Some like it wet — biological characteristics underpinning tolerance of extreme water stress events in Antarctic bryophytes
Jane Wasley A D , Sharon A. Robinson A E , Catherine E. Lovelock B and Marianne Popp CA Institute of Conservation Biology, University of Wollongong, NSW 2522, Australia.
B The Centre for Marine Studies, The University of Queensland, St Lucia, Qld 4072, Australia.
C Institute of Ecology and Conservation Biology, University of Vienna, Althanstr. 14, A-1090 Vienna, Austria.
D Current address: Environmental Protection and Change in Antarctica, Department of Environment and Heritage, 203 Channel Highway Kingston, Tasmania 7050, Australia.
E Corresponding author. Email: sharonr@uow.edu.au
F This paper originates from a presentation at ECOFIZZ 2005, North Stradbroke Island, Queensland, Australia, November 2005.
Functional Plant Biology 33(5) 443-455 https://doi.org/10.1071/FP05306
Submitted: 15 December 2005 Accepted: 28 March 2006 Published: 2 May 2006
Abstract
Antarctic bryophyte communities presently tolerate physiological extremes in water availability, surviving both desiccation and submergence events. We investigated the relative ability of three Antarctic moss species to tolerate physiological extremes in water availability and identified physiological, morphological, and biochemical characteristics that assist species performance under such conditions. Tolerance of desiccation and submergence was investigated using chlorophyll fluorescence during a series of field- and laboratory-based water stress events. Turf water retention and degree of natural habitat submergence were determined from gametophyte shoot size and density, and δ13C signatures, respectively. Finally, compounds likely to assist membrane structure and function during desiccation events (fatty acids and soluble carbohydrates) were determined. The results of this study show significant differences in the performance of the three study species under contrasting water stress events. The results indicate that the three study species occupy distinctly different ecological niches with respect to water relations, and provide a physiological explanation for present species distributions. The poor tolerance of submergence seen in Ceratodon purpureus helps explain its restriction to drier sites and conversely, the low tolerance of desiccation and high tolerance of submergence displayed by the endemic Grimmia antarctici is consistent with its restriction to wet habitats. Finally the flexible response observed for Bryum pseudotriquetrum is consistent with its co-occurrence with the other two species across the bryophyte habitat spectrum. The likely effects of future climate change induced shifts in water availability are discussed with respect to future community dynamics.
Keywords: Antarctica, chlorophyll fluorescence, climate change, desiccation, δ13C, fatty acids, soluble carbohydrates, submergence.
Acknowledgments
This research was supported by grant funding and logistic support from the Australian Antarctic Division and an Australian Postgraduate Award to JW. We thank all members of ANARE who helped us with field work in Antarctica. We especially thank Johanna Turnbull and Jodie Dunn for their assistance with field work and Dr Wolfgang Wanek for running the stable isotope analyses. Dr Peter Convey and two anonymous reviewers provided helpful suggestions to improve this manuscript.
Anderson WH,
Hawkins J,
Gellerman JL, Schlenk H
(1974) Fatty acid composition as a criterion in the taxonomy of mosses. Journal of the Hattori Botanical Laboratory 38, 99–103.
Andersson B,
Anderson WH,
Chipault J,
Ellison E,
Fenton S,
Gellerman JL,
Hawkins J, Schlenk H
(1974) 9,12,15-Octadecatrien-6-ynoic acid, a new acetylenic acid from mosses. Lipids 9, 506–511.
Barsig M,
Schneider K, Gehrke C
(1998) Effects of UV-B radiation on fine-structure carbohydrates and pigments in Polytrichum commune. The Bryologist 101, 357–365.
| Crossref |
Bottger T,
Schidlowski M, Wand U
(1993) Stable carbon isotope fractionation in lower plants from the Schirmacher and Untersee oases (Central Dronning Maud Land, East Antarctica) (Preliminary report). Isotopenpraxis 29, 21–25.
Chapin FS
(1983) Direct and indirect effects of temperature on Arctic plants. Polar Biology 2, 47–52.
| Crossref | GoogleScholarGoogle Scholar |
Collins NJ, Callaghan TV
(1980) Predicted patterns of photosynthetic production in maritime Antarctic mosses. Annals of Botany 45, 601–620.
Crowe JH,
Hoekstra FA, Crowe LM
(1992) Anhydrobiosis. Annual Review of Physiology 54, 579–599.
| Crossref | GoogleScholarGoogle Scholar |
Davey MC
(1997) Effects of short-term dehydration and rehydration on photosynthesis and respiration by Antarctic bryophytes. Environmental and Experimental Botany 37, 187–198.
| Crossref | GoogleScholarGoogle Scholar |
Davey MC
(1999) The elemental and biochemical composition of bryophytes from the maritime Antarctic. Antarctic Science 11, 157–159.
Gellerman JL,
Anderson WH, Schlenk H
(1972) Highly unsaturated lipids of Mnium, Polytrichum, Marchantia and Matteuccia. The Bryologist 75, 550–557.
| Crossref |
Ghasempour HR,
Gaff DF,
Williams RPW, Gianello RD
(1998) Contents of sugars in leaves of drying desiccation tolerant flowering plants, particularly grasses. Plant Growth Regulation 24, 185–191.
| Crossref | GoogleScholarGoogle Scholar |
Hietz P,
Wanek W, Popp M
(1999) Stable isotopic composition of carbon and nitrogen and nitrogen content in vascular epiphytes along an altitudinal transect. Plant, Cell & Environment 22, 1435–1443.
| Crossref | GoogleScholarGoogle Scholar |
Hobbie SE, Chapin FS
(1998) The response of tundra plant biomass, aboveground production, nitrogen, and CO2 flux to experimental warming. Ecology 79, 1526–1544.
| Crossref |
Hulbert AJ
(2003) Life, death and membrane bilayers. Journal of Experimental Biology 206, 2303–2311.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Koster KL, Leopold AC
(1988) Sugars and desiccation tolerance in seeds. Plant Physiology 88, 829–832.
Li MH,
Hoch G, Körner C
(2002) Source / sink removal affects mobile carbohydrates in Pinus cembra at the Swiss treeline. Trees – Structure and Function 16, 331–337.
Liu LX,
Howe P,
Zhou YF,
Xu ZQ,
Hocart C, Zhang R
(2000) Fatty acids and β-carotene in Australian purslane (Portulaca oleracea) varieties. Journal of Chromatography A 893, 207–213.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lovelock CE, Robinson SA
(2002) Surface reflectance properties of Antarctic moss and their relationship to plant species, pigment composition and photosynthetic function. Plant, Cell & Environment 25, 1239–1250.
| Crossref | GoogleScholarGoogle Scholar |
Lyons JM,
Wheaton TA, Pratt HK
(1964) Relationship between the physical nature of mitochondrial membranes and chilling sensitivity in plants. Plant Physiology 39, 262–268.
Melick DR, Seppelt RD
(1992) Loss of soluble carbohydrates and changes in freezing point of Antarctic bryophytes after leaching and repeated freeze–thaw cycles. Antarctic Science 4, 399–404.
Melick DR, Seppelt RD
(1994) The effect of hydration on carbohydrate levels, pigment content and freezing point of Umbilicaria decussata at a continental Antarctic locality. Cryptogamic Botany 4, 212–217.
Melick DR, Seppelt RD
(1997) Vegetation patterns in relation to climatic and endogenous changes in Wilkes Land, continental Antarctica. Journal of Ecology 85, 43–56.
Montiel PO
(1998) Profiles of soluble carbohydrates and their adaptive role in maritime Antarctic terrestrial arthropods. Polar Biology 19, 250–256.
| Crossref | GoogleScholarGoogle Scholar |
Montiel PO
(2000) Soluble carbohydrates (trehalose in particular) and cryoprotection in polar biota. Cryo Letters 21, 83–90.
| PubMed |
Pantis JD,
Diamantoglon S, Margaris NS
(1987) Altitudinal variation in total lipids and soluble sugar content in herbaceous plants on Mount Olympus (Greece). Vegetatio 72, 21–25.
Popp M,
Lied W,
Meyer AJ,
Richter A,
Schiller P, Schwitte H
(1996) Sample preservation for determination of organic compounds: microwave versus freeze-drying. Journal of Experimental Botany 47, 1469–1473.
Proctor MCF
(2000) The bryophyte paradox: tolerance of desiccation, evasion of drought. Plant Ecology 151, 41–49.
| Crossref | GoogleScholarGoogle Scholar |
Proctor MCF,
Raven JA, Rice SK
(1992) Stable carbon isotope discrimination measurements in Sphagnum and other bryophytes: physiological and ecological implications. Journal of Bryology 17, 193–202.
Pukacka S, Pukacki PM
(1997) Changes in soluble sugars in relation to desiccation tolerance and effects of dehydration on freezing characteristics of Acer platanoides and Acer pseudoplatanus seeds. Acta Physiologiae Plantarum 19, 147–154.
Rice SK, Giles L
(1996) The influence of water content and leaf anatomy on carbon isotope discrimination and photosynthesis in Sphagnum. Plant, Cell & Environment 19, 118–124.
Richter A,
Thonke B, Popp M
(1990) 1D-1-O-methyl-muco-inositol in Viscum album and members of the Rhizophoraceae. Phytochemistry 29, 1785–1786.
| Crossref | GoogleScholarGoogle Scholar |
Robinson SA,
Wasley J,
Popp M, Lovelock CE
(2000) Desiccation tolerance of three moss species from continental Antarctica. Australian Journal of Plant Physiology 27, 379–388.
Robinson SA,
Wasley J, Tobin AK
(2003) Living on the edge — plants and global change in continental and maritime Antarctica. Global Change Biology 9, 1681–1717.
| Crossref | GoogleScholarGoogle Scholar |
Robinson SA,
Turnbull JD, Lovelock CE
(2005) Impact of changes in natural ultraviolet radiation on pigment composition, physiological and morphological characteristics of the Antarctic moss, Grimmia antarctici. Global Change Biology 11, 476–489.
Roser DJ,
Melick DR,
Ling HU, Seppelt RD
(1992) Polyol and sugar content of terrestrial plants from continental Antarctica. Antarctic Science 4, 413–420.
Selkirk PM, Seppelt RD
(1987) Species distribution within a moss bed in Greater Antarctica. Symposia Biologica Hungarica 25, 279–284.
Simon T
(1987) The leaf-area index of three moss species (Tortula ruralis, Ceratodon purpureus, and Hypnum cupressiforme). Symposia Biologica Hungarica 35, 699–706.
Sveinbjornsson B, Oechel WC
(1991) Carbohydrate and lipid-levels in 2 Polytrichum moss species growing on the Alaskan Tundra. Holarctic Ecology 14, 272–277.
Swanson ES,
Anderson WH,
Gellerman JL, Schlenk H
(1976) Ultrastructure and lipid-composition of mosses. The Bryologist 79, 339–349.
| Crossref |
Tokioka T
(1995) Climate changes predicted by climate models for the increase of greenhouse gases. Progress in Nuclear Energy 29, 151–158.
| Crossref | GoogleScholarGoogle Scholar |
Wardlaw IF
(2005) Consideration of apoplastic water in plant organs: a reminder. Functional Plant Biology 32, 561–569.
| Crossref | GoogleScholarGoogle Scholar |
Wasley J,
Robinson SA,
Lovelock CE, Popp M
(2006) Climate change manipulations show Antarctic flora is more strongly affected by elevated nutrients than water. Global Change Biology In press ,
Weinstein RN,
Montiel PO, Johnstone K
(2000) Influence of growth temperature on lipid and soluble carbohydrate synthesis by fungi isolated from fellfield soil in the maritime Antarctic. Mycologia 92, 222–229.
Woitke M,
Hartung W,
Gimmler H, Heilmeier H
(2004) Chlorophyll fluorescence of submerged and floating leaves of the aquatic resurrection plant Chamaegigas intrepidus. Functional Plant Biology 31, 53–62.
| Crossref | GoogleScholarGoogle Scholar |
Ye H, Mather JR
(1997) Polar snow cover changes and global warming. International Journal of Climatology 17, 155–162.
| Crossref | GoogleScholarGoogle Scholar |
Zuniga GE,
Alberdi M, Corcuera LJ
(1996) Non-structural carbohydrates in Deschampsia antarctica Desv. from South Shetland Islands, maritime Antarctic. Environmental and Experimental Botany 36, 393–399.
| Crossref | GoogleScholarGoogle Scholar |
