Seed Germination in Desert Annuals: An Empirical Test of Adaptive Bet Hedging

Temporal variability in survivorship and reproduction is predicted to affect the evolution of life-history characters. Desert annual plants experience temporal variation in reproductive success that is largely caused by precipitation variability. We studied several populations of the desert annual Plantago insularis along a precipitation gradient. Whereas models of bet hedging in unpredictable environments generally predict one optimal germination fraction for a population, empirical studies have shown that environmental conditions during germination can cause a range of germination fractions to be expressed. In a 4-yr field study, we found that populations in historically more xeric environments had lower mean germination fractions, as is predicted by bet-hedging models. However, populations exhibited significant variation in germination among years. Two experimental studies measuring germination under several environment conditions were conducted to elucidate the source of this in situ variation. Germination fractions exhibited phenotypic plasticity in response to water availability and date within the season. Populations differed in their norms of reaction such that seeds from more xeric populations germinated under less restrictive conditions. A pattern of delayed germination consistent with among-year bet-hedging predictions arose in the field through the interaction of seed germinability and the distribution of environmental conditions during germination.     

Can seeds predict their future? Germination strategies of density‐regulated desert annuals

Annual plants in unpredictable environments maintain dormant seeds to avoid extinction. Here, we present results for four desert annual species suggesting that germination rates are variable even in the absence of abiotic cues. Namely, seeds produced in a copious year had lower germination rates than seeds produced in drought years. Inspired by our data, we have extended previous bet-hedging models by including a structured seed bank. With density-dependence, the ESS (environmental stable strategy) involved a negative relationship between seed yield and subsequent germination probability. We suggest that heterogeneous germination rates are selected for by competition among seedlings after years with high seed production. In summary, our findings are suggestive of an intriguingly simple and effective mechanism that may allow annual plants to partly predict their future success.     

Adaptive traits of wild barley plants of Mediterranean and desert origin

Reciprocal introduction of seeds and seedlings was used to test for local adaptation and to identify a set of co-adapted traits of Mediterranean and desert ecotypes of wild barley Hordeum spontaneum. Evidence for local adaptation was found in seedling introductions into intact environments and from ecotype colonization success in the first generation after seed dispersal. Estimates of fitness were obtained at particular stages of the life cycle (seed, seedling and adult). Experiments that manipulated the environment (vegetation removal, different plant density) demonstrated the intensity and direction of natural selection in different life history episodes, but there was no strong evidence for local adaptation under these circumstances. The observed genetically determined differences between Mediterranean and desert ecotypes can be summarized as the following: reproductive output was higher in desert plants, with smaller seeds than in Mediterranean plants. There was a higher competitive ability of Mediterranean than desert plants. Plants of desert origin had significant reductions in yield when grown in mixed stands with Mediterranean plants; no such effect was observed for plants of Mediterranean origin. Seed germination and seedling survival was lower in seeds of desert origin. This was due to both: genetically determined higher dormancy of desert seeds and a trade-off between no. of seeds and their size (directly related to seed/seedling vigour).     

Seed mass and dormancy of annual plant populations and communities decreases with aridity and rainfall predictability

Several theoretical and empirical studies have examined the influence of environmental conditions on seed traits and germination strategies of annual species. A positive relationship between seed mass and dormancy has been described for annuals occupying climatically unpredictable ecosystems. Larger-seeded species tend to have higher seedling survival rates, while dormancy allows a bet-hedging strategy in unpredictable environments. Until now, these ideas have been addressed primarily for only one or a few focal species, without considering differences among populations and communities. The novelty of the present study lies in the population and community-level approach, where a comprehensive seed trait database including 158 annual species occurring along a gradient of rainfall variability and aridity in Israel was used to ask the following question: Does average seed mass and dormancy of annual populations and communities decrease with increasing aridity and rainfall unpredictability?Soil seed bank samples were collected at the end of the summer drought, before the onset of the rains, from four plant communities. Germination was tested under irrigated conditions during three consecutive germination seasons to determine the overall seed germinability in each soil sample. Seed mass was obtained from newly produced seeds collected at the study sites in late spring. The community level results showed that, in contrast to common theoretical knowledge, seed mass and dormancy of the dominant annual species decreased with increasing aridity and rainfall variability. Accordingly, a negative correlation was found between seed mass and seed germination fractions. The present study demonstrates that an analysis of seed traits along climatic gradients is significantly improved by approaches that target both population and community levels simultaneously. A critical evaluation sheds new light upon the selective pressures that act on seed ecology of annuals along a climatic gradient and facilitates formulation of more mechanistic hypotheses about factors governing critical seed traits.     

Ecological significance of the aerial seed pool of a desert lignified annual,Blepharis sindica (Acanthaceae)

Reproductive traits of a lignified annual plant, Blepharis sindica were studied in relation to the formation of an 'aerial seed pool' on dead plants in an arid grassland in the Thar Desert of northwestern India. The dead plants remained standing on the soil surface and retained fruits for more than one year. Aerial seed pools developed about 6 cm above the ground. There were no seed pools on or below the ground surface. Only 5.7% of seeds died on dead plants because of insect predation or fungi infection during one year. Seed release was cued by rainfall, and a fraction of seeds on the aerial seed pools was released in each rainfall event. After 13 rainfall events during the monsoon season, 25% of seeds was still retained on the plants. Seed predation on the ground surface was intensive; all cones placed on the soil surface were removed within four days, and 97% of fruits were removed within 10 days. Fifty percent of seeds germinated within 3.5 h, and there were no differences in viability and time required for germination between first year seeds and older seeds. The results indicate that the aerial seed-holding on dead plants is an available way to avoid seed predation in harsh desert environments where seed predation is intense and favorable periods for growth are temporally limited and unpredictable.     

Aerial and soil seed banks enable populations of an annual species to cope with an unpredictable dune ecosystem

Background and Aims

Simultaneous formation of aerial and soil seed banks by a species provides a mechanism for population maintenance in unpredictable environments. Eolian activity greatly affects growth and regeneration of plants in a sand dune system, but we know little about the difference in the contributions of these two seed banks to population dynamics in sand dunes.

Methods

Seed release, germination, seedling emergence and survival of a desert annual, Agriophyllum squarrosum (Chenopodiaceae), inhabiting the Ordos Sandland in China, were determined in order to explore the different functions of the aerial and soil seed banks.

Key Results

The size of the aerial seed bank was higher than that of the soil seed bank throughout the growing season. Seed release was positively related to wind velocity. Compared with the soil seed bank, seed germination from the aerial seed bank was lower at low temperature (5/15 °C night/day) but higher in the light. Seedling emergence from the soil seed bank was earlier than that from the aerial seed bank. Early-emerged (15 April–15 May) seedlings died due to frost, but seedlings that emerged during the following months survived to reproduce successfully.

Conclusions

The timing of seed release and different germination behaviour resulted in a temporal heterogeneity of seedling emergence and establishment between the two seed banks. The study suggests that a bet-hedging strategy for the two seed banks enables A. squarrosum populations to cope successfully with the unpredictable desert environment.     

两种集合繁殖体形态及间歇性萌发特性——以蒺藜和欧夏至草为例

集合繁殖体(synaptospermy)是荒漠植物为适应恶劣环境条件而演化出的关键性特征,其作为植物生活史特性之一,有助于了解在荒漠环境下集合繁殖体植物的适应策略。蒺藜(Tribulus terrestris)和欧夏至草(Marrubium vulgare)分别为一年生及多年生草本植物,蒺藜扩散单位由一朵花发育而成的集合繁殖体组成,欧夏至草扩散单位由多朵花发育的集合繁殖体和种子组成,以这两种植物为材料,对其集合繁殖体形态、活力、吸水及萌发特性进行初步研究。结果显示:(1)蒺藜集合繁殖体依照发育成熟先后位置在质量、附属物刺的长度、附属物占质量百分比、种子数、活力、吸水量、萌发率及萌发速率均存在显著差异;欧夏至草集合繁殖体质量及吸水量明显大于种子,而活力、萌发率及萌发速率不存在显著差异。(2)萌发位置上,蒺藜集合繁殖体仅在长刺端位置的种子萌发,属非随机萌发,而欧夏至草集合繁殖体萌发不具有规律性,属随机萌发;萌发时间上,蒺藜和欧夏至草集合繁殖体在当季下均只萌发部分种子,具间歇性萌发特性。(3)对不同生活型植物而言,其集合繁殖体附属物对种子的保护、保水、扩散及萌发行为的功能相同,但一年生草本植物的萌发行为侧重于种群繁衍,因此蒺藜集合繁殖体在当季萌发率及萌发速率较高;多年生草本植物的萌发行为侧重于种群扩散,因此欧夏至草扩散单位多样化,且萌发率及萌发速率较低。     

温带半干旱地区一年生植物种子的萌发特性

在实验室条件下研究了中国温带半干旱地区科尔沁沙地的23种1年生植物的种子萌发特性（新采集种子、冷藏和干藏种子）.大籽蒿、虎尾草、冠芒草、沙蓬和地锦的新种子萌发率达90%左右,11种植物新种子萌发率均低于70%,说明这些植物的新种子具有或多或少的休眠属性.经过150d的冷干藏后,大籽蒿、虎尾草萌发率保持在90%以上,说明这两种植物完全没有休眠机制;冠芒草、沙蓬和地锦的种子萌发率下降较多,可能是储藏的环境条件导致的2次休眠现象;冷藏和干藏处理均能使绿珠藜、毛马唐、细叶益母草、雾冰藜、金狗尾草、苋菜、马齿苋、碱地肤和水稗草的种子在生长季开始时完成生理后熟,萌发率达到80%以上;干藏有利于促进毛马唐、细叶益母草、马齿苋和鹤虱的种子成熟,冷藏有利于促进绿珠藜和金狗尾草的种子成熟;黄蒿、灰绿藜、画眉草和烛台虫实在不同处理下的萌发率都比较低,说明种子内在生理休眠作用较强,具有减少种子一次性萌发数量的风险分摊策略.大多数1年生植物均能在较短时间内达到最终萌发率的90%,表现出迅速萌发的特性;黄蒿、灰绿藜、碱地肤和沙蓬种子则在不同处理中表现出延长萌发时间的策略来适应半干旱地区不确定的环境条件.最后,探讨了几种主要1年生植物的种子萌发对策与其对环境适应机制之间的关系.     

Seed aging,delayed germination and reduced competitive ability in Bromus tectorum

In annual plants, increased competitive advantage has often been attributed to rapid germination and early establishment. In contrast, many annual species exhibit some degree of delayed germination (i.e., seed dormancy) that results in the formation of age structure within the seed population. Delayed germination can be an effective bet-hedging strategy in variable or unpredictable environments as a seed bank can buffer against years with reproductive failures and reduce the probability of local extinction. However, there has been little consideration of the direct effects of aging within the seed pool although the potential demographic costs of such a strategy (e.g., mortality in the seed bank or delayed reproduction) are well known. We used aged (4 year-old) and freshly produced seed from meadow steppe and sagebrush steppe populations of an annual grass (Bromus tectorum)to investigate the importance of seed age on seedling vigor and competitive ability. Aged seed from the meadow steppe population exhibited delays in germination that reduced plant growth and final biomass when the plants were grown with competition. Aged seed from the sagebrush steppe population did not exhibit delays in germination. By including a treatment that experimentally delayed the germination of freshly produced meadow steppe seed, we also examined the effects of delayed germination alone. A comparison of results from this delay treatment with those from the aged seed treatment suggested that the reduced competitive ability of meadow steppe plants produced from aged seed, although largely a result of the temporal delay in germination, was partly due to reduced seed vigor. Together these results indicate that physiological costs associated with seed age may affect aboveground competitive interactions and, in turn, the relative fitness of older cohorts in the soil seed bank.     

荒漠植物种子逆境萌发研究进展

对水分、温度、光照、沙埋深度、盐分胁迫及以上几种综合因素在逆境条件下对荒漠植物种子萌发的影响进行了综述。降雨次数、雨量大小、分布及土壤湿度是决定荒漠植物种子萌发的重要生态因子;温度是影响荒漠植物种子萌发的关键生态因子之一,变温有利于荒漠植物种子萌发;光照并非大多数荒漠植物种子萌发的必要条件,少部分荒漠植物种子萌发需要光照,有些要在黑暗中萌发,有些则对光照无特殊要求,光照对有些荒漠植物种子萌发有一定的抑制;不同沙埋深度具有不同的土壤湿度,土壤温度和光照等条件,综合调控荒漠植物种子的萌发;盐分胁迫抑制种子的萌发。荒漠植物种子的萌发在以上几种因素的共同协调作用下表现出一定的适应性。随着研究的不断深入和生态环境建设的需求,需要加强荒漠植物生理生态研究的深度和研究的系统性。     

Two Mediterranean annuals feature high within-population trait variability and respond differently to a precipitation gradient

Intraspecific trait variability plays an important role in species adaptation to climate change. However, it still remains unclear how plants in semi-arid environments respond to increasing aridity. We investigated the intraspecific trait variability of two common Mediterranean annuals (Geropogon hybridus and Crupina crupinastrum) with similar habitat preferences. They were studied along a steep precipitation gradient in Israel similar to the maximum predicted precipitation changes in the eastern Mediterranean basin (i.e. −30% until 2100). We expected a shift from competitive ability to stress tolerance with decreasing precipitation and tested this expectation by measuring key functional traits (canopy and seed release height, specific leaf area, N- and P-leaf content, seed mass). Further, we evaluated generative bet-hedging strategies by different seed traits. Both species showed different responses along the precipitation gradient. C. crupinastrum exhibited only decreased plant height towards aridity, while G. hybridus showed strong trends of generative adaptation to aridity. Different seed trait indices suggest increased bet-hedging of G. hybridus in arid environments. However, no clear trends along the precipitation gradient were observed in leaf traits (specific leaf area and leaf N-/P-content) in both species. Moreover, variance decomposition revealed that most of the observed trait variation (≫50%) is found within populations. The findings of our study suggest that responses to increased aridity are highly species-specific and local environmental factors may have a stronger effect on intraspecific trait variation than shifts in annual precipitation. We therefore argue that trait-based analyses should focus on precipitation gradients that are comparable to predicted precipitation changes and compare precipitation effects to effects of local environmental factors.     

Annual plants in arid and semi-arid desert regions

Annual plants are the main vegetation in arid and semi-arid desert regions.Because of their unique traits,they are the optimal experimental subjects for eco-logical studies.In this article,we summarize annual plants' seed germination strategies,seedling adaptability mechanism to environments,seed dispersal,and soil seed banks.We also discuss the biotic and abiotic factors affecting the composition and dynamics of annual plant populations and communities.Because annual plants have important ecological functions in desert vegetation systems,this study on annual plants will be of great bene-fit to the conservation and restoration of desert ecosys-tems,the rational utilization of resources,and the sustainable development of desert regions.     

Effects of Biological Soil Crusts on Seed Bank, Germination and Establishment of Two Annual Plant Species in the Tengger Desert (N China)

The presence of biological soil crusts can affect the germination and survival of vascular plants, but the reasons are not well investigated. We have conducted a field investigation and greenhouse experiments to test the effect of crusts on two desert annual plants, which occur on the stabilized dunes of the Tengger Desert in N China. The results showed that biological soil crusts negatively influenced the seed bank of Eragrostis poaeoides and Bassia dasyphylla. The important effect of biological soil crusts on seed germination and establishment were performed indirectly through reducing the amount of germinating seeds. Field investigation and experimental results with regard to the seed bank indicated that higher seedling density was found in disturbed crust soil and bare soil surface than in intact crust soils. Greenhouse experiments showed that the effects of biological soil crusts on germination and establishment of the two plants are not obvious in moist condition, while disturbed crusts are more favorable to seed germination in dry treatment. Significant differences in biomass were found between disturbed crust soil and bare soil. Survival and growth of the two annual plants were enhanced in both algal and moss crusts during the season of rainfall or in moist environment, but crusts did not affect seedling survival in the dry period. The small seeded E. poaeoides has higher germination than larger-seeded B. dasyphylla in crust soils, but B. dasyphylla has a relatively higher survival rate than E. poaeoides in crust soils.     

种子异型性及其生态意义的研究进展

种子异型性是指同一植株产生不同形状或行为种子的现象。根据异型种子在植株上的生长位置, 种子异型性可划分为地上下结实性和地上种子异型性两类。此现象已在26科129属292种被子植物中报道。异型性种子植物主要分布于干旱半干旱区、荒漠和盐渍土地区等干扰强烈的环境, 在菊科和藜科中最为常见, 主要出现在一年生植物中。种子异型性在避免密集负效应、减弱同胞子代间的竞争、采取两头下注策略以适应时空异质性环境等方面具有重要的进化生态意义。该文系统总结了国内外种子异型性的研究工作, 主要内容包括: 1)种子异型性的概念、类型和种类, 2)具有异型种子植物的生境和生活型, 3)异型种子的生态学特性, 4)种子异型性的理论模型, 5)种子异型性的生态意义。在综述文献的基础上, 对今后的研究进行了展望。针对国内外的研究现状, 提出两点建议: 1)系统调查具有种子异型性现象的植物种类, 摸清其生物学特性; 2)确定研究种子异型性现象的模式植物, 从生态学、生理学和分子生物学等学科角度来研究种子异型性的个体发育机制及分子调控机理。     

Populational dynamics of three annual species of alpine plants in the Rocky Mountains

Summary Survivorship, fecundity, and seed bank size were measured over two years in alpine populations of the annuals, Koenigia islandica, Polygonum confertiflorum, and P. douglasii. The major loss of individuals from all populations occurred between seed dispersal and germination. Survival of vegetative plants to maturity was high in all species, usually above 80%, and the average number of seeds produced per plant was less than 10 in all species in both years. Seed banks existed for all three species but were small since more than 80% of the viable seeds in the soil germinated in the spring. Both survival and fecundity were negatively correlated with density in P. confertiflorum. These patterns of population dynamics are similar to those found in many annuals of temperate environments.     

Emergence dynamics and bet hedging in a desert bee,Perdita portalis

Bees (series Apiformes, superfamily Apoidea) are most diverse in arid regions of the world. Arid regions (deserts and semi-deserts) are characterized by discrete rainy seasons and extreme temporal variability in rainfall. This paper documents several novel mechanisms by which one desert bee species (Perdita portalis) copes with harsh and unpredictable conditions in xeric habitats. These same mechanisms are likely to be present in diverse bee families. First, diapausing P. portalis follow a bet-hedging emergence pattern, such that only approximately half of the larvae pupate under optimal conditions. Second, emergence is condition dependent such that larvae with a low average body weight are significantly more likely to emerge than are larvae with a high average body weight under similar conditions. Finally, larval emergence is induced by exposure to high humidity (rainfall). The parallels between bee larvae and angiosperm seeds in arid environments are striking. In both cases there is clear evidence of bet hedging, emergence (or germination) is dependent on larval (or seed) condition and rainfall triggers emergence (or germination). These patterns of emergence are significant for understanding bee species diversity in arid regions.     

Germination behaviour of annual plants under changing climatic conditions: separating local and regional environmental effects

The role of local adaptation and factors other than climate in determining extinction probabilities of species under climate change has not been yet explicitly studied. Here we performed a field experiment with annual plants growing along a steep climatic gradient in Israel to isolate climatic effects for local trait expression. The focus trait was seed dormancy, for which many theoretical predictions exist regarding climate-driven optimal germination behaviour. We evaluated how germination is consistent with theory, indicating local adaptation to current and changing climatic conditions, and how it varies among species and between natural and standardised soil conditions. We reciprocally sowed seeds from three or four origins for each of three annual species, Biscutella didyma, Bromus fasciculatus and Hymenocarpos circinnatus, in their home and neighbouring sowing locations along an aridity gradient. Our predictions were: lower germination fraction for seeds from more arid origins, and higher germination at wetter sowing locations for all seed origins. By sowing seeds in both local and standard soil, we separated climatic effects from local conditions. At the arid sowing location, two species supported the prediction of low germination of drier seed origins, but differences between seed origins at the other sites were not substantial. There were no clear rainfall effects on germination. Germination fractions were consistently lower on local soil than on standard soil, indicating the important role of soil type and neighbour conditions for trait expression. Local environmental conditions may override effects of climate and so should be carefully addressed in future studies testing for the potential of species to adapt or plastically respond to climate change.     

Neighbor effects on germination, survival, and growth in two arctic tundra plant communities

In relatively harsh environments such as arctic tundra, abiotic factors have traditionally been considered the primary determinants of community structure, overwhelming any effects of biotic interactions such as competition. Two common low arctic tundra types that differ in soil properties, moist acidic and moist non-acidic tussock tundra (MAT and MNT, respectively), occur in close proximity in northern Alaska. Several plant species occur in both communities with different relative abundance, while others are restricted to one. This study experimentally examined how neighboring vegetation affects germination, survival, and growth of species in these two communities that differ in soil pH, cation availability, and other characteristics. Germination of sown seeds was greater than background levels suggesting seed limitation may restrict recruitment of these clonal, perennial species. Germination of sown seeds was greater at both sites when both mosses and vascular plants had been removed compared to plots with intact vegetation. However, neighbors had almost no effect on survival and growth of adult transplants. Patterns of germination, survival and growth of several species differed depending on the community of origin and the community of destination of the seeds or transplanted adults. For example, transplants of the sedge Eriophorum vaginatum grew better if they were from MAT, and this species germinated better when sown at MNT. Although of relatively short duration (three growing seasons), this study suggests that biotic interactions may affect local species composition by restricting germination and establishment in these two communities, but have less of an effect on adult plants. Not surprisingly, site-specific abiotic conditions also exhibit control over species occurrence and relative abundance. Without disturbance to clear bare ground for recruitment of new individuals, these populations for the most part must rely on clonal growth to persist.     

Spreading recruitment over time to cope with environmental variability

Seedling establishment is one of the most vulnerable life cycle stages, and a key component for the population dynamics in short-lived plants. In unpredictable environments, timing of emergence is critical for the success of plant performance, and different adaptive bet-hedging strategies have evolved to reduce the risk of failure in recruitment. In this study we describe the spatio-temporal pattern of seedling emergence (overall rate and timing) and survival in four contrasting Mediterranean habitats for Plantago coronopus, a small herb with dimorphic seeds. We then explore the importance of spreading germination within years, as well as the role of the two types of seeds from a broader temporal perspective. Populations strongly differed for all recruitment components analyzed in a given year, but this spatial differentiation diluted when a longer period was considered. Apical (smaller) seeds germinated later and in a significantly lower proportion than basal (larger) seeds. Both late emergents and seedlings from apical seeds had lower survival probability in a rainy year. However, our results suggest that in a population having the lowest production of apical seeds, late emergents coming from apical seeds may constitute a large fraction of yearly recruitment and that their performance was non-significantly different from that of early emergents over the 4-year study period. This study provides evidence of the importance of two related traits (spreading seedling emergence through time by producing dimorphic seeds) as bet-hedging strategies to cope with environmental unpredictability. This is at least partly accomplished by increasing the potential of recruitment in favourable years, instead of buffering such important process in extremely bad years.     

Comparison of germination and seed bank dynamics of dimorphic seeds of the cold desert halophyte Suaeda corniculata subsp. mongolica

Background and Aims

Differences in dormancy and germination requirements have been documented in heteromorphic seeds of many species, but it is unknown how this difference contributes to maintenance and regeneration of populations. The primary aim of this study was to compare the seed bank dynamics, including dormancy cycling, of the two seed morphs (black and brown) of the cold desert halophyte Suaeda corniculata and, if differences were found, to determine their influence on regeneration of the species.

Method

Seeds of the two seed morphs were buried, exhumed and tested monthly for 24 months over a range of temperatures and salinities, and germination recovery and viability were determined after exposure to salinity and water stress. Seedling emergence and dynamics of the soil seed bank were also investigated for the two morphs.

Key Results

Black seeds had an annual dormancy/non-dormancy cycle, while brown seeds, which were non-dormant at maturity, remained non-dormant. Black seeds also exhibited an annual cycle in sensitivity of germination to salinity. Seedlings derived from black seeds emerged in July and August and those from brown seeds in May. Seedlings were recruited from 2·6 % of the black seeds and from 2·8 % of the brown seeds in the soil, and only 0·5 % and 0·4 % of the total number of black and brown seeds in the soil, respectively, gave rise to seedlings that survived to produce seeds. Salinity and water stress induced dormancy in black seeds and decreased viability of brown seeds. Brown seeds formed only a transient soil seed bank and black seeds a persistent seed bank.

Conclusions

The presence of a dormancy cycle in black but not in brown seeds of S. corniculata and differences in germination requirements of the two morphs cause them to differ in their germination dynamics. The study contributes to our limited knowledge of dormancy cycling and seed bank formation in species producing heteromorphic seeds.