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Stipa Tenacissima Does Not Affect the Foliar Δ13c and Δ15n of Introduced Shrub Seedlings in a Mediterranean Semi-Arid Steppe

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Stipa Tenacissima Does Not Affect the Foliar Δ13c and Δ15n of Introduced Shrub Seedlings in a Mediterranean Semi-Arid Steppe Journal of Integrative Plant Biology 2006, 48 (8): 897−905 Stipa tenacissima Does not Affect the Foliar δ13C and δ15N of Introduced Shrub Seedlings in a Mediterranean Semi-arid Steppe Fernando T. Maestre1, 2*, Susana Bautista1, 3 and Jordi Cortina1 (1. Departamento de Ecología, Universidad de Alicante, Apartado de correos 99, 03080 Alicante, Spain; 2. Department of Biology, Duke University, Phytotron Building, Science Drive, Box 90340, Durham, North Carolina 27708-0340, USA; 3. Centro de Estudios Ambientales del Mediterráneo, C/ Charles Darwin 14, 46980 Paterna, Spain) Abstract Recent studies have shown that the tussock grass Stipa tenacissima L. facilitates the establishment of late-successional shrubs, in what constitutes the first documented case of facilitation of woody plants by grasses. With the aim of increasing our knowledge of this interaction, in the present study we investigated the effects of S. tenacissima on the foliar δ13C, δ15N, nitrogen concentration, and carbon : nitrogen ratio of introduced seedlings of Pistacia lentiscus L., Quercus coccifera L., and Medicago arborea L. in a semi-arid Mediterranean steppe. Six months after planting, the values of δ13C ranged between –26.9‰ and –29.6‰, whereas those of δ15N ranged between –1.9‰ and 2.7‰. The foliar C : N ratio ranged between 10.7 and 53.5, and the nitrogen concentration ranged between 1.0% and 4.4%. We found no significant effect of the microsite provided by S. tenacissima on these variables in any of the species evaluated. The values of δ13C were negatively correlated with predawn water potentials in M. arborea and were positively correlated with relative growth rate in Q. coccifera. The values of δ15N were positively correlated with the biomass alloca- tion to roots in the latter species. The present results suggest that the modification of environmental conditions in the are surrounding S. tenacissima was not strong enough to modify the foliar isotopic and nitrogen concentration of shrubs during the early stages after planting. Key words: facilitation; Medicago arborea; Pistacia lentiscus; Quercus coccifera; stable isotopes; steppe; Stipa tenacissima. Maestre FT, Bautista S, Cortina J (2006). Stipa tenacissima does not affect the foliar δ13C and δ15N of introduced shrub seedlings in a Mediterranean semi-arid steppe. J Integr Plant Biol 48(8), 897−905. www.blackwell-synergy.com; www.jipb.net In arid and semi-arid ecosystems, vegetation is sparse and ing to the development of “resource islands” under the discrete spatial distribution of soil properties is markedly patchy, lead- plant patches surrounded by relatively infertile soils (Schlesinger and Pilmanis 1998; Reynolds et al. 1999). These resource is- lands are points of high biological activity where facilitation Received 29 Nov. 2005 Accepted 6 Apr. 2006 may be the dominant interaction between the plant species Supported by the REDMED collaborative research project (contract number forming the patch (Callaway 1995; Cheng et al. 2006). Facilita- ENV4-CT97-0682). tive interactions strongly influence the dynamics of plant Publication of this paper is supported by the National Natural Science patches in arid and semi-arid ecosystems, and are a key force Foundation of China (30424813) and Science Publication Foundation of the shaping their structure and functioning (Whitford 2002). Chinese Academy of Sciences. Stable carbon and nitrogen isotope ratios (δ13C and δ15N, *Author for correspondence. Tel: +94 91 488 8511; Fax: +94 91 664 7490; E- respectively) are a powerful tool to evaluate the physiological mail: <[email protected]>. status of plant, and are becoming increasingly used to under- Present address: Unidad de Biodiversidady Conservación, Escuela Supe- stand plant-plant interactions in semi-arid areas (e.g. Williams rior de Ciencias Experimentalesy Tecnológicas, Universidad Rey Juan et al. 1991; Ehleringer 1993; Gebauer et al. 2000). The δ13C of Carlos, c/ Tulipán s/n, 28933 Móstoles, Spain. plant leaf tissues is a useful index of long-term water use 898 Journal of Integrative Plant Biology Vol. 48 No. 8 2006 efficiency (WUE), defined as the ratio between photosynthe- study site was only 55 mm, 51% of the 30 yr average at the sis per unit leaf area and stomatal conductance (Farquhar et nearest weather station (located 10 km from the study site; al. 1989). As WUE increases, values of δ13C become less nega- Pérez Cueva 1994). The average values of δ13C ranged be- tive and this relationship can be used to evaluate WUE during tween –26.9‰ and –29.6‰, whereas those of δ15N ranged periods of stress (Ehleringer et al. 1992; Dawson et al. 2002). between –1.9‰ and 2.7‰ (Figure 1). The average values of Despite the fact that the interpretation of the δ15N of leaves is the C : N ratio ranged between 10.7 and 53.5, whereas those not straightforward (Handley et al. 1999), this variable can of nitrogen concentration ranged between 1.0% and 4.4% provide plant ecologists with useful information on the nitrogen (Figure 1). MANOVA analyses revealed significant and margin- sources used by plants, especially when the nitrogen supply ally significant differences between microsites in M. arborea rate is low in relation to plant demand (Högberg 1997). and P. lentiscus, respectively, but not in Q. coccifera (Table Recent studies have shown that the tussock grass Stipa 1). These were driven mainly by differences between the val- tenacissima L. facilitates the establishment of late-succes- ues obtained in the nursery with those from the field, because sional shrub species (Pistacia lentiscus L., Quercus coccifera none of the variables evaluated differed between tussock and L., and Medicago arborea L.) in semi-arid steppes of the Medi- open microsites (Figure 1). Despite this, some differential re- terranean Basin (Maestre et al. 2001, 2003a; Maestre and sponses to the microsite provided by S. tenacissima were Cortina 2004). This interaction is of considerable interest be- observed. When compared with values obtained in the nursery, cause it is the first documented case of the facilitation of woody a significant increase in δ13C was found for M. arborea in both plants by grasses in semi-arid ecosystems. In these tussock and open microsites. For Q. coccifera, this increase environments, studies have mainly described the facilitation of was only found in the tussock microsite. Similarly, a significant grasses by woody plants, or woody plant seedlings by adults, decrease in δ15N was found for M. arborea in both tussock and either conspecific or not (Callaway 1995; Maestre et al. 2005). open microsites, but for P. lentiscus this reduction was only With the aim of increasing our knowledge of this interaction, in found in the tussock microsite. Foliar nitrogen concentration the present study we investigated the effects of S. tenacissima decreased significantly in both P. lentiscus and M. arborea on the foliar δ13C, δ15N, nitrogen concentration, and the carbon : when passing from the nursery to the field. Compared with nitrogen (C : N) ratio of seedlings of P. lentiscus, Q. coccifera, and M. arborea in a semi-arid steppe of southeastern (SE) Spain. Soils under the canopy of S. tenacissima commonly Table 1. Results of MANOVA and ANOVA tests showing the effects of have higher organic matter and nutrient contents than inter- Microsite (nursery, tussock, and open) on the foliar carbon (C) and δ13 δ15 tussock areas, as well as improved physical soil properties, nitrogen (N) isotopic composition ( C and N, respectively), N such as lower surface compaction, higher infiltration rates, concentration, and C : N ratio of shrub seedlings and higher water retention capacities after rainfall events Species Pillai’s trace F d.f. P (Puigdefábregas et al. 1999; Maestre et al. 2001, 2002; Armas Medicago arborea 1.010 2.54 8, 20 0.044 and Pugnaire 2005). In the present study, we tested the hy- Quercus coccifera 0.651 1.21 8, 20 0.345 pothesis that seedlings growing in the vicinity of S. tenacissima Pistacia lentiscus 0.969 2.35 8, 20 0.058 δ13 δ15 will have lower C and N values, and higher nitrogen ANOVA results Variable F df P concentration, than those seedlings growing in bare ground δ13 areas devoid of vascular plants. Previous studies have found M. arborea C 5.87 2, 12 0.017 δ15 a strong negative relationship between foliar δ13C and water N 16.39 2, 12 <0.001 : availability (Stewart et al. 1995). Thus, we expected to find C N ratio 18.79 2, 12 <0.001 lower δ13C values in seedlings growing in the vicinity of S. %N 17.42 2, 12 <0.001 tenacissima because of increased water availability in this Q. coccifera δ13C 4.80 2, 12 0.029 15 microsite. Lower δ N values, and higher nitrogen δ15N 1.24 2, 12 0.323 concentrations, were also expected because of the increase C : N ratio 2.69 2, 12 0.108 – in overall nutrient availability and NO3 uptake, promoted by %N 3.11 2, 12 0.081 increased nitrogen mineralization in the vicinity of S. P. lentiscus δ13C 0.683 2, 12 0.524 tenacissima tussocks (Djellali et al. 1985; Armas and Pugnaire δ15N 6.921 2, 12 0.010 2005). C : N ratio 5.551 2, 12 0.020 %N 7.453 2, 12 0.008 Results Separate analyses were conducted for each species. Significant values (P<0.05) are in bold and indicate significant During the first 6 months after planting, the precipitation at the differences between microsites. Foliar δ13C and δ15N of Shrub Seedings in a Semiarid Steppe 899 Figure 1. Values of foliar δ13C, δ15N, nitrogen concentration (N), and carbon-to-nitrogen ratio (C : N) for seedlings in the nursery and in the field (tussock and open microsites). Data are the mean ± SE (n = 5). Different letters indicate significant differences between microsites (P < 0.05, Tukey’s b-test).
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