Status, legislation and action plans for the use of pesticides in relation to public goods
We use the term ‘pesticide’ as the common term for herbicides, fungicides, insecticides, acaricides, nematicides, molluscicides, rodenticides, growth regulators and repellents. Most pesticides are chemically synthesised (synthetic), although some are based on naturally occurring compounds. In 2014, the total sale of pesticides in Denmark was 9075 t corresponding to 0.5% of the total sale of pesticides in the EU-28. The proportion of herbicides and plant growth regulators was considerably higher in Denmark (63% of total pesticide sale) compared to the EU-28 (33% of total pesticide sale), whilst the relative sale of fungicides, bactericides and insecticides on the other hand was considerably lower in Denmark than in the EU-28 (27 compared to 44% of total pesticide sale) (Eurostat 2016). In order to protect consumer and animal health, the EU has introduced maximum residue levels (MRLs) for pesticides in food and feed of plant and animal origin in EU Reg. 396/2005, which also apply to organic food and feed products. This regulation also lays down rules for the official control of MRLs, reporting and sanctions by the Member States, and it amends Council Directive 91/414/EEC of 15 July 1991, which is the basic legislation for authorisation of pesticides. According to the pesticide residue control programme of the EU for 2015, the share of organic food samples with pesticide residues was 13.5%, compared to 43.9% with pesticide residues for the conventional food samples (Table 1; EFSA 2017). The Danish pesticide residue control programme in 2015 found residues in more than 50% of samples from imported fruits and vegetables, whilst the proportion was lower in Danish products (Table 1). Only one organic sample contained pesticide residues, which the authorities found was most likely due to unintentional contamination from a neighbouring conventional field (Fødevarestyrelsen 2016).
The use of pesticides in the EU in relation to public goods is regulated by Directive 2009/128/EC, establishing a framework for community actions to achieve the sustainable use of pesticides. According to Preamble 5 of this Directive, the Member States should use ‘National Action Plans aimed at setting quantitative objectives, targets, measures, timetables and indicators to reduce risks and impacts of pesticide use on human health and the environment and at encouraging the development and introduction of integrated pest management and of alternative approaches or techniques in order to reduce dependency on the use of pesticides’. Danish pesticide action plans implemented since 2004 (Ministerierne for Miljø og Fødevarer 2004) lately aimed at reducing the impact of pesticides on health, nature and environment with 40% by the end of 2015 compared to 2011 (Miljøministeriet 2012). This was not fully achieved (Miljøstyrelsen 2017). Policy tools for the reduction of pesticides use include restrictive approval of pesticides, pesticide tax, restrictions on the use of pesticides in certain areas (e.g. areas with groundwater interests) and CAP support to avoid the use of pesticides, e.g. by supporting organic farming.
Relevant organic principles and legal requirements
The principles of organic farming in EU Reg. 834/2007, Articles 4 and 5, state that ‘the use of chemically synthesised inputs is restricted to exceptional cases, where other methods or inputs are not available. Instead, the maintenance of plant health should be based on preventive measures, such as the choice of appropriate species and varieties resistant to pests and diseases, appropriate crop rotations, mechanical and physical methods and the protection of natural enemies of pests’. Thus, pest management in organic farms should be based on preventive measures and use of agroecological practices (Wezel et al. 2009). The few active pesticide substances of natural origin that are allowed in organic farming in cases where other measures are not sufficient are listed in Annex II of EU Reg. 889/2008.
Potential contribution of organic farming to public goods due to very restrictive use of pesticides
In Denmark, 156 active substances are approved for plant protection in conventional agriculture, whilst 492 active substances are allowed in the EU (DG Sanco 2017). Besides, basic substances that are covered by the definition of ‘foodstuff’ in EU Reg. 178/2002, only 23 active substances are allowed in organic farming, of which some may only be used for very restricted purposes and some only in traps in orchards (EU Reg. 889/2008 amended version, Annex II). In Denmark, only 22 active substances are allowed as there is a general ban on the use of copper fungicides in Denmark since 1995. Plant growth regulators and herbicides are not allowed in organic agriculture. Instead, weed control ideally is based on a balanced crop rotation, which often includes legumes and/or clover grass and in combination with mechanical or other physical weed control. Diseases and insect pests in organic farming may also be controlled by crop rotation, companion planting, robust and resistant crop varieties and promotion of beneficial insects (predators) by functional biodiversity initiatives such as hedgerows, insect hotels and flower stripes in the field. The direct consequences of the restrictive use of pesticides and the indirect effects of the implementation of agroecological practices on different public goods are analysed in more detail in the following.
Influence on nature and biodiversity
Comparative studies have documented that organic farming potentially increases biodiversity in fields and adjacent habitats with 30% relative to conventional farms (Bengtsson et al. 2005; Hole et al. 2005). In a comprehensive meta-analysis, Tuck et al. (2014) has confirmed that the 30% increase is a robust result, which has been valid for 30 years, and that the increase in the number of species on organic farms especially depends on how intensively the farming area is managed, measured as the number of fields in rotation of the total area. The more intensively the whole area is managed, the greater positive effect of organic farms, and the effect is greatest on wild plants and pollinating insects. However, Birkhofer et al. (2014) found the greatest effect of organic farming on birds, beetles and butterflies, which shows the difficulties in getting an unambiguous/precise picture of the effects. The number and diversity of natural enemies of pest animals, including spiders, parasitic wasps and ground beetles, is also higher in organic fields (Crowder et al. 2010). The documented beneficial effects can be directly related to the absence of pesticides, but also to the utilisation of organic manure and a different crop composition on organic farms (Andersen et al. 2014; Boutin et al. 2014). Additionally, the requirement that organic cattle must have access to daily grazing in the summer period also affects the biodiversity of certain groups of organisms positively. The few non-synthetic insecticides and fungicides that are allowed in organic production are only used sparingly in fruit orchards and vegetable production and not in agricultural crops, so direct as well as indirect effects of pesticides are normally absent in organic agriculture, though contamination from spraying of neighbouring conventional fields may take place.
As described above, Danish organic farms generally have a more varied crop composition in the rotation than conventional farms with more legumes and clover grass. Flowering legumes are attractive food sources for pollinators (Hanley et al. 2011; Knight et al. 2009). Besides, organic farms have more perennial grass fields with low yield and higher diversity of wild plants than conventional farms (Aude et al. 2003; Henriksen 2013; Petersen et al. 2006). This is a response not only to restrictive pesticide use but also other organic regulation such as limited fertiliser use and requirements for grazing of all livestock, as discussed below. The absence of pesticides, the crop composition, the share of perennial crops, the soil tillage and crop residues all have great influence on the diversity of soil organisms (Vályi et al. 2014). Surface dwelling earthworms and soil microarthropodes are negatively influenced in number and species diversity by mechanical soil cultivation, especially ploughing (Crittenden et al. 2015; Ernst and Emmerling 2009; Peigné et al. 2009). Tests in other countries have shown that ploughing reduces the biodiversity of arbuscular mycorrhiza in the soil (Köhl et al. 2014; Säle et al. 2015), and the fields in rotation are generally ploughed more in organic than in conventional agriculture. However, research has shown that the diversity of microorganisms is higher in soils with organic compared to conventional production (Oehl et al. 2004; Stagnari et al. 2014), so other factors may have greater influence on the soil biodiversity than ploughing.
Moreover, the use—or not—of herbicides affects the biodiversity of the uncultivated habitats close to the fields negatively. Analyses of the flora in Danish windbreaks between fields have shown that there are much more dicotyledon plant species in the bottom of the windbreaks on organic farms than on conventional, independently of soil type and age of the windbreak (Boutin et al. 2014; Bruus et al. 2008). These and other studies (Petersen et al. 2006) have also shown that re-colonisation of the windbreaks with the complete flora by conversion to organic farming may take very long time (up to more than 30 years), whilst the re-colonisation of the field areas is much faster. Finally, however, the contribution of organic agriculture to biodiversity preservation is questioned by some biologists claiming that this production form does not in itself protect the specific red-listed species; many of which depend on uncultivated land (Ejrnæs 2017).
Influence on environment
Besides biodiversity preservation, the main agri-environmental challenges and focus areas in Denmark are the impact from nitrogen and pesticides on groundwater, nitrogen and phosphorous eutrophication of freshwater and marine water and the maintenance of soil resources and quality. Non-use of pesticides potentially has direct and indirect effects on all aspects. In Denmark, almost all drinking water is tapped from the groundwater, for which reason there is focus on the risk of pesticide and nitrate contamination. Based on the EU Drinking Water Directive (Council Directive 98/83/EC, 1998), the limit value for pesticides and degradation products thereof in groundwater and drinking water in Denmark is set at 0.1 μg/l for each compound and at 0.5 μg/l for the sum of compounds (Miljø- og Fødevareministeriet 2016b). In 2014, pesticides were found in 26% of the water drillings of common waterworks (minimum 10 households) and the threshold limit value was exceeded in 3.6% of the water drillings selected for testing (Miljøstyrelsen 2016). However, the findings mainly concerned pesticides or degradation products thereof that are no longer allowed in Denmark. Because of the ban on the use of synthetic pesticides, organic agriculture has been proposed as a means to protect drinking water resources in areas that are characterised as particularly vulnerable to pesticide leaching (Naturstyrelsen 2015). Besides leaching, pesticides may be lost by air drifting during the process of application. A Danish study showed that the pesticide concentration in streams near agricultural land often exceeds the limits for growth of algae and daphnia and thus impacts the entire microflora and microfauna (Rasmussen et al. 2015). This is supported by an EU-wide study (Malaj et al. 2014).
The ban on pesticide use increases the need for mechanical weeding resulting in bare soil in certain periods of the year. This, in combination with the fact that N fertilisation is based on organic sources like manure and N-fixing legumes, where nitrification takes place in periods with no crop uptake of N, increases the risks of nitrate leaching. Under Danish conditions, the nitrate leaching from the root zone in organic cash crop rotations are on level with conventional, despite of a lower overall application of nitrogen to the organic crops (Knudsen et al. 2014).
Influence on energy use and climate change
There are no specific requirements in the EU Organic Regulation nor the Danish guidelines on organic farming regarding energy consumption or climate change mitigation except for general objectives of EU Reg. 834/2007, Article 3, stating that ‘organic farming shall make responsible use of energy and natural resources’. The very restricted use of pesticides in organic farming induces a change in the whole cropping system to more varied crop rotations with more legumes and clover grass for nitrogen fixation and application of mechanical and thermal weeding methods. This, together with the ban on chemical fertilisers, gives rise to changes in energy consumption and emissions of greenhouse gasses compared to similar conventional plant production systems.
Comparisons of energy consumption per ha for organic vs. conventional crops generally show lower energy use in organic farming, especially because of the non-use of chemical fertilisers, which normally is attributed an indirect energy ‘cost’ in MJ per kg N. This energy cost often amounts to levels comparable with the direct energy cost from diesel use for the field operations (approximately 100–140 MJ per ha under Danish conditions). The diesel use is either similar in the two systems for the same crops or sometimes higher in organic agriculture due to manure handling (Halberg et al. 2008b; Halberg 2012), whilst the extra diesel use from mechanical weeding replacing pesticides in most cases is of minor importance when comparing systems. However, there is an indirect energy cost, which may be attributed to the N content in manure imported to organic farms, in a situation where the manure N could have replaced N in chemical fertiliser on a conventional cash crop farm (Halberg et al. 2008b; Knudsen et al. 2011). This indirect energy cost in MJ per kg N is normally not included in the comparisons of organic and conventional farms. When comparing energy use per kg crop produced, the higher conventional yields—which again are due to the combined use of pesticides and fertiliser—partly compensate for the higher-energy input, and therefore, the relative energy use per kg cash crop is only marginally lower in organic systems (Halberg et al. 2008b). In fact, organic crops with very low yields compared with conventional, such as potatoes, have higher energy costs per kg crop compared with conventional (Halberg 2012).
In 2014, the Danish agricultural sector contributed with 20% of the overall greenhouse gas (GHG) emission in CO2 equivalents, and next to the energy sector, it is the largest source of GHG emission in Denmark. The emission of GHG in organic crop production is generally lower per ha in organic farming than in conventional farming but not always lower per produced unit due to lower yields in organic crops (Knudsen et al. 2011). Knudsen et al. (2014) calculated the GHG emission for organic and conventional crop production based on a dry matter production of 4100 kg DM/ha in organic farming compared to 5750 kg DM/ha in conventional production in long-term crop rotation experiments. The GHG emission for organic crop production was 0.440 kg CO2 equivalents/kg DM and 1757 kg CO2 equivalents/ha compared to 0.425 kg CO2 equivalents/kg DM and 2396 kg CO2 equivalents/ha in conventional production. However, across a large number of studies, GHG emission per produced unit is comparable between organic and conventional crops with some studies showing higher emission in conventional crops and others the reverse (Mondelaers et al. 2009; Knudsen 2011; Tuomisto et al. 2012; Meier et al. 2015).
Influence on human health and welfare
The direct effect of the ban of synthetic pesticides in organic farming is a much lower frequency of detected pesticide residues in organic food samples compared to conventional (see Table 1), which means a lower exposure to pesticides for consumers of organic food. In addition, the very restricted use of pesticides also reduces the occupational exposure of farm workers to pesticides. Several studies on the negative effects of pesticides on human health are related to occupational exposure (Mie and Wivstad 2015), whereas only few look into the effect from exposure to pesticide-contaminated food. A main motivation for consumers buying organic food products is belief in positive health attributes especially due to avoidance of pesticides and medicine residues in the food (Christensen et al. 2014; Denver and Christensen 2010). However, it is not possible to give clear scientific evidence that organic diets generally improve human health, because the biological and sociological interactions are too complex. Negative effects on children’s cognitive development from organophosphate pesticides have been presented in a recent report from European Parliamentary Research Service (EPRS), where organic food was suggested as a way to minimise exposure, in particular during pregnancy and infancy (STOA 2016). In these studies, it was metabolites that were measured and the uncertainties using these metabolites were not discussed in the report, e.g. that the metabolites also can originate from other substances than pesticides. Chiu et al. (2015) investigated the relation between quality of semen and intake of fruits and vegetables and found a correlation between low semen quality and fruits and vegetables with high levels of pesticides. Contrary to that, they found a positive correlation between semen quality and intake of fruits and vegetables with low or moderate levels of pesticides, and the authors concluded that more data are needed before final conclusions can be made. Generally, toxicological studies are performed on effects of single pesticides and focusing on high contamination levels above the defined MRL. In relation to assessment of a reduced human health risk related to organic food compared to conventional food, it is necessary to assess the risk of pesticide intake below MRL and also to include the cumulative risk related to simultaneous intake of several types of pesticides (cocktail effects) (Hass et al. 2012). Consumption of organic food will minimise the pesticide exposure of organic consumers and may have a positive health impact, though the exact effects are difficult to assess.
Some crops, especially cereals, may be contaminated with mycotoxins, i.e. toxins produced by certain fungi, which amongst other things may cause cancer or endocrine disruption. The risk of finding mycotoxins in organic cereal grains and flour products might be expected to be elevated compared to conventional grains and flour products, because of the non-use of synthetic fungicides in organic agriculture. However, the greatest risk for formation of mycotoxins is connected to the humidity of the grains during harvest, drying and storage, and analyses by the Danish Veterinary and Food Administration have shown that there is no difference in the content of mycotoxins between conventional and organic grain and flour products (Petersen et al. 2013). Studies on oats, barley and wheat in Norway, Poland and the UK confirm these findings, and for some toxins, organic grains had lower content of mycotoxins than conventional (Bernhoft et al. 2010; Blajet-Kosicka et al. 2014; Edwards 2009a, b).
Influence on animal health and welfare
During the period of 2007–2014, the Danish Veterinary and Food Administration analysed 2803 samples of feedstuffs and found pesticide residues in 22% of the samples, of which 66% contained one pesticide, whilst the remaining 34% contained between 2 and 15 different pesticides. In total, 69 different pesticides were found and the pesticide residues were mainly found in feed grains and their by-products, soya bean meal, soya bean hulls and citrus pulp, but in concentrations below the EU limit values for pesticide residues in food products (Fødevarestyrelsen 2015a). The pesticides most often found in the pesticide-contaminated samples were glyphosate and chlormequat (42%, respectively; 30% of the contaminated samples). Therefore, animals consuming conventional plant feed products will most often ingest pesticide residues in the feed. In the Danish 2017–2021 Pesticide Strategy, the spraying of crops with glyphosate later than 30 days before harvest is prohibited in crops for human consumption but this restriction does not apply to crops for animal feed (Anonymous 2017).
The influence of pesticides on animal health and welfare is sparsely documented except for honeybees, which are particularly sensitive to some insecticides. Pesticides are in fact a key factor for explaining honeybee declines; others are pathogens and parasites and lack of suitable feed resources. Sub-lethal amounts of neonicotinoids can cause impaired communication and disorientation and affect the winterisation of healthy colonies, subsequently leading to colony collapse disorder (CCD) (Lu et al. 2014). Most animal feeding studies have been performed as models for human health aspects, but they have generally been aimed at comparing the difference between organic and conventional feeding and not focused on differences in the content of pesticide residues. This has been considered in a two-generation rat study using four experimental feeds produced under controlled conditions using organic (manure) vs. mineral fertiliser and organic vs. conventional plant protection. The study showed no main effects of the differences in crop protection, but a range of significant interactions between differences in fertilisation and crop protection occurred (Srednicka-Tober et al. 2013). Denmark, like other European countries, imports large amounts of protein feed from outside Europe in the form of soya bean products, which are mainly from glyphosate (roundup) resistant genetically modified (GM) soya plants. About 80% of the soya bean meal are used in pig feed, whilst the rest are used for cattle and broilers (Bosselmann and Gylling 2014). Glyphosate is not only a herbicide but also patented as a remedy against parasites, bacteria and other microorganisms. Thus, beneficial bacteria in the gut of animals may be affected by glyphosate that enters the digestive system via the diet, whilst other potentially pathogenic bacteria such as Salmonella sp. and Escherichia coli are less sensitive to glyphosate (Myers et al. 2016; Sørensen et al. 2014). Glyphosate also binds to a wide range of metals, which may lead to deficiencies of trace minerals and result in problems for animals in particularly sensitive phases (weaning, early pregnancy, birth, etc.), where the minerals are essential for several vital body functions. However, until now, too few feeding studies have been carried out with GM soya containing glyphosate residues vs. glyphosate-free non-GM soya in relation to their influence on the gut microbiota and micromineral status of farm animals to draw any conclusions (Sørensen et al. 2014). In the feed of organic animals, it is forbidden to use products of GM plants, but it is allowed as a derogation until the end of 2017 to use up to 5% non-GMO conventional protein feed to monogastric organic animals (EU Reg. 889/2008 amended version). Thus, the risk of finding negative impact of glyphosate residues on the health of organic animals is lower than for conventional animals.
Overview of direct and indirectly derived effects of restricted use of pesticides
In summary, the ban on synthetic pesticides has a number of direct positive effects on different public goods, i.e. on Environment (no pesticides in groundwater and surface water), Nature and Biodiversity (more diverse flora and fauna on and around the farm) and Human and Animal Health and Welfare (pesticide-free food and feed products and no exposure of farm workers to pesticides). Figure 2 presents an overview of the systemic effects of using agro-ecological practices as a response to the non-use of pesticides—and the linked reduced fertiliser use—in organic agriculture.
Besides, there are a number of indirect positive effects on the public goods due to the cropping methods implemented to compensate for the non-use of pesticides, i.e. diversified crop rotation including legumes and perennial clover grass, lower N supply in organic fertilisers, mechanical weeding and protection of natural enemies of pests. Their effects are also positive in relation to several public goods, except for mechanical weeding, which has negative influence on the environment due to increased risk of nitrate leaching and on biodiversity because of disturbance of the microflora and macroflora and fauna. The effect of the ban on synthetic pesticides combined with lower N supply also has a negative effect on the yields in organic farming compared to conventional and hereby on climate change per unit produced, but the opposite is the case per area unit.
Status, legislation and action plans for the use of antibiotics in relation to public goods
Antibiotics are used for treatment or prevention of bacterial infections. They are produced by certain microorganisms (fungi or bacteria/actinomycetes) or they may be of synthetic origin. Antimicrobial resistance (AMR) is the ability of microorganisms to resist antimicrobial treatments, especially antibiotics. Excessive and inappropriate use of antimicrobial medicines for humans and animals and poor infection control practices has transformed AMR into a serious threat to public health worldwide. This has triggered increasing health care costs, prolonged hospital stays, treatment failures and a significant number of deaths and an annual cost of approximately € 1.5 billion for health care and productivity losses in the EU. Infections by multidrug-resistant bacteria are estimated to cause about 25,000 deaths in the EU every year (EMA 2017). In Denmark, the number of persons infected annually with methicillin-resistant Staphylococcus aureus (MRSA) has tripled from 2010 to 2015, where 40% of the 2973 infections were transmitted from animals (Statens Seruminstitut 2017).
The sales of antibiotics to animal producing farms is expressed by means of a Population Correction Unit (PCU). This is applied as a proxy for the size of the food-producing animal population and used for expression of the sales in milligrammes of active ingredient sold per PCU. According to the European Medicine Agency (EMA), the largest amounts of veterinary antibiotic agents sold in 29 European countries in 2014 in mg/PCU were tetracyclines (33.4%), penicillins (25.5%) and sulphonamides (11%) (EMA 2016). There was a large difference in the sales between countries in the range from 3.1 mg/PCU (Norway) to 418.8 mg/PCU (Spain). In Denmark, the sale was 44.2 mg/PCU, and the major part was used for pigs, followed by cattle and poultry. There has been a slight reduction of 2.4% in the amount sold in the EU in the period of 2011–2014. Ten countries including Denmark lowered their sale (in mg/PCU) with more than 5%, whilst there was an increase of more than 5% in five countries during the 5-year period (EMA 2016).
Concerns about development of antimicrobial resistance and transfer of antibiotic resistance genes from animal to human microbiota led to withdrawal of antibiotics as growth promotors in animal feeds in the EU from 1 January 2006, after which date antibiotics are only allowed for veterinary purposes. In the Danish antibiotic resistance surveillance and control programmes, Salmonella sp. was found in 1.3% of the samples from pig caeca (803 pig samples) and pig carcass swabs (15,905 pork samples) in 2015. Of the isolates from pigs, 49% contained Salmonella sp. resistant to at least one antimicrobial agent, whilst this was the case for 50% of the isolates from pork. Campylobacter sp., which is the most commonly reported cause of gastrointestinal bacterial infections in humans in Denmark as well as in the EU, was found in 29% of the samples from broilers and domestically produced broiler meat (286 samples in total), of which 32 and 26%, respectively, were resistant to at least one antimicrobial agent (DANMAP 2015). In 2014, a Danish screening for MRSA, four out of 64 organic pig herds (6%) were tested MRSA positive compared with 68% of the conventional pig farms (Fødevarestyrelsen 2015b).
In 2011, the European Commission passed its first Action Plan against the rising threats from antimicrobial resistance (COM 2011), and in 2017, the commission will launch a second Action Plan including securing EU funds and instruments in order to promote innovation and research against AMR through National Action Plans. According to an opinion paper prepared jointly by EMA and the European Food Safety Agency (EFSA) for the European Commission, measures to reduce antimicrobial use and AMR in animal husbandry should focus on the principles of ‘reduce, replace and rethink’ (EMA and EFSA 2017). Of these, the following recommendation is particularly interesting in relation to organic farming and its potential role as model: ‘rethinking the livestock system by implementing farming practices that prevent the introduction and spread of disease’.
In 2014, the Danish cattle industry set a target for antibiotic use of 20% reduction for the period of 2010–2018, and in 2015, the Danish pig industry set a 10% reduction target for the period of 2015–2020 (DANMAP 2015). These initiatives were followed by adoption of a 4-year National Action Plan for control of MRSA in farm animals in 2015 (Anonymous 2015), according to which the following initiatives were to be implemented: a 15% reduction of the consumption of antibiotics in pig production from 2015 to 2018, improved hygiene for staff working in pig stables, reduction of infection transmission in the individual farms, program for surveillance of the development of animal AMR/MRSA and strengthening of research in transmission routes for animal MRSA and international initiatives—including putting pressure to promote the antibiotic strategy of the EU.
Relevant organic principles and legal requirements
According to Council Regulation (EC) 834/2007, Article 5, the main principles for organic animal production in the EU is that ‘Animal health shall be maintained by encouraging the natural immunological defence of the animal, as well as the selection of appropriate breeds and husbandry practices’. This means that ‘animal husbandry practices shall be applied, which enhance the immune system and strengthen the natural defence against diseases, in particular including regular exercise and access to open air areas and pastureland where appropriate’.
A number of specific requirements to organic livestock farmers are related to the prevention of needs for medication such as Articles 19–22 (in EU Reg. 834/2007), which specify longer weaning periods for organic animals compared to conventional, maximum use of grazing pasture, daily feeding of roughage to all animals and minimum 60% roughage for herbivores. Likewise, Halberg et al. (2008a, b) specify that the livestock shall have permanent access to open air areas when conditions and weather permit this and that ‘stocking densities and housing conditions shall ensure that the developmental, physiological and ethological needs of animals are met’. Thus, the space requirements per animal are considerably larger for organic compared with conventional animals, and other conditions, e.g. light, daily access to roughage, weaning age and other factors that are important for animal health and welfare, are also stricter.
Other articles deal with disease prevention and specify that preventive treatment with allopathic veterinary medicine including antibiotics is forbidden, except for vaccination of animals. Moreover, growth promotors and synthetic amino acids cannot be used. On the other hand, the regulation stress that when ill, livestock should in fact be treated immediately to avoid their unnecessary suffering, and ‘chemically synthesised allopathic veterinary medicinal products including antibiotics may be used where necessary and under strict conditions when the use of phytotherapeutic, homoeopathic and other products is inappropriate’ (Article 14). As a precautionary measure, the withdrawal period for animals treated with chemically synthesised allopathic medicine including antibiotics is twice the legal withdrawal period for conventional animals. Animals, which have been treated with allopathic medicine including antibiotics more than three times within 12 months, or more than once, if their productive life cycle is shorter, may not be sold as organic, neither live nor as food products.
Contribution of organic farming to public goods due to very restrictive use of antibiotics
In general, the design and management of organic livestock systems reflect the emphasis on prevention of diseases and promotion of the health of organic animals by good housing standards including hygiene, feeding according to the needs of the animal species and age groups with daily provision of roughage for all species, later weaning plus outdoor access and grazing when the weather permits. The health-promoting measures and management practices applied to reduce or avoid the need for antibiotic treatment of organic farm animals are analysed in relation to each of the public goods in more detail below:
Influence on nature and biodiversity
Antibiotic residues from treated livestock are often present in their manure and hereby transferred to the soil where the residues may influence biodiversity through selective effects on microbiota and insects. The presence of antibiotic resistant microorganisms in the soil may be a consequence of certain antibiotics in the manure applied to the soil (Graham et al. 2016; Jechalke et al. 2014). Jechalke et al. (2014) reviewed a number of studies, demonstrating that antibiotics entering into agricultural soil via manure can affect the soil microbial community—and in particular the abundance, diversity and transferability of resistance genes in the short term. Ollivier et al. (2013) found that application of manure from sulfadiazine-treated pigs affected the abundance and diversity of nitrifying microbes in the soil, and led to a decrease in ammonia-oxidising bacteria and an increase of ammonia-oxidising archaea.
The results are varied however; negative (Bartiková et al. 2016) as well as no effects (Baguer et al. 2000) have been reported for environmentally relevant antibiotic concentrations, and it has been argued that focus on effects on non-target microorganisms is needed (Brandt et al. 2015). Recent studies have shown that antibiotics may significantly affect the microbiota in dung and dung beetles negatively (Hammer et al. 2017). In Denmark, more than half (57.1%) of the dung beetles are listed on the Danish Redlist (Department of Bioscience 2017), and one of the reasons for this may be the extensive use of antibiotics for livestock. Therefore, soil biodiversity may benefit from the very restrictive use of antibiotics in organic farming.
Until now, only a few studies have considered the effects on non-target organisms of antibiotic resistant bacteria in manure from medically treated animals. The presence of manure borne AMR microbes diminish relatively soon after the application is stopped. Marti et al. (2014) found in a field study with plots cropped with vegetables and fertilised with pig or dairy manure that under conditions characteristic of agriculture in a humid continental climate, a 1-year period following a commercial application of raw manure is sufficient to ensure that an additional soil burden of antibiotic resistance genes approaches background. They therefore recommended pre-treatment by, e.g. composting of the manure before application. Antibiotics and AMR genes occur naturally in soil as almost 50% of Actinomycetes isolated from soil are capable of synthesising antibiotics for competition reasons, which provide a natural content of antibiotic residues in the soil (Popowska et al. 2012). The use of antibiotics as feed additives for growth promotion in conventional husbandry was prohibited from 2006, but copper (Cu) and zinc (Zn) are still used as feed additives in high amounts. In some cases, they may exert a stronger environmental selection pressure for resistance to antibiotics of the soil microbiota than the specific antibiotic itself (Song et al. 2017).
Influence on environment
Besides the mentioned effects on biodiversity in and above soils, the main environmental consequences of organic livestock production are ammonia loss and risks of eutrophication due to the wider requirements for feeding and housing livestock, which are linked to the focus on antibiotic prevention. The requirements for outdoor access, roughage and organic feed together with avoidance of synthetic amino acids lead to higher feed use per produced kg pig and chicken meat and higher protein N content per kg feed (Halberg et al. 2010; Larsen et al. 2000; Olsson et al. 2014). This leads to higher risks of losing nitrogen through ammonia volatilisation and leaching especially from manure droppings on concrete outdoor runs, respectively, in the fields where sows roam. Moreover, the larger space requirement and floor design indoors may also lead to a higher ammonia emission, and according to Olsson et al. (2014), higher ammonia emission is typically seen in organic pig and poultry production compared to conventional production.
There is a higher N leaching from organic pig production compared with conventional per ha and per kg pig produced (Halberg et al. 2010; Larsen et al. 2000) mainly caused by the high manure N load on fields with outdoor sows, especially from feeding and soiling spots (Eriksen 2001) resulting in low N use efficiency in the following crops.
In organic egg production, there is a requirement for outdoor runs (e.g. 4 m2 per hen in EU, 8 m2 per hen in Denmark) but no requirements for removing the nutrients from hen droppings through harvesting of crops in intermediate periods. This creates a risk of nitrate leaching from the outdoor runs (Hegelund et al. 2005), which needs to be reduced by planting and harvesting certain crops such as willow which may provide shelter for hens and be used for bioenergy purposes (Steenfeldt 2015).
In dairy production, analysis of nutrient balances on farms in combination with nitrate leaching measurements have established that under Danish conditions with a maximum of 1.4 livestock units per ha in organic dairy farms, the leaching is considerably lower (30–40 kg N less per ha) compared to conventional dairy farms (Kristensen and Hermansen 2008; Nielsen and Kristensen 2005).
Influence on energy use and climate change
The restricted use of antibiotics in organic animal husbandry indirectly influences the use of energy and emissions of greenhouse gasses in organic compared to conventional livestock production due to the mentioned management requirements aiming at improving health and welfare in order to avoid treatments. Thus, the differences between farming systems are mainly caused by the same factors as related to nutrient management (see section on Environment), especially the increased feed use in organic livestock production.
The emission of the GHG nitrous oxide (N2O) and methane (CH4) is mainly related to livestock production, which in Denmark is dominated by cattle and pigs (DCE 2016). GHG emission per kg livestock product was almost identical in organic and conventional systems for pig meat (Halberg et al. 2010) and milk (Halberg 2012; Kristensen et al. 2011). Knudsen (2011) in a review found that GHG emission from organic milk production was 10–20% lower in six of ten comparative studies. However, the variation between farms is high, and Kristensen et al. (2011) found that variation in feed use efficiency caused some organic farms to have higher GHG emissions than most conventional whilst others had lower. There are methodological difficulties in accounting for (differences in) the soil carbon sequestration in such comparisons, but modelling studies suggest that inclusion of this factor would decrease the net GHG emissions more per kg pork or milk produced in organic than in conventional systems (Halberg et al. 2010). In Danish experiments, conventional grass fields and organic clover grass fields have been estimated to sequester about 1000 kg carbon (C)/ha annually (Christensen et al. 2009; Schjønning et al. 2012). Because of the larger share of clover grass fields in organic crop rotations, the carbon sequestration is probably in average higher in organic agriculture than in conventional.
Influence on human health and welfare
Antimicrobial resistance is recognised as an important threat to human health. The mentioned regulation of antibiotics use in organic farming and restrictions on marketing of products after medication considerably reduce the risk of finding antibiotic residues in organic animal products delivered to dairies and slaughterhouses. Because the use of antibiotics in organic animal production is low compared to conventional production (Wingstrand et al. 2010; see also next section), there is a lower occurrence of antimicrobial resistance in bacteria isolated from organic production animals (Rosenquist et al. 2009). Low use of antibiotics also provides less risk of mistakes in the production chain, e.g. incorrect delivery of milk to the dairy from antibiotic-treated cows or slaughter of pigs with antibiotic residues. In relation to risks or health benefits for the consumer, it is important that the improved quality is maintained throughout the production chain. Unfortunately, a European study of organic pork production from several countries (France, Sweden and Denmark) showed that the significant differences in the level of antimicrobial resistance observed at herd level (Österberg et al. 2016) seemed to disappear after slaughter and handling of the meat (Jensen and Aabo 2014). This negative change implies cross contamination and may be handled through improved hygiene and management, although the mechanism behind this observation is not yet clear.
As an indirect effect, the requirements for feeding and access to grazing for organic livestock result in differences in the composition of fatty acids in organic milk and eggs compared with conventional. The proportion of healthier fatty acids is more favourable to humans in organic eggs and milk compared to conventional (Anderson 2011; Larsen et al. 2014; Shapira 2010; Schwendel et al. 2015), although studies demonstrating the actual effect on human health are lacking.
Influence on animal health and welfare
The use of antibiotics and the antibiotic resistance is significantly lower in organic pig production compared to conventional (Wingstrand et al. 2010). The reduced use of antibiotics in organic pig production could be due to differences in treatment thresholds in the two production systems, and the lower application of antibiotics in organic pig production could indicate a welfare problem if diseased animals are not treated or treated too late. However, the mortality rate for sows and slaughter pigs in Denmark is not higher in organic than in conventional production (Sørensen 2015). The level of lesions found at meat inspection is higher for some lesions in organic production than in conventional indoor production (Kongsted and Sørensen 2017), but this does not seem to be linked with under-treatment because the level of lesions in conventional outdoor pig production, having the same antibiotic treatment regime as in conventional indoor pig production, is similar to organic pig production. The difference in the level of lesions therefore seems more related to differences in the production system than to differences in the veterinary treatment regime. The piglet mortality rate is higher in organic than in conventional pig farms, which is linked with the requirements for outdoor rearing (Sørensen and Pedersen 2013).
The consumption of antibiotics in the production of 1 kg of organic milk is only about two thirds of the consumption for the production of 1 kg conventional milk (Bennedsgaard et al. 2010). Research has shown that a determined effort in Danish organic dairy herds can reduce the use of antibiotics even further (Bennedsgaard et al. 2010; Ivemeyer et al. 2011). In a recent review, Arnott et al. (2017) concluded that pasture-based systems, such as organic milk production in general, provide better animal welfare to dairy cows than indoor-based systems. They found lower levels of lameness, hoof pathologies, hock lesions and mastitis in organic dairy cows than in conventional, which evidently would explain the lower medicine use. Pasture-based systems therefore seem to reduce the need for antibiotic treatments. The lower antibiotic use did not increase the mortality rate of calves which was between 7 and 8% in organic and conventional dairy herds in 2016 (Raundal et al. 2017). In a Danish study comparing 15 organic and conventional dairy herds, Reiten (2014), however, found a higher level of diarrhoea but a lower level of respiratory diseases in organic calves compared to conventional calves of 0–6 months.
Previous studies have shown that many organic farmers emphasise active care treatment (Vaarst et al. 2003). Focus on animal care, such as assigning hospital pens with extra bedding and extra milking, promote the welfare of diseased animals. The veterinarian’s experience with the herd-specific conditions on organic livestock farms with very restrictive use of antibiotics is important for the prevention and control of diseases. However, often, the veterinarians do not have sufficient experience in facilitating health management on organic livestock farms with a low use of antibiotics (Duval et al. 2016). The duration of antibiotic treatment in organic cattle herds is shorter than in conventional cattle herds. It may be because all medical treatments in Danish organic animal production must be administered by a veterinarian, and therefore, it is more expensive than in conventional animal production, where the farmer is allowed to administer the follow-up treatment himself on the condition that he has a health advisory agreement with a veterinarian. Bennedsgaard et al. (2010) showed that mastitis was treated on average three times in conventional herds where the farmer had a health advisory agreement, whilst in organic herds and herds without a health advisory agreement, the antibiotic treatment was only 1.5 times on average. A shorter duration of treatment may result in a lower bacteriological curing rate and hereby an increased risk of recurrence and development of antibiotic resistance. However, Bennedsgaard et al. (2006) found no differences in the incidence of penicillin-resistant S. aureus in the milk from cows with high somatic cell counts in organic and conventional dairy farms in Denmark.
Combating of antibiotic resistance in animal production requires not only a reduction in the use of antibiotics but also a better understanding of the effects of Zn and Cu supplementation in animal diets in relation to antibiotic resistance. Resistance to Zn is often linked with resistance to methicillin in staphylococci, and Zn supplementation to animal feed may increase the proportion of multiresistant E. coli in the gut. Resistance to Cu in bacteria, in particular enterococci, is often associated with resistance to antimicrobial drugs like macrolides and glycopeptides (e.g. vancomycin) (Yazdankhah et al. 2014). The maximum content of Zn and Cu in the feed is regulated by EU legislation that applies to conventional as well as organic husbandry. However, for some age groups, the limits herein are too high compared to the need of the animals, and this is particularly true for organic monogastrics that in contrast to conventional monogastrics get a considerable part of their feed from outdoor areas (EGTOP 2015). Already more than 10 years ago, DG Sanco Scientific Committee (2003) stated that the high level of 170-mg Cu/kg feed authorised for piglets not only covers their nutritional requirement but also act as an efficient growth promotor. In 2016, EFSA proposed a lowering of the maximum Cu contents for piglets from 170- to 25-mg Cu/kg complete feed (EFSA 2016), and the same year, the maximum content of Zn in mg/kg complete feed was lowered for several animal species (COM 2016).
Overview of direct and indirectly derived effects of restricted use of antibiotics
In summary, the restrictive use of antibiotics in organic livestock production has some direct positive effects on the public goods, i.e. on Human Health and Welfare (less antibiotic residues and antibiotic resistant bacteria in animal food products) and Nature and Biodiversity (avoiding negative effects on the composition of the soil and manure microbiota and insects). Moreover, the required management practices aimed at securing livestock health and welfare and preventing medicine needs impact animal health, environment and climate emissions (Fig. 3).
More space outdoors and access to grazing contribute positively to Human Health and Welfare, because the animal products have a healthier fatty acid composition due to grazing. However, these requirements result in both positive and negative effects on the Environment. Leaching of nitrate is lower on organic dairy farms due to larger areas with clover grass fields and lower stocking rates, but ammonia volatilisation and nitrate leaching are higher on organic pig and poultry farms.