Ecological Research

, Volume 33, Issue 1, pp 205–212 | Cite as

Tree diversity has contrasting effects on predation rates by birds and arthropods on three broadleaved, subtropical tree species

  • Bo Yang
  • Bin Li
  • Yuxuan He
  • Lipeng Zhang
  • Helge Bruelheide
  • Andreas Schuldt
Original Article

Abstract

Plant diversity is hypothesized to strengthen biological control by promoting top-down pressure of predators on herbivores. However, studies on the effects of plant diversity on actual predation rates are still scarce, particularly in forest ecosystems. We analyzed the effect of tree species richness, and the potential influence of neighbor tree density, on predation rates of arthropods and birds on artificial clay caterpillars in a large-scale forest biodiversity experiment in south-east China. Our study was focused on three broadleaved tree species that are frequently damaged by lepidopteran caterpillars. Predation rates were influenced by tree species richness on only one of the three tree species, on which arthropod predation increased and bird predation decreased with increasing tree species richness. Importantly, these relationships were mediated by neighbor tree density, being most pronounced when focal trees had fewer surrounding neighbor trees. Our findings indicate that low tree density reduced arthropod predator abundances and predation rates, but that negative effects of this reduction were compensated for in more diverse tree mixtures by a functionally more diverse predator community. In contrast, lower tree densities might have benefited insectivorous birds by making trees more accessible particularly in monocultures, which are often structurally more uniform and denser than tree mixtures. Overall, our results point to an important role of species-specific and density-dependent mechanisms in modifying the consequences of biodiversity loss on top-down effects in forest ecosystems. Future work should aim at separating the effects of different predator guilds and those of host diversity from host density.

Keywords

BEF-China biodiversity and ecosystem function density-dependence predator trophic interaction 

Notes

Acknowledgements

We thank Xuefei Yang, Chen Lin, Sabine Both, Keping Ma and all members of the BEF-China consortium that coordinated and helped with the establishment and maintenance of the experiment. We gratefully acknowledge funding by the German Research Foundation (DFG FOR 891/1, 891/2 and 891/3), the Sino-German Centre for Research Promotion in Beijing (GZ 524, 592, 698, 699, 785, 970 and 1020), and Jiangxi Provincial Department of Education (GJJ151285). BEF-China is supported by the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig (DFG FZT 118).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11284_2017_1531_MOESM1_ESM.docx (156 kb)
Supplementary material 1 (DOCX 155 kb)

References

  1. Barbaro L, Rusch A, Muiruri EW, Gravellier B, Thiery D, Castagneyrol B (2017) Avian pest control in vineyards is driven by interactions between bird functional diversity and landscape heterogeneity. J Appl Ecol 54:500–508CrossRefGoogle Scholar
  2. 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 40:1–20CrossRefGoogle Scholar
  3. Baruffol M et al (2013) Biodiversity promotes tree growth during succession in subtropical forest. PLoS ONE 8:e81246CrossRefGoogle Scholar
  4. Brown JH (2014) Why are there so many species in the tropics? J Biogeo 41:8–22CrossRefGoogle Scholar
  5. Bruelheide H et al (2014) Designing forest biodiversity experiments: general considerations illustrated by a new large experiment in subtropical China. Methods Ecol Evol 5:74–89CrossRefGoogle Scholar
  6. Franzreb KE (1983) A comparison of avian foraging behavior in unlogged and logged mixed-coniferous forest. Wilson Bull 95:60–76Google Scholar
  7. Gelman A (2008) Scaling regression inputs by dividing by two standard deviations. Stat Med 27:2865–2873CrossRefPubMedGoogle Scholar
  8. Haase J et al (2015) Contrasting effects of tree diversity on young tree growth and resistance to insect herbivores across three biodiversity experiments. Oikos 124:1674–1685CrossRefGoogle Scholar
  9. Haddad NM, Crutsinger GM, Gross K, Haarstad J, Knops JMH, Tilman D (2009) Plant species loss decreases arthropod diversity and shifts trophic structure. Ecol Lett 12:1029–1039CrossRefPubMedGoogle Scholar
  10. Hillebrand H, Matthiessen B (2009) Biodiversity in a complex world: consolidation and progress in functional biodiversity research. Ecol Lett 12:1405–1419CrossRefPubMedGoogle Scholar
  11. Holmes RT, Robinson SK (1981) Tree species preferences of foraging insectivorous birds in a northern hardwoods forest. Oecologia 48:31–35CrossRefPubMedGoogle Scholar
  12. 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 131:325–329CrossRefGoogle Scholar
  13. Jactel H, Brockerhoff EG (2007) Tree diversity reduces herbivory by forest insects. Ecol Lett 10:835–848CrossRefPubMedGoogle Scholar
  14. Koh LP, Menge DNL (2006) Rapid assessment of lepidoptera predation rates in neotropical forest fragments. Biotropica 38:132–134Google Scholar
  15. Koricheva J, Mulder CPH, Schmid B, Joshi J, Huss-Danell K (2000) Numerical responses of different trophic groups of invertebrates to manipulations of plant diversity in grasslands. Oecologia 125:271–282CrossRefPubMedGoogle Scholar
  16. Kröber W, Zhang S, Ehmig M, Bruelheide H (2014) Linking xylem hydraulic conductivity and vulnerability to the leaf economics spectrum—A cross-species study of 39 evergreen and deciduous broadleaved subtropical tree species. PLoS ONE 9:e109211CrossRefPubMedPubMedCentralGoogle Scholar
  17. Kuznetsova A, Brockhoff PB, Christensen RHB (2016) lmerTest: tests for random and fixed effects for linear mixed effect models (lmer objects of lme4 package). R package version 2.0-32. Available at https://CRAN.R-project.org/package=lmerTest
  18. Lefcheck JS (2016) PiecewiseSEM: Piecewise structural equation modelling in r for ecology, evolution, and systematics. Methods Ecol Evol 7:573–579CrossRefGoogle Scholar
  19. Leles B, Xiao X, Pasion BO, Nakamura A, Tomlinson KW (2017) Does plant diversity increase top–down control of herbivorous insects in tropical forest? Oikos 126:1142–1149CrossRefGoogle Scholar
  20. 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 40:573–592CrossRefGoogle Scholar
  21. Lövei GL, Ferrante M (2017) A review of the sentinel prey method as a way of quantifying invertebrate predation under field conditions. Insect Sci 24:528–542CrossRefPubMedGoogle Scholar
  22. Low PA, Sam K, McArthur C, Posa MRC, Hochuli DF (2014) Determining predator identity from attack marks left in model caterpillars: guidelines for best practice. Entomol Exp Appl 152:120–126CrossRefGoogle Scholar
  23. Marquard E, Weigelt A, Roscher C, Gubsch M, Lipowsky A, Schmid B (2009) Positive biodiversity–productivity relationship due to increased plant density. J Ecol 97:696–704CrossRefGoogle Scholar
  24. Moles AT, Ollerton J (2016) Is the notion that species interactions are stronger and more specialized in the tropics a zombie idea? Biotropica 48:141–145CrossRefGoogle Scholar
  25. 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 107:7335–7340CrossRefPubMedPubMedCentralGoogle Scholar
  26. Muiruri EW, Rainio K, Koricheva J (2016) Do birds see the forest for the trees? Scale-dependent effects of tree diversity on avian predation of artificial larvae. Oecologia 180:619–630CrossRefPubMedGoogle Scholar
  27. Ozanne CMP, Speight MR, Hambler C, Evans HF (2000) Isolated trees and forest patches: Patterns in canopy arthropod abundance and diversity in Pinus sylvestris (Scots Pine). Forest Ecol Manag 137:53–63CrossRefGoogle Scholar
  28. Powell S, Costa AN, Lopes CT, Vasconcelos HL (2011) Canopy connectivity and the availability of diverse nesting resources affect species coexistence in arboreal ants. J Anim Ecol 80:352–360CrossRefPubMedGoogle Scholar
  29. Richards LA, Coley PD (2007) Seasonal and habitat differences affect the impact of food and predation on herbivores: a comparison between gaps and understory of a tropical forest. Oikos 116:31–40CrossRefGoogle Scholar
  30. Riihimäki J, Vehviläinen H, Kaitaniemi P, Koricheva J (2006) Host tree architecture mediates the effect of predators on herbivore survival. Ecol Entomol 31:227–235CrossRefGoogle Scholar
  31. Robinson SK, Holmes RT (1982) Foraging behavior of forest birds: the relationships among search tactics, diet, and habitat structure. Ecology 63:1918–1931CrossRefGoogle Scholar
  32. Root RB (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol Monogr 43:95–124CrossRefGoogle Scholar
  33. Roslin T et al (2017) Higher predation risk for insect prey at low latitudes and elevations. Science 356:742–744CrossRefPubMedGoogle Scholar
  34. Sam K, Remmel T, Molleman F (2015) Material affects attack rates on dummy caterpillars in tropical forest where arthropod predators dominate: an experiment using clay and dough dummies with green colourants on various plant species. Entomol Exp Appl 157:317–324CrossRefGoogle Scholar
  35. Schemske DW, Mittelbach GG, Cornell HV, Sobel JM, Roy K (2009) Is there a latitudinal gradient in the importance of biotic interactions? Annu Rev Ecol Evol Syst 40:245–269CrossRefGoogle Scholar
  36. Schmitz OJ (2006) Predators have large effects on ecosystem properties by changing plant diversity, not plant biomass. Ecology 87:1432–1437CrossRefPubMedGoogle Scholar
  37. Schuldt A, Scherer-Lorenzen M (2014) Non-native tree species (Pseudotsuga menziesii) strongly decreases predator biomass and abundance in mixed-species plantations of a tree diversity experiment. Forest Ecol Manag 327:10–17CrossRefGoogle Scholar
  38. Schuldt A, Both S, Bruelheide H, Härdtle W, Schmid B, Zhou H, Assmann T (2011) Predator diversity and abundance provide little support for the enemies hypothesis in forests of high tree diversity. PLoS ONE 6:e22905CrossRefPubMedPubMedCentralGoogle Scholar
  39. Schuldt A, Bruelheide H, Durka W, Michalski SG, Purschke O, Assmann T (2014) Tree diversity promotes functional dissimilarity and maintains functional richness despite species loss in predator assemblages. Oecologia 174:533–543CrossRefPubMedGoogle Scholar
  40. Schuldt A et al (2015) Early positive effects of tree species richness on herbivory in a large-scale forest biodiversity experiment influence tree growth. J Ecol 103:563–571CrossRefPubMedPubMedCentralGoogle Scholar
  41. Schuldt A et al (2017a) Belowground top-down and aboveground bottom-up effects structure multitrophic community relationships in a biodiverse forest. Sci Rep 7:4222CrossRefPubMedPubMedCentralGoogle Scholar
  42. Schuldt A et al (2017b) Herbivore and pathogen effects on tree growth are additive, but mediated by tree diversity and plant traits. Ecol Evol 7:7462–7474CrossRefPubMedPubMedCentralGoogle Scholar
  43. Shipley B (2009) Confirmatory path analysis in a generalized multilevel context. Ecology 90:363–368CrossRefPubMedGoogle Scholar
  44. 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 160:279–288CrossRefPubMedPubMedCentralGoogle Scholar
  45. Sperber CF, Nakayama K, Valverde MJ, Neves FdS (2004) Tree species richness and density affect parasitoid diversity in cacao agroforestry. Basic Appl Ecol 5:241–251CrossRefGoogle Scholar
  46. Vehviläinen H, Koricheva J, Ruohomaki K (2008) Effects of stand tree species composition and diversity on abundance of predatory arthropods. Oikos 117:935–943CrossRefGoogle Scholar
  47. Whelan CJ (2001) Foliage structure influences foraging of insectivorous forest birds: an experimental study. Ecology 82:219–231CrossRefGoogle Scholar
  48. Yang X et al (2013) Establishment success in a forest biodiversity and ecosystem functioning experiment in subtropical China (BEF-China). Eur J Forest Res 132:593–606CrossRefGoogle Scholar
  49. Zhang Y, Adams J (2011) Top-down control of herbivores varies with ecosystem types. J Ecol 99:370–372Google Scholar
  50. Zhang J et al (2017) Tree diversity promotes generalist herbivore community patterns in a young subtropical forest experiment. Oecologia 183:455–467CrossRefPubMedGoogle Scholar

Copyright information

© The Ecological Society of Japan 2017

Authors and Affiliations

  1. 1.Key Laboratory of Plant Resources and Biodiversity of Jiangxi ProvinceJingdezhen UniversityJingdezhenChina
  2. 2.Institute of Biology/Geobotany and Botanical GardenMartin-Luther-University Halle-WittenbergHalleGermany
  3. 3.German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-LeipzigLeipzigGermany

Personalised recommendations