Forum
Globalizing Conservation Efforts
to Save Species and Enhance
Food Production
RICARDO DOBROVOLSKI, RAFAEL LOYOLA, GUSTAVO A. B.
AND MIGUEL B. ARAÚJO
da
FONSECA, JOSÉ A. F. DINIZ-FILHO,
If the growing needs of humans are to be met, food production must increase; however, increasing food production will further compromise
biodiversity. Can this seemingly irreconcilable conflict be mitigated? The solutions proposed so far include reducing food waste and closing yield
gaps. Here, we investigate an alternative approach to reducing the impact of agricultural expansion on biodiversity without compromising food
production by combining two strategies: taking agricultural production into consideration to solve the biodiversity crisis and promoting the
definition of protected areas on the basis of a globalized blueprint. We found that combining these strategies could result in a 78% reduction
in the agricultural opportunity costs incurred in the implementation of protected areas. Furthermore, a 30% increase in biodiversity protection
could be achieved. We show that the movement toward global governance of natural resources would lead to reduced conflict between the needs
of food production and biodiversity conservation.
Keywords: agriculture production, biodiversity conservation, conservation conflict, food security, spatial conservation prioritization
E
arth is home to over 7 billion people, and this number is expected to increase to 10.6 billion by 2050 (UNPD
2011). Approximately 842 million people are chronically
malnourished or lack access to food (FAO 2013). Improving
the well-being of people in a world with an increasing
population will inevitably lead to increased pressure on
natural resources. Agriculture already accounts for 24% of
Earth’s primary net productivity and 30%–35% of global
greenhouse gas emissions; moreover, agriculture uses 70%
of the freshwater and 38% of the ice-free surface on Earth,
representing its largest land use, which has a direct impact
on biodiversity (for a review, see Foley et al. 2011, Balmford
et al. 2012). Feeding an increasing human population with
a rising per capita consumption while sustainably managing the environmental externalities of agriculture is one of
the greatest challenges of human society. Ecologically and
sustainably intensifying agricultural production (Cassman
1999, Tscharntke et al. 2012, Garnett et al. 2013), reducing
food waste, shifting diets, increasing agricultural resource
efficiency, closing yield gaps (Foley et al. 2011), and fostering organic agriculture (Seufert et al. 2012) might contribute
to the solution. However, if the current rates of converting
natural habitats into crop landscapes for food production
remain unchanged, greater threats to biodiversity are inevitable. The critical question is whether food production needs
can be met without further compromising biodiversity.
Spatial conservation priorities are mostly determined
at the national level, but priorities constrained by political
boundaries can lead to poor returns on the investment in
comparison with unconstrained conservation solutions (e.g.,
Rodrigues and Gaston 2002, Araújo et al. 2007, Vazquez
et al. 2008, Kark et al. 2009, Moilanen et al. 2013). Examples
of conservation priorities that are defined across the political
boundaries of individual countries include the Natura 2000
Networking Programme, designed by the European Union
to complement individual countries’ protected areas (Araújo
et al. 2011), and the Mesoamerican Biological Corridor,
which is designed to create a common network of protected
areas in eight countries (Holland 2012). However, these initiatives are the exception rather than the norm. Conservation
strategies tend to be implemented mostly at the subnational
and national levels, and they are rarely informed by prioritization blueprints that are intended to effectively allocate
limited financial resources for the conservation of globally
relevant biodiversity (Zimmerer et al. 2004). Here, we argue
that the lack of globalized planning may lead to an ineffective distribution of efforts dedicated to both expanding food
production and protecting biodiversity.
It has been argued that conservation actions such as the
creation of protected areas may negatively affect the development of the surrounding communities and the countries
in which they are implemented (Adams et al. 2004, McShane
BioScience 64: 539–545. © The Author(s) 2014. Published by Oxford University Press on behalf of the American Institute of Biological Sciences. All rights
reserved. For Permissions, please e-mail: [email protected].
doi:10.1093/biosci/biu064
Advance Access publication 14 May 2014
http://bioscience.oxfordjournals.org
June 2014 / Vol. 64 No. 6 • BioScience 539
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et al. 2011, but see Andam et al. 2010). Therefore, if a globalized conservation blueprint implies greater conservation
coverage in countries that are poor, underdeveloped, or
economically dependent on agriculture, it would be more
difficult to persuade such countries to agree to this globalized conservation strategy. In addition, the effects of losing
food production would be intensified for these countries,
because they tend to have fewer economic alternatives.
Consequently, forecasting the economic winners and losers
of globalized conservation strategies would help clarify the
difficulty of implementing a politically integrated conservation blueprint in different parts of the world and would
help in the designing of compensation policies that would
encourage countries to agree to larger conservation areas in
their territories without compromising their development.
In this study, we compared blueprints for global conservation and food production obtained by aggregating national
or regional priorities to a global extent and comparing them
with blueprints obtained by optimizing global conservation and food production. Our response variables were
the relative amount of food production lost (agricultural
opportunity cost) and the representation of the geographic
distribution of species in each blueprint. We also examined
whether the poorest countries, the least developed countries, or those countries with economies more dependent
on agricultural production are exposed to higher losses in
food production as a consequence of a high percentage of
their land area’s being assigned to conservation under the
global strategy.
We overlaid the geographic ranges of 5216 terrestrial
mammal species obtained from the International Union for
Conservation of Nature’s Red List of Endangered Species
(www.iucnredlist.org/initiatives/mammals) onto a grid with a
spatial resolution of 0.5 degrees (°) × 0.5°. We considered a
species to be present in a cell if any of its mapped distribution occurred in the focal grid cell.
We chose mammals because they are the focus of many
conservation programs (Trimble and Aarde 2010). Among
mammals, there are many species that are charismatic,
conservation “flagships,” or potential “umbrellas” for the
conservation of other species (Redford et al. 2011). In addition, approximately one-quarter of all mammal species are
threatened with extinction, and this situation is far from
improving (Hoffmann et al. 2011). Finally, this group is often
considered to represent a potential surrogate for other taxonomic groups (e.g., Lamoreux et al. 2006, Qian et al. 2008).
We created maps of potential agricultural production in the
twenty-first century by synthesizing two maps: the extent of
agriculture and potential productivity (supplemental ­figure S1).
The areas forecast to be in use for agricultural production
in the twenty-first century were defined according to the
land-cover map produced by the Integrated Model to Assess
the Global Environment (IMAGE, version 2.2, Netherlands
Environmental Assessment Agency, Bilthoven), which incorporates six socioeconomic scenarios (from Nakićenović et al.’s
2000 Special Report on Emissions Scenarios [SRES] report).
540 BioScience • June 2014 / Vol. 64 No. 6
The SRES scenarios represent different socioeconomic
storylines, or development pathways, that human societies can follow. These scenarios represent combinations of
changes in technology, policy, economy, lifestyle, and political integration and are used as inputs to model different
processes, such as climate change and land use. All SRES
scenarios are deemed equally probable. IMAGE uses these
scenarios to construct land-use maps. We combined the
60 IMAGE maps, at a resolution of 0.5° × 0.5°, from 2010
to 2100 (one map for every 10 years across six scenarios) to
produce an average map for agricultural expansion in the
twenty-first century (see Dobrovolski et al. 2013).
Information on the productivity of agricultural lands was
obtained from Fischer and colleagues (2008). We assumed
maximum productivity (100%) for all grid cells unless the
environmental constraints related to climate, relief, or soil
were defined by Fischer and colleagues (2008). Moreover,
we added information on the impact of irrigation, which
represents a potential gain in productivity (see Naidoo and
Iwamura 2007 for a similar approach). Therefore, we defined
the total global production (P) as
P = ∑piaiti + wi(piaiti),
where pi is the productivity of cell i of the area determined
by environmental constraints, a is the area of the grid cell,
t is the average time that the grid cell is cultivated over the
twenty-first century and across all six SRES scenarios, and
w is the proportion of the productivity that can be added
by irrigation. All of the results shown here are presented
as a proportion of the total agricultural production for the
twenty-first century.
We defined the global spatial priorities for mammal
conservation using Zonation (version 3.0.5, Conservation
Biology Informatics Group, Helsinki, Finland; http://
cbig.it.helsinki.fi/software/zonation; Moilanen et al. 2011).
Zonation’s original core-area algorithm provides a maximum utility conservation solution and generates a nested
hierarchical ranking of the study area, which maximizes
the highest occurrence level (here, the presence or absence
of data for mammal species) divided by the cost of the cell
(here, the potential agricultural production) and accounting
for complementarity in species’ ranges (see Moilanen et al.
2011). Zonation’s original core-area removal rule considers
sites that contain higher proportions of species’ geographical
distribution to be more valuable, thus favoring the rarest species in the final solution. Zonation is also able to incorporate
mask files, which can be used to guarantee that specific areas
of interest (e.g., a country or a region) are prioritized.
To evaluate the effect of incorporating agricultural costs
in setting conservation priorities, we developed two different
conservation solutions. We developed the first solution without considering any cost layer (the costs of all sites were set to
be equal), focusing on obtaining the maximum possible coverage of mammal biodiversity. We found the second solution
by constraining the prioritization process with agricultural
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potential production. Therefore, given the same biodiversity
importance of two sites (e.g., presence of the same species),
the site with the lowest cost (i.e., potential agricultural productivity) has the highest value for conservation.
We evaluated the effect of political integration by performing, within each of the two approaches above, conservation prioritization analyses at the national, regional,
and global scales. For the global approach, we generated a
global conservation solution as if there were no political
boundaries. We created a regional approach by integrating
the conservation solutions that were found separately for
each group of countries, which were integrated according
to current economic blocks (e.g., the European Union, the
North American Free Trade Agreement, the Union of South
American Nations) using mask files in Zonation. This political scenario is based on the assumption that the economic
integration represented by these blocks can lead to common
conservation strategies across member states. The national
approach is the result of the integration of the best conservation solutions obtained individually for each country
using mask files in Zonation. The latter political scenario
­represents the business-as-usual conservation strategy.
Given the ongoing debate of how much is enough in
terms of area requirements for conservation (e.g., Soulé and
Sanjayan 1998), we developed different spatial conservation
targets, from 5% to 50% and with 5% intervals in between.
However, following the Convention on Biological Diversity
(CBD 2010), which proposed that 17% of the terrestrial
areas should be protected until 2020, we focused our analyses on the cutoff of 17%.
To compare the different conservation solutions, we evaluated conservation benefits by calculating the mean proportion of the geographical range of the species that would be
protected if each conservation solution were implemented
and the agricultural opportunity cost as the percentage
of the global productivity in the twenty-first century that
would be lost for each conservation solution. Furthermore,
we investigated whether the differences in the proportion
of the species’ geographical range protected would preferentially affect those species with the smallest ranges. We
performed an analysis of variance using the proportion
of geographical range protected for the species within the
lowest quartile of the range–size frequency distribution
(the 25% of species with the smallest range) as the response
variable and the conservation strategy (national, regional, or
global) as the independent variable.
To investigate the relationship between agricultural losses
and the development of countries participating in a globalized conservation blueprint, we correlated the percentage
of food production and area loss (productive or not) due
to sparing land for biodiversity conservation with three
development indicators: the Human Development Index
­
(HDI; http://hdr.undp.org/en/data), the per capita gross
domestic product (GDP), and the percentage of GDP added
by agriculture (the latter two obtained from the World Bank;
http://data.worldbank.org/indicator).
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When conservation areas for mammals were selected at a
national scale without considering the potential agricultural
production, 17% of the most suitable areas would overlap
with those that were predicted to produce 18.9% of the
world’s food throughout the twenty-first century. Selecting
at a regional scale, 24.1% of global food production would be
lost for conservation purposes. Selecting at the global scale,
27.6% of agricultural lands would be off limits to food production (figure 1a). However, if the selection of priority sites
were constrained by food production, they would overlap
with only 4% of global food production when selecting at a
national scale, with 4.2% at a regional scale, and with 4.2%
at a global scale (figure 1a). We found that, when searching
for 17% of the terrestrial area that maximized the conservation of mammals in the globalized conservation blueprint,
explicitly avoiding conservation in productive arable lands
could lead to a 78% reduction in the loss of agricultural
production (figure 1a).
When conservation priorities are identified without consideration of agricultural production, the conservation benefits are the highest for the global-scale strategy (64.2%
of species’ geographic ranges protected versus 51.5% and
35.6% with regional and national solutions, respectively;
figure 1b). However, as was indicated above, the conflict
between food production and conservation is higher when
priorities are established globally rather than regionally or
nationally. However, when agricultural production is taken
into account while planning for biodiversity, the effectiveness of the global conservation network of areas for mammal species can improve by 29.8% (43.1% of species’ ranges
protected by the global solution compared with 39% in the
regional and 33.2% in the national solutions; figure 1b). In
fact, a global solution that accounts for the most likely conflict between biodiversity protection and food production
outperforms the unconstrained national solution (43.1%
versus 35.6% of species’ ranges protected, respectively;
figure 1b). Furthermore, when agriculture was considered
in conservation planning, the quartile of the species with
the smallest ranges was represented to a greater extent in
the global or regional solutions than in the national one
(F(3912,2) = 27.87, p < .001).
The spatial location of priority areas for mammal conservation varied across strategies. The coverage of protected
areas increased at low latitudes in the global solution when
agricultural costs were excluded (figure 2, supplemental
figure S2 and table S1). As was expected, the areas with the
high productivity, such as the western United States and the
South American grasslands, became off limits to conservation solutions when information about food production
was included (figure 3, supplemental figures S3 and S4).
Furthermore, we detected edge artifacts when the priorities
were defined nationally; that is, many priority sites were
located along country borders (e.g., the southern borders of
Canada and the Russian Federation; Moilanen et al. 2013).
When we compared the effects of the different conservation strategies on the agricultural production of individual
June 2014 / Vol. 64 No. 6 • BioScience 541
17%
Glo;Agro
Glo;Bio
Reg;Bio
Reg;Agro
Nat;Bio
Nat;Agro
.2
.
.4
.6
.8
a
17%
.6
.8
1
b
.4
Figure 2. Best unconstrained conservation solution for
mammals, considering a target of 17% global protected
area coverage. The upper map represents the globally
integrated solution, and the middle and bottom maps
represent conservation strategies that were designed to
maximize biodiversity at regional and national levels,
respectively.
.2
0
Mean roportion of ange ize rotected
0
Proportion of gricultural roduction ost
Forum
10
Glo;Agro
Glo;Bio
Reg;Bio
Reg;Agro
Nat;Bio
Nat;Agro
20
30
Target (percentage)
40
50
Figure 1. (a) The proportion of the global agricultural
production during the twenty-first century that would
be affected by biodiversity conservation. (b) The mean
proportion of the geographical range of mammal species
that will be protected by the selected priority areas.
The target represents the proportion of world land
area that may be set aside for conservation purposes.
Abbreviations: Agro, the approach in which agriculture
was included; Bio, the approach in which agriculture
was ignored; Glo, the global-scale analysis; Nat, the ­
national-scale analysis; Reg, the regional-scale analysis.
countries, we found that most countries were unaffected when
agricultural production was included in the conservation-­
planning process (132 out of 174 countries). The difference in food production, when comparing the global and
national conservation strategies, showed no correlation
542 BioScience • June 2014 / Vol. 64 No. 6
with the HDI (Pearson’s r(27)= .27, p = .16) and per capita
GDP (r(26) = .30, p = .12), but it was negatively c­ orrelated
with the percentage of GDP derived from agriculture­
(r(23) = –.54, p = .005) when agricultural production was
considered (supplemental figure S5). When we compared
the global and the national conservation strategies, the
following countries lost more than 5% of their agriculture production: Comoros, the Comoros Islands, Solomon
Islands, Samoa, Armenia, São Tomé and Príncipe, Costa Rica,
Papua New Guinea, Ecuador, Panama, Madagascar, Taiwan,
Rwanda, and Sri Lanka; this list includes countries with a
low HDI, a low per capita GDP, and a high dependence on
agriculture. The Comoros Islands, Papua New Guinea, and
Rwanda are countries of special concern, because they have
more than 30% of their GDP associated with agriculture
and are considered least-developed countries (supplemental
table S2). In terms of the change in available area, the number of countries with no change was much lower (23 out
of 174). We found weak positive correlations between the
area lost to agriculture in a country and the HDI (Pearson’s
r(150) = .22, p = .006) and between the area and the
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Forum
Hemisphere (Moilanen et al. 2013). We
previously reported an analysis of the
consequences of incorporating agricultural expansion in setting conservation priorities (Dobrovolski et al. 2013).
Here, we extend our previous analyses
by both incorporating data about land
productivity and extending our analysis
to the entire group of mammals. Finally,
we show that incorporating forecasts of
agricultural food production in a globalized conservation blueprint could lead
to important reductions in the cost of a
global network of protected areas.
Although setting priorities at the
regional scale is bound to produce intermediate levels of benefits for both conservation and food production, regional
action at the scale of existing economic
blocks may emerge as a realistic option.
Global governance issues have proven to
be difficult to resolve because of development disparities among regions and
other causes (Murphy 2000, Sand 2001,
Zimmerer et al. 2004). This suggests that
converting economic integration into
policies directed toward the conservation of biodiversity could represent a
first step toward a global integration
with significant improvements for their
efficiency. Such regional conservation
actions can expand the list of the few
current exceptions, which include the
Natura 2000 Network, implemented
across the European Union, and the
Mesoamerica Biological Corridor.
Figure 3. The best conservation solution for mammals, taking into account
The weak or nonexistent correlation
agricultural cost and considering a target of 17% global protected area coverage.
between
either the change in food proThe upper map represents the globally integrated solution, and the middle and
duction
or
the available area for counbottom maps represent conservation strategies that were designed to maximize
tries’
economic
growth and the level of
biodiversity at regional and national levels, respectively.
development of countries suggests that
poor countries choosing to engage in
per capita GDP (r(139) = .19, p = .03). There was no correlaglobal cooperation will generally not be more affected than
tion between a country’s area lost to conservation and the
richer ones. This is in accordance with results for established
percentage of GDP arising from agriculture (r(134) = –.15,
protected areas (Upton et al. 2007). However, particular cases
p = .08; figure S5, supplemental table S3).
in which poor countries could be negatively affected by a
Our results reinforce previous findings of the imporsignificant loss of food production deserve special attention
tance of considering the distribution of agricultural areas
within the existing international agreements. The positive
while setting conservation priority schemes (Naidoo and
correlation between agricultural production and economic
Iwamura 2007, Araújo et al. 2008, Carwardine et al. 2008,
dependence on agricultural activity (the percentage of GDP
Dobrovolski et al. 2011, 2013). Moreover, our proposal
from agriculture) supports this statement. Consequently,
extends to the global scale the benefits of political integrathe adoption of a globalized conservation solution must be
tion that were found in previous studies performed in North
tightly linked to the transfer of funds and compensatory
America (Vazquez et al. 2008), southern Africa (Rodrigues
payments for poorer countries to guarantee a fair scenario
and Gaston 2002), the Iberian Peninsula (Araújo et al. 2007),
for all countries (James et al. 1999). This flow of internathe Mediterranean Basin (Kark et al. 2009), and the Western
tional assistance from richer to poorer countries can help
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the latter integrate this global conservation task and can also
contribute to overcoming the social problems that impair
their conservation actions, such as poverty and inequality
(Mikkelson et al. 2007) and a lack of governance (Eklund
et al. 2011).
Humans will face two great coupled challenges for food
production in the future: meeting future food demand while
mitigating its impacts on the global environment, including
biodiversity. Globalizing conservation action (Zimmerer
et al. 2004) while explicitly searching for solutions that optimize the conservation benefit and food production is one
promising approach to meeting these challenges. For such
an approach to become viable, international agreements
should be reached at the level of biodiversity-related conventions, such as the CBD, the Convention on the Conservation
of Migratory Species of Wild Animals, the Convention
on International Trade in Endangered Species of Wild
Fauna and Flora, the International Treaty on Plant Genetic
Resources for Food and Agriculture, the Ramsar Convention
on Wetlands, and the World Heritage Convention. These
efforts must be informed by the need to expand agricultural
production coupled with reducing food waste, promoting the ecological intensification of agriculture, including
planning agricultural landscapes and other related efforts
(Cassman 1999, Tscharntke et al. 2012, Garnett et al. 2013).
Here, we show that biodiversity and food production
can be reconciled if agriculture opportunity costs are considered in a globalized conservation solution. This implies
that there is a need to act globally, in addition to thinking
globally and acting locally (Brundtland 1987). The leading
mechanisms available for addressing global biodiversity
conservation goals, targets, and priorities are biodiversityrelated ­conventions—in particular, the CBD. Therefore, food
production considerations must be discussed at the level of
these international agreements along with their respective
financial mechanisms, such as the Global Environment
Facility. Analogous negotiations involving the role of climate-smart agriculture in reducing greenhouse gas emissions are currently under way under the United Nations
Framework Convention on Climate Change. Both biodiversity conservation and food production would benefit
from a paradigm shift in the way conservation planning and
policy have been conducted so far in terms of international
negotiation.
Acknowledgments
We thank John Lamoreux, Atte Moilanen, Fábio Scarano,
Paulo De Marco Jr., Levi Carina Terribile, Ludmila Rattis,
Fabricio Villalobos, and Sidney F. Gouveia for useful comments on earlier versions of the manuscript. RD’s work was
supported by fellowships from the Brazilian National Council
for Technological and Scientific Development (CNPq) and
the Coordination for the Improvement of Higher Education
(CAPES). RL’s research has been constantly funded by
CNPq (grants no. 304703/2011-7, no. 479959/2013-7, and
no. 407094/2013-0), Conservation International Brazil, and
544 BioScience • June 2014 / Vol. 64 No. 6
the O Boticário Group Foundation for the Protection of
Nature (PROG_0008_2013). Work by JAFD-F and RDL has
been continuously supported by productivity grants from
CNPq. MBA is funded through European Commission
Research and Innovation grant no. 1/SAESCTN/ALENT-070224-FEDER-001755. MBA also acknowledges the Imperial
College London’s Grand Challenges in Ecosystems and the
Environment for support of his research.
Supplemental material
The supplemental material is available online at http://
bioscience.oxfordjournals.org/lookup/suppl/doi:10.1093/biosci/
biu064/-/DC1.
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Ricardo Dobrovolski ([email protected]) is affiliated with the
Department of Zoology at the Federal University of Bahia in Salvador
and with the Graduate Program in Ecology and Evolution at the Federal
University of Goiás, in Goiânia, Brazil. RD and Miguel B. Araújo are
affiliated with the Research Center for Biodiversity and Genetic Resources’
(CIBIO) InBIO Research Network, in Évora, Portugal. MBA is also affiliated
with the Department of Biogeography and Global Change at the National
Museum of Natural Sciences, in Madrid, Spain, and with Imperial College
London, in Ascot, United Kingdom. José A. F. Diniz-Filho and Rafael Loyola
are affiliated with the Department of Ecology, at the Federal University of
Goiás in Goiânia, Brazil. Gustavo A. B. da Fonseca is affiliated with the
Global Environment Facility, in Washington, DC, and with the Department
of Zoology at the Federal University of Minas Gerais, in Belo Horizonte,
Brazil.
June 2014 / Vol. 64 No. 6 • BioScience 545