Recent advances in plant-herbivore interactions

Abstract

Plant-herbivore interactions shape community dynamics across marine, freshwater, and terrestrial habitats. From amphipods to elephants and from algae to trees, plant-herbivore relationships are the crucial link generating animal biomass (and human societies) from mere sunlight. These interactions are, thus, pivotal to understanding the ecology and evolution of virtually any ecosystem. Here, we briefly highlight recent advances in four areas of plant-herbivore interactions: (1) plant defense theory, (2) herbivore diversity and ecosystem function, (3) predation risk aversion and herbivory, and (4) how a changing climate impacts plant-herbivore interactions. Recent advances in plant defense theory, for example, highlight how plant life history and defense traits affect and are affected by multiple drivers, including enemy pressure, resource availability, and the local plant neighborhood, resulting in trait-mediated feedback loops linking trophic interactions with ecosystem nutrient dynamics. Similarly, although the positive effect of consumer diversity on ecosystem function has long been recognized, recent advances using DNA barcoding to elucidate diet, and Global Positioning System/remote sensing to determine habitat selection and impact, have shown that herbivore communities are probably even more functionally diverse than currently realized. Moreover, although most diversity-function studies continue to emphasize plant diversity, herbivore diversity may have even stronger impacts on ecosystem multifunctionality. Recent studies also highlight the role of risk in plant-herbivore interactions, and risk-driven trophic cascades have emerged as landscape-scale patterns in a variety of ecosystems. Perhaps not surprisingly, many plant-herbivore interactions are currently being altered by climate change, which affects plant growth rates and resource allocation, expression of chemical defenses, plant phenology, and herbivore metabolism and behavior. Finally, we conclude by noting that although the field is advancing rapidly, the world is changing even more rapidly, challenging our ability to manage these pivotal links in the food chain.

Keywords: climate impact; herbivore diversity; plant defense theory; plant-herbivore interactions.

Figure 1.. Plant-herbivore interactions shape community dynamics across terrestrial, freshwater, and marine habitats.

These interactions encompass a huge range of taxa and organismal size for both plants and herbivores. Common herbivores across these ecosystems are ( A) spicebush swallowtail caterpillar ( Papilio troilus) feeding on spicebush ( Lindera benzoin); ( B) impala ( Aepyceros melampus) browsing shrubs in an African savanna; ( C) white rhinoceros ( Ceratotherium simum) grazing African grasses; ( D) Daphnia dentifera, an important grazer on freshwater phytoplankton; ( E) the white tuberculed crayfish ( Procambarus spiculifer) consuming a freshwater macrophyte ( Egeria densa); ( F) Canada goose ( Branta canadensis), an important herbivore on freshwater macrophytes and terrestrial grasses; ( G) the isopod Erichsonella attenuata, a mesograzer of epiphytes and seaweeds in seagrass meadows; ( H) blue parrotfish ( Scarus coeruleus) grazing filamentous algae on a coral reef; and ( I) West Indian manatee ( Trichechus manatus) curiously eating a red mangrove plant ( Rhizophora mangle). Photo credits: Eric Lind ( A), John Parker ( B, E, F, G, I), Deron Burkepile ( C), Alan Wilson ( D), Thomas Adam ( H).

Figure 2.. The impact of risk of predation on plant-herbivore interactions often depends on many context-dependent factors such as habitat complexity.

Catano et al. used taxidermy decoy black grouper to manipulate risk in areas of low and high complexity on a Caribbean coral reef. They measured rates of herbivory and quantified bites of common parrotfishes and surgeonfishes at increasing distances from the decoy grouper. In areas of low complexity ( A), overall rates of herbivory by parrotfishes and surgeonfishes are lower than in control areas without grouper decoys (not shown) but are significantly higher than in areas of higher complexity ( B). In areas of higher complexity, rates of herbivory are significantly lower at closer distances to the decoy grouper than in the low-complexity areas. However, feeding by the smallest herbivorous fishes was greatest at closer distances in the higher-complexity areas, potentially due to the smaller fishes being less vulnerable to large grouper and also due to having more refuge from predation in the complex habitats. Illustration courtesy of Laura Catano.

Figure 3.. Climate warming may have idiosyncratic effects on plant-herbivore interactions, depending on the species involved

Lemoine et al. showed that increasing temperature affects growth rates of Japanese beetles ( Popilla japonica, at right skeletonizing an Oenothera biennis leaf) differently depending on the plant species they are feeding on. For example, Japanese beetle growth increased with temperature on plants such as Platanus occidentalis (purple points) but declined on species such as Viburnum prunifolium (pink points). These data highlight the difficulty in predicting the impact of climate warming on plant-herbivore interactions. Data redrawn after Lemoine et al. . Image from Dejeanne Doublet.