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Clonal integration improves compensatory growth in heavily grazed ramet populations of two inland-dune grasses
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Flora 204 (2009) 298–305 www.elsevier.de/flora
Clonal integration improves compensatory growth in heavily grazed ramet populations of two inland-dune grasses Hai-Dong Liua,b, Fei-Hai Yua,, Wei-Ming Hea, Yu Chua, Ming Donga, a State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, Nanxincun 20, Xiangshan, Haidian District, Beijing 100093, China b Research Centre of Environmental Impact Assessment, Environmental Development Centre, Environmental Protection Administration, Beijing 100029, P.R. China
Received 12 June 2007; accepted 5 March 2008
Abstract Herbaceous species possess several mechanisms to compensate for tissue loss. For clonal herbaceous species, clonal integration may be an additional mechanism. This may especially hold true when tissue loss is very high, because other compensatory mechanisms may be insufficient. On inland dunes in northern China, we subjected Bromus ircutensis and Psammochloa villosa ramets within 0.5 m 0.5 m plots to three clipping treatments, i.e., no clipping, moderate (50% shoot removal) and heavy clipping (90% shoot removal), and kept rhizomes at the plot edges connected or disconnected. Moderate clipping did not reduce ramet, leaf or biomass density of either species. Under moderate clipping, rhizome connection significantly improved the performance of Psammochloa, but not that of Bromus. Heavy clipping reduced ramet, leaf and biomass density in the disconnected plots of both species, but such negative effects were negated or greatly ameliorated when the rhizomes were connected. Therefore, clonal integration contributed greatly to the compensatory growth of both species. The results suggest that clonal integration is an additional compensatory mechanism for clonal plants and may be important for their long-term persistence in the heavily grazed regions in northern China. r 2008 Elsevier GmbH. All rights reserved. Keywords: Bromus ircutensis; Clonal plants; Herbivory; Physiological integration; Psammochloa villosa; Resource sharing
Introduction Herbaceous species are frequently exposed to various levels of grazing (Smith, 1998). Grazing directly leads to the loss of photosynthetic tissue, which, however, does not always result in a proportional growth reduction in Corresponding author. Tel.: +86 10 62836635; fax: +86 10 82594676. E-mail addresses: [email protected] (F.-H. Yu), [email protected] (M. Dong).
0367-2530/$ - see front matter r 2008 Elsevier GmbH. All rights reserved. doi:10.1016/j.flora.2008.03.003
herbaceous species (Ferraro and Oesterheld, 2002; Geissler and Gzik, 2008; Maschinski and Whitham, 1989; McNaughton, 1983; Rosenthal and Lederbogen, 2008; van Staalduinen and Anten, 2005). This especially holds true when the grazing damage is not so severe, because herbaceous species possess mechanisms with which the growth of the grazed plants can be maintained (full compensation) or even improved (over compensation; Esmaeili et al., 2009; Ferraro and Oesterheld, 2002; Maschinski and Whitham, 1989; McNaughton, 1983; van Staalduinen and Anten, 2005).
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Several mechanisms have been proposed to explain the grazing-induced compensatory growth of plants (Ferraro and Oesterheld, 2002; McNaughton, 1983; Strauss and Agrawal, 1999). Compensatory growth may result from an increase in net photosynthetic rate (Nowak and Caldwell, 1984), a decrease in self-shading (Oesterheld and McNaughton, 1991), a reallocation of carbohydrate storage (Briske et al., 1996), and/or an activation of additional meristems due to release of apical dominance (Hay and Newton, 1996). In herbaceous clonal plants, ramets connected by rhizomes or stolons can share carbohydrates, water and nutrients through clonal integration, and integration can contribute greatly to the growth of stressed ramets (Alpert, 1999; Alpert and Mooney, 1986; Hutchings and de Kroon, 1994; Stuefer et al., 1994; Wijesinghe and Handel, 1994). Herbaceous clonal plants, especially those with a guerilla growth form (i.e., connections between ramets have many and/or long internodes and thus ramets of the same clone are widely spaced; LovettDoust, 1981; Pfeiffer, 2007; Ye et al., 2006), can form very large, interconnected clones in the field. For example, Chen et al. (2001) found that in a clone of Psammochloa villosa 261 ramets were interconnected over distances of 46 m on an inland dune; Evans (1988, 1991) found that in a clone of Hydrocotyle bonariensis more than 1500 ramets were interconnected and they covered an area of over 100 m2 on dunes. In the field, therefore, often only part of the connected ramets of such clones are heavily grazed (Piqueras, 1999). In this case, clonal integration may help the grazed ramet to regrow (Bach, 2000; Bullock et al., 1994; Schmid et al., 1988) and thus act as a mechanism of compensatory growth (Liu et al., 2007a). This may especially hold true when ramets are heavily grazed, because under such conditions other means of compensatory growth may not be sufficient (Bullock et al., 1994). Although several studies have examined the effects of clonal integration on grazing-induced compensatory growth of individual ramets (Bach, 2000; Bullock et al., 1994; Jo´nsdo´ttir and Callaghan, 1989; Schmid et al., 1988), few have tested the effects at ramet population level on inland-dune species. The two rhizomatous perennial grasses, Bromus ircutensis Kom. and P. villosa (Trin.) Bor., are pioneer colonists on dunes in the drylands in northern China (Dong and Alaten, 1999; Ma, 1994). Psammochloa forms very large clones (Chen et al., 2001; Liu et al., 2007b; Wang et al., 1999) and displays a more guerilla form than Bromus. On dunes in the Otindag Sandland in northern China, we subjected Psammochloa and Bromus ramets within 0.5 m 0.5 m plots to three clipping treatments (no, moderate and heavy clipping), combined with two rhizome-severing treatments (connected or disconnected). We aimed to examine the roles of clonal integration in the compensatory growth of the two grass
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species. Specifically, we address in this study the following questions: (1) do the two species show compensatory growth after shoot clipping? (2) does clonal integration contribute to the compensatory growth of the two species? (3) do the effects of integration on the compensatory growth differ among the two species?
Materials and methods Plant species B. ircutensis and P. villosa are good forage for livestock and also excellent sand-binding species (Dong and Alaten, 1999; Ma, 1994; Yu et al., 2004). The genet of Psammochloa possesses a more guerilla form than Bromus: the average distance between adjacent rhizome nodes is 4.7 cm in Bromus (H.-D. Liu unpublished) and 8 cm in Psammochloa (Yu et al., 2004). Mature ramets of Bromus are up to 50 cm high (Ma, 1994) and its sympodially growing rhizomes lie mainly at a depth of about 15 cm under the ground surface. Mature ramets of Psammochloa are up to 100 cm high (Ma, 1994) and its monopodially growing rhizomes lie mainly at a depth less than 50 cm under the ground surface.
Study site The study was carried out at Otindag Sandland Ecological Station (421530 N, 1161010 E; Institute of Botany, Chinese Academy of Sciences), located in the hinterland of the Otindag Sandland in Inner Mongolia, China. It is a semi-arid area with a mean annual temperature of 1.8 1C and a mean annual precipitation of 367.1 mm (annual reports 1960–2000 Weather Bureau of Zhenglan Banner). Its zonal vegetation is temperate grassland. However, due to severe desertification in the past decades, the present vegetation is dominated by sparse trees (e.g., Ulmus pumila), shrubs (e.g., Caragana microphylla and Hedysarum laeve) and herbs (e.g., Polygonum divaricatum, Potentilla acaulis, Cleistogenes squarrosa and Carex duriuscula). This area is mainly composed of stable, semi-moving or moving dunes and inter-dune lowlands. We selected an area of ca. 8 ha as the study site, located 1.5 km away from the ecological station. At this site, Bromus and Psammochloa occur both on dunes and on lowlands. Because nutrient availability may influence plant responses to grazing (Hicks and Turkington, 2000; Maschinski and Whitham, 1989), all experimental plots were established on four dunes to minimize potential differences in nutrient availability. Each dune is 4–6 m high and more than 70 m long. On the dunes Bromus and Psammochloa together had
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a cover of about 15%; other common plant species include Artemisia intramongolica, Astragalus melilotoides, Polygonum divaricatum, Thalictrum squarrosum and Corispermum puberulum.
Experimental design For each study species, we set up 48 0.5 m 0.5 m plots, of which 24 plots were randomly selected for rhizome-severing (disconnected plots) and the remaining 24 connected plots were used as controls. Along the edges of the disconnected plots, the rhizomes were severed by inserting a sharp blade perpendicular to the sand surface to a depth of 30 cm for Bromus and 80 cm for Psammochloa. Both the connected and disconnected plots were randomly assigned to one of the three clipping treatments: (i) no clipping (control), (ii) moderate clipping (all shoots were clipped to 50% of their height) and (iii) heavy clipping (all shoots were clipped to 10% of their height). There were eight replicates. At the beginning of the experiment, the number of ramets was 13.371.4 (mean7SE) in the Bromus plots and 9.071.6 in the Psammochloa plots; mean ramet height was 20.973.1 cm in the Bromus plots and 65.773.7 cm in the Psammochloa plots. No ramet in the plots was flowering at this time. The clipping treatments were carried out on June 20–21, 2004. The regrowth of a grazed plant may be influenced by neighbor competition (Hicks and Turkington, 2000; Hja¨lte´n et al., 1993), so we removed aboveground biomass of all other species during the experiment.
leaf density, shoot mass density and rhizome mass density. Three-way ANOVA was used to test the effects of species identity, rhizome connection and shoot clipping on all traits. For each species, we also compared the differences in trait means among treatments using Duncan’s method. All data were transformed to natural log before analyses. The analyses were performed using SPSS 10.0 software (Chicago, IL, USA).
Results Ramet and leaf density Effects of rhizome connection on ramet and leaf density depended on the clipping treatments (significant R C effect; Table 1). In the control, rhizome connection did not affect ramet or leaf density of either species (Fig. 1). Under moderate clipping, ramet and leaf density were significantly higher in the connected than in the disconnected plots in Psammochloa, but not in Bromus (Fig. 1). Under heavy clipping, ramet and leaf density were higher in the connected than in the disconnected plots in both species (Fig. 1). As compared with the control, moderate clipping did not significantly decrease ramet or leaf density in the connected plots of either species, but decreased leaf density in the disconnected plots of Psammochloa (Fig. 1). Heavy clipping significantly decreased ramet and leaf density in the disconnected plots of both species, but it increased ramet density in the connected plots of both species (Fig. 1).
Measurements and analyses
Shoot and rhizome mass density
On September 11–12, 2004, we counted the number of ramets and leaves per plot. Then shoots and rhizomes of the Psammochloa and Bromus plants in the plots were harvested, dried and weighed. We calculated ramet density as the number of ramets in a plot divided by the plot size (0.25 m2). Using a similar approach, we derived
Rhizome connection affected the responses of shoot mass density (significant R C effect; Table 1), but not those of rhizome mass density, to clipping (Table 1). In the control, rhizome connection did not affect shoot or rhizome mass density of either species (Fig. 2). Under moderate clipping, shoot mass density was significantly
Table 1.
Effects of species identity, rhizome connection and clipping intensity on traits measured
Effect
DF
Ramet density
Leaf density
Shoot mass density
Rhizome mass density
Shoot mass per ramet
Leaf number per ramet
Species (S) Rhizome connection (R) Clipping (C) SR SC RC SRC
1,84 1,84 2,84 1,84 2,84 2,84 2,84
498.53*** 12.01** 4.87* 0.53ns 3.05ns 21.39*** 2.17ns
269.31*** 14.82*** 46.93*** 0.62ns 3.22* 15.03*** 1.85ns
447.54*** 15.21*** 22.76*** 0.02ns 0.65ns 4.35* 2.47ns
329.46*** 17.81*** 15.61*** 0.28ns 0.57ns 0.27ns 0.09ns
1156.80*** 3.91ns 15.81*** 1.07ns 4.09* 3.74* 2.47ns
77.58*** 0.63ns 90.13*** 0.02ns 0.59ns 1.20ns 0.50ns
F values and degree of freedom (df) of three-way ANOVA are given. Significance level: ***po0.001, **po0.001, *po0.05 and
ns
pX0.05.
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Bromus 150
Connected
301
Psammochloa 60
Disconnected
Leaf density (no. m-2)
Ramet density (no. m-2)
a ab
100
cd
a
ab
a
40
bc
a
bc
bc c
d
50
20
0
0
600
300
ab
400
a
a
ab
a
a bc
b
b
c
200
d c
200
100
0
0 No
Moderate
Heavy
No
Moderate
Heavy
Shoot clipping
Fig. 1. Ramet density (a, b) and leaf density (c, d) of Bromus ircutensis and Psammochloa villosa under three clipping and two rhizome-severing treatments. Mean+SE are given (n ¼ 8). Bars sharing the same letter are not different at p ¼ 0.05.
higher in the connected than in the disconnected plots in Psammochloa, but not in Bromus (Fig. 2a and b). Under heavy clipping, shoot and rhizome mass density were higher in the connected than in the disconnected plots of both species (Fig. 2). As compared with the control, moderate clipping did not significantly decrease shoot or rhizome mass density in the connected plots of either species, but decreased shoot mass density in the disconnected plots of Psammochloa (Fig. 2). Except in the case of shoot mass density in the connected plots of Psammochloa, heavy clipping significantly decreased shoot and rhizome mass density in both connected and disconnected plots of both species (Fig. 2).
Psammochloa (Fig. 3d), but not that in connected or disconnected plots of Bromus (Fig. 3c). Heavy clipping decreased or tended to decrease shoot mass and leaf number per ramet in both connected and disconnected plots of both species (Fig. 3).
Shoot mass and leaf number per ramet
In the connected plots, moderate and heavy clipping significantly increased ramet density of both Bromus and Psammochloa (Fig. 1a and b). Also, in the disconnected plots, moderate clipping increased ramet density of Bromus (Fig. 1a and b). Similar positive effects of clipping on ramet production have been found in many other species (e.g. Briske and Anderson, 1990; Butler and Briske, 1988; Riba, 1998). This is most likely because clipping released apical dominance and thus
Rhizome connection did not affect shoot mass or leaf number per ramet of either species (Table 1; Fig. 3). As compared with the control, moderate clipping decreased shoot mass per ramet in both connected and disconnected plots of Bromus (Fig. 3a), but not in that of Psammochloa (Fig. 3b). Moderate clipping decreased leaf number per ramet in the connected plots of
Discussion The effects of clipping on the growth of both Bromus and Psammochloa depended greatly on the clipping intensity and rhizome connections.
Compensatory growth of both species
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Bromus
Shoot mass density (g m-2)
25
20
Connected
Psammochloa
Disconnected
a ab
60
ab
bc
ab
ab
cd
15
bc
b
40 10
20
5
0
25
50 a
20
d
c
0
Rhizome mass density (g m-2)
a
80
a ab
40 ab
bc
b bc
15
ab ab
d
30
c
10
20
5
10
0
c
0 No
Moderate
Heavy
No
Moderate
Heavy
Shoot clipping
Fig. 2. Shoot biomass density (a, b) and rhizome biomass density (c, d) of Bromus ircutensis and Psammochloa villosa under three clipping and two rhizome-severing treatments. Mean+SE are given (n ¼ 8). Bars sharing the same letter are not different at p ¼ 0.05.
activated axillary meristem growth (Hendrickson and Briske, 1997; McNaughton, 1983). In terms of rhizome mass density, both Bromus and Psammochloa demonstrated full compensatory growth responses to moderate clipping. In terms of shoot mass density, Bromus showed full compensation and the connected plots of Psammochloa even showed overcompensation. These results suggest that both species can compensate for tissue loss due to moderate clipping. However, heavy clipping decreased or tended to decrease rhizome and shoot mass density in both connected and disconnected plots of both species, suggesting that neither species could fully compensate for the biomass loss caused by heavy clipping. The connected plots of both species had denser but smaller individuals under heavy clipping than in the control. Therefore, both species tended to invest more energy in the production of new ramets rather than in regrowth of the grazed ramets. Small individual size associated with short plant height and small leaf mass are typical responses of grazing avoidance (Butler and Briske, 1988; Dı´ az et al., 2001; Noy-Meir et al., 1989).
Clonal integration as a mechanism of compensatory growth Rhizome connection markedly increased ramet, leaf and biomass density of both Bromus and Psammochloa under heavy clipping and also increased those of Psammochloa under moderate clipping. These results support the hypothesis that clonal integration contributed greatly to the compensatory growth of clonal plants. This was most likely because the clipped ramets received carbohydrates from their connected nonclipped partners through clonal integration, and thus the negative effects of clipping were greatly mitigated. Clonal integration was also found to ameliorate the negative effects of simulated herbivory on Aster lanceolatus and Solidago canadensis in oldfields (Schmid et al., 1988) and Ipomoea pes-caprae in beach dunes (Bach, 2000). Under moderate clipping, however, rhizome connection did not increase the performance of Bromus, suggesting that integration contributed little to the compensatory growth of this species under such conditions. Similarly,
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Bromus 0.3
Connected
Psammochloa 2.0
Disconnected
Leaf number per ramet
Shoot mass per ramet (g)
a
ab
a ab
1.5
ab
0.2
303
ac
bc
bc c c
c
1.0
c
0.1 0.5
0
0.0
8
8
6
6
a a
a a
ab
b
b
a
4
b
b
c
4
c
2
2
0
0 No
Moderate
No
Heavy
Moderate
Heavy
Shoot clipping
Fig. 3. Shoot biomass per ramet (a, b) and leaf number per ramet (c, d) of Bromus ircutensis and Psammochloa villosa under three clipping and two rhizome-severing treatments. Mean+SE are given (n ¼ 8). Bars sharing the same letter are not different at p ¼ 0.05.
Wang et al. (2004) found that clonal integration did not affect biomass and ramet production of Leymus chinensis in grasslands after clipping to a height of 10–15 cm (o70% shoot removal; Z. Wang personal communication). This is likely because under moderate clipping other means of compensatory mechanisms were sufficient for the regrowth of the clipped ramets, so that integration was not involved. This agrees with the notion that clonal integration is more important in locally more stressful conditions. Under moderate grazing, Psammochloa benefited greatly from integration, but Bromus did not, indicating that the role of clonal integration in the compensatory growth may be species-specific. The difference may result from the differences in ramet aggregation, since ramet aggregation is believed to affect the extent of clonal integration (Herben, 2004; Jo´nsdo´ttir and Watson, 1997; Pauliukonis and Gough, 2004). Moreover, differences in branching pattern of rhizomes (i.e., sympodial vs. monopodial) between the two species may also have influenced the effect of clonal integration.
In the drylands in northern China, desertification is a serious problem and excessive grazing is one major cause (Chen and Cai, 2003; Mitchell et al., 1998). The findings of this study suggest that clonal integration may greatly improve the ability of the rhizomatous sand-binding species to tolerate heavy grazing and may be an important adaptive strategy of clonal plants growing in desertified environments with frequent disturbances. Thus, protecting and planting indigenous clonal species such as Bromus and Psammochloa could be an effective means of restoring natural vegetation and anchoring shifting dunes.
Acknowledgments We thank Chuangye Song for assistance with field measurement and Dr. Zhenwen Wang for helpful discussions. We are also very grateful to Dr. Mary Endress for linguistic corrections and two anonymous referees for valuable comments on an early version of the manuscript. This research was supported by the Chinese Academy of Sciences (KSCX1-08-02) and NSFC (30330130, 30770357).
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Flora 204 (2009) 298–305 www.elsevier.de/flora
Clonal integration improves compensatory growth in heavily grazed ramet populations of two inland-dune grasses Hai-Dong Liua,b, Fei-Hai Yua,, Wei-Ming Hea, Yu Chua, Ming Donga, a State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, Nanxincun 20, Xiangshan, Haidian District, Beijing 100093, China b Research Centre of Environmental Impact Assessment, Environmental Development Centre, Environmental Protection Administration, Beijing 100029, P.R. China
Received 12 June 2007; accepted 5 March 2008
Abstract Herbaceous species possess several mechanisms to compensate for tissue loss. For clonal herbaceous species, clonal integration may be an additional mechanism. This may especially hold true when tissue loss is very high, because other compensatory mechanisms may be insufficient. On inland dunes in northern China, we subjected Bromus ircutensis and Psammochloa villosa ramets within 0.5 m 0.5 m plots to three clipping treatments, i.e., no clipping, moderate (50% shoot removal) and heavy clipping (90% shoot removal), and kept rhizomes at the plot edges connected or disconnected. Moderate clipping did not reduce ramet, leaf or biomass density of either species. Under moderate clipping, rhizome connection significantly improved the performance of Psammochloa, but not that of Bromus. Heavy clipping reduced ramet, leaf and biomass density in the disconnected plots of both species, but such negative effects were negated or greatly ameliorated when the rhizomes were connected. Therefore, clonal integration contributed greatly to the compensatory growth of both species. The results suggest that clonal integration is an additional compensatory mechanism for clonal plants and may be important for their long-term persistence in the heavily grazed regions in northern China. r 2008 Elsevier GmbH. All rights reserved. Keywords: Bromus ircutensis; Clonal plants; Herbivory; Physiological integration; Psammochloa villosa; Resource sharing
Introduction Herbaceous species are frequently exposed to various levels of grazing (Smith, 1998). Grazing directly leads to the loss of photosynthetic tissue, which, however, does not always result in a proportional growth reduction in Corresponding author. Tel.: +86 10 62836635; fax: +86 10 82594676. E-mail addresses: [email protected] (F.-H. Yu), [email protected] (M. Dong).
0367-2530/$ - see front matter r 2008 Elsevier GmbH. All rights reserved. doi:10.1016/j.flora.2008.03.003
herbaceous species (Ferraro and Oesterheld, 2002; Geissler and Gzik, 2008; Maschinski and Whitham, 1989; McNaughton, 1983; Rosenthal and Lederbogen, 2008; van Staalduinen and Anten, 2005). This especially holds true when the grazing damage is not so severe, because herbaceous species possess mechanisms with which the growth of the grazed plants can be maintained (full compensation) or even improved (over compensation; Esmaeili et al., 2009; Ferraro and Oesterheld, 2002; Maschinski and Whitham, 1989; McNaughton, 1983; van Staalduinen and Anten, 2005).
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Several mechanisms have been proposed to explain the grazing-induced compensatory growth of plants (Ferraro and Oesterheld, 2002; McNaughton, 1983; Strauss and Agrawal, 1999). Compensatory growth may result from an increase in net photosynthetic rate (Nowak and Caldwell, 1984), a decrease in self-shading (Oesterheld and McNaughton, 1991), a reallocation of carbohydrate storage (Briske et al., 1996), and/or an activation of additional meristems due to release of apical dominance (Hay and Newton, 1996). In herbaceous clonal plants, ramets connected by rhizomes or stolons can share carbohydrates, water and nutrients through clonal integration, and integration can contribute greatly to the growth of stressed ramets (Alpert, 1999; Alpert and Mooney, 1986; Hutchings and de Kroon, 1994; Stuefer et al., 1994; Wijesinghe and Handel, 1994). Herbaceous clonal plants, especially those with a guerilla growth form (i.e., connections between ramets have many and/or long internodes and thus ramets of the same clone are widely spaced; LovettDoust, 1981; Pfeiffer, 2007; Ye et al., 2006), can form very large, interconnected clones in the field. For example, Chen et al. (2001) found that in a clone of Psammochloa villosa 261 ramets were interconnected over distances of 46 m on an inland dune; Evans (1988, 1991) found that in a clone of Hydrocotyle bonariensis more than 1500 ramets were interconnected and they covered an area of over 100 m2 on dunes. In the field, therefore, often only part of the connected ramets of such clones are heavily grazed (Piqueras, 1999). In this case, clonal integration may help the grazed ramet to regrow (Bach, 2000; Bullock et al., 1994; Schmid et al., 1988) and thus act as a mechanism of compensatory growth (Liu et al., 2007a). This may especially hold true when ramets are heavily grazed, because under such conditions other means of compensatory growth may not be sufficient (Bullock et al., 1994). Although several studies have examined the effects of clonal integration on grazing-induced compensatory growth of individual ramets (Bach, 2000; Bullock et al., 1994; Jo´nsdo´ttir and Callaghan, 1989; Schmid et al., 1988), few have tested the effects at ramet population level on inland-dune species. The two rhizomatous perennial grasses, Bromus ircutensis Kom. and P. villosa (Trin.) Bor., are pioneer colonists on dunes in the drylands in northern China (Dong and Alaten, 1999; Ma, 1994). Psammochloa forms very large clones (Chen et al., 2001; Liu et al., 2007b; Wang et al., 1999) and displays a more guerilla form than Bromus. On dunes in the Otindag Sandland in northern China, we subjected Psammochloa and Bromus ramets within 0.5 m 0.5 m plots to three clipping treatments (no, moderate and heavy clipping), combined with two rhizome-severing treatments (connected or disconnected). We aimed to examine the roles of clonal integration in the compensatory growth of the two grass
299
species. Specifically, we address in this study the following questions: (1) do the two species show compensatory growth after shoot clipping? (2) does clonal integration contribute to the compensatory growth of the two species? (3) do the effects of integration on the compensatory growth differ among the two species?
Materials and methods Plant species B. ircutensis and P. villosa are good forage for livestock and also excellent sand-binding species (Dong and Alaten, 1999; Ma, 1994; Yu et al., 2004). The genet of Psammochloa possesses a more guerilla form than Bromus: the average distance between adjacent rhizome nodes is 4.7 cm in Bromus (H.-D. Liu unpublished) and 8 cm in Psammochloa (Yu et al., 2004). Mature ramets of Bromus are up to 50 cm high (Ma, 1994) and its sympodially growing rhizomes lie mainly at a depth of about 15 cm under the ground surface. Mature ramets of Psammochloa are up to 100 cm high (Ma, 1994) and its monopodially growing rhizomes lie mainly at a depth less than 50 cm under the ground surface.
Study site The study was carried out at Otindag Sandland Ecological Station (421530 N, 1161010 E; Institute of Botany, Chinese Academy of Sciences), located in the hinterland of the Otindag Sandland in Inner Mongolia, China. It is a semi-arid area with a mean annual temperature of 1.8 1C and a mean annual precipitation of 367.1 mm (annual reports 1960–2000 Weather Bureau of Zhenglan Banner). Its zonal vegetation is temperate grassland. However, due to severe desertification in the past decades, the present vegetation is dominated by sparse trees (e.g., Ulmus pumila), shrubs (e.g., Caragana microphylla and Hedysarum laeve) and herbs (e.g., Polygonum divaricatum, Potentilla acaulis, Cleistogenes squarrosa and Carex duriuscula). This area is mainly composed of stable, semi-moving or moving dunes and inter-dune lowlands. We selected an area of ca. 8 ha as the study site, located 1.5 km away from the ecological station. At this site, Bromus and Psammochloa occur both on dunes and on lowlands. Because nutrient availability may influence plant responses to grazing (Hicks and Turkington, 2000; Maschinski and Whitham, 1989), all experimental plots were established on four dunes to minimize potential differences in nutrient availability. Each dune is 4–6 m high and more than 70 m long. On the dunes Bromus and Psammochloa together had
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a cover of about 15%; other common plant species include Artemisia intramongolica, Astragalus melilotoides, Polygonum divaricatum, Thalictrum squarrosum and Corispermum puberulum.
Experimental design For each study species, we set up 48 0.5 m 0.5 m plots, of which 24 plots were randomly selected for rhizome-severing (disconnected plots) and the remaining 24 connected plots were used as controls. Along the edges of the disconnected plots, the rhizomes were severed by inserting a sharp blade perpendicular to the sand surface to a depth of 30 cm for Bromus and 80 cm for Psammochloa. Both the connected and disconnected plots were randomly assigned to one of the three clipping treatments: (i) no clipping (control), (ii) moderate clipping (all shoots were clipped to 50% of their height) and (iii) heavy clipping (all shoots were clipped to 10% of their height). There were eight replicates. At the beginning of the experiment, the number of ramets was 13.371.4 (mean7SE) in the Bromus plots and 9.071.6 in the Psammochloa plots; mean ramet height was 20.973.1 cm in the Bromus plots and 65.773.7 cm in the Psammochloa plots. No ramet in the plots was flowering at this time. The clipping treatments were carried out on June 20–21, 2004. The regrowth of a grazed plant may be influenced by neighbor competition (Hicks and Turkington, 2000; Hja¨lte´n et al., 1993), so we removed aboveground biomass of all other species during the experiment.
leaf density, shoot mass density and rhizome mass density. Three-way ANOVA was used to test the effects of species identity, rhizome connection and shoot clipping on all traits. For each species, we also compared the differences in trait means among treatments using Duncan’s method. All data were transformed to natural log before analyses. The analyses were performed using SPSS 10.0 software (Chicago, IL, USA).
Results Ramet and leaf density Effects of rhizome connection on ramet and leaf density depended on the clipping treatments (significant R C effect; Table 1). In the control, rhizome connection did not affect ramet or leaf density of either species (Fig. 1). Under moderate clipping, ramet and leaf density were significantly higher in the connected than in the disconnected plots in Psammochloa, but not in Bromus (Fig. 1). Under heavy clipping, ramet and leaf density were higher in the connected than in the disconnected plots in both species (Fig. 1). As compared with the control, moderate clipping did not significantly decrease ramet or leaf density in the connected plots of either species, but decreased leaf density in the disconnected plots of Psammochloa (Fig. 1). Heavy clipping significantly decreased ramet and leaf density in the disconnected plots of both species, but it increased ramet density in the connected plots of both species (Fig. 1).
Measurements and analyses
Shoot and rhizome mass density
On September 11–12, 2004, we counted the number of ramets and leaves per plot. Then shoots and rhizomes of the Psammochloa and Bromus plants in the plots were harvested, dried and weighed. We calculated ramet density as the number of ramets in a plot divided by the plot size (0.25 m2). Using a similar approach, we derived
Rhizome connection affected the responses of shoot mass density (significant R C effect; Table 1), but not those of rhizome mass density, to clipping (Table 1). In the control, rhizome connection did not affect shoot or rhizome mass density of either species (Fig. 2). Under moderate clipping, shoot mass density was significantly
Table 1.
Effects of species identity, rhizome connection and clipping intensity on traits measured
Effect
DF
Ramet density
Leaf density
Shoot mass density
Rhizome mass density
Shoot mass per ramet
Leaf number per ramet
Species (S) Rhizome connection (R) Clipping (C) SR SC RC SRC
1,84 1,84 2,84 1,84 2,84 2,84 2,84
498.53*** 12.01** 4.87* 0.53ns 3.05ns 21.39*** 2.17ns
269.31*** 14.82*** 46.93*** 0.62ns 3.22* 15.03*** 1.85ns
447.54*** 15.21*** 22.76*** 0.02ns 0.65ns 4.35* 2.47ns
329.46*** 17.81*** 15.61*** 0.28ns 0.57ns 0.27ns 0.09ns
1156.80*** 3.91ns 15.81*** 1.07ns 4.09* 3.74* 2.47ns
77.58*** 0.63ns 90.13*** 0.02ns 0.59ns 1.20ns 0.50ns
F values and degree of freedom (df) of three-way ANOVA are given. Significance level: ***po0.001, **po0.001, *po0.05 and
ns
pX0.05.
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Bromus 150
Connected
301
Psammochloa 60
Disconnected
Leaf density (no. m-2)
Ramet density (no. m-2)
a ab
100
cd
a
ab
a
40
bc
a
bc
bc c
d
50
20
0
0
600
300
ab
400
a
a
ab
a
a bc
b
b
c
200
d c
200
100
0
0 No
Moderate
Heavy
No
Moderate
Heavy
Shoot clipping
Fig. 1. Ramet density (a, b) and leaf density (c, d) of Bromus ircutensis and Psammochloa villosa under three clipping and two rhizome-severing treatments. Mean+SE are given (n ¼ 8). Bars sharing the same letter are not different at p ¼ 0.05.
higher in the connected than in the disconnected plots in Psammochloa, but not in Bromus (Fig. 2a and b). Under heavy clipping, shoot and rhizome mass density were higher in the connected than in the disconnected plots of both species (Fig. 2). As compared with the control, moderate clipping did not significantly decrease shoot or rhizome mass density in the connected plots of either species, but decreased shoot mass density in the disconnected plots of Psammochloa (Fig. 2). Except in the case of shoot mass density in the connected plots of Psammochloa, heavy clipping significantly decreased shoot and rhizome mass density in both connected and disconnected plots of both species (Fig. 2).
Psammochloa (Fig. 3d), but not that in connected or disconnected plots of Bromus (Fig. 3c). Heavy clipping decreased or tended to decrease shoot mass and leaf number per ramet in both connected and disconnected plots of both species (Fig. 3).
Shoot mass and leaf number per ramet
In the connected plots, moderate and heavy clipping significantly increased ramet density of both Bromus and Psammochloa (Fig. 1a and b). Also, in the disconnected plots, moderate clipping increased ramet density of Bromus (Fig. 1a and b). Similar positive effects of clipping on ramet production have been found in many other species (e.g. Briske and Anderson, 1990; Butler and Briske, 1988; Riba, 1998). This is most likely because clipping released apical dominance and thus
Rhizome connection did not affect shoot mass or leaf number per ramet of either species (Table 1; Fig. 3). As compared with the control, moderate clipping decreased shoot mass per ramet in both connected and disconnected plots of Bromus (Fig. 3a), but not in that of Psammochloa (Fig. 3b). Moderate clipping decreased leaf number per ramet in the connected plots of
Discussion The effects of clipping on the growth of both Bromus and Psammochloa depended greatly on the clipping intensity and rhizome connections.
Compensatory growth of both species
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Bromus
Shoot mass density (g m-2)
25
20
Connected
Psammochloa
Disconnected
a ab
60
ab
bc
ab
ab
cd
15
bc
b
40 10
20
5
0
25
50 a
20
d
c
0
Rhizome mass density (g m-2)
a
80
a ab
40 ab
bc
b bc
15
ab ab
d
30
c
10
20
5
10
0
c
0 No
Moderate
Heavy
No
Moderate
Heavy
Shoot clipping
Fig. 2. Shoot biomass density (a, b) and rhizome biomass density (c, d) of Bromus ircutensis and Psammochloa villosa under three clipping and two rhizome-severing treatments. Mean+SE are given (n ¼ 8). Bars sharing the same letter are not different at p ¼ 0.05.
activated axillary meristem growth (Hendrickson and Briske, 1997; McNaughton, 1983). In terms of rhizome mass density, both Bromus and Psammochloa demonstrated full compensatory growth responses to moderate clipping. In terms of shoot mass density, Bromus showed full compensation and the connected plots of Psammochloa even showed overcompensation. These results suggest that both species can compensate for tissue loss due to moderate clipping. However, heavy clipping decreased or tended to decrease rhizome and shoot mass density in both connected and disconnected plots of both species, suggesting that neither species could fully compensate for the biomass loss caused by heavy clipping. The connected plots of both species had denser but smaller individuals under heavy clipping than in the control. Therefore, both species tended to invest more energy in the production of new ramets rather than in regrowth of the grazed ramets. Small individual size associated with short plant height and small leaf mass are typical responses of grazing avoidance (Butler and Briske, 1988; Dı´ az et al., 2001; Noy-Meir et al., 1989).
Clonal integration as a mechanism of compensatory growth Rhizome connection markedly increased ramet, leaf and biomass density of both Bromus and Psammochloa under heavy clipping and also increased those of Psammochloa under moderate clipping. These results support the hypothesis that clonal integration contributed greatly to the compensatory growth of clonal plants. This was most likely because the clipped ramets received carbohydrates from their connected nonclipped partners through clonal integration, and thus the negative effects of clipping were greatly mitigated. Clonal integration was also found to ameliorate the negative effects of simulated herbivory on Aster lanceolatus and Solidago canadensis in oldfields (Schmid et al., 1988) and Ipomoea pes-caprae in beach dunes (Bach, 2000). Under moderate clipping, however, rhizome connection did not increase the performance of Bromus, suggesting that integration contributed little to the compensatory growth of this species under such conditions. Similarly,
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Bromus 0.3
Connected
Psammochloa 2.0
Disconnected
Leaf number per ramet
Shoot mass per ramet (g)
a
ab
a ab
1.5
ab
0.2
303
ac
bc
bc c c
c
1.0
c
0.1 0.5
0
0.0
8
8
6
6
a a
a a
ab
b
b
a
4
b
b
c
4
c
2
2
0
0 No
Moderate
No
Heavy
Moderate
Heavy
Shoot clipping
Fig. 3. Shoot biomass per ramet (a, b) and leaf number per ramet (c, d) of Bromus ircutensis and Psammochloa villosa under three clipping and two rhizome-severing treatments. Mean+SE are given (n ¼ 8). Bars sharing the same letter are not different at p ¼ 0.05.
Wang et al. (2004) found that clonal integration did not affect biomass and ramet production of Leymus chinensis in grasslands after clipping to a height of 10–15 cm (o70% shoot removal; Z. Wang personal communication). This is likely because under moderate clipping other means of compensatory mechanisms were sufficient for the regrowth of the clipped ramets, so that integration was not involved. This agrees with the notion that clonal integration is more important in locally more stressful conditions. Under moderate grazing, Psammochloa benefited greatly from integration, but Bromus did not, indicating that the role of clonal integration in the compensatory growth may be species-specific. The difference may result from the differences in ramet aggregation, since ramet aggregation is believed to affect the extent of clonal integration (Herben, 2004; Jo´nsdo´ttir and Watson, 1997; Pauliukonis and Gough, 2004). Moreover, differences in branching pattern of rhizomes (i.e., sympodial vs. monopodial) between the two species may also have influenced the effect of clonal integration.
In the drylands in northern China, desertification is a serious problem and excessive grazing is one major cause (Chen and Cai, 2003; Mitchell et al., 1998). The findings of this study suggest that clonal integration may greatly improve the ability of the rhizomatous sand-binding species to tolerate heavy grazing and may be an important adaptive strategy of clonal plants growing in desertified environments with frequent disturbances. Thus, protecting and planting indigenous clonal species such as Bromus and Psammochloa could be an effective means of restoring natural vegetation and anchoring shifting dunes.
Acknowledgments We thank Chuangye Song for assistance with field measurement and Dr. Zhenwen Wang for helpful discussions. We are also very grateful to Dr. Mary Endress for linguistic corrections and two anonymous referees for valuable comments on an early version of the manuscript. This research was supported by the Chinese Academy of Sciences (KSCX1-08-02) and NSFC (30330130, 30770357).
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