Global pressures, such as climate change and population growth, require that agricultural production must increase with less negative environmental and climatic effects. Globally, winter wheat is one of the main crops for food security (Shiferaw et al., 2013), and in Germany, it is the most grown crop, producing very high yields in intensive production systems (BMEL, 2021; FAOSTAT, 2021). Such an intensification of agriculture has effects on the environment and land use. Due to the potential production losses by pests and diseases (Savary et al., 2019), plant protection chemicals are a part of winter wheat management. Therefore, the production of wheat has special importance regarding the implementation of integrated plant protection. Also, there are political and societal pressures to reduce the use of synthetic plant protection for this crop. The most recent incorporation of these pressures is the strategy, From Farm to Fork, which is a cornerstone of the European Green Deal, released recently by the European Union. It states that by 2030, chemical pesticides shall be reduced by 50%. Also, the German National Action Plan on the Sustainable Use of Plant Protection Products intends to reduce plant protection applications to the necessary minimum that secures economic cultivation of crops. Due to these reasons, it can be expected that the spectrum and quantity of available substances for plant protection will be strongly reduced in the future (Schwarz et al., 2018) and this will have great effects on managing pathogens.

Crop resistances also play a crucial role in disease management. Plant breeders constantly develop newer and better varieties to assure or increase agricultural production and safeguard our food security. Plant breeding has upheld and improved winter wheat production even under reduced input conditions (Voss-Fels et al., 2019). It is well-understood that a large determinant in the rise of yield levels in Germany was genetic gains by plant breeding and that this breeding-induced yield increase is not stagnating (Ahlemeyer and Friedt, 2010; Laidig et al., 2014; Voss-Fels et al., 2019). New varieties have accumulated genetic variants with beneficial effects on the important yield enhancing traits, such as nutrient use and photosynthetic efficiency as well as disease resistance (Voss-Fels et al., 2019; Zetzsche et al., 2019, 2020). Over time, variety aging decreases the yield ability of varieties and is mainly induced by a steady breakdown of resistances due to pathogen evolution (Mackay et al., 2011; Fischer et al., 2014; Laidig et al., 2014; Piepho et al., 2014). Therefore, continued breeding for resistance is the key to uphold or increase the yield quantities and qualities.

Among the diseases causing losses in winter wheat production, pathogenic fungi are very dominant (Russell, 2013; Simón et al., 2021). Consequently, fungicides are the most used category of plant protection products in winter wheat production systems in Germany, regarding application rate and treatment frequency (Roßberg, 2016). Single fungal pathogens can cause yield losses of up to 70% in susceptible varieties (Zetzsche et al., 2020). In recent decades, the use of fungicides and the increasing cultivation of resistant varieties have prevented devastating epidemics in Europe (Hovmøller and Justesen, 2007; Dubin and Brennan, 2009; Singh et al., 2016; Figueroa et al., 2018), while genetic resistances are said to be the most effective and sustainable approach (Ghimire et al., 2020). In the history of breeding, genetic resistance against rusts and powdery mildew have been the most successful (Singh and Rajaram, 2002). Resistant varieties, as part of integrated disease management, can contribute to reducing the use of chemical synthetic plant protection (Schwarz et al., 2018). In Germany, contrary to the continuously increasing resistance levels of new varieties, the treatment frequency and intensity of fungicides augmented slightly over time between 2011 and 2017, a trend that was influenced by disease-promoting weather conditions and by a focus of producers on yield protection (Roßberg, 2016; Kehlenbeck, 2018).

Given this background, it is vital to better understand the economic effect of the increased resistance of the varieties to fungal pathogens. According to Marasas et al. (2003) and Nalley et al. (2010), research that analyzes the economic impacts of breeding programs often overlooks the important aspect of breeding for resistance, which has the goal to maintain high yields and quality levels. In addition, a large part of the research that addresses the subject focuses on the impact of specific breeding programs in developing countries, where cultivation is less intensive (Smale et al., 1998; Marasas et al., 2003; Dixon et al., 2006; Dubin and Brennan, 2009; Nalley et al., 2010; Lantican et al., 2016). Also, analyses for intensive cropping systems have found that the cultivation of resistant varieties is a major, cost-efficient, effective, and ecological technology to control diseases (Clifford and Lester, 1988; Hogenboom, 1993; Wiik and Rosenqvist, 2010; Hysing et al., 2012; Russell, 2013; Thompson et al., 2014). Nevertheless, the breeding of resistant varieties and further the exploitation of these resistances in practice poses difficulties due to potential risk aversion, insufficient information on the variety, high inter- and intra-annual variability in disease pressures, and other factors (Clifford and Lester, 1988; Russell, 2013; TeBeest et al., 2013). Yet, Hogenboom (1993) anticipated that new innovations in resistance breeding will increase the economic value of this method to manage diseases. Due to limited variety-specific data availability and trials, these analyses face the difficulty to approximate the pure breeding effect on yield and other parameters as well as the resulting economic impacts. In Germany, the economic assessment of different cropping systems with a special focus on disease resistance measured the economic effect of a small set of selected winter wheat varieties and showed that the resistant varieties have a high potential to reduce fungicide applications and consequently reduce costs (Kehlenbeck and Rajmis, 2018; Klocke et al., 2018; Rajmis and Kehlenbeck, 2018; Sommerfeldt, 2018).

To the best of our knowledge, so far, there is no microeconomic transformation of variety-specific resistances, purely induced by breeding, in a region where wheat is grown intensively, such as in Germany. Our research aims to contribute to closing this research gap by answering the following question: In the last 50 years, what has been the effect of resistance breeding on winter wheat gross margins in Germany? We chose Germany as a representative country in central Europe where winter wheat dominates and achieves very high yields (BMEL, 2021) due to good soils, sufficient precipitation, and moderate winters. Moreover, winter wheat breeding for this target environment is also quite intensive and competitive. We are the first to perform an economic analysis of resistance breeding with field-experimental data comprising ~180 old and new varieties cultivars that represent the most important German winter wheat varieties of the last 50 years (Voss-Fels et al., 2019; Zetzsche et al., 2020). This allows us to monetize the sole breeding-induced effect of increased resistances, without any masking effects from other production factors, and also reduces the statistical bias which can arise when only a few preselected varieties are analyzed.

Based on the trial data, we can compare the performance of varieties in treatments with and without fungicide applications, and with the help of the latter, we can deduct the impact of resistance breeding. We hypothesize that under treatments without fungicides, resistant varieties achieve higher yields than the less resistant varieties, as they withstand the fungal pathogens without external disease management while maintaining yield quantity and quality. Consequently, we assume that varietal resistances increase gross margins in winter wheat productions, as they secure or increase yields, in the absence of fungicide applications, which are costly due to their product and application costs.

To test these hypotheses, we estimate variety-specific gross margins and then employ regression and post-estimation analyses. These methods and the underlying data are explained in section Materials and Methods. In section Results: Effect of Resistance Breeding on Winter Wheat Gross Margins, we describe the results which are discussed in section Discussion.

Breeding varieties with increased resistance to fungal pathogens is an integral part of plant breeding programs and it was an important goal of the last 50 years of winter wheat breeding around the world, and also in Germany. Such breeding ties up monetary and human resources and yet, so far, the microeconomic impact of resistance breeding has not been analyzed with a field-experimental data set which covers 50 years of breeding progress and which enables us to isolate the purely breeding-induced effect. Our research contributes to filling this research gap. We show that breeding for resistances has created large positive economic effects on winter wheat production in Germany. The results of the regression models show that resistance breeding had a largely positive and statistically significant effect on the microeconomic target variable gross margin (Tables 3, 4; Figures 1, 2). The strong and statistically significant effect of the year of release indicates that younger varieties are more profitable as they contain breeding-induced innovations, which older varieties lack on average. The effect of the resistances to individual fungal pathogens showed that rusts and Fusarium resistances had the largest effect on the economic profitability of the varieties. Confirming our hypothesis, the validation models including the agronomic management variables, show that fungicide applications had a statistically significant and large negative effect on the gross margin of a specific variety. This is due to the high costs for fungicide products and their application. These results indicate that a careful choice of resistant varieties can be more profitable than applying a full dosage of fungicides or high levels of nitrogen. Similarly, high nitrogen fertilization has a negative impact on economic performance. This was true even though in the trials, nitrogen (N) application was reduced to the necessary minimum, which means that in comparison to an average location of German winter wheat cultivation, nitrogen application was low. Due to the given high N-supply capacity of the soil at the trial site, the statements regarding the economic efficiency of the N-fertilizer application cannot be transferred to all sites. On other soils with a lower N-supply capacity, a higher economic efficiency of the N fertilization can be assumed. Appropriate fertilizer management is also important for reducing the disease intensity depending on the nutritional habit of the present pathogen (Simón et al., 2020). Overall, the trial year had a significant effect on the gross margin. As the management and input use are the same across varieties of a certain treatment, this can be explained by the different meta-environments prevailing during each trial year. During the trials, production was mainly limited by the plant-available water during late spring and summer. According to the soil moisture, 2016, the reference year in the models, was the least dry year. In 2015, soil moisture was 29.3%, in 2016 it was 31.0%, and in 2017, it was 29.1%. Hence, during the first and last trial years, plants had to cope with strong drought stress (Zetzsche et al., 2020). Moreover, drought periods need to be considered when interpreting the effects of fertilization, as they caused some fertilizer to remain undissolved so that the effect of fertilization was limited or delayed in these years.

The regression results are backed up with the results of the post-estimation analyses. These show that the gross margin increased over the decades (Figure 3; Table 5) and also with the increased breeding-induced leaf and spike health (Table 6). Furthermore, the difference between fungicide-treated and untreated winter wheat cultivation decreased over time due to increased plant health (Table 5; Figure 4). This underlines that resistant varieties are also profitable without disease management and under biotic pressures from fungal pathogens. The peaks in 1986 and 1996, as well as the strong drop down in 1991 visible in Figure 3, are caused by single varieties with particular behavior that were released in this year. The subset of popular winter wheat varieties (Table 7) shows that on average, the gross margin of more resistant varieties decreases with fungicide applications. Even though the yield and protein contents of the resistant varieties increase slightly with applications, this yield and protein-boosting effect is not large enough to compensate for the high fungicide costs. In general, the trial produced above-average protein contents due to the prevailing dry conditions.

Usual gross margin calculators include the standard gross margin categories revenue, which is influenced by yield quantity, quality, and the producer price, as well as the variable costs of production for inputs, labor, etc. (KTBL, 2020; Mußhoff and Hirschauer, 2020; LfL, 2021). Due to the trial setup and economic analysis method, our variety-specific gross-margin calculations allow us to assess the microeconomic effect of the last 50 years of breeding for resistance to fungal pathogens. Studies on winter wheat found that the continued innovation of breeding in Germany has created higher-yielding crops, which are more resistant and stable across environments and treatment variants (Voss-Fels et al., 2019; Zetzsche et al., 2020). Our research shows that this positive yield effect has translated into increased profitability of more resistant varieties.

The results show that due to their high costs, fungicide applications have a negative effect on the gross margin and that the gross margin-enhancing effect of a full fungicide rate has been diminishing over time. The profitability of fungicide applications depends on many factors: weather conditions, and corresponding disease intensity as well as risks, the efficacy of the applied active ingredients, application costs and rates, timing, agronomic management, the current wheat price, and the variety-specific resistance (Wegulo et al., 2011). Wegulo et al. (2011) conclude that foliar fungicide treatments can be profitable in years with moderate to high disease severity but can be unprofitable when fungicides are used in years with low disease severity. In line with our results, Weisz et al. (2011) found that the costs of the fungicide application need to be offset by yield gains induced by these applications. Therefore, routine applications solely based on the wheat growth stage or general experience are only profitable if such a yield gain is achieved (Weisz et al., 2011). However, when diseases are present, the likelihood that application costs and benefits break even or that benefits outweigh the costs increase (Weisz et al., 2011). In Germany, farmers increasingly plant winter wheat varieties with broad resistances to diseases; nevertheless, the fungicide application intensity in fields planted with such varieties is not significantly different from those planted with less-resistant varieties (Dachbrodt-Saaydeh, 2018). This indicates that the gross margin-enhancing potential of resistant varieties is generally not realized in practice. Weather and other factors, such as available labor and machinery as well as rules and regulations, influence the decision of an operating farm to apply or not apply fungicides (Dachbrodt-Saaydeh, 2018). Analyzing operating farms in Germany, the majority of situation-specific fungicide applications are economically superior to general applications, as farm businesses can save on product and application costs (Kehlenbeck and Rajmis, 2018). In particular, less application can save the overall costs for disease management. Depending on the weather and disease conditions, modern, resistant varieties can allow for some fungicide applications to be skipped within the season and therefore save product and application costs. As described, knowledge of the farmers and their options to allocate farm resources for disease monitoring and other practices are relevant. The high application costs for fungicides can be avoided by not applying fungicides when the variety- and site-specific damage thresholds are not surpassed. This implies using locally adapted disease management systems that adjust according to yearly and local variations in disease intensity (Jalli et al., 2020).

Despite the breeding progress, the results also show that, on average, the grain yield performance was always superior when applying fungicides. Hence, under certain conditions, fungicide applications can be beneficial for increasing yields, also if plants with higher resistance levels are sprayed. This was also found by other trials where the yield advantage highly depended on yield potential, location, and disease conditions of the varieties (Thompson et al., 2014). One explanation for this finding is a possible preventive effect of applying fungicides before a specific fungal pathogen is present. This option can be influenced by the application timing and the applied active ingredients which usually target several pathogens and not only the pathogen for which a damage threshold was surpassed. This preventive effect can decrease plant stress, delay senescence, or prolong the green leaf area retention and hence create plant health and economic benefits (Bertelsen et al., 2001; Wu and von Tiedemann, 2001; Zhang et al., 2010; Wegulo et al., 2011; Berdugo et al., 2012; Lopez et al., 2015). Recent literature analyzing new groups of fungicides reported that apart from the protective attributes of fungicides, they can also positively alter plant physiology so that grain yield and other traits improve (van Dingenen et al., 2017; Amaro et al., 2020). Along with farm resource allocation, these findings can partly explain why some farmers tend to spray fungicides rather as a preventative measure than according to variety- and site-specific disease risks (Rajmis and Kehlenbeck, 2018). Also, plant injuries caused by fungicide applications do not seem to have a yield-decreasing effect (Robinson et al., 2013) that could influence the economic profitability of the crop. Some studies conclude that the profitability of fungicide applications depends on the grain price; hence applications are unprofitable in years with low prices and in particular, when the host plant is resistant (Wiik and Rosenqvist, 2010; Wegulo et al., 2011; Hysing et al., 2012; Thompson et al., 2014). Also, an analysis of 25 years of winter wheat cultivation in southern Sweden found that the average net return from fungicide applications was not more than 12 EUR ha⁻¹, and was even negative in 10 years (Wiik and Rosenqvist, 2010). Contrary to our findings, fungicide treatments were more profitable in the latter part of the trial period from 1995 to 2007 (Wiik and Rosenqvist, 2010). Modeling the fungicide choices of farmers, TeBeest et al. (2013) conclude that in years with high disease severity too low doses of fungicides can result in a net loss; therefore, risk-adverse farmers prefer to apply a high fungicide dosage as insurance to avoid such losses.

It is no surprise for agronomists that the specific meta-environment or weather during the field trials decisively impacted the variety-specific gross margins. Albers et al. (2017) estimated that 43% of the total actual wheat yield volatility is driven by weather. The authors also estimated that 49% of the yield volatility is driven by inputs. Our results indicate that the meta-environment had a much larger impact on the gross margin than inputs. This can be explained by the strong water-stress conditions during the trial years.

A combination of resistant varieties, intensive inventory scoring, and independent consultation is necessary to reduce fungicide applications and decrease the risks thereof (Helbig et al., 2018). Farmers need more actionable, accessible, and affordable information on the resistance traits of varieties along with current weather conditions and subplot specific pathogen risk. Digital farming and data analysis tools, such as non-uniform, sensor-controlled spraying (Tackenberg et al., 2018), can help to pursue site- and variety-specific fungal disease management, while optimizing the farm resource allocation (labor, machinery, etc.). Such tools must be adapted in such a manner that they are profitable for farmers and yet facilitate the achievement of certain standards. Therefore, it is also necessary to better understand the spraying decisions of farmers and what factors influence them. The described positive impacts of resistance breeding on winter wheat production gross margins can be further increased by practitioners, who pair a good variety selection with variety-, pathogen-, and site-specific management. This implies that less fungicide could be applied. Fungicide use could be reduced by only treating the pathogen present on a specific variety and on a specific plot. This way, the resistances of a variety to other pathogens can be exploited, which could imply that no further gross-margin decreasing applications are necessary.

Our analysis is the first to calculate the microeconomic effect of resistance breeding for such a large and historical set of 176 varieties for which we can compare the important traits of grain yield, protein content, plant health, and the resulting gross margin. All varieties received the same variants of agronomic management and growing conditions, which enables us to single out the sole breeding-induced economic effect of breeding for increased resistance to fungal pathogens. Our findings are also relevant for other regions in the world as new and more aggressive strains of pathogens, such as stripe rust are distributed around the world (Carmona et al., 2020). Therefore, international collaboration is needed to sustain the quality and quantity of wheat production and assuring profitable production methods for farmers. Future work on the economics of resistance breeding for wheat could set up trials at locations that differ in their soil conditions, and apply variety-, pathogen-, and site-specific fungicide treatments. Such fungicide application trials could further increase the economic effect of the resistance of varieties. To assure the availability of agricultural innovations, such as more resistant varieties, regulatory reforms, and a public debate with more focus on scientific evidence is needed (Qaim, 2020).

This analysis provides compelling evidence that resistance breeding has created large positive effects on the profitability of winter wheat production. Therefore, for farmers, an optimal choice of resistant varieties can be highly profitable with regard to the gross margin of winter wheat production. Resistances can help decrease input use while producing high-yield quantities and qualities. The use of resistant varieties additionally contributes to climate protection by reducing the carbon footprint of the energy-intensive production of synthetic agrochemicals. Thus, the use of fungicides at full rates is not forward-looking when varieties are carefully chosen and cultivated, neither from an economic nor an environmental perspective. Social and political as well as climatic and ecological pressures make it clear that agricultural producers, stakeholders along the value chain, and policymakers must consider other target indicators, such as minimizing external environmental costs, apart from profit maximization. As wheat is a major staple food around the world, our findings show that resistance breeding can contribute to achieving the United Nations Sustainable Development goals. It can help reduce the poverty levels of wheat-producing farmers while decreasing hunger through larger product quantities and better qualities. It can also enable climate action and improve life on land by reducing potential negative environmental effects of intensive agricultural systems and reducing the pressure on land. Also, the German National Action Plan for Plant Protection intends to reduce fungicide applications to the necessary minimum. This target can be achieved with the support of healthier varieties. Therefore, resistance breeding creates benefits at the farm level and beyond.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

SL organized and contributed to the research conceptualization and design, data gathering and analysis, and also wrote and edited the manuscript. HZ, BW, AS, and OM contributed to the research conceptualization and design, data provision, and analysis as well as manuscript editing. FO lead the project, whose data was used for the here presented research, and edited the manuscript. All authors contributed to the article and approved the submitted version.

This work was supported by the Federal Ministry of Education and Research (BMBF Grant No: 031A354 E and F). We acknowledge support by the German Research Foundation (DFG) and the Open Access Publication Fund of Humboldt-Universität zu Berlin.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.