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Ecology |
Smithsonian Environmental Research Center, P.O. Box 28, Edgewater, Maryland 21037 USA
Received for publication February 1, 2000. Accepted for publication September 19, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: clonal plants • environmental heterogeneity • foraging • patch selection • Uvularia perfoliata • Uvularia puberula • Uvularia sessilifolia.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Simulation models of clonal plants predict that foraging can be aided by other morphological changes in plagiotropic stems such as stolons and rhizomes in response to patch quality (Sutherland and Stillman, 1988
; Cain, 1994
; Oborny, 1994
). Increased branching frequency and shortening of internodes in favorable patches can position ramets, which contain resource-acquiring organs, more effectively for maximizing resource uptake. Conversely, suppression of branching and the lengthening of internodes in unfavorable patches may promote escape from such patches. However, these morphological changes may contribute largely to the fine-tuning of the foraging response rather than being obligatory for its expression. For example, although there is a consistent increase in branching of plagiotropic stems in response to resource-rich patches, internode length is relatively unresponsive to patch quality even when there is selective placement of organs (Hutchings and de Kroon, 1994
). The unresponsive nature of internodes may allow clones to explore their environments continuously. When high-quality patches are located, they are exploited by means of localized morphological adjustments in leaves and roots (de Kroon and Hutchings, 1995
).
Plagiotropic stems perform multiple functions. In addition to supporting ramets, these stems are reservoirs of meristems and storage products (Jónsdóttir and Watson, 1997
). When storage is their primary function, plagiotropic stems do not show architectural plasticity in the way predicted by simulation models (de Kroon and Knops, 1990
; Dong and de Kroon, 1994
). Instead, the pattern of branching, internode elongation, and biomass allocation in these stems appears to be an outcome of resource acquisition rather than a means of selecting favorable patches ("passive" growth vs. "active" foraging; Cain, 1994
). Therefore, in order to understand the ability of these species to exploit heterogeneous habitats, a careful distinction has to be made between growth and foraging responses. De Kroon and Hutchings (1995)
have suggested that a suitable null model for foraging is that resource availability affects biomass accumulation (growth) without accompanying selective distribution of resource-acquiring organs in high-quality patches (foraging). However, while there is evidence that some fast-growing species may forage for resources by selective placement of leaves or roots in high-quality patches (e.g., Wijesinghe and Hutchings, 1996
; Einsmann et al., 1999
), other species may acquire patchy resources by physiological adjustments in uptake rather than by morphological adjustments in resource-acquiring organs (e.g., Jackson and Caldwell, 1996
; Fransen, de Kroon, and Berendse, 1998
).
An important attribute of clonal plants that modulates the foraging response is physiological integration of ramets. Numerous studies have shown that neighboring ramets in integrated clones share resources (see review by Jónsdóttir and Watson, 1997
). Thus, physiological integration can mitigate local shortfalls in resources experienced by individual ramets, resulting ultimately in an "averaging" of the habitat patchiness experienced by the entire clone (Pitelka and Ashmun, 1985
; Jónsdóttir and Watson, 1997
; Marshall and Price, 1997
). There is great variation among clonal plants in the duration of physical connections or physiological integration between ramets. Jónsdóttir and Watson (1997)
recognized several categories of integration patterns, ranging from "disintegrators" (or "genet splitters" sensu Eriksson and Jerling, 1990
) with ramets that become independent soon after birth to "integrators" with large, fully integrated ramet systems maintained for many seasons. There are two contradictory views of the influence of physiological integration on foraging. Some authors have suggested that integration enhances foraging efficiency (e.g., Hutchings and Slade, 1988
; Evans and Cain, 1995
). However, de Kroon and Schieving (1990)
have suggested that clones with physiologically autonomous ramets should be more effective at searching for high-quality patches than highly integrated clones, which tend to linger in unfavorable patches as a result of subsistence from ramets in favorable patches. Thus, this view implies that disintegrators or clones with restrictive patterns of integration (sensu Jónsdóttir and Watson, 1997
) should show a stronger foraging response in heterogeneous environments than fully integrated clones.
In this paper, we present a study that compared the ability of three closely related woodland species to forage and explore patches in nutritionally heterogeneous environments by means of morphological plasticity. Our first objective was to determine whether or not the foraging response in clonal species, i.e., selective placement of roots in favorable patches, was accompanied by other morphological changes conducive for foraging. The second was to determine whether or not the species differed in foraging ability depending on the extent of physiological integration. Our third objective was to determine how variability in environmental quality influenced the performance of the three species irrespective of their foraging abilities. The order in which high- and low-quality patches are encountered by a plant (patch configuration) can have a significant effect on its overall performance (Wijesinghe and Hutchings, 1996
). In this study, biomass was greater when plants grew in environments with contiguous high-quality patches or when plants grew from high- to low-quality patches than when they grew from low- to high-quality patches.
We selected three species belonging to the genus Uvularia (U. perfoliata, U. puberula, and U. sessilifolia), which differ in type and function of plagiotropic stems and the extent of physiological integration. Harvey and Pagel (1991)
have suggested that comparisons of congeners should be highly informative because all variables in common to the species under consideration are automatically held constant. An additional feature of this study is that all three species occur in woodland habitats where resource availability is both temporally and spatially variable (Hicks and Chabot, 1985
; Chazdon, 1988
; Lechowicz and Bell, 1991
; Zak and Grigal, 1991
).
We tested the following hypotheses. Hypothesis 1: All three species should show preferential location of roots in high-nutrient soil patches, i.e., all three species should forage actively. Hypothesis 2: Clonal species of Uvularia should show architectural changes in response to nutrient availability that are theoretically predicted to facilitate foraging. Stolons or stolon internodes should be shorter, and rhizome branching and ramet density should be greater in high- than in low-nutrient patches, whereas rhizome internode length should not respond to patch quality. Hypothesis 3: The ability to locate and exploit nutrient-rich patches should increase with increasing degree of physiological integration. Conversely, if physiological integration limits foraging efficiency, the ability to locate and exploit nutrient-rich patches should decrease with increasing degree of physiological integration. Hypothesis 4: For all three species, the order in which high- and low-quality patches are encountered would affect performance. Yield and estimators of fitness should be greater in treatments where more high-quality patches are encountered consecutively than in treatments where fewer high-quality patches are encountered consecutively during growth.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Hayashi et al., 1998
). They are deciduous, spring-flowering forest understory perennials and most show some form of clonal growth. All species typically produce only one flower per shoot. Seeds are shed in late summer and dispersed by ants (Whigham, 1974
). The aerial shoots die back in autumn, leaving only the belowground structures to overwinter. The nomenclature of the species used in this study follows that of Wilbur (1963)
.
U. perfoliata L
Each plant (parent ramet) bears a single aerial shoot and a cluster of fleshy storage roots arising from a short caudex (<1 cm long). These roots are replaced annually. Individuals in patches propagate clonally by producing one or two offspring ramets per season (Wijesinghe and Whigham, 1997
). Each offspring ramet consists of a shoot bud and a cluster of storage roots borne at the tip of a slender, unbranched, subterranean stolon (<2 mm in diameter). The stolon grows centrifugally from the caudex of the parent and is, on average, 20 cm in length. The offspring ramet separates from its parent and becomes fully independent sometime during autumn or early winter of the year of its birth when the connecting stolon decays. Thus, the stolon is not important for long-term storage, but acts more as a conduit between parent and offspring for transfer of carbon and mineral nutrients. The offspring is fully dependent on the parent for photosynthates during the year of its birth, since its bud develops into an aerial shoot only in the following year. In addition to the aerial shoot, the offspring may also produce up to two third-generation ramets in its first year of independent life (Wijesinghe and Whigham, 1997
). The third-generation ramets develop from lateral buds initiated in the previous growing season. Although the production of offspring ramets lessens the likelihood of survival of the parent, some parent ramets can persist for at least 3 yr and continue to produce offspring (Wijesinghe and Whigham, 1997
). This species can be categorized as a disintegrator because the longevity of its physiological ramet connections is similar to its ramet generation time (see Jónsdóttir and Watson, 1997
).
U. sessilifolia L
Each plant consists of several aerial shoots arising from a sympodially branched, fleshy, subterranean rhizome system that stores resources over the long term. During the growing season, up to two new rhizome branches (on average 
10 cm long), each of which bears an upright bud, are produced from the base of each shoot. These buds develop into aerial shoots the following spring. Each new branch also bears between 2 and 10 fleshy roots, usually at the distal half of the branch. In contrast to the aerial shoots, the rhizome system is perennial and will remain intact for several seasons. New aerial shoots are formed at the distal, growing edge of the rhizome system, which has a roughly fan-shaped "zone of occupation" (sensu Angevine and Handel, 1986
; see also Geber, de Kroon, and Watson, 1997
). In contrast, roots are formed on both young and old segments of the rhizome. This species is an integrator because the longevity of its physiological ramet connections is greater than ramet generation time (see Jónsdóttir and Watson, 1997
).
U. puberula Michx
This species is not clonal. Each plant produces several aerial stems that arise in a clump from a caudex that is 1 cm long (Wilbur, 1963
) and bears a cluster of fleshy, sparsely branched roots. The roots, which can persist for more than one season, function as nutrient-acquiring, exploratory, and storage organs. At the end of each growing season, new buds are formed on the caudex, some of which may develop into shoots the following spring.
The experiment
The experiment was conducted in a shadehouse at the Smithsonian Environmental Research Center in Edgewater, Maryland, USA. The three species were collected in September 1993 from natural populations in Maryland and Virginia and planted in experimental arenas. A single plant was placed in each arena which was a circular area 60 cm in diameter with its perimeter delimited with plastic lawn edging (Fig. 1). It was filled to a depth of 10 cm with two substrates in different patterns depending on treatment. The nutrient-rich substrate was peat-based potting compost enriched with a slow-release granular fertilizer, Osmocote 13-13-13 (with a 1:1:1 ratio of N, P, K released over 8–9 mo; Scotts-Sierra Horticultural Products Company, Marysville, Ohio, USA), mixed in a ratio of 2 g per 1 L of compost. The nutrient-poor substrate was Turface® (AIMCOR, Deerfield, Illinois, USA), a granular clay material that can be used as an inert potting medium for plants. It has good water-holding capacity but does not provide any mineral nutrients for plant growth. The arenas were assembled on three 1.5 x 15 m raised beds, the surfaces of which were first covered in plastic sheeting with holes cut out for drainage. The gaps between the arenas were filled with chipped bark. Each species was allocated its own bed. All beds were similar in the amounts of light and water received.
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In each replicate containing U. perfoliata, a single ramet, newly produced in the summer of establishing the experiment, was planted in the center of the arena. In replicates with U. sessilifolia, rhizome segments 10 cm long, with a single bud at the tip, were used. These rhizomes were also newly produced in the summer. In this case, one rhizome segment was planted in each arena with the bud positioned directly in the center. For each replicate of U. puberula, a cluster of roots with one or more shoot buds was planted with the buds positioned in the center of the arena. For all three species, the fresh mass of the material used was determined before planting.
Plants in all treatments were provided, throughout the growing season, with 20% of ambient full daylight. This corresponded to average light levels observed in canopy gaps in woodlands where Uvularia species occur. The plants were watered regularly with tap water. The experiment was continued for two growing seasons. At the end of the 1994 growing season, the substrate was removed from the surface of each arena in order to expose belowground structures of the plants while taking care not to disturb them. These structures were mapped, and the number and distribution of roots in each patch were recorded. The presence of new shoot buds or offspring ramets was also noted. The substrate was then replaced and plants were allowed to continue growth for another season. In April of 1995, the compost patches in each treatment were enriched for a second time with Osmocote granules applied in the same concentration as the year before. The granules were gently worked into the top layer of compost in each patch taking care not to disturb the plants. At the end of the 1995 growing season, data were recorded as in the previous year before shoots and belowground structures were harvested separately from the areas designated as patches 1, 2, and 3 in each treatment (see Fig. 1). Biomass samples were dried at 80°C to a constant mass.
Data analysis
For each species, biomass, architectural traits, and estimators of fitness were analyzed using one-way analyses of covariance (ANCOVA) with the soil heterogeneity treatment as the main factor. Architectural traits were analyzed only for the two clonal species, and the traits used were stolon length for U. perfoliata and the number of branches and internode length for U. sessilifolia. Estimators of fitness used were genet size for U. perfoliata and the size of the bud bank for U. sessilifolia and U. puberula. These are suitable measures of fitness because the number of independent ramets comprising a clone is an indicator of its capacity for risk spreading and persistence (Cook, 1979
), while the size of the bud bank is a measure of the future capacity of plants to respond to environmental heterogeneity (Watson, Hay, and Newton, 1997
). The distribution of belowground structures of U. perfoliata and U. sessilifolia in patches 1, 2, and 3 (see Fig. 1) was analyzed using one-way multivariate analysis of covariance (MANCOVA). Fresh biomass of the material used to set up the experiment in 1993, i.e., ramet, root cluster, or rhizome segment, was used as the covariate for tests of each species. Data were transformed, when necessary, using log or angular (in the case of proportions) transformations to correct for non-normality and heteroscedasticity.
The preferential location of roots (foraging) in the three species was examined in greater detail using the distribution of roots of each species in patches 1, 2, and 3 of the heterogeneous treatments A and B. Only the 1995 data were used since the belowground structures of two of the species (U. perfoliata and U. sessilifolia) had not extended as far as patch 3 in 1994. The nonparametric Mann-Whitney U test was used to compare the proportion of the total number of roots and of root biomass distributed in each patch in the two treatments. Patch 1 in both treatments is nutrient rich (Fig. 1). In treatment A, patch 3 is also nutrient rich and foraging roots have to traverse the nutrient-poor patch 2 to reach it. In treatment B, patch 3 is nutrient-poor and foraging activity should be more confined to the inner nutrient-rich area of patches 1 and 2 (Fig. 1). Thus, if plants are actively foraging, placement of roots in patches 1 and 3 should be significantly greater in treatment A than in treatment B. The analyses of root number and of root biomass gave similar results, therefore only the former are presented.
Foraging abilities of the three species were compared by examining the overall distribution of roots in rich patches in treatment A. The proportion of the total number of roots distributed in rich patches (patches 1 + 3) of treatment A was compared between the three species using the nonparametric Kruskal-Wallis test. In addition, the pattern of patch use by each species was examined. A "patch use ratio" (PUR) was calculated for each species as follows:
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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In U. puberula, there were some differences in root proliferation between treatments, with plants in treatment D producing significantly fewer roots than plants in the other treatments in 1994 (Table 1). However, these differences had disappeared by 1995. In this year, root placement was significantly different between treatments A and B, indicating selectivity (Fig. 2c). In treatment A, >70% of the roots were located in patch 1 compared to only 41% in treatment B (Mann-Whitney U test: U = 87, P < 0.01). Conversely, in treatment B, 54% of roots were located in patch 2 compared to only 25% in treatment A (Mann-Whitney U test: U = 10, P < 0.01). Plants in both treatments mostly exploited the central area (patches 1 + 2) of the arenas, while there was very little exploration of patch 3. A similar proportion of roots was placed in this patch in both treatments (Mann-Whitney U test: U = 48, P = n.s.; Fig. 2c).
Hypothesis 2: facilitatory morphological changes
In both 1994 and 1995, U. perfoliata stolon length did not differ between treatments (Table 1). For 1994 this was the predicted result, since the parent ramets occupied nutrient-rich patch 1 in all cases. However, by 1995 the majority of parent ramets in treatments A and D were occupying nutrient-poor patch 2, whereas the majority of their counterparts in treatments B and C were occupying nutrient-rich patch 2 (Fig. 1). The expectation that stolons of U. perfoliata in treatments B and C should be shorter than stolons of A and D was not confirmed for 1995. The distribution of ramets also did not conform to the predictions. If ramets are positioned in nutrient-rich patches to maximize acquisition, the expected distributions should be D > A > B 
C for patch 1, B C > A D for patch 2, and A > C > D B for patch 3. However, ramet distribution in the three patches was essentially similar for all treatments (MANCOVA of the proportion of ramets in patches 1, 2, and 3 in 1995: Wilks' Lambda = 0.68, F9,78 = 1.51, P = n.s.; for univariate tests see Table 2).
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Hypothesis 3: relative foraging abilities
The proportion of roots located in high-quality patches in treatment A was greatest in U. puberula and least in U. sessilifolia, with U. perfoliata in an intermediate position (Kruskal-Wallis test: the proportion of roots in nutrient-rich patches, H = 10.79, P < 0.01; Fig. 3a). However, the PURs reveal that U. puberula and U. perfoliata made use of different favorable patches (Kruskal-Wallis test: PUR for patch 1, H = 5.92, P < 0.05; PUR for patch 3, H = 6.69, P < 0.05; Fig. 3b). Uvularia puberula overutilized patch 1 and U. perfoliata overutilized patch 3 in treatment A relative to their use of the same patches in treatment B. Uvularia sessilifolia used the two patches in a similar manner in both treatments, confirming the earlier results obtained for the analyses of selective placement of roots (Fig. 2b).
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There was no treatment effect in both years on the estimator of fitness, i.e., clone size measured as the total number of ramets comprising each clone, of U. perfoliata (ANCOVA: 1994, F3,34 = 0.69, P = n.s.; 1995, F3,34 = 1.41, P = n.s.; Fig. 4a). In 1994, clones in all treatments consisted of approximately two ramets. This number increased to 5–6 ramets at the end of 1995 (Fig. 4a). Although clones in all treatments were of similar size, there was a significant impact of treatment on the survivorship of older ramets. By the beginning of the growing season in 1995, 56 and 50% of the replicates in treatments D and A, respectively, had lost the original ramets used in the set-up of the experiment, while none of the replicates had lost these ramets in treatment C (4 x 2 contingency table: df = 3, G = 11.91, P < 0.01; Fig. 5). Thus, in treatment C, nearly all replicates consisted of three overlapping generations of ramets, i.e., the original first generation ramet, second generation ramets (the cohorts produced in 1994 and 1995 by the original ramet), and third generation ramets (those produced in 1995 by the 1994 cohort). In contrast, in 1995, the majority of the replicates in treatments D and A consisted of only second and third generation ramets (Fig. 5).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). In U. perfoliata, selective placement of roots in high-quality patches occurred without accompanying changes in stolon length or ramet density. Some authors have suggested that plagiotropic stems should show little plasticity in response to resource availability compared to orthotropic stems (de Kroon and Hutchings, 1995
; Huber, 1996
; Stuefer, 1996
). Plagiotropic stems growing in the horizontal plane would encounter both heterogeneously and unpredictably distributed light and edaphic resources, whereas the availability of light for orthotropic stems growing in the vertical plane would be, although heterogeneous, much more predictable (Huber, 1996
; Stuefer, 1996
). It is thought that plasticity is unlikely to be adaptive in heterogeneous environments if those environments are also unpredictable (Scheiner, 1993
; Stuefer, 1996
).
Relative foraging abilities
Uvularia puberula showed greater capacity than the other two species for positioning roots in high-quality patches of heterogeneous environments. However, this species exploited only those patches nearest to it (Fig. 3b). Although it was capable of producing roots of sufficient length to reach patch 3, it hardly explored this patch. In contrast, U. perfoliata exploited the more distant patches (Fig. 3b). Uvularia perfoliata is the most mobile of the three species and its greater mobility appears to enable clones to explore their environments more widely than individual plants of the nonclonal U. puberula whose exploration is spatially limited. The mobility of U. perfoliata may enable individual ramets to avoid patches previously or presently occupied by other members of the same genet (e.g., those in patch 1 in the experimental treatments), thus lessening the likelihood of establishing in patches depleted of resources. This is an effective form of ramet dispersal in a species that shows limited seed production. In contrast to U. puberula and U. perfoliata, U. sessilifolia clones, with their longer-lived physiologically integrated rhizome systems, did not show selective placement of roots in high-quality patches. Thus, our results provide evidence for the view that highly integrated clones are less effective than clones with physiologically more autonomous ramets at selective exploitation of patches in heterogeneous environments (de Kroon and Schieving, 1990
).
Integration vs. disintegration
Pitelka and Ashmun (1985)
have suggested that physiological integration is adaptive in patchy environments where functional connections between ramets are necessary in order to grow across unfavorable patches, and to maintain links between ramets occupying favorable patches. Physiological integration enabled clones of U. sessilifolia to continuously explore the habitat while simultaneously sampling numerous patches of different quality. Thus, by 1995, when plants were able to sample all patches in the heterogeneous experimental environments, they produced clones of essentially similar biomass to those in the homogeneously favorable environment (Fig. 4b; Table 1). In contrast, disintegrators such as U. perfoliata can sample only a few patches at any one time. For these species the scope for "averaging" habitat heterogeneity should be limited and the capacity for active foraging by individual ramets should become more important. This argument can be extended to include nonclonal species and clonal species with restricted integration whose ramet systems consist of several small independent integrated physiological units (see Jónsdóttir and Watson, 1997
). Active foraging by resource-acquiring organs should be particularly important when morphological adjustments cannot be made that promote the precise placement of ramets in patches, i.e., aggregation in high-quality patches and escape from low-quality patches. In highly integrated clones, the lack of precise placement of ramets and selective placement of organs can be compensated by transfer of resources between ramets occupying patches of different quality.
It has been suggested that despite the adaptive nature of physiological integration in heterogeneous environments, rapid decay of ramet connections, as seen in U. perfoliata, should be favored if the costs of maintaining connections are high (Pitelka and Ashmun, 1985
; Eriksson and Jerling, 1990
; Caraco and Kelly, 1991
). There is evidence from an earlier study (Wijesinghe and Whigham, 1997
) that the production and maintenance of offspring ramets are costly for U. perfoliata parent ramets. These costs were expressed as increased risk of mortality and reduced growth potential of the parents. The present study shows that the mortality risk for parents was greater when their offspring occupied lower quality patches, suggesting that the offspring in such patches acted as stronger sinks for nutrients than their counterparts in more favorable patches. However, clone size was maintained across a range of environments, with older ramets being sacrificed for the production of new ramets in the less favorable environments. These results show that the provisioning of new ramets by the old can maintain U. perfoliata genets in unfavorable environments for several seasons. Kudoh et al. (1999)
have described this as a "waiting strategy" in which vegetative propagation prolongs the life of genets until more optimal conditions occur under which individual ramets can attain sizes conducive to seed production.
Responses to environmental heterogeneity
In common with other perennial species (Geber, de Kroon, and Watson, 1997
), past experiences can exert a prolonged influence on future developmental events in all three species of Uvularia. In U. perfoliata, the type of shoot (flowering or nonflowering) and the maximum number of offspring produced by each ramet, and in U. sessilifolia and U. puberula, the type and maximum number of shoots produced by the plant in the following season are predetermined during the current growing season. Thus, responses to present environmental conditions can set an upper limit on the plant's capacity to respond to future conditions (Watson, Hay, and Newton, 1997
). This could be a disadvantage if current conditions are less favorable than those that occur in the future, and the plant is constrained by the lack of means, e.g., meristems, to track precisely changes in resource availability. Thus the nature of consecutive, but also contiguous, patches should have an important influence on the overall performance of the plant. However, we did not find a significant effect of patch configuration on the performance of any Uvularia species, other than a reduced pool of buds in U. sessilifolia and U. puberula in treatment D where consecutive unfavorable patches were encountered (Fig. 4). For example, the bud bank of U. sessilifolia in 1994 was significantly larger in the homogeneously favorable treatment C than in the heterogeneous treatment A. However, in 1995, similar numbers of buds developed into shoots in both treatments, although the rhizome segments that bore these shoots occupied qualitatively different patches (see Table 1 for analysis of shoot biomass in patch 2). In addition, for U. sessilifolia and U. puberula, there was also at least a season's delay in emergence of differences in the size of the bud bank between the least favorable treatment (D) and the most favorable treatment (C; Fig. 4b, c).
A possible explanation for the above results is storage. Storage of carbon and minerals is expected to even out spatial and temporal variability in the availability of these essential resources (Chapin, Schulze, and Mooney, 1990
; Eriksson and Jerling, 1990
). Physiological integration on its own should buffer clones against short-term fluctuations in patch quality encountered during a single growing season, whereas storage coupled with physiological integration should have a longer term impact, spread over several growing seasons, on performance (Eriksson and Jerling, 1990
). All three species of Uvularia store resources in belowground structures. However, the storage roots of each U. perfoliata ramet are replaced annually, whereas the storage structures of U. sessilifolia and U. puberula persist for more than one season. While the long-term performance of U. perfoliata genets in heterogeneous environments is maintained by recycling of resources from parent to offspring ramets, the performance of plants belonging to the other two species may be regulated mainly by storage. Thus, U. sessilifolia and U. puberula, as well as U. perfoliata, can withstand fluctuations in the quality of the environment for at least one growing season.
Conclusions
The three species of Uvularia have different strategies for living in patchy environments. Uvularia perfoliata and U. puberula forage actively for nutrients in favorable patches in their habitats. However, the latter exploits only those patches in its immediate vicinity, while the more mobile U. perfoliata is able to move across its environment exploring new patches. Uvularia sessilifolia, on the other hand, appears to have a conservative strategy (sensu de Kroon and Schieving, 1990
), which involves enhanced growth in response to high resource availability without active foraging in high quality patches. Unlike U. perfoliata, U. sessilifolia does not actively avoid unfavorable patches and seek favorable patches, but rather makes use of the latter as they are encountered. The conservative strategy of this species may be aided by a high degree of physiological integration coupled with storage, which enables clones to expand and occupy space. All three species can withstand unfavorable conditions for at least one growing season and are thus expected to be capable of surviving until conditions improve in their spatially and temporally patchy woodland habitat.
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FOOTNOTES |
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2 Current address: Flat 2, 8 Cromwell Road, Hove, East Sussex BN3 3EA UK.
3 Author for reprint requests.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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