Comparative floral ecology and breeding systems between sympatric populations of Nothoscordum bivalve and Allium stellatum (Amaryllidaceae)
DOI:
https://doi.org/10.26786/1920-7603(2020)585Abstract
We compared the floral biology of two sympatric populations of closely related species over two seasons. In 2018, Nothoscordum bivalve (L.) Britton bloomed from April 23 to May 7 and Allium stellatum Nutt. Ex Ker Gawl bloomed from August 28 to October 4. Erect, white flowers of N. bivalve were scented and had septal nectaries. Erect, pink-purple flowers of A. stellatum had septal nectaries, no discernible scent, and a style that lengthened over the floral lifespan. Both species were pollinated by bees with the most common geometric mean of body dimensions between 2-3 mm. Most bees carried pure loads of the host plant’s pollen. Despite phenological isolation, the two herbs shared three bee species. Allium stellatum was also pollinated by the beetle Chauliognathus pensylvanicus DeGeer (Cantharidae). Tepal nyctinasty ensured mechanical self-pollination in N. bivalve. Protandry occurred in A. stellatum. In N. bivalve, the proportion of pollen tubes penetrating ovules was highest in bagged, self-pollinating flowers. However, in A. stellatum it was highest in exposed flowers and hand cross-pollinated flowers. Fruit set in N. bivalve was highest in exposed and bagged, self-pollinating flowers. In A. stellatum, fruit set was highest in both exposed and hand cross-pollinated flowers. Seed set was the same among all treatments for both species. We interpret these results as evidence that A. stellatum is a self-incompatible, obligate outcrosser. Nothoscodum bivalve is a self-compatible, obligate inbreeder employing mechanical and insect-mediated self-pollination. Outbreeding depression appears to occur in N. bivalve with a partial trend towards intraspecific cross-incompatibility.
References
Aizen MA (1993) Self-pollination shortens flower lifespan in Portulaca umbraticola H.B.K. (Portulacaceae). International Journal of Plant Sciences 154:412-415. https://doi.org/10.1086/297123
Angiosperm Phylogeny Group (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Botanical Journal of the Linnean Society 161:105-121. https://doi.org/10.1111/j.1095-8339.2009.00996.x
Arditti J (1992) Fundamentals of orchid biology. John Wiley & Sons, New York.
Armbruster WS, Mulder CPH, Baldwin BG, Kalisz S, Wessa B, Nute H (2002) Comparative analysis of late floral development and mating-system evolution in tribe Collinsieae (Scrophulariaceae s.l.). American Journal of Botany 89:37-49. https://doi.org/10.3732/ajb.89.1.37
Baskin JM, Baskin CC (1979) The ecological life cycle of Nothoscordum bivalve in Tennessee cedar glades. Castanea 44:193-202.
Bernhardt P, Kenrick J, Knox RB (1984) Pollination biology and the breeding system of Acacia retinodes (Leguminosae: Mimosoideae). Annals of the Missouri Botanical Garden 71:17-29. https://doi.org/10.2307/2399054
Bernhardt P, Knox RB, Calder DM (1980) Floral biology and self-incompatibility in some Australian mistletoes of the genus Amyema (Loranthaceae). Australian Journal of Botany 28:437-451. https://doi.org/10.1071/BT9800437
Block E (2010) Garlic and other Alliums: the lore and the science, 1 edition. Royal Society of Chemistry, Cambridge, UK. https://doi.org/10.1039/9781839168369
Boyd RS, Teem A, Wall MA (2011) Floral biology of an Alabama population of the federally endangered plant, Xyris tennesseensis Kral (Xyridaceae). Castanea 76:255-265. https://doi.org/10.2179/11-006.1
Cariveau D, Irwin RE, Brody AK, Garcia-Mayeya LS, Ohe AVD (2004) Direct and indirect effects of pollinators and seed predators to selection on plant and floral traits. Oikos 104:15-26. https://doi.org/10.1111/j.0030-1299.2004.12641.x
Cecich R (1997) Pollen tube growth in Quercus. Forest Science 43:140-146. https://doi.org/10.1093/forestscience/43.1.140
Choi HJ, Davis AR, Cota-Sánchez JH (2011) Comparative floral structure of four New World Allium (Amaryllidaceae) species. Systematic botany 36:870-882. https://doi.org/10.1600/036364411X604895
Christenhusz MJM, Byng JW (2016) The number of known plants species in the world and its annual increase. Phytotaxa 261:201-217. https://doi.org/10.11646/phytotaxa.261.3.1
Churchill S (1986) Flora of the Great Plains McGregor RL, Barkley TM (eds). Univ Pr of Kansas, Lawrence, Kan.
Clinebell R, Bernhardt P (1998) The pollination ecology of five species of Penstemon (Scrophulariaceae) in the tallgrass prairie. Annals of the Missouri Botanical Garden 85:126. https://doi.org/10.2307/2992002
Crabtree T (2016) Tennessee Natural Heritage Program rare plant list.
Cronquist A, Takhtadzhi︠a︡n AL (1981) An integrated system of classification of flowering plants. Columbia University Press, New York, USA.
Cruden RW (1977) Pollen-ovule ratios: a conservative indicator of breeding systems in flowering plants. Evolution 31:32-46. https://doi.org/10.2307/2407542
Currah L, Ockendon DJ (1978) Protandry and the sequence of flower opening in the onion (Allium cepa L.). New Phytologist 81:419-428. https://doi.org/10.1111/j.1469-8137.1978.tb02647.x
Darwin C, Darwin F (1880) The power of movement in plants. John Murray, London. [online] URL: http://archive.org/details/ https://doi.org/10.5962/bhl.title.102319
Davis L (2005) False garlic Nothoscordum bivalve (L.) Britt.
Dibble AC, Drummond FA, Averill AL, Bickerman-Martens K, Bosworth SC, Bushmann SL, Hoshide AK, Leach ME, Skyrm K, Venturini E, White A (2018) Bees and their habitats in four New England states. The Universty of Maine.
Dyer AF (1967) The maintenance of structural heterozygosity in Nothoscordum fragrans Kunth. Caryologia 20:287-308. https://doi.org/10.1080/00087114.1967.10796267
Edens-Meier R, Arduser M, Westhus E, Bernhardt P (2011) Pollination ecology of Cypripedium reginae Walter (Orchidaceae): size matters. Telopea 13 https://doi.org/10.7751/telopea20116024
Edens-Meier R, Vance N, Luo Y-B, Li P, Westhus E, Bernhardt P (2010) Pollen-pistil interactions in North American and Chinese Cypripedium L. (Orchidaceae). International Journal of Plant Sciences. 171(4): 370-381. 4:370-381. https://doi.org/10.1086/651225
Egea J, Burgos L (1996) Detecting cross-incompatibility of three North American apricot cultivars and establishing the first incompatibility group in apricot. Journal of the American Society for Horticultural Science 121:1002-1005. https://doi.org/10.21273/JASHS.121.6.1002
Endangered, threatened, rare and extirpated plants of Indiana (2016)
Everitt J, Drawe L (1974) Spring food habits of white-tailed deer in the South Texas Plains. Journal of Range Management 27:15-20. https://doi.org/10.2307/3896430
Farkas A, Molnar R, Morschhauser T, Hahn I (2012) Variation in nectar volume and sugar concentration of Allium ursinum L. ssp. ucrainicum in three habitats. The Scientific World Journal 2012 [online] URL: https://www.hindawi.com/journals/tswj/2012 https://doi.org/10.1100/2012/138579
Fernández VA, Galetto L, Astegiano J (2009) Influence of flower functionality and pollination system on the pollen size-pistil length relationship. Organisms Diversity & Evolution 9:75-82. https://doi.org/10.1016/j.ode.2009.02.001
Gómez EM, Dicenta F, Batlle I, Romero A, Ortega E (2019) Cross-incompatibility in the cultivated almond (Prunus dulcis): Updating, revision and correction. Scientia Horticulturae 245:218-223. https://doi.org/10.1016/j.scienta.2018.09.054
Grubb PJ, Jackson RV (2007) The adaptive value of young leaves being tightly folded or rolled on monocotyledons in tropical lowland rain forest, an hypothesis in two parts. Plant Ecology 192:317-327. https://doi.org/10.1007/s11258-007-9302-0
Kumar J, Gupta JK (1993) Nectar sugar production and honeybee foraging activity in 3 species of onion (Allium species). Apidologie 24:391-396. https://doi.org/10.1051/apido:19930405
Li Q-Q, Zhou S-D, He X-J, Yu Y, Zhang Y-C, Wei X-Q (2010) Phylogeny and biogeography of Allium (Amaryllidaceae: Allieae) based on nuclear ribosomal internal transcribed spacer and chloroplast rps16 sequences, focusing on the inclusion of species endemic to China. Annals of Botany 106:709-733. https://doi.org/10.1093/aob/mcq177
Lu Y, Kermicle JL, Evans MMS (2014) Genetic and cellular analysis of cross-incompatibility in Zea mays. Plant Reproduction 27:19-29. https://doi.org/10.1007/s00497-013-0236-5
Lyon, D. (1992). Bee pollination of facultatively xenogamous Sanguinaria canadensis L. Bulletin of the Torrey Botanical Club 119: 368-375. https://doi.org/10.2307/2996724
Maune JF, Camadro EL, Erazzú LE (2017) Cross-incompatibility and self-incompatibility: unrelated phenomena in wild and cultivated potatoes? Botany 96:33-45. https://doi.org/10.1139/cjb-2017-0070
McNeal Jr D, Jacobsen TD (2002) Allium & Nothoscordum. In: Flora of North America North of Mexico. Oxford University Press, Inc., pp 244-278.
Minorsky PV (2019) The functions of foliar nyctinasty: a review and hypothesis. Biological Reviews 94:216-229. https://doi.org/10.1111/brv.12444
Molano-Flores B, Hendrix SD, Heard SB (1999) The effect of population size on stigma pollen load, fruit set, and seed set in Allium stellatum Ker. (Liliaceae). International Journal of Plant Sciences 160:753-757. https://doi.org/10.1086/314160
Ordway E (1966) The Bionomics of Augochlorella striata and A. persimilis in Eastern Kansas (Hymenoptera: Halictidae). Journal of the Kansas Entomological Society 39:270-313.
Ornduff R (1969) Reproductive biology in relation to systematics. Taxon 18:121-133. https://doi.org/10.2307/1218671
Pires JC, Maureira IJ, Givnish TJ, Systma KJ, Seberg O, Peterson GP, Davis JI, Stevenson DW, Rudall PJ, Fay MF, Chase MW (2006) Phylogeny, genome size, and chromosome evolution of Asparagales. Aliso: A Journal of Systematic and Evolutionary Botany 22:287-304. https://doi.org/10.5642/aliso.20062201.24
powermovementin06darwgoog (accessed 13 June 2019).
Rahn K (1998) Alliaceae. In: Kubitzki K (ed) The families and genera of vascular plants. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 70-78. https://doi.org/10.1007/978-3-662-03533-7_9
Rare native Ohio plants 2018-19 status list (2018)
Rehan SM, Glastad KM, Lawson SP, Hunt BG (2016) The genome and methylome of a subsocial small carpenter bee, Ceratina calcarata. Genome Biology and Evolution 8:1401-1410. https://doi.org/10.1093/gbe/evw079
Schemske DW, Willson MF, Melampy MN, Miller LJ, Verner L, Schemske KM, Best LB (1978) Flowering ecology of some spring woodland herbs. Ecology 59:351-366. https://doi.org/10.2307/1936379
Seymour FC (1969) Flora of New England. Charles E. Tuttle Co., Rutland, Vermont.
Sogo A, Noguchi J, Jaffré T, Tobe H (2004) Pollen-tube growth pattern and chalazogamy in Casuarina equisetifolia (Casuarinaceae). Journal of Plant Research 117:37-46. https://doi.org/10.1007/s10265-003-0129-z
Sogo A, Tobe H (2006) Delayed fertilization and pollen-tube growth in Pistils of Fagus japonica (Fagaceae). American Journal of Botany 93:1748-1756. https://doi.org/10.3732/ajb.93.12.1748
Stahl E (1897) Uber den Pflanzenschlaf und verwandte Erscheinungen. Botanische Zeitung 55:71-109.
The Angiosperm Phylogeny Group (2003) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Botanical Journal of the Linnean Society 141:399-436. https://doi.org/10.1046/j.1095-8339.2003.t01-1-00158.x
Waser, N.M., Price, M.V. (1994) Crossing-distance effects in Delphinium nelsonii: Outbreeding and inbreeding depression in progeny fitness. Evolution 48: 842-852. https://doi.org/10.1111/j.1558-5646.1994.tb01366.x
Whitehead MR, Lanfear R, Mitchell RJ, Karron JD (2018) Plant mating systems often vary widely among populations. Frontiers in Ecology and Evolution 6 [online] URL: https://www.frontiersin.org/articles/10.3389/fevo.2018.00038/full (accessed 13 June 2019). https://doi.org/10.3389/fevo.2018.00038
Willmer P (2011) Pollination and floral ecology. Princeton University Press. https://doi.org/10.23943/princeton/9780691128610.001.0001
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