Evolutionary Ecology

, Volume 29, Issue 3, pp 419–435 | Cite as

Long corollas as nectar barriers in Lonicera implexa: interactions between corolla tube length and nectar volume

  • Amparo Lázaro
  • Clara Vignolo
  • Luis Santamaría
Original Paper


Long corollas are a classical example of nectar barriers, because they prevent undesired visitors from consuming the reward intended for more effective pollinators. As the investment in nectar barriers increases, flower attractiveness and nectar rewards may also increase to maintain loyal visitation of most effective pollinators; and flowers may become more prone to nectar robbing. We evaluated the effect of nectar barriers (corolla tube length), two related traits (nectar volume and upper lip size) and the associated risk of nectar robbing, on the fecundity of Lonicera implexa plants from three populations differing in the abundance of its most efficient pollinator, the hummingbird hawkmoth Macroglossum stellatarum. Corolla tube length varied most among individuals within populations (45–46 % of total variance) and inflorescences within individuals (23–32 %), and showed little variation among populations (0.2–11 %). Longer corolla tubes were always associated with larger nectar volumes and larger upper lips, although the strength of the relationships varied across populations and years. Robbing frequency increased with corolla tube length, decreased with nectar volume and upper lip size, and its weak effects on fecundity were predominantly positive. Plant fecundity peaked at two different optima: long corollas with little nectar and short corollas with abundant nectar. However, the exact shape of the interaction between corolla length and nectar volume, as well as the combination of traits showing the highest fecundity, differed between populations and years. This variation could be explained by among-population differences in pollinator assemblages, and inter-annual changes in resources dedicated to reproduction. Our study shows that large nectar volumes can modulate the effect of corolla length as a nectar barrier, and that the combination of these two traits that maximises fecundity may be related to the identity of pollinators within each population.


Corolla tube length Fecundity Floral display Nectar robbing Nectar volume Non-additive effects Selective pressures 



This work was supported by a ‘Juan de la Cierva’ contract (Spanish Ministry of Economy and Competitiveness) financed to AL. LS received funding from project COLVISPOL (CGL2010-16795, Spanish Ministry of Education).

Supplementary material

10682_2014_9736_MOESM1_ESM.doc (36 kb)
Supplementary material 1 (DOC 35 kb)
10682_2014_9736_MOESM2_ESM.doc (215 kb)
Supplementary material 2 (DOC 208 kb)


  1. Arizmendi MC, Domínguez CA, Dirzo R (1996) The role of an avian nectar robber and of hummingbird pollinators in the reproduction of two plant species. Funct Ecol 10:119–127CrossRefGoogle Scholar
  2. Castellanos MC, Wilson P, Thompson JD (2004) ‘Anti-bee’ and ‘pro-bird’ changes during the evolution of hummingbird pollination in Penstemon flowers. J Evol Biol 17:876–885CrossRefPubMedGoogle Scholar
  3. Castro S, Silveira P, Navarro L (2008) Consequences of nectar robbing for the fitness of a threatened plant species. Plant Ecol 199:201–208CrossRefGoogle Scholar
  4. Castro S, Silveira P, Navarro L (2009) Floral traits variation, pollinator attraction and nectar robbers in Polygala vayredae (Polygalaceae). Ecol Res 24:47–55CrossRefGoogle Scholar
  5. Castro S, Loureiro J, Ferrero V, Silveira P, Navarro L (2013) So many visitors and so few pollinators: variation in insect frequency and effectiveness governs the reproductive success of an endemic milkwort. Plant Ecol 214:1233–1245CrossRefGoogle Scholar
  6. Conner JK (2002) Genetic mechanisms of floral trait correlations in a natural population. Nature 420:407–410CrossRefPubMedGoogle Scholar
  7. Cresswell JE (1999) The influence of nectar and pollen availability on pollen transfer by individual flowers of oil-seed rape (Brassica napus) when pollinated by bumblebees (Bombus lapidarius). J Ecol 87:670–677CrossRefGoogle Scholar
  8. Cresswell JE, Galen C (1991) Frequency dependent selection and adaptive surfaces for floral trait combinations: the pollination of Polemonium viscosum. Am Nat 138:1342–1353CrossRefGoogle Scholar
  9. Devesa JA, Ruíz T (2007) Lonicera. CLV Caprifoliaceae-Caprifoliae. In: Flora Iberica, vol. XV Rubiaceae-Dipsacaceae. Devesa, J. A., Gonzalo, R. and Herrero, A. (eds). Dpto. de Publicaciones del CSIC, pp: 167–190Google Scholar
  10. Ellis AG, Johnson SD (2010) Gender differences in the effects of floral spur length manipulation on fitness in a hermaphrodite orchid. Int J Plant Sci 171:1010–1019CrossRefGoogle Scholar
  11. Galen C (1996) Rates of floral evolution: adaptation to bumblebee pollination in an alpine wildflower, Polemonium viscosum. Evolution 50:120–125CrossRefGoogle Scholar
  12. Galen C (1999) Flowers and enemies: predation by nectar-thieving ants in relation to variation in floral form of an alpine wildflower, Polemonium viscosum. Oikos 85:426–434CrossRefGoogle Scholar
  13. Galen C, Cuba J (2001) Down the tube: pollinators, predators, and the evolution of flower shape in the alpine skypilot, Polemonium viscosum. Evolution 55:1963–1971CrossRefPubMedGoogle Scholar
  14. Gómez JM, Bosch J, Perfectti F, Fernandez JD, Abdelaziz M, Camacho JPM (2008) Association between floral traits and rewards in Erysimum mediohispanicum (Brassicaceae). Ann Bot 101:1413–1420CrossRefPubMedCentralPubMedGoogle Scholar
  15. Goyret J, Markwell PM, Raguso RA (2007) The effect of decoupling olfactory and visual stimuli on the foraging behavior of Manduca sexta. J Exp Biol 210:1398–1405CrossRefPubMedGoogle Scholar
  16. Guitian P, Guitián J, Navarro L (1993) Pollen transfer and diurnal versus nocturnal pollination in Lonicera etrusca 14:219–227Google Scholar
  17. Herrera CM (1990) The adaptedness of the floral phenotype in a relict endemic, hawkmoth-pollinated violet. 2, Patterns of variation among disjunct populations. Biol J Linn Soc 40:275–291CrossRefGoogle Scholar
  18. Higashi S, Ohara M, Arai H, Matsuo K (1988) Robber-like pollinators: overwintered queen bumblebees foraging on Corydalis ambigua. Ecol Entomol 13:411–418CrossRefGoogle Scholar
  19. Inoue MN, Ushijima J, Yokoyama J (2007) Effect of Weiggela hortensis (Caprifoliaceae) floral morphology on pollinator behavior. Plant Species Biol 22:77–86CrossRefGoogle Scholar
  20. Inouye D (1980) The terminology of floral lacerny. Ecology 61:1251–12253CrossRefGoogle Scholar
  21. Irwin RE (2006) The consequences of direct versus indirect species interactions to selection on traits: Pollination and nectar robbing in Ipomopsis aggregata. Am Nat 167:315–328Google Scholar
  22. Irwin RE, Brody AK (1999) Nectar-robbing bumble bees reduce the fitness of Ipomopsis aggregata (Polemoniaceae). Ecology 80:1703–1712CrossRefGoogle Scholar
  23. Irwin RE, Brody AK, Waser NM (2001) The impact of floral lacerny on individuals, populations and communities. Oecologia 129:161–168CrossRefGoogle Scholar
  24. Jordano P (1990) Biología de la reproducción de tres especies del género Lonicera (Caprifoliaceae) en la Sierra de Cazorla. An Jard Bot Madr 48:31–52Google Scholar
  25. Kaczorowski RL, Gardener MC, Holtsford TP (2005) Nectar traits in Nicotiana section Alatae (Solanaceae) in relation to floral traits, pollinators and mating system. Am J Bot 92:1270–1283CrossRefPubMedGoogle Scholar
  26. Kaczorowski RL, Juenguer TE, Holtsford TP (2008) Heritability and correlation structure of nectar and floral morphology traits in Nicotiana alata. Evolution 62:1738–1750CrossRefPubMedGoogle Scholar
  27. Kelber A (1996) Colour learning in the hawkmoth Macroglossum stellatarum. The J Exp Biol 199:1127–1131Google Scholar
  28. Kelly D (1994) The evolutionary ecology of mast seeding. Trends Ecol Evol 9:465–470CrossRefPubMedGoogle Scholar
  29. Lara C, Ornelas JF (2001) Preferential nectar robbing of flowers with long corollas: experimental studies of two hummingbird species visiting three plant species. Oecologia 128:263–273Google Scholar
  30. Laverty TM (1980) The flower visiting behaviour of bumblebees: floral complexity and learning. Can J Zool 58:1324–1335CrossRefGoogle Scholar
  31. Lázaro A, Nielsen A, Totland Ø (2010) Factors related to the inter-annual variation in plants’ pollination generalization levels within a community. Oikos 119:825–834CrossRefGoogle Scholar
  32. Lázaro A, Santamaría L (unpublished data) Flower visitor-selection on floral integration and the covariation of floral traits in three contrasting populations of Lonicera implexa Google Scholar
  33. Maad J, Alexandersson R (2004) Variable selection in Platanthera bifolia (Orchidaceae): phenotypic selection differed between sex functions in a drough year. J Evol Biol 17:642–650CrossRefPubMedGoogle Scholar
  34. Maloof JE, Inouye DW (2000) Are nectar robbers cheaters or mutualists? Ecology 81:2651–2661CrossRefGoogle Scholar
  35. Martins DJ, Johnson SD (2013) Interactions between hawkmoths and flowering plants in East Africa: polyphagy and evolutionary specialization in an ecological context. Biol J Linn Soc 110:199–213CrossRefGoogle Scholar
  36. McDade LA, Kinsman S (1980) The impact of floral parasitism in two neotropical hummingbird-pollinated plant species. Evolution 34:944–958CrossRefGoogle Scholar
  37. Miller RB (1981) Hawkmoths and the geographic patterns of floral variation in Aquilegia caerulea. Evolution 35:763–774CrossRefGoogle Scholar
  38. Morris WF (1996) Mutualism denied? Nectar-robbing bumble bees do not reduce female or male success of bluebells. Ecology 12:1451–1462CrossRefGoogle Scholar
  39. Navarro L (2000) Pollination ecology of Anthyllis vulneraria subsp. vulgaris (Fabaceae): nectar robbers as pollinators. Am J Bot 87:980–985CrossRefPubMedGoogle Scholar
  40. Navarro L, Medel R (2009) Relationship between floral tube length and nectar robbing in Duranta erecta L. (Verbenaceae). Biol J Linn Soc 96:392–398CrossRefGoogle Scholar
  41. Price MV, Waser NM, Irwin RE, Campbell DR, Brody AK (2005) Temporal and spatial variation in pollination of a montane herb: a seven-year study. Ecology 86:2106–2116CrossRefGoogle Scholar
  42. R Development Core Team. 2008. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0, URL http://www.RprojectOrg
  43. Real LA, Rathcke BJ (1991) Individual variation in nectar production and its effect on fitness in Kalmia latifolia. Ecology 72:149–155CrossRefGoogle Scholar
  44. Reznick D (1985) Costs of reproduction: an evaluation of the empirical evidence. _. Oikos 44:257–267CrossRefGoogle Scholar
  45. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  46. Riffell JA, Alarcón R, Abrell L, Davidowitz G, Bronstein JL, Hildebrand JG (2008) Behavioral consequences of innate preferences and olfactory learning in hawkmoth–flower interactions. PNAS 105:3404–3409CrossRefPubMedCentralPubMedGoogle Scholar
  47. Rodríguez-Gironés MA, Santamaría L (2006) Models of optimal foraging and resource partitioning: deep corollas for long tongues. Behav Ecol 17:905–910CrossRefGoogle Scholar
  48. Rodríguez-Gironés MA, Santamaría L (2007) Resource competition, character displacement, and the evolution of deep corolla tubes. Am Nat 170:456–464CrossRefGoogle Scholar
  49. Rodríguez-Gironés MA, Santamaría L (2010) How foraging behaviour and resource partioning can drive the evolution of flowers and the structure of pollination networks. Open J Ecol 3:1–11CrossRefGoogle Scholar
  50. Sandring S, Ågren J (2009) pollinator-mediated selection on floral display and flowering time in the perennial herb Arabidopsis lyrata. Evolution 63:1292–1300CrossRefPubMedGoogle Scholar
  51. Schaefer MH, Schaefer V, Levey DJ (2004) How plant-animal interactions signal new insights in communication. Trends Ecol Evol 19:577–584CrossRefGoogle Scholar
  52. Sletvold N, Grindeland JM, Ågren J (2010) Pollinator mediated floral display, spur length and flowering phenology in the deceptive orchid Dactylorhiza lapponica. New Phytol 188:385–392CrossRefPubMedGoogle Scholar
  53. Thomson JD, McKenna MA, Cruzan MB (1989) Temporal patterns of nectar and pollen production in Aralia Hispida: implications for reproductive success. Ecology 70:1061–1068CrossRefGoogle Scholar
  54. Totland Ø (2001) Environment-dependent pollen limitation and selection ofn floral traits in an alpine species. Ecology 82:2233–2244CrossRefGoogle Scholar
  55. Totland Ø, Eide W (1999) Environmentally-dependent pollen limitation on seed production in alpine Ranunculus acris. Ecoscience 6:173–179Google Scholar
  56. Traveset A, Wilson MF, Sabag C (1998) Effect of nectar-robbing birds on fruit set of Fuchsia magellanica in Tierra del Fuego: a disrupted mutualism. Funct Ecol 12:459–464CrossRefGoogle Scholar
  57. Waddington KD (2001) Subjective evaluation and choice behavior by nectar- and pollen-collecting bees. In: Cognitive ecology of pollination: animal behaviour and floral evolution. Chittka L, Thomson JD (eds), pp 41–60Google Scholar
  58. Wang Q, Li Y, Pu X, Zhu L, Tang Z, Liu Q (2013) Pollinators and nectar robbers cause directional selection for large spur circle in Impatiens oxyanthera (Balsaminaceae). Plant Syst Evol 299:1263–1274CrossRefGoogle Scholar
  59. Wolfe LM (1997) Differential flower herbivory and gall formation on males and females of Neea psychotrioides, a dioecious tree. Biotropica 29:169–174CrossRefGoogle Scholar
  60. Zimmerman M (1983) Plant reproduction and optimal foraging: experimental nectar manipulations in Delphinium nelsonii. Oikos 41:57–63CrossRefGoogle Scholar
  61. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Amparo Lázaro
    • 1
  • Clara Vignolo
    • 1
  • Luis Santamaría
    • 2
  1. 1.Mediterranean Institute for Advanced Studies (IMEDEA)UIB-CSICEsporlesSpain
  2. 2.Doñana Biological StationSevilleSpain

Personalised recommendations