An official website of the United States government
Virtually all plants employ direct and indirect defenses against herbivores. While it is known that plant defenses can be affected by belowground symbiotic microbes under controlled conditions, studies showing these multitrophic interactions in nature are surprisingly scarce. Here we tested for effects of rhizobia on insect attraction and direct defense (cyanogenesis) in wild lima bean (Phaseolus lunatus) plants in Costa Rica. We performed bioassays with rhizobia-inoculated (R+) and rhizobiafree (R-) potted plants distributed among native lima bean communities at two spatially separated field sites (450 km apart) and in two field seasons. Without affecting overall plant size, rhizobia altered leaf chemistry (cyanogenesis and soluble leaf nitrogen) and ultimately insect communities visiting the plants. Natural herbivorous chrysomelid beetles were strongly attracted to R+ plants, while natural enemies, ants and parasitoid wasps, preferred R- plants resulting in a particularly high herbivore:carnivore ratio on R + plants. This suggests that symbiotic microbes mediate trophic interactions by influencing both direct and indirect plant defenses against herbivores. Our results show that rhizobia affect the plant defensive phenotype and have cascading effects on plant-insect interactions in nature.
more »
« less
Dispensing a Synthetic Green Leaf Volatile to Two Plant Species in a Common Garden Differentially Alters Physiological Responses and Herbivory
Herbivore-induced plant volatile (HIPV)-mediated eavesdropping by plants is a well-documented, inducible phenomenon that has practical agronomic applications for enhancing plant defense and pest management. However, as with any inducible phenomenon, responding to volatile cues may incur physiological and ecological costs that limit plant productivity. In a common garden experiment, we tested the hypothesis that exposure to a single HIPV would decrease herbivore damage at the cost of reduced plant growth and reproduction. Lima bean (Phaseolus lunatus) and pepper (Capsicum annuum) plants were exposed to a persistent, low dose (~10 ng/h) of the green leaf volatile cis-3-hexenyl acetate (z3HAC), which is a HIPV and damage-associated volatile. z3HAC-treated pepper plants were shorter, had less aboveground and belowground biomass, and produced fewer flowers and fruits relative to controls, while z3HAC-treated lima bean plants were taller and produced more leaves and flowers than did controls. Natural herbivory was reduced in z3HAC-exposed lima bean plants, but not in pepper. Cyanogenic potential, a putative direct defense mechanism in lima bean, was lower in young z3HAC-exposed leaves, suggesting a growth–defense tradeoff from z3HAC exposure alone. Plant species-specific responses to an identical volatile cue have important implications for agronomic costs and benefits of volatile-mediated interplant communication under field conditions.
more »
« less
- PAR ID:
- 10227764
- Date Published:
- Journal Name:
- Agronomy
- Volume:
- 11
- Issue:
- 5
- ISSN:
- 2073-4395
- Page Range / eLocation ID:
- 958
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
null (Ed.)1. Plants face many environmental stresses that can impact their survival, development and fitness. Insects are the most diverse, abundant and threatening herbivores in nature. As a consequence, plants produce direct chemical and physical defences to reduce herbivory. They also release volatiles to recruit natural enemies that indirectly protect them from herbivory. The recruitment of parasitic wasps can benefit plant fitness because they ultimately kill their insect hosts. 2. Recently, studies showed that parasitoids can indirectly mediate plant defences by modulating herbivore oral secretions. In addition to the direct benefits of parasitoids in terms of reducing herbivore survival, we tested if the reduction in induced defences by parasitized caterpillars compared to non-parasitized caterpillars may reduce the costs associated with defence expression. 3. We provide evidence that tomato plants treated with saliva from parasitized caterpillars have significantly higher fitness parameters including increased flower numbers (16.3%) and heavier fruit weight (13.5%), compared to plants treated with saliva from non-parasitized caterpillars. Since plants were grown without actual herbivores, the higher values for these fitness parameters were due to lower costs of induced defences and not due to reduced herbivory by parasitized caterpillars. Furthermore, the resulting seed germination time was shorter and the germination rate was higher when the maternal plants were previously exposed to parasitized herbivore treatment compared to control (non-treated) plants. 4. Overall, application of saliva did not result in transgenerational priming of offspring defence responses. However, offspring of parents exposed to caterpillar saliva had lower constitutive levels and higher induced levels of trypsin inhibitor than offspring from unexposed parents. 5. This study shows that the saliva of parasitized caterpillars can modulate plant defences and further demonstrates that the lower induction of plant defences is associated with elevated plant fitness in the absence of herbivore feeding, suggesting that induced plant defences are costly.more » « less
-
Abstract Over the last decade, a large effort has been made to understand how extreme climate events disrupt species interactions. Yet, it is unclear how these events affect plants and herbivores directly, via metabolic changes, and indirectly, via their subsequent altered interaction. We exposed common milkweed (Asclepias syriaca) and monarch caterpillars (Danaus plexippus) to control (26:14°C, day:night) or heat wave (HW) conditions (36:24°C, day:night) for 4 days and then moved each organism to a new control or HW partner to disentangle the direct and indirect effects of heat exposure on each organism. We found that the HW directly benefited plants in terms of growth and defence expression (increased latex exudation and total cardenolides) and insect her'bivores through faster larval development. Conversely, indirect HW effects caused both plant latex and total cardenolides to decrease after subsequent herbivory. Nonetheless, increasing trends of more toxic cardenolides and lower leaf nutritional quality after herbivory by HW caterpillars likely led to reduced plant damage compared to controls. Our findings reveal that indirect impacts of HWs may play a greater role in shaping plant‐herbivore interactions via changes in key physiological traits, providing valuable understanding of how ecological interactions may proceed in a changing world.more » « less
-
Understanding the distribution of herbivore damage among leaves and individual plants is a central goal of plant–herbivore biology. Commonly observed unequal patterns of herbivore damage have conventionally been attributed to the heterogeneity in plant quality or herbivore behaviour or distribution. Meanwhile, the potential role of stochastic processes in structuring plant–herbivore interactions has been overlooked. Here, we show that based on simple first principle expectations from metabolic theory, random sampling of different sizes of herbivores from a regional pool is sufficient to explain patterns of variation in herbivore damage. This is despite making the neutral assumption that herbivory is caused by randomly feeding herbivores on identical and passive plants. We then compared its predictions against 765 datasets of herbivory on 496 species across 116° of latitude from the Herbivory Variability Network. Using only one free parameter, the estimated attack rate, our neutral model approximates the observed frequency distribution of herbivore damage among plants and especially among leaves very well. Our results suggest that neutral stochastic processes play a large and underappreciated role in natural variation in herbivory and may explain the low predictability of herbivory patterns. We argue that such prominence warrants its consideration as a powerful force in plant–herbivore interactions.more » « less
-
Abstract A central goal in ecology is to understand the mechanisms by which biological diversity is maintained. The diversity of plant chemical defences and the strategies by which they are deployed in nature may influence biological diversity. Trees in neotropical forests are subject to relatively high herbivore pressure. Such consistent pressure is thought to select for constitutive, non‐flexible defence‐related phytochemistry with limited capacity for inducible phytochemical responses. However, this has not been explored for volatile organic compounds (VOCs) that have a relatively low ratio of production costs to ecological benefits. To test this, I sampled VOCs emitted from canopy leaves of 10 phylogenetically diverse tree species (3 Magnoliids and 7 Rosids) in the Peruvian Amazon before and after induction with the phytohormone methyl jasmonate (MeJA). There was no phylogenetic signal in induction or magnitude of MeJA‐induced VOC emissions from intact leaves: all trees induced VOC profiles dominated by β‐ocimene, linalool, and α‐farnesene of varying ratios. Moreover, overall inducibility of VOCs from intact leaves was unrelated to phytochemical diversity or richness. In contrast, experimentally wounded leaves showed considerable phylogeny‐based and MeJA‐independent variation the richness and diversity of constitutive wound‐emitted VOCs. Moreover, VOC inducibility from wounded leaves correlated negatively with phytochemical richness and diversity, potentially indicating a tradeoff in constitutive and inducible defence strategies for non‐volatile specialised metabolites but not for inducible VOCs. Importantly, there was no correlation between any chemical profile and either natural herbivory or leaf toughness. The coexistence of multiple phytochemical strategies in a hyper‐diverse forest has broad implications for competitive and multitrophic interactions, and the evolutionary forces that maintain the exceptional plant biodiversity in neotropical forests.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3390/agronomy11050958
