Self-assembling Plants and Integration across Ecological Scales

Annals of Botany 99: 1023–1034, 2007 doi:10.1093/aob/mcm037, available online at www.aob.oxfordjournals.org Self-assembling Plants and Integration across Ecological Scales RO DE R IC K H UN T 1, * and R . L . CO L A S AN T I 2, 3 1 School of Biosciences, University of Exeter, The Innovation Centre, Rennes Drive, Exeter, EX4 4RN, UK, 2US Environmental Protection Agency, 200 SW 35th Street, Corvallis, OR 97333, USA and 3CSIRO, Long Pocket Laboratories, 120 Meiers Road, Indooroopilly, QLD 4068, Australia Received: 6 November 2006 Returned for revision: 8 December 2006 Accepted: 24 January 2006 Key words: Self-assembling plants, cellular automata, vegetation dynamics, L-system, population, community, emergent properties, biodiversity. IN TROD UCT IO N Although individual plants are distinct entities exhibiting behaviour typical of all complex organisms ( preferential placement of food-gathering organs, differential distribution of biomass as a consequence of environment, interactions with other organisms at their own and higher levels of organization), they have no identifiable centres of tactical, as opposed to strategic, control. Within the strategic limits set by its genetics, it appears possible that a plant’s tactical behaviour is emergent solely from the resourcehandling properties of its constituent organs. A new class of model, the self-assembling cellular automaton (CA), now makes this hypothesis testable. Preceding investigations into emergent topology have been in the domain of L-system models. These can produce topographically correct images (Lindenmayer, 1968; Room et al., 1994; Room and Prusinkiewicz, 1996) that are photo-realistic and three-dimensional. Their spatial rules of growth are based upon ‘real’ plant morphology. L-systems can be made environmentally sensitive, such that the structure of the plant is influenced by the space that it occupies; these models are referred to as ‘sighted’ (Borchert and Honda, 1984; Bell, 1986; Ford, 1987; Sutherland and Stillman, 1988). Other types of virtual plant models can simulate population dynamics but usually ignore explicit plant–plant interactions (Mech and Prusinkiewicz, 1996). These mathematical representations of individual plants interact with one another under the control of a further, supervisor model. Unlike CA, L-systems need complicated rulesets in order to generate realistic plant topologies. However, the botanical and ecological processes included in these rulesets serve purely to create the desired endpoint, a photo-realistic image. Topology and form are at the heart of L-system rulebases; botanical, and certainly ecological, issues play a secondary role to visual ones. In order to use CA to investigate our premise that individual plants exhibit no identifiable centre of organization, we needed to model at the same modular level as that addressed by L-systems. Simpler, ‘chequerboard’ spatial CA modelling (e.g. Colasanti and Grime, 1993) would not do. However, the emphasis of our methodology had * For correspondence. E-mail # The Author 2007. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: † Background and Aims Although individual plants exhibit much complex behaviour in response to environmental stimuli, they appear to do so without any identifiable centres of organization. We review a special class of model with the aim of testing whether plants can effectively be self-assembling, modular-driven organisms, in the sense that whole-plant organization and behaviour emerges solely from the interactions of much smaller structural elements. We also review evidence that still higher-level behaviour, at the population and community levels of organization, can emerge from this same source. † Methods In previous work we devised a special cellular automaton (CA) model of plant growth. This comprises a section depicting a two-dimensional plant in its above- and below-ground environments. The whole plant is represented by branching structures made up from identical ‘modules’. The activity of these modules is driven by morphological, physiological and reproductive rulesets derived from comparative plant ecology, a feature which lends itself to experimentation at several ecological scales. † Key Results From real experiments using virtual plants we show that the model can reproduce a very wide range of whole-plant-, population- and community-level behaviour. All of these properties emerge successfully from a ruleset acting only at the level of the CA module. † Conclusions The CA model can, with advantage, be driven by C-S-R plant strategy theory. As this theory can ascribe a functional classification to any temperate angiosperm on the basis of a few simple tests, any community of such plants can be redescribed in terms of its ‘functional signature’ and the net environment that it experiences. To a valuable first approximation, therefore, a C-S-R version of the CA model can simulate the most essential properties both of natural vegetation and of its environment. We have thus achieved a position from which we can test a plethora of high-level community processes, such as diversity, vulnerability, resistance, resilience, stability, and habitat-community heterogeneity – processes which, if investigated on the scales truly required for a full understanding, would fall beyond the practical scope of even the largest real-life investigation. 1024 Hunt and Colasanti — Self-Assembling Plants and Integration across Scales HOW T H E MOD E L WOR KS As our central assumption is that whole-plant behaviour could emerge solely from modular action and interaction, our model mimics the form and function of a whole, individual plant through the behaviour of fundamental, indivisible, subcomponents. Each of these subcomponents is a binary branching module. Within the simulation there is thus no such thing as a ‘whole plant’ that is engaged in whole-plant processes, there is simply an interconnected collection of plant modules. In the same way that ecological behaviour emerges out of the actions of individual plants, we provide the opportunity for ‘whole plant’ behaviour to emerge solely from the interconnections and interactions of individual modules (Fig. 1). As in other CA models, the spatial area within the simulation is divided into an array of cells. In our case, these represent a vertical section through the two-dimensional plant and its environment. The plant modules (if any) within each cell are linked into two branched networks, the ‘root’ and ‘shoot’ systems. This structure represents the plant as a collection of linked branching units seen through a vertical plane. The way in which the binary tree is structured, the way in which its internal relations are managed, and the way in which its external relations with its environment and with neighbouring modules are managed, are all described in outline by Colasanti and Hunt (1997a (...truncated)