Lower dormancy with rapid germination is an important strategy for seeds in an arid zone with unpredictable rainfall

English version

Autoři: Corrine Duncan ^aff001; Nick Schultz ^aff001; Wolfgang Lewandrowski ^aff002; Megan K. Good ^aff004; Simon Cook ^aff001
Působiště autorů: School of Health and Life Sciences, Federation University, Mt Helen, VIC, Australia ^aff001; Kings Park Science, Department of Biodiversity, Conservation and Attractions, Kings Park, WA, Australia ^aff002; School of Biological Sciences, The University of Western Australia, Crawley, WA, Australia ^aff003; School of BioSciences, The University of Melbourne, Melbourne, VIC, Australia ^aff004
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0218421

Souhrn

Seed germination traits are key drivers of population dynamics, yet they are under-represented in community ecology studies, which have predominately focussed on adult plant and seed morphological traits. We studied the seed traits and germination strategy of eight woody plant species to investigate regeneration strategies in the arid zone of eastern Australia. To cope with stochastic and minimal rainfall, we predict that arid seeds will either have rapid germination across a wide range of temperatures, improved germination under cooler temperatures, or dormancy and/or longevity traits to delay or stagger germination across time. To understand how temperature affects germination responses, seeds of eight keystone arid species were germinated under laboratory conditions, and under three diurnal temperatures (30/20°C, 25/15°C and 17/7°C) for 30 days. We also tested for decline in seed viability across 24 months in a dry-aging treatment (~20°C). Six of the eight arid species studied had non-dormant, rapidly germinating seeds, and only two species had physiological dormancy traits. Seed longevity differed widely between species, from one recalcitrant species surviving only months in aging (P50 = <3 months) and one serotinous species surviving for many years (P50 = 84 months). Our results highlight the importance of understanding the reproductive strategies of plant species in arid environments. Rapid germination, the dominant seed trait of species included in this study, allows arid species to capitalise on sporadic rainfall. However, some species also exhibit dormancy and delayed germination; this an alternative strategy which spreads the risk of germination failure over time.

Klíčová slova:

Biology and life sciences – Plant science – Organisms – Eukaryota – Plants – Engineering and technology – Population biology – Population dynamics – Developmental biology – Embryology – Embryos – Equipment – Ecology and environmental sciences – Ecology – Plant physiology – Plant anatomy – Ecosystems – Laboratory equipment – Seeds – Plant reproduction – Seed germination – Seedlings – Shrubs – Filter paper

Zdroje

1. Larson J, Funk J. Regeneration: an overlooked aspect of trait-based plant community assembly models. Journal of Ecology. 2016;104: 1284–98.

2. Guo Q, Brown J, Valone T, Kachman S. Constraints of seed size on plant distribution and abundance. Ecology. 2000;81: 2149–55.

3. Wagner F, Rossi V, Baraloto C, Bonal D, Stahl C, Hérault B. Are Commonly Measured Functional Traits Involved in Tropical Tree Responses to Climate? International Journal of Ecology. 2014;2014: 1–10.

4. Kleyer M, Bekker R, Knevel I, Bakker J, Thompson K, Sonnenschein M, et al. The LEDA Traitbase: A database of life‐history traits of the Northwest European flora. Journal of Ecology. 2008;96: 1266–74.

5. Pérez-Harguindeguy N, Díaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, et al. New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany. 2013;61: 167–234.

6. Saatkamp A, Cochrane A, Commander L, Guja L, Jimenez-Alfaro B, Larson J, et al. A research agenda for seed-trait functional ecology. New Phytol. 2019;221: 1764–75. doi: 10.1111/nph.15502 30269352

7. Kleyer M, Minden V. Why functional ecology should consider all plant organs: An allocation-based perspective. Basic and Applied Ecology. 2015;16: 1–9.

8. Jiménez‐Alfaro B, Silveira F, Fidelis A, Poschlod P, Commander L. Seed germination traits can contribute better to plant community ecology. Journal of Vegetation Science. 2016;27: 637–45.

9. Pierce S, Bottinelli A, Bassani I, Ceriani R, Cerabolini B. How well do seed production traits correlate with leaf traits, whole-plant traits and plant ecological strategies? Plant Ecology. 2014;215: 1351–9.

10. Huang Z, Liu S, Bradford K, Huxman T, Venable L. The contribution of germination functional traits to population dynamics of a desert plant community. Ecology. 2016;97: 250–61. doi: 10.1890/15-0744.1 27008793

11. Moles A, Westoby M. Seedling survival and seed size: a synthesis of the literature. Journal of Ecology. 2004;92: 372–83.

12. Norden N, Daws M, Antoine C, Gonzalez M, Garwood N, Chave J. The relationship between seed mass and mean time to germination for 1037 tree species across five tropical forests. Funct Ecology. 2008;23: 203–10.

13. Gomaa N, Picó F. Seed germination, seedling traits, and seed bank of the tree Moringa peregrina (Moringaceae) in a hyper‐arid environment. American Journal of Botany. 2011;98: 1024–30. doi: 10.3732/ajb.1000051 21653511

14. Westoby M, Jurado E, Leishman M. Comparative evolutionary ecology of seed size. Trends in Ecology and Evolution 1992;7: 368–72. doi: 10.1016/0169-5347(92)90006-W 21236070

15. Baraloto C, Forget P, D. G. Seed mass, seedling size and neotropical tree seedling establishment. Journal of Ecology. 2005;93: 1156–66.

16. Westoby M, Falster D, Moles A, Vesk P, Wright I. Plant ecological strategies: Some leading dimensions of variation between species. Annual Review of Ecology and Systematics. 2002;33: 125–59.

17. Saatkamp A, Poschlod P, Venable D. The functional role of soil seed banks in natural communities. In: Gallagher R, editor. Seeds—the ecology of regeneration in plant communities. 3 ed. Wallingford, UK: CABI; 2014. p. 263–94.

18. Long R, Gorecki M, Renton M, Scott J, Colville L, Goggin D, et al. The ecophysiology of seed persistence: a mechanistic view of the journey to germination or demise. Biological Reviews. 2015;90: 31–59. doi: 10.1111/brv.12095 24618017

19. Donohue K. Seeds and seasons: interpreting germination timing in the field. Seed Science Research. 2005;15: 175–87.

20. Simons A, Johnston M. Variation in seed traits of Lobelia inflata (Campanulaceae): sources and fitness consequences. American Journal of Botany. 2000;87: 124–32. 10636835

21. Hoyle G, Steadman K, Good R, McIntosh E, Galea L, Nicotra A. Seed germination strategies: an evolutionary trajectory independent of vegetative functional traits. Frontiers in Plant Science. 2015;6 (Oct): 1–13. doi: 10.3389/fpls.2015.00001 25653664

22. Al-Shamsi N, El-Keblawy A, Mosa K, Navarro A. Drought tolerance and germination response to light and temperature for seeds of saline and non-saline habitats of the habitat-indifferent desert halophyte Suaeda vermiculata. Acta Physiologiae Plantarum. 2018;40: 1–13.

23. Zeng Y, Wang Y, Zhang J. Is reduced seed germination due to water limitation a special survival strategy used by xerophytes in arid dunes? Journal of Arid Environments. 2010;74: 508–11.

24. Choinski J, Tuohy J. Effect of water potential and temperature on the germination of 4 species of African savanna trees. Annals of Botany. 1991;68: 227‐33.

25. Salazar A, Goldstein G, Franco A, Miralles-Wilhelm F. Timing of seed dispersal and dormancy, rather than persistent soil seed-banks, control seedling recruitment of woody plants in Neotropical savannas. Seed Science Research. 2011;21: 103–16.

26. Poschlod P, Abedi M, Bartelheimer M, Drobnik J, Rosbakh S, Saatkamp A. Seed ecology and assembly rules in plant communities. In: van der Maarel E, Franklin J, editors. Vegetation Ecology. 2nd ed. Hoboken: Wiley-Blackwell; 2013. p. 164–202.

27. Grime J, Mason G, Curtis A. A comparative study of germination characteristics in a local flora. Journal of Ecology. 1981;69: 1017–59.

28. Vivrette N. Distribution and ecological significance of seed-embryo types in Mediterranean climates in California, Chile, and Australia. In: Arroyo M, Zedler P, Fox M, editors. Ecology and Biogeography of Mediterranean Ecosystems in Chile, California and Australia. New York, USA: Springer Verlag; 1995. p. 274–88.

29. Vandelook F, Janssens S, Probert R. Relative embryo length as an adaptation to habitat and life cycle in Apiaceae. New Phytologist. 2012;195: 479–87. doi: 10.1111/j.1469-8137.2012.04172.x 22621412

30. Gremer J, Kimball S, Venable D. Within and among year germination in Sonoran Desert winter annuals: bet hedging and predictive germination in a variable environment. Ecology Letters. 2016;19: 1209–18. doi: 10.1111/ele.12655 27515951

31. Lewandrowski W, Erickson T, Dalziell E, Stevens J. Ecological niche and bet-hedging strategies for Triodia (R.Br.) seed germination. Annals of Botany. 2018;121: 367–75. doi: 10.1093/aob/mcx158 29293867

32. Commander L, Golos P, Miller B, Merritt D. Seed germination traits of desert perennials. Plant Ecology. 2017;218: 1077–91.

33. Tielbörger K, Petruů M, Lampei C. Bet‐hedging germination in annual plants: a sound empirical test of the theoretical foundations. Oikos. 2012;121: 1860–8.

34. Baskin C, Baskin J. Classification, biogeograhpy, and phylogenetic relationships of seed dormancy. In: Smith R, Dickie J, Linington S, Pritchard H, Probert R, editors. Seed conservation: turning science into practice. London: The Royal Botanic Gardens, Kew; 2003. p. 518–44.

35. Volis S, Bohrer G. Joint evolution of seed traits along an aridity gradient: Seed size and dormancy are not two substitutable evolutionary traits in temporally heterogeneous environment. New Phytologist. 2013;197: 655–67. doi: 10.1111/nph.12024 23171296

36. Brown J, Venable D. Evolutionary ecology of seed-bank annuals in temporally varying environments. American Naturalist. 1986;127: 31–47.

37. Harel D, Holzapfel C, Sternberg M. Seed mass and dormancy of annual plant populations and communities decreases with aridity and rainfall predictability. Basic and Applied Ecology. 2011;12: 674–84.

38. Bochet E, García-Fayos P, Alborch B, Tormo J. Soil water availability effects on seed germination account for species segregation in semiarid roadslopes. Plant and Soil. 2007;295: 179–91.

39. Jurado E, Westoby M. Germination biology of selected central Australian plants. Australian Journal of Ecology. 1992;17: 341–8.

40. Parsons R. Incidence and ecology of very fast germination. Seed Science Research. 2012;22: 161–7.

41. Chesson P, Gebauer R, Schwinning S, Huntly N, Wiegand K, Ernest M, et al. Resource pulses, species interactions, and diversity maintenance in arid and semi-arid environments. Oecologia. 2004;141: 236–53. doi: 10.1007/s00442-004-1551-1 15069635

42. Sluiter I, Schultz N. Rehabilitation report on 2017 monitoring of revegetation at the Ginkgo Mineral Sands Mine. Merbein, VIC: Ogyris Pty. Ltd. and Cristal Mining Australia Ltd, 2017.

43. BOM. Monthly rainfall and temperature data: Pooncarie Mail Agency: Commonwealth of Australia, Bureau of Meteorology; 2018 [12 Oct 2018]. Available from: http://www.bom.gov.au/climate/data/.

44. Baskin C, Baskin J. A revision of Martin's seed classification system, with particular reference to his dwarf-seed type. Seed Science Research. 2007;17: 11–20.

45. Martin A. The comparative internal morphology of seeds. American Midland Naturalist. 1946;36: 513–660.

46. Baskin C, Baskin J. Seeds: Ecology, biogeography and evolution of dormancy and germination. 2nd ed. San Diego, USA: Academic Press; 2014.

47. Turner S, Merritt D, Ridley E, Commander L, Baskin J, Baskin C, et al. Ecophysiology of Seed Dormancy in the Australian Endemic Species Acanthocarpus preissii (Dasypogonaceae). Annals of Botany. 2006;98: 1137–44. doi: 10.1093/aob/mcl203 17008351

48. Sweedman L, Merritt D. Australian Seeds–a guide to their collection, identification and biology. Collingwood, Victoria: CSIRO Publishing; 2006.

49. Ellis R, Roberts H. Improved equations for the prediction of seed longevity. Annals of Botany. 1980;45: 13–30.

50. R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2018.

51. Environdata. WeatherMation Live: Historical data from Gingko weather station Warwick, Qld: Environdata; 2018 [15 February 2019]. Available from: https://www.weathermation.net.au/.

52. Gutterman Y. Regeneration of plants in arid ecosystems resulting from patch disturbance. Dordrecht, Kluwer: Springer; 2001.

53. Ogyris. Preliminary report on the flora of the Ginkgo Sand Mine Prospect near Pooncarie, Southwest New South Wales. Ogyris Ecological Research, Mildura VIC: Prepared for BeMaX Resources NL., 2000.

54. Read I. The Bush. A guide to the vegetated landscapes of Australia Frenchs Forest, NSW: Reed Books; 1987.

55. Callister K. Casuarina pauper (belah) woodlands of Northwest Victoria: Monitoring and regeneration. Mt Helen, Victoria: University of Ballarat; 2004.

56. Wallace A, Rhoads W, Frolich E. Germination behaviour of Salsola as influenced by temperature, moisture, depth of planting and gamma irradiation. Agronomy Journal. 1968;60: 76–8.

57. Leishman M, Westoby M. The role of seed size in seedling establishment in dry soil conditions—experimental evidence from semi-arid species. Journal of Ecology. 1994;82: 249–58.

58. Bergholz K, Jeltsch F, Weiss L, Pottek J, Geißler K, Ristow M. Fertilization affects the establishment ability of species differing in seed mass via direct nutrient addition and indirect competition effects. Oikos. 2015;124: 1547–54.

59. Lebrija-Trejos E, Reich P, Hernández A, Wright S. Species with greater seed mass are more tolerant of conspecific neighbours: A key driver of early survival and future abundances in a tropical forest. Ecology Letters. 2016;19: 1071–80. doi: 10.1111/ele.12643 27346439

60. Moles A. Being John Harper: Using evolutionary ideas to improve understanding of global patterns in plant traits. Journal of Ecology. 2018;106: 1–18.

61. Moles A, Hodson D, Webb C. Seed size and shape and persistence in the soil in the New Zealand flora. Oikos. 2000;89: 541–5.

62. Callister K, Florentine S, Westbrooke M. An investigation of the soil seedbank and seed germination of perennial species in Belah (Casuarina Pauper) woodlands in north-west Victoria. Australian Journal of Botany. 2018;66: 202–12.

63. Dalziell E, Tomlinson S. Reduced metabolic rate indicates declining viability in seed collections: an experimental proof-of-concept. Conservation Physiology. 2017;5. Available from: https://doi.org/10.1093/conphys/cox058.

64. Bell D. The process of germination in Australian species. Australian Journal of Botany. 1999;47: 475–517.

65. Ooi M. Dormancy classification and potential dormancy-breaking cues for shrub species from fire-prone south-eastern Australia. Adkins S, Ashmore S& Navie S eds Seeds: Biology, Development and Ecology. Oxfordshire, UK: CAB International; 2007. p. 205–16.

66. Auld T. The ecology of the Rutaceae in the Sydney region of south-eastern Australia: poorly known ecology of a neglected family. Cunninghamia. 2001;7: 213–39.

67. Martyn A, Seed L, Ooi M, Offord C. Seed fill, viability and germination of NSW species in the family Rutaceae. Cunninghamia. 2009;11: 203–12.

68. Fan B, Zhou Y, Ma Q, Yu Q, Zhao C, Sun K. The bet-hedging strategies for seedling emergence of Calligonum mongolicum to adapt to the extreme desert environments in northwestern China. Frontiers in Plant Science. 2018;9:[1167 p.]. Available from: https://doi.org/10.3389/fpls.2018.01167.

69. Meyer S, Carlson S, Garvin S. Seed germination regulation and field seed bank carryover in shadscale (Atriplex confertifolia: Chenopodiaceae). Journal of Arid Environments. 1998;38: 255–67.

70. Meyer S. Atriplex L. In: Bonner F, Karrfalt R, Nisley R, editors. The Woody Plant Seed Manual Agriculture Handbook 727 Part II—Specific Handling Methods and Data for 236 Genera. USA: United States Department of Agriculture and Forest Service; 2008. p. 283–90.

71. Sluiter I, Sluiter K. Pre-clearance vegetation and soils report of land at Cristal Mining Australia Ltd. Murray-Darling Basin Sites: Snapper Mine–Autumn 2015. Ogyris Pty. Ltd. and Cristal Mining Australia Ltd, 2015.

72. Gremer J, Venable D. Bet hedging in desert winter annual plants: optimal germination strategies in a variable environment. Ecology Letters. 2014;17: 380–7. doi: 10.1111/ele.12241 24393387

73. Venable D. Bet hedging in a guild of desert annuals. Ecology. 2007;88: 1086–90. doi: 10.1890/06-1495 17536393

74. de Waal C, Anderson B, Ellis A. Dispersal, dormancy and life-history tradeoffs at the individual, population and species levels in southern African Asteraceae. New Phytologist. 2016;210: 356–65. doi: 10.1111/nph.13744 26555320

75. Rees M. Trade-offs among dispersal strategies in British plants. Nature. 1993;366: 150–2.

76. Thompson K, Bakker J, Bekker R, Hodgson J. Ecological correlates of seed persistence in soil in the north‐west European flora. Journal of Ecology. 1998;86: 163–9.

77. Letnic M, Dickman C, Gayle M. Bet‐hedging and germination in the Australian arid zone shrub Acacia ligulata Austral Ecology. 2000;25: 368–74.

78. Auld T. Soil seedbank patterns of four trees and shrubs from arid Australia. Journal of Arid Environments. 1995;29: 33–45.

79. Wotton N. Aspects of the autecology of the Pearl Bluebush, Mairenana Sedifolia. Adelaide, SA: University of Adelaide; 1993.

80. Murdoch F. Restoration ecology in the semi-arid woodlands of North-west Victoria: Federation University, Ballarat, VIC; 2005.

81. Chesterfield C, Parsons R. Regeneration of three tree species in arid South-eastern Australia. Australian Journal of Botany. 1985;33: 715–32.

82. Govt of SA. Significant flora fact sheet: Bullock Bush, Rosewood, Alectryon oliefolius. 2010. [19 August 2019]; Available from: https://www.naturalresources.sa.gov.au/aridlands/plants-and-animals/native-plants-and-animals/native-plants.

83. Tuljapurkar S. Delayed reproduction and fitness in variable environments. Proceedings of the National Academy of Sciences, USA. 1990;87: 1139–43.

84. Rees M. Delayed germination of seeds: a look at the effects of adult longevity, the timing of reproduction, and population age/stage structure. American Naturalist. 1994;144: 43–64.

85. Groom P, Lamont B. Fruit‐seed relations in Hakea: Serotinous species invest more dry matter in predispersal seed protection. Australian Journal of Ecology. 1997;22: 352–5.

86. Bradshaw S, Dixon K, Hopper S, Lambers H, Turner S. Little evidence for fire-adapted plant traits in Mediterranean climate regions. Trends in Plant Science. 2011;16: 69–76. doi: 10.1016/j.tplants.2010.10.007 21095155

87. Hall E, Specht R, Eardley C. Regeneration of the vegetation on Koonamore Vegetation Reserve, 1926–1962. Australian Journal of Botany. 1964;12.

88. Snyder R. Multiple risk reduction mechanisms: can dormancy substitute for dispersal? Ecology Letters. 2006;9: 1106–14. doi: 10.1111/j.1461-0248.2006.00962.x 16972874

89. Siewert W, Tielbörger K. Dispersal-dormancy relationships in annual plants: putting model predictions to the test. American Naturalist. 2010;176: 490–500. doi: 10.1086/656271 20738207

90. Klinkhamer P, de Jong T, Metz J, Val J. Life history tactics of annual organisms: the joint effects of dispersal and delayed germination. Theoretical Population Biology. 1987;32: 127–56.

91. Merritt D, Martyn A, Ainsley P, Young R, Seed L, Thorpe M, et al. A continental-scale study of seed lifespan in experimental storage examining seed, plant, and environmental traits associated with longevity. Biodiversity and Conservation. 2014;23: 1081–104.

92. Probert R, Daws M, Hay F. Ecological correlates of ex situ seed longevity: a comparative study on 195 species. Annals of Botany. 2009;104: 57–69. doi: 10.1093/aob/mcp082 19359301

93. Merritt D. Seed longevity of Australian species. Australasian Plant Conservation: Journal of the Australian Network for Plant Conservation. 2014;22: 8–10.

94. Zeineddine M, Jansen V. To age, to die: parity, evolutionary tracking and Cole’s paradox. Evolution. 2009;63: 1498–507. doi: 10.1111/j.1558-5646.2009.00630.x 19492994

95. Ehrlén J, Van Groenendael J. The trade-off between dispersability and longevity: an important aspect of plant species diversity. Applied Vegetation Science. 1998;1: 29–36.

Lower dormancy with rapid germination is an important strategy for seeds in an arid zone with unpredictable rainfall

Souhrn

Klíčová slova:

Zdroje

PLOS One

Aktuální možnosti diagnostiky a léčby litiáz