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Pollination of the Australian cycad Cycas ophiolitica (Cycadaceae): the limited role of wind pollination in a cycad with beetle pollinator mutualists, and its ecological significance

Published online by Cambridge University Press:  17 April 2018

John A. Hall*
School of Biological Sciences, The University of Queensland, Brisbane, QLD 4072, Australia
Gimme H. Walter
School of Biological Sciences, The University of Queensland, Brisbane, QLD 4072, Australia
*Corresponding author. Email:


Cycads in the Zamiaceae are well known for their host-specific insect pollination mutualisms. Pollination of Cycas in the sister family Cycadaceae is less well-documented, with beetle pollination possibly coexisting with a limited potential for wind pollination, a hypothesis we tested for C. ophiolitica in Central Queensland, Australia. Cones were associated with three species of beetle: an undescribed weevil (Curculionidae), Hapalips sp. (Erotylidae) and Ulomoides sp. (Tenebrionidae). Pollination-vector exclusion experiments compared the pollination success (quantified as % ovules pollinated per cone) of control cones against bagged or netted cones that excluded wind or insects respectively (n = 10 for all treatments). Insects do pollinate C. ophiolitica in the absence of wind, the median (first quartile-third quartile) pollination success of control plants being 83.7% (60.8–87.2%) while bagged cones, from which wind, but not insects, were excluded, pollinated at 52.9% (19.5–74.8%). For netted cones, (excluding insects but not wind), pollination fell to 12.6% (10.9–45.9%). Airborne pollen (as quantified by capture on a series of adhesive pollen traps) decreased rapidly with distance from male cones, potentially becoming ineffective for wind pollination at ~5 m. Airborne pollen load in the vicinity of female cones, and distance of females from neighbouring males, suggests wind pollination may occur sporadically, but only at high spatial densities. Although Cycas appears to be primarily insect pollinated, this limited potential for ambophily may be significant given the history of dispersal and pollinator host shifts among these cycads.

Research Article
Copyright © Cambridge University Press 2018 

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ACKERMANN, J. D. 2000. Abiotic pollen and pollination: ecological, functional, and evolutionary perspectives. Plant Systematics and Evolution 222:167185.Google Scholar
AZUMA, H. & KONO, M. 2006. Estragole (4-allylanisole) is the primary compound in volatiles emitted from the male and female cones of Cycas revoluta. Journal of Plant Research 119:671676.Google Scholar
BANNERT, M. & STAMP, P. 2007. Cross-pollination of maize at long distance. European Journal of Agronomy 27:4451.Google Scholar
BITTENCOURT, J. V. M. & SEBBENN, A. M. 2007. Patterns of pollen and seed dispersal in a small fragmented population of the wind-pollinated tree Araucaria angustifolia in southern Brazil. Heredity 207:580591.Google Scholar
BITTENCOURT, J. V. M. & SEBBENN, A. M. 2008. Pollen movement within a continuous forest of wind-pollinated Araucaria angustifolia, inferred from paternity and TwoGENER analysis. Conservation Genetics 9:855868.Google Scholar
BROOKES, D. R., HEREWARD, J. P., TERRY, L. I. & WALTER, G. H. 2015. Evolutionary dynamics of a cycad obligate pollination mutualism – pattern and process in extant Macrozamia cycads and their specialist thrips pollinators. Molecular Phylogenetics and Evolution 93:8393.Google Scholar
COOK, J. M., BEAN, D., POWER, S. A. & DIXON, D. J. 2004. Evolution of a complex coevolved trait: active pollination in a genus of fig wasps. Journal of Evolutionary Biology 17:238246.Google Scholar
CULLEY, T. M., WELLER, S. G. & SAKAI, A. K. 2002. The evolution of wind pollination in angiosperms. Trends in Ecology and Evolution 17:361369.Google Scholar
DAFNI, A. 1992. Pollination ecology: a practical approach. IRL Press, Oxford. 250 pp.Google Scholar
DEHGAN, B. & DEHGAN, N. B. 1988. Comparative pollen morphology and taxonomic affinities in Cycadales. American Journal of Botany 75:15011516.Google Scholar
DONALDSON, J. S. 1997. Is there a floral parasite mutualism in cycad pollination? The pollination biology of Encephalartos villosus. American Journal of Botany 84:13981406.Google Scholar
DOW, B. D. & ASHLEY, M. V. 1998. Factors influencing male mating success in bur oak Quercus macrocarpa. New Forests 15:161180.Google Scholar
FAEGRI, K. & VAN DER PIJL, L. 1979. The principles of pollination ecology. Pergamon Press, Oxford. 244 pp.Google Scholar
FORSTER, P., MACHIN, P., MOUND, L. & WILSON, G. 1994. Insects associated with reproductive structures of cycads in Queensland and North East New South Wales, Australia. Biotropica 26:217222.Google Scholar
GAO, Z. & THOMAS, B. A. 1989. A review of fossil cycad megasporophylls, with new evidence of Crossozamia pomel and its associated leaves from the Lower Permian of Taiyuan, China. Review of Palaeobotany and Palynology 60:205223.Google Scholar
GODSOE, W., YODER, J. B., SMITH, C. I. & PELLMYR, O. 2008. Coevolution and divergence in the Joshua tree/yucca moth mutualism. American Naturalist 171:816823.Google Scholar
GOODE, D. 2001. Cycads of Africa: volume 1. Cycads of Africa Publishers, Gallomanor. 351 pp.Google Scholar
GRIFFITHS, A. D., SCHULT, H. J. & GORMAN, J. 2005. Wild harvest of Cycas arnhemica (Cycadaceae): impact on survival, recruitment and growth in Arnhem Land, northern Australia. Australian Journal of Botany 53:771779.Google Scholar
HALL, J. A. & WALTER, G. H. 2011. Does pollen aerodynamics correlate with pollination vector? Pollen settling velocity as a test for wind versus insect pollination among cycads (Gymnospermae: Cycadaceae: Zamiaceae). Biological Journal of the Linnean Society 104:7592.Google Scholar
HALL, J. A., WALTER, G. H., BERGSTROM, D. M. & MACHIN, P. 2004. Pollination ecology of the Australian cycad Lepidozamia peroffskyana (Zamiaceae). Australian Journal of Botany 52:333343.Google Scholar
HAMADA, T., TERRY, I. & MARLER, T. E. 2015a. Habitats, trade winds, and pollination of the endangered Cycas micronesica: is there a role for wind as pollen vector on the island of Guam? International Journal of Plant Sciences 176:525543.Google Scholar
HAMADA, T., TERRY, I., ROEMER, R. & MARLER, T. E. 2015b. Potential drift of pollen of Cycas micronesica on the island of Guam: a comparative study. Hortscience 50:11061117.Google Scholar
HERRE, E. A., JANDER, K. C. & MACHADO, C. A. 2008. Evolutionary ecology of figs and their associates: recent progress and outstanding puzzles. Annual Review of Ecology, Evolution and Systematics 39:439458.Google Scholar
HILL, K. D. 1994. The Cycas rumphii complex (Cycadaceae) in New Guinea and the Western Pacific. Australian Systematic Botany 7:543567.Google Scholar
HILL, K. D. 1998. Cycadaceae. Pp. 598635 in McCarthy, P. M. (ed.). Flora of Australia volume 48, ferns gymnosperms and allied groups. ABRS/CSIRO Australia, Melbourne.Google Scholar
HILL, K. D. 1999. Cycas – an evolutionary perspective. Pp. 98115 in Chen, C. J. (ed.). Proceedings of the fourth international conference on cycad biology. International Academic Publishers, Beijing.Google Scholar
JONES, D. L. 2002. Cycads of the world. (Second edition). Reed New Holland Books, Sydney. 456 pp.Google Scholar
KEPPEL, G., HODGSKISS, P. D. & PLUNKETT, G. M. 2008. Cycads in the insular South-West Pacific: dispersal or vicariance? Journal of Biogeography 35:10041015.Google Scholar
KONO, M. & TOBE, H. 2007. Is Cycas revoluta (Cycadaceae) wind or insect pollinated? American Journal of Botany 94:847855.Google Scholar
LESCHEN, R. A. B. 2003. Fauna of New Zealand 47. Erotylidae (Insecta: Coleoptera: Cucujoidea): phylogeny and review. Manaaki Whenua Press, Lincoln. 108 pp.Google Scholar
MACGILLIVRAY, D. B. 1987. A centrifuging method for the removal of insect pollen loads. Journal of the Entomological Society of Southern Africa 50:522523.Google Scholar
MARLER, T. E. 2010. Cycad mutualist offers more than pollen transport. American Journal of Botany 97:841845.Google Scholar
MARSHALL, J., GROBBELAAR, N., COETZEE, J. & OSBORNE, R. 1989. Pollen morphology of the Cycadales with special reference to the Encephalartos species. Pollen et Spores 31:229249.Google Scholar
MCCARTNEY, H. A. & LACEY, M. E. 1991. Wind dispersal of pollen from crops of oilseed rape (Brassica napus L.). Journal of Aerosol Science 22:467477.Google Scholar
MELÉNDEZ-RAMÍREZ, V., PARRA-TABLA, V., KEVAN, P. G., RAMÍREZ-MORILLO, I., HARRIES, H., FERNÀNDEZ-BARRERA, M. & ZIZUMBO-VILLAREAL, D. 2004. Mixed mating strategies and pollination by insects and wind in coconut palm (Cocos nucifera L. (Arecaceae)): importance in production and selection. Agricultural and Forest Entomology 6:155163.Google Scholar
NIKLAS, K. J. & NORSTOG, K. 1984. Aerodynamics and pollen grain depositional patterns on cycad megastrobili: implications on the reproduction of three cycad genera (Cycas, Dioon and Zamia). Botanical Gazette 145:92104.Google Scholar
NORSTOG, K. J., STEVENSON, D. W. & NIKLAS, K. J. 1986. The role of beetles in the pollination of Zamia furfuracea. Biotropica 18: 300306.Google Scholar
OBERPRIELER, R. G. 1995a. The weevils (Coleoptera: Curculionoidea) associated with cycads 1. Classification, relationships, and biology. Pp. 295334 in Vorster, P. (ed.). Proceedings of the third international conference on cycad biology. The Cycad Society of South Africa, Stellenbosch.Google Scholar
OBERPRIELER, R. G. 1995b. The weevils (Coleoptera: Curculionoidea) associated with cycads 2. Host specificity and implications for cycad taxonomy. Pp. 335365 in Vorster, P. (ed.). Proceedings of the third international conference on cycad biology. The Cycad Society of South Africa, Stellenbosch.Google Scholar
ORNDUFF, R. 1991. Size classes, reproductive behaviour and insect associates of Cycas media in Australia. Botanical Gazette 152:203207.Google Scholar
ORNDUFF, R. 1992. Features of coning and foliar phenology, size classes and insect associates of Cycas armstrongii in the Northern Territory, Australia. Bulletin of the Torrey Botanical Club 119:3943.Google Scholar
PELLMYR, O. 2003. Yuccas, yucca moths and coevolution: a review. Annals of the Missouri Botanical Garden 90:3555.Google Scholar
PELLMYR, O., THOMPSON, J. N., BROWN, J. M., HARRISON, R. G. 1996. Evolution of pollination and mutualism in the yucca moth lineage. American Naturalist 148:827847.Google Scholar
PROCHES, S. & JOHNSON, S. D. 2009. Beetle pollination of the fruit-scented cones of the South African cycad Stangeria eriopus. American Journal of Botany 96:17221730.Google Scholar
PROCTOR, M., YEO, P. & LACK, A. 1996. The natural history of pollination. Harper Collins Publishers, London. 479 pp.Google Scholar
RAJU, A. J. S. & JONATHAN, K. H. 2010a. Anemophily, accidental cantharophily, seed dispersal and seedling ecology of Cycas sphaerica Roxb. (Cycadaceae), a data-deficient red-listed species of northern Eastern Ghats. Current Science 99:11051111.Google Scholar
RAJU, A. J. S. & JONATHAN, K. H. 2010b. Reproductive ecology of Cycas beddomei Dyer (Cycadaceae), an endemic and critically endangered species of southern Eastern Ghats. Current Science 99:18331840.Google Scholar
ROEMER, R., TERRY, I., CHOCKLEY, C. & JACOBSEN, J. 2005. Experimental evaluation and thermo-physical analysis of thermogenesis in male and female cycad cones. Oecologia 144:8897.Google Scholar
ROEMER, R., TERRY, I., & MARLER, T. E. 2013. Cone thermogenesis and its limits in the tropical Cycas micronesica (Cycadaceae): association with cone growth, dehiscence, and post-dehiscence phases. American Journal of Botany 100:19811990.Google Scholar
SALAS-LEIVA, D. E., MEEROW, A. W., CALONJE, M., GRIFFITH, M. P., FRANCISCO-ORTEGA, J., NAKAMURA, K., STEVENSON, D. W., LEWIS, C. E. & NAMOFF, S. 2013. Phylogeny of the cycads based on multiple single-copy nuclear genes: congruence of concatenated parsimony, likelihood and species tree inference methods. Annals of Botany 112:12631278.Google Scholar
SKELLEY, P., XU, G., TANG, W., LINDSTROM, A. J., MARLER, T., KHURAIJAM, J. S., SINGH, R. P., RADHA, P. & RICH, S. 2017. Review of Cycadophila Xu, Tang & Skelley (Coleoptera: Erotylidae: Pharaxonothinae) inhabiting Cycas (Cycadaceae) in Asia, with descriptions of a new subgenus and thirteen new species. Zootaxa 4267:163.Google Scholar
SUINYUY, T. N., DONALDSON, J. S. & JOHNSON, S. D. 2009. Insect pollination in the African cycad Encephalartos friderici-guilielmi Lehm. South African Journal of Botany 75:682688.Google Scholar
SUINYUY, T. N., DONALDSON, J. S. & JOHNSON, S. D. 2015. Geographical matching of volatile signals and pollinator olfactory responses in a cycad brood-site mutualism. Proceedings of the Royal Society Series B – Biological Sciences 282:20152053.Google Scholar
TANG, W. 1987a. Insect pollination in the cycad Zamia pumila. American Journal of Botany 74:9099.Google Scholar
TANG, W. 1987b. Heat production in cycad cones. Botanical Gazette 148:165174.Google Scholar
TANG, W., OBERPRIELER, R. & YANG, S. L. 1999. Beetles (Coleoptera) in cones of Asian Cycas: diversity, evolutionary patterns, and implications for Cycas taxonomy. Pp. 280297 in Chen, C. J. (ed.). Proceedings of the fourth international conference on cycad biology. International Academic Publishers, Beijing.Google Scholar
TERRY, I. 2001. Thrips and weevils as dual, specialist pollinators of the Australian cycad Macrozamia communis (Zamiaceae). International Journal of Plant Sciences 162:12931305.Google Scholar
TERRY, I., WALTER, G. H., DONALDSON, J. S., SNOW, E., FORSTER, P. I. & MACHIN, P. J. 2005. Pollination of Australian Macrozamia cycads (Zamiaceae): effectiveness and behaviour of specialist vectors in a dependant mutualism. American Journal of Botany 92:931940.Google Scholar
TERRY, I., HULL, C., MOORE, C. & WALTER, G. 2007. The role of host cone odour in mediating behaviour of Cycadothrips and Tranes weevils to their specific cycad. Memoirs of the New York Botanical Garden 97:346371.Google Scholar
TERRY, I., ROE, M., TANG, W. & MARLER, T. E. 2009. Cone insects and putative pollen vectors of the endangered cycad, Cycas micronesica. Micronesica 41:8399.Google Scholar
WANG, Q., LI, C. L., YANG, S. Y., HUANG, R. & CHEN, F. L. 1997. Pollination biology of Cycas panzhihuaensis L. Zhou et SY Yang. Acta Botanica Sinica 39:156163.Google Scholar
WATKINSON, A. R. & POWELL, J. C. 1997. The life history and population structure of Cycas armstrongii in monsoonal northern Australia. Oecologia 111:341349.Google Scholar
WEIBLEN, G. D. 2002. How to be a fig wasp. Annual Review of Entomology 47:299330.Google Scholar
WILSON, G. W. 2002. Insect pollination in the cycad genus Bowenia (Stangeriaceae). Biotropica 34:438441.Google Scholar
WOODALL, P. F. 2016. Notes on Cycas megacarpa at Kroombit Tops National Park, Central Queensland. Queensland Naturalist 54:4752.Google Scholar
XU, G., TANG, W., SKELLEY, P., LIU, N. & RICH, S. 2015. Cycadophila, a new genus (Coleoptera: Erotylidae: Pharaxonothinae) inhabiting Cycas debaoensis (Cycadaceae) in Asia. Zootaxa 3986:251278.Google Scholar
YANG, Q. G., Li, N., Li, Z. G., LIN, P. Y. & YU, H. Q. 2010. Studies on the pollination vectors of Cycas enlongata. Journal of Tropical and Subtropical Botany 18:129132.Google Scholar