Skip to main content

Advertisement

Log in

Ecosystem carbon exchange in response to locust outbreaks in a temperate steppe

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

Abstract

It is predicted that locust outbreaks will occur more frequently under future climate change scenarios, with consequent effects on ecological goods and services. A field manipulative experiment was conducted to examine the responses of gross ecosystem productivity (GEP), net ecosystem carbon dioxide (CO2) exchange (NEE), ecosystem respiration (ER), and soil respiration (SR) to locust outbreaks in a temperate steppe of northern China from 2010 to 2011. Two processes related to locust outbreaks, natural locust feeding and carcass deposition, were mimicked by clipping 80 % of aboveground biomass and adding locust carcasses, respectively. Ecosystem carbon (C) exchange (i.e., GEP, NEE, ER, and SR) was suppressed by locust feeding in 2010, but stimulated by locust carcass deposition in both years (except SR in 2011). Experimental locust outbreaks (i.e., clipping plus locust carcass addition) decreased GEP and NEE in 2010 whereas they increased GEP, NEE, and ER in 2011, leading to neutral changes in GEP, NEE, and SR across the 2 years. The responses of ecosystem C exchange could have been due to the changes in soil ammonium nitrogen, community cover, and aboveground net primary productivity. Our findings of the transient and neutral changes in ecosystem C cycling under locust outbreaks highlight the importance of resistance, resilience, and stability of the temperate steppe in maintaining reliable ecosystem services, and facilitate the projections of ecosystem functioning in response to natural disturbance and climate change.

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
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Albani M, Moorcroft PR, Ellison AM, Orwig DA, Foster DR (2010) Predicting the impact of hemlock woolly adelgid on carbon dynamics of eastern United States forests. Can J For Res 40:119–133

    Article  CAS  Google Scholar 

  • Amiro BD, Barr AG, Barr JG, Black TA, Bracho R, Brown M, Chen J, Clark KL, Davis KJ, Desai AR et al (2010) Ecosystem carbon dioxide fluxes after disturbance in forests of North America. J Geophys Res 115(G4). doi:10.1029/2010JG001390

  • Bardgett RD (2005) The biology of soil: a community and ecosystem approach. Oxford University Press, New York

    Book  Google Scholar 

  • Barton PS, Cunningham SA, Lindenmayer DB, Manning AD (2013) The role of carrion in maintaining biodiversity and ecological processes in terrestrial ecosystems. Oecologia 171:761–772

    Article  PubMed  Google Scholar 

  • Begna SH, Fielding DJ (2005) Response of barley to grasshopper defoliation in interior Alaska: dry matter and grain yield. J Econ Entomol 98:1969–1976

    Article  PubMed  Google Scholar 

  • Begna SH, Fielding DJ (2008) Growth and yield of barley in relation to grasshopper feeding damage. Can J Plant Sci 88:219–227

    Article  Google Scholar 

  • Belovsky GE, Slade JB (2000) Insect herbivory accelerates nutrient cycling and increases plant production. Proc Natl Acad Sci USA 97:14412–14417

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Blais JR (1981) Mortality of balsam fir and white spruce following a spruce budworm outbreaks in the Ottawa River watershed in Québec. Can J For Res 11:620–629

    Article  Google Scholar 

  • Blumer P, Diemer M (1996) The occurrence and consequences of grasshopper herbivory in an alpine grassland, Swiss Central Alps. Arct Alp Res 28:435–440

    Article  Google Scholar 

  • Branson DH (2010) Density-dependent effects of an early season insect herbivore on a later developing insect herbivore. Environ Entomol 39:346–350

    Article  PubMed  Google Scholar 

  • Branson DH, Haferkamp MA (2014) Insect herbivory and vertebrate grazing impact food limitation and grasshopper populations during a severe outbreak. Ecol Entomol 39:371–381

    Article  Google Scholar 

  • Brown DG (1994) Beetle folivory increases resource availability and alters plant invasion in monocultures of goldenrod. Ecology 75:1673–1683

    Article  Google Scholar 

  • Brown M, Black TA, Nesic Z, Foord VN, Spittlehouse DL, Fredeen AL, Trofymow JA (2010) Impact of mountain pine beetle on the net ecosystem production of lodgepole pine stands in British Columbia. Agric For Meteorol 150:254–264

    Article  Google Scholar 

  • Burleson WH, Hewitt GB (1982) Response of needle-and-thread and Western wheatgrass to defoliation by grasshoppers. J Rangel Manage 35:223–226

    Article  Google Scholar 

  • Carlton RG, Goldman CR (1984) Effects of a massive swarm of ants on ammonium concentrations in a subalpine lake. Hydrobiologia 111:113–117

    Article  Google Scholar 

  • Carson WP, Root RB (1999) Top-down effects of insect herbivores during early succession: influence on biomass and plant dominance. Oecologia 121:260–272

    Article  Google Scholar 

  • Carson WP, Root RB (2000) Herbivory and plant species coexistence: community regulation by an outbreaking phytophagous insect. Ecol Monogr 70:73–99

    Article  Google Scholar 

  • Cease AJ, Elser JJ, Ford CF, Hao SG, Kang L, Harrison JF (2012) Heavy livestock grazing promotes locust outbreaks by lowering plant nitrogen content. Science 335:467–469

    Article  CAS  PubMed  Google Scholar 

  • Chase JM (1996) Abiotic controls of trophic cascades in a simple grassland food chain. Oikos 77:495–506

    Article  Google Scholar 

  • Chen YL (1999) The locust and grasshopper pests of China. China Forestry Publishing House, Beijing

    Google Scholar 

  • Chen SH, Wulanbater, Cao YF (2006) Effects of climatic change on grassland locust in Inner Mongolia. Prata Sci 23:78–82

    CAS  Google Scholar 

  • Clark KL, Skowronski N, Hom J (2010) Invasive insects impact forest carbon dynamics. Glob Change Biol 16:88–101

    Article  Google Scholar 

  • Cobb R (2010) Species shift drives decomposition rates following invasion by hemlock woolly adelgid. Oikos 119:1291–1298

    Article  Google Scholar 

  • Cook BD, Bolstad PV, Martin JG, Heinsch FA, Davis KJ, Wang WG, Teclaw RM (2008) Using light-use and production efficiency models to predict photosynthesis and net carbon exchange during forest canopy disturbance. Ecosystems 11:26–44

    Article  CAS  Google Scholar 

  • COPR (Centre for Overseas Pest Research) (1982) The locust and grasshopper agricultural manual. Centre Overseas Pest Research, London

    Google Scholar 

  • Coupe MD, Cahill JF (2003) Effects of insects on primary production in temperate herbaceous communities: a meta-analysis. Ecol Entomol 28:511–521

    Article  Google Scholar 

  • Despland E, Rosenberg J, Simpson SJ (2004) Landscape structure and locust swarming: a satellite’s eye view. Ecography 27:381–391

    Article  Google Scholar 

  • Dyer MI, Turner CL, Seastedt TR (1993) Herbivory and its consequences. Ecol Appl 3:10–16

    Article  Google Scholar 

  • Dymond CC, Neilson ET, Stinson G, Porter K, MacLean DA, Gray DR, Campagna M, Kurz WA (2010) Future spruce budworm outbreak may create a carbon source in eastern Canadian forests. Ecosystems 13:917–931

    Article  CAS  Google Scholar 

  • Esper J, Büntgen U, Frank DC, Nievergelt D, Liebhold A (2007) 1200 years of regular outbreaks in alpine insects. Proc R Soc B 274:671–679

    Article  PubMed Central  PubMed  Google Scholar 

  • Fonte SJ, Schowalter TD (2005) The influence of a neotropical herbivore (Lamponius portoricensis) on nutrient cycling and soil processes. Oecologia 146:423–431

    Article  CAS  PubMed  Google Scholar 

  • Frost CJ, Hunter MD (2004) Insect canopy herbivory and frass deposition affect soil nutrient dynamics and export in oak mesocosms. Ecology 85:3335–3347

    Article  Google Scholar 

  • Fry B, Joern A, Parker PL (1978) Grasshopper food web analysis: use of carbon isotope ratios to examine feeding relationships among terrestrial herbivores. Ecology 59:498–506

    Article  Google Scholar 

  • Gibson DJ, Freeman CC, Hulbert LC (1990) Effects of small mammal and invertebrate herbivory on plant species richness and abundance in tallgrass prairie. Oecologia 84:169–175

    Article  Google Scholar 

  • Hawlena D, Strickland MS, Bradford MA, Schmitz OJ (2012) Fear of predation slows plant-litter decomposition. Science 336:1434–1438

    Article  CAS  PubMed  Google Scholar 

  • Hewitt GB, Onsager JA (1982) A method for forecasting potential losses from grasshopper feeding on northern mixed prairie forages. J Rangel Manage 35:53–57

    Article  Google Scholar 

  • Hewitt GB, Burleson WH, Onsager JA (1976) Forage losses caused by the grasshopper Aulocara elliotti on shortgrass rangeland. J Rangel Manage 29:376–380

    Article  Google Scholar 

  • Hollinger DY (1986) Herbivory and the cycling of nitrogen and phosphorus in isolated California oak trees. Oecologia 70:291–297

    Article  Google Scholar 

  • Hoogesteger J, Karlsson PS (1992) Effects of defoliation on radial stem growth and photosynthesis in the mountain birch (Betula pubescens ssp. tortuosa). Funct Ecol 6:317–323

    Article  Google Scholar 

  • Hunter MD (2001) Insect population dynamics meets ecosystem ecology: effects of herbivory on soil nutrient dynamics. Agric For Entomol 3:77–84

    Article  Google Scholar 

  • Jardon Y, Filion L, Cloutier C (1994) Long-term impact of insect defoliation on growth and mortality of eastern larch in boreal Québec. Ecoscience 1:231–238

    Google Scholar 

  • Kula AAR, Hartnett DC, Wilson GWT (2005) Effects of mycorrhizal symbiosis on tallgrass prairie plant-herbivore interactions. Ecol Lett 8:61–69

    Article  Google Scholar 

  • Kurz WA, Apps MJ (1999) A 70-year retrospective analysis of carbon fluxes in the Canadian forest sector. Ecol Appl 9:526–547

    Article  Google Scholar 

  • Kurz WA, Dymond CC, Stinson G, Rampley GJ, Neilson ET, Carroll AL, Ebata T, Safranyik L (2008a) Mountain pine beetle and forest carbon feedback to climate change. Nature 452:987–990

    Article  CAS  PubMed  Google Scholar 

  • Kurz WA, Stinson G, Rampley GJ, Dymond CC, Neilson ET (2008b) Risk of natural disturbances makes future contribution of Canada’s forests to the global carbon cycle highly uncertain. Proc Natl Acad Sci USA 105:1551–1555

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Landsberg J, Ohmart C (1989) Levels of insect defoliation in forests: patterns and concepts. Trends Ecol Evol 4:96–100

    Article  Google Scholar 

  • Lecoq M (2001) Recent progress in desert and migratory locust management in Africa. Are preventative actions possible? J Orthop Res 10:277–291

    Article  Google Scholar 

  • Li H (2007) Prediction of grassland locusts based on meteorological data in Inner Mongolia. Master’s thesis, Graduate School of Chinese Academy of Agricultural Sciences, Beijing

  • Lima M (2007) Locust plagues, climate variation, and the rhythms of nature. Proc Natl Acad Sci USA 104:15972–15973

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu L, Guo A (2004) Analysis of meteorological and ecological conditions of grasshopper infestation in Inner Mongolia in 2004. Meteorol Mon 11:55–57

    Google Scholar 

  • Loranger H, Weisser WW, Ebeling A, Eggers T, de Luca E, Loranger J, Roscher C, Meyer ST (2014) Invertebrate herbivory increases along an experimental gradient of grassland plant diversity. Oecologia 174:183–193

    Article  PubMed  Google Scholar 

  • Lovett GM, Canham CD, Arthur MA, Weathers KC, Fitzhugh RD (2006) Forest ecosystem response to exotic pests and pathogens in eastern North America. Bioscience 56:395–405

    Article  Google Scholar 

  • Ma SC, Ding YC, Yi DM (1965) Study on long-term prediction of locust population fluctuations. Acta Entomol Sinica 14:319–338

    Google Scholar 

  • MacLean DA (1984) Effects of spruce budworm outbreaks on the productivity and stability of balsam fir forests. For Chron 60:273–279

    Article  Google Scholar 

  • Mattson WJ, Addy ND (1975) Phytophagous insects as regulators of forest primary production. Science 190:515–522

    Article  Google Scholar 

  • Meehl GA, Tebaldi C (2004) More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305:994–997

    Article  CAS  PubMed  Google Scholar 

  • Moore DJP, Trahan NA, Wilkes P, Quaife T, Stephens BB, Elder K, Desail AR, Negron J, Monson RK (2013) Persistent reduced ecosystem respiration after insect disturbance in high elevation forests. Ecol Lett 16:731–737

    Article  PubMed Central  PubMed  Google Scholar 

  • Niu SL, Wu MY, Han Y, Xia JY, Zhang Z, Yang HJ, Wan SQ (2010) Nitrogen effects on net ecosystem carbon exchange in a temperate steppe. Glob Change Biol 16:144–155

    Article  Google Scholar 

  • Nowlin WH, González MJ, Vanni MJ, Stevens MH, Fields MW, Valente JJ (2007) Allochthonous subsidy of periodical cicadas affects the dynamics and stability of pond communities. Ecology 88:2174–2186

    Article  PubMed  Google Scholar 

  • Orians CM, Thorn A, Gómez S (2011) Herbivore-induced resource sequestration in plants: why bother? Oecologia 167:1–9

    Article  PubMed  Google Scholar 

  • Ott SR, Verlinden H, Rogers SM, Brighton CH, Quah PS, Vleugels RK, Verdonck R, Broeck JV (2012) Critical role for protein kinase A in the acquisition of gregarious behavior in the desert locust. Proc Natl Acad Sci USA 109:E381–E387

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Parmenter RR, MacMahon JA (2009) Carrion decomposition and nutrient cycling in a semiarid shrub-steppe ecosystem. Ecol Monogr 79:637–661

    Article  Google Scholar 

  • Pedgley DE (1989) Weather and the current desert locust plague. Weather 44:168–171

    Article  Google Scholar 

  • Redak RA, Capinera JL (1994) Changes in western wheatgrass foliage quality following defoliation: consequences for a graminivorous grasshopper. Oecologia 100:80–88

    Article  Google Scholar 

  • Reef R, Ball MC, Lovelock CE (2012) The impact of a locust plague on mangroves of the arid Western Australia coast. J Trop Ecol 28:307–311

    Article  Google Scholar 

  • Risley LS, Crossley DA Jr (1993) Contribution of herbivore-caused greenfall to litterfall nitrogen flux in several southern Appalachian forested watersheds. Am Midl Nat 129:67–74

    Article  Google Scholar 

  • Ritchie ME, Tilman D (1992) Interspecific competition among grasshoppers and their effect on plant abundance in experimental field environments. Oecologia 89:524–532

    Article  Google Scholar 

  • Ritchie ME, Tilman D (1993) Predictions of species interactions from consumer-resource theory: experimental tests with grasshoppers and plants. Oecologia 94:516–527

    Article  Google Scholar 

  • Rose KE, Russell FL, Louda SM (2011) Integral projection model of insect herbivore effects on Cirsium altissimum populations along productivity gradients. Ecosphere 2:art97. doi:10.1890/ES11-00096.1

    Article  Google Scholar 

  • Sánchez-Zapata JA, Donázar JA, Delgado A, Forero MG, Ceballos O, Hiraldo F (2007) Desert locust outbreak in the Sahel: resource competition, predation and ecological effects of pest control. J Appl Ecol 44:323–329

    Article  Google Scholar 

  • Schär C, Vidale PL, Lüthi D, Frei C, Häberli C, Liniger MA, Appenzeller C (2004) The role of increasing temperature variability in European summer heatwaves. Nature 427:332–336

    Article  PubMed  Google Scholar 

  • Scherber C, Heimann J, Köhler G, Mitschunas N, Weisser WW (2010) Functional identity versus species richness: herbivory resistance in plant community. Oecologia 163:707–717

    Article  PubMed Central  PubMed  Google Scholar 

  • Schiermeier Q (2011) Increased flood risk linked to global warming. Nature 470:315

    Google Scholar 

  • Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602

    Article  Google Scholar 

  • Schowalter TD, Hargrove WW, Crossley DA (1986) Herbivory in forested ecosystems. Annu Rev Entomol 31:177–196

    Article  Google Scholar 

  • Schowalter TD, Fonte SJ, Geaghan J, Wang J (2011) Effects of manipulated herbivore inputs on nutrient flux and decomposition in a tropical rainforest in Puerto Rico. Oecologia 167:1141–1149

    Article  CAS  PubMed  Google Scholar 

  • Seastedt TR, Tate CM (1981) Decomposition rates and nutrient contents of arthropod remains in forest litter. Ecology 62:13–19

    Article  CAS  Google Scholar 

  • Stige LC, Chan KS, Zhang ZB, Frank D, Stenseth NC (2007) Thousand-year-long Chinese time series reveals climatic forcing of decadal locust dynamics. Proc Natl Acad Sci USA 104:16188–16193

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Stinson G, Kurz WA, Smyth CE, Neilson ET, Dymond CC, Metsaranta JM, Boisvenue C, Rampley GJ, Li Q, White TM, Blain D (2011) An inventory-based analysis of Canada’s managed forest carbon dynamics, 1990 to 2008. Glob Change Biol 17:2227–2244

    Article  Google Scholar 

  • Sun T, Zhao JX, Tian LH, Liu ZY, Long RJ (2010) Reasons for an outbreak of grassland grasshoppers and sustainable management strategies for them. Acta Prata Sinica 19:220–227

    Google Scholar 

  • Suwa T, Louda SM (2012) Combined effects of plant competition and insect herbivory hinder invasiveness of an introduced thistle. Oecologia 169:467–476

    Article  PubMed  Google Scholar 

  • Tanaka S (2006) Corazonin and locust phase polyphenism. Appl Entomol Zool 41:179–193

    Article  CAS  Google Scholar 

  • Tanaka S, Zhu D (2005) Outbreaks of the migratory locust Locusta migratoria (Orthoptera: Acrididae) and control in China. Appl Entomol Zool 40:257–263

    Article  Google Scholar 

  • Thompson DC, McDaniel KC, Torell LA (1996) Feeding by a native grasshopper reduces broom snakeweed density and biomass. J Rangel Manage 49:407–412

    Article  Google Scholar 

  • Tian HD, Stige LC, Cazelles B, Kausrud KL, Svarverud R, Stenseth NC, Zhang ZB (2011) Reconstruction of a 1,910-y-long locust series reveals consistent associations with climate fluctuations in China. Proc Natl Acad Sci USA 108:14521–14526

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Todd MC, Washington R, Cheke RA, Kniveton D (2002) Brown locust outbreaks and climate variability in southern Africa. J Appl Ecol 39:31–42

    Article  Google Scholar 

  • Topaz CM, D’Orsogna MR, Edelstein-Keshet L, Bernoff AJ (2012) Locust dynamics: behavioral phase change and swarming. PLoS Comput Biol 8:e1002642. doi:10.1371/journal.pcbi.1002642

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Towne EG (2000) Prairie vegetation and soil nutrient responses to ungulate carcasses. Oecologia 122:232–239

    Article  Google Scholar 

  • Veblen TT, Hadley KS, Reid MS, Rebertus AJ (1991) The response of subalpine forests to spruce beetle outbreaks in Colorado. Ecology 72:213–231

    Article  Google Scholar 

  • Wang ZJ, Qin QL, He SG, Chen YL, Li HC, Li DM (2002) Present status of locust outbreak and its sustainable control strategies in China. Entomol Knowl 39:172–175

    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 

  • Xia JY, Niu SL, Wan SQ (2009) Response of ecosystem carbon exchange to warming and nitrogen addition during two hydrologically contrasting growing seasons in a temperate steppe. Glob Change Biol 15:1544–1556

    Article  Google Scholar 

  • Yamagishi M, Tanaka S (2009) Overwintering biology and morphological characteristics of the migratory locust, Locusta migratoria after outbreaks on Iheya Island, Japan. Appl Entomol Zool 44:165–174

    Article  Google Scholar 

  • Yang LH (2004) Periodical cicadas as resource pulses in North American forests. Science 306:1565–1567

    Article  CAS  PubMed  Google Scholar 

  • Yang LH (2013) Resource pulses of dead periodical cicadas increase the growth of American bellflower rosettes under competitive and non-competitive conditions. Arthropod-Plant Interact 7:93–98

    Article  Google Scholar 

  • Yu G, Shen HD, Liu J (2009) Impacts of climate change on historical locust outbreak in China. J Geophys Res 114(D18). doi:10.1029/2009JD011833

  • Zhang ZB, Li DM (1999) A possible relationship between outbreaks of the oriental migratory locust (Locusta migratoria manilensis Meyen) in China and the E1 Niño episodes. Ecol Res 14:267–270

    Article  Google Scholar 

  • Zhang ZB, Cazelles B, Tian HD, Stige LC, Bräuning A, Stenseth NC (2009) Periodic temperature-associated drought/flood drives locust plagues in China. Proc R Soc B 276:823–831

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhang G, Han X, Elser JJ (2011) Rapid top-down regulation of plant C:N:P stoichiometry by grasshoppers in an inner Mongolia grassland ecosystem. Oecologia 166:253–264

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Amy Austin, two anonymous reviewers, Guoyong Li, Zhongling Yang, Yinzhan Liu, Cancan Zhao, Dandan Wang, Tingjuan Wu, Feng Wang, Xiaoming Li, Fanglong Su, Yuan Miao, Gaigai Ma, and Bin Liu for their thoughtful comments and suggestions, which helped in improving the manuscript. The authors thank Zhikun Feng, Anqun Chen, Lili Zhu, Jianyang Xia, Haijun Yang, Junyi Liang, Qian Zhang, Minghao Cui, Jingjing Gao, and Zhenxing Zhou for their help in the field and laboratory. This study was financially supported by the Ministry of Science and Technology (2013CB956300) and the Natural Science Foundation (41030104/D0308) of China.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shiqiang Wan.

Additional information

Communicated by Amy Austin.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Song, J., Wu, D., Shao, P. et al. Ecosystem carbon exchange in response to locust outbreaks in a temperate steppe. Oecologia 178, 579–590 (2015). https://doi.org/10.1007/s00442-015-3248-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-015-3248-z

Keywords

Navigation