Skip to main content
Log in

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

  • Community ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adler PB, Levine JM (2007) Contrasting relationships between precipitation and species richness in space and time. Oikos 116:221–232

    Article  Google Scholar 

  • Agrawal AA, Fishbein M (2006) Plant defense syndromes. Ecology 87:S132–S149

    Article  PubMed  Google Scholar 

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  • Anderson MJ (2005) Permutational multivariate analysis of variance

  • Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62:245–253. doi:10.1111/j.1541-0420.2005.00440.x

    Article  PubMed  Google Scholar 

  • Behmer ST (2009) Insect herbivore nutrient regulation. Annu Rev Entomol 54:165–187. doi:10.1146/annurev.ento.54.110807.090537

    Article  CAS  PubMed  Google Scholar 

  • Behmer ST, Joern A (1993) Diet choice by a grass-feeding grasshopper based on the need for a limiting nutrient. Funct Ecol 7:522–527

    Article  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Berner D, Blanckenhorn WU, Korner C (2005) Grasshoppers cope with low host plant quality by compensatory feeding and food selection: N limitation challenged. Oikos 111:525–533

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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 86:528–537

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Burnham KP (2004) Multimodel inference: understanding AIC and BIC in model selection. Sociol Methods Res 33:261–304. doi:10.1177/0049124104268644

    Article  Google Scholar 

  • Chambers P, Simpson SJ, Raubenheimer D (1995) Behavioural mechanisms of nutrient balancing in Locusta migratoria nymphs. Anim Behav 50:1513–1523

    Article  Google Scholar 

  • Chapin FS, Autumn K, Pugnaire F (1993) Evolution of suites of traits in response to environmental stress. Am Nat 142:S78–S92

    Article  Google Scholar 

  • Chase JM, Leibold MA, Downing AL, Shurin JB (2000) The effects of productivity, herbivory, and plant species turnover in grassland food webs. Ecology 81:2485–2497

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Cleland EE, Harpole WS (2010) Nitrogen enrichment and plant communities. Year in ecology and conservation biology 2010. Blackwell, Oxford, pp 46–61

    Google Scholar 

  • Cleland EE, Peters HA, Mooney HA, Field CB (2006) Gastropod herbivory in response to elevated CO2 and N addition impacts plant community composition. Ecology 87:686–694

    Article  PubMed  Google Scholar 

  • 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 139:221–233

    Article  Google Scholar 

  • Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899. doi:10.1126/science.230.4728.895

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • Denno RF, Fagan W (2003) Might nitrogen limitation promote omnivory among carnivorous arthropods? Ecology 84:2522–2531

    Article  Google Scholar 

  • Denno RF, Gratton C, Peterson M (2002) Bottom-up forces mediate natural-enemy impact in a phytophagous insect community. Ecology 83:1443–1458

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 408:578–580

    Article  CAS  PubMed  Google Scholar 

  • 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 160:784–802

    Article  PubMed  Google Scholar 

  • Fink P, von Elert E (2006) Physiological responses to stoichiometric constraints: nutrient limitation and compensatory feeding in a freshwater snail. Oikos 115:484–494

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 12:1029–1039

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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 157:92–105

    Article  Google Scholar 

  • Huxel GR (1999) On the influence of food quality in consumer-resource interactions. Ecol Lett 2:256–261

    Article  Google Scholar 

  • Joern A, Behmer ST (1998) Impact of diet quality on demographic attributes in adult grasshoppers and the nitrogen limitation hypothesis. Ecol Entomol 23:174–184

    Article  Google Scholar 

  • Knapp AK, Briggs JM, Hartnett DC, Collins SL (eds) (1998) Grassland dynamics. Oxford University Press, New York

    Google Scholar 

  • 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 

  • Lauenroth WK, Burke IC (eds) (2008) Ecology of the shortgrass steppe: a long-term perspective. Oxford University Press, Oxford

    Google Scholar 

  • Loaiza V, Jonas JL, Joern A (2008) Does dietary P affect feeding and performance in the mixed-feeding grasshopper, (Acrididae) Melanoplus bivitattus? Environ Entomol 37:333–339

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161. doi:10.1146/annurev.es.11.110180.001003

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Milchunas DG, Sala OE, Lauenroth WK (1988) A generalized-model of the effects of grazing by large herbivores on grassland community structure. Am Nat 132:87–106

    Article  Google Scholar 

  • Milchunas DG, Lauenroth WK, Chapman PL, Kazempour MK (1990) Community attributes along a perturbation gradient in a shortgrass steppe. J Veg Sci 1:375–384

    Article  Google Scholar 

  • Oedekoven MA, Joern A (2000) Plant quality and spider predation affects grasshoppers (Acrididae): food-quality-dependent compensatory mortality. Ecology 81:66–77

    Article  Google Scholar 

  • Risser PG, Birney EC, Blocker HD, May SW, Parton WJ, Wins JA (eds) (1981) The true prairie ecosystem. Hutchinson Ross, Stroudsburg

    Google Scholar 

  • Schmitz OJ (2003) Top predator control of plant biodiversity and productivity in an old-field ecosystem. Ecol Lett 6:156–163

    Article  Google Scholar 

  • Schmitz OJ (2008a) Effects of predator hunting mode on grassland ecosystem function. Science 319:952–954. doi:10.1126/science.1152355

    Article  CAS  PubMed  Google Scholar 

  • Schmitz OJ (2008b) Herbivory from individuals to ecosystems. Annu Rev Ecol Evol Syst 39:133–152. doi:10.1146/annurev.ecolsys.39.110707.173418

    Article  Google Scholar 

  • Siemann E (1998) Experimental tests of effects of plant productivity and diversity on grassland arthropod diversity. Ecology 79:2057–2070

    Article  Google Scholar 

  • Sterner R, Elser JJ, Hessen D (1992) Stoichiometric relationships among producers, consumers and nutrient cycling in pelagic ecosystems. Biogeochemistry 17:49–67

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Whiles MR, Charlton RE (2006) The ecological significance of tallgrass prairie arthropods. Annu Rev Entomol 51:387–412

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kimberly J. La Pierre.

Additional information

Communicated by Andreas Prinzing.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 44 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

La Pierre, K.J., Smith, M.D. Soil nutrient additions increase invertebrate herbivore abundances, but not herbivory, across three grassland systems. Oecologia 180, 485–497 (2016). https://doi.org/10.1007/s00442-015-3471-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-015-3471-7

Keywords

Navigation