Elevated atmospheric carbon dioxide concentrations alter root morphology and reduce the effectiveness of entomopathogenic nematodes

Abstract

Aims

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.

Methods

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.

Results

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.

Conclusions

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Abbreviations

EPN:

Entomopathogenic nematode

aCO2 :

Ambient carbon dioxide (400 μmol mol−1)

eCO2 :

Elevated carbon dioxide (640 μmol mol−1)

CO2 :

Carbon dioxide

SEM:

Structural equation modeling

References

  1. 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

    PubMed  CAS  Google Scholar 

  2. 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

    CAS  Google Scholar 

  3. 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

    PubMed  CAS  Google Scholar 

  4. Burnell AM, Stock SP (2000) Heterorhabditis, Steinernema and their bacterial symbionts - lethal pathogens of insects. Nematology 2:31–42

    Google Scholar 

  5. 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

    Google Scholar 

  6. Cheng W, Johnson DW (1998) Elevated CO2, rhizosphere processes, and soil organic matter decomposition. Plant Soil 202:167–174

    CAS  Google Scholar 

  7. 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

    Google Scholar 

  8. 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

    PubMed  CAS  Google Scholar 

  9. 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

    PubMed  PubMed Central  CAS  Google Scholar 

  10. 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

    PubMed  Google Scholar 

  11. 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

    Google Scholar 

  12. 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

    Google Scholar 

  13. 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

    Google Scholar 

  14. 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

    PubMed  CAS  Google Scholar 

  15. Fierer N, Strickland MS, Liptzin D, Bradford MA, Cleveland CC (2009) Global patterns in belowground communities. Ecol Lett 12:1238–1249

    PubMed  Google Scholar 

  16. 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

    Google Scholar 

  17. Grace JB (2006) Structural equation modeling and natural systems. Cambridge University Press, Cambridge

    Google Scholar 

  18. Gregory PJ (2006) Plant roots - growth, activity and interaction with soils, 1st edn. Blackwell Publishing, Oxford

    Google Scholar 

  19. 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

    Google Scholar 

  20. 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

    Google Scholar 

  21. 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

    Google Scholar 

  22. 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

    Google Scholar 

  23. Hiltpold I, Hibbard BE (2018) Indirect root defenses cause induced fitness costs in Bt-resistant western corn rootworm. J Econ Entomol 111:2349–2358

    PubMed  CAS  Google Scholar 

  24. Hiltpold I, Turlings TCJ (2008) Belowground chemical signaling in maize: when simplicity rhymes with efficiency. J Chem Ecol 34:628–635

    PubMed  CAS  Google Scholar 

  25. 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

    CAS  Google Scholar 

  26. 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

    Google Scholar 

  27. 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

    Google Scholar 

  28. Johnson SN, McNicol JW (2010) Elevated CO2 and aboveground-belowground herbivory by the clover root weevil. Oecologia 162:209–216

    PubMed  Google Scholar 

  29. Johnson SN, Riegler M (2013) Root damage by insects reverses the effects of elevated atmospheric CO2 on eucalypt seedlings. PLoS One 8:e79479

    PubMed  PubMed Central  Google Scholar 

  30. 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

    Google Scholar 

  31. 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

    PubMed  PubMed Central  Google Scholar 

  32. Kaya HK, Gaugler R (1993) Entomopathogenic nematodes. Annu Rev Entomol 38:181–206

    Google Scholar 

  33. 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

    PubMed  CAS  Google Scholar 

  34. 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

    Google Scholar 

  35. Long SP, Ainsworth EA, Rogers A, Ort DR (2004) Rising atmospheric carbon dioxide: plants face the future. Annu Rev Plant Biol 55:591–628

    PubMed  CAS  Google Scholar 

  36. Marston N, Campbell B (1973) Comparison of nine diets for rearing Galleria mellonella. Ann Entomol Soc Am 66:132–136

    Google Scholar 

  37. Newman JA, Anand M, Henry HAL, Hunt S (2011) Climate change biology. CABI, Cambridge

  38. 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

    Google Scholar 

  39. Pritchard SG (2011) Soil organisms and global climate change. Plant Pathol 60:82–99

    Google Scholar 

  40. Pritchard SG, Rogers HH (2000) Spatial and temporal deployment of crop roots in CO2-enriched environments. New Phytol 147:55–71

    CAS  Google Scholar 

  41. Pritchard SG, Rogers HH, Prior SA, Peterson CM (1999) Elevated CO2 and plant structure: a review. Glob Chang Biol 5:807–837

    Google Scholar 

  42. R Development Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  43. 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

    PubMed  CAS  Google Scholar 

  44. Rogers HH, Prior SA, Runion GB, Mitchell RJ (1996) Root to shoot ratio of crops as influenced by CO2. Plant Soil 187:229–248

    CAS  Google Scholar 

  45. 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

  46. 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

    Google Scholar 

  47. 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

    Google Scholar 

  48. Torr P, Heritage S, Wilson MJ (2004) Vibrations as a novel signal for host location by parasitic nematodes. Int J Parasitol 34:997–999

    PubMed  CAS  Google Scholar 

  49. Turlings TCJ, Hiltpold I, Rasmann S (2012) The importance of root-produced volatiles as foraging cues for entomopathogenic nematodes. Plant Soil 358:47–56

    Google Scholar 

  50. 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

    Google Scholar 

  51. White GF (1927) A method for obtaining infective nematode larvae from cultures. Science 66:302–303

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

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

Author information

Affiliations

Authors

Corresponding author

Correspondence to Ivan Hiltpold.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Responsible Editor: Matthew G. Bakker.

Electronic supplementary material

Online Resource 1

(PDF 311 kb)

Online Resource 2

(PDF 486 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

Keywords

  • Soil microbiome
  • Climate change
  • Root morphology
  • Root herbivore
  • Pest control