The Scale–Precision Trade-off in Spacial Resource Foraging by Plants: Restoring Perspective

Annals of Botany 99: 1017–1021, 2007 doi:10.1093/aob/mcm026, available online at www.aob.oxfordjournals.org VIEWPOINT The Scale –Precision Trade-off in Spacial Resource Foraging by Plants: Restoring Perspective J . P. G R I M E Unit of Comparative Plant Ecology, Department of Animal and Plant Sciences, The University, Sheffield, S10 2TN, UK Received: 22 November 2006 Returned for revision: 13 December 2006 Accepted: 11 January 2007 Published electronically: 20 March 2007 Key words: Resource foraging, scale/precision trade-off, nutrient supply. IN TROD UCT IO N Although individuals of most plant species remain confined to the same local patch throughout their lives, this need not prevent the development of ecological theories that resonate strongly with those used to comparing the resource foraging activities of animals. A common approach is possible because, for both animals and plants, alternative foraging behaviours can be examined by measuring net resource gain and fitness under controlled conditions of resource provision. Viewed in the context of such cost – benefit analyses, it is of little consequence that foraging in some (but not all) animals is achieved by wide-ranging locomotion, whereas most vascular land-plants forage locally and unobtrusively by growth processes that respond to changing patterns of resources and bring about a relocation of the absorptive surfaces of the plant both above and below ground. In order to obtain reliable and relevant information on the ways in which plant foraging behaviour varies across species it has been necessary to develop techniques that allow accurate measurements of the reactions of root and shoot systems when these are exposed to controlled patchiness in resource supply. Particular difficulties arise in assays of root foraging for mineral nutrients. Controlled patchiness in mineral nutrient supply can be maintained by the use of partitions, but these do not allow a realistic simulation of the circumstances in which the root system may sustain mineral nutrient capture by local extensions that facilitate ‘escape’ from the depletion zones that are a common feature of the rhizosphere (Bhat and Nye, 1973; Drew et al., 1973). An alternative method involving the creation of nutrient patches without the use of partitions and For correspondence. E-mail first described in this journal (Campbell and Grime, 1989) has the following advantages. (1) Use of a continuous drip-feed of nutrient solution at four equidistant radii into a column of freely draining sand creates four geometrically exact quadrants, each of constant dimensions and uniform chemistry from top to bottom of a cylindrical container. (2) Planting of a freshly germinated seedling at the central meeting point of the four quadrants ensures that regardless of initial seedling size and root morphology there is equal access to the four quadrants. (3) The drip-feed system permits an initial phase during which mineral nutrient supply can be identical in the four quadrants, simulating the experience of an establishing seedling. After a standard time, depletion zones resembling those arising from encroaching root systems of neighbouring established plants can be introduced to half of the rooting volume by severely reducing the concentration supplied to an opposite pair of quadrants. At this point half of the containers can be harvested to measure the dry weight of root in each quadrant. The remaining replicates can be harvested after a further period of growth, permitting a calculation of the increment of root growth in depleted and undepleted quadrants. The drip-feed method was used in an assay of root foraging characteristics that formed an important part of a large-scale experimental screening programme (the Integrated Screening Programme, ISP) measuring a wide range of plant traits in forty-three common plants of the Sheffield region in north-central England. The results of # 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 From the results of a comparative study using quantitative standardized assays of the scale and precision of responses of root and shoot systems to resource patchiness, Campbell et al. (1991; Oecologia 87: 532– 538) proposed a mechanism of species coexistence in herbaceous communities involving a dynamic equilibrium between, respectively, the coarse- and fine-scale foraging of dominant and subordinate species. The purpose of this paper is to reject a recent assertion that with respect to root systems the scale – precision hypothesis has been falsified. † Discussion and Conclusion Reference to the original papers confirms that the scope of the hypothesis was confined to circumstances (eg. mown meadows) where the vigour of potential dominants is restricted by intermittent removal of biomass. This qualification in the original hypothesis is a crucial omission from the meta-analysis conducted by Kembel and Cahill (2005; American Naturalist 166: 216 – 230). The original papers also contain examples that illustrate the operation of forms of selection that prevent the development of precise foraging below ground; these also appear to have escaped the attention of recent participants in this field of research. 1018 Grime — Scale – Precision Trade-off in Spacial Resource Foraging this whole study have been published (Grime et al., 1997) but the parts relating specifically to root (and shoot) foraging were judged to be sufficiently novel and interesting to merit more detailed and early presentation. There were three additional reasons for special attention to the foraging data from the ISP. A consequence of the decision to publish early the results of the root and shoot foraging tests in the ISP has been the appearance of a series of papers (Campbell et al., 1991a, b; Grime et al., 1991; Grime, 1994, 1998; Grime and Mackey, 2002) that, among several objectives, has explored the significance of one particular feature present in these data – evidence of a trade-off between the scale and precision of foraging. This research has recently culminated in a theoretical framework (Grime et al., 2007) in which the trade-off is recognized as one of five mechanisms capable, in specific circumstances, of sustaining co-existence in species-rich plant communities. Against this background it was a matter of surprise when two papers (Kembel and Cahill, 2005; de Kroon and Mommer, 2006) were published, each expressing the opinion that the notion of a trade-off between the scale and precision of foraging by root systems had been falsified. The purpose of this paper is to examine the validity of this conclusion in the light of two sources. The first consists of publications by those who conducted the ISP foraging experiments, whilst the second refers exclusively to Kembel and Cahill (2005) and de Kroon and Mommer (2006). S CA L E – P R E C I S I ON (...truncated)