Plants have different strategies to deal with insect herbivores; some use chemical defenses to ward them off. Phenolic compounds are understood as a good way to measure plant response to herbivory by the scientific community. However, they have their limitations. Studies show that different insect herbivores elicit different reactions in plants in terms of phenolic compounds and that phenolic compound use depends on a plant's environment. Phenolic compound concentration can be explained by the Resource Availability Hypothesis in addition to use in deterring insect herbivores. Despite their limitations and context-dependence, phenolic compounds are consistently used to protect plants from insect herbivores.
Introduction
Plants have a lot of things going against them: they can't move, they start out very small, and lots of things are out to get them, or, eat them. Plants make up the base of the food chain and it's easy to see why: they're everywhere, they won't run away, and they're pretty nutritious and delicious too. Just about everything we eat comes from plants or something that eats them. But we aren't the only things out there eating plants, one group of creatures particularly enjoys snacking on plants, and these guys have quite made quite a name for themselves!
Insects.
Insects are an especially successful group of organisms due to their ability to fly nearly anywhere they want and have several generations of offspring in a short time. Not only that, but they are very efficient reproducers, and insects are one of the most abundant groups of organisms to reflect this. This strategy results in the introduction of an incomprehensible number of insects that all need something to eat, and a lot of them turn to plants because they're nutritious enough and pretty easy targets to boot.
Or so they think.
Plants have been eaten at since they'be been growing in the ground, and they've developed some pretty potent strategies themselves for dealing with the insects that would otherwise limit their survival. This phenomenon of insects eating plant tissue is something scientists call herbivory, and this isn't the last time we'll see this word throughout this post! Plants and insects are perfectly capable of coexisting, in fact, the feeding damage of insects can stimulate the growth of many plants (Schuldt et al. 2015), but once insect plant-eaters cross a threshold of being too harmful to their host plants, they start to focus on developing countermeasures. One such countermeasure many plants use to ward off the insects that would eat them is a group of chemicals called phenolic compounds. As we've discussed in previous blog posts, phenolic compounds have a variety of uses for plants, including structural support, chemical defenses, and attracting beneficial microorganisms. While the first and last are also very important to plants, insects are most concerned about the chemical-defense application of phenolics.
One would expect that what is basically plant-made insecticide would deter insect herbivores, and that's pretty much what scientists expect too (Moreira et al. 2019). Several studies use phenolic compound concentration as a measure of how stressed a plant is or how responsive it is to threats (Salminen, Karonen. 2011), demonstrating just how established a reputation phenolic compounds have on the scientific community. However, one study recently rocked the boat in concluding that phenolic concentrations are essentially overstated in quantifying plant responses to insect damage and that other plant reactions to herbivory such as overcompensation (plants growing faster when they are damaged) and differences in nutritional quality should be evaluated instead (Moiera et al. 2018). On paper, this conclusion opposes the established importance of phenolic compounds, but, to have a proper perspective, we need to delve into the scientific community.
Research Analysis
Despite the variety of emerging research into plant defenses, there are existing scientific assumptions about them and how they operate. One of these is the Resource Availability Hypothesis, which proposes that plants that grow in nutrient-limited conditions grow slower and allocate more resources to defense than those that are less limited by nutrients (Coley, 1985). This explanation is pretty intuitive, as plants that don't have as many resources aren't as able to recover from potential herbivory than plants who can afford to overcompensate for tissue loss. The Resource Availability Hypothesis is an idea that has been repeatedly challenged throughout its existence, and several studies reference it, especially in reference to phenolic compounds.
Insects aren't the only things out there that would influence phenolic production either. In the last blog post, we discussed plant-plant interactions and how this relationship affects phenolic compound production. If insects can be said to sabotage their host plants, they might be comparable to weeds, which are known to stimulate phenolic production as they attempt to outcompete other plants, a phenomenon called allelopathy (Cheng & Cheng, 2015), reinforcing the impact of plant community composition on phenolic compounds (Mraja et al. 2011). Because insect herbivores cause direct damage to plants, it's even easier to assume that plants are going to demonstrate a response for them than for weeds as well.
A study conducted by Rosado et al. wanted to test how the responses in plants elicited by different insect herbivores differed under varying conditions of plant diversity, as in if a community of several species of plants responded differently to insect feeding. These scientists reared beetle larva and caterpillars to compare the differences between four possible scenarios: beetles feeding on one species of plant, beetles feeding on a community of plants, caterpillars feeding on one species of plant, and caterpillars feeding on a community of plants. Several measurements of the plants were taken after the experiment to evaluate the impact these herbivores had on the plants and were then compared.
The table above (Rosado et al. 2018) displays degrees of freedom, F values, and p values of a set of relationships between community plant diversity, beetle damage, and caterpillar damage on four plant traits: total phenolics, condensed tannins (a type of phenolic compound found in plant leaves), trichomes, specific leaf area, and growth rate. There were significant relationships between beetle damage and total phenolics, beetle damage and condensed tannins, and plant community diversity and specific leaf area. These results suggest that while beetle damage significantly increases total phenolics and condensed tannins in plants, caterpillar damage lacks this association. These scientists speculate that life-cycle characteristics including dispersal behavior and pheromone-related aggregation contribute to this disparity in phenolic concentrations. In terms of what we're addressing in this blog post, different insect herbivores cause different responses in the plants they feed on, and we're still speculating on the mechanisms that contribute to this.
Another group of scientists studied how latitude (particularly in the northern hemisphere) affects several plant traits, including the concentation of phenolic compounds. Moreira et al. studied 38 sites with populations of English oak across a latitudinal gradient in Europe and measured these traits between late August and early October, between the end of the growing season and leaf senescence (when the leaves fall off the trees). Plant material from the oaks sampled across this gradient was processed to quantify these plant traits. It is notable that these scientists were explicitly interested in phenolic compounds as a measure of plant responses to herbivory, supporting possible preconceptions about phenolics made earlier in this post!
The figure above (Moreira et al. 2018) displays the relationship between latitude and a variety of plant traits, including nutrition and measures of chemical defenses, including phenolic compounds such as tannins and flavonoids as a linear regression. R2 and p-values are also displayed, which explain how much variation the model explains and the likelihood that there is an association between these two variables, respectively. While there are several significant relationships between these plant traits and latitude, the relationship between total phenolic compounds and its constituents (flavonoids and condensed tannins) is particularly strong, with rather high R2 values for the condensed tannins and total phenolics models. This means that as latitude increases (the more north), the more overall phenolics will be present in oaks. This is an unexpected conclusion that has some pretty interesting connotations!
Implications and Theory
The relationship between herbivory and phenolic compounds seems simple on an intuitive level, but, as these studies demonstrate, it's actually pretty complicated and we don't understand a lot yet. While phenolic compounds do generally act as insect deterrents, their effects vary between herbivores (Rosado et al. 2018) and likely between plants too. Given how interconnected these systems are, every interaction between insects and plants is probably unique in some way, and that's super frustrating for scientists to admit since we like to look for general explanations for what we study. It's important to distinguish that there are patterns in nature that have value, but scientists should be careful not to oversell these as we could with phenolics when there are other important factors at play.
The latitude study conducted by Moreira's team has two important conclusions that can be made from it, in that it supports the Resource Availability Hypothesis while dispelling some preconceived notions about latitude and the chemical defenses of plants. This study found that as latitude increases, the concentration of phenolic compounds also increases, which, if thinking about high concentrations of phenolic compounds as a response to herbivory (a connection that is easy to assume), frankly makes no sense. Because biodiversity and organism abundance are understood to increase closer to the equator, one would expect there to be more herbivory further south, and therefore higher concentrations of phenolic compounds to ward off herbivores. However, the Resource Availability Hypothesis offers an explanation that is consistent with these results:
When the going gets tough, get tougher.
While plants growing at latitudes close to the equator have more herbivores to address, they also have more optimal growing time, temperature, and precipitation. Plants at higher latitudes lack these resources, so they have to change their strategy. They need to hunker down and make the most of what little they have, and that often means beefing up their chemical defenses to compensate for their inability to bounce back from potential herbivory. This is in contrast with plants closer to the equator, as they have more resources with which they're more able to recover from insect feeding with strategies like overcompensation.
Conclusion
Phenolic compounds have a unique relationship with insect herbivores: they generally are used to ward them off but can have different reactions depending on the insect that feeds on their plants. These compounds are also affected by the environment to an extent, with latitudes farther away from the equator being associated with higher concentrations. While general statements about phenolic compounds and their properties (namely their ability to deter potential herbivores) still stand, it is important to acknowledge the limitations of generalizing them. There are obvious gaps in research surrounding phenolic compounds that should be addressed, especially in profiling their relationships with different groups of herbivores and in their associations with plant phenology and morphology.
References
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Moreira, X., Abdala, R. L., Berny Mier y Teran, J. C., Covelo, F., de la Mata, R., Francisco, M., … Tack, A. J. M. (2019). Impacts of urbanization on insect herbivory and plant defences in oak trees. Oikos, 128(1), 113–123.
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