Skip to main content
SpringerLink
Log in

Morpho-anatomical studies on the leaf reduction in Casuarina: the ecology of xeromorphy

  • Original Article
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Key message

The foliage characters found in Casuarina seedlings may represent the ancestral, scleromorphic ones found in the Casuarinaceae. In the adults studied, these are replaced by derived xeromorphic features.

Abstract

The ontogenetic changes in the foliage of two Casuarina species were investigated. While the cotyledons are flattened linear structures, all other leaf-types are strongly reduced. Except for the two primary leaves, all subsequent leaves are strongly fused to each other and also to the shoot axis, except for the leaf tips; the shoot axis is completely surrounded by photosynthetic leaf tissue and the branchlet is not made up of cladodes but of extended leaf sheaths which are a novel strategy for achieving reduced photosynthetic area. In seedlings there are four leaves per node, forming four shallow vertical furrows where light-exposed and non-encrypted stomata are developed. These features are also developed in the adult foliage within the strictly scleromorphic genus Gymnostoma, clearly the most mesic of the present day genera of Casuarinaceae and very likely to include the ancestral types. Thus, we assume that the Casuarina-seedling leaves reflect the ancestral scleromorphic condition. In the adult foliage, the number of leaves per node is strongly increased, which leads to the formation of several nearly closed vertical furrows on the shoot, where stomata are shaded and strongly encrypted. Thus, the adult foliage shows several xeromorphic features that are absent in the juvenile foliage. Our morpho-anatomical data mapped on ecological and palaeobotanical data show that within Casuarinaceae the foliage shifted from scleromorphic to xeromorphic. Thus, the adult xeromorphic foliage in Casuarina is the derived, advanced state.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Ashton DH, Bond H, Morris GC (1975) Drought damage on Mount Towrong, Victoria. Proc Linn Soc New South Wales 100:44–69

    Google Scholar 

  • Beadle NCW (1966) Soil phosphate and its role in molding segments of the Australian flora and vegetation with special reference to xeromorphy and sclerophylly. Ecology 47:992–1007

    Article  Google Scholar 

  • Blum A (1996) Crop responses to drought and the interpretation of adaptation. Plant Growth Regul 20:135–148

    Article  CAS  Google Scholar 

  • Blum A, Arkin GF (1984) Sorghum root growth and water use as affected by water supply and growth duration. Field Crop Res 9:131–142

    Article  Google Scholar 

  • Boland DJ, Brooker MIH, Chippendale GM, Hall N, Hyland BPM, Johnston RD, Kleinig DA, McDonald, MW, Turner JD (2006) Forest trees of Australia, 5th edn. CSIRO, Collingwood

  • Bosabalidis AM, Kofidis G (2002) Comparative effects of drought stress on leaf anatomy of two olive cultivars. Plant Sci 163:375–379

    Article  CAS  Google Scholar 

  • Cutler HC (1939) Monograph of the North American species of the genus Ephedra. Ann Mo Bot Gard 26:373–428

    Article  Google Scholar 

  • Dörken VM (2013) Leaf dimorphism in Thuja plicata and Platycladus orientalis (thujoid Cupressaceae s. str., Coniferales): the changes in morphology and anatomy from juvenile needle leaves to mature scale leaves. Plant Syst Evol 299:1991–2001

    Article  Google Scholar 

  • Dörken VM (2014) Leaf-morphology and leaf-anatomy in Ephedra altissima Desf. (Ephedraceae, Gnetales) and their evolutionary relevance. Feddes Repert 123:243–255

    Article  Google Scholar 

  • Dörken VM, Jagel A (2014) Pinus sylvestris—Wald-Kiefer (Pinaceae), Baum des Jahres 2007. Jahrb Bochumer Bot Ver 5:246–254

    Google Scholar 

  • Dörken VM, Parsons R (2016) Morpho-anatomical studies on the change in the foliage of two imbricate-leaved New Zealand podocarps: Dacrycarpus dacrydioides and Dacrydium cupressinum. Plant Syst Evol 302:41–54

    Article  Google Scholar 

  • Düll R, Kutzelnigg H (2011) Taschenlexikon der Pflanzen Deutschlands und angrenzender Länder, 7th edn. Quelle & Meyer, Wiebelsheim

    Google Scholar 

  • Eckenwalder JE (2009) Conifers of the World. Timber Press, Portland

    Google Scholar 

  • Farjon A (2005) A monograph of Cupressaceae and Sciadopitys. Royal Botanic Gardens, Kew

    Google Scholar 

  • Farjon A (2010a) A handbook of the world’s conifers, vol I. Brill, Leiden

    Book  Google Scholar 

  • Farjon A (2010b) A handbook of the world’s conifers, vol II. Brill, Leiden

    Book  Google Scholar 

  • Feustel H (1921) Anatomie und Biologie der Gymnospermenblätter. Beih Bot Centralbl 38:177–253

    Google Scholar 

  • Foster AS, Gifford EM (1974) Comparative morphology of vascular plants. 2nd edn. Freeman, San Francisco

    Google Scholar 

  • Freitag H, Maier-Stolte M (2003) The genus Ephedra in NE tropical Africa. Kew Bull 58:415–426

    Article  Google Scholar 

  • Gaskin JF (2003) Tamaricaceae. In: Kubitzki K, Bayer C (eds) The families and genera of vascular plants, vol 5. Springer, Berlin, pp 336–338

    Google Scholar 

  • Gerlach, D (1984) Botanische Mikrotomtechnik, eine Einführung. 2nd edn. Thieme, Stuttgart

    Google Scholar 

  • Heywood VH (1978) Flowering plants of the world. Oxford University Press, Oxford

    Google Scholar 

  • Hill RS (1990) Evolution of the modern high latitude southern hemisphere flora. Evidence from the Australian macrofossil record. In: Douglas JG, Christophel DC (eds) Proceedings 3rd IOP conference, Melbourne 1988. A-Z Publishers, Melbourne, pp 31–42

    Google Scholar 

  • Hill RS (1998) Fossil evidence for the onset of xeromorphy and scleromorphy in Australian Proteaceae. Aust Syst Bot 11:391–400

    Article  Google Scholar 

  • Hill RS, Brodribb TJ (2001) Macrofossil evidence for the onset of xeromorphy in Australian Casuarinaceae and tribe Banksieae (Proteaceae). J Mediterr Ecol 2:127–136

    Google Scholar 

  • Hill RS, Merrifield HE (1993) An early Tertiary macroflora from West Dale, southwestern Australia. Alcheringa 17:285–326

    Article  Google Scholar 

  • Inamdar JA, Bhatt DC (1971) Epidermal structure and ontogeny of stomata in vegetative and reproductive organs of Ephedra and Gnetum. Ann Bot (Oxford) 36:1041–1046

    Article  Google Scholar 

  • Korner C (2003) Alpine plant life, 2nd edn. Springer, Berlin

    Book  Google Scholar 

  • Krüssmann G (1976) Handbuch der Laubgehölze, vol. 1, 2nd edn. Parey, Berlin

    Google Scholar 

  • Krüssmann G (1977) Handbuch der Laubgehölze, vol 2, 2nd edn. Parey, Berlin

    Google Scholar 

  • Krüssmann G (1978) Handbuch der Laubgehölze, vol. 3, 2nd edn. Parey, Berlin

    Google Scholar 

  • Krüssmann G (1983) Handbuch der Nadelgehölze, 2nd edn. Parey, Berlin

    Google Scholar 

  • Kubitzki K (2004) The families and genera of vascular plants, vol 6. Flowering plants, dicotyledons: Celastrales, Oxalidales, Rosales, Cornales, Ericales. Springer, Berlin

    Google Scholar 

  • Kubitzki K, Rohwer JG, Bittrich V (1993) The families and genera of vascular plants, vol 2. Flowering plants, dicotyledons: Magnoliid, Hamamelid and Caryophylloid families. Springer, Berlin

    Google Scholar 

  • Ladd PG (1988) The status of Casuarinaceae in Australian Forests. In: Frawley KJ, Semple NM (eds) Australia’s ever changing forests. Proceedings of the first national conference on Australian forest history, pp 63–85

  • Loveless AR (1961) A nutritional interpretation of sclerophylly based on differences in the chemical composition of sclerophyllous and mesophytic leaves. Ann Bot (Oxford) 25:168–184

    Article  CAS  Google Scholar 

  • Loveless AR (1962) Further evidence to support a nutritional interpretation of sclerophylly. Ann Bot (Oxford) 26:551–561

    Article  Google Scholar 

  • Niinemets Ü, Lukjanova A, Sparrow AD, Turnbull MH (2005) Light acclimation of cladode photosynthetic potentials in Casuarina glauca: trade-offs between physiological and structural investments. Funct Plant Biol 32:571–582

    Article  Google Scholar 

  • Parsons RF (2010) Whipcord plants: a comparison of south-eastern Australia with New Zealand. Cunninghamia 11:277–281

    Google Scholar 

  • Pedley L (1986) Derivation and dispersal of Acacia (Leguminosae), with particular reference to Australia and the recognition of Senegalia and Racosperma. Bot J Linn Soc 92:219–254

    Article  Google Scholar 

  • Rao AN (1972) Anatomical studies on succulent cladodes in Casuarina equisetifolia Linn. Proc Indian Acad Sci B 76:262–270

    Google Scholar 

  • Reddel P, Yun Y, Shipton WA (1997) Cluster roots and mycorrhizae in Casuarina cunninghamiana: their occurrence and formation in relation to phosphorus supply. Aust J Bot 45:41–51

    Article  Google Scholar 

  • Reddell P, Bowen GD, Robson AD (1986) Nodulation of Casuarinaceae in relation to host species and soil properties. Aust J Bot 34:435–444

    Article  Google Scholar 

  • Rehder A (1967) Manual of cultivated trees and shrubs, 2nd edn. The Macmillan Company, New York

    Google Scholar 

  • Salleo S, Nardini A (2000) Sclerophylly: evolutionary advantage or mere epiphenomenon. Plant Biosyst 134(3):247–259

    Article  Google Scholar 

  • Schütt P, Schuck HJ, Stimm B (2002) Lexikon der Baum- und Straucharten. Nikol, Hamburg

    Google Scholar 

  • Scriven LJ, Hill RS (1995) Macrofossil Casuarinaceae, their identification and the oldest macrofossil record, Gymnostoma antiquum sp. nov., from the Late Palaeocene of New South Wales, Australia. Aust Syst Bot 8:1035–1053

    Article  Google Scholar 

  • Seddon G (1974) Xerophytes, xeromorphs and sclerophylls: the history of some concepts in ecology. Biol J Linn Soc 6:65–87

    Article  CAS  Google Scholar 

  • Seidling W, Ziche D, Beck W (2012) Climate responses and interrelations of stem increment and crown transparency in Norway Spruce, Scots Pine and Common Beech. Forest Ecol Manag 284:196–204

    Article  Google Scholar 

  • Steane DA, Wilson KL, Hill RS (2003) Using matK sequence data to unravel the phylogeny of Casuarinaceae. Mol Phylogenet Evol 28:47–59

    Article  CAS  PubMed  Google Scholar 

  • Stebbins GL (1950) Variation and evolution in plants. Columbia University Press, New York

    Google Scholar 

  • Stevens PF (2015) Angiosperm Phylogeny Website, Version 13. http://www.mobot.org/MOBOT/research/-APweb/ (04 Oct 2015)

  • Taylor TN, Taylor EL, Krings M (2009) Palaeobotany: the biology and evolution of fossil plants. Academic Press, Burlington

    Google Scholar 

  • Tetzlaf M (2005) Die Anatomie des Gymnospermenblattes unter funktionellen und evolutiven Gesichtspunkten. Diploma. Ruhr-University, Bochum

    Google Scholar 

  • Thoday D (1931) The significance of reduction in the size of leaves. J Ecol 19(2):297–303

    Article  Google Scholar 

  • Thompson WP (1912) The anatomy and relationships of Gnetales. I. The genus Ephedra. Ann Bot (Oxford) 27:1077–1104

    Article  Google Scholar 

  • Torrey JG, Berg RH (1988) Some morphological features for generic characterization among the Casuarinaceae. Am J Bot 75:864–874

    Article  Google Scholar 

  • Voth PD (1934) A study of the vegetative phases of Ephedra. Bot Gaz 96:298–313

    Article  Google Scholar 

  • Warrier KCS, Suganthi A, Singh BG (2013) A new record of abnormal phylloclad modification in Casuarina equisetifolia. Int J Agric Sci Res 2:8–11

    Google Scholar 

  • Wilson KL, Johnson LAS (1989) Casuarinaceae. In: George AS (ed) Flora of Australia, vol 3. Hamamelidales to Casuarinales. Australian Government Publishing Service, Canberra, pp 100–175

    Google Scholar 

  • Zamaloa MC, Gandolfo MA, Gonzales CC, Romero EJ, Cuneo NR, Wilf P (2006) Casuarinaceae from the Eocene of Patagonia, Argentina. Int J Plant Sci 167:1279–1289

    Article  Google Scholar 

  • Zimpfer JF, Igual JM, McCarty B, Smyth C, Dawson JO (2004) Casuarina cunninghamia tissue extracts stimulate the growth of Frankia and differentially alter the growth of other soil microorganisms. J Chem Ecol 30:439–452

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to Mr. Otmar Ficht and Mrs. Anne Kern (Botanic Garden, University of Konstanz, Germany) for producing the seedlings. Furthermore, we thank the Botanic Garden of the Ruhr-University of Bochum (Germany) for generously providing research material and Dr. Michael Laumann and Mrs. Lauretta Nejedli (Electron Microscopy Center, Department of Biology, University of Konstanz, Germany) for technical support (paraffin technique). Finally, we thank Dr. Philip Ladd (Murdoch University, Australia), Dr. Mike Bayly (University of Melbourne, Australia) and Dr. Ian Staff (LaTrobe University, Australia) for helpful advice.

Author information

Authors and Affiliations

  1. Department of Biology, University of Konstanz, M 613, Universitätsstr. 10, 78457, Constance, Germany

    Veit M. Dörken

  2. Department of Ecology, Environment and Evolution, La Trobe University, Bundoora, Melbourne, VIC, 3086, Australia

    Robert F. Parsons

Authors
  1. Veit M. Dörken
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robert F. Parsons
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Veit M. Dörken.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by L. Gratani.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dörken, V.M., Parsons, R.F. Morpho-anatomical studies on the leaf reduction in Casuarina: the ecology of xeromorphy. Trees 31, 1165–1177 (2017). https://doi.org/10.1007/s00468-017-1535-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-017-1535-5

Keywords

Search

Navigation