Plasticity in Dynamics and Hygrochastic Persistence in Anastatica Hierochuntica L

POLISH JOURNAL OF ECOLOGY 61 3 493–504 2013 (Pol. J. Ecol.)

Regular research paper

A. K. HEGAZY1, 2*, H. F. KABIEL1, A. A. ALATAR2, J. LOVETT-DOUST3

1 Department of Botany, Faculty of Science, Cairo University, Giza 12613, Egypt *e-mail: [email protected] (corresponding author) 2 Department of Botany & Microbiology, College of Science, King Saud University, Riyadh, Saudi Arabia 3 Department of Biological Sciences, University of Windsor, Windsor, Ontario, Canada

PLASTICITY IN DYNAMICS AND HYGROCHASTIC PERSISTENCE IN ANASTATICA HIEROCHUNTICA L. (BRASSICACEAE) POPULATIONS UNDER SIMULATED RAINFALL TREATMENTS

ABSTRACT: Anastatica hierochuntica is a be reduced by water stress. Populations of A. hiero- monocarpic desert annual whose dry skeletons, chuntica characterized by weak plant growth and enclosing mature fruits, often persist for a number a preponderance of small size-classes will be more of years. The aerial seed bank in these hygrochas- vulnerable to extinction due to their low reproduc- tic ‘resurrection plants’ therefore persists too. Life tive output and reduced aerial seed bank reserve. tables and fecundity schedules were constructed for A. hierochuntica populations raised under four KEY WORDS: seed bank, seed dispersal, water treatments, equivalent to 100, 200, 500 and life table, fecundity schedule, tumbleweeds, hy- 1000 mm rainfall. Seedling survivorship showed a grochastic plants, rose of Jerico, bradyspory and Deevey type III curve for 100 mm, and a type II restricted dispersal curve for 200 mm, while 500 and 1000 mm treatments produced Deevey type I curves. Fewer seeds germinated and seedling survivorship was lower in 1. INTRODUCTION the low water treatments. The stage-specific mortality rate reached 0.75 under the 100 mm treat- Anastatica hierochuntica L. (Brassica- ment in the seed germination stage, compared ceae), the rose of Jericho, is a desert plant to 0.08 under the 1000 mm treatment. Increased known for its use in folk medicine (Ham- water availability resulted in greater plant growth miche and Maiza 2006, AlGamdi et al. and reproductive output, in terms of both number 2011), and its active chemical constituents of seeds per individual and reproductive value. In (Nakashima et al. 2010), as much as for field studies, aerial seed banks of small plant size- 3 its adaptive features for arid environments classes (from 1 to 32 cm ) were depleted within (Friedman et al. 1978, 1981, Gutterman 3-to-7 years. For the large size-classes, > 32 cm3, only a portion (79.7-44.4%) of the seeds produced 1994, Hegazy et al. 2006, Hegazy and Ka- were dispersed during the observational experi- biel 2010). The species is found across North ment (the rest remaining within the tumbleweed Africa from Morocco to Egypt and in western ball, available for subsequent germination). The Asia to Pakistan. Typical microhabitats in- projected seed bank life-time for populations clude runnels with gravel to coarse sandy soil, raised under different water treatments increased and depressions having coarse to fine sandy more than fivefold (from 3 to 17 years) for the 100 soil (Hegazy and Kabiel 2007). mm compared to the 1000 mm rainfall treatments. Persistence of A. hierochuntica is depen- Local persistence of populations was thus likely to dent upon the way in which seeds are pro- 494 A. K. Hegazy et al. tected against desiccation and predation and be likely (Harper 1977, Freas and Kemp adapted to respond rapidly to unpredictable 1983, Gutterman 2000). Delayed germina- rainfall (Friedman et al. 1981). After fruit tion, either through dormancy or regulation ripening, the desiccated plant rolls up into of seed dispersal in time (bradispory) would a tight ball, forming a protective structure serve as a bet-hedging strategy to the unpre- around the fruits, which may remain viable dictability of the desert environment (Phil- within the ball for several years. Typically, lipi 1993, Hegazy 2001). following about an hour of continuous rain- Most cases of bradispory have been asso- fall, the wet plant skeleton uncoils and some ciated with hygrochasy and fruit dehiscence of the fruits will open due to the sheer force upon wetting, permitting intermittent seed of raindrops (Friedman et al. 1978, Hega- dispersal from the aerial seed bank (Van zy and Kabiel 2010). The moistened, now Oudtshoorn and Van Rooyen 1999, mucilaginous seeds are then released and ad- Hegazy et al. 2006). The importance of dry here to the moist soil surface. Seeds within skeletons to the persistent seed bank has been a given ball are not all released together, but reported in A. hierochuntica (Steinbrinck rather only a few at a time, during episodes and Schinz 1908, Evenari 1949, Friedman of rainfall which may occur over more than et al. 1978, Evenari et al. 1982, Danin 1983) a decade. The fruit is a short silique contain- as well as in many other desert plant species ing four seeds; two on each side of a septum (Hildebrand 1873, Zohary and Fahn 1941, (Hegazy and Kabiel 2007). If there is suffi- Gutterman 1972, Evenari et al. 1982, Yea- cient rain, seeds may begin to germinate after ton and Esler 1990, Esler et al. 1992, Gut- about ten hours. terman and Ginott 1994, Nel 1994). According to Friedman and Stein Although A. hierochuntica is an annual (1980), A. hierochuntica shows two major monocarpic plant, the dry skeleton balls al- patterns of seed dispersal. Primary dispersal low intermittent release of seeds to brief peri- or ‘‘dispersal on the spot’’ occurs in response ods of suitable environmental conditions. The to light rainfall events, and secondary disper- curling and uncurling of skeletons is facilitat- sal or ‘‘dispersal to a distance’’ results from ed by the hygrochastic nature of the branches, high rainfall followed by runoff. In the first, which results in a delayed seed dispersal and seeds are dislodged and germinate near the ongoing reserve of seeds until depletion of parent skeleton, perhaps even within its dead the aerial seed bank (Evenari 1949, May- branches, while in the secondary strategy er and Poljakoff-Mayber 1982, Hegazy seeds are carried away by water runoff and et al. 2006). germinate at some distance from the par- In previous studies of A. hierochuntica ent individual. The size of A. hierochuntica under different water treatments (simulat- plants is highly responsive to the amount of ing 50, 100 and 200 mm rainfall), contrasting water in the habitat. This phenotypic plastic- patterns of resource allocation have been not- ity leads to skeleton size-class distributions ed (cf. Evenari et al. 1982, Hegazy 1990b). in natural populations that likely reflect dif- However the effect of varying amounts of ferent amounts of rainfall. We have earlier rainfall on population dynamics and their suggested these size-distribution patterns of ecological implications has not been reported. plant skeletons in A. hierochuntica might be Other species raised under controlled condi- used as a “rain gauge,” of previous rainfall, or tions have been studied (e.g., Werner 1975, water received in a habitat over, say, ten years Werner and Caswell 1977), where individ- (Hegazy and Kabiel 2010). uals have been followed from emergence to Long-term survival of desert annuals is senescence. In the present study, life table and ensured by only allowing a portion of seeds fecundity schedule analysis were used to dif- to germinate in each rainfall event, leaving ferentiate among plants raised under an array a persistent, viable seed reserve within the of simulated rainfall treatments. skeleton ball. In contrast, if all seeds germi- It was hypothesized that populations of nated in response to a light rain shower that A. hierochuntica may persist for several years was insufficient to guarantee survival to the in a location, depending upon the size of the reproductive stage, local extinction would dry aerial seed bank, and the amount of rain- Population dynamics of Anastatica hierochuntica 495 fall and the time taken for all seeds to dis- 2.2. Greenhouse experiment perse. The aim of this investigation was to: (1) investigate the dynamics of plants and seed The experiment was conducted in an cohorts raised under different amounts of open greenhouse at the Faculty of Science, simulated rainfall, and (2) simulate the maxi- Cairo University over a five month period mum duration for local persistence of A. hi- from mid March to mid August, 2009. A total erochuntica plants and seed cohorts, grown of 50 randomly selected dry skeletons were under natural conditions. collected from a natural population occupy- ing an area of about 0.6 km2 in Wadi Hagoul. 2. MATERIALS AND METHODS Seeds were manually extracted from the 50 plants dry skeletons by direct pressing on the 2.1. Field data wet fruit valves and mixed into one stock. Seeds were sown at 0.5 cm depth in wooden Naturally growing populations of Ana- boxes (50 ´ 50 cm2 area and 50 cm height) statica hierochuntica were monitored in filled with sandy-gravel soil collected from Wadi Hagoul (on the Cairo-Suez desert road, the site in Wadi Hagoul. A total of 100 seeds 29°55’08.0’’N and 32°11’55.9’’E). The size of was sown in every box. Four water treatments individual dry skeletons was measured in were applied equivalent to 100, 200, 500 and terms of the volume of the skeleton-ball. As 1000 mm rainfall, scheduled throughout the plants dry up, only the lignified plant skel- experiment. Four replicate boxes containing eton remains, bearing the fruits (Hegazy 100 seeds each per treatment were observed. et al. 2006). The dry skeleton of the dead In each of the treatments the survival plant enclosing its fruits forms a sphere. The of individuals was observed from the sown volume of the spherical skeletons was mea- seed stage to senescence of adult individu- sured as 4/3πr3, where ‘r’ is the mean radius als. Plant life history was differentiated into of the skeleton (=diameter/2), measured by seven stages: (1) The seed stage, represented inserting a fine metal rod into the skeleton by the number of sown seeds; (2) Emergence from different sides, and the mean value cal- stage, from plumule emergence above the soil culated from five estimates. Skeleton-balls surface to the expansion of the cotyledon- were sorted into 10 size classes (Table 1). ary leaves; (3) Seedling stage, from expan- Five skeletons per size class were selected sion of the cotyledons to the appearance of at random and the number of closed fruits one expanded true leaf; (4) Juvenile stage, was tallied in each individual. The percent- from the appearance of the second leaf to the age of seeds dispersed in each size-class was appearance of the first flower bud; (5) Flow- calculated based on the number of opened ering stage, from the appearance of the first fruits, where each fruit typically contains flower until the number of flowers per indi- four seeds. vidual was no longer greater than the number

Table 1. Volume range of dry, adult skeletons of Anastatica hierochuntica grouped from smallest (1) to largest (10) size-classes. Size-class Volume range (cm3) 1 <1 2 1–2 3 2.1–4 4 4.1–8 5 8.1–16 6 16.1–32 7 32.1–64 8 64.1–128 9 128.1–256 10 > 256 496 A. K. Hegazy et al. of fruits per individual; (6) Fruiting stage, the 2.4. Simulation of seed dispersal period where the number of fruits per individual was greater than the number of flow- By reference to field data, we estimated ers, until the beginning of die-back and leaf the length of time that skeleton balls would death; and (7) Senescence stage, from the be- persist under the different water treatments. ginning of die-back to where no green struc- To estimate the likely persistence of skeleton tures (stems or leaves) remain. balls in each treatment, the size class that was of greatest abundance in the experiment 2.3. Life table and fecundity schedule was taken as representative of that rainfall intensity. The largest size-class in different A dynamic life table and fecundity sched- populations showed maximum persistence ule for A. hierochuntica populations raised by having the highest number of seeds under different water treatments was con- trapped in the dry skeletons. The life-time structed (Pielou 1977, Hegazy, 1990a). The of the seed bank was taken from field data first column of the life-table (see APPEN- on seed dispersal over a seven year observa- DIX) sets out the various growth stages. The tional study (1996–2003). Estimation of the second and third columns give the estimated seed bank persistence was performed for age in days (x) and the corresponding num- populations raised under conditions simu- ber of individuals (Nx) surviving to day x. The lating 500 and 1000 mm rainfall treatments data are standardized in the fourth column, (noting that seed dispersal was not complete starting with a value of 1.0; the proportions within the experimental period, for the large of the original cohort surviving to the start of size-classes). The annual, gradual depletion each stage (lx) were calculated. Accordingly, of the seed bank was determined by multi- the proportion of the original cohort dying plying the mean rate of seed dispersal over during each stage (dx) and the stage-specific the experimental period by the initial num- mortality rate (qx) were calculated. The rate or ber of seeds available. intensity of mortality during any stage, which The standardized proportion of seeds reflects the killing power (kx), was computed remaining within the aerial seed bank was from the (Nx) values. The expectation of fu- calculated by dividing the number of non- ture life (ex) in age units was estimated by the dispersed seeds per skeleton-ball per treat- summation of lx for all ages following and in- ment each year until all seeds had been dis- cluding that of age x. The fecundity schedule persed, by the original number of seeds. The was constructed from the seed output. The dispersed seeds per skeleton-ball per size- average number of seeds per individual per class were calculated based on the number of stage (bx), and the average seed contribution opened fruits, where each fruit typically con- by any individual at a given age to the popula- tains four seeds. The expected persistence of tion of future generations (Vx) was calculat- A. hierochuntica populations from one year to ed. The equations used in computing the life the next was calculated by dividing the sum- table and fecundity schedule parameters are mation of the proportion of non-dispersed found in Hegazy (1992). One-way Analysis seeds from that year until complete seed dis- of Variance was used to test the significance persal, by the proportion of non-dispersed of differences between means of the life table seeds in the specified year. parameters for different treatments.

Table 2. Reproductive traits of Anastatica hierochuntica populations raised under simulated rainfall treatments. Treatment (mm rainfall) Reproductive trait 100 200 500 1000

Average number of seeds per individual (bx) 21.6 98.3 695.9 2919.5

Reproductive value Vx 19.3 82.4 510.4 1560.6

Reproductive rate lxbx 0.6 17.3 260.3 983.2 Figures

Population dynamics of Anastatica hierochuntica 497

(A) (B)

100 mm 1.0 1.0 b 200 mm 500 mm b c c ab b 1000 mm 0.8 b 0.8 b )

c x a ab

) x ab c c a a b a 0.6 c 0.6 a c a b c b c 0.4 0.4 b b b bc Mortality rate (q Mortality Survivorship (l b 0.2 a 0.2 c a b a a a a a 0.0 0.0 01234567 01234567

Stage Stage

) 5.0 2.5 x c c 4.5 c c c 2.0 4.0 c ) b x 3.5 c 1.5 c 3.0 b b b b c b b a 1.0 b ab 2.5 c a ab a a b ab a a a 2.0 ab a ab a a Killing power (k 0.5 a a a a a a 1.5 a a a future life (e of Expectation 0.0 a 1.0 01234567 01234567 Stage Stage

Fig. 1. Life table statistics of Anastatica hierochuntica populations raised under different water treatments, representing 100, 200, 500 and 1000 mm rainfall. (A) Survivorship curves, (B) Mortality rate, (C) Killing power, and (D) Expectation of future life. The growth stages are: 1 = Sowing, 2 = Emergence, 3 = Seedling, 4 = Juvenile, 5 = Flowering, 6 = Fruiting, 7 = Senescence. Error bars represent standard deviations. Different letters between different water treatments at the same stage indicate significant difference. Figure 1

3. RESULTS ity. Only few individuals in the driest environment were able to complete the life cycle. 3.1. Population dynamics Under the 200 mm treatment, the survivor- ship1 curve matches a Deevey type II model Life tables and fecundity schedules were which is characterized by density dependent constructed for A. hierochuntica plants raised decrease in survivorship during the plant under contrasting simulated rainfall treat- life span. For the highest water treatments, ments to examine the relationships between equivalent to 500 and 1000 mm rainfall, the rainfall, plant size, seed production and po- survivorship curves approach a Deevey type tential persistence of the seed bank through I, with low seedling mortality and sharp de- successive years. In the four water treatments, crease in the final stages of the plant life survivorship values fell from the maximum span, and more than half of the individuals initial value in the seed germination stage surviving to reproduce (c. 70% in the 1000 to a zero value in the senescence stage cor- mm treatment and 53% in the 500 mm treat- responding to the end of the plant life span ment). Individuals of A. hierochuntica raised (Fig. 1A). Under the lowest water treatment, under low water experienced high mortality the survivorship curve matches a Deevey throughout emergence, seedling and juvenile type III model, where seedlings showed high stages. Mortality was steepest under the 100 mortality reflected in the steep early mortal- mm rainfall treatment; percent emergence 498 A. K. Hegazy et al. was greater for greater levels of rainfall, and 3.2. Seed dispersal and expected persistence started with a 25% emergence, reaching 92% under 1000 mm rainfall treatment. During the field monitoring of the seed Stage-specific mortality rates and kill- dispersal over seven years observation, only ing power under the four water treatments skeletons of size-classes 1–6 dispersed all of are shown in the corresponding survivorship their seeds (Fig. 2). The period to complete curves (Fig. 1B and C). All plants had died by the seed dispersal ranged from three years the end of the fruiting stage, as this species is in size-class 1 to seven years for size-class monocarpic. Overall mortality and mortality 6. For the other size-classes (7-to-10) where at all life history stages was greatest in the low complete seed dispersal did not occur during water treatments. Under the high water treat- the seven years of observation, the percent ments, stage-specific mortality ranged from of seeds dispersed during the monitoring 0.02 to 0.16 and the killing power from 0.01 time decreased from 79.7% in size-class 7 to to 2.4. 44.4 % in size-class 10. Generally, the expectation of future life According to the rate of seed dispersal, increased with increasing water supplied the expected life-span of A. hierochuntica (Fig. 1D). Maximum values of ex were ob- populations under different water treatments tained for the 1000 mm treatment, in all decreased gradually towards the end of the growth stages, then values decreased and the seed bank life-time, i.e., the time for complete other water treatments followed the same seed dispersal under the four water treat- trend. Under the 100 mm rainfall treatment, ments (Fig. 3–4). Regarding the duration of ex attained 1.15 in the seed germination stage, living plant life span from seed sowing to while in the emergence stage reached 2.16. senescence (real life span) and the expected For the fruiting stage, the reproductive seed bank life-time needed for complete seed value (Vx) and reproductive rate (lxbx) in- dispersal (expected life span), a significant creased with increase in water availability, as extension of the life span is expected where did the mean number of seeds per individual the dead skeletons provide seeds each season (bx) (Table 2). Extremely low values of Vx and according to the amount of rainfall. While the lxbx were recorded under the lowest water real life-span did not extend more than 149 treatment, as compared to the highest values days in the highest water treatment, the pre- recorded under the highest water treatment. dicted life-span may extend for 3, 4, 11 and

Seventh year 100 Sixth year Fiftht year Fourth year Third year 80 Second year First year

40 Seed dispersal (%) Seed dispersal

0 12345678910

Size-class

Fig. 2. Seed dispersal of Anastatica hierochuntica Figureas based 2 on the defined size-classes during seven years of observations. See Table 1 for size-classes volume range in cubic centimeters.

2 Population dynamics of Anastatica hierochuntica 499

17 years under 100, 200, 500 and 1000 mm rainfall, respectively.

4. DISCUSSION

11 4.1 Population dynamics 100 mm 200 mm 9 500 mm Generally, survivorship curves of mono- 7 1000 mm carpic plants follow a Deevey type I curve (Deevey 1947, Baskin and Baskin 1974, 5 Leverich and Levin 1979). However, 3

Deevey type III survivorship curves have also life-time seed bank of ectation p 1 been reported in annuals (Sharitz and Mc- Ex 0 2 4 6 8 10 12 14 16 18 Cormick 1975). A Deevey type III curve Age (years) indicates a sharp mortality during the early growth stages and slow decrease until the fi- Figure 3 nal stages. Survivorship curves and related stage-specific mortality rate and killing power Fig. 3. Projected temporal pattern of seed disper- are not characteristic of a particular species, sal of Anastatica hierochuntica populations raised as these features may vary significantly ac- under different simulated water treatments equiv- cording to habitat conditions and population alent to 100, 200, 500 and 1000 mm rainfall. density (Symonides 1974, 1983, and 1988, value reflects the relatively small proportion Klemow and Raynal 1981, 1983, Beeftink of seeds able to germinate and survive under 1985). Moreover, variation in survivorship 100 mm rainfall treatment. curves of the same species was reported by With regard to the stages of the life span Mack and Pyke (1983) for Bromus tectorum after seedling establishment (the juvenile and in different habitat types. Low water treat- flowering stages), the stage-specific mortality ments (equivalent to 100 and 200 mm rain- and killing power showed the highest values fall) allowed only a small proportion of A. hi- in the juvenile stage, reaching 0.50 and 0.30 erochuntica seeds to germinate and few of the respectively, and lowest values in the flower- seedlings survived to the reproductive and se- ing stage (0.25 and 0.12 respectively). This nescence stages. Survivorship curves of plants suggests juvenile stage is as vulnerable as the raised under low water treatments therefore seedling stage, while plants that reach the followed a Deevey type III curve, while those flowering stage are likely to complete the fi- raised under the high water treatments fol- nal stages of seed production and senescence. lowed a Deevey type I curve, characterized The other treatments produced a similar by low mortality risk until post-reproductive trend, except that the 500 mm rainfall3 treat- senescence. ment showed higher stage-specific mortality The proportion of seeds germinating af- and killing power for seedlings than for juve- ter rain events depends on the quantity of nile plants. water input to the soil (Beatley 1974, Lo- Throughout the plant life cycle, the 500 ria and Noy-Meir 1979/80). Subsequent and 1000 mm rainfall treatments showed survival also increased with increasing water stage-specific mortality and killing power availability (Klemow and Reynal 1981, values that were always lower than those ob- Hegazy and Ismail 1992, Hegazy and Ka- tained under 100 and 200 mm rainfall treat- biel 2010). Likewise, low water treatments ment. The killing power in the fruiting stage showed higher pre-reproductive mortality obviously showed the maximum values, in than high water treatments. This tendency all water treatments, as all plants enter se- was especially marked under 100 mm rain- nescence and die back to form a desiccated fall treatment, where stage-specific mortal- skeleton-ball. ity reached a maximum value of 0.75 in the With higher water availability plants were seed germination stage as compared to 0.08 larger, and produced more seeds. From seed under the 1000 mm rainfall treatment. This germination to flowering the expectation of 500 A. K. Hegazy et al.

in space and time by synchronizing dispersal with rain events (Harper 1977, Baskin and 16 real expected Baskin 1993, Van Oudtshoorn and Van Rooyen 1999). Consequently dispersal and 12 germination can be spread over time (Co- hen 1966). This is shown in A. hierochuntica, 8 where seeds are non-dormant and may germinate within a few hours of dispersal and Age (years) 4 wetting (Friedman et al. 1981, Gutterman 1990, 1993 and 2000). Since the force of rain 0 controls the fruit opening and seed dispersal 100 200 500 1000 (Friedman et al. 1978), the number of dispersed seeds will be directly correlated with Treatment (mm rainfall) the amount of rainfall. Fig. 4. The real and expected life-span of A. hi- As a monocarpic plant, A. hierochuntica erochuntica populations under different simulated individuals senesce after reproducing. The water treatments. presence of a seed bank delays population extinction, compared to populations lacking a future life values rangedFigure from 4 2.12 to 1.54, un- seed bank (Kalisz and McPeek 1993). This der 100 mm rainfall treatment, and from 4.76 “aerial seed bank” of natural populations of to 1.98, under 1000 mm rainfall treatment. A. hierochuntica would be added to each year The 100 mm rainfall treatment showed lower and the seed cohorts would be larger or small- expectation of future life in the seed germi- er, depending on the sizes of the plants in each nation than in the emergence stage, while the successive year, and the rate of disintegration 200 mm rainfall treatment showed approxi- of the dry skeletons in subsequent years’ rain- mately similar values of ex at these stages. fall. In the present work, seed bank persis- The number of seeds produced per in- tence could extend from three years (at the dividual, reproductive rate and reproductive 100 mm rainfall treatment) to about 17 years, value were greatest for plants experiencing at the 1000 mm rainfall treatment (Fig. 4), higher water treatments. Reduced repro- based solely on the size of skeleton-balls and ductive output under water stress has been seed output, which in turn depends on plant observed for other species, e.g., Mott and size. Old dry skeletons of A. hierochuntica, McComb (1975), Loria and Noy-Meir observed by Friedman et al. (1978), were es- (1979/80) and Steyn et al. (1996). The very timated to be more than ten years old. At the low lxbx (0.58) under 100 mm rainfall treat- population level, higher rainfall would gener- ment in the fruiting stage compared to 983.2 ate populations with more, and larger plants, under 1000 mm rainfall treatment indicated a and consequently larger aerial seed banks, low probability of population persistence for which could tide the population over several A. hierochuntica populations under repeated years of drought or low rainfall. Therefore, years of low rainfall conditions. the larger the size-classes comprised within A. hierochuntica populations, the longer the 4.2. Seed dispersal and expected persistence probability of persistence of that population. Two extremes of plant life history strate- Seed dispersal affects local population gy have been described: the r-strategy is seen size and may help in the foundation of new in species with short life span and high seed populations (Silvertown and Lovett- production and the K-strategy where individ- Doust 1993). For many species, selection uals live longer and reproduce several times has favored adaptations that allow dispersal or more over the lifespan (MacArthur and in time as well as space (Cook 1980). Bra- Wilson 1967, Silvertown and Lovett- dispory protects seeds from predation (Ell- Doust 1993). For A. hierochuntica, indi- ner and Shmida 1981). Furthermore, grad- viduals profit from the merits of phenotypic ual seed release from the dispersal structure plasticity enabling both strategies (Hegazy maximizes the chance of seed germination 1990b, Hegazy and Kabiel 2010).

4 Population dynamics of Anastatica hierochuntica 501

5. CONCLUSIONS Beatley J.C. 1974 – Phenological events and their environmental triggers in Mojave desert The presence of an aerial (plant skeleton- – Ecosyst. Ecol. 55: 856–863. ball) seed bank in Anastatica hierochuntica Beeftink W.G. 1985 – Population dynamics allows a cohort of seeds to germinate at dif- of annual Salicornia species in the tidal salt marches of the Oosterschelde, The Nether- ferent times, indeed over several years, in lands – Vegetatio 61: 127–137. an opportunistic manner. Thus, despite the Cohen D. 1966 – Optimizing reproduction in monocarpic life history, overlapping genera- a randomly variable environment – J. Theor. tions (plants from different seed cohorts) can Biol. 12: 119–129. co-exist. The size of the aerial seed bank is re- Cook R. 1980 – The biology of seeds in the soil. duced under conditions of low rainfall. Plant (In: Demography and evolution in plant popu- populations established in the field that expe- lations, Ed. O. T. Solbrig) – Blackwell Sci. Publ. rience several successive years of low rainfall pp: 107–129. will be unlikely to persist, as the plants will be Danin A. 1983 – Desert vegetation of Israel and few, small and likely to produce smaller seed Sinai – Cana Publishing House, Jerusalem, 148 cohorts that will survive fewer years of low pp. Deevey E.S. 1947 – Life tables for natural rainfall. populations of animals – Quart. Rev. Biol. 22: If the experimental plants were taken 283–314. to represent natural populations in sites ex- Ellner S., Shmida A. 1981 – Why are adapta- periencing a range of natural rainfall, plant tions for long-range seed dispersal rare in des- growth and fecundity would be greatest in ert plants? – Oecologia, 51: 133–144. highest rainfall sites, and therefore both the Esler K.J., Cowling R.M., Ivey P. 1992 – seed bank and its longevity would be great- Seed biology of three species of Mesembryan- est there. In reliably wetter conditions each themaceae in the southern Succulent Karoo – year, a greater proportion of seeds is expected South Afr. J. Bot. 58: 343–348. to germinate. The essential element in des- Evenari M. 1949 – Germination inhibitors – ert environment is not just the low average Bot. Rev. 15: 153–194. Evenari M., Shanan L., Tadmor N. 1982 – rainfall, but the highly unpredictable rainfall The Negev. The challenge of a Desert. 2rd edi- from year to year at a given location. There- tion – Cambridge, M.A., Harvard Univ. Press, fore populations that experienced a particu- 345 pp. larly wet year could generate a larger aerial Freas K.E., Kemp R.R. 1983 – Some rela- seed bank, protecting persistence of the pop- tionships between environmental reliability ulation more, through years of subsequent and seed dormancy in desert annual plants drought. – J. Ecol. 71: 211–217. Friedman J., Gunderman N., Ellis M. ACKNOWLEDGEMENTS: We thank the 1978 – Water response of the hygrochastic deanship of scientific research, College of Science skeletons of the true rose of Jericho (Anastati- Research Center, King Saud University for sup- ca hierochuntica L.) – Oecologia, 32: 289–301. porting this publication. Friedman J., Stein Z. 1980 – The influence of seed-dispersal mechanisms on the dispersion of Anastatica hierochuntica (Cruciferae) in the 6. REFERENCES Negev desert, Israel – J. Ecol. 68: 43–50. Friedman J., Stein Z., Rushkin E. 1981 – AlGamdi N., Mullen W., Crozier A. 2011 Drought tolerance of germinating seeds and – Tea prepared from Anastatica hirerochuntica young seedlings of Anastatica hierochuntica L. seeds contains a diversity of antioxidant flavo- – Oecologia, 51: 400–403. noids, chlorogenic acids and phenolic com- Gutterman Y. 1972 – Delayed seed dispersal pounds – Phytochemistry, 72: 248–254. and rapid germination as survival mechanisms Baskin J.M., Baskin C.C. 1974 – Germina- of the desert plant Blepharis persica (Burm.) tion and survival in a population of the winter Kuntze – Oecologia, 10: 145–150. annual Alyssum alyssoides – Can. J. Bot. 52: Gutterman Y. 1990 – Seed dispersal by rain 2439–2445. (Ombrohydrochory) in some of the flowering Baskin J.M., Baskin C.C. 1993 – Annual desert plants in the deserts of Israel and the Si- seed dormancy cycles in two desert winter an- nai Peninsula – Mitt. Inst. Allg. Bot. Hamburg nuals – J. Ecol. 81: 551–556. 22b: 841–852. 502 A. K. Hegazy et al.

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APPENDIX. Life table and fecundity schedule of Anastatica hierochuntica populations, at various growth stages of the life cycle, raised under different water treatments. x = age in days (Mean ± SD), Nx = number of individuals surviving to day x, lx = Survivorship (proportion of original cohort surviving to day x), dx = proportion of original cohort dying during each stage, qx = stage-specific mortality rate, kx = killing power, ex = expectation of future life.

Treatment/Stage x Nx lx dx qx kx ex

100 mm rainfall Seed germination 4.0 ± 1.0 400 1.00 0.75 0.75 0.60 1.54 Emergence 5.0 ± 1.0 100 0.25 0.11 0.44 0.25 2.16 Seedling 7.5 ± 2.5 56 0.14 0.06 0.43 0.24 2.07 Juvenile 10.5 ± 5.5 32 0.08 0.04 0.50 0.30 1.88 Flowering 17.5 ± 2.5 16 0.04 0.01 0.25 0.12 1.75 Fruiting 22.5 ± 7.5 12 0.03 0.03 1.00 1.08 1.00 Senescence 11.0 ± 3.0 0 0.00 – – – – 200 mm rainfall Seed germination 5.0 ± 2.0 400 1.00 0.32 0.32 0.17 3.11 Emergence 6.0 ± 2.0 272 0.68 0.14 0.21 0.10 3.10 Seedling 8.0 ± 1.0 216 0.54 0.14 0.26 0.13 2.65 Juvenile 14.5 ± 6.5 160 0.40 0.12 0.30 0.15 2.23 Flowering 22.0 ± 3.0 112 0.28 0.07 0.25 0.12 1.75 Fruiting 28.5 ± 6.5 84 0.21 0.21 1.00 1.92 1.00 Senescence 10.0 ± 2.0 0 0.00 – – – – 500 mm rainfall Seed germination 6.0 ± 3.0 400 1.00 0.15 0.15 0.07 4.39 Emergence 7.0 ± 3.0 340 0.85 0.07 0.08 0.04 3.99 Seedling 12.5 ± 2.5 312 0.78 0.11 0.14 0.07 3.26 Juvenile 21.0 ± 4.0 268 0.67 0.09 0.13 0.06 2.63 Flowering 25.5 ±3.5 232 0.58 0.07 0.12 0.06 1.88 Fruiting 37.5 ± 7.5 204 0.51 0.51 1.00 2.31 1.00 Senescence 16.0 ± 4.0 0 0.00 – – – – 1000 mm rainfall Seed germination 7.5 ± 4.5 400 1.00 0.08 0.08 0.04 4.76 Emergence 9.0 ± 5.0 368 0.92 0.11 0.12 0.06 4.09 Seedling 15.0 ± 3.0 324 0.81 0.05 0.06 0.03 3.51 Juvenile 27.5 ±8.5 304 0.76 0.12 0.16 0.07 2.67 Flowering 28.5 ± 4.5 256 0.64 0.01 0.02 0.01 1.98 Fruiting 42.5 ± 10.5 252 0.63 0.63 1.00 2.40 1.00 Senescence 19.5 ± 2.5 0 0.00 – – – –