, Volume 180, Issue 3, pp 619–630 | Cite as

Do birds see the forest for the trees? Scale-dependent effects of tree diversity on avian predation of artificial larvae

  • Evalyne W. MuiruriEmail author
  • Kalle Rainio
  • Julia Koricheva
Highlighted Student Research


The enemies hypothesis states that reduced insect herbivory in mixed-species stands can be attributed to more effective top–down control by predators with increasing plant diversity. Although evidence for this mechanism exists for invertebrate predators, studies on avian predation are comparatively rare and have not explicitly tested the effects of diversity at different spatial scales, even though heterogeneity at macro- and micro-scales can influence bird foraging selection. We studied bird predation in an established forest diversity experiment in SW Finland, using artificial larvae installed on birch, alder and pine trees. Effects of tree species diversity and densities on bird predation were tested at two different scales: between plots and within the neighbourhood around focal trees. At the neighbourhood scale, birds preferentially foraged on focal trees surrounded by a higher diversity of neighbours. However, predation rates did not increase with tree species richness at the plot level and were instead negatively affected by tree height variation within the plot. The highest probability of predation was observed on pine, and rates of predation increased with the density of pine regardless of scale. Strong tree species preferences observed may be due to a combination of innate bird species preferences and opportunistic foraging on profitable-looking artificial prey. This study therefore finds partial support for the enemies hypothesis and highlights the importance of spatial scale and focal tree species in modifying trophic interactions between avian predators and insect herbivores in forest ecosystems.


Biodiversity and ecosystem functioning Insectivorous birds Insect pests Satakunta forest diversity experiment Tri-trophic interactions 



We are grateful to Fatih Kayaanan, Miika Laihonen and Elisa Männistö for help in the field and to Ilkka Jussila for installation of the camera traps. This study was financially supported by the grant from the Kone Foundation.

Author contribution statement

JK designed the study, KR and JK conducted fieldwork, EWM performed statistical analyses and wrote the manuscript. All authors have been involved in editing the manuscript drafts.

Supplementary material

442_2015_3391_MOESM1_ESM.docx (126 kb)
Supplementary material 1 (DOCX 126 kb)


  1. Amo L, Jansen JJ, van Dam NM et al (2013) Birds exploit herbivore-induced plant volatiles to locate herbivorous prey. Ecol Lett 16:1348–1355. doi: 10.1111/ele.12177 CrossRefPubMedGoogle Scholar
  2. Anderson DR, Link WA, Johnson DH, Burnham KP (2001) Suggestions for presenting the results of data analyses. J Wildl Manag 65:373–378. doi: 10.2307/3803088 CrossRefGoogle Scholar
  3. Andow DA (1991) Vegetational diversity and arthropod population response. Annu Rev Entomol 36:561–586. doi: 10.1146/annurev.en.36.010191.003021 CrossRefGoogle Scholar
  4. Aplin LM, Farine DR, Cockburn A et al (2015) Experimentally induced innovations lead to persistent culture via conformity in wild birds. Nature 518:538–541. doi: 10.1038/nature13998 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Arvidsson B, Klaesson P (1986) Territory size in a willow warbler Phylloscopus trochilus population in mountain birch forest in Swedish Lapland. Ornis Scand 17:24–30. doi: 10.2307/3676749 CrossRefGoogle Scholar
  6. Barbosa P, Hines J, Kaplan I et al (2009) Associational resistance and associational susceptibility: having right or wrong neighbors. Annu Rev Ecol Evol Syst 40:1–20. doi: 10.1146/annurev.ecolsys.110308.120242 CrossRefGoogle Scholar
  7. Bates D, Maechler M, Bolker B (2012) lme4: Linear mixed-effects models using S4 classesGoogle Scholar
  8. Bereczki K, Csoka G, Ódor P, Baldi A (2012) Birds as control agents of caterpillars in oak forests. In: BOU proceedings ecosystem services: do we need birds?
  9. Bereczki K, Ódor P, Csóka G et al (2014) Effects of forest heterogeneity on the efficiency of caterpillar control service provided by birds in temperate oak forests. For Ecol Manag 327:96–105. doi: 10.1016/j.foreco.2014.05.001 CrossRefGoogle Scholar
  10. Bommarco R, Banks J (2003) Scale as modifier in vegetation diversity experiments: effects on herbivores and predators. Oikos 102:440–448CrossRefGoogle Scholar
  11. Brodmann PA, Reyer HU (1999) Nestling provisioning in water pipits (Anthus spinoletta): do parents go for specific nutrients or profitable prey? Oecologia 120:506–514. doi: 10.1007/s004420050884 CrossRefGoogle Scholar
  12. Burnham KP, Anderson DR (2004) Multimodel inference: understanding AIC and BIC in model selection. Sociol Methods Res 33:261–304. doi: 10.1177/0049124104268644 CrossRefGoogle Scholar
  13. Diaz M, Illeraz JC, Atienza JC (1998) Food resource matching by foraging tits Parus spp. during spring–summer in a Mediterranean mixed forest: evidence for an ideal free distribution. Ibis 140:654–660. doi: 10.1111/j.1474-919X.1998.tb04711.x CrossRefGoogle Scholar
  14. Eeva T, Lehikoinen E, Pohjalainen T (1997) Pollution-related variation in food supply and breeding success in two hole-nesting passerines. Ecology 78:1120–1131. doi:10.1890/0012-9658(1997)078[1120:PRVIFS]2.0.CO;2Google Scholar
  15. Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage, Thousand OaksGoogle Scholar
  16. Gabbe AP, Robinson SK, Brawn JD (2002) Tree-species preferences of foraging insectivorous birds: implications for floodplain forest restoration. Conserv Biol 16:462–470. doi: 10.1046/j.1523-1739.2002.00460.x CrossRefGoogle Scholar
  17. Giffard B, Corcket E, Barbaro L, Jactel H (2012) Bird predation enhances tree seedling resistance to insect herbivores in contrasting forest habitats. Oecologia 168:415–424. doi: 10.1007/s00442-011-2089-7 CrossRefPubMedGoogle Scholar
  18. Giffard B, Barbaro L, Jactel H, Corcket E (2013) Plant neighbours mediate bird predation effects on arthropod abundance and herbivory. Ecol Entomol 38:448–455. doi: 10.1111/een.12035 CrossRefGoogle Scholar
  19. Gripenberg S, Roslin T (2007) Up or down in space? Uniting the bottom-up versus top-down paradigm and spatial ecology. Oikos 116:181–188. doi: 10.1111/j.2006.0030-1299.15266.x CrossRefGoogle Scholar
  20. Groner E, Ayal Y (2001) The interaction between bird predation and plant cover in determining habitat occupancy of darkling beetles. Oikos 93:22–31. doi: 10.1034/j.1600-0706.2001.930102.x CrossRefGoogle Scholar
  21. Heinrich B, Collins S (1983) Caterpillar leaf damage, and the game of hide-and-seek with birds. Ecology 64:592–602. doi: 10.2307/1939978 CrossRefGoogle Scholar
  22. Hino T, Unno A, Nakano S (2002) Prey distribution and foraging preference for tits. Ornithol Sci 1:81–87. doi: 10.2326/osj.1.81 CrossRefGoogle Scholar
  23. Holmes R, Robinson S (1981) Tree species preferences of foraging insectivorous birds in a northern hardwoods forest. Oecologia 48:31–35. doi: 10.1007/BF00346985 CrossRefGoogle Scholar
  24. Howe A, Lövei GL, Nachman G (2009) Dummy caterpillars as a simple method to assess predation rates on invertebrates in a tropical agroecosystem. Entomol Exp Appl 131:325–329. doi: 10.1111/j.1570-7458.2009.00860.x CrossRefGoogle Scholar
  25. Huang Q, Swatantran A, Dubayah R, Goetz SJ (2014) The influence of vegetation height heterogeneity on forest and woodland bird species richness across the United States. PLoS ONE 9:e103236. doi: 10.1371/journal.pone.0103236 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Jactel H, Brockerhoff EG (2007) Tree diversity reduces herbivory by forest insects. Ecol Lett 10:835–848. doi: 10.1111/j.1461-0248.2007.01073.x CrossRefPubMedGoogle Scholar
  27. Johnson D (1980) The comparison of usage and availability measurements for evaluating resource preference. Ecology 61:65–71CrossRefGoogle Scholar
  28. Kaitaniemi P, Riihimäki J, Koricheva J, Vehviläinen H (2007) Experimental evidence for associational resistance against the European pine sawfly in mixed tree stands. Silva Fenn 41:259–268CrossRefGoogle Scholar
  29. Lang AC, Härdtle W, Bruelheide H et al (2011) Horizontal, but not vertical canopy structure is related to stand functional diversity in a subtropical slope forest. Ecol Res 27:181–189. doi: 10.1007/s11284-011-0887-3 CrossRefGoogle Scholar
  30. Langellotto GA, Denno RF (2004) Responses of invertebrate natural enemies to complex-structured habitats: a meta-analytical synthesis. Oecologia 139:1–10. doi: 10.1007/s00442-004-1497-3 CrossRefPubMedGoogle Scholar
  31. Letourneau DK, Jedlicka JA, Bothwell SG, Moreno CR (2009) Effects of natural enemy biodiversity on the suppression of arthropod herbivores in terrestrial ecosystems. Annu Rev Ecol Evol Syst 40:573–592. doi: 10.1146/annurev.ecolsys.110308.120320 CrossRefGoogle Scholar
  32. Letourneau DK, Armbrecht I, Rivera BS et al (2011) Does plant diversity benefit agroecosystems? A synthetic review. Ecol Appl 21:9–21. doi: 10.1890/09-2026.1 CrossRefPubMedGoogle Scholar
  33. Low PA, Sam K, McArthur C et al (2014) Determining predator identity from attack marks left in model caterpillars: guidelines for best practice. Entomol Exp Appl 152:120–126. doi: 10.1111/eea.12207 CrossRefGoogle Scholar
  34. MacArthur R, MacArthur J (1961) On bird species diversity. Ecology 42:594–598CrossRefGoogle Scholar
  35. Mäntylä E, Alessio GA, Blande JD et al (2008) From plants to birds: higher avian predation rates in trees responding to insect herbivory. PLoS ONE 3:e2832. doi: 10.1371/journal.pone.0002832 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Mäntylä E, Klemola T, Laaksonen T (2011) Birds help plants: a meta-analysis of top-down trophic cascades caused by avian predators. Oecologia 165:143–151. doi: 10.1007/s00442-010-1774-2 CrossRefPubMedGoogle Scholar
  37. Mason C (1997) Association between willow warbler Phylloscopus trochilus territories and birch in woodlands in southeastern England. Ibis 139:411–412. doi: 10.1111/j.1474-919X.1997.tb04648.x CrossRefGoogle Scholar
  38. Metcalfe DB, Asner GP, Martin RE et al (2014) Herbivory makes major contributions to ecosystem carbon and nutrient cycling in tropical forests. Ecol Lett 17:324–332. doi: 10.1111/ele.12233 CrossRefPubMedGoogle Scholar
  39. Muiruri EW, Milligan HT, Morath S, Koricheva J (2015) Moose browsing alters tree diversity effects on birch growth and insect herbivory. Funct Ecol 29:724–735. doi: 10.1111/1365-2435.12407 CrossRefGoogle Scholar
  40. Naef-Daenzer B, Keller LF (1999) The foraging performance of great and blue tits (Parus major and P. caeruleus) in relation to caterpillar development, and its consequences for nestling growth and fledging weight. J Anim Ecol 68:708–718. doi: 10.1046/j.1365-2656.1999.00318.x CrossRefGoogle Scholar
  41. Naef-Daenzer L, Naef-Daenzer B, Nager RG (2000) Prey selection and foraging performance of breeding Great Tits Parus major in relation to food availability. J Avian Biol 31:206–214. doi: 10.1034/j.1600-048X.2000.310212.x CrossRefGoogle Scholar
  42. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R 2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142. doi: 10.1111/j.2041-210x.2012.00261.x CrossRefGoogle Scholar
  43. Poch TJ, Simonetti JA (2013) Insectivory in Pinus radiata plantations with different degree of structural complexity. For Ecol Manag 304:132–136. doi: 10.1016/j.foreco.2013.04.044 CrossRefGoogle Scholar
  44. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical ComputingGoogle Scholar
  45. Riihimäki J, Kaitaniemi P, Koricheva J, Vehviläinen H (2005) Testing the enemies hypothesis in forest stands: the important role of tree species composition. Oecologia 142:90–97. doi: 10.1007/s00442-004-1696-y CrossRefPubMedGoogle Scholar
  46. Root RB (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol Monogr 43:95–124. doi: 10.2307/1942161 CrossRefGoogle Scholar
  47. Russell E (1989) Enemies hypothesis: a review of the effect of vegetational diversity on predatory insects and parasitoids. Environ Entomol 18:590–599CrossRefGoogle Scholar
  48. Schuldt A, Fahrenholz N, Brauns M et al (2008) Communities of ground-living spiders in deciduous forests: does tree species diversity matter? Biodivers Conserv 17:1267–1284. doi: 10.1007/s10531-008-9330-7 CrossRefGoogle Scholar
  49. Schuldt A, Both S, Bruelheide H et al (2011) Predator diversity and abundance provide little support for the enemies hypothesis in forests of high tree diversity. PLoS ONE 6:e22905. doi: 10.1371/journal.pone.0022905 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Siemann E, Tilman D, Haarstad J, Ritchie M (1998) Experimental tests of the dependence of arthropod diversity on plant diversity. Am Nat 152:738–750. doi: 10.1086/286204 CrossRefPubMedGoogle Scholar
  51. Šipoš J, Kindlmann P (2013) Effect of the canopy complexity of trees on the rate of predation of insects. J Appl Entomol 137:445–451. doi: 10.1111/jen.12015 CrossRefGoogle Scholar
  52. Smith JNM, Dawkins R (1971) The hunting behaviour of individual great tits in relation to spatial variations in their food density. Anim Behav 19:695–706. doi: 10.1016/S0003-3472(71)80173-2 CrossRefGoogle Scholar
  53. Sobek S, Scherber C, Steffan-Dewenter I, Tscharntke T (2009) Sapling herbivory, invertebrate herbivores and predators across a natural tree diversity gradient in Germany’s largest connected deciduous forest. Oecologia 160:279–288. doi: 10.1007/s00442-009-1304-2 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Sperber CF, Nakayama K, Valverde MJ, Neves FDS (2004) Tree species richness and density affect parasitoid diversity in cacao agroforestry. Basic Appl Ecol 5:241–251. doi: 10.1016/j.baae.2004.04.001 CrossRefGoogle Scholar
  55. Stephens DW, Krebs JR (1986) Foraging Theory, 1st edn. Princeton University Press, PrincetonGoogle Scholar
  56. Stostad HN, Menéndez R (2014) Woodland structure, rather than tree identity, determines the breeding habitat of willow warblers Phylloscopus trochilus in the northwest of England. Bird Study 61:246–254. doi: 10.1080/00063657.2014.901293 CrossRefGoogle Scholar
  57. Straub CS, Simasek NP, Dohm R et al (2014) Plant diversity increases herbivore movement and vulnerability to predation. Basic Appl Ecol 15:50–58. doi: 10.1016/j.baae.2013.12.004 CrossRefGoogle Scholar
  58. Strode PK (2009) Spring tree species use by migrating Yellow-Rumped Warblers in relation to phenology and food availability. Wilson J Ornithol 121:457–468. doi: 10.1676/05-148.1 CrossRefGoogle Scholar
  59. Tinbergen L (1960) The natural control of insects in pinewoods I. Factors influencing the intensity of predation by songbirds. Arch Neerl Zool 13:265–343CrossRefGoogle Scholar
  60. Tonhasca A (1993) Effects of agroecosystem diversification on natural enemies of soybean herbivores. Entomol Exp Appl 69:83–90CrossRefGoogle Scholar
  61. Van der Meij MAA, Bout RG (2004) Scaling of jaw muscle size and maximal bite force in finches. J Exp Biol 207:2745–2753. doi: 10.1242/jeb.01091 CrossRefPubMedGoogle Scholar
  62. Vehviläinen H, Koricheva J, Ruohomäki K (2008) Effects of stand tree species composition and diversity on abundance of predatory arthropods. Oikos 117:935–943. doi: 10.1111/j.2008.0030-1299.15972.x CrossRefGoogle Scholar
  63. Whelan CJ, Şekercioğlu ÇH, Wenny DG (2015) Why birds matter: from economic ornithology to ecosystem services. J Ornithol. doi: 10.1007/s10336-015-1229-y Google Scholar
  64. Wiens J, Rotenberry J (1981) Habitat associations and community structure of birds in shrubsteppe environments. Ecol Monogr 51:21–42. doi: 10.2307/2937305 CrossRefGoogle Scholar
  65. Xiong L-H, Wu X, Lu J-J (2010) Bird predation on concealed insects in a reed-dominated estuarine tidal marsh. Wetlands 30:1203–1211. doi: 10.1007/s13157-010-0104-0 CrossRefGoogle Scholar
  66. Zhang Y, Adams J (2011) Top-down control of herbivores varies with ecosystem types. J Ecol 99:370–372. doi: 10.1111/j.1365-2745.2010.01770.x Google Scholar
  67. Zou Y, Sang W, Bai F, Axmacher JC (2013) Relationships between plant diversity and the abundance and α-diversity of predatory ground beetles (Coleoptera: Carabidae) in a mature Asian temperate forest ecosystem. PLoS ONE 8:e82792. doi: 10.1371/journal.pone.0082792 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.School of Biological SciencesRoyal Holloway University of LondonSurreyUK
  2. 2.Department of BiologyUniversity of TurkuTurkuFinland

Personalised recommendations