Evolutionary Ecology

, Volume 21, Issue 3, pp 395–409 | Cite as

Flowering phenology of Ulex europaeus: ecological consequences of variation within and among populations

  • Michèle Tarayre
  • Gillianne Bowman
  • Agnès Schermann-Legionnet
  • Myriam Barat
  • Anne Atlan
Original Paper

Abstract

Reproductive phenology of gorse (Ulex europaeus L., Genisteae, Fabaceae) is unusual in that the onset and duration of flowering vary greatly among individuals within populations: some plants initiate flowering in autumn or winter and continue flowering through spring, others initiate flowering in early spring. To understand the origin of this diversity and its ecological consequences, we investigated flowering phenology of randomly sampled individuals from five different natural populations in Brittany (France). Reproductive success was evaluated for individuals with contrasting flowering patterns, from 16 natural populations. Flower production, pod production, seed production and seed predation were estimated. Plants initiating flowering in spring produced larger numbers of flowers and pods over a shorter period than plants flowering from winter to spring, which produced few flowers and pods at a time but over a longer period. Pod production of long-flowering plants did not differ significantly between winter and spring, but their pods were more intensively attacked by seed predators in spring than in winter. We discuss our results in relation to biotic and abiotic parameters. We postulate that long-flowering can be interpreted as a bet-hedging strategy, spreading the risk of pod failure (rotting or freezing) in winter and of seed predation in spring.

Keywords

Ulex europaeus-Apion ulicis Flowering phenology Asynchrony Seed predation Bet-hedging 

References

  1. Augspurger CK (1981) Reproductive synchrony of a tropical shrub: experimental studies on effects of pollinators and seed predators on Hybanthus prunifolius (Violaceae). Ecology 62:775–788CrossRefGoogle Scholar
  2. Bawa KS (1983) Patterns of flowering in tropical plants. In: Jones CE, Little RJU (eds) A handbook of experimental pollination ecology. Van Nostrand pp 394–410Google Scholar
  3. Bolmgren K, Eriksson O, Linder HP (2003) Contrasting flowering phenology and species richness in abiotically and biotically pollinated angiosperms. Evolution 57:2001–2011PubMedGoogle Scholar
  4. Brody AK (1997) Effects of pollinators, herbivores, and seed predators on flowering phenology. Ecology 78:1624–1631CrossRefGoogle Scholar
  5. Bronstein JL, Gouyon PH, Gliddon C, Kjellberg F, Michaloud G (1990) The ecological consequences of flowering asynchrony in monoecious figs: a simulation study. Ecology 71:2145–2156CrossRefGoogle Scholar
  6. Carroll SP, Loye JE (1987) Specialization of Jadera Species (Hemiptera: Rhopalidae) on the seeds of Sapindaceae (Sapindales), and coevolutionary responses of defense and attack. Ann Entomol Soc Am 80:373–378Google Scholar
  7. Chater EH (1931) A contribution to the study of the natural control of gorse. Bull Entomol Res 22:225–235CrossRefGoogle Scholar
  8. Cochran WG (1977) Sampling techniques, 3rd ed. Wiley,New YorkGoogle Scholar
  9. Cubas P (1999) Ulex L. In: Talavera S, Aedo C, Castroviejo S, Romero Zarco C, Saez L, Salgueiro FJ, Velayos M (eds) Flora Iberica: Plantas vasculares de la Península Iberica e Islas Baleares, vol VII (I). Real Jardín Botánico CSIC, Madrid,pp 212–239Google Scholar
  10. Davies WM (1928) The bionomics of Apion ulicis Forst. (gorse weevil) with special reference to its role in the control of Ulex europaeus in New Zealand. Ann Appl Biol 15:263–386CrossRefGoogle Scholar
  11. Des Abbayes H, Claustres G, Corillon R Corillon R, Dupont P (1971) Flore et végétation du Massif armoricain. Presse Universitaire de Bretagne, Saint-BrieucGoogle Scholar
  12. Dieringer G (1991) Variation in individual flowering time and reproductive success of Agalinis strictifolia (Scrophulariaceae). Am J Bot 78:497–503CrossRefGoogle Scholar
  13. Ehret JM (1990) Les Apions de France: clés d’identification commentées (Coleoptera Curculionidae Apioninae). Bull Mens Soc Linn Lyon 59:209–292Google Scholar
  14. Ellner S, Sasaki A (1996) Patterns of genetic polymorphism maintained by fluctuating selection with overlapping generations. Theor Pop Biol 50:31–65CrossRefGoogle Scholar
  15. Endler JA (1986) Natural selection in the wild. Princeton University Press Princeton, New JerseyGoogle Scholar
  16. English-Loeb GM, Karban R (1992) Consequences of variation in flowering phenology for seed herbivory and reproductive success in Erigeron glaucus (Compositae). Oecologia 89:588–595Google Scholar
  17. Forup ML, Memmott J (2005) The relationship between abundances of bumblebees and honeybees in a natural habitat. Ecol Entomol 30:47–57CrossRefGoogle Scholar
  18. Frank SA, Slatkin M (1990) Evolution in a variable environment. Am Nat 136:244–260CrossRefGoogle Scholar
  19. Gentry AH (1974) Flowering phenology and diversity in tropical Bignoniaceae. Biotropica 6:64–68CrossRefGoogle Scholar
  20. Gillespie JH (1991) The causes of molecular evolution. Oxford Univ. Press Oxford, UKGoogle Scholar
  21. Green TW, Palmbald IG (1975) Effects of insect seed predators on Astragalus cibarius and Astragalus utahensis. Ecology 56:1435–1440CrossRefGoogle Scholar
  22. Haldane JBS, Jayakar SD (1963) Polymorphism due to selection of varying direction. J Genet 58:237–242CrossRefGoogle Scholar
  23. Hallé F (2004) Architecture de Plantes. JPC éditions, Paris, FranceGoogle Scholar
  24. Hendry AP, Day T (2005) Population structure attributable to reproductive time: isolation by time and adaptation by time. Mol Ecol 14:901–916PubMedCrossRefGoogle Scholar
  25. Herrera CM (1992) Individual flowering time and maternal fecundity in a summer-flowering Mediterranean shrub: making the right prediction for the wrong reason. Acta Oecol 13:13–24Google Scholar
  26. Herrera J (1999) Fecundity above the species level: ovule number and brood size in the Genisteae (Fabaceae: Papilionoideae). Int J Plant Sci 160(5):887–896PubMedCrossRefGoogle Scholar
  27. Hill RL, Sandrey RA (1986) The costs and benefits of gorse. Proc.-39th N.Z. Weed and Pest Control conf. Hasting, New Zealand, pp 70–73Google Scholar
  28. Hill RL, Gourlay AH, Martin L (1991) Seasonal and geographic variation in the predation of gorse seed, Ulex europeaus L., by seed weevil Apion ulicis Forst. N Zeal J Zool 18:37–43Google Scholar
  29. Hill RL, Gourlay AH, Barker RJ (2001) Survival of Ulex europaeus seeds in the soil at three sites in New Zealand. N Zeal J Bot 39:235–244Google Scholar
  30. Ims RA (1990) The ecology and evolution of reproductive synchrony. Trends Ecol Evol 5:135–140CrossRefGoogle Scholar
  31. Janzen DH 1971 Seed predation by animals. Ann Rev Ecol Syst 2:465–492CrossRefGoogle Scholar
  32. Kelly MG, Levin DA 2000 Directional selection on initial flowering date in Phlox drummondii (Polemoniaceae). Am J Bot 87:382–391PubMedCrossRefGoogle Scholar
  33. Kelly D, Harrison AL, Lee WG, Payton IJ, Wilson PR, Schauber EM (2000) Predator satiation and extreme mast seeding in 11 species of Chionochloa (Poaceae). Oikos 90:477–488CrossRefGoogle Scholar
  34. Kochmer JP, Handel SN (1986) Constraints and competition in the evolution of flowering phenology. Ecol Monogr 56:303–325CrossRefGoogle Scholar
  35. Lacey EP, Roach DA, Herr D, Kincaid S, Perrott R (2003) Multigenerational effects of flowering and fruiting phenology in Plantago lanceolata. Ecology 84(9):2462–2475Google Scholar
  36. Mahoro S (2002) Individual flowering schedule, fruit set, and flower and seed predation in Vaccinium hirtum Thunb. (Ericaceae). Can J Bot 80:82–92CrossRefGoogle Scholar
  37. Markin GP, Yoshioka E (1996) The phenology and growth rates of the weed gorse (Ulex europaeus) in Hawaii. Newsletter Hawaiian Bot Soc 35(3–4):45–50Google Scholar
  38. Marquis RJ (1988) Phenological variation in the neotropical understory shrub Piper arieianum: causes and consequences. Ecology 69:1552–1565CrossRefGoogle Scholar
  39. McGuire AD, Armbruster WS (1991) An experimental test for reproductive interactions between two sequentially blooming Saxifraga species (Saxifragaceae). Am J Bot 78:214–219CrossRefGoogle Scholar
  40. Meagher TR, Delph LF (2001) Individual flower demography, floral phenology and floral display size in Silene latifolia. Evol Ecol Res 3:845–860Google Scholar
  41. Miller D (1970) Biological control of weeds in New Zealand. J Agr 24:123–129Google Scholar
  42. Misset MT (1992) Meiotic abnormalities during microsporogenesis and low fertility in prostrate ecotypes of Ulex species (Papilionoideae, Genisteae). Can J Bot 70(6):1223–1227Google Scholar
  43. Moss GR (1959) Gorse: a weed problem on thousands of acres of farm land. N Zeal J Agr Res 100:561–567Google Scholar
  44. Nakagawa H, Yamagishi J, Miyamoto N, Motoyama M, Yano M, Nemoto K (2005) Flowering response of rice to photoperiod and temperature: a QTL analysis using a phenological model. Theor Appl Genet 110(4):778–786PubMedCrossRefGoogle Scholar
  45. New DA (1984) Ulex control in Chile: a national problem. Visit report, July 1984, 7 ppGoogle Scholar
  46. Norembuena H, Piper G (2000) Impact of Apion ulicis Forster on Ulex europaeus L. seed dispersal. Biol Control 17:267–271CrossRefGoogle Scholar
  47. Ollerton J, Lack AJ (1992) Flowering phenology: an example of relaxation of natural selection? Trends Ecol Evol 7(8): 274–276CrossRefGoogle Scholar
  48. Ollerton J, Lack AJ (1998) Relationships between flowering phenology, plant size and reproductive success in Lotus corniculatus (Fabaceae). Plant Ecol 139:35–47CrossRefGoogle Scholar
  49. Pandurang V, Pandurang S (1984) Sampling theory of surveys with applications. Publisher: Ames, Iowa, USA: New Delhi, India : Iowa State University Press, Indian Soc Agr StatGoogle Scholar
  50. Pico FX, Retana J (2001) The flowering pattern of the perennial herb Lobularia maritima: an unusual case in the Mediterranean basin. Acta Oecol 22:209–217CrossRefGoogle Scholar
  51. Post E, Levin SA, Iwasa Y, Stenseth NC (2001) Reproductive asynchrony increases with environmental disturbance. Evolution 55:830–834PubMedCrossRefGoogle Scholar
  52. Primack RB (1980) Variation in the phenology of natural populations of montane shrubs in New Zealand. J Ecol 68:849–862CrossRefGoogle Scholar
  53. Putterill J, Laurie R, Macknight R (2004) It’s time to flower: the genetic control of flowering time. BioEssays 26(4):363–373PubMedCrossRefGoogle Scholar
  54. Rathcke B, Lacey EP (1985) Phenological patterns of terrestrial plants. Ann Rev Ecol Syst 16:179–214CrossRefGoogle Scholar
  55. Schemske DW, Willson MF, Melampy MN, Miller LJ, Verner L, Schemske KM, Best LB (1978) Flowering ecology of some spring woodland herbs. Ecology 59:351–366CrossRefGoogle Scholar
  56. Schröder D, Zwölfer H (1970) Studies of insects associated with gorse, Ulex europaeus L. Proc Int Symp Biol Contr Weeds, Simmons FJ (ed) pp 55–58Google Scholar
  57. Simons AM, Johnston MO (1997) Developmental instability as a bet-hedging strategy. Oikos 80:401–406CrossRefGoogle Scholar
  58. Silva C, Garcia-Mas J, Sanchez AM, Arus P, Oliveira MM (2005) Looking into flowering time in almond (Prunus dulcis (Mill) D.A. Webb): the candidate gene approach. Theor Appl Genet 110(5):959–968PubMedCrossRefGoogle Scholar
  59. Skipper EG (1922) The ecology of gorse (Ulex) with special reference to the growth-forms on Hindhead Common. J Ecol 10:24–52CrossRefGoogle Scholar
  60. Slatkin M (1974) Hedging one’s evolutionary bets. Nature 250:704–705Google Scholar
  61. Widén B 1991 Phenotypic selection on flowering phenology in Senecio integrifolius, a perennial herb. Oikos 61:205–215CrossRefGoogle Scholar
  62. Wolfe LM, Burns JL (2001) A rare continual flowering strategy and its influence of offspring quality in a gynodioecious plant. Am J Bot 88:1419–1423CrossRefGoogle Scholar
  63. Wright JW, Meagher TR (2003) Pollination and seed predation drive flowering phenology in Silene latifolia (Caryophyllaceae). Ecology 84:2062–2073Google Scholar
  64. Yin X, Struik PC, van Eeuwijk FA, Stam P, Tang J (2005) QTL analysis and QTL-based prediction of flowering phenology in recombinant inbred lines of barley. J Exp Bot 56:967–976PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Michèle Tarayre
    • 1
  • Gillianne Bowman
    • 2
  • Agnès Schermann-Legionnet
    • 1
  • Myriam Barat
    • 1
  • Anne Atlan
    • 1
  1. 1.Laboratoire “ECOBIO”-UMR 6553Université de Rennes 1Rennes CedexFrance
  2. 2.Institut für UmweltwissenschaftenUniversität ZürichZürichSwitzerland

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