ISSN : 2287-8327
Background: Temperature-driven variation in pollinator assemblage and activity are important information, especially at high altitudes, where rising temperature trends exceed global levels. Temporal patterns of pollinators in a flowering season can be used as a proxy to predict the changes of high-altitude plants’ mutualistic relationships. We observed a spring temperature change in one population of a high-altitude endemic species, Megaleranthis saniculifolia on Mt. Sobaeksan, and related it to pollinator assemblage and activity changes. Methods: This study was conducted at two sites, each facing different slopes (NE and NW), for two times in the spring of 2013 (early-flowering, April 27–28, vs. mid-flowering, May 7–8, 2013). We confirmed that the two sites were comparable in snowmelt regime, composition of flowering plants, and flower density, which could affect pollinator assemblage and activity. Pollinator assemblage and activity were investigated at three quadrats (1m2 with 5-m distance) for each site, covering a total of 840min observation for each site. We analyzed correlations between the temperature and visitation frequency. Results: Twelve pollinator species belonging to four orders were observed for M. saniculifolia at both sites during earlyand mid-flowering times. Diptera (five species) and hymenopteran species (four species) were the most abundant pollinators. Pollinator richness increased at both sites toward the mid-flowering time [early vs. mid = 7 (NE) and 3 (NW) vs. 9 (NE) and 5 (NW)]. Compared to the early-flowering time, visitation frequency showed a fourfold increase in the mid-flowering time. With the progression of spring, major pollinators changed from flies to bees. Upon using data pooled over both sites and flowering times, hourly visitation frequency was strongly positively correlated with hourly mean air temperature. Conclusions: The spring temperature change over a relatively brief flowering period of M. saniculifolia at high altitudes can alter pollinator assemblages through pollinator dominance and visitation frequency changes. Thus, this study emphasizes information on intra- and inter-annual variations in the mutualistic relationship between pollinators and M. saniculifolia to further assess the warming impacts on M. saniculifolia’s reproductive fitness.
Arroyo MTK, Armesto JJ, Primack RB. Community studies in pollination ecology in the high temperate Andes of central Chile II. Effect of temperature on visitation rates and pollination possibilities. Plant Syst Evol. 1985;149:187–203.
Arroyo MTK, Primack R, Armesto J. Community studies in pollination ecology in the high temperate Andes of central Chile. I. Pollination mechanisms and altitudinal variation. Am J Bot. 1982;69:82–97.
Ashman T, Knight TM, Steets JA, Amarasekare P, Burd M, Campbell DR, Dudash MR, Johnston MO, Mazer SJ, Mitchell RJ, Morgan MT, Wilson WG. Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology. 2004;85:2408–21.
Bingham RA, Orthner AR. Efficient pollination of alpine plants. Nature. 1998;391:238–9.
Campbell DR, Motten AF. The mechanism of competition for pollination between two forest herbs. Ecology. 1985;66:554–63.
Choi DY. Conservation strategy based on genetic structure and mating system of rare plants, Kirengeshoma koreana Nakai and Megaleranthis saniculifolia Ohwi. Seoul: Seoul National University; 2002.
Duan YW, Zhang TF, Liu JQ. Interannual fluctuations in floral longevity, pollinator visitation and pollination limitation of an alpine plant (Gentiana straminea Maxim., Gentianaceae) at two altitudes in the Qinghai-Tibetan Plateau. Plant Syst Evol. 2007;267:255–65.
Ebeling A, Klein A, Schumacher J, Weisser WW, Tscharntke T. How does plant richness affect pollinator richness and temporal stability of flower visits? Oikos. 2008;117:1808–15.
Gómez JM, Bosch J, Perfectti F, Fernández J, Abdelaziz M. Pollinator diversity affects plant reproduction and recruitment: the tradeoffs of generalization. Oecologia. 2007;153:597–605.
Han JW, Lee GH, Yang SG, Kang SH. Distribution of Megaleranthis saniculifolia Ohwi (Ranunculaceae) in Mt. Halla, Jeju island, Korean Journal of Plant. Resources. 2010;23:179–86.
Hegland SJ, Boeke L. Relationship between the density and diversity of floral resources and flower visitor activity in a temperate grassland community. Ecol Entomol. 2006;31:532–8.
Hegland SJ, Nielsen A, Lázaro A, Bjerknes A, Totland Ø. How does climate warming affect plant-pollinator interactions? Ecol Lett. 2009;12:184–95.
Hirao AS, Kameyama Y, Ohara M, Isagi Y, Kudo G. Seasonal changes in pollinator activity influence pollen dispersal and seed production of the alpine shrub Rhododendron aureum (Ericaceae). Mol Ecol. 2006;15:1165–73.
Hoiss B, Krauss J, Potts SG, Roberts S, Steffan-Dewenter I. Altitude acts as an environmental filter on phylogenetic composition, traits and diversity in bee communities. Proc R Soc Lond B Biol Sci. 2012;279:4447–56.
Inouye DW, Larson BMH, Ssymank A, Kevan PG. Flies and flowers III: ecology of foraging and pollination. J Pollination Ecol. 2015;16:115–33.
IPCC. 5th Annual Report. Climate change 2013: the physical science basis. New York: Cambridge University Press; 2013.
Jang SK, Cheon KS, Jeong JH, Kim ZS, Yoo KO. Environmental characteristics and vegetation of Megaleranthis saniculifolia Ohwi habitats. Korean J Environ Biol. 2009;27:314–22.
Jeong JH, Kim EH, Guo W, Yoo KO, Jo DG, Kim ZS. Genetic diversity and structure of the endangered species Megaleranthis saniculifolia in Korea as revealed by allozyme and ISSR markers. Plant Syst Evol. 2010;289:67–76.
Kearns CA. Anthophilous fly distribution across an elevation gradient. Am Midl Nat. 1992;127:172–82.
Kim DI, Park KR. Pollination study of Euphorbia helioscopia (Euphorbiaceae). Korean J Plant Taxon. 2014;44:281–7.
Kim, Y.S., Kim, H., & Son, S.W. (2016). Megaleranthis saniculifolia. The IUCN Red List of Threatened Species, 2016, e.T72136660A72136663.
Kudo G. Effects of snowmelt timing on reproductive phenology and pollination process of alpine plants. Mem Natl Inst Polar Res. 1996;51:71–82.
Lázaro A, Hegland SJ, Totland Ø. The relationship between floral traits and specificity of pollination systems in three Scandinavian plant communities. Oecologia. 2008;157:249–57.
Lee H, Lee H, Kang H. Mating systems and flowering characteristics of Megaleranthis saniculifolia Ohwi in a subalpine zone of Sobaeksan National Park. Korean J Ecol Environ. 2017;50:116–25.
Lefebvre V, Villemant C, Fontaine C, Daugeron C. Altitudinal, temporal and trophic partitioning of flower-visitors in alpine communities. Sci Rep. 2018;8:4706.
Mizunaga Y, Kudo G. A linkage between flowering phenology and fruit-set success of alpine plant communities with reference to the seasonality and pollination effectiveness of bees and flies. Oecologia. 2017;185:453–64.
Primack RB. Variability in New Zealand montane and alpine pollinator assemblages. N Z J Ecol. 1978;1:66–73.
Primack RB, Inouye DW. Factors affecting pollinator visitation rates: a biogeographic comparison. Curr Sci. 1993;65:257–62.
R Core Team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2017. URL https://www.R-project.org/
Son DC, Cho KJ, Ko SC. Comparison of the morphology and distribution of the genus Megaleranthis Ohwi with those its relative genera (Ranunculaceae). Korean J Plant Taxon. 2011;41:315–23.
Straka JR, Starzomski BM. Fruitful factors: what limits seed production of flowering plants in the alpine? Oecologia. 2015;178:249–60.
Thomson JD. Flowering phenology, fruiting success and progressive deterioration of pollination in an early-flowering geophyte. Philos Trans R Soc B Biol Sci. 2010;365:3187–99.
Totland Ø. Pollination in alpine Norway: flowering phenology, insect visitors, and visitation rates in two plant communities. Can J Bot. 1993;71:1072–9.
Totland Ø. Intraseasonal variation in pollination intensity and seed set in an alpine population of Ranunculus acris in southwestern Norway. Ecography. 1994a;17:159–65.
Totland Ø. Influence of climate, time of day and season, and flower density on insect flower visitation in alpine Norway. Arct Alp Res. 1994b;26:66–71.
Wagner J, Lechleitner M, Hosp D. Pollen limitation is not the rule in nival plants:a study from the European Central Alps. Am J Bot. 2016;103:375–87.
Yoo KO, Lee WT, Oh YJ. External morphology and vegetation of Megaleranthis saniculifolia populations in four different habitats. Korean J Plant Resour. 1999;12:312–23.
Zhao ZG, Wang YK. Selection by pollinators on floral traits in generalized Trollius ranunculoides (Ranunculaceae) along altitudinal gradients. PLoS One. 2015;10:e0118299.