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South African Journal of 75 (2009) 537–545 www.elsevier.com/locate/sajb

Dormancy and germination characteristics of the trimorphic of Garhadiolus papposus (), an annual ephemeral from the Junggar Desert, China ⁎ ⁎ H.Z. Sun a, J.J. Lu a, D.Y. Tan a, , J.M. Baskin b, C.C. Baskin b,c,

a Key Laboratory of Grassland Resources and Ecology, College of Grassland and Environment Sciences, Xinjiang Agricultural University, Urümqi 830052, China b Department of Biology, University of Kentucky, Lexington, Kentucky 40506-0225, USA c Department of and Soil Sciences, University of Kentucky, Lexington, Kentucky 40546-0312, USA Received 16 March 2009; received in revised form 8 May 2009; accepted 12 May 2009

Abstract

Dormancy and germination of dimorphic achenes have been compared within and between numerous species of Asteraceae, whereas only a few such comparisons have been made with trimorphic achenes. Garhadiolus papposus is an annual ephemeral species of disturbed desert habitats that produces three kinds of achenes that differ in size, morphology, pappus development and germination requirements. Fresh central achenes germinated to 10–21% in light at 15/2 and 20/10 °C, while intermediate and peripheral achenes germinated to b5%. Germination was enhanced by excising the embryo in peripheral but not in intermediate achenes. For peripheral and intermediate achenes, pericarps and/or phyllaries did not inhibit germination of isolated embryos, indicating that water-soluble germination inhibitors were not present in these structures. For central and intermediate achenes, germination percentage increased with duration of dry storage at room temperature. Darkness decreased germination of central and intermediate achenes, while peripheral ones, which were viable, did not germinate at any condition. These data show that 1) the three morphs differ in germination requirements, and 2) difference in germination may be caused by low growth potential of the embryo and mechanical resistance (to embryo growth) of the thick pericarp and/or lignified phyllary. © 2009 SAAB. Published by Elsevier B.V. All rights reserved.

Keywords: Dormancy; Garhadiolus papposus; Germination; Junggar Desert; Trimorphic achenes

1. Introduction 1982; Venable et al., 1987, 1995; Maun and Payne, 1989; Mandák, 1997); it is a form of bet-hedging (Venable, 1985; Each desert-inhabiting plant has its own complex of Venable et al., 1987, 1995; Mandák, 1997). strategies that enables it to persist in desert habitats (Gutterman, Imbert (2002) reported that heterocarpy/heterospermy is 1994). Heterocarpy or heteromorphism, the production of known to occur in 18 families of angiosperms, being most two or more fruit types on a single plant (Tanowitz et al., 1987; common in Asteraceae and Chenopodiaceae. Sixty-three and Mandák, 1997), is one of these strategies (Venable and Lawlor, three-tenths percent of the species and 52.5% of the genera 1980; Maxwell, 1994; Ruiz de Clavijo, 1995). Heterocarpy belong to the Asteraceae and 8.3 and 10%, respectively, to the typically occurs in annual species of open, arid habitats and may Chenopodiaceae. In Asteraceae, fruit heteromorphism, i.e. the increase the flexibility of adaptation to highly variable difference between central and peripheral achenes (McDo- environments (Koller and Roth, 1964; Baker and O'Dowd, nough, 1975),maybeassociatedwithadifferencein germination behaviour, e.g. in Bidens, Senecio, Picris and (McEvoy, 1984; Rocha, 1996; Imbert et al., 1999; Imbert ⁎ Corresponding authors. Baskin is to be contacted at Department of Biology, University of Kentucky, Lexington, Kentucky 40506-0225, USA. 2002; Brändel, 2004, 2007). Central achenes are often less E-mail addresses: [email protected] (D.Y. Tan), [email protected] dormant and germinate over a wider range of temperatures, to (C.C. Baskin). higher percentages and at faster rates than peripheral ones

0254-6299/$ - see front matter © 2009 SAAB. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.sajb.2009.05.001 538 H.Z. Sun et al. / South African Journal of Botany 75 (2009) 537–545

Fig. 1. Capitulum and morphology of the three types of achenes in G. papposus. 1. Infructescence (longitudinal section); 2. Peripheral connected to phyllary (PA+Ph); 3. Peripheral achene without phyllary (PA); 4. Intermediate achene (IA); 5. Central achene (CA). In panel 1, the peripheral achene cannot be seen because it is covered by a phyllary.

(Baskin and Baskin, 1976; Forsyth and Brown, 1982; Corkidi wind-dispersed pappus (central) to short, wide achenes without et al., 1991; Rocha, 1996; Brändel, 2007). For a few species, pappus (peripheral) (Fig. 1). dormancy of peripheral achenes is less than that of the central The specific objectives of the study on G. papposus were to ones (Brändel, 2004). Pericarp structure or anatomy may be, in (1) describe the differences in size, form and structure of the part, responsible for the different germination responses three types of achenes; (2) compare dormancy and germination between central and peripheral achenes (McEvoy, 1984; behavior among the three achene types; and (3) explore possible Venable and Levin, 1985a; Tanowitz et al., 1987; Ruiz de reasons why intact achenes of the three morphs differ in depth Clavijo, 2001; Brändel, 2007). of dormancy. Thus, the study of fruit heteromorphism in Asteraceae has received particular attention during the last few decades (Koller 2. Materials and methods and Roth, 1964; McDonough, 1975; Forsyth and Brown, 1982; Venable and Levin, 1985a,b; Imbert et al., 1996; Gibson, 2001; 2.1. Field site description and achene collection Imbert, 2002; Brändel, 2004, 2007). However, most such studies have been done with species that produce dimorphic achenes, and Freshly-matured achenes were collected in June 2007 from only a relatively few have compared the dormancy and in natural G. papposus populations growing in the hilly germination characteristics of those that produce trimorphic gravel desert in the vicinity of Urümqi on the southern edge of achenes (but see Venable et al., 1987; Kigel, 1992; Ruiz de the Junggar Basin of Xinjiang (43°48′41.8″ N, 87°32′21.6″ E, Clavijo, 1995, 2005; Hensen, 1999). Further, at least three of these 850 m asl). Achenes from the capitula were bulked into one studies on trimorphic achenes have not investigated the collection, separated into three types and stored at ambient germination responses of fresh achenes (Kigel, 1992; Ruiz de conditions in the laboratory (18–25 °C, 15–20% RH) in paper Clavijo, 1995, 2005). In this study, we report the presence of bags until used. trimorphic achenes (heterocarpy) in Garhadiolus papposus This area has typical desert vegetation, gravelly grey desert Boiss. et Buhse and investigate the differences in germination soil and a continental climate. Mean annual temperature is responses of fresh and after-ripened achenes. Further, in an 6.8 °C, and the extreme temperatures of the coldest (January) attempt to explain differences in dormancy among the three and hottest (July) months are −32.8 °C and 40.5 °C, morphs, we compared anatomical cross-sections of the pericarps respectively. Annual precipitation (including rain and snow) is and also tested their possible roles in chemical and mechanical 234 mm, 62.7% of which occurs in spring and summer, and the inhibition of embryo growth, i.e. germination. snow that falls in winter begins to melt in March or April. The Garhadiolus papposus is an annual ephemeral Asteraceae annual potential evaporation is N2000 mm (Jiang et al., 1992). species that occurs in Central , , , Caucasia and China (Zhou et al., 1987; An et al., 1999). This is the only 2.2. Number, mass, morphology and anatomy of achenes species of Garhadiolus found in China, and it grows only in the southern part of the Junggar Basin, Xinjiang. It is one of the Number of central, intermediate and peripheral achenes per very common ephemeral species that germinates in early spring head was recorded in a sample of 50 heads. Eight replications of in the Junggar Desert (Mao and Zhang, 1994; Wang et al., 100 central, intermediate and peripheral achenes each collected in 2006). During 2 years of field observations, we found only one June 2007 and stored dry at laboratory conditions for 11 months newly-germinated seedling in autumn but many in spring were weighed to determine the mass of each achene type using a (March, April). Plants begin to flower in late April or early May, Sartorius BS210S electronic-balance (0.0001 g). After weighing and most of them are dead by early July. Three types of achenes achenes with embryos, the embryos were removed, and pericarps are produced in each head (capitulum): central, intermediate and of 100 achenes of each morph were weighed. Embryo mass was peripheral, and they range in shape from elongated achenes with calculated by the difference between that of achenes and that of H.Z. Sun et al. / South African Journal of Botany 75 (2009) 537–545 539 pericarps. Achene and pappus lengths were measured using 2.3.3. Effect of cold stratification on dormancy break digital calipers, and the number of pappus capillary bristles was Fifty freshly-matured intermediate and peripheral achenes recorded for each of 50 achenes in each of the three morphs. (collected in June 2007) each were placed on moist sand in 12- To compare anatomical characteristics of the pericarp of the cm-diameter Petri dishes and cold-stratified at 5±2 °C for 4, 8, three types of achenes, 10 nearly-mature achenes of each morph 12 or 16 weeks in light or for 16 weeks in darkness. After each collected in June 2007 were fixed in formalin–acetic acid– cold stratification period, seeds were incubated in light at the alcohol (FAA) for 3 months. The material was dehydrated in a five temperature regimes for 2 weeks. Since one to four graded ethanol series, cleared in a graded dimethylbenzene intermediate achenes, but no peripheral achenes, germinated series, infiltrated in paraffin and embedded in paraffin following during the cold stratification treatments, germinated achenes the methods of Zheng and Gu (1993). Thin sections (8–12 µm) were removed before incubation. The non-germinated achenes were made on an exact revolving microtome (HistoSTAT 820), were incubated for 2 weeks, after which germination percen- and the sections were stained with safranin and fast green. tages were calculated. Images were taken using a camera mounted on an Olympus BH- 2 biology microscope. 2.3.4. Light requirement for germination of achenes Maximum germination percentages of central, intermediate 2.3. Germination and peripheral achenes stored dry at room temperatures for 3 months were about 55, 45 and 0%, respectively; thus, only Experiments were conducted in temperature- and light- central and intermediate achenes stored for 3 months were used controlled incubators. Achenes were tested for germination in to test the effects of light on germination. Achenes were − − light (12 h of ≈100 µmol m 2 s 1, 400–700 nm, cool white incubated at the five temperature regimes in light and in fluorescent light each day) or in constant darkness (Petri dishes constant darkness. To test germination percentages of achenes with seeds in them were wrapped with aluminium foil) at 12/ in constant darkness, Petri dishes containing the achenes were 12 h daily temperature regimes of 5/2, 15/2, 20/10, 25/15 and wrapped with plastic film to retard loss of water and then with 30/15 °C or only at 15/2 °C in light. The four higher temperature aluminium foil to provide darkness. Germination in the light regimes approximate mean daily maximum and minimum was monitored every 24 h, at which time germinated achenes monthly air temperatures in the vicinity of Urümqi during the were counted and removed from the Petri dishes. After 14 days, growing season: March, April and November, 15/2 °C; May, experiments in light were terminated. Achenes incubated in September and October, 20/10 °C; June and August, 25/15 °C; darkness were checked only at the end of the 14-day period; and July, 30/15 °C. Since the winter temperature in the vicinity thus, they were not exposed to any light during the incubation of Urümqi is below 0 °C and achenes would not germinate at period. this temperature, the 5/2 °C temperature regime was used to simulate late winter temperature and test the effects of low 2.3.5. Role of pericarp and phyllary for inhibiting germination temperature on the germination of achenes. Only the achene types that germinated to ≤10% under all Achenes were incubated in 90-mm-diameter Petri dishes on conditions tested in preliminary experiments conducted in two layers of Whatman No. 1 filter paper soaked in distilled September 2006 were used. These included the intermediate water, and water was added as needed during the experiments to and peripheral achenes, which were treated as follows. keep the paper moist. Unless otherwise stated, three replications of 50 achenes each were used for each treatment. 2.4. For intermediate achenes Protrusion of the radicle was the criterion for germination. Viability of un-germinated seeds was determined by pinching (1) Control: achenes were left intact. them with forceps under a microscope to see if the embryos (2) Embryos without pericarps were used to determine whether were white and firm, revealing that they were alive, or grey and the pericarp inhibited germination either mechanically or soft, indicating they were nonviable. Five experiments (a–e) chemically. were set up on 28 June 2007 using seeds collected in June 26, (3) Excised embryos as well as pericarps were placed 2007. together in Petri dishes to test whether soluble chemicals that leached from the pericarp inhibited germination. 2.3.1. Germination of freshly harvested achenes The three types of freshly-matured achenes were incubated 2.5. For peripheral achenes on June 28 at the five temperature regimes in light for 30 days. Dishes were examined for germinated seeds at 2-day intervals. (1) Control: un-manipulated dispersal units (achene with phyllary). 2.3.2. Effect of dry storage (after-ripening) on dormancy break (2) Achenes without phyllaries. Achenes stored dry at room conditions (20–22 °C, 20%– (3) Embryos without pericarps and phyllaries. 30% RH) for 0, 1, 2 and 3 months were tested at the five (4) Excised embryos and pericarps were placed together in temperature regimes in light. After each storage interval, seeds Petri dishes. were incubated for 16 days, and dishes were examined for (5) Experiments were conducted at 15/2 °C in light on fresh germinated achenes at 2-day intervals. seeds (0 months old) and on seeds that had been stored in 540 H.Z. Sun et al. / South African Journal of Botany 75 (2009) 537–545

Table 1 3. Results Mass (mean±SE) of 100 achenes, embryos and pericarps each of peripheral (not including phyllary), intermediate and central achenes of G. papposus. 3.1. Number, mass, morphology and anatomy of achenes Morphs Achene mass Embryo mass Pericarp mass Peripheral achenes 0.119±0.001c 0.046±0.000b 0.072±0.001c Three morphs are distinguishable within each capitulum Intermediate achenes 0.093±0.002b 0.036±0.000a 0.057±0.002b a a a (Fig. 1). Number of central achenes per head ranged from 4 to 9 Central achenes 0.069±0.000 0.034±0.001 0.035±0.001 with a mean (±SE) of 5.8±0.2 and number of intermediate χ2 value 17.830 13.817 17.818 df 222 achenes from 4 to 7 (5.0±0.2). Number of peripheral achenes P 0.000 0.001 0.000 per head from the same sample was invariant at 5. Peripheral Different superscript letters within a column indicate significant differences achenes are yellow or whitish-yellow, 6.7±1.0 mm in length (Tukey's HSD, P=0.05). and have a scarcely-developed pappus. They are subtended by the inner involucral (phyllaries). Central achenes are brown, elongated (with a length of 9.7±1.4 mm, not including the laboratory for 1 and 2 months after they were the beak) and have a well-developed pappus (17.36±0.53 collected in June 2007. Three replications of 35 achenes bristles per achene, 1.0±0.3 mm in length). Intermediate were used for each treatment. Germination was monitored achenes are dark yellow, 7.6±1.1 mm in length and have a at 2-day intervals, beginning on day 1 of incubation and moderately-well-developed, or no, pappus. continuing until day 17 of incubation. Total achene mass, embryo mass and pericarp mass of periph- eral achenes were significantly higher than those of intermediate and central achenes (total: χ2 =17.830; df=2; Pb0.01; embryo: 2.6. Data analysis χ2 =13.817; df=2; P b0.01; pericarp: χ2 =17.818; df=2; Pb0.01 ) (Table 1). Mean mass of peripheral achenes was 1.28 All data were analyzed for normality and homogeneity of and 1.72 times greater than that of intermediate and central variance prior to analysis to fulfill requirements of ANOVA. achenes, respectively, and intermediate achenes 1.35 times greater Percentage data were arcsine transformed before statistical than that of central achenes. analysis to ensure homogeneity of variance (non-transformed The pericarp of peripheral achenes was nearly twice as thick data appear in all figures). If mass data were normal and as that of the central achenes, and it contained many more homogeneous, they were subjected to further analysis; if not sclerenchymatous cells (Fig. 2). Only the peripheral achenes normal or homogeneous, the values were logarithmically have thick lignified phyllaries. transformed before analyzing them. If the variance of transformed data of percentage and mass were still not 3.2. Germination homogenous, a nonparametric test was used to analyze the data. When variances of data were homogeneous, ANOVA was 3.2.1. Germination of freshly harvested achenes used to determine differences among the three morphs of Differences in germination percentages of the three types of achenes in mean mass and mean germination percentage among fresh achenes were obvious at 15/2 °C in light (Fig. 3). At the three achene morphs. Tukey's HSD test was performed for maturity, central achenes germinated to 21% and 10% in light at multiple comparison to determine significant (Pb0.05) differ- 15/2 and 20/10 °C, respectively, and intermediate achenes to ences among the three morphs. When the transformed data were 4.7% and 0% at these two temperature regimes, respectively. No still not homogenous, differences among the three achene peripheral achenes germinated at any temperature. The morphs were determined by the Kruskal–Wallis test, a difference between germination of central and intermediate nonparametric test. All data analyses were performed with the achenes at 15/2 °C was significant (F=6.819, Pb0.05). Central software SPSS 13.0 (SPSS Inc, Chicago, Illinois, USA), and all and intermediate achenes began to germinate after 4 and 9 days, data were expressed as mean±SE. Statistical tests were respectively, while no peripheral achenes germinated (within conducted at P=0.05 (Sokal and Rohlf, 1995). 30 days).

Fig. 2. Cross-section of pericarp of the three types of achenes in G. papposus. A. Peripheral achene connected to phyllary, bar=400 µm. B. Peripheral achene, bar=100 µm. C. Intermediate achene, bar=100 µm. D. Central achene, bar=100 µm. SC: sclerenchymatous cells in the pericarp; Ph: phyllary; PA: peripheral achene. H.Z. Sun et al. / South African Journal of Botany 75 (2009) 537–545 541

for those stratified in light for 16 weeks and incubated at 15/ 2 °C (only 1 achene germinated).

3.2.4. Light requirement for germination of achenes Darkness caused a reduction in final germination percen- tages of 3-month-old central and intermediate achenes and also reduced the temperature range for germination (Fig. 5). At the optimum temperature (15/2 °C), 52.4% of central achenes germinated in light and 16.7% in darkness, and 23% and 4.6% of intermediate achenes germinated in light and darkness, Fig. 3. Percentage germination of the three types of fresh achenes of G. respectively. The 80% reduction for intermediate achenes was papposus over a range of temperatures in light (12-h photoperiod) for 30 days. significantly higher than the 68% reduction for central achenes (F=31.73, Pb0.01).

3.2.2. Effect of dry storage (after-ripening) on dormancy break 3.2.5. Role of pericarp and phyllary for inhibiting germination Dormant central and intermediate achenes gradually became Germination of untreated fresh-intermediate and fresh- non-dormant, and thus germination percentage and temperature peripheral achenes of G. papposus was 4.7% and 0%, range over which seeds germinated increased with age. respectively. Excising embryos did not significantly increase Intermediate achenes became non-dormant more rapidly than germination percentage of intermediate achenes (P=0.38). central ones (Fig. 4). However, all, or nearly all, of the However, the three treatments of excising embryos in peripheral peripheral achenes remained dormant and did not germinate at achenes increased the germination percentage significantly any temperature even after 3 months of dry storage (after- (P=0.02, 0.01 and b0.01, respectively), but final germination ripening) in the laboratory. percentage among the three treatments did not differ (P=0.303) (Fig. 6). 3.2.3. Effect of cold stratification on dormancy break Storage influenced germination of excised embryos. Germi- Up to 16 weeks of cold stratification were almost completely nation percentage of excised peripheral-fresh embryos differed ineffective in breaking dormancy in any of the three achene from that of those of 1-month-stored and 2-month-stored types. The highest germination percentages were for inter- achenes. After storage for 2 months, excised embryos from mediate achenes stratified in darkness and germinated in light at intermediate and peripheral achenes germinated to 96.8% and 15/2 °C (3 achenes germinated) and 25/15 °C (3 achenes 84.9%, respectively. When intermediate and peripheral embryos germinated). The only germination of peripheral achenes was were placed in close contact with pericarps, their germination

Fig. 4. Final germination percentages (mean±SE) (within 14 days) of central, intermediate and peripheral achenes of G. papposus incubated in light (12 h photoperiod) at five temperature regimes following 0–3 months of dry storage at laboratory conditions. The final germination percentages at 5/2 °C were b10% (data not shown). 542 H.Z. Sun et al. / South African Journal of Botany 75 (2009) 537–545

Fig. 5. Final germination percentages (mean±SE) (within 14 days) of 3-month-old central, intermediate and peripheral achenes of G. papposus incubated in light (12 h photoperiod) and in constant darkness at five temperature regimes.

Fig. 6. Effect of different treatments on germination percentages of 0-month (A, A'), 1-month (B, B') and 2-month-old (C, C') peripheral and intermediate achenes or embryos of G. papposus in light (12-h photoperiod) at 15/2 °C. H.Z. Sun et al. / South African Journal of Botany 75 (2009) 537–545 543 was not inhibited (Fig. 6). The germination percentages of germination. The pericarp could exert its influence by (1) treated peripheral and intermediate achenes were significantly containing soluble chemicals that inhibit germination; (2) higher than those of complete dispersal units (peripheral: blocking diffusion of gasses and/or uptake of water; and (3) F=530.58, Pb0.01; intermediate: F=125.48, Pb0.01). physically impeding germination (McEvoy, 1984). In some Asteraceae species of desert habitats, the achenes remain 4. Discussion enclosed within involucral bracts, which form an important barrier against water absorption (Gutterman, 1993). Conse- The present study demonstrates the existence of three quently, germination can only occur when rainfall is consider- morphologically- and physiologically-distinct types of achenes able, increasing the likelihood of seedling survival (Imbert, in a capitulum of G. papposus. The elongated central achenes 2002). Tanowitz et al. (1987) assumed that the thicker pericarp seem to be well adapted to dispersal, since they have a long beak of peripheral achenes may inhibit germination for prolonged with well-developed pappus and are more exposed to the wind periods in Hemizonia increscens. Studies with Bidens pilosa than the other two types. On the other hand, peripheral achenes, suggested that the pericarp of different morphs varies in which are partly covered by lignified phyllaries and scarcely concentration of germination inhibitors (Forsyth and Brown, have a pappus, remained on the capitulum and were dispersed 1982). However, results of the present study showed that only when the capitulum broke apart. Some of the intermediate isolated pericarps and/or phyllaries did not inhibit germination achenes were dispersed together with central achenes immedi- of the embryos of G. papposus, indicating that water-soluble ately after maturation, while others remained in the capitulum germination inhibitors were not leached from the pericarps or and were dispersed along with peripheral achenes (Hua Zh. Sun, phyllaries. The thick pericarp and phyllary of the peripheral personal observation). achenes and thick pericarp of the intermediate achenes of G. Variation in morphology is usually correlated with papposus may be the reason these two achene types are more diverse patterns of dormancy and germination (Venable et al., dormant than the central achenes. That is, these structures exert 1987; Mandák, 2003). A high proportion of the three morphs of more mechanical restraint on the embryo than the relatively thin G. papposus were dormant, probably because of the low growth pericarp exerts on the embryo of the central achene. potential of the embryo and the mechanical restraint of embryo Differencesinmorphologyandlevelofdormancyofachenes growth by the thick, lignified pericarp and/or phyllary, as within a capitulum enable plants to spread their offspring in space evidenced by low germination percentages and rates over a and time (Venable, 1985). In the majority of species with wide range of temperatures, i.e. physiological dormancy (sensu heteromorphic achenes, morphs with low dispersal ability have Baskin and Baskin, 2004). However, central achenes were less high seed dormancy, and those with high dispersal ability have dormant than the outer ones, e.g. 21% and 4.7% were the highest reduced dormancy (Imbert, 2002). The results of our study germination percentages for freshly-matured central and inter- suggest that the strategy and ecological adaptation of G. papposus mediate achenes, respectively. The peripheral achenes were morphs are similar to those of most other heteromorphic species. strictly dormant and did not germinate in any of the test Production of different kinds of achenes by a single plant of G. conditions. Dormancy of some of the central and intermediate papposus enables this species to adopt two strategies to adapt to achenes was broken during dry storage in laboratory conditions, the unpredictable environment of the Junggar Desert. At maturity, while none of the peripheral ones germinated at any temperature the high proportion of dormant achenes of G. papposus could be a even after 3 months of storage. After storage for 3 months, central mechanism to ensure that all dispersed achenes do not germinate and intermediate achenes were less dormant than those of at the same time. In fact, the lack of dispersal and the delay of peripheral ones, and they germinated faster and to higher germination of peripheral achenes constitute a very safe means of percentages at 15/2 and 20/10 °C. This germination response is reproduction and an available achene reserve on/in soil of the similar to that of most species of Asteraceae with heteromorphic desert habitat, and thus increase the probability of a population's achenes, with peripheral achenes germinating under more persistence of G. papposus. High dispersal ability and reduced restricted conditions than the central ones (McDonough, 1975; dormancy of central achenes allow this species to reach new areas Baskin and Baskin, 1976; McEvoy, 1984; Venable and Levin, and hence to expand its distribution in space. 1985a; Tanowitz et al., 1987; Imbert, 2002; Brändel, 2007). The After dry storage at room temperature for several months, a relative germination percentage of the three achene morphs of G. portion of central and intermediate achenes has after-ripened. In papposus is the same as that in pinnatum (Venable the field, after-ripening would occur in summer, and seeds would et al., 1987)andLeontodon taraxacoides subsp. longirrostris be non-dormant in autumn, when the soil is probably too dry for (Hensen, 1999) (Asteraceae), i.e. centralNintermediateNperiph- them to germinate. Thus, germination of these non-dormant eral. Regardless of how the germination characteristics of the seed achenes would be delayed until the next spring, when soil types of a species differ, the result is that they do not germinate at moisture (precipitation plus snow melt) and temperature are thesametime(Baskin and Baskin, 1976). suitable for germination (Wang et al., 2006). In November 2007, Variations in germination behavior among the morphs may before the first snowfall in Urümqi, we searched for seedlings of be due to presence of inhibitors in surrounding tissues (Beneke G. papposus in the field but found only one. Searching for et al., 1992, 1993), thick pericarp (McEvoy, 1984; Tanowitz seedlings during winter is impossible because the area is covered et al., 1987) or innate dormancy (Negbi and Tamari, 1963). by snow. However, many seedlings were found in spring (late Thickness and structure of pericarp play a major role in March and April), and presumably these had germinated only 544 H.Z. Sun et al. / South African Journal of Botany 75 (2009) 537–545 recently. Because of their deeper dormancy, peripheral achenes Gutterman, Y., 1994. Strategies of seed dispersal and germination in plants – probably persist for a longer period of time than central or inhabiting deserts. The Botanical Review 60, 373 425. Hensen, I., 1999. Life strategies of semi-arid grassland community-mechanisms intermediate achenes before they germinate. We have not of dispersal and reproduction within Lapiedro martinezii–Stipetum identified the dormancy-breaking requirements for this morph. tenacissimae (southeastern) Spain. Feddes Repertorium 110, 265–285. Achenes of Asteraceae contain no endosperm at maturity, Imbert, E., 2002. Ecological consequences and ontogeny of seed heteromorph- and nutrients are stored in the embryo (Venable and Levin, ism. Perspectives in Plant Ecology, Evolution and Systematics 5, 13–36. 1985a). Thus, the differences among embryo mass of the three Imbert, E., Escarré, J., Lepart, J., 1996. Achene dimorphism and among- population variation in Crepis sancta (Asteraceae). International Journal of morphs is ecologically significant in that seedlings originating Plant Sciences 157, 309–315. from different morphs may differ in competitive performance as Imbert, E., Escarré, J., Lepart, J., 1999. 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