Plant Ecology

, Volume 203, Issue 1, pp 111–122 | Cite as

Birds and guelder rose Viburnum opulus: selective consumption and dispersal via regurgitation of small-sized fruits and seeds

  • Ángel HernándezEmail author


The evolution of fleshy fruit size, in particular in bird-dispersed plants, is believed to be influenced by the size of seed-dispersing vertebrates through gape limitation. Also, it has been demonstrated that seed size correlates positively with fruit size, especially in single- or few-seeded fruits. However, there is little evidence of current selection pressure by disperser birds on fruit and seed size within populations of a particular plant species. In the present study, this aspect was investigated in guelder rose Viburnum opulus (Caprifoliaceae) fruit consumption by birds in an area in NW Spain. Guelder rose fruits are sub-globose drupes that can exceed 11 mm in width, with a single hard seed of up to 8.5 mm in width. Most of the seeds were dispersed by the robin Erithacus rubecula (gape width < 8 mm) and a small thrush, the song thrush Turdus philomelos (gape width < 11 mm), which swallowed the fruits whole, and some were destroyed by the bullfinch Pyrrhula pyrrhula. Most of the seeds were regurgitated rather than defecated by disperser birds, probably because seed size limited gut processing. The mean size of the ingested seeds was smaller than the mean diameter of Turdus droppings, which in turn was smaller than the mean size of the seeds of the fruits available on the plants. As winter progressed, only larger fruits and seeds remained on the plants (seed and fruit size were positively correlated), and the size of ingested seeds increased. Thus, the largest fruits were consumed less by seed-dispersing birds and were exposed to seed-predators (bullfinches and climbing rodents) for longer. Selection pressure on smaller guelder rose seeds must therefore be effective in the dispersal stage in the study area.


Fruit size Gape limitation Gut processing Seed-dispersing birds Seed size Selection pressure 



I wish to thank Pilar Zaldívar, Pedro Rey and an anonymous reviewer for their critical reading of the manuscript. This paper is a research contribution of the Ecology and Conservation of Flora and Fauna Group at Valladolid University, Spain.


  1. Alcántara JM, Rey PJ (2003) Conflicting selection pressures on seed size: evolutionary ecology of fruit size in a bird-dispersed tree, Olea europaea. J Evol Biol 16:1168–1176. doi: 10.1046/j.1420-9101.2003.00618.x PubMedCrossRefGoogle Scholar
  2. Alonso-Blanco C, Blankestijn-de Vries H, Hanhart CJ, Koornneff M (1999) Natural allelic variation at seed size loci in relation to other life history traits of Arabidopsis thaliana. Proc Natl Acad Sci USA 96:4710–4717. doi: 10.1073/pnas.96.8.4710 PubMedCrossRefGoogle Scholar
  3. Ballian D (2000) Preliminary study of variation in morphological characteristics of wild cherry Prunus avium seeds. Sumarski List 124:271–278Google Scholar
  4. Cipollini ML, Levey DJ (1997) Secondary metabolites of fleshy vertebrate-dispersed fruits: adaptive hypotheses and implications for seed dispersal. Am Nat 150:346–372. doi: 10.1086/286069 PubMedCrossRefGoogle Scholar
  5. Cramp S, Perrins CM (eds) (1993) The birds of the western Palearctic, vol VII. Oxford University Press, OxfordGoogle Scholar
  6. Englund R (1993) Fruit removal in Viburnum opulus: copious seed predation and sporadic massive seed dispersal in a temperate shrub. Oikos 67:503–510. doi: 10.2307/3545362 CrossRefGoogle Scholar
  7. Fenner M, Thompson K (2005) The ecology of seeds. Cambridge University Press, CambridgeGoogle Scholar
  8. Forget PM, Dennis AJ, Mazer SJ, Jansen PA, Kitamura S, Lambert JE, Westcott DA (2007) Seed allometry and disperser assemblages in tropical rainforests: a comparison of four floras on different continents. In: Dennis AJ, Schupp EW, Green RJ, Westcott DA (eds) Seed dispersal. Theory and its application in a changing world. CABI Publishing, Wallingford, pp 5–36Google Scholar
  9. Foster MS (1990) Factors influencing bird foraging preferences among conspecific fruit trees. Condor 92:844–854. doi: 10.2307/1368720 CrossRefGoogle Scholar
  10. Fowler J, Cohen L, Jarvis P (1998) Practical statistics for field biology, 2nd edn. Wiley, ChichesterGoogle Scholar
  11. Fuentes M (1992) Latitudinal and elevational variation in fruiting phenology among western-european bird-dispersed plants. Ecography 15:177–183. doi: 10.1111/j.1600-0587.1992.tb00021.x CrossRefGoogle Scholar
  12. Fuentes M (1994) Diets of fruit-eating birds: what are the causes of interspecific differences? Oecologia 97:134–142. doi: 10.1007/BF00317917 CrossRefGoogle Scholar
  13. Hampe A (2003) Large-scale geographical trends in fruit traits of vertebrate-dispersed temperate plants. J Biogeogr 30:487–496CrossRefGoogle Scholar
  14. He JS, Flynn DFB, Wolfe-Bellin K, Fang J, Bazzaz FA (2005) CO2 and nitrogen, but not population density, alter the size and C/N ratio of Phytolacca americana seeds. Funct Ecol 19:437–444. doi: 10.1111/j.1365-2435.2005.00981.x CrossRefGoogle Scholar
  15. Hernández A (2003) Variations in spindle Euonymus europaeus consumption by frugivorous birds during the fruiting season. Ardeola 50:171–180Google Scholar
  16. Hernández A (2005) Blackcaps Sylvia atricapilla and blackbirds Turdus merula feeding their nestlings and fledglings on fleshy fruit. Folia Zool (Brno) 54:379–388Google Scholar
  17. Hernández A (2007) Alimentación de aves frugívoras en setos y bordes de bosque del norte de España: importancia de algunas especies de plantas en invierno y primavera. Ecología 21:145–156Google Scholar
  18. Hernández A (2008a) Fruit removal by climbing rodents in guelder rose: comparison with birds and differences between inner and outer racemes. Mamm Biol. doi: 10.1016/jmambio200802005
  19. Hernández A (2008b) Cherry removal by seed-dispersing mammals: mutualism through commensal association with frugivorous birds. Pol J Ecol 56:127–138Google Scholar
  20. Hernández A, Alegre J (1991) Estructura de la comunidad de paseriformes en setos de la provincia de León (noroeste de España). Doñana Acta Vertebr 18:237–250Google Scholar
  21. Herrera CM (1984) Adaptation to frugivory of Mediterranean avian seed dispersers. Ecology 65:609–617. doi: 10.2307/1941423 CrossRefGoogle Scholar
  22. Herrera CM (1987) Vertebrate-dispersed plants of the Iberian Peninsula: a study of fruit characteristics. Ecol Monogr 57:305–331. doi: 10.2307/2937089 CrossRefGoogle Scholar
  23. Herrera CM (1995) Plant-vertebrate seed dispersal systems in the Mediterranean: ecological, evolutionary, and historical determinants. Annu Rev Ecol Syst 26:705–727Google Scholar
  24. Herrera CM (2002) Seed dispersal by vertebrates. In: Herrera CM, Pellmyr O (eds) Plant–animal interactions. An evolutionary approach. Blackwell Science, Oxford, pp 185–208Google Scholar
  25. Herrera CM (2004) Ecología de los pájaros frugívoros ibéricos. In: Tellería JL (ed) La ornitología hoy. Editorial Complutense-SEO, Madrid, pp 127–153Google Scholar
  26. Izhaki I (2002) The role of fruit traits in determining fruit removal in east Mediterranean ecosystems. In: Levey DJ, Silva WR, Galetti M (eds) Seed dispersal and frugivory. Ecology, evolution and conservation. CABI Publishing, Wallingford, pp 161–175Google Scholar
  27. Izhaki I, Tsahar E, Paluy I, Friedman J (2002) Within population variation and interrelationships between morphology, nutritional content, and secondary compounds of Rhamnus alaternus fruits. New Phytol 156:217–223. doi: 10.1046/j.1469-8137.2002.00515.x CrossRefGoogle Scholar
  28. Jones E, Wheelwright NT (1987) Seasonal changes in the fruits of Viburnum opulus, a fleshy-fruited temperate-zone shrub. Can J Bot 65:2291–2296. doi: 10.1139/b87-312 CrossRefGoogle Scholar
  29. Jordano P (1995a) Angiosperm fleshy fruits and seed dispersers: a comparative analysis of adaptation and constraints in plant-animal interactions. Am Nat 145:163–191. doi: 10.1086/285735 CrossRefGoogle Scholar
  30. Jordano P (1995b) Frugivore-mediated selection on fruit and seed size: birds and St. Lucie’s cherry, Prunus mahaleb. Ecology 76:2627–2639. doi: 10.2307/2265833 CrossRefGoogle Scholar
  31. Jordano P (2000) Fruits and frugivory. In: Fenner M (ed) Seeds. The ecology of regeneration in plant communities, 2nd edn. CABI Publishing, Wallingford, pp 125–165Google Scholar
  32. Kollmann J, Grubb PJ (2002) Viburnum lantana L and Viburnum opulus L (V. lobatum Lam, Opulus vulgaris Borkh). J Ecol 90:1044–1070. doi: 10.1046/j.1365-2745.2002.00724.x CrossRefGoogle Scholar
  33. Kwit C, Levey DJ, Greenberg CH, Pearson SF, McCarty JP, Sargent S (2004) Cold temperature increases winter fruit removal rate of a bird-dispersed shrub. Oecologia 139:30–34. doi: 10.1007/s00442-003-1470-6 PubMedCrossRefGoogle Scholar
  34. Leishman M, Wright IJ, Moles AT, Westoby M (2000) The evolutionary ecology of seeds. In: Fenner M (ed) Seeds. The ecology of regeneration in plant communities, 2nd edn. CABI Publishing, Wallingford, pp 31–57Google Scholar
  35. Levey DJ (1987) Seed size and fruit-handling techniques of avian frugivores. Am Nat 129:471–485. doi: 10.1086/284652 CrossRefGoogle Scholar
  36. López G (2004) Guía de los árboles y arbustos de la península Ibérica y Baleares, 2nd edn. Mundi-Prensa, MadridGoogle Scholar
  37. Lord JM (2004) Frugivore gape size and the evolution of fruit size and shape in southern hemisphere floras. Austral Ecol 29:430–436. doi: 10.1111/j.1442-9993.2004.01382.x CrossRefGoogle Scholar
  38. Mack AL (1993) The sizes of vertebrate-dispersed fruits: a Neotropical–Paleotropical comparison. Am Nat 142:840–856. doi: 10.1086/285575 CrossRefGoogle Scholar
  39. Mazer SJ, Wheelwright NT (1993) Fruit size and shape: allometry at different taxonomic levels in bird-dispersed plants. Evol Ecol 7:556–575. doi: 10.1007/BF01237821 CrossRefGoogle Scholar
  40. Meyer GA, Witmer MC (1998) Influence of seed processing by frugivorous birds on germination success of three North American shrubs. Am Midl Nat 140:129–139. doi: 10.1674/0003-0031(1998)140[0129:IOSPBF]2.0.CO;2 CrossRefGoogle Scholar
  41. Parciak W (2002a) Environmental variation in seed number, size, and dispersal of a fleshy-fruited plant. Ecology 83:780–793Google Scholar
  42. Parciak W (2002b) Seed size, number, and habitat of a fleshy-fruited plant: consequences for seedling establishment. Ecology 83:794–808CrossRefGoogle Scholar
  43. Pizo MA (2002) The seed-dispersers and fruit syndromes of Myrtaceae in the Brazilian Atlantic forest. In: Levey DJ, Silva WR, Galetti M (eds) Seed dispersal and frugivory. Ecology, evolution and conservation. CABI Publishing, Wallingford, pp 129–143Google Scholar
  44. Pizo MA, von Allmen C, Morellato LPC (2006) Seed size variation in the palm Euterpe edulis and the effects of seed predators on germination and seedling survival. Acta Oecol 29:311–315. doi: 10.1016/j.actao.2005.11.011 CrossRefGoogle Scholar
  45. Rey PJ, Gutiérrez JE, Alcántara J, Valera F (1997) Fruit size in wild olives: implications for avian seed dispersal. Funct Ecol 11:611–618. doi: 10.1046/j.1365-2435.1997.00132.x CrossRefGoogle Scholar
  46. Sallabanks R (1993) Hierarchical mechanisms of fruit selection by an avian frugivore. Ecology 74:1326–1336. doi: 10.2307/1940063 CrossRefGoogle Scholar
  47. Snow B, Snow D (1988) Birds and berries. Poyser, CaltonGoogle Scholar
  48. Sorensen AE (1983) Taste aversion and frugivore preference. Oecologia 56:117–120. doi: 10.1007/BF00378226 CrossRefGoogle Scholar
  49. Stanley MC, Lill A (2002) Importance of seed ingestion to an avian frugivore: an experimental approach to fruit choice based on seed load. Auk 119:175–184. doi: 10.1642/0004-8038(2002)119[0175:IOSITA]2.0.CO;2 CrossRefGoogle Scholar
  50. Stiles EW (2000) Animals as seed dispersers. In: Fenner M (ed) Seeds. The ecology of regeneration in plant communities, 2nd edn. CABI Publishing, Wallingford, pp 111–124Google Scholar
  51. Sutherland WJ (2004) Diet and foraging behavior. In: Sutherland WJ, Newton I, Green RE (eds) Bird ecology and conservation. A handbook of techniques. Oxford University Press, Oxford, pp 233–250CrossRefGoogle Scholar
  52. Traveset A, Willson MF, Gaither JC (1995) Avoidance by birds of insect-infested fruits of Vaccinium ovalifolium. Oikos 73:381–386. doi: 10.2307/3545962 CrossRefGoogle Scholar
  53. Werker E (1997) Seed anatomy. Gebrüder Borntraeger, BerlinGoogle Scholar
  54. Wheelwright NT (1993) Fruit size in a tropical tree species: variation, preference by birds, and heritability. Vegetatio 107–108:163–174Google Scholar
  55. Witmer MC (2001) Nutritional interactions and fruit removal: cedar waxwing consumption of Viburnum opulus fruits in spring. Ecology 82:3120–3130Google Scholar
  56. Witmer MC, Van Soest PJ (1998) Contrasting digestive strategies of fruit-eating birds. Funct Ecol 12:728–741. doi: 10.1046/j.1365-2435.1998.00242.x CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  1. 1.Department of AgroforestryUniversity of Valladolid (Palencia Campus)PalenciaSpain

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