Pollination ecology of the invasive tree tobacco Nicotiana glauca: comparisons across native and non-native ranges
DOI:
https://doi.org/10.26786/1920-7603(2012)12Abstract
Interactions with pollinators are thought to play a significant role in determining whether plant species become invasive, and ecologically generalised species are predicted to be more likely to invade than more specialised species. Using published and unpublished data we assessed the floral biology and pollination ecology of the South American native Nicotiana glauca (Solanaceae) which has become a significant invasive of semi-arid parts of the world. In regions where specialised bird pollinators are available, for example hummingbirds in California and sunbirds in South Africa and Israel, N. glauca interacts with these local pollinators and sets seed by both out-crossing and selfing. In areas where there are no such birds, such as the Canary Islands and Greece, abundant viable seed is set by selfing, facilitated by the shorter stigma-anther distance compared to plants in native populations. Surprisingly, in these areas without pollinating birds, the considerable nectar resources are only rarely exploited by other flower visitors such as bees or butterflies, either legitimately or by nectar robbing. We conclude that Nicotiana glauca is a successful invasive species outside of its native range, despite its functionally specialised hummingbird pollination system, because it has evolved to become more frequently self pollinating in areas where it is introduced. Its invasion success is not predictable from what is known of its interactions with pollinators in its home range.
References
Aigner PA (2004) Ecological and genetic effects on demographic processes: pollination, clonality and seed production in Dithyrea maritima. Biological Conservation 116: 27-34. DOI: https://doi.org/10.1016/S0006-3207(03)00170-8
Aizen MA, Morales CL, Morales JM (2008) Invasive mutualists erode native pollination webs. PLOS Biology 6: 396-403. DOI: https://doi.org/10.1371/journal.pbio.0060031
Alarcón R, Waser NM, Ollerton J (2008) Year-to-year variation in the topology of a plant-pollinator interaction network. Oikos 117: 1796-1807. DOI: https://doi.org/10.1111/j.0030-1299.2008.16987.x
Armbruster, WS (1988) Multilevel comparative analysis of the morphology, function, and evolution of Dalechampia blossoms. Ecology 69:1746–1761. DOI: https://doi.org/10.2307/1941153
Baker, HG (1974) The evolution of weeds. Annual Review of Ecology and Systematics 5: 1-24. DOI: https://doi.org/10.1146/annurev.es.05.110174.000245
Bartomeus I, Vila M, Santamaria L (2008) Contrasting effects of invasive plants in plant-pollinator networks. Oecologia 155: 761-770. DOI: https://doi.org/10.1007/s00442-007-0946-1
Bjerknes A-L, Totland Ø, Hegland SJ, Nielsen A (2007) Do alien plant invasions really affect pollination success in native plant species? Biological Conservation 138: 1-12. DOI: https://doi.org/10.1016/j.biocon.2007.04.015
Bogdanović S, Mitić B, Rušćić M, Dolina K (2006) Nicotiana glauca Graham (Solanaceae), a new invasive plant in Croatia. Acta Botanica Croatica 65:203-209.
Bornmuller J (1898) Ein Beitrag zur Kenntnis der Flora von Syrien und Palastina. Verhandlungen der Zoologisch-Botanischen Gesellschaft in Wien 48: 544–653.
Bramwell D (1982) Conserving biodiversity in the Canary Islands. Annals of the Missouri Botanical Gardens 77: 28-37. DOI: https://doi.org/10.2307/2399622
Cariveau DP, Norton AP (2009) Spatially contingent interactions between an exotic and native plant mediated through flower visitors. Oikos 118:107-114. DOI: https://doi.org/10.1111/j.1600-0706.2008.16705.x
Chittka L, Schürkens S (2001) Successful invasion of a floral market. Nature 411:653-653. DOI: https://doi.org/10.1038/35079676
Clement P (1995) The chiffchaff. Hamlyn, London.
Corbet SA (2006) A typology of pollination systems: implications for crop management and the conservation of wild plants. In: Waser NM, Ollerton J (eds.) Plant-pollinator interactions: from specialization to generalization, University of Chicago Press, Chicago.
Cohen N (2007) The effects of alkaloids in the floral nectar on the relationships between Nicotiana glauca and ants. M.Sc. Thesis. University of Haifa, Israel.
Dafni A, Kevan PG, Husband BC (2005) Practical pollination biology. Enviroquest, Cambridge, Ontario.
Dietzsch AC, Stanley DA, Stout JC (2011) Relative abundance of an invasive alien plant affects native pollination processes. Oecologia 167:469-479. DOI: https://doi.org/10.1007/s00442-011-1987-z
Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JT (2004) Pollination syndromes and floral specialization. Annual Review of Ecology, Evolution and Systematics 35:375-403. DOI: https://doi.org/10.1146/annurev.ecolsys.34.011802.132347
Fishbein M, Venable DL (1996) Diversity and temporal change in the effective pollinators of Asclepias tuberosa. Ecology 77: 1061-1073. DOI: https://doi.org/10.2307/2265576
Florentine SK, Westbrooke ME (2005) Invasion of the noxious weed Nicotiana glauca R. Graham after an episodic flooding event in the arid zone of Australia. Journal of Arid Environments 60: 531-545. DOI: https://doi.org/10.1016/j.jaridenv.2004.07.015
Florentine SK, Westbrooke ME, Gosney K, Ambrose G, O'Keefe M (2006) The arid land invasive weed Nicotiana glauca R. Graham (Solanaceae): Population and soil seed bank dynamics, seed germination patterns and seedling response to flood and drought. Journal of Arid Environments 66: 218-230. DOI: https://doi.org/10.1016/j.jaridenv.2005.10.017
Forster PI (1994) Diurnal insects associated with the flowers of Gomphocarpus physocarpus E Mey (Asclepiadaceae), an introduced weed in Australia. Biotropica 26: 214-217. DOI: https://doi.org/10.2307/2388811
Galetto L, Bernardello L (1993a) Nectar sugar composition in angiosperms from Chaco and Patagonia (Argentina): an animal visitor’s matter? Plant Systematics and Evolution 238: 69–86. DOI: https://doi.org/10.1007/s00606-002-0269-y
Galetto L, Bernardello L (1993b) Nectar secretion pattern and removal effects in 3 species of Solanaceae Canadian Journal of Botany 71: 1394-1398. DOI: https://doi.org/10.1139/b93-167
Geerts S, Pauw A (2009) African sunbirds hover to pollinate an invasive, hummingbird-pollinated plant. Oikos 118: 573-579. DOI: https://doi.org/10.1111/j.1600-0706.2009.17167.x
Harmon-Threatt AN, Burns JH, Shemyakina LA, Knight TM (2009) Breeding system and pollination ecology of introduced plants compared to their native relatives. American Journal of Botany 96: 1544–1550. DOI: https://doi.org/10.3732/ajb.0800369
Henderson L (1991) Invasive alien woody plants of the Northern Cape. Bothalia 21: 177-189. DOI: https://doi.org/10.4102/abc.v21i2.885
Hernández HM (1981) Sobre la biología reproductiva de Nicotiana glauca Graham: una maleza de distribución cosmopolita. Boletin de la Sociedad de Botánica de México 41: 47-73. DOI: https://doi.org/10.17129/botsci.1248
Herrera CM (1988) Variation in mutualisms - the spatio-temporal mosaic of a pollinator assemblage. Biological Journal of the Linnean Society 35:95-125. DOI: https://doi.org/10.1111/j.1095-8312.1988.tb00461.x
Hobbs JN (1961) The birds of Southwest New South Wales. Emu 61: 21-55. DOI: https://doi.org/10.1071/MU961021
Janecek S, Patacova E, Bartos M, Padysakova E, Spitzer L, Tropek R (2011) Hovering sunbirds in the Old World: occasional behaviour or evolutionary trend? Oikos 120: 178-183. DOI: https://doi.org/10.1111/j.1600-0706.2010.18612.x
Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colorado, Niwot.
Knuth P (1898-1905) Handbuch der Blütenbiologie. Engelmann, Leipzig.
Koptur SA (2006) The conservation of specialized and generalized pollination systems in subtropical ecosystems: a case study. In: Waser NM, Ollerton J (eds.) Plant-pollinator interactions: from specialization to generalization, University of Chicago Press, Chicago.
Kunkel G (1976) Notes on the introduced elements in the Canary Islands’ flora. In: Kunkel G (ed) Biogeography and ecology in the Canary Islands. Dr W. Junk, The Hague, pp249-266. DOI: https://doi.org/10.1007/978-94-010-1566-0_8
Lamborn E, Ollerton J (2000) Experimental assessment of the functional morphology of inflorescences of Daucus carota (Apiaceae): testing the "fly catcher effect". Functional Ecology 14:445-454. DOI: https://doi.org/10.1046/j.1365-2435.2000.00440.x
Loayza A, Rios R, Castillo C (1999) Actividad alimenticia de Patagona gigas en arbustos de Nicotiana glauca (Solanaceae). Ecología en Bolivia 33:75-79.
Lopezaraiza-Mikel ME, Hayes RB, Whalley MR, Memmott J (2007) The impact of an alien plant on a native plant-pollinator network: an experimental approach. Ecology Letters 10: 539-550. DOI: https://doi.org/10.1111/j.1461-0248.2007.01055.x
Marloth R (1901) Die Ornithophilie der Flora Süd-Afrikas. Berichte der Deutschen Botanischen Gesellschaft 19: 176-179. DOI: https://doi.org/10.1111/j.1438-8677.1901.tb04983.x
Memmott J, Waser NM (2002) Integration of alien plants into a native flower-pollinator visitation web. Proceedings of the Royal Society of London B 269: 2395-2399. DOI: https://doi.org/10.1098/rspb.2002.2174
Moraes AD, de Melo E, Agra MD, Franca F (2009) The Solanaceae family from the inselbergs of semi-arid Bahia, Brazil. Iheringia Serie Botanica 64: 109-122.
Moragues E, Traveset A (2005) Effect of Carpobrotus spp. on the pollination success of native plant species of the Balearic Islands. Biological Conservation 122: 611-619. DOI: https://doi.org/10.1016/j.biocon.2004.09.015
Morales CL, Traveset A (2009) A meta-analysis of impacts of alien vs. native plants on pollinator visitation and reproductive success of co-flowering native plants. Ecology Letters 12: 716-728. DOI: https://doi.org/10.1111/j.1461-0248.2009.01319.x
Nattero J, Cocucci AA (2007) Geographic variation in floral traits of the tree tobacco in relation to its hummingbird pollinator fauna. Biological Journal Linnean Society 90: 657-667. DOI: https://doi.org/10.1111/j.1095-8312.2007.00756.x
Nattero J, Sérsic AN, Cocucci AA (2010) Patterns of contemporary phenotypic selection and flower integration in the hummingbird-pollinated Nicotiana glauca between populations with different flower-pollinator combinations. Oikos: 119: 852-863. DOI: https://doi.org/10.1111/j.1600-0706.2009.17766.x
Nienhuis CM, Dietzsch AC, Stout JC (2009) The impacts of an invasive alien plant and its removal on native bees. Apidologie 40: 450-463. DOI: https://doi.org/10.1051/apido/2009005
Nienhuis CM, Stout JC (2009) Effectiveness of native bumblebees as pollinators of the alien invasive plant Impatiens glandulifera (Balsaminaceae) in Ireland. Journal of Pollination Ecology 1: 1-11. DOI: https://doi.org/10.26786/(2009)
Olesen JM, Eskildsen LI, Venkatasamy S (2002) Invasion of pollination networks on oceanic islands: importance of invader complexes and endemic super generalists. Diversity and Distributions 8: 181-192. DOI: https://doi.org/10.1046/j.1472-4642.2002.00148.x
Ollerton J, Killick A, Lamborn E, Watts S, Whiston M (2007) Multiple meanings and modes: on the many ways to be a generalist flower. Taxon 56: 717-728. DOI: https://doi.org/10.2307/25065855
Ollerton J, Cranmer L, Stelzer R, Sullivan S, Chittka L (2008) Bird pollination of Canary Island endemic plants. Naturwissenschaften 96: 221-232. DOI: https://doi.org/10.1007/s00114-008-0467-8
Ortega-Olivencia A, Rodríguez-Riaño T, Valtueña FJ, López J, Devesa JA (2005) First confirmation of a native bird-pollinated plant in Europe. Oikos 110:578-590. DOI: https://doi.org/10.1111/j.0030-1299.2005.13877.x
Padrón B, Traveset A, Biedenweg T, Díaz D, Nogales M, Olesen JM. (2009) Impact of alien plant invaders on pollination networks in two archipelagos. PLoS One 4: e6275. DOI: https://doi.org/10.1371/journal.pone.0006275
Richardson DM, Allsopp N, D'Antonio CM, Milton SJ, Rejmanek M (2000) Plant invasions - the role of mutualisms. Biological Reviews 75: 65-93. DOI: https://doi.org/10.1111/j.1469-185X.1999.tb00041.x
Rodger JG, van Kleunen M, Johnson SD (2010) Does specialized pollination impede plant invasions? International Journal of Plant Sciences 171: 382-391. DOI: https://doi.org/10.1086/651226
Saini MS, Ghattor HS (2007) Taxonomy and food plants of some bumble bee species of Lahaul and Spiti valley of Himachal Pradesh. Zoos' Print Journal 22: 2648-2657. DOI: https://doi.org/10.11609/JoTT.ZPJ.1434.2648-57
Schürkens S, Chittka L (2001) The significance of the invasive crucifer species Bunias orientalis (Brassicaceae) as a nectar source for central European insects. Entomologia Generalis 25: 115-120. DOI: https://doi.org/10.1127/entom.gen/25/2001/115
Schueller SK (2002) Hummingbird pollination and floral evolution of introduced Nicotiana glauca and native Epilobium canum: California island-mainland comparisons. Ph.D. dissertation, University of Michigan, Ann Arbor, Michigan, USA.
Schueller SK (2004) Self-pollination in island and mainland populations of the introduced hummingbird-pollinated plant, Nicotiana glauca (Solanaceae). American Journal of Botany 91: 672-681. DOI: https://doi.org/10.3732/ajb.91.5.672
Schueller SK (2007) Island-mainland difference in Nicotiana glauca (Solanaceae) corolla length: a product of pollinator-mediated selection? Evolutionary Ecology 21: 81-98. DOI: https://doi.org/10.1007/s10682-006-9125-9
Simberloff D (1995) Why do introduced species appear to devastate islands more than mainland areas? Pacific Science 49: 87-97.
Skead CJ (1967) The sunbirds of southern Africa. Balkema, Cape Town.
Stiles FG (1973) Food supply and the annual cycle of the Anna Hummingbird. University of California Publications in Zoology 97: 1-116.
Stiles FG (1976) On taste preferences, color preferences, and flower choice in hummingbirds. The Condor 78: 10-26. DOI: https://doi.org/10.2307/1366912
Stout JC (2007) Reproductive biology of the invasive exotic shrub, Rhododendron ponticum L. (Ericaceae). Botanical Journal of the Linnean Society 155: 373-381. DOI: https://doi.org/10.1111/j.1095-8339.2007.00719.x
Stout JC, Parnell JAN, Arroyo J, Crowe TP (2006) Pollination ecology and seed production of Rhododendron ponticum in native and exotic habitats. Biodiversity and Conservation 15:755-777. DOI: https://doi.org/10.1007/s10531-004-1065-5
Stout JC, Morales CL (2009) Ecological impacts of invasive alien species on bees. Apidologie 40: 388-409. DOI: https://doi.org/10.1051/apido/2009023
Tadmor-Melamed H (2004) The ecological role of secondary metabolites in floral nectar governing the interaction between Nicotiana glauca and Nectarinia osea. M.Sc. Thesis. The Hebrew University of Jerusalem, Israel.
Tadmor-Melamed H, Markman S, Arieli A, Distl M, Wink M, Izhaki I (2004) Limited ability of Palestine Sunbirds Nectarinia osea to cope with pyridine alkaloids in nectar of Tree Tobacco Nicotiana glauca. Functional Ecology 18:844-850. DOI: https://doi.org/10.1111/j.0269-8463.2004.00929.x
Theoharides KA, Dukes JS (2007) Plant invasion across space and time: factors affecting nonindiginous species success during four stages of invasion. New Phytologist 176: 256-273. DOI: https://doi.org/10.1111/j.1469-8137.2007.02207.x
Thompson K, Davis MA (2011) Why research on traits of invasive plants tells us very little. Trends in Ecology and Evolution 26: 155–156. DOI: https://doi.org/10.1016/j.tree.2011.01.007
Tillberg CV, Holway DA, LeBrun EG, Suarez AV (2007) Trophic ecology of invasive Argentine ants in their native and introduced ranges. Proceedings of the National Academy of Sciences USA 104: 20856–20861. DOI: https://doi.org/10.1073/pnas.0706903105
Valido A, Dupont YL, Olesen JM (2004) Bird-flower interactions in the Macaronesian islands. Journal of Biogeography 31: 1945-1953. DOI: https://doi.org/10.1111/j.1365-2699.2004.01116.x
Vilá M, Bartomeus I, Dietzsch AC, Petanidou T, Steffan-Dewenter I, Stout JC, Tscheulin T (2009) Invasive plant integration into native plant–pollinator networks across Europe. Proceedings of the Royal Society series B 276: 3887-3893. DOI: https://doi.org/10.1098/rspb.2009.1076
Vogel S, Westerkamp C, Thiel B, Gessner K (1984) Ornithophilie auf den Canarischen Inseln. Plant Systematics and Evolution 146: 225-248. DOI: https://doi.org/10.1007/BF00989548
Westerkamp C (1990) Bird-flowers - hovering versus perching exploitation. Botanica Acta 103: 366-371. DOI: https://doi.org/10.1111/j.1438-8677.1990.tb00176.x
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2012 Jeff Ollerton, Stella Watts, Shawn Connerty, Julia Lock, Leah Parker, Ian Wilson, Sheila Schueller, Julieta Nattero, Andrea A. Cocucci, Ido Izhaki, Sjirk Geerts, Anton Pauw, Jane C. Stout

This work is licensed under a Creative Commons Attribution 4.0 International License.



