, Volume 180, Issue 2, pp 485–497 | Cite as

Soil nutrient additions increase invertebrate herbivore abundances, but not herbivory, across three grassland systems

  • Kimberly J. La PierreEmail author
  • Melinda D. Smith
Community ecology - Original research


Resource availability may influence invertebrate communities, with important consequences for ecosystem function, such as biomass production. We assessed: (1) the effects of experimental soil nutrient additions on invertebrate abundances and feeding rates and (2) the resultant changes in the effects of invertebrates on aboveground plant biomass at three grassland sites spanning the North American Central Plains, across which plant tissue chemistry and biomass vary. Invertebrate communities and rates of herbivory were sampled within a long-term nutrient-addition experiment established at each site along the broad Central Plains precipitation gradient. Additionally, the effects of invertebrates on aboveground plant biomass were determined under ambient and elevated nutrient conditions. At the more mesic sites, invertebrate herbivore abundances increased and their per capita rate of herbivory decreased with nutrient additions. In contrast, at the semi-arid site where plant biomass is low and plant nutrient concentrations are high, invertebrate herbivore abundances did not vary and per capita rates of herbivory increased with nutrient additions. No change in the effect of invertebrate herbivores on aboveground plant biomass was observed at any of the sites. In sum, nutrient additions induced shifts in both plant biomass and leaf nutrient content, which altered invertebrate abundances and feeding rate. However, due to the inverse relationship between changes in herbivore abundance and per capita rates of herbivory, nutrient additions did not alter the effect of invertebrates on aboveground biomass. Overall, we suggest that this inverse response of herbivore abundance and per capita feeding rate may buffer ecosystems against changes in invertebrate damage in response to fluctuations in nutrient levels.


Nitrogen Per capita herbivory rate Phosphorus Plant tissue chemistry Central Plains 



The authors are grateful for field assistance from M. Avolio, D. Blumenthal, C. Brown, L. Dev, K. Harmony, J. Klein, A. Kuhl, B. La Pierre, A. Potter, R. Ramundo, A. Joern, and the SGS field crew. O. Schmitz, K. Gross, K. Burghardt, and three anonymous reviewers provided helpful feedback on earlier drafts of the manuscript. Funding was provided by a Yale Institute for Biospheric Studies Center for Field Ecology Pilot Grant, a Yale Institute for Biospheric Studies Dissertation Improvement Grant, and a grant from the Lee Pierce Fund to K. La Pierre, the Konza Prairie LTER, and the Shortgrass Steppe LTER. This work was generated using data from three sites within the Nutrient Network collaborative experiment, funded at the site scale by individual researchers and coordinated through Research Coordination Network funding from the National Science Foundation to E. Borer and E. Seabloom (NSF-DEB-1042132). N fertilizer was donated by Crop Production Services, Loveland, Colorado. K. La Pierre was supported by an National Science Foundation Graduate Research Fellowship.

Author contribution statement

K. J. L. and M. D. S. conceived and designed the experiments. K. J. L. performed the experiments and analyzed the data. K. J. L. wrote the manuscript with editorial input from M. D. S.

Supplementary material

442_2015_3471_MOESM1_ESM.docx (44 kb)
Supplementary material 1 (DOCX 44 kb)


  1. Adler PB, Levine JM (2007) Contrasting relationships between precipitation and species richness in space and time. Oikos 116:221–232CrossRefGoogle Scholar
  2. Agrawal AA, Fishbein M (2006) Plant defense syndromes. Ecology 87:S132–S149CrossRefPubMedGoogle Scholar
  3. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  4. Anderson MJ (2005) Permutational multivariate analysis of varianceGoogle Scholar
  5. Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62:245–253. doi: 10.1111/j.1541-0420.2005.00440.x CrossRefPubMedGoogle Scholar
  6. Behmer ST (2009) Insect herbivore nutrient regulation. Annu Rev Entomol 54:165–187. doi: 10.1146/annurev.ento.54.110807.090537 CrossRefPubMedGoogle Scholar
  7. Behmer ST, Joern A (1993) Diet choice by a grass-feeding grasshopper based on the need for a limiting nutrient. Funct Ecol 7:522–527CrossRefGoogle Scholar
  8. Behmer ST, Joern A (2008) Coexisting generalist herbivores occupy unique nutritional feeding niches. Proc Natl Acad Sci 105:1977–1982. doi: 10.1073/pnas.0711870105 PubMedCentralCrossRefPubMedGoogle Scholar
  9. Berner D, Blanckenhorn WU, Korner C (2005) Grasshoppers cope with low host plant quality by compensatory feeding and food selection: N limitation challenged. Oikos 111:525–533CrossRefGoogle Scholar
  10. Blue JD, Souza L, Classen AT, Schweitzer JA, Sanders NJ (2011) The variable effects of soil nitrogen availability and insect herbivory on aboveground and belowground plant biomass in an old-field ecosystem. Oecologia 167:771–780. doi: 10.1007/s00442-011-2028-7 CrossRefPubMedGoogle Scholar
  11. Borer ET, Seabloom EW, Shurin JB, Anderson K, Blanchette CA, Broitman B, Cooper SD, Halpern BS (2005) What determines the strength of a trophic cascade? Ecology 86:528–537CrossRefGoogle Scholar
  12. Borer ET, Seabloom EW, Tilman D, Novotny V (2012) Plant diversity controls arthropod biomass and temporal stability. Ecol Lett 15:1457–1464. doi: 10.1111/ele.12006 CrossRefPubMedGoogle Scholar
  13. Borer ET, Seabloom EW, Gruner DS, Harpole WS, Hillebrand H et al (2014) Herbivores and nutrients control grassland plant diversity via light limitation. Nature 508:517–520. doi: 10.1038/nature13144 CrossRefPubMedGoogle Scholar
  14. Burnham KP (2004) Multimodel inference: understanding AIC and BIC in model selection. Sociol Methods Res 33:261–304. doi: 10.1177/0049124104268644 CrossRefGoogle Scholar
  15. Chambers P, Simpson SJ, Raubenheimer D (1995) Behavioural mechanisms of nutrient balancing in Locusta migratoria nymphs. Anim Behav 50:1513–1523CrossRefGoogle Scholar
  16. Chapin FS, Autumn K, Pugnaire F (1993) Evolution of suites of traits in response to environmental stress. Am Nat 142:S78–S92CrossRefGoogle Scholar
  17. Chase JM, Leibold MA, Downing AL, Shurin JB (2000) The effects of productivity, herbivory, and plant species turnover in grassland food webs. Ecology 81:2485–2497CrossRefGoogle Scholar
  18. Chen Y, Olson DM, Ruberson JR (2010) Effects of nitrogen fertilization on tritrophic interactions. Arthropod Plant Interact 4:81–94. doi: 10.1007/s11829-010-9092-5 CrossRefGoogle Scholar
  19. Cleland EE, Harpole WS (2010) Nitrogen enrichment and plant communities. Year in ecology and conservation biology 2010. Blackwell, Oxford, pp 46–61Google Scholar
  20. Cleland EE, Peters HA, Mooney HA, Field CB (2006) Gastropod herbivory in response to elevated CO2 and N addition impacts plant community composition. Ecology 87:686–694CrossRefPubMedGoogle Scholar
  21. Coffin DP, Laycock WA, Lauenroth WK (1998) Disturbance intensity and above- and belowground herbivory effects on long-term (14 y) recovery of a semiarid grassland. Plant Ecol 139:221–233CrossRefGoogle Scholar
  22. Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899. doi: 10.1126/science.230.4728.895 CrossRefPubMedGoogle Scholar
  23. Cronin JP, Tonsor SJ, Carson WP (2010) A simultaneous test of trophic interaction models: which vegetation characteristic explains herbivore control over plant community mass? Ecol Lett 13:202–212. doi: 10.1111/j.1461-0248.2009.01420.x CrossRefPubMedGoogle Scholar
  24. De Sassi C, Staniczenko PPA, Tylianakis JM (2012) Warming and nitrogen affect size structuring and density dependence in a host-parasitoid food web. Philos Trans R Soc Lond B Biol Sci 367:3033–3041. doi: 10.1098/rstb.2012.0233 PubMedCentralCrossRefPubMedGoogle Scholar
  25. Denno RF, Fagan W (2003) Might nitrogen limitation promote omnivory among carnivorous arthropods? Ecology 84:2522–2531CrossRefGoogle Scholar
  26. Denno RF, Gratton C, Peterson M (2002) Bottom-up forces mediate natural-enemy impact in a phytophagous insect community. Ecology 83:1443–1458CrossRefGoogle Scholar
  27. Duffy JE, Cardinale BJ, France KE, McIntyre PB, Thébault E, Loreau M (2007) The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecol Lett 10:522–538. doi: 10.1111/j.1461-0248.2007.01037.x CrossRefPubMedGoogle Scholar
  28. Elser JJ, Sterner RW, Gorokhova E, Fagan WF, Markow TA, Cotner JB, Harrison JF, Hobbie SE, Odell GM, Weider LW (2000a) Biological stoichiometry from genes to ecosystems. Ecol Lett 3:540–550. doi: 10.1046/j.1461-0248.2000.00185.x CrossRefGoogle Scholar
  29. Elser JJ, Fagan WF, Denno RF, Dobberfuhl DR, Folarin A, Huberty A, Interlandi S, Kilham SS, McCauley E, Schulz KL, Siemann EH, Sterner RW (2000b) Nutritional constraints in terrestrial and freshwater food webs. Nature 408:578–580CrossRefPubMedGoogle Scholar
  30. Fagan WF, Siemann E, Mitter C, Denno RF, Huberty AF, Woods HA, Elser JJ (2002) Nitrogen in insects: implications for trophic complexity and species diversification. Am Nat 160:784–802CrossRefPubMedGoogle Scholar
  31. Fink P, von Elert E (2006) Physiological responses to stoichiometric constraints: nutrient limitation and compensatory feeding in a freshwater snail. Oikos 115:484–494CrossRefGoogle Scholar
  32. Forkner RE, Hunter MD (2000) What goes up must come down? Nutrient addition and predation pressure on oak herbivores. Ecology 81:1588. doi: 10.2307/177309 CrossRefGoogle Scholar
  33. 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
  34. Hall SR (2009) Stoichiometrically explicit food webs: feedbacks between resource supply, elemental constraints, and species diversity. Annu Rev Ecol Evol Syst 40:503–528. doi: 10.1146/annurev.ecolsys.39.110707.173518 CrossRefGoogle Scholar
  35. Hall SR, Knight CJ, Becker CR, Duffy MA, Tessier AJ, Cáceres CE (2009) Quality matters: resource quality for hosts and the timing of epidemics. Ecol Lett 12:118–128. doi: 10.1111/j.1461-0248.2008.01264.x CrossRefPubMedGoogle Scholar
  36. Hartley MK, Rogers WE, Siemann E, Grace JB (2007) Responses of prairie arthropod communities to fire and fertilizer: balancing plant and arthropod conservation. Am Midl Nat 157:92–105CrossRefGoogle Scholar
  37. Huxel GR (1999) On the influence of food quality in consumer-resource interactions. Ecol Lett 2:256–261CrossRefGoogle Scholar
  38. Joern A, Behmer ST (1998) Impact of diet quality on demographic attributes in adult grasshoppers and the nitrogen limitation hypothesis. Ecol Entomol 23:174–184CrossRefGoogle Scholar
  39. Knapp AK, Briggs JM, Hartnett DC, Collins SL (eds) (1998) Grassland dynamics. Oxford University Press, New YorkGoogle Scholar
  40. La Pierre KJ, Joern A, Smith MD (2015) Invertebrate, not small vertebrate, herbivory interacts with nutrient availability to impact tallgrass prairie community composition and forb biomass. Oikos. doi: 10.1111/oik.01869 Google Scholar
  41. Lauenroth WK, Burke IC (eds) (2008) Ecology of the shortgrass steppe: a long-term perspective. Oxford University Press, OxfordGoogle Scholar
  42. Loaiza V, Jonas JL, Joern A (2008) Does dietary P affect feeding and performance in the mixed-feeding grasshopper, (Acrididae) Melanoplus bivitattus? Environ Entomol 37:333–339PubMedGoogle Scholar
  43. Loaiza V, Jonas JL, Joern A (2011) Grasshoppers (Orthoptera: Acrididae) select vegetation patches in local-scale responses to foliar nitrogen but not phosphorus in native grassland. Insect Sci 18:533–540. doi: 10.1111/j.1744-7917.2010.01376.x CrossRefGoogle Scholar
  44. Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161. doi: 10.1146/ CrossRefGoogle Scholar
  45. McCulley R, Burke IC, Lauenroth WK (2009) Conservation of nitrogen increases with precipitation across a major grassland gradient in the Central Great Plains of North America. Oecologia 159:571–581. doi: 10.1007/s00442-008-1229-1 CrossRefPubMedGoogle Scholar
  46. Milchunas DG, Sala OE, Lauenroth WK (1988) A generalized-model of the effects of grazing by large herbivores on grassland community structure. Am Nat 132:87–106CrossRefGoogle Scholar
  47. Milchunas DG, Lauenroth WK, Chapman PL, Kazempour MK (1990) Community attributes along a perturbation gradient in a shortgrass steppe. J Veg Sci 1:375–384CrossRefGoogle Scholar
  48. Oedekoven MA, Joern A (2000) Plant quality and spider predation affects grasshoppers (Acrididae): food-quality-dependent compensatory mortality. Ecology 81:66–77CrossRefGoogle Scholar
  49. Risser PG, Birney EC, Blocker HD, May SW, Parton WJ, Wins JA (eds) (1981) The true prairie ecosystem. Hutchinson Ross, StroudsburgGoogle Scholar
  50. Schmitz OJ (2003) Top predator control of plant biodiversity and productivity in an old-field ecosystem. Ecol Lett 6:156–163CrossRefGoogle Scholar
  51. Schmitz OJ (2008a) Effects of predator hunting mode on grassland ecosystem function. Science 319:952–954. doi: 10.1126/science.1152355 CrossRefPubMedGoogle Scholar
  52. Schmitz OJ (2008b) Herbivory from individuals to ecosystems. Annu Rev Ecol Evol Syst 39:133–152. doi: 10.1146/annurev.ecolsys.39.110707.173418 CrossRefGoogle Scholar
  53. Siemann E (1998) Experimental tests of effects of plant productivity and diversity on grassland arthropod diversity. Ecology 79:2057–2070CrossRefGoogle Scholar
  54. Sterner R, Elser JJ, Hessen D (1992) Stoichiometric relationships among producers, consumers and nutrient cycling in pelagic ecosystems. Biogeochemistry 17:49–67CrossRefGoogle Scholar
  55. Throop HL, Lerdau M (2004) Effects of nitrogen deposition on insect herbivory: implications for community and ecosystem processes. Ecosystems 7:109–133. doi: 10.1007/s10021-003-0225-x CrossRefGoogle Scholar
  56. Whiles MR, Charlton RE (2006) The ecological significance of tallgrass prairie arthropods. Annu Rev Entomol 51:387–412CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyYale UniversityNew HavenUSA
  2. 2.Department of Integrative BiologyUniversity of California, BerkeleyBerkeleyUSA
  3. 3.Department of BiologyColorado State UniversityFort CollinsUSA

Personalised recommendations