Anales del Jardín Botánico de Madrid, Vol 70, No 1 (2013)

Flowering patterns of Thymelaea velutina at the extremes of an altitudinal gradient


https://doi.org/10.3989/ajbm.2307

M. Carmen de la Bandera
Universitat de les Illes Balears, Spain

Anna Traveset
Institut Mediterrani d’Estudis Avançats (CSIC-UIB), Spain

Abstract


Environmental variability may cause changes in flowering phenology affecting plant reproductive success. Plasticity in phenological processes may guarantee species survival under new environmental conditions, such as those caused by global warming. Here we examined the flowering patterns of Thymelaea velutina (Thymelaeaceae), a dioecious shrub endemic to the Balearic Islands. We compared the two contrasting habitats where the species occurs: coastal dunes at sea level and mountain areas (c. 1200 m a.s.l.). We determined the relationship between three components of flowering phenology: initial date, flower duration, and synchrony, and assessed their association with traits describing plant size and fecundity. The increase in altitude results into a delayed flowering initiation and a shorter flowering period. In both habitats, male plants flowered earlier and for longer periods than females. At the mountain site, fruit set was associated to flower initiation, so that plants flowering earlier produced greater proportions of fruits. By contrast, fruit set at the dune site did not depend upon either flower initiation or flowering period; here, larger plants had longer flowering periods, though not necessarily produced more flowers and did not set more fruits than smaller plants. We attribute the differences in flowering patterns at different altitudes to phenotypic plasticity of the species; it is adapted to mountain conditions delaying the flowering period (probably adjusting it to the insect abundance at this altitude). Moreover, shortening of the flowering period may be also advantageous to reduce the stressful effects of higher temperature, radiation and drought that occur later in the summer.

Keywords


altitudinal variation; flowering phenology; reproductive success; Balearic Islands; Thymelaeaceae

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References


Aerts, R., Cornelissen, J.H.C. & Dorrepal, E. 2006. Plant performance in a warmer world: General responses of plants from cold, northern biomes and the importance of winter and spring events. Plant Ecology 182: 65-77.

Aizen, M.A. 2003. Influences of animal pollination and seed dispersal on winter flowering in a temperate mistletoe. Ecology 84: 2613-2627. http://dx.doi.org/10.1890/02-0521

Albert, M.J., Iriondo, J.M., Escudero, A. & Torres, E. 2008. Dissecting componets of flowering patterns: size effects on female fitness. Botanical Journal of the Linnean Society 156: 227-236. http://dx.doi.org/10.1111/j.1095-8339.2007.00735.x

Alomar, G., Mus, M. & Rosselló, J.A. 1997. Flora endèmica de les Balears. Consell Insular de Mallorca, FODESMA. Palma.

Arft, A.M., Walker, M.D., Gurevitch, J. et al. 1999. Response patterns of tundra plant species to experimental warming: a meta-analysis of the International Tundra Experiment. Ecological Monographs 69: 491-511.

Arroyo, J. 1990a. Ritmos climáticos y de floración en matorrales del SW de España. Lagascalia 16: 25-50.

Arroyo, J. 1990b. Geographic variation of flowering phenology in twenty six common shrubs in SW Spain. Flora 184: 43-49.

Arroyo, J. 1990c. Spatial variation of flowering phenology in the Mediterranean shrublands of Southern Spain. Israel Journal of Botany 39: 249-262.

Arroyo, M.T.K., Armesto, J.J. & Villagran, C. 1981. Plant phenological patterns in the high Andean Cordillera of Central Chile. Journal of Ecology 69: 205-223. http://dx.doi.org/10.2307/2259826

Augspurger, C.K. 1983. Phenology, flowering synchrony, and fruit set of six neotropical shrubs. Biotropica 15: 257-267. http://dx.doi.org/10.2307/2387650

Bawa, K.S. 1980. Evolution of dioecy in flowering plants. Annual Review of Ecology and Systematics 11: 15-19. http://dx.doi.org/10.1146/annurev.es.11.110180.000311

Bishop, J.G. & Schemske, D.W. 1998. Variation in flowering phenology and its consequences for Lupines colonizing mount St. Helens. Ecology 79: 534-546. http://dx.doi.org/10.1890/0012-9658(1998)079[0534:VIFPAI]2.0.CO;2

Bolmgren, K. & Lönnberg, K. 2005. Herbarium data reveal an association between fleshy fruits type and earlier flowering time. International Journal of Plant Sciences 166: 663-670. http://dx.doi.org/10.1086/430097

Buide, M.L., Díaz-Peromingo, J.A. & Guitián, J. 2002. Flowering phenology and female success in Silene acutifolia Link ex Rohrb. Plant Ecology 163: 93-103. http://dx.doi.org/10.1023/A:1020356706052

Bullock, S.H., & Bawa, K.S. 1981. Sexual dimorphism and the annual flowering patterns in Jacaratia dolichaula (D. Smith) Woodson (Caricaeae) in a Costa Rican rain forest. Ecology 62: 1494-1504. http://dx.doi.org/10.2307/1941506

Cleland, E., Chiariello, N., Loarie, S., Mooney, H. & Field, C. 2006. Diverse responses of phenology to global chages in a grassland ecosystem. Proceedings of the National Academy of Sciences, USA 103: 13740-13744. http://dx.doi.org/10.1073/pnas.0600815103 PMid:16954189 PMCid:PMC1560087

De la Bandera, M.C. & Traveset, A. 2006a. Breeding system and spatial variation in the pollination biology of the heterocarpic Thymelaea velutina (Thymelaeaceae). Plant Systematics and Evolution 257: 9-23. http://dx.doi.org/10.1007/s00606-005-0380-y

De la Bandera, M.C. & Traveset, A. 2006b. Reproductive ecology of Thymelaea velutina (Thymelaeaceae). Factors contributing to the maintenance of heterocarpy. Plant Systematics and Evolution 256: 97-112. http://dx.doi.org/10.1007/s00606-005-0355-z

De la Bandera, M.C., Traveset, A., Valladares, F. & Gulías, J. 2008. Gender, season and habitat: Patterns of variation in photosynthetic activity, growth and fecundity in Thymelaea velutina. Acta Oecologica 34: 294-302. http://dx.doi.org/10.1016/j.actao.2008.06.002

Dunne, J.A., Harte, J. & Taylor, K.J. 2003. Subalpine meadow flowering phenology responses to climate change: integrating experimental and gradient methods. Ecological Monographs 73: 69-86. http://dx.doi.org/10.1890/0012-9615(2003)073[0069:SMFPRT]2.0.CO;2

Ehrlen, J. 1991. Why do plants produce surplus flowers? A reserve-ovary model. The American Naturalist 138: 918-923. http://dx.doi.org/10.1086/285260

Ehrlén, J. & Münzbergová, Z. 2009. Timing of flowering: opposed selection on different fitness components and traits covariation. The American Naturalist 173: 819-830. http://dx.doi.org/10.1086/598492 PMid:19335224

Formaciari, M., Galán, C., Mediavilla, A., Domínguez, E. & Romano, B. 2000. Aeropalinological and phenological study in two different Mediterranean olive areas: Córdoba (Spain) and Perugia (Italy). Plant Biosystems 134: 199-204. http://dx.doi.org/10.1080/11263500012331358474

Frankie, G.W. Baker, H.G. & Opler, P.A. 1974. Comparative phenological studies of trees in tropical wet and dry forests in the lowlands of Costa Rica. Ecology 62: 881-919. http://dx.doi.org/10.2307/2258961

Galán, C., García-Mozo, H., Vázquez, L., Ruiz, L., Díaz de la Guardia, C. & Trigo, M.M. 2005. Heat requirement for the onset of the Olea europaea L. pollen season in several sites of Andalusia and the effect of the expected future climate change. International Journal of Biometeorology 51: 81-191.

García-Camacho, R. 2009. Evaluación del éxito reproductivo de Armeria caespitosa en el contexto del cambio climático en la alta montaña mediterránea. PhD Thesis. Universidad Juan Carlos I. Madrid.

Giménez-Benavides, I., Escudero, A. & Iriondo, J.M. 2007. Reproductive limits of a late-flowering high-mountain Mediterranean plant along an elevational climate gradient. New Phytologist 173: 367-382. http://dx.doi.org/10.1111/j.1469-8137.2006.01932.x PMid:17204083

Godoy, O., Richardson, D.M., Valladares, F. & Castro-Díez, P. 2009. Flowering phenology of invasive alien plant species compared to native species in three Mediterranean-type ecosystems. Annals of Botany 103: 485-494. http://dx.doi.org/10.1093/aob/mcn232 PMid:19033284 PMCid:PMC2707327

Gómez, J.M. 1993. Phenotypic selection on flowering synchrony in a high mountain plant, Hormathophylla spinosa. (Cruciferae). Journal of Ecology 81: 605-613. http://dx.doi.org/10.2307/2261659

Gordo, O. & Sanz, J.J. 2005. Phenology and climate change: a long-term study in a Mediterranean locality. Oecologia 146: 484-495. http://dx.doi.org/10.1007/s00442-005-0240-z PMid:16170564

Guijarro, J.A. 1986. Contribución a la bioclimatología de Baleares. PhD Thesis. Universitat de les Illes Balears. Palma.

Guitián, J. 1995. Sex ratio, reproductive investment and flowering phenology in dioecious Rhamnus alaternus (Rhamnaceae). Nordic Journal of Botany 15: 139-143. http://dx.doi.org/10.1111/j.1756-1051.1995.tb00130.x

Gulías, J. & Traveset, A 2012. Altitudinal variation in the reproductive performance of the Mediterranean shrub Rhamnus lycioides L. Journal of Plant Ecology 9: 1-7.

Hartmann, H.T. & Whisler, J.E. 1975. Flower production in olive as influenced by various chilling temperature regimes. Journal of the American Society for Horticultural Science 100: 670-674.

Herrera, J. 2005. Flower size variation in Rosmarinus officinalis: individuals, populations and habitats. Annals of Botany 95: 431-437. http://dx.doi.org/10.1093/aob/mci041 PMid:15585545

Hobbs, R.J., Arico, S., Aronson, J. et al. 2006. Novel ecosystems: theoretical and management aspects of the new ecological world order. Global Ecology and Biogeography 15: 1-7. http://dx.doi.org/10.1111/j.1466-822X.2006.00212.x

Jump, A.S. & Pe-uelas, J. 2005. Running to stand still: adaptation and the response of plants to rapad climate change. Ecology Letters 8: 1010-1020. http://dx.doi.org/10.1111/j.1461-0248.2005.00796.x

Kochmer, J.P. & Handel, S.N. 1986. Constraints and competition in the evolution of flowering phenology. Ecological Monographs 6: 303-325. Kozlowski, J. 1992. Optimal allocation of resources to growth and reproduction: implications for age and size maturity. Trends in Ecology and Evolution 7: 15-18.

Lande, R. & Arnold, S. 1983. The measurement of selection on correlated characters. Evolution 37: 1210-1226. http://dx.doi.org/10.2307/2408842

McClure, H.E., 1966. Flowering, fruiting and animals in the canopy of a tropical rain forest. Malaysian Forester 29: 192-203.

McKey, D. 2012. Flowering phenology and mimicry of the rattan Calamus cataneus (Arecaceae) in southern Thailand. Botany 90: 856-865. http://dx.doi.org/10.1139/b2012-058

Michalski, S.G. & Durka, W. 2007. Synchronous pulsed flowering: Analysis of the flowering phenology in Juncus (Juncaceae). Annals of Botany 100: 1271-1285. http://dx.doi.org/10.1093/aob/mcm206 PMid:17881343 PMCid:PMC2759248

Mitchell-Olds, T. & Shaw, R. 1987. Regression analysis of natural selection: statistical inference and biological interpretations. Evolution 41: 1149-1161. http://dx.doi.org/10.2307/2409084

Molau, U. 1993. Relationships between flowering phenology and life-history strategies in tundra plants. Artic and Alpine Research 25: 391-402. http://dx.doi.org/10.2307/1551922

Nickens, T.E. 2007. Walden warming. National Wildlife 45: 36-41.

Nikkanen, T. 2001. Reproductive phenology in a Norway spruce seed orchard. Silva Fennica 35: 39-53.

Ollerton, J. & Lack, A. 1998. Relationships between flowering phenology, plant size and reproductive success in Lotus corniculatus (Fabaceae). Plant Ecology 139: 35-47. http://dx.doi.org/10.1023/A:1009798320049

Orlandi, F., Vázquez, L.M., Ruga, L., Bonofiglio, T., Fornaciari, M, García Mozo, H. Domínguez, E., Romano, E. & Galán, C. 2005. Bioclimatic requirements for olive flowering in two Mediterranean regions located at the same latitude (Andalucia, Spain, and Sicily, Italy). Annals of Agricultural and Environmental Medicine 12: 47-52. PMid:16028866

Parmesan, C. & Yohe, G. 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421: 37–42. http://dx.doi.org/10.1038/nature01286 PMid:12511946

Pedrol, J. 1997. Thymelaea Mill. (nom. cons), In: Castroviejo, S. & al. (eds.), Flora iberica 8: 50-51. Madrid.

Pe-uelas, J., Gordon C., Llorens, L., Nielsen, T., Tietema, A., Beier, C., Bruna, P., Emmett, B., Estiarte, M. & Gorissen, A. 2004. Non-intrusive field experiments show different plant responses to warming and drought among sites, seasons and species in a North-South European gradient. Ecosystems 7: 598-612.

Primack, R.B., Ibá-ez, I., Higuchi, H., Lee, S.D., Miller-Rushing, A.J., Wilson, A.M. & Silander, J.A. Jr. 2009. Spatial and interspecific variability in phenological responses to warming temperatures. Biological Conservation 142: 2569-2577. http://dx.doi.org/10.1016/j.biocon.2009.06.003

Rallo, L. & Martin, G.C. 1991. The role of chilling in releasing olive floral buds from dormancy. Journal of the American Society for Horticultural Science 116: 1058-1062.

Ratchke, B. & Lacey, E.P. 1985. Phenologycal patterns of terrestrial plants. Annual Review of Ecology and Systematics 16: 179-214. http://dx.doi.org/10.1146/annurev.es.16.110185.001143

Reekie, F.G. & Bazzaz, F.A. 1987. Reproductive effort in plants. The American Naturalist 129: 876-919. http://dx.doi.org/10.1086/284681

Root, T,L, MacMynowski, D.P., Mastrandrea, M.D. & Schneider, S.H. 2005. Human-modified temperatures induce species changes: joint attribution. Proceedings of the National Academy of Sciences, USA 102: 7465-7469. PMid:15899975 PMCid:PMC1129055

Sherry, R.A., Zhou, X., Gu, S., Arnone, J.A.III, Shimell, D.S., Verburg, P.S., Wallace, L.L. & Luo, Y. 2007. Divergence of reproductive phenology under climate warming. Proceedings of the National Academy of Sciences, USA 104: 198-202. PMid:17182748 PMCid:PMC1713188

Silim, S.N. & Omanga, P.A. 2001. The response of short-duration pigeonpea lines to variation in temperature under field conditions in Kenya. Field Crops Research 72: 97-108. http://dx.doi.org/10.1016/S0378-4290(01)00167-8

Sola, A.J. & Ehrlén, J. 2007. Vegetative phenology constrains the onset of flowering in the perennial herb Lathyrus vernus. Journal of Ecology 95: 208-216. http://dx.doi.org/10.1111/j.1365-2745.2006.01191.x

Starr, G., Oberbauer, S.F. & Poe, E.W. 2000. Effects on lengthened growing seasonal soil warming on the phenology and physiology of Polygonum bistoria. Global Change Biology 6: 357-369. http://dx.doi.org/10.1046/j.1365-2486.2000.00316.x

Stinson, K.A. 2004. Natural selection favors rapid reproductive phenology in Potentilla pulcherrima (Rosaceae) at opposite ends of a subalpine snowmelt gradient. American Journal of Botany 91: 531-539. http://dx.doi.org/10.3732/ajb.91.4.531 PMid:21653408

Tébar, J. & Llorens, L. 1992. Variations dans la phénologie de trois espèces des communautés xérochaméphytiques de l'Ile de Majorque. Bulletin de la Société Botanique de France 139: 161-174.

Walker, M.D., Ingersol, R.C. & Webber, P.J. 1995. Effects of interannual climate variation on phenology and growth of two alpine forbs. Ecology 76: 1067-1083. http://dx.doi.org/10.2307/1940916

Widén, B. 1991. Environmental and genetic influences on phenology and plant size in a perennial herb, Senecio integrifolius. Canadian Journal of Botany 69: 209-217. http://dx.doi.org/10.1139/b91-029

Williams, J.W. & Jackson, S.T. 2007. Novel climates, no-analog communities, and ecological surprises. Frontiers in Ecology and the Environment 5: 475-482 http://dx.doi.org/10.1890/070037

Willson, M.F. 1983. Plant reproductive ecology. John Wiley. New York.

Wolfe, L.M. & Burns, J.L. 2001. A rare continual flowering strategy and its influence on offspring quality in a gynodioecious plant. American Journal of Botany 88: 1419-1423. http://dx.doi.org/10.2307/3558448 PMid:21669673




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