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Springer 2006 Plant Ecology (2006) 185:191 –198 DOI 10.1007/s11258-005-9094-z Effects of sand burial depth and seed mass on seedling emergence and growth of Nitraria sphaerocarpa Q.Y. Li1,2,*, W.Z. Zhao1,2 and H.Y. Fang3 1 Cold and Arid Regions Environmental and Engineering Research Institute, Chinese Academy of Sciences, Lanzhou, 730000, China; 2Chinese Ecosystem Network Research Linze Inland River Basin Comprehensive Research Station, Lanzhou, 730000, China; 3Institute of Geographical Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing, 100101, China; *Author for correspondence (e-mail: [email protected]) Received 8 September 2005; accepted in revised form 22 December 2005 Key words: Biomass allocation, Optimal burial depth, Sand burial, Seed size, Seedling emergence, Seedling size Abstract A greenhouse experiment was conducted to test the effects of sand burial depth and seed mass on seedling emergence and growth of Nitraria sphaerocarpa. Seeds of Nitraria sphaerocarpa were sorted into three sizeclasses (large, medium, small) and artificially buried at 0, 1, 2, 3, 4, 5 and 6 cm depths in plastic pots filled with unsterilized sand. In the seven treatments, the percent emergence, seedling mass and seedling height, significantly affected by both burial depth and seed size, were highest at the optimal burial depth of 2 cm burial depth, and decreased with increasing burial depth in each seed size-class. Although seedling mass was usually greatest for large seeds and least for small seeds at each burial depth, little difference was observed in seedling height at shallow burial depths of 0 –3 cm. In each seed size-class, with increasing burial depth, both root-mass ratio and aboveground stem-mass ratio decreased, while belowground stem-mass ratio increased. In each burial depth, with decreasing seed size, belowground stem-mass ratio increased, while root-mass ratio decreased. Introduction In dune systems, sand accretion and deflation mediated by wind may be important selective forces in the evolution of the species (Zhang et al. 2002). The germination of seeds is directly related to the depth at which seeds are buried (Zhang and Maun 1994). Shallow burial, particularly improves the germination of seeds and the subsequent emergence and survival of seedlings. Seeds beneath a prospective layer of sand experience a much more moderate environment (e.g. temperature, moisture), because it prevents them from drying out (Harper and Benton 1966). However, deep burial depth may prevent seedlings from emergence above the sand and affect survival, because pre-emergence mortality results from a cessation of seedling growth before it reaches the soil surface or the seeds are unable to germinate due to lack of oxygen, light and temperature fluctuation (Maun and Riach 1981; Van Assche and Vanlerberghe 1989; Zhang and Maun 1990; Vleeshouwers 1997). These traits suggest that there is an optimal range of burial depth to maximize the seedling emergence and subsequent seedling growth. 192 The optimal burial depth of seedling emergence could be strongly influenced by seed mass (Chen and Maun 1999). Seed mass plays a key role in the establishment of the juvenile phase of a plant’s life cycle, and seed mass is a parameter that profoundly influences both germination characteristics and seedling traits. Larger seeds are generally superior to smaller seeds by having a higher probability of emergence (Dolan 1984; Stanton 1984; Winn 1988), and by developing into seedlings with better competitive ability (Stanton 1984), higher survival (Simons and Johnston 2000), and better performance in later life stages (Wulff 1986; Vaughton and Ramsey 2001). Often, larger seeds have higher germination rates than smaller seeds (Simons and Johnston 2000), but the opposite has also been observed (Dolan 1984; Susko and Lovett-Doust 2000). Several researches have observed that, within populations, large seed mass confers an advantage during at least one stage of the life cycle, principally under conditions where resources are scarce (Sivertown 1989; Manga and Yadav 1995; Grubb and Coomes 1997; Meyer and Carlson 2001). However, in contrast to the advantages of relatively larger seed mass, several studies have detected ecological factors that can lead to the opposite trend, particularly during the phase when seeds remain in the soil. The predation has been observed to be greater on large seeds, presumably because of richer energy resource or large seeds are more visible to the predators than small seeds (Hulme 1993; Vander Wall 1994). For any given species, the effect of seed mass on plant performance may depend both on the intrinsic effects of seed mass on seed-seedling behavior and on its interactions with other ecological factors. The selective pressures influencing the evolution of seed mass are likely to differ among species and habitats (Foster 1986). The adaptation of the seedlings of dune species to sand accretion may rely on their morphology and biomass allocation (Maun and Riach 1981; Maun and Lapierre 1986; Zhang et al. 2002). In herbaceous species, the adaptation of seedlings to burial has been attributed to the effective elongation of the coleoptile, subcoleoptile, first internode or hypocotyls (Maun and Riach 1981; Maun and Lapierre 1986). In large-seeded tree species, with increasing burial depth and decreasing seed size, the biomass allocation to stems increased, while allocation to roots decreased (Seiwa et al. 2002). In desert shrub species, little is known concerning how buried seeds allocate reserves to the stems in order to facilitate seedling emergence and to what extent the allocation is changed in relation to the availability of seed mass. In this study, we buried seeds of different mass of Nitraria sphaerocarpa at various depths in a greenhouse to examine the effects of sand burial depth and seed size on seedling emergence and growth, to test the biomass allocation at various sand burial depths, and to assess the optimal depth for establishment success of Nitraria sphaerocarpa affected by sand burial and seed size. Materials and methods Study site This study was conducted in a greenhouse in the Chinese Ecosystem Network Research Linze Inland River Basin Comprehensive Research Station in northwest China (3921¢N, 10007¢E) with an elevation of 1382 m. The mean annual temperature and rainfall are 7.6 C and 117.1 mm, respectively. The mean monthly temperature ranged from )27 C (January) to 39.1 C (July). Soil is dominated by blown sand with coarse texture and loose structure. The vegetation is dominated by shrubs, including Nitraria sphaerocarpa, Hedysarum scoparium, Nitraria tangutorum, Calligonum mongolicum, subshrubs, like Reaumuria soongorica, and annuals such as Suaeda glauca, Agriophyllum squarrosum, Bassia dasyphylla, Halogeton arachnoideus, and so on. Plant species Nitraria sphaerocarpa is one of the major sand binding species in the sandlands of northwest China. Seeds of Nitraria sphaerocarpa are dispersed by wind when they mature, and dispersed single seed may be picked up again by wind and moved over longer distances. Seeds and seedlings of the species may be buried by sand to various depths during the establishment. Burial by sand may be a critical episode for the successful establishment of the seedlings. After emergence and 193 establishment, seedlings of Nitraria sphaerocarpa can populate the mobile dunes or semi-mobile dunes in the sandland habitat. Experimental procedure Fruits were collected in the fall of 2004 from multiple individuals in desert. One fruit has only one seed. Seeds were cleaned, dried at room temperature for 2 –3 weeks then stored at 8 C under dry, dark conditions. Seeds were weighed singly and sorted into three seed size-classes based on mass per seed: large (23.49 ± 2.999 mg, mean ± SE, n = 700), medium (17.31 ± 1.545 mg, mean ± SE, n = 700) and small (10.78 ± 1.874 mg, mean ± SE, n = 700). For each group, counted seeds (20 each) were planted at 0, 1, 2, 3, 4, 5 and 6 cm depths in plastic pots (15.5 cm in diameter, 20 cm in depth) filled with unsterilized sifted sand. The drainage outlet at the bottom of the pots was covered with strips of nylon mesh to prevent the loss of sand while allowing drainage of excess water. Sand was poured into each pot up to the lower mark and moistened. Seeds were then placed on the sand surface and the pots were filled up to the upper mark with additional sand. There were five pots per treatment. Pots were watered daily with tap water. Temperature in the greenhouse was maintained at 23 C during the day (16 h photoperiod) and 14 C at night. Emerged seedlings were counted daily. Seedling emergence was defined as the first appearance of a seedling at the sand surface. After 8 weeks of seedling emergence and growth in the greenhouse, the experiment was terminated. All the seedlings were measured for their height above the sand surface, and then they were harvested. At harvest, the seedlings were dug out by hand and trowel, and care was taken to collect as many roots belonging to the seedling as possible. Roots were cleaned with water. Seedlings were separated into three parts: aboveground stems, belowground stems and roots. After drying at 70 C for 48 h, each fraction was weighed. biomass allocation (root mass ratio, belowground and aboveground stem-mass ratio) were analyzed using two-way ANOVAs in the treatments. Tukey –Kramer multiple comparison test was used to determine differences in each trait among seed size-classes within a single burial depth class. Since no seedlings emerged from the small seeds in all of the replicates at 6 cm burial depth, interaction between seed sizes and burial depth was not calculated. Results Seedling emergence In the seven treatments, the percent emergence was significantly affected by both burial depth (F=98.134, d.f.=6, p<0.0001) and seed size (F=18.668, d.f.=2, p=0.0002). Seedling emergence was highest at 2 cm burial depth, but decreased with increasing burial depth in each seed size-class (Figure 1). The percent emergence was not significantly different between large and small sized seeds, although the emergence was usually highest for large seeds, and lowest for small seeds at each sand burial depth. In the sand burial depth of 0 cm, the emergence was lower for the drought. There was a significant decline in emergence at 4 and 5 cm burial depths. No seedlings emerged from 6 cm burial depth for the small size seeds. Time to emergence often determines whether a plant competes successfully with its neighbors, is consumed by herbivores, infected with diseases, and whether it flowers, reproduces, and matures properly by the end of the growing season. The mean number of days to the first seedling emergence was affected by sand burial depth (F=25.235, d.f.=5, p<0.0002), but not by seed size (F=2.648, d.f.=2, p=0.119). Seedling emergence occurred earliest for the seeds from shallow burial depths (0 –2 cm), and delayed with the increasing burial depth (Figure 2). Statistical analysis Seedling size The effects of burial depth and seed size on the mean number of days to emergence, percent emergence, seedling mass, seedling height and Seedling size was measured in terms of seedling mass and seedling height. Seedling mass and 194 90 L M S 80 Emergence (%) 70 60 50 40 30 20 10 0 0 1 2 3 4 5 6 Sand burial depth (cm) Figure 1. Mean (±SE) percent emergence of seedlings at various sand burial depths (0, 1, 2, 3, 4, 5, 6 cm) for large (L), medium (M) and small (S) sized seeds of Nitraria sphaerocarpa. 16 L M S Time to emergence (day) 14 12 10 8 6 4 2 0 0 1 2 3 4 5 6 Sand burial depth (cm) Figure 2. Mean (±SE) number of days to the first emergence of seedlings at various sand burial depths (0, 1, 2, 3, 4, 5, 6 cm) for large (L), medium (M) and small (S) sized seeds of Nitraria sphaerocarpa. seedling height were significantly affected by both burial depth (F=22.660, d.f.=5, p<0.0001; F=18.922, d.f.=5, p<0.0001, respectively) and seed size (F=22.744, d.f.=2, p<0.0002; F=6.190, d.f.=2, p=0.018, respectively). Both seedling mass and seedling height were usually greatest at 2 cm burial depth, and decreased with an increase in burial depth for all seed size-classes (Figures 3 and 4). Although seedling mass was usually greatest for large seeds and least for small seeds at each burial depth, little difference was observed in seedling height at shallow burial depths (0 –3 cm). Biomass allocation Both root-mass ratio and belowground stem-mass ratio were significantly affected by both burial depth (F=35.178, d.f.=5, p<0.0001; F=25.749, d.f.=5, p<0.0001, respectively) and seed size 195 9 L M S 8 Seedling mass (mg) 7 6 5 4 3 2 1 0 0 1 2 3 4 5 6 Sand burial depth (cm) Figure 3. Mean (±SE) seedling mass at various sand burial depths (0, 1, 2, 3, 4, 5, 6 cm) for large (L), medium (M) and small (S) sized seeds of Nitraria sphaerocarpa. 14 L M S Seedling height (cm) 12 10 8 6 4 2 0 0 1 2 3 4 5 6 Sand burial depth (cm) Figure 4. Mean (±SE) seedling height at various sand burial depths (0, 1, 2, 3, 4, 5, 6 cm) for large (L), medium (M) and small (S) sized seeds of Nitraria sphaerocarpa. (F=18.561, d.f.=2, p=0.0004; F=7.162, d.f.=2, p=0.012, respectively), while aboveground stemmass ratio was affected by only burial depth (F=10.292, d.f.=5, p=0.001) but not by seed size (F=0.465, d.f.=2, p=0.641). In each seed sizeclass, with increasing burial depth, both root-mass ratio and aboveground stem-mass ratio decreased, while belowground stem-mass ratio increased. In each burial depth, with decreasing seed size, belowground stem-mass ratio increased, while root-mass ratio decreased (Figure 5). Discussion Seedling performance at sand burial depth Seed burial has both positive and negative consequences for seedling emergence. The most obvious negative consequence is burial so deep that seed germination is prevented. Germination sometimes occurs with deep burial but seed reserves may be exhausted before the seedling reaches the soil surface, which leads to seedling death. As might be 196 100% 90% Biomass allocation 80% 70% 60% 50% 40% 30% 20% 10% 0% L0 M0 S0 L1 M1 S1 L2 M2 S2 L3 M3 S3 Sand burial depth (cm) L4 M4 S4 L5 M5 S5 L6 M6 Figure 5. Biomass allocation of seedlings at various sand burial depths (0, 1, 2, 3, 4, 5, 6 cm) for large (L), medium (M) and small (S) sized seeds of Nitraria sphaerocarpa. () Aboveground stem; ( ) belowground stem; (j) root. expected, deep burial is more detrimental to small seeded than to large seeded species (King and Oliver 1994; Forcella et al. 2000). The benefits of burial are reduced exposure to air. Soil overlying very young seedlings creates mulch that maintains high humidity and allows growth to proceed relatively rapidly. Moreover, soil burial also provides protection of seeds and seedlings from abnormally low and high air temperatures as well as predators that dwell on or near the soil surface. Consequently, emergence patterns of the species exhibit parabolic relationships with soil burial depth (Forcella et al. 2000). The burial experiment of Nitraria sphaerocarpa showed that deep burial reduced seedling emergence. Similar relationship was reported in other species. The highest percent emergence of Calamovilfa longifolia seedlings occurred from 1 –2 cm depths, however, as the depth of burial increased from 2 to 12 cm there was a significant decrease in seed percent emergence (Maun and Riach 1981). Zhang and Maun (1990) showed that seedlings of Panicum virgatum emerged from a mean depth of 4.73 and 11 cm was the maximum depth of in the field. Greater seedling emergence was observed for large seeds compared with small seeds, probably due to the greater food reserves that can produce longer shoots thus facilitating their emergence above the surface soil. Seedling mass and height of the Nitraria sphaerocarpa were significantly affected by burial depth, mainly due to the following reasons. A greater fraction of seed reserves would be exhausted by the time of the seedling emergence, because seedlings that emerged from deep burial showed smaller plant size initially. These seedlings would have less initial investment to future growth. And since seedlings from deeper burial depths usually emerge later than those from shallower burial depths, the period of growing season will be shorter and biomass gain and vertical growth will be lower than the seedlings from shallow buried seeds. Seed mass effects on establishment success A bigger seed means more energy reserves and hence, greater vigor and higher chance for emergence of seedlings from deeper locations and is better at tolerating a wide range of environmental stresses, such as predators, nutrient deprivation, drought, or prolonged periods in deep shade (Weller 1985; Leishman and Westoby 1994; Westoby et al. 1996; Leishman et al. 2000). And smaller seeds give rise to seedlings more liable to suffer high mortality from drought, physical disturbance by predators, or to suffer overtopping if they are adjacent to seedlings from larger seeds under favorable conditions. The same may be true for Nitraria sphaerocarpa seeds. The seed mass of Nitraria sphaerocarpa 197 used in this study ranged from 8.906 to 26.489 mg per seed. Once seedlings emerged, those from large seeds would probably have better survivorship because they have the greatest height and bigger root-mass ratio, showing the selective advantages of large seeds for effective resource acquisition, which would be of adaptive significance on sand dune systems because it would enhance absorption of water and nutrients and avoid drought stress near the surface. Similar results were also reported that seedlings of Strophostyles helvola from large seeds had greater survival than smaller seeds when they were subjected to the burial treatment (Yanful and Maun 1996). However, the opposite evidences were observed in other studies, which showed that there was no relationship between seed mass and percentage seedling emergence (Jurado and Westoby 1992; Reader 1993; Jones et al. 1994; Eriksson 1997; Chen et al. 2002) or no relationship between relative growth rate and seed mass (Fenner 1983; Shipley and Peters 1990; Swanborough and Westoby 1996). This suggested that the establishment success might depend on the species assemblage as well as growth conditions. Morphological changes in response to sand burial depth The seedlings from deep burial showed greater biomass allocation to stem, particularly the part below the ground surface, instead of the roots in each seed size-class. Such plastic response in biomass allocation suggests that the seedlings allocates lower energy reserves to the roots and diverts the rest to the stem to facilitate emergence from a deep location, as suggested by Seiwa et al. (2002). A similar phenomena has also been observed in some grass species in sand dunes that seedlings from a deeper location had a longer first internode or subcoleoptile internode but shorter roots than those in a more shallow planting (Maun and Riach 1981; Redmann and Qi 1992). This study, furthermore, revealed that the increasing investment to belowground stems instead of roots was also observed as the seed size decreased in each of the burial depths, suggesting that seedling emergence from small seeds is also facilitated by the morphologically adaptive allocation of the limited seed reserve. Optimal burial depth for establishment success Seed burial has both positive and negative consequences for seedling emergence, so there is an optimal range of burial depth to maximize the seedling emergence and subsequent seedling growth. In this study, the shallow burial depth seems to be advantageous for seedling establishment of the Nitraria sphaerocarpa, because the greatest emergence, height and mass were observed at 2 cm burial depth in this experiment. If optimal caching depth for a propagule is considered as the probability of escaping predation by a forager times the probability that it will emerge, grow and survive in the absence of predation, is maximized (Vander Wall 1993; Seiwa et al. 2002), the optimal depth for a seed of Nitraria sphaerocarpa is in the range of a shallow burial depth, approximately, 2 cm sand burial depth. In the optimal burial depth of 2 cm, there was little difference in the seedling emergence and the seedling height among seed size-classes, although seedling mass was dependent on seed size. During the restoration of the dune systems, Nitraria sphaerocarpa will be one of the most important species. And suitable environmental conditions can be selectively ameliorated to promote the seedling establishment success and seedling growth. The seeds of Nitraria sphaerocarpa with bigger mass are buried at 2 cm sand burial depth in practice will be valuable information. 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