivore arrivals may influence the outcome of interactions between two herbivores. How these aspects affect, in turn, subsequently arriving herbivores that feed on double herbivore‐induced plants has not been widely investigated. 2. This study tested whether the order and timing of arrival of two inducing herbivores from different feeding guilds affected the preference and performance of a subsequently arriving third herbivore, caterpillars of Mamestra brassicae L. (Lepidoptera: Noctuidae). Aphids [Brevicoryne brassicae L. (Hemiptera: Aphididae)] and caterpillars [Plutella xylostella L. (Lepidoptera: Yponomeutidae)] were introduced onto wild Brassica oleracea L. (Brassicaceae) plants in different sequences and with different arrival times. The effects of these plant treatments on M. brassicae caterpillars were assessed in pairwise preference tests and no‐choice performance tests. 3. The caterpillars of M. brassicae preferred to feed from undamaged plants rather than double herbivore‐induced plants. Compared with undamaged plants, they preferred plant material on which aphids had arrived first followed by caterpillars, whereas they avoided plant material with the reverse order of herbivore arrival. Performance of the caterpillars increased with increasing arrival time between herbivore infestations in double herbivore‐induced plants. Although M. brassicae grew faster on plants induced by aphids than on those induced by caterpillars alone, its performance was not affected by the order of previous herbivore arrival. 4. These results imply that the timing of colonisation by multiple herbivores determines the outcome of plant‐mediated herbivore–herbivore interactions.     

Echinacea angustifolia and its specialist ant‐tended aphid: a multi‐year study of manipulated and naturally‐occurring aphid infestation

1. The impact of herbivores on plant fitness depends on multiple ecological mechanisms, including interactions between herbivore guilds. 2. This study assessed the effects of a specialist aphid (Aphis echinaceae) on performance and foliar herbivore damage of a long‐lived perennial plant (Echinacea angustifolia) native to the North American tallgrass prairie. A 2‐year field experiment manipulating aphid infestation on 100 plants was compared with concurrent and past observations of unmanipulated plants in the same outdoor experimental plot. Because ants co‐occur with aphids, the experiment tested the combined effects of aphids and ants. 3. Neither manipulated nor naturally‐occurring aphid infestations led to measurable declines in plant performance. Results for foliar herbivore damage differed between experimental and observational studies: the occurrence of foliar herbivore damage decreased with aphid infestation in the first year of the experiment and increased with aphid infestation over 5 years in unmanipulated plants. 4. While the experimental results concur with other experiments of ant–hemipteran–herbivore relationships, the observational results suggest that ant–aphid interactions do not naturally play a major role in determining patterns of foliar herbivory in this system. This result demonstrates the value of using field observations to interpret the relevance of experimental results.     

Additive and non‐additive effects of birch genotypic diversity on arthropod herbivory in a long‐term field experiment

Herbivores are important drivers of plant population dynamics and community composition in natural and managed systems. Intraspecific genetic diversity of long‐lived plants like trees might shape patterns of herbivory by different guilds of herbivores that trees experience through time. However, previous studies on plant genetic diversity effects on herbivores have been largely short‐term. We investigated how tree genotypic variation and diversity influence herbivory of silver birch Betula pendula in a long‐term field experiment. Using clones of eight genotypes, we constructed experimental plots consisting of one, two, four or eight genotypes, and measured damage by five guilds of arthropod herbivores twice a year over three different years (four, six and nine years after the experiment was established). Genotypes varied significantly for most types of herbivore damage, but genotype resistance rankings often shifted over time, and none of the clones was more resistant than all others to all types of herbivores. At the plot level, birch genotypic diversity had significant positive additive effect on leaf rollers and negative non‐additive effects on chewing herbivores and gall makers. In contrast, leaf‐mining and leaf‐tying damage was not influenced by birch genotypic diversity. Within diverse plots, the direction of genotypic diversity effects varied depending on birch genotype, some having lower and some having higher herbivory in mixed stands. This research highlights the importance of long‐term studies including different feeding guilds of herbivores to understand the effects of plant genetic diversity on arthropod communities. Different responses of various feeding guilds to genotypic diversity and shifts in resistance of individual genotypes over time indicate that genotypic mixtures are unlikely to result in overall reduction in herbivory over time.     

The effect of rhizosphere microbes outweighs host plant genetics in reducing insect herbivory

Rhizosphere microbes affect plant performance, including plant resistance against insect herbivores; yet, a direct comparison of the relative influence of rhizosphere microbes versus plant genetics on herbivory levels and on metabolites related to defence is lacking. In the crucifer Boechera stricta, we tested the effects of rhizosphere microbes and plant population on herbivore resistance, the primary metabolome, and select secondary metabolites. Plant populations differed significantly in the concentrations of six glucosinolates (GLS), secondary metabolites known to provide herbivore resistance in the Brassicaceae. The population with lower GLS levels experienced ~60% higher levels of aphid (Myzus persicae) attack; no association was observed between GLS and damage by a second herbivore, flea beetles (Phyllotreta cruciferae). Rhizosphere microbiome (disrupted vs. intact native microbiome) had no effect on plant GLS concentrations. However, aphid number and flea beetle damage were respectively about three‐ and seven‐fold higher among plants grown in the disrupted versus intact native microbiome treatment. These differences may be attributable to shifts in primary metabolic pathways previously implicated in host defence against herbivores, including increases in pentose and glucoronate interconversion among plants grown with an intact microbiome. Furthermore, native microbiomes with distinct community composition (as estimated from 16s rRNA amplicon sequencing) differed two‐fold in their effect on host plant susceptibility to aphids. The findings suggest that rhizosphere microbes, including distinct native microbiomes, can play a greater role than population in defence against insect herbivores, and act through metabolic mechanisms independent of population.     

Community structure and abundance of insects in response to early‐season aphid infestation in wild cabbage populations

1. Changes in the arthropod community structure can be attributed to differences in constitutively expressed plant traits or those that change depending on environmental conditions such as herbivory. Early‐season herbivory may have community‐wide effects on successive insect colonisation of host plants and the identity of the initially inducing insect may determine the direction and strength of the effects on the dynamics and composition of the associated insect community. 2. Previous studies have addressed the effect of early infestation with a chewing herbivore. In the present study, the effect of early infestation was investigated with a phloem‐feeding aphid [Brevicoryne brassicae L. (Hemiptera, Aphididae)] on the insect community associated with three wild cabbage (Brassica oleracea L.) populations, which are known to differ in defence chemistry, throughout the season in field experiments. 3. Aphid infestation had asymmetric effects on the associated insect community and only influenced the abundance of the natural enemies of aphids, but not that of chewing herbivores and their natural enemies. The effect size of aphid infestation further depended on the cabbage population. 4. Aphid feeding has been previously reported to promote host‐plant quality for chewing herbivores, which has been attributed to antagonism between the two major defence signalling pathways controlled by the hormones salicylic acid (SA) and jasmonic acid (JA), respectively. Our results show no effects of early infestation by aphids on chewing herbivores, suggesting the absence of long‐term JA–SA antagonism. 5. Investigating the effects of the identity of an early‐season coloniser and genotypic variation among plant populations on insect community dynamics are important in understanding insect–plant community ecology.     

Plant chemistry underlies herbivore‐mediated inbreeding depression in nature

The cost of inbreeding (inbreeding depression, ID) is an important variable in the maintenance of reproductive variation. Ecological interactions such as herbivory could modulate this cost, provided that defence traits harbour deleterious mutations and herbivores are responsible for differences in fitness. In the field, we manipulated the presence of herbivores on experimentally inbred and outcrossed plants of Solanum carolinense (horsenettle) for three years. Damage was greater on inbred plants, and ID for growth and fitness was significantly greater under herbivory. Inbreeding reduced phenolic expression both qualitatively (phytochemical diversity) and quantitatively, indicating deleterious load at loci related to the biosynthesis of defence compounds. Our results indicate that inbreeding effects on plant–herbivore interactions are mediated by changes to functional plant metabolites, suggesting that variation in inbreeding could be a predictor of defence trait variation. The magnitude of herbivore‐mediated, ecological ID indicates that herbivores could maintain outcrossing mating systems in nature.     

Global patterns of arthropod herbivory on an invasive plant,the physic nut (Jatropha curcas L.)

The physic nut (Jatropha curcas L.) is a multipurpose and oil‐producing shrub of Central and South American origin. Since the 15th century, this shrub has existed across tropical regions. Despite its presumed resistance to herbivores, reports show that arthropod herbivores infest it. However, no comprehensive account of arthropod herbivores, which consume the physic nut, exists. Here, we conducted a literature review that provides a comprehensive account of arthropod herbivores of the physic nut. Based on the co‐evolutionary hypothesis, we expected to find a higher herbivore of species richness and a larger proportion of native herbivores within the native range than elsewhere. As physic nut is a well‐defended plant chemically, we expected to find evidence for highest herbivory levels in plant parts that are the least defended. By the literatures review, we compiled 78 arthropod herbivores representing nine orders and from 31 families that feed on physic nut across the globe. As expected, the highest numbers of herbivores (34 species) were documented within the native range of the J. curcas and the lowest species number (21 species) in Africa. Of the 34 species in Central and South America, 94% were of native origin. Nine species were found feeding on J. curcas on more than one continent. Origins of 49% of species were from the native range of J. curcas. The highest percentage (54%) of species belonged to Hemiptera. With regard to feeding guilds, 59% of the herbivores belonged to sucking and 41% to chewing species. Forty‐one per cent of species were flower or fruit feeders, and 36% foliage feeders. We conclude that J. curcas is, despite its toxicity, vulnerable to herbivory, mainly to foliage, flower and fruit feeders.     

How do herbivorous insects respond to drought stress in trees?

Increased frequency and severity of drought, as a result of climate change, is expected to drive critical changes in plant–insect interactions that may elevate rates of tree mortality. The mechanisms that link water stress in plants to insect performance are not well understood. Here, we build on previous reviews and develop a framework that incorporates the severity and longevity of drought and captures the plant physiological adjustments that follow moderate and severe drought. Using this framework, we investigate in greater depth how insect performance responds to increasing drought severity for: (i) different feeding guilds; (ii) flush feeders and senescence feeders; (iii) specialist and generalist insect herbivores; and (iv) temperate versus tropical forest communities. We outline how intermittent and moderate drought can result in increases of carbon‐based and nitrogen‐based chemical defences, whereas long and severe drought events can result in decreases in plant secondary defence compounds. We predict that different herbivore feeding guilds will show different but predictable responses to drought events, with most feeding guilds being negatively affected by water stress, with the exception of wood borers and bark beetles during severe drought and sap‐sucking insects and leaf miners during moderate and intermittent drought. Time of feeding and host specificity are important considerations. Some insects, regardless of feeding guild, prefer to feed on younger tissues from leaf flush, whereas others are adapted to feed on senescing tissues of severely stressed trees. We argue that moderate water stress could benefit specialist insect herbivores, while generalists might prefer severe drought conditions. Current evidence suggests that insect outbreaks are shorter and more spatially restricted in tropical than in temperate forests. We suggest that future research on the impact of drought on insect communities should include (i) assessing how drought‐induced changes in various plant traits, such as secondary compound concentrations and leaf water potential, affect herbivores; (ii) food web implications for other insects and those that feed on them; and (iii) interactions between the effects on insects of increasing drought and other forms of environmental change including rising temperatures and CO₂ levels. There is a need for larger, temperate and tropical forest‐scale drought experiments to look at herbivorous insect responses and their role in tree death.     

Ant attendance of the cotton aphid is beneficial for okra plants: deciphering multitrophic interactions

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Induced plant responses to multiple damagers: differential effects on an herbivore and its parasitoid

Herbivore-induced plants responses can affect the preference and performance of herbivores and their natural enemies. These responses may vary depending on the identity and number of herbivore species feeding on the plant so that when herbivores from different guilds feed on plants, the interactions between plants, herbivores, and natural enemies may be disrupted. Tomato plants were damaged either by the caterpillar Spodoptera exigua, or the aphid Macrosiphum euphorbiae, or damaged by both herbivores, or undamaged controls. We measured the preference and performance of S. exigua and its parasitoid Cotesia marginiventris, and activity of proteinase inhibitors (PI) as an indicator of induced resistance. Compared to undamaged plants, caterpillar damage reduced the number of eggs laid by S. exigua adults, reduced growth, consumption, and survival of larval S. exigua and C. marginiventris, and increased activity of PIs 43%; but did not increase attraction of C. marginiventris. While pupal mass of S. exigua was not affected, the pupal mass of C. marginiventris decreased on caterpillar-damaged plants compared to controls. In contrast, plants damaged by aphids were preferred for oviposition by S. exigua, and had increased larval consumption and survival, compared to controls. Aphid feeding did not affect the preference or performance of C. marginiventris, or PI activity, compared to controls. While oviposition was deterred on caterpillar-damaged plants, plants damaged by both herbivores received the same amount of oviposition as controls. The attraction of C. marginiventris to plants damaged by caterpillars and aphids was increased compared to controls. However, plants damaged by both herbivores had similar PI activity, larval growth and survival of S. exigua and C. marginiventris, as plants singly damaged by caterpillars. Overall, the preference component for both the herbivore and parasitoid was more strongly affected by damage due to multiple herbivores than the performance component.     

Colonization of Tanacetum vulgare by aphids is reduced by earthworms

Soil organisms affect plant growth and chemistry and have subsequent effects on aboveground herbivore performance. However, whether herbivores discriminate between plants exposed to different soil organisms when colonizing their host plants is largely unexplored. In a greenhouse study, Tanacetum vulgare L. (Asteraceae) growing in a ruderal plant community in the presence and absence of arbuscular mycorrhizal fungi (AMF) and earthworms [Aporrectodea spp. (Haplotaxida: Lumbricidae)] was colonized by aphids [Myzus persicae Sulzer (Hemiptera: Aphididae)]. The aphids preferred to colonize plants without earthworms in the soil, and the numbers of aphids remained lower on the plants with earthworms, irrespective of the presence of AMF. Although the N, C, and P concentrations of the shoots were not affected by the soil organisms, AMF increased total aboveground biomass, total N, C, and P content, and photosynthetic activity (measured as electron transport rate) in the leaves under high light intensity. These results suggest that earthworms affect chemical cues that are used by aphids to judge host quality prior to feeding. Discrimination between plants with and without exposure to earthworms by aboveground herbivores is a novel aspect of plant‐mediated interactions between below‐ and aboveground organisms.     

Stress magnitude matters: different intensities of pulsed water stress produce non‐monotonic resistance responses of host plants to insect herbivores

Abstract 1. Water stress may increase or reduce the suitability of plants for herbivores. The recently proposed ‘pulsed stress hypothesis’ suggests consideration of stress phenology (pulsed vs. continuous stress) to explain these conflicting effects of plant water stress on herbivore performance. 2. This hypothesis was tested for the effect of differing stress intensity on performance and preference of insect herbivores belonging to different feeding guilds, namely leaf‐chewing insects (Spodoptera littoralis caterpillars) and phloem‐feeding insects (Aphis pomi aphids), on apple plants (Malus domestica). The plants were non‐stressed or exposed to a low or high intensity of pulsed water stress. 3. Plant responses to the different stress levels were generally monotonic. Growth, stomatal conductance (g_s), leaf water, and old‐leaf nitrogen concentration decreased, whereas young‐leaf nitrogen concentration and leaf mass per area (LMA) increased with increasing stress intensity. The stable isotope composition of foliar carbon (δ¹³C) responded non‐monotonically to the drought treatments. The δ¹³C values were highest in low‐stress plants, intermediate in high‐stress plants, and lowest in non‐stressed plants. 4. The preference and performance responses of the caterpillars were also non‐monotonic. Non‐stressed plants were intermediately, low‐stress plants least, and high‐stress plants most attractive or suitable. Aphid population growth was highest on non‐stressed plants and lowest on low‐stress plants. 5. The results highlight the importance of water stress intensity for the outcome of interactions between herbivores and drought‐affected plants. They show that pulsed water stress may enhance or reduce insect herbivore performance and plant resistance, depending on stress intensity.