The exploitation of heterogeneity by a clonal plant in habitats with contrasting productivity levels

Transcription

1 Journal of Ecology 1999, The exploitation of heterogeneity by a clonal plant in habitats with contrasting productivity levels DAVID KLEIJN*{ and JAN M. VAN GROENENDAEL{ {Department of Theoretical Production Ecology, Wageningen Agricultural University, PO Box 430, 6700 AK, Wageningen, the Netherlands; and {Department of Ecology, University of Nijmegen, PO Box 9010, 6500 GL, Nijmegen, the Netherlands Summary 1 We investigated habitat exploitation by the rhizomatous grass Elymus repens in a heterogeneous environment in both productive and unproductive habitats. We tested whether there was selective entry of rhizomes into favourable microsites or random exploration of the habitat, and whether the bene ts of selective exploitation were higher in productive than unproductive habitats. 2 Trays were divided into four quadrants around a common central area. Homogeneous environments were created by planting vegetation throughout the trays; heterogeneous environments were created by planting only centre and two opposite quadrants. Contrasting productivity levels were established by fertilizing half of the trays of each environment type. A single rhizome fragment of E. repens was planted in the centre of the trays and allowed to exploit the trays for two growing seasons. 3 Elymus repens e ectively exploited habitat heterogeneity at both productivity levels. However, only unproductive trays showed preferential growth of rhizomes into bare quadrants. 4 In the productive trays individual rhizomes that grew into bare quadrants showed a signi cantly greater production of shoots and total biomass than those that grew into vegetated quadrants. Smaller, non-signi cant e ects were observed at lower productivity. 5 Increased growth of primary rhizomes, once they had entered a bare quadrant, with or without selective growth into these patches, led to similar increases in heterogeneous compared to homogeneous trays at the two productivity levels (3.0 vs. 2.7). Heterogeneity was not therefore more e ectively exploited at high productivity. 6 We suggest that sectorial transport of nutrients through the rhizomes, resulting in directional outgrowth of bud meristems into the bare quadrants, may have been responsible for the selective placement of rhizomes in the unproductive trays. Our results suggest that selective entry of rhizomes into favourable microsites may complement morphological plasticity in enabling rhizomatous plants to forage in heterogeneous environments. Key-words: Agropyron repens, directional meristem outgrowth, Elymus repens, foraging, physiological integration, rhizome, selective ramet placement Journal of Ecology (1999) Introduction In most habitats resources are distributed patchily (Robertson et al. 1988; Smith et al. 1992; Gross et al. *Present address and correspondence: David Kleijn, De partement de Biologie/Ecologie, Universite de Fribourg/ Pe rolles, CH-1700 Fribourg, Switzerland (fax ; David.Kleijn@unifr.ch). 1995). Many plant species can cope with this patchiness by concentrating root or shoot growth in resource-rich areas (Jackson & Caldwell 1989; Campbell et al. 1991; Birch & Hutchings 1994; Hutchings & de Kroon 1994). The production of new shoots and roots by which this is generally achieved, is made possible by the acquisition of resources in the resource-rich patch (St John et al. 1983; Gross et al. 1993). The overall productivity of

2 874 Clonal exploitation of heterogeneity the habitat is believed to be a key factor controlling the way in which a species exploits favourable microsites. In unproductive habitats the net costs involved in producing a new organ may not be o set by the bene ts gained by the plant from that organ, as encounters with favourable microsites (and thus returns) may be too rare to compensate for the investments (Grime 1979; Grime et al. 1986; Crick & Grime 1987; Campbell et al. 1991; Ballare 1994). The bene ts of exploiting favourable patches within a heterogeneous environment by the production of new organs should therefore increase with increasing productivity of the habitat. Plant species that propagate vegetatively through rhizomes or stolons may spread over much larger distances than non-clonal species, so that they may regularly encounter contrasts between favourable and non-favourable patches. Clonal plant species show root and shoot concentration but may have adapted to such variability in growing conditions by also evolving plasticity in ramet placement (Slade & Hutchings 1987a,b; Cain 1994). The production of spacers with shorter internodes and/or increased branching intensities in good patches may result in a concentration of ramets in those patches, thus maximizing acquisition of resources (Hutchings & Mogie 1990). This type of plastic response allows a plant to `forage' for the best microsites within its environment (Slade & Hutchings 1987a,b). Clonal plants that produce rhizomes generally demonstrate less plasticity in response to environmental heterogeneity, particularly in internode length and to a lesser extent in branching intensity, than stoloniferous plants (Schmid & Bazzaz 1992; Dong & de Kroon 1994; de Kroon & Hutchings 1995; Dong et al. 1996). This may be because rhizomes of some species can function primarily as storage rather than foraging structures (Dong & de Kroon 1994). However, Huber-Sannwald et al. (1997, 1998) have recently found that the number of primary rhizomes initiated by a mother plant of Elymus lanceolatus growing in the presence of other species was signi cantly a ected by the identity of its neighbours. Furthermore, MacDonald & Lie ers (1993) found that the rhizomatous grass species Calamagrostis canadensis selectively exploited heterogeneous environments by increased branching intensity and by growing more primary rhizomes into favourable than into unfavourable patches. Such directional outgrowth of primary rhizomes towards resource-rich patches has received little attention, but it may be an important additional mechanism by which rhizomatous species deal with the heterogeneous distribution of resources in their habitat. Elymus repens (L.) Gould (syn. Agropyron repens (L.) Beauv.) is a rhizomatous grass species that, in contrast to most previously studied rhizomatous species (de Kroon & Knops 1990; MacDonald & Lie ers 1993; Evans & Cain 1995; Humphrey & Pyke 1997), is most abundant in fertile, disturbed habitats, where it increases in abundance with increasing productivity (Tilman 1987). Seed production is usually poor and its main mode of reproduction is therefore by rhizomes. Together with other clonal species such as Poa compressa and Trifolium repens, it was found to be an e ective colonizer of dung pats and molehills in pastures (Parish & Turkington 1990). Under these conditions, selective placement of rhizomes could be a highly e cient mechanism for capturing the resources available in resource-rich patches more rapidly, thus creating a competitive advantage over neighbouring plants. Elymus can therefore be used to compare the plasticity in ramet placement in heterogeneous habitats with contrasting productivity levels. We ask whether E. repens exploits heterogeneity in its habitat by selective entry of rhizomes into favourable microsites and thus by selective placement of emerging tillers (which establish a new ramet) in the good patches within a habitat. Subsequent promotion of ramet growth under good conditions might result in an even stronger concentration of biomass in the favourable microsites. However, if interconnected ramets of a single clone remain physiologically integrated (Marshall 1990, 1996) their growth may depend on the distribution of resources over the di erent patches (de Kroon et al. 1998). Responses to establishment in a good patch may range from an enhanced growth of ramets in all patch types (Stuefer et al. 1994) to support of ramet growth in bad patches at the expense of ramet growth in good patches (Salzman & Parker 1985; de Kroon et al. 1998). Such responses may o set any tendency to concentrate clone biomass in the favourable patches. A concentration of plant biomass in favourable microsites could also occur if E. repens rhizomes are placed randomly and rapid growth responses occur in good patches, once they have been encountered. Again, exchange of resources between ramets in physiologically integrated plants may dilute this e ect. The overall productivity of a habitat is likely to determine the extent of the growth response, and the response to habitat heterogeneity may therefore be expected to be larger in more productive environments (Grime et al. 1986; Crick & Grime 1987; Dong et al. 1996). However, it is less clear whether the qualitative mechanisms used to exploit heterogeneity will be the same at di erent productivity levels and this question has rarely been addressed (but see Thompson 1993). We therefore examined both the strategy and the bene ts of selective habitat exploitation by E. repens in productive compared with unproductive habitats.

3 875 D. Kleijn & J.M. van Groenendael Methods THE SPECIES Elymus repens is a rhizomatous, hemi-cryptophytic grass. Its rhizomes consist of a succession of nodes, each bearing a single bud, positioned on alternating sides of the rhizome (1/2 phyllotaxy). In early spring, the tip of each rhizome produces a primary tiller (which may be followed rapidly by secondary tillers) and, once the primary tiller has passed the two-leaf stage, one±four primary rhizomes (HaÊ kansson 1967). Secondary rhizomes are produced only under favourable growing conditions (Palmer 1958), when release of apical dominance of the main meristem allows outgrowth of buds along the primary rhizome (McIntyre 1965, 1967). Few primary or secondary rhizomes produce tillers until the following spring, when a primary tiller from each rhizome supports further growth (HaÊ kansson 1967). This implies that there is a 1-year interval between each generation of ramets. In early April 1995, rhizomes of Elymus were collected randomly from a m patch in a 3- year-old fallow arable eld and divided into twonode sections. Sections of similar size were selected; 24 were used for planting and a further 20 were used to determine initial dry weight (mean 2 SE = g). EXPERIMENTAL DESIGN The experiment was carried out in large trays ( m deep), constructed so that an E. repens plant growing from the middle of the tray in a random direction would have an equal chance of either growing into a compartment with vegetation or growing into a bare compartment (Fig. 1). Wooden partitions divided the trays into four quadrants over the total depth but left an open connection between quadrants in the central m ±2 of the trays. The bottom 0.1 m of the trays was lled with gravel covered with rooting cloth, and a further 0.3 m of topsoil from an unfertilized lawn from which the sod had been removed was then added. Soil type was loamy-sand with a ph of The vegetation was generated by transplanting (on 7 April 1995) seedlings of Holcus lanatus and Rumex acetosa in a regular pattern in the centre and in two opposite quadrants, at a density of 67 plants m ±2 (Fig. 1b). Homogeneous trays, with vegetation in all four quadrants as well as in the centre, served as controls. On the same date a twonode section of Elymus rhizome was planted diagonally in the centre of each tray with the two buds pointing towards the partition separating the north and west quadrants (Fig. 1b), so that Elymus rhizomes had an equal chance of growing into each quadrant. To neutralize potential e ects of di er- Fig. 1 Tray showing partitioning into four quadrants interconnected at the centre. (a) Cross-section of a heterogeneous tray in the middle of the growing season; (b) top-view of such a tray at planting showing the orientation of the rhizome fragment and (dashed lines) where di erent sections were severed at harvest.

4 876 Clonal exploitation of heterogeneity ences in size and shape of quadrants, half the replicates had the east±west quadrants vegetated, and the other half the north±south quadrants. Analysis of the total biomass production of Elymus (averaged over all treatments) in the east±west as opposed to the north±south quadrants showed no signi cant di erences, indicating that quadrant shape did not a ect the results. During the growing season, 90% shade-cloth was used to separate quadrants aboveground and to avoid edge e ects (Fig. 1a). Throughout the experiment the bare quadrants were kept free above-ground of all plants except Elymus, although roots of any of the three species could have grown into these quadrants from the centre. Thus, the heterogeneous trays had contrasting patches where levels of both above- and belowground competition were lower in the bare quadrants than in the centre and in the vegetated quadrants. Above- and below-ground competition was high throughout the homogeneous trays. To produce contrasting productivity levels, half the trays were fertilized by distributing an arti cial NPK fertilizer evenly over the entire tray every 3 months (8 g N m ±2 year ±1 as NO 3 and NH 4, 6.4 g P m ±2 year ±1 as P 2 O 5 and 12.8 g K m ±2 year ±1 as K 2 O) while the other trays were not fertilized. Experiments in the eld had demonstrated that this level of fertilization would raise biomass production by at least 30% (Kleijn & Snoeijing 1997). The trays were placed in four replicated blocks, each with one pair (fertilized and unfertilized) of homogeneous trays and two pairs of heterogeneous trays, giving a total of 24 trays. The experiment was conducted in a greenhouse with partially open sides. Temperature in the greenhouse was somewhat higher than ambient, but followed the normal uctuations well, and 73% of outside radiation reached the plants. The trays were watered as necessary (water was never limiting) and all vegetation in the trays was cut and removed at the end of the rst growing season (September 1995). The daughter ramets that emerged in spring 1996 were then followed to assess their response to conditions in their quadrant during the second growing season. HARVEST The trays were harvested block-wise between 12 and 22 August Above-ground biomass was harvested separately for each quadrant and for the centre. Holcus and Rumex were separated from Elymus. The number of Elymus shoots was recorded for each sampled area. Soil sections were separated by cutting the soil, roots and rhizomes along lines joining the ends of the partitions (dashed lines in Fig. 1b), and the number of rhizomes entering each of the four quadrants was determined. As these predominantly originated directly from the shoot-complex in the centre of the trays, they were called primary rhizomes. Roots and rhizomes were then separated from the soil. The number of rhizome nodes was counted for each quadrant and for the centre of each tray. Dry weight was determined after drying for 48 h at 80 C for the above-ground Holcus± Rumex vegetation, and for shoots, roots and rhizomes of Elymus. As biomass of roots, shoots and rhizomes all closely paralleled total biomass production, only total biomass data are presented. The data from the two bare quadrants within each tray were pooled before analysis, as were the data from the two vegetated quadrants within each tray. DATA ANALYSIS The experimental design was a randomized block design with two levels of heterogeneity (homogeneous and heterogeneous) and two levels of productivity (fertilized and unfertilized). Each of the four replicated blocks consisted of two homogeneous trays and four heterogeneous trays, with the two productivity levels divided equally over the two tray types within each block. Total tray biomass of both the Holcus±Rumex vegetation and the Elymus clones were analysed by means of a two-way ANOVA with unequal replication. If the variance of the response variate was not constant, the data were ln-transformed prior to analysis. The distribution of primary rhizomes, shoots and nodes over bare and vegetated quadrants was analysed by means of a regression analysis that incorporated block e ects (Generalized Linear Regression procedure; GENSTAT 1993). The response of these data was binary: placement of individual rhizomes in either bare or vegetated quadrants. Therefore we used logistic regression to transform the data to a linear scale with the logit function: y 0 = ln( y/(n ± y)), with y being the number of observations in the bare quadrants and n being the total number of observations in a tray (GENSTAT 1993). After analysis for treatment e ects (heterogeneity and productivity), t- tests were used to test whether the mean proportion of rhizomes, shoots or nodes found in the bare quadrants was signi cantly di erent from the 50% that would have indicated a random distribution, and thus suggested selective placement. No signi cant deviation from 50% indicated random placement. To check whether the observed distribution of Elymus ramets was due to systematic e ects other than the treatments, the homogeneous trays were analysed in a similar fashion. For this purpose vegetated quadrants that had the same orientation as the bare quadrants in the heterogeneous trays within their replicated block were labelled `pseudo-bare quadrants'. Physiological integration could possibly o set the concentration of Elymus biomass in the bare quad-

5 877 D. Kleijn & J.M. van Groenendael Table 1 Mean above-ground biomass production (2 SE) of the Holcus lanatus±rumex acetosa vegetation in homogeneous and heterogeneous trays at two productivity levels (in g m ±2 ). The homogeneous trays were replicated four times, the heterogeneous trays eight times. Pseudo-bare quadrants were the vegetated quadrants in the homogeneous trays that had the same orientation as the bare quadrants in the heterogeneous trays. Only total tray data were analysed by means of ANOVA followed by LSD tests; di erent characters indicate signi cant di erences (P < 0.05) Low productivity High productivity Tray type Homogeneous Heterogeneous Homogeneous Heterogeneous Pseudo-bare quadrants Centre Vegetated quadrants Total tray 432 a a c b 2 65 rants, because it implies sharing of resources between ramets growing in vegetated and bare quadrants. Physiological integration would therefore result in ramets growing in vegetated quadrants being signi cantly larger when they are connected to other ramets growing in bare quadrants than when they are connected to ramets that grow in vegetated quadrants. Thus, to test whether physiological integration had any signi cant e ect upon distribution of clonal biomass, we compared biomass of (i) primary rhizomes growing in vegetated quadrants but connected via the mother-plant with primary rhizomes growing in bare quadrants; (ii) those growing in vegetated quadrants but connected to those growing in vegetated quadrants; and (iii) those in bare quadrants connected to those in vegetated quadrants. Half of the heterogeneous trays were randomly assigned to be analysed for connection type 1, and half for connection type 3, to yield a randomized complete block design with four replicated blocks, two productivity levels and three rhizome connection types. Data were analysed by means of a two-way ANOVA. When signi cant treatment e ects were found, means were tested for signi cant di erences using LSD tests. Signi cantly higher mean biomass production of type 1 primary rhizomes compared with type 2 primary rhizomes would indicate signi cant e ects of physiological integration. Results Biomass of the Holcus±Rumex vegetation was significantly greater in the high than in the low productivity treatments (Table 1). Thus, the application of fertilizer produced vegetation that contrasted signi cantly with respect to productivity. In the homogeneous trays, productivity of the pseudo-bare (the vegetated quadrants in the homogeneous trays that had the same orientation as the bare quadrants in the heterogeneous trays) and the vegetated quadrants was similar, con rming that a homogeneous environment was available for the Elymus plants. In the heterogeneous trays, the contrast between the bare and the vegetated trays was much more pronounced in the more productive trays (0±834 vs. 0± 639 g m ±2 ). Productivity in the centre of the trays was much higher than in vegetated quadrants, possibly because root and shoot systems of these plants could expand radially along the partitions. They may therefore have had more growing space than plants growing in the quadrants whose expansion would be restricted when they reached the partitions or the sides of the tray. In the heterogeneous trays central plants were also able to grow roots into bare quadrants. The primary rhizomes, and subsequently the shoots, of Elymus were found predominantly in the north and west quadrants, in correspondence with the initial north-west orientation of the buds (Table 2 and Fig. 1). This growth bias did not invalidate the further analysis of treatment e ects because the rhizomes still had an equal chance of encountering a bare or a vegetated quadrant, with half the heterogeneous trays having a bare north quadrant and a vegetated west quadrant and the other half the reverse pattern. Table 2 Distribution of primary rhizomes and number of shoots of Elymus repens over the four quadrants within all 48 trays Quadrant orientation North West South East Centre Number of primary rhizomes ± Number of shoots

6 878 Clonal exploitation of heterogeneity Fig. 2 The mean distribution of Elymus repens ramets (2 SE) over (pseudo-)bare (open bars) and vegetated quadrants (hatched bars) at the end of the second growing season. Clones were grown in homogeneous (n = 4) and heterogeneous trays (n = 8) at high and low productivity levels. (a) Number of primary rhizomes; (b) number of nodes; (c) number of shoots; and (d) total biomass (g). Arrows indicate values for completely random (50% in vegetated quadrants, 50% in bare quadrants) distributions from which signi cant deviations are shown (*P < 0.05, **P < 0.01). For explanation of pseudobare see Table 1. The standard error was obtained from analysis of logit-transformed data. The means 2 SE were backtransformed to the normal scale before they were presented graphically. This results in asymmetric error bars. The placement of primary rhizomes by Elymus in the bare and vegetated quadrants deviated signi cantly from random only in the unproductive heterogeneous trays (Fig. 2a; t 16 = 2.143, P = 0.049). In these trays a signi cantly higher proportion of primary rhizomes had grown into the bare quadrants, indicating selective entry of rhizomes into the more favourable environment. The homogeneous trays at the same productivity level showed an even distribution of primary rhizomes between quadrants. Although in the productive trays placement of rhizomes appeared strongly biased towards the vegetated quadrants, this was not signi cant, even for the heterogeneous trays. In all but the productive heterogeneous trays, the distribution of the number of nodes and shoots and the total biomass of Elymus re ected that of the primary rhizomes (Fig. 2b±d). In unproductive heterogeneous trays, nodes, shoots and total biomass were even more clearly concentrated in the bare quadrants than the primary rhizomes, and the e ect was highly signi cant in all cases (nodes: t 16 = 3.234, P = 0.006; shoots: t 16 = 3.529, P = 0.004; biomass: t 16 = 3.263, P = 0.006). In the productive heterogeneous trays, although none of the di erences was signi cant, more nodes, shoots and biomass were produced in

7 879 D. Kleijn & J.M. van Groenendael Fig. 3 Characteristics of Elymus repens rhizomes at the end of the second growing season. (a) Mean number of nodes; (b) mean number of shoots; and (c) mean biomass (g) per primary rhizome (2 SE) in (pseudo-)bare (open bars) and vegetated quadrants (hatched bars). Arrows indicate the average value for nodes, shoots or biomass of all four quadrants within a tray, asterisks indicate a signi cant deviation the average value (*P < 0.05, **P < 0.01). bare quadrants, the reverse of the e ect on rhizomes. This suggests that, especially in the productive heterogeneous trays, there was a further pronounced response after placement of primary rhizomes into a particular quadrant type. For an individual primary rhizome the average biomass, and number of nodes and shoots, did not di er signi cantly between vegetated and bare quadrants in the unproductive heterogeneous trays but did so in the productive heterogeneous trays (Fig. 3a±c; nodes: t 16 = 3.394, P = 0.005; shoots: t 16 = 2.750, P = 0.015; biomass: t 16 = 3.309, P = 0.006). Each node could in theory produce branches and shoots but the proportion that did so was not signi cantly di erent between the vegetated and bare quadrants (Fig. 4). This indicated that the signi cantly higher number of shoots per primary rhizome in the productive heterogeneous trays was not the result of increased branching but of a growth response that resulted in more ramets with the same clonal architecture. Thus, while the increased biomass production in favourable quadrants of heterogeneous trays is primarily due to selective placement of ramets when productivity is low, it is the result of increased growth of ramets after placement in these quadrants when productivity is high. No evidence was found to indicate that the distribution of Elymus biomass was in any way a ected by physiological integration between ramets in dif-

8 880 Clonal exploitation of heterogeneity Fig. 4 The percentage of Elymus repens nodes that produced shoots in (pseudo-)bare (open bars) and vegetated quadrants (hatched bars) at the end of the second growing season. Clones were grown in homogeneous (n = 4) and heterogeneous trays (n = 8) at high and low productivity levels. Arrows indicate the average percentage of all four quadrants within a tray. No signi cant di erences were found. See Table 1 for explanation of pseudo-bare. Fig. 6 Mean total biomass production (g) per tray of Elymus repens in homogeneous (n = 4) and heterogeneous trays (n = 8) at high and low productivity levels. E ects of productivity level on the ratio of dry weight in homogeneous and heterogeneous trays were analysed by ANOVA; no signi cant di erences were found. Bars: black, roots; diagonally hatched, rhizomes; open, shoots. ferent patches. At both productivity levels, mean biomass of primary rhizomes in the vegetated quadrants connected via the mother-plant to rhizomes in bare quadrants was similar to that of primary rhizomes connected via the mother-plant to rhizomes in vegetated quadrants (Fig. 5). Mean primary rhizome biomass was higher in bare quadrants but this was signi cant only in the unproductive trays (Fig. 5). In unproductive trays, mean total biomass of Elymus was 3.01 times greater in heterogeneous than in homogeneous trays. In productive trays this ratio was 2.67 (Fig. 6) but these ratios were not signi cantly di erent. This suggests that the exploitation of heterogeneity by Elymus was equally e ective in productive and unproductive trays. Fig. 5 Mean biomass (g 2 SE) of primary rhizomes that grow in one type of quadrant but that are connected to primary rhizomes growing in another type of quadrant. Di erences in mean biomass were analysed by ANOVA, followed by LSD tests; di erent characters indicate signi cant di erences (P < 0.05). The standard error was obtained from analysis of ln-transformed data. Discussion Elymus repens exploits heterogeneity by growing rhizomes selectively into the favourable microsites of a patchy environment. In the unproductive heterogeneous trays, mother plants were able to grow signi cantly more primary rhizomes into bare quadrants than into vegetated quadrants despite the fact that they had immediately adjacent vegetation on all sides. This ability of a plant to anticipate qualitative di erences in its proximate environment may increase the e ciency of habitat exploitation (Aphalo & Ballare 1995; Sachs & Novoplansky 1997). A tiller emerging from the central vegetated zone into a bare patch will be self-supporting more rapidly and will grow more vigorously as competition for light and nutrients is less intense. Thus, investment costs of ramets placed in vegetation gaps are lower and returns are higher. When planted at the edge of a vegetated and a bare compartment, another rhizomatous grass species, Calamagrostis canadensis, grew signi cantly more rhizomes into

9 881 D. Kleijn & J.M. van Groenendael the bare section than the vegetated section (MacDonald & Lie ers 1993). It was also found that rhizomes growing in vegetated compartments had a signi cantly higher number of branches per rhizome, but growth and morphological responses were not distinguished. In contrast with foraging theory, which predicts that branching will increase in favourable patches, Huber-Sannwald et al. (1997) found that more rhizomes of E. lanceolatus branched when in contact with a neighbouring Pseudoroegneria spicata plant than when they were growing free of contact. However, when grown with Agropyron desertorum, contact had no signi cant e ect on branching frequency. The present study failed to nd any signi cant di erence in the proportion of nodes producing shoots between the vegetated and bare quadrants within a tray. This ratio may be considered a measure of branching intensity (de Kroon & Knops 1990). Although the other potential morphological response that may aid a clonal plant to acquire limiting resources, plasticity in internode length, was not investigated, our results suggest that such responses may not be necessary. Selective ramet placement can instead be achieved by outgrowth of meristems selectively towards good patches. The selectivity in rhizome entry depended on the productivity of the habitat. In the productive heterogeneous trays, Elymus rhizomes were sent out randomly by the mother-plant despite their larger contrast in above-ground vegetation (Table 1), suggesting that below-ground contrasts played a crucial role. The root biomass of the Holcus±Rumex vegetation was much lower in the unvegetated quadrants (D. Kleijn, personal observations) than in the vegetated quadrants, and nutrient resources must therefore have been depleted more extensively in the vegetated quadrants (Nye 1966; Bhat & Nye 1973; Yanai et al. 1995). This would have created a perceptible contrast, but because both the bare and the vegetated quadrants were fertilized every 3 months, this may have been neutralized repeatedly for a period of time in the productive trays. The absence of selective rhizome entry may thus have been an unanticipated side-e ect of the fertilizer application. Shoot and biomass production per primary rhizome within the quadrants did, however, di er between quadrants of the high productivity trays, indicating the existence of an ecologically meaningful contrast. The results are in line with the hypotheses of de Kroon & Schieving (1990) and de Kroon & Hutchings (1995) that, in productive habitats, clonal species exploit their environment predominantly by continuous, random exploration with their stolons or rhizomes, combined with rapid growth responses of individual ramets once a favourable patch has been encountered. Furthermore, foraging responses, such as selective entry of rhizomes into favourable microsites, may only be bene cial when favourable microsites are predictable in time and space (Oborny 1994). In productive habitats, favourable patches generally do not persist for long (Grime et al. 1986) and selective placement of rhizomes may be too slow to have signi cant e ects. The higher net returns for a rhizome entering a bare quadrant in productive compared with unproductive trays (Fig. 3) is in line with the hypothesis (Grime 1979, 1994) that investments in foraging organs are more likely to be repaid in productive than in unproductive habitats. However, in this case, because of the lower number of rhizomes placed in the bare quadrants in the productive trays, the net bene t to the whole plant of exploiting habitat heterogeneity was no greater in high than low productivity habitats. The relative biomass increase was similar at both productivity levels (Fig. 6), indicating that heterogeneity was exploited equally well. Foraging responses at the root level, such as an increased root length density in the more favourable patches (Fransen et al. 1998), may have played a role in the exploitation of bare quadrants in the productive heterogeneous trays. These results indicate that, when examining the foraging responses of clonal plants, it is important to determine responses both at the ramet level and at the root and shoot level, as each may act at di erent spatial or temporal scales. No evidence was found for support of ramets in vegetated quadrants by connected ramets in bare quadrants. Although this study was not designed to test whether di erent rhizomes were physiologically integrated, the results do suggest that clonal integration had no signi cant e ect on distribution of biomass between good and bad patches for interconnected Elymus ramets. The patch scale used in our experiment corresponds with that often encountered by Elymus in the eld. The results agree with those of Forde (1966) and Rogan & Smith (1974) with respect to transport of assimilates, that mature Elymus plants can be regarded as an association of largely independent units or modules each consisting of an established tiller. Studies of translocation of assimilates in connected tillers demonstrated that transport of 14 CO 2 from one tiller through the rhizome to the next tiller occurred only after repeated defoliation of the second tiller, irrespective of it being the younger or older tiller. This pattern of largely independent units under normal conditions, and re-integration under extreme conditions, has been observed in other clonal species (Price et al. 1992; Marshall 1996). Such independent growth of di erent connected plant parts facilitates a rapid concentration of plant biomass in favourable patches (de Kroon & Schieving 1990), irrespective of selectivity in ramet placement.

10 882 Clonal exploitation of heterogeneity The mechanism that triggered the selective placement of primary rhizomes in bare quadrants may have been sectorial transport of nutrients. Sectoriality implies that buds arrayed in a common orthostichy, or rank (which therefore have a similar orientation), are connected to each other by common vascular bundles (Watson & Casper 1984). Sectoriality in clonal plants has been well documented for members of the Lamiaceae (Murphy & Watson 1996; Price et al. 1996) but grasses are generally not considered to be sectorial (Watson & Casper 1984; Pitelka & Ashmun 1985; Marshall 1996). However, preliminary results from a study using fuchsin dye to examine xylem transport in unstressed and unbranched Elymus rhizomes did suggest predominantly sectorial transport (D. Kleijn, unpublished results) and the 1/2 phyllotaxy of Elymus rhizomes means that buds are orientated alternately on opposite sides of the rhizome. The extra nutrients obtained by roots growing into the bare quadrant may have been restricted to vascular bundles on the bare quadrant-facing side of the rhizome. Because nitrogen releases buds from dormancy (McIntyre 1965; Leakey et al. 1977; Qureshi & McIntyre 1979), only buds on this side of the rhizome may have grown out. Therefore, we hypothesize that directional meristem outgrowth, caused by sectorial transport of nutrients, may have been responsible for the observed selective placement of primary rhizomes in the bare quadrants. Such a mechanism may in general provide those clonal plants that have a limited number of meristems per ramet (e.g. Trifolium, Glechoma, Hydrocotyle, Poaceae) with the means to direct rhizomes or stolons towards favourable patches once they have been detected. However, there is clearly a need for experiments that verify this hypothesis, as there is currently little information in the literature that may be used to test it. In conclusion, we have demonstrated that the rhizomatous grass species E. repens is able to exploit spatially heterogeneous habitats by selective entry of rhizomes into the favourable microsites within its environment. The response of this clonal plant to heterogeneity depended upon the productivity level of the habitat, which suggests that the overall productivity level of an environment may be important in determining the type of response exhibited. A clonal plant growing in a productive environment may experience a given increase in resource supply when moving from a bad to a good patch in a di erent way than a plant growing in an unproductive environment. It is therefore important that experiments examining the morphological responses of plants are performed at productivity levels that are in accordance with those in their natural habitats. 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