Reconstructing the origin and elaboration of insect-trapping inflorescences in the araceae

American Journal of Botany

Volumn 99, Issue 10, 2012, Pages 1666-1679

  Bröderbauer, David ^a   Diaz, Anita ^b   Weber, Anton ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b BOURNEMOUTH UNIVERSITY   (United Kingdom)

Author keywords

Araceae; Character evolution; Deception; Epicuticular wax; Flies; Floral traits; Insect attachment; Morphology; Pollination; Trap

Indexed keywords

DICOTYLEDON; EVOLUTIONARY BIOLOGY; FLORAL TRAIT; FLY; MORPHOLOGY; PHYLOGENETICS; RECONSTRUCTION; TRAPPING;

ANIMAL; ARACEAE; ARTICLE; CYTOLOGY; EVOLUTION; HISTOLOGY; INFLORESCENCE; INSECT; PHYLOGENY; PHYSIOLOGY; PLANT EPIDERMIS; POLLINATION;

ANIMALS; ARACEAE; BIOLOGICAL EVOLUTION; INFLORESCENCE; INSECTS; PHYLOGENY; PLANT EPIDERMIS; POLLINATION;

EID: 84867619360     PISSN: 00029122     EISSN: None     Source Type: Journal    
DOI: 10.3732/ajb.1200274     Document Type: Article

References (97)

1. AKAIKE, H. 1974. A new look at the statistical model identifi cation. IEEE Transactions on Automatic Control 19: 716-723.
2. ALCANTARA, S., AND L. G. LOHMANN. 2010. Evolution of floral morphology and pollination system in Bignonieae (Bignoniaceae). American Journal of Botany 97: 782-796.
3. ARMSTRONG, J. A. 1979. Biotic pollination mechanisms in the Australian fl ora-A review. New Zealand Journal of Botany 17: 467-508.
4. BARTHLOTT, W., C. NEINHUIS, D. CUTLER, F. DITSCH, I. MEUSEL, I. THEISEN, AND H. WILHELMI. 1998. Classifi cation and terminology of plant epicuticular waxes. Botanical Journal of the Linnean Society 126: 237-260.
5. BARTHLOTT, W., AND E. WOLLENWEBER. 1981. Zur Feinstruktur, Chemie und taxonomischen Signifi kanz epicuticularer Wachse und ähnlicher Sekrete. Tropische und subtropische Pfl anzenwelt 32: 7-67.
6. BERMADINGER-STABENTHEINER, E., AND A. STABENTHEINER. 1995. Dynamics of thermogenesis and structure of epidermal tissues in infl orescences of Arum maculatum. New Phytologist 131: 41-50.
7. BERNHARDT, P. 2000. Convergent evolution and adaptive radiation of beetlepollinated angiosperms. Plant Systematics and Evolution 222: 293-320.
8. BOLIN, J. F., E. MAASS, AND L. J. MUSSELMAN. 2009. Pollination biology of Hydnora africana Thunb. (Hydnoraceae) in Namibia: Brood-site mimicry with insect imprisonment. International Journal of Plant Sciences 170: 157-163.
9. BOLLBACK, J. P. 2006. SIMMAP: Stochastic character mapping of discrete traits on phylogenies. BMC Bioinformatics 7: 88.
10. BOWN, D. 2000. Aroids: Plants of the Arum family, 2nd ed. Timber Press, Portland, Oregon, USA.
11. BOYCE, P. C., AND T. B. CROAT. 2012 [onward, continuously updated]. The Überlist of Araceae. Website http://www.aroid.org/genera/ [accessed 09 May 2012].
12. BOYCE, P. C., AND S. Y. WONG. 2007. Studies on Schismatoglottideae (Araceae) of Borneo IV: Preliminary observations of spathe senescence mechanics in Schismatoglottis Zoll. & Moritzi, in Sarawak, Malaysian Borneo. Aroideana 30: 56-70.
13. CHARTIER, M. 2011. Evolution des interactions plantes-pollinisateurs chez les Aracées: Contraintes phylogénétiques et écologiques. Ph.D. dissertation, Université de Toulouse, Toulouse, France.
14. CLAßEN-BOCKHOFF, R., T. SPECK, E. T WERASER, P. W ESTER, S. THIMM, AND M. REITH. 2004. The staminal lever mechanism in Salvia L. (Lamiaceae): A key innovation for adaptive radiation? Organisms, Diversity & Evolution 4: 189-205.
15. CLEGHORN, M. L. 1913. Notes on the pollination of Colocasia antiquorum. Journal of the Proceedings of the Asiatic Society of Bengal 9: 313-315.
16. COOMBS, G., A. P. DOLD, AND C. I. PETER. 2011. Generalized fl y-pollination in Ceropegia ampliata (Apocynaceae-Asclepiadoideae): The role of trapping hairs in pollen export and receipt. Plant Systematics and Evolution 296: 137-148.
17. CRISP, M. D., AND L. G. COOK. 2005. Do early branching lineages signify ancestral traits? Trends in Ecology & Evolution 20: 122-128.
18. CUSIMANO, N., M. D. BARRETT, W. L. A. HETTERSCHEID, AND S. S. RENNER. 2010. A phylogeny of the Areae (Araceae) implies that Typhonium, Sauromatum, and the Australian species of Typhonium are distinct clades. Taxon 59: 439-447.
19. CUSIMANO, N., J. BOGNER, S. J. MAYO, P. C. BOYCE, S. Y. WONG, M. HESSE, W. L. A. HETTERSCHEID, ET AL. 2011. Relationships within the Araceae: Comparison of morphological patterns with molecular phylogenies. American Journal of Botany 98: 654-668.
20. CUSIMANO, N., L. B. ZHANG, AND S. S. RENNER. 2008. Reevaluation of the cox1 group I intron in Araceae and angiosperms indicates a history dominated by loss rather than horizontal transfer. Molecular Biology and Evolution 25: 265-276.
21. DAFNI, A. 1984. Mimicry and deception in pollination. Annual Review of Ecology and Systematics 15: 259-278.
22. DAKWALE, S., AND S. BHATNAGAR. 1982. Sauromatum guttatum (Schott)-A fl y catcher and sampler Aroid. Current Science 51: 1076-1077.
23. DAKWALE, S., AND S. BHATNAGAR. 1985. Insect-trapping behaviour and diel periodicity in Sauromatum guttatum Schott (Araceae). Current Science 54: 699-702.
24. DEWITT SMITH, S. 2010. Using phylogenetics to detect pollinator-mediated floral evolution. New Phytologist 188: 354-363.
25. DIAZ, A., AND G. C. KITE. 2002. A comparison of the pollination ecology of Arum maculatum and A. italicum in England. Watsonia 24: 171-181.
26. DIAZ, A., AND G. C. KITE. 2006. Why be a rewarding trap? The evolution of floral rewards in Arum (Araceae), a genus characterized by saprophilous pollination systems. Biological Journal of the Linnean Society 88: 257-268.
27. EIGENBRODE, S. D. 2004. The effects of plant epicuticular waxy blooms on attachment and effectiveness of predatory insects. Arthropod Structure & Development 33: 91-102.
28. ENDRESS, P. K. 2011. Evolutionary diversifi cation of the fl owers in angiosperms. American Journal of Botany 98: 370-396.
29. FAEGRI, K., AND L. VAN DER PIJL. 1971. The principles of pollination ecology, 2nd ed. Pergamon Press, Oxford, UK.
30. FENSTER, C. B., W. S. ARMBRUSTER, P. WILSON, M. R. DUDASH, AND J. D. THOMSON. 2004. Pollination syndromes and floral specialization. Annual Review of Ecology, Evolution and Systematics 35: 375-403.
31. FRIIS, E. M., K. R. P EDERSEN, AND P. R. C RANE. 2006. Cretaceous angiosperm fl owers: Innovation and evolution in plant reproduction. Palaeogeography, Palaeoclimatology, Palaeoecology 232: 251-293.
32. GARCÍA, M. T. A., B. G. GALATI, AND P. S. HOC. 2007. Ultrastructure of the corona of scented and scentless fl owers of Passifl ora spp. (Passifl oraceae). Flora 202: 302-315.
33. GAUME, L., P. PERRET, E. GORB, S. GORB, J. J. LABAT, AND N. ROWE. 2004. How do plant waxes cause fl ies to slide? Experimental tests of wax-based trapping mechanisms in three pitfall carnivorous plants. Arthropod Structure & Development 33: 103-111.
34. GIBERNAU, M. 2003. Pollinators and visitors of aroid infl orescences. Aroideana 26: 66-83.
35. GIBERNAU, M. 2011. Pollinators and visitors of aroid infl orescences: An addendum. Aroideana 34: 70-83.
36. GIBERNAU, M., D. BARABE, P. CERDAN, AND A. DEJEAN. 1999. Beetle pollination of Philodendron solimoesense (Araceae) in French Guiana. International Journal of Plant Sciences 160: 1135-1143.
37. GIBERNAU, M., D. BARABE, AND D. LABAT. 2000. Flowering and pollination of Philodendron melinonii (Araceae) in French Guiana. Plant Biology 2: 331-334.
38. GIBERNAU, M., M. C HARTIER, AND D. B ARABE. 2 010. Recent advances towards an evolutionary comprehension of Araceae pollination. In O. Seberg, G. Petersen, A. S. Barford, and J. Davis [eds.], Diversity, phylogeny, and evolution in the monocotyledons: Proceedings of the Fourth International Conference on the Comparative Biology of the Monocotyledons, 101-114. Aarhus University Press, Aarhus, Denmark.
39. GIBERNAU, M., D. MACQUART, AND G. PRZETAK. 2004. Pollination in the genus Arum-A review. Aroideana 27: 148-166.
40. GRAYUM, M. H. 1990. Evolution and phylogeny of the Araceae. A nnals of the Missouri Botanical Garden 77: 628-697.
41. HADACEK, F., AND M. WEBER. 2002. Club-shaped organs as additional osmophores within the Sauromatum infl orescence: Odour analysis, ultrastructural changes and pollination aspects. Plant Biology 4: 367-383.
42. HARRIS, E. M. 1999. Capitula in the Asteridae: A widespread and varied phenomenon. Botanical Review 65: 348-369.
43. HUELSENBECK, J. P., AND F. RONQUIST. 2001. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754-755.
44. IVANCIC, A., V. LEBOT, O. ROUPSARD, J. Q. GARCIA, AND T. OKPUL. 2004. Thermogenic fl owering of taro (Colocasia esculenta, Araceae). Canadian Journal of Botany 82: 1557-1565.
45. KITE, G. C., W. L. A. HETTERSCHEID, M. J. LEWIS, P. C. BOYCE, J. OLLERTON, E. COCKLIN, A. DIAZ, AND M. S. J. SIMMONDS. 1998. Infl orescence odours and pollinators of Arum and Amorphophallus (Araceae). In S. J. Owens and P. J. Ruddall [eds.], Reproductive biology, 295-315. Royal Botanic Gardens, Kew, UK.
46. KNOLL, F. 1926. Die Arum-Blütenstände und ihre Besucher (Insekten und Blumen IV). Abhandlungen der Zoologisch-Botanischen Gesellschaft in Wien 12: 381-481.
47. KOCH, K., B. BHUSHAN, AND W. BARTHLOTT. 2008. Diversity of structure, morphology and wetting of plant surfaces. Soft Matter 4: 1943-1963.
48. KOHN, J. R., S. W. GRAHAM, B. MORTON, J. J. DOYLE, AND S. C. H. BARRETT. 1997. Reconstruction of the evolution of reproductive characters in Pontederiaceae using phylogenetic evidence from chloroplast DNA restriction-site variation. Evolution 50: 1454-1469.
49. KRAEMER, M., AND U. SCHMITT. 1999. Possible pollination by hummingbirds in Anthurium sanguineum Engl. (Araceae). Plant Systematics and Evolution 217: 333-335.
50. LACK, A. J., AND A. DIAZ. 1991. The pollination of Arum maculatum L.-A historical review and new observations. Watsonia 18: 333-342.
51. LINZ, J., J. STÖKL, I. URRU, T. KRÜGEL, M. C. STENSMYR, AND B. S. HANSSON. 2010. Molecular phylogeny of the genus Arum (Araceae) inferred from multi-locus sequence data and AFLPs. Taxon 59: 405-415.
52. MADDISON, D. R., AND W. P. MADDISON. 2000. MacClade 4: Analysis of phylogeny and character evolution, version 4.0. Sinauer, Sunderland, Massachusetts, USA.
53. MADDISON, W. P., AND D. R. MADDISON. 2007. Mesquite: A modular system for evolutionary analysis, version 2.0, website: http://mesquiteproject. org [accessed 01 March 2011].
54. MAIA, A. C. D., AND C. SCHLINDWEIN. 2006. Caladium bicolor (Araceae) and Cyclocephala celata (Coleoptera, Dynastinae): A well-established pollination system in the northern Atlantic rainforest of Pernambuco, Brazil. Plant Biology 8: 529-534.
55. MANSION, G., G. ROSENBAUM, N. SCHOENENBERGER, G. BACCHETTA, J. A. ROSSELLO, AND E. CONTI. 2008. Phylogenetic analysis informed by geological history supports multiple, sequential invasions of the Mediterranean Basin by the angiosperm family Araceae. Systematic Biology 57: 269-285.
56. MAYO, S. J., J. BOGNER, AND P. C. BOYCE. 1997. The genera of Araceae. The Trustees, Royal Botanic Gardens, Kew, U.K.
57. MEEUSE, B. J. D., AND M. H. HATCH. 1960. Beetle pollination in Dracunculus and Sauromatum (Araceae). Coleopterists Bulletin 14: 70-74.
58. MILLER, M. A., W. PFEIFFER, AND T. SCHWARTZ. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop (GCE 2010), 1-8, New Orleans, Louisiana, USA.
59. MIYAKE, T., AND M. YAFUSO. 2003. Floral scents affect reproductive success in fl y-pollinated Alocasia odora (Araceae). American Journal of Botany 90: 370-376.
60. MIYAKE, T., AND M. YAFUSO. 2005. Pollination of Alocasia cucullata (Araceae) by two Colocasiomyia fl ies known to be specifi c pollinators for Alocasia odora. Plant Species Biology 20: 201-208.
61. NAUHEIMER, L., P. C. BOYCE, AND S. S. RENNER. 2012. Giant taro and its relatives: A phylogeny of the large genus Alocasia (Araceae) sheds light on Miocene fl oristic exchange in the Malesian region. Molecular Phylogenetics and Evolution 63: 43-51.
62. OMLAND, K. E. 1999. The assumptions and challenges of ancestral state reconstructions. Systematic Biology 48: 604-611.
63. ORGAARD, M., AND N. JACOBSEN. 1998. SEM study of surface structures of the spathe in Cryptocoryne and Lagenandra (Araceae: Ariodeae: Cryptocoryneae). Botanical Journal of the Linnean Society 126: 261-289.
64. PŁACHNO, B. J., P. SWIATEK, AND G. SZYMCZAK. 2010. Can a stench be beautiful? Osmophores in stem-succulent stapeliads (Apocynaceae-Asclepiadoideae-Ceropegieae-Stapeliinae). Flora 205: 101-105.
65. POPPINGA, S., K. KOCH, H. F. BOHN, AND W. BARTHLOTT. 2010. Comparative and functional morphology of hierarchically structured anti-adhesive surfaces in carnivorous plants and kettle trap fl owers. Functional Plant Biology 37: 952-961.
66. POSADA, D. 2008. jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution 25: 1253-1256.
67. PROCTOR, M., P. YEO, AND A. LACK. 1996. The natural history of pollination. Timber Press, Portland, Oregon, USA.
68. QUEK, S. P., S. J. DAVIES, T. ITINO, AND N. E. PIERCE. 2004. Codiversifi cation in an ant-plant mutualism: Stem texture and the evolution of host use in Crematogaster (Formicidae: Myrmicinae) inhabitants of Macaranga (Euphorbiaceae). Evolution; International Journal of Organic Evolution 58: 554-570.
69. RENNER, S. S., AND L. B. ZHANG. 2004. Biogeography of the Pistia clade (Araceae): Based on chloroplast and mitochondrial DNA sequences and Bayesian divergence time inference. Systematic Biology 53: 422-432.
70. RONQUIST, F., AND J. P. HUELSENBECK. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
71. RUDALL, P. J., AND R. M. BATEMAN. 2002. Roles of synorganisation, zygomorphy and heterotopy in floral evolution: The gynostemium and labellum of orchids and other lilioid monocots. Biological Reviews of the Cambridge Philosophical Society 77: 403-441.
72. SAKAI, S. 2002. Aristolochia spp. (Aristolochiaceae) pollinated by fl ies breeding on decomposing fl owers in Panama. American Journal of Botany 89: 527-534.
73. SCHIESTL, F. P., AND S. DÖTTERL. 2012. The evolution of floral scent and olfactory preferences in pollinators: Coevolution or pre-existing bias? Evolution 66: 2042-2055.
74. SCHMUCKER, T. 1930. Blütenbiologische und-morphologische Beobachtungen. Planta 9: 718-747.
75. SCHULTZ, T. R., AND G. A. CHURCHILL. 1999. The role of subjectivity in reconstructing ancestral character states: A Bayesian approach to unknown rates, states, and transformation asymmetries. Systematic Biology 48: 651-664.
76. SHUTTLEWORTH, A., AND S. D. JOHNSON. 2010. The missing stink: Sulfur compounds can mediate a shift between fl y and wasp pollination systems. Proceedings of the Royal Society, B, Biological Sciences 2 77: 2811-2819.
77. SMITH, S. A., AND M. J. DONOGHUE. 2008. Rates of molecular evolution are linked to life history in fl owering plants. Science 322: 86-89.
78. STAMATAKIS, A., P. HOOVER, AND J. ROUGEMONT. 2008. A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57: 758-771.
79. STEBBINS, G. L. 1970. Adaptive radiation of reproductive characteristics in angiosperms. I: Pollination mechanisms. Annual Review of Ecology and Systematics 1: 307-326.
80. STÖKL, J., A. STRUTZ, A. DAFNI, A. SVATOS, J. DOUBSKY, M. KNADEN, S. SACHSE, ET AL. 2010. A deceptive pollination system targeting drosophilids through olfactory mimicry of yeast. Current Biology 20: 1846-1852.
81. STPICZYŃSKA, M. 2001. Osmophores of the fragrant orchid Gymnadenia conopsea L. (Orchidaceae). Acta Societatis Botanicorum Poloniae 70: 91-96.
82. TAKENAKA, K., J. T. YIN, S. Y. WEN, AND M. J. TODA. 2006. Pollination mutualism between a new species of the genus Colocasiomyia de Meijere (Diptera: Drosophilidae) and Steudnera colocasiifolia (Araceae) in Yunnan, China. Entomological Science 9: 79-91.
83. THIEN, L. B., P. BERNHARDT, M. S. DEVALL, Z. D. CHEN, Y. B. LUO, J. H. FAN, L. C. YUAN, ET AL. 2009. Pollination of basal angiosperms (ANITA grade). American Journal of Botany 96: 166-182.
84. TODA, M. J., AND M. B. LAKIM. 2011. Genus Colocasiomyia (Drosophilidae: Diptera) in Sabah, Bornean Malaysia: High species diversity and use of host aroid infl orescences. Entomological Science 14: 262-270.
85. TODA, M. J., AND T. OKADA. 1983. Ecological studies of fl oricolous Drosophiella in Burma with descriptions of 3 new species from Burma and the Philippines (Diptera, Drosophilidae). Kontyu 51: 169-184.
86. URRU, I., M. C. STENSMYR, AND B. S. HANSSON. 2011. Pollination by broodsite deception. Phytochemistry 72: 1655-1666.
87. VOGEL, S. 1961. Die Bestäubung der Kesselfallen-Blüten von Ceropegia. Beiträge zur Biologie der Pfl anzen 36: 159-237.
88. VOGEL, S. 1963. Duftdrüsen im Dienste der Bestäubung. Über Bau und Funktion der Osmophoren. Abhandlungen der Akademie der Wissenschaften und der Literatur 10: 601-763.
89. VOGEL, S. 1965. Kesselfallen-Blumen. Die Umschau in Wissenschaft und Technik 1: 12-17.
90. VOGEL, S. 1978. Pilzmückenblumen als Pilzmimeten. Flora 167: 329-366.
91. VOGEL, S. 1999. Die Funktionstypen der Kesselfallen-Blumen. 9. Jahrestagung der Gesellschaft für Tropenökologie, Ulm, Germany, 17-20 March 1999 [abstract].
92. VOGEL, S., AND J. MARTENS. 2000. A survey of the function of the lethal kettle traps of Arisaema (Araceae), with records of pollinating fungus gnats from Nepal. Botanical Journal of the Linnean Society 133: 61-100.
93. WHITTALL, J. B., AND S. A. HODGES. 2007. Pollinator shifts drive increasingly long nectar spurs in columbine fl owers. Nature 447: 706-712.
94. WILLMER, P. 2011. Pollination and floral ecology. Princeton University Press, Princeton, New Jersey, USA.
95. YADAV, S. R. 1998. Adaptive signifi cance of phenology and spadix architecture in Araceae of western Ghats of India. Acta Botanica Yunnanica 20: 31-40.
96. YOUNG, H. J. 1986. Beetle pollination of Dieffenbachia longispatha (Araceae). American Journal of Botany 73: 931-944.
97. ZHU, G. H., AND T. B. CROAT. 2004. Revision of Dracontium (Araceae). Annals of the Missouri Botanical Garden 91: 593-667.