Abstract
Petals of the alpine, arctic perennial herb Ranunculus glacialis are retained also during seed maturation, as opposed to most species where the petals wither after they have contributed to insect attraction during anthesis. To assess the adaptive significance of perianth retention after anthesis for annual reproduction, we experimentally removed perianths of R. glacialis and explored its impact on achene surface temperature, the growth rate of achenes, carbon allocation, and seed production. Perianth removal immediately after anthesis decreased achene surface temperature, decelerated the growth of achenes and reduced seed set, compared to plants with intact perianth. Measurement of mass allocation showed no further perianth growth during seed maturation, and a 13C labelling experiment demonstrated that photosynthate allocation to perianths during seed maturation was much smaller than developing achenes. Thus, annual seed production of R. glacialis might be accelerated by perianth retention during seed maturation, while the cost of perianth retention is small compared to that of seed development. In alpine and arctic environments, cold temperatures limit the growth rate of achenes. Hence, the heating of developing achenes by perianth retention might be an adaptive trait that enhances female reproductive success in this arctic, alpine species.
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References
Andersson S (2005) Floral costs in Nigella sativa (Ranunculaceae): compensatory responses to perianth removal. Am J Bot 92:279–283
Arft AM, Walker MD, Gurevitch J, Alatalo JM, Bret-Harte MS, Dale M, Diemer M, Gugerli F, Henry GHR, Jones MH, Hollister RD, Jonsdottir IS, Laine K, Lévesque E, Marion GM, Molau U, Mølgaard P, Nordenhäll U, Raszhivin V, Robinson CH, Starr G, Stenström A, Stenström M, Totland Ø, Turner PL, Walker LJ, Webber PJ, Welker JM, Wookey PA (1999) Responses of tundra plants to experimental warming: meta-analysis of the International Tundra Experiment. Ecol Monogr 69:491–511
Ashman TL (1994) A dynamic perspective on the physiological cost of reproduction in plants. Am Nat 144:300–316
Ashman TL, Schoen DJ (1996) Floral longevity: Fitness consequences and resource costs. In: Lloyd DG, Barrett SCH (eds) Floral biology. Chapman and Hall, New York, pp 112–139
Bell G (1985) On the function of flowers. Proc R Soc B 224:223–265
Bell G, Bliss LC (1979) Autecology of Kobresia bellardii: why winter snow accumulation limits local distribution. Ecol Monogr 49:377–402
Bliss LC (1971) Arctic and alpine plant life cycles. Ann Rev Ecol Syst 2:405–438
Bokhorst S, Huiskes A, Aerts R, Convey P, Cooper EJ, Dalen L, Erschbamer B, Gudmundsson J, Hofgaard A, Hollister RD, Johnstone J, Jonsdottir IS, Lebouvier M, Van De Vijver B, Wahren CH, Dorrepaal E (2013) Variable temperature effects of open top chambers at polar and alpine sites explained by irradiance and snow depth. Global Change Biol 19:64–74
Deleens E, Cliquet JB, Prioul JL (1994) Use of 13C and 15N plant label near natural abundance for monitoring carbon and nitrogen partitioning. Aust J Plant Physiol 21:133–146
Dyer AG, Whitney HM, Arnold SEJ, Glover BJ, Chittka L (2006) Bees associate warmth with floral colour. Nature 442:525
Fajardo A, Piper FI, Pfund L, Körner C, Hoch G (2012) Variation of mobile carbon reserves in trees at the alpine treeline ecotone is under environmental control. New Phytol 195:794–802
Fitzmaurice GM, Laird NM, Ware JH (2004) Applied longitudinal analysis. Wiley-Interscience, Hoboken
Galen C (1989) Measuring pollinator-mediated selection on morphometric floral traits: bumblebees and the alpine sky pilot, Polemonium viscosum. Evolution 43:882–890
Galen C (1999) Why do flowers vary? The functional ecology of variation in flower size and form within natural plant populations. Bioscience 49:631–640
Galen C (2006) Solar furnaces or swamp coolers: costs and benefits of water use by solar-tracking flowers of the alpine snow buttercup, Ranunculus adoneus. Oecologia 148:195–201
Galen C, Dawson TE, Stanton ML (1993) Carpels as leaves: meeting the carbon cost of reproduction in an alpine buttercup. Oecologia 95:187–193
Gimenez-Benavides L, Escudero A, Iriondo JM (2007) Reproductive limits of a late-flowering high-mountain Mediterranean plant along an elevational climate gradient. New Phytol 173:367–382
Gulmon SL, Mooney HA (1986) Costs of defence and their effects on plant productivity. In: Givnish TJ (ed) On the economy of plant form and function. Cambridge University Press, London, pp 681–698
Haig D, Westoby M (1988) On limits to seed production. Am Nat 131:757–759
Haig D, Westoby M (1991) Seed size, pollination costs and angiosperm success. Evol Ecol 5:231–247
Haselberg C, Ludders P, Stosser R (2004) Pollen tube growth, fertilization and ovule longevity in the carob tree (Ceratonia siliqua L.). J Appl Bot 78:32–40
Hedhly A, Hormaza JI, Herrero M (2003) The effect of temperature on stigmatic receptivity in sweet cherry (Prunus avium L.). Plant Cell Environ 26:1673–1680
Henry GHR, Molau U (1997) Tundra plants and climate change: the International Tundra Experiment (ITEX). Global Change Biol 3(Suppl 1):1–9
Hoch G, Körner C (2003) The carbon charging of pines at the climatic treeline: a global comparison. Oecologia 135:10–21
Hoch G, Körner C (2012) Global patterns of mobile carbon stores in trees at the high-elevation tree line. Global Ecol Biogeogr 21:861–871
Horibata S, Hasegawa SF, Kudo G (2007) Cost of reproduction in a spring ephemeral species, Adonis ramosa (Ranunculaceae): carbon budget for seed production. Ann Bot 100:565–571
Ida TY, Harder LD, Kudo G (2013) Demand-driven resource investment in annual seed production by a perennial angiosperm precludes resource limitation. Ecology 94:51–61
Inouye DW, McGuire AD (1991) Effects of snowpack on timing and abundance of flowering in Delphinium nelsonii (Ranunculaceae): implications for climate change. Am J Bot 78:997–1001
Ishii HS, Harder LD (2006) The size of individual Delphinium flowers and the opportunity for geitonogamous pollination. Funct Ecol 20:1115–1123
Kenward MG, Roger JH (1997) Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53:983–997
Kevan PG (1990) Sexual differences in temperatures of blossoms on a dioecious plant, Salix arctica: significance for life in the arctic. Arct Alp Res 22:283–289
Körner C (1998) A re-assessment of high elevation treeline positions and their explanation. Oecologia 115:445–459
Körner C (2003) Alpine plant life: functional plant ecology of high mountain ecosystems. Springer, Berlin
Kudo G (1991) Effects of snow-free period on the phenology of alpine plants inhabiting snow patches. Arct Alp Res 23:436–443
Kudo G (1995) Ecological significance of flower heliotropism in the spring ephemeral Adonis ramosa (Ranunculaceae). Oikos 72:14–20
Kudo G, Ida TY (2013) Early onset of spring increases the phenological mismatch between plants and pollinators. Ecology 94:2311–2320
Kudo G, Ida TY, Tani T (2008) Linkage between phenology, pollination, photosynthesis, and reproduction in deciduous forest understory plants. Ecology 89:321–331
Ladinig U, Hacker J, Neuner G, Wagner J (2013) How endangered is sexual reproduction of high-mountain plants by summer frosts? Frost resistance, frequency of frost events and risk assessment. Oecologia 171:743–760
Lloyd DG (1988) Benefits and costs of biparental and uniparental reproduction in plants. In: Michod RE, Levin BR (eds) The evolution of sex. Sinauer, Sunderland, pp 233–252
Lord J, Westoby M (2006) Accessory costs of seed production. Oecologia 150:310–317
Lord J, Westoby M (2012) Accessory costs of seed production and the evolution of angiosperms. Evolution 60:200–210
Lovett-Doust J, Cavers PB (1982) Biomass allocation in hermaphrodite flowers. Can J Bot 60:2530–2534
Miller GA (1986) Pubescence, floral temperature and fecundity in species of Puya (Bromeliaceae) in the Ecuadorian Andes. Oecologia 70:155–160
Molau U (1993) Relationships between flowering phenology and life history strategies in tundra plants. Arct Alp Res 25:391–402
Morris WF, Doak DF (1998) Life history of the long-lived gynodioecious cushion plant, Silene acaulis (Caryophyllaceae), inferred from size-based population projection matrices. Am J Bot 85:784–793
Oberhuber W, Swidrak I, Pirkebner D, Gruber A (2011) Temporal dynamics of nonstructural carbohydrates and xylem growth in Pinus sylvestris exposed to drought. Can J For Res 41:1590–1597
Obeso JR (2002) The cost of reproduction in plants. New Phytol 155:321–348
Seymour RS, Schultze-Motel P (1996) Thermoregulating lotus flowers. Nature 383:305
Simard SW, Durall DM, Jones MD (1997) Carbon allocation and carbon transfer between Betula papyrifera and Pseudotsuga menziesii seedlings using a 13C pulse-labeling method. Plant Soil 191:41–55
Smith AP (1975) Insect pollination and heliotropism in Oritrophium limnophilum (Compositae) of the Andean paramo. Biotropica 7:284–286
Song B, Zhang Z-Q, Stöcklin J, Yang Y, Niu Y, Chen J-G, Sun H (2013) Multifunctional bracts enhance plant fitness during flower and seed development in Rheum nobile (Polygonaceae), a giant herb endemic to the high Himalayas. Oecologia 172:359–370
Stanton ML, Galen C (1989) Consequences of flower heliotropism for reproduction in an alpine buttercup (Ranunculus adoneus). Oecologia 78:477–485
Steinacher G, Wagner J (2012) Effect of temperature on the progamic phase in high-mountain plants. Plant Biol 14:295–305
Sunmonu N, Ida TY, Kudo G (2013) Photosynthetic compensation by the reproductive structures in the spring ephemeral Gagea lutea. Plant Ecol 214:175–188
Thompson K, Stewart AJA (1981) The measurement and meaning of reproductive effort in plants. Am Nat 117:205–211
Totland Ø (1996) Heliotropism in an alpine population of Ranunculus acris (Ranunculaceae): effects on flower temperature, insect visitation, and seed production. Am J Bot 83:452–458
Totland Ø (2004) No evidence for a role of pollinator discrimination in causing selection on flower size through female reproduction. Oikos 106:558–564
Totland Ø, Alatalo JM (2002) Effects of temperature and date of snowmelt on growth, reproduction, and flowering phenology in the arctic/alpine herb, Ranunculus glacialis. Oecologia 133:168–175
Tsukaya H, Tsuge T (2001) Morphological adaptation of inflorescences in plants that develop at low temperatures in early spring: the convergent evolution of a “downy Plants”. Plant Biol 3:536–543
Wagner J, Ladinig U, Steinacher G, Larl I (2011) From the flower bud to the mature seed: Timing and dynamics of flower and seed development in high-mountain plants. In: Lutz C (ed) Plants in alpine regions. Springer, New York
Weiss MR (1995) Floral color change: a widespread functional convergence. Am J Bot 82:167–185
Wiens D (1984) Ovule survivorship, brood size, life history, breeding systems, and reproductive success in plants. Oecologia 64:47–53
Willson MF, Michaels HJ, Bertin RI, Benner B, Rice S, Lee TD, Hartgerink AP (1990) Intraspecific variation in seed packaging. Am Mid Nat 123:179–185
Acknowledgments
We thank the staff of the Finse Field Station of University of Oslo and Bergen for the support of our stay in Finse, and two anonymous reviewers for helpful comments on the manuscript. This study was supported by a Japan-Norway Researcher Mobility Programme FY2013 [228029/F11] by Japan Society for the Promotion of Science and the Research Council of Norway to T. Y. Ida.
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Ida, T.Y., Totland, Ø. Heating effect by perianth retention on developing achenes and implications for seed production in the alpine herb Ranunculus glacialis . Alp Botany 124, 37–47 (2014). https://doi.org/10.1007/s00035-014-0129-8
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DOI: https://doi.org/10.1007/s00035-014-0129-8