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Journal of Plant Ecology VOLUME 4, NUMBER 3, PAGES 169–177 SEPTEMBER 2011 doi: 10.1093/jpe/rtq025 Seed germination traits of two plant functional groups in the saline deltaic ecosystems Advanced Access published on 8 September 2010 available online at www.jpe.oxfordjournals.org Xiao-dong Zhang, Wen-ting Xu, Bo Yang, Ming Nie and Bo Li* Coastal Ecosystems Research Station of the Yangtze River Estuary, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Institute of Biodiversity Science, Fudan University, 220 Handan Road, Shanghai 200433, People’s Republic of China *Correspondence address. Coastal Ecosystems Research Station of the Yangtze River Estuary, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Institute of Biodiversity Science, Fudan University, 220 Handan Road, Shanghai 200433, People’s Republic of China. Tel: +86-21-65642178; Fax: +86-21-65642178; E-mail: [email protected] or [email protected] Abstract Aims Salt stress resulting from soil salinization is one of the driving forces of the land degradation throughout the world. The modern Yellow River delta is one of the most saline areas in China. Phytoremediation can be an effective way to restore the salinized ecosystems, which requires selecting appropriate plant species. This study explored the germination responses of common plant species from contrasting habitats in the Yellow River delta to varying salinity, offering experimental information for ecosystem restoration in the Yellow River delta. Methods In this study, 15 common plant species from the Yellow River delta were divided into two groups (high-salinity and low-salinity groups) by their natural habitats using Canonical Correlation Analysis. Seeds of each species were treated with five salinity levels (0, 5, 10, 20 and 30 ppt), using a randomized complete block design, and germinated seeds were counted and removed daily for 28 days to calculate the final germination proportion and mean time to germination. The germination responses of seeds to salinity treatments were compared between the two groups. INTRODUCTION Salt stress resulting from soil salinization is one of the driving causes of the land degradation throughout the world. Estuarine wetlands occasionally experience seasonally high salinity resulting from the high evaporation, and are often undergoing secondary salinization due to their generally lower elevation, which are exposed to saline groundwater (Jolly et al. 2008). Nevertheless, a wide range of plant species, growing naturally on the coastal saline areas, can survive high salinity that is Important Findings In relation to salinity, seed germination behavior of the test species was closely related to the salinity level of the habitats over which they were distributed. Species from the habitats with higher salinity had generally higher final germination proportion but shorter mean time to germination than those from the habitats with lower salinity in all of five salinity treatments used. The final germination proportion and mean time to germination of low-salinity group species were more sensitive to salinity than those of high-salinity group species. Selecting the species with high final germination proportion and short mean time to germination is important for restoration of salinized land. Keywords: deltaic ecosystems traits d restoration d salinity d functional groups germination Received: 14 April 2010 Revised: 26 July 2010 Accepted: 1 August 2010 equal to or greater than that of seawater because of their particular physical mechanisms to accumulate ions in their vacuoles and cytoplasm or excrete the salt out of the leaves (Gorham 1995). Salt-tolerant species are often selected to reconstruct natural hydrologically-balanced communities. Here, an important question is: how are the plant species selected for revegetation? Aronson (1989) defines the species occurring under naturally saline conditions as ‘halophytes’, and the opposite as ‘glycophytes’. Barrett-Lennard (2002) has summarized the effects of salinity on growth of salt-tolerant Ó The Author 2010. Published by Oxford University Press on behalf of the Institute of Botany, Chinese Academy of Sciences and the Botanical Society of China. All rights reserved. For permissions, please email: [email protected] d 170 Journal of Plant Ecology species; and Chinnusamy et al. (2005) have reviewed the molecular basis of salt tolerance in plants. However, most previous studies have focused on the responses of plants to salinity within species (e.g., Houle et al. 2001; Megdiche et al. 2007; Rumbaugh et al. 1993). A few studies have been conducted to explore the general differences in plant traits between halophytes and glycophytes in relation to salinity. Woodell (1985) has systematically studied the relationship between germination dynamics and natural distribution of plant species. He used 27 coastal plant species, and grouped them into three types according to their germination responses to salinity treatments, finding that their natural distribution could be explained partially by their germination traits. Leyer and Pross (2009) have also revealed that species restricted to adjacent habitats have distinctive seed traits and germination behavior, although the habitats are distinguished by whether the river is flooded or not. Moreover, the seeds of plants growing in coastal meadows periodically exposed to sea water are more tolerant of salt stress than those of plants growing in dunes less exposed to sea water (Necajeva and Levinsh 2008). The composition, persistence and dynamics of natural plant communities are greatly influenced by the seed germination traits, which greatly determine the presence or absence of one species in particular habitats (Bungard et al. 1997). In salinized lands, continuous evaporation of water deposits salt on the soil surface, where many seeds are available (Tobe et al. 2001). Thus, germination traits play a major role in the distribution of species in saline environments (Ungar 1978). Most studies addressing the functional ecology of plant communities typically start with partitioning the total species pool into distinct clusters based on a set of a priori selected plant traits. Likewise, species in contrasting microhabitats can also be separated into several functional groups by their growing environments, and the distinction of some specific biological traits among the environmentally-based groups could be observed, e.g., seed traits and germination behavior strongly are related to flooding status in different habitats (Leyer and Pross 2009). In order to explore the differences of germination traits of species from salinity-varying environments and to offer experimental information for ecosystem restoration in the Yellow River delta, we conducted a laboratory study with field calibration. Specifically, the aims of our study reported here are two-fold: (i) to determine the effects of environmental variables on distribution patterns of plant species in saline ecosystems and (ii) to compare the germination traits of plant functional groups classified by environmental variables in relation to salinity. MATERIALS AND METHODS Seed collection The modern Yellow River delta (from 37°35’ to 37°54’N and 118°43’ to 119°20’E), formed from the repeated diversions of the river course and sediment deposition of the Yellow River since 1955 (Gao et al. 1989), is one of the saline areas in China. The hardly ameliorated zone, including salt marshes and the terraced uplands with secondarily salinized soil, covers >70% of the total area of the Yellow River delta, and the soil salt content in this area ranges from 2 to 30 ppt (Guan et al. 2001). Fifteen common species in the Yellow River delta were selected for germination test, whose major attributes are presented in Table 1, covering ;1600 km2. In mid-November 2006, seeds of 15 species were collected when they were mature in the salt marshes of the Yellow River delta. Bulk seeds of each species were obtained from at least 50 individuals, but Table 1: test species and their major attributes Species Family Life forma Halophyte or glycophyteb Functional group Seed mass (mg per seed) Polygonum aviculare Polygonaceae A Low salinity 2.89 6 0.15 Atriplex centralasiatica Chenopdiaceae A + High salinity 2.04 6 0.19 Suaeda glauca Chenopdiaceae A + High salinity 3.37 6 0.07 Suaeda salsa Chenopdiaceae A + High salinity 1.88 6 0.06 Salsola collina Chenopdiaceae A + Low salinity 1.11 6 0.09 Abutilon theophrasti Malvaceae A High salinity 8.00 6 0.68 Cucumis bisexualis Cucurbitaceae A + Low salinity 5.46 6 0.11 Limonium bicolor Plumbaginaceae P + High salinity 0.46 6 0.03 Apocynum venetum Apocynaceae P + High salinity 0.37 6 0.01 Metaplexis japonica Asclepiadaceae P High salinity 2.69 6 0.11 Rubia cordifolia Rubiaceae P Low salinity 10.37 6 0.78 Leonurus artemisia Labiatae A or B Low salinity 0.73 6 0.01 Tripolium vulgare Compositae A or B Low salinity 0.74 6 0.11 Artemisia lavandulaefolia Compositae P Low salinity 0.17 6 0.02 Artemisia scoparia Compositae A or P Low salinity 0.08 6 0.02 a b + ‘A’ for annual; ‘P’ for perennial and ‘B’ for biennial. Functional types classified by Zhao and Li (1999): ‘+’ for halophyte and ‘ ’ for glycophyte. Zhang et al. | Seed germination traits of plant functional groups 171 those of Cucumis bisexualis from a dozen of individuals as most plants had shed their seeds. The seeds were stored in refrigerator at 4°C for 2 months to break their dormancy. The florets of Polygonum aviculare and Limonium bicolor, the bracts of Atriplex centralasiatica and the cactus-like perianth of Suaeda glauca were removed to ensure the presence of seeds. Follicles and seed hairs were removed from Apocynum venetum and Metaplexis japonica seeds. The pericarps of C. bisexualis and Rubia cordifolia were removed from the seeds. Seeds of the other species could be directly obtained. Seeds were only used if they had intact seed coats and appeared to have embryos. Seed mass was obtained by weighing three lots of one-hundred seeds for each species. Germination test Germination experiments were carried out from mid-April to mid-May 2007. Fifteen species were tested for their germination responses to varying salinity. All seeds used in this study were surface sterilized in 1% sodium hypochlorite for 1 min, followed by repeated rinsing with distilled water twice. One experimental unit consisted of 50 seeds of one species evenly placed on five filter paper layers imbibed with 10 ml of NaCl solution of constant concentration in 90-mm petri dishes with covers. Totally 1000 seeds of each species were treated at five salinity levels (0, 5, 10, 20 and 30 ppt), with four replicates per treatment. The experiment used a randomized complete block design, with the petri dishes blocked by growth chambers. Germination was carried out in the dark at 20°C, and seeds were considered as germinated when their emerging radicals were visible. Germinated seeds were counted and removed daily for a period of 28 days, after which no more germination was observed. In order to avoid the variation in salinity due to evaporation, one empty petri dish with a five-filter-paper layer imbibed with 10-ml deionized water was placed in the same chamber as control check. The mass of the petri dishes was weighed before and after being placed in the chamber for 1 week, and 2 g of mass loss was found, indicating that 2 g of water was evaporated within 1 week. Thus, 2 ml of deionized water was added to each dish to keep the moisture and salinity of filter paper. Species grouping based on field investigation It is hard to identify whether one species is halophyte or glycophyte. In order to determine if a species is adapted to saline environments, a field investigation was carried out in September 2007. Twelve sites (Fig. 1) were randomly selected in the Yellow River delta to explore the relationship between species distribution and environmental factors of natural communities, with six 1 3 1 m quadrats for each site. A total of 72 quadrats were sampled, and the abundance of each species was recorded. Three evenly distributed soil cores of 2.8 cm in diameter and 15 cm in depth were taken and mixed within each quadrat. Soil pH, salinity and water content of each quadrat with three replicates were measured. Figure 1: the sampling sites in the Yellow River delta. Circles stand for sampled communities along the Yellow River and triangles for the towns nearby the sampled sites. The abundance of the 13 species (other two species not included and explained below) were extracted and transformed to frequency by the formula: Aij Qij = 13 ; + Aij j 1 where Qij stands for the frequency of species j in quadrat i, Aij is the abundance of species j in quadrat i and j is from 1 to 13. The frequency matrix of 13 species in 72 quadrats with environmental variables, pH, salinity and water content was analyzed by Canonical Correlation Analysis (CCA) method using CANOCO V. 4.5. Data analyses The final germination proportion was calculated and the mean time to germination was then estimated by the formula (Brenchley and Probert 1998): 28 + Nij 3 dj MTG = j 1 28 ; + Nij j 1 where MTGi is the mean time to germination of species i, and Nij is the number of seeds of species i germinating on day j. The means of final germination proportion and mean time to germination for five treatments of high-salinity group and low-salinity group species (based on the result of species 172 Journal of Plant Ecology grouping) were compared using independent sample t-test. In order to avoid the interspecific difference in the trends of final germination proportion and mean time to germination with the increasing salinity, the data on final germination proportion were transformed to relative final germination proportion as proportionF/proportionM, where proportionF is the final germination proportion in each salinity treatment and proportionM is the mean proportion of final germination in control treatment. The trends of relative final germination proportion and mean time to germination of high- and low-salinity group species were linearly regressed and an analysis of covariance (ANCOVA) was performed to test the difference in slope of two groups with salinity as covariate. All statistic analyses were analyzed by using SPSS13.0. RESULTS Species grouping The 15 species were separated into two groups (Fig. 2), highand low-salinity group species, which correspond to halophytes and glycophytes, respectively. The mean salinity of the habitats for the upper cluster was >3 ppt and that for the lower cluster of seven species was all <2 ppt. However, two species, Leonurus artemisia and R. cordifolia, were not included in CCA (Fig. 2), because they did not occur in randomly selected quadrats but were common in the Yellow River delta. Because these two species are typical glycophytes (Zhao and Li 1999), they were classified into low-salinity group. The high-salinity group species, including A. centralasiatica, S. glauca, Suaeda salsa, L. bicolor, A. venetum and M. japonica, were mainly distributed in the environments with the salinity ranging from 0.7 to 14.8 ppt with the mean (6standard error (SE)) of 4.46 6 2.22 ppt, and the low-salinity group species, including P. aviculare, Salsola collina, C. bisexualis, R. cordifolia, L. artemisia, Tripolium vulgare, Artemisia lavandulaefolia, Abutilon theophrasti and Artemisia scoparia, were distributed mainly in the environments with the salinity ranging from 0.5 to 3.1 ppt with the mean (6SE) of 1.51 6 0.34 ppt. The first two axes of CCA of species–environment relations explained 89.5% of the total variance. Final germination proportion The mean final germination proportion of high-salinity group species was significantly higher than that of low-salinity group species in all of five salinity treatments (Fig. 3 and Fig. 4A). Final germination proportions of almost all high-salinity group species were very high, being close to 1.0 in controls, while those of only four of low-salinity group species including C. bisexualis, S. collina , R. cordifolia and T. vulgare were slightly >0.5 in controls. Five low-salinity group species including C. bisexualis, L. artemisia, P. aviculare, R. cordifolia, A. scoparia and A. lavandulaefolia failed to germinate at the salinity of >20 ppt, while germination of all high-salinity group species occurred in all salinity treatments (Fig. 3). Final germination proportion of both high- and low-salinity group species generally decreased with increasing salinity, but Figure 2: thirteen species were classified into high- and low-salinity groups by environmental factors. Closed symbols stand for halophytic species and open symbols for glycospecies species according to Zhao and Li (1999). Numbers in parentheses indicate the salinity of the habitats of the species. Species codes are 1, Atriplex centralasiatica; 2, Cucumis bisexualis; 3, Artemisia lavandulaefolia; 4, Limonium bicolor; 5, Metaplexis japonica; 6, Salsola collina; 7, Tripolium vulgare; 8, Abutilon theophrasti; 9, Polygonum aviculare; 10, Suaeda glauca; 11, Artemisia scoparia; 12, Apocynum venetum and 13, Suaeda salsa. high-salinity group species were obviously less sensitive to salinity than low-salinity group species. Though the relative germination proportion of both groups was negatively related to the salinity (Table 2), ANCOVA results showed that the interaction between salinity and functional group was significant (Table 3), indicating that the relative germination proportion of low-salinity group species declined with increasing salinity faster than that of high-salinity group species. Final germination proportion of A. centralasiatica, A. venetum, S. salsa and M. japonica of highsalinity group even had a slight increase from 0 to 5 ppt of salinity, but no species in low-salinity group had similar responses at low salinities. Final germination proportions of five of highsalinity group species were close to 1.0 at salinities of 0, 5 and 10 ppt, S. glauca and S. salsa of which showed consistently high germination proportion even at salinities of 20 and 30 ppt. Metaplexis japonica, A. venetum and L. bicolor had a dramatic decline in final germination proportion from >0.8 to <0.5 between 10 and 20 ppt. Final germination proportions of six species of low-salinity group declined from 5 ppt (Fig. 3). Mean time to germination Mean time to germination of both functional groups increased with increasing salinity, and that of low-salinity group was significantly longer than that of high-salinity group for all of five Zhang et al. | Seed germination traits of plant functional groups 173 Figure 3: final germination proportion and mean time to germination (days) of 15 common species collected in the Yellow River delta. salinity treatments (P < 0.05) (Fig. 4B). Mean time to germination of high-salinity group species was <3 days, while that of the low-salinity group species steadily increased from 3.8 to 6.8 days when the salinity increased from 0 to 10 ppt. Both of the two functional groups had a dramatically increasing mean time to germination between 10 and 20 ppt, from 2.8 to 6.5 days for high-salinity group and from 6.8 to 14.4 days for low-salinity group. Cucumis bisexualis, P. aviculare and R. cordifolia failed to germinate at 20 and 30 ppt, and L. artemisia and A. scoparia failed to germinate at 30 ppt (Fig. 3). Salinity treatments generally increased the mean time to germination of both groups (Table 2), but high-salinity group species were obviously less sensitive to salinity than lowsalinity group species. The ANCOVA results showed that the interaction between salinity and functional group was significant (Table 3), indicating that the mean time to germination of 174 Journal of Plant Ecology study, we focused on the salinity effects on two germination traits, final germination proportion and mean time to germination. Distinctive patterns of germination traits of high- and lowsalinity group species were observed in relation to salinity. Classification of functional groups Traditionally, four trait-based classification systems have been used to divide plant species into different functional groups (Lavorel et al. 1997), one of which is built on the relationship between species distribution pattern and the environmental factors (Deckers et al. 2004; Purdy et al. 2005). Here we divided the 15 species into two groups based on their natural habitats that are mainly different in soil salinity. Although the three environmental factors, pH, salinity and water content, might not be adequate to characterize the habitats, the community composition in the Yellow River delta is determined primarily by soil salinity (Zhang et al. 2007). Similar results can be observed in similar ecosystems, e.g., the upper intertidal ecosystems in south California (Callaway et al. 1990) and the brackish riverbanks in New Zealand (Wilson et al. 1996). Our CCA results demonstrated that the distribution pattern of highsalinity group species was determined primarily by soil salinity, while that of low-salinity group species was affected by several other factors. However, in this study some of the previously defined halophytes were classified into glycophytes or vice versa. Three species (S. collina, C. bisexualis and T. vulgare) that are considered as halophytes by Zhao and Li (1999) were sorted into low-salinity group, while two species (M. japonica and A. theophrasti) that are not considered as halophytes were sorted into high-salinity group in this study. This inconsistence may to a certain degree reflect the complex responses of plants to salt stress through tolerance or adaptation. The germination behavior of these above five species was similar to that of the other species within their groups (Fig. 3). Therefore, the classification of the 15 species by the seed germination traits basically reflected their distributions that were observed in the field. Figure 4: germination responses of high- and low-salinity group species to salinity (ppt). (A) Mean germination proportion; and (B) Mean time to germination (days). Values are mean 6 SE. Significant differences (t-test, P < 0.05) are marked by asterisks. low-salinity group species increased with increasing salinity faster than that of high-salinity group species. Mean time to germination of A. theophrasti, A. venetum, L. bicolor and M. japonica of high-salinity group increased dramatically from 10 to 20 ppt and that of others of high-salinity group only slightly increased through all five treatments. DISCUSSION Species growing in similar habitats often have similar ways of responding to the abiotic factors. The aim of this paper was to explore the differences of germination traits between two functional groups that are distributed over and might have adapted themselves to the environments of varying salinity. In this Differential germination responses of two groups to salinity For individual species, it has been widely recognized that final germination proportion decreases and mean time to germination increases along the salinity gradient (Egan and Ungar 1999; Huang et al. 2003; Nolasco et al. 1996), but how different germination traits are among the functional groups remains largely unclear. This study provided the evidence that seed germination was strongly correlated with the salinity under natural conditions in which plants grow. Generally, the final germination proportion of high-salinity group species was higher than that of lowsalinity group species (Fig. 4A), and the high-salinity group species germinated faster than low-salinity group species in all of five salinity treatments (Fig. 4B) as observed in previous studies (Ungar 1978). This implies that species growing in saline habitats might have adapted themselves to the high soil salinity, possessing the ability of well germinating in saline Zhang et al. | Seed germination traits of plant functional groups 175 Table 2: summary of linear regression analyses between salinity (x) and final germination proportion and mean time to germination (y) of two functional groups R2 (adjusted) P 0.020 0.479 <0.001 0.034 0.715 <0.001 1.468 0.199 0.223 <0.001 3.581 0.358 0.327 <0.001 y Groups Intercept Final germination proportion High salinity 1.078 Low salinity 0.965 Mean time to germination High salinity Low salinity Slope Table 3: analysis of covariance testing the difference in germination response of two functional groups (main factor) to salinity (covariate) Final germination proportion Mean time to germination Source of variation Degrees of freedom (df) F P df F P Salinity 1, 296 269.49 <0.001 1, 296 18.88 <0.001 Functional group 1, 296 83.72 0.008 1, 296 13.38 0.001 Salinity 3 group 1, 296 2.13 <0.001 1, 296 7.12 0.008 environments. High germination proportion and short germination time could facilitate plants to get established faster in the salt marshes when their seeds are deposited on a ‘safe site’ during their drift with the tidal water (Mariko et al. 1992). Final germination proportion and mean time to germination of high-salinity group species were almost unaffected by low salinities of 5 and 10 ppt (Fig. 3), which has also been observed in other salt marsh plants (Mariko et al. 1992) and inland desert halophytes (Yang et al. 2009). Two species (S. salsa and S. glauca) had high final germination proportion and short mean time to germination even at 30 ppt, at which the other species hardly germinated. In the field, S. salsa is the pioneer species in newly formed mudflats and most saline environments where other species cannot grow well. S. glauca seemed not to be as salt-tolerant as S. salsa as it is usually mixed with other species in upland rather than intertidal areas. However, S. glauca may be more competitive than S. salsa as the former always has greater aboveground biomass and higher occurrence frequency in mildly saline communities (He et al. 2009). The low-salinity group species with lower germination proportion and longer germination time (Fig. 4) may take the riskavoiding strategy through delaying germination, making their seeds geminate in milder environments with lower salinity and higher temperature so that they are able to become a stronger competitor during the growing season (Purdy et al. 2005; Ungar 1998). Species from unstable and unpredictable environments may have low germination proportion as well as germination speed because seedling establishment is unpredictable as germination phase of a species lasting for a longer time can avoid the risk of seedling mortality caused by environmental stochasticity like disastrous events (Mariko et al. 1992). Final germination proportions of all low-salinity group species were close to zero when the salinity increased to 20 ppt (Fig. 3). Although it is hard to ascertain whether or not the decrease of final germination proportion at high salinity is adaptive, the inhibition might be an advantage for plants to keep their seed bank and wait for the coming of benign conditions. Final germination proportion and mean time to germination of low-salinity group species were more sensitive to salinity than those of high-salinity group species (Table 2), which basically explained the natural distribution of the study species in the field. When the soil salinity was low, the low-salinity group species dominated the communities as they were more competitive during growing stage. On the other hand, when the soil salinity was high, the high-salinity group species dominated the communities in the field partially because they had good germination performance under the saline environments. Implications for land restoration Studying seed germination of functional groups in saline environments can provide important information for species selection in ecosystem restoration. Species in the same group have similar patterns of responding to salinity. Although not all species in the saline deltaic ecosystems were tested in this study, the patterns revealed from this study may also help us to predict the germination dynamics of untested species. An earlier study conducted by Woodell (1985) grouped coastal plants into three types according to their germination behavior in response to salinity and explained their distribution patterns in the field through using their germination traits. Our study shared the similar aim to Woodell’s (1985), while it was verified in an opposite way. Woodell’s sites and ours were both located close to the sea, and the ecosystems were largely affected by salinity. Thus, the relationship may be applicable to similar coastal ecosystems, while the application in other systems (e.g. arid regions) needs further research. Halophytes’ seeds possess varying degree of salt tolerance during germination (Ungar 1995). The salinity of the natural habitats (<10 ppt for high-salinity group species and <2 ppt for 176 low-salinity group species) was much lower than that used in this experiment. Final germination proportion and mean time to germination of a particular species in a natural community cannot be directly determined only by the salinity level in its habitats, but should also be linked to other environmental conditions such as temperature and water availability at the time of germination (Noe and Zedler 2000). The mean temperature in the Yellow River delta in spring (April) when most of seeds germinate was 13.4°C in 2007, which was much lower than the temperature used in our experiment. Another possible reason for the high final germination proportion was that the seeds were placed on filter paper in water-filled petri dishes, while the actual soil water content was much lower in the field. In addition, the soil salinity fluctuates seasonally as the precipitation varies throughout the year (Sumner and Belaineh 2005). In spring, the precipitation was 14.7 mm, being much lower than that in August (237.9 mm) (Zhao 2007), and thus, the soil salinity may be much higher during the germinating season than during the growing season. This may indicate that many species in the Yellow River delta may be filtrated during the germination stage at which the conditions are much more severe than those during the growing season. This has also proved that selecting the species with high final germination proportion and short mean time to germination is important for the restoration of saline lands. CONCLUSIONS Our study demonstrated that seed germination behavior of plant species, in relation to soil salinity, was closely related to the salinity of the habitats over which they are distributed. High-salinity group species had generally higher final germination proportion and shorter mean time to germination than low-salinity group species in all of five salinity treatments. Final germination proportion and mean time to germination of lowsalinity group species were more sensitive to salinity than those of high-salinity group species. Our results suggested that some species in Yellow River delta may be filtrated during the germination stage at which the conditions are much more severe than those during the growing season, especially in the environments with high salinity. Therefore, selecting the species that have greater germinating ability and germinate faster is critical to the success of saline land restoration through revegetation. FUNDING National Basic Research Program of China (2006CB403305), and a Research Award for Outstanding Doctoral Students of Fudan University to Xiao-dong Zhang. ACKNOWLEDGEMENTS We thank Mr. Naishun Bu for field guidance and seed collection and Ms. Tingting Zhang for drawing the map. Our appreciation also goes to Prof. Fazeng Li for species identification. Conflict of interest statement: None declared. Journal of Plant Ecology REFERENCES Aronson JA (1989) Haloph: A Database of Salt Tolerant Plants of the World. Tucson, AZ: Office of Arid Lands Studies, University of Arizona. Barrett-Lennard EG (2002) Restoration of saline land through revegetation. Agric Water Manage 53:213–26. Brenchley JL, Probert RJ (1998) Seed germination responses to some environmental factors in the seagrass Zostera capricorni from eastern Australia. Aquat Bot 62:177–88. Bungard RA, Daly GT, McNeil DL, et al. (1997) Clematis vitalba in a New Zealand native forest remnant: does seed germination explain distribution? N Z J Bot 35:525–34. Callaway RM, Jones S, Ferren WR, et al. (1990) Ecology of a mediterranean-climate estuarine wetland at Carpinteria, California: plant distributions and soil salinity in the upper marsh. Can J Bot 68:1139–46. Chinnusamy V, Jagendorf A, Zhu JK (2005) Understanding and improving salt tolerance in plants. Crop Sci 45:437–48. Deckers B, Verheyen K, Hermy M, et al. (2004) Differential environmental response of plant functional types in hedgerow habitats. Basic Appl Ecol 5:551–66. Egan TP, Ungar IA (1999) The effects of temperature and seasonal change on the germination of two salt marsh species, Atriplex prostrata and Salicornia europaea, along a salinity gradient. Int J Plant Sci 160:861–7. Gao S, Li Y, An F, et al. (1989) The Formation and Deposition Environment of Yellow River Delta. Beijing, China: Science Press. Gorham J (1995) Mechanism of salt tolerance of halophytes. In: Allah CRC, Malcolm CV, Handy A (eds). Halophytes and Biosaline Agriculture. New York: Marcel Dekker, 207–23. Guan YX, Liu GH, Wang JF (2001) Saline-alkali land in the Yellow River delta:Amelioration zonation based on GIS. J Geogr Sci 11:313–20. He Q, Cui BS, Cai YZ, et al. (2009) What confines an annual plant to two separate zones along coastal topographic gradients? Hydrobiologia 630:327–40. Houle G, Morel L, Reynolds CE, et al. (2001) The effect of salinity on different developmental stages of an endemic annual plant, Aster laurentianus (asteraceae). Am J Bot 88:62–7. Huang ZY, Zhang XS, Zheng GH, et al. (2003) Influence of light, temperature, salinity and storage on seed germination of Haloxylon ammodendron. J Arid Environ 55:453–64. Jolly ID, McEwan KL, Holland KL (2008) A review of groundwatersurface water interactions in arid/semi-arid wetlands and the consequences of salinity for wetland ecology. Ecohydrology 1: 43–58. Lavorel S, McIntyre S, Landsberg J, et al. (1997) Plant functional classifications: from general groups to specific groups based on response to disturbance. Trends Ecol Evol 12:474–8. Leyer I, Pross S (2009) Do seed and germination traits determine plant distribution patterns in riparian landscapes? Basic Appl Ecol 10:113–21. Mariko S, Kachi N, Ishikawa S, et al. (1992) Germination ecology of coastal plants in relation to salt environment. Ecol Res 7:225–33. Megdiche W, Ben Amor N, Debez A, et al. (2007) Salt tolerance of the annual halophyte Cakile maritima as affected by the provenance and the developmental stage. Acta Physiol Plant 29:375–84. Zhang et al. | Seed germination traits of plant functional groups Necajeva J, Levinsh G (2008) Seed germination of six coastal plant species of the baltic region: effect of salinity and dormancy-breaking treatments. Seed Sci Res 18:173–7. Noe GB, Zedler JB (2000) Differential effects of four abiotic factors on the germination of salt marsh annuals. Am J Bot 87:1679–92. Nolasco H, VegaVillasante F, RomeroSchmidt HL, et al. (1996) The effects of salinity, acidity, light and temperature on the germination of seeds of cardon (Pachycereus pringlei (S Wats) Britton & Rose, Cactaceae). J Arid Environ 33:87–94. Purdy BG, MacDonald SE, Lieffers VJ (2005) Naturally saline boreal communities as models for reclamation of saline oil sand tailings. Restor Ecol 13:667–77. Rumbaugh MD, Pendery BM, James DW (1993) Variation in the salinity tolerance of strawberry clover (Trifolium-fragiferum L.). Plant Soil 153:265–71. Sumner DM, Belaineh G (2005) Evaporation, precipitation, and associated salinity changes at a humid, subtropical estuary. Estuaries 28:844–55. Tobe K, Zhang LP, Qiu GYY, et al. (2001) Characteristics of seed germination in five non-halophytic Chinese desert shrub species. J Arid Environ 47:191–201. 177 Ungar IA (1978) Halophyte seed-germination. Bot Rev 44:233–64. Ungar IA (1995) Seed germination and seed bank ecology of halophytes. In: Kijel J, Galili G (eds). Seed Development and Germination. New York: Marcel and Dekker Inc., 599–627. Ungar IA (1998) Are biotic factors significant in influencing the distribution of halophytes in saline habitats? Bot Rev 64:176–99. Wilson JB, King WM, Sykes MT, et al. (1996) Vegetation zonation as related to the salt tolerance of species of brackish riverbanks. Can J Bot 74:1079–85. Woodell SRJ (1985) Salinity and seed-germination patterns in coastal plants. Vegetatio 61:223–9. Yang HL, Huang ZY, Baskin CC, et al. (2009) Responses of caryopsis germination, early seedling growth and ramet clonal growth of Bromus inermis to soil salinity. Plant Soil 316:265–75. Zhang G, Wang R, Song B (2007) Plant community succession in modern Yellow River delta, China. J Zhejiang Univ Sci B 8:540–8. Zhao HR (editor) (2007) Dongying Statistical Yearbook 2007. Statistic Bureau of Dongying City, Shandong Province, China. Zhao KF, Li FZ (1999) Chinese Halophytes. Beijing, China: Science Press.