Skip to main content

Advertisement

Log in

Bird predation enhances tree seedling resistance to insect herbivores in contrasting forest habitats

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

Abstract

According to the associational resistance hypothesis, neighbouring plants are expected to influence both the insect herbivore communities and their natural enemies. However, this has rarely been tested for the effects of canopy trees on herbivory of seedlings. One possible mechanism responsible for associational resistance is the indirect impact of natural enemies on insect herbivory, such as insectivorous birds. But it remains unclear to what extent such trophic cascades are influenced by the composition of plant associations (i.e. identity of ‘associated’ plants). Here, we compared the effect of bird exclusion on insect leaf damage for seedlings of three broadleaved tree species in three different forest habitats. Exclusion of insectivorous birds affected insect herbivory in a species-specific manner: leaf damage increased on Betula pendula seedlings whereas bird exclusion had no effect for two oaks (Quercus robur and Q. ilex). Forest habitat influenced both the extent of insect herbivory and the effect of bird exclusion. Broadleaved seedlings had lower overall leaf damage within pine plantations than within broadleaved stands, consistent with the resource concentration hypothesis. The indirect effect of bird exclusion on leaf damage was only significant in pine plantations, but not in exotic and native broadleaved woodlands. Our results support the enemies hypothesis, which predicts that the effects of insectivorous birds on insect herbivory on seedlings are greater beneath non-congeneric canopy trees. Although bird species richness and abundance were greater in broadleaved woodlands, birds were unable to regulate insect herbivory on seedlings in forests of more closely related tree species.

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

Similar content being viewed by others

References

  • Atlegrim O (1989) Exclusion of birds from bilberry stands—impact on insect larval density and damage to the bilberry. Oecologia 79:136–139

    Article  Google Scholar 

  • Barbaro L, Pontcharraud L, Vetillard F, Guyon D, Jactel H (2005) Comparative responses of bird, carabid, and spider assemblages to stand and landscape diversity in maritime pine plantation forests. Ecoscience 12:110–121

    Article  Google Scholar 

  • Barbaro L, van Halder I (2009) Linking bird, carabid beetle and butterfly life-history traits to habitat fragmentation in mosaic landscapes. Ecography 32:321–333

    Article  Google Scholar 

  • Barber NA, Marquis RJ (2009) Spatial variation in top-down direct and indirect effects on white oak (Quercus alba L.). Am Midl Nat 162:169–179

    Article  Google Scholar 

  • Barbosa P, Hines J, Kaplan I, Martinson H, Szczepaniec A, Szendrei Z (2009) Associational resistance and associational susceptibility: having right or wrong neighbors. Annu Rev Ecol Evol Syst 40:1–20

    Article  Google Scholar 

  • Batzer HO, Benzie JW, Popp MP (1987) Spruce budworm damage in aspen/balsam fir stands affected by cutting methods. North J Appl For 4:73–75

    Google Scholar 

  • Björkman M, Hambäck PA, Hopkins RJ, Rämert B (2010) Evaluating the enemies hypothesis in a clover-cabbage intercrop: effects of generalist and specialist natural enemies on the turnip root fly (Delia floralis). Agric For Entomol 12:123–132

    Article  Google Scholar 

  • Bock CE, Bock JH, Grant MC (1992) Effects of bird predation on grasshopper densities in an Arizona grassland. Ecology 73:1706–1717

    Article  Google Scholar 

  • Borenstein M, Hedges LV, Higgins JPT, Rothstein HR (2009) Introduction to meta-analysis, 1st edn. Wiley, Chichester

    Book  Google Scholar 

  • Bridgeland WT, Beier P, Kolb T, Whitham TG (2010) A conditional trophic cascade: birds benefit faster growing trees with strong links between predators and plants. Ecology 91:73–84

    Article  PubMed  Google Scholar 

  • Brockerhoff EG, Jactel H, Parrota JA, Quine CP, Sayer J (2008) Plantation forests and biodiversity: oxymoron or opportunity? Biodivers Conserv 17:925–951

    Article  Google Scholar 

  • Coley PD, Bryant JP, Chapin FS III (1985) Resource availability and plant antiherbivore defense. Science 230:895–899

    Article  PubMed  CAS  Google Scholar 

  • Crawley MJ (1989) Insect herbivores and plant-population dynamics. Annu Rev Entomol 34:531–564

    Article  Google Scholar 

  • Dial R, Roughgarden J (1995) Experimental removal of insectivores from rain forest canopy: direct and indirect effects. Ecology 76:1821–1834

    Article  Google Scholar 

  • Finch S, Collier RH (2000) Host-plant selection by insects—a theory based on ‘appropriate/inappropriate landings’ by pest insects of cruciferous plants. Entomol Exp Appl 96:91–102

    Article  Google Scholar 

  • Forkner RE, Hunter MD (2000) What goes up must come down? Nutrient addition and predation pressure on oak herbivores. Ecology 81:1588–1600

    Article  Google Scholar 

  • Giertych MJ, Karolewski P, Zytkowiak R, Oleksyn J (2006) Differences in defence strategies against herbivores between two pioneer tree species: Alnus glutinosa (L.) Gaertn. and Betula pendula. Roth. Pol J Ecol 54:181–187

    Google Scholar 

  • Glen DM (2004) Birds as predators of lepidopterous larvae. In: Van Emden HF, Rothschild M (eds) Insect and Bird Interactions. Intercept, Andover, pp 89–108

    Google Scholar 

  • González-Gómez P, Estades CF, Simonetti JA (2006) Strengthened insectivory in a temperate fragmented forest. Oecologia 148:137–143

    Article  PubMed  Google Scholar 

  • Greenberg R, Bichier P, Angon AC, MacVean C, Perez R, Cano E (2000) The impact of avian insectivory on arthropods and leaf damage in some Guatemalan coffee plantations. Ecology 81:1750–1755

    Article  Google Scholar 

  • Greenberg R, Bichier P, Angon AC, Reitsma R (1997) Bird populations in shade and sun coffee plantations in Central Guatemala. Conserv Biol 11:448–459

    Article  Google Scholar 

  • Hedges LV, Olkin I (1985) Statistical methods for meta-analysis. Academic, New York

    Google Scholar 

  • Holmes RT (1990) Ecological and evolutionary impacts of bird predation on forest insects: an overview. Stud Avian Biol 13:6–13

    Google Scholar 

  • Holmes RT, Schultz JC, Nothnagle P (1979) Bird predation on forest insects: an exclosure experiment. Science 206:462–463

    Article  PubMed  CAS  Google Scholar 

  • Jactel H, Brockerhoff EG (2007) Tree diversity reduces herbivory by forest insects. Ecol Lett 10:835–848

    Article  PubMed  Google Scholar 

  • Kaitaniemi P, Riihimaki J, Koricheva J, Vehvilainen H (2007) Experimental evidence for associational resistance against the European pine sawfly in mixed tree stands. Silva Fenn 41:259–268

    Google Scholar 

  • Kalka MB, Smith AR, Kalko EKV (2008) Bats limit arthropods and herbivory in a tropical forest. Science 320:71

    Article  PubMed  CAS  Google Scholar 

  • Karban R (2010) Neighbors affect resistance to herbivory—a new mechanism. New Phytol 186:564–566

    Article  PubMed  Google Scholar 

  • Keenan R, Lamb D, Sexton G (1995) Experience with mixed species rainforest plantations in North Queensland. Commonw For Rev 74:315–321

    Google Scholar 

  • Lemen C (1981) Elm trees and elm leaf beetles—patterns of herbivory. Oikos 36:65–67

    Article  Google Scholar 

  • Low C, Connor EF (2003) Birds have no impact on folivorous insect guilds on a montane willow. Oikos 103:579–589

    Article  Google Scholar 

  • Maetô K, Fukuyama K (1997) Mature tree effect of Acer mono on seedling mortality due to insect herbivory. Ecol Res 12:337–343

    Article  Google Scholar 

  • Mäntylä E, Alessio GA, Blande JD, Heijari J, Holopainen JK, Laaksonen T, Piirtola P, Klemola T (2008) From plants to birds: higher avian predation rates in trees responding to insect herbivory. Plos ONE 3:e2832

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Marquis RJ, Whelan CJ (1994) Insectivorous birds increase growth of white oak through consumption of leaf-chewing insects. Ecology 75:2007–2014

    Article  Google Scholar 

  • Marquis RJ, Whelan CJ (1996) Plant morphology and recruitment of the third trophic level: subtle and little-recognized defenses? Oikos 75:330–334

    Article  Google Scholar 

  • Mazía CN, Thomas K, Enrique JC (2004) Interannual changes in folivory and bird insectivory along a natural productivity gradient in northern Patagonian forests. Ecography 27:29–40

    Article  Google Scholar 

  • Mooney KA, Gruner DS, Barber NA, Van Bael SA, Philpott SM, Greenberg R (2010) Interactions among predators and the cascading effects of vertebrate insectivores on arthropod communities and plants. Proc Natl Acad Sci USA 107:7335–7340

    Article  PubMed  CAS  Google Scholar 

  • Nakagawa S, Cuthill IC (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev 82:591–605

    Article  PubMed  Google Scholar 

  • Norghauer JM, Grogan J, Malcolm JR, Felfili JM (2010) Long-distance dispersal helps germinating mahogany seedlings escape defoliation by a specialist caterpillar. Oecologia 162:405–412

    Article  PubMed  Google Scholar 

  • Pace ML, Cole JJ, Carpenter SR, Kitchell JF (1999) Trophic cascades revealed in diverse ecosystems. Trends Ecol Evol 14:483–488

    Article  PubMed  Google Scholar 

  • Perfecto I, Vandermeer JH, Bautista GL, Nuñez GI, Greenberg R, Bichier P, Langridge S (2004) Greater predation in shaded coffee farms: the role of resident neotropical birds. Ecology 85:2677–2681

    Article  Google Scholar 

  • Philpott SM, Soong O, Lowenstein JH, Pulido AL, Lopez DT, Flynn DFB, DeClerck F (2009) Functional richness and ecosystem services: bird predation on arthropods in tropical agroecosystems. Ecol Appl 19:1858–1867

    Article  PubMed  Google Scholar 

  • Pigot AL, Leather SR (2008) Invertebrate predators drive distance-dependent patterns of seedling mortality in a temperate tree Acer pseudoplatanus. Oikos 117:521–530

    Article  Google Scholar 

  • Pinheiro J, Bates D (2004) Mixed-effects models in S and S-PLUS. Springer, New York

    Google Scholar 

  • Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu Rev Ecol Syst 11:41–65

    Article  Google Scholar 

  • R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing. V, Austria, ISBN:3-900051-07-0, http://www.R-project.org

  • 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

    Article  PubMed  Google Scholar 

  • Robinson SK, Holmes RT (1984) Effects of plant-species and foliage structure on the foraging behavior of forest birds. Auk 101:672–684

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Rosenberg MS, Adams DC, Gurevitch J (2000) Metawin: statistical software for meta-analysis, version 2.0. Sinauer, Sunderland

    Google Scholar 

  • Russell EP (1989) Enemies hypothesis: a review of the effect of vegetational diversity on predatory insects and parasitoids. Environ Entomol 18:590–599

    Google Scholar 

  • Schuldt A, Baruffol M, Böhnke M, Bruelheide H, Härdtle W, Lang AC, Nadrowski K, Von Oheimb G, Voigt W, Zhou H, Assmann T (2010) Tree diversity promotes insect herbivory in subtropical forests of south-east China. J Ecol 98:917–926

    Article  PubMed  Google Scholar 

  • Sipura M (1999) Tritrophic interactions: willows, herbivorous insects and insectivorous birds. Oecologia 121:537–545

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Van Bael SA, Philpott SM, Greenberg R, Bichier P, Barber NA, Mooney KA, Gruner DS (2008) Birds as predators in tropical agroforestery systems. Ecology 89:928–934

    Article  PubMed  Google Scholar 

  • van Halder I, Barbaro L, Corcket E, Jactel H (2008) Importance of semi-natural habitats for the conservation of butterfly communities in landscapes dominated by pine plantations. Biodivers Conserv 17:1149–1169

    Article  Google Scholar 

  • Vásquez PA, Grez AA, Bustamante RO, Simonetti JA (2007) Herbivory, foliar survival and shoot growth in fragmented populations of Aristotelia chilensis. Acta Oecol 31:48–53

    Article  Google Scholar 

  • Vehviläinen H, Koricheva J, Ruohomäki K (2007) Tree species diversity influences herbivore abundance and damage: meta-analysis of long-term forest experiments. Oecologia 152:287–298

    Article  PubMed  Google Scholar 

  • Vehviläinen H, Koricheva J, Ruohomäki K (2008) Effects of stand tree species composition and diversity on abundance of predatory arthropods. Oikos 117:935–943

    Article  Google Scholar 

  • Vehviläinen H, Koricheva J, Ruohomäki K, Johansson T, Valkonen S (2006) Effects of tree stand species composition on insect herbivory of silver birch in boreal forests. Basic Appl Ecol 7:1–11

    Article  Google Scholar 

  • Whelan CJ (2001) Foliage structure influences foraging of insectivorous forest birds: an experimental study. Ecology 82:219–231

    Article  Google Scholar 

  • Whelan CJ, Wenny DG, Marquis RJ (2008) Ecosystem services provided by birds. Ann NY Acad Sci 1134:25–60

    Article  PubMed  Google Scholar 

  • White JA, Whitham TG (2000) Associational susceptibility of cottonwood to a box elder herbivore. Ecology 81:1795–1803

    Article  Google Scholar 

Download references

Acknowledgments

We thank Fabrice Vetillard and Pierre Menassieu for their help with constructing cages and the set-up of field experiments and Paul Tourneur and Amandine Blanc for assistance in the field. The authors declare that the experiments performed in this study comply with the current laws of France. Brice Giffard was supported by a grant from the French Ministry of Higher Education and Research. We thank Eckehard G. Brockerhoff, Christopher J. Whelan and one anonymous reviewer for invaluable comments on previous versions of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Brice Giffard.

Additional information

Communicated by Jacqui Shykoff.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 128 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Giffard, B., Corcket, E., Barbaro, L. et al. Bird predation enhances tree seedling resistance to insect herbivores in contrasting forest habitats. Oecologia 168, 415–424 (2012). https://doi.org/10.1007/s00442-011-2089-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-011-2089-7

Keywords

Navigation