Research article |
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Germination strategies of annual and short-lived perennial species in the Arabian Desert |
Arvind BHATT1, David J GALLACHER2,*(), Paulo R M SOUZA-FILHO3 |
1Lushan Botanical Garden, Chinese Academy of Sciences, Jiujiang 332900, China 2School of Life and Environmental Sciences, The University of Sydney, Narrabri NSW 2390, Australia 3Multidisciplinary Center of Barra, Federal University of Western Bahia, Barra 47100-000, Brazil |
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Abstract Germination timing is highly regulated in short-lived plant species since it strongly influences recruitment success of vegetation. In deserts, the spatiotemporal distribution of plant-available water is highly episodic and unpredictable, making winter months more favorable for seed germination when other abiotic conditions co-occur. We hypothesized that changes in photoperiod and thermoperiod would impact germination more in seeds that had undergone in situ storage. We assessed 21 annual and short-lived perennial species in the Arabian Desert to find (1) if seeds were dormant at maturity, (2) if in situ seed storage increased germination percentage compared with no storage, (3) if photoperiod and thermoperiod germination requirements were influenced by in situ storage, and (4) if a phylogenetic association in seed germination could be observed. Seeds of each species collected in early 2017 were divided into two batches. One was tested for germination within one week (fresh seeds). The other was stored in situ at the maternal location (stored seeds) until October 2017 and tested for seed germination in the first week of November. Seed germination was conducted in incubators at two thermoperiods (15°C/20°C and 20°C/30°C; 12 h/12 h), and two photoperiods (12 and 0 h light per day). Results indicated that seed germination percentages of 13 species were significantly enhanced by in situ storage. A thermoperiod response was exhibited by stored, but not fresh seeds. Light exposure increased germination of fresh seeds but had only a minimal effect on stored seeds. Germination traits exhibited no phylogenetic correlation. This result indicated that selection pressure for germination strategy was stronger than that for taxonomic traits of these desert species.
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Received: 09 March 2020
Published: 10 November 2020
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Corresponding Authors:
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About author: *David J GALLACHER (E-mail: d.gallacher@sydney.edu.au)
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[1] |
Adondakis S, Venable D L. 2004. Dormancy and germination in a guild of Sonoran Desert annuals. Ecology, 85(9):2582-2590.
|
|
|
[2] |
Almazroui M, Islam N M, Athar H, et al. 2012. Recent climate change in the Arabian Peninsula: annual rainfall and temperature analysis of Saudi Arabia for 1978-2009. International Journal of Climatology, 32(6):953-966.
|
|
|
[3] |
Atia A, Smaoui, A, Barhoumi Z, et al. 2011. Differential response to salinity and water deficit stress in Polypogon monspeliensis (L.) Desf. provenances during germination. Plant Biology, 13(3):541-545.
doi: 10.1111/j.1438-8677.2010.00401.x
pmid: 21489106
|
|
|
[4] |
Baker K S, Steadman K J, Plummer J A, et al. 2005 The changing window of conditions that promotes germination of two fire ephemerals, Actinotus leucocephalus (Apiaceae) and Tersonia cyathiflora (Gyrostemonaceae). Annals of Botany, 96(7):1225-1236.
|
|
|
[5] |
Barua D, Butler C, Tisdale T E, et al. 2012. Natural variation in germination responses of Arabidopsis to seasonal cues and their associated physiological mechanisms. Annals of Botany, 109(1):209-226.
doi: 10.1093/aob/mcr264
pmid: 22012958
|
|
|
[6] |
Baskin C C, Baskin J M. 2014. Seeds: Ecology, Biogeography, and Evolution of Dormancy and Germination (2nd ed.). San Diego: Academic Press, 666.
|
|
|
[7] |
Baskin J M, Baskin C C. 1988. Role of temperature in regulating the timing of germination in Portulaca oleracea. Canadian Journal of Botany, 66:563-567.
|
|
|
[8] |
Baskin J M, Baskin C C. 2004. A classification system for seed dormancy. Seed Science Research, 14(1):1-16.
|
|
|
[9] |
Bates D, Mullen K M, Nash J C, et al. 2014. Minqa: Derivative-Free Optimization Algorithms by Quadratic Approximation. R package version 1.2.4.[2020-02-10]. http://CRAN. R-project.org/package=minqa.
|
|
|
[10] |
Bhatt A, Carón M M, Verheyen K, et al. 2016a. Germination and seedling performance of five native legumes of the Arabian Desert. Flora, 220:125-133.
|
|
|
[11] |
Bhatt A, Pérez-García F, Phondani P C. 2016b. Foliage colour influence on seed germination of Bienertia cycloptera in Arabian Desert. Nordic Journal of Botany, 34(4):428-434.
|
|
|
[12] |
Bhatt A, Phondani P C, Phartyal S S, et al. 2016c. Influence of aerial seed banks on germination response in three desert plant species. Journal of Plant Ecology, 10(6):994-1000.
|
|
|
[13] |
Bhatt A, Pérez-García F, Mercedes Carón M, et al. 2016d. Germination response of Salsola schweinfurthii (Chenopodiaceae) to salinity and winged perianth removal. Seed Science and Technology, 44(2):428-434.
|
|
|
[14] |
Bhatt A, Gairola S, El-Keblawy A. 2016e. Seed colour affects dormancy and germination requirements in two species of Lotus (Fabaceae). Revista de Biologia Tropical, 64:483-492.
doi: 10.15517/rbt.v64i2.18575
pmid: 29451749
|
|
|
[15] |
Bhatt A, Pérez-García F. 2016. Seed dormancy of Ochradenus baccatus (Resedaceae), a shrubby species from Arabian desert regions. Revista de Biologia Tropical, 64:965-974.
|
|
|
[16] |
Bhatt A, Santo A. 2017. Effects of photoperiod, thermoperiod, and salt stress on Gymnocarpos decandrus seeds: potential implications in restoration ecology activities. Botany, 95(11):1093-1098.
|
|
|
[17] |
Bhatt A, Santo A. 2018. Different ecological strategies during the seed germination phase of nine grasses inhabiting the hyper-arid Arabian Desert. Plant Species Biology, 33(4):305-311.
|
|
|
[18] |
Böer B. 1997. An introduction to the climate of the United Arab Emirates. Journal of Arid Environments, 35(1):3-16.
|
|
|
[19] |
Burns J H, Strauss S Y. 2011. More closely related species are more ecologically similar in an experimental test. Proceedings of the National Academy of Sciences of the United States of America, 108(13):5302-5307.
|
|
|
[20] |
Capon B, van Asdall W. 1967. Heat pre-treatment as a means of increasing germination of desert annual seeds. Ecology, 48(2):305-306.
|
|
|
[21] |
Carta A, Probert R J, Moretti M, et al. 2014. Seed dormancy and germination in three Crocus ser. verni species (Iridaceae): implications for evolution of dormancy within the genus. Plant Biology, 16(6):1065-1074.
pmid: 24533601
|
|
|
[22] |
Clauss M J, Venable D L. 2000. Seed germination in desert annuals: an empirical test of adaptive bet hedging. The American Naturalist, 155(2):168-186.
doi: 10.1086/303314
pmid: 10686159
|
|
|
[23] |
Commander L E, Merritt D J, Rokich D P, et al. 2009. The role of after-ripening in promoting germination of arid zone seeds: a study on six Australian species. Botanical Journal of the Linnean Society, 161(4):411-421.
|
|
|
[24] |
de Clavijo E R. 2005. The reproductive strategies of the heterocarpic annual Calendula arvensis (Asteraceae). Acta Oecologica, 28(2):119-126.
|
|
|
[25] |
Délye C M, Jasieniuk V, Le Corre V. 2013. Deciphering the evolution of herbicide resistance in weeds. Trends in Genetics, 29(11):649-658.
doi: 10.1016/j.tig.2013.06.001
pmid: 23830583
|
|
|
[26] |
Donohue K. 2002. Germination timing influences natural selection on life-history characters in Arabidopsis thaliana. Ecology, 83(4):1006-1016.
|
|
|
[27] |
Donohue K, Rubio de Casas R, Burghardt L, et al. 2010. Germination, postgermination adaptation, and species ecological ranges. Annual Review of Ecology, Evolution, and Systematics, 41:293-319.
|
|
|
[28] |
El-Keblawy A, Al Neyadi S S, Rao M V, et al. 2011. Interactive effects of salinity, light and temperature on seed germination of sand dunes glycophyte Cyprus conglomeratus growing in the United Arab Emirates deserts. Seed Science and Technology, 39(2):364-376.
|
|
|
[29] |
El-Keblawy A, Bhatt A, Gairola S. 2013. Perianth colour affects germination behaviour in wind-pollinated Salsola rubescens in Arabian deserts. Botany, 92(1):69-75.
|
|
|
[30] |
El-Keblawy A. 2017. Light and temperature requirements during germination of potential perennial grasses for rehabilitation of degraded sandy Arabian deserts. Land Degradation & Development, 28(5):1687-1695.
|
|
|
[31] |
El-Keblawy A, Gairola S. 2017. Dormancy regulating chemicals alleviate innate seed dormancy and promote germination of desert annuals. Journal of Plant Growth Regulation, 36:300-311.
|
|
|
[32] |
Erickson T E. 2015. Seed dormancy and germination traits of 89 arid zone species targeted for mine-site restoration in the Pilbara region of Western Australia. Ph. Dissertation. Perth: University of Western Australia.
|
|
|
[33] |
Evans A S, Cabin R J. 1995. Can dormancy affect the evolution of post-germination traits? The case of Lesquerella fendleri. Ecology, 76(2):344-356.
|
|
|
[34] |
Fenner M, Thompson K. 2005. The Ecology of Seeds. Cambridge: Cambridge University Press, 250.
|
|
|
[35] |
Finch-Savage W E, Leubner-Metzger G. 2006. Seed dormancy and the control of germination. New Phytologist, 171(3):501-523.
|
|
|
[36] |
Gallart M, Verdú A M C, Mas M T. 2008. Dormancy breaking in Digitaria sanguinalis seeds: the role of the caryopsis covering structures. Seed Science and Technology, 36(2):259-270.
|
|
|
[37] |
Gutterman Y. 1972. Delayed Seed dispersal and rapid germination as survival mechanisms of the desert plant Blepharis persica (Burm.). Knntze. Oecologia, 10:145-149.
doi: 10.1007/BF00347986
pmid: 28306860
|
|
|
[38] |
Gutterman Y. 2002. Survival Strategies of Annual Desert Plants. Heidelberg: Springer, 348.
|
|
|
[39] |
Gutterman Y. 2012. Seed Germination in Desert Plants. New York: Springer Science & Business Media, 253.
|
|
|
[40] |
Harel D, Holzapfel C, Sternberg M. 2011. Seed mass and dormancy of annual plant populations and communities decreases with aridity and rainfall predictability. Basic and Applied Ecology, 12(8):674-684.
|
|
|
[41] |
Holdsworth M J, Bentsink L, Soppe W J J. 2008. Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytologist, 179(1):33-54.
|
|
|
[42] |
Hothorn T, Bretz F, Westfall P. 2008. Simultaneous inference in general parametric models. Journal of Mathematical Methods in Biosciences, 50(3):346-363.
|
|
|
[43] |
Jombart T, Dray S. 2008. Adephylo: Exploratory analyses for the phylogenetic comparative method. Bioinformatics, 26:1907-1909.
doi: 10.1093/bioinformatics/btq292
pmid: 20525823
|
|
|
[44] |
Jordan G L, Haferkamp M R. 1989. Temperature responses and calculated heat units for germination of several range grasses and shrubs. Rangeland Ecology & Management, 42(1):41-45.
|
|
|
[45] |
Khan M I, Hassan G, Khan I, et al. 2006. Germination of Asphodelus tenuifolius biotypes as influenced by temperature, dormancy breaking chemicals and their concentrations. Pakistan Journal of Weed Science Research, 12:313-318.
|
|
|
[46] |
Lai L M, Chen L J, Jiang L H, et al. 2016. Seed germination of seven desert plants and implications for vegetation restoration. AoB Plants, 8: plw031.
|
|
|
[47] |
Lenth R V. 2016. Least-squares means: the R package lsmeans. Journal of Statistical Software, 69:1-33.
|
|
|
[48] |
Liu K, Cao S, Du G, et al. 2018. Linking seed germination and plant height: a case study of a wetland community on the eastern Tibet Plateau. Plant Biology, 30:886-893.
|
|
|
[49] |
Liu S Z, Liu Y J, Ji Y F, et al. 2013. Seed germination of Corispermum patelliforme in different storage length at room temperature: a dominant annual plant species in the deserts of northern China. Pakistan Journal of Botany, 45:737-742.
|
|
|
[50] |
McIvor J G, Howden S M. 2000. Dormancy and germination characteristics of herbaceous species in the seasonally dry tropics of northern Australia. Austral Ecology, 25:213-222.
doi: 10.1046/j.1442-9993.2000.01026.x
pmid: 32313444
|
|
|
[51] |
Menon K, Jayakumar A P, Shahid M, et al. 2014. Seed dormancy and effect of salinity on germination of Citrullus colocynthis. International Journal of Environmental Science and Development, 5:566.
|
|
|
[52] |
Michael P J, Steadman K J, Plummer J A. 2006. Climatic regulation of seed dormancy and emergence of diverse Malva parviflora populations from a Mediterranean-type environment. Seed Science Research, 16(4):273-281.
|
|
|
[53] |
Milberg P, Andersson L, Thompson K. 2000. Large-seeded spices are less dependent on light for germination than small-seeded ones. Seed Science Research, 10(1):99-104.
|
|
|
[54] |
Mira S, González-Benito M E, Ibars A M, et al. 2011. Dormancy release and seed ageing in the endangered species Silene diclinis. Biodiversity and Conservation, 20:345-358.
|
|
|
[55] |
Murdoch A J, Ellis R H. 2000. Dormancy, viability and longevity. In: Fenner M. Seeds: the Ecology of Regeneration in Plant Communities (2nd ed.). Wallingford: CABI Publishing, 183-214.
|
|
|
[56] |
Norton J, Abdul Majid S, Allan D, et al. 2009. An Illustrated Checklist of the Flora of Qatar. Gosport: Browndown Publications, 67.
|
|
|
[57] |
Oksanen A J, Blanchet F G, Kindt R, et al. 2019. Vegan: Community Ecology Package. R package version 2.5-4. [2019-11-09]. https://cran.rproject.org/package=vegan.
|
|
|
[58] |
Omar S A S, Al-Mutawa Y, Zaman S. 2007. Vegetation of Kuwait. Kuwait: Kuwait Institute for Scientific Research, 47-89.
|
|
|
[59] |
Onofri A, Carbonell E A, Piepho H P, et al. 2010. Current statistical issues in weed research. Weed Research, 50(1):5-24.
|
|
|
[60] |
Petrie J M. 2007. Arabian desert primer: ornamental potential of hyper-arid adapted plants from Saudi Arabia. Desert Plants, 19-32.
|
|
|
[61] |
Pons T L. 2000. Seed responses to light. In: Fenner M. Seeds-the Ecology of Regeneration in Plant Communities. New York: CABI Publishing, 237-260.
|
|
|
[62] |
Revell L J. 2012. Phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3(2):217-223.
|
|
|
[63] |
Rühl A T, Eckstein R L, Otte A, et al. 2016. Distinct germination response of endangered and common arable weeds to reduced water potential. Plant Biology, 18(S1):83-90.
|
|
|
[64] |
Ruiz de Clavijo E. 2005. The reproductive strategies of the heterocarpic annual Calendula arvensis (Asteraceae). Acta Oecologica, 28(2):119-126.
|
|
|
[65] |
Sakcali MS, Serin M. 2009. Seed germination behaviour of Diplotaxis tenuifolia. EurAsian Journal of BioSciences, 3:107-112.
|
|
|
[66] |
Schütz W, Milberg P. 1997. Seed germination in Launaea arborescens: a continuously flowering semi-desert shrub. Journal of Arid Environments, 36(6):113-122.
|
|
|
[67] |
Schütz W, Milberg P, Lamont B B. 2002. Seed dormancy, after-ripening and light requirements of four annual Asteraceae in southwestern Australia. Annals of Botany, 90:707-714.
doi: 10.1093/aob/mcf250
pmid: 12451026
|
|
|
[68] |
Seglias A E, Williams E, Bilge A, et al. 2018. Phylogeny and source climate impact seed dormancy and germination of restoration-relevant forb species. PLoS ONE, 13: e0191931, https://doi. org/10.1371/journal.pone.0191931.
doi: 10.1371/journal.pone.0191931
pmid: 29401470
|
|
|
[69] |
Sileshi G W. 2012. A critique of current trends in the statistical analysis of seed germination and viability data. Seed Science Research, 22(3):145-159.
|
|
|
[70] |
Silva L M, Fernandes G W. 2014. Effect of seed storage on germination, seedling growth and survival of Mimosa foliolosa (Fabaceae): implications for seed banks and restoration ecology. Tropical Ecology, 55(3):385-392.
|
|
|
[71] |
Terradas J. 1991. Mediterranean woody plant growth-forms, biomass and production in the eastern part of the Iberian Peninsula. In: Ros J D, Prat N. Hom-age to Ramon Margalef or Why Is There Such Pleasure in Studying Nature (Oecologia aquatica; 10), Barcelona: University of Barcelona, 337-349.
|
|
|
[72] |
Therneau T M, Grambsch P M. 2000. Modeling Survival Data: Extending the Cox Model. New York, Springer. [2019-11-02]. https://doi. org/10.1007/978-1-4757-3294-8.
|
|
|
[73] |
Tudela-Isanta M, Ladouceur E, Wijayasinghe M, et al. 2018. The seed germination niche limits the distribution of some plant species in calcareous or siliceous alpine bedrocks. Alpine Botany, 128:83-95.
|
|
|
[74] |
Voigt P W, Tischler C R. 1997. Effect of seed treatment on germination and emergence of 3 warm-season grasses. Rangeland Ecology & Management, 50(2):170-174.
|
|
|
[75] |
Wang J H, Baskin C C, Cui X L, et al. 2009. Effects of phylogeny, life history and habitat correlates on seed germination of 69 arid and semi-arid zone species from Northwest China. Evolutionary Ecology, 23:827-846.
|
|
|
[76] |
Webb C O, Donoghue M J. 2005. Phylomatic: Tree assembly for applied phylogenetics. Molecular Ecology Notes, 5(1):181-183.
|
|
|
[77] |
Zanne A E, Tank D C, Cornwell W K, et al. 2014. Three keys to the radiation of angiosperms into freezing environments. Nature, 506:89-92.
doi: 10.1038/nature12872
pmid: 24362564
|
|
|
[78] |
Zhang L W, Liu H L, Zhang D Y, et al. 2015. Seed dormancy release and germination characteristics of Corispermum lehmannianum Bunge, an endemic species in the Gurbantunggut Desert of China. Phyton, 84(1):58-63.
|
|
|
[79] |
Zuur A, Elena N I, Walker N, et al. 2009. Mixed Effects Models and Extensions in Ecology with R. New York: Springer Science & Business Media, 579.
|
|
|
|
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