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Global Environmental Change 38 (2016) 195–204

Contents lists available at ScienceDirect

Global Environmental Change


journal homepage: www.elsevier.com/locate/gloenvcha

Land use biodiversity impacts embodied in international food trade


Abhishek Chaudharya,* , Thomas Kastnerb
a
Institute of Environmental Engineering, ETH Zurich, 8093 Zurich, Switzerland
b
Institute of Social Ecology Vienna, Alpen-Adria Universität Klagenfurt, Schottenfeldgasse 29, Wien, Graz, A-1070 Vienna, Austria

A R T I C L E I N F O A B S T R A C T

Article history:
Received 20 December 2015 Agricultural land use to meet the demands of a growing population, changing diets, lifestyles and biofuel
Received in revised form 14 March 2016 production is a significant driver of biodiversity loss. Globally applicable methods are needed to assess
Accepted 23 March 2016 biodiversity impacts hidden in internationally traded food items. We used the countryside species area
Available online xxx relationship (SAR) model to estimate the mammals, birds, amphibians and reptiles species lost (i.e.
species ‘committed to extinction’) due to agricultural land use within each of the 804 terrestrial
Keywords: ecoregion. These species lost estimates were combined with high spatial resolution global maps of crop
Biodiversity yields to calculate species lost per ton for 170 crops in 184 countries. Finally, the impacts per ton were
Agriculture
linked with the bilateral trade data of crop products between producing and consuming countries from
Global trade
FAO, to calculate the land use biodiversity impacts embodied in international crop trade and
Land use
Sustainability consumption. We found that 83% of total species loss is incurred due to agriculture land use devoted for
Consumption domestic consumption whereas 17% is due to export production. Exports from Indonesia to USA and
China embody highest impacts (20 species lost at the regional level each). In general, industrialized
countries with high per capita GDP tend to be major net importers of biodiversity impacts from
developing tropical countries. Results show that embodied land area is not a good proxy for embodied
biodiversity impacts in trade flows, as crops occupying little global area such as sugarcane, palm oil,
rubber and coffee have disproportionately high biodiversity impacts.
ã 2016 Elsevier Ltd. All rights reserved.

1. Introduction Several international agreements aimed at reducing the current


rate of biodiversity loss have failed to meet their targets (Tittensor
Terrestrial biodiversity fulfills important functions such as et al., 2014). In addition to traditional measures such as setting
pollination, pest control, nutrient cycling and its loss has economic aside areas for species conservation, novel policies aimed at
as well as human health implications (Cardinale et al., 2012; directly addressing the human drivers of biodiversity loss (e.g.
Hooper et al., 2012). The conversion of natural forests has consumption patterns) are required (Lenzen et al., 2012; Tanentzap
negatively affected the flows of many important ecosystem et al., 2015). It is thus important to identify the hotspots of
services, such as carbon storage, water filtration, and habitat agriculture driven biodiversity loss and global food trade flows
provision for biodiversity (MEA, 2005; Foley et al., 2005). The embodying high biodiversity impacts.
International Union for Conservation of Nature (IUCN) red list As the world’s economies are becoming increasingly intercon-
shows that 322 species of vertebrates have gone extinct since 1500, nected, international trade flows of biomass products have been
and approximately 41% of amphibians, 26% of mammals, 13% of increasing (Erb et al., 2009). It is important to inform the consumers
birds, 40% of described invertebrate species and 30% of plant regarding the environmental impacts ‘hidden’ in products they
species are considered threatened with extinction (IUCN, 2014). It consume. Environmentally extended input output analysis is a
has been estimated that agricultural activities negatively impact common tool to assess the impact of traded commodity in the
53% of threatened terrestrial species (Tanentzap et al., 2015). country of origin and upstream supply chains (Wiedmann et al.,
Overall, the current rate of extinction is about 100 times the 2011). Biophysical accounting methods have also been applied to
background extinction rate (Ceballos et al., 2015). trace the origin of consumed products and to assess embodied
natural resource inputs such as land or water use in international
supply chains (MacDonald et al., 2015; Kastner et al., 2014a).
Assessments of carbon emissions embodied in world trade have also
* Corresponding author.
E-mail addresses: abhishek@ifu.baug.ethz.ch, abhinain2010@yahoo.com been carried out (Peters et al., 2011), but similar analyses of
(A. Chaudhary). biodiversity impacts are rare.

http://dx.doi.org/10.1016/j.gloenvcha.2016.03.013
0959-3780/ ã 2016 Elsevier Ltd. All rights reserved.
196 A. Chaudhary, T. Kastner / Global Environmental Change 38 (2016) 195–204

The study by Lenzen et al. (2012) is the first and to this date countryside SAR model. Terrestrial ecoregions were chosen as
only attempt at quantifying biodiversity loss embodied in global spatial units because they contain distinct communities of species,
trade of goods and services. They assessed the species threats and their boundaries approximate the original extent of natural
caused by production of different commodities and combined it ecosystems prior to major land use change (Olson et al., 2001). The
with economic multi-region input output (MRIO) tables to countryside SAR thus predicted the fraction of species lost
evaluate the trade of these threats between countries. Their compared to those occurring naturally prior to human intervention
results showed that industrialized countries are the main in that ecoregion. The total predicted species loss due to land use
importers of threats that occur outside their borders, mainly in was then allocated to individual land use types based on the area
tropical developing countries. However, a similar analysis linking occupied by them within the ecoregion and the affinity of taxa to
biophysical accounting trade databases (e.g. Kastner et al., 2014a) them to derive so called characterization factors (CFs) i.e. the
with biodiversity loss at a global scale is still lacking. Alternative factors indicating biodiversity damage caused by unit area of a
globally applicable methods and metrics to quantify biodiversity particular land use in a particular region.
loss are needed to test the robustness of results obtained by
Lenzen et al. (2012). 1.2. Objective and scope

1.1. Assessing land use impacts on biodiversity This study extends the analysis carried out by Chaudhary et al.
(2015) by combining the CFs (in units—species lost/m2) per
Biodiversity loss due to land use has been studied at different ecoregion for agricultural land with high-resolution maps of
spatial scales  local, regional and global. The estimates of local harvested area and crop yield for individual crops to derive the
biodiversity loss are typically obtained from plot-scale biodiversity impacts per unit mass produced (species lost per ton) for 170 crops
monitoring studies, comparing species richness between the in 184 countries for four vertebrate taxa. We then obtain
disturbed site (e.g. agricultural land) and the natural, undisturbed 170 matrices containing mass of each of the crop traded between
habitat (reference site) of the same region (Gibson et al., 2011). different countries for the year 2011 using FAOSTAT trade database
Such spatial comparisons assume that human intervention have (FAOSTAT, 2015; Kastner et al., 2014a). Finally, the newly calculated
caused the biodiversity differences between otherwise similar impacts per ton at crop level are combined with these trade
sites (Newbold et al., 2015). In order to predict regional and global matrices to assess the biodiversity impacts embodied in interna-
biodiversity loss due to land use, the models describing species- tional food trade and consumption.
area relationships (SARs) are often employed.
Traditionally the classic SAR model, defining species richness as 2. Materials and methods
a power function, S = cAz, (where A is the area, S is the number of
species, and c and z are model parameters), has been used to We here briefly summarize the methodology to calculate the
predict species extinction following habitat loss in a region (Brooks species loss and how to link these estimates to crop products trade
et al., 2002). However it assumes that the areas converted to and consumption (see Chaudhary et al., 2015; Kastner et al., 2011,
agriculture or used for forestry are totally hostile to biodiversity, 2014a for full details). For each taxon g, countryside SAR predicts
thereby overestimating extinctions (Koh and Ghazoul, 2010). There the number of species lost ðSlost Þ caused by all (cumulative) land
is a growing recognition that human-modified habitats also play use within an ecoregion j as a function of the number of species
important role in biodiversity conservation (Karp et al., 2012). Sorg;j occurring in the original natural habitat area Aorg;j as
Alternative models that account for habitat heterogeneity have presented in Eq. (1). Anew;j is the remaining natural habitat area
been proposed to assess patterns of species richness in multi- in the region, hg;i;j is the affinity of taxa g to the land use type i
habitat landscapes such as the matrix SAR model (Koh and (annual crops, permanent crops, pasture, urban, extensive forestry,
Ghazoul, 2010) or countryside SAR model (Pereira and Daily, 2006; intensive forestry), Ai;j is the area of individual land use type i in the
Pereira et al., 2014). ecoregion and zj (z-value) is the SAR exponent:
Unlike classic or matrix SAR, the countryside SAR model 0 1z j
Xn
recognizes the fact that species adapted to human-modified Anew;j þ h  Ai;j
@ i¼1 g;i;j A
habitats also survive in the absence of natural habitat. The Slost;g;j ¼ Sorg;g;j  Sorg;g;j  ð1Þ
Aorg;j
countryside SAR model has recently been proven to perform better
than both matrix and classic SAR in predicting species extinction
hg;i;j is a function of the z-value and the relative local species
from habitat loss in heterogeneous, human modified landscapes
richness of the taxa in land use type i to that in natural forest of the
(Pereira et al., 2014; Proença and Pereira, 2013; Guilherme and
same region (Pereira and Daily, 2006; Pereira et al., 2014). The
Pereira, 2013).
value of hg;i;j for natural habitat is 1 and decreases till zero as land
Using the current extent of land use, the countryside SAR
use becomes increasingly hostile for the taxon (Pereira et al., 2014).
predicts the final, equilibrium level of species extinctions per
The area estimates per ecoregion (Anew;j ; Aorg;j and Ai;j ) were
ecoregion taking levels prior to human intervention as baseline
but does not inform on the timing of extinctions. In other words, obtained from global land use maps (Ellis and Ramankutty, 2008),
SARs provide an estimate of species ‘committed to extinction’ species richness per ecoregion (Sorg;g;j ) from WWF database
(Wearn et al., 2012) rather than species immediately going (WildFinder, 2006), z-values (zj ) from Drakare et al. (2006) and
extinct. The term “extinction debt” has been coined to refer to the taxa affinities ðhg;i;j Þ from global literature review (Chaudhary
future biodiversity losses due to past habitat destruction that et al., 2015). More details on model parameters and their sources
have yet to be realized because of time delays in extinction. are listed in supplementary information.
During this time delay it is possible to take conservation
measures (e.g. restoring habitat) to safeguard the persistence 2.1. Allocating the total species loss to each land use type
of biodiversity that is otherwise committed to extinction (see
Wearn et al., 2012). The species loss due to total land use in an ecoregion j is
Recently, Chaudhary et al. (2015) calculated species lost due to allocated to each land use type i according to their relative area
total land use within each of the 804 terrestrial ecoregions for four share in the current human modified area and the taxa affinity to
taxa (mammals, birds, amphibians and reptiles) using the these land use types in the region through an allocation factor ðai;j Þ.
A. Chaudhary, T. Kastner / Global Environmental Change 38 (2016) 195–204 197

X 6 2.4. Total biodiversity damage due to food consumption per country


Note that ai;j = 1.
i¼1  
Ai;j  1  hi;j Biodiversity impacts caused by food consumption in each
ai;j ¼ X6   ð2Þ country consist of impacts due to use of domestic land plus impacts
A  1  hi;j
i¼1 i;j occurring outside its borders from imported items, minus the
exported impacts. For impacts occurring inside a country we
Combining Eqs. (1) and (2), the characterization factors (CFs) for
multiplied its crop production (in tons) with impacts per ton of
each taxa g, in an ecoregion j are then calculated as:
that crop in that country (Ic;k;g , Eq. (4). For imported impacts, the
Slost;g;j  ai;j crop mass imported was multiplied with corresponding impacts
CF regional;i;j;g ¼ ð3Þ
Ai;j per ton for that crop  country combination.

CFs in equation 3 thus give an estimate of regional species loss (i.e.


2.5. Embodied regional species loss
species ‘committed to extinction’ at the regional level) per m2 of six
different land use types in each of the 804 terrestrial ecoregion
The biodiversity damage associated with each trade flow is
(Chaudhary et al., 2015).
calculated by multiplying the mass traded of each crop from one
country to other with newly calculated impacts (species lost per
2.2. Country-specific biodiversity impacts per ton of crop production ton, Eq. (4)) for that combination of crop and country. This gives the
species loss embodied in individual trade of each crop from
We obtained the harvested area and annual production (Pc;p in exporting to importing country.
tons) of each of 170 crops at a 5 min by 5 min pixel level from
Monfreda et al. (2008) (which follows the FAOSTAT crop 2.6. Characterization factors (CFs) for global species loss
classification system). Pfister et al. (2011) adjusted this crop area
per pixel for multiple cropping, using length of growing season CFs in Eq. (3) give an estimate of regional species loss per m2 of
estimates of each crop in different agro-ecological zones. We used agriculture land use in ecoregion j. However it does not tell if the
this adjusted area occupied by a crop c per pixel p (denoted as Ac;p extinction occurs in that region only or if it is a global extinction. If
hereafter) for further analysis. For each taxon g, the characteriza- a species is endemic to a region, its loss will mean permanent
tion factors per ecoregion (CF g;j ) for annual and permanent crops global extinction. For example consider Region 1 that hosts just the
(Eq. (3)) were taken from Chaudhary et al. (2015) and it was range edges of 10 species as compared to a Region 2 which hosts
assumed that CF value is the same for all pixels p occurring within 10 endemic species (i.e. 100% of their habitat range). Following a
an ecoregion j (i.e. CF g;p ¼ CF g;f 8 p 2 j). human land use intervention, if both regions are made totally
The impact per ton of each crop (Ic;k;g ) was then obtained by unsuitable for these 10 species, the actual biodiversity damage will
dividing the total impact caused by each crop in each country k be more severe in Region 2, as it results in global loss of the
with its total production: 10 species. While avoiding high regional species loss is necessary to
Xn ensure resilience of ecosystem services of the region (Hooper et al.,
p¼1
CF g;p  Ac;p 2012), preventing global extinctions is also important in order to
Ic;k;g ¼ Xn ð4Þ preserve genetic diversity of life on Earth (Mace et al., 2003). In
P
p¼1 c;p order to get an estimate of global (permanent) species extinctions,
Here n is the total number of pixels within the country k and CF g;p is we replaced species richness (Sorg;g;j in Eq. (1)) with number of
the characterization factor for taxa g in pixel p (units—species lost endemic species per ecoregion (Send;g;j ) and calculated another set
per m2). Ac;p and Pc;p are the area (in m2) and production (in tons) of of CFs, hereafter referred to as global CFs. Global species loss per ton
crop c in pixel p. This resulted in a total of 170  184 = 31,280 Ic;k;g were calculated using equations 2–4. Finally, we also quantified the
values. embodied global species loss in international trade flows.

3. Results
2.3. Crop trade
3.1. Country-specific biodiversity impacts per ton of crop production
We first obtained bilateral trade linkages between 184 countries
for 450 agricultural commodities (in metric tons) from FAOSTAT for Table S1 presents the regional biodiversity impacts per ton
the year 2011 (for details see Kastner et al., 2014a). Each processed (Eq. (4)) for each crop and country combination. As not every crop
food and livestock item was first converted into primary crop is grown in every country, the impacts per ton for a total of 8458
equivalents (total of 170 crops) based on factors calculated as the crop  country combinations are calculated. Highest impacts are
ratio of dry matter content of the processed product and the dry observed for cropland use in tropical regions, followed by
matter content of the primary product (for details see Kastner temperate regions and lowest for boreal regions. For all four taxa,
et al., 2014a). Next, using the approach proposed by Kastner et al. the impacts for a particular cropland use varies over six orders of
(2011), we link the (apparent) consumption of each crop product magnitude (104 to 1011 species lost/ton) depending upon the
(including crop product feed embodied in animal product trade) to country. For example, one ton of wheat cultivation in Guatemala
the actual country of crop production, eliminating trade links with results in 2.69  106 mammal species lost as compared to
countries where only processing takes place. For instance, if Swiss 2.90  108 in Estonia (Table S1).
chocolate, made with cocoa beans originating from Ecuador is
exported to China, our trade matrix will show the link between 3.2. Hotspots of biodiversity loss due to agricultural land use
consumption in China and cocoa cultivation in Ecuador. This
resulted in 170 matrices indicating for each of the 184 countries the The impacts per ton were multiplied by volumes of current crop
country of production for the consumed crops (in tons of primary production (in tons) in each country to identify which crop causes
equivalents; including the amount of domestic production for high land-use impacts in each country (Table S2). This enables
domestic consumption). identifying the hotspots of biodiversity loss due to global
198 A. Chaudhary, T. Kastner / Global Environmental Change 38 (2016) 195–204

agricultural land use. Wheat, rice and maize land use contributed cropland use plus imported impacts minus the impacts associated
to 2220 species lost (40% of global agricultural land use impacts). with exported crop items). As expected, populous, biodiversity rich
This was expected because together these three crops occupy 40% nations like China, India, Brazil, Indonesia, Mexico, Nigeria,
of global cropland. However, the crops such as sugarcane, palm oil, Philippines and Thailand with large agricultural area occupy top
coconut, cassava, rubber, and coffee are responsible for surpris- ranks in terms of total biodiversity impacts due to their
ingly high land use driven species loss (together accounting for just consumption (Fig. 1a, Table S3). As domestic land use is used for
below 23% of global impacts) considering the fact that together producing commodities for domestic consumption as well as
they only occupy less than 10% of global cropland. Globally, 70% of exports, we decoupled these impacts. Fig. 1b shows that in terms of
agricultural land use biodiversity impacts are accounted for by the exported impacts—Indonesia, Thailand, India and Malaysia, rank
13 crops (Table S2). There exist important regional differences in very high for all taxa. Cropland use for producing export items
terms of impacts. For example, while wheat in Canada and Russia results in a total of 156, 65, 63 and 62 species lost in these
occupy large areas, their contribution to global biodiversity loss is countries, respectively. The exported impacts differ in terms of
meagre owing to low characterization factors (Eq. (3)) and thus low taxa, e.g. exports from Mexico embody significant amphibian
impacts per ton (Eq. (4), Table S1). Land use for rice, coconut, species loss, exports from Australia high reptile species loss and
rubber and palm oil production in the South-east Asian countries exports from USA, Viet Nam and Argentina are causing significant
Indonesia, Malaysia and Philippines were found to contribute the birds species loss (Table S3).
most to biodiversity loss among all crop-country combinations Next, Fig. 1c shows that imports into the USA and China
(see Table S2 for the full list). embody highest species lost. It is interesting to see that even
countries with smaller populations such as Japan, Germany,
3.3. Total biodiversity damage due to food consumption per country South Korea, UK, France, and Italy—all cause high biodiversity loss
abroad owing to their high per capita consumption and import
Fig. 1a shows the top 10 countries with highest biodiversity levels. We found that in total 83% of total regional species loss
impacts due to food consumption (i.e. impacts due to domestic (4747 species) is incurred due to land use devoted for domestic

a) Consumpon impacts
0 100 200 300 400 500 600 700 800 900

India
Indonesia
China
Philippines
Viet Nam
Brazil
Mexico
Nigeria
USA
Myanmar

b) Exported impacts
0 20 40 60 80 100 120 140 160 180

Indonesia
Thailand
India
Australia
Malaysia
Viet Nam
USA
Brazil
Sri Lanka
Ecuador

c) Imported impacts
0 20 40 60 80 100 120 140

USA
China
Japan
Germany
India
South Korea
Indonesia
Russia
Italy
France

Fig. 1. Top ranking countries for biodiversity impacts due to consumption, exports and imports. Unit: number of species lost (regional species loss estimate). See Table S3 for
full list.
A. Chaudhary, T. Kastner / Global Environmental Change 38 (2016) 195–204 199

Table 1
Top-ranking net importers and net exporters of biodiversity impacts. Group I (‘importers’) consist of nations where biodiversity impacts rest more abroad than domestically
and whose exports embody little impacts. Group II (‘traders’) countries are that both import and export biodiversity impacts. Countries in group III (‘exporters’), export
significant impacts but import little from abroad. Group IV (‘domestic-oriented’) comprises of countries with relatively little engagement in global biodiversity trade. Unit:
number of species lost (regional species loss estimate). GDP per capita values are in US$ for the year 2011 (IMF, 2011). See Table S4 for full list.

Country Total Consumption impacts Of which Exported impacts Imports–exports Group GDP/capita

Domestic Imported
China 489 382 107 13 94 II 6091
USA 181 66 115 46 68 II 51749
Japan 78 20 58 0 58 I 46720
Germany 46 3 43 2 41 I 41863
South Korea 32 2 29 0 29 I 22590
Russia 59 33 26 6 20 II 14037
Italy 47 21 26 6 20 I 33072
U.K 33 11 22 3 19 I 39093
France 27 4 23 5 19 I 39772
Saudi Arabia 17 1 16 0 16 I 25136

Indonesia 529 503 27 156 129 II 3557


Thailand 129 123 6 65 58 III 5480
Australia 36 31 6 62 57 III 67556
Malaysia 70 50 20 62 42 II 10432
Ecuador 42 41 1 36 35 III 5425
Brazil 222 213 9 44 35 III 11340
Sri Lanka 73 70 3 36 34 III 2923
Viet Nam 224 208 17 49 32 II 1755
India 785 751 34 63 29 IV 1489
Cameroon 46 45 2 25 23 III 1167

consumption whereas 17% due to export production (a total of Kong etc.) and European industrialized countries such as Germany,
969 species). France, Austria, Netherlands, Belgium, Sweden, Norway, Finland
and Denmark where 80–99% of impacts occur through imported
3.4. Synthetic typologies of biodiversity trade items. For example, total German food consumption was estimated
to result in 46 species lost, of which 43 are from imported food
Table 1 below shows the ranking of countries in terms of net items (Table 1).
biodiversity impacts imported (= imported  exported impacts). The second group consists of nations that both import and
Countries that export more impacts than they import are net export biodiversity impacts. These countries include USA, Canada,
biodiversity exporters, and vice versa. Following the approach by Malaysia, Spain, China (Table S4) who often trade oil crops or other
MacDonald et al. (2015), we also divided the countries into four high-value commodities with staple crops. For example, Canadian
major groups depending upon the relative role they play in imports embody 15 species lost (mainly through rubber imports
agricultural globalization and the trade of biodiversity impacts (see from Indonesia and coffee from Mexico, Colombia, and Guatemala)
Table 1, Table S4). In the first group are those where the majority of and its exports cause 19 species loss domestically (mainly through
biodiversity impacts rest abroad rather than domestically and rapeseed and wheat destined for China, Japan and USA).
whose exports embody little impacts. This includes small countries In group III lie countries exporting significant biodiversity
with negligible arable land (e.g. Singapore, Saudi Arabia, Hong impacts but importing little impacts from abroad. For example,

Table 2
Top-ranking bilateral international trade flows in terms of embodied biodiversity impacts, major crops causing the impact and their ranking in terms of embodied cropland
area (see Table S5 and S6 for full list). Unit: number of species lost (regional species loss estimate).

Impacts in Driven by Mammals Birds Amphibians Reptiles Total Major causes Rank area
Indonesia USA 7 5 2 6 20 Rubber, cocoa, coffee 23
Indonesia China 8 5 2 6 20 Palm oil, rubber 26
Mexico USA 7 4 2 5 19 Coffee, vegetables, fruits 32
Indonesia India 7 4 2 5 18 Palm oil, cashew, nuts 22
Thailand China 8 4 1 3 16 Rubber, cassava, fruits 15
Malaysia China 7 4 2 3 15 Palm oil, rubber 46
Indonesia Japan 5 3 1 4 13 Rubber, coffee, cocoa 54
Ecuador USA 5 3 2 3 13 Cocoa beans, coffee 189
Viet Nam China 4 3 1 1 10 Cassava, rubber, rice 108
India China 3 4 0 1 9 Cotton, castor, rapeseed 9
USA China 2 5 1 1 9 Soybean, cotton 1
Australia Indonesia 1 4 0 2 8 Wheat 11
Australia Japan 1 4 0 2 7 Wheat, barley 10
Brazil China 2 1 2 1 7 Soybean 2
USA Mexico 2 4 0 1 7 Wheat, soybean, sorghum 3
Guatemala USA 2 1 1 2 6 Coffee, bananas 243
Indonesia Germany 2 2 1 2 6 Palm oil, rubber, coffee 125
Viet Nam Indonesia 3 2 0 1 6 Rice 154
Indonesia S. Korea 2 1 1 2 6 Rubber, coconut, palm oil 156
Sri Lanka Russia 2 1 1 2 6 Tea 966
200 A. Chaudhary, T. Kastner / Global Environmental Change 38 (2016) 195–204

exports from Thailand are responsible for 35% of total species lost 3 countries in terms of total consumption impacts (Fig. 1a), they
domestically while imports account for just 5% of their total rank way lower at 79, 20 and 136th position respectively in terms
consumption impacts. At the extreme end of this group are of per capita consumption impacts. On the other hand,
Australia, Argentina, and Paraguay whose exports actually embody Luxembourg ranked 146th when total impacts were considered
more species loss than incurred due to land used for their domestic compared to 22nd position in terms of per capita impacts.
consumption (Table S4). Biodiverse Central American or Caribbean countries such as Belize,
Group IV comprises of countries that have relatively little Suriname, Panama, Jamaica and Haiti suffering high species loss
engagement in global biodiversity trade. Here both the exports and and with small populations come at top with respect to per capita
imports embody little impacts and the local consumption is mainly impacts (Table S4).
met through crops grown domestically. These domestic-oriented
countries lie exclusively in SE Asia (e.g. Myanmar, Nepal), Africa 3.5. Embodied impacts in bilateral trade links
(e.g. Nigeria, Tanzania) and Caribbean (e.g. Haiti, Jamaica).
In general, industrialized countries with high per capita GDP Table 2 shows the top 20 trade flows in terms of embodied
tend to be major net importers of biodiversity impacts, while many regional species loss (see Table S5 for full list) along with the
developing tropical countries suffer habitat degradation and major crops causing biodiversity damage in the exporting
consequent biodiversity loss for the sake of producing crop items country. Exports from Indonesia and Mexico to USA embody
for exports. Average GDP per capita for group I countries stood at highest impacts (20 and 19 species lost respectively). Exports
31,000$ as compared to 11,200$ (group II); 9258$ (group III) and from Brazil, Thailand, Malaysia and Indonesia to China also cause
3700$ for group IV (IMF, 2011). high species loss. For amphibian species loss, exports from Brazil
In terms of imported impacts per capita, 35 out of top to China show the highest values. For reptiles, exports from
40 countries belonged to group I signifying their high consumption Australia to Japan and Indonesia were identified as having
levels (see Table S4). While India, Indonesia and China were top significant impacts.

Fig. 2. (a) Total biodiversity impacts imported by the United States from different countries and, (b) total impacts exported by Indonesia to other countries. Unit: number of
species lost (regional species loss estimate).
A. Chaudhary, T. Kastner / Global Environmental Change 38 (2016) 195–204 201

The main crops causing high impact of these bilateral links are 3 global extinctions (rank 32nd) compared to 106 regional
also shown in Table 2. Exports of rubber from Indonesia to USA extinctions (rank 13th).
alone is responsible for a total of 14 species lost at the regional We found that in total 81% of total global species loss
level, while oil palm exports from Indonesia, Malaysia to India, (514 species) is incurred due to land use devoted for domestic
China and Pakistan also embody high species loss. Rubber exports consumption whereas 19% due to export production (a total of
from Indonesia, Thailand and Malaysia to China, USA and Japan 117 species). Overall, the synthetic typologies as listed in Table 1
also cause high impacts on biodiversity. In addition, land used for above changed little when global extinctions are considered. Note
coffee and cocoa exports from the Central American countries that SAR gives an estimate of total species loss within a region but
Mexico, Colombia, Ecuador to the USA are identified as causing doesn’t tell which species are lost. Therefore with our approach, we
high species loss. Also, tea exports from Sri Lanka to Russia were are not able to tell how many species in the regional estimate are
identified as having high impact on amphibians and reptiles (full lost in all the regions they occur in. As a result, the estimated global
list in Table S6). extinctions are a conservative estimate as they consider only
It is interesting to note that the embodied cropland use area species strictly endemic to individual ecoregions.
between countries is not a good proxy for embodied biodiversity
impacts. As shown in Table 2, in terms of embodied land, exports 4. Discussion
from Ecuador to USA rank 189 (0.28 million ha) but in terms of
species loss, it ranks 8th among all international trade flows. 4.1. Methodological aspects
Similarly, agricultural goods exports from Canada to USA embody
3.6 million ha land (5th highest) but this trade flow ranks 36th in The study is first to quantify the land use driven biodiversity
terms of embodied total species loss (Table S6). impacts embodied in internationally traded crop items by
The international trade in biodiversity impacts can be visual- combining ecological models with biophysical trade flows. We
ized using global maps. Fig. 2 below illustrates the flows of used countryside SAR model along with high-resolution spatial
embodied biodiversity impacts for two countries: imports to the information on global crop area and production to calculate
USA and exports from Indonesia. US imports are responsible for a regional species extinctions per unit mass of each crop produced in
total of 115 species lost abroad mainly in Mexico and Indonesia but each country. These impacts were linked with international food
also in Ecuador, Colombia, Guatemala and Costa Rica (Fig. 2a). In trade and consumption data to identify trade flows embodying
Indonesia 156 species are lost due to land use devoted to export high biodiversity damage. Note that SARs provide an estimate of
production—mainly destined for USA, China and India followed by species ‘committed to extinction’ (Wearn et al., 2012) rather than
Japan, Germany, South Korea and Malaysia (Fig. 2b). species immediately going extinct. This implies that not all the
calculated extinctions have already taken place and the producing
3.6. Global species loss countries can still act towards preventing a part of them.
Additionally, we also estimated the embodied global extinctions
Table 3 shows the global (=endemic) species loss embodied in by considering only endemic species which are unique to each
bilateral crop item trade flows between different countries (see ecoregion and thus highly vulnerable to any future habitat loss.
Table S7 for full list). It can be seen that the ranking of several trade This study corroborates the findings of earlier researchers
flows changed compared to regional species loss. For example, (Lenzen et al., 2012) and shows that imported agricultural goods
exports from Sri Lanka to Russia and from the Philippines to the are causing significant loss of biodiversity in the country of origin
USA now rank 3rd and 8th respectively in terms of embodied global and highlighted the major crops in different countries causing high
species extinctions in contrast to ranks 20 and 31 when embodied biodiversity extinctions (Table S2). This information is useful for
regional extinctions were considered. Conversely, exports from producing countries to identify the hotspots of species loss within
USA to Mexico ranked 15th in terms of regional species loss but their borders and perhaps become a starting point for further in-
appear only at position 288 in the global loss rankings (Table S8). depth investigations aimed at designing specific mitigation
Table S7 shows the total global species loss caused by food measures. For example, many of the crops responsible for high
consumption in each country along with global extinctions damage have below par yields (tons/ha) owing to technological or
exported and imported. Here also the ranking of countries other factors in the country of production (Mueller et al., 2012;
changed: for example, Haiti now ranks 8th in terms of total Pradhan et al., 2015). If yields were raised, some of the existing
consumption impacts (19 global species extinctions) while it agricultural area could be abandoned and left for regenerating,
ranked 29th when the regional species loss was considered thereby benefitting local biodiversity. This would need, however,
(Table S7). On the other hand, Bangladesh’s consumption results in accompanying measures to ensure that higher yields do not fuel
overall production (and area) increases due to increased

Table 3
Top-10 international supply chains in terms of embodied global (=endemic) biodiversity impacts and comparison with embodied regional species loss ranking. See Table S8
for all flows. Unit: number of species lost (global species loss estimate).

Impacts suffered in Driven by Global species loss Trade flow rank for regional species loss
Ecuador USA 3 8
Indonesia USA 2 1
Sri Lanka Russia 2 20
Brazil China 2 14
Indonesia China 2 2
Mexico USA 2 3
Malaysia China 2 6
Philippines USA 2 31
Indonesia Japan 2 7
Indonesia India 2 4
202 A. Chaudhary, T. Kastner / Global Environmental Change 38 (2016) 195–204

profitability of agriculture (Rudel et al., 2009). Our results also these pathways and quantify the resulting species loss. Hence our
allow for comparing similar crop items from different countries results likely underestimate the biodiversity impacts traded.
(Table S1). Countries experiencing high rates of biodiversity loss Projects such as world food LCA database (Peano et al., 2012)
and looking to expand their cropland area may avoid future aim to gather detailed environmental emissions data for several
extinctions by considering importing the corresponding crops food items and thus will be useful in future to assess complete
grown in countries with low impacts per ton. impacts associated with them. In this regard, the estimates by
On the consumption side, the results are relevant to countries Lenzen et al. (2012) are more complete as they also account for
such as China, USA, Germany, Japan (Table 1) to help identify the other threats caused during different stages of food production.
most damaging imported items such as rubber, soybeans, palm oil,
coffee and their origins (Tables 2 and 3). For example, China, 4.3. Limitations and data gaps
importing soybean for use as livestock feed, could encourage its
population to adopt change from meat towards more environ- The input data used to calculate species extinctions through
mentally benign dietary options, thereby helping to reduce the SAR model come with uncertainties and limitations that should be
biodiversity damage occurring in exporting tropical countries such considered when interpreting the results. For example, the species
as Brazil. Here a nutritional assessment of traded food items will be affinity estimates (hg;i;j , Eq. (1)) were derived from empirical data
useful to guide such policy changes (D’Odorico et al., 2014). Using from global literature review (see Chaudhary et al., 2015). As more
human-edible crops to feed animals has been shown to be an plot-scale local biodiversity monitoring data becomes available
inefficient way to provide calories to humans (Cassidy et al., 2013). (e.g. PREDICTS database, Hudson et al., 2014), these estimates can
be updated and accuracy of results can be improved.
4.2. Comparison of results with existing studies While the crop trade data was obtained from FAOSTAT for the
year 2011, the yield and harvested area maps used to derive
Our approach provides an alternative to that of Lenzen et al. impacts per ton (Eq. (4)) were based on the year 2000 available
(2012) who used an economic MRIO model to explore embodied from Monfreda et al., 2008. Yields of some crops might have
biodiversity impacts in global supply chains. In the MRIO approach increased (or decreased) over last decade. Thus we might have
impacts are connected to final consumption based on monetary over- or underestimated some of the traded impacts but currently
links between economic sectors of countries or world regions. In these maps are the best available source for high resolution impact
contrast, we apply purely biophysical accounting methods based assessment of global cropland use. Next, our trade and consump-
on bilateral trade links of crops and products processed from them. tion data only covers the crop portion of livestock feed but does not
Studies have shown different results based on whether MRIO or include data on pasture land use associated with livestock
purely biophysical approaches are used to determine the land area products, implying that biodiversity impacts due to livestock
associated with traded crop items (Kastner et al., 2014b; Bruckner grazing are not accounted for. Additionally, our account does not
et al., 2015) with both approaches having their pros and cons. Our include areas planted to fodder crops such as alfalfa or clover
results indicate that China is a net cropland and biodiversity (Kastner et al., 2014a).
impact importer (Table 1). In contrast, recent MRIO studies based Limitation of using species richness loss as an indicator of
on monetary trade data predict that China is a net exporter of biodiversity damage as in our study is that complex changes in
embodied cropland (Weinzettel et al., 2013; Yu et al., 2013) and composition and community structure that are commonly caused
also a net exporter of biodiversity impacts (354 threats imported by human land use are not accounted for. Biodiversity indicators
vs. 434 exported, Lenzen et al., 2012). Reasons for these disparities that compare compositional (e.g., Sørensen’s similarity index,
include, on the one hand, the coarse sector aggregation of current Sørensen, 1948) or population (mean species abundance, Alke-
MRIO models that lump together crops with very different made et al., 2009) changes in the species community between a
economic value compared to the product level resolution of reference and agricultural land use, could reveal further insights
purely biophysical accounts. On the other hand, the purely and identify additional/different trade flows embodying high
biophysical approach used by us does not take into account flows impacts. However, monitoring data required for such indicators is
associated with more complex supply chains (e.g., biomass used in rarely available on a global scale for multiple taxa. Future studies
the production of cars). should explore these alternative measures of biodiversity. Further,
Recent review by Bruckner et al. (2015) concluded that owing to the lack of species richness per ecoregion data in the IUCN
biophysical accounting such as employed in this study is more and WWF databases, we could not calculate the impacts on
appropriate for land footprint analysis of food products that invertebrates, fungi and bacteria that contribute to several
typically undergo only a few processing steps, as well as when ecological services and together make up 80% of global terrestrial
aiming at a detailed product resolution. MRIO accounting as used species.
by Lenzen et al. (2012) on the other hand is more suited for the
analysis of land flows embodied in non-food land-based products 5. Conclusions
such as wood products, paper, biofuels, textiles, and leather.
In this study, we calculated species extinctions in different Our results are potentially useful to both, decision makers in
ecoregions due to total land use (equation-1) and then allocated countries currently importing or exporting biodiversity impacts.
the total species loss to agriculture land use in that region Whether the responsibility for reducing the impacts lies with
according to the species affinity to them (Eq. (2)). However, apart producing or consuming countries is a subject of debate (Liu,
from agriculture land use impacts on biodiversity through habitat 2015). Producers control production methods and exert the
loss/degradation, crop production also causes biodiversity damage impacts but consumer demand and lifestyle drives production, so
through other environmental pathways. For example, fertilizer that responsibility is shared between them (Lenzen et al., 2007).
run-off from fields leads to eutrophication of rivers affecting While some countries are totally reliant on imports because of
aquatic biodiversity (MacDonald et al., 2012). Irrigation water use land and resource constraints (e.g. Hong Kong, Saudi Arabia etc.),
might lead to water scarcity in the region (Hoekstra and countries such as Germany, France could theoretically reduce the
Mekonnen, 2012), while pollution from machinery use on farm displaced impacts abroad by devoting more of their domestic
and during processing, transport of crops can also negatively affect resources to local crop production (Fader et al., 2013). Reducing the
flora and fauna. It was beyond the scope of this study to model
A. Chaudhary, T. Kastner / Global Environmental Change 38 (2016) 195–204 203

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