The effects of increasing atmospheric carbon dioxide (CO2) concentrations on beneficial soil fauna, such as entomopathogenic nematodes (EPNs), are poorly understood. We hence aimed to characterize how elevated CO2 (eCO2) affects maize plant (Zea mays) growth, root morphology and the effectiveness of the EPN Heterorhabditis bacteriophora.
We grew plants under ambient CO2 (aCO2; 400 μmol mol-1) and eCO2 (640 μmol mol-1) and quantified shoot growth and six root traits. We simultaneously quantified the effectiveness of EPNs (mortality of insect hosts (Galleria mellonella) and EPN density within hosts) when foraging in planted and plant-free environments. Structural equation modeling (SEM) was used to model direct and indirect relationships between atmospheric CO2, root morphology and EPN effectiveness.
Root systems of plants grown under eCO2 grew faster, longer, denser, and larger than plants grown under aCO2. This in turn reduced EPN effectiveness as, despite no significant difference between aCO2 and eCO2 in host mortality, significantly more nematodes were recovered from hosts in the vicinity of plants grown in aCO2 environment. The SEM model revealed that this impact was indirect and mediated by the increased root morphological traits.
We provide the first example of how changes in atmospheric CO2 indirectly reduce the effectiveness of an EPN used globally for crop protection. Other factors (e.g. plant volatile emissions) may moderate or exacerbate these patterns but our findings suggest that modifications in root traits at eCO2 negatively impact EPN effectiveness and therefore soil-dwelling insect pest management.
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- aCO2 :
Ambient carbon dioxide (400 μmol mol−1)
- eCO2 :
Elevated carbon dioxide (640 μmol mol−1)
- CO2 :
Structural equation modeling
Ainsworth EA, Leakey ADB, Ort DR, Long SP (2008) FACE-ing the facts: inconsistencies and interdependence among field, chamber and modeling studies of elevated [CO2] impacts on crop yield and food supply. New Phytol 179:5–9
Ayres E, Wall DH, Simmons BL, Field CB, Milchunas DG, Morgan JA, Roy J (2008) Belowground nematode herbivores are resistant to elevated atmospheric CO2 concentrations in grassland ecosystems. Soil Biol Biochem 40:978–985
Block A, Vaughan MM, Christensen SA, Alborn HT, Tumlinson JH (2017) Elevated carbon dioxide reduces emission of herbivore-induced volatiles in Zea mays. Plant Cell Environ 40:1725–1734
Burnell AM, Stock SP (2000) Heterorhabditis, Steinernema and their bacterial symbionts - lethal pathogens of insects. Nematology 2:31–42
Campbell JF, Gaugler RR (1997) Inter-specific variation in entomopathogenic nematode foraging strategy: dichotomy or variation along a continuum? Fundam Appl Nematol 20:393–398
Cheng W, Johnson DW (1998) Elevated CO2, rhizosphere processes, and soil organic matter decomposition. Plant Soil 202:167–174
Choo HY, Kaya HK (1991) Influence of soil texture and presence of roots on host finding by Heterorhabditis bacteriophora. J Invertebr Pathol 58:279–280
Cohen I, Rapaport T, Berger RT, Rachmilevitch S (2018) The effects of elevated CO2 and nitrogen nutrition on root dynamics. Plant Sci 272:294–300
Degenhardt J, Hiltpold I, Köllner TG, Frey M, Gierl A, Gershenzon J, Hibbard BE, Ellersieck MR, Turlings TCJ (2009) Restoring a maize root signal that attracts insect-killing nematodes to control a major pest. Proc Natl Acad Sci U S A 106:13213–13218
Demarta L, Hibbard BE, Bohn MO, Hiltpold I (2014) The role of root architecture in foraging behavior of entomopathogenic nematodes. J Invertebr Pathol 122:32–39
Ehlers R-U (2007) Entomopathogenic nematodes: from science to commercial use. In: Vincent C, Toettel MS, Lazarovits G (eds) Biological control: a global perspective. CABI Publishing, Oxfordshire, pp 136–151
Eisenhauer N, Cesarz S, Koller R, Worm K, Reich PB (2012) Global change belowground: impacts of elevated CO2, nitrogen, and summer drought on soil food webs and biodiversity. Glob Chang Biol 18:435–447
Eisenhauer N, Bowker MA, Grace JB, Powell JR (2015) From patterns to causal understanding: structural equation modeling (SEM) in soil ecology. Pedobiologia 58:65–72
Ennis DE, Dillon AB, Griffin CT (2010) Simulated roots and host feeding enhance infection of subterranean insects by the entomopathogenic nematode Steinernema carpocapsae. J Invertebr Pathol 103:140–143
Fierer N, Strickland MS, Liptzin D, Bradford MA, Cleveland CC (2009) Global patterns in belowground communities. Ecol Lett 12:1238–1249
Frederiksen HB, Rønn R, Christensen S (2001) Effect of elevated atmospheric CO2 and vegetation type on microbiota associated with decomposing straw. Glob Chang Biol 7:313–321
Grace JB (2006) Structural equation modeling and natural systems. Cambridge University Press, Cambridge
Gregory PJ (2006) Plant roots - growth, activity and interaction with soils, 1st edn. Blackwell Publishing, Oxford
Gregory PJ, Nortcliff S (2013) The new challenge – sustainable production in a changing environment. In: Gregory PJ, Nortcliff S (eds) Soil conditions and plant growth. Wiley Blackwell, Chichester, pp 417–448
Grewal PS, Lewis EE, Gaugler R, Campbell JF (1994) Host finding behaviour as a predictor of foraging strategy in entomopathogenic nematodes. Parasitology 108:207–215
Haimi J, Laamanen J, Penttinen R, Räty M, Koponen S, Kellomäki S, Niemelä P (2005) Impacts of elevated CO2 and temperature on the soil fauna of boreal forests. Appl Soil Ecol 30:104–112
Hiltpold I (2015) Prospects in the application technology and formulation of entomopathogenic nematodes for biological control of insect pests. In: Campos-Herrera R (ed) Nematode pathogenesis of insects and other pests. Sustainability in plant and crop protection. Springer International Publishing, Heildelberg, pp 187–205
Hiltpold I, Hibbard BE (2018) Indirect root defenses cause induced fitness costs in Bt-resistant western corn rootworm. J Econ Entomol 111:2349–2358
Hiltpold I, Turlings TCJ (2008) Belowground chemical signaling in maize: when simplicity rhymes with efficiency. J Chem Ecol 34:628–635
Hiltpold I, Toepfer S, Kuhlmann U, Turlings TCJ (2010) How maize root volatiles affect the efficacy of entomopathogenic nematodes in controlling the western corn rootworm? Chemoecology 20:155–162
Hiltpold I, Johnson SN, Le Bayon R-C, Nielsen U (2017) Climate change in the underworld: impacts for soil-dwelling invertebrates. In: Johnson SN, Jones TH (eds) Global climate change and terrestrial invertebrates. Wiley, Chichester, pp 201–228
IPCC (2013) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge
Johnson SN, McNicol JW (2010) Elevated CO2 and aboveground-belowground herbivory by the clover root weevil. Oecologia 162:209–216
Johnson SN, Riegler M (2013) Root damage by insects reverses the effects of elevated atmospheric CO2 on eucalypt seedlings. PLoS One 8:e79479
Johnson SN, Barton AT, Clark KE, Gregory PJ, McMenemy LS, Hancock RD (2011) Elevated atmospheric carbon dioxide impairs the performance of root-feeding vine weevils by modifying root growth and secondary metabolites. Glob Chang Biol 17:688–695
Johnson SN, Gherlenda AN, Frew A, Ryalls JMW (2016) The importance of testing multiple environmental factors in legume-insect research: replication, reviewers and rebuttal. Front Plant Sci 7:489
Kaya HK, Gaugler R (1993) Entomopathogenic nematodes. Annu Rev Entomol 38:181–206
Lacey LA, Grzywacz D, Shapiro-Ilan DI, Frutos R, Brownbridge M, Goettel MS (2015) Insect pathogens as biological control agents: Back to the future. J Invertebr Pathol 132:1–41
Lewis EE, Gaugler R, Harrison R (1993) Response of cruiser and ambusher entomopathogenic nematodes (Steinernematidae) to host volatile cues. Can J Zool 71:765–769
Long SP, Ainsworth EA, Rogers A, Ort DR (2004) Rising atmospheric carbon dioxide: plants face the future. Annu Rev Plant Biol 55:591–628
Marston N, Campbell B (1973) Comparison of nine diets for rearing Galleria mellonella. Ann Entomol Soc Am 66:132–136
Newman JA, Anand M, Henry HAL, Hunt S (2011) Climate change biology. CABI, Cambridge
Niklaus PA, Alphei J, Ebersberger D, Kampichler C, Kandeler E, Tscherko D (2003) Six years of in situ CO2 enrichment evoke changes in soil structure and soil biota of nutrient-poor grassland. Glob Chang Biol 9:585–600
Pritchard SG (2011) Soil organisms and global climate change. Plant Pathol 60:82–99
Pritchard SG, Rogers HH (2000) Spatial and temporal deployment of crop roots in CO2-enriched environments. New Phytol 147:55–71
Pritchard SG, Rogers HH, Prior SA, Peterson CM (1999) Elevated CO2 and plant structure: a review. Glob Chang Biol 5:807–837
R Development Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TCJ (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737
Rogers HH, Prior SA, Runion GB, Mitchell RJ (1996) Root to shoot ratio of crops as influenced by CO2. Plant Soil 187:229–248
Rudorff BFT, Mulchi CL, Lee EH, Rowland R, Pausch R (1996) Effect of enhanced O3 and CO2 on plant characteristics in wheat and corn. Environ Pollut 94:53–60
Shapiro-Ilan DI, Hiltpold I, Lewis EE (2017) Nematodes. In: Hajek AE, Shapiro-Ilan DI (eds) Ecology of invertebrate diseases. Wiley, Chichester, pp 415–440
Staley JT, Johnson SN (2008) Climate change impacts on root herbivores. In: Johnson SN, Murray PJ (eds) Root feeders - an ecosystem perspective. CABI, Wallingford, pp 192–213
Torr P, Heritage S, Wilson MJ (2004) Vibrations as a novel signal for host location by parasitic nematodes. Int J Parasitol 34:997–999
Turlings TCJ, Hiltpold I, Rasmann S (2012) The importance of root-produced volatiles as foraging cues for entomopathogenic nematodes. Plant Soil 358:47–56
Wand SJE, Midgley GF, Jones MH, Curtis PS (1999) Responses of wild C4 and C3 grass (Poaceae) species to elevated atmospheric CO2 concentration: a meta-analytic test of current theories and perceptions. Glob Chang Biol 5:723–741
White GF (1927) A method for obtaining infective nematode larvae from cultures. Science 66:302–303
We thank Abisha Srikumar for her support in this project. She was funded by a Summer Student Award from the Hawkesbury Institute for the Environment. This research was funded by the Australian Research Council project DP14100363 awarded to SNJ and BDM
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Hiltpold, I., Moore, B.D. & Johnson, S.N. Elevated atmospheric carbon dioxide concentrations alter root morphology and reduce the effectiveness of entomopathogenic nematodes. Plant Soil 447, 29–38 (2020). https://doi.org/10.1007/s11104-019-04075-0
- Soil microbiome
- Climate change
- Root morphology
- Root herbivore
- Pest control