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Effects of seed storage on germination of two succulent desert halophytes with little dormancy and transient seed bank
Acta Ecologica Sinica 33 (2013) 338–343
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Effects of seed storage on germination of two succulent desert halophytes with little dormancy and transient seed bank Ali El-Keblawy ⇑ Dept. of Applied Biology, Faculty of Science and Sharjah Research Academy, University of Sharjah, Sharjah, United Arab Emirates
a r t i c l e
i n f o
Article history: Received 9 March 2012 Revised 13 April 2013 Accepted 18 September 2013
Keywords: Dormancy Germination Desert halophytes Seed storage Transient seed bank
a b s t r a c t Seeds of both Salsola imbricata and Haloxylon salicornicum have high germination level and germination speed, and form a transient seed bank in nature. The impacts of storage period and condition on germination level and speed were assessed in the two species. Storage for three months significantly increased both germination level and speed of seeds stored under the different conditions, compared to that of fresh seeds. In both species, nine months storage did not affect germination percentage in cold storage seeds, but completely inhibited it in field seeds. Storage for longer time in room and warm temperatures resulted in significant reduction or complete inhibition in the germination of the two species, so this was more pronounced in H. salicornicum. Storage significantly increased germinate rate index of seeds stored in all conditions till 17 months in S. imbricata and till 12 months in H. salicornicum. In both species, fridge storage had little effects on final germination and germination speed of seeds incubated at the different temperatures, compared to fresh seeds. However, room temperature and warm storages significantly reduced final germination and germination speed at the different temperatures, so the reduction was more pronounced at 35 °C, especially in H. salicornicum. Ó 2013 Ecological Society of China. Published by Elsevier B.V. All rights reserved.
1. Introduction It has been documented that natural selection favors environmental cueing mechanisms that decrease the probability of encountering unacceptable growth conditions following germination [1]. Generally, germination-timing mechanisms have evolved in response to selection pressures on both seed and seedlings [2,3]. In areas with winter rains and hot dry summer, seeds ripe and shed at the beginning of summer. In temperate areas, with cold winters and summer rains, seed ripening and shedding is frequent in autumn. In both cases, time of seed shedding does not coincide with conditions suitable for germination and seedling establishment. Consequently, seeds of many plants in both geographical regions develop innate dormancy and require a period of after-ripening to break their dormancy. Dry storage at high temperatures during summer months has been used to break dormancy in several winter species of arid and semi-arid deserts that shed their seeds at spring [3–5]. However, cold stratification (chilling) is required to break dormancy in many summer species of temperate climatic regions that their seeds spend the unfavourable cold winter in dormant state [2,6].
⇑ Permanent address: Dept. of Biology, Faculty of Education in Al-Arish, Suez Canal University, Egypt. E-mail address: [email protected]
Haloxylon salicornicum and Salsola imbricata (Chenopodiaceae) are perennial shrubs widely distributed in sandy habitats of the Arabian deserts. Both species are succulent halophytes and welladapted to endure severe environmental stresses and human disturbances in the deserts. H. salicornicum has been considered one of the most promising species for re-seeding deteriorating desert range vegetation and for sand dune fixation [7]. In addition, S. imbricata has the ability to stabilize sand dunes and to restore degraded, oil-polluted soils [8,9]. Both H. salicornicum and S. imbricata ripen and shed their seeds early in the growing season (early winter). This coincides with the onset of suitable conditions for germination and seedling establishment (e.g., availability of rainfall and lower temperatures) are optimum for germination and seedling establishment). Shortly after effective rainfalls, many seedlings appear under and around the maternal plants (Ali El-Keblawy, unpublished data). Under laboratory conditions, fresh harvested seeds of both species germinate to a very high level with high speed [10,11]. Seed bank studies indicated that a transient nature of the seed bank both in S. imbricata [12,13] and H. salicornicum [14,15]. Dry storage usually results in the decrease in germination requirements in seeds of many species of arid and semiarid lands. Generally, germination requirements usually become less specific after seed dry storage [1]. For example, the need for high temperature and light to achieve greater germination in fresh seeds of Prosopis juliflora was significantly reduced after seed stored dry
1872-2032/$ - see front matter Ó 2013 Ecological Society of China. Published by Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.chnaes.2013.09.008
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at room temperatures for 8 months [16]. Similarly, seeds of the desert herb Plantago coronopus stored for two months germinated under narrow range of temperatures, but germinated under wider range of temperatures when stored in their inflorescences under natural desert habitats for one year [17]. These species developed innate dormancy and form persistent seed bank. However, few studies have assessed the impact of different storage conditions on temperature requirement for desert shrubs with a transient seed bank (but see [7,18,38]. The aim of this study was to assess the impact of different storage periods and conditions (e.g., cold, warm, room temperatures and natural field conditions) on germination level and speed of the two desert shrubs Haloxylon salicornicum and Salsola imbricata, which have a transient seed bank. In addition, the study also aimed at assessing the impact of the different storage conditions for a period of one year on the temperature requirement during germination in the two species. 2. Materials and methods Fresh seeds of H. salicornicum and S. imbricata were collected during December from large populations in the inland desert of the United Arab Emirates (UAE), near Al-Ain. Seeds were randomly collected from about 50 plants of each species that represent the genetic diversity of the populations. Seeds of each species were divided into five groups. Seeds of one group were germinated immediately after collection (within 5 days, hereafter referred as fresh seeds). Seeds of the other four groups were put into 4 cm 6 cm mesh bags. The bags were stored in air conditioned room temperatures (20–23 °C), at freezer ( 4 °C, hereafter referred as cold storage), in oven adjusted at 40 °C ± 2 °C (hereafter referred as warm storage) and on soil surface of a natural habitat, where the two species are naturally grown. The moisture content of the seed during room temperatures, cold and warm storage ranged between 14% and 15%. However, moisture content of seeds stored in natural habitats varied greatly between 20% during day times to 40% during night and morning times (Ali El-Keblawy, unpublished data). When the local weather forecast expected a rain, seeds of the natural habitats were removed and returned back shortly after improvement of the weather. The site of natural seed storage received only one effective rain during the study period. Seeds of the two species were tested for germination after 3, 9, 12 and 17 months of storage. Seeds were germinated in incubators adjusted to 15 °C for H. salicornicum and 20 °C for S. imbricata under continuous illumination with daylight fluorescent tubes (110 lmol photons/m2/s, 400–700 nm). The highest germination in light was recorded at 15 °C in H. salicornicum [11] and at 20 °C in S. imbricata [10]. In order to assess the impact of different storage conditions on temperature requirements, seeds stored for one year in room temperature, freezer and oven were tested for germination in four incubators adjusted at 15, 20, 25 and 30 °C under continuous illumination with daylight fluorescent tubes. The germination was conducted in 9-cm Petri-dishes containing one disk of Whatman No. 1 filter paper, with 10 ml of distilled water. Four replicate dishes, each with 20 seeds, were used for each treatment. Seeds were considered to be germinated with the emergence of the radicles. Germinated seedlings were counted and removed every alternative day for 14 days following sowing. The rate of germination was estimated using a modified Timson’s index of germination velocity = RG/t, where G is the percentage of seed germination at 2 d intervals and t is the total germination period [20]. The maximum value possible using this index with these experiments was 700/14 = 50. The higher the value, the more rapid is the germination. Two way-ANOVAs were used to assess the impact of storage condition and seed storage period or temperature of incubation
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on final germination percentage and germination speed. Tukey test (Honestly significant differences, HSD) was used to estimate least significant range between means. The germination percentages were arcsine transformed to meet the assumptions of ANOVA. The transformation improved normality of distribution of data. All statistical methods were performed using SYSTAT, version 11.0. 3. Results 3.1. Effect of storage period and storage condition 3.1.1. Effect on final germination Both storage period and storage conditions and their interactions significantly affected final germination percentage of the two species (P < 0.001, Table 1). Generally, storage in freezer didn’t affect the level of final germination, compared to the other storage conditions, especially seeds stored under natural field conditions. The germination of fresh seeds was 76% and 68.3% in H. salicornicum and S. imbricata, respectively. Storage for three months significantly increased germination of seeds stored under different conditions, compared to germination of fresh seeds. The range of the germination increase was between 10.5% for seeds stored under warm conditions and 22.8% for seeds stored in field conditions in H. salicornicum and between 18.9% for seeds stored in freezer and 37.4% for seeds stored under warm conditions in S. imbricata. In H. salicornicum, storage for nine and 12 months completely inhibited germination of seeds stored in the field and significantly reduced germination of seeds stored in warm and room temperature conditions, but not affected germination of seeds stored in freezer, compared to fresh seeds. Further storage for 17 months led for almost complete inhibition in germination of seeds stored in warm and room temperature conditions and to a significant reduction for the germination of seeds stored in the freezer (Fig. 1a). For S. imbricata, nine months storage inhibited germination of field seeds, but not affect it for seeds stored under the other conditions. Storage for 12 and 17 months significantly reduced final germination of cold, room and warm storage seeds, but did not completely deteriorate it. The deteriorations in final germination, compared to fresh seeds, under warm, room temperature and cold conditions were 32.6%, 21.1% and 17.2%, respectively, after 12 months and 60%, 55.4% and 27.7%, respectively, after 17 months (Fig. 1b). 3.1.2. Effect on germination speed Similar to the impact on final germination, both storage period and storage conditions and their interactions significantly affected final germination speed of the two species (P < 0.001, Table 1). There was no significant difference in germination rate index between fresh seeds and those stored for three months under different conditions. Storage significantly increased germinate rate index of seeds stored for nine months in all storage conditions, except field seeds, which did not germinate. After 12 and 17 months, the increase in germination speed, compare to fresh seeds, was significant for S. imbricata stored at the different conditions, but was significant only for seeds of H. salicornicum stored in freezer (Fig. 2). After 17 months, the germination rate index of H. salicornicum seeds stored in room temperatures and warm conditions was significantly low, compared to that of fresh seeds (Fig. 2a). 3.2. Effects of storage condition and temperature of incubation 3.2.1. Effect on final germination The effects of storage condition and temperature of incubation and their interaction on final germination were significant in both
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Table 1 Two-way ANOVA showing the effect of storage period and storage condition on final germination percentage and germination rate index of Haloxylon salicornicum and Salsola imbricata seeds. Source of variation
df
Final germination percentage A: Haloxylon salicornicum Storage period (SP) Storage condition (SC) SP⁄SC Error
Mean-square
3 3 9 40
2.363 0.633 0.165 0.021
112.4 30.1 7.8
<0.001 <0.001 <0.001
B: Salsola imbricata Storage period (SP) Storage condition (SC) SP⁄SC Error
3 3 9 40
1.162 0.445 0.088 0.015
75.2 28.8 5.7
<0.001 <0.001 <0.001
Germination rate index A: Haloxylon salicornicum Storage period (SP) Storage condition (SC) SP⁄SC Error
3 3 9 40
12.806 18.546 4.985 0.265
48.3 69.9 18.8
<0.001 <0.001 <0.001
B: Salsola imbricata Storage period (SP) Storage condition (SC) SP⁄SC Error
3 3 9 40
2.332 23.394 2.840 0.001
3218.6 32281.8 3919.1
<0.001 <0.001 <0.01
80 60 40 Cold Field Room Warm
20 0
P
50 Germination rate index
Final germination (%)
100
F-ratio
3 9 12 17 Storage period (months)
40 30 20 Cold Field Room Warm
10 0
(a) Haloxylon salicornicum
3 9 12 17 Storage period (months)
(a) Haloxylon salicornicum 100
60 40 Cold Field Room Warm
20 0
3 9 12 17 Storage period (months)
(b) Salsola imbricata Fig. 1. Effect of storage period and storage conditions on final germination percentage of Haloxylon salicornicum and Salsola imbricata seeds.
H. salicornicum and S. imbricata (P < 0.01, Table 2). Germination of the fresh and stored seeds was significantly greater at 15, 20 and 25 °C, compared to 35 °C. Final germination of H. salicornicum seeds at the different temperatures didn’t differ significantly (P > 0.05) between fresh seeds and seeds stored at freezer. However, the final germination of both room and warm stored seeds of H. salicornicum was significantly
Germination rate index
Final germination (%)
50 80
40 30 20 Cold Field Room Warm
10 0
3 9 12 17 Storage period (months)
(b) Salsola imbricata Fig. 2. Effect of storage period and storage conditions on germination rate index of Haloxylon salicornicum and Salsola imbricata seeds.
reduced at 15, 20 and 25 °C, and was almost inhibited at 35 °C (Fig. 3a). In S. imbricata, final germination at 15 °C was less affected by storage in room and warm conditions and significantly increased
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Table 2 Two-way ANOVA showing the effect of storage condition and temperature of incubation on final germination percentage and germination rate index of Haloxylon salicornicum and Salsola imbricata seeds. Ns: insignificant at F equal or less than 0.05. Source of variation
df
Mean-square
F-ratio
P
Final germination percentage A: Haloxylon salicornicum Storage condition (S) Incubation temperature (T) S⁄T Error
3 3 9 44
1.404 0.763 0.040 0.008
184.3 100.2 5.29
<0.001 <0.001 <0.001
B: Salsola imbricata Storage condition (S) Incubation temperature (T) S⁄T Error
3 3 9 44
0.078 0.482 0.024 0.007
11.4 71.1 3.6
<0.001 <0.001 <0.01
Germination rate index A: Haloxylon salicornicum Storage condition (S) Incubation temperature (T) S⁄T Error
3 3 9 44
2.058 5.787 1.873 0.543
3.8 10.6 3.45
<0.05 <0.001 <0.01
B: Salsola imbricata Storage condition (S) Incubation temperature (T) S⁄T Error
3 3 9 44
0.213 0.420 0.313 0.225
0.957 1.87 1.39
Ns Ns Ns
Final germination (%)
100 80 60 40 15 20 25 35
20 0
Fresh
Cold Warm Room Storage condition
(a) Haloxylon salicornicum
Final germination (%)
100
3.2.2. Effect on germination speed The effects of storage condition and temperature of incubation and their interaction on germination speed was significant (P < 0.05) in H. salicornicum, but not for S. imbricata seeds (P > 0.05). In H. salicornicum, storage in freezer, but not in room and warm conditions, significantly increased germination rate index, compared to fresh seeds. There were no significant differences between the germination speeds at the different temperature for fresh seeds, but germination speed was significantly reduced at 35 °C, compared to other temperatures, for stored seeds (see Fig. 4). Cold storage significantly increased germination speed at 15, 20 and 25 °C, but not at 35 °C. In addition, warm storage and storage at room temperatures did not affect germination speed at 15, 20 and 25 °C, but significantly reduced it at 35 °C. The ecological advantage of this is to ensure that seeds of H. salicornicum stored on soil surface or under the shade of vegetation will not germinate easily under high temperatures of summer, even if rainfall is enough for seedling emergence.
80 4. Discussion
60 40 15 20 25 35
20 0
Fresh
Cold Warm Room Storage condition
(b) Salsola imbricata Fig. 3. Effect of storage condition and incubation temperature on final germination percentage of Haloxylon salicornicum and Salsola imbricata seeds.
by storage in freezer, compared to that of fresh seeds. At 35 °C, there was no significant difference between final germination of fresh seeds and that of seeds stored in the different conditions (Fig. 3b).
Seed dormancy has been hypothesized to be evolved as an adaptation for survival during a season when environmental conditions are unfavourable for seedling establishment ([2,3]. Dormancy can influence patterns of plant distribution, recruitment dynamics, and persistence in the plant community [21]. Consequently, dormancy is very crucial in formation of soil seed banks, which play important roles in maintaining plant populations and also in restoring vegetation after destruction [22]. The results of the present study, however, indicated that both S. imbricata and H. articulata have transient seed bank; seeds germinate immediately after ripening and lost their viability after 9 months under natural field conditions. This result is consistent with those of the earlier studies about S. imbricata [12,13] and H. salicornicum [14,15]. In some species, maintenance of seed dormancy when conditions are optimal for germination can be disadvantage, as seeds are exposed to lethal environmental factors such as granivory and extreme temperatures for longer periods [18]. In addition,
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Germination rate index
50 40 30 20 15 20 25 35
10 0
Fresh
Cold Warm Room Storage condition
(a) Haloxylon salicornicum
Germination rate index
50 40 30 20 15 20 25 35
10 0
Fresh
Cold Warm Room Storage condition
(b) Salsola imbricata Fig. 4. Effect of storage period and storage conditions on germination rate index of Haloxylon salicornicum and Salsola imbricata seeds.
species with non-dormant seeds might be expected to benefit from earlier germination more than those with dormant seeds, because such a response might reduce mortality, due to factors such as seed predation, sibling competition or shade intolerance [23]. Furthermore, storage of the seeds reduce germination speed, which usually reduce the competitive ability of the seedlings, as they emerge later in the season, compared to other species [24–26]. Seed dormancy respond to diurnal fluctuations in temperature [27], but the response differs according to the level and kind of dormancy [2]. Several researchers have reported that high temperatures and wide daily temperature fluctuations break seed dormancy in many species [2]. For example, seeds with physical seed-coat dormancy require temperature fluctuations, such as that on soil surface, to break their dormancy [28]. Seeds with low dormancy, however, would lose their viability faster when stored on soil surface, compared with seeds with physical dormancy [18]. For example, seeds of Acacia berlandieri with no dormancy deteriorated faster on soil surface compared to seeds of Leucaena pulverulenta, which have physical seed coat dormancy [18]. In the two species of the present study, which have little seed dormancy, nine months of storage under field conditions resulted in complete inhibition for the seed germination. Seeds in soils undergo hydration–dehydration cycles in concert with fluctuations in the humidity of their surroundings [29]. In the coastal and inland areas of the UAE deserts, dew and morning dense fogs are frequent events that result in moistening the fruits of both S. imbricata and H. salicornicum; especially the winged structures of their fruits keep them exposed on the soil surface. During dew formation, soil surfaces can become saturated, and seeds with permeable seed coats imbibe water [19].The effect of hydration–dehydration cycles on seed germination speed and level
are important in natural plant populations. These cycles had resulted in an earlier germination of desert cacti [30], but led to loss of seed viability in Acacia tortolis and A. nilotica [31]. The hydration–dehydration cycles would be responsible for the complete deterioration of the field-stored seeds of the studied species. Such deterioration was attributed to the accumulation of reactive oxygen species, which lead to oxidative stress and cellular damage [32]. In addition, both membrane permeability, measured by ion conductivity, and the seed respiratory activity were significantly increased following the hydration-dehydration cycles [33]. Maintenance of seed viability requires relatively both low moisture content by drying and a lower temperature environment [34,35]. In the present study, storage for 12 and 17 months maintained the high germination percentage for seeds stored in fridge in both S. imbricata and H. salicornicum. This result agrees with that of Zaman et al. [13], which indicated that seeds of S. imbricata stored at 18 °C and 4 °C for 24 months had 80–100% germination, compared with 0% for those stored at ambient temperature and at 50 °C. The result is also coincide with that of Clor et al. [7], which showed that seeds of H. salicornicum from Iraqi deserts maintained their viability for one year when stored at 5 °C, but lost it at room temperatures. However, seeds of eight out of nine annual plant species from the Mojave and Sonoran Deserts of North America germinated to high percentages after dry storage for 1–5 weeks at 50 °C, but they gave poor germination when stored at 4 °C [4]. Similarly, less than 18 months storage at cool temperatures increased seed moisture content, reduced viability and did not promote germination in three Australian everlasting daisy species, but storage at high temperatures decreased seed moisture content, maintained viability and improved germination [36]. The difference in the response to cold storage between S. imbricata and H. salicornicum and the other mentioned species could be attributed to the degree of seed development and consequently the need for after-ripening. Seeds of S. imbricata and H. salicornicum are fully developed and germinated to high level immediately following dispersal, but seeds of the other species require high temperatures following seed dispersal to promote seed maturation [4]. In another shrubby chenopod, Haloxylon ammodendron, with fully developed seeds and only 10-months longevity, seeds survived for longer period during storage at low temperatures, but lost their viability sharply in natural conditions [37]. It has been reported that fresh seeds usually germinate under specific narrow range of conditions, but such conditions gradually become wider as a result of seed storage [17,38,39]. In the annual desert herb Plantago coronopus of the Negev Desert, Gutterman et al. [17] reported greater and faster germination at a wide range of temperatures after seeds stored at naturally fluctuating daily temperatures of 13/55 °C or at constant 40 °C. Similarly, dry storage at high temperatures reduced seed dormancy and widen the germination temperature requirements in Bromus tectorum [40] and light and GA3 requirements in Arabidopsis thaliana [41]. In addition, Probert et al. [42] indicated that the proportion of Dactylis glomerata seeds that require light and/or alternating temperatures to trigger germination declines during dry storage. After prolonged storage, non-dormant seeds of D. glomerata are capable of maximum germination, even in the dark, at constant temperatures [42]. In the present study, however, fridge storage had little effect on the temperature requirement during seed germination of both H. salicornicum and S. imbricata. In addition, room temperature and warm storages significantly reduced final germination and germination speed at the different temperatures; the reduction was more pronounced at 35 °C. The ecological advantage of narrowing the germination window at 35 °C is to ensure that seeds stored on soil surface or under the shade of vegetation will not germinate easily under high temperatures of summer, even if rainfall is enough for seedling emergence.
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Repeated environmental stresses facing desert plants coupled with great human disturbances in the Arabian Gulf deserts increase the chance of the shrubs mortality [43]. In addition, the inability of the two shrubs S. imbricata and H. salicornicum to produce persistent seed bank would threaten their life under repeated drought stress and human disturbances in the deserts. In order to ensure annual seedling recruitment, high annual fruit production should compensate the high mortality rate of the seeds and plants of both S. imbricata and H. salicornicum. Both species produce enormous amount of highly dispersed fruits every year, even in the dry seasons. These plants mainly rely on atmospheric moisture and fog as main sources of water for their growth [10,11]. The high annual fruit production, even in the dry years, would compensate for the depletion of the transient seed bank, and consequently could ensure the regeneration of the two species in the harsh deserts. In addition, the greater dispersal ability of the fruits would enhance their ability in exploring the unpredictable deserts for more safe sites for germination and establishment [3]. References [1] R.J. Probert, The role of temperature in the regulation of seed dormancy and germination, in: M. Fenner (Ed.), Seeds: The Ecology of Regeneration in Plant Communities, CAB International, Wallingford, 2000, pp. 261–292. [2] C.C. Baskin, J.M. Baskin, Seeds: Ecology, Biogeography and Evolution of Dormancy and Germination, Academic Press, New York, 1998. [3] A. El-Keblawy, Progeny and seed dormancy traits in relation to achene heteromorphism in the two ephemerals Hedypnois cretica (L.) Dum.-Cours. and Crepis aspera L. (Asteracea), Canadian Journal and Botany 81 (2003) 550–559. [4] B. Capon, W. Van Asdall, Heat pre-treatment as a means of increasing germination of desert annual seeds, Ecology 48 (1967) 305–306. [5] Y. Gutterman, Strategies of seed dispersal and germination in plants inhabiting deserts, Botanical Review 60 (1994) 373–425. [6] W. Schutz, Germination responses of temperate Carex-species to diurnally fluctuating temperatures – a comparative study, Flora 194 (1999) 21–32. [7] M.A. Clor, T.A. Al-Ani, F. Charchafchy, Germinability and seedling vigor of Haloxylon salicornicum as affected by storage and seed size, Journal of Rangeland Management 29 (1976) 60–62. [8] A.K. Hegazy, Plant succession and its optimization on tar-polluted coasts in the Arabian Gulf region, Environmental Conservation 24 (1997) 149–158. [9] S.S. Radwan, H. Al-Awadhi, N.A. Sorkhoh, I.M. El-Nemr, Rhizospheric hydrocarbon-utilizing microorganisms as potential contributors to phytoremediation for the oily Kuwaiti desert, Microbiological Research 153 (1998) 247–252. [10] A. El-Keblawy, F. Al-Ansari, N. Hassan, N. Al-Shamsi, Salinity, temperature and light affect germination of Salsola imbricata, Seed Science and Technology 35 (2007) 272–281. [11] A. El-Keblawy, N.AL. Shamsi, Effects of salinity, temperature and light on seed germination of Haloxylon salicornicum, a common perennial shrub of the Arabian deserts, Seed Science and Technology 36 (2008) 679–688. [12] M.A. Khan, Relationship of seed bank to plant distribution in saline arid communities, Pakistan Journal of Botany 25 (1993) 73–82. [13] S. Zaman, S. Padmesh, H. Tawfiq, Seed germination and viability of Salsola imbricata Forssk, International Journal of Biodiversity and Conservation 2 (2010) 388–394. [14] G. Brown, S. Al-Mazrooei, Germination ecology of Haloxylon salicornicum from Kuwait, Botanische Jahrbücher für Systematik 193 (2001) 133–140. [15] G. Brown, S. Porembski, Miniature dunes and blow-outs as ‘‘safe-sites’’ for plants in an oil-contaminated area of Northern Kuwait, Environmental Conservation 27 (2000) 242–249. [16] A. El-Keblawy, A. Al-Rawai, Effects of seed maturation time and dry storage on light and temperature requirements during germination in invasive Prosopis juliflora, Flora 201 (2006) 135–143. [17] Y. Gutterman, S. Shem-Tov, S. Gozlan, The effect of post-maturation temperature and duration on seed germinability of Plantago coronopus occurring in natural populations in the Negev Desert highlands, Israel, Journal of Arid Environments 38 (1998) 451–463.
343
[18] M.K. Owens, R.B. Wallace, S. Archer, Seed dormancy and persistence of Acacia berlandieri and Leucaena pulverulenta in a semi-arid environment, Journal of Arid Environments 29 (1995) 15–23. [19] Z.Y. Huang, I. Boubriak, D.J. Osborne, Possible role of pectin-containing mucilage and dew in repairing embryo DNA of seeds adapted to desert conditions, Annals of Botany 101 (2008) 277–283. [20] M.A. Khan, I.A. Ungar, The effect of salinity and temperature on the germination of polymorphic seeds and growth of Atriplex triangularis Willd, American Journal of Botany 71 (1984) 481–489. [21] J.L. Harper, Population Biology of Plants, Academic Press, New York, 1977. [22] J.W. Silvertown, J. Lovett-Doust, Introduction to Plant Population Biology, Blackwell Scientific Publications, Oxford, 1993. [23] A. Traveset, M. Verdú, A meta-analysis of gut treatment on seed germination, in: D.J. Levey, M. Galetti, W.R. Silva (Eds.), Frugivores and Seed Dispersal: Ecological, Evolutionary and Conservation Issues, CAB International, Wallingford, 2002, pp. 339–350. [24] M. Rees, Evolutionary ecology of seed dormancy and seed size, Philosophical Transactions of the Royal Society of London – Series B 351 (1996) 1299–1308. [25] M.E. Rogers, C.L. Noble, G.E. Hallorn, M.E. Nicolas, The effect of NaCl on germination and early seedling growth of white clover (Trifoliummm repens L.) population selected from high and low salinity tolerance, Seed Science and Technology 23 (1995) 277–287. [26] S. Zia, M.A. Khan, Effect of light, salinity, and temperature on seed germination of Limonium stocksii, Canadian Journal of Botany 82 (2004) 151–157. [27] T.L. Pons, H.F.J.M. Schröder, Significance of temperature fluctuation and oxygen concentration for germination of the rice field weeds Fibristylis littoralis and Scirpus juncoides, Oecologia 68 (1986) 315–319. [28] J.M. Baskin, C.C. Baskin, Physiology of dormancy and germination in relation to seed bank ecology, in: M.A. Leck, V.T. Parker, R.L. Simpson (Eds.), Ecology of Soil Seed Banks, Academic Press, New York, 1989, pp. 53–66. [29] S.B. Wuest, Vapour is the principal source of water imbibed by seeds in unsaturated soils, Seed Science Research 17 (2007) 3–9. [30] J.G. Dubrovsky, Seed Hydration Memory in Sonoran Desert Cacti and its Ecological Implication, American Journal of Botany 83 (1996) 624–632. [31] T.B. Wilson, T.F. Witkowsk, Water requirements for germination and early seedling establishment in four African savanna woody plant species, Journal of Arid Environments 38 (1998) 541–550. [32] C. Bailly, Active oxygen species and antioxidants in seed biology, Seed Science Research 14 (2004) 93–107. [33] B. Bai, N. Sikron, T. Gendler, Y. Kazachkova, S. Barak, G. Grafi, I. KhozinGoldberg, A. Fait, Ecotypic variability in the metabolic response of seeds to diurnal hydration–dehydration cycles and its relationship to seed vigor, Plant and Cell Physiology 53 (2011) 38–52. [34] G.H. Zheng, Seed physiology research at the Beijing Botanical Garden, Seed Science and Technology 12 (1984) 723–729. [35] G.H. Zheng, Physiological, biochemical and ultrastructural aspects of imbibitional chilling injury in seeds, Seed Science Research 1 (1991) 127–134. [36] Z. Peishi, J.A. Plummer, D.W. Turner, D. Choengsaat, D.T. Bell, Low- and hightemperature storage effects on viability and germinability of seeds of three Australian Asteraceae, Australian Journal of Botany 47 (1999) 265–275. [37] Z. Huang, X. Zhang, G. Zheng, Y. Gutterman, Influence of light, temperature, salinity and storage on seed germination of Haloxylon ammodendron, Journal of Arid Environments 55 (2003) 453–464. [38] A. Orozco-Segovia, A.E. Brechu-Franco, L. Zambrano-Polaco, R. OsunaFernández, G. Laguna-Hernández, M.E. Sánchez-Coronado, Effects of maternal light environment on germination and morphological characteristics of Sicyos deppei seeds, Weed Research 40 (2000) 495506. [39] M.M. Qaderi, P.B. Cavers, M.A. Bernards, Pre- and post-dispersal factors regulate germination patterns and structural characteristics of Scotch thistle (Onopordum acanthium) cypselas, New Phytologist 159 (2003) 263–278. [40] S.E. Meyer, P.S. Allen, Ecological genetics of seed germination regulation in Bromus tectorum L. II. Reaction norms in response to a water stress gradient imposed during seed maturation, Oecologia 120 (1999) 35–43. [41] M.P.M. Derkx, C.M. Karssen, Variability in light-, gibberellin- and nitrate requirement of Arabidopsis thaliana seeds due to harvest time and conditions of dry storage, Journal of Plant Physiology 141 (1993) 574–582. [42] R.J. Probert, R.D. Smith, P. Birch, Germination responses to light and alternating temperatures in European populations of Dactylis glomerata L. IV. The effects of storage, New Phytologist 101 (1985) 521–529. [43] K.H. Batanouny, Biodiversity strategy and rangelands in the Arab world, in: R. Hamzah, S.A. Alaa El-Din, M.N. Mohammed (Eds.), National Biodiversity Planning in the Arab World, Arabian Gulf University Publication, Bahrain, 2002, pp. 121–142.
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Effects of seed storage on germination of two succulent desert halophytes with little dormancy and transient seed bank Ali El-Keblawy ⇑ Dept. of Applied Biology, Faculty of Science and Sharjah Research Academy, University of Sharjah, Sharjah, United Arab Emirates
a r t i c l e
i n f o
Article history: Received 9 March 2012 Revised 13 April 2013 Accepted 18 September 2013
Keywords: Dormancy Germination Desert halophytes Seed storage Transient seed bank
a b s t r a c t Seeds of both Salsola imbricata and Haloxylon salicornicum have high germination level and germination speed, and form a transient seed bank in nature. The impacts of storage period and condition on germination level and speed were assessed in the two species. Storage for three months significantly increased both germination level and speed of seeds stored under the different conditions, compared to that of fresh seeds. In both species, nine months storage did not affect germination percentage in cold storage seeds, but completely inhibited it in field seeds. Storage for longer time in room and warm temperatures resulted in significant reduction or complete inhibition in the germination of the two species, so this was more pronounced in H. salicornicum. Storage significantly increased germinate rate index of seeds stored in all conditions till 17 months in S. imbricata and till 12 months in H. salicornicum. In both species, fridge storage had little effects on final germination and germination speed of seeds incubated at the different temperatures, compared to fresh seeds. However, room temperature and warm storages significantly reduced final germination and germination speed at the different temperatures, so the reduction was more pronounced at 35 °C, especially in H. salicornicum. Ó 2013 Ecological Society of China. Published by Elsevier B.V. All rights reserved.
1. Introduction It has been documented that natural selection favors environmental cueing mechanisms that decrease the probability of encountering unacceptable growth conditions following germination [1]. Generally, germination-timing mechanisms have evolved in response to selection pressures on both seed and seedlings [2,3]. In areas with winter rains and hot dry summer, seeds ripe and shed at the beginning of summer. In temperate areas, with cold winters and summer rains, seed ripening and shedding is frequent in autumn. In both cases, time of seed shedding does not coincide with conditions suitable for germination and seedling establishment. Consequently, seeds of many plants in both geographical regions develop innate dormancy and require a period of after-ripening to break their dormancy. Dry storage at high temperatures during summer months has been used to break dormancy in several winter species of arid and semi-arid deserts that shed their seeds at spring [3–5]. However, cold stratification (chilling) is required to break dormancy in many summer species of temperate climatic regions that their seeds spend the unfavourable cold winter in dormant state [2,6].
⇑ Permanent address: Dept. of Biology, Faculty of Education in Al-Arish, Suez Canal University, Egypt. E-mail address: [email protected]
Haloxylon salicornicum and Salsola imbricata (Chenopodiaceae) are perennial shrubs widely distributed in sandy habitats of the Arabian deserts. Both species are succulent halophytes and welladapted to endure severe environmental stresses and human disturbances in the deserts. H. salicornicum has been considered one of the most promising species for re-seeding deteriorating desert range vegetation and for sand dune fixation [7]. In addition, S. imbricata has the ability to stabilize sand dunes and to restore degraded, oil-polluted soils [8,9]. Both H. salicornicum and S. imbricata ripen and shed their seeds early in the growing season (early winter). This coincides with the onset of suitable conditions for germination and seedling establishment (e.g., availability of rainfall and lower temperatures) are optimum for germination and seedling establishment). Shortly after effective rainfalls, many seedlings appear under and around the maternal plants (Ali El-Keblawy, unpublished data). Under laboratory conditions, fresh harvested seeds of both species germinate to a very high level with high speed [10,11]. Seed bank studies indicated that a transient nature of the seed bank both in S. imbricata [12,13] and H. salicornicum [14,15]. Dry storage usually results in the decrease in germination requirements in seeds of many species of arid and semiarid lands. Generally, germination requirements usually become less specific after seed dry storage [1]. For example, the need for high temperature and light to achieve greater germination in fresh seeds of Prosopis juliflora was significantly reduced after seed stored dry
1872-2032/$ - see front matter Ó 2013 Ecological Society of China. Published by Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.chnaes.2013.09.008
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at room temperatures for 8 months [16]. Similarly, seeds of the desert herb Plantago coronopus stored for two months germinated under narrow range of temperatures, but germinated under wider range of temperatures when stored in their inflorescences under natural desert habitats for one year [17]. These species developed innate dormancy and form persistent seed bank. However, few studies have assessed the impact of different storage conditions on temperature requirement for desert shrubs with a transient seed bank (but see [7,18,38]. The aim of this study was to assess the impact of different storage periods and conditions (e.g., cold, warm, room temperatures and natural field conditions) on germination level and speed of the two desert shrubs Haloxylon salicornicum and Salsola imbricata, which have a transient seed bank. In addition, the study also aimed at assessing the impact of the different storage conditions for a period of one year on the temperature requirement during germination in the two species. 2. Materials and methods Fresh seeds of H. salicornicum and S. imbricata were collected during December from large populations in the inland desert of the United Arab Emirates (UAE), near Al-Ain. Seeds were randomly collected from about 50 plants of each species that represent the genetic diversity of the populations. Seeds of each species were divided into five groups. Seeds of one group were germinated immediately after collection (within 5 days, hereafter referred as fresh seeds). Seeds of the other four groups were put into 4 cm 6 cm mesh bags. The bags were stored in air conditioned room temperatures (20–23 °C), at freezer ( 4 °C, hereafter referred as cold storage), in oven adjusted at 40 °C ± 2 °C (hereafter referred as warm storage) and on soil surface of a natural habitat, where the two species are naturally grown. The moisture content of the seed during room temperatures, cold and warm storage ranged between 14% and 15%. However, moisture content of seeds stored in natural habitats varied greatly between 20% during day times to 40% during night and morning times (Ali El-Keblawy, unpublished data). When the local weather forecast expected a rain, seeds of the natural habitats were removed and returned back shortly after improvement of the weather. The site of natural seed storage received only one effective rain during the study period. Seeds of the two species were tested for germination after 3, 9, 12 and 17 months of storage. Seeds were germinated in incubators adjusted to 15 °C for H. salicornicum and 20 °C for S. imbricata under continuous illumination with daylight fluorescent tubes (110 lmol photons/m2/s, 400–700 nm). The highest germination in light was recorded at 15 °C in H. salicornicum [11] and at 20 °C in S. imbricata [10]. In order to assess the impact of different storage conditions on temperature requirements, seeds stored for one year in room temperature, freezer and oven were tested for germination in four incubators adjusted at 15, 20, 25 and 30 °C under continuous illumination with daylight fluorescent tubes. The germination was conducted in 9-cm Petri-dishes containing one disk of Whatman No. 1 filter paper, with 10 ml of distilled water. Four replicate dishes, each with 20 seeds, were used for each treatment. Seeds were considered to be germinated with the emergence of the radicles. Germinated seedlings were counted and removed every alternative day for 14 days following sowing. The rate of germination was estimated using a modified Timson’s index of germination velocity = RG/t, where G is the percentage of seed germination at 2 d intervals and t is the total germination period [20]. The maximum value possible using this index with these experiments was 700/14 = 50. The higher the value, the more rapid is the germination. Two way-ANOVAs were used to assess the impact of storage condition and seed storage period or temperature of incubation
339
on final germination percentage and germination speed. Tukey test (Honestly significant differences, HSD) was used to estimate least significant range between means. The germination percentages were arcsine transformed to meet the assumptions of ANOVA. The transformation improved normality of distribution of data. All statistical methods were performed using SYSTAT, version 11.0. 3. Results 3.1. Effect of storage period and storage condition 3.1.1. Effect on final germination Both storage period and storage conditions and their interactions significantly affected final germination percentage of the two species (P < 0.001, Table 1). Generally, storage in freezer didn’t affect the level of final germination, compared to the other storage conditions, especially seeds stored under natural field conditions. The germination of fresh seeds was 76% and 68.3% in H. salicornicum and S. imbricata, respectively. Storage for three months significantly increased germination of seeds stored under different conditions, compared to germination of fresh seeds. The range of the germination increase was between 10.5% for seeds stored under warm conditions and 22.8% for seeds stored in field conditions in H. salicornicum and between 18.9% for seeds stored in freezer and 37.4% for seeds stored under warm conditions in S. imbricata. In H. salicornicum, storage for nine and 12 months completely inhibited germination of seeds stored in the field and significantly reduced germination of seeds stored in warm and room temperature conditions, but not affected germination of seeds stored in freezer, compared to fresh seeds. Further storage for 17 months led for almost complete inhibition in germination of seeds stored in warm and room temperature conditions and to a significant reduction for the germination of seeds stored in the freezer (Fig. 1a). For S. imbricata, nine months storage inhibited germination of field seeds, but not affect it for seeds stored under the other conditions. Storage for 12 and 17 months significantly reduced final germination of cold, room and warm storage seeds, but did not completely deteriorate it. The deteriorations in final germination, compared to fresh seeds, under warm, room temperature and cold conditions were 32.6%, 21.1% and 17.2%, respectively, after 12 months and 60%, 55.4% and 27.7%, respectively, after 17 months (Fig. 1b). 3.1.2. Effect on germination speed Similar to the impact on final germination, both storage period and storage conditions and their interactions significantly affected final germination speed of the two species (P < 0.001, Table 1). There was no significant difference in germination rate index between fresh seeds and those stored for three months under different conditions. Storage significantly increased germinate rate index of seeds stored for nine months in all storage conditions, except field seeds, which did not germinate. After 12 and 17 months, the increase in germination speed, compare to fresh seeds, was significant for S. imbricata stored at the different conditions, but was significant only for seeds of H. salicornicum stored in freezer (Fig. 2). After 17 months, the germination rate index of H. salicornicum seeds stored in room temperatures and warm conditions was significantly low, compared to that of fresh seeds (Fig. 2a). 3.2. Effects of storage condition and temperature of incubation 3.2.1. Effect on final germination The effects of storage condition and temperature of incubation and their interaction on final germination were significant in both
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Table 1 Two-way ANOVA showing the effect of storage period and storage condition on final germination percentage and germination rate index of Haloxylon salicornicum and Salsola imbricata seeds. Source of variation
df
Final germination percentage A: Haloxylon salicornicum Storage period (SP) Storage condition (SC) SP⁄SC Error
Mean-square
3 3 9 40
2.363 0.633 0.165 0.021
112.4 30.1 7.8
<0.001 <0.001 <0.001
B: Salsola imbricata Storage period (SP) Storage condition (SC) SP⁄SC Error
3 3 9 40
1.162 0.445 0.088 0.015
75.2 28.8 5.7
<0.001 <0.001 <0.001
Germination rate index A: Haloxylon salicornicum Storage period (SP) Storage condition (SC) SP⁄SC Error
3 3 9 40
12.806 18.546 4.985 0.265
48.3 69.9 18.8
<0.001 <0.001 <0.001
B: Salsola imbricata Storage period (SP) Storage condition (SC) SP⁄SC Error
3 3 9 40
2.332 23.394 2.840 0.001
3218.6 32281.8 3919.1
<0.001 <0.001 <0.01
80 60 40 Cold Field Room Warm
20 0
P
50 Germination rate index
Final germination (%)
100
F-ratio
3 9 12 17 Storage period (months)
40 30 20 Cold Field Room Warm
10 0
(a) Haloxylon salicornicum
3 9 12 17 Storage period (months)
(a) Haloxylon salicornicum 100
60 40 Cold Field Room Warm
20 0
3 9 12 17 Storage period (months)
(b) Salsola imbricata Fig. 1. Effect of storage period and storage conditions on final germination percentage of Haloxylon salicornicum and Salsola imbricata seeds.
H. salicornicum and S. imbricata (P < 0.01, Table 2). Germination of the fresh and stored seeds was significantly greater at 15, 20 and 25 °C, compared to 35 °C. Final germination of H. salicornicum seeds at the different temperatures didn’t differ significantly (P > 0.05) between fresh seeds and seeds stored at freezer. However, the final germination of both room and warm stored seeds of H. salicornicum was significantly
Germination rate index
Final germination (%)
50 80
40 30 20 Cold Field Room Warm
10 0
3 9 12 17 Storage period (months)
(b) Salsola imbricata Fig. 2. Effect of storage period and storage conditions on germination rate index of Haloxylon salicornicum and Salsola imbricata seeds.
reduced at 15, 20 and 25 °C, and was almost inhibited at 35 °C (Fig. 3a). In S. imbricata, final germination at 15 °C was less affected by storage in room and warm conditions and significantly increased
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Table 2 Two-way ANOVA showing the effect of storage condition and temperature of incubation on final germination percentage and germination rate index of Haloxylon salicornicum and Salsola imbricata seeds. Ns: insignificant at F equal or less than 0.05. Source of variation
df
Mean-square
F-ratio
P
Final germination percentage A: Haloxylon salicornicum Storage condition (S) Incubation temperature (T) S⁄T Error
3 3 9 44
1.404 0.763 0.040 0.008
184.3 100.2 5.29
<0.001 <0.001 <0.001
B: Salsola imbricata Storage condition (S) Incubation temperature (T) S⁄T Error
3 3 9 44
0.078 0.482 0.024 0.007
11.4 71.1 3.6
<0.001 <0.001 <0.01
Germination rate index A: Haloxylon salicornicum Storage condition (S) Incubation temperature (T) S⁄T Error
3 3 9 44
2.058 5.787 1.873 0.543
3.8 10.6 3.45
<0.05 <0.001 <0.01
B: Salsola imbricata Storage condition (S) Incubation temperature (T) S⁄T Error
3 3 9 44
0.213 0.420 0.313 0.225
0.957 1.87 1.39
Ns Ns Ns
Final germination (%)
100 80 60 40 15 20 25 35
20 0
Fresh
Cold Warm Room Storage condition
(a) Haloxylon salicornicum
Final germination (%)
100
3.2.2. Effect on germination speed The effects of storage condition and temperature of incubation and their interaction on germination speed was significant (P < 0.05) in H. salicornicum, but not for S. imbricata seeds (P > 0.05). In H. salicornicum, storage in freezer, but not in room and warm conditions, significantly increased germination rate index, compared to fresh seeds. There were no significant differences between the germination speeds at the different temperature for fresh seeds, but germination speed was significantly reduced at 35 °C, compared to other temperatures, for stored seeds (see Fig. 4). Cold storage significantly increased germination speed at 15, 20 and 25 °C, but not at 35 °C. In addition, warm storage and storage at room temperatures did not affect germination speed at 15, 20 and 25 °C, but significantly reduced it at 35 °C. The ecological advantage of this is to ensure that seeds of H. salicornicum stored on soil surface or under the shade of vegetation will not germinate easily under high temperatures of summer, even if rainfall is enough for seedling emergence.
80 4. Discussion
60 40 15 20 25 35
20 0
Fresh
Cold Warm Room Storage condition
(b) Salsola imbricata Fig. 3. Effect of storage condition and incubation temperature on final germination percentage of Haloxylon salicornicum and Salsola imbricata seeds.
by storage in freezer, compared to that of fresh seeds. At 35 °C, there was no significant difference between final germination of fresh seeds and that of seeds stored in the different conditions (Fig. 3b).
Seed dormancy has been hypothesized to be evolved as an adaptation for survival during a season when environmental conditions are unfavourable for seedling establishment ([2,3]. Dormancy can influence patterns of plant distribution, recruitment dynamics, and persistence in the plant community [21]. Consequently, dormancy is very crucial in formation of soil seed banks, which play important roles in maintaining plant populations and also in restoring vegetation after destruction [22]. The results of the present study, however, indicated that both S. imbricata and H. articulata have transient seed bank; seeds germinate immediately after ripening and lost their viability after 9 months under natural field conditions. This result is consistent with those of the earlier studies about S. imbricata [12,13] and H. salicornicum [14,15]. In some species, maintenance of seed dormancy when conditions are optimal for germination can be disadvantage, as seeds are exposed to lethal environmental factors such as granivory and extreme temperatures for longer periods [18]. In addition,
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Germination rate index
50 40 30 20 15 20 25 35
10 0
Fresh
Cold Warm Room Storage condition
(a) Haloxylon salicornicum
Germination rate index
50 40 30 20 15 20 25 35
10 0
Fresh
Cold Warm Room Storage condition
(b) Salsola imbricata Fig. 4. Effect of storage period and storage conditions on germination rate index of Haloxylon salicornicum and Salsola imbricata seeds.
species with non-dormant seeds might be expected to benefit from earlier germination more than those with dormant seeds, because such a response might reduce mortality, due to factors such as seed predation, sibling competition or shade intolerance [23]. Furthermore, storage of the seeds reduce germination speed, which usually reduce the competitive ability of the seedlings, as they emerge later in the season, compared to other species [24–26]. Seed dormancy respond to diurnal fluctuations in temperature [27], but the response differs according to the level and kind of dormancy [2]. Several researchers have reported that high temperatures and wide daily temperature fluctuations break seed dormancy in many species [2]. For example, seeds with physical seed-coat dormancy require temperature fluctuations, such as that on soil surface, to break their dormancy [28]. Seeds with low dormancy, however, would lose their viability faster when stored on soil surface, compared with seeds with physical dormancy [18]. For example, seeds of Acacia berlandieri with no dormancy deteriorated faster on soil surface compared to seeds of Leucaena pulverulenta, which have physical seed coat dormancy [18]. In the two species of the present study, which have little seed dormancy, nine months of storage under field conditions resulted in complete inhibition for the seed germination. Seeds in soils undergo hydration–dehydration cycles in concert with fluctuations in the humidity of their surroundings [29]. In the coastal and inland areas of the UAE deserts, dew and morning dense fogs are frequent events that result in moistening the fruits of both S. imbricata and H. salicornicum; especially the winged structures of their fruits keep them exposed on the soil surface. During dew formation, soil surfaces can become saturated, and seeds with permeable seed coats imbibe water [19].The effect of hydration–dehydration cycles on seed germination speed and level
are important in natural plant populations. These cycles had resulted in an earlier germination of desert cacti [30], but led to loss of seed viability in Acacia tortolis and A. nilotica [31]. The hydration–dehydration cycles would be responsible for the complete deterioration of the field-stored seeds of the studied species. Such deterioration was attributed to the accumulation of reactive oxygen species, which lead to oxidative stress and cellular damage [32]. In addition, both membrane permeability, measured by ion conductivity, and the seed respiratory activity were significantly increased following the hydration-dehydration cycles [33]. Maintenance of seed viability requires relatively both low moisture content by drying and a lower temperature environment [34,35]. In the present study, storage for 12 and 17 months maintained the high germination percentage for seeds stored in fridge in both S. imbricata and H. salicornicum. This result agrees with that of Zaman et al. [13], which indicated that seeds of S. imbricata stored at 18 °C and 4 °C for 24 months had 80–100% germination, compared with 0% for those stored at ambient temperature and at 50 °C. The result is also coincide with that of Clor et al. [7], which showed that seeds of H. salicornicum from Iraqi deserts maintained their viability for one year when stored at 5 °C, but lost it at room temperatures. However, seeds of eight out of nine annual plant species from the Mojave and Sonoran Deserts of North America germinated to high percentages after dry storage for 1–5 weeks at 50 °C, but they gave poor germination when stored at 4 °C [4]. Similarly, less than 18 months storage at cool temperatures increased seed moisture content, reduced viability and did not promote germination in three Australian everlasting daisy species, but storage at high temperatures decreased seed moisture content, maintained viability and improved germination [36]. The difference in the response to cold storage between S. imbricata and H. salicornicum and the other mentioned species could be attributed to the degree of seed development and consequently the need for after-ripening. Seeds of S. imbricata and H. salicornicum are fully developed and germinated to high level immediately following dispersal, but seeds of the other species require high temperatures following seed dispersal to promote seed maturation [4]. In another shrubby chenopod, Haloxylon ammodendron, with fully developed seeds and only 10-months longevity, seeds survived for longer period during storage at low temperatures, but lost their viability sharply in natural conditions [37]. It has been reported that fresh seeds usually germinate under specific narrow range of conditions, but such conditions gradually become wider as a result of seed storage [17,38,39]. In the annual desert herb Plantago coronopus of the Negev Desert, Gutterman et al. [17] reported greater and faster germination at a wide range of temperatures after seeds stored at naturally fluctuating daily temperatures of 13/55 °C or at constant 40 °C. Similarly, dry storage at high temperatures reduced seed dormancy and widen the germination temperature requirements in Bromus tectorum [40] and light and GA3 requirements in Arabidopsis thaliana [41]. In addition, Probert et al. [42] indicated that the proportion of Dactylis glomerata seeds that require light and/or alternating temperatures to trigger germination declines during dry storage. After prolonged storage, non-dormant seeds of D. glomerata are capable of maximum germination, even in the dark, at constant temperatures [42]. In the present study, however, fridge storage had little effect on the temperature requirement during seed germination of both H. salicornicum and S. imbricata. In addition, room temperature and warm storages significantly reduced final germination and germination speed at the different temperatures; the reduction was more pronounced at 35 °C. The ecological advantage of narrowing the germination window at 35 °C is to ensure that seeds stored on soil surface or under the shade of vegetation will not germinate easily under high temperatures of summer, even if rainfall is enough for seedling emergence.
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Repeated environmental stresses facing desert plants coupled with great human disturbances in the Arabian Gulf deserts increase the chance of the shrubs mortality [43]. In addition, the inability of the two shrubs S. imbricata and H. salicornicum to produce persistent seed bank would threaten their life under repeated drought stress and human disturbances in the deserts. In order to ensure annual seedling recruitment, high annual fruit production should compensate the high mortality rate of the seeds and plants of both S. imbricata and H. salicornicum. Both species produce enormous amount of highly dispersed fruits every year, even in the dry seasons. These plants mainly rely on atmospheric moisture and fog as main sources of water for their growth [10,11]. The high annual fruit production, even in the dry years, would compensate for the depletion of the transient seed bank, and consequently could ensure the regeneration of the two species in the harsh deserts. In addition, the greater dispersal ability of the fruits would enhance their ability in exploring the unpredictable deserts for more safe sites for germination and establishment [3]. References [1] R.J. Probert, The role of temperature in the regulation of seed dormancy and germination, in: M. Fenner (Ed.), Seeds: The Ecology of Regeneration in Plant Communities, CAB International, Wallingford, 2000, pp. 261–292. [2] C.C. Baskin, J.M. Baskin, Seeds: Ecology, Biogeography and Evolution of Dormancy and Germination, Academic Press, New York, 1998. [3] A. El-Keblawy, Progeny and seed dormancy traits in relation to achene heteromorphism in the two ephemerals Hedypnois cretica (L.) Dum.-Cours. and Crepis aspera L. (Asteracea), Canadian Journal and Botany 81 (2003) 550–559. [4] B. Capon, W. Van Asdall, Heat pre-treatment as a means of increasing germination of desert annual seeds, Ecology 48 (1967) 305–306. [5] Y. Gutterman, Strategies of seed dispersal and germination in plants inhabiting deserts, Botanical Review 60 (1994) 373–425. [6] W. Schutz, Germination responses of temperate Carex-species to diurnally fluctuating temperatures – a comparative study, Flora 194 (1999) 21–32. [7] M.A. Clor, T.A. Al-Ani, F. Charchafchy, Germinability and seedling vigor of Haloxylon salicornicum as affected by storage and seed size, Journal of Rangeland Management 29 (1976) 60–62. [8] A.K. Hegazy, Plant succession and its optimization on tar-polluted coasts in the Arabian Gulf region, Environmental Conservation 24 (1997) 149–158. [9] S.S. Radwan, H. Al-Awadhi, N.A. Sorkhoh, I.M. El-Nemr, Rhizospheric hydrocarbon-utilizing microorganisms as potential contributors to phytoremediation for the oily Kuwaiti desert, Microbiological Research 153 (1998) 247–252. [10] A. El-Keblawy, F. Al-Ansari, N. Hassan, N. Al-Shamsi, Salinity, temperature and light affect germination of Salsola imbricata, Seed Science and Technology 35 (2007) 272–281. [11] A. El-Keblawy, N.AL. Shamsi, Effects of salinity, temperature and light on seed germination of Haloxylon salicornicum, a common perennial shrub of the Arabian deserts, Seed Science and Technology 36 (2008) 679–688. [12] M.A. Khan, Relationship of seed bank to plant distribution in saline arid communities, Pakistan Journal of Botany 25 (1993) 73–82. [13] S. Zaman, S. Padmesh, H. Tawfiq, Seed germination and viability of Salsola imbricata Forssk, International Journal of Biodiversity and Conservation 2 (2010) 388–394. [14] G. Brown, S. Al-Mazrooei, Germination ecology of Haloxylon salicornicum from Kuwait, Botanische Jahrbücher für Systematik 193 (2001) 133–140. [15] G. Brown, S. Porembski, Miniature dunes and blow-outs as ‘‘safe-sites’’ for plants in an oil-contaminated area of Northern Kuwait, Environmental Conservation 27 (2000) 242–249. [16] A. El-Keblawy, A. Al-Rawai, Effects of seed maturation time and dry storage on light and temperature requirements during germination in invasive Prosopis juliflora, Flora 201 (2006) 135–143. [17] Y. Gutterman, S. Shem-Tov, S. Gozlan, The effect of post-maturation temperature and duration on seed germinability of Plantago coronopus occurring in natural populations in the Negev Desert highlands, Israel, Journal of Arid Environments 38 (1998) 451–463.
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[18] M.K. Owens, R.B. Wallace, S. Archer, Seed dormancy and persistence of Acacia berlandieri and Leucaena pulverulenta in a semi-arid environment, Journal of Arid Environments 29 (1995) 15–23. [19] Z.Y. Huang, I. Boubriak, D.J. Osborne, Possible role of pectin-containing mucilage and dew in repairing embryo DNA of seeds adapted to desert conditions, Annals of Botany 101 (2008) 277–283. [20] M.A. Khan, I.A. Ungar, The effect of salinity and temperature on the germination of polymorphic seeds and growth of Atriplex triangularis Willd, American Journal of Botany 71 (1984) 481–489. [21] J.L. Harper, Population Biology of Plants, Academic Press, New York, 1977. [22] J.W. Silvertown, J. Lovett-Doust, Introduction to Plant Population Biology, Blackwell Scientific Publications, Oxford, 1993. [23] A. Traveset, M. Verdú, A meta-analysis of gut treatment on seed germination, in: D.J. Levey, M. Galetti, W.R. Silva (Eds.), Frugivores and Seed Dispersal: Ecological, Evolutionary and Conservation Issues, CAB International, Wallingford, 2002, pp. 339–350. [24] M. Rees, Evolutionary ecology of seed dormancy and seed size, Philosophical Transactions of the Royal Society of London – Series B 351 (1996) 1299–1308. [25] M.E. Rogers, C.L. Noble, G.E. Hallorn, M.E. Nicolas, The effect of NaCl on germination and early seedling growth of white clover (Trifoliummm repens L.) population selected from high and low salinity tolerance, Seed Science and Technology 23 (1995) 277–287. [26] S. Zia, M.A. Khan, Effect of light, salinity, and temperature on seed germination of Limonium stocksii, Canadian Journal of Botany 82 (2004) 151–157. [27] T.L. Pons, H.F.J.M. Schröder, Significance of temperature fluctuation and oxygen concentration for germination of the rice field weeds Fibristylis littoralis and Scirpus juncoides, Oecologia 68 (1986) 315–319. [28] J.M. Baskin, C.C. Baskin, Physiology of dormancy and germination in relation to seed bank ecology, in: M.A. Leck, V.T. Parker, R.L. Simpson (Eds.), Ecology of Soil Seed Banks, Academic Press, New York, 1989, pp. 53–66. [29] S.B. Wuest, Vapour is the principal source of water imbibed by seeds in unsaturated soils, Seed Science Research 17 (2007) 3–9. [30] J.G. Dubrovsky, Seed Hydration Memory in Sonoran Desert Cacti and its Ecological Implication, American Journal of Botany 83 (1996) 624–632. [31] T.B. Wilson, T.F. Witkowsk, Water requirements for germination and early seedling establishment in four African savanna woody plant species, Journal of Arid Environments 38 (1998) 541–550. [32] C. Bailly, Active oxygen species and antioxidants in seed biology, Seed Science Research 14 (2004) 93–107. [33] B. Bai, N. Sikron, T. Gendler, Y. Kazachkova, S. Barak, G. Grafi, I. KhozinGoldberg, A. Fait, Ecotypic variability in the metabolic response of seeds to diurnal hydration–dehydration cycles and its relationship to seed vigor, Plant and Cell Physiology 53 (2011) 38–52. [34] G.H. Zheng, Seed physiology research at the Beijing Botanical Garden, Seed Science and Technology 12 (1984) 723–729. [35] G.H. Zheng, Physiological, biochemical and ultrastructural aspects of imbibitional chilling injury in seeds, Seed Science Research 1 (1991) 127–134. [36] Z. Peishi, J.A. Plummer, D.W. Turner, D. Choengsaat, D.T. Bell, Low- and hightemperature storage effects on viability and germinability of seeds of three Australian Asteraceae, Australian Journal of Botany 47 (1999) 265–275. [37] Z. Huang, X. Zhang, G. Zheng, Y. Gutterman, Influence of light, temperature, salinity and storage on seed germination of Haloxylon ammodendron, Journal of Arid Environments 55 (2003) 453–464. [38] A. Orozco-Segovia, A.E. Brechu-Franco, L. Zambrano-Polaco, R. OsunaFernández, G. Laguna-Hernández, M.E. Sánchez-Coronado, Effects of maternal light environment on germination and morphological characteristics of Sicyos deppei seeds, Weed Research 40 (2000) 495506. [39] M.M. Qaderi, P.B. Cavers, M.A. Bernards, Pre- and post-dispersal factors regulate germination patterns and structural characteristics of Scotch thistle (Onopordum acanthium) cypselas, New Phytologist 159 (2003) 263–278. [40] S.E. Meyer, P.S. Allen, Ecological genetics of seed germination regulation in Bromus tectorum L. II. Reaction norms in response to a water stress gradient imposed during seed maturation, Oecologia 120 (1999) 35–43. [41] M.P.M. Derkx, C.M. Karssen, Variability in light-, gibberellin- and nitrate requirement of Arabidopsis thaliana seeds due to harvest time and conditions of dry storage, Journal of Plant Physiology 141 (1993) 574–582. [42] R.J. Probert, R.D. Smith, P. Birch, Germination responses to light and alternating temperatures in European populations of Dactylis glomerata L. IV. The effects of storage, New Phytologist 101 (1985) 521–529. [43] K.H. Batanouny, Biodiversity strategy and rangelands in the Arab world, in: R. Hamzah, S.A. Alaa El-Din, M.N. Mohammed (Eds.), National Biodiversity Planning in the Arab World, Arabian Gulf University Publication, Bahrain, 2002, pp. 121–142.