, Volume 234, Issue 1, pp 195–205 | Cite as

Physiological consequences of desiccation in the aquatic bryophyte Fontinalis antipyretica

  • Ricardo Cruz de Carvalho
  • Cristina Branquinho
  • Jorge Marques da Silva
Original Article


The moss Fontinalis antipyretica, an aquatic bryophyte previously described as desiccation-intolerant, is known to survive intermittent desiccation events in Mediterranean rivers. To better understand the mechanisms of desiccation tolerance in this species and to reconcile the apparently conflicting evidence between desiccation tolerance classifications and field observations, gross photosynthesis and chlorophyll a fluorescence were measured in field-desiccated bryophyte tips and in bryophyte tips subjected in the laboratory to slow, fast, and very fast drying followed by either a short (30 min) or prolonged (5 days) recovery. Our results show, for the first time, that the metabolic response of F. antipyretica to desiccation, both under field and laboratory conditions, is consistent with a desiccation-tolerance pattern; however, drying must proceed slowly for the bryophyte to regain its pre-desiccation state following rehydration. In addition, the extent of dehydration was found to influence metabolism whereas the drying rate determined the degree of recovery. Photosystem II (PSII) regulation and structural maintenance may be part of the induced desiccation tolerance mechanism allowing this moss to recover from slow drying. The decrease in the photochemical quenching coefficient (qP) immediately following rehydration may serve to alleviate the effects of excess energy on photosystem I (PSI), while low-level non-photochemical quenching (NPQ) would allow an energy shift enabling recovery subsequent to extended periods of desiccation. The findings were confirmed in field-desiccated samples, whose behavior was similar to that of samples slowly dried in the laboratory.


Aquatic bryophytes Bryophyta Chlorophyll a fluorescence Desiccation tolerance Fontinalis Recovery 



Analysis of variance


Carbon dioxide


Desiccation tolerance


Full desiccation tolerance


Maximum quantum efficiency of photosystem II


Modified desiccation tolerance


Non-photochemical quenching




Photosynthetic active radiation


Photosystem I


Photosystem II


Photochemical quenching coefficient


Relative humidity


Relative water content


Water content



This work was supported by Fundação para a Ciência e Tecnologia (FCT) [grant no. SFRH/BD/31424/2006] and FEDER POCI 2010 [grant no. POCI/AMB/63160/2004, PPCDT/AMB/63160/2004], Lisbon, Portugal. Thanks to Ana Rute Vieira for providing Fontinalis antipyretica specimens.


  1. Abel WO (1956) Die Austrocknungsresistenz der Laubmoose. Sitzenb Osterr Acad der Wiss, Math-naturw Ki, Abt 1 165:619–707Google Scholar
  2. Akiyama H (1995) Rheophytic mosses: their morphological, physiological, and ecological adaptations. Acta Phytotax Geobot 46:77–98Google Scholar
  3. Alpert P (2006) Constraints of tolerance: why are desiccation-tolerant organisms so small or rare? J Exp Bio 209:1575–1584CrossRefGoogle Scholar
  4. Alpert P, Oliver MJ (2002) Drying without dying. In: Black M, Pritchard HW (eds) Desiccation and survival in plants: drying without dying. CABI Publishing, Wallingford, pp 3–43CrossRefGoogle Scholar
  5. Baker NR, Oxborough K (2005) Chlorophyll fluorescence as a probe of photosynthetic productivity. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence—a signature of photosynthesis. Springer, Berlin, pp 65–82Google Scholar
  6. Bewley JD (1979) Physiological aspects of desiccation tolerance. Ann Rev Plant Physiol 30:195–238CrossRefGoogle Scholar
  7. Bilger W, Björkman O (1994) Relationships among violaxanthin deepoxidation, thylakoid membrane conformation, and nonphotochemical chlorophyll fluorescence quenching in leaves of cotton (Gossypium hirsutum L.). Planta 193:238–246CrossRefGoogle Scholar
  8. Brown DH, Buck GW (1979) Desiccation effects and cation distribution in bryophytes. New Phytol 82:115–125CrossRefGoogle Scholar
  9. Crowe JH, Carpenter JF, Crowe LM (1998) The role of vitrification in anhydrobiosis. Annu Rev Physiol 60:73–103PubMedCrossRefGoogle Scholar
  10. Davey MC (1997) Effects of continuous and repeated dehydration on carbon fixation by bryophytes from the maritime Antarctic. Oecologia 110:25–31CrossRefGoogle Scholar
  11. Deltoro VI, Catalaynd A, Gimeno C, Abadía A, Barreno E (1998) Changes in chlorophyll a fluorescence, photosynthetic CO2 assimilation and xanthophyll cycle interconversions during dehydration in desiccation-tolerant and intolerant liverworts. Planta 207:224–228CrossRefGoogle Scholar
  12. Demmig-Adams B (1990) Carotenoids and photoprotection in plants. A role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020:1–24CrossRefGoogle Scholar
  13. Foyer C (2002) The contribution of photosynthetic oxygen metabolism to oxidative stress in plants. In: Inzé D, van Montagu M (eds) Oxidative stress in plants, chap 2. Taylor & Francis, London, pp 33–68Google Scholar
  14. Franks AJ, Bergstrom DM (2000) Corticolous bryophytes in microphyll fern forests of south-east Queensland: distribution on Antarctic beech (Nothofagus moorei). Austral Ecol 25:386–393CrossRefGoogle Scholar
  15. Glime JM (1971) Response of two species of Fontinalis to field isolation from stream water. Bryologist 74:383–386CrossRefGoogle Scholar
  16. Glime JM (1980) Effects of temperature and flow on rhizoid production in Fontinalis. Bryologist 83:477–485CrossRefGoogle Scholar
  17. Glime JM (2007) Physiological ecology. Bryophyte ecology, vol 1. EBook sponsored by Michigan Technological University and the International Association of Bryologists. Accessed 6 Aug 2008
  18. Glime JM, Vitt DH (1984) The structural adaptations of aquatic Musci. Lindbergia 10:95–110Google Scholar
  19. Hamerlynck EP, Csintalan Z, Nagy Z, Tuba Z, Goodin D, Henebry GM (2002) Ecophysiological consequences of contrasting microenvironments on the desiccation tolerant moss, Tortula ruralis. Oecologia 131:498–505CrossRefGoogle Scholar
  20. Havaux M, Strasser R (1992) Plasticity of the stress tolerance of the photosystem II in vivo. In: Murata N (ed) Research in photosynthesis, vol IV. Kluwer, Dordrecht, pp 149–152Google Scholar
  21. Hinshiri HM, Proctor MCF (1971) The effect of desiccation on subsequent assimilation and respiration of the bryophytes Anomodon viticulosus and Porella platyphylla. New Phytol 70:527–538Google Scholar
  22. Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Phys 47:655–684CrossRefGoogle Scholar
  23. Irmscher E (1912) Über die Resistenz der Laubmoose gegen Austrocknung und Kalte. Jb Wiss Bot 50:387–449Google Scholar
  24. Karsten U, Lütz C, Holzinger A (2010) Ecophysiological performance of the aeroterrestrial green alga Klebsormidium crenulatum (Charophyceae, Streptophyta) isolated from an alpine soil crust with an emphasis on desiccation stress. J Phycol 46:1187–1197CrossRefGoogle Scholar
  25. Kimmerer RW, Allen TFH (1982) The role of disturbance in the pattern of a riparian bryophyte community. Am Midl Nat 107:370–383CrossRefGoogle Scholar
  26. Krochko JE, Bewley JD, Pacey J (1978) The effects of rapid and very slow speeds of drying on the ultrastructure and metabolism of the desiccation-sensitive moss Cratoneuron filicinum (Hedw.) Spruce. J Exp Bot 29:905–917Google Scholar
  27. Lee JA, Stewart GR (1971) Desiccation injury in mosses. I. Intra-specific differences in the effect of moisture stress on photosynthesis. New Phytol 70:1061–1068CrossRefGoogle Scholar
  28. Martins RJE, Pardo R, Boaventura RAR (2004) Cadmium (II) and zinc (II) adsorption by the aquatic moss Fontinalis antipyretica: effect of temperature, pH and water hardness. Water Res 38:693–699PubMedCrossRefGoogle Scholar
  29. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668PubMedCrossRefGoogle Scholar
  30. Mayaba N, Minibayeva F, Beckett RP (2002) An oxidative burst of hydrogen peroxide during rehydration following desiccation in the moss Atrichum androgynum. New Phytol 155:275–283CrossRefGoogle Scholar
  31. National Information System of Water Resources (2010) Accessed 25 Jan 2010
  32. Oliver MJ (2008) Biochemical and molecular mechanisms of desiccation tolerance in bryophytes. In: Goffinet B, Shaw J (eds) Bryophyte biology, 2nd edn. Cambridge University Press, New York, pp 269–298Google Scholar
  33. Oliver MJ, Bewley JD (1997) Desiccation tolerance of plant tissues: a mechanistic overview. Hort Rev 18:171–213Google Scholar
  34. Oliver MJ, Tuba Z, Mishler BD (2000) The evolution of vegetative desiccation tolerance in land plants. Plant Ecol 151:85–100CrossRefGoogle Scholar
  35. Oliver MJ, Velten J, Mishler BD (2005) Desiccation tolerance in bryophytes: a reflection of the primitive strategy for plant survival in dehydrating habitats? Integr Comp Biol 45:788–799PubMedCrossRefGoogle Scholar
  36. Pressel S, Duckett JG (2010) Cytological insights into the desiccation biology of a model system: moss protonemata. New Phytol 185:944–963PubMedCrossRefGoogle Scholar
  37. Proctor MCF (2000) The bryophyte paradox: tolerance of desiccation, evasion of drought. Plant Ecol 151:41–49CrossRefGoogle Scholar
  38. Proctor MCF (2001) Patterns of desiccation tolerance and recovery in bryophytes. Plant Growth Regul 35:147–156Google Scholar
  39. Proctor MCF (2008) Physiological ecology. In: Goffinet B, Shaw J (eds) Bryophyte biology, 2nd edn. Cambridge University Press, New York, pp 237–268Google Scholar
  40. Proctor MCF, Pence VC (2002) Vegetative tissues: bryophytes, vascular resurrection plants and vegetative propagules. In: Black M, Pritchard HW (eds) Desiccation and survival in plants: drying without dying. CABI Publishing, Wallingford, pp 207–237CrossRefGoogle Scholar
  41. Proctor MCF, Smirnoff N (2000) Rapid recovery of photosystems on rewetting desiccation-tolerant mosses: chlorophyll fluorescence and inhibitor experiments. J Exp Bot 51:1695–1704PubMedCrossRefGoogle Scholar
  42. Proctor MCF, Smirnoff N (2011) Ecophysiology of photosynthesis in bryophytes: major roles for oxygen photoreduction and non-photochemical quenching? Physiol Plant 141:130–140PubMedCrossRefGoogle Scholar
  43. Proctor MCF, Ligrone R, Duckett JG (2007a) Desiccation tolerance in the moss Polytrichum formosum: physiological and fine-structural changes during desiccation and recovery. Ann Bot 99:75–93CrossRefGoogle Scholar
  44. Proctor MCF, Oliver MJ, Wood AJ, Alpert P, Stark LR, Cleavitt NL, Mishler BD (2007b) Desiccation-tolerance in bryophytes: a review. Bryologist 110:595–621CrossRefGoogle Scholar
  45. Schonbeck MW, Bewley JD (1981) Responses of the moss Tortula ruralis to desiccation treatments. I. Effects of minimum water content and rates of dehydration and rehydration. Can J Bot 59:2698–2706CrossRefGoogle Scholar
  46. Schöttler MA, Kirchhoff H, Weis E (2004) The role of plastocyanin in the adjustment of the photosynthetic electron transport to the carbon metabolism in tobacco. Plant Physiol 136:4265–4274PubMedCrossRefGoogle Scholar
  47. Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62CrossRefGoogle Scholar
  48. Seel WE, Baker NR, Lee JA (1992) Analysis of the decrease in photosynthesis on desiccation of mosses from xeric and hydric environments. Physiol Plant 86:451–458CrossRefGoogle Scholar
  49. Sérgio C, Séneca C, Máguas C, Branquinho C (1992) Biological responses of Sphagnum auriculatum Schimp. to water pollution by heavy metals. Cryptogamie Bryol L 13:155–163Google Scholar
  50. Šinžar-Sekulić J, Sabovljević M, Stevanović B (2005) Comparison of desiccation tolerance among mosses from different habitats. Arch Biol Sci Belgrade 57:189–192Google Scholar
  51. Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 125:27–58CrossRefGoogle Scholar
  52. Toldi O, Tuba Z, Scott P (2009) Vegetative desiccation tolerance: is it a goldmine for bioengineering crops? Plant Sci 176:187–199CrossRefGoogle Scholar
  53. Traubenberg RC, Ah-Peng C (2004) A procedure to purify and culture a clonal strain of the aquatic moss Fontinalis antipyretica for use as a bioindicator of heavy metals. Arch Environ Con Tox 46:289–295CrossRefGoogle Scholar
  54. Tuba Z, Csintalan Z, Proctor MCF (1996) Photosynthetic responses of a moss, Tortula ruralis, ssp. ruralis, and the lichens Cladonia convoluta and C. furcata to water deficit and short periods of desiccation, and their ecophysiological significance: a baseline study at present-day CO2 concentration. New Phytol 133:353–361CrossRefGoogle Scholar
  55. Vieira C (2008) Rheophilous saxicolous bryophytes of the mountain streams of Northwest Portugal. PhD Dissertation, Oporto University, PortugalGoogle Scholar
  56. Vieira AR, Gonzalez C, Martins-Loução MA, Branquinho C (2009) Intracellular and extracellular ammonium (NH4 +) uptake and its toxic effects on the aquatic biomonitor Fontinalis antipyretica. Ecotoxicology 18:1087–1094PubMedCrossRefGoogle Scholar
  57. Wood AJ (2007) Frontiers in bryological and lichenological research. The nature and distribution of vegetative desiccation tolerance in hornworts, liverworts and mosses. Bryologist 110:163–167CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Ricardo Cruz de Carvalho
    • 1
  • Cristina Branquinho
    • 2
  • Jorge Marques da Silva
    • 1
  1. 1.Faculdade de Ciências (FC), Departamento de Biologia Vegetal (DBV) and Center for Biodiversity, Functional and Integrative Genomics (BioFIG)Universidade de Lisboa (UL)LisbonPortugal
  2. 2.Faculdade de Ciências (FC), Centro de Biologia Ambiental (CBA)Universidade de Lisboa (UL)LisbonPortugal

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