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RESEARCH ARTICLE

Applications of fipronil (Adonis 3UL) and Metarhizium acridum for use against locusts have minimal effect on litter decomposition and microbial functional diversity in Australian arid grassland

Kimberly Maute A E , Paul Story B , Grant C. Hose C , C. M. Bull D and Kris French A
+ Author Affiliations
- Author Affiliations

A School of Biological Sciences, University of Wollongong, Wollongong, NSW 2522, Australia.

B Australian Plague Locust Commission, GPO Box 858, Canberra, ACT 2601, Australia.

C Department of Biological Sciences, Faculty of Science and Engineering, Macquarie University, Sydney, NSW 2109, Australia.

D School of Biological Sciences, Flinders University, GPO Box 2100, Adelaide, SA 5001, Australia.

E Corresponding author. Email: kmaute@uow.edu.au

Soil Research 55(2) 172-181 https://doi.org/10.1071/SR16002
Submitted: 4 January 2016  Accepted: 19 May 2016   Published: 12 September 2016

Abstract

Litter and microbes are key drivers of nutrient cycles, particularly in arid ecosystems where decomposition rates are low. Locust control in arid regions represents a potentially important hazard to microbes, because local taxa are unlikely to have adapted to pesticide exposure and operations often occur during times of high microbial activity. We monitored the response of aboveground litter decomposition and soil bacteria functional diversity to aerial applications of fipronil (a chemical pesticide) barrier treatments and Metarhizium acridum (a fungal biopesticide) blanket treatments. Decomposition was monitored over 2 years (before and after treatments) using a replicated litter-bag experiment, whereas changes in bacteria functional diversity were measured over 1 month. Analysis of litter mass loss indicated there were no pesticide treatment effects relative to control. Less litter decomposed in small than large mesh bags, and less litter decomposed during the second year of the study. Litter had higher mean nitrogen (N) and carbon (C), and a lower C : N ratio, during the first year of the study. In contrast, within-treatment site analysis revealed a significant increase in litter mass remaining in bags at M. acridum-treated subsites. However, these values were only 4% different from control sites, suggesting that the effect detected may not be biologically significant. There appeared to be no pesticide treatment effect on bacterial community functional diversity and no significant temporal variation. The lack of large-scale pesticide treatment effects suggests that arid zone fungi and bacteria are resilient to such disturbances. Differences in decomposition was explained by differences in the activity of arthropods and in the shade provided by the two mesh sizes, and an annual decline could be attributed to lower litter C and N content and lower annual rainfall in Year 2. Results show the temporal variation possible in decomposition and microbe community measures in arid systems.


References

Aerts R (1997) Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship. Oikos 79, 439–449.
Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship.Crossref | GoogleScholarGoogle Scholar |

Austin AT (2011) Has water limited our imagination for aridland biogeochemistry? Trends in Ecology & Evolution 26, 229–235.
Has water limited our imagination for aridland biogeochemistry?Crossref | GoogleScholarGoogle Scholar |

Austin AT, Vivanco L (2006) Plant litter decomposition in a semi-arid ecosystem controlled by photodegradation. Nature 442, 555–558.
Plant litter decomposition in a semi-arid ecosystem controlled by photodegradation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xnsl2jsLg%3D&md5=a04f424e46993f078f53801fdc2ef4b5CAS | 16885982PubMed |

Austin AT, Yahdjian L, Stark JM, Belnap J, Porporato A, Norton U, Ravetta DA, Schaeffer SM (2004) Water pulses and biogeochemical cycles in arid and semiarid ecosystems. Oecologia 141, 221–235.
Water pulses and biogeochemical cycles in arid and semiarid ecosystems.Crossref | GoogleScholarGoogle Scholar | 14986096PubMed |

Barnes PW, Throop HL, Archer SR, Breshears DD, McCulley RL, Tobler MA (2015) Sunlight and soil–litter mixing: drivers of litter decomposition in drylands. In ‘Progress in botany. Vol. 76’. (Eds U Luttge, W Beyschlag) pp. 273–302. (Springer: Switzerland)

Bünemann EK, Schwenke GD, Van Zwieten L (2006) Impact of agricultural inputs on soil organisms: a review. Soil Research 44, 379–406.
Impact of agricultural inputs on soil organisms: a review.Crossref | GoogleScholarGoogle Scholar |

Campbell C, Grayston S, Hirst D (1997) Use of rhizosphere carbon sources in sole carbon source tests to discriminate soil microbial communities. Journal of Microbiological Methods 30, 33–41.
Use of rhizosphere carbon sources in sole carbon source tests to discriminate soil microbial communities.Crossref | GoogleScholarGoogle Scholar |

Carrera AL, Bertiller MB (2013) Combined effects of leaf litter and soil microsite on decomposition process in arid rangelands. Journal of Environmental Management 114, 505–511.
Combined effects of leaf litter and soil microsite on decomposition process in arid rangelands.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjs1eksA%3D%3D&md5=0fdede5655b783466cd391fc5e20044cCAS | 23186724PubMed |

Christie E (1979) Ecosystem processes in semiarid grasslands. II.* Litter production decomposition and nutrient dynamics. Australian Journal of Agricultural Research 30, 29–42.
Ecosystem processes in semiarid grasslands. II.* Litter production decomposition and nutrient dynamics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXht1SgsL4%3D&md5=9b87d2cded3dca17288eb1a467259973CAS |

Curiel Yuste J, Fernandez-Gonzalez AJ, Fernandez-Lopez M, Ogaya R, Penuelas J, Sardans J, Lloret F (2014) Strong functional stability of soil microbial communities under semiarid Mediterranean conditions and subjected to long-term shifts in baseline precipitation. Soil Biology & Biochemistry 69, 223–233.
Strong functional stability of soil microbial communities under semiarid Mediterranean conditions and subjected to long-term shifts in baseline precipitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXisVynsQ%3D%3D&md5=8cf7d0ac2ef6d0a50b3343d0201d0067CAS |

Cycoń M, Piotrowska-Seget Z (Eds) (2012) Response of soil microflora to pesticides. In ‘Pesticides: evaluation of environmental pollution’. pp. 233–251. (CRC Press: Boca Raton, FL)

Devashree Y, Dutta B, Paul S, Choudhury S (2014) The effect of Paraquat and Fipronil on the soil and rhizosphere microflora of tea (Camellia sinensis (L) O. kuntze). International Journal of Innovation and Applied Studies 7, 1534–1543.

Draganova S, Donkova R, Georgieva D (2008) Impact of strains of entomopathogenic fungi on some main groups of soil microorganisms. Journal of Plant Protection Research 48, 169–179.

Gallo ME, Sinsabaugh RL, Cabaniss SE (2006) The role of ultraviolet radiation in litter decomposition in arid ecosystems. Applied Soil Ecology 34, 82–91.
The role of ultraviolet radiation in litter decomposition in arid ecosystems.Crossref | GoogleScholarGoogle Scholar |

Garland JL, Mills AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Applied and Environmental Microbiology 57, 2351–2359.

Green RH (1979) ‘Sampling design and statistical methods for environmental biologists.’ (John Wiley and Sons: New York, NY)

Gunasekara AS, Truong T, Goh KS, Spurlock F, Tjeerdema RS (2007) Environmental fate and toxicology of fipronil. Journal of Pesticide Science 32, 189–199.
Environmental fate and toxicology of fipronil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVyjtLbP&md5=391ee4dd4038777e39673da2c2bfc1d1CAS |

Hu G, Leger RJS (2002) Field studies using a recombinant mycoinsecticide (Metarhizium anisopliae) reveal that it is rhizosphere competent. Applied and Environmental Microbiology 68, 6383–6387.
Field studies using a recombinant mycoinsecticide (Metarhizium anisopliae) reveal that it is rhizosphere competent.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xptlarurk%3D&md5=3669ab3dbd3e65033512ff7d9aae9aefCAS | 12450863PubMed |

Imfeld G, Vuilleumier S (2012) Measuring the effects of pesticides on bacterial communities in soil: a critical review. European Journal of Soil Biology 49, 22–30.
Measuring the effects of pesticides on bacterial communities in soil: a critical review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjs1Oksro%3D&md5=a4f9de4b26e07921fe530373aa7e13e5CAS |

Ingham E, Trofymow J, Ames R, Hunt H, Morley C, Moore J, Coleman D (1986) Trophic interactions and nitrogen cycling in a semi-arid grassland soil. II. System responses to removal of different groups of soil microbes or fauna. Journal of Applied Ecology 23, 615–630.
Trophic interactions and nitrogen cycling in a semi-arid grassland soil. II. System responses to removal of different groups of soil microbes or fauna.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XlslWhtrw%3D&md5=ae798d1b3dc3abc10f017800929c6312CAS |

Itoh H, Navarro R, Takeshita K, Tago K, Hayatsu M, Hori T, Kikuchi Y (2014) Bacterial population succession and adaptation affected by insecticide application and soil spraying history. Frontiers in Microbiology 5, 457

IUSS Working Group WRB (2015) World Reference Base for Soil Resources 2014, update 2015. International soil classification system for naming soils and creating legends for soil maps. World Soil Resources Reports No. 106, 1-192, FAO, Rome.

Jacobsen CS, Hjelmsø MH (2014) Agricultural soils, pesticides and microbial diversity. Current Opinion in Biotechnology 27, 15–20.
Agricultural soils, pesticides and microbial diversity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXovVKkuro%3D&md5=89534581e1cc6b42f2a7a0956f6cd433CAS | 24863892PubMed |

Korbel KL, Hancock PJ, Serov P, Lim RP, Hose GC (2013) Groundwater ecosystems vary with land use across a mixed agricultural landscape. Journal of Environmental Quality 42, 380–390.

Lo C-C (2010) Effect of pesticides on soil microbial community. Journal of Environmental Science and Health Part B, Pesticides, Food Contaminants, and Agricultural Wastes 45, 348–359.
Effect of pesticides on soil microbial community.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXms1Ojsr0%3D&md5=111efaac5e879f9ffae64d400c1b90a8CAS | 20512724PubMed |

Lorena C, Noé V, Victoria C, Beatriz B, Leticia S, Julia M (2005) Soil nitrogen in relation to quality and decomposability of plant litter in the Patagonian Monte, Argentina. Plant Ecology 181, 139–151.
Soil nitrogen in relation to quality and decomposability of plant litter in the Patagonian Monte, Argentina.Crossref | GoogleScholarGoogle Scholar |

Maute K, French K, Bull CM, Story P, Hose G (2015) Current insecticide treatments used in locust control have less of a short-term impact on Australian arid-zone reptile communities than does temporal variation. Wildlife Research 42, 50–59.
Current insecticide treatments used in locust control have less of a short-term impact on Australian arid-zone reptile communities than does temporal variation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXptFWru7g%3D&md5=fe3b6801f162e2f91f3f226c92003e54CAS |

Maute K, French K, Story P, Bull C, Hose GC (2016) Effects of two locust control methods on wood-eating termites in arid Australia. Journal of Insect Conservation 20, 107–118.
Effects of two locust control methods on wood-eating termites in arid Australia.Crossref | GoogleScholarGoogle Scholar |

Moretto A, Distel R, Didoné N (2001) Decomposition and nutrient dynamic of leaf litter and roots from palatable and unpalatable grasses in a semi-arid grassland. Applied Soil Ecology 18, 31–37.
Decomposition and nutrient dynamic of leaf litter and roots from palatable and unpalatable grasses in a semi-arid grassland.Crossref | GoogleScholarGoogle Scholar |

Noble JC, Müller W, Whitford W, Pfitzner G (2009) The significance of termites as decomposers in contrasting grassland communities of semi-arid eastern Australia. Journal of Arid Environments 73, 113–119.
The significance of termites as decomposers in contrasting grassland communities of semi-arid eastern Australia.Crossref | GoogleScholarGoogle Scholar |

Pascual J, García C, Hernandez T (1999) Lasting microbiological and biochemical effects of the addition of municipal solid waste to an arid soil. Biology and Fertility of Soils 30, 1–6.
Lasting microbiological and biochemical effects of the addition of municipal solid waste to an arid soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXntVCmsbw%3D&md5=ab81907293a01cee6e39c0917e711f3cCAS |

Pucheta E, Llanos M, Meglioli C, Gaviorno M, Ruiz M, Parera C (2006) Litter decomposition in a sandy Monte desert of western Argentina: influences of vegetation patches and summer rainfall. Austral Ecology 31, 808–816.
Litter decomposition in a sandy Monte desert of western Argentina: influences of vegetation patches and summer rainfall.Crossref | GoogleScholarGoogle Scholar |

Rayment GE, Lyons DJ (2011) ‘Soil chemical methods: Australasia.’ (CSIRO Publishing: Melbourne)

Ros M, Goberna M, Moreno J, Hernandez T, Garcia C, Insam H, Pascual JA (2006) Molecular and physiological bacterial diversity of a semi-arid soil contaminated with different levels of formulated atrazine. Applied Soil Ecology 34, 93–102.
Molecular and physiological bacterial diversity of a semi-arid soil contaminated with different levels of formulated atrazine.Crossref | GoogleScholarGoogle Scholar |

Rose MT, Cavagnaro TR, Scanlan CA, Rose TJ, Vancov T, Kimber S, Kennedy IR, Kookana RS, Van Zwieten L (2016) Impact of herbicides on soil biology and function. In ‘Advances in agronomy. Vol. 136’. (Ed. LS Donald) pp. 133–220. (Academic Press: London)

Saetre P, Stark JM (2005) Microbial dynamics and carbon and nitrogen cycling following re-wetting of soils beneath two semi-arid plant species. Oecologia 142, 247–260.
Microbial dynamics and carbon and nitrogen cycling following re-wetting of soils beneath two semi-arid plant species.Crossref | GoogleScholarGoogle Scholar | 15490245PubMed |

Santos PF, Whitford WG (1981) The effects of microarthropods on litter decomposition in a Chihuahuan desert ecosystem. Ecology 62, 654–663.
The effects of microarthropods on litter decomposition in a Chihuahuan desert ecosystem.Crossref | GoogleScholarGoogle Scholar |

Scheepmaker JW, van de Kassteele J (2011) Effects of chemical control agents and microbial biocontrol agents on numbers of non-target microbial soil organisms: a meta-analysis. Biocontrol Science and Technology 21, 1225–1242.
Effects of chemical control agents and microbial biocontrol agents on numbers of non-target microbial soil organisms: a meta-analysis.Crossref | GoogleScholarGoogle Scholar |

Schneider T, Gerrits B, Gassmann R, Schmid E, Gessner MO, Richter A, Battin T, Eberl L, Riedel K (2010) Proteome analysis of fungal and bacterial involvement in leaf litter decomposition. Proteomics 10, 1819–1830.
Proteome analysis of fungal and bacterial involvement in leaf litter decomposition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlsVOrtLo%3D&md5=de0552d0363e6ac0e694cd14602b27afCAS | 20198641PubMed |

Schuurman G (2005) Decomposition rates and termite assemblage composition in semiarid Africa. Ecology 86, 1236–1249.
Decomposition rates and termite assemblage composition in semiarid Africa.Crossref | GoogleScholarGoogle Scholar |

Shunthirasingham C, Mmereki B, Masamba W, Oyiliagu C, Lei Y, Wania F (2010) Fate of pesticides in the arid subtropics, Botswana, Southern Africa. Environmental Science & Technology 44, 8082–8088.
Fate of pesticides in the arid subtropics, Botswana, Southern Africa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1OnurnP&md5=99417ef2848e28b6b87ea05c178a4277CAS |

Tiessen H, Cuevas E, Chacon P (1994) The role of soil organic matter in sustaining soil fertility. Nature 371, 783–785.
The role of soil organic matter in sustaining soil fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmvF2qtrw%3D&md5=0b4af9b11948ddf05b516ac7006180d9CAS |

Van Der Heijden MGA, Bardgett RD, Van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology Letters 11, 296–310.
The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems.Crossref | GoogleScholarGoogle Scholar |

Wall DH, Bradford MA, St. John MG, Trofymow JA, Behan-Pelletier V, Bignell DE, Dangerfield JM, Parton WJ, Rusek J, Voigt W, Wolters V, Gardel HZ, Ayuke FO, Bashford R, Beljakova OI, Bohlen PJ, Brauman A, Flemming S, Henschel JR, Johnson DL, Jones TH, Kovarova M, Kranabetter JM, Kutny LES, Lin KC, Maryati M, Masse D, Pokarzhevskii A, Rahman H, SabarÁ MG, Salamon JA, Swift MJ, Varela A, Vasconcelos HL, White D, Zou X (2008) Global decomposition experiment shows soil animal impacts on decomposition are climate-dependent. Global Change Biology 14, 2661–2677.

West NE (Ed.) (1991) Nutrient cycling in soils of semiarid and arid regions. In ‘Semiarid lands and deserts: soil resource and reclamation’. pp. 295–332. (CRC Press: London)

Yuste JC, Peñuelas J, Estiarte M, Garcia-Mas J, Mattana S, Ogaya R, Pujol M, Sardans J (2011) Drought-resistant fungi control soil organic matter decomposition and its response to temperature. Global Change Biology 17, 1475–1486.
Drought-resistant fungi control soil organic matter decomposition and its response to temperature.Crossref | GoogleScholarGoogle Scholar |

Zaady E, Groffman P, Shachak M (1998) Nitrogen fixation in macro- and microphytic patches in the Negev desert. Soil Biology & Biochemistry 30, 449–454.
Nitrogen fixation in macro- and microphytic patches in the Negev desert.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjtFeit7k%3D&md5=a3dcba12b22cfdae4d86d5791baf0b5eCAS |

Zhu G, Wu H, Guo J, Kimaro FM (2004) Microbial degradation of fipronil in clay loam soil. Water, Air, and Soil Pollution 153, 35–44.
Microbial degradation of fipronil in clay loam soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXitFWqsrY%3D&md5=a036e1ec6ac4c1ad60ae55f288d4de35CAS |

Zimmermann G (2007) Review on safety of the entomopathogenic fungus Metarhizium anisopliae. Biocontrol Science and Technology 17, 879–920.
Review on safety of the entomopathogenic fungus Metarhizium anisopliae.Crossref | GoogleScholarGoogle Scholar |