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A better use of fertilizers is needed for global food security and environmental sustainability

A better use of fertilizers is needed for global food security and environmental sustainability The massive use of fertilizers during the last decades allowed a great increase in the global capacity of food produc- tion. However, in the last years, several studies highlight the inefficiency and country asymmetries in the use of these fertilizers that generated environmental problems, soil nutritional imbalances and not optimal food production. We have aimed to summarize this information and identify and disentangle the key caveats that should be solved. Inadequate global management of fertilization produces areas with serious nutrient deficits in croplands linked with insufficient access to fertilizers that clearly limit food production, and areas that are overfertilized with the consequent problems of environmental pollution affecting human health. A more efficient use of nitrogen (N), phosphorus (P) and potassium (K) fertilizers for food security while preserving the environment is thus needed. Nutrient imbalances, particularly the disequilibrium of the N:P ratio due to the unbalanced release of N and P from anthropogenic activi- ties, mainly by crop fertilization and expanding N-fixing crops that have continuously increased the soil N:P ratio, is another issue to resolve. This imbalance has already affected several terrestrial and aquatic ecosystems, altering their species composition and functionality and threatening global biodiversity. The different economic and geopolitical traits of these three main macronutrient fertilizers must be considered. P has the fewest reserves, depending mostly on mineable efforts, with most of the reserves concentrated in very few countries (85% in Morocco). This problem is a great concern for the current and near-future access to P for low-income countries. N is instead readily available due to the well-established and relatively low-cost Haber–Bosch synthesis of ammonium from atmospheric N , which is increasingly used, even in some low-income countries producing an increasing imbalance in nutrient ratios with the application of P and K fertilizers. The anthropogenic inputs of these three macronutrients to the environment have reached the levels of the natural fluxes, thereby substantially altering their global cycles. The case of the excess of N fertilization is especially paradigmatic in several areas of the world, where continental water sources have become useless due to the higher nitrate concentrations. The management of N, P and K fertilizers is thus in the center of the main dichotomy between food security and environmentally driven problems, such as climate change or eutrophica- tion/pollution. Such a key role demands new legislation for adopting the well-known and common-sense 4R princi- ple (right nutrient source at the right rate, right time and right place) that would help to ensure the appropriate use of nutrient resources and the optimization of productivity. Keywords Fertilizers, Food security, Environmental security, Nitrogen, Phosphorus, Potassium, Imbalance, Stoichiometry, Eutrophication, Global cycles Introduction *Correspondence: Josep Penuelas The global population is expected to increase by about josep.penuelas@uab.cat 35% over the next 40 years [87]. Agricultural output will CSIC, Global Ecology Unit CREAF-CSIC-UAB, 08913 Bellaterra, Catalonia, need to increase substantially to accommodate the grow- Spain CREAF, 08913 Cerdanyola del Vallès, Catalonia, Spain ing population. Most of the increase (in agricultural © The Author(s) 2023. 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The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Penuelas et al. Agriculture & Food Security (2023) 12:5 Page 2 of 9 output) is expected to be from producing more fod on potassium”, “ We have thereafter selected the studies of existing farmland (i.e., intensification), although some the last 30 years with a global perspective. new farmland will likely be needed [26]. Such intensifica - tion and expansion might, however, lead to undesirable N fertilization impacts on carbon (C) stocks in soil and vegetation and N fertilization has increased by an order of magnitude in on biodiversity in the most productive croplands of the the last six decades [66]. Converting atmospheric N to world [8]. ammonium as a source for N fertilization has been the Boosting crop yields and closing the gap between actual main process responsible for the increased agricultural and attainable yields can be achieved by implementing yield since the end of World War II [24]. The average and advancing numerous practices and technologies, e.g., increase in yield during 1930–2000 attributable to inputs the adequate use of fertilizers and efficient nutrient man - of N fertilizers generally ranged from about 40–64% in agement can play key roles for global food security [82, temperate climates (USA and England) and tended to be 89]. However, the fertilization intensification of the last much higher in the tropics [24, 82]. Higher N inputs to decades aimed to increase yields has produced some new improve crop yield should be possible without exceed- global environmental and geopolitical problems, such ing the critical regional N concentration in runoff in as nutrient imbalances, [31, 50, 59, 61, 68], leaching of some areas of the world, such as southeastern Asia, Latin nutrients from crops to environment and the associated America, Oceania, the Caribbean and sub-Saharan Africa impacts [45, 68, 72, 85, 94], and increasing cost of ferti- (except South Africa) [8]. lizers with serious geopolitical and economic problems The response of agricultural systems to increased N for the food security in poor countries [3, 40, 57, 89]. The fertilization has evolved differently in countries dur - rise of fertilizer application at global scales has grown ing the last five decades. Some countries have improved exponentially for N than for P and K (Lu and Tian [50]), their agro-environmental performances, but increased [59, 60, 61, 75]. The levels of human driven N, P and K fertilization in other countries has produced low agro- annual loads to environment have reached similar values nomic benefits and higher environmental losses [43], than natural fluxes and a substantial rise in human driven such as accelerated emissions of nitrous oxide leading N:P and N:K ratios [59, 60, 61, 72, 75]. to global climate change and high N loadings leading In this commentary, we aim to discuss the problems to contaminated drinking water and toxic algal blooms caused and associated by the exponential of fertilizers use in downstream ecosystems [17, 30]. In addition to the such as environmental pollution, global nutrient imbal- strictly environmental impact, excess N fertilization has ances and food security mainly in poor countries, their also been associated with threats to human health, such causes, interactions, and consequences, both for current as cancer, upper respiratory diseases [101] and immuno- conditions and for the coming decades, also disentan- genic pathologies, such as coeliac disease [59]. gling the potential solutions to mitigate and adapt to this Achieving a worldwide reduction of total anthro- global change driver, the human driven global changes in pogenic inputs of N into the biosphere and humans is N, P and K stocks, cycling and stoichiometry produced thus a major challenge that requires sustained actions by continuous temporally and spatially asymmetric con- to improve the management practices of N fertilization sumption of fertilizers. This should improve a global view and reduce the losses of N to the environment. More N, linking human use of fertilizers, with global food security though, will be needed to feed the additional 1.5–2 bil- and environmental quality and environmental services lion people that will be added to the global population potential. We aimed to make so by summarizing and before population growth stabilizes later in this century connecting the main bibliography on this topic. [46]. Some studies have observed that an adequate man- We have checked the current bibliography and reports agement of N fertilizers in several countries has influ - about global use of fertilizers and their relationships and enced N pollution much more than crop yields and that impacts on food production and environment. We have the trade-off between reducing N pollution and increas - checked google, google scholar and Web of Science. We ing yields was small. Countries that have caused 35% less have used combinations of words, such as: “fertilizer & N pollution than their neighbors generally only had a 1% environment”, “fertilizer & food security”, “fertilizer & loss of potential yield. Explanatory variables of which phosphorus”, “fertilizer & nitrogen”, “fertilizer & potas- countries cause the most pollution relative to their crop sium” “N:P ratio & fertilizer & environment”, “N:P ratio yields include economic development, population size, & phosphorus & nitrogen & fertilizer & environment”, institutional quality and foreign financial flows to land “environment & food security & poor countries”, “nitro- resources and overall agricultural intensity and share in gen & phosphorus & N: ratio”, “fertilizer & phospho- the economy. These findings provide consistent evidence rus & nitrogen”, “fertilizer & phosphorus & nitrogen & that many national governments have an impressive P enuelas et al. Agriculture & Food Security (2023) 12:5 Page 3 of 9 capacity to reduce global N pollution without having fertilityty management that included N fertilizers with to sacrifice much agricultural production [97]. Unique slow N releasing, sensors in soil crops to monitor the measures could likely resolve this complex issue, and a actual status of soil N, and an adequate combination of combination of measures should probably be immedi- crop species in intercropping or crop rotation improving ately applied at the global scale. the use of N -fixing crops [35]. Several options for reducing the environmental effects of the food system while improving world capacity to P fertilization supply food to humans have been proposed. Their syner - P fertilization has increased much less than N-fertiliza- gistic combination will be needed to sufficiently mitigate tion in the last decades [68]. The demand for P fertiliz - the projected increase in environmental pressures [8]. ers, however, is expected to increase in the next decades; These options include dietary changes toward healthier, the global peak in P production has been predicted to more plant-based diets, improvements in technologies occur around 2030 [14]. Estimates of when existing P and management and reductions in the loss and waste reserves could be exhausted, however, range widely from of food [12, 37]. However, scenario projections indicate the next 40–400  years [15, 57], US [88]. The exact tim - that supply-side measures such as the improvement of ing of peak P production is disputed, but the quality of N-use efficiency are more important than demand-side the remaining phosphate rock is widely acknowledged efforts for food security when introducing regional N tar - to be continuously decreasing [18, 36], so production gets. International trade also plays a key role in sustain- costs are increasing and thus hindering the access of low- ing global food security under N-boundary constraints if income countries to P fertilizers. The situation can be only a limited set of mitigative options is deployed [8]. more problematic, because some models project that the Agricultural sustainability, defined as the ability to global needs of P fertilizers can be doubled by 2050 [56] use soil crops to produce continuous food without envi- and also project an increase in the loss of soil P, including ronmental (basically soil) degradation and other envi- croplands, by soil erosion linked to climate change, which ronmental impacts [99], proposes a large list of new or will increase the need for P fertilizers to sustain crop pro- changed practices that can be applied including the duction [1]. inoculation of Arbuscular mycorrhizal fungi (AMF), The situation is further complicated by the distribution cyanobacteria, and beneficial nematodes, which enhance of mineable sources of P, which are concentrated in very water use efficiency and nutrient availability to plants, few countries (85% in Morocco) [57]. This unequal dis - phytohormones production, soil nutrient cycling, and tribution and the unequal economic capacity of different plant resistance to environmental stresses [99]. Farming countries has caused large surpluses in most of eastern practices have shown that organic and/or regenerative Asia, western and southern Europe, the coastal USA and farming with conservation tillage, manual and biologi- southern Brazil but deficits in Africa [52, 89]. Over-ferti- cal weeding and pest control and use of farming and crop lized soils are frequently saturated with P because of their waster as fertilizers to reduce the need to apply industrial historically high applications [15, 60]. P deficits occur fertilizer, smart intercrop and crop rotation manage- across 30% of the world’s cropland area, and prolonged P ments; all them improving soil health by increasing the deficits can deplete soil P and limit crop yields [52]. The abundance, diversity, and activity of microorganisms [21, low-income and food-deficient countries in sub-Saharan 33, 42, 76, 84, 91]. Africa, central Asia and Latin America generally suffer −1 Precision farming has allowed to make a step forward from low P inputs (0–5 kg  ha ) to their systems of agri- in the technology application to improve fertilizers and cultural production. P scarcity is thus seriously threaten- other resources use efficiency and diminish environ - ing soil fertility, agricultural production and global food mental impacts is [29]. Precision farming aims to use security in several areas [15, 100]. the most advanced technology tools to tailor manage- Managing this scarcity, however, is possible. Up to 80% ment to site crop type and environmental conditions. It of the initial P supplied to overfertilized crops is esti- is based on the “diagnostic” of the situation of crop and mated to be lost before consumption, mostly due to the in base to this provide the application of adequate tools. erosion of soil [1, 15, 57]. Reductions in waste could free For instance, the spectral indexes are one of the most up this resource for low-income, food-deficient coun - precise diagnostic tools. The sensors and scanner are fre - tries [57]. If the current volumes of P fertilizers were to quently mounted on tractors and provide information be redistributed and used more efficiently at the global of soil nutrient status along crop fields, allowing a site- scale, cropland would not be deficient in P. If 21% of the P specific fertilization [20, 55]. Similarly, advances can be fertilizers used in all areas with high surpluses were to be also applied in the case of N to increase its use efficiency redistributed across all P-deficit cropland, the total crop such as those based on smart agriculture including new requirements for P in these locations would effectively be Penuelas et al. Agriculture & Food Security (2023) 12:5 Page 4 of 9 met, eliminating all P deficits globally [52]. Opportuni - supply is becoming an important constraint to crop pro- ties for recovering P and reducing demand are thus also duction in developing countries [4]. This constraint can possible and constitute an institutional challenge [14]. be increased by climate change, with terrestrial areas To achieve P sustainability, several actors must contrib- consequently becoming increasingly arid and semi-arid ute, farmers need to use P more efficiently and societies (Huang et al., 2016), [78]. Very low rates of application of and states should develop technologies and practices potash fertilizer in agricultural production in India and to recycle P from the food chain [23]. For instance, the other developing countries lead to the rapid depletion of global increase in livestock production by threefold for K in the soil. The depletion of plant-available K in soils human consumption over the last five decades has been has a variety of negative impacts, including preventing a key driver of scarcity, environmental distribution, optimal uses of N and P fertilizers, threatening the yields and decrease in the efficiency of P use [50]. Currently of the cropping systems and decreasing farmer income monogastric livestock, as pigs and poultry, suppose a [4, 54]. 70% of the global livestock production, and taking into account the low capacity of these species to absorb P The imbalances among fertilizers from phytases drive to the production of manure very This complex situation between N, P and K fertilizers rich in P and with low N:P ratios leading to a very low leads to imbalances in their use around the world [50, 59, P use-efficiency [58, 62, 92], that, moreover, has contrib- 60]. The case of the African continent is paradigmatic: P uted to exacerbate the environmental imbalances in N:P fertilization should be increased 2.3-fold to be optimal ratios [52, 59, 60, 77]. u Th s, advance in a global change of given the current inputs of N. Inputs of N that would human diet behavior toward a diet more based on plant- allow Africa to close the gaps in yield should be increased based foods should be considered for several reasons but at least fivefold, so the application of P fertilizer should be also for a higher global P-use efficiency in food produc - increased 11.7-fold [89]. Arranging all these imbalances tion [65, 96].. in P provision would greatly increase the pressure on the Furthermore, it is already possible to improve P use current global extraction of P resources, which is not an efficiency based on available new technologies, includ - easy solution due to the scarcity and high cost of minea- ing the use of modern chemically modified phosphate ble P, and/or as commented previously, with a net “trans- fertilizers with controlled release of phosphorus [34] fer” of P fertilizers from overfertilized to under fertilized and new crop genotypes genetically engineered to be areas. In addition, if P fertilizers cannot be made increas- more efficient in P mobilization, capture and use [32]. All ingly accessible, the projections of crop yields of the Mil- these methodological and technological advances drive lennium Ecosystem Assessment imply an increase in to a more efficient management of N and P fertilization nutrient deficits in developing regions [61]. In fact, some avoiding imbalances in N:P ratios and excessive use of studies have found that cropland areas receiving high fertilizers and subsequent associated cascades of food doses of P fertilizers have low P-use efficiencies in crop - security and environmental problems [13, 63, 69, 95]. land yield production [52], and similar observations for N fertilization have been provided [2, 64]. These imbal - K fertilization ances are a particular concern, because anthropogenic Fertilization with industrial fertilizers containing the inputs of these three macronutrients to the environment third key nutrient, K, from mineable reserves has con- have reached the levels of the natural fluxes, thereby sub - tinuously increased since the Industrial Revolution. As stantially affecting their global cycles. The impacts could with P, we are currently in a scenario, where rich coun- thus seriously affect cropland N:P:K ratios but also those tries tend to overfertilize with K, implying environmen- of other ecosystems, both terrestrial and aquatic [59, 61, tal problems and even potential threats to human health, 73, 74]. The impacts of the changes in these ratios have whereas poor countries frequently have problems with been widely observed to alter the structure and function access to K fertilizers, limiting their crop production. of several ecosystems around the world [59, 61, 73, 74]. This dichotomy parallels a scenario of increasing limi - Managing N fertilizers better could also help to resolve tation of mineable K sources and an increase in aridity these general imbalances and the asymmetrical distribu- under climate change and the potential demand by crop tion of fertilizer. The maximum anthropogenic use of N intensification [72]. Future access to K is thus urgently fertilizers needed to prevent the substantial eutrophica- needed in regions most threatened by increasing aridity tion of aquatic ecosystems is considered to be around 62 –1 and food security (e.g., the Sahel, areas with Mediterra-Tg N  y from industrial fertilizers and N-fixing crops nean climates and parts of Asia and South America) due [19], but we have already surpassed this threshold by at to the crucial role of K in the uptake, transport and use least threefold [81]. A few agricultural regions with very efficiency of water by plants ([72], 2021). Insufficient K high rates of N application are the main contributors to P enuelas et al. Agriculture & Food Security (2023) 12:5 Page 5 of 9 the transgression of this “de Vries” boundary, suggest- and PK ratios have been associated with the trade-off ing that a redistribution of N could simultaneously boost between plant growth and energy production [51], and global crop production and reduce the transgression of different abilities in the efficiency of energy production the “de Vries” boundary at the regional level [81]. In the among N, P and K for plant growth and development absence of N mitigation or redistribution, pressure on the have been inferred [51]. The most probable trade-off that environment will probably increase [79], even though the may, at least in part, determine the optimal N:K ratio is need of N fertilizers for sustaining the global human pop- that between the allocation to growth (where N is more ulation is certainly large, even with the efficient use of the determinant) versus the allocation to anti-stress defense, fertilizers [19]. The total amounts of N fertilizers needed mainly against water stress, where the role of K is more to feed the human population in 2030 under the cur- important [44, 71, 72]. Erica multiflora, a sclerophyllous –1 rent distribution of fertilizers could reach 271 Tg  N  y Mediterranean shrub, has the highest foliar N:K and P:K [49], 4.5-fold higher than the threshold estimated by de ratios in spring, coinciding with the period of growth, Vries et  al. [19]. Maintaining the equilibrium of the fer- and the lowest foliar ratios in summer, coinciding with tilizer N:P:K ratios in this scenario would require annual the period of water stress [67]. K fertilization, however, increases in the application P and K fertilizers that can also be important for plant and yield production, but could strain the fertilizer markets even more [57], with only when the N supply reaches a specific level [5]. N:K unknown impacts on global food security, especially ratios are larger in in non-crop plant–soil systems due in low-income countries. The environmental effects of to N deposition [28], affecting the resistance of plants to the food system in the scenario for 2050 could increase stresses, such as drought [70]. The role of the P:K ratio in by 50–90% in the absence of technological changes and non-crop ecosystems, however, has rarely been studied. dedicated mitigative measures due to expected changes Optimal N:K and N:P ratios can be different and higher in population and income levels, reaching levels much for plants under elevated atmospheric CO concentra- higher than acceptable planetary boundaries that define a tions, because higher net photosynthetic rates under ele- safe operating space for humanity [8].vated CO concentrations increase the plant demand of The use of N, P and K fertilizers is greatly unbalanced all three macronutrients but with a higher proportion of around the world, including in the largest countries, N, mainly to reach a higher maximum rate of carboxyla- such as India [7] and the USA [90], in all cases leading tion [16]. The impacts of the unbalanced use of N and P to deficient production of food [50, 68, 90]. Nutrient bal- fertilizers with K fertilizer on non-crop ecosystems, how- ance is essential for achieving global food security [6] and ever, remains to be widely studied. for conserving N and P fertilizers [53]. Lu and Tian [50] found a global increase in the fertilizer N:P ratio of 0.8 –1 (g  g ) per decade (p < 0.05) during 1961–2013, which Toward a more rational use of fertilizers may have an important global implication for anthropo- The present and future management of N, P and K ferti - genic impacts on agroecosystem functions in the long lizers at the global scale is directly linked to food security term. These imbalances can alter soil stoichiometry and and environmental health and, therefore, to human life, have been observed to differ in important cropland areas health and well-being. Human food security and environ- [90]. The inexorable change in the stoichiometry of C and mental health cannot be accomplished without measures N relative to P has no equivalent in Earth history [61], leading to strategic and adequate N, P and K fertilization, 2020). The N:P ratio of atmospheric deposition in sev - which should be addressed simultaneously for the three eral parts of the world has reached values over 100–200 nutrients. on a mass basis [9]. This anthropogenic imprint on the N Several strategies have been proposed to balance the and P cycles and N:P stoichiometry has already had con- N:P:K input ratios in fertilization management to opti- sequences in several natural ecosystems to the structure, mize yield increases and the quantity and quality of functioning, and diversity of terrestrial [38, 59, 60, 61] production while minimizing nutrient losses and thus and aquatic [22, 59, 60, 61, 73] organisms. environmental impacts. Precision farming is thus a key The role of the N:P ratio has been widely studied, and tool at this regard [29]. Adoption of the 4R principle its importance for the growth of crop plants and for the (right nutrient source at the right rate, right time and structure, diversity and functioning of other ecosystems right place) should also help to ensure the appropriate has also been widely observed [22, 61, 73], 2020), but use of nutrient resources and to optimize productivity the importance of N:K and P:K ratios has been studied [82]. less. Some studies, however, have observed that opti- New legislation considering the different fertilizers mal N:K and P:K ratios in fertilizers are important for altogether is also urgently needed for achieving these plant growth and yield in diverse crops [25, 41, 51]. N:K objectives, and in fact, it is already in the agendas of some Penuelas et al. Agriculture & Food Security (2023) 12:5 Page 6 of 9 high-income countries, such as the European Union [93]. increasing aridity (e.g., the Sahel, areas with Mediter- We, however, need more international agreement about a ranean climates and parts of Asia and South America) global strategy of fertilization, because adequate fertilizer due to the crucial role of K in the uptake, transport and use increases water-use efficiency, crop and food pro - use efficiency of water by plants, that makes K a nec - duction, the resistance of crop production against arid- essary tool to try to maintain acceptable levels of food ity and the preservation of environments and biodiversity production under increasing water scarcity. In the case and can provide several feedbacks to mitigate climate of P, if it is sufficiently applied, it can be stored in soil change [59, 60, 98]. In this context and at this moment, in not available forms, whereas mine reserves can be the European Union is a paradigm; in fact, European Sus- emptied faster and its access can progressively become tainable Phosphorus Platform for an Integrated Nutrient prohibitive for poor countries. This can, moreover, be Management Action Plan (INMAP) is fully in line with related to higher prices of P fertilizers which can hinder these ambitions and its pressure on European Commis- even more the access to fertilizer of millions of farmers sion in principle will act to reduce nutrient losses by at in poor countries and decrease even more the already least 50%, while ensuring that there is no deterioration in low efficiency of crop production in several areas of soil fertility, with a short-time scenario of a reduction of poor countries, such as in Africa or Asia impairing the use of fertilizers by at least 20% by 2030 [93]. Unfor- even more their food security. There are though several tunately, apart from general declarations, concrete law new technologies and crop management methodolo- measures to more controlled, efficient and environmen - gies that can help to improve fertilize use and effi - tally friendly use of fertilizers are at this moment effective ciency. Smart, precision and regenerative agriculture in very few other parts of world. Recently, in Canada the approaches together with new biotechnologies appli- government has proposed a reduction of a 30% in the use cation can help to correct this global change driver, of industrial fertilizers within the global country plan to so they should be quickly at global scale. Meanwhile, reduce greenhouse emissions [27]. Theoretically, China is new legislation adopting the well-known and common- another state with strict legislation of fertilizers use [11], sense 4R principle (right nutrient source at the right being prohibited to import, produce, sell or use un-reg- rate, right time and right place) would help to ensure istered fertilizers, and fertilizer sold in China shall also the appropriate use of fertilizers and the optimization meet relevant product standards. However, there is still of crop productivity for food security and environmen- a lot of room in most countries to take a more serious tal sustainability. policy about fertilizer use and to endorse all the technical Acknowledgements improvements to reduce fertilizer use while increasing We thank the insightful exchange of ideas on the topic of this article with the use efficiency [10, 83, 89]. It is necessary to overcome the members of the Global Ecology Unit CREAF-CSIC-UAB, Barcelona, Catalonia, Spain. constrains imposed by conventional intensive agriculture and the scarce economical capacity and little access of Author contributions farmers of several countries to adequate information [10, JP and JS designed the study, JP, FC and JS gathered the information and wrote this comment. All authors read and approved the final manuscript. 83, 89]. Funding Open Access funding provided thanks to the CRUE-CSIC agreement with Conclusions Springer Nature. Authors acknowledge the financial support from the Catalan Human-driven N and P loads to environment have Government Grant SGR 2017–1005, the Spanish Government Grants PID2019- 110521 GB-I00, PID2020115770RB-I, and TED2021-132627B-I00, and the reached levels comparable to natural fluxes. The con - Fundación Ramón Areces grant CIVP20A6621. tinuous exponential increases of N loads rising faster than P and K loads have increased N:P ratios in several Availability of data and materials Not applicable. areas of the world with unprecedented impacts on eco- systems and their services capacities. These imbalances Declarations have serious impacts on food production capacity, mainly in poor countries, where the increases in N:P Ethics approval and consent to participate and N:K ratios are further favoured by the higher costs We approve and consent. of K and mainly P fertilizers than the costs of N fertiliz- Consent for publication ers. In the case of the excess of N, its consequences can We consent. also affect human health by the pollution of waters and Competing interests excessive N fertilization. Aridity is expected to increase Authors declare no competing interests. in the next decades and more lands will be affected by decreased availability of water. 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Nature Food. 2020;1:713–9. 98. Xiong W, Tarnavsky E. Better agronomic management increases climate resilence of maize to drought in Tanzania. Atmosphere. 2020;11:982. Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in pub- lished maps and institutional affiliations. Re Read ady y to to submit y submit your our re researc search h ? Choose BMC and benefit fr ? Choose BMC and benefit from om: : fast, convenient online submission thorough peer review by experienced researchers in your field rapid publication on acceptance support for research data, including large and complex data types • gold Open Access which fosters wider collaboration and increased citations maximum visibility for your research: over 100M website views per year At BMC, research is always in progress. Learn more biomedcentral.com/submissions http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Agriculture & Food Security Springer Journals

A better use of fertilizers is needed for global food security and environmental sustainability

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Abstract

The massive use of fertilizers during the last decades allowed a great increase in the global capacity of food produc- tion. However, in the last years, several studies highlight the inefficiency and country asymmetries in the use of these fertilizers that generated environmental problems, soil nutritional imbalances and not optimal food production. We have aimed to summarize this information and identify and disentangle the key caveats that should be solved. Inadequate global management of fertilization produces areas with serious nutrient deficits in croplands linked with insufficient access to fertilizers that clearly limit food production, and areas that are overfertilized with the consequent problems of environmental pollution affecting human health. A more efficient use of nitrogen (N), phosphorus (P) and potassium (K) fertilizers for food security while preserving the environment is thus needed. Nutrient imbalances, particularly the disequilibrium of the N:P ratio due to the unbalanced release of N and P from anthropogenic activi- ties, mainly by crop fertilization and expanding N-fixing crops that have continuously increased the soil N:P ratio, is another issue to resolve. This imbalance has already affected several terrestrial and aquatic ecosystems, altering their species composition and functionality and threatening global biodiversity. The different economic and geopolitical traits of these three main macronutrient fertilizers must be considered. P has the fewest reserves, depending mostly on mineable efforts, with most of the reserves concentrated in very few countries (85% in Morocco). This problem is a great concern for the current and near-future access to P for low-income countries. N is instead readily available due to the well-established and relatively low-cost Haber–Bosch synthesis of ammonium from atmospheric N , which is increasingly used, even in some low-income countries producing an increasing imbalance in nutrient ratios with the application of P and K fertilizers. The anthropogenic inputs of these three macronutrients to the environment have reached the levels of the natural fluxes, thereby substantially altering their global cycles. The case of the excess of N fertilization is especially paradigmatic in several areas of the world, where continental water sources have become useless due to the higher nitrate concentrations. The management of N, P and K fertilizers is thus in the center of the main dichotomy between food security and environmentally driven problems, such as climate change or eutrophica- tion/pollution. Such a key role demands new legislation for adopting the well-known and common-sense 4R princi- ple (right nutrient source at the right rate, right time and right place) that would help to ensure the appropriate use of nutrient resources and the optimization of productivity. Keywords Fertilizers, Food security, Environmental security, Nitrogen, Phosphorus, Potassium, Imbalance, Stoichiometry, Eutrophication, Global cycles Introduction *Correspondence: Josep Penuelas The global population is expected to increase by about josep.penuelas@uab.cat 35% over the next 40 years [87]. Agricultural output will CSIC, Global Ecology Unit CREAF-CSIC-UAB, 08913 Bellaterra, Catalonia, need to increase substantially to accommodate the grow- Spain CREAF, 08913 Cerdanyola del Vallès, Catalonia, Spain ing population. Most of the increase (in agricultural © The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Penuelas et al. Agriculture & Food Security (2023) 12:5 Page 2 of 9 output) is expected to be from producing more fod on potassium”, “ We have thereafter selected the studies of existing farmland (i.e., intensification), although some the last 30 years with a global perspective. new farmland will likely be needed [26]. Such intensifica - tion and expansion might, however, lead to undesirable N fertilization impacts on carbon (C) stocks in soil and vegetation and N fertilization has increased by an order of magnitude in on biodiversity in the most productive croplands of the the last six decades [66]. Converting atmospheric N to world [8]. ammonium as a source for N fertilization has been the Boosting crop yields and closing the gap between actual main process responsible for the increased agricultural and attainable yields can be achieved by implementing yield since the end of World War II [24]. The average and advancing numerous practices and technologies, e.g., increase in yield during 1930–2000 attributable to inputs the adequate use of fertilizers and efficient nutrient man - of N fertilizers generally ranged from about 40–64% in agement can play key roles for global food security [82, temperate climates (USA and England) and tended to be 89]. However, the fertilization intensification of the last much higher in the tropics [24, 82]. Higher N inputs to decades aimed to increase yields has produced some new improve crop yield should be possible without exceed- global environmental and geopolitical problems, such ing the critical regional N concentration in runoff in as nutrient imbalances, [31, 50, 59, 61, 68], leaching of some areas of the world, such as southeastern Asia, Latin nutrients from crops to environment and the associated America, Oceania, the Caribbean and sub-Saharan Africa impacts [45, 68, 72, 85, 94], and increasing cost of ferti- (except South Africa) [8]. lizers with serious geopolitical and economic problems The response of agricultural systems to increased N for the food security in poor countries [3, 40, 57, 89]. The fertilization has evolved differently in countries dur - rise of fertilizer application at global scales has grown ing the last five decades. Some countries have improved exponentially for N than for P and K (Lu and Tian [50]), their agro-environmental performances, but increased [59, 60, 61, 75]. The levels of human driven N, P and K fertilization in other countries has produced low agro- annual loads to environment have reached similar values nomic benefits and higher environmental losses [43], than natural fluxes and a substantial rise in human driven such as accelerated emissions of nitrous oxide leading N:P and N:K ratios [59, 60, 61, 72, 75]. to global climate change and high N loadings leading In this commentary, we aim to discuss the problems to contaminated drinking water and toxic algal blooms caused and associated by the exponential of fertilizers use in downstream ecosystems [17, 30]. In addition to the such as environmental pollution, global nutrient imbal- strictly environmental impact, excess N fertilization has ances and food security mainly in poor countries, their also been associated with threats to human health, such causes, interactions, and consequences, both for current as cancer, upper respiratory diseases [101] and immuno- conditions and for the coming decades, also disentan- genic pathologies, such as coeliac disease [59]. gling the potential solutions to mitigate and adapt to this Achieving a worldwide reduction of total anthro- global change driver, the human driven global changes in pogenic inputs of N into the biosphere and humans is N, P and K stocks, cycling and stoichiometry produced thus a major challenge that requires sustained actions by continuous temporally and spatially asymmetric con- to improve the management practices of N fertilization sumption of fertilizers. This should improve a global view and reduce the losses of N to the environment. More N, linking human use of fertilizers, with global food security though, will be needed to feed the additional 1.5–2 bil- and environmental quality and environmental services lion people that will be added to the global population potential. We aimed to make so by summarizing and before population growth stabilizes later in this century connecting the main bibliography on this topic. [46]. Some studies have observed that an adequate man- We have checked the current bibliography and reports agement of N fertilizers in several countries has influ - about global use of fertilizers and their relationships and enced N pollution much more than crop yields and that impacts on food production and environment. We have the trade-off between reducing N pollution and increas - checked google, google scholar and Web of Science. We ing yields was small. Countries that have caused 35% less have used combinations of words, such as: “fertilizer & N pollution than their neighbors generally only had a 1% environment”, “fertilizer & food security”, “fertilizer & loss of potential yield. Explanatory variables of which phosphorus”, “fertilizer & nitrogen”, “fertilizer & potas- countries cause the most pollution relative to their crop sium” “N:P ratio & fertilizer & environment”, “N:P ratio yields include economic development, population size, & phosphorus & nitrogen & fertilizer & environment”, institutional quality and foreign financial flows to land “environment & food security & poor countries”, “nitro- resources and overall agricultural intensity and share in gen & phosphorus & N: ratio”, “fertilizer & phospho- the economy. These findings provide consistent evidence rus & nitrogen”, “fertilizer & phosphorus & nitrogen & that many national governments have an impressive P enuelas et al. Agriculture & Food Security (2023) 12:5 Page 3 of 9 capacity to reduce global N pollution without having fertilityty management that included N fertilizers with to sacrifice much agricultural production [97]. Unique slow N releasing, sensors in soil crops to monitor the measures could likely resolve this complex issue, and a actual status of soil N, and an adequate combination of combination of measures should probably be immedi- crop species in intercropping or crop rotation improving ately applied at the global scale. the use of N -fixing crops [35]. Several options for reducing the environmental effects of the food system while improving world capacity to P fertilization supply food to humans have been proposed. Their syner - P fertilization has increased much less than N-fertiliza- gistic combination will be needed to sufficiently mitigate tion in the last decades [68]. The demand for P fertiliz - the projected increase in environmental pressures [8]. ers, however, is expected to increase in the next decades; These options include dietary changes toward healthier, the global peak in P production has been predicted to more plant-based diets, improvements in technologies occur around 2030 [14]. Estimates of when existing P and management and reductions in the loss and waste reserves could be exhausted, however, range widely from of food [12, 37]. However, scenario projections indicate the next 40–400  years [15, 57], US [88]. The exact tim - that supply-side measures such as the improvement of ing of peak P production is disputed, but the quality of N-use efficiency are more important than demand-side the remaining phosphate rock is widely acknowledged efforts for food security when introducing regional N tar - to be continuously decreasing [18, 36], so production gets. International trade also plays a key role in sustain- costs are increasing and thus hindering the access of low- ing global food security under N-boundary constraints if income countries to P fertilizers. The situation can be only a limited set of mitigative options is deployed [8]. more problematic, because some models project that the Agricultural sustainability, defined as the ability to global needs of P fertilizers can be doubled by 2050 [56] use soil crops to produce continuous food without envi- and also project an increase in the loss of soil P, including ronmental (basically soil) degradation and other envi- croplands, by soil erosion linked to climate change, which ronmental impacts [99], proposes a large list of new or will increase the need for P fertilizers to sustain crop pro- changed practices that can be applied including the duction [1]. inoculation of Arbuscular mycorrhizal fungi (AMF), The situation is further complicated by the distribution cyanobacteria, and beneficial nematodes, which enhance of mineable sources of P, which are concentrated in very water use efficiency and nutrient availability to plants, few countries (85% in Morocco) [57]. This unequal dis - phytohormones production, soil nutrient cycling, and tribution and the unequal economic capacity of different plant resistance to environmental stresses [99]. Farming countries has caused large surpluses in most of eastern practices have shown that organic and/or regenerative Asia, western and southern Europe, the coastal USA and farming with conservation tillage, manual and biologi- southern Brazil but deficits in Africa [52, 89]. Over-ferti- cal weeding and pest control and use of farming and crop lized soils are frequently saturated with P because of their waster as fertilizers to reduce the need to apply industrial historically high applications [15, 60]. P deficits occur fertilizer, smart intercrop and crop rotation manage- across 30% of the world’s cropland area, and prolonged P ments; all them improving soil health by increasing the deficits can deplete soil P and limit crop yields [52]. The abundance, diversity, and activity of microorganisms [21, low-income and food-deficient countries in sub-Saharan 33, 42, 76, 84, 91]. Africa, central Asia and Latin America generally suffer −1 Precision farming has allowed to make a step forward from low P inputs (0–5 kg  ha ) to their systems of agri- in the technology application to improve fertilizers and cultural production. P scarcity is thus seriously threaten- other resources use efficiency and diminish environ - ing soil fertility, agricultural production and global food mental impacts is [29]. Precision farming aims to use security in several areas [15, 100]. the most advanced technology tools to tailor manage- Managing this scarcity, however, is possible. Up to 80% ment to site crop type and environmental conditions. It of the initial P supplied to overfertilized crops is esti- is based on the “diagnostic” of the situation of crop and mated to be lost before consumption, mostly due to the in base to this provide the application of adequate tools. erosion of soil [1, 15, 57]. Reductions in waste could free For instance, the spectral indexes are one of the most up this resource for low-income, food-deficient coun - precise diagnostic tools. The sensors and scanner are fre - tries [57]. If the current volumes of P fertilizers were to quently mounted on tractors and provide information be redistributed and used more efficiently at the global of soil nutrient status along crop fields, allowing a site- scale, cropland would not be deficient in P. If 21% of the P specific fertilization [20, 55]. Similarly, advances can be fertilizers used in all areas with high surpluses were to be also applied in the case of N to increase its use efficiency redistributed across all P-deficit cropland, the total crop such as those based on smart agriculture including new requirements for P in these locations would effectively be Penuelas et al. Agriculture & Food Security (2023) 12:5 Page 4 of 9 met, eliminating all P deficits globally [52]. Opportuni - supply is becoming an important constraint to crop pro- ties for recovering P and reducing demand are thus also duction in developing countries [4]. This constraint can possible and constitute an institutional challenge [14]. be increased by climate change, with terrestrial areas To achieve P sustainability, several actors must contrib- consequently becoming increasingly arid and semi-arid ute, farmers need to use P more efficiently and societies (Huang et al., 2016), [78]. Very low rates of application of and states should develop technologies and practices potash fertilizer in agricultural production in India and to recycle P from the food chain [23]. For instance, the other developing countries lead to the rapid depletion of global increase in livestock production by threefold for K in the soil. The depletion of plant-available K in soils human consumption over the last five decades has been has a variety of negative impacts, including preventing a key driver of scarcity, environmental distribution, optimal uses of N and P fertilizers, threatening the yields and decrease in the efficiency of P use [50]. Currently of the cropping systems and decreasing farmer income monogastric livestock, as pigs and poultry, suppose a [4, 54]. 70% of the global livestock production, and taking into account the low capacity of these species to absorb P The imbalances among fertilizers from phytases drive to the production of manure very This complex situation between N, P and K fertilizers rich in P and with low N:P ratios leading to a very low leads to imbalances in their use around the world [50, 59, P use-efficiency [58, 62, 92], that, moreover, has contrib- 60]. The case of the African continent is paradigmatic: P uted to exacerbate the environmental imbalances in N:P fertilization should be increased 2.3-fold to be optimal ratios [52, 59, 60, 77]. u Th s, advance in a global change of given the current inputs of N. Inputs of N that would human diet behavior toward a diet more based on plant- allow Africa to close the gaps in yield should be increased based foods should be considered for several reasons but at least fivefold, so the application of P fertilizer should be also for a higher global P-use efficiency in food produc - increased 11.7-fold [89]. Arranging all these imbalances tion [65, 96].. in P provision would greatly increase the pressure on the Furthermore, it is already possible to improve P use current global extraction of P resources, which is not an efficiency based on available new technologies, includ - easy solution due to the scarcity and high cost of minea- ing the use of modern chemically modified phosphate ble P, and/or as commented previously, with a net “trans- fertilizers with controlled release of phosphorus [34] fer” of P fertilizers from overfertilized to under fertilized and new crop genotypes genetically engineered to be areas. In addition, if P fertilizers cannot be made increas- more efficient in P mobilization, capture and use [32]. All ingly accessible, the projections of crop yields of the Mil- these methodological and technological advances drive lennium Ecosystem Assessment imply an increase in to a more efficient management of N and P fertilization nutrient deficits in developing regions [61]. In fact, some avoiding imbalances in N:P ratios and excessive use of studies have found that cropland areas receiving high fertilizers and subsequent associated cascades of food doses of P fertilizers have low P-use efficiencies in crop - security and environmental problems [13, 63, 69, 95]. land yield production [52], and similar observations for N fertilization have been provided [2, 64]. These imbal - K fertilization ances are a particular concern, because anthropogenic Fertilization with industrial fertilizers containing the inputs of these three macronutrients to the environment third key nutrient, K, from mineable reserves has con- have reached the levels of the natural fluxes, thereby sub - tinuously increased since the Industrial Revolution. As stantially affecting their global cycles. The impacts could with P, we are currently in a scenario, where rich coun- thus seriously affect cropland N:P:K ratios but also those tries tend to overfertilize with K, implying environmen- of other ecosystems, both terrestrial and aquatic [59, 61, tal problems and even potential threats to human health, 73, 74]. The impacts of the changes in these ratios have whereas poor countries frequently have problems with been widely observed to alter the structure and function access to K fertilizers, limiting their crop production. of several ecosystems around the world [59, 61, 73, 74]. This dichotomy parallels a scenario of increasing limi - Managing N fertilizers better could also help to resolve tation of mineable K sources and an increase in aridity these general imbalances and the asymmetrical distribu- under climate change and the potential demand by crop tion of fertilizer. The maximum anthropogenic use of N intensification [72]. Future access to K is thus urgently fertilizers needed to prevent the substantial eutrophica- needed in regions most threatened by increasing aridity tion of aquatic ecosystems is considered to be around 62 –1 and food security (e.g., the Sahel, areas with Mediterra-Tg N  y from industrial fertilizers and N-fixing crops nean climates and parts of Asia and South America) due [19], but we have already surpassed this threshold by at to the crucial role of K in the uptake, transport and use least threefold [81]. A few agricultural regions with very efficiency of water by plants ([72], 2021). Insufficient K high rates of N application are the main contributors to P enuelas et al. Agriculture & Food Security (2023) 12:5 Page 5 of 9 the transgression of this “de Vries” boundary, suggest- and PK ratios have been associated with the trade-off ing that a redistribution of N could simultaneously boost between plant growth and energy production [51], and global crop production and reduce the transgression of different abilities in the efficiency of energy production the “de Vries” boundary at the regional level [81]. In the among N, P and K for plant growth and development absence of N mitigation or redistribution, pressure on the have been inferred [51]. The most probable trade-off that environment will probably increase [79], even though the may, at least in part, determine the optimal N:K ratio is need of N fertilizers for sustaining the global human pop- that between the allocation to growth (where N is more ulation is certainly large, even with the efficient use of the determinant) versus the allocation to anti-stress defense, fertilizers [19]. The total amounts of N fertilizers needed mainly against water stress, where the role of K is more to feed the human population in 2030 under the cur- important [44, 71, 72]. Erica multiflora, a sclerophyllous –1 rent distribution of fertilizers could reach 271 Tg  N  y Mediterranean shrub, has the highest foliar N:K and P:K [49], 4.5-fold higher than the threshold estimated by de ratios in spring, coinciding with the period of growth, Vries et  al. [19]. Maintaining the equilibrium of the fer- and the lowest foliar ratios in summer, coinciding with tilizer N:P:K ratios in this scenario would require annual the period of water stress [67]. K fertilization, however, increases in the application P and K fertilizers that can also be important for plant and yield production, but could strain the fertilizer markets even more [57], with only when the N supply reaches a specific level [5]. N:K unknown impacts on global food security, especially ratios are larger in in non-crop plant–soil systems due in low-income countries. The environmental effects of to N deposition [28], affecting the resistance of plants to the food system in the scenario for 2050 could increase stresses, such as drought [70]. The role of the P:K ratio in by 50–90% in the absence of technological changes and non-crop ecosystems, however, has rarely been studied. dedicated mitigative measures due to expected changes Optimal N:K and N:P ratios can be different and higher in population and income levels, reaching levels much for plants under elevated atmospheric CO concentra- higher than acceptable planetary boundaries that define a tions, because higher net photosynthetic rates under ele- safe operating space for humanity [8].vated CO concentrations increase the plant demand of The use of N, P and K fertilizers is greatly unbalanced all three macronutrients but with a higher proportion of around the world, including in the largest countries, N, mainly to reach a higher maximum rate of carboxyla- such as India [7] and the USA [90], in all cases leading tion [16]. The impacts of the unbalanced use of N and P to deficient production of food [50, 68, 90]. Nutrient bal- fertilizers with K fertilizer on non-crop ecosystems, how- ance is essential for achieving global food security [6] and ever, remains to be widely studied. for conserving N and P fertilizers [53]. Lu and Tian [50] found a global increase in the fertilizer N:P ratio of 0.8 –1 (g  g ) per decade (p < 0.05) during 1961–2013, which Toward a more rational use of fertilizers may have an important global implication for anthropo- The present and future management of N, P and K ferti - genic impacts on agroecosystem functions in the long lizers at the global scale is directly linked to food security term. These imbalances can alter soil stoichiometry and and environmental health and, therefore, to human life, have been observed to differ in important cropland areas health and well-being. Human food security and environ- [90]. The inexorable change in the stoichiometry of C and mental health cannot be accomplished without measures N relative to P has no equivalent in Earth history [61], leading to strategic and adequate N, P and K fertilization, 2020). The N:P ratio of atmospheric deposition in sev - which should be addressed simultaneously for the three eral parts of the world has reached values over 100–200 nutrients. on a mass basis [9]. This anthropogenic imprint on the N Several strategies have been proposed to balance the and P cycles and N:P stoichiometry has already had con- N:P:K input ratios in fertilization management to opti- sequences in several natural ecosystems to the structure, mize yield increases and the quantity and quality of functioning, and diversity of terrestrial [38, 59, 60, 61] production while minimizing nutrient losses and thus and aquatic [22, 59, 60, 61, 73] organisms. environmental impacts. Precision farming is thus a key The role of the N:P ratio has been widely studied, and tool at this regard [29]. Adoption of the 4R principle its importance for the growth of crop plants and for the (right nutrient source at the right rate, right time and structure, diversity and functioning of other ecosystems right place) should also help to ensure the appropriate has also been widely observed [22, 61, 73], 2020), but use of nutrient resources and to optimize productivity the importance of N:K and P:K ratios has been studied [82]. less. Some studies, however, have observed that opti- New legislation considering the different fertilizers mal N:K and P:K ratios in fertilizers are important for altogether is also urgently needed for achieving these plant growth and yield in diverse crops [25, 41, 51]. N:K objectives, and in fact, it is already in the agendas of some Penuelas et al. Agriculture & Food Security (2023) 12:5 Page 6 of 9 high-income countries, such as the European Union [93]. increasing aridity (e.g., the Sahel, areas with Mediter- We, however, need more international agreement about a ranean climates and parts of Asia and South America) global strategy of fertilization, because adequate fertilizer due to the crucial role of K in the uptake, transport and use increases water-use efficiency, crop and food pro - use efficiency of water by plants, that makes K a nec - duction, the resistance of crop production against arid- essary tool to try to maintain acceptable levels of food ity and the preservation of environments and biodiversity production under increasing water scarcity. In the case and can provide several feedbacks to mitigate climate of P, if it is sufficiently applied, it can be stored in soil change [59, 60, 98]. In this context and at this moment, in not available forms, whereas mine reserves can be the European Union is a paradigm; in fact, European Sus- emptied faster and its access can progressively become tainable Phosphorus Platform for an Integrated Nutrient prohibitive for poor countries. This can, moreover, be Management Action Plan (INMAP) is fully in line with related to higher prices of P fertilizers which can hinder these ambitions and its pressure on European Commis- even more the access to fertilizer of millions of farmers sion in principle will act to reduce nutrient losses by at in poor countries and decrease even more the already least 50%, while ensuring that there is no deterioration in low efficiency of crop production in several areas of soil fertility, with a short-time scenario of a reduction of poor countries, such as in Africa or Asia impairing the use of fertilizers by at least 20% by 2030 [93]. Unfor- even more their food security. There are though several tunately, apart from general declarations, concrete law new technologies and crop management methodolo- measures to more controlled, efficient and environmen - gies that can help to improve fertilize use and effi - tally friendly use of fertilizers are at this moment effective ciency. Smart, precision and regenerative agriculture in very few other parts of world. Recently, in Canada the approaches together with new biotechnologies appli- government has proposed a reduction of a 30% in the use cation can help to correct this global change driver, of industrial fertilizers within the global country plan to so they should be quickly at global scale. Meanwhile, reduce greenhouse emissions [27]. Theoretically, China is new legislation adopting the well-known and common- another state with strict legislation of fertilizers use [11], sense 4R principle (right nutrient source at the right being prohibited to import, produce, sell or use un-reg- rate, right time and right place) would help to ensure istered fertilizers, and fertilizer sold in China shall also the appropriate use of fertilizers and the optimization meet relevant product standards. However, there is still of crop productivity for food security and environmen- a lot of room in most countries to take a more serious tal sustainability. policy about fertilizer use and to endorse all the technical Acknowledgements improvements to reduce fertilizer use while increasing We thank the insightful exchange of ideas on the topic of this article with the use efficiency [10, 83, 89]. It is necessary to overcome the members of the Global Ecology Unit CREAF-CSIC-UAB, Barcelona, Catalonia, Spain. constrains imposed by conventional intensive agriculture and the scarce economical capacity and little access of Author contributions farmers of several countries to adequate information [10, JP and JS designed the study, JP, FC and JS gathered the information and wrote this comment. All authors read and approved the final manuscript. 83, 89]. Funding Open Access funding provided thanks to the CRUE-CSIC agreement with Conclusions Springer Nature. Authors acknowledge the financial support from the Catalan Human-driven N and P loads to environment have Government Grant SGR 2017–1005, the Spanish Government Grants PID2019- 110521 GB-I00, PID2020115770RB-I, and TED2021-132627B-I00, and the reached levels comparable to natural fluxes. The con - Fundación Ramón Areces grant CIVP20A6621. tinuous exponential increases of N loads rising faster than P and K loads have increased N:P ratios in several Availability of data and materials Not applicable. areas of the world with unprecedented impacts on eco- systems and their services capacities. These imbalances Declarations have serious impacts on food production capacity, mainly in poor countries, where the increases in N:P Ethics approval and consent to participate and N:K ratios are further favoured by the higher costs We approve and consent. of K and mainly P fertilizers than the costs of N fertiliz- Consent for publication ers. In the case of the excess of N, its consequences can We consent. also affect human health by the pollution of waters and Competing interests excessive N fertilization. Aridity is expected to increase Authors declare no competing interests. in the next decades and more lands will be affected by decreased availability of water. 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Nature Food. 2020;1:713–9. 98. Xiong W, Tarnavsky E. Better agronomic management increases climate resilence of maize to drought in Tanzania. Atmosphere. 2020;11:982. Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in pub- lished maps and institutional affiliations. Re Read ady y to to submit y submit your our re researc search h ? Choose BMC and benefit fr ? Choose BMC and benefit from om: : fast, convenient online submission thorough peer review by experienced researchers in your field rapid publication on acceptance support for research data, including large and complex data types • gold Open Access which fosters wider collaboration and increased citations maximum visibility for your research: over 100M website views per year At BMC, research is always in progress. Learn more biomedcentral.com/submissions

Journal

Agriculture & Food SecuritySpringer Journals

Published: Mar 23, 2023

Keywords: Fertilizers; Food security; Environmental security; Nitrogen; Phosphorus; Potassium; Imbalance; Stoichiometry; Eutrophication; Global cycles

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