Physiological integration impacts nutrient use and stoichiometry in three clonal plants under heterogeneous habitats
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- He, W., Yu, F. & Zhang, L. Ecol Res (2010) 25: 967. doi:10.1007/s11284-010-0724-0
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Physiological integration facilitates clonal plants to deal with heterogeneous resources. However, little is known about how nutrient patchiness affects its use and stoichiometry in clonal plants. We conducted an experiment with Cynodon dactylon, Glechoma longituba, and Potentilla reptans to address the effects of physiological integration on nutrient use efficiency and N:P ratios. For C. dactylon, the effects of nutrient patchiness on N use efficiency (NUE), P use efficiency (PUE), and N:P ratio were stronger in daughter ramets than in parent ramets; for G. longituba, nutrient patchiness affected PUE and N:P ratio of parent and daughter ramets, but not NUE; for P. reptans, nutrient patchiness decreased NUE, PUE, and N:P ratio, regardless of parent or daughter ramets. PUE was associated with N:P ratios in three clonal plants and this association of NUE with N:P ratios varied with species. Our findings suggest that physiological integration alters nutrient use efficiency and N:P ratios of clonal plants under patchy nutrients and that these effects are linked to clonal species identity.
KeywordsCynodon dactylonGlechoma longitubaNutrient use efficiencyPhysiological integrationPotentilla reptansSoil nutrient patchesStoichiometry
In nature, resources essential to plant growth and reproduction are patchily distributed (Kolasa and Pickett 1991; Caldwell and Pearcy 1994; Price and Marshall 1999; He et al. 2004). Clonal plants with long spacers usually position their ramets in different resource patches and tend to exhibit diverse strategies to deal with such patchiness such as biomass allocation and division of labor (Alpert and Mooney 1986; van Groenendael and de Kroon 1990; Alpert 1991, 1996; Stuefer 1996; Hutchings and Wijesinghe 1997). There are two types of resource transfer within clones: acropetal movement (from older ramets to younger ramets) and basipetal movement (from younger ramets to older ramets) (Alpert and Mooney 1986; Alpert 1991, 1996; Dietz and Steilein 2001).
Here we focus on soil N and P only because both elements are the two most limiting elements to terrestrial plants (Güsewell 2004; Reich and Oleksyn 2004; Lovelock et al. 2007; Elser et al. 2007). The movement of nutrients among ramets is mainly acropetal (Alpert and Mooney 1986; Price and Hutchings 1992). Nutrient status in clonal plants is related to two processes: direct nutrient uptake by ramets per se and nutrient transfer among ramets. Given that nutrient patchiness induces nutrient transfer, this process may confer influences on nutrient use efficiency and stoichiometry (i.e., the quantitative relationships between constituents in a chemical substance, Sterner and Elser 2002).
Since natural resources are heterogeneous, it is required to consider nutrient use and stoichiometry under the context of heterogeneity. However, it remains poorly understood how heterogeneous resources impact resource use efficiencies and stoichiometry of plants. It is well documented that physiological integration allows clonal plants to benefit from patchy environments. To our knowledge, no studies explicitly address the effects of physiological integration on nutrient use efficiency and stoichiometry in clonal plants. In fact, such studies can deepen our understanding of the adaptation of clonal plants to patchy habitats.
We hypothesize that physiological integration affects nutrient use efficiency and stoichiometry of parent and daughter ramets growing in different soil patches, created due to different soil nutrient availabilities. More specifically, when parent ramets are grown in high nutrient conditions and daughter ramets are grown in low nutrient conditions, we predict that (1) parent ramets exhibit increased nutrient use efficiency as a compensatory response to meet the resource demand from daughters under nutrient-poor conditions, (2) parent ramets show flexible N:P ratios because this ratio varies with plant strategies (i.e., stress-tolerant > competitive > ruderal) (Güsewell 2004), and (3) daughter ramets have relatively conservative nutrient-use efficiency and N:P ratios in that they can obtain nutrients from their parent ramets and depend less on local patches. Additionally, we discuss the likely associations of nutrient use efficiency with N:P ratios.
It is important to note that we selected three clonal species to obtain a more general conclusion. Cynodon dactylon prefers to occupy disturbed habitats, Potentilla reptans prefers to appear in undisturbed habitats, and Glechoma longituba usually grows in these two types of habitats. In other words, three species may exhibit habitat preference.
Cynodon dactylon (L.) Pess., a perennial grass, is composed of three types of modules (plagiotropic stolons and rhizomes, and orthotropic shoots), and is widely distributed in China (Editorial Board of Flora of China 1990). Glechoma longituba L., a perennial stoloniferous herb, has two zygomorphic leaves, whose leaf axil bears one bud that may grow into a secondary stolon, and it often grows in forests, on roadsides, or by creeks (Wu and Chen 1974). Potentilla reptans L., a perennial stoloniferous herb, consists of a number of ramets interconnected by stolons, whose spacer length spans from 10 to 20 cm, and it prefers to inhabit humid and shaded environments (Editorial Board of Flora of China 1985). From here on, these three species are referred to with their genus names only.
At the end of the experiment, all ramets were harvested, dried at 85°C for 48 h, and then weighed. All the oven-dried materials were ground into a fine powder for N and P analyses. The N content was determined by extracting with 25 ml of 2 M KCl and through analyzing with a Skalar SANplus Segmented Flow Analyzer (Skalar Analytical B.V., the Netherlands), and the P content was determined by extracting with 25 ml mixture of 0.05 M HCl and 0.025 M H2SO4 and through analyzing with a UV–visible spectrophotometer (UV-2550, Shimadzu Corporation, Japan). The total amounts of N and P per plant were calculated through whole-plant biomass by N and P concentrations in the determined samples. The N:P ratios were expressed as mass ratios (g N/g P). Nutrient (i.e., N and P) use efficiency (g g−1), defined as the carbon fixation per unit nutrient taken up, was calculated as the ratio of total biomass to total N or P.
This experiment covered three contrasts: comparison of ramets from uniform low nutrients versus uniform high nutrients, comparison of daughter ramets from a nutrient-low patch versus uniform low nutrients, and comparison of parent ramets from a nutrient-high patch versus uniform high nutrients. All comparisons were carried out between parent ramets growing in different habitats or between daughter ramets growing in different habitats. We did not compare parent ramets with daughter ramets and neither did we compare two types of ramets grown in a patchy soil.
Student’s t test was used to examine whether there were differences at p = 0.05 in N:P ratios, N use efficiency (NUE), and P use efficiency (PUE) within a contrast. One-way ANOVA was used to test whether the inter-specific variations were significant at p = 0.05 in N:P ratios, NUE, and PUE. None of the data was transformed because it met the ANOVA requirements. All statistical analyses were conducted using SPSS (13.0 SPSS).
Soil nutrient patchiness affected NUE of Cynodon and Potentilla, but not Glechoma (Fig. 2d–f). Specifically, soil patchiness increased NUE of Cynodon, decreased NUE of Potentilla, and had no effect on NUE of Glechoma, regardless of parent ramets in high nutrients or daughter ramets in low nutrients. Soil nutrient patchiness affected PUE in three species. For daughter ramets under low nutrients, soil patchiness decreased PUE of Cynodon and Potentilla, but increased PUE of Glechoma; for parent ramets under high nutrients, soil patchiness had no effect on PUE of Cynodon, but decreased PUE of Glechoma and Potentilla (Fig. 2g–i).
Not all parent ramets in three clonal plants exhibited higher nutrient use efficiency (NUE) in patchy habitats than corresponding counterparts in uniform high nutrients, which partially supports our first prediction that parent ramets exhibit increased NUE. Specifically, soil nutrient patchiness decreased, enhanced, or had no effect on NUE in parent ramets of Cynodon, Glechoma, and Potentilla. Nutrient use strategy is directly linked to the adaptation of plants to their habitats (Aerts and Chapin 2000). The parent ramets of Cynodon, Glechoma, and Potentilla exhibited different strategies to deal with nutrient patchiness. Given that heterogeneity can induce clonal plants in patchy nutrients to share nutrients among interconnected ramets (Alpert and Mooney 1986; van Groenendael and de Kroon 1990; Stuefer 1996; Hutchings and Wijesinghe 1997), this patchiness-induced effect on NUE may be associated with physiological integration.
Soil nutrient patchiness had no effect on the N:P ratio in parent ramets of Cynodon, but greatly decreased N:P ratios in parent ramets of Glechoma and Potentilla, suggesting that parent ramets of Glechoma and Potentilla, but not Cynodon, are sensitive to nutrient patchiness. These findings partially support our second prediction that parent ramets exhibit flexible N:P ratios. This flexibility may be associated with different adaptive strategies of parent ramets to cope with short soil N. One likely consequence of decreased N:P ratios is that nutrient patchiness reduces the soil N limitation to plant performance, because soil N is the scarcest element to terrestrial plants relative to other soil nutrients (Kay et al. 2005). In addition, the interspecific variations in N:P ratios suggest that the soil N limitation to plants may decrease in the order, Glechoma > Potentilla > Cynodon.
The N:P ratio is regulated primarily via adjusting N and P uptake rates induced by signaling mechanisms that are sensitive to the composition of the phloem (Imsande and Touraine 1994; Raghotama 1999; Forde 2002; Tournier et al. 2006). This regulation is positive and negative: N-deficient plants can increase the rate of N uptake and reduce the rate of P uptake while P-deficient plants follow the opposite direction (Aerts and Chapin 2000). Internal nutrient translocation also can influence N:P ratios of individual plant organs such as leaves, stems, and rhizomes (Güsewell 2004, 2005).
For daughter ramets, soil nutrient patchiness increased NUE of Cynodon and N:P ratio and PUE of Glechoma, and decreased N:P ratios and PUE of Cynodon and Potentilla and NUE of Potentilla. These findings totally do not support our third prediction that daughter ramets have relatively conservative nutrient use efficiency and N:P ratios. In other words, daughter ramets are flexible in NUE and N:P ratios. Thus, daughter ramets strongly exhibit non-local responses to nutrient patchiness and physiological integration confers key impacts on the performance of daughter ramets growing patchy habitats.
Changing N:P ratios are linked to important aspects of ecological functioning (Elser and Urabe 1999). Cherif and Loreau (2007) proposed that stoichiometry constrains resource use. N:P ratios and PUE exhibited similar response to nutrient patchiness in Cynodon,Glechoma, and Potentilla. In other words, PUE is closely associated with N:P ratios in these three plants. The association of N:P ratios with NUE was detected in Potentilla, but not in Cynodon and Glechoma, suggesting that this relationship varies with species. Thus, patchiness-induced changes in N:P ratios may be associated with nutrient use efficiency and these associations may exhibit species-dependence. Additionally, changing N:P ratios also affect the physiological responses of plants (Elser and Urabe 1999; Güsewell 2004; Cherif and Loreau 2007).
In summary, our study is the first to provide evidence for the effects of physiological integration on nutrient use efficiency and stoichiometry in clonal plants. Specifically, physiological integration greatly alters nutrient use efficiencies and N:P ratios in parent or daughter ramets of three clonal plants that grew in heterogeneous habitats; there are close links between nutrient use efficiency and N:P ratios; daughter ramets exhibit more sensitivity to patchy nutrients than do parent ramets. Additionally, these effects are linked to clonal species identity and nutrient elements per se. For example, the changes in nutrient use efficiency and N:P ratio with patchiness differed among Cynodon, Glechoma, and Potentilla, and the effects of physiological integration depend on nutrient availability in a given patch. In other words, clonal species identity and nutrient availability matter in determining links between nutrient patchiness and nutrient use efficiency or stoichiometry in clonal plants.
We are grateful to Giles C. Thelen at the University of Montana for his checking and polishing the language of this paper. This work was funded by grants from the National Natural Science Foundation of China (30770335 & 30870395).