Response of microbial organisms (aquatic and terrestrial) to pesticides
Accepted: 14 November 2012
The present document has been produced and adopted by the bodies identified above as author(s). This task has been carried out exclusively by the author(s) in the context of a contract between the European Food Safety Authority and the author(s), awarded following a tender procedure. The present document is published complying with the transparency principle to which the Authority is subject. It may not be considered as an output adopted by the Authority. The European food Safety Authority reserves its rights, view and position as regards the issues addressed and the conclusions reached in the present document, without prejudice to the rights of the authors.
A systematic literature search was carried out in order to assess the response of microbial organisms to pesticides in aquatic and terrestrial environments. The major literature databases have been interrogated, and after a refinement of keywords, thousands of records were retrieved and manually screened for relevance, quality, publication date, language and suitability for quantitative meta-analyses. 234 records for the terrestrial lot and 42 records for the aquatic lot were retained after screening and analysed for the extraction of several relevant information regarding the type of study, the pesticide application dose, the microbial parameters measured. From each record, a number of case studies were extracted, a case study being represented by the measurement of a single product, at a specific dose on a specific microbiological endpoint. A high number of case studies (3405 for terrestrial and 458 for aquatic) were obtained, stored and analysed through an Access database query system. With such a query system, it was possible to show on a detailed semi-quantitative way that pesticides affect microbes in a number of ways, with significant reductions in microbiological endpoints of biomass and activity detected in less than half of the cases considered. Furthermore, a number of temporary effects were identified, with microbial endpoints being firstly affected and then restored to the original conditions. This report confirms on one hand the complexity of microbial parameters in terrestrial and aquatic environments, on the other the importance of considering carefully microbial features in the risk assessment of pesticides. In this context, the adoption of a macro-categorization of microbial responses (biomass, activity and structure) can be useful for handling complex data and to identify patterns that can be potentially used for the goal of protecting microorganisms from potential adverse effects of pesticides. Carrying out risk assessment for non-target microbes on single molecules, as usually done for the risk assessment of pesticides, will be very important in order to identify which ones are eventually causing more detrimental effects. The literature survey also indicated that the pesticide applied dose strongly affect the outcomes, with less impacts when the pesticides are being applied at recommended field doses: it is thus recommended to further promote policies for use of pesticides according to good agricultural practices, since this can reduce side-effects on non-target soil microorganisms.
Project developed on the procurement project CT/EFSA/PRAS/2011/04
The present work has been carried out in order to analyse the relevant peer-reviewed scientific literature on the effects of pesticides on non-target microbes and to provide conclusions and recommendations that can be useful for a risk assessment of pesticides on non-target soil microbes. In a first search strategy, more than 50 000 bibliographic records were retrieved, most of them not related to the topic of interest. A key-words refinement was thus agreed, ending up in 8904 records for the terrestrial lot and 5302 for the aquatic. All these records were manually screened for duplicates, relevance, publication date, full record availability, quality criteria and suitability for the extraction of quantitative info, ending up in 234 full records for the terrestrial and 42 for the aquatic lot. The info contained in each of these records was extracted and organized in a number of case studies, each case study being represented by the measurement of a certain pesticide in a specific environment, at a specific dose on a specific microbiological endpoint. The latter were organized in three major classes: biomass (measurements of the size of total microbial populations or of specific groups of microbes), activity (measurements of functions performed by microbes) and structure (measurements of the structural organization of microbial communities). Per each of these endpoints, a semi-quantitative scale of responses was applied, in order to allow comparisons between different methods. Specifically, 6 levels were applied to biomass or activity measurements, namely complete inhibition, more than doubled decrease, significant decrease, significant decrease followed by no differences, no significant differences, significant increase followed by no difference, more than doubled increase. For structure end-points, 3 levels were instead applied: no significant changes, significant changes, and transient significant changes. As a result of this approach, the information contained in the selected records was exploded in 3405 case studies for the terrestrial lot and 458 for the aquatic. An Access database system was then developed to manage, store and interrogate the case studies info, with a query system allowing a summary of the outcomes at different level of details (i.e., effect of a class of pesticides on general end-points, effect of a class of pesticides on specific end-points, effect of a specific pesticide on general end-points, effects of a specific pesticide on specific-endpoints).
By the application of this queries system, it was found that pesticides are affecting in a number of cases terrestrial and aquatic microbial communities. In terrestrial environments, significant decreases of microbial activities are found in 35% of case studies for herbicides, 32% for fungicides and 25% for insecticides. Quite high are also the cases where no significant differences are found: 45% for insecticides and fungicides, 40% for herbicides. The rest of case studies relate to significant increases, which are also important outcomes: pesticides can indeed have also a positive effect on soil microbes, since they can stimulate the levels of some microbial activities. A similar trend was found for biomass: in 55 % of cases for herbicides, 38% for insecticides and 25% for fungicides, no effects are found. Significant decreases are dominating for fungicides (45%), while for the other two classes negative effects are more limited: 27% herbicides and 15% insecticides. Analyses at structure level indicate that in most cases pesticides are inducing changes in the structure of terrestrial microbial communities: no significant changes were found in a minority of cases, namely 5% for insecticides and fungicides, 13% for herbicides. In a quite limited number of cases (11% for herbicide, 7% for fungicides) these effects were transient, i.e., at the end of the experiment the microbial communities returned to a structure similar to the one they had before the pesticides application. Interestingly, no transient structure changes are reported for insecticides.
These analyses were also repeated by considering the applied doses of fungicides, and taking into account separately the cases were pesticides were applied at recommended field doses or multiples of it (10X and 100X). Outcomes of this assessment showed that, in general, significant effects are increasing with the dose applied. A correct use of pesticides according to good agricultural practices should thus reduce (albeit not eliminate) the risks related to soil microbes, and policies in this direction will be useful also for the protection of soil microbes.
As requested by the Contract, a detailed analysis of the effects of fungicides was carried out analysing in detail the 8 bibliographic records dealing with the topic, with a few active compounds covered (captan, chlorothalonil, triclosan, metalaxyl, endosulfan, carbeindazim, fluazinam, imazalil, epoxiconazole, tebuconazole and azoxystrobin). Apart from a few exceptions (e.g., captan never showing significant effects), in most cases biomass, activity and structure measurements were affected by fungicides. Results are however not always predictable: the effects induced have been stimulating or inhibiting depending on the species and the endpoint considered, with different results obtained with the same end-point measured in different species.
On the basis of these outcomes, the recommendation is to improve the inclusion of microorganisms in the risk assessment of pesticides by taking into account measures of biomass, activity and structure of microbes. The fact that the risk assessment is done for each compound separately is very useful for non-target soil microbes: as outlined in this report, responses are very variable from one compound to the other: it will be thus important to identify eventual limitations for specific compounds that are causing more detrimental effects. For performing properly and easily such studies, standardized methods should be tested and promoted, and applied for risk assessment purposes, for example during registration purposes. Another recommendation is to take into account for risk assessment the recovery of microbial functions, as for example it is already done for chemical persistence in the REACH Legislation. Finally, a careful use of pesticides according to good agricultural practices must be promoted in order to reduce the negative effects on soil microbes. As outlined here, the literature clearly indicates that pesticides effects on microbes are dose-dependent, with more significant effects detected at doses higher than the recommended ones.