Feed-feces-fertilizer: Greenhouse study and interviews with fertilizer producers indicate persistence and negative effect of glyphosate residue in manure-based fertilizers

doi:10.21203/rs.3.rs-4347203/v1

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Research Article

Feed-feces-fertilizer: Greenhouse study and interviews with fertilizer producers indicate persistence and negative effect of glyphosate residue in manure-based fertilizers

https://doi.org/10.21203/rs.3.rs-4347203/v1

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published 19 Aug, 2024

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BACKGROUND: The herbicide glyphosate is the most widely used active ingredient in pesticides globally. Residues have been found in people, livestock, food and animal feed, and in the environment, but little is known about glyphosate residue in manure-based fertilizer. “Feed-feces-fertilizer” describes how manure fertilizer can be contaminated with glyphosate. This exposure can harm sensitive plants, such as tomato, and pose a risk to effective waste disposal and nutrient cycling along principles of the circular economy. We review the use and history and present a mixed methods research based on a real-world case from Finland where glyphosate residue in poultry manure fertilizer was suspected of inhibiting commercial organic tomato production. To test the fertilizer, we grew 72 ‘Encore’ variety tomatoes for 14 weeks using the same commercial greenhouse methods. To ascertain awareness and potential contamination mitigation measures, we also contacted five fertilizer companies with sales of biogenic fertilizer in Finland, representatives of two farming organizations, and two government organizations working on nutrient cycling and agricultural circular economy.

RESULTS: The total harvest of tomatoes grown with fertilizer with glyphosate residue was 35% smaller and the yield of first-class tomatoes 37% lower than that of the control. Two of the five fertilizer companies identified poultry manure as a source of glyphosate contamination. Companies with awareness of pesticide residues reported interest in establishing parameters for pesticide residues.

CONCLUSIONS: The extent of glyphosate contamination of recycled fertilizers is unknown, but this study shows that such contamination occurs with negative impacts on crop production. The example from Finland shows that a model of co-production between fertilizer producers and state regulatory agencies to establish safe limits can benefit both fertilizer producers and their customers.

glyphosate-based herbicide

agrochemical pollution

horticulture

sustainable agriculture

circular economy

organic fertilizer

tomato

greenhouse experiment

poultry manure

Persistence of agrichemicals are challenge to livelihoods, health, and the environment. Glyphosate is the most widely used active ingredient in pesticides in the world (Vicini et al., 2019; Székács and Darvas 2018; Benbrook, 2016), and glyphosate residues have been found in a wide range of foodstuffs, in humans and livestock and in the environment (Hyland et al., 2023; Zioga et al., 2022; Winters et al., 2023; Sørensen et al., 2021; Gillezeau et al., 2019; Helander et al., 2019; Benbrook, 2016; Wang et al., 2016). Little is known about glyphosate residues in fertilizers, but research and extension agencies report experience from the field that herbicide residues in organo-fertilizers and mulches harm crop production (Finnish Food Authority, 2023; McKinnon et al., 2021; Fløistad, 2020). Tomato is one of a variety of crops known to be particularly sensitive to herbicides (Warmund et al., 2022; Cederlund, 2017; Lovelace et al., 2009; Fagliari et al., 2005), and glyphosate-based herbicides are labeled to indicate that the products should not be used on or near tomatoes (Goldy, 2016). Such labelling, however, is ineffective for horticultural producers if the route of exposure is fertilizer.

Nutrient recycling is central to the agricultural circular economy, and contamination of raw materials recycled as fertiliser can limit how and where the fertilizer can be used. Failure to recycle manure and other agricultural waste results in both loss of nutrients to agriculture and increased nutrient pollution in the environment. Contamination of biological fertilizers is of particular importance for organic producers, as mineral nitrogen fertilizer is proscribed (EU 2018/848).

The objectives of this study were to 1) examine the effect of a glyphosate-contaminated poultry manure fertilizer on tomato production and 2) understand the current operating environment including industry experience and response to potential glyphosate contamination of fertilizer raw materials. For the former, we conducted an empirical study to assess the effect of glyphosate residue in manure fertilizer on the growth and total production of greenhouse tomatoes. In the latter, we contacted fertilizer companies and select experts in Finland about potential glyphosate residues in side-stream materials – particularly poultry manure– used in the production of fertilizer suitable for use in organic horticulture and agriculture.

Glyphosate use is complex and contentious. To adequately frame the issue, we first present glyphosate as an herbicide, how it became so ubiquitous, and the status of its regulation in Europe and the United States. Second, we describe the issue of glyphosate residue as a contaminant in fertilizers of biogenic origin (hereafter referred to as organic fertilizers or manure). Third, we present the study system and the real-world case – poultry manure contamination – from which this research is based. The empirical and qualitative studies are then described sequentially in their own sub-sections in Materials and Methods and then Results. The strands of inquiry are brought together in Discussion, and future needs and directions are elaborated in Conclusion.

1.1 Glyphosate: A controversial ‘miracle’ herbicide

Glyphosate is a systemic, broad-spectrum herbicide used both within and outside agriculture (Helander et al., 2012; Székács and Darvas, 2018). Considered a 'once in a century herbicide’ (Duke and Powles, 2008), glyphosate was patented as an herbicide in 1971 and released into the pesticide market in 1974 under the trade name “Roundup®” (Mesnage and Antoniou, 2018). Surge in use of glyphosate-based herbicides is linked to: 1) availability of generic glyphosate-based products following the expiration of the original patent in 1991 and 2) genetically modified glyphosate tolerant crops, such as soybean and maize, which became commercially available in the 1990s (Bøhn and Millstone, 2019; Vicini et al., 2019; Benbrook, 2016; Mesnage and Antoniou, 2018; Duke and Powles, 2008). Monsanto Company retained exclusive rights to glyphosate in the United States until 2000 and actively maintained market share through product innovation and bundling of seeds and crop protection products (Moschini et al., 2019; Mesnage and Antoniou, 2018; Barboza, 2001).

Globally, glyphosate-based herbicides are used in agriculture in three ways: 1) pre-sowing application to prepare fields for sowing in minimum tillage cropping systems; 2) in-crop to control weeds, often in conjunction with glyphosate tolerant GM-crops and; 3) pre-harvest as a desiccant to ensure uniform ripening and drying of grain crops (Winters et al., 2023; Andert et al., 2019; Székács and Darvas, 2018; Benbrook, 2016). Use as a desiccant is more common in northern regions in which cold and wet weather conditions are common during harvest (Benbrook, 2016).

In Europe, one third of herbicide sales (volume of active ingredients) in EU28 + 3 countries are of glyphosate, but more research is needed on how and where glyphosate is applied throughout the crop rotations (Antier et al., 2020). Although the European Union (EU) requires permits for the cultivation of genetically modified (GM) crops including herbicide tolerant crops (Purnhagen and Wesseler, 2021; Andert et al., 2019), a wide variety of GM crops are allowed into the market as food and feed (European Commission a, undated). The EU forbids glyphosate use ‘with the intention to control the time point of harvest or to optimise the threshing’, but the European Commission acknowledges that such use does occur and, therefore, advises member countries in its Implementing Regulation (EU 2016/1313) to pay particular attention to compliance of pre-harvest uses.

In the United States, Roundup held a patent on glyphosate products until 2000, when the patent expired and new products with higher glyphosate concentrations entered the market (Perry et al., 2019). Despite packaging including instructions for adjusting dosage based on the higher concentration, application of glyphosate increased (ibid).

As an herbicide, glyphosate acts by inhibiting plant growth via disruption of the shikimate pathway, which is a metabolic pathway found in the cells of plants and some micro-organisms but is not present in animal cells (Helander et al., 2012; Duke and Powles, 2008). This mode-of-action is the reason glyphosate has historically been considered a safe pesticide for humans and other vertebrates (Schrödl et al., 2014; Helander et al., 2012; Duke and Powles, 2008; Williams et al., 2000). However, there is a growing literature that glyphosate and its primary metabolite, aminomethylphosphonic acid (AMPA), is ubiquitous in nature and the food system and has adverse consequences to human health and non-target organisms (Ruuskanen et al., 2023; Puigbo et al., 2022; Battisti et al., 2021; Ruuskanen et al., 2020a; Leino et al., 2020; Bøhn and Millstone, 2019; Székács and Darvas, 2018; Benbrook, 2016).

In recent years, a variety of regulatory bodies have considered the safety of glyphosate with mixed outcomes. The Joint Meeting on Pesticide Residues (JMPR), which evaluates and sets maximum residue levels (MRLs) for pesticides in food behalf of the Food and Agriculture Organisation (FAO) and World Health Organisation (WHO), has declared it unnecessary to establish acute reference doses (ARfDs) or MRLs for glyphosate (World Health Organization, 2021). The decision was based on epidemiological evidence restricted to studies on cancer outcomes (FAO and WHO, 2016). However, both the European Food Safety Agency (EFSA) and United States Environmental Protection Agency (EPA) have established MRL for glyphosate (EC 396/2005; European Commission b, undated; EFSA, 2023; USA 40 C.F.R. § 180.364, 2023; EPA, 2023). The MRLs set by EFSA and EPA differ substantially from each other, and controversy remains. Benbrook (2016) asserts that regulatory bodies have accommodated requests by glyphosate registrants to adjust MRL upwards to allow for the glyphosate residues in post-harvest foodstuffs caused by pre-harvest spraying. Scientists have presented evidence in support of lowering glyphosate MRL to a level 17 times lower than the EPA’s and five times lower than EFSA’s current levels (Benbrook, 2016; Antoniou et al., 2012). EFSA considers current glyphosate exposure levels via feed generally safe for livestock (EFSA, 2018a), and Sørensen et al. (2021) note that EFSA proposed (EFSA 2018b) 30% increases of MRLs for rapeseed, barley and wheat. In November 2023, the European Commission announced renewal of the approval of glyphosate for a period of 10 years. Approval is reported to come with caveats including prohibition as a pre-harvest dessicant and unspecified restrictions to protect non-target organisms (European Commission, 2023; Casassus, 2023).

1.2 Feed-feces-fertilizer: glyphosate accumulation in organic fertilizer

The route by which glyphosate may enter livestock and eventually accumulate in manure is dietary exposure. The EU’s EFSA and USA’s Food and Drug Administration (FDA) have monitoring programmes for commodity crops and may test crops entering the market for glyphosate and other agrochemical residues. However, the MRL are to ensure food safety for human consumption, and EU’s MRLs for livestock, for example, are considered only in regard to their impact on human health (EFSA, 2018a; EFSA, 2018b). By virtue of diet, however, livestock exposure to glyphosate via ingestion is generally substantially higher than that of humans (Sørensen et al. 2021). Feed produced and consumed on-farm or domestically via farmer-to-farmer networks is unlikely to be tested.

Both EFSA and the FDA report non-violative (below the MRL) glyphosate residues in commodities commonly used as feeds, including soybean, corn, barley, and wheat (EFSA, 2023; FDA, 2022; Vicini et al., 2019). Pre-harvest dessication and in-crop application on glyphosate tolerant crops are likely sources of glyphosate contamination in feed (Winters et al., 2023; Sørensen et al., 2021). Glyphosate from consumed feed has been found in the urine of a range of livestock, and EFSA has previously concluded that glyphosate is rapidly excreted from the body (cf. Winters et al., 2023; EFSA, 2015; Krüger et al., 2014a; Krüger et al., 2014b; Krüger et al., 2013).

To our knowledge, there are no public regulations in Europe or elsewhere establishing maximum residue levels for glyphosate in fertilizers. However, it is known that 1) some crop plants are highly sensitive to synthetic agrochemicals including glyphosate, and 2) glyphosate from feed accumulates in the animal and may become more concentrated compared to the initial feed residues (what goes in eventually comes out), and this concentrating effect potentially exacerbates glyphosate contamination in manure used for fertilizer (Muola et al., 2021; Ruuskanen et al., 2020a).

This study focuses on poultry manure as a fertilizer raw material. Poultry manure is one of the biological products approved as fertilizer under the European Union’s organic production and implementing regulations (EU 2018/848, EU 2021/1165). Poultry manure, a side-stream product from egg and poultry meat production, is one of the most common commercially available organic fertilizers. Availability of poultry manure is facilitated by the growth of the poultry industry and the desire to recycle the manure instead of disposing of it as waste (Kleyn and Ciacciariello, 2021; Hoover et al., 2019). Glyphosate contamination of crops via poultry manure have only been studied in a few cases. Muola et al. (2021) found negative impacts of glyphosate contaminated poultry manure on both meadow fescue and strawberry in the first year of establishment. However, further study of the strawberry plants revealed a positive effect on fruit weight in the second year (Fuchs et al., 2022).

1.3 Finland case

The study was conducted in Finland, a European Union member state since 1995, where egg and broiler chicken production are the primary sources of poultry manure. Egg production is spread across approximately 230 farms with an average stocking rate of 20,000 hens/farm that produce a total of 77.5 million kg of chicken eggs annually (Natural Resources Institute Finland 2023a, 2023b; Finnish Poultry Association, 2023). Broiler production takes place on approximately 200 farms with an average stocking rate of 60 000 broilers and yields about 147 million kg of meat (Natural Resources Institute Finland 2023b). Layer feed is most commonly a mix of domestic grains combined with proteins such as soybean (imported) or domestic fava bean or peas and is usually mixed in large batches on-farm to create a grain-based concentrate (Finnish Poultry Association, 2023). Commercial feed is also produced by several companies (ibid).

Fertilizer use and quality in Finland is legislated nationally by the Fertilizers Act (711/2022), states that fertilizers must be safe and may not contain materials that are harmful to people, animals, plants or the environment when as instructed. Finland has a relatively low rate of pesticide use compared to other countries. In 2018, sale of plant protection products (pesticides) per utilised agricultural area in the EU was 3 kg/ha but only 0.6 kg/ha in Finland (Ketola et al., 2021; Natural Resources Institute Finland, 2018). Of this, glyphosate-based herbicides accounted for about half of all plant protection products sold for agriculture in Finland (Natural Resources Institute Finland, 2019). The Finnish Safety and Chemicals Agency cites (EU) 2016/1313 in forbidding glyphosate as a pre-harvest desiccant, but glyphosate may be used, under certain conditions, to control weeds in feed crops prior to harvesting (Finnish Safety and Chemicals Agency, 2020; Kaija Kallio-Mannila, personal communication. See Discussion 4.2 for conditions in detail.).

This study was inspired by the experience of a commercial organic tomato producer that experienced production problems they traced to a commercial poultry manure fertilizer approved for organic use but containing glyphosate residues. The producer used a commercial chicken manure sourced from Finland and certified as suitable for organic production. The producer sent the fertilizer to an independent laboratory for testing, and the results revealed that the fertilizer contained 0.94 mg/kg of glyphosate. No other contaminants were found. With this information, the producer commissioned researchers at University of Turku, Finland to examine the effect of the fertilizer containing glyphosate residue on tomato production.

2.1 Empirical study

The empirical study was undertaken in 2016 in the University of Turku research greenhouses at Ruissalo Botanical Garden, Finland. Tomato seedlings and growth substrate were provided by the commercial organic tomato producer. In the beginning of April 2016 (week 14), the producer delivered 72 "Encore" variety tomato seedlings, 36 sacks of peat (70 L each) and two flexible intermediate bulk containers (FIBC) with a volume of 1000 L of organic chicken manure fertilizer. The two FIBC consisted of ‘G’ glyphosate-residue, the original fertilizer tested by the company as containing glyphosate residue; and ‘C’ control, a comparable commercially available fertilizer that underwent similar testing. Prior to delivery, the seedlings were grown by the producer together with seedlings for commercial production.

The two manure-based fertilizers were produced in Europe and marketed for professional horticultural use. As manure-based fertilizers, both products were marketed as organic, which in this context refers to the product being allowed in certified organic farming; it does not mean the manure is from certified organic livestock. The G fertilizer was an ECOCERT-certified (https://www.ecocert.com/en/home) chicken-manure fertilizer intended for professional use. The C fertilizer was produced from manure from free-range hens certified by the Dutch inspection authority for poultry, eggs and egg products (‘de Stichting Controlebureau voor Pluimvee, Eieren en Eiproducten’: CPE -certified poultry farms).

Prior to commencing the study, the fertilizers were again tested for glyphosate residue All tests for glyphosate and any other contaminants were conducted by by Groen AgroControl-Laboratory (Delft, Netherlands; certified laboratory). The samples were analysed using liquid chromatography-tandem mass spectrometry (Ruuskanen et al. 2020b), and the detection limit was 0.01 mg/ kg. Results were 0.94 mg/kg in the G fertilizer and 0.23 mg/kg in the C fertilizer. These values indicate slight variation from the 0.73 mg/kg and 0 mg/kg, respectively, previously performed by the same laboratory on samples from the same bags. Control (C) fertilizer’s NPKCa nutrient composition was 4.0–2.7–2.2–10.0 and pH 7.4. Values for the glyphosate residue (G) fertilizer were 3.6–2.8–2.2–9.6 and pH 6.4.

2.1.1 Experimental setup and management of the tomatoes

The greenhouse experiment consisted of nine glyphosate-residue (G) replicates and nine control (C) replicates across three test blocks (watering lines). Each test block contained three G and three C replicates (Fig. 1). For each replicate, two 70 l sacks of peat growth medium (Novarbo peat sacks) were opened and joined together to form a grow bed. A small area was dug in the centre of each replicate, and 9.5 kg of either C or G fertilizer was added and lightly covered with peat before covering the whole grow bed with plastic. At a distance of approximately 15 cm from the fertilizer, holes were made at the corners of each replicate for total of four holes (a-d) per replicate. One tomato seedling per hole was planted for a total of 36 C and 36 G plants (72 plants total). Planting took place during mid-April (week 15).

Figure 1. Layout of the greenhouse tomato experiment. One tomato seedling was planted at each corner of the peat sacks for a total of four plants (a, b, c, d) in each replicate. G = fertilizer containing glyphosate residue. C = control fertilizer.

The greenhouse temperature was set to 20°C, but outdoor heat frequently cause the temperature to rise to 24°C. Artificial lighting was set to 12/12 light cycle. Moisture was set to 70% with automatic mist spraying. Watering was carried out according to need so that the moisture remained optimal along the watering line. Tomatoes were managed following the conventions for commercial production, and this included weekly pruning to remove the lowest three leaves and any extraneous growth (side shoots/ suckers). Plants were attached to training ties hanging from the ceiling, and the ties were let out as necessary. To ensure pollination, plants were shaken in the morning three times per week for the duration of the experiment. Predatory mites were used as biological pest control.

2.1.2 Measurements

Fertilizer samples were tested for glyphosate at the beginning of the experiment, and again at the end of the experiment when samples were taken and tested from five C and five G grow beds, respectively. The purpose of this sampling was to control for any possible variation between the different grow beds. Ripe tomatoes from plants in both the C and G groups were tested for glyphosate residues at the end of the experiment.

Plant growth and fruit production were followed for 14 weeks (Table 1). Plant length, length and width of leaves above the third fruit clutch, distance between fruit clutches, number of clutches per plant, and number of tomatoes per clutch were measured.

Tomatoes ready for harvesting were collected, counted and weighed. The lowest tomato clutches were harvested whole when over half of the tomatoes in the clutch were ripe (harvesting dates: June 6th and 20th ). During the period June 30 through July 18, ripe tomatoes were collected separately from individual clutches and were weighed and classified into either first or second class. Quality classification was a blind test – the person classifying the tomatoes did not know whether the tomatoes were from G or C fertilised plants. The commercial tomato producer inspected the researchers’ classification to assure the sorting accurately reflected professional standards of commercial tomato production. Upon conclusion of the experiment on July 18, both ripe tomatoes and all clutches with at least one green (raw) tomato with a minimum circumference of 1 cm were weighed.

Table 1

Timeline of the experiment.
Experiment task	Date
Seedlings and other materials delivered	Beginning April (week 14)
Tomatoes planted and experiment commences	Mid-April (week 15)
First harvesting	June 6th and 20th (weeks 23 and 25)
Ripe tomatoes harvested and classified	June 30 – July 18 (weeks 26 − 29)
Final harvesting and measuring; Experiment concluded	July 18 (week 29)

2.1.3 Statistical analysis

For each plant, the mean value based on the morphologically descriptive variables of leaf length and width as well as distance between tomato clutches was calculated, and the daily plant production was recorded. Differences between the mean values of the G and C groups were tested using t-test with degrees of freedom (df) and statistical significance (p-value), and accumulation of the overall harvest during the six-week period was explored with the aid of the figures. Relationship between the two treatments and the production was determined through correlation analysis.

Tomato production was measured three ways: 1) total yield, 2) ripe tomatoes, and 3) first class tomatoes (Table 2).

Table 2

Production from tomatoes grown with glyphosate-residue (G) and control (C) fertilizers were measured as the weight of the total yield, the ripe tomatoes and the first-class tomatoes.
Measure	Description
Total yield	All ripe and unripe tomatoes (ripe tomatoes consisted of the first and second tomato clutches, ripe tomatoes from period June 30 to July 18, and any unripe tomatoes at the end of the experiment)
Ripe tomatoes	Weight of all ripe tomatoes harvested during the experiment period (June 30 to July 18)
First-class	Weight of the first-class tomatoes harvested during the experiment period (June 30 to July 18)

2.2 Qualitative study

Based on prior knowledge and online search of fertilizer companies marketing fertilizer in Finland suitable for organic production, we identified five companies to contact to gain perspective on how the industry views glyphosate contamination in organic fertilizers. We reviewed the company websites and contacted representatives of the five companies via email. We inquired about three themes:

Are glyphosate residues an issue in organic fertilizer production?
Are criteria for glyphosate residues in use?
Any views or experiences to share about pesticide residues in recycled fertilizers?

Interviews following initial contact aimed to elicit responses to these three themes and were tailored to the level of engagement – via email or telephone–from the respondent. Notes were taken during telephone calls, and respondents were contacted as needed for follow-up or clarification.

We also contacted four experts in Finland to gain perspectives from the poultry and organic farming associations and to understand the state of knowledge and any action taken regarding pesticide residues in organic fertilizers. These experts represent: Organic Growers Association, Poultry Producers Association, the Centre for Economic Development, Transport and the Environment (Ely-Centre), and Finnish Food Authority.

3.1 Empirical study

Testing for glyphosate at the beginning of the experiment showed that the glyphosate content of the glyphosate-contaminated fertilizer (G) had a glyphosate content of 0.94 mg/kg, which was 76% higher than the 0.23 mg/kg found in the control fertilizer (C).

Compared to the G plants, C plants were more lush with longer (G average 48.4 cm and C 50.3 cm; t = 2.4, df = 63, p = 0.020) and wider leaves (G 44.7 cm and K 56.0 cm; t = 6.6, df = 54, p < 0.001). The lower leaf biomass of the G plants caused some leaves to look sparse and "parsley-like" (Fig. 2, lower row).

Plant height did not differ significantly between the C and G plants. Control plants did, however, produce more tomato clutches (mean: G 10.2 clutches vs. C 11.2 clutches; t = 3.4, df = 54, p = 0.002), and clutches were produced more densely on the plant (mean distance of clutches: C 25.2 cm vs. G 26.6 cm; t = 2.0, df = 57, p = 0.049).

Growth variables were correlated with each other. Additionally, some growth variables, particularly the mean width of leaves (Table 3), length of leaves and clutch distance were clearly correlated to production variables.

Table 3

Relationship of leaf width to production variables. Results are presented with correlation coefficients, with * indicating the strength of the correlation (** p < 0.01, *** p < 0.0001)
Measure	Leaf width
All tomatoes, total	0.49***
Ripe tomatoes, total	0.47***
July 18 harvested ripe	0.37**
July 18 harvested raw	0.61***

Many of the G tomato plants appeared successful at the beginning of the experiment, and tomatoes ripened first on the G replicates. However, the number of ripe tomatoes in G plants diminished toward the end of the experiment (Fig. 3).

Although ripening started out the same along all three watering lines, C plants began to overtake G plants in all harvest variables during the period July 6–13 (weeks 27–28). These differences continued to grow throughout the experiment. At the end of the experiment, the C plants had produced 121.4 kg while the G plants produced 78.9 kg of tomatoes (t = 5.7, df = 66, p < 0.001), which is a 35% difference. Difference in total production was particularly pronounced for the raw tomatoes. The C tomatoes increased production rate around the time when the production rate in the G tomatoes began to level off for both ripe (Fig. 4) and first-class fruits (Fig. 5).

The G plants underperformed by all measures of production compared to the C plants (Table 4). For the ripe tomatoes, C plants produced 49.2 kg and G plants produced 37.9 kg, which is a 23% decline in ripe tomatoes (statistically significant difference t = 2.9, df = 69, p = 0.005). For the first-class tomatoes, C plants produced 34.3 kg and the G plants 21.5 kg, a difference of 37% (statistically significant difference t = 3.3, df = 56, p = 0.002).

Table 4

Final harvest results of the 14-week greenhouse experiment for the tomatoes fertilised with either glyphosate-residue fertilizer (G) or control fertilizer (C).
	Production (G & C)		Difference in production (G-C)
	G (kg)	C (kg)	G-C (kg)	G-C (%)
Total harvest	78.9	121.4	-42.5	-35%
Ripe tomatoes	37.9	49.2	-11.3	-23%
First-class tomatoes	21.5	34.3	-12.8	-37%

Mean growbed glyphosate levels at the end of the experiment were 0.44 mg/kg for G growbeds and 0.24 mg/kg for C growbeds. No glyphosate residue was found in the ripe tomatoes from plants in either treatment.

3.2 Qualitative study

3.2.1 Industry representatives

The five fertilizer companies interviewed represent the majority of fertilizer sales in Finland. The representatives interviewed held researcher, operations director or other positions in which they were well placed to know about company policy and experience regarding quality control and potential contaminants. All the companies produce fertilizer marketed for use in organic farming in Finland. The company profiles varied (Table 5), as did their knowledge and experience of glyphosate or other pesticide contamination in side-stream raw materials or potential raw materials considered for upcycling as fertilizer. Companies A, B, and E were the most knowledgeable and forthcoming on experiences, procedures, and expressing views about glyphosate and other pesticide residues.

Table 5

Overview of the companies contacted in this research. The list is not exhaustive of all raw materials used by the companies.
Stakeholder	Types of manures used
Company A	Domestic chicken manure.
Company B	GMO-free domestic chicken manure.
Company C	GMO-free domestic chicken manure.
Company D	Variety of organic fertilizers from livestock manure including cattle, pigs and poultry.
Company E	No manure used. Organic-certified (private label) fertilizer from non-manure raw material.

Representatives from the Finnish Organic Association and the Poultry Producers Association emphasized the importance of feed consistency in production and confirmed that feed is normally mixed in large batches on-farm using the farm’s own grains and additional protein such as soybean, oilseed, and fish by-products as well as oils and minerals. The Organic Association expressed specific interest in discussions about the legislative definition of ‘industrial’ and the effect the definition has on the quality of fertilizer products used in organic farming.

3.2.2 Glyphosate residues in fertilizer production

Two companies, A and B, stated that glyphosate contamination of poultry manure is an issue of concern or past concern and is explicitly addressed in their quality control. Company A identified domestic grains as a prior source of contamination, and Company B identified imported feed, specifically soybean, as the major source of contamination for poultry manure (Table 6). Company A traced contamination to feed grain on individual farms and described a case where they worked together within their network to educate the farmers about the problem and monitor manure from specific farms to eliminate contamination. To reduce glyphosate contamination, Company B’s manure providers are under contract that manure comes from livestock fed GMO-free feed. Company C reported no knowledge of glyphosate residues in their poultry manure, but also indicated that their manure is sourced from GMO-free poultry and expected that this should limit potential contamination. Company D stated that they are unaware of glyphosate residues in the manure they source, and emphasized that pre-harvest desiccation is not allowed in Finland. Company E indicated that they have not encountered glyphosate in the side-stream products they use, which do not include animal manure.

Table 6

Summarised responses for thematic question ‘Is glyphosate residue an issue in organic fertilizer production?’
Stakeholder	Glypho-sate residue an issue? (Yes/No)	Summary of responses
Company A	Yes	Glyphosate residue in raw material was first encountered in poultry manure about 10 years ago and was traced to on-farm feed. Residue in poultry manure was resolved through communication with poultry producers and monitoring. Glyphosate and AMPA are occasionally found in other side-stream products. In 2018, the company rejected domestic oilseed rape meal as unsuitable due to contamination levels of 16 mg/kg glyphosate and 0.33 mg/kg AMPA. Bakery waste has high levels of glyphosates. Other pesticides are also found, particularly pyralids and diuron.
Company B	Yes	Aware of potential glyphosate contamination of poultry manure and have set a condition with poultry manure providers for a maximum permitted level of 0.2 mg/kg but are continuing to revise this limit. Strategy to limit glyphosate risk is to purchase manure from GMO-free poultry producers who do not use glyphosate-tolerant soybean feed.
Company C	No	The company does not test for glyphosate residue in manure. The producer supplying the poultry manure has an agreement with the feed provider for GMO-free feed, and the company thinks this should be sufficient.
Company D	No	No knowledge of glyphosate residue in company’s production. They are aware that KRAV (Swedish organic label) would like information about possible pesticide-residues for some pesticides.
Company E	No	Do not use manure, but do use plant waste. No glyphosate or AMPA residues were found from the side-stream products (e.g. sugar beet processing leftovers) tested (Galab 500PLUS). However, clopyralid is a challenge because it causes problems, e.g. for tomatoes, at the level allowed for feed and is not suitable for field use. Diuron has also been found.

Companies A, B and E have internal testing and criteria to monitor for pesticide residues including glyphosate (Table 6). According to its representative, Company C does not test for glyphosate or other pesticide contaminants. Company D reported only that they follow all applicable regulations if such exist. Representatives for A, B and E reported testing for pesticide residues, primarily using external laboratories, and one company informed that they also have a wide range of crop experiments because ‘not everything can be analyzed and the plants know more’.

3.2.3 Identifying risks, knowledge gaps, and residue limits

Concerns can be illustrated by questions and comments, especially from companies A, B and E. Two asked whether glyphosate breaks down during processing for biogas or through heat treatment used in sugar beet production, and one asked if the researchers know of or could suggest recommended limits for glyphosate in manure or fertilizers. One representative commented in depth:

If some risk is known, it is better to respond to that risk than just ignore it. Glyphosate and pyralids should be measured the same way as other contaminants such as heavy metals. We need to know how quickly they break down in the conditions we have here. In the same way as for sludge, we need to research and control these other side-streams.

Four of the five companies have experience cooperating with research or governmental organizations on the safety of recycled fertilizers. One of these projects is ‘Kiertokas: Towards a sustainable circular economy: Residue of plant protection agents in recycled fertilizers and growing media, and their management’ (Finnish Food Authority, 2023). Kiertokas is the first project in Finland to focus exclusively on pesticide residues in organic fertilizers. The project is funded for the period 2023–2026 with Finnish food Authority, Finnish Ministry of Agriculture and Forestry, and several fertilizer companies as partners. A key aim of the project is to establish upper thresholds for pesticides including glyphosate in organic fertilizers.

The need for common standards for glyphosate and other potential contaminants was described by the contacted stakeholders as having multiple benefits, including product quality, providing a legal foundation for the fertilizer companies if they are sued for crop damage attributed to pesticide residues in fertilizer, and in providing clear guidelines for the providers of raw materials. Some of the companies noted their legal obligation to provide a clean product and expressed concern about attempts to valorize side-stream products as fertilizer raw materials without understanding and examining potential risks:

‘We want cleaner production, and independent research is needed to take it forward… Some do not understand the risks, and some just ignore them’.

Standards for pesticide residues in fertilizers were also considered important because feed, raw materials and fertilizers travel across borders. Based on their own internal testing, the companies identified some products of concern, including sugar beet, oilseed rape, side-stream materials from insect prodution, and bakery waste. Pesticide residues of concern included especially diuron and pyralids (specifically clopyralid). Glyphosate was considered as mainly under control through testing. Some of the companies noted that the allowable residue limits (MRL) for glyphosate and pyralids in crops resulted in pesticide residue levels that are problematic for sensitive crops including tomatoes and peas.

Interviews with two researchers in the Kiertokas project further elucidated the challenges in measuring and monitoring for pesticide residues and establishing MRL for fertilizers. The project is partially influenced by prior efforts to include chemical testing in legislation, as well as knowledge that Sweden and Norway already have some recommendations for pesticide residues in fertilizers. The researchers reported that key challenges of the project include what pesticides to test for and on which products. They indicated that although all raw materials should be tested, this is not possible due to resource limitations. Based on their own discussions with fertilizer producers, the Kiertokas researchers confirmed that the producers are particularly interested in the decomposition processes of the pesticide residues, including the possible effects of light, temperature, composting, and biogas production in accelerating decomposition. As a starting point, the Kiertokas project researchers indicated that the project intends to use, where available, the fertilizer producers’ internal residue limits as reference values in testing. Project results will be available online as they become available (Finnish Food Authority, 2023).

4.1 Negative impacts of glyphosate residues

The two fertilizers were substantively similar, and the difference in tomato production across the two treatments can reasonably be attributed to the glyphosate residue present in a commercial fertilizer marketed (at the time) as suitable organic horticultural production.

Tomatoes are known to be highly sensitive to many herbicides (Goldy, 2016; Kruger et al., 2012), and tomato has been described as the "canary in the coalmine" of the vegetable world for herbicide drift including glyphosate (Goldy, 2016). The difference in harvest between the glyphosate residue and control tomato was particularly pronounced toward the end of the experiment, which suggests that that the difference in tomato harvest would have been even greater if the study were continued longer.

The correlation between the growth variables measured early in the experiment and the production measured at the end of the experiment suggest that plant production can be predicted based on growth behaviour at the beginning of the growing season. Over time, the small-leaved and sparse plants do not produce as well as lush plants.

4.2 How widespread is glyphosate residue in fertilizer?

Currently, no-one knows how widespread glyphosate residue is in fertilizers, and it probably varies globally. Our empirical study, however, shows that glyphosate residue in fertilizer at the level found on a batch on the market can be a risk for herbicide-sensitive crops like tomato. Interviews with the fertilizer producers revealed that glyphosate can enter the fertilizer production chain through contaminated raw materials such as poultry manure and that vigilance is needed to prevent such contamination. The potential for glyphosate contamination entering via feed depends on a variety of factors including how glyphosate is used and what types of monitoring are in place to minimize the risk of contaminated product reaching the market.

The finding by one company that herbicide residue in bakery waste is too high for fertilizer production illustrates that foodstuff MRLs alone do not assure that products can be safely recycled into the food system as fertilizer. Finland’s major grain purchasers require farmers to guarantee their grain has not been desiccated with glyphosate or other herbicides, but bakery waste includes both imported and domestic grains.

The Finnish Safety and Chemical Agency (Tukes) has settled on a strict interpretation of the EU legislation on glyphosate (EU 2016/1313) and forbidden pre-harvest application of glyphosate in grains destined for human consumption. However, it does allow pre-harvest application of glyphosate for control of couch grass (Elymus repens) in feed crops of barley and oat and in rapeseed under conditions of maximum 30% moisture content and with a 10-day holding period (Kaija Kallio-Mannila, Tukes, personal communication). It is likely that the legislative loophole that allows pre-harvest spraying for weed control in livestock feed crops is the source of the domestic glyphosate residue identified by Company A. This supposition is supported by the fact that the company was able to eliminate the glyphosate by raising awareness with the manure providers and conducting farm-level testing of the manure. Company B and C’s strategy of avoiding genetically modified feed is a prudent choice in line with research that glyphosate residue in livestock and feed is primarily from genetically modified crops like soybean and pre-harvest dessication (Winters et al., 2023; Billenkamp et al., 2021; Schrödl et al., 2014). It does not, however, eliminate the risk from pre-harvest dessication or pre-harvest weed control.

4.3 Mechanisms of glyphosate breakdown is a knowledge gap

The companies’ questions about the effect of biogas production and other heat treatment in possibly breaking down pesticide residue components indicates an extremely relevant knowledge gap for recycled fertilizer that could be addressed through cooperative, multi-actor research with processers and fertilizer companies. Prior efforts to understand glyphosate degradation systems have revealed both abiotic and biotic mechanisms (Chen et al. 2022). The abiotic mechanisms, photolysis (radiation) and especially adsorption (for example by using biochar) are worth studying in more detail. Presently microbial degradation pathways and the relevant enzymes are better known. Microbes have two main ways to break down (= consume glyphosate components) glyphosate (Chen et al., 2022; Sviridov et al., 2021), where one degradation pathway produces AMPA – which is more stable and toxic for most organisms – and the other produces sarcosine that readily mineralizes to NH₃ and CO₂. The sarcosine pathway has been found in e.g. in some Pseudomonas and Agrobacterium lines, but their use in field conditions has turned out to be difficult. Further, their relevant enzymes are poorly active in field conditions in Finland characterized by cold climate and acidic soils.

4.4 Addressing pesticide contamination

Although the focus of the interviews with the companies was glyphosate, three of the companies brough up chlopyralid and diuron residues as issues of greater concern. The finding that companies are interested in collaboration with officials to establish maximum limits for pesticide residues in fertilizers is in line with the finding by Osuuskunta Visia (2019) that fertilizer producers have a positive attitude toward efforts to update legislation governing organic fertilizers.

Overall, the results of this empirical study, the stakeholder interviews and the background to glyphosate presented in Introduction show that glyphosate contamination is a complex issue with far-reaching implications. This study supports the finding that, although use of poultry manure as fertilizer is encouraged by EU policy, glyphosate residues originating in contaminated feed can inadvertently affect other agricultural production (Fuchs et al., 2022; Muola et al., 2021). It also supports the assertion by Ferrante et al. (2023) that glyphosate can reach non-target destinations and that a One Health perspective accepting that human, animal, plant and microbial health are interwoven is essential to understanding the impacts of glyphosate.

Uptake of organic fertilizers is important for fostering nutrient cycling as part of circular economy, meeting organic production aims, and reducing dependency on mineral fertilizers. However, glyphosate residues and other contaminants can cause unforeseen production problems that may be difficult and costly to identify. For these reasons, it is particularly important to establish parameters for herbicide residues in fertilizers.

Persistence of glyphosate and other agrichemicals in the agricultural production chain are a challenge for just transitions toward sustainable agriculture. Contamination through a feed-feces-fertilizer chain is understudied and mainly unregulated. Science-based limits on pesticide residues in organic fertilizers are urgently needed. Multi-actor networking that engages stakeholders throughout the production chain can be effective in identifying and addressing contaminants in fertilizer raw materials. However, effective legislation that reduces the source of contamination, i.e. reduces pesticide loads, is also needed. A ‘One Health’ approach or a similar holistic framing is essential to effectively implementing agricultural circular economy in practice.

FUNDING:

Ikaalisten Luomu; Research Council of Finland grant n:o 311077 to MH

ACKNOWLEDGEMENTS

The empirical research of this project was paid for by Ikaalisten Luomu Oy. Funding was provided in part by Research Council of Finland grant no. 311077 awarded to MH. We thank the representatives of the five fertilizer companies for sharing their perspectives and experiences; Finnish Food Authority researchers Liisa Maunuksela and Anne Relander; Anni-Kaisa Karhunen of Ely-Centre; and representatives of the Finnish Organic Association and the Poultry Producers Association for their time and expertise.

ETHICS AND CONSENT

The research contains results of communications, either emails or telephone interviews, with stakeholders from fertilizer companies operating in Finland. Respondents were made aware when contacted that they are being contacted as a part of research conducted by University of Turku on the issue of glyphosate/ herbicide residues in fertilizer raw materials. Participation in the study, including level of engagement with the researchers, was voluntary. No personal information was collected beyond name and job title of the respondent. In accordance with EU GDPR and applicable national legislation, respondent privacy has been protected. Results the fertilizer company inquiry are presented in an anonymized fashion with identifying details removed. Professional organisations and expert individuals who provided knowledge and expertise have been acknowledged in Acknowledgements. All attributed personal communications been verified and approved for publication by the subject.

FUNDING

The empirical research of this project was paid for by Ikaalisten Luomu Oy, an organic horticultural producer. The producer approached the researchers about investigating the effect of glyphosate residue in fertilisers on tomato production after experiencing unexplained problems in production and an independent laboratory identified glyphosate residue in a batch of manure fertiliser used in the production. The horticulture producer provided the fertilisers and seedlings as well as advice on growing method. The research itself was conducted independently by the university researchers in the university’s facilities.

The authors declare that they do not have any conflicts of interest.

CONTRIBUTIONS

All authors contributed substantially to the manuscript. M.H. and I.S. conceptualized the empirical study, which was carried out by M.H. and K.S. Statistical analysis was done by I.S. and visualization by M.H. and K.S. The manuscript was written by T.B., who also conducted the qualitative research. All authors participated in revision of the manuscript.

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Competing interest reported. The empirical research of this project was paid for by Ikaalisten Luomu Oy, an organic horticultural producer. The producer approached the researchers about investigating the effect of glyphosate residue in fertilizers on tomato production after experiencing unexplained problems in production and an independent laboratory identified glyphosate residue in a batch of manure fertilizer used in the production. The horticulture producer provided the fertilizers and seedlings as well as advice on growth method. The research itself was conducted independently by the university researchers in the university’s facilities.

The authors declare that they do not have any conflicts of interest.

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Feed-feces-fertilizer: Greenhouse study and interviews with fertilizer producers indicate persistence and negative effect of glyphosate residue in manure-based fertilizers

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Abstract

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1. INTRODUCTION

1.1 Glyphosate: A controversial ‘miracle’ herbicide

1.2 Feed-feces-fertilizer: glyphosate accumulation in organic fertilizer

1.3 Finland case

2. MATERIALS AND METHODS

2.1 Empirical study

2.1.1 Experimental setup and management of the tomatoes

2.1.2 Measurements

2.1.3 Statistical analysis

2.2 Qualitative study

3. RESULTS

3.1 Empirical study

3.2 Qualitative study

3.2.1 Industry representatives

3.2.2 Glyphosate residues in fertilizer production

3.2.3 Identifying risks, knowledge gaps, and residue limits

4. DISCUSSION

4.1 Negative impacts of glyphosate residues

4.2 How widespread is glyphosate residue in fertilizer?

4.3 Mechanisms of glyphosate breakdown is a knowledge gap

4.4 Addressing pesticide contamination

5. CONCLUSION

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