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Ground greening in vineyards promotes the Woodlark Lullula arborea and their invertebrate prey

  • Laura BoscoEmail author
  • Raphaël Arlettaz
  • Alain Jacot
Original Article

Abstract

Vineyards are intensively managed monocultures, constituting homogeneously cultivated landscapes. They often have a mineral appearance, not only because they occur mostly in xeric biomes but also as a result of the herbicide treatments used to combat ground vegetation. However, new vineyard management practices are being developed that tolerate more vegetation cover on the ground, potentially having positive impacts on biodiversity. We have investigated the effects of ground greening on habitat preferences of the Woodlark (Lullula arborea), an emblematic, insectivorous passerine typical of vineyards in central and southern Europe. We first investigated the role of ground vegetation cover and plant species richness on habitat use by Woodlarks, while accounting for various additional habitat characteristics. Second, we assessed whether the dependence of Woodlarks on ground vegetation cover could be mediated by an increased occurrence of invertebrate prey. Ground-dwelling invertebrates were sampled with pitfall traps placed in vineyard fields visited by Woodlarks (presence fields) and in adjacent vineyards where Woodlarks had not been observed (pseudo-absence fields). We show that increased ground vegetation cover, plant species richness and wider inter-rows were the main drivers of Woodlark occurrence. Overall invertebrate prey abundance increased with ground vegetation cover. Similarly, the abundance and number of beetle and spider families were primarily driven by increased ground vegetation cover, plant species richness or wider inter-rows. We conclude that less intensive management, which involves the restricted use of herbicides and concomitantly favors a diverse plant community, promotes Woodlarks and their invertebrate prey, thus having a positive impact on vineyard biodiversity at multiple trophic levels.

Keywords

Ground vegetation Habitat preferences Herbicides Plant species richness 

Zusammenfassung

Begrünte Weinberge fördern die Heidelerche Lullula arborea und ihre Beute

Weinberge sind intensive genutzte Monokulturen, welche oftmals homogen bewirtschaftete Landschaften prägen. Sie haben meist ein mineralisches Erscheinungsbild, nicht nur, weil sie vor allem in trockenen Biomen vorkommen, aber auch durch die regelmässigen Herbizid-Anwendungen zur Abtötung der Bodenvegetation. Es werden jedoch zunehmend neue Bewirtschaftungsweisen entwickelt, welche eine Bodenbegrünung zulassen – was positive Effekte auf die Biodiversität haben kann. Wir haben die Effekte der Bodenbegrünung auf die Habitatansprüche der Heidelerche (Lullula arborea) erforscht, eine typische, insektivore Singvogelart der zentral- und südeuropäischen Weinberge. In einem ersten Schritt untersuchten wir die Rolle der Bodenbegrünung und ihrer Artenvielfalt auf die Lebensraumnutzung der Heidelerche, wobei wir verschiedene zusätzliche Habitatvariablen berücksichtigten. In einem nächsten Schritt wollten wir verstehen, ob die Präferenz der Heidelerchen für begrünte Weinberge möglicherweise durch eine erhöhte Beutedichte erklärt wird. Bodenlebende Wirbellose wurden mit Bodenfallen gefangen, welche wir in zwei unterschiedlichen Kategorien von Weinbergen platzierten: Solche, die von Heidelerchen besucht wurden (Präsenz Parzellen) und angrenzende Parzellen, in welchen wir keine Heidelerchen beobachteten (Pseudo-absenz Parzellen). Wir zeigen, dass hauptsächlich eine erhöhte Bodenbegrünung, Anzahl an Pflanzenarten und breitere Fahrgassen zwischen den Reblinien die Vorkommenswahrscheinlichkeit der Heidelerche beeinflussten. Die totale Abundanz der Wirbellosen war ebenfalls höher in begrünten Weinbergen. Auch die Abundanz und Anzahl der Käfer- und Spinnenfamilien konnten entweder durch eine erhöhte Bodenbegrünung, Pflanzenvielfalt oder breitere Fahrgassen erklärt werden. Wir schliessen daraus, dass eine weniger intensive Bewirtschaftungsweise, welche den Herbizideinsatz vermindert und dadurch eine vielfältige Pflanzengesellschaft ermöglicht, die Heidelerche und ihre Beute fördert und somit positive Effekte auf die Biodiversität auf mehreren trophischen Ebenen hat.

Notes

Acknowledgements

We thank all vine growers and the Valais association for viticulture (VITIVAL) for their support and collaboration, and for providing access to their vineyards. We are grateful to Livio Rey for field and lab assistance and Antoine Sierro for helping with site selection.

Author contributions

All authors contributed equally to this paper.

Funding

This study was supported by the Swiss National Science Foundation, Grant 31003A_149780 to Alain Jacot.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interest.

Ethical statement

The experiments conducted in this study comply with the current laws of the country in which they were performed.

Supplementary material

10336_2019_1666_MOESM1_ESM.docx (141 kb)
Supplementary material 1 (DOCX 141 kb)
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Supplementary material 2 (DOCX 2438 kb)
10336_2019_1666_MOESM3_ESM.docx (4.1 mb)
Supplementary material 3 (DOCX 4242 kb)

References

  1. Altieri MA, Nicholls CI (2002) The simplification of traditional vineyard based agroforests in northwestern Portugal: some ecological implications. Agrofor Syst 56:185–191CrossRefGoogle Scholar
  2. Archaux F, Gosselin F, Bergès L, Chevalier R (2006) Effects of sampling time, species richness and observer on the exhaustiveness of plant censuses. J Veg Sci 17:299–306CrossRefGoogle Scholar
  3. Arlettaz R, Schaad M, Reichlin TS, Schaub M (2010) Impact of weather and climate variation on Hoopoe reproductive ecology and population growth. J Ornithol 151:889–899CrossRefGoogle Scholar
  4. Arlettaz R, Maurer ML, Mosimann-Kampe P, Nussle S, Abadi F, Braunisch V, Schaub M (2012) New vineyard cultivation practices create patchy ground vegetation, favoring Woodlarks. J Ornithol 153:229–238CrossRefGoogle Scholar
  5. Assandri G, Bogliani G, Pedrini P, Brambilla M (2016) Diversity in the monotony? Habitat traits and management practices shape avian communities in intensive vineyards. Agric Ecosyst Environ 223:250–260CrossRefGoogle Scholar
  6. Assandri G, Bogliani G, Pedrini P, Brambilla M (2017a) Assessing common birds’ ecological requirements to address nature conservation in permanent crops: lessons from Italian vineyards. J Environ Manag 191:145–154CrossRefGoogle Scholar
  7. Assandri G, Giacomazzo M, Brambilla M, Griggio M, Pedrini P (2017b) Nest density, nest-site selection, and breeding success of birds in vineyards: management implications for conservation in a highly intensive farming system. Biol Conserv 205:23–33CrossRefGoogle Scholar
  8. Assandri G, Bogliani G, Pedrini P, Brambilla M (2018) Beautiful agricultural landscapes promote cultural ecosystem services and biodiversity conservation. Agric Ecosyst Environ 256:200–210CrossRefGoogle Scholar
  9. Atkinson PW, Fuller RJ, Vickery JA, Conway GJ, Tallowin JRB, Smith REN, Haysom KA, Ings TC, Asteraki EJ, Brown VK (2005) Influence of agricultural management, sward structure and food resources on grassland field use by birds in lowland England. J Appl Ecol 42:932–942CrossRefGoogle Scholar
  10. Balmford A, Jayasuriya AHM, Green MJB (1996) Using higher-taxon richness as a surrogate for species richness: II. Local applications. P Roy Soc B Biol Sci 263:1571–1575CrossRefGoogle Scholar
  11. Bartón K (2016) MuMIn: multi-model inference. R package version 1.10.6. https://CRAN.R-project.org/package=MuMIn
  12. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  13. Benton TG, Bryant DM, Cole L, Crick HQP (2002) Linking agricultural practice to insect and bird populations: a historical study over three decades. J Appl Ecol 39:673–687CrossRefGoogle Scholar
  14. Benton TG, Vickery JA, Wilson JD (2003) Farmland biodiversity: is habitat heterogeneity the key? Trends Ecol Evol 18:182–188CrossRefGoogle Scholar
  15. Biaggini M, Consorti R, Dapporto L, Dellacasa M, Paggetti E, Corti C (2007) The taxonomic level order as a possible tool for rapid assessment of arthropod diversity in agricultural landscapes. Agric Ecosyst Environ 122:183–191CrossRefGoogle Scholar
  16. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135CrossRefGoogle Scholar
  17. Bowden CGR (1990) Selection of foraging habitats by Woodlarks (Lullula arborea) nesting in pine plantations. J Appl Ecol 27:410–419CrossRefGoogle Scholar
  18. Brambilla M, Rubolini D (2009) Intra-seasonal changes in distribution and habitat associations of a multi-brooded bird species: implications for conservation planning. Anim Conserv 12:71–77CrossRefGoogle Scholar
  19. Brambilla M, Falco R, Negri I (2012) A spatially explicit assessment of within-season changes in environmental suitability for farmland birds along an altitudinal gradient. Anim Conserv 15:638–647CrossRefGoogle Scholar
  20. Brambilla M, Ilahiane L, Assandri G, Ronchi S, Bogliani G (2017) Combining habitat requirements of endemic bird species and other ecosystem services may synergistically enhance conservation efforts. Sci Total Environ 586:206–214CrossRefGoogle Scholar
  21. Buehler R, Bosco L, Arlettaz R, Jacot A (2017) Nest site preferences of the Woodlark (Lullula arborea) and its association with artificial nest predation. Acta Oecol 78:41–46CrossRefGoogle Scholar
  22. Burfield I, Bommel FV, Gallo-Orsi U (2004) Birds in Europe population estimates, trends and conservation status. BirdLife International, CambridgeGoogle Scholar
  23. Burgio G, Marchesini E, Reggiani N, Montepaone G, Schiatti P, Sommaggio D (2016) Habitat management of organic vineyard in northern Italy: the role of cover plants management on arthropod functional biodiversity. Bull Entomol Res 106:759–768CrossRefGoogle Scholar
  24. Campedelli T, Londi G, La Gioia G, Frassanito AG, Florenzano GT (2015) Steppes vs crops: is cohabitation for biodiversity possible? Lessons from a national park in southern Italy. Agric Ecosyst Environ 213:32–38CrossRefGoogle Scholar
  25. Caprio E, Nervo B, Isaia M, Allegro G, Rolando A (2015) Organic versus conventional systems in viticulture: comparative effects on spiders and carabids in vineyards and adjacent forests. Agric Syst 136:61–69CrossRefGoogle Scholar
  26. Castro-Caro JC, Carpio AJ, Tortosa FS (2014) Herbaceous ground cover reduces nest predation in olive groves. Bird Study 61:537–543CrossRefGoogle Scholar
  27. Conway G, Wotton S, Henderson I, Eaton M, Drewitt A, Spencer J (2009) The status of breeding Woodlarks Lullula arborea in Britain in 2006. Bird Study 56:310–325CrossRefGoogle Scholar
  28. Coudrain V, Arlettaz R, Schaub M (2010) Food or nesting place? Identifying factors limiting Wryneck populations. J Ornithol 151:867–880CrossRefGoogle Scholar
  29. Dormann CF, Elith J, Bacher S et al (2012) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36:27–46CrossRefGoogle Scholar
  30. Fischer J, Brosi B, Daily GC, Ehrlich PR, Goldman R, Goldstein J, Lindenmayer DB, Manning AD, Mooney HA, Pejchar L, Ranganathan J, Tallis H (2008) Should agricultural policies encourage land sparing or wildlife-friendly farming? Front Ecol Environ 6:382–387CrossRefGoogle Scholar
  31. Foley JA, Ramankutty N, Brauman KA et al (2011) Solutions for a cultivated planet. Nature 478:337–342CrossRefGoogle Scholar
  32. Gelman A, Su YS (2015) Arm: data analysis using regression and multilevel/hierarchical models. R package version 1.9-3. http://CRAN.R-project.org/package=arm
  33. Gillespie M, Wratten SD (2012) The importance of viticultural landscape features and ecosystem service enhancement for native butterflies in New Zealand vineyards. J Insect Conserv 16:13–23CrossRefGoogle Scholar
  34. Gillies CS, Hebblewhite M, Nielsen SE, Krawchuk MA, Aldridge CL, Frair JL, Saher DJ, Stevens CE, Jerde CL (2006) Application of random effects to the study of resource selection by animals. J Anim Ecol 75:887–898CrossRefGoogle Scholar
  35. Glutz von Blotzheim UN, Bauer KM (1985) Handbuch der Vögel Mitteleuropas. Aula-Verlag, WiesbadenGoogle Scholar
  36. Graham MH (2003) Confronting multicollinearity in ecological multiple regression. Ecology 84:2809–2815CrossRefGoogle Scholar
  37. Guillod N, Arlettaz R, Jacot A (2016) Impact of spatial variation of a crucial prey, the molecricket, on Hoopoe territory occupancy and reproduction. J Avian Biol 47:697–705CrossRefGoogle Scholar
  38. Guyot C, Arlettaz R, Korner P, Jacot A (2017) Temporal and spatial scales matter: circannual habitat selection by bird communities in vineyards. PLoS One 12:e0170176.  https://doi.org/10.1371/journal.pone.0170176 CrossRefGoogle Scholar
  39. Hallmann CA, Foppen RPB, van Turnhout CAM, de Kroon H, Jongejans E (2014) Declines in insectivorous birds are associated with high neonicotinoid concentrations. Nature 511:341–343CrossRefGoogle Scholar
  40. Harrison CJO, Forster J (1959) Woodlark territories. Bird Study 6:60–68CrossRefGoogle Scholar
  41. Heldbjerg H, Sunde P, Fox AD (2018) Continuous population declines for specialist farmland birds 1987–2014 in Denmark indicates no halt in biodiversity loss in agricultural habitats. Bird Conserv Int 28(2):278–292CrossRefGoogle Scholar
  42. Keller V, Ayé R, Müller W, Spaar R, Zbinden N (2010a) Species of national conservation concern in Switzerland: revision 2010. Ornithol Beob 107:265–285Google Scholar
  43. Keller V, Gerber A, Schmid H, Volet B, Zbinden N (2010b) Rote Liste Brutvögel. Gefährdete Arten der Schweiz, Stand 2010. Bundesamt für Umwelt/Schweizerische Vogelwarte, Bern/SempachGoogle Scholar
  44. Korner-Nievergelt F (2015) Bayesian data analysis in ecology using linear models with R, BUGS, and Stan. Academic Press, AmsterdamGoogle Scholar
  45. Mallord JW, Dolman PM, Brown A, Sutherland WJ (2007) Nest-site characteristics of Woodlarks Lullula arborea breeding on heathlands in southern England: are there consequences for nest survival and productivity? Bird Study 54:307–314CrossRefGoogle Scholar
  46. Mendenhall CD, Karp DS, Meyer CFJ, Hadly EA, Daily GC (2014) Predicting biodiversity change and averting collapse in agricultural landscapes. Nature 509:213–217CrossRefGoogle Scholar
  47. Menz MHM, Mosimann-Kampe P, Arlettaz R (2009) Foraging habitat selection in the last Ortolan Bunting Emberiza hortulana population in Switzerland: final lessons before extinction. Ardea 97:323–333CrossRefGoogle Scholar
  48. Pithon JA, Beaujouan V, Daniel H, Pain G, Vallet J (2016) Are vineyards important habitats for birds at local or landscape scales? Basic Appl Ecol 17:240–251CrossRefGoogle Scholar
  49. Praus L, Hegemann A, Tieleman BI, Weidinger K (2014) Predators and predation rates of Skylark Alauda arvensis and Woodlark Lullula arborea nests in a semi-natural area in the Netherlands. Ardea 102:87–94CrossRefGoogle Scholar
  50. Puig-Montserrat X, Stefanescu C, Torre I, Palet J, Fabregas E, Dantart J, Arrizabalaga A, Flaquer C (2017) Effects of organic and conventional crop management on vineyard biodiversity. Agric Ecosyst Environ 243:19–26CrossRefGoogle Scholar
  51. QGIS Development Team (2018) QGIS geographic information system. Open source geospatial foundation project. http://qgis.osgeo.org
  52. R Development Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/
  53. Schaefer T, Vogel B (2000) Why do Woodlarks need field-forest ecotones? An analysis of possible factors. J Ornithol 141:335–344CrossRefGoogle Scholar
  54. Schaub M, Martinez N, Tagmann-Ioset A, Weisshaupt N, Maurer ML, Reichlin TS, Abadi F, Zbinden N, Jenni L, Arlettaz R (2010) Patches of bare ground as a staple commodity for declining ground-foraging insectivorous farmland birds. PLoS One 5:e13115CrossRefGoogle Scholar
  55. Schmitt T, Augenstein B, Finger A (2008) The influence of changes in viticulture management on the butterfly (Lepidoptera) diversity in a wine growing region of southwestern Germany. Eur J Entomol 105:249–255CrossRefGoogle Scholar
  56. Searcy WA (1979) Female choice of mates—general model for birds and its application to red-winged blackbirds (Agelaius phoeniceus). Am Nat 114:77–100CrossRefGoogle Scholar
  57. Sierro A, Arlettaz R (2003) L’avifaune du vignoble en Valais central: évaluation de la diversité à l’aide de transects. Nos Oiseaux 50:89–100Google Scholar
  58. Sirami C, Brotons L, Martin JL (2011) Woodlarks Lullula arborea and landscape heterogeneity created by land abandonment. Bird Study 58:99–106CrossRefGoogle Scholar
  59. Strebel G, Jacot A, Horch P, Spaar R (2015) Effects of grassland intensification on Whinchats Saxicola rubetra and implications for conservation in upland habitats. IBIS 157:250–259CrossRefGoogle Scholar
  60. The European Parliament and the Council of the European Union (2010) Legislation L20. Directive 2009/147/EC of the European parliament and of the Council of 30 November 2009 on the conservation of wild birds. Off J Eur Union 53:7–25. https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A32009L0147
  61. Thomson LJ, Hoffmann AA (2009) Vegetation increases the abundance of natural enemies in vineyards. Biol Control 49:259–269CrossRefGoogle Scholar
  62. Traba J, Morales MB, de la Morena ELG, Delgado MP, Kristin A (2008) Selection of breeding territory by little bustard (Tetrax tetrax) males in Central Spain: the role of arthropod availability. Ecol Res 23:615–622CrossRefGoogle Scholar
  63. Trivellone V, Schoenenberger N, Bellosi B, Jermini M, de Bello F, Mitchell EAD, Moretti M (2014) Indicators for taxonomic and functional aspects of biodiversity in the vineyard agroecosystem of southern Switzerland. Biol Conserv 170:103–109CrossRefGoogle Scholar
  64. Tscharntke T, Clough Y, Wanger TC, Jackson L, Motzke I, Perfecto I, Vandermeer J, Whitbread A (2012) Global food security, biodiversity conservation and the future of agricultural intensification. Biol Conserv 151:53–59CrossRefGoogle Scholar
  65. Vandermeer J, Perfecto I (2007) The agricultural matrix and a future paradigm for conservation. Conserv Biol 21:274–277CrossRefGoogle Scholar
  66. Vickery J, Arlettaz R (2012) The importance of habitat heterogeneity at multiple scales for birds in European agricultural landscapes. In: Fuller RJ (ed) Birds and habitat: relationships in changing landscapes. Cambridge University Press, Cambridge, pp 177–204CrossRefGoogle Scholar
  67. Viers JH, Williams JN, Nicholas KA, Barbosa O, Kotze I, Spence L, Webb LB, Merenlender A, Reynolds M (2013) Vinecology: pairing wine with nature. Conserv Lett 6:287–299Google Scholar
  68. Williams PH, Gaston KJ (1994) Measuring more of biodiversity—can higher-taxon richness predict wholesale species richness. Biol Conserv 67:211–217CrossRefGoogle Scholar

Copyright information

© Deutsche Ornithologen-Gesellschaft e.V. 2019

Authors and Affiliations

  1. 1.Division of Conservation Biology, Institute of Ecology and Evolution (IEE)University of BernBernSwitzerland
  2. 2.Swiss Ornithological Institute, Valais Field StationSionSwitzerland

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