Germination characteristics of Artemisia ordosica(Asteraceae) in relation to ecological restoration innorthern China

Yuanrun Zheng, Glyn M. Rimmington, Yong Gao, Lianhe Jiang, Xuerong Xing,Ping An, Kamal El-Sidding, and Hideyuki Shimizu

Abstract: Artemisia ordosica Krasch. (Asteraceae) is the dominant psammophytic shrub species on the Ordos Plateauof northern China and is used for revegetation of semi-arid areas. Experiments were conducted to determine the effectsof light intensity, constant temperature, alternating temperatures, and water potential on germination to determine whyair-dispersed achenes fail to germinate well in the field. Achenes germinated within a wide alternating temperaturewindow, except under the 5:15 °C (night:day) temperature regime in darkness. Final percent germination (FPG) washigher in darkness than in light at alternating temperature regimes, except under the 20:30 °C (night:day) temperatureregime. Achenes subjected to a range of constant temperatures in the dark had high FPG over 76.8% except at 30 °C(8%). Photosynthetic photon flux densities (PPFD) of 100 and 400 µmol·m–2·s–1 significantly lowered FPG under a10:20 °C (night:day) regime, while at 0–25 µmol·m–2·s–1 PPFD, the FPG was over 92%. Few achenes germinated at–1.4 MPa. The most suitable temperature for germination of achenes placed under water stress was 20 °C. The besttiming for air dispersal is mid-May, so seeds would become covered with sand at a time when temperature and soilmoisture conditions were optimal for germination.

Key words: air dispersal, Artemisia ordosica, hydrothermal time, psammophytes, semi-arid regions, temperature.

Résumé : L’Artemisia ordosica Krasch (Asteraceae) est une espèce arbustive psammophyte dominante sur le plateaud’Ordos, du nord de la Chine, et est utilisé pour revégétaliser les régions semi-arides. Les auteurs ont conduit des es-sais pour déterminer les effets de l’intensité lumineuse, de températures constantes, de températures alternées et du po-tentiel hydrique, sur la germination, afin de déterminer pourquoi les achènes dispersés par le vent, ne germent pas bienaux champs. Les achènes peuvent germer sous une large gamme de températures, sauf à 5:15 °C à l’obscurité. Lepourcentage final de germination (FPG) est plus élevé à l’obscurité qu’à la lumière, avec des régimes de températuresalternées, sauf à 20:30 °C. Les achènes soumis à une gamme de températures constantes, à l’obscurité, montrent unFPG élevé de 76,8 %, sauf à 30 °C (8 %). Les densités de flux de photons photosynthétiques (PPFD) de 100 et400 µmol·m–2·s–1 diminuent significativement le FPG sous un régime de 10:20 °C, alors qu’avec des PPFD de 0 à25 µmol·m–2·s–1, le FPG est supérieur à 92 %. Peu d’achènes germent à –1,4 MPa. La température la plus favorablepour les achènes soumis au stress hydrique est de 20 °C. Le meilleur moment pour la dispersion des achènes est versla mi-mai, ainsi les graines devraient être recouvertes de sable, à un moment où les conditions de température etd’humidité du sol sont optimales pour la germination.

Mots clés : dispersion par le vent, Artemisia ordosica, temps hydrothermique, psammophytes, régions semi-arides, tem-pérature.

[Traduit par la Rédaction]

Zheng et al. 1028

1021

Can. J. Bot. 83: 1021–1028 (2005) doi: 10.1139/B05-059 © 2005 NRC Canada

Received 22 February 2005. Published on the NRC Research Press Web site at http://canjbot.nrc.ca on 26 September 2005.

Y. Zheng.1 Laboratory of Quantitative Vegetation Ecology, Institute of Botany, Chinese Academy of Sciences, No. 20 XiangshanNanxin Cun, Beijing, 100093, China, and National Institute for Environmental Studies, Tsukuba, 305-8506, Japan.G.M. Rimmington. Office of Global Learning, Wichita State University, Wichita, KS 67260-0013, USA.Y. Gao. Inner Mongolia Agricultural University, Hohhot, 010018, China.L. Jiang and X. Xing. Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China.P. An. Arid Land Research Center, Tottori University 1390 Hamasaka, Tottori, 680-0001, Japan.K. El-Sidding. Agricultural Research Corporation, P.O. Box 126, Wad Medani, Sudan.H. Shimizu. National Institute for Environmental Studies, Tsukuba, 305-8506, Japan.

1Corresponding author (e-mail: zhengyuanrun@hotmail.com).

Introduction

Artemisia ordosica Krasch. is regarded as the most impor-tant and dominant shrub species in Ordos Plateau, northernChina. It is widely used for combating desertification, espe-cially by dispersal of seeds by airplanes (air dispersal), insemi-arid area of China (Zhang 1994). In theory, this is aneffective method for vegetation restoration (Qi 1998). How-ever, there are some problems, because seedling recruitmentfrom achenes was lower than expected (based on laboratorygermination percentages) after conducting air dispersal (Wen1992), and factors responsible for this are still unclear. Sinceair dispersal usually is conducted in June, there may beproblems with temperatures being too high on the sand sur-face and (or) soil moisture being too low to promote germi-nation. Also, the effects of burial by sand on germination arenot known. Thus, it is necessary to explain the behavior ofachenes during germination to improve technologies of airdispersal.

Seed germination is a complex physiological process thatis affected by many environmental signals, including tem-perature, water potential, light, and other factors (Bewleyand Black 1994). Over the last century, many studies onseed germination responses have been conducted under con-trolled environmental conditions. A primary influence onseed germination seems to be temperature, which affectsboth the capacity for germination by regulating dormancyand the speed of germination (Gummerson 1986; Finch-Savage and Phelps 1993; Dahal and Bradford 1994; Trudgillet al. 2000; Alvarado and Bradford 2002). Alternating dayand night temperatures is associated with improved germina-tion in a number of species (Okusanya 1977; Gul and Weber1999; Gulzar and Khan 2001). Alternating and constant tem-perature have different effects on germination (Garcia-Huidobro et al. 1982; Thompson and Grime 1983; Washitaniand Takenaka 1984; Ghersa et al. 1992).

Light is another important regulatory environmental signalin the life cycle of desert plants and their seed germination(Gutterman 1993). The requirement for light is probably agenetic characteristic and may be mediated by phytochrome(Jones and Hall 1979), which, when active, can stimulate thesynthesis of growth-promoting substances that initiate ger-mination (Okusanya and Ungar 1983; Gul and Weber 1999).Light alone in some species controls germination, whereasin others it operates in combination with temperature(Kyereh et al. 1999).

Finally, water stress plays a key role in germination. Highmolecular weight polyethylene glycol (e.g., PEG 6000) doesnot penetrate the cell wall and is therefore inert (Redmann1974; Carpita et al. 1979; Hardegree and Emmerich 1990).Use of PEG provides an ideal method for studying the effectof water stress on germination (Choinski and Tuohy 1991;Geraldine and Lisa 1999). Water potential interacts withtemperature during germination, and some equations to re-flect this relationship have been derived by Lafond andBaker (1986), Romo and Haferkamp (1987), Finch-Savageand Phelps (1993), and Finch-Savage et al. (2001).

Since achenes of A. ordosica dispersed from airplanes insemi-arid areas of China do not germinate well, it is impor-tant to better understand the interaction between tempera-ture, light, and water potential on the germination of

A. ordosica achenes. However, there is little informationavailable on the interaction among temperature, light, andwater potential on the germination of A. ordosica. Huangand Gutterman (2000) described germination strategies ofA. ordosica and concluded that achenes can germinate wellunder light but not in dark. Field observations of achenesfollowing air dispersal revealed good germination under alayer of sand at specific temperatures, and poor germinationon the sand surface (Wen 1992). In addition, Huang andGutterman (2000) reported that the higher the sand moisturecontent, from 1.7% to 14.7%, the higher and earlier the ger-mination; while for 19.4% or higher moisture content, ger-mination and emergence were delayed. Finally, they madeno recommendations for using achenes of this species invegetation rehabilitation. The aims of the present study wereto determine the germination response of A. ordosicaachenes to various alternating and constant temperatures inthe dark and (or) under light, different light intensities underspecific alternating temperature regimes, and different waterpotentials. This information may help in understanding therecruitment and performance of A. ordosica in natural eco-systems and in the restoration process.

Materials and methods

Achenes of A. ordosica Krasch. mature in the end of au-tumn and are dispersed by wind. Germination mostly takesplace in spring. In this study, achenes were collected at theMu Us sandy land (37°27′–39°22′N, 107°20′–111°30′E), P.R.China on 20–25 October 2001. This area has an annualmean precipitation and annual mean temperature of 345.2mm and 6.7 °C, respectively (Fig. 1) (Zhang 1994). Acheneswere collected randomly from the whole population to getan adequate representation of genetic diversity. The col-lected achenes were transported to Japan, and stored at 4 °Cuntil used. The experiments were conducted in Japan in2003.

Soil temperature and moisture from different layers weremeasured in Ordos Sandland Ecological Station, ChineseAcademy of Sciences (39°20′N, 109°53′E), in Mu Us sandyland. The maximum and minimum temperatures at the sandsurface and at 5, 10, and 30 cm depth were recorded dailywith a thermometer. Temperatures were monitored from

© 2005 NRC Canada

1022 Can. J. Bot. Vol. 83, 2005

Precipitation (mm)

Prec

ipita

tion

(mm

)

Temperature ( C)°

Tem

pera

ture

(C

)°

Month

Jan

Feb

Mar

Apr

May Jun

Jul

Aug Sep

Oct

Nov

Dec

Fig. 1. Annual mean precipitation and annual mean temperature(mean from 1969 to 1999) in Mu Us sandy land, north China.

1983 to 2003. Soil moisture was measured in early, middle,and late June each year over a 3-year period (2000–2002).Soil samples for measuring soil moisture were obtained us-ing a stainless steel cylinder, 10 cm in length and 8 cm in di-ameter, which was pushed into the soil. Then soil samplesfrom different layers (0.5, 1, 1.5, 2, 3, 4, 5, 6, 7 cm depth)were carefully extracted and immediately weighed (wetmass) using an electronic balance (Mettler PM4600, MettlerInstrument AG, Germany). Next, the soil samples were driedin an oven at 80 °C for 3 d, and their masses (dry mass)were measured again. Finally, gravimetric soil moisture wasderived as follows: (wet mass – dry mass)/(dry mass) × 100(Table 1). For both soil moisture and temperature, five repli-cates were collected on each sampling occasion.

Germination experiments were carried out within auto-matic temperature- and light-controlled growth chambers(Koito Industries Ltd., Yokohama, Japan). The chamberswere set for daily photoperiods of 14 h : 10 h (day:night, re-spectively) using cool white fluorescent lights.

In all experiments, achenes were surface-sterilized for 1min with 0.52% sodium hypochlorite solution, and thenrinsed several times with distilled water to avoid fungus at-tack (Khan and Ungar 1984). Next, achenes were put onthreefold filter paper (Toyo, No. 1) on 90 mm × 15 mm Petridishes. The filter paper was moistened with distilled wateror a solution of PEG-6000, and about half of the achenemass was immersed in the solution (Tobe et al. 2000). Afully randomized factorial design was used in the germina-tion tests. Each treatment had five replicates, and for eachreplicate, 25 randomly selected achenes were used (Gul andWeber 1999).

Achenes were placed under a photosynthetic photon fluxdensity (PPFD) of 9.8 µmol·m–2·s–1 (measured at the top ofthe Petri dish) and inspected daily; they were consideredgerminated if radicles emerged. Germinated achenes werediscarded after counting. The tests continued until germina-tion percentage became almost steady (Tobe et al. 2000;Zheng et al. 2004).

Germination was calculated using two indices: final per-cent germination (FPG) and germination rate (GR). TheFPG is defined as the percentage of achenes germinated.The GR is estimated with a modified Rozema (1975) index,

100Gnt

i

i∑ , where n is the number of achenes used in an ex-

periment, and Gi is the number of new achenes germinatedon day ti (ti = 0, 1, 2, 3…). Higher values represent rapidgermination.

Arcsine square root transformation was used to ensure ho-mogeneity of variance for FPG data (Gulzar and Khan2001). Values of GR were not transformed, because they metthe homogeneity of variance requirement. The transformed

values of FPG and untransformed data for GR were ana-lyzed using two-way or one-way analysis of variance(ANOVA) procedures. Differences between mean values fortreatments were tested by Tukey’s test. All statistical analy-ses, including test for homogeneity of variance, were per-formed using the SPSS 10.0 package (SPSS 2000). Thehydrothermal time model was used to understand the physio-logical processes occurring during germination for experi-ment 3. The concept of hydrothermal time was proposed byGummerson (1986), further developed by Bradford (1990),and has been used by Bauer et al. (1998); Kebreab andMurdoch (1999); Alvarado and Bradford (2002); Bradford(2002), and Allen (2003). The hydrothermal time model isdescribed by the following equation:

θHT = (T – Tb)(Ψ – Ψb(g))tg

where θHT is the hydrothermal time (MPa·°C·d) required forthe fraction g of achenes to germinate, T and Ψ are tempera-ture and water potential of the incubation medium, respec-tively, Tb is the theoretical base temperature, at or belowwhich germination will not occur, Ψb(g) is the theoreticalbase water potential at or below which germination of thefraction g will not occur, and tg is the time elapsed for whenfraction g of achenes have germinated (Kebreab andMurdoch 1999; Bradford 2002). We assumed that the effectof temperature could be treated as suboptimal and thereforenot require further elaboration of the above formula forsuperoptimal conditions (Alvarado and Bradford 2002). Wefollowed the Bradford method (Bradford 2002) to calculateall parameters of hydrothermal time for A. ordosica achenes.

Three experiments were conducted to examine some ofthe major germination requirements of A. ordosica.

Experiment 1: Effects of alternating temperatureregimes on germination under a specific light intensityor in the dark

The effects of temperature on germination were deter-mined using five alternating temperature regimes, including5:15, 10:20, 15:25, 20:30, and 25:35 °C (night:day) in a ran-domized complete block design. The five temperature re-gimes closely approximate the spring and summergermination conditions in semi-arid areas in China, based on30 years of observations of microenvironments (Qi 1998).Two levels of PPFD were applied, namely 215 µmol·m–2·s–1

for photoperiods of 0 and 14 h.

Experiment 2: Effects of photosynthetic photon fluxdensity on germination

The PPFD levels included 0 (dark), 25, 100, and400 µmol·m–2·s–1, with a 10:20 °C temperature regime. ThePPFD was adjusted by wrapping the outside of plastic ger-

© 2005 NRC Canada

Zheng et al. 1023

Depth of soil (cm)

0.5 1.0 1.5 2.0 3.0 4.0 5.0 6.0 7.0

Soil water content 0.87 1.50 1.96 2.17 2.39 2.57 2.63 2.66 2.75SE 0.03 0.06 0.07 0.07 0.05 0.11 0.12 0.15 0.11

Note: Values are means of five replicates.

Table 1. Gravimetric soil water content (g water·(100 g dry soil)–1) at different layers in shiftingdune in Mu Us sandy land in early June.

mination boxes with layers of white and black plastic nets.Black boxes were used to provide completely dark environ-ments. Achenes at each PPFD were generally checked daily.For the dark treatment, achenes were only inspected on thelast day. Achenes in the light treatments were moved to darkboxes after percentage of germination became steady, andwere finally checked 1 week later.

Experiment 3: Effects of water potential andtemperature on germination

Achenes were moistened using solutions of PEG-6000with known water potentials (θW). The PEG solutions wereprepared according to the methods of Tobe et al. (2000).About two thirds (by volume) of the water or solution ineach Petri dish were replaced daily to avoid a significantchange in the θW of the solution (Tobe et al. 2000). The wa-ter potentials were ostensibly set to 0, –0.2, –0.4, –0.6, –0.8,–1.0, –1.2, –1.4, –1.6, –1.8, and –2.0 MPa. All experimentswere performed in constant darkness, and five constant tem-perature regimes were used, including 10, 15, 20, 25, and30 °C.

Results

Effects of alternating temperature regimes ongermination under a specific light intensity or in thedark

Final percent germination of A. ordosica varied signifi-cantly with temperature, light, and their interaction (Table 2;Fig. 2A). In the dark, FPG was higher (over 85%) and didnot show significant variance with temperature except under5:15 °C, when the lowest value of 29.6% occurred. In con-trast, FPG increased with temperatures until 20:30 °C andthen declined under light. There were significant differencesbetween FPGs under light and dark for all temperature re-gimes except 20:30 °C. FPG was lowest under 5:15 °C bothin the dark and under light (Fig. 2A).

The effects of temperature and light on GR largely paral-leled those on FPG, except that the difference for GR wasmuch higher than that of FPG between light and dark(Fig. 2C).

Achenes subjected to constant temperature in the dark hadan FPG of over 76.8%, except at 30 °C when it was 8%.

Both FPG and GR data were measured for a water potentialof 0 MPa in experiment 3. Germination did not decline sig-nificantly with temperature, except at 30 °C (Fig. 2B). Atemperature regime of 10–25 °C appeared to be favourablefor germination with the optimum being 20 °C (Fig. 2D).

Effects of photosynthetic photon flux density ongermination

There were significant differences among FPG values un-der different PPFD levels and in the dark. FPGs were high-est and similar in the dark and at 25 µmol·m–2·s–1 PPFD(92%), and an increase in PPFD caused a reduction in FPG;the values at 100 and 400 µmol·m–2·s–1 were not signifi-cantly different (Table 3). When achenes were moved into adark environment, the FPG was not significantly differentfrom that for achenes continuously in the dark (Fig. 3A).

The germination rate of A. ordosica declined significantlywith increasing PPFD (Fig. 3B).

Effects of water potential and temperature ongermination

Final percent germination of A. ordosica increased signifi-cantly with increasing temperature, up to 25 °C, and de-creased significantly with decreasing water potential, andvaried in response to their interaction (Table 2). It washigher in distilled water (0 MPa) at all temperature regimesexcept 30 °C. Few achenes germinated at or below –1.4MPa. Final percent germination was lowest at 10 °C and30 °C, moderately high at 15 °C and 25 °C, and was optimalat 20 °C (Table 4). The germination process of achenes ofA. ordosica was well described by the hydrothermal timemodel with an R2 of 0.82 (P < 0.001). The parameters of Tb,θHT, and σΨb are 0 °C, 53 MPa·°C·d, and 0.32 MPa,respectively. Ψb(50) at 10, 15, 20, and 25 °C are –0.73, –0.89,–1.01, and –0.78 MPa, respectively.

The responses to water potential and temperature of GRparalleled those of FPG.

Discussion

Agami (1986) reported that seed germination ofZygophyllum dumosum was independent of temperaturewithin the range of 10–25 °C, but strongly inhibited at 30and 35 °C. Our results exhibited a similar pattern at constanttemperature. When considering the effect of temperature andlight, there was a wider temperature window for germinationof A. ordosica in the dark than that under light. Seeds usu-ally exhibit a base or minimum temperature for germination(Tb) and an optimal temperature at which germination ismost rapid (To), and a maximum or ceiling temperature atwhich germination is prevented (Tc) (Alvarado and Bradford2002). Cluff et al. (1983) reported that a temperature regimeof 10:40 °C (16:8 h) is optimal for seed germination ofDistichlis spicata, whereas –5 and 50 °C are the lower andupper threshold temperatures for seed germination. For ourexperiment, the base temperature was 0 °C, which was inagreement with the results for temperate species accordingto Allen et al. (2000).

Diurnal fluctuations in temperature may be favorable forseed germination (Warington 1936; Thompson 1974). Ourresults revealed that FPG was not significantly different be-

© 2005 NRC Canada

1024 Can. J. Bot. Vol. 83, 2005

Dependent variables

ExperimentsIndependentvariables df % germination

Germinationrate

1 L 1 145.47*** 484.39***TA 4 101.03*** 90.73***L × TA 4 10.30*** 26.23***

3 WP 10 281.12*** 542.29***TC 4 73.66*** 416.81***WP × TC 40 60.13*** 44.07***

Note: 1, effects of light (L), alternating temperatures (TA), and theircombinations (L × TA); 3, effects of constant temperature (TC), water po-tential (WP), and their interaction (TC × WP). Values are means of fivereplicates. ***, significantly different at P < 0.001.

Table 2. F values obtained by a two-way ANOVA for final per-cent germination and germination rate of Artemisia ordosica inrelation to different factors in different experiments.

tween 10:20 °C and 25:35 °C and for the constant tempera-ture of 10–25 °C in the dark.

Light is an important factor for achene germination(Baskin and Baskin 1995; Benvenuti 1995). Baskin andBaskin (1995) determined that out of 41 species, germina-tion is promoted by light in 20 species, by darkness in 10,and had no effect in 11 species. Germination in Salicorniapacifica var. utahensis is 50% lower in the dark than in thelight (Khan and Weber 1986). For Triglochin bulsbosa andTriglochin striata germination in the dark is only 10%,whereas that in the light is 90% (Naidoo and Naicker 1992).For A. ordosica, our results showed that germination wassignificantly lower under light than under dark and nearlydark (25 µmol·m–2·s–1) conditions at 10:20 °C. This is inagreement with an air seeding experiment by Wen (1992),but not with the findings of Hang and Gutterman (2000).The causes for this difference are not certain, but the follow-ing might be considered. The requirement for light is ge-netic, but can be modified by the environment in which theseeds develop on the parent plant. Thus, differences between

our data and those of Huang and Gutterman (2000) may bedue to differences in maternal environment, collection tim-ing, or storage conditions. All of these need to be clarified infuture studies. Further, most Artemisia species have freshseeds with minor physiological dormancy, which can be bro-ken by a short period at low temperature (4–5 °C) undermoist conditions. Seeds also will be released from dormancywhen stored in dry conditions at 4 or 5 °C for severalmonths (Gutterman 1993; Baskin and Baskin 1995). Thus,when working with A. ordosica, care must be exercised toensure that the seeds are released from dormancy, especiallybefore air seeding.

The FPG decreases with decreasing soil water potential,and each of the species appears to have its own thresholdwater potential below which germination does not occur(Fyfield and Gregory 1989). In general, researchers haveconcluded that water stress is inhibitory to seed germinationin two ways: (i) preventing germination process at or belowa critical soil water potential for the species; and (ii) delay-ing the germination at higher, but still unfavorable, soil wa-

© 2005 NRC Canada

Zheng et al. 1025

ab

ce

cde

b

cd d d d

0

20

40

60

80

100

5:15 10:20 15:25 20:30 25:35

Alternating temperature (ºC)

Light

Dark

Darka

bc cab

d

0

20

40

60

80

100

10 15 20 25 30

Constant temperature (ºC)

bddbd

aa

c

ee

c

ab

0

5

10

15

20

25

30

5:15 10:20 15:25 20:30 25:35

LightDark

Dark

d

b

c

b

a

0

5

10

15

20

25

30

10 15 20 25 30

Ger

min

atio

n ra

te

Ger

min

atio

n ra

te

Fina

l per

cent

ger

min

atio

n

Fina

l per

cent

ger

min

atio

n

Alternating temperature (ºC) Constant temperature (ºC)

(A) (B)

(D)(C)

Fig. 2. Final percent germinations (±SE) (A) and germination rates (±SE) (C) of Artemisia ordosica in a given photosynthetic photonflux density (215 µmol·m–2·s–1, 14 h light per day) and in the dark under alternating temperature (5:15, 10:20, 15:25, 20:30, and25:35 °C (night:day)) regimes; and final percent germinations (±SE) (B) and germination rates (±SE) (D) in the dark under constanttemperature (10, 15, 20, 25, and 30 °C) regimes. Each bar represents the mean of five replicates; bars with different letters are signifi-cantly different from each other at P < 0.05 (Tukey test).

ter potentials (Ungar 1995). Germination of Allenrolfeaoccidentalis seeds occurs at soil water potentials of –4 MPa(Blank et al. 1994), and seeds germinate readily over a widerange of constant and alternating temperatures, but warmer

temperatures are more favorable (Young et al. 1995). Ac-cording to our results, FPG tended toward zero at the highesttemperature (30 °C), and interaction between high tempera-ture and lower water potential (drought) had serious effectson germination. This conclusion is in agreement with studiescited above. As concluded by Allen et al. (2000),psammophytes are characterized by high Ψb(50), low θHT,and intermediate to low σΨb values. Artemisia ordosica ismainly distributed in sandy areas in northern China, so it isnot surprising that its values of Ψb(50), θHT, and σΨb are sim-ilar to those values of temperate psammophytes such asArtemisia cana (Allen et al. 2000) (θHT = 43 MPa·°C·dand σΨb = 0.34 MPa, and Ψb(50)T=10 = –0.86 MPa andΨb(50)T=20 = –0.99 MPa).

The characteristics of achenes germination at various tem-peratures in dark and light indicated that they could be dis-persed from mid-spring to early autumn in the field, whenthey would be covered by windblown sand. In general, ifachenes germinate at depths between 2 and 6 cm, the seed-lings may still emerge (Maun and Lapierre 1986). ForA. ordosica, the maximum depth from which seedlings areable to emerge was reported to be 3 cm, although manyseeds may be as deep as about 20 cm (Wen 1992). Based on20-year microenvironment observations in Mu Us sandyland, the average daily minimum and maximum tempera-tures in early June were 14.5 and 54.1 °C, respectively, atthe surface of sandy dunes, and reduced to 13.4 and 27.9 °Cat 5 cm depth. It is obvious that achenes at 1–3 cm depth ex-perience temperatures somewhere between those at the soilsurface and at 5 cm, which are more suitable for germina-tion.

It is therefore recommended that achenes should be dis-persed when they are most likely to be covered bywindblown sand in mid-spring to early autumn. High valuesof final percent germination after 49 d (our test experimentfor germinability) indicated that achenes could remain viablelong enough for suitable moisture conditions. This meansthat A. ordosica achenes should be dispersed earlier so thatthey germinate, when they encounter suitable conditions.

In the study area, the soil water content at a depth of 3 cmis usually less than 2.5%, and 1% at the surface (Table 1),which translates to a soil water potential lower than –1.0MPa at 3 cm depth (Slatyer 1967). This indicates coverageof achenes by windblown sand improves soil water contentand increases the probability of reaching suitable soil waterconditions after rain.

Our results indicated a variety of germination responses.From these it can be concluded that vegetation restoration is

© 2005 NRC Canada

1026 Can. J. Bot. Vol. 83, 2005

PPFD (µmol·m–2·s–1)Final %germination

Recovery final% germination Germination rate

Dark 92.0±2.1b25 92.8±1.5b 95.2±2.0b 9.9±0.8b100 63.2±6.6a 94.4±1.6b 5.2±0.7ab400 46.4±5.1a 97.6±1.6b 3.7±0.4a

Note: Achenes were exposed to three PPFD levels (25, 100, 400 µmol·m–2·s–1, 14 h light per day) and darkat 10:20 °C. Values are means ± SE for five replicates. Within a column, values that are followed by differentletters are significantly different at P < 0.05 (Tukey test).

Table 3. Results of multivariable comparison of light effects on final percent germination, recov-ery final percent germination, and germination rate of Artemisia ordosica.

Time (day)

PPFD ( mol·m ·s )µ –2 –1

Ger

min

atio

n ra

tePe

rcen

t ger

min

atio

n

Fig. 3. The effect of photosynthetic photon flux density (PPFD;25, 100, or 400 µmol·m–2·s–1) at 10:20 °C (night:day) on thepercent germination (±SE) over time (A) and on germination rate(±SE) (B) of Artemisia ordosica. Each point represents the meanof five replicates.

© 2005 NRC Canada

Zheng et al. 1027

best conducted at particular times when desert conditionswere more favourable. Germination of A. ordosica achenesrequires an absence of light, associated with coverage bywindblown sand, suitable temperature, and moist soil. Thiscan occur from late spring to early autumn, when achenesare covered by sands, and rainfall coincides with suitabletemperature in June, July, and August in the Mu Us sandyland of China. However, in that area, the frost-free period isusually short (120 d). To protect seedlings from frost dam-age, it is best if achenes germinate in early summer. Becauseachenes of A. ordosica can remain viable for a long time,they should be dispersed by airplane in mid-May rather thanin early June, as is the current practice. This procedure willincrease the likelihood of achenes being covered with sandby prevailing strong wind in that area in spring and subse-quently being exposed to favourable soil water and tempera-ture conditions. This will enable achenes to germinaterapidly, and undergo a longer period for seedling growth andestablishment so they are stronger, and more resistant tofrost in the following winter.

Acknowledgments

The authors thank the Fund for Field Station in Resourceand Environment Fields, Chinese Academy of Sciences, theFund of the President of the Chinese Academy of Sciences,and the National Key Basic Research Program(G2000018600) for their support in collecting achenes inChina. The authors greatly appreciate Professor B. Downiefor insightful comments and careful editing of this paper,Professor K.J. Bradford for kindly supplying several papersrelated to applications of hydrothermal time model, and Dr.D.W. Still for kindly donating his own SAS program forhydrotime analysis and for many suggestions for using thismodel. The authors also thank the Association of Interna-tional Research Initiatives for Environmental Studies, Japan,for funding this research, and the National Institute for Envi-ronment Studies for providing equipment essential for thisstudy.

References

Agami, M. 1986. The effects of different soil water potentials, tem-perature and salinity on germination of seeds of the desert shrubZygophyllum dumosum. Physiol. Plant. 67: 305–309.

Allen, P.S. 2003. When and how many? Hydrothermal models andthe prediction of seed germination. New Phytol. 158: 1–9.

Allen, P.S, Meyer, S.E., and Khan, M.A. 2000. Hydrothermal timeas a tool in comparative germination studies. In Seed biology:advance and applications. Edited by M. Black, K.J. Bradford,and J. Vázquez-Ramos. CAB International, Cambridge Univer-sity Press, Wallingford. pp. 401–410.

Alvarado, V., and Bradford, K.J. 2002. A hydrothermal time modelexplains the cardinal temperatures for seed germination. PlantCell Environ. 25: 1061–1069.

Baskin, C.C., and Baskin, J.M. 1995. Dormancy types and dor-mancy-breaking and germination requirements in seeds ofhalophytes. In Biology of salt tolerant plants. Edited by M.A.Khan and I.A. Ungar. Department of Botany, University ofKarachi, Karachi, Pakistan. pp. 23–30.

Bauer, M.C., Meyer, S.E., and Allen, P.S. 1998. A simulationmodel to predict seed dormancy loss in the field for Bromustectorum L. J. Exp. Bot. 49: 1235–1244.

Benvenuti, S. 1995. Soil light penetration and dormancy ofjimsonweed (Dtura stramonium) seeds. Weed Sci. 43: 389–393.

Bewley, J.D., and Black, M. 1994. Seeds: Physiology of develop-ment and germination. Plenum Press, London.

Blank, R.R., Young, J.A., Martens, E., and Palmquist, D.E. 1994.Influence of temperature and osmotic potential on germinationof Allenrolfea Occidentalis seeds. J. Arid Environ. 26: 339–347.

Bradford, K.J. 1990. A water relations analysis of seed germina-tion rates. Plant Physiol. 94: 840–849.

Bradford, K.J. 2002. Applications of hydrothermal time to quanti-fying and modeling seed germination and dormancy. Weed Sci.50: 248–260.

Carpita, N., Sabularrse, D., Montezinos, D., and Delmer, D.H.1979. Determination of the pore size of cell walls of living plantcells. Science (Washington, D.C.), 205: 1144–1147.

Choinski, J.S., and Tuohy, J.M. 1991. Effect of water potential andtemperature on the germination of four species of African sa-vanna trees. Ann. Bot. (London), 68: 227–233.

Cluff, G.J., Evans, R.A., and Young, J.A. 1983. Desert salt grass

Water potential (MPa) 10 °C 15 °C 20 °C 25 °C 30 °C

0.0 76.8±4.1a 95.2±1.5a 96.8±1.5a 83.2±2.0a 8.0±3.3a–0.2 52.8±2.7b 87.2±4.8ab 94.4±2.0a 80.0±5.2a 16.0±1.3b–0.4 40.0±2.2c 79.2±5.3b 92.8±2.7a 76.8±6.1a 2.4±1.6ac–0.6 24.0±2.2d 76.0±3.3bc 87.2±3.4a 55.2±7.3b 1.6±1.0c–0.8 7.2±2.3e 60.0±3.3c 68.8±3.9b 25.6±5.5c 0.0±0.0c–1.0 1.6±1.0f 35.2±6.0d 48.8±2.9b 37.6±2.7bc 0.0±0.0c–1.2 0.0±0.0f 8.8±2.3e 24.0±2.5c 9.6±2.0d 0.0±0.0c–1.4 0.0±0.0f 0.8±0.8f 8.8±3.4d 0.8±0.8e 0.0±0.0c–1.6 0.8±0.8f 0.0±0.0f 0.0±0.0e 1.6±1.0e 0.0±0.0c–1.8 0.0±0.0f 0.0±0.0f 0.0±0.0e 0.0±0.0e 0.0±0.0c–2.0 0.0±0.0f 0.0±0.0f 0.0±0.0e 0.0±0.0e 0.0±0.0c

Note: Achenes were exposed to 11 different water potentials (0, –0.2, –0.4, –0.6, –0.8, –1.0, –1.2, –1.4, –1.6, –1.8, –2.0 MPa) under five constant temperature (10, 15, 20, 25, and 30 °C) regimes in the dark. Valuesare means ± SE for five replicates. Within a column, different letters indicate significantly different final per-cent germinations between different water potentials under the same temperature treatments at P < 0.05 (Tukeytest).

Table 4. Results of multivariable comparison of temperature and water potential effects on finalpercent germination of Artemisia ordosica.

seed germination and seedbed ecology. J. Range Manage. 36:419–422.

Dahal, P., and Bradford, K.J. 1994. Hydrothermal time analysis oftomato seed germination at suboptimal temperature and reducedwater potential. Seed Sci. Res. 4: 71–80.

Finch-Savage, V.E., and Phelps, K. 1993. Onion (Alium cepa)seedling emergence patterns can be explained by the influenceof soil temperature and water potential on seed germination. J.Exp. Bot. 44: 407–414.

Finch-Savage, V.E., Phelps, K., Steckel, J.R.A., Whalley, W.R.,and Rowse, H.R. 2001. Seed reserve-dependent growth re-sponses to temperature and water potential in carrot (Daucuscarota). J. Exp. Bot. 52: 2187–2197.

Fyfield, T.P., and Gregory, P.J. 1989. Effects of temperature andwater potential on germination, radical elongation and emer-gence of mungbean. J. Exp. Bot. 40: 667–674.

Garcia-Huidobro, J., Monteith, J.L., and Squire, G.R. 1982. Time,temperature and germination of pearl millet. I. Constant temper-ature. J. Exp. Bot. 33: 287–295.

Geraldine, L.D., and Lisa, A.D. 1999. Water potential and ionic ef-fects on germination and seedling growth of two cold desertshrubs. Am. J. Bot. 86: 1146–1153.

Ghersa, C.M., Arnold, R.L.B., and Martinezghersa, M.A. 1992.The role of fluctuating temperatures in germination and estab-lishment of sorghum-halepense regulation of germination at in-creasing depths. Funct. Ecol. 6: 460–468.

Gul, B., and Weber, D.J. 1999. Effects of salinity, light and temper-ature on germination in Allenrolfea occidentalis. Can. J. Bot. 77:240–246.

Gulzar, S., and Khan, M.A. 2001. Seed germination of halophyticgrass Aeluropus lagopoides. Ann. Bot. (London), 87: 319–324.

Gummerson, R.J. 1986. The effects of constant temperatures andosmotic potentials on the germination of sugar beet. J. Exp. Bot.37: 729–741.

Gutterman, Y. 1993. Seed germination of desert plants. Springer-Verlag, Berlin.

Hardegree, S.P., and Emmerich, W.E. 1990. Partitioning water po-tential and specific salt effect on seed germination of fourgrasses. Ann. Bot. (London), 66: 585–587.

Huang, Z.Y., and Gutterman, Y. 2000. Comparison of germinationstrategies of Artemisia ordosica with its two congeners fromdeserts of China and Israel. Acta Bot. Sin. 42: 71–80.

Jones, I.F., and Hall, M.A. 1979. Studies on the seed requirementfor carbon dioxide and ethylene for germination of Spergulaarvensis seeds. Plant Sci. Lett. 16: 87–93.

Kebreab, E., and Murdoch, A.J. 1999. Modelling the effects of wa-ter stress and temperature on germination rate of Orobancheaegyptiaca seeds. J. Exp. Bot. 50: 655–664.

Khan, M.A., and Ungar, I.A. 1984. The effects of salinity and tem-perature on the germination of polymorphic seeds and growth ofAtriplex triangularis Willd. Am. J. Bot. 71: 481–489.

Khan, M.A., and Weber, D.J. 1986. Factors influencing seed ger-mination in Salicornia pacifica var. utahensis. Am. J. Bot. 73:1163–1167.

Kyereh, B., Swaine, M.D., and Thompson, J. 1999. Effect of lighton the germination of forest trees in Ghana. J. Ecol. 87: 772–783.

Lafond, G.P., and Baker, R.J. 1986. Effects of temperature, mois-ture stress and seed size on germination of nine spring wheatcultivars. Crop Sci. 26: 563–567.

Maun, M.A., and Lapierre, J. 1986. Effects of burial by sand onseed germination and seedling emergence of four dune species.Am. J. Bot. 73: 450–455.

Naidoo, G., and Naicker, K. 1992. Seed germination in the coastalhalophytes Triglochin bulbosa and Triglochin striata. AquaticBot. 42: 217–229.

Okusanya, O.T. 1977. The effect of seawater and temperature onthe germination behavior of Crithmum maritimum. Physiol.Plant. 41: 265–267.

Okusanya, O.T., and Ungar, I.A. 1983. The effect of time of seedproduction on the germination response of Spergularia marina.J. Plant Physiol. 59: 335–342.

Qi, J. 1998. Aerial sowing for sand control in China. SciencePress, Beijing.

Redmann, R.E. 1974. Osmotic and specific ion effects on the ger-mination of alfalfa. Can. J. Bot. 52: 803–808.

Romo, J.T., and Haferkamp, M.R. 1987. Forage kochia germina-tion response to temperature, water stress and specific ions.Agron. J. 79: 27–30.

Rozema, J. 1975. The influence of salinity, inundation and temper-ature on germination of some halophytes and non-halophytes.Oecol. Plant. 10: 341–353.

Slatyer, R.O. 1967. Plant-water relationships. Academic Press,London.

SPSS. 2000. SPSS 10.0 for windows. SPSS Inc., Chicago, Ill.Thompson, K., Grime, J.P. 1983. A comparative study of germina-

tion responses to diurnally fluctuating temperatures. J. Appl.Ecol. 20: 141–156.

Thompson, P.A. 1974. Effects of fluctuating temperatures germina-tion. J. Exp. Bot. 25: 164–175.

Tobe, K., Li, X., and Omasa, K. 2000. Seed germination and radi-cle growth of a Halophyte, Kalidium caspicum(Chenopodiaceae). Ann. Bot. (London), 85: 391–396.

Trudgill, D.L., Squire, G.R., and Thompson, K. 2000. A thermaltime basis for comparing the germination requirements of someBritish herbaceous plants. New Phytol. 145: 107–114.

Ungar, I.A. 1995. Seed germination and seed bank ecology inhalophytes. In Seed development and seed germination. Editedby J. Kigel, and G. Galili. Marcel Dekker, New York. pp. 599–628.

Warington, K. 1936. The effect of constant and fluctuating temper-atures on the germination of weed seeds in arable soils. J. Ecol.47: 483–497.

Washitani, I., and Takenaka, A. 1984. Germination responses innon-dormant seed population of Amarathus patulus to constanttemperatures in the sub-optimal range. Plant Cell Environ. 7:353–358.

Wen, Y. 1992. A study on the effect of rainfall on airial seeding. InCollected papers of the Maowusu Sands Exploitation and Con-trol Research Centre. Inner Mongolia University Press, Hohhot,China. pp. 43–46. [In Chinese.]

Young, J.A., Black, R.R.D., Palmquist, E., and Trent, J.T. 1995.Allenrolfea desert in western North American. J. Arid LandStud. 4: 197–205.

Zhang, X.S. 1994. Principles and optimal models for developmentof Maowusu sandy grassland. Acta Phytoecol. Sin. 18: 1–16. [InChinese with English abstract.]

Zheng, Y.R., Gao, Y., An, P., Shimizu, H., Rimmington, G.M.2004. Germination characteristics of Agriophyllum squarrosum.Can. J. Bot. 82: 1662–1670.

© 2005 NRC Canada

1028 Can. J. Bot. Vol. 83, 2005