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—-1 —0 —+1 William Tang and Charles W. O'brien William Tang and Charles W. O’Brien 351 the Third International Conference on Cycad Biology. The Cycad Society of South Africa, Stellenbosch, South Africa. O’Brien, C. W. & G. J. Wibmer. 1982. Annotated checklist of the weevils (Curculionidae sensu lato) of North America, Central America, and the West Indies (Coleoptera: Curculionoi- dea). Mem. Amer. Entomol. Inst. 34. Stevenson, D. W. 1993. The Zamiaceae in Panama with comments on phytogeography and species relationships. Brittonia 45: 1– 16. Tang, W. 1987. Insect pollination in the cycad Zamia pumila (Zamiaceae). Amer. J. Bot. 74: 90– 99. ———. 2004. Cycad insects and pollination. Pp. 383– 394 in P. C. Srivastava (ed.), Vistas in Palaeobotany and Plant Morphology: Evolutionary and Environmental Perspectives, Professor D. D. Pant Memorial Volume. U. P. Off set, Lucknow, India. Terry, I., G. Walter, C. Moore, R. Roemer & C. Hull. 2007. Odor- mediated push- pull pollination in cycads. Science 318(5847): 70. Van Bael, S., P. Bichier, I. Ochoa & R. Greenberg. 2007. Bird diversity in cacao farms and forest fragments of western Panama. Biodivers. & Conservation 16: 2245– 2256. Vovides, A. 1991. Insect symbionts of some Mexican cycads in their natural habitat. Biotropica 23:102– 104. Zherikhen, V. V. & V. G. Gratshev. 1995. A comparative study of the hind wing venation of the superfamily Curculionoidea with phyloge ne tic implications. Pp. 634– 777 in J. Pakaluk & S. A. Slipinski (eds.), Biology, Phylogeny, and Classifi cation of Coleoptera. Papers Celebrating the 80th Birthday of Roy A. Crowson. Vol. 2. Muzeum i Instytut Zoologii PAN, Warsaw, Poland. —-1 —0 —+1 529-50504_ch02_2P.indd 351 7/26/12 5:52 PM Reproductive Biology Chapter 24 An Overview of Cycad Pollination Studies Irene Terry, William Tang, Alberto S. Taylor Blake, John S. Donaldson, Rita Singh, Andrew P. Vovides, and Angélica Cibrián Jaramillo Abstract • 353 Resumen • 353 Introduction • 353 Results and Discussion • 357 Cycad Cone Traits • 357 Cone Insects of Cycas in Southeast Asia, India, and Guam • 358 India • 359 Guam • 360 Pollination of Australian Cycads • 363 Pollination of African Cycads • 366 Pollination of American Cycads • 368 Baiting Cycad Pollinators on the Isthmus of Panama • 369 Idioblasts and Cycad Cones • 375 Population- genetic Techniques in the Study of Cycad Pollination • 381 Conclusions • 384 Ac know ledg ments • 386 Literature Cited • 386 -1— 0— +1— 529-50504_ch02_2P.indd 352 7/26/12 5:52 PM Irene Terry et al. 353 Abstract Interest in cycad pollination biology has steadily increased since the 1980s, when the fi rst defi nitive studies demonstrated that specialist insects were the pollen vectors of their cycad host. In this review several aspects of cycad pollination are discussed briefl y, in- cluding the known and putative insect pollinators of cycads from diff erent regions, sam- pling techniques to determine putative pollinator- adult habitats during coning or nonconing season, experiments on cones excluding/including insects or wind to deter- mine their roles in pollination, cone thermogenesis and volatile emission studies, and behavioral studies of insect pollinators. In addition, understudied areas and new research questions and techniques are identifi ed. Resumen El interés en la biología de la polinización de cícadas ha aumentado constantemente desde la década de 1980, cuando los primeros estudios defi nitivos demostraron que in- sectos especialistas eran los vectores de polen de sus hospederos de cícadas. En esta re- visión se discuten brevemente varios aspectos de la polinización de cícadas, con la inclusión de polinizadores de cícadas conocidos y putativos de diferentes regiones, técni- cas de muestreo para determinar polinizadores adultos putativos en hábitats durante la época de formación o no de conos de polinización , experimentos sobre conos que ex- cluyen/incluyen insectos o viento para determinar su papels en la polinización, estudios de la termogénesis y emisiones volátiles del cono, y estudios del comportamiento de los insectos polinizadores. Además, se identifi can áreas poco estudiadas y preguntas nove- dosas sobre investigación y técnica. Introduction Reports of insect associations with cycad cones began as early as 1772 with Carl Thun- berg’s discovery of a long-snouted weevil infesting seeds of a South African cycad (see Oberprieler, 1989). During the early 20th century there were several more accounts from diff erent regions reporting that cycads have beetles closely associated with their cones —-1 (see reviews by Stevenson et al., 1998; Tang, 2004). Pronouncements by Chamberlain —0 —+1 529-50504_ch02_2P.indd 353 7/26/12 5:52 PM 354 Mem. New York Bot. Gard., Vol. 106 Figure 24- 1. A. Receptive ovulate cone of Dioon sp. showing tightly overlapping sporophylls except at the base of the cone, where beetles gain entry. B. Part of a cross section of ovulate cone showing a pollen droplet at tip of micropyle. (1935), a leading authority on gymnosperm biology, that these fi ndings had little to do with cycad pollination, as “gymnosperms” are wind- pollinated, probably suppressed study of this topic for many decades. During the 1980s and early 1990s several studies laid the foundation for a reassessment of cycad pollination, a pro cess that is currently ongoing. The closed nature of the ovulate cones (Fig. 24- 1A) of most cycads, except possibly in the family Cycadaceae, suggested that wind- blown pollen cannot penetrate through the small gaps between sporophylls and reach the inwardly facing micropylar tip, where a pollen droplet is released. Wind- tunnel studies with cones of Dioon edule Lindl., Zamia furfuracea L.f, Z. integrifolia L.f., and Cycas rumphii Miq. (Niklas & Norstog, 1984) confi rmed that wind alone was ineff ec tive as a pollen vector for cycads. The pro- duction of heat and odors was shown to be widespread in cycad cones (Tang, 1987a; Pellmyr et al., 1991), suggesting that cycad pollination systems have similar traits as those used by insect-pollinated fl owering plants. Wind and insect exclusion experiments on ovulate cones and detailed observations of the life cycle and behavior of the cone beetles in two Zamia species (Norstog et al., 1986, 1992; Tang, 1987b; Norstog & Fawcett, -1— 1989) demonstrated the primary role of specialist insects as pollen vectors. These and 0— later studies demonstrated that some of the pollination interactions entail intricate be- +1— 529-50504_ch02_2P.indd 354 7/26/12 5:52 PM Irene Terry et al. 355 haviors between the cones and their insect inhabitants, with partic ular cone thermo- genic and volatile cues eliciting specifi c responses in the insects, i.e., movement between pollen and ovulate cones (e.g., Norstog & Fawcett, 1989; Donaldson, 1997; Terry et al., 2007). How these cone characters and cone cues may choreograph pollinator activity is an important focus of current research. Surveys of cycads in Australia (Forster et al., 1994), Africa (Oberprieler, 1995a), Asia (Tang et al., 1999), North and South America (Vovides, 1991a; Tang & O’Brien, 2012) have revealed the widespread presence of certain insect groups in cycad cones as well as more specialized insects that are restricted to cycads on certain landmasses. The most common insects are beetles (Coleoptera)— mainly Curculionoidea and Erotylidae beetles. Erotylidae beetles have been found on cycad cones from all of these continents; however, the erotylid genera on cycads of three of the major regions outlined above are not closely related and appear to have colonized cycad cones in de pen dently (Leschen, 2003; Oberprieler, 2004). Weevils (Curculionoidea), again in diverse lineages, appear to have colonized cycad cones in de pen dently in Africa, Asia, Australia, and Central Amer- ica (Oberprieler, 2004). Boganiidae is another beetle family that has members that are specialists inhabiting cycad cones and these insects are found on cycads in Africa and western Australia. Members of the genus Cycadothrips of the insect order Thysanoptera are sole pollinators of some species of Macrozamia cycads found in Australia. A summary of the important cycad- cone insects and their hosts is displayed in Table 24- 1. In the following we present an overview of pollination studies of cycads based on individual pre sen ta tions during a pollinator workshop at the Eighth International Cycad Conference in January 2008. These summaries focus on par tic u lar aspects of pollination biology whereas more comprehensive examinations of cycad cone insects and their cy- cad associations and interactions can be found in one of several reviews (Norstog et al., 1995; Oberprieler, 1995a, 1995b, 2004; Norstog & Nicholls, 1997; Stevenson et al., 1998; Tang, 2004). The following presen ta tion summarizes what is known about polli- nators of cycads in the major geographic regions and then discusses more specifi c topics of cone thermogenesis and volatile emissions, idioblast chemistry and structure of sporo- phyll tissue, manipulation of pollen cones as baits for sampling insects to determine their presence in natural habitats, and the use of population ge ne tics to analyze wind versus insect pollination. We highlight perplexing questions concerning pollinator-cycad in- —-1 teractions that require focused investigation of various cone chemical and physical traits —0 —+1 529-50504_ch02_2P.indd 355 7/26/12 5:52 PM +1— -1— 0— 529-50504_ch02_2P.indd 356 Table 24- 1 Beetle and thrips genera found on cycad cones in various regions of the world, that are likely candidates as pollinatorsa. Geographic Beetles Other
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