Clonal plants could modify phenotypic responses to nutrients heterogeneously distributed both in space and time by physiological integration. It will take times to do phenotypic responses to modifications which are various in different growth periods. An optimal phenotype is reached when there is a match between nutrient conditions and foraging ability. A single plantlet of Buchloe dactyloides with two stolons was transplanted into heterogeneous nutrient conditions. One stolon grew in homogeneous nutrient patch, while the other cultured in different scales of heterogeneous nutrient patches. As compared to the other nutrient treatment, heterogeneous nutrient treatments with small scale of 25×25 cm resulted in a higher biomass, and larger number of ramets, clumps and stolons in B. dactyloides at both genet and clonal fragment levels. Significant differences of number of ramets, clumps and stolons were detected at the rapid growth stage, but not in the early stage of the experiment. Foraging ability was more efficient in heterogeneous than in homogeneous nutrient conditions as assessed by higher root mass and root to shoot ratio. Different nutrient treatments did not prompt significant differences in internode and root length. Physiological integration significantly increased biomass, but did not influence other growth or morphological characters. These results suggest that physiological integration modifies phenotypic plasticity of B. dactyloides for efficient foraging of nutrients in heterogeneous nutrient conditions. These effects are more pronounced at genet and clonal fragment levels when the patch scale is 25×25 cm. Time is a key factor when phenotypic plasticity of B. dactyloides in heterogeneous nutrient conditions is examined.
Citation: Luo D, Qian Y-Q, Han L, Liu J-X, Sun Z-Y (2013) Phenotypic Responses of a Stoloniferous Clonal Plant Buchloe dactyloides to Scale-Dependent Nutrient Heterogeneity. PLoS ONE 8(6): e67396. https://doi.org/10.1371/journal.pone.0067396
Editor: Miguel A. Blazquez, Instituto de Biología Molecular y Celular de Plantas, Spain
Received: January 12, 2013; Accepted: May 16, 2013; Published: June 27, 2013
Copyright: © 2013 Luo et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This research is supported by the National Natural Science Foundation of China (31070625, 31100505), grant for National Non-profit Research Institutions (CAFYBB2012043, RIF2010-11), and Beijing Natural Science Foundation (6122031). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
The availability of nutrients in natural habitats occurs at a variety of spatial and temporal scales. De Kroon et al.  proposed that a whole plant consists of many modules. Clonal plants can form large interconnected systems consisting of numerous connected modules for a period of time via the clonal growth –. Thus, the modules of a single clonal plant may occupy different quality patches –. This results in different parts of the same module or different modules of the same plant, expressing a range of phenotypic responses to their local conditions , .
Physiological integration is one of the most important traits of clonal plants as it can optimize the resource allocation among modules of the whole plant. It also allows transporting photosynthates, water, nutrients, and signals via connected stolon or rhizome internodes from source modules to sink modules of the same genet , . Physiological integration increases the capacity of resource acquisition and utilization for all integrated modules, and helps clonal plants to cope with complex habitats –. Since it will take times to do morphological reactions to physiological responses which are various in different growth periods, clonal plants may employ phenotypic plasticity as a behavioral adaptation to modify the suitability of variable habitats, exploiting favorable and avoiding unfavorable patches of habitats, by changing the responses at different growth periods –. De Kroon and Hutchings  indicated that increased branching in favorable conditions could be interpreted as a positive growth response. Plants might shorten their internodes to form the clumping ramets in order to maximize the acquisition of required nutrients in a local environment under favorable conditions. On the other hand, these internodes were extended to form the spreading ramets that explore new habitats when they grew in unfavorable conditions. Physiological integration among ramets modified morphological, physiological and mycorrhizal plasticity of roots to allow locating more roots in favorable patches to maximize the nutrient acquisition from heterogeneous habitats –.
Phenotypic responses of clonal plants to different nutrients depend on the spatial and temporal distribution of the nutrient, the size of patches selected for ramet placement, and the ability of nutrient acquisition –. Positive phenotypic responses are shown when all the above described factors are in harmony. Reactions of clonal plants to habitats involve the responses of its modules to localized conditions, and these responses are modified through physiological integration with other modules exposed to different conditions. This results in an integrated and adaptive response at the levels of individual modules and the whole plant. The present study was conducted to test the phenotypic responses of B. dactyloides to heterogeneous nutrients of different scales, measured as growth and morphological characters in homogeneous and three scales of heterogeneous treatments with the same amounts of essential nutrients in different growth periods. Phenotypic plasticity of a clonal plant under heterogeneous environments is affected by local conditions as well as the interactions between connected modules of the same genet in contrasting conditions . We thus also attempted to test the effects of physiological integration among the clonal fragments of B. dactyloides in heterogeneous nutrient conditions on phenotypic responses.
Materials and Methods
Plant Species and Experimental Material
Buchloe dactyloides, buffalograss, is a perennial herb of the Poaceae family with ramets connected by aboveground stolons. It can form large, morphologically and physically interconnected systems consisting of clonal modules of different levels via clonal growth . The plant material used in this study was a B. dactyloides clonal ramet with two new connected stolons, and the ramets were all in the same genotype and similar in size.
The experiment was carried out in natural light conditions at the Nan Yuan field station of Chinese Academy of Forestry (CAF) in early 2012 during the growing season. The boxes with dimensions 100×100×25 cm in size were placed into the field and filled with immature soil as the substrate. Four different nutrient treatments including one homogeneous nutrient and three scales of heterogeneous nutrient treatments were given within the boxes (Fig. 1). Treatment 1 (T1) consisted of one homogeneous and one large scale (50×50 cm) heterogeneous nutrient patches; Treatment 2 (T2) consisted of one homogeneous and one middle scale (50×25 cm) heterogeneous nutrient patches; Treatment 3 (T3) consisted of one homogeneous and one small scale (25×25 cm) heterogeneous nutrient patches; Treatment 4 (T4) consisted of two homogeneous nutrient patches. Adjacent nutrients in the same box were physically separated and a single plantlet with two stolons was transplanted to the centre of the box. It might acquire additional resources when the ramet extends over the box. This will affect results of experiment. Thus, the plants were allowed to grow for only seven weeks to ensure not rooting beyond the boxes. There were six replicates for each nutrient treatment. The total nutrient supply was the same in all nutrient treatments. Each treatment contained 150.0 g of controlled release fertilizer Osmocote 313s (16-9-12-2.5MGO +TE, Everris, ICL Group). This nutrient was considered sufficient maintaining the growth of B. dactyloide during the experiment.
The boxex used in this study were 100×100×25 cm in size. Three scales of heterogeneous nutrient treatments and one homogeneous nutrient treatment, coded as T1, T2, T3 and T4, were implemented in the boxes. The box was divided into two parts, one was filled with homogeneous nutrient and the other with 3 scales of heterogeneous nutrients (the three small boxes were divided respectively into two, four and eight patches, half of patches in each small box were filled with high nutrient and the other half low nutrient).
Harvests and Measurements
The growth characters included the number of ramets, clumps and stolons, aboveground mass, root mass, total mass and root to shoot ratio. The clumps were defined as the nodes from which the new ramets, stolons and roots produced. The morphological characters included the internode and root length. The number of ramets, clumps and stolons were recorded once a week. After seven weeks of growth, the aboveground and root parts of B. dactyloides were harvested separately, dried at 108°C for 30 min, then at 80°C to a constant weight, and biomass was recorded. The morphological characters were also measured. All the characters were recorded separately from each nutrient patch.
Multivariate analysis of variance (MANOVA) followed by Duncan’s Multiple Range Tests (DMRT) was used to compare the differences of number of ramets, number of clumps and number of stolons surveyed at the same time among the four different treatments at genet level, and between homogeneous and heterogeneous patches of the same treatment at clonal fragment level. Independent t-test was used to determine the means of the growth and morphological characters between homogeneous and heterogeneous patches of the same treatment at the end of the experiment (on the 49th day). One-way ANOVA followed by DMRT was used to compare the means of growth and morphological characters among homogeneous patch of homogeneous nutrient treatment and heterogeneous patches of the three scales of heterogeneous nutrient treatments on the 49th day. Analyses in this study were conducted with SPSS 16.0 (SPSS, Chicago, IL, USA).
The number of ramets, clumps and stolons significantly increase as time progressed, and the significant differences were found among the four nutrient treatments at different times (Fig. 2, Table 1), the number of ramets and clumps differed on the 7th, 14th, 42nd and 49th days while the number of stolons differed on the 14th, 35th and 49th days (Table 2). At the end of the experiment (the 49th day), the number of ramets, clumps and stolons were higher in the heterogeneous (T1, T2 and T3) than in the homogeneous nutrient treatments (T4), but no significant differences were observed among the three heterogeneous nutrient treatments (Fig. 2A, B, C). Aboveground mass, root mass and total mass were the highest at the small scale (T3, 25×25 cm) heterogeneous nutrient treatment (Fig. 2D). Root to shoot ratio was the highest at the middle scale (T2, 50×25 cm) heterogeneous nutrient treatment (Fig. 3A). No significant differences were observed in internode length or root length among the four nutrient treatments (Fig. 3B, C).
The growth characters include number of ramets (A), number of clumps (B), number of stolons (C) and biomass (D). The biomass include total mass, aboveground mass and root mass. Bars are mean values (± S. E.). Bars sharing the same letters are not different at p = 0.05. Treatment codes are in Figure 1.
Mean values (± S. E.) of root to shoot ratio (A), internode length (B) and root length (C) are given. Bars sharing the same letters are not different at p = 0.05. Treatment codes are in Figure 1.
The number of ramets, clumps and stolons significantly increased as time progressed, and the significant differences were found between the homogeneous and heterogeneous patches of the same nutrient treatments at different times (Fig. 4A, B, C, Table 2), the number of ramets and clumps were higher in heterogeneous than in homogeneous patches of the same middle or small scale (T2, 50×25 cm or T3, 25×25 cm) nutrient treatment on the 42nd and 49th days (Table 2). Root mass was higher in heterogeneous than homogeneous patches of the same large or small scale (T1, 50×50 cm or T3, 25×25 cm) nutrient treatment (Fig. 4F), while no significant differences were observed in aboveground mass, total mass, root to shoot ratio, internode length or root length (Figs. 4D, E, 5A, B, C).
The growth characters include number of ramets, clumps, stolons, aboveground mass, root mass and total mass. Mean values (± S. E.) of number of ramets (A), number of clumps (B), number of stolons (C), total mass (D), aboveground mass (E) and root mass (F) between the homogeneous and heterogeneous patches of the same treatment are given. * means P<0.05. Mean values (± S. E.) of the growth characters in the heterogeneous (D) and homogeneous patches (E) are given. * means P<0.05. ns means P>0.05. Treatment codes are in Figure 1.
Mean values (± S. E.) of root to shoot ratio (A), internode length (B) and root length (C) between the homogeneous and heterogeneous patches of the same treatment are given. * means P<0.05. ns means P>0.05. Treatment codes are in Figure 1.
The number of ramets, clumps and stolons were higher in heterogeneous patches of heterogeneous nutrient treatments than homogeneous patch of homogeneous nutrient treatment, but no significant differences were observed in heterogeneous patches of the three scales of heterogeneous nutrient treatments (Fig. 6A). Aboveground mass, root mass, total mass and root to shoot ratio were highest in small scale (T3, 25×25 cm) heterogeneous patches (Figs. 6B, 7A). No significant differences were observed in internode and root length (Fig. 7B, C). The number of ramets, clumps and stolons were larger in homogeneous patches of large scale (T1, 50×50 cm) heterogeneous nutrient treatments than the homogeneous patches of the other treatments (T2-T4, Fig. 6A). Aboveground mass, root mass and total mass were the highest in homogeneous patches of small scale (T3, 25×25 cm) heterogeneous nutrient treatments (Fig. 6B). No significant differences were found in root to shoot ratio, internode length or root length (Fig. 7A, B, C).
The growth characters include number of ramets, clumps, stolons (A) and biomass (B). Bars are mean values (± S. E.). Bars sharing the same letters are not different at p = 0.05. Treatment codes are in Figure 1.
Physiological integration among clonal ramets modifies the growth of clonal plant at module and genet level, enables the plants to cope with complex habitats –. The growth of B. dactyloides was found to be significantly affected by nutrient distribution in soil. Compared to the homogeneous nutrient conditions, the growth characters were relatively higher in the heterogeneous conditions at genet level. These results are concurrent with previous reports on the effect of nutrient distribution on clonal growth , –. Significant differences were also detected in the heterogeneous nutrient conditions at clonal fragment level. Meanwhile, the phenotypic response to heterogeneous nutrients was also strongly determined by the nutrient patch scale. Since the growth characters were greater in the 25×25 cm nutrient conditions at both genet and clonal fragment levels, the phenotypic responses of B. dactyloides to heterogeneous nutrient conditions were more effective in small-size patch .
In contrast to the research of Wijesinghe and Hutchings , no significant differences were found in root length highlighting the physiological integration did not affect the morphological plasticity to all nutrient conditions in this study, however, the aboveground mass and root mass showed a greater root to shoot ratio. This indicates the roots to grow better in heterogeneous at the genet and clonal fragment levels especially at the smaller scale of 50×25 cm or 25×25 cm –. There were no marked differences in internode length in either the heterogeneous or the homogeneous nutrient conditions. This was in contrast to the escape theory that posited that ramets growing in worse conditions generated a smaller number of longer internodes to escape the unfavorable conditions –. Nevertheless, a greater root biomass and the same internode length could be an indication of a stronger nutrient-capture capacity in heterogeneous nutrient conditions. Therefore, our study demonstrates that the physiological integration increases the nutrient-foraging capability of B. dactyloides clonal ramets for acquiring more nutrients from the middle and small scales nutrient conditions.
The phenotypic responses of clonal plants are various at different growth and development stages, and the clonal plants by their own expansion might themselves reduce heterogeneity among different environments. A few studies have implicated the time as a key factor to examine their phenotypic response to heterogeneous nutrients –. However, at the early stage, differences due to nutrient variability were not detected in number of ramets, clumps and stolons. As a result of the preferential allocation of the ramet to different nutrient conditions, significant differences were found at the rapid growth stage, when relatively optimal ramet spacing was achieved in small scale heterogeneous nutrient conditions. Significant changes in growth characters were observed because of different growth stages but not the nutrient depletion , .
In conclusion, our results support the module concept of de Kroon , and indicate that physiological integration modifies the phenotypic responses of B. dactyloides clonal ramets for efficient foraging of nutrients in heterogeneous nutrient conditions. These effects are more pronounced at genet and clonal fragment levels in the patch scale of 25×25 cm. For the different morphological responses at different growth periods, time should be taken into account when examine the phenotypic plasticity of B. dactyloides in heterogeneous nutrient conditions.
We thank Jia Hao, Shu-hua Song and Gu Gong for assistance with harvest and measurements.
Conceived and designed the experiments: DL YQQ ZYS. Performed the experiments: DL YQQ. Analyzed the data: DL LH. Contributed reagents/materials/analysis tools: DL YQQ JXL. Wrote the paper: DL YQQ.
- 1. de Kroon H, Huber H, Stuefer JF, van Groenendael J (2005) A modular concept of phenotypic plasticity in plants. New Phytol 166: 73–82.
- 2. Price EAC, Marshall C (1999) Clonal plants and environmental heterogeneity. Plant Ecol 141: 3–7.
- 3. Oborny B, Bartha S (1995) Clonality in plant communities - an overview. Abst Bot 19: 115–127.
- 4. Klimeš L, Klimesova J, Hendriks R, van Groenendael J (1997) Clonal plant architecture: A comparative analysis of form and function. In de Kroon H, van Groenendael J, eds. The Ecology and Evolution of Clonal Plants. Backhuys Publishers, Leiden, The Netherlands. 1–29.
- 5. Jackson RB, Caldwell MM (1993) Geostatistical patterns of soil heterogeneity around individual perennial plants. J Ecol 81: 683–692.
- 6. Farley RA, Fitter AH (1999) The responses of seven co-occurring woodland herbaceous perennials to localized nutrient-rich patches. J Ecol 87: 849–859.
- 7. Caldwell MM, Pearcy RW (1994) Exploitation of environmental heterogeneity in plants: ecophysiological processes above- and belowground. Academic Press, San Diego, California.
- 8. Hutchings MJ, Wijesinghe DK, John EA (2000) The effects of heterogeneous nutrient supply on plant performance: a survey of responses, with special reference to clonal herbs. In: Hutchings MJ, John EA, Stewart AJA, eds. The ecological consequences of environmental heterogeneity. Blackwell, Oxford. 91–110.
- 9. Ryel RJ, Caldwell MM (1996) Nutrient acquisition from soils with patchy nutrient distribution as assessed with simulation models. Ecology 79: 2735–2744.
- 10. Stuefer JF (1996) Potential and limitations of current concepts regarding the response of clonal plants to environmental heterogeneity. Vegetatio 127: 55–70.
- 11. Cain ML, Subler S, Evans JP, Fortin MJ (1999) Sampling spatial and temporal variation in soil nitrogen. Oecologia 118: 397–404.
- 12. Hutchings MJ, de Kroon H (1994) Foraging in plants: the role of morphological plasticity in resource acquisition. Adv Ecol Res 25: 159–238.
- 13. Huber H, Fijan A, During H (1998) A comparative study of spacer plasticity in erect and stoloniferous herbs. Oikos 81: 576–586.
- 14. Slade AJ, Hutchings MJ (1987) An analysis of the costs and benefits of physiological integration between ramets in the clonal perennial herb Glechoma hederacea. Oecologia 73: 425–431.
- 15. Saitoh T, Seiwa K, Nishiwaki A (2002) Importance of physiological integration of dwarf bamboo to persistence in forest under storey: a field experiment. J Ecol 90: 78–85.
- 16. Hartnett DC, Bazzaz FA (1983) Physiological integration among intraclonal ramets in Solidago canadensis. Ecology 64: 779–788.
- 17. Stuefer JF, During HJ, de Kroon H (1994) High benefits of clonal integration in two stoloniferous species, in response to heterogeneous light environments. J Ecol 82: 511–518.
- 18. Wijesinghe DK, Handel ST (1994) Advantages of clonal growth in heterogeneous habitats: an experiment with Potentilla simplex. J Ecol 82: 495–502.
- 19. Roiloa SR, Retuerto R (2005) Presence of developing ramets of Fragaria vesca L. increases photochemicals in parent ramets. Int J Plant Sci 166: 795–803.
- 20. Pitelka LF, Ashmun JW (1985) Physiology and integration of ramets in clonal plants. In: Jackson JBC, Population biology and evolution of clonal organisms. Yale University Press, New Haven, Connecticut, USA. 399–435.
- 21. Schmid B (1990) Some ecological and evolutionary consequences of modular organization and clonal growth in plants. Evol Trends in Plants 4(1): 25–34.
- 22. Alpert P (1996) Nitrogen sharing in natural clonal fragments of Fragaria chiloensis. Ecology 84: 395–406.
- 23. Alpert P (1999) Clonal integration in Fragaria chiloensis differs between populations: ramets from grassland are selfish. Oecologia 120: 69–76.
- 24. Marshall C, Price EAC (1999) Clonal plants and environmental heterogeneity - space, time and scale. Plant Ecol 141: 1–199.
- 25. Yu FH, Wang N, He WM, Chu Y, Dong M (2008) Adaptation of rhizome connections in drylands: Increasing tolerance of clones to wind erosion. Ann Bot 102: 571–577.
- 26. Wang N, Yu FH, Li PX, He WM, Liu FH, et al. (2008) Clonal integration affects growth, photosynthetic efficiency and biomass allocation, but not the competitive ability, of the alien invasive Alternanthera philoxeroides Ann Bot. 101: 671–678.
- 27. He WM, Alpert P, Yu FH, Zhang L-L, Dong M (2011) Reciprocal and coincident patchiness of multiple resources differentially affect benefits of clonal integration in two perennial plants. J Ecol 99: 1202–1210.
- 28. Roiloa SR, Retuerto R (2006) Small scale in soil quality influences photosynthetic efficiency and habitat selection in a clonal plant. Ann bot 98: 1043–1052.
- 29. de Kroon H, Schieving F (1990) Resource partitioning in relation to clonal growth strategy. In: van Groenendael J, de Kroon H, eds. Clonal Growth in Plants: Regulation and Function. SPB Academic Publishing, The Hague, The Netherlands. 113–130.
- 30. Jackson RB, Caldwell MM (1996) Integrating resource heterogeneity and plant plasticity: modeling nitrate and phosphate uptake in a patchy soil environment. J Ecol 84, 891–903.
- 31. Pigliucci M, Pollard H, Cruzan MB (2003) Comparative studies of evolutionary responses to light environments in Arabidopsis. Am Nat 161: 68–82.
- 32. Weinig C, Delph LF (2001) Phenotypic plasticity early in life constrains developmental responses later. Evolution 55: 930–936.
- 33. Yu FH, Wang N, Alpert P, He WM, Dong M (2009) Physiological integration in an introduced, invasive plant increases its spread into experimental communities and modifies their structure. Am J Bot 96: 1983–1989.
- 34. de Kroon H, Hutchings MJ (1995) Morphological plasticity in clonal plants: the foraging concept reconsidered. J Ecol 83: 143–152.
- 35. Oborny B (1994) Spacer length in clonal plants and efficiency of resource capture in heterogeneous environments: a Monte Carlo simulation. Folia Geobot Phytotaxon 29: 139–158.
- 36. Oborny B, Cain ML (1997) Models of spatial spread and foraging in clonal plants. In: de Kroon H, van Groenendael J, eds. The Ecology and Evolution of Clonal Plants. Backhuys Publishers, Leiden, The Netherlands. 155–183.
- 37. Skálová H, Krahulec F (1992) The response of three Festuca rubra clones to changes in light quality and plant density. Func Ecol 6: 282–290.
- 38. de Kroon H, Schieving F (1990) Resource partitioning in relation to clonal growth strategy. In: van Groenendael J, de Kroon H, eds. Clonal growth in plants: regulation and function. SPB Academic Publishing, The Hague. 113–130.
- 39. Cain ML (1994) Consequences of foraging in clonal plant species. Ecology 75: 933–944.
- 40. Dong M, de Kroon H (994) Plasticity in morphology and biomass allocation in Cynodon dactylon, a grass species forming stolons and rhizomes. Oikos 70: 99–106.
- 41. Wijesinghe DK, Hutchings MJ (1997) The effects of spatial scale of environmental heterogeneity on the growth of a clonal plant: an experimental study with Glechoma hederacea. J Ecol 85: 17–28.
- 42. Wijesinghe DK, John EA, Beurskens S, Hutchings MJ (2001) Root system size and precision in nutrient foraging: responses to spatial pattern of nutrient supply in six herbaceous species. J Ecol 89: 972–983.
- 43. Day KJ (2001) Studies of the effects of spatial heterogeneity in nutrient supply on plants and their populations. DPhil Thesis. University of Sussex, UK.
- 44. Qian YQ, Li DY, Han L, Sun ZY (2010) Inter-ramet photosynthate translocation in buffalograss under differential water stress. J Am Soc Hortic Sci 135(4): 308–314.
- 45. Salzman AG, Parker MA (1985) Neighbours ameliorate local salinity stress for a rhizomatous plant in a heterogeneous environment. Oecologia 65: 273–277.
- 46. Friedman D, Alpert P (1991) Reciprocal transport between ramets increases growth of Fragaria chiloensis when light and nitrogen occur in separate patches but only if patches are rich. Oecologia 86: 76–80.
- 47. Evans JP, Whitney S (1992) Clonal integration across a salt gradient by a nonhalophyte, Hydrocotyle bonariensis (Apiaceae). Am J Bot 79: 1344–1347.
- 48. Bullock JM, Mortimer AM, Begon M (1994) Physiological integration among tillers of Holcus lanatus: Agedependence and responses to clipping and competition. New Phytol 128: 737–747.
- 49. Stuefer JF, de Kroon H, During H (1996) Exploitation of environmental heterogeneity by spatial division of labour in a clonal plant. Funct Ecol 10: 328–334.
- 50. Alpert P, Stuefer JF (1997) Division of labour in clonal plants. In: de Kroon H, van Groenendael J, eds. The ecology and evolution of clonal plants. Backhuys Publishers, Leiden. 137–154.
- 51. Song YB, Yu FH, Keser HL, Dawson W, Fischer M, et al. (2013) United we stand, divided we fall: a meta-analysis of experiments on clonal integration and its relationship to invasiveness. Oecologia 171: 317–327.
- 52. Xu L, Yu FH, van Drunen E, Schieving F, Dong M, et al. (2012) Trampling, defoliation and physiological integration affect growth, morphological and mechanical properties of a root-suckering clonal tree. Ann Bot 109: 1001–1008.
- 53. Liu HD, Yu FH, He WM, Chu Y, Dong M (2009) Clonal integration improves compensatory growth in heavily grazed ramet populations of two inland dune grasses. Flora 204: 298–305.
- 54. Brezina S, Koubek T, Munzbergova Z, Herben T (2006) Ecological benefits of integration of Calamagrostis epigejos ramets under field conditions. Flora 201: 461–467.
- 55. Roiloa SR, Alpert P, Tharayil N, Hancock G, Bhowmik PC (2007) Greater capacity for division of labour in clones of Fragaria chiloensis from patchier habitats. J Ecol 95: 397–405.
- 56. Birch CPD, Hutchings MJ (1994) Exploitation of patchily distributed soil resources by the clonal herb Glechoma hederacea. J Ecol 82: 653–664.
- 57. Wijesinghe DK, Hutchings MJ (1999) The effects of environmental heterogeneity on the performance of Glechoma hederacea: the interaction between patch contrast and patch scale. J Ecol 87: 860–872.
- 58. Einsmann JC, Jones RH, Pu M, Mitchell RJ (1999) Nutrient foraging traits in 10 co-occurring plant species of contrasting life forms. J Ecol 87: 609–619.
- 59. van Vuuren MMI, Robinson D, Griffiths BS (1996) Nutrient inflow and root proliferation during the exploitation of a temporally and spatially discrete source of nitrogen in soil. Plant Soil 178: 185–192.
- 60. Fransen B, de Kroon H, Berendse F (1998) Root morphological plasticity and nutrient acquisition of perennial grass species from habitats of different nutrient availability. Oecologia 115: 351–358.
- 61. Hodge A, Robinson D, Griffiths BS, Fitter AH (1999) Nitrogen capture by plants grown in N-rich organic patches of contrasting size and strength. J Exp Bot 50: 1243–1252.
- 62. de Kroon H, Schieving F (1990) Resource partitioning in relation to clonal growth strategy. In: van Groenendael J, de Kroon H, eds. Clonal Growth in Plants: Regulation and Function. SPB Academic Publishing, The Hague, The Netherlands. 113–130.
- 63. Skálová H, Krahulec F (1992) The response of three Festuca rubra clones to changes in light quality and plant density. Funct Ecol 6: 282–290.
- 64. Huber-Sannwald E, Pyke DA, Caldwell MM, Durham S (1998) Effects of nutrient patches and root system on the clonal plasticity of a rhizomatous grass. Ecology 79: 2267–2280.
- 65. Welham CVJ, Turkington R, Sayre C (2002) Morphological plasticity of white clover (Trifolium repens L.) in response to spatial and temporal resource heterogeneity. Oecologia 130: 231–238.
- 66. Macek P, Lepš J (2003) The effect of environmental heterogeneity on clonal behaviour of Prunella vulgaris L. Plant Ecol. 168: 31–43.
- 67. Gersani M, Sachs T (1992) Development correlations between roots in heterogeneous environments. Plant Cell Environ 15: 463–469.
- 68. Gruntman M, Novoplansky A (2004) Physiologically mediated self/non-self discrimination in roots. PNAS 101: 3863–3867.