The performance and population dynamics of insect herbivores depend on the nutritive and defensive traits of their host plants1. The literature on plant–herbivore interactions focuses on plant trait mean values2, 3, 4, but recent studies showing the importance of plant genetic diversity for herbivores suggest that plant trait variance may be equally important5, 6. The consequences of plant trait variance for herbivore performance, however, have been largely overlooked. Here we report an extensive assessment of the effects of within-population plant trait variance on herbivore performance using 457 performance datasets from 53 species of insect herbivores. We show that variance in plant nutritive traits substantially reduces mean herbivore performance via non-linear averaging of performance relationships that were overwhelmingly concave down. By contrast, relationships between herbivore performance and plant defence levels were typically linear, with variance in plant defence not affecting herbivore performance via non-linear averaging. Our results demonstrate that plants contribute to the suppression of herbivore populations through variable nutrient levels, not just by having low average quality as is typically thought. We propose that this phenomenon could play a key role in the suppression of herbivore populations in natural systems, and that increased nutrient heterogeneity within agricultural crops could contribute to the sustainable control of insect pests in agroecosystems.
At a glance
- Host plant quality and fecundity in herbivorous insects. Annu. Rev. Entomol. 47, 817–844 (2002) &
- Defended fortresses or moving targets? Another model of inducible defenses inspired by military metaphors. Am. Nat. 144, 813–832 (1994) &
- The benefits of induced defenses against herbivores. Ecology 78, 1351–1355 (1997) , &
- Multiplicity in Unity: Plant Subindividual Variation & Interactions with Animals (Univ. Chicago Press, 2009)
- Plant genotypic diversity predicts community structure and governs an ecosystem process. Science 313, 966–968 (2006) et al.
- Plant genotypic diversity reduces the rate of consumer resource utilization. Proc. R. Soc. Lond. B 280, 20130639 (2013) &
- Science and society: protecting crop genetic diversity for food security: political, ethical and technical challenges. Nat. Rev. Genet. 6, 946–953 (2005)
- Vive la difference: plant functional diversity matters to ecosystem processes. Trends Ecol. Evol. 16, 646–655 (2001) &
- Functional traits in agriculture: agrobiodiversity and ecosystem services. Trends Ecol. Evol. 30, 531–539 (2015) et al.
- 15–41 (Academic Press, 1983) in Variable Plants and Herbivores in Natural and Managed Systems (eds & )
- Jensen’s inequality predicts effects of environmental variation. Trends Ecol. Evol. 14, 361–366 (1999) &
- Why intraspecific trait variation matters in community ecology. Trends Ecol. Evol. 26, 183–192 (2011) et al.
- Sur les fonctions convexes et les inegalites entre les valeurs moyennes. Acta Math. 30, 175–193 (1906)
- Does Bertrand’s rule apply to macronutrients? Proc. R. Soc. Lond. B 272, 2429–2434 (2005) , &
- A multi-level analysis of feeding behaviour: the geometry of nutritional decisions. Philos. Trans. R. Soc. B 342, 381–402 (1993) &
- The essential trace elements. Science 213, 1332–1338 (1981)
- On the role of trace substances in agriculture. Eighth Int. Congr. Appl. Chem. 28, 30–40 (1912)
- Toxicology rethinks its central belief. Nature 421, 691–692 (2003) &
- Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci. 17, 293–302 (2012) &
- Vegetational diversity and arthropod population response. Annu. Rev. Entomol. 36, 561–586 (1991)
- Genetic diversity and disease control in rice. Nature 406, 718–722 (2000) et al.
- Plant traits that predict resistance to herbivores. Funct. Ecol. 25, 358–367 (2010) , &
- Handbook of Meta-analysis in Ecology and Evolution (eds , & ) 52–60 (Princeton Univ. Press, 2013) , , , & in
- Generalized Additive Models: An Introduction with R (Chapman and Hall/CRC, 2006)
- R Core Team. R: A Language and Environment for Statistical Computing. http://www.R-project.org/ (2015)
- Estimating the form of natural selection on a quantitative trait. Evolution 42, 849–861 (1988)
- Handbook of Meta-analysis in Ecology and Evolution (eds. , & ) 61–71 (Princeton Univ. Press, 2013) , & in
- Conducting meta-analyses in R with the metafor package. J. Stat. Softw. 36, 1–48 (2010)
- lme4: Linear mixed-effects models using Eigen and S4. R package version 1.7 (2014) , , &
- Handbook of Meta-analysis in Ecology and Evolution (Princeton Univ. Press, 2013) , & (eds)
Extended data figures and tables
Extended Data Figures
- Extended Data Figure 1: Graphical summary of database. (275 KB)
a–c, Number of herbivore species per order (a), mobility of feeding stage (b), and host breadth (c). b, Each mobility level indicates the maximum extent at which the feeding stage of an herbivore commonly moves. For example, species in the ‘plant’ category move within plant individuals but do not typically move between plants. Species within the ‘patch’ category readily move among neighbouring plant individuals but do not typically move between patches of plants. Species in the ‘tissue’ category are restricted to a single organ within an individual plant (for example, leaf or root). Species in the ‘region’ category readily move among plant patches across entire geographic regions. c, Host breadth categories monophagous (mono), oligophagous (oligo), and polyphagous (poly) indicate that an herbivore species feeds on plant species in one genus, plant species across multiple genera within one plant family, and plant species across two or more plant families, respectively. d–h, Number of herbivore performance curves per trait type (d), defence class (e), nutrient class (f), date of publication (g), and study sample size (h).
- Extended Data Figure 2: Visual representation of quantitative methods. (286 KB)
Diagram summarizes the bootstrapping algorithm used to calculate a distribution of Jensen’s effects for each empirical dataset for herbivore growth. For more details and for differences in methods between growth and survival, see Methods and Supplementary Methods.
- Extended Data Figure 3: Jensen’s effects by plant trait type (defences and nutrients) and mobility of the feeding stage. (86 KB)
Defence variance had mean effects near to zero and nutrient variability had generally negative effects regardless of the mobility of the feeding stage of the herbivore species. Species in the ‘plant’ category move within plant individuals but do not typically move between plants. Species within the ‘patch’ category readily move among neighbouring host plants but do not typically move between patches. Species within the ‘region’ category commonly move among host plant patches. Each point is one herbivore species, jittered for visibility. Diamonds and error bars show mean values and 95% confidence intervals. See Supplementary Methods for more details.
- Extended Data Figure 4: Jensen’s effects by plant trait type (defences and nutrients) and host breadth. (85 KB)
Defence variance had mean effects near to zero and nutrient variability had generally negative effects regardless of the host breadth of the herbivore species. Oligophagous species (‘oligo’) feed on plant species in multiple genera but are restricted to one plant family. Polyphagous species (‘poly’) feed on plant species across two or more plant families. Each point represents one herbivore species, jittered for visibility. Diamonds and error bars are mean values with 95% confidence intervals. See Supplementary Methods for more details.
- Extended Data Figure 5: Funnel plots for growth and survival. (81 KB)
a, b, The lack of a relationship between the sample size of a study and its Jensen’s effect for growth (a) or survival (b) suggests that publication bias did not have a major influence on the results. Dashed line shows zero. Solid lines show linear regressions for growth (F1,248 = 0.23, P = 0.63, R2 = 0.0) and survival (F1,203 = 1.04, P = 0.31, R2 = 0.0).
- Extended Data Figure 6: Jensen’s effect for each observation by the year of publication for growth and survival. (99 KB)
a, b, The lack of temporal trends in Jensen’s effects for growth (a) or survival (b) suggests that publication bias did not play a major role.
- Supplementary Information (606 KB)
This file contains Supplementary Methods, Supplementary Tables, a Supplementary Discussion and Supplementary References.