Skip to main content
SpringerLink
Log in

Placing arbuscular mycorrhizal fungi on the risk assessment test battery of plant protection products (PPPs)

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Arbuscular mycorrhizal fungi (AMF) are mutualistic symbionts considered a key group in soil systems involved in the provision of several ecosystem services. Recently they have been listed by EFSA as organisms to be included in the test battery for the risk assessment of plant protection product (PPPs). This study aimed to contribute to improve the ISO Protocol (ISO 10832: 2009) by assessing the feasibility of using other AMF species under different test conditions. Overall, results showed that AMF species Gigaspora albida and Rhizophagus clarus (selected out of five AMF species) are suitable to be used in spore germination tests using the ISO protocol (14 days incubation with sand or artificial soil as substrate) to test PPPs. However, several modifications to the protocol were made in order to accommodate the use of the tested isolates, namely the incubation temperature (28 °C instead of 24 °C) and the change of reference substance (boric acid instead of cadmium nitrate). The need for these changes, plus the results obtained with the three fungicides tested (chlorothalonil, mancozeb and metalaxyl-M) and comparisons made with literature on the relevance of the origin of AMF isolates in dictating the adequate test conditions, emphasize the importance of adjusting test conditions (AMF species/isolates and test temperature) when assessing effects for prospective risk assessment targeting different climatic zones. So, further studies should be conducted with different AMF species and isolates from different climatic regions, in order to better define which species/isolate and test conditions should be used to assess effects of a particular PPP targeting a given climatic zone.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alvares CA, Stape JL, Sentelhas PC, de Moraes Gonçalves JL, Sparovek G (2013) Köppen’s climate classification map for Brazil. Meteorol Z 22:711–728. https://doi.org/10.1127/0941-2948/2013/0507

    Article  Google Scholar 

  • Alves PRL, Natal-da-Luz T, Sousa JP, Cardoso EJBN (2015) Ecotoxicological characterization of sugarcane vinasses when applied to tropical soils. Sci Total Environ 526:222–232. https://doi.org/10.1016/j.scitotenv.2015.03.150

    Article  CAS  Google Scholar 

  • Amorim MJB, Natal-da-Luz T, Sousa JP, Loureiro S, Becker L, Römbke J, Soares AMVM (2012) Boric acid as reference substance: pros, cons and standardization. Ecotoxicol 21:919–924. https://doi.org/10.1007/s10646-011-0832-9

    Article  CAS  Google Scholar 

  • Antunes PM, Koch AM, Morton JB, Rillig MC, Klironomos JN (2011) Evidence for functional divergence in arbuscular mycorrhizal fungi from contrasting climatic origins. New Phytol 189:507–514. https://doi.org/10.1111/j.1469-8137.2010.03480.x

    Article  Google Scholar 

  • Antunes PM, Koyama A (2017) Mycorrhizas as nutrient and energy pumps of soil food webs: multitrophic interactions and feedbacks. In: Johnson NC, Gehring C, Jansa J (eds) Mycorrhizal mediation of soil. Elsevier Inc, Amsterdam, pp 149–173. 10.1016/B978-0-12-804312-7.00009-7

    Chapter  Google Scholar 

  • Azcón-Aguilar C, Barea JM (1997) Arbuscular mycorrhizas and biological control of soil-borne plant pathogens – an overview of the mechanisms involved. Mycorrhiza 6:457–464. https://doi.org/10.1007/s005720050147

    Article  Google Scholar 

  • Basu S, Rabara RC, Negi S (2018) AMF: The future prospect for sustainable agriculture. Physiol Mol Plant Pathol 102:36–45. https://doi.org/10.1016/j.pmpp.2017.11.007

    Article  Google Scholar 

  • Buysens C, Dupré De Boulois H, Declerck S (2015) Do fungicides used to control Rhizoctonia solani impact the non-target arbuscular mycorrhizal fungus Rhizophagus irregularis? Mycorrhiza 25:277–288. https://doi.org/10.1007/s00572-014-0610-7

    Article  CAS  Google Scholar 

  • Carballar-Hernández S, Hernández-Cuevas LV, Montaño NM, Larsen J, Ferrera-Cerrato R, Taboada-Gaytán OR, Montiel-González AM, Alarcón A (2017) Native communities of arbuscular mycorrhizal fungi associated with Capsicum annuum L. respond to soil properties and agronomic management under field conditions. Agric Ecosyst Environ 245:43–51. https://doi.org/10.1016/j.agee.2017.05.004

    Article  Google Scholar 

  • Cavagnaro TR, Bender SF, Asghari HR, van der Heijden MGA (2015) The role of arbuscular mycorrhizas in reducing soil nutrient loss. Trends Plant Sci 20:283–290. https://doi.org/10.1016/j.tplants.2015.03.004

    Article  CAS  Google Scholar 

  • Clark R (1997) Arbuscular mycorrhizal adaptation, spore germination, root colonization, and host plant growth and mineral acquisition at low pH. Plant Soil 192:15–22. https://doi.org/10.1023/A:1004218915413

    Article  CAS  Google Scholar 

  • Demenois J, Carriconde F, Bonaventure P, Maeght JL, Stokes A, Rey F (2018) Impact of plant root functional traits and associated mycorrhizas on the aggregate stability of a tropical Ferralsol. Geoderma 312:6–16. https://doi.org/10.1016/j.geoderma.2017.09.033

    Article  Google Scholar 

  • Druille M, Omacini M, Golluscio RA, Cabello MN (2013) Arbuscular mycorrhizal fungi are directly and indirectly affected by glyphosate. Appl Soil Ecol 72:143–149. https://doi.org/10.1016/j.apsoil.2013.06.011

    Article  Google Scholar 

  • EC - Environment Canada (2005) Guidance document on statistical methods for environmental toxicity tests, Method development and applications section. Report EPS 1/RM/46. In: Environmental Protection Series. Environment Canada. Environmental Technology Centre, Ottawa, ON.

  • EFSA PPR Panel (EFSA Panel on Plant Protection Products and their Residues), Ockleford C, Adriaanse P, Berny P, Brock T, Duquesne S, Grilli S, Hernandez-Jerez AF, Bennekou SH, Klein M, Kuhl T, Laskowski R, Machera K, Pelkonen O, Pieper S, Stemmer M, Sundh I, Teodorovic I, Tiktak A, Topping CJ, Wolterink G, Craig P, de Jong F, Manachini B, Sousa JP, Swarowsky K, Auteri D, Arena M, Rob S (2017) Scientific Opinion addressing the state of the science on risk assessment of plant protection products for in-soil organisms. EFSA J. https://doi.org/10.2903/j.efsa.2017.4690

  • Fernandez CW, Kennedy PG (2015) Moving beyond the black-box: fungal traits, community structure, and carbon sequestration in forest soils. New Phytol 205:1378–1380. https://doi.org/10.1111/nph.13289

    Article  CAS  Google Scholar 

  • Garcia MVB (2004) Effects of pesticides on soil fauna: development of ecotoxicological test methods for tropical regions. Thesis, University of Bonn.

  • Gerdemann JY, Nicolson TH (1963) Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Trans Brit Mycol Soc 46:235–244. https://doi.org/10.1016/S0007-1536(63)80079-0

    Article  Google Scholar 

  • Giovannetti M, Avio L, Sbrana C (2010) Fungal spore germination and pre-symbiotic mycelial growth – physiological and genetic aspects. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function. Springer, Dordrecht, pp 3–32. 10.1007/978-90-481-9489-6_1

    Chapter  Google Scholar 

  • Giovannetti M, Turrini A, Strani P, Sbrana C, Avio L, Pietrangeli B (2006) Mycorrhizal fungi in ecotoxicological studies: Soil impact of fungicides, insecticides and herbicides. Preven Today 2:47–62

    Google Scholar 

  • González-Cortés JC, Vega-Fraga M, Varela-Fregoso L, Martínez-Trujillo M, Carreón-Abud Y, Gavito ME (2012) Arbuscular mycorrhizal fungal (AMF) communities and land use change: the conversion of temperate forests to avocado plantations and maize fields in central Mexico. Fungal Ecol 5:16–23. https://doi.org/10.1016/j.funeco.2011.09.002

    Article  Google Scholar 

  • Harrier L, Watson C (2004) The potential role of arbuscular mycorrhizal (AM) fungi in the bioprotection of plants against soil-borne pathogens in organic and/or other sustainable farming systems. Pest Manag Sci 60:149–157. https://doi.org/10.1002/ps.820

    Article  CAS  Google Scholar 

  • Ipsilantis I, Samourelis C, Karpouzas DG (2012) The impact of biological pesticides on arbuscular mycorrhizal fungi. Soil Biol Biochem 45:147–155. https://doi.org/10.1016/j.soilbio.2011.08.007

    Article  CAS  Google Scholar 

  • ISO (International Organization for Standardization)) (2009) Soil quality – effects of pollutants on mycorrhizal fungi – spore germination test. ISO 10832:2009, Genève, Switzerland

    Google Scholar 

  • Jansa J, Treseder KK (2016) Mycorrhizas and the carbon cycle. In: Johnson NC, Gehring C, Jansa J (eds) Mycorrhizal mediation of soil. Elsevier Inc, Amsterdam, pp 343–355. 10.1016/B978-0-12-804312-7.00019-X

    Google Scholar 

  • Karpouzas DG, Papadopoulou E, Ipsilantis I, Friedel I, Petric I, Udikovic-Kolic N, Djuric S, Kandeler C, Menkissoglu-Spiroudi U, Martin-Laurent F (2014) Effects of nicosulfuron on the abundance and diversity of arbuscular mycorrhizal fungi used as indicators of pesticide soil microbial toxicity. Ecol Indic 39:44–53. https://doi.org/10.1016/j.ecolind.2013.12.004

    Article  CAS  Google Scholar 

  • Kivlin SN, Emery SM, Rudgers JA (2013) Fungal symbionts alter plant responses to global change. Am J Bot 100:1445–1457. https://doi.org/10.3732/ajb.1200558

    Article  Google Scholar 

  • Leal PL, Siqueira JO, Stürmer SL (2013) Switch of tropical Amazon forest to pasture affects taxonomic composition but not species abundance and diversity of arbuscular mycorrhizal fungal community. Appl Soil Ecol 71:72–80. https://doi.org/10.1016/j.apsoil.2013.05.010

    Article  Google Scholar 

  • Niemeyer JC, Chelinho S, Sousa JP (2017) Soil ecotoxicology in Latin America: current research and perspectives. Environ Toxicol Chem 36:1795–1810. https://doi.org/10.1002/etc.3792

    Article  CAS  Google Scholar 

  • Niemeyer JC, Carniel LSC, Santo FB, Silva M, Klauberg-Filho O (2018) Boric acid as reference substance for ecotoxicity tests in tropical artificial soil. Ecotoxicology 27(4):395–401. https://doi.org/10.1007/s10646-018-1915-7. Epub 2018 Feb 28

    Article  CAS  Google Scholar 

  • Novais CB, Borges WL, Jesus EC, Saggin-Júnior OJ, Siqueira JO (2014) Inter- and intraspecific functional variability of tropical arbuscular mycorrhizal fungi isolates colonizing corn plants. Appl Soil Ecol 76:78–86. https://doi.org/10.1016/j.apsoil.2013.12.010

    Article  Google Scholar 

  • OECD (Organization for Economic Cooperation and Development) (1984) Earthworm acute toxicity test. OECD Guideline for Testing of Chemicals No. 207, Paris, France

    Google Scholar 

  • OECD (Organization for Economic Cooperation and Development) (2016) Predatory mite (Hypoaspis (Geolaelaps) aculeifer) Reproduction test in soil. OECD guideline for the testing of chemicals No. 226, Paris, France

    Google Scholar 

  • Princz J, Becker L, Scheffczyk A, Stephenson G, Scroggins R, Moser T, Römbke J (2017) Ecotoxicity of boric acid in standard laboratory tests with plants and soil organisms. Ecotoxicol 26:471–481. https://doi.org/10.1007/s10646-017-1789-0

    Article  CAS  Google Scholar 

  • Rahman SFSA, Singh E, Pieterse CMJ, Schenk PM (2018) Emerging microbial biocontrol strategies for plant pathogens. Plant Sci. https://doi.org/10.1016/j.plantsci.2017.11.012

  • Rillig MC, Aguilar-Trigueros CA, Bergmann J, Verbruggen E, Veresoglou SD, Lehmann A (2015) Plant root and mycorrhizal fungal traits for understanding soil aggregation. New Phytol 205:1385–1388. https://doi.org/10.1111/nph.13045

    Article  CAS  Google Scholar 

  • Rivera-Becerril F, van Tuinen D, Chatagnier O, Rouard N, Béguet J, Kuszala C, Soulas G, Gianinazzi-Pearson V, Martin-Laurent F (2017) Impact of a pesticide cocktail (fenhexamid, folpel, deltamethrin) on the abundance of Glomeromycota in two agricultural soils. Sci Total Environ 577:84–93. https://doi.org/10.1016/j.scitotenv.2016.10.098

    Article  CAS  Google Scholar 

  • Rohyadi A (2005) Spore germination and colonization of Gigaspora margarita as influenced by aluminium concentration. J Microb Indones 10:71–74

    Google Scholar 

  • Singh S, Tripathi DK, Singh S, Sharma S, Dubey NK, Chauhana DK, Vaculíke M (2017) Toxicity of aluminium on various levels of plant cells and organism: a review. Environ Exp Bot 74:1883–1889. https://doi.org/10.1016/j.envexpbot.2017.01.005

    Article  CAS  Google Scholar 

  • Siqueira JO, Mahmud AW, Hubbell DH (1986) Differential behavior of Vesicular-Arbuscular Mycorrhizal fungi in relation to soil acidity. R Bras Cien Solo 10:11–16

    CAS  Google Scholar 

  • Souza FA, Sturmer SL, Carrenho R, Trufem SF (2010) Classificação e taxonomia de fungos micorrízicos arbusculares, sua diversidade e ocorrência no Brasil. In: Siqueira JO, Souza FA, Cardoso EJBN, Tsai SM (eds) Micorrizas: 30 anos de pesquisa no Brasil. UFLA, Lavras, Brazil, pp 15–73

    Google Scholar 

  • StatSoft, Inc (2011) STATISTICA (Data analysis software system), version 10. Tulsa, USA. Available from: http://www.statsoft.com.

  • Stutz JC, Morton JB (1996) Successive pot cultures reveal high species richness of arbuscular endomycorrhizal fungi in arid ecosystems. Can J Bot 74:1883–1889. https://doi.org/10.1139/b96-225

    Article  Google Scholar 

  • Turrini A, Bedini A, Bonilla Loor M, Santini G, Sbrana C, Giovannetti M, Avio L (2018) Local diversity of native arbuscular mycorrhizal symbionts differentially affects growth and nutrition of three crop plant species. Biol Fertil Soils 54:203–217. https://doi.org/10.1007/s00374-017-1254-5

    Article  Google Scholar 

  • van der Heijden MG, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310. https://doi.org/10.1111/j.1461-0248.2007.01139.x

    Article  Google Scholar 

  • van der Heijden MG, Martin FM, Selosse M, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the presente, and the future. New Phytol 205:1406–1423. https://doi.org/10.1111/nph.13288

    Article  CAS  Google Scholar 

  • Veresoglou SD, Chen B, Rillig M (2012) Arbuscular mycorrhiza and soil nitrogen cycling. Soil Biol Biochem 46:53–62. https://doi.org/10.1016/j.soilbio.2011.11.018

    Article  CAS  Google Scholar 

  • Vimal SR, Singh JS, Arora NK, Singh S (2017) Soil-plant-microbe interactions in stressed agriculture management: A Review. Pedosphere 27:177–192. https://doi.org/10.1016/S1002-0160(17)60309-6

    Article  Google Scholar 

  • Vos C, Schouteden N, van Tuinen D, Chatagnier O, Elsen A, De Waele D, Panis B, Gianinazzi-Pearson V (2013) Mycorrhiza-induced resistance against the rooteknot nematode Meloidogyne incognita involves priming of defense gene responses in tomato. Soil Biol Biochem 60:45–54. https://doi.org/10.1016/j.soilbio.2013.01.013

    Article  CAS  Google Scholar 

Download references

Funding

Gilvani Carla Mallmann was funded by a Promop/UDESC D.D Grant. José Paulo Sousa was funded by a “Fundação CAPES” Visitors Research Grant under the project no. 079/2012 of “Ciência sem Fronteiras—CAPES” programme.

Author information

Authors and Affiliations

  1. Soil Science Department, Universidade do Estado de Santa Catarina, CAV, Lages, Brazil

    Gilvani Carla Mallmann & Osmar Klauberg-Filho

  2. Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, Coimbra, Portugal

    José Paulo Sousa

  3. Swedish University of Agricultural Sciences, Uppsala, Sweden

    Ingvar Sundh

  4. Federal Environment Agency, UBA, Dessau-Roßlau, Germany

    Silvia Pieper

  5. Food Safety Authority (EFSA), Parma, Italy

    Maria Arena

  6. Universidade Federal de Santa Catarina, UFSC Curitibanos, Curitibanos, Brazil

    Sonia Purin da Cruz

Authors
  1. Gilvani Carla Mallmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. José Paulo Sousa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ingvar Sundh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Silvia Pieper
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Maria Arena
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sonia Purin da Cruz
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Osmar Klauberg-Filho
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Osmar Klauberg-Filho.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mallmann, G.C., Sousa, J.P., Sundh, I. et al. Placing arbuscular mycorrhizal fungi on the risk assessment test battery of plant protection products (PPPs). Ecotoxicology 27, 809–818 (2018). https://doi.org/10.1007/s10646-018-1946-0

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-018-1946-0

Keywords

Search

Navigation