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Importexport balance of nitrogen and phosphorus in food, fodder and fertilizers in the Baltic Sea drainage area Eero Asmala a, , Laura Saikku b , Sanna Vienonen c a Finnish Environment Institute, Marine Research Centre, P.O. Box 140, FI-00251 Helsinki, Finland b University of Helsinki, Faculty of Biological and Environmental Sciences, P.O. Box 65, FI-00014 University of Helsinki, Finland c Finnish Environment Institute, Freshwater Centre, P.O. Box 140, FI-00251 Helsinki, Finland abstract article info Article history: Received 31 December 2010 Received in revised form 5 August 2011 Accepted 15 August 2011 Available online 9 September 2011 Keywords: Baltic Sea Eutrophication Phosphorus Nitrogen International trade Food production Nitrogen (N) and phosphorus (P) are essential elements for life, but in excess they contribute to aquatic eutro- phication. The Baltic Sea is a brackish semi-enclosed sea that is heavily inuenced by anthropogenic loading of nutrients, resulting in a major environmental problem, eutrophication. In this study, the nutrient balance of the food production and consumption system in seven countries in the Baltic Sea drainage area was quantied for the period 20022005. The food production and consumption system accumulates nutrients in the Baltic Sea drainage area, due to extensive imports to the system. The average annual net surplus of nutrients was 1 800 000 tons N and 320 000 tons P in 20022005, or annually 28 kg N and 5 kg P per capita. The average total annual import was 2 100 000 tons N and 340 000 tons P during 20022005. The largest imports to the system were fertilizers, totaling 1 700 000 tons N and 290 000 tons P. Traded nutrients in food and fodder amounted to a net annual surplus of 180 000 tons N and 25 000 tons P. The nutrient load to the Baltic Sea due to the food consumption and production system was 21% N and 6% P of the respective annual net inputs to the region. This study shows that large amounts of nutrients to Baltic Sea drainage area are inputs from outside the region, eventually contributing to eutrophication. To reduce the nutrient imports, fertilizers should be used more ef- ciently, nutrients should be recycled more efciently inside the region, and food system should be guided toward low-nutrient intensive diets. © 2011 Elsevier B.V. All rights reserved. 1. Introduction For life on Earth, nitrogen (N) and phosphorus (P) are indispensable elements. They are essential components of e.g. macromolecules aden- osine triphosphate and deoxyribonucleic acid (ATP and DNA), which carry energy and genetic information in living cells. Both nitrogen and phosphorus have been used in continuously increasing amounts as fer- tilizers in agricultural production, which in turn has been increasing the nutrient runoff to aquatic environments globally (Compton et al., 2000; Galloway et al., 2004). While their biogeochemistry differs greatly, N and P enrichment are the cause of eutrophication problems encoun- tered in many freshwater and estuarine and marine systems However, the biogeochemistry of nitrogen and phosphorus differs substantially (Vitousek et al., 2003; Filippelli, 2008). The Baltic Sea is a unique brackish water environment, with a salinity ranging from freshwater toward oceanic salinities (mean salinity 7 psu). The Baltic Sea is also a small water body due to its shallowness its mean depth is only 54 m (Leppäranta and Myrberg, 2009). These physical properties combined with the inuence of the about 90 million inhabitants of 14 countries in the 1720000 km 2 drainage basin result in high anthropogenic pressure on the environment and nonuniform eco- logical responses, e.g. to nutrient loading (Tamminen and Andersen, 2007). The interplay of the two elements examined in this study, nitro- gen and phosphorus, is highly pronounced in the Baltic Sea eutrophica- tion (Conley et al., 2009a). Eutrophication, i.e. the process of ecological response to the enrichment of growth-limiting nutrients (specically ni- trogen and phosphorus) is considered to be the single greatest threat to the Baltic Sea environment (Elmgren, 2001; HELCOM, 2009). Nutrient enrichment leads to increased primary production, which in turn has consequences as alterations in species structure, biodiversity and recre- ational values (Rönnberg and Bonsdorff, 2004). The low-saline northernmost part of the Baltic Sea, Gulf of Bothnia exhibits strong phosphorus deciency in primary production, while the almost oceanic saline waters of the Danish Straits are limited by the availability of nitrogen (HELCOM, 2009). Hence, current trends in combating eutrophication emphasize the need for reducing the load of both nitrogen and phosphorus (Howarth and Marino, 2006; Conley et al., 2009a; Paerl, 2009).In the Baltic Sea, there are also internal pro- cesses leading to changes in the budgets of bioavailable nutrients, such as binding of phosphorus to sediment particles and release of gas- eous nitrogen to the atmosphere via denitrication (Gunnars and Science of the Total Environment 409 (2011) 49174922 Corresponding author at: Marine Research Centre, Finnish Environment Institute (SYKE), Erik Palménin aukio 1, P.O. Box 140, FI-00251 Helsinki, Finland. E-mail address: eero.asmala@ymparisto.(E. Asmala). 0048-9697/$ see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.scitotenv.2011.08.030 Contents lists available at SciVerse ScienceDirect Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv

Import–export balance of nitrogen and phosphorus in food, fodder and fertilizers in the Baltic Sea drainage area

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Science of the Total Environment 409 (2011) 4917–4922

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Science of the Total Environment

j ourna l homepage: www.e lsev ie r .com/ locate /sc i totenv

Import–export balance of nitrogen and phosphorus in food, fodder and fertilizers inthe Baltic Sea drainage area

Eero Asmala a,⁎, Laura Saikku b, Sanna Vienonen c

a Finnish Environment Institute, Marine Research Centre, P.O. Box 140, FI-00251 Helsinki, Finlandb University of Helsinki, Faculty of Biological and Environmental Sciences, P.O. Box 65, FI-00014 University of Helsinki, Finlandc Finnish Environment Institute, Freshwater Centre, P.O. Box 140, FI-00251 Helsinki, Finland

⁎ Corresponding author at: Marine Research Centre,(SYKE), Erik Palménin aukio 1, P.O. Box 140, FI-00251 H

E-mail address: [email protected] (E. Asmala

0048-9697/$ – see front matter © 2011 Elsevier B.V. Alldoi:10.1016/j.scitotenv.2011.08.030

a b s t r a c t

a r t i c l e i n f o

Article history:Received 31 December 2010Received in revised form 5 August 2011Accepted 15 August 2011Available online 9 September 2011

Keywords:Baltic SeaEutrophicationPhosphorusNitrogenInternational tradeFood production

Nitrogen (N) and phosphorus (P) are essential elements for life, but in excess they contribute to aquatic eutro-phication. The Baltic Sea is a brackish semi-enclosed sea that is heavily influenced by anthropogenic loading ofnutrients, resulting in a major environmental problem, eutrophication. In this study, the nutrient balance ofthe food production and consumption system in seven countries in the Baltic Sea drainage area was quantifiedfor the period 2002–2005. The food production and consumption system accumulates nutrients in the BalticSea drainage area, due to extensive imports to the system. The average annual net surplus of nutrients was 1800 000 tons N and 320 000 tons P in 2002–2005, or annually 28 kg N and 5 kg P per capita. The average totalannual import was 2 100 000 tons N and 340 000 tons P during 2002–2005. The largest imports to the systemwere fertilizers, totaling 1 700 000 tons N and 290 000 tons P. Traded nutrients in food and fodder amountedto a net annual surplus of 180 000 tons N and 25 000 tons P. The nutrient load to the Baltic Sea due to the foodconsumption and production system was 21% N and 6% P of the respective annual net inputs to the region.This study shows that large amounts of nutrients to Baltic Sea drainage area are inputs from outside the region,eventually contributing to eutrophication. To reduce the nutrient imports, fertilizers should be used more effi-ciently, nutrients should be recycledmore efficiently inside the region, and food system should be guided towardlow-nutrient intensive diets.

Finnish Environment Instituteelsinki, Finland.).

rights reserved.

© 2011 Elsevier B.V. All rights reserved.

1. Introduction

For life on Earth, nitrogen (N) and phosphorus (P) are indispensableelements. They are essential components of e.g. macromolecules aden-osine triphosphate and deoxyribonucleic acid (ATP and DNA), whichcarry energy and genetic information in living cells. Both nitrogen andphosphorus have been used in continuously increasing amounts as fer-tilizers in agricultural production, which in turn has been increasing thenutrient runoff to aquatic environments globally (Compton et al., 2000;Galloway et al., 2004). While their biogeochemistry differs greatly, Nand P enrichment are the cause of eutrophication problems encoun-tered in many freshwater and estuarine and marine systems However,the biogeochemistry of nitrogen and phosphorus differs substantially(Vitousek et al., 2003; Filippelli, 2008).

TheBaltic Sea is a unique brackishwater environment,with a salinityranging from freshwater toward oceanic salinities (mean salinity 7 psu).The Baltic Sea is also a small water body due to its shallowness — itsmean depth is only 54 m (Leppäranta and Myrberg, 2009). These

physical properties combinedwith the influence of the about 90 millioninhabitants of 14 countries in the 1720000 km2 drainage basin result inhigh anthropogenic pressure on the environment and nonuniform eco-logical responses, e.g. to nutrient loading (Tamminen and Andersen,2007). The interplay of the two elements examined in this study, nitro-gen and phosphorus, is highly pronounced in the Baltic Sea eutrophica-tion (Conley et al., 2009a). Eutrophication, i.e. the process of ecologicalresponse to the enrichment of growth-limitingnutrients (specifically ni-trogen and phosphorus) is considered to be the single greatest threat tothe Baltic Sea environment (Elmgren, 2001; HELCOM, 2009). Nutrientenrichment leads to increased primary production, which in turn hasconsequences as alterations in species structure, biodiversity and recre-ational values (Rönnberg and Bonsdorff, 2004).

The low-saline northernmost part of the Baltic Sea, Gulf of Bothniaexhibits strong phosphorus deficiency in primary production, whilethe almost oceanic saline waters of the Danish Straits are limited bythe availability of nitrogen (HELCOM, 2009). Hence, current trends incombating eutrophication emphasize the need for reducing the loadof both nitrogen and phosphorus (Howarth and Marino, 2006; Conleyet al., 2009a; Paerl, 2009).In the Baltic Sea, there are also internal pro-cesses leading to changes in the budgets of bioavailable nutrients,such as binding of phosphorus to sediment particles and release of gas-eous nitrogen to the atmosphere via denitrification (Gunnars and

4918 E. Asmala et al. / Science of the Total Environment 409 (2011) 4917–4922

Blomqvist, 1997; Tuominen et al., 1998). Nitrogen and phosphorus lim-itation has been widely discussed by Elser et al. (2007).

The largest contributors of nutrient loading to the Baltic Sea are dif-fuse loading from agriculture and municipal wastewater treatmentplants, which account for over 90% of both nitrogen and phosphorusloading (HELCOM, 2009). Agricultural practices in the Baltic Sea regionare intensive. In the Scandinavian countries, the separation of crop andanimal production culminated in the1980s in Sweden, Finland andDen-mark (Granstedt, 2000). Also, specialized forms of agriculture based onchemical fertilizers, nonrenewable energy, and pesticide usewere intro-duced. On average in the Baltic Sea region, farms have a high density ofanimals and large surpluses of nutrients (Granstedt, 2000).

Global estimates of nutrient fluxes from agriculture have been stud-ied in general by Vitousek et al. (2009), while Kyllingsbaek and Hansen(2007) focused on the Baltic Sea region of Denmark by and Eriksson etal. (2007) the region of Poland. In addition, there are studies calculatingnutrient balances of food consumption andproduction related to theBal-tic Sea region at different levels: for the EU12 countries in 1988 (Van derVoet et al., 1996), for Finland in 1995–1999 (Antikainen et al., 2005), andfor a Swedish city until 2000 (Neset et al., 2006). However, informationon the nutrient balances of food consumption and the food productionsystem of the Baltic Sea region is scarce, and the data in previous studiesare largely outdated: roughly from the late 1990s or the early 2000s.

To date, no previous studies have examined the Baltic Sea region as awhole or determined the nutrient balances due to trade and inputs offood, fodder and fertilizers. The objective of this study is to identifyand quantify the flows of nitrogen and phosphorus in internationaltrade in the Baltic Sea drainage area as related to food production andthe consumption system. More specifically, the aim is to assess therole of food, fodder, and fertilizers in fluxes of nitrogen and phosphorusin the Baltic Sea drainage area during years 2002–2005. Our results,however, cannot be used as such to representwhat ends up to the BalticSea, as much of the nutrients may be retained in e.g. soil and organicmatter or transformed within the terrestrial system. Therefore, the netbalance results are compared with the reported land-to-sea fluxes.

2. Material and methods

2.1. System definition

In this study, the trade and external inputs related to the food pro-duction and consumption system in the Baltic Sea drainage area wereanalyzed. The time period analyzed covered the years 2002–2005.Seven countries in the Baltic Sea drainage system were included:Denmark, Estonia, Finland, Latvia, Lithuania, Poland, and Sweden. Inall, these countries have 65 million inhabitants, which is app. 70% ofthe total population in the area (Eurostat, 2010). These countriesare almost entirely within the Baltic Sea drainage area. In addition,there are seven other countries that are partially within the water-shed: Belarus, Czech Republic, Germany, Norway, Russia, Slovakia,and Ukraine. We ignored these countries in this study, due to theirsmall proportion of the drainage area, or, in the case of Russia, dueto insufficient availability of data. For instance, Russia respondedwith 14% N and 28% P of the riverine, coastal, and direct point and dif-fuse source inputs of nutrients to the Baltic Sea in the seven countriesexamined during 2002–2005 (HELCOM, 2008). The contribution tonutrient loading from Germany in the Baltic Sea was much lowerthan in Russia. Furthermore, some countries that are included arenot entirely situated in the drainage area.

2.2. Nutrient balance calculation

The nutrient balance of nitrogen and phosphorus for each studycountry was calculated with the following formula:

B ¼ Io−Eo

where B is the balance of nitrogen/phosphorus in the study country, Iothe import of nitrogen/phosphorus from countries outside the BalticSea area, and Eo the export of nitrogen/phosphorus to countries out-side the Baltic Sea area. If BN0, then there is a surplus input of nitro-gen or phosphorus in the study country from outside the Baltic Seadrainage area.

In this study, we ignored trade within Baltic Sea countries, i.e. wedid not include imports from other Baltic Sea countries in the totalbudget. Inputs as imports and outputs as exports consist of food forhuman consumption, animal fodder, and fertilizers for agriculturalproduction. The use of noncommercial, unreported nutrient sources,such as manure and wastewater, were not considered in this study.Food items can be used either as ingredients for food production orbe readily consumed. Imported animal fodder is used in animal pro-duction, mostly in production of animals used for human consump-tion. Fertilizers are used in agricultural plant production, which is inturn directed to food or fodder consumption. These categories applyto both import and export for food and fodder, but only imports aretaken into account for fertilizers. Imports of food and fodder to theseven study countries from outside the area were regarded as importsto Baltic Sea drainage area. Regardless of the origin, fertilizers werecalculated as imports to the system, since atmospheric nitrogen androck phosphorus are outside the biological realm before manufactur-ing them into fertilizers (Smil, 2000; Galloway and Cowling, 2002).

The net balance results are compared with the land-to-sea fluxeswith data from HELCOM (2008). Shares of for different sectors foryear 2000 were available at HELCOM (2004).

2.3. Data sources and quantification methods

2.3.1. Trade dataTrade statistics of fertilizers, fodder, and food were obtained from

the Food and Agricultural Organization (FAO) of the United Nationsstatistical database (FAOSTAT, 2010). Since fertilizers were regardedas imports to the system, fertilizer consumption data were used forall countries. No fish trade statistics were available for all the coun-tries studied. However, we estimated the trade in fish based on thedata available for Finland in all these studied countries (Vihervuori,2003, 2004, 2005, 2006). All items traded were included; these arelisted in Appendix A.

2.3.2. Nutrient content dataThe nitrogen contents were calculated from the protein amount,

using a factor of 0.16 (Block and Bolling, 1946). The protein and phos-phorus contents of food and fodder were mainly obtained from theFinnish Food Composition Database (Fineli, 2009) maintained by theNational Institute forHealth andWelfare and are presented in AppendixA. The nitrogen and phosphorus content in fish are an average of theseven species that comprise over 90% of the annual catch in the BalticSea (ICES, 2009) and are presented in Appendix B. For food waste, themedian of the nitrogen and phosphorus content of all foodstuffs wasused. The nitrogen and phosphorus contents of fertilizerswere calculat-ed, based on the chemical properties of the fertilizers, are presented inAppendix C. Population data for the countries studied were obtainedfrom the statistical office of the European Union (Eurostat, 2010).

3. Results

Combining the food, fodder and fertilizers together, the total annualimports of nutrients related to the food production and consumptionsystem in the Baltic Sea drainage area averaged 2 100 000 tons N and340 000 tons P during 2002–2005 (Table 1). The export from the BalticSea drainage area was 220 000 tons N and 25 000 tons P. This resultedin a net surplus of nutrients: 1 800 000 tons N and 320 000 tons P.

When separating food and fodder, and fertilizers, the internationaltrade in food and fodder resulted in a net import of 180 000 tons N

4919E. Asmala et al. / Science of the Total Environment 409 (2011) 4917–4922

and 25 000 tons P, on average during 2002–2005. Import of fertilizersinto the system totaled 1 700 000 tons N and 290 000 tons P (Table 2).

Net imports of nitrogen and phosphorus in food, fodder and fer-tilizers per capita in the region studied averaged 28 tons N and5 tons P on average (Figs. 1 and 2). Nitrogen import varied fromLithuania's 10 kg per capita to Denmark's 67 kg per capita per year,and phosphorus from Latvia's 2 kg per capita to Estonia's 15 kg percapita per year.

The nitrogen to phosphorus (N:P) ratio of fertilizer consumptionvaries widely between countries, from Denmark's 16 to Lithuania's0.7 (Table 3). The average N:P ratio of fertilizer inputs is 5.7, whilefor food and fodder, the average N:P ratio of net imports is 7.5.

Wheat is the most important imported food item, totaling 13000 tons N and 1400 tons P. Wheat is also the most importantexported food item, with 42 000 tons and 4600 tons of nitrogenand phosphorus respectively. The 10 most important import and ex-port articles are presented in Tables 4 and 5. The food items aresorted by the total amount of nitrogen coming into or going out ofthe system.

The average riverine, coastal, and direct point and diffuse sourceload of nutrients to the Baltic Sea in the seven countries studied during2002–2005was 530 000 tons N and 23 000 tons P, annually. The partic-ular nutrient load due to the food consumption and production system(including wastewater, fish farming and agriculture, and managed for-estry) were estimated as 390 000 tons N and 18 000 tons P (calculatedbased on the year 2000 percentages for different sectors). In compari-son to the net inputs of N and P in food, fodder, and fertilizers in2002–2005 in the studied region, the percentage of the reported loadversus the respective hypothetical net inputs to the Baltic Sea food con-sumption and production system, was 21% for N and 6% for P.

4. Discussion

4.1. Significance of the results

Of all the imports, fertilizers account for an average of 80% and 85%of nitrogen and phosphorus. All individual countries' total imports ofboth nutrients are dominated by fertilizers (N50%), emphasizing the in-dustrial nature of modern food production systems. The net inputs offertilizers per capita varied from 34 kg N (Denmark and Finland) to7 kg N (Lithuania) and from 15 kg P (Estonia) to 2 kg P (Denmark, Lat-via and Sweden). The net input of nitrogen fertilizers varies widely on aglobal scale, from 7 kg ha–1 yr–1 N and 8 kg ha–1 yr–1 P in Kenya to588 kg ha–1 yr–1 N and 92 kg ha–1 yr–1 P in northern China (Vitouseket al., 2009).

Regarding food and fodder, the Baltic Sea drainage area is a netimporter of nutrients. About 2.8 kg N per capita and 0.4 kg P percapita were imported annually on average during 2002–2005. Netimports of nitrogen to the Baltic Sea drainage area were similar tothose of the European Union (EU12) countries in 1988, where the im-port of nitrogen in food and fodder was approximately 4.7 kg per

Table 1Annual average of total nitrogen and phosphorus in imports to the Baltic Sea drainage area

Food, fodder and fertilizers

Import Export

Nitrogen Phosphorus Nitrogen

Denmark 360 057 32 277 99 531Estonia 32 840 20 646 5096Finland 198 270 20 232 13 068Latvia 39 931 5807 6571Lithuania 36 244 39 893 16 298Poland 1 180 444 195 883 47 395Sweden 218 896 27 534 32 885Total 2 066 683 342 272 220 842

person, and the export of 2.1 kg per person (Van der Voet et al.,1996). The net imports per capita for Finland calculated in thisstudy, 5 kg yr–1 N and 0.5 kg yr–1 P in 2002–2005, differ slightlyfrom those of another Finnish study. The annual net imports of nutri-ents in food and fodder in 1995–1999 in Finland were estimated to behigher for nitrogen (about 3 kg N per capita), and lower for phospho-rus (0.1 kg P per capita) (Antikainen et al., 2005). In another compar-ison, the net import of nitrogen in food and fodder in the Netherlandswas 23 kg per person in 1995 (Olsthoorn and Fong, 1998).

There are significant differences in countries' nitrogen and phos-phorus balances per capita, influenced by the production and con-sumption structures. There is no uniform relationship betweentrade and domestic consumption of food in the Baltic Sea countries(FAOSTAT, 2010). Resource intensive meat consumption is fairlyhigh in Denmark, 110 kg per capita in 2005, while in other countriesit varied between 50 and 80 kg per capita. Denmark, Sweden, and Fin-land consumedmore than 90 kg fruits per capita, whereas the EasternEuropean countries all consumed less than 70 kg. However, the lattercountries consumed more vegetables per person. The average annualconsumption of cereals was 127 kg/person, with Denmark, Polandand Lithuania being the most intensive consumers (FAOSTAT, 2010).

Wheat is both the most imported and the most exported food itemto and from the countries in the Baltic Sea drainage area. Other cerealsare also significant food items in the import–export balance. Six out ofthe 10 most important imported and exported food items are commonto all the seven Baltic Sea countries (FAOSTAT, 2010) highlighting theinternational nature of modern food production and consumption sys-tems. Denmark has a heavy meat industry and most of the meat isexported. The flow of food toward the Baltic Sea drainage area is mainlydirected from central and Southern Europe. The most significant coun-try importing food to the Baltic Sea drainage area is Germany, followedby the Netherlands, Spain, and Italy (FAOSTAT, 2010). The appropria-tion of nitrogen and phosphorus resources caused by e.g. food produc-tion can be quantified with footprint approach (Galloway et al., 2008;Lott et al., 2009).

In comparison to the net inputs of food, fodder, and fertilizers in2002–2005 calculated in this study, the percentage output versusthe respective hypothetical inputs to the Baltic Sea was 21% N and6% P. The percentages of nutrients in the Baltic Sea compared withthe net inputs of food, fodder, and fertilizers are consistent with pre-vious estimates for nitrogen (26%) and somewhat smaller than thosefor phosphorus (11%) for Finland (Antikainen et al., 2005). The foodproduction system and related nutrient pathways, accumulation,and leakages are described in detail by Antikainen et al. (2005). InFinland in 1995–1999, an approximately 5-fold amount of nitrogenand 7-fold of phosphorus in fertilizers were applied to the soil com-pared with the amount of nutrients in the food and fodder processingindustry after accounting for the international trade in food and fod-der. In Denmark, the nutrient use efficiency, as total nutrient outputversus total nutrient input, was 37% for nitrogen and 52% for phos-phorus in 2003/2004 (Kyllingsbaek and Hansen, 2007).

2002–2005 (tons yr–1).

Net

Phosphorus Nitrogen Phosphorus

9142 260 527 23 135720 27 745 19 926

2253 185 202 17 979662 33 360 5145

1915 19 946 37 9776538 1 133 049 189 3453978 186 011 23 556

25 209 1 845 840 317 063

Table 2Annual average nitrogen and phosphorus contents in imports and exports of food and fodder, and in imports of fertilizers in to the Baltic Sea drainage area 2002–2005 (tons yr–1).

Food and fodder Fertilizers

Import Export Net Import=net

Nitrogen Phosphorus Nitrogen Phosphorus Nitrogen Phosphorus Nitrogen Phosphorus

Denmark 175 628 20 369 99 531 9142 76 097 11 226 184 430 11 909Estonia 6075 850 5096 720 979 130 26 766 19 796Finland 20 958 4758 13 068 2253 7890 2505 177 312 15 474Latvia 4829 631 6571 662 −1742 −31 35 102 5175Lithuania 10 534 1397 16 298 1915 −5763 −519 25 709 38 496Poland 143 782 16 141 47 395 6538 96 387 9603 1 036 662 179 741Sweden 42 301 5551 32 885 3978 9416 1573 176 596 21 983Total 404 107 49 698 220 842 25 209 183 265 24 489 1 662 576 292 574

4920 E. Asmala et al. / Science of the Total Environment 409 (2011) 4917–4922

The net nutrient inputs to the Baltic Sea drainage area are largerthan the nutrient loading to the Baltic Sea, five times larger annuallyfor nitrogen and 17 times larger for phosphorus. Thus, a significantlylarger proportion of nitrogen than phosphorus resulting from tradetheoretically ends up in the Baltic Sea. This is probably due to themore sparing use of phosphorus in fertilizers and also by the more ef-ficient wastewater treatment processes for phosphorus. Phosphorusis also more effectively adsorbed onto soil, thus reducing the amountof phosphorus that leaches to the aquatic systems from terrestrialones (Sims et al., 1998). The ratio of net flows of nitrogen and phos-phorus per capita in Denmark is 12 and in Estonia and Lithuaniaaround 1, which may result from differences in affluence, agriculturalpractices, and consumption patterns.

4.2. Reducing the input of nutrients to the Baltic Sea drainage area

To reduce the environmental impacts related to nutrients, thecycle of nutrients should be closed and harmful emissions minimized,following the principles of industrial ecology (van der Voet, 2002).Decreasing the contemporary surplus input of nutrients in food, fod-der, and fertilizers to the Baltic Sea drainage area can be attained bydecreasing the volume of the entire food system or by reducing theinputs of fertilizers to the system.

The nutrient inputs to the Baltic Sea drainage area are related tothe demand for food. The intake of the population for nitrogen andphosphorus in food is currently above the level of nutrient intake rec-ommendations. Furthermore, there is projected growth in meat de-mand and consumption in the Baltic Sea area, most likely to lead inincreasing nutrient loading in the drainage, the net effect for total ni-trogen loading ranging from e.g. 3% to 72% throughout the basin(Hägg et al., 2010). Respectively, reducing the nutrient input wouldmainly occur by reducing the intake of animal products and increas-ing the intake of plant products (e.g. Goodland and Pimentel, 2000;Antikainen et al., 2005; Engström et al., 2007). However, changes in

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Import-N Export-N Net-N

Fig. 1. Annual average nitrogen import-export balance of food, fodder, and fertilizers inthe Baltic Sea drainage area 2002–2005 (kg/per capita).

food consumption patterns are slowand difficult to achieve (Thøgersen,2005; Saikku and Asmala, 2010).

The input of fertilizers can be directly reduced by increasing the ef-ficiency of food production and through more efficient use of nutrientsin fertilizers. Influencing the production efficiency can also be achievedthrough agricultural policies, subsidy systems, legislation, and market-ing of agricultural products. The use of nitrogen fertilizers can be re-duced by systematic crop rotation, optimizing the timing and amountof nitrogen fertilizers applied tofields, and developing crops that use ni-trogenmore efficiently, among others (Canfield et al., 2010). Onemeansfor increasing the yields, thus indirectly decreasing the fertilization perunit of product, is to control the water balance and acidity of the fields(Uusitalo et al., 2007). In transitional countries such as Poland, however,the potential for reducing diffuse nitrogen emissions from agricultureby reducing fertilization is constricted in areas with low-nitrogen sur-plus (Eriksson et al., 2007).

Cycling nutrients reduces the need for an external input of fertilizersin multiple food production sectors from crop farming to aquaculture(Asmala and Saikku, 2010). Changing currently practiced conventionalfarming systems, toward low-input recycling systems is one option.Larsson and Granstedt (2010) hypothesized that by transforming exist-ing agricultural practices to ecological recycling agriculture, dramaticreductions in nitrogen and phosphorus surplus (as much as 50% and100% respectively) could be achieved in the Baltic Sea countries. How-ever, this requires further knowledge of costs as well as internationalcoordination on a relatively short term (Larsson and Granstedt, 2010).Economic incentives for using phosphorus fertilizers more sparinglyand implementing technologies for recycling phosphorus are beingimplemented, guided by the scarcity of global phosphate rock reserves.The maximum rate of global phosphorus extraction, the peak phospho-rus, is predicted to occur sometime within this century (Cordell et al.,2009; Tenkorang and Lowenberg-DeBoer, 2009). In addition toprolonging the resource life-time, phosphorus recycling in developed

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Fig. 2. Annual average phosphorus import–export balance of food, fodder, and fertil-izers in the Baltic Sea drainage area 2002–2005 (kg/per capita).

Table 3Annual average nitrogen to phosphorus ratio in food and fodder, and fertilizer net bal-ance in the Baltic Sea drainage area 2002–2005 (w/w).

Food and feed Fertilizers

Denmark 6.8 15.5Estonia 7.5 1.4Finland 3.1 11.5Latvia 56.8a 6.8Lithuania 11.1a 0.7Poland 10.0 5.8Sweden 6.0 8.0Total 7.5 5.7

a Negative values, i.e. net export ratio.

Table 5Most exported food items and the amount of exports of nitrogen and phosphorus fromthe system (tons/yr).

Nitrogen Phosphorus

Wheat 41 618 4557Pig meat 39 783 2159Barley 17 566 2343Cheese 15 527 2026Oats 9458 1601Chicken and turkey meat 5792 265Cattle meat 4817 269Dry onions 2530 395Rye 2101 478Frozen vegetables 1691 287

4921E. Asmala et al. / Science of the Total Environment 409 (2011) 4917–4922

countries also increases the developing countries' percentage of the re-source (Weikard and Seyhan, 2009).

In addition to reducing the nutrient load by decreasing the inputof nutrients to the Baltic Sea Basin, there are other means of combat-ing eutrophication of the Baltic Sea that are however, beyond thescope of this study (e.g. Stigebrandt and Gustafsson, 2007; Conleyet al., 2009b). Some studies have examined agricultural nutrient bal-ances, e.g. Hoang and Alauddin (2010) for the OECD countries. Manyothers have discussed reducing leakage from agricultural fields e.g.Ekholm et al. (2007), while still others have included managementof wastewaters (e.g. Wulff et al., 2007).

It must be noted that in the European Union, there are future plansand targets set to increase the use of renewable energy, including bio-mass for transportation (Beursken and Hekkenberg, 2011). Regardingnutrient balance of the Baltic Sea region, this can either increase theimport of agricultural biomass used for energy, or direct agriculturalproduction toward producing agricultural biomass for energy, in-crease imports of food.

4.3. Sources of uncertainty and setting of system boundaries

Several factors, such as system boundary settings, trade statistics,and nutrient concentration data added uncertainty to our results. Tominimize the signals of interannual variation, we studied an annualaverage of a 4-year dataset. The preparation of FAO statistics isexplained in more detail in (FAOSTAT, 2010). The statistics for Polandand the Baltic countries were gathered after joining the EU in 2004.

There are problems due to inaccurate system definition. The sys-tem defined in this study covers around two thirds of the total popu-lation in the Baltic Sea drainage area (Eurostat, 2010). This probablyled to underestimation of nutrient flows when the Baltic Sea drainagearea as a whole was examined. However, the results were much moreconcise when the seven countries included were considered.

The use of noncommercial, unreported nutrient sources, such asmanure and wastewater, were not considered in this study. For in-stance, the percentage ofmanure has been reported around one fourth

Table 4Most imported food items and the amount of imports of nitrogen and phosphorus tothe system (tons/yr).

Nitrogen Phosphorus

Wheat 13146 1440Barley 6442 860Cheese 4336 566Maize 4046 658Cattle meat 4238 252Pig meat 4131 224Chicken and turkey meat 3966 180Rice 2620 517Rye 1616 389Oranges, orange juice, grapes, etc. 869 174

of total nitrogen fertilization (Neset et al., 2006 for Linköping, Swedenin 2000, Antikainen et al., 2005 for Finland during 1995–1999).

In this study, for simplicity and clearness, we considered only nutri-ents in trade. In reality, when eutrophication is considered, the path-ways of nutrients are highly variable, and there are local differences inwhether the nutrient inputs end up in cities or rural environments.There are also climatic effects related to eutrophication; mostly, rainfalldictates the transport of nutrients from terrestrial systems to the BalticSea. Furthermore, transport systems of nutrients from the catchment tothe Baltic Sea are poorly known.

When commodities are traded, different types of ecological impactsare displaced from one country to another along with the products, af-fecting global ecosystems (Berlik et al., 2002; Mayer et al., 2005).Importing nutrients in food and fodder outsources the environmentalimpacts related to agriculture, in comparison to exporting fertilizers.There are ecological impacts related to eutrophication, as generated inthe production of traded goods, such as leakage from agricultural soiland nutrient emissions in production stages that were not included inthis study. There are also many other environmental issues related tothe food production and consumption system that were not consideredhere. Grote et al. (2005) discussed several policy measures influencingglobal agricultural trade and nutrient imbalances.

5. Conclusions

Along with the international trade in food and fodder and input offertilizers, a surplus flow of nitrogen and phosphorus is directed tothe Baltic Sea drainage area. These net flows amounted to 1.8 mil-lion tons N and 320 000 tons P in 2002–2005 annually on average.The nutrient load to the Baltic Sea due to the food consumption andproduction systemwas 21% N and 6% P when compared to the respec-tive annual inputs to the region. In comparing different sources of ni-trogen and phosphorus loading, it is evident that food production andconsumption system is the main driver of eutrophication in the BalticSea. The need for external nutrient input is decreased through usingfertilizers more efficiently, as well as through reducing the total nutri-ent volume of the food system by reducing the consumption of re-source intensive animal products. Closing the nutrient cycles, i.e.using the nutrients already inside the Baltic Sea drainage areawould offer solutions for decreasing the net inflow of nutrients. Theeutrophication of the Baltic Sea must be dealt with by regarding allrelevant sectors and actors jointly and by considering agriculture,wastewater treatment, and eventually food consumption patterns.Another point for future studies might be tracking of energy contentinstead of nutrients. In this study, we examined the nutrient balanceof trade as related to the food sector and showed that important andrelevant information to environmental policy and decision-makingcan be achieved by determining the material flows in different sectorsand as related to international trade.

Supplementary materials related to this article can be found on-line at doi:10.1016/j.scitotenv.2011.08.030.

4922 E. Asmala et al. / Science of the Total Environment 409 (2011) 4917–4922

Acknowledgments

This work was supported by Research Foundation of the Universi-ty of Helsinki and the Academy of Finland, grant 117822.

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