5 - Fern adaptations to xeric environments  pp. 140-176

Fern adaptations to xeric environments

By Peter Hietz

Image View Previous Chapter Next Chapter

Key points

  • 1. Ferns are most prominent in shady and humid environments, but many species are also found in drought-prone habitats, either (semi) arid ecosystems or locations with discontinuous water supply within otherwise humid ecosystems. These locations include tree branches and rocks, both substrates with little water storage capacity.
  • 2. Drought tolerance is gained through adaptations in water uptake, water loss, water storage and, in many ferns, desiccation tolerance, a feature that ferns share with other cryptogams. The little information available on the cuticle's efficiency to limit water loss suggests that it may be similar to other vascular plants. Thus many xerophytic ferns, while tolerating desiccation, normally avoid it through low cuticular and stomatal water loss and may not be considered truly poikilohydric. Exceptions are filmy ferns with very little control of water loss and whose water relations are akin to mosses rather than vascular plants.
  • 3. Other adaptations found in xerophytic ferns include photoprotection with pigments, antioxidants, dense indument, leaf curling and drought avoidance by shedding leaves in the dry season. Crassulacean acid metabolism (CAM) is a common adaptation of xerophytic angiosperms, but is very rare in ferns. Succulence is not strongly developed in xerophytic ferns.
  • 4. Drought adaptations of ferns are analyzed in light of their phylogenetic positions and compared with those of angiosperms. This chapter discusses the potentially underlying causes of drought tolerance in ferns and points to gaps in our understanding as well as possible future research.
Alpert, P. (2000). The discovery, scope, and puzzle of desiccation tolerance in plants. Plant Ecology, 151, 5–17.
Altesor, A. , Ezcurra, E. and Silva, C. (1992). Changes in the photosynthetic metabolism during the early ontogeny of four cactus species. Acta Oecologica, 13, 777–85.
Beckett, R. P. (1997). Pressure–volume analysis of a range of poikilohydric plants implies the existence of negative turgor in vegetative cells. Annals of Botany, 79, 145–52.
Benzing, D. H. (1990). Vascular Epiphytes: General Biology and Related Biota. Cambridge, UK: Cambridge University Press.
Brodribb, T. J. , Holbrook, N. M. , Edwards, E. J. and Gutiérrez, M. V. (2003). Relations between stomatal closure, leaf turgor and xylem vulnerability in eight tropical dry forest trees. Plant, Cell and Environment, 26, 443–50.
Brodribb, T. J. , Holbrook, N. M. , Zwieniecki, M. A. and Palma, B. (2005). Leaf hydraulic capacity in ferns, conifers and angiosperms: impacts on photosynthetic maxima. New Phytologist, 165, 839–46.
Brodribb, T. J. and Feild, T. S. (2000). Stem hydraulic supply is linked to leaf photosynthetic capacity: evidence from New Caledonian and Tasmanian rainforests. Plant, Cell and Environment, 23, 1381–8.
Brodribb, T. J. and Holbrook, N. M. (2004). Stomatal protection against hydraulic failure: a comparison of coexisting ferns and angiosperms. New Phytologist, 162, 663–70.
Cardelús, C. L. , Colwell, R. K. and Watkins, J. E. , Jr. (2006). Vascular epiphyte distribution patterns: explaining the mid-elevation richness peak. Journal of Ecology, 94, 144–56.
Carlquist, S. and Schneider, E. L. (2001). Vessels in ferns: structural, ecological, and evolutionary significance. American Journal of Botany, 88, 1–13.
Carlquist, S. and Schneider, E. L. (2007). Tracheary elements in ferns: new techniques, observations, and concepts. American Fern Journal, 97, 199–211.
Carter, J. P. and Martin, C. E. (1994). The occurrence of crassulacean acid metabolism among epiphytes in a high rainfall region of Costa Rica. Selbyana, 15, 104–6.
Casper, C. , Eickmeier, W. and Osmond, C. (1993). Changes of fluorescence and xanthophyll pigments during dehydration in the resurrection plant Selaginella lepidophylla in low and medium light intensities. Oecologia, 94, 528–33.
Demmig-Adams, B. and Adams, W. W. , III. (1992). Photoprotection and other responses of plants to high light stress. Annual Review of Plant Physiology, 43, 599–626.
Demmig-Adams, B. and Adams, W. W. , III. (1994). Light stress and photoprotection related to the xanthophyll cycle. In Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants, ed. C. H. Foyer and P. M. Mullineaux . Boca Raton, FL, USA: CRC Press, pp. 105–26.
Earnshaw, M. J. , Winter, K. , Ziegler, H. , et al. (1987). Altitudinal changes in the incidence of crassulacean acid metabolism in vascular epiphytes and related life forms in Papua New Guinea. Oecologia, 73, 566–72.
Eickmeier, W. G. (1986). The correlation between high-temperature and desiccation tolerances in a poikilohydric desert plant. Canadian Journal of Botany, 64, 611–17.
Eickmeier, W. G. , Casper, C. and Osmond, B. (1993). Chlorophyll fluorescence in the resurrection plant Selaginella lepidophylla (Hook. & Grev.) Spring during high-light and desiccation stress, and evidence for zeaxanthin-associated photoprotection. Planta, 189, 30–8.
Esau, K. (1965). Plant Anatomy, 2nd edn. New York: John Wiley.
Gaff, D. F. (1987). Desiccation tolerant plants in South America. Oecologia, 74, 133–6.
Gildner, B. S. and Larson, D. W. (1992). Photosynthetic response to sunflecks in the desiccation-tolerant fern Polypodium virginianum . Oecologia, 89, 390–6.
Gordon, C. , Woodin, S. J. , Alexander, I. J. and Mullins, C. E. (1999a). Effects of increased temperature, drought and nitrogen supply on two upland perennials of contrasting functional type: Calluna vulgaris and Pteridium aquilinum . New Phytologist, 142, 243–58.
Gordon, C. , Woodin, S. J. , Mullins, C. E. and Alexander, I. J. (1999b). Effects of environmental change, including drought, on water use by competing Calluna vulgaris (heather) and Pteridium aquilinum (bracken). Functional Ecology, 13, 96–106.
Griffiths, H. (1989). Carbon dioxide concentrating mechanisms and the evolution of CAM in vascular epiphytes. In Vascular Plants as Epiphytes: Evolution and Ecophysiology, ed. U. Lüttge . Heidelberg, Germany: Springer-Verlag, pp. 42–86.
Griffiths, H. , Lüttge, U. , Stimmel, K. H. , et al. (1986). Comparative ecophysiology of CAM and C3 bromeliads. III. Environmental influences on CO2 assimilation and transpiration. Plant, Cell and Environment, 9, 385–93.
Griffiths, H. , Ong, B. L. , Avadhani, P. N. and Goh, C. J. (1989). Recycling of respiratory CO2 during crassulacean acid metabolism: alleviation of photoinhibition in Pyrrosia piloselloides . Planta, 179, 115–22.
Hemp, A. (2001). Ecology of the pteridophytes on the southern slopes of Mt. Kilimanjaro. II. Habitat selection. Plant Biology, 3, 493–523.
Hemp, A. (2002). Ecology of the pteridophytes on the southern slopes of Mt. Kilimanjaro. I. Altitudinal distribution. Plant Ecology, 159, 211–39.
Hew, C. S. and Wong, Y. S. (1974). Photosynthesis and respiration of ferns in relation to their habitats. American Fern Journal, 64, 40–8.
Hietz, P. , Wanek, W. and Popp, M. (1999). Stable isotopic composition of carbon and nitrogen and nitrogen content in vascular epiphytes along an altitudinal transect. Plant, Cell and Environment, 22, 1435–43.
Hietz, P. and Briones, O. (1998). Correlation between water relations and within-canopy distribution of epiphytic ferns in a Mexican cloud forest. Oecologia, 114, 305–16.
Hietz, P. and Briones, O. (2001). Photosynthesis, chlorophyll fluorescence and within-canopy distribution of epiphytic ferns in a Mexican cloud forest. Plant Biology, 3, 279–87.
Hietz, P. and Hietz-Seifert, U. (1995). Composition and ecology of vascular epiphyte communities along an altitudinal gradient in central Veracruz, Mexico. Journal of Vegetation Science, 6, 487–98.
Holtum, J. A. M. and Winter, K. (1999). Degrees of crassulacean acid metabolism in tropical epiphytic and lithophytic ferns. Australian Journal of Plant Physiology, 26, 749–57.
Hovenkamp, P. (1986). A monograph of the fern genus Pyrrosia . Leiden Botanical Series, 9, 1–80.
Hungerbühler, R. (1957). Die Xeromorphosen der Farne mit besonderer Berücksichtigung der Blattanatomie. Unpublished Ph.D. thesis, University of Zürich.
Jacobsen, W. B. G. (1983). The Ferns and Fern Allies of Southern Africa. Durban/Pretoria, Republic of South Africa: Butterworths.
Kappen, L. (1965). Untersuchungen über die Widerstandsfähigkeit der Gametophyten einheimischer Polypodiaceae gegenüber Frost, Hitze und Trockenheit. Flora, 156, 101–15.
Kappen, L. (1966). Der Einfluss des Wassergehaltes auf die Widerstandsfähigkeit von Pflanzen gegenüber hohen und tiefen Temperaturen, untersucht an Blättern einiger Farne und von Ramonda myconi . Flora, 156, 427–45.
Keeley, J. E. (1981). Isoëtes howellii: a submerged aquatic CAM plant? American Journal of Botany, 68, 420.
Kessler, M. (2001). Pteridophyte species richness in Andean forests in Bolivia. Biodiversity and Conservation, 10, 1473–95.
Kluge, M. , Avadhani, P. N. and Goh, C. J. (1989a). Gas exchange and water relations in epiphytic tropical ferns. In Vascular Plants as Epiphytes, ed. U. Lüttge . Heidelberg, Germany: Springer-Verlag, pp. 87–108.
Kluge, M. , Friemert, V. , Ong, B. L. , Brulfert, J. and Goh, C. J. (1989b). In situ studies of crassulacean acid metobolism in Drymoglossum piloselloides, an epiphytic fern of the humid tropics. Journal of Experimental Botany, 40, 441–52.
Kluge, M. and Ting, J. P. (1978). Crassulacean Acid Metabolism: Analysis of an Ecological Adaptation. Ecological Studies 30. Heidelberg, Germany: Springer-Verlag.
Kramer, K. U. , Schneller, J. J. and Wollenweber, E. (1995). Farne und Farnverwandte. Stuttgart, Germany: Georg Thieme.
Lüttge, U. (1989). Vascular Plants as Epiphytes: Evolution and Ecophysiology. Heidelberg, Germany: Springer-Verlag.
Larcher, W. (2002). Physiological Plant Ecology. Berlin, Germany: Springer-Verlag.
Lebkuecher, J. G. , and Eickmeier, W. G. (1991). Reduced photoinhibition with stem curling in the resurrection plant Selaginella lepidophylla . Oecologia, 88, 597–604.
Lebkuecher, J. G. and Eickmeier, W. G. (1993). Physiological benefits of stem curling for resurrection plants in the field. Ecology, 74, 1073–80.
Lehnert, M. (2007). Diversity and evolution of pteridophytes, with emphasis on the neotropics. Unpublished Ph.D. thesis, University of Göttingen.
Long, S. P. , Humphries, S. and Falkowski, P. G. (1994). Photoinhibition and photosynthesis in nature. Annual Review of Plant Physiology, 45, 633–62.
Müller, L. , Starnecker, G. and Winkler, S. (1981). Zur Ökologie epiphytischer Farne in Südbrasilien. I. Saugschuppen. Flora, 171, 55–63.
Maherali, H. , Pockman, W. T. and Jackson, R. B. (2004). Adaptive variation in the vulnerability of woody plants to xylem cavitation. Ecology, 85, 2184–99.
Marrs, R. H. , and Watt, A. S. (2006). Biological flora of the British Isles: Pteridium aquilinum (L.) Kuhn. Journal of Ecology, 94, 1272–321.
Martin, C. E. , Allen, M. T. and Haufler, C. H. (1995). C3 photosynthesis in the gametophyte of the epiphytic CAM fern Pyrrosia longifolia (Polypodiaceae). American Journal of Botany, 82, 441–4.
Martin, C. E. , Lin, K. C. , Hsu, C. C. and Chiou, W. L. (2004). Causes and consequences of high osmotic potentials in epiphytic higher plants. Journal of Plant Physiology, 161, 1119–24.
Martin, S. L. , Davis, R. , Protti, P. , et al. (2005). The occurrence of crassulacean acid metabolism in epiphytic ferns, with an emphasis on the Vittariaceae. International Journal of Plant Sciences, 166, 623–30.
Mehltreter, K. (2008). Phenology and habitat specificity of tropical ferns. In Biology and Evolution of Ferns and Lycophytes, ed. T. A. Ranker and C. H. Haufler . Cambridge, UK: Cambridge University Press, pp. 201–21.
Muslin, E. H. , and Homann, P. H. (1992). Light as a hazard for the desiccation-resistant ‘resurrection’ fern Polypodium polypodioides L. Plant, Cell and Environment, 15, 81–9.
Nobel, P. S. (1978). Microhabitat, water relations, and photosynthesis of a desert fern, Notholaena parryi. Oecologia, 31, 293–309.
Nobel, P. S. (1991). Physicochemical and Environmental Plant Physiology. San Diego, CA, USA: Academic Press.
Oliver, M. J. , Tuba, Z. and Mishler, B. D. (2000). The evolution of vegetative desiccation tolerance in land plants. Plant Ecology, 151, 85–100.
Ong, B. L. , Kluge, M. and Friemert, V. (1986). Crassulacean acid metabolism in the epiphytic ferns Drymoglossum piloselloides and Pyrrosia longifolia: studies on responses to environmental signals. Plant, Cell and Environment, 9, 547–57.
Ong, B. L. and Ng, L. (1998). Regeneration of drought-stressed gametophytes of the epiphytic fern, Pyrrosia piloselloides (L.) Price. Plant Cell Reports, 18, 225–8.
Page, C. N. (1979). The diversity of ferns. An ecological perspective. In The Experimental Biology of Ferns, ed. A. F. Dyer . London: Academic Press, pp. 9–56.
Page, C. N. (2002). Ecological strategies in fern evolution: a neopteridological overview. Review of Palaeobotany and Palynology, 119, 1–33.
Pandé, S. K. (1935). Notes on the anatomy of a xerophytic fern Niphobolus adnascens from the Malay peninsula. Proceedings of the Indian Academy of Sciences, Section B, 1, 556–64.
Pence, V. C. (2000). Cryopreservation of in vitro grown fern gametophytes. American Fern Journal, 90, 16–23.
Pickett, F. L. (1931). Notes on xerophytic ferns. American Fern Journal, 21, 49–57.
Pierce, S. , Winter, K. and Griffiths, H. (2002). Carbon isotope ratio and the extent of daily CAM use by Bromeliaceae. New Phytologist, 156, 75–83.
Porembski, S. and Barthlott, W. (2000). Granitic and gneissic outcrops (inselbergs) as centers of diversity for desiccation-tolerant vascular plants. Plant Ecology, 151, 19–28.
Powles, S. B. (1984). Photoinhibition of photosynthesis induced by visible light. Annual Review of Plant Physiology, 35, 15–44.
Proctor, M. C. F. (2003). Comparative ecophysiological measurements on the light responses, water relations and desiccation tolerance of the filmy ferns Hymenophyllum wilsonii Hook, and H. tunbrigense (L.) Smith. Annals of Botany, 91, 717–27.
Proctor, M. C. F. and Tuba, Z. (2002). Poikilohydry and homoihydry: antithesis or spectrum of possibilities? New Phytologist, 156, 327–49.
Reynolds, T. L. and Bewley, J. D. (1993a). Abscisic acid enhances the ability of the desiccation-tolerant fern Polypodium virginianum to withstand drying. Journal of Experimental Botany, 44, 1771–9.
Reynolds, T. L. and Bewley, J. D. (1993b). Characterization of protein synthetic changes in a desiccation-tolerant fern, Polypodium virginianum: comparison of the effects of drying, rehydration and abscisic acid. Journal of Experimental Botany, 44, 921–8.
Ribeiro, M. L. R. C. , Santos, M. G. and Moraes, M. G. (2007). Leaf anatomy of two Anemia Sw. species (Schizaeaceae: Pteridophyte) from a rocky outcrop in Niterói, Rio de Janeiro, Brazil. Revista Brasileira de Botânica, 30, 695–702.
Rivera, G. , Elliott, S. , Caldas, L. , et al. (2002). Increasing day-length induces spring flushing of tropical dry forest trees in the absence of rain. Trees – Structure and Function, 16, 445–56.
Rut, G. , Krupa, J. , Miszalski, Z. , Rzepka, A. and Ślesak, I. (2008). Crassulacean acid metabolism in the epiphytic fern Platycerium bifurcatum . Photosynthetica, 46, 156–60.
Schreuder, M. D. J. , Brewer, C. A. and Heine, C. (2001). Modeled influences of non-exchanging trichomes on leaf boundary layers and gas exchange. Journal of Theoretical Biology, 210, 23–32.
Schulze, E.-D. , Beck, E. and Müller-Hohenstein, K. (2005). Plant Ecology. Berlin, Germany: Springer-Verlag.
Shreve, F. (1911). Studies on Jamaican Hymenophyllaceae. Botanical Gazette, 51, 184–209.
Sinclair, R. (1983). Water relations of tropical epiphytes. I. Relationships between stomatal resistance, relative water content and the components of water potential. Journal of Experimental Botany, 34, 1652–63.
Starnecker, G. and Winkler, S. (1982). Zur Ökologie epiphytischer Farne in Südbrasilien. II. Anatomische und physiologische Anpassungen. Flora, 172, 57–68.
Stone, C. and Pratt, L. W. (1995). Hawai‘i's Plants and Animals: Biological Sketches of Hawai‘i Volcanoes National Park. Honolulu, HI, USA: University of Hawai‘i Press.
Stuart, T. S. (1968). Revival of respiration and photosynthesis in dried leaves of Polypodium polypodioides . Planta, 83, 185–206.
Tausz, M. , Hietz, P. and Briones, O. (2001). The significance of carotenoids and tocopherols in photoprotection of seven epiphytic fern species of a Mexican cloud forest. Australian Journal of Plant Physiology, 28, 775–83.
Tryon, R. M. (1964). Evolution in the leaf of living ferns. Bulletin of the Torrey Botanical Club, 21, 73–85.
Tryon, R. M. , and Tryon, A. F. (1982). Ferns and Allied Plants with Special Reference to Tropical America. New York: Springer-Verlag.
Tyree, M. T. and Sperry, J. S. (1989). Vulnerability of xylem to cavitation and embolism. Annual Review of Plant Physiology and Plant Molecular Biology, 40, 19–38.
Watkins, J. E. , Jr., Kawahara, A. Y. , Leicht, S. A. , et al. (2006). Fern laminar scales protect against photoinhibition from excess light. American Fern Journal, 96, 83–92.
Watkins, J. E. , Jr., Mack, M. C. , Sinclair, T. R. and Mulkey, S. S. (2007a). Ecological and evolutionary consequences of desiccation tolerance in tropical fern gametophytes. New Phytologist, 176, 708–17.
Watkins, J. E. , Jr., Rundel, P. and Cardelús, C. (2007b). The influence of life form on carbon and nitrogen relationships in tropical rainforest ferns. Oecologia, 153, 225–32.
Winter, K. , Osmond, C. B. and Hubick, K. T. (1986). Crassulacean acid metabolism in the shade: studies on an epiphytic fern, Pyrrosia longifolia, and other rain forest species from Australia. Oecologia, 68, 224–30.
Winter, K. , Wallace, B. J. , Stocker, G. C. and Roksandic, Z. (1983). Crassulacean acid metabolism in Australian vascular epiphytes and some related species. Oecologia, 57, 129–41.
Wollenweber, E. (1978). The distribution and chemical constituents of the farinose exudates in gymnogrammoid ferns. American Fern Journal, 68, 13–28.
Wollenweber, E. , Scheele, C. and Tryon, A. F. (1987). Flavonoids and spores of Platyzoma microphyllum, an endemic fern of Australia. American Fern Journal, 77, 28–32.
Woodhouse, R. M. and Nobel, P. S. (1982). Stipe anatomy, water potentials, and xylem conductances in seven species of ferns (Filicopsida). American Journal of Botany, 69, 135–40.
Zotz, G. (2005). Vascular epiphytes in the temperate zones: a review. Plant Ecology, 176, 173–83.
Zotz, G. and Ziegler, H. (1997). The occurrence of crassulacean acid metabolism among vascular epiphytes from central Panama. New Phytologist, 137, 223–9.