Advertisement

Oecologia

, Volume 142, Issue 2, pp 212–220 | Cite as

Limitations on reproductive success in endemic Aquilegia viscosa (Ranunculaceae) relative to its widespread congener Aquilegia vulgaris: the interplay of herbivory and pollination

  • Sébastien Lavergne
  • Max Debussche
  • John D. Thompson
Plant Animal Interactions

Abstract

Plant reproduction can be strongly affected by herbivory and different features of pollination ecology, such as pollinator visitation rates and capacity for self-pollination. The purpose of this study is to compare the relative impact of herbivory and pollination on maternal reproductive success in endemic Aquilegia viscosa and its widespread congener Aquilegia vulgaris. We conducted herbivore exclusion experiments in two populations of each species in 2 different years and showed that the maternal fertility of A. viscosa was significantly more limited by floral predation and pre-dispersal seed predation than its widespread congener. In the absence of herbivory, A. viscosa retained significantly lower maternal fertility than A. vulgaris. Experimental pollinations in an insect-free glasshouse showed that the two species have an equal seed/ovule ratio both in the absence of pollinators and in the presence of non-limiting outcross pollination. Pollinator visitation rates were significantly higher in populations of A. vulgaris than in populations of A. viscosa. In addition, path analyses showed that spur length, an important trait for pollinator attraction in Aquilegia, and, indirectly sepal and petal width, contribute positively to the seed/ovule ratio in A. vulgaris, but not in A. viscosa. These results indicate that maternal fertility of endemic A. viscosa is strongly reduced by flower and seed predation despite low rates of pollinator visitation, and that pollen or resource limitation in the wild may further reduce maternal fertility. Finally, floral trait variation appears to be decoupled from fertility variation in endemic A. viscosa, which possibly constrains the evolution of reproductive traits in this species.

Keywords

Endemism Reproductive success Pollination Herbivory Ranunculaceae 

Notes

Acknowledgements

The authors thank Clélia Sirami, Claire Lagaye and Sophie Dubois for help with field work and Annabelle Dos Santos and Geneviève Debussche for technical help. The CNRS, the European Laboratory (LEA) “Mediterranean ecosystems in a changing world”, the Conservatoire Botanique National Méditerranéen de Porquerolles, l’Institut Français de la Biodiversité and the Région Languedoc-Roussillon provided financial support. The authors thank the Conservatoire-Etudes des Ecosystèmes de Provence and the Conservatoire des Espaces Naturels du Languedoc-Roussillon for logistic help and the Conservatoire Botanique National Méditerranéen for permission to sample plant material.

References

  1. Ågren J (1996) Population size, pollinator limitation, and seed set in the self-incompatible herb Lythrum salicaria. Ecology 77:1779–1790Google Scholar
  2. Affre L, Thompson JD, Debussche M (1995) The reproductive biology of the Mediterranean endemic Cyclamen balearicum. Bot J Linn Soc 118:309–330CrossRefGoogle Scholar
  3. Ayre DJ, Whelan RJ (1989) Factors controlling fruit set in hermaphrotidic plants: studies with Australian Proteaceae. Trends Ecol Evol 4:267–272CrossRefGoogle Scholar
  4. Baker AM, Barrett SCH, Thompson JD (2000) Variation of pollen limitation in the early-flowering Mediterranean geophyte Narcissus assoanus (Amaryllidaceae). Oecologia 124:529–535CrossRefGoogle Scholar
  5. Bevill RL, Louda SM, Stanforth LM (1999) Protection from natural enemies in managing rare plant species. Conserv Biol 13:1323–1331CrossRefGoogle Scholar
  6. Brunet J, Eckert CG (1998) Effects of floral morphology and display on outcrossing in Blue Colombine, Aquilegia caerulea (Ranunculaceae). Funct Ecol 12:596–606CrossRefGoogle Scholar
  7. Burd M (1994) Bateman’s principle and plant reproduction: the role of pollen limitation in fruit and seed set. Bot Rev 60:83–139Google Scholar
  8. Byers DL, Meagher TR (1997) A comparison of demographic characteristics in a rare and a common species of Eupatorium. Ecol Appl 7:519–530Google Scholar
  9. Charpentier A, Grillas P, Thompson JD (2000) The effects of population size limitation on fecundity in mosaic populations of the clonal macrophyte Scirpus martitimus. Am J Bot 87:502–507PubMedGoogle Scholar
  10. Chauvet M (1989) Plantes sauvages menacées de France: bilan et protection. Actes du colloque de Brest. Lavoisier, Cachan, 8–10 October 1987Google Scholar
  11. Cowling RM, Witkowski ETF, Milewski AV, Newbey KR (1994) Taxonomic, edaphic and biological aspects of narrow endemism on matched sites in mediterranean South Africa and Australia. J Biogeogr 21:651–664Google Scholar
  12. Desmet PG, Cowling RM (1999) Biodiversity, habitat and range size of a flora from a winter-rainfall desert in north-western Namaqualand, South Africa. Plant Ecol 142:23–33CrossRefGoogle Scholar
  13. Eckert CG, Schaefer A (1998) Does self-pollination provide reproductive assurance in Aquilegia canadensis (Ranunculaceae)? Am J Bot 85:919–924Google Scholar
  14. Ehrlèn J (1996) Spatiotemporal variation in predispersal seed predation intensity. Oecologia 108:708–713Google Scholar
  15. Eriksson O, Jakobsson A (1998) Abundance, distribution and life-histories of grassland plants: a comparative study of 81 species. J Ecol 86:922–933CrossRefGoogle Scholar
  16. Escarré J, Lepart J, Sans X, Sentuc JJ, Gorse V (1999) Effects of herbivory on the growth and reproduction of Picris hieracioides in the Mediterranean region. J Veg Sci 10:101–110Google Scholar
  17. Fletcher JD, Shipley LA, McShea WJ, Shumway DL (2001) Wildlife herbivory and rare plants: the effects of white-tailed deer, rodents, and insects on growth and survival of Turk’s cap lily. Biol Conserv 101:229–238CrossRefGoogle Scholar
  18. Gaston KJ, Kunin WE (1997) Rare-common differences: an overview. In: Kunin WE, Gaston KJ (eds) The biology of rarity: causes and consequences of rare-common differences. Chapman and Hall, London, pp 12–29Google Scholar
  19. Hedge SG, Ellstrand NC (1999) Life history differences between rare and common flowering plant species of California and the British Isles. Int J Plant Sci 160:1083–1091CrossRefPubMedGoogle Scholar
  20. Herrera CM (2000) Measuring the effects of pollinators and herbivores: evidence for non-additivity in a perennial herb. Ecology 81:2170–2176Google Scholar
  21. Herrera CM, Sanchez-Lafuente A, Medrano M, Guitian J, Cerda X, Rey P (2001) Geographical variation in autonomous self-pollination levels unrelated to pollinator service in Helleborus foetidus (Ranunculaceae). Am J Bot 88:1025–1032PubMedGoogle Scholar
  22. Herrera CM, Medrano M, Rey PJ, Sánchez-Lafuente AM, García MB, Guitián J, Manzaneda AJ (2002) Interaction of pollinators and herbivores on plant fitness suggests a pathway for correlated evolution of mutualism- and antagonism-related traits. Proc Natl Acad Sci USA 99:16823–16828 CrossRefPubMedGoogle Scholar
  23. Hodges SA, Arnold ML (1994) Columbines: a geographically widespread species flock. Proc Natl Acad Sci USA 91:25129–25132Google Scholar
  24. Karron JD (1997) Genetic consequences of different patterns of distribution and abundance. In: Kunin WE, Gaston KJ (eds) The biology of rarity: causes and consequences of rare-common differences. Chapman and Hall, London, pp 174–189Google Scholar
  25. Kéry M, Matthies D, Spillmann H (2000) Reduced fecundity and offspring performance in small populations of the declining grassland plants Primula veris and Gentiana lutea. J Ecol 88:17–30CrossRefGoogle Scholar
  26. Kéry M, Matthies D, Fischer M (2001) The effect of plant population size on the interactions between the rare Gentiana cruciata and its specialized herbivore Maculinea rebeli. J Ecol 89:418–427CrossRefGoogle Scholar
  27. Kunin WE (1997) Population biology and rarity: on the complexity of density dependence in insect–plant interactions. In: Kunin WE, Gaston KJ (eds) The biology of rarity: causes and consequences of rare-common differences. Chapman and Hall, London, pp 150–173Google Scholar
  28. Landa K, Rabinowitz D (1983) Relative preference of Arphia sulphurea (Orthoptera:Acridiae) for sparse and common prairie grasses. Ecology 64:392–395Google Scholar
  29. Lavergne S, Garnier E, Debussche M (2003) Do rock endemic and widespread plant species differ under the Leaf-Height-Seed plant ecology strategy scheme? Ecol Lett 6:398–404Google Scholar
  30. Lavergne S, Thompson JD, Garnier E, Debussche M (2004) The biology and ecology of endemic and widespread plants: a comparative study of trait variation in 20 congeneric pairs. Oikos (in press) Google Scholar
  31. Levri MA, Real LA (1998) The role of resources and pathogens in mediating the mating system of Kalmia latifolia. Ecology 79:1602–1609Google Scholar
  32. Lord JM, Kelly D (1999) Seed production in Festuca novae-zelandiae: the effect of altitude and pre-dispersal predation. N Z J Bot 37:503–509Google Scholar
  33. Louda SM (1982) Limitation of the recruitment of the shrub Haplopappus squarrosus (Asteraceae) by flower and seed feeding insects. J Ecol 70:42–53Google Scholar
  34. Matsumura C, Whashitani I (2000) Effects of population size and pollinator limitation on seed set of Primula sieboldii populations in a fragmented landscape. Ecol Res 15:307–322 CrossRefGoogle Scholar
  35. Médail F, Verlaque R (1997) Ecological characteristics and rarity of endemic plants from southeast France and Corsica: implications for biodiversity conservation. Biol Conserv 80:269–281CrossRefGoogle Scholar
  36. Murray BR, Thrall PH, Gill AM, Nicotra AB (2002) How plant life-history and ecological traits relate to species rarity and commonness at varying spatial scales. Aust Ecol 27:291–310Google Scholar
  37. Robertson AW, Kelly D, Ladley JJ, Sparrow AD (1998) Effects of pollinator loss on endemic New Zealand Mistletoes (Loranthaceae). Conserv Biol 13:499–508CrossRefGoogle Scholar
  38. Saez L, Rossello JA, Vigo J (1998) Catàleg de les plantes vasculars endèmiques, rares o amenaçades de Catalunya. I. Tàxons endèmics. Acta Bot Barcinonensia 45:309–321Google Scholar
  39. SAS (1999) SAS/STAT user’s guide. SAS Institute, Cary, N.C.Google Scholar
  40. Scheidel U, Bruelheide H (1999) Selective slug grazing on montane meadow plants. J Ecol 87:828–838CrossRefGoogle Scholar
  41. Sih A, Baltus M-S (1987) Patch size, pollinator behavior, and pollinator limitation in Catnip. Ecology 68:1679–1690Google Scholar
  42. Silvertown J, Franco M, Pisanty I, Mendoza A (1993) Comparative plant demography—relative importance of life-cycle components to the finite rate of increase in woody and herbaceous perennials. J Ecol 81:465–476Google Scholar
  43. Simon J, Bosch M, Molero J, Blanché C (2001) Conservation biology of the Pyrenean larkspur (Delphinium montanum): a case conflict of plant versus animal conservation? Biol Conserv 98:305–314CrossRefGoogle Scholar
  44. Solbrig OT, Rollins RC (1977) The evolution of autogamy in species of the mustard genus Leavenworthia. Evolution 31:265–281Google Scholar
  45. Strauss SY, Armbruster WS (1997) Linking herbivory and pollination: new perspectives on plant and animal ecology and evolution. Ecology 78:1617–1618Google Scholar
  46. Strauss SY, Conner JK, Rush SL (1996) Foliar herbivory affects floral characters and plant attractiveness to pollinators: implications for male and female fitness. Am Nat 147:1098–1107CrossRefGoogle Scholar
  47. Thompson JD (2001) How do visitation patterns vary among pollinators in relation to floral display and floral design in a generalist pollination system? Oecologia 126:386–394CrossRefGoogle Scholar
  48. Thompson JD, Tarayre M, Gauthier P, Litrico I, Linhart YB (2004) Multiple genetic contributions to plant performance in Thymus vulgaris. J Ecol 92:45–56Google Scholar
  49. Wyatt R (1986) Ecology and evolution of self-pollination in Arenaria uniflora (Caryophyllaceae). J Ecol 74:403–418Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Sébastien Lavergne
    • 1
  • Max Debussche
    • 1
  • John D. Thompson
    • 1
  1. 1.Centre d’Ecologie Fonctionnelle et EvolutiveCNRSMontpellier cedex 5France

Personalised recommendations