Oecologia

, Volume 165, Issue 1, pp 143–151

Birds help plants: a meta-analysis of top-down trophic cascades caused by avian predators

Plant-Animal interactions - Original Paper

Abstract

The tritrophic interactions between plants, herbivores and avian predators are complex and prone to trophic cascades. We conducted a meta-analysis of original articles that have studied birds as predators of invertebrate herbivores, to compare top-down trophic cascades with different plant responses from different environments and climatic areas. Our search found 29 suitable articles, with a total of 81 separate experimental study set-ups. The meta-analysis revealed that plants benefited from the presence of birds. A significant reduction was observed in the level of leaf damage and plant mortality. The presence of birds also positively affected the amount of plant biomass, whereas effects on plant growth were negligible. There were no differences in the effects between agricultural and natural environments. Similarly, plants performed better in all climatic areas (tropical, temperate and boreal) when birds were present. Moreover, both mature plants and saplings gained benefits from the presence of birds. Our results show that birds cause top-down trophic cascades and thus they play an integral role in ecosystems.

Keywords

Herbivory Indirect effects Meta-analysis Predation Trophic interactions 

Supplementary material

442_2010_1774_Fig2_ESM.jpg (6.1 mb)

Electronic Supplemental Material 1 A normal quantile plot with 95 % confidence interval lines for examining publication bias of the studies used in the overall effect meta-analysis (N = 44) (JPEG 6221 kb)

442_2010_1774_Fig3_ESM.jpg (434 kb)

Electronic Supplemental Material 2 A funnel plot showing the relationship between the effect size (lnR) and sample size of the original studies (N = 44). N is the combined sample size of treatment and control plots. The two outliers are the two studies of algae as plants (Wootton 1992, 1995) (JPEG 434 kb)

References

  1. Agrawal AA (1999) Induced responses to herbivory in wild radish: effects on several herbivores and plant fitness. Ecology 80:1713–1723. doi:10.2307/176559 CrossRefGoogle Scholar
  2. Atlegrim O (1989) Exclusion of birds from bilberry stands: impact on insect larval density and damage to the bilberry. Oecologia 79:136–139. doi:10.1007/BF00378251 CrossRefGoogle Scholar
  3. Aunapuu M, Dahlgren J, Oksanen T, Grellmann D, Oksanen L, Olofsson J, Rammul Ü, Schneider M, Johansen B, Hygen HO (2008) Spatial patterns and dynamic responses of arctic food webs corroborate the exploitation ecosystems hypothesis (EEH). Am Nat 171:249–262. doi:10.1086/524951 CrossRefPubMedGoogle Scholar
  4. 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. doi:10.1674/0003-0031-162.1.169 CrossRefGoogle Scholar
  5. Bejer B (1988) The nun moth in European spruce forests. In: Berryman AA (ed) Dynamics of forest insect populations: patterns, causes, implications. Plenum, New York, pp 211–231Google Scholar
  6. BirdLife International (2008) State of the world’s birds: indicators for our changing world. BirdLife International, CambridgeGoogle Scholar
  7. Bock CE, Bock JH, Grant MC (1992) Effects of bird predation on grasshopper densities in an Arizona grassland. Ecology 73:1706–1717. doi:10.2307/1940022 CrossRefGoogle Scholar
  8. Boege K, Marquis RJ (2006) Plant quality and predation risk mediated by plant ontogeny: consequences for herbivores and plants. Oikos 115:559–572. doi:10.1111/j.2006.0030-1299.15076.x CrossRefGoogle Scholar
  9. Borkhataria RR, Collazo JA, Groom MJ (2006) Additive effects of vertebrate predators on insects in a Puerto Rican coffee plantation. Ecol Appl 16:696–703. doi:10.1890/1051-0761(2006)016[0696:AEOVPO]2.0.CO;2 CrossRefPubMedGoogle Scholar
  10. Bridgeland WT, Beier P, Kolb T, Whitham T (2010) A conditional trophic cascade: birds benefit faster growing trees with strong links between predators and plants. Ecology 91:73–84. doi:10.1890/08-1821.1 CrossRefPubMedGoogle Scholar
  11. Cooper H (1998) Synthesizing research: a guide for literature reviews, 3rd edn. Sage, Thousand OaksGoogle Scholar
  12. Doak DF (1992) Lifetime impacts of herbivory for a perennial plant. Ecology 73:2086–2099. doi:10.2307/1941457 CrossRefGoogle Scholar
  13. Dunham AE (2008) Above and below ground impacts of terrestrial mammals and birds in a tropical forest. Oikos 117:571–579. doi:10.1111/j.2007.0030-1299.16534.x CrossRefGoogle Scholar
  14. Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH (2004) Airborne signals prime plants against insect herbivore attack. Proc Natl Acad Sci USA 101:1781–1785. doi:10.1073/pnas.0308037100 CrossRefPubMedGoogle Scholar
  15. Fayt P, Machmer MM, Steeger C (2005) Regulation of spruce bark beetles by woodpeckers—a literature review. For Ecol Manag 206:1–14. doi:10.1016/j.foreco.2004.10.054 CrossRefGoogle Scholar
  16. Floyd T (1996) Top-down impacts on creosotebush herbivores in a spatially and temporally complex environment. Ecology 77:1544–1555. doi:10.2307/2265550 CrossRefGoogle Scholar
  17. Forkner RE, Hunter MD (2000) What goes up must come down? Nutrient addition and predation pressure on oak herbivores. Ecology 81:1588–1600. doi:10.2307/177309 CrossRefGoogle Scholar
  18. Fowler AC, Knight RL, Luke George T, McEwen LC (1991) Effects of avian predation on grasshopper populations in North Dakota grasslands. Ecology 72:1775–1781. doi:10.2307/1940976 CrossRefGoogle Scholar
  19. Garibaldi LA, Kitzberger T, Mazía N, Chaneton EJ (2010) Nutrient supply and bird predation additively control insect herbivory and tree growth in two contrasting forest habitats. Oikos 119:337–349. doi:10.1111/j.1600-0706.2009.17862.x CrossRefGoogle Scholar
  20. Gates S (2002) Review of methodology of quantitative reviews using meta-analysis in ecology. J Anim Ecol 71:547–557. doi:10.1046/j.1365-2656.2002.00634.x CrossRefGoogle Scholar
  21. Greenberg R, Bichier P, Cruz Angon A, 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. doi:10.2307/177321 CrossRefGoogle Scholar
  22. Gruner DS (2004) Attenuation of top-down and bottom-up forces in a complex terrestrial community. Ecology 85:3010–3022. doi:10.1890/04-0020 CrossRefGoogle Scholar
  23. Gurevitch J, Hedges LV (2001) Meta-analysis. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Oxford University Press, New York, pp 347–369Google Scholar
  24. Gurevitch J, Morrow LL, Wallace A, Walsh JS (1992) A meta-analysis of competition in field experiments. Am Nat 140:539–572. doi:10.1086/285428 CrossRefGoogle Scholar
  25. Gurevitch J, Morrison JA, Hedges LV (2000) The interaction between competition and predation: a meta-analysis of field experiments. Am Nat 155:435–453. doi:10.1086/303337 CrossRefPubMedGoogle Scholar
  26. Hairston NG, Smith FE, Slobodkin LB (1960) Community structure, population control, and competition. Am Nat 94:421–425. doi:10.1086/282146 CrossRefGoogle Scholar
  27. Halaj J, Wise DH (2001) Terrestrial trophic cascades: how much do they trickle? Am Nat 157:262–281. doi:10.1086/319190 CrossRefPubMedGoogle Scholar
  28. Heinrich B, Collins SL (1983) Caterpillar leaf damage, and the game of hide-and-seek with birds. Ecology 64:592–602. doi:10.2307/1939978 CrossRefGoogle Scholar
  29. Hogstad O (2005) Numerical and functional responses of breeding passerine species to mass occurrence of geometrid caterpillars in a subalpine birch forest: a 30-year study. Ibis 147:77–91. doi:10.1111/j.1474-919x.2004.00338 CrossRefGoogle Scholar
  30. Holmes RT, Schultz JC, Nothnagle P (1979) Bird predation on forest insects: an exclosure experiment. Science 206:462–463. doi:10.1126/science.206.4417.462 CrossRefPubMedGoogle Scholar
  31. Hooks CRR, Pandey RR, Johnson MW (2003) Impact of avian and arthropod predation of lepidopteran caterpillar densities and plant productivity in an ephemeral agroecosystem. Ecol Entomol 28:522–532. doi:10.1046/j.1365-2311.2003.00544.x CrossRefGoogle Scholar
  32. Hunter MD, Price PW (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:724–732Google Scholar
  33. Joern A (1986) Experimental study of avian predation on coexisting grasshopper populations (Orthoptera: Acrididae) in a sandhills grassland. Oikos 46:243–249. doi:10.2307/3565473 CrossRefGoogle Scholar
  34. Kalka MB, Smith AR, Kalko EKV (2008) Bats limit arthropods and herbivory in a tropical forest. Science 320:71. doi:10.1126/science.1153352 CrossRefPubMedGoogle Scholar
  35. Kaplan I, Denno RF (2007) Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecol Lett 10:977–994. doi:10.1111/j.1461-0248.2007.01093.x CrossRefPubMedGoogle Scholar
  36. Kaspari M, Joern A (1993) Prey choice by three insectivorous grassland birds: reevaluating opportunism. Oikos 68:414–430. doi:10.2307/3544909 CrossRefGoogle Scholar
  37. Kellermann JL, Johnson MD, Stercho AM, Hackett SC (2008) Ecological and economic services provided by birds on Jamaican Blue Mountain coffee farms. Conserv Biol 22:1177–1185. doi:10.1111/j.1523-1739.2008.00968.x CrossRefPubMedGoogle Scholar
  38. Koh LP (2008) Birds defend oil palms from herbivorous insects. Ecol Appl 18:821–825. doi:10.1890/07-1650.1 CrossRefPubMedGoogle Scholar
  39. Kolehmainen J, Julkunen-Tiitto R, Roininen H, Tahvanainen J (1995) Phenolic glucosides as feeding cues for willow-feeding leaf beetles. Entomol Exp Appl 74:235–243. doi:10.1007/BF02381787 CrossRefGoogle Scholar
  40. Koricheva J, Larsson S, Haukioja E (1998) Insect performance on experimentally stressed woody plants: a meta-analysis. Annu Rev Entomol 43:195–216. doi:10.1146/annurev.ento.43.1.195 CrossRefPubMedGoogle Scholar
  41. Kotiaho JS, Tomkins JL (2002) Meta-analysis, can it ever fail? Oikos 96:551–553. doi:10.1034/j.1600-0706.2002.960316.x CrossRefGoogle Scholar
  42. Leimu R, Lehtilä K (2006) Effects of two types of herbivores on the population dynamics of a perennial herb. Basic Appl Ecol 7:224–235. doi:10.1016/j.baae.2005.09.002 CrossRefGoogle Scholar
  43. Lichtenberg JS, Lichtenberg DA (2002) Weak trophic interactions among birds, insects and white oak saplings (Quercus alba). Am Midl Nat 148:338–349. doi:10.1674/0003-0031(2002)148[0338:WTIABI]2.0.CO;2 CrossRefGoogle Scholar
  44. Lindström L, Alatalo RV, Mappes J (1999) Reactions of hand-reared and wild-caught predators toward warningly colored, gregarious, and conspicuous prey. Behav Ecol 10:317–322. doi:10.1093/beheco/10.3.317 CrossRefGoogle Scholar
  45. Loyn RH, Runnalls RG, Forward GY, Tyers J (1983) Territorial bell miners and other birds affecting populations of insect prey. Science 221:1411–1413. doi:10.1126/science.221.4618.1411 CrossRefPubMedGoogle Scholar
  46. Mäntylä E, Klemola T, Haukioja E (2004) Attraction of willow warblers to sawfly-damaged mountain birches: novel function of inducible plant defenses? Ecol Lett 7:915–918. doi:10.1111/j.1461-0248.2004.00653.x CrossRefGoogle Scholar
  47. Mäntylä E, Alessio GA, Blande JD, Heijari J, Holopainen JK, Laaksonen T, Piirtola P, Klemola T (2008a) From plants to birds: higher avian predation rates in trees responding to insect herbivory. PLoS ONE 3(7):e2832. doi:10.1371/journal.pone.0002832 CrossRefPubMedGoogle Scholar
  48. Mäntylä E, Klemola T, Sirkiä P, Laaksonen T (2008b) Low light reflectance may explain the attraction of birds to defoliated trees. Behav Ecol 19:325–330. doi:10.1093/beheco/arm135 CrossRefGoogle Scholar
  49. Marquis RJ (1984) Leaf herbivores decrease fitness of a tropical plant. Science 226:537–539. doi:10.1126/science.226.4674.537 CrossRefPubMedGoogle Scholar
  50. Marquis RJ, Whelan CJ (1994) Insectivorous birds increase growth of white oak through consumption of leaf-chewing insects. Ecology 75:2007–2014. doi:10.2307/1941605 CrossRefGoogle Scholar
  51. Mattson WJ, Simmons GA, Witter JA (1988) The spruce budworm in eastern North America. In: Berryman AA (ed) Dynamics of forest insect populations: patterns, causes, implications. Plenum, New York, pp 309–330Google Scholar
  52. Mazía CN, Kitzberger T, Chaneton EJ (2004) Interannual changes in folivory and bird insectivory along a natural productivity gradient in northern Patagonian forests. Ecography 27:29–40. doi:10.1111/j.0906-7590.2004.03641.x CrossRefGoogle Scholar
  53. Mazía CN, Chaneton EJ, Kitzberger T, Garibaldi LA (2009) Variable strength of top-down effects in Nothofagus forests: bird predation and insect herbivory during an ENSO event. Austral Ecol 34:359–367. doi:10.1111/j.1442-9993.2009.01933.x Google Scholar
  54. Mols CMM, Visser ME (2002) Great tits can reduce caterpillar damage in apple orchards. J Appl Ecol 39:888–899. doi:10.1046/j.1365-2664.2002.00761.x CrossRefGoogle Scholar
  55. Mooney KA (2007) Tritrophic effects of birds and ants on a canopy food web, tree growth, and phytochemistry. Ecology 88:2005–2014. doi:10.1890/06-1095.1 CrossRefPubMedGoogle Scholar
  56. Mooney KA, Linhart YB (2006) Contrasting cascades: insectivorous birds increase pine but not parasitic mistletoe growth. J Anim Ecol 75:350–357. doi:10.1111/j.1365-2656.2006.01054.x CrossRefPubMedGoogle Scholar
  57. 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. doi:10.1073/pnas.1001934107 CrossRefPubMedGoogle Scholar
  58. Morris WF, Hufbauer RA, Agrawal AA, Bever JD, Borowicz VA, Gilbert GS, Maron JL, Mitchell CE, Parker IM, Power AG, Torchin ME, Vázquez DP (2007) Direct and interactive effects of enemies and mutualists on plant performance: a meta-analysis. Ecology 88:1021–1029. doi:10.1890/06-0442 CrossRefPubMedGoogle Scholar
  59. Murakami M, Nakano S (2000) Species-specific bird functions in a forest-canopy food web. Proc R Soc Lond B 267:1597–1601. doi:10.1098/rspb.2000.1184 CrossRefGoogle Scholar
  60. Norrdahl K, Klemola T, Korpimäki E, Koivula M (2002) Strong seasonality may attenuate trophic cascades: vertebrate predator exclusion in boreal grassland. Oikos 99:419–430. doi:10.1034/j.1600-0706.2002.12025.x CrossRefGoogle Scholar
  61. Oksanen L, Oksanen T (2000) The logic and realism of the hypothesis of exploitation ecosystems. Am Nat 155:703–723. doi:10.1086/303354 CrossRefPubMedGoogle Scholar
  62. Oksanen L, Fretwell SD, Arruda J, Niemelä P (1981) Exploitation ecosystems in gradients of primary productivity. Am Nat 118:240–261. doi:10.1086/283817 CrossRefGoogle Scholar
  63. Pace ML, Cole JJ, Carpenter SR, Kitchell JF (1999) Trophic cascades revealed in diverse ecosystems. Trends Ecol Evol 14:483–488. doi:10.1016/S0169-5347(99)01723-1 CrossRefPubMedGoogle Scholar
  64. Paine RT (1980) Food webs: linkage, interaction strength and community infrastructure. J Anim Ecol 49:667–685CrossRefGoogle Scholar
  65. Palmer AR (1999) Detecting publication bias in meta-analyses: a case study of fluctuating asymmetry and sexual selection. Am Nat 154:220–233. doi:10.1086/303223 CrossRefGoogle Scholar
  66. Persson L (1999) Trophic cascades: abiding heterogeneity and the trophic level concept at the end of the road. Oikos 85:385–397. doi:10.2307/3546688 CrossRefGoogle Scholar
  67. Polis GA, Strong DR (1996) Food web complexity and community dynamics. Am Nat 147:813–846. doi:10.1086/285880 CrossRefGoogle Scholar
  68. Polis GA, Anderson WB, Holt RD (1997) Toward an integration of landscape and food web ecology: the dynamics of spatially subsided food webs. Annu Rev Ecol Syst 28:289–316. doi:10.1146/annurev.ecolsys.28.1.289 CrossRefGoogle Scholar
  69. Ritchie ME (2000) Nitrogen limitation and trophic vs. abiotic influences on insect herbivores in a temperate grassland. Ecology 81:1601–1612. doi:10.2307/177310 CrossRefGoogle Scholar
  70. Rosenberg MS, Adams DC, Gurevitch J (2000) METAWIN. Statistical software for meta-analysis, vol 2. Sinauer, MassachusettsGoogle Scholar
  71. Rosenthal R (1979) The “file drawer problem” and tolerance for null results. Psychol Bull 86:638–641. doi:10.1037/0033-2909.86.3.638 CrossRefGoogle Scholar
  72. Rustad LE, Campbell JL, Marion GM, Norby RJ, Mitchell MJ, Hartley AE, Cornelissen JHC, Gurevitch J, GCTE-NEWS (2001) A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126:543–562. doi:10.1007/s004420000544 CrossRefGoogle Scholar
  73. Salo P, Korpimäki E, Banks PB, Nordström M, Dickman CR (2007) Alien predators are more dangerous than native predators to prey populations. Proc R Soc Lond B 274:1237–1243. doi:10.1098/rspb.2006.0444 CrossRefGoogle Scholar
  74. Sanz JJ (2001) Experimentally increased insectivorous bird density results in a reduction of caterpillar density and leaf damage to Pyrenean oak. Ecol Res 16:387–394. doi:10.1046/j.1440-1703.2001.00403.x CrossRefGoogle Scholar
  75. Schmitz OJ, Hambäck PA, Beckerman AP (2000) Trophic cascades in terrestrial systems: a review of the effects of carnivore removals on plants. Am Nat 155:141–153. doi:10.1086/303311 CrossRefPubMedGoogle Scholar
  76. Schmitz OJ, Krivan V, Ovadia O (2004) Trophic cascades: the primacy of trait-mediated indirect interactions. Ecol Lett 7:153–163. doi:10.1111/j.1461-0248.2003.00560.x CrossRefGoogle Scholar
  77. Sekercioglu CH (2006a) Ecological significance of bird populations. In: del Hoyo J, Elliott A, Christie DA (eds) Handbook of the birds of the world, vol 11. Lynx, Barcelona, pp 15–51Google Scholar
  78. Sekercioglu CH (2006b) Increasing awareness of avian ecological function. Trends Ecol Evol 21:464–471. doi:10.1016/j.tree.2006.05.007 CrossRefPubMedGoogle Scholar
  79. Sekercioglu CH, Daily GC, Ehrlich PR (2004) Ecosystem consequences of bird declines. Proc Natl Acad Sci USA 101:18042–18047. doi:10.1073/pnas.0408049101 CrossRefPubMedGoogle Scholar
  80. Sherry TW (1984) Comparative dietary ecology of sympatric, insectivorous neotropical flycatchers (Tyrannidae). Ecol Monogr 54:313–338. doi:10.2307/1942500 CrossRefGoogle Scholar
  81. Shurin JB, Borer ET, Seabloom EW, Anderson K, Blanchette CA, Broitman B, Cooper SD, Halpern BS (2002) A cross-ecosystem comparison of the strength of trophic cascades. Ecol Lett 5:785–791. doi:10.1046/j.1461-0248.2002.00381.x CrossRefGoogle Scholar
  82. Sigel BJ, Robinson WD, Sherry TW (2010) Comparing bird community responses to forest fragmentation in two lowland Central American reserves. Biol Conserv 143:340–350. doi:10.1016/j.biocon.2009.10.020 CrossRefGoogle Scholar
  83. Sipura M (1999) Tritrophic interactions: willows, herbivorous insects and insectivorous birds. Oecologia 121:537–545. doi:10.1007/s004420050960 CrossRefGoogle Scholar
  84. Slobodkin LB (1960) Ecological energy relationships at the population level. Am Nat 94:213–236. doi:10.1086/282124 CrossRefGoogle Scholar
  85. Strengbom J, Witzell J, Nordin A, Ericson L (2005) Do multitrophic interactions override N fertilization effects on Operophtera larvae? Oecologia 143:241–250. doi:10.1007/s00442-004-1799-5 CrossRefPubMedGoogle Scholar
  86. Strong DR (1992) Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems. Ecology 73:747–754. doi:10.2307/1940154 CrossRefGoogle Scholar
  87. Strong AM, Sherry TW, Holmes RT (2000) Bird predation on herbivorous insects: indirect effects on sugar maple saplings. Oecologia 125:370–379. doi:10.1007/s004420000467 CrossRefGoogle Scholar
  88. Sundell J (2006) Experimental tests of the role of predation in the population dynamics of voles and lemmings. Mammal Rev 36:107–141. doi:10.1111/j.1365-2907.2006.00083.x CrossRefGoogle Scholar
  89. Van Bael SA, Brawn JD (2005) The direct and indirect effects of insectivory by birds in two contrasting Neotropical forests. Oecologia 143:106–116. doi:10.1007/s00442-004-1774-1 CrossRefPubMedGoogle Scholar
  90. Van Bael SA, Brawn JD, Robinson SK (2003) Birds defend trees from herbivores in a Neotropical forest canopy. Proc Natl Acad Sci USA 100:8304–8307. doi:10.1073/pnas.1431621100 CrossRefPubMedGoogle Scholar
  91. Van Bael SA, Bichier P, Greenberg R (2007) Bird predation on insects reduces damage to the foliage of cocoa trees (Theobroma cacao) in western Panama. J Trop Ecol 23:715–719. doi:10.1017/S0266467407004440 Google Scholar
  92. Van Bael SA, Philpott SM, Greenberg R, Bichier P, Barber NA, Mooney KA, Gruner DS (2008) Birds as predators in tropical agroforestry systems. Ecology 89:928–934. doi:10.1890/06-1976.1 CrossRefPubMedGoogle Scholar
  93. 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. doi:10.1016/j.baae.2005.05.003 CrossRefGoogle Scholar
  94. Whelan CJ, Wenny DG, Marquis RJ (2008) Ecosystem services provided by birds. Ann NY Acad Sci 1134:25–60. doi:10.1196/annals.1439.003 CrossRefPubMedGoogle Scholar
  95. Williams-Guillén K, Perfecto I, Vandermeer J (2008) Bats limit insects in a Neotropical agroforestry system. Science 320:70. doi:10.1126/science.1152944 CrossRefPubMedGoogle Scholar
  96. Wootton JT (1992) Indirect effects, prey susceptibility, and habitat selection: impacts on birds on limpets and algae. Ecology 73:981–991. doi:10.2307/1940174 CrossRefGoogle Scholar
  97. Wootton JT (1995) Effects of birds on sea urchins and algae: a lower-intertidal trophic cascade. Ecoscience 2:321–328Google Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Elina Mäntylä
    • 1
  • Tero Klemola
    • 1
  • Toni Laaksonen
    • 1
    • 2
  1. 1.Section of Ecology, Department of BiologyUniversity of TurkuTurkuFinland
  2. 2.Finnish Museum of Natural HistoryUniversity of HelsinkiHelsinkiFinland

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