The effects of herbicides on soil life
Part 2: Beneficial fungi and bacteria

October 2018

DR MARYKE CRAVEN, CHARNÉ MYBURGH, OWEN RHODE and DR JEANETTA SAAYMAN-DU TOIT, ARC-Grain Crops, Potchefstroom

Weeds are a persistent threat to crop productivity worldwide. In an effort to optimise yield by controlling these unwanted plants, modern agriculture has become heavily dependent on the use of herbicides. Non-target organisms are unfortunately equally exposed to these chemicals which have the potential to, unintentionally, also harm them. 

According to international literature, this may lead to a reduction in biodiversity and the provision of ecosystem services that support food security and on-farm profitability. Glyphosate is the world’s most commonly used herbicide and has been extensively studied for its effect on soil microbial communities than any other herbicide. 

In this second part of our series we will focus on some of the international findings surrounding the effects of glyphosate and other herbicides observed on the beneficial fungal and bacterial communities. Due to the sheer magnitude of research findings available, we will only highlight some of the findings published internationally and the various views surrounding this topic. 

Why are fungi and bacteria important?
The simple answer to this question would be that fungi and bacteria are the decomposers in the biological world. They digest the decaying leaves and rotting bodies of plants and animals, and in so doing return their elements to the soil. Without them, the earth would basically be littered with dead organic material, and all life would cease to exist as plants will not have the required nutrients to grow, which have a knock-on effect on every living thing. 

However, fungi and bacteria degrade plant residues differently and have different roles in the recycling of nutrients, which is partly due to the different habitats they prefer within the soil and the different types of organic matter they consume. Bacteria within the rhizosphere (the region of soil in the vicinity of plant roots) are involved in biogeochemical processes within the soil such as carbon, nitrogen, and phosphorus cycling. 

Fungi and bacteria differ in their responses to changes in agricultural management practices with fungi usually being more sensitive to these changes. The fungal-to-bacterial ratio is therefore a good indicator of environmental changes in the soil. Based on the function of fungi and bacteria in soil, a reduction of their numbers may affect soil respiratory activity, soil enzymes and microbial diversity, as well as rates of carbon and nitrogen turnover. 

Herbicides and its effect on fungi and bacteria in general
As already indicated in Part 1 of our series (SA Graan/Grain September-issue), there is an overwhelming number of contradictory findings concerning the impact of herbicides on fungi and bacteria. The effects of paraquat and glyfosinate on soil bacteria and fungi are either positive or negative effects^{1 - 4}, or no significant effect at all⁵. 

A similar trend is observed with international research findings pertaining to glyphosate, with some studies reporting a negative effect on fungal growth⁶ and reduced colonisation by beneficial bacteria⁷, or negligible or minor effects on microbial community structure when glyphosate was applied at recommended field-rate (stated as 50 mg/kg)^{8 - 12}. 

Other studies state that despite an initial negative effect directly after application, the rhizobacterial community managed to recover by the time the plants reached their final growth stage¹³.

Researchers speculate that the reason for inconsistencies in findings can be anything from microbes reacting differently to different chemicals¹¹, to differences in soil characteristics¹⁴ or to different formulations being used¹⁵, to name but a few. Some studies, however, refute certain aspects of such speculations. A research study, published during 2012¹³ concluded that although the composition of the bacterial communities differed between the soil types included in their study, the effects of the herbicides tested remained very similar with regards to the same bacterial groups. 

Comparative studies have, however, indicated that not all herbicides are equally damaging. An acetochlor and terbuthylazine product evaluated, demonstrated to be in general much more aggressive than the glyphosate-based product tested in various studies^13,16. 

What about herbicides and biocontrol agents?
Several Pseudomonas species have been employed as effective biocontrol agents due to their production of a range of antibiotic compounds, iron-scavenging molecules and plant growth promotors. A recent study found negative consequences of glyphosate on this genus¹⁷ with the effects observed being both species and strain-dependent. 

When P. protegens, a bacteria used as a biocontrol agent for cereal crops, and P. fluorescens, used as a fungus biocontrol for fruit trees, were exposed to varying glyphosate concentrations, no negative effects were observed. In two species of P. putida, used as soil fungus control for maize and other crops, the bacteria had notably stunted growth. 

A study published during 2008 report similar effects regarding the toxic effect of glyphosate and 2,4-D on the water hyacinth biocontrol agent, Alternaria alternata¹⁸. Although neither of the two herbicides actually killed the fungus, both inhibited its growth. Glyphosate though, delayed mycelial growth yet stimulated sporulation while 2,4-D inhibited both growth and sporulation. 

Glyphosate at low concentration did not affect the virulence of A. alternata, while fungi grown on 2,4-D amended plates lost their virulence. Another study¹⁹ discourages the joint application of P. lagenophorae (a biocontrol agent for the annual weed Senecio vulgaris) with 2,4-D, glyphosate and linuron to control S. vulgaris due the detrimental effect that these herbicides have on the bio­control agent. 

Rollan and his research group²⁰ were, however, not able to find any detrimental effect of herbicides such as glyphosate, imazamox or imazethapyr on Trichoderma harzianum and again underlined the critique against herbicide studies which focuses on soil-free media, rather than adding the herbicide directly to soil. 

As herbicide application could potentially have an effect on the efficiency of the biocontrol agents, producers should discuss this matter with the relevant suppliers before applying them. Consideration could be given to different application times for herbicides and biocontrol agents. 

A study of note…
A study by an USA based research group²¹, which published their results during 2014, investigated the effect of long term glyphosate use on the microbial community. The community evaluation included gram positive bacteria, gram negative bacteria, fungi, actinomycetes, arbuscular mycorrhizal fungi and eucaryotes. 

Two soils were compared, one with no-glyphosate use history as opposed to one with a history of more than ten years of glyphosate tolerant cropping practices. Glyphosate treated and untreated residues were respectively also added to these soils and the microbial activity monitored for 30 days.

With this study Ney and his colleagues demonstrated that the initial response of the two soil types differed during plant decomposition, but that the effect diminished over time. The residue type used, in addition, did not have an effect on the end result.

They concluded that the microbial community had adjusted over time to such an extent that the soil with a glyphosate history had a community primed for glyphosate residues, whereas the non-glyphosate soil was starting to change, or adjust in response to the decomposition of glyphosate residues. Their data suggested that the microbial communities in the soil with a history of long-term glyphosate exposure had adapted to glyphosate tolerant residues and thus would show fewer microbial responses during decomposition than that of a soil with no glyphosate use history. 

Their study also answered the question whether plant residues from a glyphosate tolerant cultivar would impact on soil health, in that they concluded that it is the exposure to glyphosate and not the genetically tolerant plant material itself that causes microbial responses.

Food for thought
It is internationally accepted that the behaviour of pesticides in soil will depend on a number of factors. The chemical and physical properties of the pesticide itself as well as environmental factors such as temperature, precipitation, wind, sunlight, soil properties such as moisture, organic matter, pH, available nutrients, interactions between solid, liquid and gaseous phases of the soil are all part and parcel to establishing the persistence, availability and toxicity of pesticides²². 

Based on their review of international research findings, two authors (Lock and Zablotowicz)²³ which contributed to the book titled Managing soil quality: Challenges in modern agriculture, concluded that microbial and faunal populations generally demonstrated tolerance of pesticides, with only minor short lived disturbances being exhibited when recommended rates are used, whilst major biotic processes such as enzyme activity, respiration and carbon and nitrogen transformations are generally minimally impacted. 

There is, however, the other side of the coin that links in with the Ney research group findings²¹, and which must be considered. In a recent study published in February 2018, an Australian-based research group²⁴ which focused on the effects of glyphosate, glyphosinate, paraquat and paraquat-diquat on soil microbial and bacterial diversity, were unable to provide evidence of any negative effect on the various parameters measured due to a once-off application by the various herbicides. 

They concluded that the lack of observed reaction of microbial communities might, amongst others, be due to the fact that years of herbicide application on the soils used in the study might have resulted in only herbicide tolerant populations of microbes being present in the soil.

Population shifts, on the basis of survival of the fittest, might have accordingly already occurred in our soils over the past couple of decades as a result of extensive usage of various herbicides.

A USA research group²⁵ similarly concluded that shifts in subpopulations of particularly the Xanthamonadales and Acidobacteria bacterial groups are possible under long-term glyphosate tolerant cropping. Their study suggested that bacteria from the family Xanthomonadacea are better adapted to and/or enriched by environments containing glyphosate.

On the other hand, Acidobacteria which is highly involved in biogeochemical processes, such as cellulose degradation (process involved with breaking down of cell walls of plant material), decreased in response to glyphosate application. 

Decreases in the abundance of these bacteria over the long-term could impair the ability of soil to perform certain biogeochemical reactions performed by these organisms. 

Interestingly they found the reduction effect to be more dramatic in maize as opposed to what was observed in soybean, suggesting that any subsequent effects on biogeochemical processes due to this bacterial group would be more pronounced in maize. The authors concluded by stating that it is still unknown whether this shift affects functional capacity of the soil under glyphosate tolerant cropping systems²⁵. 

The question we should be asking is whether we are accordingly still seeing or measuring today what was present before we became so reliant on not only herbicides but pesticides in general, or are we actually looking at adapted communities, that continue to evolve based on what we expose them to? 

If the latter is the case, how efficient are these newly adapted communities compared to their ‘predecessors’, and does that have any effect at all on our current agricultural outputs?

In Part 3 of this series, focus will be placed on research findings published on the impact of glyphosate and other herbicides on pathogenic fungi.

Readers are welcome to contact the authors at ARC-Grain Crops with any enquires they might have at 018 299 6100.

References 

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Publication: October 2018

Section: On farm level