BET HEDGING IN HETEROMORPHIC ACHENES OF HETERACIA SZOVITSII (ASTERACEAE), A DESERT EPHEMERAL

doi:10.3773/j.issn.1005-264x.2009.05.009

Abstract

Abstract:

Aims Heteracia szovitsii is a common ephemeral Asteraceae species that germinates in early spring in the Junggar Desert of China and produces three types of achenes with different morphologies in one infructescence. To better understand how this species is adapted to its desert habitat, we studied 1) the morphological, structural and dispersal characteristics of the three types of achenes and 2) according to the bet-hedging strategy, how heterocarpy spreads the risk of survival in the desert environment.
Methods For the three types of achenes, we recorded number, mass, morphology, surface ornamentation (via scanning electron micrographs), pericarp structure, dispersal distance and landing time in the laboratory and mode of dispersal and its duration in the field.
Important findings Compared with central achenes, the pericarps of peripheral and intermediate achenes were thicker, darker in color, and contained a higher amount of phenolic compounds and more sclerenchyma, which could protect the embryo better and cause the seeds to be more dormant. Embryo mass of peripheral and intermediate achenes was greater than that of central achenes, and thus could produce larger and more competitive seedlings. After maturation, central achenes with pappus dispersed over a wide range, while peripheral and intermediate achenes with no pappus usually dispersed near the mother plant. The different number of heteromorphic achenes could spread the risk of dispersal and settlement for this species. The larger number of central achenes increases chance for their random dispersal, and this is favorable for exploiting a larger geographical range for the population. The lower number of peripheral and intermediate achenes could decrease sibling competition due to dispersal near the mother plant. Formation of heteromorphic achenes is a form of bet hedging that could spread the risk of mortality in the extreme environment of the Junggar Desert. The peripheral and intermediate achenes presumably represent a “low-risk” strategy and the central achenes a “high-risk” strategy in one capitulum. Based on these strategies, H. szovitsii can spread the risk of survival and ensure its reproductive success.

Key words: ephemerals, Heteracia szovitsii, heteromorphic achenes, achene morphology and structure, dispersal, bet hedging

CHENG Xiao-Jun, TAN Dun-Yan. BET HEDGING IN HETEROMORPHIC ACHENES OF HETERACIA SZOVITSII (ASTERACEAE), A DESERT EPHEMERAL[J]. Chin J Plant Ecol, 2009, 33(5): 901-910.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.plant-ecology.com/EN/10.3773/j.issn.1005-264x.2009.05.009

https://www.plant-ecology.com/EN/Y2009/V33/I5/901

Figures/Tables 5

References 46

[1]	An ZX (安争夕), Shen GM (沈观冕), Zhai DT (翟大彤) (1999). Flora Xinjiangensis (新疆植物志). Xinjiang Science & Technology & Hygiene Publishing House, Ürümqi, 5, 371-373. (in Chinese)
[2]	Baker GA, O’Dowd DJ (1982). Effects of parent plant density on the production of achene types in the annual Hypochoeris glabra. Journal of Ecology, 70, 201-215. DOI URL
[3]	Baskin JM, Baskin CC (1976). Germination dimorphism in Heterotheca subaxillaris var. subaxillari. Bulletin of the Torrey Botanical Club, 103, 201-206. DOI URL
[4]	Bewley JD, Black M (1982). Physiology and Biochemistry of Seeds in Relation to Germination, Vol. 2. Viability, Dormancy and Environmental Control. Springer-Verlag, Berlin.
[5]	Bradbeer JW (1988). Seed Dormancy and Germination. Blackie & Son Ltd.,Glasgow.
[6]	Brändel M (2004). Dormancy and germination of heteromorphic achenes of Bidens frondosa. Flora, 199, 228-233. DOI URL
[7]	Brändel M (2007). Ecology of achene dimorphism in Leontodon saxatilis. Annals of Botany, 100, 1189-1197. DOI URL PMID
[8]	Eriksson A, Eriksson O (1997). Seedling recruitment in semi-natural pastures: the effects of disturbance, seed size, phenology and seed bank. Nordic Journal of Botany, 17, 469-482. DOI URL
[9]	Evans MEK, Dennehy JJ (2005). Germ banking: bet-hedging and variable release from egg and seed dormancy. Quarterly Review of Biology, 80, 431-451. DOI URL
[10]	Evans MEK, Ferrière R, Kane MJ, Venable DL (2007). Bet hedging via seed banking in desert evening primroses (Oenothera, Onagraceae): demographic evidence from natural populations. The American Naturalist, 169, 184-194. DOI URL PMID
[11]	Forsyth C, Brown NAC (1982). Germination of the dimorphic fruits of Bidens pilosa L. New Phytologist, 90, 151-164. DOI URL
[12]	Gibson JP (2001). Ecological and genetic comparison between ray and disc achene pools of the heteromorphic speciesPrionopsis ciliata(Asteraceae). International Journal of Plant Sciences, 162, 137-145. DOI URL
[13]	Gravuer K, von Wettberg EJ, Schmitt J (2003). Dispersal biology of Liatris scariosa var. novae-angliae(Asteraceae), a rare New England grassland perennial. American Journal of Botany, 90, 1159-1167. DOI URL PMID
[14]	Harborne JB (1982). Introduction to Ecological Biochemistry. Academic Press, London.
[15]	Harper JL (1977). Population Biology of Plants. Academic Press, New York.
[16]	Hedrick PW, Ginevan ME, Ewing EP (1976). Genetic polymorphism in heterogeneous environments. Annual Review of Ecology, Evolution, and Systematics, 7, 1-32. DOI URL
[17]	Imbert E, Escarré J, Lepart J (1996). Achene dimorphism and among-population variation in Crepis sancta(Asteraceae). International Journal of Plant Sciences, 157, 309-315. DOI URL
[18]	Imbert E (1999). The effects of achene dimorphism on the dispersal in time and space in Crepis sancta(Asteraceae). Canadian Journal of Botany, 77, 508-513. DOI URL
[19]	Imbert E (2002). Ecological consequences and ontogeny of seed heteromorphism. Perspectives in Plant Ecology, Evolution and Systematics, 5, 13-36. DOI URL
[20]	Lloyd DG (1984). Variation strategies of plants in heterogeneous environments. Biological Journal of the Linnean Society, 21, 357-385. DOI URL
[21]	Mao ZM (毛祖美), Zhang DM (张佃民) (1994). The conspectus of ephemeral flora in northern Xinjiang. Arid Zone Research (干旱区研究), 11(3), 1-26. (in Chinese)
[22]	Mayer AM, Poljakoff-Mayber A (1982). The Germination of Seeds 3rd edn. Pergamon Press, Oxford, UK.
[23]	Maxwell CD, Zobel A, Woodfine D (1994). Somatic polymorphism in the achenes ofTragopogon dubious. Canadian Journal of Botany, 72, 1282-1288. DOI URL
[24]	McEvoy PB (1984). Dormancy and dispersal in dimorphic achenes of tansy ragwort,Senecio jacobaea L.(Compositae). Oecologia, 61, 160-168. DOI URL PMID
[25]	McEvoy PB, Cox CS (1987). Wing dispersal distances in dimorphic achenes of ragwort,Senecio jacobaea. Ecology, 68, 2006-2015. DOI URL PMID
[26]	McGinley MA (1989). Within and among plant variation in seed mass and pappus size in Tragopogon dubious. Canadian Journal of Botany, 67, 1298-1304. DOI URL
[27]	McGinley MA, Temme DH, Geber A (1987). Parental investment in offspring in variable environments: theorectical and empirical considerations. The American Naturalist, 130, 370-398. DOI URL
[28]	Meyers LA, Bull JJ (2002). Fighting change with change: adaptive variation in an uncertain world. Trends in Ecology and Evolution, 17, 551-557. DOI URL
[29]	Sakai S, Sakai A (1995). Flower size-dependent variation in seed size: theory and a test. The American Naturalist, 145, 918-934. DOI URL
[30]	Seger J, Brockmann HH (1987). What is bet-hedging? Oxford Surveys in Evolutionary Biology, 4, 182-211.
[31]	Shi Z (石铸) (1997). Asteraceae. In: Flora Reipublicae Popularis Sinicae (中国植物志), Tomus 80(1). Science Press, Beijing, 300. (in Chinese)
[32]	Silvertown JW (Translated by Zhu N (祝宁), Wang YH (王义弘), Chen WB (陈文斌))(1987). The Introduction of Population Ecology 2nd edn (in English). Northeast Forestry University Press, Harbin.(in Chinese)
[33]	Stearns SC (1992). The Evolution of Life Histories. Oxford University Press, Oxford.
[34]	Sun HZ (孙华之), Tan DY (谭敦炎), Qu RM (曲荣明) (2008). Characteristics of heteromorphic achenes of Garhadiolus papposus, an ephemeral Asteraceae species, with reference to their adaptations to desert environment. Biodiversity Science (生物多样性), 16, 353-361. (in Chinese with English abstract) DOI URL
[35]	Tanowitz BD, Salopek PF, Mahall BE (1987). Differential germination of ray and disc achenes in Hemizonia increscens(Asteraceae). American Journal of Botany, 74, 303-312. DOI URL
[36]	Telenius A (1992). Seed heteromorphism in a population of Spergularia media in relation to the ambient vegetation density. Acta Botanica Neerlandica, 41, 305-318. DOI URL
[37]	Telenius A, Torstensson P (1989). The seed dimorphism of Spergularia marina in relation to dispersal by wind and water. Oecologia, 80, 206-210. DOI URL PMID
[38]	Tuljapurkar S (1990). Delayed reproduction and fitness in variable environments. Proceedings of the National Academy of Sciences of the United States of America, 87, 1139-1143. DOI URL PMID
[39]	Venable DL (1985). The evolutionary ecology of seed heteromorphism. The American Naturalist, 126, 577-595. DOI URL
[40]	Venable DL (2007). Bet hedging in a guild of desert annuals. Ecology, 88, 1086-1090. DOI URL PMID
[41]	Venable DL, Lawlor L (1980). Delayed germination and dispersal in desert annuals: escape in space and time. Oecologia, 46, 272-282. DOI URL PMID
[42]	Venable DL, Levin DA (1985a). Ecology of achene dimorphism in Heterotheca latifolia. I.Achene structure, germination and dispersal. Journal of Ecology, 73, 113-145. DOI URL
[43]	Venable DL, Levin DA (1985b). Ecology of achene dimorphism in Heterotheca latifolia. II.Demographic variation within populations. Journal of Ecology, 73, 743-755. DOI URL
[44]	Venable DL, Burquez AM, Corral G, Morales E, Espinosa F (1987). The ecology of seed heteromorphism in Heterosperma pinnatum in Central Mexico. Ecology, 68, 65-76. DOI URL
[45]	Wang L, Huang ZY, Baskin CC, Baskin JM, Dong M (2008). Germination of dimorphic seeds of the desert annual halophyte Suaeda aralocaspica(Chenopod- iaceae), a C₄ plant without Kranz anatomy. Annals of Botany, 102, 757-769. DOI URL PMID
[46]	Zheng GC (郑国锠), Gu ZP (谷祝平) (1993). Biological Microtechnology (生物显微技术). Higher Education Press, Beijing. (in Chinese)

观测指标 Observation index	外围果 Peripheral achene	过渡果 Intermediate achene	中央果 Central achene	F	p
形状 Shape	倒四棱锥形, 背腹扁压Obpyramidal, back and front compressed	倒四棱锥形, 背腹微扁压 Obpyramidal, back and front compressed slightly	倒圆锥形, 不扁压 Turbinate, not compressed	-	-
颜色 Color	暗红色 Dark-wine	紫红色 Purple-red	灰褐色 Gray-brown	-	-
附属结构 Additional structure	两侧有较宽的翅, 腹面及背面有较宽的棱, 果喙短, 不具冠毛 Wide bilateral wings, front and back have wide ribs, fruit beak short, no pappus	两侧有较窄的翅, 腹面及背面有较窄的棱, 果喙较长, 不具冠毛 Narrow bilateral wings, front and back have narrow ribs, fruit beak elongated, no pappus	具细长的果喙, 在喙顶部有1~3轮污白色冠毛 1-3 whorls of well developed white pappus at top of elongated fruit beak	-	-
果体长 Length of achenes (mm)	3.54±0.05^Aa	3.20±0.03^Bb	3.07±0.03^Bc	43.19	＜ 0.01
两侧宽 Width from side to side (mm)	3.27±0.05^Aa	1.70±0.05^Bb	1.03±0.02^Cc	732.54	＜ 0.01
背腹宽 Width from back to front (mm)	2.25±0.05^Aa	1.42±0.04^Bb	1.00±0.03^Cc	260.37	＜ 0.01
侧翅宽 Width of lateral wing (cm)	1.21±0.03^Aa	0.71±0.03^Bb	-	148.70	＜ 0.01
腹棱宽 Width of front ribs (cm)	0.79±0.17^a	0.42±0.02^b	-	4.63	＜ 0.05
果喙长 Length of beaks (mm)	1.05±0.03^Cc	2.21±0.10^Bb	9.22±0.37^Aa	396.24	＜ 0.01
果体长/果喙长 The ratio of length of fruit body to beak	3.47±0.09^Aa	1.60±0.07^Bb	0.42±0.07^Cc	398.32	＜ 0.01
冠毛数量 No. of pappi	-	-	40.32±1.02	-	-
冠毛长 Length of pappi (mm)	-	-	3.00±0.03	-	-

观测指标 Observation index	外围果 Peripheral achene	过渡果 Intermediate achene	中央果 Central achene	F	p
形状 Shape	倒四棱锥形, 背腹扁压Obpyramidal, back and front compressed	倒四棱锥形, 背腹微扁压 Obpyramidal, back and front compressed slightly	倒圆锥形, 不扁压 Turbinate, not compressed	-	-
颜色 Color	暗红色 Dark-wine	紫红色 Purple-red	灰褐色 Gray-brown	-	-
附属结构 Additional structure	两侧有较宽的翅, 腹面及背面有较宽的棱, 果喙短, 不具冠毛 Wide bilateral wings, front and back have wide ribs, fruit beak short, no pappus	两侧有较窄的翅, 腹面及背面有较窄的棱, 果喙较长, 不具冠毛 Narrow bilateral wings, front and back have narrow ribs, fruit beak elongated, no pappus	具细长的果喙, 在喙顶部有1~3轮污白色冠毛 1-3 whorls of well developed white pappus at top of elongated fruit beak	-	-
果体长 Length of achenes (mm)	3.54±0.05^Aa	3.20±0.03^Bb	3.07±0.03^Bc	43.19	＜ 0.01
两侧宽 Width from side to side (mm)	3.27±0.05^Aa	1.70±0.05^Bb	1.03±0.02^Cc	732.54	＜ 0.01
背腹宽 Width from back to front (mm)	2.25±0.05^Aa	1.42±0.04^Bb	1.00±0.03^Cc	260.37	＜ 0.01
侧翅宽 Width of lateral wing (cm)	1.21±0.03^Aa	0.71±0.03^Bb	-	148.70	＜ 0.01
腹棱宽 Width of front ribs (cm)	0.79±0.17^a	0.42±0.02^b	-	4.63	＜ 0.05
果喙长 Length of beaks (mm)	1.05±0.03^Cc	2.21±0.10^Bb	9.22±0.37^Aa	396.24	＜ 0.01
果体长/果喙长 The ratio of length of fruit body to beak	3.47±0.09^Aa	1.60±0.07^Bb	0.42±0.07^Cc	398.32	＜ 0.01
冠毛数量 No. of pappi	-	-	40.32±1.02	-	-
冠毛长 Length of pappi (mm)	-	-	3.00±0.03	-	-

测量指标 Measurement index	外围果 Peripheral achene	过渡果 Intermediate achene	中央果 Central achene	F	p
每果序中果实数(个) No. of achenes per infructescence	7.87±0.11^Aa	10.50±0.39^Bb	14.20±0.58^Cc	60.35	＜ 0.01
果实百粒重 Mass per 100 achenes (mg)	355.07±4.01^Aa	146.05±1.10^Bb	73.06±0.84^Cc	3 566.84	＜ 0.01
胚百粒重 Mass per 100 dispersal units (mg)	54.27±0.38^Aa	43.56±0.22^Bb	37.02±0.14^Cc	1 065.67	＜ 0.01
果皮/果实质量比 Mass ratio of pericarp to achene (％)	84.79±0.18^Aa	70.16±0.18^Bb	49.27±0.60^Cc	2 269.01	＜ 0.01

测量指标 Measurement index	外围果 Peripheral achene	过渡果 Intermediate achene	中央果 Central achene	F	p
每果序中果实数(个) No. of achenes per infructescence	7.87±0.11^Aa	10.50±0.39^Bb	14.20±0.58^Cc	60.35	＜ 0.01
果实百粒重 Mass per 100 achenes (mg)	355.07±4.01^Aa	146.05±1.10^Bb	73.06±0.84^Cc	3 566.84	＜ 0.01
胚百粒重 Mass per 100 dispersal units (mg)	54.27±0.38^Aa	43.56±0.22^Bb	37.02±0.14^Cc	1 065.67	＜ 0.01
果皮/果实质量比 Mass ratio of pericarp to achene (％)	84.79±0.18^Aa	70.16±0.18^Bb	49.27±0.60^Cc	2 269.01	＜ 0.01