, Volume 18, Issue 2, pp 287–309 | Cite as

Soil Development and Nutrient Availability Along a 2 Million-Year Coastal Dune Chronosequence Under Species-Rich Mediterranean Shrubland in Southwestern Australia

  • Benjamin L. TurnerEmail author
  • Etienne Laliberté


Soil chronosequences provide valuable model systems to investigate pedogenesis and associated effects of nutrient availability on biological communities. However, long-term chronosequences occurring under seasonally dry climates remain scarce. We assessed soil development and nutrient dynamics along the Jurien Bay chronosequence, a 2 million-year sequence of coastal dunes in southwestern Australia. The chronosequence is significant because it occurs in a Mediterranean climate and supports hyperdiverse shrublands within a global biodiversity hotspot. Young soils formed during the Holocene (<6,500 years old) are strongly alkaline and contain abundant carbonate, which is leached from the profile within a few thousand years. Middle Pleistocene soils (ca 120,000–500,000 years old) are yellow decalcified sands with residual iron oxide coatings on quartz grains over a petrocalcic horizon that occurs at increasing depth as soils age. Early Pleistocene soils (>2,000,000 years old) are completely leached of iron oxides and consist of bleached quartz sand several meters deep. Changes in soil organic matter and nutrient status along the Jurien Bay chronosequence are consistent with patterns observed along other long-term chronosequences and correspond closely to expectations of the Walker and Syers (1976) model of biogeochemical change during pedogenesis. Organic carbon and nitrogen (N) accumulate rapidly to maximum amounts in intermediate-aged Holocene dunes and then decline as soils age. In contrast, total phosphorus (P) declines continuously along the chronosequence to extremely low levels after 2 million years of pedogenesis, eventually representing some of the lowest P soils globally. Ratios of soil organic carbon to P and N to P increase continuously along the chronosequence, consistent with a shift from N limitation on young soils to extreme P limitation on old soils. Phosphorus fractionation by sequential extraction reveals a rapid decline in primary and non-occluded phosphate and an increase in organic and occluded P as soils age. Concentrations of extractable (that is, readily bioavailable) N and P, as well as exchangeable cations, are greatest in Holocene dunes and decline to low levels in Pleistocene dunes. Extractable micronutrient concentrations were generally very low and varied little across the chronosequence. We conclude that the Jurien Bay chronosequence is an important example of changing patterns of nutrient limitation linked to long-term soil and ecosystem development under a Mediterranean climate.


chronosequence ecosystem development pedogenesis nutrients phosphorus nitrogen 



Funding was provided by a Discovery Early Career Researcher Award (DE120100352) from the Australian Research Council and a Research Collaboration Award from The University of Western Australia (both to EL). The authors thank Dayana Agudo, Pedro Araúz, Aleksandra Bielnicka, and Paola Escobar for laboratory support; and Felipe Albornoz, Patrick Hayes, Hans Lambers, Kenny Png, François Teste, Karl-Heinz Wyrwoll, and Graham Zemunik for assistance in the field. Figure 1 was created using base maps provided by the Department of Agriculture and Food of Western Australia.

Supplementary material

10021_2014_9830_MOESM1_ESM.docx (33 kb)
Supplementary material 1 (DOCX 34 kb)
10021_2014_9830_MOESM2_ESM.xls (46 kb)
Supplementary material 2 (XLS 46 kb)


  1. Adriano DC. 1986. Trace elements in the terrestrial environment. New York: Springer.Google Scholar
  2. Baisden WT, Amundson R, Brenner DL, Cook AC, Kendall C, Harden J. 2002. A multi-isotope C and N modeling analysis of soil organic matter turnover and transport as a function of soil depth in a California annual grassland soil chronosequence. Glob Biogeochem Cycles 16:1135. doi: 10.1029/2001GB001823.Google Scholar
  3. Barrows TT, Juggins S. 2005. Sea-surface temperatures around the Australian margin and Indian Ocean during the Last Glacial Maximum. Quat Sci Rev 24:1017–47.Google Scholar
  4. Bastian LV. 1996. Residual soil mineralogy and dune subdivision, Swan Coastal Plain, Western Australia. Aust J Earth Sci 43:31–44.Google Scholar
  5. Beard JS. 1984. Biogeography of the kwongan. In: Pate JS, Beard JS, Eds. Kwongan: plant life of the sandplain. Nedlands: University of Western Australia Press. p 1–26.Google Scholar
  6. Bell DT, Hopkins AJM, Pate JS. 1984. Fire in the kwongan. In: Pate JS, Beard JS, Eds. Kwongan: plant life of the sandplain. Nedlands: University of Western Australia Press. p 178–204.Google Scholar
  7. Bell DT, Plummer JA, Taylor SK. 1993. Seed germination ecology in southwestern Western Australia. Bot Rev 59:24–73.Google Scholar
  8. Berger WH. 2008. Sea level in the late Quaternary: patterns of variation and implications. Int J Earth Sci 97:1143–50.Google Scholar
  9. Brooke BP, Olley JM, Pietsch T, Playford PE, Haines PW, Murray-Wallace CV, Woodroffe CD. 2014. Chronology of Quaternary coastal aeolianite deposition and the drowned shorelines of southwestern Western Australia—a reappraisal. Quat Sci Rev 93:106–24.Google Scholar
  10. Burges A, Drover D. 1953. The rate of podzol development in sands of the Woy Woy District, NSW. Aust J Bot 1:83–94.Google Scholar
  11. Carter MC, Darwin Foster C. 2004. Prescribed burning and productivity in southern pine forests: a review. For Ecol Manag 191:93–109.Google Scholar
  12. Certini G. 2005. Effects of fire on properties of forest soils: a review. Oecologia 143:1–10.PubMedGoogle Scholar
  13. Coomes DA, Bellingham PJ. 2011. Temperate and tropical podocarps: how ecologically alike are they? In: Turner BL, Cernusak LA, Eds. Ecology of the Podocarpaceae in tropical forests. Smithsonian Contributions to Botany. Washington, DC: Smithsonian Institution Scholarly Press. p 119–40.Google Scholar
  14. Coomes D, Bentley W, Tanentzap A, Burrows L. 2013. Soil drainage and phosphorus depletion contribute to retrogressive succession along a New Zealand chronosequence. Plant Soil 367:77–91.Google Scholar
  15. Crews TE, Kitayama K, Fownes JH, Riley RH, Herbert DA, Mueller-Dombois D, Vitousek PM. 1995. Changes in soil phosphorus fractions and ecosystem dynamics across a long chronosequence in Hawaii. Ecology 76:1407–24.Google Scholar
  16. Denton M, Veneklaas EJ, Freimoser F, Lambers H. 2007. Banksia species (Proteaceae) from severely phosphorus-impoverished soils exhibit extreme efficiency in the use and re-mobilization of phosphorus. Plant Cell Environ 30:1557–65.PubMedGoogle Scholar
  17. Dodson JR. 2001. Holocene vegetation change in the mediterranean-type climate regions of Australia. Holocene 11:673–80.Google Scholar
  18. Enright NJ, Lamont BB, Miller BP. 2005. Anomalies in grasstree fire history reconstructions for south-western Australian vegetation. Austral Ecol 30:668–73.Google Scholar
  19. Fujioka T, Chappell J, Fifield LK, Rhodes EJ. 2009. Australian desert dune fields initiated with Pliocene-Pleistocene global climatic shift. Geology 37:51–4.Google Scholar
  20. Gee GW, Or D. 2002. Particle size analysis. In: Dane JH, Topp C, Eds. Methods of soil analysis, Part 4—Physical methods. Madison: Soil Science Society of America. p 255–93.Google Scholar
  21. Geological Survey of Western Australia. 1990. Geology and Mineral Resources of Western Australia. Perth: Western Australian Geological Survey. p 827.Google Scholar
  22. Glassford DK, Killigrew LP. 1976. Evidence for Quaternary westward extension of the Australian desert into south-western Australia. Search 7:394–6.Google Scholar
  23. Griffin EA, Burbidge AA. 1990. Description of the region. In: Burbidge AA, Hopper DS, van Leeuwen S, Eds. Nature conservation, landscape and recreation values of the Lesueur area. Perth: Environmental Protection Authority. p 15–24.Google Scholar
  24. Harden JW. 1982. A quantitative index of soil development from field descriptions: example from a chronosequence in central California. Geoderma 28:1–28.Google Scholar
  25. Hayes P, Turner BL, Lambers H, Laliberté E. 2014. Foliar nutrient concentrations and resorption efficiency in plants of contrasting nutrient-acquisition strategies along a 2-million-year dune chronosequence. J Ecol 102:396–410.Google Scholar
  26. Hearty PJ, O’Leary MJ. 2008. Carbonate eolianites, quartz sands, and Quaternary sea-level cycles, Western Australia: a chronostratigraphic approach. Quat Geochronol 3:26–55.Google Scholar
  27. Hedley MJ, Stewart JWB, Chauhan BS. 1982. Changes in inorganic and organic soil phosphorus fractions induced by cultivation practices and by laboratory incubations. Soil Sci Soc Am J 46:970–6.Google Scholar
  28. Hendershot WH, Lalande H, Duquette M. 2008. Chapter 18. Ion exchange and exchangeable cations. In: Carter MR, Gregorich E, Eds. Soil sampling and methods of analysis. Boca Raton: Canadian Society of Soil Science and CRC Press. p 173–8.Google Scholar
  29. Hewgill FR, Kendrick GW, Webb RJ, Wyrwoll KH. 1983. Routine ESR dating of emergent Pleistocene marine units in Western Australia. Search 14:215–17.Google Scholar
  30. Holloway RE, Graham RD, Stacey SP. 2008. Micronutrient deficiencies in Australian field crops. In: Alloway BJ, Ed. Micronutirent deficiencies in global crop production. Berlin: Springer. p 63–92.Google Scholar
  31. Hopper SD. 2014. Sandplain and kwongan: historical spellings, meanings, synonyms, geography and definition. In: Lambers H, Ed. Plant life on the sandplains in Southwest Australia, a global biodiversity hotspot. Crawley: University of Western Australia Publishing. Google Scholar
  32. Hopper SD, Gioia P. 2004. The Southwest Australian Floristic Region: evolution and conservation of a global hot spot of biodiversity. Annu Rev Ecol Evol Syst 35:623–50.Google Scholar
  33. Huggett RJ. 1998. Soil chronosequences, soil development, and soil evolution: a critical review. Catena 32:155–72.Google Scholar
  34. Isbell RF. 2002. The Australian soil classification. revised edn. Collingwood: CSIRO Publishing.Google Scholar
  35. Izquierdo JE, Houlton BZ, van Huysen TL. 2013. Evidence for progressive phosphorus limitation over long-term ecosystem development: examination of a biochemical paradigm. Plant Soil 367:135–47.Google Scholar
  36. Jangid K, Whitman WB, Condron LM, Turner BL, Williams MA. 2013. Soil bacterial community succession during long-term ecosystem development. Mol Ecol 22:3415–24.PubMedGoogle Scholar
  37. Jenny H. 1941. Factors of soil formation: a system of quantitative pedology. New York: McGraw-Hill. p 281.Google Scholar
  38. Kendrick GW, Wyrwoll K-H, Szabo BJ. 1991. Pliocene-Pleistocene coastal events and history along the western margin of Australia. Quat Sci Rev 10:419–39.Google Scholar
  39. Lajtha K, Schlesinger WH. 1988. The biogeochemistry of phosphorus cycling and phosphorus availability along a desert soil chronosequence. Ecology 69:24–39.Google Scholar
  40. Laliberté E, Turner BL, Costes T, Pearse SJ, Wyrwoll K-H, Zemunik G, Lambers H. 2012. Experimental assessment of nutrient limitation along a 2-million-year dune chronosequence in the south-western Australia biodiversity hotspot. J Ecol 100:631–42.Google Scholar
  41. Laliberté E, Grace JB, Huston MA, Lambers H, Teste FP, Turner BL, Wardle DA. 2013a. How does pedogenesis drive plant diversity? Trends Ecol Evol 28:331–40.PubMedGoogle Scholar
  42. Laliberté E, Turner BL, Zemunik G, Wyrwoll K-H, Pearse SJ, Lambers H. 2013b. Nutrient limitation along the Jurien Bay dune chronosequence: response to Uren & Parsons (2013). J Ecol 101:1088–92.Google Scholar
  43. Laliberté E, Zemunik G, Turner BL. 2014. Environmental filtering explains variation in plant diversity along resource gradients. Science 345:1602–5.PubMedGoogle Scholar
  44. Lambeck K, Chappell J. 2001. Sea level change through the last glacial cycle. Science 292:679–86.PubMedGoogle Scholar
  45. Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ. 2006. Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot 98:693–713.PubMedCentralPubMedGoogle Scholar
  46. Lambers H, Raven JA, Shaver GR, Smith SE. 2008. Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103.PubMedGoogle Scholar
  47. Lambers H, Cawthray GR, Giavalisco P, Kuo J, Laliberte E, Pearse SJ, Scheible W-R, Stitt M, Teste F, Turner BL. 2012. Proteaceae from severely phosphorus-impoverished soils extensively replace phospholipids with galactolipids and sulfolipids during leaf development to achieve a high photosynthetic phosphorus-use-efficiency. New Phytol 196:1098–108.PubMedGoogle Scholar
  48. Lamont BB, Hopkins AJM, Hnatiuk RJ. 1984. The flora—composition, diversity and origins. In: Pate JS, Beard JS, Eds. Kwongan: plant life of the sandplain. Nedlands: University of Western Australia Press. p 27–50.Google Scholar
  49. Lamont BB, Maitre DCL, Cowling RM, Enright NJ. 1991. Canopy seed storage in woody plants. Bot Rev 57:277–317.Google Scholar
  50. Lewis SE, Sloss CR, Murray-Wallace CV, Woodroffe CD, Smithers SG. 2013. Post-glacial sea-level changes around the Australian margin: a review. Quat Sci Rev 74:115–38.Google Scholar
  51. Lichter J. 1998. Rates of weathering and chemical depletion in soils across a chronosequence of Lake Michigan sand dunes. Geoderma 85:255–82.Google Scholar
  52. Lindsay WL, Norvell WA. 1978. Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci Soc Am J 42:421–8.Google Scholar
  53. Lisiecki LE, Raymo ME. 2005. A Pliocene-Pleistocene stack of 57 globally distributed benthic δ18O records. Paleoceanography 20:PA1003.Google Scholar
  54. Loeppert RH, Suarez DL. 1996. Carbonate and gypsum. In: Sparks D et al., Eds. Methods in soil analysis, Part 3—Chemical methods. Madison: Soil Science Society of America. p 437–74.Google Scholar
  55. Lowry DC. 1977. Perth Basin yellow sand. Search 8:54–6.Google Scholar
  56. McArthur WM. 2004. Reference soils of south-western Australia. Perth: Department of Agriculture. p 285.Google Scholar
  57. McArthur WM, Bettenay E. 1974. Development and distribution of soils of the Swan Coastal Plain, Western Australia. Canberra: CSIRO.Google Scholar
  58. McArthur WM, Russell WGR. 1978. Soil morphological properties in relation to depth to groundwater table in a sandy landscape near Perth. Aust J Soil Res 16:347–9.Google Scholar
  59. Mehlich A. 1984. Mehlich 3 soil test extractant: a modification of Mehlich 2 extractant. Commun Soil Sci Plant Anal 15:1409–16.Google Scholar
  60. Melton JR, Mahtab SK, Swoboda AR. 1973. Diffusion of zinc in soils as a function of applied zinc, phosphorus, and soil pH. Soil Sci Soc Am J 37:379–81.Google Scholar
  61. Menge DNL, Hedin LO. 2009. Nitrogen fixation in different biogeochemical niches along as 120 000-year chronosequence in New Zealand. Ecology 90:2190–201.PubMedGoogle Scholar
  62. Miller KG, Kominz MA, Browning JV, Wright JD, Mountain GS, Katz ME, Sugarman PJ, Cramer BS, Christie-Blick N, Pekar SF. 2005. The Phanerozoic record of global sea-level change. Science 310:1293–8.PubMedGoogle Scholar
  63. Murray-Wallace CV, Kimber RWL. 1989. Quaternary marine aminostratigraphy: Perth Basin, Western Australia. Aust J Earth Sci 36:553–68.Google Scholar
  64. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J. 2000. Biodiversity hotspots for conservation priorities. Nature 403:853–8.PubMedGoogle Scholar
  65. Parfitt RL, Ross DJ, Coomes DA, Richardson SJ, Smale MC, Dahlgren RA. 2005. N and P in New Zealand soil chronosequences and relationships with foliar N and P. Biogeochemistry 75:305–28.Google Scholar
  66. Peltzer DA, Wardle DA, Allison VJ, Baisden WT, Bardgett RD, Chadwick OA, Condron LM, Parfitt RL, Porder S, Richardson SJ, Turner BL, Vitousek PM, Walker J, Walker LR. 2010. Understanding ecosystem retrogression. Ecol Monogr 80:509–29.Google Scholar
  67. Playford PE, Cockbain AE, Lowe GH. 1976. Geology of the Perth Basin, Western Australia. Bulletin 124 of the Geological Survey of Western Australia. Perth: Geological Survey of Western Australia.Google Scholar
  68. Playford PE, Cockbain AE, Berry PF, Roberts AP, Haines PW, Brooke B. 2013. The geology of Shark Bay. East Perth: Geological Survey of Western Australia.Google Scholar
  69. Prakongkep N, Gilkes RJ, Singh B, Wong S. 2012. Pyrite and other sulphur minerals in giant aquic spodosols, Western Australia. Geoderma 181–182:78–90.Google Scholar
  70. Price DM, Brooke BP, Woodroffe CD. 2001. Thermoluminescence dating of aceolianites from Lord Howe Island and south-west Western Australia. Quat Sci Rev 20:841–6.Google Scholar
  71. Salisbury EJ. 1925. Note on the edaphic succession in some dune soils with special reference to the time factor. J Ecol 13:322–8.Google Scholar
  72. Selmants PC, Hart SC. 2008. Substrate age and tree islands influence carbon and nitrogen dynamics across a retrogressive semiarid chronosequence. Glob Biogeochem Cycles. doi: 10.1029/2007GB003062.Google Scholar
  73. Selmants PC, Hart SC. 2010. Phosphorus and soil development: does the Walker and Syers model apply to semiarid ecosystems? Ecology 91:474–84.PubMedGoogle Scholar
  74. Semeniuk V, Searle DJ. 1986. Variability of Holocene sealevel history along the southwestern coast of Australia—evidence for the effect of significant local tectonism. Mar Geol 72:47–58.Google Scholar
  75. Sniderman JMK, Jordan GJ, Cowling RM. 2013. Fossil evidence for a hyperdiverse sclerophyll flora under a non-Mediterranean-type climate. Proc Natl Acad Sci 110:3423–8.PubMedCentralPubMedGoogle Scholar
  76. Soil Survey Staff. 1999. Soil taxonomy: A basic system of soil classification for making and interpreting soil surveys. Lincoln: United States Department of Agriculture–Natural Resources Conservation Service.Google Scholar
  77. Stevens PR, Walker TW. 1970. The chronosequence concept and soil formation. Q Rev Biol 45:333–50.Google Scholar
  78. Stirling CH, Esat TM, Lambeck K, McCulloch MT. 1998. Timing and duration of the Last Interglacial: evidence for a restricted interval of widespread coral reef growth. Earth Planet Sci Lett 160:745–62.Google Scholar
  79. Sulpice R, Ishihara H, Schlereth A, Cawthray GR, Encke B, Giavalisco P, Ivakov A, Arrivault S, Jost R, Krohn N, Kuo J, LalibertÉ E, Pearse SJ, Raven JA, Scheible W-R, Teste F, Veneklaas EJ, Stitt M, Lambers H. 2014. Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus-use efficiency of Proteaceae species. Plant Cell Environ 37:1276–98.PubMedCentralPubMedGoogle Scholar
  80. Syers JK, Adams JA, Walker TW. 1970. Accumulation of organic matter in a chronosequence of soils developed on wind-blown sand in New Zealand. J Soil Sci 21:146–53.Google Scholar
  81. Tackett NW, Craft CB. 2010. Ecosystem development on a coastal barrier island dune chronosequence. J Coast Res 26:736–42.Google Scholar
  82. Tapsell P, Newsome D, Bastian L. 2003. Origin of yellow sand from Tamala Limestone on the Swan Coastal Plain, Western Australia. Aust J Earth Sci 50:331–42.Google Scholar
  83. Tejan-Kella MS, Chittleborough DJ, Fitzpatrick RW, Thompson CH, Prescott JR, Hutton JT. 1990. Thermoluminescence dating of coastal sand dunes at Cooloola and North Stradbroke Island, Australia. Aust J Soil Res 28:465–81.Google Scholar
  84. Thompson CH. 1981. Podzol chronosequence on coastal dunes of eastern Australia. Nature 291:59–61.Google Scholar
  85. Thompson CH. 1992. Genesis of podzols on coastal dunes in Southern Queensland: I. Field relationships and profile morphology. Aust J Soil Res 30:593–613.Google Scholar
  86. Turner BL, Condron LM. 2013. Pedogenesis, nutrient dynamics, and ecosystem development: the legacy of T.W. Walker and J.K. Syers. Plant Soil 367:1–10.Google Scholar
  87. Turner BL, Romero TE. 2009. Short-term changes in extractable inorganic nutrients during storage of tropical rain forest soils. Soil Sci Soc Am J 73:1972–9.Google Scholar
  88. Turner BL, Condron LM, Richardson SJ, Peltzer DA, Allison VJ. 2007. Soil organic phosphorus transformations during pedogenesis. Ecosystems 10:1166–81.Google Scholar
  89. Turner BL, Condron LM, Wells A, Andersen KM. 2012. Soil nutrient dynamics during podzol development under lowland temperate rain forest. Catena 97:50–62.Google Scholar
  90. Vitousek PM. 2004. Nutrient cycling and limitation. Princeton: Princeton University Press.Google Scholar
  91. Vitousek PM, Farrington H. 1997. Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry 37:63–75.Google Scholar
  92. Walker TW, Syers JK. 1976. The fate of phosphorus during pedogenesis. Geoderma 15:1–19.Google Scholar
  93. Walker J, Thompson CH, Fergus IF, Tunstall BR. 1981. Plant succession and soil development in coastal sand dunes of subtropical eastern Australia. In: West DC, Shugart HH, Botkin DB, Eds. Forest succession: concepts and application. New York: Springer. p 107–31.Google Scholar
  94. Walker LR, Wardle DA, Bardgett RD, Clarkson BD. 2010. The use of chronosequences in studies of ecological succession and soil development. J Ecol 98:725–36.Google Scholar
  95. Wardle DA, Walker LR, Bardgett RD. 2004. Ecosystem properties and forest decline in contrasting long-term chronosequences. Science 305:509–13.PubMedGoogle Scholar
  96. Wardle DA, Bardgett RD, Walker LR, Peltzer DA, Lagerström A. 2008. The response of plant diversity to ecosystem retrogression: evidence from contrasting long-term chronosequences. Oikos 117:93–103.Google Scholar
  97. Wells A, Goff J. 2007. Coastal dunes in Westland, New Zealand, provide a record of paleoseismic activity on the Alpine fault. Geology 35:731–4.Google Scholar
  98. White PJ. 2012. Long-distance transport in the xylem and phloem. In: Marschner P, Ed. Marschner’s mineral nutrition of higher plants. London: Academic Press. p 49–70.Google Scholar
  99. Williamson WM, Wardle DA, Yeates GW. 2005. Changes in soil microbial and nematode communities during ecosystem decline across a long-term chronosequence. Soil Biol Biochem 37:1289–301.Google Scholar
  100. Woods PJ, Searle DJ. 1983. Radiocarbon dating and Holocene history of the Becher/Rockingham Beach ridge Plain, West Coast, Western Australia. Search 14:44–6.Google Scholar
  101. Wyrwoll KH, King PD. 1984. A criticism of the proposed regional extent of Late Cenozoic arid zone advances into south-western Australia. Catena 11:273–88.Google Scholar
  102. Wyrwoll K-H, Turner BL, Findlater P. 2014. On the origins, geomorphology and soils on the sandplains of south-western Australia. In: Lambers H, Ed. Plant life on the sandplains in Southwest Australia, a global biodiversity hotspot. Crawley: University of Western Australia Publishing. p 3–23.Google Scholar

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Authors and Affiliations

  1. 1.Smithsonian Tropical Research InstituteAnconRepublic of Panama
  2. 2.School of Plant BiologyThe University of Western AustraliaPerthAustralia

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