Gordon G. McNickle

Synthesis and modeling perspectives of rhizosphere priming.

The rhizosphere priming effect (RPE) is a mechanism by which plants interact with soil functions. The large impact of the RPE on soil organic matter decomposition rates (from 50% reduction to 380% increase) warrants similar attention to that being paid to climatic controls on ecosystem functions. Furthermore, global increases in atmospheric CO2 concentration and surface temperature can significantly alter the RPE. Our analysis using a game theoretic model suggests that the RPE may have resulted from an evolutionarily stable mutualistic association between plants and rhizosphere microbes. Through model simulations based on microbial physiology, we demonstrate that a shift in microbial metabolic response to different substrate inputs from plants is a plausible mechanism leading to positive or negative RPEs. In a case study of the Duke Free-Air CO2 Enrichment experiment, performance of the PhotoCent model was significantly improved by including an RPE-induced 40% increase in soil organic matter decomposition rate for the elevated CO2 treatment--demonstrating the value of incorporating the RPE into future ecosystem models. Overall, the RPE is emerging as a crucial mechanism in terrestrial ecosystems, which awaits substantial research and model development.

Plants integrate information about nutrients and neighbors.

Plant root growth is modified in the presence of within-species competition and uneven local resource distributions. Animals regularly integrate information about the location of resources and the presence of competitors, altering their foraging behavior accordingly. We studied the annual plant Abutilon theophrasti to determine whether a plant can demonstrate a similarly complex response to two conditions: presence of a competitor and heterogeneous resource distributions. Individually grown plants fully explored the pot by using a broad and uniform rooting distribution regardless of soil resource distributions. Plants with competitors and uniform soil nutrient distributions exhibited pronounced reductions in rooting breadth and spatial soil segregation among the competing individuals. In contrast, plants with competitors and heterogeneous soil nutrient distributions reduced their root growth only modestly, indicating that plants integrate information about both neighbor and resource distributions in determining their root behavior.

Focusing the metaphor: plant root foraging behaviour

Many authors assert that plants exhibit complex behaviours which are analogous to animal behaviour. However, plant ecologists rarely root these studies in a conceptual foundation as fertile as that used by animal behaviourists. Here we adapt the optimality principles that facilitated numerous advances in the study of animal foraging behaviour to create one possible framework for plant foraging behaviour. Following the traditions of animal foraging ecology, we discuss issues of search and handling in relation to plant root foraging. We also develop a basic plant-centered model that incorporates modular growth and foraging currencies relevant to plant growth. We conclude by demonstrating how this new foundation could be adapted to address five fundamental questions in plant foraging ecology.

Game theory and plant ecology

The fixed and plastic traits possessed by a plant, which may be collectively thought of as its strategy, are commonly modelled as density-independent adaptations to its environment. However, plant strategies may also represent density- or frequency-dependent adaptations to the strategies used by neighbours. Game theory provides the tools to characterise such density- and frequency-dependent interactions. Here, we review the contributions of game theory to plant ecology. After briefly reviewing game theory from the perspective of plant ecology, we divide our review into three sections. First, game theoretical models of allocation to shoots and roots often predict investment in those organs beyond what would be optimal in the absence of competition. Second, game theoretical models of enemy defence suggest that an individuals investment in defence is not only a means of reducing its own tissue damage but also a means of deflecting enemies onto competitors. Finally, game theoretical models of trade with mutualistic partners suggest that the optimal trade may reflect competition for access to mutualistic partners among plants. In short, our review provides an accessible entrance to game theory that will help plant ecologists enrich their research with its worldview and existing predictions.

Plant root growth and the marginal value theorem

All organisms must find and consume resources to live, and the strategies an organism uses when foraging can have significant impacts on their fitness. Models assuming optimality in foraging behavior, and which quantitatively account for the costs, benefits, and biological constraints of foraging, are common in the animal literature. Plant ecologists on the other hand have rarely adopted an explicit framework of optimality with respect to plant root foraging. Here, we show with a simple experiment that the marginal value theorem (MVT), one of the most classic models of animal foraging behavior, can provide novel insights into the root foraging behavior of plants. We also discuss existing data in the literature, which has not usually been linked to MVT to provide further support for the benefits of an optimal foraging framework for plants. As predicted by MVT, plants invest more time and effort into highly enriched patches than they do to low-enriched patches. On the basis of this congruency, and the recent calls for new directions in the plant foraging literature, we suggest plant ecologists should work toward a more explicit treatment of the idea of optimality in studies of plant root foraging. Such an approach is advantageous because it forces a quantitative treatment of the assumptions being made and the constraints on the system. While we believe significant insight can be gained from the use of preexisting models of animal foraging, ultimately plant ecologists will have to develop taxa-specific models that account for the unique biology of plants.

Heterogeneity of plant phenotypes caused by herbivore-specific induced responses influences the spatial distribution of herbivores

Abstract 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.

Molecular identification of roots from a grassland community using size differences in fluorescently labelled PCR amplicons of three cpDNA regions.

Elucidating patterns of root growth is essential for a better understanding of the functioning of plant‐dominated ecosystems. To this end, reliable and inexpensive methods are required to determine species compositions of root samples containing multiple species. Previous studies use a range of PCR‐based approaches, but none have examined a species pool greater than 10 or 30 when evaluating mixed and single species samples, respectively. We present a method that evaluates size differences in fluorescently labelled PCR amplicons (fluorescent fragment length polymorphism) of the trnL intron and the trnT‐trnL and trnL‐trnF intergenic spacers. Amplification success of the trnT‐trnL spacer was limited, but variation in the trnL intron and the trnL‐trnF spacer was sufficient to distinguish over 80% of the 95 species (97% of the 77 genera) evaluated from a diverse fescue grassland community. Moreover, we identified species known to be present in mixed samples of 4, 8, 12, and 16 species on average 82% of the time. However, this approach is sensitive to detecting species known to be absent (false positives) when using our key of 95 species. Comparing unknowns to a limited species pool ameliorates this problem, comparable to a researcher using prior knowledge of what species could be found in a sample to constrain the identification of species. Comparisons to other methods and future improvements are discussed. This method is efficient, cost‐ effective and broadly applicable to many ecosystems.

Nutrient foraging behaviour of four co-occurring perennial grassland plant species alone does not predict behaviour with neighbours

Summary The spatial arrangement of nutrients and neighbours in soil influences plant growth and reproduction. Plants often respond to such stimuli through plasticity in root proliferation (root mass per soil volume), or the breadth of their root system. Here, we asked how plants adjust nutrient foraging strategies when grown alone or with neighbours. We asked (i) Does root proliferation into nutrient-rich patches when plants are grown alone predict root proliferation when plants are grown with neighbours? (ii) What factors (nutrients or neighbours) best predict the probability of root placement at different soil locations? (iii) How does the spatial distribution of nutrients alter the degree to which neighbours suppress plant growth? To answer these questions, we grew four grassland species either as individual plants or in competition, in patchy or patch-free soil, in a factorial design. We used genomic DNA to identify the spatial distribution of roots of each species when plants were grown in mixtures. The root foraging behaviour of individuals grown alone did not consistently predict behaviour in mixture. Specifically, (i) the behaviour of individually grown plants predicted behaviour of competing plants inside patches, but not in background soil. We observed over-proliferation of roots in background soil relative to what was expected from plants grown alone. (ii) Neighbours were consistently the most important variable for predicting the placement of roots in soil and caused either an increase in root system breadth, or no change relative to alone. (iii) If a species experienced growth suppression when grown in competition, individuals experienced this more severely in patchy soil compared to patch-free soil. Synthesis. Game theoretic models have predicted that under interspecific competition, over-proliferation of roots in the presence of neighbours might occur for some species but not others. Our data are consistent with these predictions but more work is needed. Nutrient foraging studies have primarily focused on plants grown alone or assumed that plants do not respond separately to neighbours and nutrients. Our data call these practices into question and contribute to a growing understanding that plants integrate information about both nutrients and neighbours when placing roots in soil.

When Michaelis and Menten met Holling: towards a mechanistic theory of plant nutrient foraging behaviour

To the untrained eye plants might appear to be more like an inanimate object than the type of organism that exhibits behaviour. However, if you know where to look, you will find that plants are remarkably good at assessing and responding to environmental conditions in ways that are best described using behavioural models. Here we show that botanists and zoologists have been using rearranged forms of an identical equation to explain resource intake. By rearranging this equation, botanists may preserve existing knowledge on uptake physiology, while simultaneously gaining access to a rich literature on foraging theory.

The world's biomes and primary production as a triple tragedy of the commons foraging game played among plants

Plants appear to produce an excess of leaves, stems and roots beyond what would provide the most efficient harvest of available resources. One way to understand this overproduction of tissues is that excess tissue production provides a competitive advantage. Game theoretic models predict overproduction of all tissues compared with non-game theoretic models because they explicitly account for this indirect competitive benefit. Here, we present a simple game theoretic model of plants simultaneously competing to harvest carbon and nitrogen. In the model, a plants fitness is influenced by its own leaf, stem and root production, and the tissue production of others, which produces a triple tragedy of the commons. Our model predicts (i) absolute net primary production when compared with two independent global datasets; (ii) the allocation relationships to leaf, stem and root tissues in one dataset; (iii) the global distribution of biome types and the plant functional types found within each biome; and (iv) ecosystem responses to nitrogen or carbon fertilization. Our game theoretic approach removes the need to define allocation or vegetation type a priori but instead lets these emerge from the model as evolutionarily stable strategies. We believe this to be the simplest possible model that can describe plant production.