The Botanical Review

, Volume 83, Issue 2, pp 152–194 | Cite as

African Cycad Ecology, Ethnobotany and Conservation: A Synthesis

Article

Abstract

Africa hosts a rich assemblage of cycads: 66 Encephalartos species, Stangeria eriopus and Cycas thouarsii. Most Encephalartos and S. eriopus adults appear to be fire-tolerant, and certain Encephalartos species may be fire-dependent. Four Encephalartos species and S. eriopus are primarily insect-pollinated. African cycad populations typically have sex ratios of 1:1, with very small populations often male-biased. Coning is typically infrequent and erratic, with many species exhibiting mast-seeding. Viable seed production in Encephalartos populations tends to decline with decreasing population size, and seed predation by weevils is common. Seed dispersal in Encephalartos is usually localized, but vertebrates may facilitate dispersal over longer distances. Stem material of 25 Encephalartos species and S. eriopus is used for traditional medicine, primarily in South Africa. Two-thirds of Africa’s cycad species are threatened, with four species already Extinct in the Wild. The illegal acquisition of cycads from wild populations is the principle threat to their persistence. Further research is recommended on seed and fire ecology, population dynamics, and the outcomes of conservation interventions.

Keywords

Encephalartos Fire Germination Pollination Population Seed Stangeria eriopus 

Notes

Acknowledgements

Many thanks go to De Wet Bösenberg for producing the species distribution map. Wynand van Eeden is thanked for providing comments on the manuscript. Thanks go to John Donaldson, Piet Vorster, Gerhard van Deventer, Michael Calonje, Xander de Kock and David Muller for supplying photographs. We thank the University of the Witwatersrand, Johannesburg for providing funding.

Literature Cited

  1. Álvarez-Yépiz, J. C., M. Dovčiak, & A. Búrquez. 2011. Persistence of a rare ancient cycad: Effects of environment and demography. Biological Conservation 144: 122–130.Google Scholar
  2. Anonymous. 2004. A management plan for cycads in KwaZulu-Natal. Threatened Plant Conservation Unit, Biodiversity Conservation Advice Division, Ezemvelo KZN Wildlife.Google Scholar
  3. Arnold, T. H., C. A. Prentice, L. C. Hawker, E. E. Snyman, M. Tomalin, N. R. Crouch & C. Pottas-Bircher. 2002. Medicinal and Magical Plants of Southern Africa: an Annotated Checklist. Strelitzia 13. National Botanical Institute, Pretoria.Google Scholar
  4. Bamigboye, S. O., P. M. Tshisikhawe & P. J. Taylor. 2016. Review of extinction risk in African cycads. Phyton International Journal of Experimental Botany 85: 333–336.Google Scholar
  5. Bamigboye, S. O., P. M. Tshisikhawe & P. J. Taylor. 2017. Detecting threats to Encephalartos transvenosus (Limpopo cycad) in Limpopo province, South Africa through indigenous knowledge. Indian Journal of Traditional Knowledge 16(2): 251–255.Google Scholar
  6. Bayliss, J., C. Burrow, S. Martell & H. Staude. 2009. An ecological study of the relationship between two living fossils in Malawi: the Mulanje Tiger Moth (Callioratis grandis) and the Mulanje Cycad (Encephalartos gratus). African Journal of Ecology 48: 472–480.CrossRefGoogle Scholar
  7. Beaton, J. M. 1982. Fire and water: Aspects of Australian Aboriginal management of cycads. Archaeology in Oceania 17(1):51–58.CrossRefGoogle Scholar
  8. Bonta, M. 2010. Human geography and ethnobotany of cycads in Xi’ui, Teenek, and Nahuatl communities of northeastern Mexico. Final Report. Cleveland.Google Scholar
  9. Bonta, M., O. Flores Pinot, D. Graham, J. Haynes & G. Sandoval. 2006. Ethnobotany and conservation of Tiusinte (Dioon mejiae Standl. & L.O. Williams, Zamiaceae) in northeastern Honduras. Journal of Ethnobiology 26(2): 228–257.Google Scholar
  10. Boyd, W. M. 1995. The translocation and re-establishment of priority Encephalartos species in the Transvaal, South Africa. Pp 423–434. In: P. Vorster (ed). Proceedings of the Third International Conference on Cycad Biology. The Cycad Society of South Africa, Stellenbosch.Google Scholar
  11. Burbidge, A. H. & R. J. Whelan. 1982. Seed dispersal in a cycad, Macrozamia riedlei. Australian Journal of Ecology 7: 63–67.CrossRefGoogle Scholar
  12. Calonje, M., D. W. Stevenson & L. Stanberg. 2016. The World List of Cycads, online edition, 2013-2016. [cited 18 Feb 2016]. Available from: http://www.cycadlist.org.
  13. Chamberlain, C. J. 1919. The Living Cycads. The University of Chicago Press. Chicago.Google Scholar
  14. Chamberlain, C. J. 1935. Gymnosperm Structure and Evolution. University of Chicago Press. Chicago.Google Scholar
  15. Chang, D. C. N., N. Grobbelaar & J. Coetzee. 1988. SEM observations on cyanobacteria-infected cycad coralloid roots. South African Journal of Botany 54(5): 491–495.CrossRefGoogle Scholar
  16. Cilliers, A. 2012. Stimulation by fire of certain South African Encephalartos species. Encephalartos 110: 14–17.Google Scholar
  17. Clarke, P. J., M. J. Lawes, J. J. Midgley, B.-B. Lamont, F. Ojeda, G. E. Burrows, N. J. Enright & K. J. E. Knox. 2013. Resprouting as a key functional trait: how buds, protection and resources drive persistence after fire. New Phytologist. 197: 19–35.Google Scholar
  18. Coetzer, I. A. 2005. The living fossils of Africa’s biodiversity under threat: Can the most critically endangered Encephalartos cycads be saved from extinction? Encephalartos 82: 14–17.Google Scholar
  19. Cousins, S. R. 2012. The trade in South African Encephalartos species for traditional medicine: added pressure to the cycad extinction crisis. Encephalartos 107: 39–43.Google Scholar
  20. Cousins, S. R., V. L. Williams & E. T. F. Witkowski. 2011. Quantifying the trade in South African Encephalartos spp. in the traditional medicine markets of Johannesburg and Durban, South Africa. Economic Botany 65(4): 356–370.CrossRefGoogle Scholar
  21. Cousins, S. R., V. L. Williams & E. T. F. Witkowski, 2012. Uncovering the cycad taxa (Encephalartos species) traded for traditional medicine in Johannesburg and Durban, South Africa. South African Journal of Botany 78: 129–138.Google Scholar
  22. Cousins, S. R., V. L. Williams & E. T. F. Witkowski. 2013. Sifting through cycads: A guide to identifying the stem fragments of six south African medicinal Encephalartos species. South African Journal of Botany 84: 115–123.CrossRefGoogle Scholar
  23. Crouch, N. R., J. S. Donaldson, G. F. Smith, R. Symmonds, C. G. M. Dalzell & C. R. Scott-Shaw. 2000. Ex situ conservation of Stangeria eriopus (Stangeriaceae) at the Durban Botanic gardens, South Africa. Encephalartos 63: 16–24.Google Scholar
  24. Crouch, N. R., Smith, G. F., M. Lötter, & R. Symmonds. 2003. Encephalartos woodii – The first historically documented ethnomedicinal plant casualty in southern Africa. Encephalartos 73: 25–28.Google Scholar
  25. Cunningham, A. B. 1988. An investigation of the herbal medicine trade in Natal/KwaZulu. Investigational report, Vol. 29. Pietermaritzburg: Institute of Natural Resources.Google Scholar
  26. Da Silva, J. M., J. S. Donaldson, G. Reeves, & T. A. Hedderson. 2012. Population genetics and conservation of critically small cycad populations: A case study of the Albany cycad, Encephalartos latifrons (Lehmann). Biological Journal of the Linnean Society 105(2): 293–308.CrossRefGoogle Scholar
  27. Daly, B., J. S. Donaldson, Y. Friedmann, Q. Hahndiek, N. King, D. Newton, & A. Southwood. 2006. Albany cycad (Encephalartos latifrons) population and habitat viability assessment workshop report. Conservation breeding Specialist group (SCC/IUCN)/CBSG southern Africa. Endangered Wildlife Trust, Johannesburg.Google Scholar
  28. De Klerk, D. 2004. Encephalartos nubimontanus: A distinction between 11 variants. Published by the author.Google Scholar
  29. Dehgan, B. & C. K. K. H. Yuen. 1983. Seed morphology in relation to dispersal, evolution, and propagation of Cycas L. Botanical Gazette 144(3): 412–418.CrossRefGoogle Scholar
  30. Donaldson, J. S. 1993. Mast-seeding in the cycad genus Encephalartos: A test of the predator satiation hypothesis. Oecologia 94: 262–271.PubMedCrossRefGoogle Scholar
  31. Donaldson, J. S. 1995a. The Winterberg cycad: Surviving against the odds. Veld & Flora 81(2): 36–39.Google Scholar
  32. Donaldson, J. S. 1995b. Understanding cycad life histories: An essential basis for successful conservation. Pp 8–13. In: J. S. Donaldson (ed). Cycad conservation in South Africa: Issues, priorities, and actions. Cycad Society of South Africa, Stellenbosch.Google Scholar
  33. Donaldson, J. S. 1997. Is there floral parasite mutualism pollination in cycads? Pollination biology of Encephalartos villosus (Zamiaceae). American Journal of Botany 84(10): 1398–1406.CrossRefGoogle Scholar
  34. Donaldson, J. S. 1999. Insects associated with the cycads of Zimbabwe, Kenya and Zanzibar with comparisons to cycad insects from South Africa. Excelsa 19: 40–46.Google Scholar
  35. Donaldson, J. S. 2003. Cycads: A status survey and conservation action plan. IUCN/SSC Cycad Specialist Group, Gland.Google Scholar
  36. Donaldson, J. S. 2004a. Extinction of cycad pollinators – Do generalists or specialists survive as cycads decline? Pp 154. In: J. A. Lindstrom (ed). The biology, structure, and Systematics of the Cycadales. Proceedings of the Sixth International Conference on Cycad Biology. Nong Nooch Tropical Botanical Garden, Thailand.Google Scholar
  37. Donaldson, J. S. 2004b. Seeds of hope: Can trade in cycad seeds help save cycads from extinction? The Cycad Newsletter: 11–14.Google Scholar
  38. Donaldson, J. S. 2004c. CITES and cycad conservation: A way forward. The Cycad Newsletter: 8–11.Google Scholar
  39. Donaldson, J. S. 2008. South African Encephalartos species. NDF workshop case studies: Case study 4: Encephalartos. Mexico.Google Scholar
  40. Donaldson, J. S. & J. D. Bösenberg. 1995. Life history and host range of the leopard magpie moth, Zerenopsis leopardina Felder (Lepidoptera: Geometridae). African Entomology 3(2): 103–110.Google Scholar
  41. Donaldson, J. S. & J. D. Bösenberg. 1999. Changes in the abundance of south African cycads during the twentieth century: Preliminary data from the study of matched photographs. Biology and conservation of cycad. In: C. J. Chen (Ed.) Proceedings of the Fourth international Conference on cycad biology, 240–247. Beijing: International Academic Publishers.Google Scholar
  42. Donaldson, J. S., I. Nänni & J. D. Bösenberg. 1995. The role of insects in the pollination of Encephalartos cycadifolius. Pp 423–434. In: P. Vorster (ed). Proceedings of the third international Conference on cycad biology. The Cycad Society of South Africa, Stellenbosch.Google Scholar
  43. Douwes, E. 2002. The Stangeria eriopus conservation project: Ensuring the survival of the Natal grass cycad. Veld & Flora 87(4): 162–163.Google Scholar
  44. Douwes, E., N. R. Crouch, M. Mattson, C. G. M. Dalzell & G. F. Smith. 2004. The Stangeria eriopus conservation project, a gene-banking programme in action. Pp 85–91. In: J. A. Lindstrom (ed). The biology, structure, and Systematics of the Cycadales. Proceedings of the Sixth International Conference on Cycad Biology. Nong Nooch Tropical Botanical Garden, Thailand.Google Scholar
  45. Dyer, R. A. 1965. The cycads of southern Africa. Bothalia 8: 405–515.Google Scholar
  46. Fourie, S. P. 1995. Population census data and long-term monitoring of cycad populations. Pp 8–13. In: J. S. Donaldson (ed). Cycad conservation in South Africa: Issues, priorities, and actions. Cycad Society of South Africa. Stellenbosch.Google Scholar
  47. Giddy, C. 1984. Cycads of South Africa. 2nd edition. C. Struik (Pty) Ltd. Publishers, Cape Town.Google Scholar
  48. Giddy, C. 1995. Cycad conservation - a third world perspective. In: P. Vorster (ed). Proceedings of the third international Conference on cycad biology. Cycad Society of South Africa. Stellenbosch.Google Scholar
  49. Goode, D. G. 1989. Cycads of Africa. Struik Winchester.Google Scholar
  50. Goode, D. G. 2001. Cycads of Africa Volume I. D & E Cycads of Africa Publishers, Sandton.Google Scholar
  51. Golding, J. S. & P. J. H. Hurter. 2001. Perspectives on cycads in Africa. Encephalartos 68: 30–33.Google Scholar
  52. Golding, J. S. & P. J. H. Hurter. 2003. A red list account of Africa’s cycads and implications of considering life-history and threats. Biodiversity and Conservation 12: 507–528.CrossRefGoogle Scholar
  53. Grobbelaar, N. 1989. Disintegration of Encephalartos megastrobili. South African Journal of Botany 55(6): 581–585.CrossRefGoogle Scholar
  54. Grobbelaar, N. 1992. A more realistic conservation strategy for the south African cycads. Plant Life 6: 14–16.Google Scholar
  55. Grobbelaar, N. 1999. Coming frequency, gender ratio, and pollination of Encephalartos transvenosus (Zamiaceae) at the Modjadji nature reserve, South Africa and the germination of this cycad’s seed. Pp 309–318. In: C. Chen (ed). Biology and conservation of cycads. Proceedings of the Fourth International Conference on Cycad Biology. Beijing.Google Scholar
  56. Grobbelaar, N. 2003. The effect of light strength on the survival of Encephalartos lanatus seedlings. Encephalartos 75: 21–23.Google Scholar
  57. Grobbelaar, N. 2004. Cycads: With special reference to the southern African species. Published by the author. Pretoria.Google Scholar
  58. Grobbelaar, N., W. Hattingh & J. Marshall. 1986. The occurrence of coralloid roots on the south African species of the Cycadales and their ability to fix nitrogen symbiotically. South African Journal of Botany 52: 467–471.CrossRefGoogle Scholar
  59. Grobbelaar, N., J. J. M. Meyer & J. Burchmore. 1989. Coning and sex ratio of Encephalartos transvenosus at the Modjadji nature reserve. South African Journal of Botany 55(1): 79–82.CrossRefGoogle Scholar
  60. Grove, T. S., A. M. O’Connell & N. Malajczuk. 1980. Effects of fire on the growth, nutrient content and rate of nitrogen fixation of the cycad Macrozamia riedlei. Australian Journal of Botany 28: 271–281.CrossRefGoogle Scholar
  61. Harris, R. & W. Harris. 2003. Doornkop: Home of Encephalartos middelburgensis and E. lanatus. Encephalartos 73: 12.Google Scholar
  62. Heenan, D. 1977. Some observations on the cycads of Central Africa. Botanical Journal of the Linnean Society 74: 279–288.Google Scholar
  63. Heibloem, P. 1999. The Cycads of Central Africa. Palm and Cycad Societies of Australia, Brisbane.Google Scholar
  64. Hilton-Taylor, C. 1996a. Red data list of southern African plants. Strelitzia 4. National Botanical Institute, Pretoria.Google Scholar
  65. Hilton-Taylor, C. 1996b. Red data list of southern African plants: Corrections and additions. Bothalia 26: 177–182.CrossRefGoogle Scholar
  66. Hoffman, M., C. Hilton-Tayler, A. Angulo, M. Bohm, T. M. Brooks, S. H. M. Butchart, …, S. N. Stuart. 2010. The impact of conservation on the status of the world’s vertebrates. Science 330: 1503–1509.Google Scholar
  67. Hurter, J. 1994. Focus on Encephalartos heenanii R.A. Dyer. Encephalartos 40: 4–7.Google Scholar
  68. Hutchings, A., A. H. Scott, G. Lewis & A. B. Cunningham. 1996. Zulu Medicinal Plants: An Inventory. University of Natal Press. Pietermaritzburg.Google Scholar
  69. IUCN Red List of Threatened Species. Version 2015–4. www.iucnredlist.org. Downloaded 8 January 2016.
  70. Jones, D. L. 1993. Cycads of the World: Ancient Plants in Today’s Landscape. REED (William Heinemann). Chatswood, Australia.Google Scholar
  71. Krishnamurthy, V., L. Mandle, T. Ticktin, R. Ganesan, C. S. Saneesh & A. Varghese. 2013. Conservation status and effects of harvest on an endemic multi-purpose cycad, Cycas circinalis L., western Ghats, India. Tropical Ecology 54(3): 309–320.Google Scholar
  72. López-Gallego, C. 2008. Demographic variation in cycad populations inhabiting contrasting forest fragments. Biodiversity Conservation 17: 1213–1225.CrossRefGoogle Scholar
  73. Mander, M. 1998. Marketing of indigenous medicinal plants in South Africa: A case study in KwaZulu-Natal. FAO of the UN, Rome.Google Scholar
  74. Mander, M., L. Ntuli, N. Diederichs & K. Mavundla. 2007. Economics of the traditional medicine trade in South Africa. Pp 189–196. In: S. Harrison, R. Bhana, A. Ntuli. (eds). South African Health Review 2007. Health Systems Trust, Durban.Google Scholar
  75. Marloth, R. 1914. Notes on the entomophilous nature of Encephalartos. Transactions of the Royal Society of South Africa 4: 69–71.CrossRefGoogle Scholar
  76. Melville, R. 1957. Encephalartos in central Africa. Kew Bulletin 12: 237–257.CrossRefGoogle Scholar
  77. Miringu, B. W. 1999. The population and conservation status of the Kenyan cycads, and their potential as a horticultural crop. Pp 391–396. In: C. J. Chen, (ed). Proceedings of the Fourth international Conference on cycad biology. BeijingGoogle Scholar
  78. Moretti, A., S. Sabato & G. G. Siniscalco. 1983. Taxonomic significance of methylazoxymethanol glycosides in the cycads. Phytochemistry 22: 115–117.CrossRefGoogle Scholar
  79. Nair, J. J. & J. Van Staden. 2012. Isolation and quantification of the toxic methylazoxymethanol glycoside macrozamin in selected south African cycad species. South African Journal of Botany 82: 108–112.CrossRefGoogle Scholar
  80. Negrón-Ortiz, V. & D. L. Gorchov. 2000. Effects of fire season and postfire herbivory on the cycad Zamia pumila (Zamiaceae) in slash pine savanna, Everglades National Park, Florida. International Journal of Plant Sciences 161(4): 659–669.Google Scholar
  81. Nordling, L. 2014. Forensic chemistry could stop African plant thieves: Isotope analysis could help in the rush to save South Africa’s cycads from extinction. Nature 514(17).Google Scholar
  82. Norstog, K. J. & T. J. Nicholls. 1997. The Biology of the Cycads. Cornell University Press, Ithaca, N.Y.Google Scholar
  83. Nowak, K. & P. C. Lee. 2011. Consumption of cycads Encephalartos hildebrandtii by Zanzibar red colobus Procolobus kirkii. Journal of East African Natural History 100: 123–131.CrossRefGoogle Scholar
  84. Oberprieler, R. G. 1995a. The weevils (Coleoptera: Curculionoidea) associated with cycads. 1. Classification, relationships, and biology. Pp. 295–334. In: P. Vorster (ed). Proceedings of the third international Conference on cycad biology. Cycad Society of South Africa, Stellenbosch.Google Scholar
  85. Oberprieler, R. G. 1995b. The weevils (Coleoptera: Curculionoidea) associated with cycads. 2. Host specificity and implications for cycad taxonomy. Pp 335–365. In: P. Vorster (ed). Proceedings of the third international Conference on cycad biology. Cycad Society of South Africa, Stellenbosch.Google Scholar
  86. Oberprieler, R. G. 2004. “evil weevils” — The key to cycad survival and diversification? Pp 170–194. In: J. A. Lindstrom (ed). Proceedings of the sixth international cycad Conference on cycad biology. Nong Nooch Tropical Botanical Garden, Thailand.Google Scholar
  87. Okubamichael, D. Y., S. L. Jack, J. D. Bösenberg, M. T. Hoffman & J. S. Donaldson. 2016. Repeat photography confirms alarming decline in south African cycads. Biodiversity Conservation 25(11): 2153–2170.Google Scholar
  88. Osborne, R. 1990a. A conservation strategy for the south African cycads. South African Journal of Science 86: 220–223.Google Scholar
  89. Osborne, R. 1990b. Two new reports of cycad sex changes. Encephalartos 23: 18–20.Google Scholar
  90. Osborne, R. 1995. The world cycad census and a proposed revision of the threatened species status for cycad taxa. Biological Conservation 71: 1–12.CrossRefGoogle Scholar
  91. Osborne, R. & Gorelick, R. 2003. Sex change in cycads. Palms & Cycads 76: 10–15.Google Scholar
  92. Osborne, R. & Gorelick, R. 2007. Sex change in cycads: Cases, causes, and chemistry. Memoirs of the New York Botanical Garden 97: 335–345.Google Scholar
  93. Osborne, R., A. Grove, P. Oh, T. J. Mabry, J. C. Ng & A. A. Seawright. 1994. The magical and medicinal usage of Stangeria eriopus in South Africa. Journal of Ethnopharmacology 43: 67–72.PubMedCrossRefGoogle Scholar
  94. Pearson, H. H. W. 1905. Notes on south African cycads. Transactions of the South African Philosophical Society 16: 341–354.CrossRefGoogle Scholar
  95. Pearson, H. H. W. 1916. The Kirstenbosch cycads. Journal of the Botanical Society 2: 7–13.Google Scholar
  96. Pérez-Farrera, M. A. & A. P. Vovides. 2006. The ceremonial use of the threatened “Espadana” cycad (Dioon merolae, Zamiaceae) by a community of the central depression of Chiapas, Mexico. Boletín de la Sociedad Botánica de México 78: 107–113.Google Scholar
  97. Pérez-Farrera, M. A., A. P. Vovides, P. Octavio-Aguilar, J. González-Astorga, J. de la Cruz-Rodríguez, R. Hernández-Jonapá, S. M. Villalobos-Méndez & M. A. Pérez-Farrerra. 2006. Demography of the cycad Ceratozamia mirandae (Zamiaceae) under disturbed and undisturbed conditions in a biosphere Reserve of Mexico. Plant Ecology 187(1): 97–108.Google Scholar
  98. Phelan, J., H. Van Hensbergen & R. Osborne. 1993. The apparent seed viability of Encephalartos ferox growing in sun and shade conditions in the wild. Encephalartos 34: 11–14.Google Scholar
  99. Prado, A. 2011. The cycad herbivores. Bulletin de la Société d’entomologie du Québec. Antennae 18(1): 3–6.Google Scholar
  100. Prakash, S. & J. Van Staden. 2008. Genetic variability and species identification within Encephalartos using random amplified polymorphic DNA (RAPD) markers. South African Journal of Botany 74: 735–739.CrossRefGoogle Scholar
  101. Procheş, Ş. & S. D. Johnson. 2009. Beetle pollination of the fruit-scented cones of the south African cycad Stangeria eriopus. American Journal of Botany 96: 1722–1730.PubMedCrossRefGoogle Scholar
  102. Radha, P. & R. Singh. 2008. Ethnobotany and conservation status of Indian Cycas species. Encephalartos 93(1): 15–21.Google Scholar
  103. Raimondo, D. 2001. Investigating the impacts of plant collecting on the population dynamics of two cycad species using population projection matrices and elasticity analyses. Masters dissertation. University of Cape Town.Google Scholar
  104. Raimondo, D. & J. S. Donaldson. 2003. Responses of cycads with different life histories to the impact of plant collecting: Simulation models to determine important life history stages and population recovery times. Biological Conservation 111: 345–358.CrossRefGoogle Scholar
  105. Raimondo, D., L. Von Staden, W. Foden, J. E. Victor, N. A. Helme, R. C. Turner, D. A. Kamundi & P. A. Manyama (eds). 2009. Red list of south African plants. Strelitzia 25. South African National Biodiversity Institute, Pretoria.Google Scholar
  106. Rattray, G. 1913. Notes on the pollination of some south African cycads. Transactions of the Royal Society of South Africa 3, 259–270.CrossRefGoogle Scholar
  107. Ravele, A. M. & R. A. Makhado. 2008. The value of cycads to human wellbeing – An overview. Encephalartos 93: 23–26.Google Scholar
  108. Ravele, A. M. & R. A. Makhado. 2009. Exploitation of Encephalartos transvenosus outside and inside Mphaphuli cycads nature reserve, Limpopo Province, South Africa. African Journal of Ecology 48: 105–110.CrossRefGoogle Scholar
  109. Rayner, T. & A. Pires. 2016. Protecting highly threatened south African cycads from extinction: A new approach. Veld & Flora 102(1): 14–16.Google Scholar
  110. Retief, K., A. G. West & M. F. Pfab. 2014. Can stable isotopes and radiocarbon dating provide a forensic solution for curbing illegal harvesting of threatened cycads? Journal of Forensic Sciences 59(6): 1541–1551.PubMedCrossRefGoogle Scholar
  111. Retief, K., A. G. West & M. F. Pfab. 2015. Are you involved in the illegal cycad trade? Public misconceptions which are detrimental to the survival of South Africa’s cycads. Veld & Flora 101(1): 13–15.Google Scholar
  112. Robbertse, H., T. Naudé & R. Rousseau. 1999. Encephalartos middelburgensis population at Rhenosterpoort. Encephalartos 58: 26–29.Google Scholar
  113. Rousseau, P. 2011. Systematic analysis of the African endemic cycad genera Encephalartos Lehm. And Stangeria T. Moore. MSc. Dissertation. University of Johannesburg.Google Scholar
  114. Rousseau, P. 2013. Successive male cone production in Encephalartos. Encephalartos 114: 26–32.Google Scholar
  115. Rousseau, R. & P. Rousseau. 2011. Encephalartos middelburgensis on site propagation project: Progress and prospects with lessons learnt. Encephalartos 104: 20–24.Google Scholar
  116. Sass, C., D. P. Little, D. W. Stevenson & C. D. Specht. 2007. DNA barcoding in the Cycadales: Testing the potential of proposed barcoding markers for species identification of cycads. PLoS One 2 (11): e1154.PubMedPubMedCentralCrossRefGoogle Scholar
  117. Schneider, D., M. Wink, F. Sporer & P. Lounibos. 2002. Cycads: Their evolution, toxins, herbivores and insect pollinators. Naturwissenschaften 89: 281–294.PubMedCrossRefGoogle Scholar
  118. Scott-Shaw, C. R. 1995. Demographic studies of Encephalartos ghellinckii. Pp 435–439. In: P. Vorster (ed). Proceedings of the third international Conference on cycad biology. The Cycad Society of South Africa. Stellenbosch.Google Scholar
  119. Scott-Shaw, C. R. 1999. Rare and threatened plants of KwaZulu-Natal and Neighbouring regions. KwaZulu-Natal Nature Conservation Service, Congella, South Africa.Google Scholar
  120. Silvertown, J. W. 1980. The evolutionary ecology of mast seeding in trees. Biological Journal of the Linnean Society 14: 235–250.Google Scholar
  121. Singh, K. 2012. Population dynamics of the Zuurberg cycad and the predicted impact of climate change. Masters Dissertation. Nelson Mandela Metropolitan University, Port Elizabeth.Google Scholar
  122. Snow, E. L. & G. H. Walter. 2007. Large seeds, extinct vectors and contemporary ecology: Testing dispersal in a locally distributed cycad, Macrozamia lucida (Cycadales). Australian Journal of Botany 55: 592–600.CrossRefGoogle Scholar
  123. Staude, H. 2001. African cycads and moths: An intricate relationship of ancient origin. Pp 307-311. In: D. G. Goode. Cycads of Africa, Volume I. D & E Cycads of Africa Publishers. Sandton.Google Scholar
  124. Stiles, D. 1981. The Boni: Problems of a hunting-gathering people. Africana 8(2): 23–25.Google Scholar
  125. Stobart, M. 1989. Beetles and pollination in Encephalartos altensteinii. Encephalartos 17: 32.Google Scholar
  126. Suinyuy, T. N., J. S. Donaldson & S. D. Johnson. 2009. Insect pollination in the African cycad Encephalartos friderici-guilielmi Lehm. South African Journal of Botany 75: 682–688.CrossRefGoogle Scholar
  127. Suinyuy, T. N., J. S. Donaldson & S. D. Johnson. 2010. Scent chemistry and patterns of thermogenesis in male and female cones of the African cycad Encephalartos natalensis (Zamiaceae). South African Journal of Botany 76: 717–725.Google Scholar
  128. Suinyuy, T. N., J. S. Donaldson & S. D. Johnson. 2012. Geographical variation in cone volatile composition among populations of African cycad Encephalartos villosus. Biological Journal of the Linnean Society 106: 514–527.Google Scholar
  129. Suinyuy, T. N., J. S. Donaldson & S. D. Johnson. 2013a. Patterns of odour emission, thermogenesis and pollinator activity in cones of an African cycad: What mechanisms apply? Annals of Botany 112: 891–902.PubMedPubMedCentralCrossRefGoogle Scholar
  130. Suinyuy, T. N., J. S. Donaldson & S. D. Johnson. 2013b. Variation in the chemical composition of cone volatiles within the African cycad genus Encephalartos. Phytochemistry 85: 82–91.PubMedCrossRefGoogle Scholar
  131. Tang, W. 1987. Heat production in cycad cones. Botanical Gazette 148: 165–174.Google Scholar
  132. Tang, W., L. Sternberg & D. Price. 1987. Metabolic aspects of thermogenesis in male cones of five cycad species. American Journal of Botany 74: 1555–1559.Google Scholar
  133. Terry, I., C. J. Moore, G. H. Walter, P. I. Forster, R. B. Roemer, J. S. Donaldson & P. J. Machin. 2004. Association of cone thermogenesis and volatiles with pollinator specificity in Macrozamia cycads. Plant Systematics and Evolution 243: 233–247.CrossRefGoogle Scholar
  134. Terry, I., G. H. Walter, C. J. Moore, R. B. Roemer & C. Hull. 2007. Odor-mediated push-pull pollination in cycads. Science 318(5847): 70.Google Scholar
  135. Thieret, J. W. 1958. Economic botany of the cycads. Economic Botany 12(1): 3–41.CrossRefGoogle Scholar
  136. Van der Walt, K. 2010. The critical difference between extinction and survival: Ex situ conservation of Encephalartos species in the Lowveld National Botanical Garden, South Africa. Encephalartos 100: 11–16.Google Scholar
  137. Varghese, A. & T. Ticktin. 2006. Harvest, trade, and conservation of the endemic multiuse cycad, Cycas circinalis L., in the Nilgiri Biosphere Reserve, South India. People and Plants International and Keystone Foundation. Unpublished report. http://www.docstoc.com/docs/83695331/An-assessment-of-the-impactsof-harvest-on-Cycas-circinalis.
  138. Vice, A. 1995. Encephalartos altensteinii: A massive rape but possible recovery. Encephalartos 44: 15–19.Google Scholar
  139. Vorster, P. & E. Vorster. 1985. Focus on Stangeria eriopus. Encephalartos 198(5): 8–17.Google Scholar
  140. Vorster, P. 2004. Growth form and habitat preference of the Cycadales. Pp 121–130. In: J.A. Lindstrom (ed). The biology, structure and Systematics of the Cycadales, Proceedings of the Sixth International Conference on Cycad Biology, Nong Nooch Tropical Botanical Garden, Thailand.Google Scholar
  141. Vovides, A., N. Ogato & V. Sosa. 1997. Pollination of endangered Cuban cycad Microcycas calocoma (Miq.) a.DC. Botanical Journal of the Linnean Society 125: 201–210.Google Scholar
  142. Walter, K. S. & H. J. Gillett (eds). 1998. IUCN red list of threatened plants. Compiled by the world conservation monitoring Centre, IUCN –The World Conservation Union, Gland, Switzerland and Cambridge, UK.Google Scholar
  143. Walters, T. 2003. Off-site collections. Pp 48–53. In: J. S. Donaldson (ed). Cycads: A status survey and conservation action plan. IUCN/SSC Cycad Specialist Group, Gland.Google Scholar
  144. Watt, J. M. & M. G. Breyer-Brandwijk. 1962. The medical and poisonous plants of southern and eastern Africa, 2nd edition. Livingstone.Google Scholar
  145. Whitelock, L. M. 2002. The Cycads. Timber Press Inc. Portland, Oregon.Google Scholar
  146. Williams, V. L. 2003. Hawkers of Health: An investigation of the Faraday street traditional medicine market in Johannesburg, Gauteng. Plant ecology and conservation series no. 15 (report to Gauteng Directorate of Nature Conservation, DACEL). University of the Witwatersrand, Johannesburg.Google Scholar
  147. Williams, V. L., K. Balkwill & E. T. F. Witkowski. 2001. A lexicon of plants traded in the Witwatersrand umuthi shops, South Africa. Bothalia 31:71–98.Google Scholar
  148. Williams, V. L., S. R. Cousins & E. T. F. Witkowski. 2014. From fragments to figures: Estimating the number of Encephalartos stems in a muthi market. South African Journal of Botany 93: 242–246.CrossRefGoogle Scholar
  149. Williams, V. L., E. T. F. Witkowski & K. Balkwill. 2007. Volume and financial value of species traded in the medicinal plant markets of Gauteng, South Africa. International Journal of Sustainable Development and World Ecology 14: 584–603.CrossRefGoogle Scholar
  150. Williamson, J., O. Maurin, S. Shiba, Van der Bank, H., M. Pfab, M. Pilusa, R. Kabongo & Van der Bank, M.. 2016. Exposing the illegal trade in cycad species (Cycadophyta: Encephalartos) at two traditional medicine markets in South Africa using DNA barcoding. Genome 59(9): 771–781.Google Scholar
  151. Woodenberg, W., D. P. Erdey, N. W. Pammenter & P. Berjak. 2007. Post-shedding seed behaviour of selected Encephalartos species. South African Journal of Botany 73(3): 496.Google Scholar
  152. Zobolo, A. M. & Q. N. Mkabela. 2006. Traditional knowledge transfer of activities practised by Zulu women to manage medicinal and food plant gardens. African Journal of Range & Forage Science 23(1): 77–80.CrossRefGoogle Scholar
  153. Zunckel, K. 1990. The ecology and management of the Kaapsehoop cycad (Encephalartos laevifolius Stapf and Burtt Davy). PhD thesis. University of Cape Town.Google Scholar
  154. Zunckel, K. 1995. The role of insects and fire in the ecology of Encephalartos laevifolius and their management implications. Pp 287–293. In: P. Vorster (ed). Proceedings of the third international Conference on cycad biology. Cycad Society of South Africa, Stellenbosch.Google Scholar

Copyright information

© The New York Botanical Garden 2017

Authors and Affiliations

  1. 1.School of Animal, Plant and Environmental SciencesUniversity of the WitwatersrandJohannesburgSouth Africa

Personalised recommendations