Michael J. Hutchings

Foraging in Plants: the Role of Morphological Plasticity in Resource Acquisition

Triffids were, admittedly, a bit weird—but that was, after all, just because they were novelties. People had felt the same about novelties of other days—about kangaroos, giant lizards, black swans. And, when you came to think of it, were triffids all that much queerer than mudfish, ostriches, tadpoles, and a hundred other things? The bat was an animal that had learned to fly: well, here was a plant that had learned to walk—what of that? (from John Wyndham, The Day of the Triffids , 1951)

Morphological plasticity in clonal plants: the foraging concept reconsidered.

1 Studies of morphological plasticity in clonal plants have analysed responses to habitat quality in terms of spacer (stolon or rhizome internode) length and branching intensity. The capacity for these parameters to respond to environmental quality has been interpreted as an expression of foraging behaviour, as it confers the potential to intensify the placement of ramets in the more favourable microhabitats (patches) of a heterogeneous environment. This plasticity in clonal morphology is compared with similar responses of individual shoots and roots to habitat quality that have also been accepted as manifestations of foraging behaviour. 2 The most consistent morphological response shown by clonal species is a higher branching intensity an increased propensity of lateral meristems to grow out and form lateral rhizomes and stolons under conditions of higher resource supply. In contrast, spacer lengths show a variety of responses to light and nutrient availability, and many species exhibit no significant response. Even in stoloniferous species, where stolon internodes tend to shorten under higher photon flux densities, the degree of shortening may often be insufficient to elicit a significant concentration of ramets in favourable habitat patches. 3 Many clonal and nonclonal species have however, been shown to be very efficient in placing leaves and roots in areas of high resource supply within their environment. This is achieved by a high level of morphological plasticity of the shoot and root branches. 4 We therefore suggest that it is the highly plastic changes in the morphology of individual ramets that enable effective exploitation of local concentrations of essential resources once they have been located. The unresponsive spacer lengths of many clonal species may permit a continuous search of habitat space by the plant, rather than a selective placement of ramets. 5 The foraging concept is reformulated in more general terms relating to resourceacquisition strategies, so that it is applicable to both clonal and nonclonal species of plants.

Identification of 100 fundamental ecological questions

Summary 1. Fundamental ecological research is both intrinsically interesting and provides the basic knowledge required to answer applied questions of importance to the management of the natural world. The 100th anniversary of the British Ecological Society in 2013 is an opportune moment to reflect on the current status of ecology as a science and look forward to high-light priorities for future work.

TOWARD UNDERSTANDING THE CONSEQUENCES OF SOIL HETEROGENEITY FOR PLANT POPULATIONS AND COMMUNITIES

Several recent studies demonstrate that yield of individual plants, and their allocation of biomass between roots and shoots, can be profoundly affected by the pattern of supply of soil-based resources. Patchy provision of soil-based resources can affect the location of root biomass, as roots often proliferate in nutrient-rich patches. Root system size is important in determining whether plants access nutrient-rich patches, and the proportion of root systems located within such patches. This proportion will alter as growth proceeds. Species with small root systems have a limited ability to place roots in nutrient-rich patches even when they are very close. Of four species with different root system sizes, the growth of the species with the smallest root system was significantly limited by being located in nutrient-poor substrate even when nutrient-rich substrate was only 3.5 cm away, whereas three species with larger root systems were not disadvantaged. Both in the laboratory and in the field, root density is higher in nutrient-rich patches, and such patches can contain roots of many plants. Recent work showing that plants can respond to non-self roots sharing the same nutrient supply suggests that competition will be more severe in nutritionally patchy substrates than in homogeneous environments with the same overall nutrient supply. Taken together, these facts lead to the prediction that inter- and intraspecific plant interactions will be influenced by patterns of nutrient supply. We present evidence supporting this prediction, and indicating that population and community structure are also affected by patterns of nutrient supply. Significant differences in population yield, plant size distribution, and mortality have been recorded between populations growing under patchy and uniform conditions. Plant communities grown from identical seed inocula, with the same overall nutrient supply, provided in different spatial and temporal patterns, differed by up to 44% in total biomass, up to 70% in root biomass, and differed in species composition. These significant effects of heterogeneous resource supply on plants merit further detailed study. We present a framework of predictions of the impacts of different types of spatial heterogeneity in nutrient supply on the performance of single plants, and on plant interactions, plant populations, and plant communities.

Patchy habitats, division of labour and growth dividends in clonal plants.

Natural habitats are patchy in quality. in clonal plants, resource-acquiring structures often occupy sites that differ in quality. Clonal plants can display division of labour in resource-acquisition duties, manifested as local specialization by ramets, which enhances acquisition of each resource from sites of greatest abundance. Physiological integration can re-distribute resources internally from sites of acquisition to clone parts sited where the same resources are scarce. Recent research is showing that such specialization and resource sharing is a highly efficient strategy for acquiring resources and that it can result in considerably greater growth when resources are heterogeneously distributed than when the same quantity of resources is distributed homogeneously.

The effects of nutrient availability on foraging in the clonal herb Glechoma hederacea

(1) The growth forms of genetically identical clones of the perennial herb Glechoma hederacea were compared under three soil nutrient regimes: (i) all ramets were rooted in nutrient-rich sand, (ii) all ramets were rooted in nutrient-deficient sand, (iii) all ramets produced by one primary stolon were rooted in nutrient-rich sand while all ramets produced by the other stolon were rooted in nutrient-deficient sand (split treatment). (2) Clones growing in nutrient-rich sand had short stolon-internodes, copious branching and a rapid accumulation of many large ramets with large leaf-areas. Proportional allocation of dry weight to leaves and petioles was high, whereas allocation to stolons and roots was low. (3) Clones growing in nutrient-poor sand had long stolon-internodes, less frequent branching and a few small ramets with small leaf-areas. Proportional allocation of dry weight to leaves and petioles was low, whereas allocation to stolons and roots was high. (4) Results for the split treatment were intermediate between those of the two singular treatments. There were few significant differences between the half of the split treatment receiving a given treatment and the complete clone receiving the corresponding treatment. Analysis of the split treatment provided no evidence for integration between primary stolons subjected to different nutrient levels. (5) Leaf areas, stolon lengths, number of ramets, stolon branching and dry weight of the primary structures and whole clone increased with clonal age in all treatments. Rate of increase was highest for the nutrient-rich clones, and intermediate in the split treatment clones. (6) The phenotypic plasticity of growth revealed in this experiment may be beneficial since it enables Glechoma hederacea to consolidate its occupation and exploitation of favourable sites (intense foraging), and to pass rapidly through less favourable sites, which may increase the probability of escape into more favourable sites (extensive foraging). The lack of integration between primary stolons may be beneficial in enabling ramets in favourable sites to develop rapidly rather than diverting their accumulated resources to ramets in less favourable areas, which might limit clonal expansion.

The effects of spatial scale of environmental heterogeneity on the growth of a clonal plant: an experimental study with Glechoma hederacea

1) Habitat heterogeneity is manifested as patches differing in quality at a variety of spatial scales, durations or contrasts, but little is known about its effects on the capacity of plants to forage for resources and to grow. This paper investigates the effects of the spatial scale of heterogeneity upon growth of the clonal herb Glechoma hederacea. 2) Clones were grown in eight experimental environments, each containing the same total amount of two types of soil distributed in separate patches. Contrast between patch types was the same in all treatments. The number and size of patches differed between treatments, from two 25-cm × 50-cm patches to 64 6.25-cm × 6.25-cm patches. In six of the treatments roots could grow freely between patches. Partitions prevented root growth between patches in the remaining treatments. 3) Although all treatments provided the same quantity of nutrients, clone biomass was dependent on the scale of heterogeneity. Biomass was highest in the 25-cm × 25-cm patch-size treatment and declined significantly at smaller patch sizes. It varied by a factor of four when only the treatments allowing root growth between patches were compared, and by a factor of seven when the treatments preventing root growth between patches were included. 4) Clones displayed a scale-dependent capacity to locate roots selectively in nutrient-rich patches. Although the proportion of biomass allocated by clones to above-ground structures and roots did not differ significantly between treatments, a significantly greater proportion of the root biomass of clones was located in rich than in poor patches in the larger patch-size treatments, promoting more efficient foraging for nutrients in these treatments. As patch size decreased, the proportion of clone root biomass located in the two patch types became more equal. 5) Root: shoot ratio within clones responded to patch scale and quality. In the larger patch-size treatments, in which clones foraged more efficiently, parts of clones located in rich patches had a higher root:shoot ratio than parts of clones located in poor patches, thus enhancing nutrient acquisition from rich patches. However, G. hederacea behaved like plants with a single rooting point in the smaller patch-size treatments, in that root:shoot ratio increased when nutrients were scarce. 6) Thus, the foraging response of G. hederacea was coarse-grained in environments where patches were large. In comparison, G. hederacea apparently responded to environments with small-scale patchiness as if they were homogeneously poor. It could not adjust its morphology rapidly enough to respond to these less predictable environments where changes in patch quality were more frequent.

Studies on the feasibility of re-creating chalk grassland vegetation on ex-arable land. I. The potential roles of the seed bank and the seed rain

1. This study is an investigation of the potential of the seed bank and the seed rain to promote the re-establishment of chalk grassland vegetation on an ex-arable site which had not been cultivated for 10 years. Comparisons are drawn with the composition of the seed bank as recorded in a study undertaken close to the current site 6 years alter cultivation ceased. 2. The seed bank had the following composition: 46.6% grass seeds, 38.6% perennial forbs, 8.4% biennial forbs and 6.3% annual forbs. In comparison, annual forbs had accounted for 49.5% of the seed bank 6 years after cultivation ceased. The seed bank was concentrated near the top of the soil profile and grass seeds showed a more marked decline in abundance with depth than forb species. However, common annual forb species mostly germinated from the lower soil strata. The common grasses and perennial forbs were species with wide ecological amplitudes, characteristic of fertilized, neutral grassland. 3. Only 20 of the 68 forb species recorded in the seed bank were characteristic components of adjacent ancient chalk grassland. These species accounted for less than 20% of the total forb seed bank. Only two out of 11 recorded grass species were characteristic of the ancient chalk grassland, and these accounted for only 0.3% of all grass seedlings. The grass component of the seed bank was dominated by Agrostis stolonifera. 4. The species richness of the seed bunk has increased in recent years due mainly to acquisition of seeds of non-annuals. However, species characteristic of the ancient chalk grassland have made little contribution either to the seed bank or to the vegetation growing on the site. Those chalk grassland species which were most abundant in the seed bank tended to be short-lived species and they occurred mainly at the margins of the ex-arable site, close to the adjacent chalk grassland. Even here they rarely accounted for more than 20% of the germinable seed bank. They were strongly concentrated at the soil surface, indicating their deposition since cultivation ceased. 5. Agrostis spp., Phleum pratense and Holcus lanatus accounted for over 50% of the recorded seed rain. Of the commonly trapped species, analyses of mean dispersal breadths indicated that forb species characteristic of the adjacent chalk grassland would be comparatively slow invaders of ex-arable habitats. 6. The vegetation on transects across the ex-arable site contained few of the species which occurred in the adjacent old chalk grassland. Chalk grassland species were more abundant in vegetation at the margins of the ex-arable site, but even here similarity indices between the ex-arable vegetation and the chalk grassland vegetation were normally below 25%. 7. The slow invasion of species from the adjacent chalk grassland into this ex-arable site, which is ideally placed for their colonization, suggests that seeds of such species will often need to be artificially introduced to prevent ex-arable sites becoming dominated by fast-growing more weedy species. Further management would also be necessary to prevent more weedy species subsequently invading and eliminating the chalk grassland species.

An analysis of the costs and benefits of physiological integration between ramets in the clonal perennial herb Glechoma hederacea

SummaryThe costs and benefits, measured in terms of dry weight, of physiological integration between clonal ramets, were analysed in two experiments conducted on the clonal herb Glechoma hederacea. Firstly, integration between consecutively-produced ramets was examined in an experiment in which stolons grew from one set of growing conditions (either unshaded or shaded and either nutrient-rich or nutrient-poor) into conditions in which light or nutrient level was altered. Comparisons were made between the dry weight of the parts of the clones produced before and after growing conditions were changed, and the dry weights of the corresponding part of control clones subjected to constant growing conditions. In a second experiment, integration between two distinct parts of G. hederacea clones was investigated. In this experiment clones were grown from two connected parent ramets and the parts of the clone produced by each parent ramet were subjected independently to either nutrient-rich or nutrient-poor conditions. Ramets in resource-rich conditions provided considerable physiological support to those in resource-poor conditions. This was measured as a dry weight gain compared with the weight of the corresponding part of the control clones growing in resource-poor conditions. However, when stolons grew from resource-poor conditions into resource-rich conditions, there was no similar evidence of the resourcepoor ramtes receiving support from resource-rich ramets. Physiological integration did not result in dry weight gains when this would have necessitated basipetal translocation of resources.Because of the predominantly acropedal direction of movement of translocates in G. hederacea, the structure of the clone was important in determining the effectiveness of integration between ramets. Where physiological integration was effective, the cost to the supporting ramets in terms of dry weight was insignificant. Physiological integration allows clones to maintain a presence in less favourable sites with insignificant cost to ramets in favourable sites, thereby reducing the probability of invasion by other plants, and providing the potential for rapid clonal growth if conditions improve. Integrated support of ramets in unfavourable conditions also enables the clone to grow through unfavourable sites, thus increasing the probability of encountering more favourable conditions by wider foraging.

A modular concept of plant foraging behaviour: the interplay between local responses and systemic control

In this paper we examined the notion that plant foraging for resources in heterogeneous environments must involve: (1) plasticity at the level of individual modules in reaction to localized environmental signals; and (2) the potential for modification of these responses either by the signals received from connected modules that may be exposed to different conditions, or by the signals reflecting the overall resource status of the plant. A conceptual model is presented to illustrate how plant foraging behaviour is achieved through these processes acting in concert, from the signal reception through signal transduction to morphological or physiological response. Evidence to support the concept is reviewed, using selective root placement under nutritionally heterogeneous conditions and elongation responses of stems and petioles to shade as examples. We discussed how the adoption of this model can promote understanding of the ecological significance of foraging behaviour. We also identified a need to widen the experimental repertoires of both molecular physiology and ecology in order to increase our insight into both the regulation and functioning of foraging responses, and their relationship with the patterns of environmental heterogeneity under which plants have evolved.