Abstract
Specialized bracts are thought to be important for the successful reproduction of some plants and are regarded as adaptations to diverse driving forces. However, few empirical studies have quantified the adaptive significance of bracts within a cost–benefit framework. We explored the adaptive significance of large and showy bracts for reproduction in Rheum nobile, a giant herb endemic to the high Himalayas. We examined whether the bracts enhance reproductive success during flowering and seed development. Bracts increased flower and fruit temperature on sunny days, greatly decreased the intensity of ultraviolet-B (UV-B) radiation reaching flowers and fruits, and prevented pollen grains being washed away by rain. Experiments indicated that high temperature could promote pollen germination, while pollen grains exposed to rain and UV-B radiation at ambient levels were seriously damaged. Furthermore, bract removal decreased the number of pollinators visiting flowers. When bracts were removed before or after flowering, fecundity and progeny quality were adversely affected, but seed predation by larvae of pollinators decreased. A cost–benefit analysis demonstrated that the cost of bracts, i.e., increased seed predation, is modest. Our results suggest that the bracts of R. nobile promote pollen germination, protect pollen grains from rain and intense UV-B radiation, enhance pollinator visitation during flowering, and facilitate the development of fertilized ovules during seed development. We conclude that multifunctional bracts of R. nobile are an effective adaptive strategy in alpine environments and might have been selected for because of abiotic environmental conditions as well as for enhancing pollination success.
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References
Armbruster WS (1997) Exaptations link evolution of plant-herbivore and plant-pollinator interactions: a phylogenetic inquiry. Ecology 78:1661–1672
Ashman TL, Cole DH, Bradburn M (2004) Sex-differential resistance and tolerance to herbivory in a gynodioecious wild strawberry. Ecology 85:2550–2559. doi:10.1890/03-0495
Borges RM, Gowda V, Zacharias M (2003) Butterfly pollination and high-contrast visual signals in a low-density distylous plant. Oecologia 136:571–573. doi:10.1007/s00442-003-1336-y
Boyer JS (1982) Plant productivity and the environment. Science 218:443–448
Bynum MR, Smith WK (2001) Floral movements in response to thunderstorms improve reproductive effort in the alpine species Gentiana algida (Gentianaceae). Am J Bot 88:1088–1095
Caldwell MM (1981) Plant response to solar ultraviolet radiation. In: Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) Physiological plant ecology. I. Response to the physical environment. Encyclopedia of plant physiology, new series, vol 12. Springer, Berlin, pp 169–197
Chakrabarti B, Singh SD, Nagarajan S, Aggarwal PK (2011) Impact of temperature on phenology and pollen sterility of wheat varieties. Aust J Crop Sci 5:1039–1043
Chowdhery HJ, Agrawala DK (2009) Rheum nobile Hook. f. and Thoms. (Polygonaceae)-a rare and highly specialized plant of Himalayan region. Indian J Bot 32:145–148
Cooley JR (1995) Floral heat rewards and direct benefits to insect pollinators. Ann Entomol Soc Am 88:576–579
Dafni A (1992) Pollination ecology: a practical approach. Oxford University Press, Oxford
DeCeault MT, Polito VS (2010) High temperatures during bloom can inhibit pollen germination and tube growth, and adversely affect fruit set in the Prunus domestica cultvars ‘improved French’ and ‘muir beauty’. Acta Hortic 874:163–168
Devlin RM, Witham FH (1983) Plant physiology, 4th edn. Willard Grant, Boston
Dieringer G, Cabrera-R L, Lara M, Loya L, Reyes-Castillo P (1999) Beetle pollination and floral thermogenicity in Magnolia tamaulipana (Magnoliaceae). Int J Plant Sci 160:64–71
Egli DB, Wardlaw IF (1980) Temperature response of seed growth characteristics of soybeans. Agron J 72:560–564
Feng HY, An LZ, Tan LL, Hou ZD, Wang XL (2000) Effect of enhanced ultraviolet-B radiation on pollen germination and tube growth of 19 taxa in vitro. Environ Exp Bot 43:45–53. doi:10.1016/S0098-8472(99)00042-8
Galen C, Butchart B (2003) Ants in your plants: effects of nectar-thieves on pollen fertility and seed-siring capacity in the alpine wildflower, Polemonium viscosum. Oikos 101:521–528. doi:10.1034/j.1600-0706.2003.12144.x
Galen C, Stanton ML (2003) Sunny-side up: flower heliotropism as a source of parental environmental effects on pollen quality and performance in the snow buttercup, Ranunculus adoneus (Ranunculaceae). Am J Bot 90:724–729. doi:10.3732/ajb.90.5.724
Gulias J, Traveset A, Riera N, Mus M (2004) Critical stages in the recruitment process of Rhamnus alaternus L. Ann Bot 93:723–731. doi:10.1093/aob/mch100
Harley P, Deem G, Flint S, Caldwell M (1996) Effects of growth under elevated UV-B on photosynthesis and isoprene emission in Quercus gambelii and Mucuna pruriens. Glob Change Biol 2:149–154. doi:10.1111/j.1365-2486.1996.tb00060.x
He YP, Duan YW, Liu JQ, Smith WK (2006) Floral closure in response to temperature and pollination in Gentiana straminea Maxim. (Gentianaceae), an alpine perennial in the Qinghai-Tibetan Plateau. Plant Syst Evol 256:17–33. doi:10.1007/s00606-005-0345-1
Herre EA, Jandér C, Machado CA (2008) Evolutionary ecology of figs and their associates: recent progress and outstanding puzzles. Annu Rev Ecol Evol Syst 39:439–458. doi:10.1146/annurev.ecolsys.37.091305.110232
Herrera CM (1995) Floral biology, microclimate, and pollination by ectothermic bees in an early-blooming herb. Ecology 76:218–228
Herrera J (1997) The role of colored accessory bracts in the reproductive biology of Lavandula stoechas. Ecology 78:494–504
Huang SQ, Takahashi Y, Dafni A (2002) Why dose the flower stalk of Pulsatilia cernua (Ranunculaceae) bend during anthesis? Am J Bot 89:1599–1603. doi:10.3732/ajb.89.10.1599
Hughes HG, Lee CW (1991) Low-temperature preservation of Clianthus formosus pollen. HortScience 26:1411–1412
Iwashina T, Omori Y, Kitajima J, Akiyama S, Suzuki T, Ohba H (2004) Flavonoids in translucent bracts of the Himalayan Rheum nobile (Polygonaceae) as ultraviolet shieds. J Plant Res 117:101–107. doi:10.1007/s10265-003-0134-2
Kaur G, Kumar S, Nayyar H, Upadhyaya HD (2008) Cold stress injury during the pod-filling phase in Chickpea (Cicer arietinum L.): effects on quantitative and qualitative components of seeds. J Agron Crop Sci 194:457–464. doi:10.1111/j.1439-037X.2008.00336.x
Keasar T, Sadeh A, Gerchman Y, Shmida A (2009) The signaling function of an extra-floral display: what selects for signal development? Oikos 118:1752–1759. doi:10.1111/j.1600-0706.2009.17626.x
Kevan PG (1975) Sun-tracking solar furnaces in high arctic flowers: significance for pollination and insect. Science 189:723–726
Kevan P, Giurfa M, Chittka L (1996) Why are there so many and so few white flowers? Trends Plant Sci 1:280–284. doi:10.1016/1360-1385(96)20008-1
Knutson RM (1974) Heat production and temperature regulation in eastern skunk cabbage. Science 186:746–747
Körner C (2003) Alpine plant life, 2nd edn. Springer, Berlin
Kumar A, Omae H (2008) Estimation of seed yield and yield attributes by cumulative temperature in common bean (Phaseolus vulgaris). Indian J Agric Sci 78:127–130
Lloyd DG, Barrett SCH (1996) Floral biology: Studies on floral evolution in animal-pollinated plants. Chapman and Hall, New York
Lora J, Pérez de Oteyza MA, Fuentetaja P, Hormaza JI (2006) Low temperature storage and in vitro germination of cherimoya (Annona cherimola Mill.) pollen. Sci Hortic 108:91–94. doi:10.1016/j.bbr.2011.03.031
Mao YY, Huang SQ (2009) Pollen resistance to water in 80 angiosperm species: flower structures protect rain-susceptible pollen. New Phytol 183:892–899. doi:10.1111/j.1469-8137.2009.02925.x
Musil CF (1994) Ultraviolet-B irradiation of seeds affects photochemical and reproductive performance of the arid-environment ephemeral Dimorphotheca pluvialis. Environ Exp Bot 34:371–378. doi:10.1016/0098-8472(94)90019-1
Musil CF (1995) Differential effects of elevated ultraviolet-B radiation on the photochemical and reproductive performances of dicotyledonous and monocotyledonous arid-environment ephemerals. Plant Cell Environ 18:844–854. doi:10.1111/j.1365-3040.1995.tb00593.x
Nagy KA, Odell DK, Seymour RS (1972) Temperature regulation by the inflorescence of Philodendron. Science 178:1195–1197
Nayyar H, Kaur G, Kumar S, Upadhyaya HD (2007) Low temperature effects during seed filling on chickpea genotypes (Cicer arietinum L.): probing mechanisms affecting seed reserves and yield. J Agron Crop Sci 193:336–344. doi:10.1111/j.1439-037X.2007.00269.x
Nilsson LA (1988) The evolution of flowers with deep corolla tubes. Nature 334:147–149
Ohba H (1988) The alpine flora of the Nepal Himalayas: an introductory note. In: Ohba H, Malla SB (eds) The Himalayan plants, vol 1. University of Tokyo Press, Tokyo, pp 19–46
Omori Y, Ohba H (1996) Pollen development of Rheum nobile Hook. f. and Thomson (Polygonaceae), with reference to its sterility induced by bract removal. Bot J Linn Soc 122:269–278
Omori Y, Ohba H (1999) Thermal condition of the inflorescence of a glasshouse plant, Rheum nobile Hook. f. and Thoms., and microclimatic features of its habitat in Jaljale Himal, east Nepal. Newsl Himal Bot 25:5–11
Omori Y, Takayama H, Ohba H (2000) Selective light transmittance of translucent bracts in the Himalayan giant glasshouse plant Rheum nobile Hook. f. and Thomson (Polygonaceae). Bot J Linn Soc 132:19–27. doi:10.1006/bojl.1999.0280
Patiño S, Grace J (2002) The cooling of convolvulaceous flowers in a tropical environment. Plant Cell Environ 25:41–51. doi:10.1046/j.0016-8025.2001.00801.x
Sapir Y, Shmida A, Ne’eman G (2006) Morning floral heat as a reward to the pollinators of the Oncocyclus irises. Oecologia 147:53–59. doi:10.1007/s00442-005-0246-6
Sato S, Peet MM, Thomas JF (2002) Determining critical pre- and post-anthesis periods and physiological process in Lycopersicon esculentum mill. exposed to moderately elevated temperature. J Exp Bot 53:1187–1195. doi:10.1093/jexbot/53.371.1187
Seymour RS, Schultze-Motel P (1997) Heat-producing flowers. Endeavour 21:125–129
Seymour RS, White CR, Gibernau M (2003) Heat reward for insect pollinators. Nature 426:243–244. doi:10.1038/426243a
Skubatz H, Williamson PS, Schneider EL, Meeuse BJD (1990) Cyanide-insensitive respiration in thermogenic flowers of Victoria and Nelumbo. J Exp Bot 41:1335–1339. doi:10.1093/jxb/41.10.1335
Strauss SY, Whittall JB (2006) Non-pollinator agents of selection on floral traits. In: Harder LD, Barrett SCH (eds) Ecology and evolution of flowers. Oxford University Press, Oxford, pp 120–138
Sun JF, Gong YB, Renner SS, Huang SQ (2008) Multifunctional bracts in the dove tree Davidia involucrata (Nyssaceae: Cornales): rain protection and pollinator attraction. Am Nat 171:119–124. doi:10.1086/523953
Svensson E, Calsbeek R (2012) The adaptive landscape in evolutionary biology. Oxford University Press, Oxford
Terashima I, Masuzawa T, Ohba H (1993) Photosynthetic characteristics of a giant alpine plant, Rheum nobile Hook.f. et Thoms. and of some other alpine species measured at 4300 m, in the Eastern Himalaya, Nepal. Oecologia 95:194–201
Torabinejad J, Caldwell MM, Flint SD, Durham S (1998) Susceptibility of pollen to UV-B radiation: an assay of 34 taxa. Am J Bot 85:360–369
Totland ö (1996) Flower heliotropism in an alpine population of Ranunculus acris (Ranunculaceae): effects on flower temperature, insect visitation, and seed production. Am J Bot 83:452–458
Tsukaya H, Tsuge T (2001) Morphological adaptation of inflorescences in plants that develop at low temperatures in early spring: the convergent evolution of “downy plants”. Plant Biol 3:536–543. doi:10.1055/s-2001-17727
von Balthazar M, Endress PK (1999) Floral bract function, flowering process and breeding systems of Sarcandra and Chloranthus (Chloranthaceae). Plant Syst Evol 218:161–178. doi:10.1007/BF01089225
Wang Y (2006) Yunnan mountain climate. Science and Technology, Kunming
Wang Y, Meng LL, Yang YP, Duan YW (2010) Change in floral orientation in Anisodus luridus (Solanaceae) protects pollen grains and facilitates development of fertilized ovules. Am J Bot 97:1618–1624. doi:10.3732/ajb.1000010
Warren J, Mackenzie S (2001) Why are all colour combinations not equally represented as flower-colour polymorphisms? New Phytol 151:237–241
Waser NM, Price MV (1983) Pollinator behaviour and natural selection for flower colour in Delphinium nelsonii. Nature 302:422–424
Weberling F (1992) Morphology of flowers and inflorescences. Cambridge University Press, Cambridge
Yang Y, Sun H (2009) The bracts of Saussurea velutina (Asteraceae) protect inflorescences from fluctuating weather at high elevations of the Hengduan Mountains, Southwestern China. Arct Antarct Alp Res 41:515–521. doi:10.1657/1938-4246-41.4.515
Zhang DY, Liu BB, Zhao CM, Lu X, Wan DS, Ma F, Chen LT, Liu JQ (2010a) Ecological functions and differentially expressed transcripts of translucent bracts in an alpine ‘glasshouse’ plant Rheum nobile (Polygonaceae). Planta 231:1505–1511. doi:10.1007/s00425-010-1133-x
Zhang S, Ai HL, Yu WB, Wang H, Li DZ (2010b) Flower heliotropism of Anemone rivularis (Ranunculaceae) in the Himalayas: effects on floral temperature and reproductive fitness. Plant Ecol 209:301–312. doi:10.1007/s11258-010-9739-4
Zhu QL, Yu GR, Cai F, Liu XA, Li ZQ, Su W, Hu L (2005) Spatialization research on ultraviolet radiation in China. Resour Sci 27:108–113
Acknowledgments
We thank De-Li Peng, Gao Chen, and Yun-Gang Guo for their support during the experiments. We are also grateful to two anonymous reviewers for their constructive comments to the manuscript. This work was supported by the National Natural Science Foundation of China (40930209, 31061160184, 31100179, 31200184), Hundred Talents Program of the Chinese Academy of Sciences (2011312D11022), the Natural Science Foundation of Yunnan Province (2011FB102), Western Light Talent Culture Project to B. Song and China Postdoctoral Science Foundation funded project (2012T50787).
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Communicated by Russell Monson.
B. Song and Z.-Q. Zhang contributed equally to this work.
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Song, B., Zhang, ZQ., Stöcklin, J. et al. Multifunctional bracts enhance plant fitness during flowering and seed development in Rheum nobile (Polygonaceae), a giant herb endemic to the high Himalayas. Oecologia 172, 359–370 (2013). https://doi.org/10.1007/s00442-012-2518-2
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DOI: https://doi.org/10.1007/s00442-012-2518-2