Skip to main content

Advertisement

Log in

Bird diversity and seed dispersal along a human land-use gradient: high seed removal in structurally simple farmland

  • Plant-Animal interactions - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Only few studies have analysed the relationship between biodiversity and ecosystem function at the landscape scale although relationships and mechanisms known from experimental studies might be different in natural systems. We quantified bird diversity and seed removal from 38 wild cherry trees (Prunus avium) along a human land-use gradient from forest to structurally diverse to simple agricultural systems. High human land-use intensity led to low species richness and total abundance of the local bird community around wild cherry trees, as expected from previous studies. Nevertheless, trees in structurally simple agroecosystems were visited as frequently as trees in structurally complex landscapes and in forests. Furthermore, the number of seeds removed per tree did not decline with increasing human land-use intensity. Thus, ecosystem function was robust in spite of locally reduced bird diversity. The reason might be that movement behaviour and movement distances of birds changed along the human land-use gradient. It appears that birds moved longer distances to forage in fruiting cherry trees in structurally simple agroecosystems. This suggests that for systems where ecosystem function is mediated by highly mobile organisms, movement behaviour and distances are of considerable importance. Increases in movement distances with increasing human land-use intensity might also be common in other systems in which ecosystem function depends on mobile links.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aguilar R, Ashworth L, Galetto L, Aizen MA (2006) Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecol Lett 9:968–980

    Article  PubMed  Google Scholar 

  • Arnold GW (1983) The influence of ditch and hedgerow structure, length of hedgerows, and area of woodland and garden on bird numbers on farmland. J Appl Ecol 20:731–750

    Article  Google Scholar 

  • Balvanera P, Pfisterer AB, Buchmann N, He JS, Nakashizuka T, Raffaelli D, Schmid B (2006) Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol Lett 9:1146–1156

    Article  PubMed  Google Scholar 

  • Bauer HG, Bezzel E, Fiedler W (2005) Das Kompendium der Vögel Mitteleuropas. 2. Auflage. Aula, Wiesbaden

    Google Scholar 

  • Bianchi FJJA, Booij CHJ, Tscharntke T (2006) Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control. Proc R Soc Lond B 273:1715–1727

    Article  CAS  Google Scholar 

  • Bibby CJ, Buckland ST (1987) Bias of bird census results due to detectability varying with habitat. Acta Oecol Oecol Gen 8:103–112

    Google Scholar 

  • Bibby CJ, Burgess ND, Hill DA, Mustoe S (2000) Bird census techniques, 2nd edn. Academic Press, London

    Google Scholar 

  • Billeter R, Liira J, Bailey D, Bugter R, Arens P, Augenstein I, Aviron S, Baudry J, Bukacek R, Burel F, Cerny M, De Blust G, De Cock R, Diekötter T, Dietz H, Dirksen J, Dormann C, Durka W, Frenzel M, Hamersky R, Hendrickx F, Herzog F, Klotz S, Koolstra B, Lausch A, Le Coeur D, Maelfait JP, Opdam P, Roubalova M, Schermann A, Schermann N, Schmidt T, Schweiger O, Smulders MJM, Speelmans M, Simova P, Verboom J, van Wingerden WKRE, Zobel M, Edwards PJ (2008) Indicators for biodiversity in agricultural landscapes: a pan-European study. J Appl Ecol 45:141–150

    Article  Google Scholar 

  • Bleher B, Böhning-Gaese K (2001) Consequences of frugivore diversity for seed dispersal, seedling establishment and the spatial pattern of seedlings and trees. Oecologia 129:385–394

    Google Scholar 

  • Bond WJ (1994) Do mutualisms matter? Assessing the impact of pollinator and disperser disruption on plant extinction. Philos Trans R Soc Lond B Biol Sci 344:83–90

    Article  Google Scholar 

  • Bracken MES, Friberg SE, Gonzalez-Dorantes CA, Williams SL (2008) Functional consequences of realistic biodiversity changes in a marine ecosystem. Proc Natl Acad Sci USA 105:924–928

    Article  CAS  PubMed  Google Scholar 

  • Brennan SP, Schnell GD (2005) Relationship between bird abundance and landscape characteristics: the influence of scale. Environ Monit Assess 105:209–228

    Article  PubMed  Google Scholar 

  • Carpenter SR (1996) Microcosm experiments have limited relevance for community and ecosystem ecology. Ecology 77:677–680

    Article  Google Scholar 

  • Carrière SM, André M, Letourmy P, Olivier I, McKey DB (2002) Seed rain beneath remnant trees in a slash-and-burn agricultural system in southern Cameroon. J Trop Ecol 18:353–374

    Google Scholar 

  • Conrad L (2002) Wildkirsche (Prunus avium) Verbreitung, Ausbreitungsmechanismen und waldbauliche Behandlung. PhD thesis, University of Hamburg, Germany

  • Cordeiro NJ, Howe HF (2003) Forest fragmentation severs mutualism between seed dispersers and an endemic African tree. Proc Natl Acad Sci USA 100:14052–14056

    Article  CAS  PubMed  Google Scholar 

  • Dale V, Brown HS, Haeuber RA, Hobbs NT, Huntly N, Naiman RJ, Riebsame WE, Turner MG, Valone TJ (2000) Ecological principles and guidelines for managing the use of land. Ecol Appl 10:639–670

    Google Scholar 

  • Devictor V, Julliard R, Clavel J, Jiguet F, Lee A, Couvet D (2008) Functional biotic homogenization of bird communities in disturbed landscapes. Global Ecol Biogeogr 17:252–261

    Article  Google Scholar 

  • Dick CW (2001) Genetic rescue of remnant tropical trees by an alien pollinator. Proc R Soc Lond B Biol Sci 268:2391–2396

    Article  CAS  Google Scholar 

  • Dick CW, Etchelecu G, Austerlitz F (2003) Pollen dispersal of tropical trees (Dinizia excelsa: Fabaceae) by native insects and African honeybees in pristine and fragmented Amazonian rainforest. Mol Ecol 12:753–764

    Article  PubMed  Google Scholar 

  • DLR-DFD 2004: CORINE Land Cover; Federal Environmental Agency, DLR-DFD 2004, at http://www.corine.dfd.dlr.de/intro_en.html on the project website

  • Duncan RS, Chapman CA (1999) Seed dispersal and potential forest succession in abandoned agriculture in tropical Africa. Ecol Appl 9:998–1008

    Article  Google Scholar 

  • Dunford W, Freemark K (2004) Matrix matters: effects of surrounding land uses on forest birds near Ottawa, Canada. Landsc Ecol 20:497–511

    Article  Google Scholar 

  • Eshiamwata GW, Berens DG, Bleher B, Dean WRJ, Böhning-Gaese K (2006) Bird assemblages in isolated Ficus trees in Kenyan farmland. J Trop Ecol 22:723–726

    Article  Google Scholar 

  • Farwig N, Böhning-Gaese K, Bleher B (2006) Enhanced seed dispersal of Prunus africana in fragmented and disturbed forests? Oecologia 147:238–252

    Article  PubMed  Google Scholar 

  • Foley JA, DeFries R, Asner GP, Barford C, Bonan G, Carpenter SR, Chapin FS, Coe MT, Daily GC, Gibbs HK, Helkowski JH, Holloway T, Howard EA, Kucharik CJ, Monfreda C, Patz JA, Prentice IC, Ramankutty N, Snyder PK (2005) Global consequences of land use. Science 309:570–574

    Article  CAS  PubMed  Google Scholar 

  • Fontaine C, Dajoz I, Meriguet J, Loreau M (2006) Functional diversity of plant–pollinator interaction webs enhances the persistence of plant communities. PLoS Biol 4:129–135

    Article  CAS  Google Scholar 

  • Fuller RJ, Chamberlain DE, Burton NHK, Gough SJ (2001) Distributions of birds in lowland agricultural landscapes of England and Wales: how distinctive are bird communities of hedgerows and woodland? Agric Ecosyst Environ 84:79–92

    Article  Google Scholar 

  • Harris RJ, Reed MJ (2002) Behavioural barriers to non-migratory movements of birds. Ann Zool Fenn 39:275–290

    Google Scholar 

  • Harrison S, Bruna E (1999) Habitat fragmentation and large-scale conservation: what do we know for sure? Ecography 22:225–232

    Article  Google Scholar 

  • Hecker U (2001) BLV-Handbuch Bäume und Sträucher: das umfassende Nachschlagwerk; 800 farbige Fotos und Zeichnungen. BLV, München

    Google Scholar 

  • Herrera CM (2002) Seed dispersal by vertebrates. In: Herrera CM, Pellmyr O (eds) Plant–animal interactions: an evolutionary approach. Blackwell, Oxford, pp 185–208

    Google Scholar 

  • Herrera JM, García D (2009) The role of remnant trees in seed dispersal through the matrix: being alone is not always so sad. Biol Conserv 142:149–158

    Article  Google Scholar 

  • Herrera CM, Jordano P, Lopezsoria L, Amat JA (1994) Recruitment of a mast-fruiting, bird-dispersed tree—bridging frugivore activity and seedling establishment. Ecol Monogr 64:315–344

    Article  Google Scholar 

  • Herzon I, Aunină A, Elts J, Preikša Z (2008) Intensity of agricultural land-use and farmland birds in the Baltic States. Agric Ecosyst Environ 125:93–100

    Article  Google Scholar 

  • Hinam HL, St. Clair CC (2008) High levels of habitat loss and fragmentation limit reproductive success by reducing home range size and provisioning rates of northern saw-whet owls. Biol Conserv 141:524–535

    Article  Google Scholar 

  • Höltken AM (2005) Genetische Untersuchungen zu den Voraussetzungen und Konsequenzen einer rezedenten Lebensweise am Beispiel der Vogelkirsche (Prunus avium L.). PhD thesis, University of Göttingen, Germany

  • Hooper DU, Chapin FS, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setala H, Symstad AJ, Vandermeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35

    Article  Google Scholar 

  • Howe HF, Miriti MN (2004) When seed dispersal matters. Bioscience 54:651–660

    Article  Google Scholar 

  • Kati VI, Sekercioglu CH (2006) Diversity, ecological structure and conservation of the landbird community of Dadia reserve, Greece. Divers Distrib 12:620–629

    Article  Google Scholar 

  • Kirika JM, Farwig N, Böhning-Gaese K (2008a) Effects of local disturbance of tropical forests on frugivores and seed removal of a small-seeded afrotropical tree. Conserv Biol 22:318–328

    Article  PubMed  Google Scholar 

  • Kirika JM, Bleher B, Böhning-Gaese K, Chira RM, Farwig N (2008b) Fragmentation and local disturbance of forests reduce frugivore diversity and fruit removal in Ficus thonningii. Basic Appl Ecol 9:663–672

    Article  Google Scholar 

  • Kleijn D, van Langevelde F (2006) Interacting effects of landscape context and habitat quality on flower visiting insects in agricultural landscapes. Basic Appl Ecol 7:201–214

    Article  Google Scholar 

  • Klein A-M, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc Lond B 274:303–313

    Article  Google Scholar 

  • Kremen C (2005) Managing ecosystem services: what do we need to know about their ecology? Ecol Lett 8:468–479

    Article  Google Scholar 

  • Kremen C, Ostfeld RS (2005) A call to ecologists: measuring, analyzing, and managing ecosystem services. Front Ecol Environ 3:540–548

    Article  Google Scholar 

  • Kremen C, Williams NM, Aizen MA, Gemmill-Herren B, LeBuhn G, Minckley R, Packer L, Potts SG, Roulston T, Steffan-Dewenter I, Vázquez DP, Winfree R, Adams L, Crone EE, Greenleaf SS, Keitt TH, Klein A-M, Regetz J, Ricketts TH (2007) Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land-use change. Ecol Lett 10:299–314

    Article  PubMed  Google Scholar 

  • Kristan WB (2006) Sources and expectations for hierarchical structure and bird-habitat associations. Condor 108:5–12

    Article  Google Scholar 

  • Legendre P, Legendre L (1998) Numerical ecology. 2nd english edn. Elsevier, Amsterdam

    Google Scholar 

  • Levey DJ, Bolker BM, Tewksbury JJ, Sargent S, Haddad NM (2005) Effects of landscape corridors on seed dispersal by birds. Science 309:146–148

    Article  CAS  PubMed  Google Scholar 

  • Luck GW, Daily C (2003) Tropical countryside bird assemblages: richness, composition, and foraging differ by landscape context. Ecol Appl 13:235–247

    Article  Google Scholar 

  • Lundberg J, Moberg F (2003) Mobile link organisms and ecosystem functioning: implications for ecosystem resilience and management. Ecosystems 6:87–98

    Article  Google Scholar 

  • MacArthur RH, MacArthur JW (1961) On bird species diversity. Ecology 42:594–598

    Article  Google Scholar 

  • Marchant JH (1994) The new breeding bird survey. Br Birds 87:26–28

    Google Scholar 

  • Marzluff JM, Ewing K (2001) Restoration of fragmented landscapes for the conservation of birds: a general framework and specific recommendations for urbanizing landscapes. Restor Ecol 9:280–292

    Article  Google Scholar 

  • Orians GH, Pearson NE (1979) On the theory of central place foraging. In: Horn DJ, Mitchell RD, Stairs GR (eds) Analysis of ecological systems. Ohio University Press, Ohio, pp 154–177

  • Primack RB, Miao SL (1992) Dispersal can limit local plant distribution. Conserv Biol 6:513–519

    Article  Google Scholar 

  • R Development Core Team (2005) R: a language and environment for statistical computing. R foundation for Statistical Computing, Vienna. URL: http://www.R-project.org

  • Ricketts TH (2004) Tropical forest fragments enhance pollinator activity in nearby coffee crops. Conserv Biol 18:1262–1271

    Article  Google Scholar 

  • Ricketts TH, Regetz J, Steffan-Dewenter I, Cunningham SA, Kremen C, Bogdanski A, Gemmill-Herren B, Greenleaf SS, Klein AM, Mayfield MM, Morandin LA, Ochieng’ A, Viana BF (2008) Landscape effects on crop pollination services: are there general patterns? Ecol Lett 11:499–515

    Article  PubMed  Google Scholar 

  • Schupp EW (1993) Quantity, quality and the effectiveness of seed dispersal by animals. Vegetation 107:15–29

    Google Scholar 

  • Schupp EW, Fuentes M (1995) Spatial patterns of seed dispersal and the unification of plant-population ecology. Ecoscience 2:267–275

    Google Scholar 

  • Sekercioglu CH (2006) Increasing awareness of avian ecological function. Trends Ecol Evol 21:464–471

    Article  PubMed  Google Scholar 

  • Sekercioglu CH, Loarie SR, Brenes FO, Ehrlich PR, Daily GC (2007) Persistence of forest birds in the Costa Rican agricultural countryside. Conserv Biol 21:482–494

    Article  PubMed  Google Scholar 

  • Slocum MG, Horvitz CC (2000) Seed arrival under different genera of trees in a neotropical pasture. Plant Ecol 149:51–62

    Article  Google Scholar 

  • Snow B, Snow D (1988) Birds and berries—a study of an ecological interaction. Poyser, London

    Google Scholar 

  • Spiegel O, Nathan R (2007) Incorporating dispersal distance into the disperser effectiveness framework: frugivorous birds provide complementary dispersal to plants in a patchy environment. Ecol Lett 10:718–728

    Article  PubMed  Google Scholar 

  • Steffan-Dewenter I, Kuhn A (2003) Honeybee foraging in differentially structured landscapes. Proc R Soc Lond B 270:569–575

    Article  Google Scholar 

  • Steffan-Dewenter I, Münzenberg U, Bürger C, Thies C, Tscharntke T (2002) Scale-dependent effects of landscape context on three pollinator guilds. Ecology 83:1421–1432

    Article  Google Scholar 

  • Steffan-Dewenter I, Potts SG, Packer L (2005) Pollinator diversity and crop pollination services are at risk. Trends Ecol Evol 20:651–653

    Article  PubMed  Google Scholar 

  • Steffan-Dewenter I, Klein AM, Gaebele V, Alfert T, Tscharntke T (2006) Bee diversity and plant–pollinator interactions in fragmented landscapes. In: Waser NM, Ollerton J (eds) Plant–pollinator interactions. University of Chicago Press, Chicago, pp 387–407

    Google Scholar 

  • Tabarelli B, Peres CA (2002) Abiotic and vertebrate seed dispersal in the Brazilian Atlantic forest: implications for forest regeneration. Biol Conserv 106:165–176

    Article  Google Scholar 

  • Tscharntke T, Klein AM, Kruess A, Steffan-Dewenter I, Thies C (2005) Landscape perspectives on agricultural intensification and biodiversity-ecosystem service management. Ecol Lett 8:857–874

    Article  Google Scholar 

  • Tscharntke T, Sekercioglu CH, Dietsch TV, Sodhi NS, Hoehn P, Tylianakis JM (2008) Landscape constraints on functional diversity of birds and insects in tropical agroecosystems. Ecology 89:944–951

    Article  PubMed  Google Scholar 

  • Turček FJ (1968) Die Verbreitung der Vogelkirsche in den Wäldern durch Vögel. Waldhygiene 7:129–132

    Google Scholar 

  • Tylianakis JM, Tscharntke T, Klein A-M (2006) Diversity, ecosystem function, and stability of parasitoid–host interactions across a tropical habitat gradient. Ecology 87:3047–3057

    Article  PubMed  Google Scholar 

  • Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008a) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363

    Article  PubMed  Google Scholar 

  • Tylianakis JM, Rand TA, Kahmen A, Klein A-M, Buchmann N, Perner J, Tscharntke T (2008b) Resource heterogeneity moderates the biodiversity-function relationship in real world ecosystems. PLoS Biol 6:947–956

    CAS  Google Scholar 

  • Uwate WJ, Lin J (1981) Development of the stigmatic surface of Prunus avium L., sweet cherry. Am J Bot 68:1165–1176

    Article  Google Scholar 

  • Wenny DG, Levey DJ (1998) Directed dispersal by bellbirds in a tropical cloud forest. Proc Natl Acad Sci USA 95:6204–6207

    Article  CAS  PubMed  Google Scholar 

  • Westcott DA, Graham DL (2000) Patterns of movement and seed dispersal of a tropical frugivore. Oecologia 122:249–257

    Article  Google Scholar 

  • Westcott DA, Bentruppbäumer J, Bradford MG, McKeown A (2005) Incorporating patters of disperser behaviour into models of seed dispersal and its effects on estimated dispersal curves. Oecologia 146:57–67

    Article  PubMed  Google Scholar 

  • Willson MF (1974) Avian community organization and habitat structure. Ecology 55:1017–1029

    Article  Google Scholar 

  • With KA, Pavuk DM, Worchuk JL, Oates RK, Fisher JL (2002) Threshold effects of landscape structure on biological control in agroecosystems. Ecol Appl 12:52–65

    Article  Google Scholar 

Download references

Acknowledgements

Colour analyses of cherries were supported by C. Neumeyer and J. Schramme. J. Lenz, J. Reimann and J. Taubmann helped with field observations and measurements. S. Schueler and A. Tusch provided genetic material of three P. avium cultivars, P. Hilsendegen supplied us with leaf samples of all locally important cherry cultivars. Financial support came from the Deutsche Forschungsgemeinschaft (BO 1221/13-1) and the Ministry for Environment and Forestry Rhineland-Palatinate. This is the first PhD thesis paper of Nils Breitbach at the Institute of Zoology, University of Mainz, Germany.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nils Breitbach.

Additional information

Communicated by Esa Lehikoinen.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Appendix S1

Control variables: Materials, methods and results (PDF 136 kb)

Appendix S2

Detailed results for the bird counts during the breeding season and the tree observations (PDF 129 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Breitbach, N., Laube, I., Steffan-Dewenter, I. et al. Bird diversity and seed dispersal along a human land-use gradient: high seed removal in structurally simple farmland. Oecologia 162, 965–976 (2010). https://doi.org/10.1007/s00442-009-1547-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-009-1547-y

Keywords

Navigation