J. F. Stuefer, Department of Ecology, Nijmegen University, Toernooiveld 1, 6525ED Nijmegen, Netherlands. Tel.: +31-24-3652259; fax: +31-24-3652409; e-mail: email@example.com
A negative, genetic correlation between the total number and average size of progeny is a classical life-history trade-off that can greatly affect the fitness of organisms in their natural environments. This trade-off has been investigated for animals and for sexually reproducing plants. However, evidence for a genetical size-number trade-off for clonal progeny in plants is still scarce. This study provides experimental evidence for such a trade-off in the stoloniferous herb Potentilla reptans, and it studies phenotypic plasticity to light availability for the involved traits. Genotypes of P. reptans were collected from distinctively different environments, clonally replicated and exposed to high light and to shaded conditions. We found a significant negative correlation between the average size and the total number of offspring across genotypes for both light environments. Shading reduced ramet numbers, but hardly affected average ramet size.
Trade-offs between competing life-history functions play a central role in evolutionary ecology. General life-history theory predicts that environmental conditions select for trait combinations which enhance the fitness of organisms living in that particular habitat. Realized life-histories can be seen as selection-tailored solutions that match internal constraints to particular environmental challenges (Stearns, 1989, 1992; Futuyma, 1997).
The average size and the total number of offspring produced by an organism are two fitness-related traits that are not likely to be maximized at the same time. If survival and establishment chances for offspring individuals are positively size-dependent, resources should preferentially be used to produce large offspring. In contrast, if survival and performance are largely size-independent, the formation of relatively many, but smaller individuals should be preferred (McNaughton, 1975). Such a resource-mediated trade-off between these two life-history functions can lead to distinct investment strategies in different habitats (Johansson, 1993, 1994).
Clonal progeny of plants mainly serve the task of genet rejuvenation, local propagation, and resource harvesting from a heterogeneous environment. Variation in size-number relations of clonal offspring may lead to differential success of genets in different environments. Small individuals are easily outcompeted in dense canopies. Such habitat conditions may hence favour the production of relatively few, large offspring ramets. Open and disturbed habitats, on the other hand, should favour the production of a higher number of smaller ramets, because the production of many offspring individuals is beneficial in habitats where opportunities for invading open space arise on a regular basis. In disturbed habitats, high degrees of size-independent mortality may further intensify selection pressures for risk spreading through the formation and dispersal of as many ramets as possible. Clonal plant species with a broad ecological amplitude may be expected to comprise genotypes differing in functional trait combinations (McLellan et al., 1997).
The aim of this study is to provide answers to the following three questions: (1) Is there a genotypic trade-off between the number and size of clonal offspring in the stoloniferous herb Potentilla reptans? (2) How does light availability affect the total number and average size of clonal offspring? (3) Do the relationships between size and number of clonal offspring vary significantly among genotypes, and/or among light environments.
Materials and methods
The study was carried out with the stoloniferous herb Potentilla reptans L. Typical habitats of this species include moderately disturbed, productive pastures, mown grasslands, lake and river shores, road margins and other man-made habitats. P. reptans produces long, above-ground stolons with rooted ramets on its nodes. It can colonize bare patches and gain local dominance by rapid spread through stolon growth and ramet establishment (Stuefer, personal observation, see Eriksson, 1986, 1988 for related species). In the absence of physical disturbance, ramets remain interconnected throughout one growing season.
Eight genotypes of P. reptans were collected from a wide range of habitats in the surroundings of Utrecht, the Netherlands. One genotype was collected per site, which means that differences between genotypes represent within-species (and not within-population) variation. The sites were chosen to represent typical habitats for the species. They span a broad ecological spectrum which ranges from open and severely disturbed to relatively closed, competitive habitats. The sites included river shores, road sides, mown pastures, and practically undisturbed grasslands.
A single piece of stolon consisting of four to six interconnected ramets was collected in each of the eight sites. The stolon pieces were planted in the experimental garden of Utrecht University. Since trait correlations can be affected by within-genet variation, special care was taken in standardizing precultivation conditions and to minimize within-genet variability at the beginning of the experiment. To eliminate maternal effects, each of the genotypes was allowed to grow and propagate clonally within an area of 1.5 × 1.5 m in this common garden for 2 years. Genotype compartments were separated by plastic walls, that were inserted 15 cm into the soil and had a height of 30 cm to avoid intermingling of genets by stolon growth.
At the end of June 1994, 30 similar-sized, juvenile plants (i.e. ramets that had been formed in the same year) of each of the genotypes were excavated from the mono-genotypic stock populations, and planted individually into 11 × 11 × 11 cm pots filled with river sand. These ramets will subsequently be referred to as parent ramets. To standardize for size differences among ramets, roots on all parent ramets were cut to a length of 7 cm, and all but the youngest two leaves were removed from each ramet prior to planting. All pots were supplied weekly with a full strength liquid fertilizer (2.5 mg L−1 NH4NO3, 1.6 g L−1 KCl, 1.3 g L−1 Na2PO4).
When most of the parent ramets had initiated two stolons, 10 parent ramets per genotype were selected for similar size (i.e. number of rosette leaves) and developmental stage (plastochron age of branches), and transplanted to long plastic trays (100 × 15 × 15 cm). Trays were filled with a mixture of sand and sieved potting compost at a volumetric ratio of 1 : 2 for sand and compost, respectively. Controlled Release Fertilizer (Osmocote Plus, Grace Sierra International, Heerlen, Netherlands) was added to the substrate to give a constant nitrogen release equivalent to 20 kg ha−1 week−1. Former pilot studies had shown that this nutrient regime is sufficient to avoid nutrient limitation for growing clones of P. reptans (Stuefer, 1997). All but two primary stolons were removed from each parent plant. Parent ramets were then planted into the middle of each tray, and the two stolons were guided in opposite directions.
Five plants (parent ramets) of each genotype were randomly assigned to one of the two experimental treatments, which consisted of shading (L–) or no shading (L+, control) of plants. The experiment was performed during the summer in the outdoor experimental garden of Utrecht University. Plants in the control treatment (L+) were exposed to full daylight, whereas plants in the shade treatment (L–) received approximately 20% of full daylight. This light reduction was achieved by using shade cages covered with black, synthetic shade cloth, which did not affect the red/far-red ratio of transmitted light (Huber & Stuefer, 1997; Stuefer & Huber, 1998). Plants in the high light treatment were also put into cages to make climatic conditions comparable between treatments and to prevent herbivory. After 11 weeks all plants were harvested, the total number of ramets was recorded and the biomass of ramets was measured. All plant material was dried to constant mass at 75 °C before weighing.
Spearman correlation coefficients were used to test for character correlations within treatments. Mean values for genotypes (family means) were used to estimate genetic correlations. This non-parametric test was preferred as there was no a priori expectation about the statistical properties of the tested relationships.
Two-way analysis of variance (anova) was used to test for the effects of shading, and for variation among genotypes. Both main factors (light availability and genotype identity) were considered as fixed effects, because shade levels and genets had been chosen non-randomly in this experiment (see Bennington & Thayne, 1994; Cheplick, 1997). Mixed model analyses gave the same qualitative results.
A two-way analysis of covariance (ancova) was used to test for changes between genotypes and/or environment in the relationship between ramet numbers and average ramet size. Ramet number was used as a response variable in this analysis. The following terms were included in the ancova model (see Table 2): treatment, genotype, treatment × genotype, average ramet weight (covariable), average ramet weight × treatment, and average ramet weight × genotype. The last two interaction terms test for genotype or environment-specific changes in the relationship between the number and size of ramets.
Table 2. Analysis of variance (ANOVA) table for ramet numbers. Both main effects were considered fixed. The average ramet weight (arw) is used as a covariate in this analysis.
Number of ramets
G × T
arw × T
arw × G
The total number of ramets was negatively correlated with the average biomass of ramets across genotypes (Fig. 1). This was true for both the high light treatment (Spearman r = −0.82; P = 0.014; n = 8) and for the shade treatment (Spearman r = −0.74; P = 0.037; n = 8). Shading reduced total biomass production to about one-third of the values reached in the high-light treatment (Fig. 2a). Genotypes differed significantly in their total biomass produced and in their response to shading (see G and G × T effect in Table 1). The total number of ramets differed significantly between light treatments and genotypes (Fig. 2b). There was a significant genotype by light interaction in terms of ramet numbers but not in terms of average ramet weight (Table 1). The mean ramet biomass differed significantly between genotypes (Table 1). Average biomass of individual ramets did not respond significantly to changes in light availability (Fig. 2c, Table 1). The ancova showed a significant interaction between light treatments and average ramet weight (covariate; Table 2) indicating that the relationship between ramet size and ramet number changed significantly between the light and shade environments (Fig. 1). No significant interaction was found between average ramet biomass and genotype identity (Table 2).
Table 1. Analysis of variance (ANOVA) table for effects of light treatment (T), genotype (G), and treatment by genotype interaction (G × T). Both factor are considered fixed, as they have been chosen deliberately.
Total plant biomass
G × T
Number of ramets
Average ramet weight
T × G
This study provides experimental evidence for a genetically determined, negative correlation between the total number and the mean size of clonal offspring in the stoloniferous herb P. reptans. This study is one of the first to explicitly document this basic life-history trade-off for clonal progeny in plants. Our data suggest the existence of a basic trade-off between two alternative life-history strategies in this species. The production of a low number of big ramets can be seen as an investment strategy to enhance the survival and to increase the competitive strength of establishing ramets. The production of few big ramets is likely to be beneficial in dense, undisturbed canopies, where offspring survival and establishment is positively size-related as a consequence of inter- and intraspecific competition.
Conversely, genotypes producing many, small ramets will be at a selective disadvantage in competitive environments, because small ramets are likely to suffer high mortality rates and low establishment chances in these habitats. The production and dispersal of many potentially independent ramets is an effective strategy to spread the risk of genet death in case of localized disturbance (Cook, 1978; Eriksson & Jerling, 1990). Furthermore, the production of a high number of offspring individuals enables genets to rapidly colonize open space (Fahrig et al., 1994). This ability should translate into benefits in environ-ments, where open spaces are regularly created through disturbance.
Changes in light conditions had no significant effect on mean ramet weight, while numbers of ramets decreased sharply in shaded as compared high light conditions (Fig. 2). This suggests that a genotype-specific size of clonal offspring is maintained even under conditions of severe resource shortage, and that resource-imposed reductions in clonal growth rates are manifested in lower numbers of ramets, but not in their average biomass.
The relationship between mean ramet biomass and the total number of ramets showed significant variation (i.e. phenotypic plasticity) between the light treatments, although no evidence was found for genotype-specific variation in size-number relations. The lower and the upper limit to the range of ramet sizes are likely to be constrained by different selection pressures. A minimum size of ramets is an important trait ensuring offspring survival and establishment. The upper bound is likely to be constrained by selection pressures arising from the law of diminishing returns (Bloom et al., 1985). Resource investment into the size of individual ramets above a certain average size will not lead to equivalent fitness returns. Above this threshold, the production of additional ramets should be favoured over the additional size increase of existing ramets, because the marginal benefits of size increases will be outweighed by the benefits of producing new modules. The optimal balance is habitat dependent and is likely to depend on competitive pressures and on disturbance regimes.
We are grateful to heidrun huber and to two anonymous referees for commenting on previous versions of the manuscript.