Plant-insect chemical communication in ecological communities: an information theory perspective

Cross-species communication, where signals are sent by one species and perceived by others, is one of the most intriguing types of communication that functionally links different species to form complex ecological networks. Global change and human activity can affect communication by increasing fluctuations in species composition and phenology, altering signal profiles and intensity, and introducing noise. So far, most studies on cross-species communication have focused on a few specific species isolated from ecological communities. Scaling up investigations of cross-species communication to the community level is currently hampered by a lack of conceptual and practical methodologies. Here, we propose an interdisciplinary framework based on information theory to investigate mechanisms shaping cross-species communication at the community level. We use plants and insects, the cornerstones of most ecosystems, as a showcase and focus on chemical communication as the key communication channel. We first introduce some basic concepts of information theory, then we illustrate information patterns in plant-insect chemical communication, followed by a further exploration of how to integrate information theory into ecological and evolutionary processes to form testable mechanistic hypotheses. We conclude by highlighting the importance of community-level information as a means to better understand the maintenance and workings of ecological systems, especially during rapid global change

Climatic and soil factors explain the two-dimensional spectrum of global plant trait variation

Plant functional traits can predict community assembly and ecosystem functioning and are thus widely used in global models of vegetation dynamics and land–climate feedbacks. Still, we lack a global understanding of how land and climate affect plant traits. A previous global analysis of six traits observed two main axes of variation: (1) size variation at the organ and plant level and (2) leaf economics balancing leaf persistence against plant growth potential. The orthogonality of these two axes suggests they are differently influenced by environmental drivers. We find that these axes persist in a global dataset of 17 traits across more than 20,000 species. We find a dominant joint effect of climate and soil on trait variation. Additional independent climate effects are also observed across most traits, whereas independent soil effects are almost exclusively observed for economics traits. Variation in size traits correlates well with a latitudinal gradient related to water or energy limitation. In contrast, variation in economics traits is better explained by interactions of climate with soil fertility. These findings have the potential to improve our understanding of biodiversity patterns and our predictions of climate change impacts on biogeochemical cycles

Climatic and soil factors explain the two-dimensional spectrum of global plant trait variation

Plant functional traits can predict community assembly and ecosystem functioning and are thus widely used in global models of vegetation dynamics and land–climate feedbacks. Still, we lack a global understanding of how land and climate affect plant traits. A previous global analysis of six traits observed two main axes of variation: (1) size variation at the organ and plant level and (2) leaf economics balancing leaf persistence against plant growth potential. The orthogonality of these two axes suggests they are differently influenced by environmental drivers. We find that these axes persist in a global dataset of 17 traits across more than 20,000 species. We find a dominant joint effect of climate and soil on trait variation. Additional independent climate effects are also observed across most traits, whereas independent soil effects are almost exclusively observed for economics traits. Variation in size traits correlates well with a latitudinal gradient related to water or energy limitation. In contrast, varia- tion in economics traits is better explained by interactions of climate with soil fertility. These findings have the potential to improve our understanding of biodiversity patterns and our predictions of climate change impacts on biogeochemical cycles.Environmental Biolog

Plant defense phenotypes determine the consequences of volatile emission for individuals and neighbors

Plants are at the trophic base of terrestrial ecosystems, and the diversity of plant species in an ecosystem is a principle determinant of community structure. This may arise from diverse functional traits among species. In fact, genetic diversity within species can have similarly large effects. However, studies of intraspecific genetic diversity have used genotypes varying in several complex traits, obscuring the specific phenotypic variation responsible for community-level effects. Using lines of the wild tobacco Nicotiana attenuata genetically altered in specific well-characterized defense traits and planted into experimental populations in their native habitat, we investigated community-level effects of trait diversity in populations of otherwise isogenic plants. We conclude that the frequency of defense traits in a population can determine the outcomes of these traits for individuals. Furthermore, our results suggest that some ecosystem-level services afforded by genetically diverse plant populations could be recaptured in intensive monocultures engineered to be functionally diverse

How does plant chemical diversity contribute to biodiversity at higher trophic levels?

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Active injections of cytokinins by a free-living sap-feeding insect: a possible mechanism to delay herbivory induced senescence

Manipulations of plants by insects via growth hormones, such as cytokinins (CKs), have been suggested for decades. The focus has been on most obvious cases like “green-islands”. Evidence for an active transfer of CKs by the insect as well as manipulations of the plants perception of CKs has been elusive. We present the results on the interaction between the sap feeding mirid Tupiocoris notatus and the wild tobacco Nicotiana attenuata. We detected an increase of CK-levels and changes in CK related transcripts upon T. notatus attack. Two active CKs (isopentenyladenine and its riboside) have been detected in fifty-fold higher concentrations in the insects compared to leaves. Experiments with 15N-labeled plants showed that T. notatus transfers these CKs to the leaves on which it feeds. Plants with impaired CK perception showed a reduced attractiveness for mirids. While nutrient content was only marginally influenced by mirid feeding in wildtype plants, it was altered in plants with altered CK metabolism. Our results suggest that an active transfer of CKs by a free living insect maintains a homeostasis of nutrients even in highly damaged leaves to optimally exploit the food source

Keeping your food fresh: active manipulation of cytokinin-metabolism by a cell content feeder

Cytokinins play a central role in plant physiology, including regulation of senescence and nutrient translocation. Recent studies have revived interest in their role in plant-insect interactions. At the end of the sixties, some scientists suggested for the first time that phytophagous insects might manipulate cytokinin levels in the tissues where they feed to increase their sink strength (Engelbrecht et al., Nature, 1969). Here, we present our results on the interactions between the cell-content feeding mirid Tupiocoris notatus and the wild tobacco Nicotiana attenuata. Using highly sensitive LC-MS techniques, we detected two types of active cytokinins present in mirid bodies: isopentenyl-adenine (IP), and isopentenyl-adenosine (IPR). Surprisingly, the free base IP was ten to fifty times as concentrated in mirid bodies as in the leaf tissues where T. notatus normally feeds. By using N15-labeled plants, we showed that T. notatus specifically transfers! these two types of cytokinins into the leaves on which it feeds. The effects of T. notatus damage on the physiology of tobacco leaves was assessed by determining the concentration of soluble sugars, soluble proteins, free amino acids, and photosynthetic parameters over a time course during mirid attack. Responses were compared in wild-type plants and in transgenic plants with manipulated levels of cytokinins or impaired cytokinin perception. Even when insects had damaged the majority of the leaf-surface, levels of nutrients remained close to levels in undamaged controls. In contrast, plants with altered cytokinin metabolism and signalling showed larger changes in nutrient levels during T. notatus feeding. Our results suggest that T. notatus compensates for the damage it causes by manipulating cytokinin signalling in damaged leaves

Plant-insect chemical communication in ecological communities: an information theory perspective

Cross-species communication, where signals are sent by one species and perceived by others, is one of the most intriguing types of communication that functionally links different species to form complex ecological networks. Global change and human activity can affect communication by increasing fluctuations in species composition and phenology, altering signal profiles and intensity, and introducing noise. So far, most studies on cross-species communication have focused on a few specific species isolated from ecological communities. Scaling up investigations of cross-species communication to the community level is currently hampered by a lack of conceptual and practical methodologies. Here, we propose an interdisciplinary framework based on information theory to investigate mechanisms shaping cross-species communication at the community level. We use plants and insects, the cornerstones of most ecosystems, as a showcase and focus on chemical communication as the key communication channel. We first introduce some basic concepts of information theory, then we illustrate information patterns in plant-insect chemical communication, followed by a further exploration of how to integrate information theory into ecological and evolutionary processes to form testable mechanistic hypotheses. We conclude by highlighting the importance of community-level information as a means to better understand the maintenance and workings of ecological systems, especially during rapid global change