Intelligent behaviour is designed to maximize fitness but only in circumstances that challenge the survival of the organism and test its capability for intention (within an evolutionarily determined end point) and choice. Ecological investigators are starting to construct circumstances in which intention and choice are tested.
Foraging for food resources is an essential activity for both plants and animals. Consequently, most aspects of intelligent behaviour are exemplified in foraging for nutrients. Little is left to chance or plasticity in reproductive behaviour. For a similar reason, much plant taxonomy relies on flower structure in which plasticity is minimized. For land plants, resources appear as a complex spatial and temporal mosaic (Hutchings and deKroon, 1994), in part reflecting patchy distribution of soil materials and neighbour competition (Turkington and Harper, 1979; Salzman and Parker, 1985). Competition is certainly one environmental circumstance rarely provided in laboratory experiments. In a resource mosaic, intelligent behaviour is essential if resource collection is to be optimized in the face of competition. Foraging is a term now used much more frequently in plant ecological literature and is a proper description of the way plants behave when gathering growth resources.
Dodders (Cuscuta sp.) are parasitic plants that have lost almost all photosynthetic capability (Kuijt, 1969). Responding to an initial touch stimulus, growing shoots take several days to coil around suitable hosts. Haustorial primordia and haustoria then differentiate and nutrient resources commence transfer from the host in about 4 d (Kelly, 1990). In dodder, it is thus possible to dissociate active choice from the subsequent passive effects of acquired resources on growth that can complicate other situations. By tying suitable stem explants of dodder to touch the host, Kelly (1992) observed that 60 % of individuals rejected suitable hosts within several hours. Rejection was reduced to about 25 % if the host was pre-treated with nitrate. Active choice was thus influenced by the anticipated reward. By using a range of hosts of different reward value, measuring the length of coils and the biomass subsequently accumulated after 28 d, it was shown that the length of coiling was linearly related to subsequent reward/unit of energy invested. These data fit a simple marginal value model of resource use, applicable also to grazing animals; they also indicate plasticity in the length of coiling. Just as animals intelligently feed, so do plants. Seed set was correlated with the size of the parasite, indicating that host selection was adaptive and fitness of the parasite improved. It was suggested that rapid transfer of chemical information through the initial touch contact determined host selection and final length of coiling.
The uneven distribution of light to which wild plants are exposed is a critical factor controlling subsequent fitness. Light is critical to the acquisition of carbon resources and energy for other cellular processes. But many plants (often called sun plants to distinguish them from shade plants) do not react passively to the light mosaic in a canopy, simply accumulating dry weight when the light is strong enough. The quality and quantity of light is actively perceived (through red : far red ratios) and the position of likely future competitive neighbours mapped (Gilroy and Trewavas, 2001). Avoiding action is taken by accelerating the growth of the stem, which becomes thinner (Ballare et al., 1990; Aphalo and Ballare, 1995), or branch growth is accelerated into light of higher intensity (Trewavas, 1986b). Thus, the resource-acquiring structure(s), the stem plus leaves, is projected at speed into the resource-rich patch away from competition. Root growth is also altered, indicating communication of light perception to other parts of the organism (Aphalo and Ballare, 1995). New leaves are then especially positioned free from competitive light interruption (Ackerley and Bazzaz, 1995).
The stilt palm (Allen, 1977) is constructed from a stem raised on prop roots. When competitive neighbours approach, avoidance action is taken by moving the whole plant back into full sunlight. Such obvious ‘walking’ is accomplished by growing new prop roots in the direction of movement while those behind die off. That this is intentional behaviour is very clear. Other equally dramatic light-foraging mechanisms are to be found in tropical climbers, particularly Syngonium. On reaching the top of a tree, the growing point descends, progressively changing its morphology and leaf structure, and eventually assuming a very thin filiform shape with only scale leaves on the soil. Using skototropism (movement towards darkness), the filiform stem explores, locates and recognizes a new trunk and reverses the growth pattern. As it climbs, the internode becomes progressively thicker and leaves progressively redevelop to full size (Strong and Ray, 1975; Ray, 1987, 1992). This behaviour is analogous to animals that climb trees to forage, intelligently descend when food is exhausted or competition severe, and then climb the next tree.
Experiments with rhizomatous clonal herbs have shown that when provided with deliberate choice, the new growth of rhizomes and associated shoots is highly selective and is directed with much higher probability into favourable microhabitats. The new territories that are exploited may consist of freedom from other competitors (Evans and Cain, 1995; Kleijn and Van Groenendael, 1999), unshaded and warmer temperatures (MacDonald and Lieffers, 1993), or weaker salinity (Salzman, 1985; Salzman and Parker, 1985). When resources become abundant, dormant buds are induced to grow as shoots rather than new rhizomes (Hutchings and de Kroon, 1994). Rhizomes that pen etrate the poorer environments are generally thinner, their internodes are longer and they grow more rapidly where possible. The dispersal of any new shoots from the parent plant is thus greatly increased, and new territory is actively searched for new resource-rich patches. Limited growth resources are thus efficiently used to cover maximum ground with minimum investment. Directing the majority of rhizomes to exploit rich resources whilst allowing others to search for new resources suggests optimal strategies are in place to maximize returns and increase fitness. When resources are scarce, growth materials are invested in the organ through which scarce resources are normally sequestered: if minerals or water are scarce, enhanced root growth occurs; if light is scarce, stem growth is enhanced at the expense of root growth.
But the growth of clonal herbs responds directly to the uneven distribution of resources in the soil. When grown on soil in which resources are distributed in patches rather than uniformly, overall biomass accumulation can be up to seven-fold higher (Wijesinghe and Hutchings, 1997, 1999). Not only could Glechoma plants discriminate an optimal patch size, but they could also discriminate the strength of gradients across the boundary of the patch, showing several-fold better growth when the gradient was greatest. How the parameters of patch size and gradient strength lead to enhanced growth is not understood. It is difficult to avoid the conclusion of intention and intelligent choice and the ability to select conducive habitats in which to place and grow organs of resource exploitation. Perhaps the most surprising observations come from Evans and Cain (1995). They tested whether the clonal herb Hydrocotyle, which grows on sand dunes, could preferentially locate good patches or avoid bad patches in a heterogenous environment. They reported that rhizomes veered away from patches of grass and thus obvious competition. Intentional choice of habitat is clear.
Individual roots can track humidity and mineral gradients in soil (see summary of references in Takahashi and Scott, 1993), just as shoots can track local light sources (Trewavas, 1986b). Roots can change their branching patterns (architecture) radically when resource-rich patches are found (from herring bone structure to a highly branched motif; Fitter, 1986) and change uptake rates so that no particular resource limits growth but all remain in approximate balance. And, to avoid detrimental competition, roots (like shoots) take deliberate avoidance action to prevent contact when approached by roots of other species (Mahall and Calloway, 1991).
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