Evolutionary Ecology

, Volume 28, Issue 4, pp 669–685 | Cite as

Nectar robbing improves male reproductive success of the endangered Aconitum napellus ssp. lusitanicum

  • Carolin MayerEmail author
  • Charles Dehon
  • Anne-Laure Gauthier
  • Olivier Naveau
  • Cyrielle Rigo
  • Anne-Laure Jacquemart
Original Paper


Nectar robbery is usually thought to impact negatively on the reproductive success of plants, but also neutral or even positive effects have been reported. Very few studies have investigated the effects of nectar robbing on the behaviour of legitimate pollinators so far. Such behavioural changes may lead to the reduction of geitonogamy or to increased pollen movement. We simulated nectar robbing in experimental sites as well as in natural populations of Aconitum napellus ssp. lusitanicum, a rare plant pollinated by long-tongued bumblebees. In an experimental setup, we removed the nectaries of 40 % of the flowers, which is similar to rates of robbing observed in wild populations. Patches of plants with experimentally robbed flowers were compared with control patches containing plants with untreated flowers. We observed pollinator behaviour, mimicked male reproductive success (pollen dispersal) using fluorescent dye, and measured female reproductive success (seed set). The main legitimate visitors were bumblebees while honeybees were often observed robbing nectar. They did so by “base working”, i.e. sliding between tepals. Bumblebees tended to visit fewer flowers per plant and spent less time per single flower when these had been experimentally robbed. This change in behaviour consequently increased the proportion of flowers visited by bumblebees in patches with robbed flowers. Fluorescent dye mimicking pollen flow was dispersed larger distances after pollinators had visited patches with robbed flowers compared to control patches. Average seed set per plant was not affected by nectar robbing. Our results demonstrated that A. napellus does not suffer from nectar robbery but may rather benefit via improved pollen dispersal and thus, male reproductive success. Knowledge on such combined effects of behavioural changes of pollinators due to nectar robbery is important to understand the evolutionary significance of exploiters of such mutualistic relationships between plants and their pollinators.


Base working Bumblebees Fluorescent dye Honeybees Monkshood Nectar robbery Pollen dispersal Pollinator behaviour Seed set 



We would like to thank the “Département de la Nature et des Forêts”, Yves Storder and “Natagora” for the permission to study A. napellus ssp. lusitanicum populations in nature reserves during 2010–2012 and collect plant fragments in large and un-endangered populations in 2008 (ref. DNF/DN/PB/SLI/MLB/802.7). Renate Wesselingh (UCL) kindly provided fluorescent dyes. Fabienne Van Rossum made comments on an earlier version of the manuscript. Thanks go to Connal Eardley for language improvement. The study was conducted in accordance with current Belgian laws.


  1. Adler LS (2000) The ecological significance of toxic nectar. Oikos 91:409–420. doi: 10.1034/j.1600-0706.2000.910301.x CrossRefGoogle Scholar
  2. Adler LS, Irwin RE (2005) Ecological costs and benefits of defenses in nectar. Ecology 86:2968–2978. doi: 10.1890/05-0118 CrossRefGoogle Scholar
  3. Barrett SCH (2003) Mating strategies in flowering plants: the outcrossing–selfing paradigm and beyond. Philos Trans R Soc Lond B Biol Sci 358:991–1004. doi: 10.1098/rstb.2003.1301 PubMedCentralPubMedCrossRefGoogle Scholar
  4. Barrett SCH, Harder LD (1996) Ecology and evolution of plant mating. Trends Ecol Evol 11:73–79. doi: 10.1016/0169-5347(96)81046-9 PubMedCrossRefGoogle Scholar
  5. Brody AK, Irwin RE, McCutcheon ML, Parsons EC (2008) Interactions between nectar robbers and seed predators mediated by a shared host plant, Ipomopsis aggregata. Oecologia 155:75–84. doi: 10.1007/s00442-007-0879-8 PubMedCrossRefGoogle Scholar
  6. Bronstein JL (2001) The costs of mutualism. Am Zool 41:825–839. doi: 10.2307/3884527 CrossRefGoogle Scholar
  7. Burkle LA, Irwin RE, Newman DA (2007) Predicting the effects of nectar robbing on plant reproduction: implications of pollen limitation and plant mating system. Am J Bot 94:1935–1943. doi: 10.3732/ajb.94.12.1935 PubMedCrossRefGoogle Scholar
  8. Campagne P, Affre L, Baumel A et al (2009) Fine-scale response to landscape structure in Primula vulgaris Huds.: does hedgerow network connectedness ensure connectivity through gene flow? Popul Ecol 51:209–219. doi: 10.1007/s10144-008-0124-2 CrossRefGoogle Scholar
  9. Castro S, Silveira P, Navarro L (2008) Consequences of nectar robbing for the fitness of a threatened plant species. Plant Ecol 199:201–208. doi: 10.1007/s11258-008-9424-z CrossRefGoogle Scholar
  10. Cawoy V, Jonard M, Mayer C, Jacquemart A-L (2012) Do abundance and proximity of the alien Impatiens glandulifera affect pollination and reproductive success of two sympatric co-flowering native species? J Pollinat Ecol 10:130–139.[]=203 Google Scholar
  11. Darwin C (1872) Effects of cross and self fertilisation in the vegetable kingdom. Murray, LondonGoogle Scholar
  12. Dedej S, Delaplane KS (2005) Net energetic advantage drives honey bees (Apis mellifera L.) to nectar larceny in Vaccinium ashei Reade. Behav Ecol Sociobiol 57:398–403. doi: 10.1007/s00265-004-0852-z CrossRefGoogle Scholar
  13. Dehon C (2011) Etude de l’impact du vol de nectar sur Aconitum napellus spp. lusitanicum et sur le comportement de ses pollinisateurs. Master thesis, Université catholique de LouvainGoogle Scholar
  14. Delaplane KS, Mayer DF (2000) Crop pollination by bees. CABI, New YorkCrossRefGoogle Scholar
  15. Dohzono I, Kunitake YK, Yokoyama J, Goka K (2008) Alien bumble bee affects native plant reproduction through interactions with native bumble bees. Ecology 89:3082–3092. doi: 10.1890/07-1491.1 CrossRefGoogle Scholar
  16. Fenster CB (1991) Gene flow in Chamaecrista fasciculata (Leguminosae) I. Gene dispersal. Evolution 45:398–409. doi: 10.2307/2409673 CrossRefGoogle Scholar
  17. Ferrari S, Cribari-Neto F (2004) Beta regression for modelling rates and proportions. J Appl Statist 31:799–815. doi: 10.1080/0266476042000214501 CrossRefGoogle Scholar
  18. Galen C, Plowright RC (1985) The effects of nectar level and flower development on pollen carry-over in inflorescences of fireweed (Epilobium angustifolium) (Onagraceae). Can J Bot 63:488–491. doi: 10.1139/b85-060 CrossRefGoogle Scholar
  19. González-Gómez PL, Valdivia CE (2005) Direct and indirect effects of nectar robbing on the pollinating behavior of Patagona gigas (Trochilidae). Biotropica 37:693–696. doi: 10.1111/j.1744-7429.2005.00088.x CrossRefGoogle Scholar
  20. Gosselin M, Michez D, Vanderplanck M et al (2013) Does Aconitum septentrionale chemically protect floral rewards to the advantage of specialist bumblebees? Ecol Entomol 38:400–407. doi: 10.1111/een.12032 CrossRefGoogle Scholar
  21. Goulson D, Hawson SA, Stout JC (1998) Foraging bumblebees avoid flowers already visited by conspecifics or by other bumblebee species. Anim Behav 55:199–206. doi: 10.1006/anbe.1997.0570 PubMedCrossRefGoogle Scholar
  22. Harder LD, Barrett SCH (1995) Mating cost of large floral displays in hermaphrodite plants. Nature 373:512–515. doi: 10.1038/373512a0 CrossRefGoogle Scholar
  23. Hardy OJ, González-Martínez SC, Fréville H et al (2004) Fine-scale genetic structure and gene dispersal in Centaurea corymbosa (Asteraceae) I. Pattern of pollen dispersal. J Evol Biol 17:795–806. doi: 10.1111/j.1420-9101.2004.00713.x PubMedCrossRefGoogle Scholar
  24. Heinrich B (1979) Resource heterogeneity and patterns of movement in foraging bumblebees. Oecologia 40:235–245. doi: 10.1007/BF00345321 CrossRefGoogle Scholar
  25. Inouye DW (1980) The terminology of floral larceny. Ecology 61:1251–1253. doi: 10.2307/1936841 CrossRefGoogle Scholar
  26. Irwin RE (2003) Impact of nectar robbing on estimates of pollen flow: conceptual predictions and empirical outcomes. Ecology 84:485–495. doi: 10.1890/0012-9658(2003)084[0485:IONROE]2.0.CO;2 Google Scholar
  27. Irwin RE, Adler LS (2006) Correlations among traits associated with herbivore resistance and pollination: implications for pollination and nectar robbing in a distylous plant. Am J Bot 93:64–72. doi: 10.3732/ajb.93.1.64 CrossRefGoogle Scholar
  28. Irwin RE, Brody AK (1998) Nectar robbing in Ipomopsis aggregata: effects on pollinator behavior and plant fitness. Oecologia 116:519–527. doi: 10.1007/s004420050617 CrossRefGoogle Scholar
  29. Irwin R, Maloof J (2002) Variation in nectar robbing over time, space, and species. Oecologia 133:525–533. doi: 10.1007/s00442-002-1060-z CrossRefGoogle Scholar
  30. Irwin RE, Galen C, Rabenold JJ et al (2008) Mechanisms of tolerance to floral larceny in two wildflower species. Ecology 89:3093–3104. doi: 10.1890/08-0081.1 CrossRefGoogle Scholar
  31. Irwin RE, Bronstein JL, Manson JS, Richardson L (2010) Nectar robbing: ecological and evolutionary perspectives. Annu Rev Ecol Evol Syst 41:271–292. doi: 10.1146/annurev.ecolsys.110308.120330 CrossRefGoogle Scholar
  32. Jersáková J, Johnson SD, Kindlmann P (2006) Mechanisms and evolution of deceptive pollination in orchids. Biol Rev Camb Philos Soc 81:219–235. doi: 10.1017/S1464793105006986 PubMedCrossRefGoogle Scholar
  33. Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colorado, NiwotGoogle Scholar
  34. Lambinon J, Verloove F (2012) Nouvelle Flore de la Belgique, du Grand-Duché de Luxembourg, du Nord de la France et des Régions voisines, 6th edn. Jardin botanique national de Belgique, MeiseGoogle Scholar
  35. Le Cadre S (2005) Allee effects on plants. The case of Aconitum napellus subsp. lusitanicum. PhD Thesis, Université Pierre et Marie Curie (Paris VI)Google Scholar
  36. Le Cadre S, Tully T, Mazer SJ et al (2008) Allee effects within small populations of Aconitum napellus ssp. lusitanicum, a protected subspecies in northern France. New Phytol 179:1171–1182. doi: 10.1111/j.1469-8137.2008.02529.x PubMedCrossRefGoogle Scholar
  37. Leadbeater E, Chittka L (2008) Social transmission of nectar-robbing behaviour in bumble-bees. Proc R Soc B 275:1669–1674. doi: 10.1098/rspb.2008.0270 PubMedCentralPubMedCrossRefGoogle Scholar
  38. Maloof JE (2001) The effects of a bumble bee nectar robber on plant reproductive success and pollinator behavior. Am J Bot 88:1960–1965PubMedCrossRefGoogle Scholar
  39. Maloof JE, Inouye DW (2000) Are nectar robbers cheaters or mutualists? Ecology 81:2651–2661. doi: 10.1890/0012-9658(2000)081[2651:ANRCOM]2.0.CO;2 Google Scholar
  40. Mayer C, Van Rossum F, Jacquemart A-L (2012) Evaluating pollen flow indicators for an insect-pollinated plant species. Basic Appl Ecol 13:690–697. doi: 10.1016/j.baae.2012.09.012 CrossRefGoogle Scholar
  41. Mitchell RJ (1993) Adaptive significance of Ipomopsis aggregata nectar production: observation and experiment in the field. Evolution 47:25–35. doi: 10.2307/2410115 CrossRefGoogle Scholar
  42. Morris WF (1996) Mutualism denied? Nectar-robbing bumble bees do not reduce female or male success of bluebells. Ecology 77:1451–1462. doi: 10.2307/2265542 CrossRefGoogle Scholar
  43. Navarro L (2000) Pollination ecology of Anthyllis vulneraria subsp. vulgaris (Fabaceae): nectar robbers as pollinators. Am J Bot 87:980–985PubMedCrossRefGoogle Scholar
  44. Navarro L (2001) Reproductive biology and effect of nectar robbing on fruit production in Macleania bullata (Ericaceae). Plant Ecol 152:59–65. doi: 10.1023/A:1011463520398 CrossRefGoogle Scholar
  45. Naveau O (2012) Etude de l’impact du vol de nectar sur Aconitum napellus spp. lusitanicum et sur le comportement de ses pollinisateurs. Master thesis, Université catholique de LouvainGoogle Scholar
  46. Newman DA, Thomson JD (2005) Interactions among nectar robbing, floral herbivory, and ant protection in Linaria vulgaris. Oikos 110:497–506. doi: 10.1111/j.0030-1299.2005.13885.x CrossRefGoogle Scholar
  47. Proctor M, Yeo P, Lack A (1996) The natural history of pollination. Harper Collins Publishers (The New Naturalist), LondonGoogle Scholar
  48. Pyke GH (1984) Optimal foraging theory: a critical review. Annu Rev Ecol Syst 15:523–575. doi: 10.1146/ CrossRefGoogle Scholar
  49. R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  50. Richardson S (2004) Are nectar-robbers mutualists or antagonists? Oecologia 139:246–254. doi: 10.1007/s00442-004-1504-8 PubMedCrossRefGoogle Scholar
  51. Richardson L, Bronstein JL (2012) Reproductive biology of pointleaf manzanita (Arctostaphylos pungens) and the pollinator-nectar robber spectrum. J Pollinat Ecol 9:115–123.[]=177Google Scholar
  52. Rigo C (2013) Etude de l’impact du vol de nectar sur Aconitum napellus spp. lusitanicum et sur le comportement de ses pollinisateurs. Master thesis, Université catholique de LouvainGoogle Scholar
  53. Roubik DW (1982) The ecological impact of nectar-robbing bees and pollinating hummingbirds on a tropical shrub. Ecology 63:354–360. doi: 10.2307/1938953 CrossRefGoogle Scholar
  54. Rust RW (1979) Pollination of Impatiens capensis: pollinators and nectar robbers. J Kansas Entomol Soc 52:297–308. doi: 10.2307/25083907 Google Scholar
  55. Schiestl FP (2005) On the success of a swindle: pollination by deception in orchids. Naturwissenschaften 92:255–264. doi: 10.1007/s00114-005-0636-y PubMedCrossRefGoogle Scholar
  56. Sokal RR, Rohlf FJ (2000) Biometry: the principles and practices of statistics in biological research, 3rd edn. Freeman and Company, New YorkGoogle Scholar
  57. Stout JC, Allen JA, Goulson D (2000) Nectar robbing, forager efficiency and seed set: bumblebees foraging on the self incompatible plant Linaria vulgaris (Scrophulariaceae). Acta Oecol 21:277–283. doi: 10.1016/S1146-609X(00)01085-7 CrossRefGoogle Scholar
  58. Thomson JD (1986) Pollen transport and deposition by bumble bees in Erythronium: influences of floral nectar and bee grooming. J Ecol 74:329–341. doi: 10.2307/2260258 CrossRefGoogle Scholar
  59. Thomson JD, Plowright RC (1980) Pollen carryover, nectar rewards, and pollinator behavior with special reference to Diervilla lonicera. Oecologia 46:68–74. doi: 10.1007/BF00346968 CrossRefGoogle Scholar
  60. Torvik SE, Borgen L, Berg RY (1998) Aspects of reproduction in Pulsatilla pratensis in Norway. Nord J Bot 18:385–391. doi: 10.1111/j.1756-1051.1998.tb01515.x CrossRefGoogle Scholar
  61. Townsend PA, Levey DJ (2005) An experimental test of whether habitat corridors affect pollen transfer. Ecology 86:466–475. doi: 10.1890/03-0607 CrossRefGoogle Scholar
  62. Traveset A, Willson MF, Sabag C (1998) Effect of nectar-robbing birds on fruit set of Fuchsia magellanica in Tierra Del Fuego: a disrupted mutualism. Funct Ecol 12:459–464. doi: 10.1046/j.1365-2435.1998.00212.x CrossRefGoogle Scholar
  63. Van Geert A, Van Rossum F, Triest L (2010) Do linear landscape elements in farmland act as biological corridors for pollen dispersal? J Ecol 98:178–187. doi: 10.1111/j.1365-2745.2009.01600.x CrossRefGoogle Scholar
  64. Van Rossum F (2010) Reproductive success and pollen dispersal in urban populations of an insect-pollinated hay-meadow herb. Perspect Plant Ecol 12:21–29. doi: 10.1016/j.ppees.2009.08.002 CrossRefGoogle Scholar
  65. Van Rossum F, Stiers I, Van Geert A et al (2011) Fluorescent dye particles as pollen analogues for measuring pollen dispersal in an insect-pollinated forest herb. Oecologia 165:663–674. doi: 10.1007/s00442-010-1745-7Waser PubMedCrossRefGoogle Scholar
  66. Waser NM (1988) Comparative pollen and dye transfer by pollinators of Delphinium nelsonii. Funct Ecol 2:41–48. doi: 10.2307/2389458 CrossRefGoogle Scholar
  67. Weaver N (1956) The foraging behavior of honeybees on hairy vetch foraging methods and learning to forage. Insectes Soc 3:537–549. doi: 10.1007/BF02226457 CrossRefGoogle Scholar
  68. Williams GS (1998) The identity of the previous visitor influences flower rejection by nectar-collecting bees. Anim Behav 56:673–681. doi: 10.1006/anbe.1998.0794 PubMedCrossRefGoogle Scholar
  69. Zhang Y-W, Robert GW, Wang Y, Guo Y-H (2007) Nectar robbing of a carpenter bee and its effects on the reproductive fitness of Glechoma longituba (Lamiaceae). Plant Ecol 193:1–13. doi: 10.1007/s11258-006-9244-y CrossRefGoogle Scholar
  70. Zimmerman M, Cook S (1985) Pollinator foraging, experimental nectar-robbing and plant fitness in Impatiens capensis. Am Midl Nat 113:84–91. doi: 10.2307/2425350 CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Carolin Mayer
    • 1
    Email author
  • Charles Dehon
    • 1
  • Anne-Laure Gauthier
    • 1
  • Olivier Naveau
    • 1
  • Cyrielle Rigo
    • 1
  • Anne-Laure Jacquemart
    • 1
  1. 1.Earth and Life Institute, AgronomyUniversité Catholique de LouvainLouvain-la-NeuveBelgium

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