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Diaspore dispersal ability and degree of dormancy in heteromorphic species of cold deserts of northwest China: A review

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Review Diaspore dispersal ability and degree of dormancy in heteromorphic species of cold deserts of northwest China: A review

Jerry M. Baskin a,b, Juan J. Lu a, Carol C. Baskin a,b,c,∗, Dun Y. Tan a,∗∗, Lei Wang d a Key Laboratory of Grassland Resources and Ecology & Ministry of Education, Key Laboratory for Western Arid Region Grassland Resources and Ecology, College of Grassland and Environment Sciences, Xinjiang Agricultural University, Urümqi 830052, China b Department of Biology, University of Kentucky, Lexington, KY 40506, USA c Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY 40546, USA d State Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urümqi 830011, China article info abstract

Article history: The cold deserts of northern Xinjiang Province in northwest China are rich in diaspore-heteromorphic Received 16 August 2013 species, and diaspore biology has been compared in more heteromorphic species native to this biogeo- Received in revised form 26 January 2014 climatic region than for any other region worldwide. Our primary purpose was to compare the dispersal Accepted 14 February 2014 ability and degree of dormancy in heteromorphic diaspores in Xinjiang desert via a review of the Available online 23 February 2014 Chinese and English literature. We located literature on 20 heteromorphic species native to these deserts. Fourteen of the species are chenopods (Amaranthaceae). All 20 species are heterodiasporous (dimorphic, Keywords: 14; trimorphic, 4; polymorphic, 2) annuals, and none is amphicarphic sensu stricto. Thirteen of the species Amphi-basicarpy Central Asian cold deserts are heterocarpic, six heterospermic, one amphi-basicarpic and none heteroarthrocarpic. Diaspores of 19 Dispersal of the species differ in seed dormancy/germination. Thirteen of the 14 species to which both diaspore Dormancy dispersal ability and degree of dormancy could be assigned had at least one morph with high (or relatively Germinability high) dispersal ability and low degree of dormancy and at least one with low dispersal ability and high Heterocarpy (or relatively high) degree of dormancy. Conceptual models of the dynamics of seed dormancy of the two Heterodiaspory morphs for each of three dimorphic species suggest the ecological significance of heterodiaspory in the Heterospermy cold desert annuals. However, the ecological significance of seed/fruit heteromorphism needs to be more thoroughly demonstrated via long-term field studies that compare the life history/demography of plants derived from different morphs. © 2014 Geobotanisches Institut ETH, Stiftung Ruebel. Published by Elsevier GmbH. All rights reserved.

Contents

Introduction ...... 94 Literature on diaspore heteromorphism of native species in Xinjiang cold deserts ...... 94 Classification of diaspore heteromorphism ...... 94 Diaspore dispersal ability ...... 94 Degree of dormancy and germination of diaspores ...... 96 Life history strategy: diaspore dispersal ability and degree of dormancy...... 97 Conceptual models of diaspore dynamics in Xinjiang cold desert species ...... 97 Comparison of diaspore heteromorphism in Xinjiang with that in other regions ...... 97 Acknowledgements ...... 98 References ...... 98

∗ Corresponding author at: Department of Biology, University of Kentucky, Lexington, KY 40506, USA. Tel.: +1 859 2573996. ∗∗ Corresponding author. Tel.: +86 991 8762271. E-mail addresses: [email protected] (C.C. Baskin), [email protected] (D.Y. Tan). http://dx.doi.org/10.1016/j.ppees.2014.02.004 1433-8319/© 2014 Geobotanisches Institut ETH, Stiftung Ruebel. Published by Elsevier GmbH. All rights reserved. 94 J.M. Baskin et al. / Perspectives in Plant Ecology, Evolution and Systematics 16 (2014) 93–99

Introduction Literature on diaspore heteromorphism of native species in Xinjiang cold deserts Diaspore heteromorphism is the production by an individual plant of two or more distinct kinds of seeds and/or fruits (some- Our survey identified numerous published papers and other lit- times with accessory parts such as bracteoles, perianth or phyllary) erature on fruit/seed heteromorphism in 20 native heteromorphic that differ in size/mass (e.g. Dowling, 1933; Sun et al., 2008; Aguado species that occur in the deserts of northern Xinjiang Province in et al., 2011); shape (e.g. Baker and O’Dowd, 1982; Venable and northwest China (Table 1). While most of the studies were done on Levin, 1985a; Mandák and Pysek,ˇ 1999); dispersal ability (e.g. plants from Xinjiang, plants of Atriplex centralasiatica were from Sorensen, 1978; Payne and Maun, 1981; Talavera et al., 2012); Hebei Province, northern China (W. Li et al., 2008, 2011; Xu et al., and/or degree of dormancy (e.g. Esashi and Leopold, 1968; Baskin 2011), Atriplex dimorphostegia from Israel (Koller, 1957, 1970), and Baskin, 1976; Ruiz de Clavijo, 1994). In addition, plants pro- Atriplex tatarica from the Czech Republic, probably native in south- duced by the different morphs differ in many ways including eastern part of Czech Republic, i.e. southern Moravia (Mandák, survival (e.g. Venable and Levin, 1985b; Imbert, 1999; Braza and 2003; Kochánková and Mandák, 2009) and Suaeda corniculata Garcia, 2011); growth (e.g. Rai and Tripathi, 1982; El-Keblawy, subsp. mongolica from Inner Mongolia, northern China (Cao et al., 2003; Ruiz de Clavijo, 2001); competitive ability (e.g. Beneke et al., 2012; Yang et al., 2012). Further, plants of Chenopodium album stud- 1992a,b; Gardocki et al., 2000); and life history and demographic ied were from both the United Kingdom (introduced) (Williams characteristics (e.g. Venable and Levin, 1985b; Venable et al., and Harper, 1965) and Xinjiang (native) (Yao et al., 2010a,b,c) and 1987). those of Halogeton glomeratus from both western USA (introduced) Why should individual plants make more than one kind of (Tisdale and Zappetini, 1953; Zappetini, 1953; Holl, 1954; Bruns seed? Plants that produce heteromorphic diaspores most com- and Rasmussen, 1958; Williams, 1960; Bruns, 1965; Cronin, 1965; monly are annuals of disturbed sites and stressful environments Robocker et al., 1969) and Xinjiang (native) (Yu et al., 2009). such as deserts (Mandák, 1997; Imbert, 2002). Various mechanisms have evolved in annuals that are adaptations to harsh and variable Classification of diaspore heteromorphism environments, and seed/fruit heteromorphism is one of them. Thus, diaspores that differ in dispersal ability (e.g. with and without pap- With some modifications as discussed below, we follow the pus) and germinability (i.e. nondormant vs. dormant) allow annuals system of Mandák (1997) in classifying the species to kinds of dias- to escape the harshness and unpredictability of their habitat in pore heteromorphism. Mandák recognized two main categories space (dispersal) and time (delayed germination via dormancy). of diaspore heteromorphic plants: heterodiaspory and amphi- The majority of studies on heteromorphism have been done on carpy. Heterodiasporous plants produce two or more kinds of species that produce two kinds of diaspores (dimorphic). For dis- diaspores (morphs) on aboveground shoots, and amphicarpous persal and dormancy, it usually is found that one morph has high plants produce one or more morphs aboveground and one or or relatively high dispersal ability and little or no dormancy, while more belowground. However, whereas Mandák defined heteros- the other one has low (or no) dispersal ability and high or relatively permy, a subcategory of heterodiaspory, as two kinds of seeds in high dormancy (Venable, 1985; Ellner, 1986). the same fruit, we define the term as one type or more than one Our primary aim was to review the Chinese and English litera- type of fruit (on the same individual) that contain(s) seeds that dif- ture on dispersal ability and degree of dormancy in heteromorphic fer within or between fruits. According to Mandák, heterospermy species in the cold deserts of northern Xinjiang Province, China. may be combined with heterocarpy or heteroarthrocarpy, two More specifically, for each species studied we aimed to (1) clas- other subcategories of heterodiaspory. Thus, to avoid this “prob- sify the heteromorphic dispersal-germination units (morphs); (2) lem” we distinguish heterocarpic and heteroarthrocarpic fruits as report the number of morphs per individual, i.e. dimorphic (two not having and as having distinct proximal and distal segments, morphs), trimorphic (three) or polymorphic (more than three); respectively (see Hall et al., 2011). Further, Mandák does not use and (3) create a diaspore dispersal/dormancy formula based on the term amphi-basicarpy, in which individual plants produce dias- dispersal ability and degree of dormancy. pores (basicarps) at ground level (not subterranean) and on higher To be included in this review, a species had to be native to portions of aerial stems. Thus, we follow Barker (2005) in classify- the deserts of northern Xinjiang Province, China. These deserts are ing the one amphi-basicarpic species in our study and consider it included in the cold deserts of Central (Petrov, 1973[1976]; to be a subcategory of heterodiaspory. Walter and Box, 1983) and consist of various kinds of plant All 20 species are heterodiasporous annuals (14 Amaran- communities, such as those that occur on sand dunes and on thaceae, three , two Boraginaceae and one Brassicaceae) saline-alkaline and nonsaline soils. Depending on type of soil, (Table 1), and none is amphicarpic. Further, 13 are heterocarpic, dominant shrubs or subshrubs and semi-arboreal genera include six heterospermic and one amphi-basicarpic (Ceratocarpus are- Alhagi, Anabasis, Artemisia, Calligonum, Caragana, Ephedra, Halocne- narius, Amaranthaceae); none is heteroarthrocarpic. Fourteen of mum, Haloxylon, Halostachys, Kalidium, Nitraria, Reaumuria, Salsola, the species produce two morphs per individual (dimorphic), four Tamarix and Zygophyllum, and annual species in the Amaranthaceae three morphs (trimorphic) and two more than three morphs (poly- (chenopods), Asteraceae, Brassicaceae, Fabaceae, Poaceae and morphic). Plants of Salsola brachiata produce four dispersal-unit other families may be important components of these plant com- morphs and those of C. arenarius a basicarp morph without glochids munities (C.W. Wang, 1961; Hou, 1983). Several things make this (hair-like spines, generally with a barb at the tip) and a gradient review relevant to the biology of heteromorphic species. (1) Cen- of morphs with short to long glochids (without barbs) on aerial tral Asian deserts are rich in taxa of Amaranthaceae (McArthur and branches. Sanderson, 1984) previously assigned to Chenopodiaceae (APG-III, 2009). (2) With the exception of the Asteraceae, the chenopods contain more fruit/seed heteromorphic species than any other tax- Diaspore dispersal ability onomic group (Imbert, 2002). (3) A substantial amount of research has been done on heterodiasporous plants native to the deserts of Much less research has been done on diaspore dispersal of the northern Xinjiang, a considerable portion of which is published in 20 species than on germination (see next section). Thus, relative Chinese. dispersal ability of different morphs has been compared for only J.M. Baskin et al. / Perspectives in Plant Ecology, Evolution and Systematics 16 (2014) 93–99 95

Table 1 Diaspore-based classification and number of morphs for 20- and dispersal-dormancy formulae for 14 native (annual) heteromorphic species in the cold deserts of northwest China, Xinjiang Province. See footnotes and text for additional explanation.

Family/species Classification Number of Dispersal/dormancy Authors morphs formula

AMARANTHACEAE Atriplex aucheri Moquin-Tandon Heterocarpy Trimorphic H/H(C)–H/L(B)–L/L(A)a,b Wei et al. (2007b) A. centralasiatica Iljin Heterocarpy Dimorphic H/H(hubr)–L/L(flbl)b W. Li et al. (2008) A. dimorphostegia Karelin & Kirilov Heterocarpy Dimorphic –c Koller (1957) A. micrantha C. A. Meyer Heterocarpy Dimorphic H/H(ebr)–L/L(ebl)b Liu and Wei (2007) A. tatarica L. Heterocarpy Dimorphic H/L(B)–H/H(C)b Mandák (2003); Kochánková and Mandák (2009) Ceratocarpus arenarius L. Amphi-basicarpy Polymorphic H/H(f)–I/I(c)–L/L(a)d Gao et al. (2008); J.J. Lu et al. (2013a) Chenopodium album L. Heterospermy Dimorphic –c Williams and Harper (1965); Yao et al. (2010a,b,c) Halogeton glomeratus (M. Bieb.) Ledeb. Heterocarpy Dimorphic H/H(1–wf)–L/L(s–wf)b Tisdale and Zappetini (1953); Williams (1960); Cronin (1965); Robocker et al. (1969); Yu et al. (2009) Salsola affinis C. A. Meyer Heterocarpy Trimorphic H/H(A)–L/H(B)–L/L(C)b H.F. Wang and Wei (2007); Wei et al. (2007a) S. brachiata Pallas Heterocarpy Polymorphic H/H(A)–H/H(B)–L/H(C)–L/L(D)b H.F. Wang et al. (2007) Suaeda acuminata (C. A. Meyer) Moquin-Tandon Heterospermy Dimorphic –c H.L. Wang et al. (2012) S. aralocaspica (Bunge) Freitag & Schütze Heterospermy Dimorphic H/H(br)–L/L(bl)b L. Li et al. (2007);L.Wang et al. (2008); Liu et al. (2009); Abudureheman et al. (2012) S. corniculata (C. A. Meyer) Bunge subsp. mongolica Heterospermy Dimorphic –c Cao et al. (2012); Yang Lomon. & Freitag et al. (2012) Suaeda linifolia Pallas Heterospermy Dimorphic –c Zhang et al. (2010)

ASTERACEAE Garhadiolus papposus Boissier and Buhse Heterocarpy Trimorphic H/H(CA)–I/I(IA)–L/L(PA)d Sun et al. (2008, 2009) Heteracia szovitsii Fischer and Meyer Heterocarpy Trimorphic H/H(CA)–I/I(IA)–L/L(PA)d Cheng (2009); Cheng and Tan (2009) Senecio subdentatus Ledeb. Heterocarpy Dimorphic –d,e Mamut et al. (2011)

BORAGINACEAE Lappula duplicicarpa N. Pavl. Heterocarpy Dimorphic H/H(LN)–L/L(SN)d Ma et al. (2010); J.J. Lu et al. (2013b) L. semiglabra (Ledeb.) Gurke var. heterocaryoides M. Heterocarpy Dimorphic H/H(LN)–L/L(SN)d Ma et al. (2010) Pop. ex C. J. Wang

BRASSICACEAE Diptychocarpus strictus (Fisch. ex M. Bieb.) Trautv. Heterospermy Dimorphic H/H(uds)–L/L(lis)c J.J. Lu et al. (2010)

a The first pair of letters refers to the first morph, the second pair to the second morph (dimorphic, trimorphic and polymorphic diaspores), the third pair to the third morph (trimorphic and polymorphic diaspores) and the fourth pair to the fourth morph (only S. brachiata). The first letter of a pair of letters for a morph refers to dispersal ability and the second letter to germinability/degree of dormancy. H, high dispersal ability or high percentage germination (i.e. low degree of dormancy); L, low dispersal ability or low percentage germination (i.e. high degree of dormancy); I, intermediate dispersal ability or intermediate germination percentage (i.e. intermediate degree of dormancy); A, B, C, D, a, c, f, diaspore morphs; CA, central achenes; PA, peripheral achenes; IA, intermediate achenes, i.e. located between CA and PA in the capitulum of Asteraceae; (hubr), humped fruits with brown seeds; (flbl), flat fruits with black seeds; (ebr), brown achenes covered with more-extended bracteoles; (ebl), black achenes covered with less-extended bracteoles; (l-wf), longer-winged fruits; (s-wf), shorter-winged fruits; (br), brown seeds; (bl), black seeds; (SN), nutlets with short glochids; (LN), nutlets with long glochids; (uds), upper dehiscent fruits with mucilaginous, winged seeds; (lis), lower indehiscent fruits with non-mucilaginous, non-winged seeds. b Dispersal ability of morphs inferred based on diaspore morphology (see text) c Dispersal not studied or inferred. In Atriplex dimorphostegia, flat fruits were less dormant than humped fruits after removal of the permanently attached “fruit bracts” from the dispersal units. In Chenopodium album, Suaeda acuminata L., Suaeda corniculata var. mongolica and S. linifolia, brown seeds are nondormant and black seeds physiologically dormant. d Dispersal ability of morphs compared by actual studies e Germination not studied in enough detail to determine if differences exist between PA and CA; also, fresh achenes not tested seven species. For eight of the species, our assignment of relative 2009) was CA > IA > PA. Wind dispersal of the mucilaginous, winged dispersal ability is inferred (see below) based on comparative mor- seeds (dispersal unit) produced in upper dehiscent fruits of the phology of the diaspores of individual species, and for five species fruit and seed dimorphic species Diptychocarpus strictus was much dispersal ability was neither measure nor inferred (Table 1). greater than that of the nonmucilaginous, nonwinged seeds that For C. arenarius, the rank order of dispersal by wind, mam- are retained in the lower indehiscent fruits of this species (Lu et al., mals and ants of dispersal units a (basicarp at ground level), c 2010). (middle of plant canopy) and f (periphery of plant canopy) was In the two dimorphic species Lappula duplicicarpa and L. f>c>a(Lu et al., 2013a). The rank order for wind dispersal ability semiglabrata var. heterocaryoides, nutlets with long (LN) and/or of achenes in central (CA), peripheral (PA) and intermediate (IA) short (SN) glochids are produced by flowers in an inflorescence, positions of capitula of the trimorphic species Garhadiolus pap- and the SN/LN ratio varies from 4:0 at the bottom of the infructes- posus (Sun et al., 2008) and Heteracia szovitsii (Cheng and Tan, cence to 0:4 at the top. Thus, SN, which are firmly attached to the 96 J.M. Baskin et al. / Perspectives in Plant Ecology, Evolution and Systematics 16 (2014) 93–99 mother plant, are mostly produced at the bottom of the infructes- produces dimorphic diaspores; none of the several papers on hete- cence and the LN, which are not firmly attached to the mother rocarpy in the species was cited in any of these three papers. Thus, plant, at the top (Ma et al., 2010; Lu et al., 2013b). For both Lap- germination of the two morphs was not compared. The high germi- pula species, dispersal by wind, mammals and ants was LN > SN nation percentages obtained in all three studies indicate that only (Ma et al., 2010). Finally, although peripheral and central achenes (or mostly) black (or green, sensu Yu et al., 2009) seeds were tested of the dimorphic species Senecio subdentatus differ in color, size, (see above). mass, length of pappus and micromorphology, they did not dif- Khan et al. (2001) collected seeds of H. glomeratus in the Great − fer in dispersal distance in the field at wind speeds of 1–2 m s 1 Basin Desert of western USA and stored them dry at 4 ◦C for a short (Mamut et al., 2011). (“fall to late fall”) period of time before germination experiments As stated above, relative dispersal ability for diaspores of each were carried out. Germination percentages were >70% to c. 95% of eight species was inferred based on comparisons of their mor- at 15/25, 20/30 and 25/35 ◦C in a 12-h photoperiod. After 2 days phology. Using two examples, we will illustrate how the inferences of incubation at 25/35, c. 95% of the seeds had germinated in dis- were made. For the dimorphic species Atriplex micrantha (Liu and tilled water and >80% in a 200 mM NaCl solution. Ahmed and Khan Wei, 2007), black seeds with more extended braceoles than those (2010) collected seeds of H. glomeratus in and stored them of brown seeds should be more easily transported by wind. For dry at 4 ◦C (length of storage period not given) before initiation the trimorphic species Salsola affinis (H.-F Wang and Wei, 2007), of germination experiments. They also obtained high germination type A fruits with long wings should have greater dispersal abil- percentages at 15/25, 20/30 and 25/35 ◦C in a 12-h photoperiod. ity than type B fruits with no wings and Type C fruits with short Using a modified Timson index of germination velocity ( G/t, wings. where G is the cumulative germination percentage at 2-day inter- vals and t is the total germination period) (Khan and Ungar, 1984) and monitoring germination at 2-day intervals for 20 days, the ger- Degree of dormancy and germination of diaspores mination rate at 20/30 ◦C was 48 out of a possible maximum of 50, i.e. 1000/20 = 50. The number 48 shows that the majority of seeds In 19 of the 20 species listed in Table 1, information was pro- had germinated by the second day, the first time they were checked vided on diaspore dormancy; S. subdentatus is the exception. The for germination. diaspores of each of the 19 species differ in depth of dormancy Y. Lu et al. (2012) collected seeds of H. glomeratus from plants including (1) no dormancy vs. dormancy, (2) degree of dormancy growing in a gravel desert in Xinjiang Province (China) and stored and (3) no dormancy vs. degree of dormancy. In most cases, the dor- them in a ventilated room at −5to30◦C from November to May mant diaspore(s) have nondeep physiological dormancy (nondeep before they were used in germination experiments. The stored PD) (sensu Baskin and Baskin, 2004). Thus, dormancy was broken seeds germinated to 70–80% at 5–40 ◦C in both constant light and by scarification (Mandák, 2003; Liu and Wei, 2007; H.F. Wang et al., constant darkness. TG50 (time required for 50% of the total seed 2007; Wei et al., 2007a,b; Gao et al., 2008;L.Wang et al., 2008; Yu number to germinate) was 24 (15 ◦C)–36 h at 10–30 ◦C in dark and et al., 2009; Yang et al., 2012); dry storage (afterripening) (Tisdale 28–44 h in light. Presumably seeds in constant dark were exposed and Zappetini, 1953; Gao et al., 2008;L.Wang et al., 2008; Cheng, to light when they were checked for germination at 4-h intervals 2009; Yu et al., 2009; Sun et al., 2009; J.J. Lu et al., 2010); cold strat- for the first four days of the incubation period and then at 12-h ification (Williams and Harper, 1965; Mandák, 2003; Liu and Wei, intervals for the next 11 days; use of a green safe light not men- 2007; Wei et al., 2007a,b; Liu et al., 2009; Zhang et al., 2010; Yang tioned. These three studies show that fresh seeds (presumably most et al., 2012; He et al., 2013); removal of bracteoles/perianth (Koller, of them the black morph) of H. glomeratus are nondormant or have 1957;W.Li et al., 2008; Wei et al., 2008); gibberellic acid (L. Wang a low degree of PD, i.e. fresh seeds may have been dormant and et al., 2008; Cheng, 2009; H.L. Wang et al., 2012; Yang et al., 2012); afterripened during storage (see Cronin, 1965). The studies also and/or potassium nitrate (KNO3)(Williams and Harper, 1965; Wei suggest that the seeds of this species are very fast germinating (see et al., 2007a; Yao et al., 2010c). below). However, while the central (CA) achenes of the trimorphic Diaspores of six of the Amaranthaceae species in our study are species G. papposus (Sun et al., 2009) and H. szovitsii (Cheng, very fast germinating (sensu Parsons, 2012), i.e. germinate in <24 h. 2009) have nondeep PD, the intermediate (IA) and peripheral (PA) In most of these cases, one of the two (dimorphic) or more (trimor- achenes appear to have intermediate PD. Further, the peripheral phic/polymorphic) diaspores is fast-germinating, while the other achenes are more dormant than the intermediate achenes. In both one(s) is (are) slower germinating and exhibit some degree of PD. species, depth of dormancy is PA > IA > CA. While the black morph Five of the six very fast germinating species produce black and (naked utricle) in H. glomeratus has little dormancy (Tisdale and brown dimorphic seeds. Only brown seeds were fast-germinating Zappetini, 1953; Cronin, 1965; Yu et al., 2009), the brown morph in C. album (Harper et al., 1965; Yao et al., 2010c), S. corniculata (utricle enclosed by persistent perianth) is quite dormant. Lack subsp. mongolica (Yang et al., 2012; H.L. Wang et al., 2012) and of response of the brown morph to afterripening in dry storage Suaeda aralocaspica (L. Wang et al., 2008), only black seeds in H. in the laboratory (Tisdale and Zappetini, 1953; Cronin, 1965; Yu glomeratus (Tisdale and Zappetini, 1953; Cronin, 1965) and both et al., 2009) and the considerably higher vigor of embryos isolated black and brown seeds (actually fruits with bracteoles removed) in from cold-stratified than that of those isolated from laboratory- A. centralasiatica (W. Li et al., 2008). stored morphs (Cronin, 1965) suggest that the brown morph has The trimorphic heterocarpic species S. affinis produces three dis- intermediate PD. However, although the yellow seed morph of H. tinct dispersal units (i.e. utricles with perianth), Type A, Type B and glomeratus collected in Xinjiang and stored for up to 18 months Type C (Wei et al., 2007a). Utricles (i.e. dispersal units with peri- did not afterripen, scarification was very effective in overcoming anth removed) A and B are very fast germinating. TG50 of A was PD in it (Yu et al., 2009). Apparently, the yellow and green morphs about 12 h and 10 h at 25 and 30 ◦C, respectively, whereas for B of Yu et al. (2009) are equivalent to the brown and black morphs, it was about 4 h at both temperatures. In another study of germi- respectively, of American workers. nation of Salsola affinis by Wei et al. (2008), utricles (apparently We are aware of three other studies on seed germination of H. Type A) began to germinate 3 h from the beginning of imbibition, glomeratus (Khan et al., 2001; Ahmed and Khan, 2010; Y. Lu et al., whereas dispersal units (with perianth) did not begin to germinate 2012). These authors did not seem to be aware that the species until 30 h. J.M. Baskin et al. / Perspectives in Plant Ecology, Evolution and Systematics 16 (2014) 93–99 97

Life history strategy: diaspore dispersal ability and degree site (black seeds). Further studies are needed on this species to get of dormancy a complete picture of the seed dynamics of the two morphs in the field. Following Baskin et al. (2013) and J.J. Lu et al. (2013a),weuse Based on laboratory and greenhouse data, Yao et al. (2010b) three letters to designate diaspore dispersal ability: H for high (or proposed a model for the seed and reproduction dynamics of C. relatively high) dispersal ability, L for low dispersal ability and I for album, a worldwide weed native to (among other habitats) saline moderate or intermediate (between H and L) dispersal ability; and areas in the cold deserts of northern Xinjiang. A large proportion degree of dormancy: H for high percentage of germination, i.e. low of dormant black seeds is produced under favorable growth condi- degree of dormancy, L for low percentage of germination, i.e. high tions and a large proportion of nondormant brown seeds under (or relatively high) degree of dormancy and I for moderate percent- stressful conditions, including high salinity. These results of an age of germination or moderate degree of dormancy for a morph. increase in proportion of dormant seeds with an increase in envi- In which case, diaspore dispersal ability/degree of dormancy for a ronmental favorability are in contrast to those of most other such morph may be H/H, H/I, H/L, I/H, I/I, I/L, L/H, L/I or L/L. studies in which the diaspore with the highest dormancy has a Both dispersal ability (measured or inferred) and degree of dor- higher proportional increase under stressful conditions than the mancy were identified for 14 of the species (Table 1). In all of these one with the lowest dormancy (see J.J. Lu et al., 2012 and refer- species, except A. tatarica, both diaspores of seven of the eight ences therein). However, Tielbörger and Petru (2010) obtained a dimorphic species and two of the three or more diaspores of all negative relationship between environmental favorability (dry vs. six trimorphic/polymorphic species were H/H–L/L for these two wet) for plant growth and germination fraction of offspring of two life history states. Diaspores of the trimorphic species G. papposus species of annuals from a Mediterranean site in Israel. Black seeds (Sun et al., 2008, 2009) and H. szovitsii (Cheng, 2009; Cheng and of C. album are capable of forming a persistent seed bank, whereas Tan, 2009) and the dispersal-germination units of the polymorphic brown seeds are not. Individual plants in favorable conditions for amphi-basicarpic species C. arenarius (J.J. Lu et al., 2013a) exhibit growth produce more (total) seeds than those in stressful condi- an inverse-linear relationship between these two life history traits. tions. Since large plants produce more seeds, their offspring may be Thus, CA and morph f are H/H, PA and morph a L/L and IA and morph predicted to experience more competition from siblings (Cheplick, c I/I. Morph B of Atriplex aucheri and S. affinis, the two other trimor- 1992, 1993). The model of Yao et al. (2010b) depicts the potential phic species in Table 1 for which dispersal ability and degree of ecological differences at the life cycle and population levels that dormancy can be identified are H/L and L/H, respectively. In the may result from black vs. brown seeds. However, it needs to be sup- polymorphic species S. brachiata, two of the four diaspore morphs plemented with field data on the seed bank and on the demography are H/H, one L/L and one L/H. of this species. We view the inverse linear relationship between dispersal and The most complete model published to date on the comparative dormancy in G. papposus, H. szovitsii and C. arenarius as a refinement dynamics of the biology of diaspores of a heteromorphic species of the two-state (H/H–L/L) strategy. As far as we are aware, G. pap- native to the deserts of northern Xinjiang is the one by Cao et al. posus, H. szovitsii and C. arenarius are the only three heteromorphic (2012) on S. corniculata subsp. mongolica. This is the only one of the species (worldwide) for which this combination of dispersal and three that (1) is field based, (2) gives a season-by-season account of germination/dormancy has been recognized. However, Leontodon seed dormancy/nondormancy status and germination, along with a taraxacoides (Vill.) Mérat subsp. longirostris Finch & Sell (Aster- few-word description of temperature, precipitation and soil salin- aceae), an annual in the semiarid grasslands of southeastern Spain, ity in the habitat or (3) quantifies the states (e.g. survival) in the also appears to have H/H–I/I–L/L (Hensen, 1999). We are not aware life cycle. The model begins with an input of 1000 (10 replicates of of any theory or speculation on the ecological role of H/L or L/H 100) seeds for each of the two seed morphs and ends with seeds that diaspores in the life history of heteromorphic plants. In any case, it went into the seed bank (only black seeds, 63%) and with those that is interesting that seven of eight dimorphic and six of six trimor- gave rise to adult plants (black seeds 0.5%, brown seeds 0.4%). This phic/polymorphic species in our study in which dispersal ability model demonstrates the real-world differences that exist between and degree of dormancy could be determined produce at least one the two morphs in seed dormancy, germination and seed bank for- H/H and one L/L diaspore. mation. However, it is based only on the results for one population for 1 year and a total of only the 26 and 28 seedlings that emerged from 1000 black and 1000 brown seeds sown, respectively. To more Conceptual models of diaspore dynamics in Xinjiang cold fully document ecological reality, such models need to be based on desert species studies of more than one year and preferably of more than one population. Conceptual models have been used to summarize the dynamics of certain aspects of the life history of three of the 20 species cov- ered in this review: S. aralocaspica (L. Wang et al., 2008), C. album Comparison of diaspore heteromorphism in Xinjiang with (Yao et al., 2010a) and S. corniculata subsp. mongolica (Cao et al., that in other regions 2012). All three species produce dimorphic black and brown seeds. At maturity, the black seeds are dormant and the brown ones non- The cold deserts of northern Xinjiang Province, China, are rich dormant. The model for S. aralocaspica covers only seed dormancy, in heteromorphic species due at least in part to the high number germination and potential to form a persistent seed bank, i.e. no of annual heterodiasporous chenopods (Amaranthaceae) native to post-germination stages. The model plus other information in the them (Table 1). Diaspore heteromorphism has been studied in more paper indicate that black seeds have lower dispersal ability and species in Central Asian deserts than in any other biogeoclimatic higher dormancy and are more likely to form a persistent seed zone on earth. The only other paper that brings together infor- bank than brown seeds. Interestingly, although the brown seeds mation on diaspore dispersal and dormancy for a relatively large are nondormant at maturity they can be induced into dormancy number of heteromorphic species from a single biogeoclimatic (seeds viable but did not germinate) by high salinity. These differ- region is the one by Ellner (1986). His study included information ences represent two ecological strategies in S. aralocaspica, i.e. (1) on achene dispersal ability and degree of dormancy in 13 dimor- explore new habitats (brown seeds), and (2) maintain the home phic ligulate species of Asteraceae from the Middle Eastern deserts. 98 J.M. Baskin et al. / Perspectives in Plant Ecology, Evolution and Systematics 16 (2014) 93–99

Ellner’s findings on these life history traits are similar to what has Beneke, K., Von Teichman, I., Van Rooyen, M.W., Theron, G.K., 1992c. Fruit poly- been found for northern Xinjiang deserts, namely that a high num- morphism in ephemeral species of Namaqualand: I. Anatomical differences ber and proportion (10 of 13 in Ellner’s study) of heteromorphic between polymorphic diaspores of two Dimorphotheca species. S. Afr. J. Bot. 58, 448–455. species have an H/H–L/L strategy with respect to diaspore dispersal Beneke, K., Von Teichman, I., Van Rooyen, M.W., Theron, G.K., 1992d. Fruit poly- ability and degree of dormancy/germinability. morphism in ephemeral species of Namaqualand: II. Anatomical differences Seven heterodiasporous species, six of which are annuals, were between polymorphic diaspores of Arctotis fastuosa and Ursinia cakilefolia. S. Afr. J. Bot. 58, 456–460. included in a classification of life strategies of species in a semi- Braza, R., Garcia, M.B., 2011. Spreading recruitment over time to cope with environ- desert grassland in southeastern Spain by Hensen (1999). However, mental variability. Plant Ecol. 212, 283–292. although dispersal behavior was reported for all seven species, the Bruns, B.F., 1965. The effects of fresh water storage on the germination of certain weed seeds. Weeds 13, 38–40. only germination data presented were those for 6-month-old dias- Bruns, B.F., Rasmussen, L.W., 1958. The effects of fresh water storage on the ger- pores of the trimorphic Asteraceae species Leontodon taraxacoides mination of certain weed seeds. III. Quackgrass, green bristlegrass, yellow var. longirostris, for which the dispersal-dormancy formula appears bristlegrass, watergrass, pigweed, and halogeton. Weeds 6, 42–47. Cao, D., Baskin, C.C., Baskin, J.M., Yang, F., Huang, Z., 2012. Comparison of germination to be H/H–I/I–L/L. Thus, the relationship between dispersal and and seed bank dynamics of dimorphic seeds of the cold desert halophyte Suaeda dormancy strategy cannot be determined for the other six hetero- corniculata subsp. mongolica. Ann. Bot. 110, 1545–1558. diasporous species. Cheng, X.J., (M.S. thesis), 2009. Ecological Adaptive Strategies of Breeding System and Heterocarpy in Ephemeral Heteracia szovitsii. Xinjiang Agricultural Univer- Apparently many annual ephemeral heteromorphic species sity, Urumqi, China (in Chinese with English abstract). occur in Namaqualand, an arid region in northwestern South Africa Cheng, X.J., Tan, D.Y., 2009. Bet-hedging in heteromorphic achenes of Heteracia (Beneke et al., 1993). Germination and anatomy of the achenes of szovitsii (Asteraceae), a desert ephemeral. Chin. J. Plant Ecol. 33, 901–910 (in four achene heteromorphic species of Asteraceae from this area Chinese with English abstract). Cheplick, G.P., 1992. Sibling competition in plants. J. Ecol. 80, 567–575. have been studied by Beneke et al. (1992a,b,c,d, 1993). Based on Cheplick, G.P., 1993. Sibling competition as a consequence of restricted dispersal in germination data and presence/absence of wings and pappus on an annual cleistogamous grass. Ecology 74, 2161–2164. the diaspores, dispersal-germinability/dormancy for each of the Cronin, E.H., 1965. Ecological and physiological factors influencing chemical control of Halogeton glomeratus. USDA Tech. Bull. 1325, 1–65. four species is as follows: Dimorphotheca polyptera DC., H/H–L/L; Dowling, R.E., 1933. The reproduction of Plantago coronopus: an example of mor- Dimorphotheca sinuata DC. (trimorphic), H/H–H/L–L/L; Arctotis fas- phological and biological seed dimorphism. Ann. Bot. 47, 861–872. tuosa Jacq., L/L–L/L; and Ursinia cakilefolia DC., H/H–L/L. Thus, three El-Keblawy, A., 2003. Effects of achene dimorphism on dormancy and progeny traits in the two ephemerals Hedypnois cretica and aspera (Asteraceae). Can. J. of the four species have an H/H–L/L combination for diaspore dis- Bot. 81, 550–559. persal and germination. Low dispersal ability and low germination Ellner, S., 1986. Germination dimorphisms and parent-offspring conflict in seed (high dormancy) for both morphs of A. fastuosa appear to be the germination. J. Theor. Biol. 123, 173–185. Esashi, Y., Leopold, A.C., 1968. Physical forces in dormancy and germination of Xan- first such record for a diaspore-dimorphic species. thium seeds. Plant Physiol. 43, 871–876. Gao, R., Wei, Y., Yan, C., 2008. Amphicarpy and seed germination behavior of Cera- Acknowledgements tocarpus arenarius L. (Chenopodiaceae). Chin. J. Ecol. 27, 23–27 (in Chinese with English abstract). Gardocki, M.E., Zablocki, H., El-Keblawy, A., Freeman, D.C., 2000. Heterocarpy in This work was supported in part by the National Science Calendula micrantha (Asteraceae): the effects of competition and availability of Foundation of China (NSFC 31160063, 31160093, U1130301) water on the performance of offspring from different fruit morphs. Evol. Ecol. Res. 2, 701–718. and the Major National Scientific Research Program of China Hall, J.C., Tisdale, T.E., Donohue, K., Wheeler, A., Al-Yahya, M.A., Kramer, E.M., 2011. (2014CB954200-2). Convergent evolution of a complex fruit structure in the tribe Brassiceae (Brass- icaceae). Am. J. Bot. 98, 1989–2003. Harper, J.L., Williams, J.T., Sagar, G.R., 1965. The behaviour of seeds in soil, I. The References heterogeneity of soil surfaces and its role in determining the establishment of plants from seed. J. Ecol. 53, 273–286. Abudureheman, B., Yan, C., Liu, Y.F., Wei, Y., 2012. Seed size, germination character- He, M.X., Du, X.F., Chen, J., Lü, X.Y., Lan, H.Y., 2013. Effects of salt, alternating istics, and seed production pattern of Borsczowia aralocaspica in different growth temperature and hormone treatments on seed germination and seedling estab- years. Chin. J. Ecol. 31, 844–849 (in Chinese with English abstract). lishment of Suaeda aralocaspica (Chenopodiaceae) dimorphic seeds. Chin. J. Ecol. Aguado, M., Martinez-Sánchez, J., Reig-Arminana,˜ J., García-Breijo, F.J., Franco, J.A., 32, 45–51 (in Chinese with English abstract). Vicente, M.J., 2011. Morphology, anatomy and germination response of het- Hensen, I., 1999. Life strategies in a semi-arid grassland community – mechanisms eromorpic achenes of Anthemis chrysantha J. Gray (Asteraceae), a critically of dispersal and reproduction within Lapiedro martinezii-Stipetum tenacissimae endangered species. Seed Sci. Res. 21, 283–294. (southeastern Spain). Fedd. Repert. 110, 265–285. Ahmed, M.Z., Khan, M.A., 2010. Tolerance and recovery responses of playa halo- Holl, R.G., 1954. Study of the ecology and control of halogeton in Idaho–Part II. J. phytes to light, salinity and temperature during seed germination. Flora 205, Range Manage. 7 (4), 243–244 (Annual student issue, 1 September, 1954). 764–771. Hou, H.Y., 1983. Vegetation of China with reference to its geographical distribution. APG-III (The Angiosperm Phylogeny Group), 2009. An update of the Angiosperm Ann. Missouri Bot. Gard. 70, 509–548. Phylogeny Group classification for the orders and families of flowering plants: Imbert, E., 1999. The effects of achene dimorphism on the dispersal in time and APG-III. Bot. J. Linn. Soc. 161, 105–121. space in Crepis sancta (Asteraceae). Can. J. Bot. 77, 508–513. Baker, G.A., O’Dowd, D.J., 1982. Effects of parent plant density on the production of Imbert, E., 2002. Ecological consequences and ontogeny of seed heteromorphism. achene types in the annual Hypochoeris glabra. J. Ecol. 70, 201–215. Persp. Plant Ecol., Evol. Syst. 5, 13–36. Barker, N.P., 2005. A review and survey of basicarpy, geocarpy, and amphicarpy in Khan, M.A., Gul, B., Weber, D.J., 2001. Seed germination characteristics of Halogeton the African and Madagascan flora. Ann. Missouri Bot. Gard. 92, 445–462. glomeratus. Can. J. Bot. 79, 1189–1194. Baskin, J.M., Baskin, C.C., 1976. Germination dimorphism in Heterotheca subaxillaris Khan, M.A., Ungar, I.A., 1984. The effect of salinity and temperature on the germina- var. subaxillaris. Bull. Torrey Bot. Club 103, 201–206. tion of polymorphic seeds and growth of Atriplex triangularis Willd. Am. J. Bot. Baskin, J.M., Baskin, C.C., 2004. A classification system for seed dormancy. Seed Sci. 71, 481–489. Res. 14, 1–16. Kochánková, J., Mandák, B., 2009. How do population genetic parameters affect ger- Baskin, J.M., Lu, J.J., Baskin, C.C., Tan, D.Y., 2013. The necessity for testing germination mination of the heterocarpic species Atriplex tatarica (Amaranthaceae)? Ann. of fresh seeds in studies on diaspore heteromorphism as a life-history strategy. Bot. 103, 1303–1313. Seed Sci. Res. 23, 83–88. Koller, D., 1957. Germination-regulating mechanisms in some desert seeds. IV. Beneke, K., Van Rooyen, M.W., Theron, G.K., 1992a. Fruit polymorphism in Atriplex dimorphostegia Kar. et Kir. Ecology 38, 1–13. ephemeral species of Namaqualand: V. Intramorphic competition among plants Koller, D., 1970. Analysis of the dual action of white light on germination of Atriplex cultivated from dimorphic diaspores. S. Afr. J. Bot. 58, 461–468. dimorphostegia (Chenopodiaceae). Israel J. Bot. 19, 499–516. Beneke, K., Van Rooyen, M.W., Theron, G.K., 1992b. Fruit polymorphism in Li, L., Yang, X.L., Wang, W.H., 2007. Response of germination of dimorphic seeds of ephemeral species of Namaqualand: VI. Intermorphic competition among plants Borsczowia aralocaspica to habitat conditions. Arid Zone Res. 24, 830–834 (in cultivated from dimorphic diaspores. S. Afr. J. Bot. 58, 469–477. Chinese with English abstract). Beneke, K., Van Rooyen, M.W., Theron, G.K., Van de Venter, H.A., 1993. Li, W., An, P., Liu, X., Khan, M.A., Tsuji, W., Tanaka, K., 2008. The effect of Fruit polymorphism in ephemeral species of Namaqualand: III. Germina- light, temperature and bracteoles on germination of polymorphic seeds of tion differences between the polymorphic diaspores. J. Arid Environ. 24, Atriplex centralasiatica Iljin under saline conditions. Seed Sci. Technol. 36, 333–344. 325–338. J.M. Baskin et al. / Perspectives in Plant Ecology, Evolution and Systematics 16 (2014) 93–99 99

Li, W., Liu, X., Hanada, A., Khan, M.A., 2011. Effect of cold stratification, scarifica- Talavera, M., Arista, M., Ortiz, P.L., 2012. Evolution of dispersal traits in a biogeo- tion and hormones on germination of dimorphic seeds of Atriplex centralasiatica graphical context: a study using the heterocarpic Rumex bucephalophorus as a under saline conditions. Seed Sci. Technol. 39, 82–92. model. J. Ecol. 100, 1194–1203. Liu, P.W., Wei, Y., 2007. Seed dimorphism and germination behavior of Atriplex Tielbörger, K., Petru, M., 2010. An experimental test for effects of the maternal micrantha, an annual inhabiting Junggar Desert. Acta Ecol. Sin. 27, 4233–4239 environment on delayed germination. J. Ecol. 98, 1216–1223. (in Chinese with English abstract). Tisdale, E.W., Zappetini, G., 1953. Halogeton studies on Idaho ranges. J. Range Man- Liu, Y.F., Wei, Y., Yan, C., 2009. Germination characteristics and ecological adaptation age. 6, 225–236. of dimorphic seeds of Borsczowia aralocaspica. Acta Ecol. Sin. 29, 6609–6614 (in Venable, D.L., 1985. The evolutionary ecology of seed heteromorphism. Am. Nat. Chinese with English abstract). 126, 577–595. Lu, J.J., Ma, W.B., Tan, D.Y., Baskin, J.M., Baskin, C.C., 2013b. Effects of environmental Venable, D.L., Búrquez, A., Corral, G., Morales, E., Espinosa, F., 1987. The ecology of stress and nutlet morph on proportion and within-flower number-combination seed heteromorphism in Heterosperma pinnatum in central Mexico. Ecology 68, of morphs produced by the fruit-dimorphic species Lappula duplicicarpa (Bor- 65–76. aginaceae). Plant Ecol. 214, 351–362. Venable, D.L., Levin, D.A., 1985a. Ecology of achene dimorphism in Heterotheca lati- Lu, J.J., Tan, D.Y., Baskin, J.M., Baskin, C.C., 2010. Fruit and seed heteromorphism folia. I. Achene structure, germination and dispersal. J. Ecol. 73, 133–145. in the cold desert annual ephemeral Diptychocarpus strictus (Brassicaceae) and Venable, D.L., Levin, D.A., 1985b. Ecology of achene dimorphism in Heterotheca lati- possible adaptive significance. Ann. Bot. 105, 999–1014. folia. II. Demographic variation within populations. J. Ecol. 73, 743–755. Lu, J.J., Tan, D.Y., Baskin, J.M., Baskin, C.C., 2012. Phenotypic plasticity and bet- Walter, H., Box, E.O., 1983. The deserts of . In: West, N.E. (Ed.), Ecosystems hedging in a heterocarpic winter annual/spring ephemeral cold desert species of the World 5. Temperate Deserts and Semi-deserts. Elsevier, New York, pp. of Brassicaceae. Oikos 121, 357–366. 193–236. Lu, J.J., Tan, D.-Y., Baskin, J.M., Baskin, C.C., 2013a. Tradeoffs between seed dis- Wang, C.W., 1961. The Forests of China. Marie Moors Cabot Foundation for Botanical persal and dormancy in an amphi-basicarpic cold desert annual. Ann. Bot. 112, Research (Harvard University) Publication Number 5. 1815–1827. Wang, H.F., Wei, Y., 2007. Seed polymorphism and fruit-set patterns of Salsola affinis. Lu, Y., Lei, J.Q., Zeng, F.J., Liu, G.J., Gao, H.H., Sun, Y.G., 2012. Factors influencing seed Biodiv. Sci. 15, 419–424 (in Chinese with English abstract). germination and seedling emergence of Halogeton glomeratus (Bieb.) C. A. Mey. Wang, H.F., Wei, Y., Huang, Z.Y., 2007. Seed polymorphism and germination of Sal- (Chenopodiaceae), a dominant annual halophyte inhabiting the gravel deserts sola bracchita [brachiata], a dominant desert annual inhabiting Junggar Basin of of Xinjiang, China. Seed Sci. Technol. 40, 283–298. Xinjiang, China. J. Plant Ecol. (Chinese Version) 31, 1046–1053 (in Chinese with Ma, W.B., Zhao, X.J., Tan, D.Y., Baskin, C.C., Baskin, J.M., Xue, J.H., 2010. Nutlet English abstract). dimorphism in individual flowers of two cold desert annual Lappula species Wang, H.L., Wang, L., Tian, C.Y., Huang, Z.Y., 2012. Germination dimorphism in (Boraginaceae): implications for escape by offspring in time and space. Plant Suaeda acuminata: a new combination of dormancy types for heteromorphic Ecol. 209, 361–374. seeds. S. Afr. J. Bot. 78, 270–275. Mamut, J., Tan, D.Y., Cheng, X.J., 2011. Ecological significance of fruit heteromor- Wang, L., Huang, Z.Y., Baskin, C.C., Baskin, J.M., Dong, M., 2008. Germination of dimor- phism in the annual ephemeral Senecio subdentatus. Chin. J. Plant Ecol. 35, phic seeds of the desert annual halophyte Suaeda aralocaspica (Chenopodiaceae), 663–671 (in Chinese with English abstract). aC4 plant without Kranz anatomy. Ann. Bot. 102, 757–769. Mandák, B., 1997. Seed heteromorphism and the life cycle of plants: a review. Preslia Wei, Y., Dong, M., Huang, Z.Y., 2007a. Seed polymorphism, dormancy and germina- 69, 129–159. tion of Salsola affinis (Chenopodiaceae), a dominant desert annual inhibiting the Mandák, B., 2003. Germination requirements of invasive and non-invasive Atriplex Junggar basin of Xinjiang, China. Aust. J. Bot. 55, 464–470. species: a comparative study. Flora 198, 45–54. Wei, Y., Dong, M., Huang, Z.Y., Tan, D.Y., 2008. Factors influencing seed germination Mandák, B., Pysek,ˇ P., 1999. Effects of plant density and nutrient levels on fruit of Salsola affinis (Chenopodiaceae), a dominant annual halophyte inhabiting the polymorphism in Atriplex sagittata. Oecologia 119, 63–72. deserts of Xinjiang, China. Flora 203, 134–140. McArthur, E.D., Sanderson, S.C., 1984. Distribution, systematics and evolution of Wei, Y., Liu, P.W., An, S.Z., 2007b. Study on fruit polymorphism and germination Chenopodiaceae. In: Tiedemann, A.R., McArthur, E.D., Stutz, H.C. Stevens, R., measures of Atriplex aucheri Moq. seeds. Arid Zone Res. 24, 835–839 (in Chinese Johnson, K.L. (compilers), Proceedings – Symposium on the Biology of Atriplex with English abstract). and Related Chenopods, 1983 May 2–6; Provo, UT. Gen. Tech Rept. INT-172. Williams, J.T., Harper, J.L., 1965. Seed polymorphism and germination. I. The influ- U.S. Department of Agriculture, Forest Service, Intermountain Forest and Range ence of nitrates and low temperatures on the germination of Chenopodium Experiment Station, Ogden, UT. pp. 14–24. album. Weed Res. 5, 141–150. Parsons, R.F., 2012. Incidence and ecology of very fast germination. Seed Sci. Res. 22, Williams, M.C., 1960. Biochemical analyses, germination, and production of black 161–167. and brown seed of Halogeton glomeratus. Weeds 8, 452–461. Payne, A.M., Maun, M.A., 1981. Dispersal and floating ability of dimorphic fruit Xu, J., Yin, H., Yang, L., Xie, Z., Liu, X., 2011. Differential salt tolerance in seedlings segments of Cakile edentula var. lacustris. Can. J. Bot. 59, 2595–2602. from dimorphic seeds of Atriplex centralasiatica: from physiology to molecular Petrov, M., 1973 [1976]. Deserts of the World. Translation of Pastyni Zemnoa Shara analysis. Planta 233, 859–871. from Russian, izdatel’stovo “Nauka.” Leningrad, 1973 by the Israel Program for Yang, F., Cao, D.C., Yang, X.J., Gao, R.R., Huang, Z.Y., 2012. Adaptive strategies of Scientific Translations, Jerusalem. John Wiley and Sons, New York. dimorphic seeds of the desert halophyte Suaeda corniculata [subsp. mongolica]in Rai, J.P.N., Tripathi, R.S., 1982. Adaptive significance of seed reserves in ray achenes saline habitats. Chin. J. Plant Ecol. 36, 781–790 (in Chinese with English abstract). in Galinsoga parviflora Cav. Experientia 38, 804–805. Yao, S., Chen, S., Zhao, J., Xu, D., Lan, H., Zhang, F., 2010a. Effect of three salts Robocker, W.G., Williams, M.C., Evans, R.A., Torell, P.J., 1969. Effect of age, burial, on germination and seedling survival of Chenopodium album. Botany 88, and region on germination and viability of halogeton seed. Weed Sci. 17, 63–65. 821–828. Ruiz de Clavijo, E., 1994. Heterocarpy and seed polymorphism in Ceratocapnos het- Yao, S., Lan, H., Zhang, F., 2010b. Variation of seed heteromorphism in Chenopodium erocarpa (Fumariaceae). Int. J. Plant Sci. 155, 196–202. album and the effect of salinity stress on the descendants. Ann. Bot. 105, Ruiz de Clavijo, E., 2001. The role of dimorphic achenes in the biology of the annual 1015–1025. weed Leontodon longirrostris. Weed Res. 41, 275–286. Yao, S., You, T., Xu, D., Li, X., Wang, J., Lan, H., 2010c. Seed heteromorphism and Sorensen, A.E., 1978. Somatic polymorphism and seed dispersal. Nature 276, germination mechanism of Chenopodium album in Xinjiang Arid Region. Acta 174–176. Ecol. Sin. 30, 2909–2918 (in Chinese with English abstract). Sun, H.Z., Lu, J.J., Tan, D.Y., Baskin, J.M., Baskin, C.C., 2009. Dormancy and germination Yu, X., Yan, C., Wei, Y., 2009. Germination of dimorphism seeds in Halogeton glomer- characteristics of the trimorphic achenes of Garhadiolus papposus (Asteraceae), atus (Chenopodiaceae). Acta Ecol. Sin. 29, 1616–1621 (in Chinese with English an annual ephemeral from the Junggar Desert, China. S. Afr. J. Bot. 75, 537–545. abstract). Sun, H.Z., Tan, D.Y., Qu, R.M., 2008. Characteristics of heteromorphic achenes of Zappetini, G., 1953. The of Halogeton glomeratus. Am. Midl. Nat. 50, Garhadiolus papposus, an ephemeral Asteraceae, with reference to their adapta- 238–247. tions to desert environment. Biodiv. Sci. 16, 353–361 (in Chinese with English Zhang, Y.M., Wei, Y., Yan, C., 2010. Phenology and fruit-set pattern of Suaeda linifolia. abstract). J. Xinjiang Agric. Univ. 33, 187–191 (in Chinese with English abstract).