Interspecific competition between phytophagous insects can occur when plant responses induced by an early‐season herbivore alter host quality for later colonizers. Recent evidence for specificity in the elicitation of induced plant responses by different attackers suggests that dynamics of host use in the field may be more complex than previously anticipated, because host suitability for colonizing herbivores may depend on which herbivore species has initially damaged a plant. In each of two years, we manipulated the first herbivore to attack Solanum dulcamara plants in an experimental population using several different arthropod species and subsequently monitored colonization by natural herbivores over the course of the growing season. We additionally performed weekly herbivore counts in wild S. dulcamara populations following natural variation in herbivore arrival. Plant‐mediated interactions occurred primarily between two leaf‐feeding beetles, Psylliodes affinis and Plagiometriona clavata. In both manipulative and observational experiments, P. clavata oviposition was reduced on plants initially damaged by P. affinis (or a third leaf‐feeding beetle, Lema trilinea) relative to plants that were initially undamaged. Lowered P. clavata occurrence continued through subsequent life‐history stages, resulting in decreased emergence of second‐generation P. clavata adults on these plants. The occurrence of P. affinis was also lowered on plants damaged by conspecifics in both manipulative and observational experiments. Resistance against P. affinis also followed applications of jasmonic acid, an elicitor of plant defensive responses. Conversely, early‐season damage by P. clavata did not influence plant quality for either later conspecifics or P. affinis. Initial herbivory by the spittlebug Aphrophora saratogensis or generalist taildropper slugs (Prophysaon sp.) likewise had no influence on P. clavata and P. affinis colonization, whereas L. trilinea damage did not affect later arriving P. affinis. Hence, only a subset of early‐season damagers influenced herbivore occurrence on S. dulcamara. Preference tests examining P. affinis feeding and P. clavata oviposition confirmed that specificity in elicitation of induced plant responses produced the divergent herbivore occurrence patterns observed in the field. Overall, the existence of plant‐mediated competitive asymmetry between herbivore species on S. dulcamara highlights the dynamic nature of plant resistance and its potential role in organizing herbivore communities.
Plants in nature are attacked sequentially by herbivores, and theory predicts that herbivore-specific responses allow plants to tailor their defenses. We present a novel field test of this hypothesis, and find that specific responses of Solanum dulcamara lead to season-long consequences for two naturally colonizing herbivores, irrespective of the second herbivore to attack plants. This result indicates that responses induced by the initial herbivore made plants less responsive to subsequent attack. We show that initial herbivory by flea beetles and tortoise beetles induce distinct plant chemical responses. Initial herbivory by flea beetles lowered the occurrence of conspecifics and tortoise beetles relative to controls. Conversely, initial herbivory by tortoise beetles did not influence future herbivory. Remarkably, the experimentally imposed second herbivore to feed on plants did not modify consequences (induced resistance or lack thereof) of the first attacker. Induction of plant chemical responses was consistent with these ecological effects; i.e. the second herbivore did not modify the plant's initial induced response. Thus, canalization of the plant resistance phenotype may constrain defensive responses in a rapidly changing environment.
Plants in nature are attacked sequentially by herbivores, and theory predicts that herbivore-specific responses allow plants to tailor their defenses. We present a novel field test of this hypothesis, and find that specific responses of Solanum dulcamara lead to season-long consequences for two naturally colonizing herbivores, irrespective of the second herbivore to attack plants. This result indicates that responses induced by the initial herbivore made plants less responsive to subsequent attack. We show that initial herbivory by flea beetles and tortoise beetles induce distinct plant chemical responses. Initial herbivory by flea beetles lowered the occurrence of conspecifics and tortoise beetles relative to controls. Conversely, initial herbivory by tortoise beetles did not influence future herbivory. Remarkably, the experimentally imposed second herbivore to feed on plants did not modify consequences (induced resistance or lack thereof) of the first attacker. Induction of plant chemical responses was consistent with these ecological effects; i.e. the second herbivore did not modify the plant's initial induced response. Thus, canalization of the plant resistance phenotype may constrain defensive responses in a rapidly changing environment.
In this study, we used plant vascular architecture as a framework from which to predict induced changes in resource quality for Lema trilinea feeding on the host plant Solanum dulcamara at both low and high levels of herbivory. The systemic patterns of allocation of dye from a capillary tube inserted onto the petiole of the first true leaf and sections of the stem were used to establish the degree of vascular connectivity among different leaf positions. Induced changes in the activity of two defensive proteins, proteinase inhibitor (PI) and polyphenol oxidase (PPO), as well as larval L. trilinea performance, were measured in weakly or strongly connected leaves on plants with the first leaf damaged or undamaged by adult L. trilinea. At high levels of herbivory, larval performance decreased on the sixth leaf, which has strong vascular connections to the first leaf, yet increased on the fifth leaf, which has weak vascular connections to the first leaf. PPO activity increased in both the fifth and sixth leaf, while PI activity decreased in the fifth leaf although remaining unchanged in the sixth leaf. At low levels of herbivory, a decrease in larval performance was observed in the sixth leaf, but no change occurred in the weakly connected fifth leaf. Hence, plant vascular architecture clearly predicted within-plant changes in resource quality following only small amounts of herbivore damage.
1. Herbivory can induce resistance in a plant and the induced phenotype may be disfavoured by subsequent herbivores. Yet, as the distance between plants in a population increases, limited mobility may make a herbivore more likely to feed and oviposit on host plants in its immediate surroundings.2. The present study tested whether a herbivore's preference and distribution across plants with different induced phenotypes was influenced by the spatial distribution of plants. A fragmented population of Solanum dulcamara plants was created. This consisted of discrete, spatially separated patches with different histories of damage, either herbivory from adult flea beetles ( Psylliodes affinis ), tortoise beetles ( Plagiometriona clavata ), or mechanical damage. Each patch was separated by 7 m and consisted of 12 plants that were spaced 30 cm apart. Then a fixed number of adult tortoise beetles were introduced to each patch, and movement and oviposition within and between spatially separate homogeneous patches (receiving one type of damage) were compared with movement and oviposition within heterogeneous patches (containing all three types of damage) over the growing season.3. Flea beetle and tortoise beetle herbivory consistently induced different phytochemical responses in S. dulcamara (polyphenol oxidase and peroxidase), and adult tortoise beetles avoided oviposition on the flea beetle induced plants within heterogeneous patches. However, between homogeneous patches, plant phenotype did not influence oviposition. Colonisation by naturally occurring flea beetle adults followed a similar pattern.4. These results suggest that the heterogeneity of plant phenotypes can influence herbivore choice and distribution at small but not large spatial scales.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
hi@scite.ai
10624 S. Eastern Ave., Ste. A-614
Henderson, NV 89052, USA
Copyright © 2024 scite LLC. All rights reserved.
Made with 💙 for researchers
Part of the Research Solutions Family.