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Oecologia

, Volume 182, Issue 1, pp 43–53 | Cite as

The effects of invertebrate herbivores on plant population growth: a meta-regression analysis

  • Daniel S. W. Katz
Highlighted Student Research

Abstract

Over the last two decades, an increasing number of studies have quantified the effects of herbivory on plant populations using stage-structured population models and integral projection models, allowing for the calculation of plant population growth rates (λ) with and without herbivory. In this paper, I assembled 29 studies and conducted a meta-regression to determine the importance of invertebrate herbivores to population growth rates (λ) while accounting for missing data. I found that invertebrate herbivory often induced important reductions in plant population growth rates (with herbivory, λ was 1.08 ± 0.36; without herbivory, λ was 1.28 ± 0.58). This relationship tended to be weaker for seed predation than for other types of herbivory, except when seed predation rates were very high. Even so, the amount by which studies reduced herbivory was a poor predictor of differences in population growth rates—which strongly cautions against using measured herbivory rates as a proxy for the impact of herbivores. Herbivory reduced plant population growth rates significantly more when potential growth rates were high, which helps to explain why there was less variation in actual population growth rates than in potential population growth rates. The synthesis of these studies also shows the need for future studies to report variance in estimates of λ and to quantify how λ varies as a function of plant density.

Keywords

Insect herbivory Plant–insect interactions Integral projection models Matrix population models Meta-analysis 

Notes

Acknowledgments

Thanks are due to Inés Ibáñez for excellent advice and support throughout this project, and to Don Zak, Mark Hunter, Knute Nadelhoffer, Ben Lee, Teegan McClung, Natalie Tonn, and two anonymous reviewers for their helpful comments on an earlier version of this manuscript. The author was supported in part by a graduate research fellowship from the National Science Foundation.

Author contribution statement

DSWK conceived, designed, and executed this study and wrote the manuscript. No other person is entitled to authorship.

Compliance with ethical standards

Conflict of interest

The author declares that he has no conflict of interest.

Supplementary material

442_2016_3602_MOESM1_ESM.docx (906 kb)
Supplementary material 1 (DOCX 905 kb)

References

  1. Buckley YM, Ramula S, Blomberg SP et al (2010) Causes and consequences of variation in plant population growth rate: a synthesis of matrix population models in a phylogenetic context. Ecol Lett. doi: 10.1111/j.1461-0248.2010.01506.x Google Scholar
  2. Caswell H (1989) Matrix population models construction, analysis, and interpretation. Sinauer Associates, SunderlandGoogle Scholar
  3. Chun YJ, van Kleunen M, Dawson W (2010) The role of enemy release, tolerance and resistance in plant invasions: linking damage to performance. Ecol Lett. doi: 10.1111/j.1461-0248.2010.01498.x PubMedGoogle Scholar
  4. Crawley MJ (1989) Insect herbivores and plant population dynamics. Annu Rev Entomol. doi: 10.1146/annurev.en.34.010189.002531 Google Scholar
  5. Crone EE, Menges ES, Ellis MM et al (2011) How do plant ecologists use matrix population models? Ecol Lett 14:1–8. doi: 10.1111/j.1461-0248.2010.01540.x CrossRefPubMedGoogle Scholar
  6. Dauer JT, McEvoy PB, Van Sickle J (2012) Controlling a plant invader by targeted disruption of its life cycle. J Appl Ecol 49:322–330. doi: 10.1111/j.1365-2664.2012.02117.x CrossRefGoogle Scholar
  7. Easterling M, Ellner S, Dixon P (2000) Size-specific sensitivity: applying a new structured population model. Ecology 81:694–708CrossRefGoogle Scholar
  8. Egan JF, Irwin RE (2008) Evaluation of the field impact of an adventitious herbivore on an invasive plant, yellow toadflax, in Colorado, USA. Plant Ecol 199:99–114. doi: 10.1007/s11258-008-9415-0 CrossRefGoogle Scholar
  9. Ehrlén J (1995) Demography of the perennial herb Lathyrus vernus. II. Herbivory and population dynamics. J Ecol 83:297–308Google Scholar
  10. Ehrlén J (1996) Spatiotemporal variation in predispersal seed predation intensity. Oecologia 108:708–713CrossRefGoogle Scholar
  11. Ehrlén J (2002) Assessing the lifetime consequences of plant-animal interactions for the perennial herb Lathyrus vernus (Fabaceae). Perspect Plant Ecol Evol Syst 5:145–163. doi: 10.1078/1433-8319-00031 CrossRefGoogle Scholar
  12. Ehrlén J (2003) Fitness components versus total demographic effects: evaluating herbivore impacts on a perennial herb. Am Nat 162:796–810. doi: 10.1086/379350 CrossRefPubMedGoogle Scholar
  13. Elderd BD, Doak DF (2006) Comparing the direct and community-mediated effects of disturbance on plant population dynamics: flooding, herbivory and Mimulus guttatus. J Ecol 94:656–669. doi: 10.1111/j.1365-2745.2006.01115.x CrossRefGoogle Scholar
  14. Fagan W, Bishop J (2000) Trophic interactions during primary succession: herbivores slow a plant reinvasion at Mount St. Helens. Am Nat 155:238–251. doi: 10.1086/303320 CrossRefPubMedGoogle Scholar
  15. Fine PVA, Mesones I, Coley PD (2004) Herbivores promote habitat specialization by trees in Amazonian forests. Science 305:663–665Google Scholar
  16. Fine PVA, Miller ZJ, Mesones I et al (2006) The growth-defense trade-off and habitat specialization by plants in Amazonian forests. Ecology 87:150–162CrossRefGoogle Scholar
  17. Fröborg H, Eriksson O (2003) Predispersal seed predation and population dynamics in the perennial understorey herb Actaea spicata. Can J Bot 81:1058–1069. doi: 10.1139/b03-099 CrossRefGoogle Scholar
  18. Geman S, Geman D (1984) Stochastic relaxation, Gibbs distributions, and the Bayesian restoration of images. IEEE Trans Pattern Anal Mach Intell 6:721–741. doi: 10.1109/TPAMI.1984.4767596 CrossRefPubMedGoogle Scholar
  19. Green PT, Harms KE, Connell JH (2014) Nonrandom, diversifying processes are disproportionately strong in the smallest size classes of a tropical forest. Proc Natl Acad Sci USA. doi: 10.1073/pnas.1321892112 Google Scholar
  20. Greenland S (1987) Quantitative methods in the review of epidemiologic literature. Epidemiol Rev 9:1–30PubMedGoogle Scholar
  21. Gurevitch J, Hedges LV (2001) Meta-analysis: combining the results of independent experiments, 2nd edn. Oxford University Press, OxfordGoogle Scholar
  22. Halpern SL, Underwood N (2006) Approaches for testing herbivore effects on plant population dynamics. J Appl Ecol 43:922–929. doi: 10.1111/j.1365-2664.2006.01220.x CrossRefGoogle Scholar
  23. Hartley SE, Jones CG (1997) Plant chemistry and herbivory, or why the world is green. In: Crawley M (ed) Plant ecology. Blackwell Scientific, Cambridge, pp 284–324Google Scholar
  24. Hawkes CV, Sullivan JJ (2001) The impact of herbivory on plants in different resource conditions: a meta-analysis. Ecology 82:2045–2058CrossRefGoogle Scholar
  25. Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156CrossRefGoogle Scholar
  26. Huwaldt J, Steinhorst S (2013) Plot Digitizer. Available at: http://plotdigitizer.sourceforge.net/
  27. Ibáñez I, Katz DSW, Peltier D et al (2014) Assessing the integrated effects of landscape fragmentation on plants and plant communities: the challenge of multiprocess-multiresponse dynamics. J Ecol 102:882–895. doi: 10.1111/1365-2745.12223 CrossRefGoogle Scholar
  28. Jongejans E, Sheppard AW, Shea K (2006) What controls the population dynamics of the invasive thistle Carduus nutans in its native range? J Appl Ecol 43:877–886. doi: 10.1111/j.1365-2664.2006.01228.x CrossRefGoogle Scholar
  29. Koricheva J, Gurevitch J, Mengersen K (2013) Handbook of meta-analysis in ecology and evolution. Princeton University Press, PrincetonCrossRefGoogle Scholar
  30. Lajeunesse M (2013) Recovering missing or partial data from studies: a survey of conversions and imputations for meta-analysis. In: Koricheva J, Gurevitch J, Mengersen K (eds) Handbook of meta-analysis in ecology and evolution. Princeton University Press, Princeton, pp 196–206Google Scholar
  31. Lau JA, McCall AC, Davies KF et al (2008) Herbivores and edaphic factors constrain the realized niche of a native plant. Ecology 89:754–762CrossRefPubMedGoogle Scholar
  32. Louda SM, Rodman JE (1996) Insect herbivory as a major factor in the shade distribution of a native crucifer (Cardamine Cordifolia A. Gray, Bittercress). J Ecol 84:229–237. doi: 10.2307/2261358 CrossRefGoogle Scholar
  33. Maron JL, Crone E (2006) Herbivory: effects on plant abundance, distribution and population growth. Proc R Soc B 273:2575–2584. doi: 10.1098/rspb.2006.3587 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Miller TEX, Louda SM, Rose K, Eckberg JO (2009) Impacts of insect herbivory on cactus population dynamics: experimental demography across an environmental gradient. Ecol Monogr 79:155–172. doi: 10.1890/07-1550.1 CrossRefGoogle Scholar
  35. Morris WF, Hufbauer R, Agrawal A et al (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
  36. Nelson ESD, Harris S, Soulsbury CD et al (2010) Uncertainty in population growth rates: determining confidence intervals from point estimates of parameters. PLoS One 5:e13628. doi: 10.1371/journal.pone.0013628 CrossRefGoogle Scholar
  37. Ogle K, Pathikonda S, Sartor K et al (2014) A model-based meta-analysis for estimating species-specific wood density and identifying potential sources of variation. J Ecol 102:194–208. doi: 10.1111/1365-2745.12178 CrossRefGoogle Scholar
  38. Orwin RG (1983) A fail-safe N for effect size in meta-analysis. J Educ Behav Stat 8:157–159. doi: 10.3102/10769986008002157 CrossRefGoogle Scholar
  39. Parker MA, Root RB (1981) Insect herbivores limit habitat distribution of a native composite, Machaeranthera canescens. Ecology 62:1390–1392CrossRefGoogle Scholar
  40. Plummer M (2003) JAGS: A program for analysis of Bayesian graphical models using Gibbs sampling. Available at: http://mcmc-jags.sourceforge.net/
  41. Plummer M (2014) rjags: Bayesian graphical models using MCMC. Available at: https://cran.r-project.org/web/packages/rjags/rjags.pdf
  42. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  43. Ramula S, Buckley YM (2009) Multiple life stages with multiple replicated density levels are required to estimate density dependence for plants. Oikos 118:1164–1173. doi: 10.1111/j.1600-0706.2009.17595.x CrossRefGoogle Scholar
  44. Ramula S, Rees M, Buckley YM (2009) Integral projection models perform better for small demographic data sets than matrix population models: a case study of two perennial herbs. J Appl Ecol 46:1048–1053. doi: 10.1111/j.1365-2664.2009.01706.x CrossRefGoogle Scholar
  45. Rand T (2002) Variation in insect herbivory across a salt marsh tidal gradient influences plant survival and distribution. Oecologia 132:549–558. doi: 10.1007/s00442-002-0989-2 CrossRefGoogle Scholar
  46. Rose KE, Russell FL, Louda SM (2011) Integral projection model of insect herbivore effects on Cirsium altissimum populations along productivity gradients. Ecosphere 2:1–19. doi: 10.1890/ES11-00096.1 CrossRefGoogle Scholar
  47. Schmidt IB, Mandle L, Ticktin T, Gaoue OG (2011) What do matrix population models reveal about the sustainability of non-timber forest product harvest? J Appl Ecol 48:815–826. doi: 10.1111/j.1365-2664.2011.01999.x CrossRefGoogle Scholar
  48. Schutzenhofer MR, Valone TJ, Knight TM (2009) Herbivory and population dynamics of invasive and native Lespedeza. Oecologia 161:57–66. doi: 10.1007/s00442-009-1354-5 CrossRefPubMedGoogle Scholar
  49. Silvertown J, Franco M, Pisanty I, Mendoza A (1993) Comparative plant demography–relative importance of life-cycle components to the finite rate of increase in woody and herbaceous perennials. J Ecol 81:465–476CrossRefGoogle Scholar
  50. Spiegelhalter DJ, Best NG, Carlin BP, van der Linde A (2002) Bayesian measures of model complexity and fit. J R Stat Soc 64:583–639. doi: 10.1111/1467-9868.00353 CrossRefGoogle Scholar
  51. Stephens AE, Westoby M (2015) Effects of insect attack to stems on plant survival, growth, reproduction and photosynthesis. Oikos 124:266–273. doi: 10.1111/oik.01809 CrossRefGoogle Scholar
  52. Turcotte MM, Davies TJ, Thomsen CJM et al (2014) Macroecological and macroevolutionary patterns of leaf herbivory across vascular plants. Proc R Soc B 281:1–7. doi: 10.1098/rspb.2014.0555 CrossRefGoogle Scholar
  53. Van der Putten W (2003) Plant defense belowground and spatiotemporal processes in natural vegetation. Ecology 84:2269–2280CrossRefGoogle Scholar
  54. Viechtbauer W (2010) Conducting meta-analyses in R with the metafor package. J Stat Softw 36:1–48CrossRefGoogle Scholar
  55. von Euler T, Ågren J, Ehrlén J (2014) Environmental context influences both the intensity of seed predation and plant demographic sensitivity to attack. Ecology 95:495–504CrossRefGoogle Scholar
  56. Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer SBM, New YorkCrossRefGoogle Scholar
  57. Zhu Y, Comita LS, Hubbell SP, Ma K (2015) Conspecific and phylogenetic density-dependent survival differs across life stages in a tropical forest. J Ecol 103:957–966. doi: 10.1111/1365-2745.12414 CrossRefGoogle Scholar
  58. Zvereva EL, Lanta V, Kozlov MV (2010) Effects of sap-feeding insect herbivores on growth and reproduction of woody plants: a meta-analysis of experimental studies. Oecologia 163:949–960. doi: 10.1007/s00442-010-1633-1 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.School of Natural Resources and EnvironmentUniversity of Michigan-Ann ArborAnn ArborUSA

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