Journal of Ecology 2003 91, 27– 35
Differences in performance between genotypes of Fragaria chiloensis with different degrees of resource sharing
Blackwell Science, Ltd
P. ALPERT, C. HOLZAPFEL* and C. SLOMINSKI Department of Biology, University of Massachusetts, Amherst, MA 01003–9297, USA
Summary 1 The ability to transfer resources between separately rooted ramets through connecting stems or roots can increase the performance of clonal plants in heterogeneous environments. However, the degree to which connected ramets share resources differs between and within clonal species. This may be because a higher potential for resource sharing is selected for in more heterogeneous habitats. To test this, it was hypothesized that: (i) genotypes with a relatively high potential for resource sharing will accumulate more biomass in a highly heterogeneous environment than genotypes of the same species with a relatively low potential for resource sharing; (ii) disconnecting ramets to prevent sharing will eliminate this difference between genotypes; and (iii) there will be no relationship between potential for resource sharing and accumulation of biomass in a homogeneous environment. 2 Pairs of connected and disconnected ramets of three genotypes of the stoloniferous herb Fragaria chiloensis that had previously been shown to differ in potential for carbon sharing were grown in two environments in a glasshouse. In the heterogeneous environment, which was designed to mimic a natural pattern of resource heterogeneity encountered by F. chiloensis, one of the ramets in each pair was given lower light and higher nitrogen than the other. In the homogeneous environment, both ramets in each pair were given the same resource levels. 3 In the heterogeneous environment, the genotypes with the highest and the intermediate levels of resource sharing accumulated significantly more biomass than the genotype with the lowest level of sharing. Disconnecting ramets to prevent resource sharing eliminated these differences between genotypes, suggesting that the differences in biomass between the genotypes when grown in this environment were specifically due to differences in resource sharing. The net effect of ramet connection on biomass, measured as the difference between biomass of connected and disconnected ramets, was consistently higher in genotypes with a higher potential for resource sharing. In the homogeneous environment, the different genotypes performed similarly whether ramets were connected or not, and there was no net effect of connection on performance in any genotype. Although only three genotypes were tested in only two environments, these results were generally consistent with the hypotheses, and suggest that resource sharing in clonal plants may represent an adaptation to resource patchiness. 4 A second characteristic that is found in clonal but not in non-clonal plants is ‘division of labour’, the tendency for ramets to specialize to acquire resources that are locally abundant but scarce for ramets to which they are connected. Genotypes did not differ in their potential for division of labour between ramets, as measured by the effect of connection on allocation to roots in the heterogeneous environment. This suggests that potential for resource sharing may not be strongly associated with potential for division of labour in F. chiloensis. Key-words: clonal plant, genetic differentiation, light and nitrogen availability, physiological integration, resource patchiness Journal of Ecology (2003) 91, 27–35
© 2003 British Ecological Society
Correspondence: Peter Alpert (tel. + 1-413-545-4357; fax + 1-413-545-3243; e-mail
[email protected]). *Present address: Department of Plant Sciences, Tel Aviv University, Tel Aviv 69978, Israel.
28 P. Alpert, C. Holzapfel & C. Slominski
© 2003 British Ecological Society, Journal of Ecology, 91, 27–35
Introduction The ability to translocate resources such as photosynthates and mineral nutrients between otherwise selfsufficient plant units (i.e. ramets) through connecting stems or roots is widely agreed to increase the survival and growth of clonal plants in heterogeneous habitats. This may be because connected ramets can exchange resources that tend not to occur together or because ramets with an excess supply of a resource can subsidize the growth of other ramets with a lower supply (e.g. Hutchings & Wijesinghe 1997; Hutchings et al. 2000). However, the degree to which connected ramets share resources varies greatly between clonal species, and it has long been hypothesized that this variation is at least in part adaptive, i.e. due to differential selection in different habitats (Pitelka & Ashmun 1985; Jónsdóttir & Watson 1997). The potential for local adaptation in clonal integration is supported by studies that find genetic differentiation for clonal architecture and reproductive characteristics between genotypes of the same species in sites as little as 5 m apart (Fischer et al. 2000; van Kleunen et al. 2000; van Kleunen & Fischer 2001). Some recent theoretical and comparative empirical studies suggest that greater resource sharing may be selected for in habitats where resource availability is more spatially heterogeneous (e.g. Alpert 1999; Oborny et al. 2000; Pennings & Callaway 2000). In homogeneous environments, resource sharing might actually be disadvantageous, due to costs of maintaining connections or because costs to exporting ramets are likely to exceed benefits to importing ramets if sharing is constitutive (Alpert 1999). Having a relatively high potential for resource sharing might therefore be an adaptation to a high degree of resource patchiness. For this to be true, (i) there must be genetically based variation between genotypes within species for resource sharing, (ii) genotypes with a higher potential for resource sharing must perform better in highly heterogeneous environments than genotypes with a lower degree of resource sharing, and (iii) this difference in performance between genotypes must be smaller in less heterogeneous environments. The first of these three conditions has been demonstrated in at least three clonal species (Lötscher & Hay 1997; Alpert 1999; van Kleunen et al. 2000). The main objective of the current study was to see whether the second and third conditions can also be met by one of these three species, the stoloniferous, perennial herb Fragaria chiloensis (L.) Duchesne (beach strawberry). We therefore tested the hypotheses that: (i) genotypes of F. chiloensis with a higher potential for resource sharing perform better than genotypes with a lower potential for sharing when connected ramets experience contrasting resource availabilities (satisfying the second condition); (ii) disconnecting ramets and thereby preventing resource sharing between ramets eliminates this difference in performance between genotypes (confirming that the difference is specifically
due to resource sharing); and (iii) potential for resource sharing has no effect on performance of genotypes in a homogeneous habitat, whether ramets are connected or not (satisfying the third condition). We emphasize that by difference in ‘potential for resource sharing’ we refer to genetically based differences between genotypes in the amounts of resources that are transported between connected ramets in an environment that is both realistic and likely to induce relatively high amounts of sharing. Actual amounts of resource sharing in a given genotype may depend on genotype, environment, and genotype–environment interaction. Advantages of resource sharing in heterogeneous environments could be increased by a property of clonal plants that involves both clonal integration and morphological plasticity, namely the capacity for ‘division of labour’ between connected ramets that experience contrasting levels of resource availability (Alpert & Stuefer 1997; Hutchings & Wijesinghe 1997). Whereas non-clonal plants and disconnected ramets of clonal plants tend to specialize to acquire the resources that most limit growth, ramets of some clonal plants specialize to acquire resources that are locally abundant but limiting to connected ramets (Friedman & Alpert 1991; Birch & Hutchings 1994; Stuefer et al. 1996). Given that acquiring an abundant resource is likely to be more efficient than acquiring a scarce one, such specialization is likely to increase total clonal growth. We took advantage of our test of the three hypotheses above to test the additional hypothesis that (iv) a high potential for resource sharing is associated with a high potential for division of labour. As far as we know, division of labour has not previously been compared between genotypes of the same species known to differ in resource sharing.
Methods We selected three of 11 genotypes of F. chiloensis that had previously been screened for potential for carbon sharing (Alpert 1999), choosing the genotypes so as to represent the full range of potential sharing observed. Alpert (1999) measured potential for carbon sharing by shading one ramet in a pair of connected ramets and comparing the accumulation of biomass when the ramets were left connected and when the ramets were disconnected. Potential for carbon sharing was indicated by how much the final biomass of connected, shaded ramets exceeded that of disconnected, shaded ramets, and by how much the biomass of disconnected, unshaded ramets exceeded that of connected, unshaded ramets. In the selected genotypes, which we will refer to as the ‘high-’, ‘medium-’ and ‘low-sharing’ genotypes, the mean biomass of connected, shaded ramets was, respectively, 2.9, 2.1 and 1.7 times greater than that of unconnected, shaded ramets. Genotypes
29 Resource sharing and performance of genotypes
had been collected at Año Nuevo State Reserve (37°3′ N, 122°13′ W), about 100 km south of San Francisco along the coast of northern California, and were propagated through at least six vegetative generations in a glasshouse at the University of Massachusetts at Amherst to help eliminate any environmental effects (Schwaegerle et al. 2000). Ramets in F. chiloensis consist of a short, usually unbranched, partially buried stem with a rosette of leaves and fibrous roots. The axillary bud of a leaf can produce a stolon or an inflorescence. A stolon rarely branches and typically produces a new ramet at every other node, forming a string of sibling ramets spaced 20 – 40 cm apart. Newly produced strings of ramets were rooted without severing the stolons, with each ramet in a separate pot (11 cm diameter × 11 cm depth) filled with fine, acid-washed sand. After 2 weeks for establishment, ramets were separated into pairs of adjacent offspring by severing the stolon between every other ramet in a string. Previous work has shown that severing stolons has no effect on growth in biomass of ramets of F. chiloensis when ramets are given similar resource availabilities, and that resource sharing between connected ramets is minimal under these conditions (Alpert & Mooney 1986; Alpert 1991, 1996). This suggests that severing stolons has no marked direct effect on growth independent of its effects on resource sharing.
Ten replicate pairs of ramets from each genotype were subjected to each of two connection treatments (connected and disconnected) crossed with two environments (heterogeneous and homogeneous; Fig. 1). In the connected treatment, which allowed the possibility
© 2003 British Ecological Society, Journal of Ecology, 91, 27–35
Fig. 1 Experimental scheme, showing the connection treatments and resource availabilities given to 10 replicates of each genotype in each of two environments.
of resource sharing between ramets, the ramets in a pair were left connected by the length of stolon between them. In the disconnected treatment, which prevented resource sharing between ramets, the stolon was cut halfway between ramets just before plants were moved into the experimental environments. Marked environmental heterogeneity is encountered by connected ramets of F. chiloensis at the original collection site, as they occur both on open sand where light availability is very high and nitrogen availability is very low, and in microsites under the large, nitrogenfixing shrub Lupinus arboreus, where light availability is much lower and nitrogen availability is higher (Alpert & Mooney 1996). To simulate this pattern, one ramet in each pair was left unshaded and watered with a modified Hoagland’s solution (Alpert & Mooney 1986) containing 5 mg N-NO3 L−1 (high light, low N treatment), and the other ramet in the pair was shaded to 10% of ambient light with spectrally neutral black plastic mesh attached to a frame of thin, wooden dowels and watered with a solution containing 20 mg N-NO3 L−1 (low light, high N treatment). Because nitrogen moves mostly from older to younger ramets in F. chiloensis (Alpert 1996), and carbon appears to move equally readily in either direction (Alpert & Mooney 1986), the older ramet in each pair was given the low light, high N treatment to maximize the amount of resource sharing between connected ramets. In the homogeneous environment, both of the ramets in each pair were left unshaded and watered with a solution containing 10 mg N-NO3 L−1. This provided uniform resource levels and a nitrogen level in between the levels used in the heterogeneous environment. In both environments, each new stolon produced during the experiment was kept in the same light level as its parental ramet, and new ramets produced along a new stolon were not allowed to root. All pots were watered whenever the surface of the soil in any pot became dry. Enough solution was added at each watering to flush the soil and help prevent any build-up of nutrients. Although amounts of resources provided in the heterogeneous and homogeneous environments were not completely equal, the data analysis was designed such that this did not affect the analyses. Plants were arranged on a single glasshouse bench in 10 blocks, each with one replicate of each genotype randomly assigned to each connection treatment and environment. We were not able to randomize fully the positions of the treatments within each block because it was not possible to fully intersperse shaded and unshaded ramets without partly shading the unshaded ramets. Instead, the shaded ramets in each block were all placed adjacent to one another and treatments randomized within blocks subject to this constraint. As measures of plant growth did not differ between blocks (see data analysis), it seems unlikely that position within blocks affected plant growth. Treatments were run for 3 months, from February until April 2001. At harvest, each ramet was separated
30 P. Alpert, C. Holzapfel & C. Slominski
into roots, shoot (stem plus leaves), and any new stolons produced in the leaf axils plus any new ramets along new stolons. Dead and senescent leaves (those < 50% green on both the upper and lower surfaces) were discarded. Parts were then dried at 60 °C and weighed. Any pairs of connected ramets in which the connection showed signs of senescence at harvest were excluded from the data analysis. We used total accumulation of biomass (i.e. final total dry biomass of a ramet and any new stolons and new ramets it produced) as a measure of plant performance. Accumulation of biomass is often used as a measure of fitness in clonal plants (e.g. Prati & Schmid 2000; van Kleunen et al. 2000), in part because establishment from seed is often very rare (Klimes 2000; Verburg et al. 2000). To measure the net effect of connection on the performance more specifically, we used the difference between the biomass accumulations of a connected ramet and of the disconnected ramet of the same age (i.e. older or younger ramet in a pair), genotype, environment and block.
© 2003 British Ecological Society, Journal of Ecology, 91, 27–35
Data were analysed in 9. To test for differences in performance between genotypes, we used two twoway s, one for each environment, with genotype (high-, medium- or low-sharing) and connection (connected or disconnected) as fixed factors and biomass accumulation of ramet pairs as the dependent variable. We then compared means for individual genotypes within connection treatments using Tukey tests. We did not analyse mass of new stolons separately because it was generally small and highly variable between replicates. We omitted effect of block from all s because preliminary analyses showed that effect of block (P) was always > 0.1. To test for differences between genotypes in the net effect of connection on performance, we used three one-way s for each environment, one for the older ramets within pairs, one for the younger ramets within pairs, and one for the two ramets in a pair combined. In the heterogeneous environment, the older ramets were also the ramets given low light and high N, and the younger ramets were the ones given high light and low N. In each test, genotype was a fixed factor and net effect of connection, measured as described above, was the dependent variable. We used Tukey tests to compare individual means within each test, and orthogonal contrasts to test whether each mean differed from zero. To test for differences between genotypes in division of labour, we analysed the allometry of root and shoot mass of ramets within pairs in the heterogeneous environment. We used a three-way with genotype, connection and resource treatment to individual ramets (low light and high N, or high light and low N) as fixed factors, ramet shoot mass as a covariate, and ramet root mass as the dependent variable. We used this
Fig. 2 Final total dry biomass (mean + SE) of pairs of ramets and their progeny from a high-sharing (H), a medium-sharing (M) and a low-sharing (L) genotype of Fragaria chiloensis in (a) heterogeneous and (b) homogeneous environments. Within each environment and connection treatment, letters show which genotypes differed (P [Tukey] < 0.05).
model instead of an of root mass/total mass because the latter can mistake fixed allometry for plasticity (e.g. Coleman et al. 1994; Muller et al. 2000). We tested specific hypotheses about differences between means with orthogonal contrasts.
Results In the heterogeneous environment, pairs of connected ramets of the high-sharing and the medium-sharing genotypes accumulated more total dry biomass than pairs of connected ramets of the low-sharing genotype (Fig. 2a). This was only partly consistent with the hypothesis that genotypes with a higher potential for resource sharing will perform better than genotypes with a lower potential for sharing when connected ramets experience different levels of resource availability, as the high-sharing genotype did not accumulate more biomass than the medium-sharing genotype. Pairs of disconnected ramets of the different genotypes did not differ in biomass (Fig. 2a), which was consistent with the hypothesis that preventing resource sharing will eliminate the positive relationship between potential for resource sharing and performance in a heterogeneous habitat. Overall effect of genotype was marginally significant (F2,156 = 2.49, P = 0.09), possibly indicating that there were also some differences between genotypes in performance that were not due to effects of connection. Overall effect of connection was not significant (F1,156 = 0.01, P = 0.9).
31 Resource sharing and performance of genotypes
Fig. 3 Net effect of connection (difference between connected and disconnected treatments in final total dry biomass; mean + SE) in a high-sharing (H), a medium-sharing (M) and a low-sharing (L) genotype of Fragaria chiloensis in (a–c) heterogeneous and (d–f ) homogeneous environments, for older (a, d), younger (b, e) and both ramets combined (c, f ). In each graph, P is effect of genotype in a one-way , and letters show which means differed from each other (P [Tukey] < 0.05). Symbols show whether a mean differed from zero (P [orthogonal contrasts]: no symbol, > 0.1; +, < 0.1; * < 0.05; ** < 0.01).
In the homogeneous environment, the biomass of pairs of ramets did not differ between genotypes when ramets were connected or when they were disconnected (Fig. 2b). There was a marginally significant overall effect of genotype (F2,174 = 2.94, P = 0.06), but no indication that this bore any relationship to level of resource sharing. These results were consistent with the hypotheses that preventing resource sharing will eliminate differences between genotypes in performance that are associated with level of sharing, and that potential for resource sharing will have no effect on performance of genotypes in a homogeneous habitat. There was no significant effect of connection (F1,174 = 0.06, P = 0.8) or genotype × connection (F2,174 = 1.45, P = 0.2).
© 2003 British Ecological Society, Journal of Ecology, 91, 27–35
In the heterogeneous environment, net effect of connection on biomass (i.e. difference between final biomass accumulation of connected and disconnected ramets) differed between genotypes and showed a consistent tendency to be more positive in genotypes with a higher potential for sharing (Fig. 3). Mean net effect of connection on ramets given low light and high N was
positive in the high-sharing and medium-sharing genotypes but not in the low-sharing genotype (Fig. 3a); effect of connection on ramets given high light and low N did not differ from zero in the high- and mediumsharing genotypes and was negative in the low-sharing genotype (Fig. 3b); and effect of connection on the two ramets in a pair combined was positive in the highsharing genotype, did not differ significantly from zero in the medium-sharing genotype, and was marginally negative in the low-sharing genotype (Fig. 3c). The effect of connection on ramet pairs in the high-sharing genotype accounted for about one-fourth of the mean total biomass of these pairs (Fig. 2a). The rankings by net effect of connection of both single and pairs of ramets all matched our identification of the genotypes as high-, medium- and low-sharing. This supported the previous evidence for differences between genotypes in potential for resource sharing presented by Alpert (1999) and was consistent with the hypothesis that genotypes with a higher potential for resource sharing will perform better than genotypes with a lower potential for sharing in a heterogeneous environment. However, it was not expected that ramets would show any negative effects of connection in any genotype in these environments, and we discuss this below.
Table 1 to test for effects of genotype, connection and resource availabilities to individual ramets in the heterogeneous environment on the root mass of ramets, with shoot mass as covariate. The error term for the had 149 d.f. and a MS of 0.131. See Fig. 4 for summary of data
32 P. Alpert, C. Holzapfel & C. Slominski
Fig. 4 Allocation to roots (g dry mass of root g−1 total dry mass; mean + SE) in connected and disconnected ramets of Fragaria chiloensis in the heterogeneous environment: (a) high-sharing genotype; (b) medium-sharing genotype; (c) low-sharing genotype. Ramets were given low light and high N (shaded bars) or high light and low N (unshaded bars). See Table 1 for .
In the homogeneous environment (Fig. 3d–f), net effect of connection did not differ between genotypes, nor show a tendency to be more positive in genotypes with a higher potential for sharing, nor differ significantly from zero in any case. These results were consistent with the hypotheses that preventing resource sharing will eliminate differences between genotypes in performance that are associated with level of sharing, and that potential for resource sharing will have no effect on performance of genotypes in a homogeneous habitat.
© 2003 British Ecological Society, Journal of Ecology, 91, 27–35
In each of the three genotypes, the ramets given high light and low N allocated more of their total biomass to roots than the ramets given low light and high N when the ramets were disconnected (Fig. 4); P (orthogonal contrast across genotypes) = 0.003. In contrast, ramets in the two different light and N treatments showed no difference in allometry of roots and shoots when ramets were left connected; P (orthogonal contrast across genotypes) = 0.3. The effect of connection was thus in the direction expected for division of labour but did not go as far as apparent specialization to acquire locally scarce resources. There was no indication that the interactive effect of connection and resource availability on
Effect
d.f.
F
P
Genotype Connection Resources Genotype × connection Genotype × resources Connection × resources Genotype × connection × resources Shoot mass
2 1 1 2 2 1 2 1
7.61 5.47 1.77 7.04 0.20 3.60 0.09 227.00
< 0.001 0.02 0.2 0.001 0.8 0.06 0.9 < 0.001
allocation differed between genotypes (Table 1: effect of genotype × connection × resources). This three-way interaction was the direct test of whether potential for division of labour differed between genotypes. Results thus failed to support the hypothesis that genotypes with a higher potential for resource sharing will also show a greater potential for division of labour. Across connection treatments and resource availabilities, genotypes differed in how much biomass they allocated to roots (Table 1: effect of genotype). The effect of connection across resource availabilities also differed between genotypes (Table 1: effect of genotype × connection). Results thus did indicate the presence of some genetically based differences between the genotypes in patterns of biomass allocation.
Discussion Although we tested only three genotypes in only one heterogeneous and one homogeneous environment, results were largely consistent with our hypotheses and provide initial experimental evidence that a high level of resource sharing between ramets within plant clones may be an adaptation to a high degree of resource heterogeneity. Results mostly supported the hypothesis that genotypes with a higher potential for resource sharing will perform better than those with a lower potential for resource sharing in a spatially heterogeneous environment. We did not find that the high-sharing genotype accumulated the greatest total biomass in the heterogeneous environment when ramets were connected, but did find that the low-sharing genotype accumulated the least biomass, and that the ranking of genotypes by net effect of connection on biomass in the heterogeneous environment consistently matched their ranking by level of carbon sharing as previously measured by Alpert (1999). The fact that the ranking of genotypes by net effect of connection was the same for the ramets given low light and high N (likely to import carbon and export N) as for the ramets given high light and low N (likely to export carbon and import N) suggests that levels of carbon and nitrogen sharing varied together.
33 Resource sharing and performance of genotypes
© 2003 British Ecological Society, Journal of Ecology, 91, 27–35
Results also supported the hypotheses that the difference in performance between genotypes with different levels of resource sharing depends upon connection between ramets, and that level of resource sharing will not affect performance in a homogeneous environment. Disconnecting ramets eliminated differences between genotypes in both accumulation of biomass and net effect of connection on biomass. Growing plants in a homogeneous environment eliminated those differences between genotypes in accumulation of biomass that showed any relationship to level of resource sharing, and eliminated differences between genotypes in net effect of connection. One possible explanation for the lack of difference between the high- and medium-sharing genotypes in accumulation of biomass in the heterogeneous environment may be that level of resource sharing is not necessarily linearly related to performance in heterogeneous environments but can instead show an asymptotic or other relationship. A second possible explanation is that differences in performance between the two genotypes due to resource sharing were masked by differences due to other traits. The second explanation is consistent with the tendency of the mediumsharing genotype to accumulate more biomass than the high-sharing genotype when ramets were disconnected or when ramets were grown in the homogeneous environment (i.e. when capacity for resource sharing was not likely to affect performance). The fact that net effect of connection, a measure that factored out differences between genotypes not due to connection, was consistently more positive in the high- than in the medium-sharing genotype is also consistent with the second explanation. The net negative effect of connection on the ramets of the low-sharing genotypes that were given high light and low N in the heterogeneous environment was not expected. The simplest interpretation is probably that the benefit derived by unshaded ramets from N import was lower than the cost incurred through carbon export in the lower-sharing genotypes. The effects of level of resource sharing on the fitness of plant clones may thus be complex in habitats where multiple resources have patchy distributions. Some patterns of resource heterogeneity may select against low levels of resource sharing. Several caveats should be added. First, we again emphasize that we tested only three genotypes and that our predictions were not completely fulfilled. It seems unlikely that chance produced the degree of consistency that was observed between results and hypotheses, but it will now be useful to pursue studies with more genotypes. Secondly, degree of spatial heterogeneity is not the only factor that might select for different degrees of resource sharing in different habitats. Different levels of mean resource availability, temporal heterogeneity or predictability could also favour different degrees of resource sharing (Pitelka & Ashmun 1985; Jónsdóttir & Watson 1997). Thirdly, performance
of genotypes did show a marginally significant difference in the homogeneous environment. This possible difference showed no relationship to level of resource sharing, and may reflect effects of traits other than resource sharing on plant performance. Fourthly, spatial heterogeneity is a complex characteristic, with at least two major components, scale (i.e. sizes of patches) and contrast (i.e. differences between patches), which may interact in their effects on plant performance. For example, Wijesinghe & Hutchings (1999) found that the performance of sets of connected ramets of Glechoma hederacea increased with patch contrast when patches were large, but decreased with patch contrast when patches were small. The test of effect of resource heterogeneity that we provide here is very restricted, and other contrasts in heterogeneity could yield different results. Although limited in scope, these results may provide the first experimental evidence that a higher potential for resource sharing can confer better performance at a given level of resource patchiness. They suggest that Fragaria chiloensis can meet two important requirements for selection for a higher potential for resource sharing in more spatially heterogeneous habitats: a positive relationship between potential for resource sharing and clonal performance when resources are highly patchy, and a less positive relationship when resources are less patchy. Previous work (Alpert 1999) showed that genotypes of F. chiloensis from a spatially heterogeneous type of habitat (sand dune) had a higher mean potential for resource sharing than genotypes from a less heterogeneous habitat (grassland) at Año Nuevo State Reserve. As we selected genotypes to represent the natural range of genetic variation for potential for resource sharing encountered in F. chiloensis at Año Nuevo State Reserve, and used a heterogeneous environment designed to mimic an important natural pattern of resource availability on the sand dunes at Año Nuevo, results suggest that genetic differentiation for resource sharing between the sand dune and grassland populations could have been driven by selection for a higher potential for sharing in the more heterogeneous habitat. These results may also provide the first test for a relationship between performance and a genetically based physiological trait unique to clonal species of plants. We were able to locate 16 studies on genetically based variation in clonal characteristics within plant species (Table 2). At least six of these documented differences between genotypes from contrasting habitats, and three documented differences in physiological traits. However, only one demonstrated that a difference between genotypes was associated with greater fitness of a genotype in its home habitat, and this study did not deal with a physiological trait. Results did not support the hypothesis that a high potential for resource sharing is associated with a high potential for division of labour in different genotypes of F. chiloensis. Friedman & Alpert (1991) showed that
34 P. Alpert, C. Holzapfel & C. Slominski
Table 2 Some studies on genetically based variation in clonal characteristics within plant species. Unless otherwise noted, variation was found in each of the characteristics listed. Studies that found variation between genotypes from differing habitats are starred (*). The study that found associated fitness differences is doubly starred (**) Species
Characteristics
Reference
Agrostis stolonifera* Amphibromus scabrivalvis Amphibromus scabrivalvis
Clonal architecture Plasticity in clonal architecture Allocation to vegetative reproduction, spacing of ramets
Elymus lanceolatus Festuca rubra Fragaria chiloensis Fragaria chiloensis* Fragaria chiloensis
No variation in plasticity of ramet placement Clonal architecture, allocation to vegetative and sexual reproduction, response to ratio of red to far-red light Clonal architecture and its response to nitrogen Carbon sharing Clonal architecture and ramet morphology
Kik et al. (1990) Cheplick (1995) Cheplick (1997); Cheplick & Gutierrez (2000) Humphrey & Pyke (1997) Skálová et al. (1997)
Potentilla reptans Ranunculus reptans** Ranunculus reptans* Ranunculus repens* Trifolium repens* Trifolium repens
Integration of plastic response to shading Relative investment in sexual vs. vegetative reproduction Carbon sharing, senescence of connections between ramets Effect of connection on competition between ramets Phosphorus sharing Senescence of connections, allocation to leaves, stolon branching
an environmental treatment that induced a greater actual amount of resource sharing between ramets of F. chiloensis did not induce a greater division of labour between them. Combined, these findings suggest that aspects of clonal integration other than resource transfers may be responsible for the induction of division of labour.
Acknowledgements We thank: Bree Goldstein, Meaghan Schaffer and Madeeha Yosef for research assistance; Ronald Beckwith and Monika Johnson for glasshouse management; Shea Gardner and Mark van Kleunen for comments on the manuscript; the California Department of Parks and Recreation for permission to collect plants at Año Nuevo State Reserve; and the University of California Bodega Marine Laboratory for use of their facilities during manuscript preparation. Research was supported by US National Science Foundation grant IBN-9507497 and by a University of Massachusetts Commonwealth College Sophomore Fellowship.
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© 2003 British Ecological Society, Journal of Ecology, 91, 27–35
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