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Ecosystem Services and Beyond:
Using Multiple Metaphors to
Understand Human–Environment
Relationships
Christopher M. Raymond, Gerald G. Singh, Karina Benessaiah, Joanna R. Bernhardt, Jordan Levine,
Harry Nelson, Nancy J. Turner, Bryan Norton, Jordan Tam, and Kai M. A. Chan
Ecosystem services research has been focused on the ways that humans directly benefit from goods and services, and economic valuation techniques have been used to measure those benefits. We argue that, although it is appropriate in some cases, this focus on direct use and economic
quantification is often limiting and can detract from environmental research and effective management, in part by crowding out other understandings of human–environment relationships. Instead, we make the case that the systematic consideration of multiple metaphors of such
relationships in assessing social–ecological systems will foster better understanding of the many ways in which humans relate to, care for, and
value ecosystems. Where it is possible, we encourage a deliberative approach to ecosystem management whereby ecosystem researchers actively
engage conservationists and local resource users to make explicit, through open deliberation, the types of metaphors salient to their conservation problem.
Keywords: conservation, stewardship, deliberative approach, environmental management, ecosystem research
E
cologists and economists have drawn on the ecosystem services framework as a way of bridging human and
natural systems, accounting for environmental externalities, and supporting conservation efforts (Daily 1997, Daily
et al. 2000). Most ecosystem service assessments have been
framed using the conceptual metaphor of economic production, which has encouraged a focus on the benefits of ecosystems to humans in terms of how the processes of nature
deliver supplies and goods (Daily et al. 2000, Armsworth
et al. 2007), coupled with an economic quantification of
the costs and benefits of providing those ecosystem services
and goods (Bryan 2010, Newton et al. 2012). As Luck and
colleagues (2012) summarized it, the ecosystem services
concept has been applied for different purposes in several resource management contexts, including motivating
and structuring payments for ecosystem services programs
(e.g., Engel et al. 2008); structuring strategic policy guidance and priority setting using multicriteria assessments
(e.g., Nelson et al. 2009) and green accounting methods
(World Bank 2012); and highlighting the importance of
ecosystems and biodiversity to human well-being in a way
that promulgates dominant political and economic views
(Luck et al. 2012). The ecosystem services approach—and,
therefore, the ­production metaphor on which it relies—has
become the predominant tool used by ecologists, conservation biologists, and conservation planners to communicate
their work to the public and to implement environmental
management strategies (Pagiola et al. 2004, Ranganathan
et al. 2008, UNEP 2008, World Bank 2009, Dempsey and
Robertson 2012).
Despite its dominance, numerous critiques have been
directed at the monistic application of the economic production metaphor. By framing the problem in terms of
maximizing human benefits, with the environmental costs
measured as externalities, the ecosystem services concept
(a) often implicitly assigns rights in a manner that favors
the ­status quo, implying that individuals or groups seeking the benefits of those services have the right to despoil
nature and deserve to be paid not to do so (Van Hecken and
Bastiaensen 2010); (b) is focused disproportionally on the
production of services and less on the demand or human
access to these services (Daw et al. 2011, Robards et al. 2011);
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536 BioScience • July 2013 / Vol. 63 No. 7
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(c) does not account for ecosystem interactions beyond perceived stocks and flows (Norton and Noonan 2007, Norgaard
2010); and (d) implicitly deemphasizes the notions that
organisms and ecosystems are important in and of themselves (intrinsic value) or that they may be of benefit to
people in the future (future value)(Chan et al. 2012a). Some
have even argued that the economic production metaphor
does not incorporate important moral and ethical concerns
that humans have for nature (Luck et al. 2012), which are
embedded in held values, beliefs, and norms about nature
(Raymond et al. 2011) and in the multiple and complex
values that humans attribute to the environment (Kosoy and
Corbera 2010, Daniel et al. 2012).
A new way is needed for thinking through the different
values that humans hold or assign to the environment and
for sorting through contradictory insights and management
priorities (Norgaard 2010). Several solutions have been proposed, including more discursive forms of learning, knowing,
and governing (Zellmer et al. 2006) and shifting the unit of
analysis from the willingness to pay for discrete commodities
to development paths that protect a range of human values
and that, in doing so, recognize the multiple ways in which
humans value nature (Norton and Noonan 2007). In practice, this type of inquiry may result in many complementary
models and policies for describing human–environment
relationships that can be evaluated across multiple criteria
and scales. Such models and policies will also need to account
for complexity in human–environment relationships. For
example, individuals have the ability to express their relationship with the natural environment using multiple metaphors
and sometimes switch between metaphors to address the
interests of their audience (Klain 2010).
Systematically considering additional metaphors of
human–environment relationships has been proposed
to promote deliberation, to recognize multiple values in
ecosystem research, and to determine whether the framing of the problem is appropriate. A conceptual metaphor
is a ­simple set of relationships between known entities
expressed for the purpose of communicating more complex
analogous concepts (in contrast to an approach, which is a
method for undertaking an action; approaches may or may
not be rooted in a metaphor). Metaphor sharing promotes
collaboration and dialogue about values and goals between
scientific and traditional management systems (Armitage
2008, Larson 2011), thereby providing space for additional
voices and ideas in the public discourse. It also facilitates
the establishment of new links between science and society
by creating a language that challenges the status quo and
enables the communication of information in ways that
resonate with diverse groups in society. Larson (2011) noted
that language must not only be adequate for environmental
scientists but must also be socially adequate if the goal is to
engage diverse groups in environmental research, decisionmaking, and action.
However, systematically considering different metaphors may not lead to common ground in environmental
www.biosciencemag.org decisionmaking: “Metaphors both highlight and hide”
(Larson 2011, p. 209). This means that each metaphor
­inherently accounts for only a partial understanding and
privileges different perspectives, methods, management
objectives, indicators, conservation ethics, and decision
outcomes. Similarly, sharing multiple metaphors may not
improve environmental decisions because of the power
dynamics between individuals and institutions. Some metaphors are likely to receive more attention than others for
a variety of reasons, and these will probably dominate
environmental decisionmaking in that domain, even if
the popular metaphors are more appropriate as a tool for
­communication than as a framework for management. The
challenge for researchers is to make implicit metaphors
explicit during their ecosystem research and management
and to find ways to systematically consider the merits of different metaphors during environmental decisionmaking.
In this article, we identify and discuss the validity and
potential applicability of five metaphors for under­standing
human–environment relationships. We use case studies to
highlight the fluid boundaries of application of each metaphor and their strengths and weaknesses in regard to
communicating, understanding, and managing human–
environment interactions. We propose that multiple metaphors might apply to a conservation problem (none is truer
than the others) and that effectively engaging diverse groups
within decisionmaking requires that decisionmakers and
stakeholders proactively make implicit assumptions explicit.
Furthermore, we argue that there are both benefits and
drawbacks to the creation of decision contexts that enable
the systematic consideration of more than one metaphor.
Closing the loop by emphasizing human effects on
ecosystems
One might argue that a metaphor that equally emphasizes
humans’ positive and negative impacts on ecosystems would
mitigate any limitations of the human-use metaphor. In
this section, we explore the possibility of such a closed-loop
­production metaphor and argue that, although it has considerable promise, it also has limitations.
The closed-loop metaphor has its origins in the ­economic
production metaphor in which costs and benefits are
expressed in economic terms and how they directly affect
human welfare; however, many ecosystem services researchers and conservation practitioners have expanded the metaphor to more fully represent the range of human activities
and values that can enhance and degrade the ecosystems
on which they rely. It builds on the notion that humans
have always had a close relationship with the natural
environment. This relationship includes both supporting
and degrading activities that lead respectively to ­benefits
and costs to human well-being: from the use of fire to
increase food-plant productivity (Boyd 1999, Kimmerer and
Lake 2001) to agricultural practices and crop production
(Hails 2002). Certainly, humans have overharvested and
disrupted food webs, but in other cases, they have enhanced
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Figure 1. Closing the loop in the production metaphor by
including human activities that affect ecosystems.
wildlife populations and food webs through restoration and
other sustaining and conserving practices. By including the
human–environment interaction, the ecosystem services
concept can close the loop by highlighting the multi­
directional flow of interactions and can help us think of
human–environment relationships as including both beneficial and detrimental relationships and feedbacks. Such framing implicitly suggests that ecosystems are entities that can
be degraded, maintained, restored, or enhanced by humans
(figure 1) and that learning, adaptation, and transformation
in human–environment relationships takes time.
By employing the closed-loop production metaphor,
one seeks to understand human–environment relationships
through the quantification of key relationships in linked
social and ecological systems. Although the focus of this
metaphor is predominantly on monetary valuation as a metric for decisionmaking, such a metric is mostly used to compare the production of multiple services and is underpinned
by the quantitative measurements of stocks and flows (e.g.,
De Groot et al. 2010). Using this metaphor therefore introduces more complexity in its assessments (beyond the economic production metaphor) by considering both positive
and negative human impacts on ecosystems and, therefore,
the flow of ecosystem services under alternative scenarios
(Bennett et al. 2009, Nelson et al. 2009). Where social
dynamics are important, not only is this metaphor focused
on the ecological production of services through the incorporation of notions of equity and distributional impacts,
but it also addresses people’s ability to access those services
(Daw et al. 2011). But, ultimately, this metaphor implies that
humans have a right or entitlement to use ecosystem services
as long as those services can be used sustainably or can be
properly substituted with equivalent natural or humanmade
services (figure 2).
The closed-loop production metaphor takes into account
that ecosystems can be of disservice to human well-being.
By disservice, we refer to the negative and sometimes
­catastrophic ways in which ecosystem components and processes affect human well-being, such as the negative impact
538 BioScience • July 2013 / Vol. 63 No. 7
of locust or rodent plagues on grain production or that
of ­long-term droughts on water quality and quantity for
human consumption.
One consequence of this metaphor is that it implicitly
assumes that humans and ecosystems are distinct ­entities
that engage in a multidirectional flow of benefits (and harms).
More important, without intentional distance from the
production metaphor, the closed-loop metaphor inherits
the production metaphor’s focus on quantification. By relying on a metaphor that highlights the quantitative flows of
ecosystem services, other important benefits from ecosystems that cannot be easily measured or represented on a
commonly recognized scale (i.e., most cultural ecosystem
services) may be excluded from decisionmaking, unless
efforts are made to include some of these dimensions in a
more integrative, locally driven process (Chan et al. 2012a).
Ecosystem research and management may therefore benefit from a wider consideration of metaphors of human–­
environment relationships when diverse groups are involved
in environmental decisionmaking and where there are
­multidirectional flows of benefits (and harms).
Using additional metaphors to understand
human–environment relationships
A variety of other metaphors exist for helping us understand human–environment relationships. There are, for
instance, a variety of ways to frame humans as part of an
ecosystem. There are also ways to frame ecosystems in
modes in which their main purpose is not presupposed to
be the provision of services for humans or, conversely, to
possess an ideal, human-independent state that is either
enhanced or degraded by human interference. Norton and
Noonan (2007) suggested that the creative choice of appropriate metaphors of human–environment relationships will
guide policy-relevant choices for development paths to
protect a range of human values. A variety of metaphors for
understanding human–environment relationships exist—
for example, feedback metaphors that highlight widely held
cultural values; metaphors of consumerism, such as DNA
barcoding; and metaphors that involve terms with various
and interwoven definitions, such as sustainability (Larson
2011). Ecologists have represented ecosystems using multiple metaphors, including the ecosystem as a machine, as
an organism, as a house, and as an algorithm. Ecosystems
can also be represented using a set of metaphors describing ­resistance, resilience, diversity, or adaptability to change
(Pickett and Cadenasso 2002). Discussing a comprehensive
list of metaphors is impossible, and we instead describe
three additional metaphors—namely, the stewardship, webof-life, and ecocultural-community metaphors (figure 2).
We selected these three metaphors because, when they are
viewed in unison with the economic production metaphors,
they provide a continuum of perspectives on human–
environment relationships, ranging from the perspective
that the benefits of the environment to humans can be
assessed objectively in economic terms (in which the only
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Figure 2. Broad description of multiple metaphors for understanding human–environment relationships, including
potential associated management ethics, management objectives, and indicators of success.
issues are appropriate valuation techniques) to a completely
subjectivist perspective that human–environment relationships should be considered in terms of the interconnections
among spiritual, natural, and social realms within a given
context. Together, these five metaphors form logical endpoints from which ecosystem researchers and conservation
practitioners can begin to understand human–environment
relationships.
We recognize that metaphors are incomplete, simplified,
or generalized, in that they are rarely applied in a pure form
without elements of other metaphors. Ecosystem researchers and managers often apply multiple metaphors in their
­studies and often modify the mix of metaphors depending on the research question, the context of management,
and the prevailing needs of the funding body. Moreover,
although metaphors pertaining to human–environment
relationships do not in and of themselves prescribe parti­
cular management objectives, our experiences and the literature seem to suggest that their application is often associated
with different management ethics, objectives, and indicators
of success (figure 2). Because of these associations, which
may be triggered unwittingly by the use of a metaphor,
it behooves researchers and managers to be explicitly aware
www.biosciencemag.org of the metaphors and their associations that they apply in
their studies.
Below, we compare the economic production and closedloop production metaphors on the basis of their context
for application and assumptions, the prominence and role
of their valuation, and the related decisionmaking outputs.
We then repeat this comparative analysis for the stewardship, web-of-life, and ecocultural-community metaphors.
Together with the economic production and closed-loop
production metaphors, these metaphors provide examples
and pathways for characterizing human–environment relationships. For clarity’s sake, we simplify each metaphor
to crystallize key insights. We focus on the ways in which
human–environment interactions are conceptualized and
on how this might affect management outcomes. The name
that we give to each metaphor is partly for convenience,
and we note that there may be variants of a metaphor.
The stewardship metaphor. The stewardship metaphor com-
pares the Earth to a household in which humans hold the
position of a steward whose responsibility and obligation
it is to care for that household. Stewardship is a unifying
metaphor that embraces the notion that humans’ moral
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concerns drive the protection of ecosystems (Ratner 2004).
This metaphor was eloquently expressed by Leopold (1949)
in what is commonly known as the land ethic: “We abuse
land because we regard it as a commodity belonging to us.
When we see land as a community to which we belong,
we may begin to use it with love and respect” (p. viii). In
applying this stewardship metaphor, one recognizes that
humans hold multiple values and concerns for nature,
which derive from their affective and cognitive interactions
with other species and ecosystems. Monetary considerations
alone are not sufficient to drive environmental management
(Ludwig 2000), but rather, humans manage ecosystems out
of moral concern for them (figure 2). A variety of theories
and empirical frameworks have demonstrated that moral
and normative concerns, such as human values, environmental concerns, and personal and social norms about
conservation have direct and indirect effects on behavioral
intentions and on self-reported or actual behavior (Steg
and Vlek 2009, Raymond et al. 2011). These concerns derive
from individuals’ interactions with and ideas and feelings
about other people, species, and ecosystems. For example,
farmers in the Eyre Peninsula region of South Australia
commonly rated leaving the environment in a better condition than that in which they found it as one of their highest
land management goals and, in many cases, higher than the
goal of maximizing the income from their farm (Raymond
2009).
The web-of-life metaphor. Implicit in the web-of-life metaphor
is that species are nodes within complex webs of connections. In the web-of-life metaphor, humans are one part
of a wider ecological system and have the responsibility to
understand their impacts on the various components of the
broader system (figure 2). We therefore have a responsibility
to manage ecosystems on the basis of the complex inter­
actions between natural systems. The web-of-life metaphor
is common to both biology and indigenous worldviews—
for instance, the Vancouver Island Nuu-Chah-Nulth First
Nations’ view that hishuk ish tsawalk (“everything is one
and all is interconnected”; Atleo 2011). More recently, this
metaphor has spread across a variety of disciplines and fields
of application, inspired notably by complex systems theory
(e.g., Folke et al. 2005). The web-of-life metaphor can be
seen as underlying the ecosystem research and management
ethic that valuable species cannot be adequately managed
in isolation (McLeod and Leslie 2009). Although an understanding of the parts and components is essential, the only
way to truly determine why species do what they do is to
assess their roles within the broader ecosystem (Paine 2010)
and how those roles change depending on the time, location,
and context (Salomon et al. 2010).
The
ecocultural-community metaphor. The ecoculturalc­ ommunity metaphor is one of association, in which
humans treat nonhuman species and aspects of the environment as part of their community. Humans therefore
540 BioScience • July 2013 / Vol. 63 No. 7
have a responsibility to manage ecosystems on the basis of
the connections among the spiritual, physical, and social
worlds (figure 2). The level of integrity among these worlds
is an indicator of management success. The ecoculturalcommunity metaphor has been presented in the comanagement literature, with specific reference to how indigenous
and other long-resident peoples manage their landscape and
resources (Turner and Berkes 2006). It also encompasses the
Nuu-chah-nulth concept of hishuk ish tsawalk. Employing
the ecocultural-community metaphor also involves intrinsic
connections among land, family, ancestors, and the spiritual realm (Bohensky and Maru 2011; see also Atleo 2011).
These connections can be explored but not quantified. The
ecocultural-community metaphor also encompasses concerns for ecological systems and human species as a cohesive
whole (Toman 1994). This altruistic view is contrasted with
the economic production metaphor, which is focused on
the environmental values that are of direct use to human
beings.
Case studies of the effectiveness of the different
metaphors for ecosystem research and management
In this section, we provide examples of how each of the
metaphors of the human–environment relationship pertains
to environmental management practice.
Case 1: The economic production metaphor in the Panama Canal
watershed. Conservation efforts in the Panama Canal water-
shed illustrated by the development of protected areas and
payments for ecosystem services schemes provide an iconic
case study of the human-use metaphor. The Panama Canal
facilitates the transport of 5% of global commerce through
its locks, providing considerable revenues to the country.
Carse (2012) argued that, since the late 1970s, there has
been increased technocratic and engineered control over
watershed management, especially of forested and agricultural lands, which articulates the “notion that nature is, or
might become, infrastructure delivering critical services for
human communities and economies” (p. 2). At the heart of
the notion of infrastructure lies the concept that the benefits
of nature are measured by their use by humans.
Within this framework, several organizations have developed payments for ecosystem services projects to improve
water quality in the region. For example, ForestRe, a forestry
insurance company, uses the financial markets to encourage
insurance companies to underwrite a 25-year bond that
would pay for the reforestation of the slopes of the Panama
Canal in order to reduce eutrophication and siltation and
to increase water flow in the dry season. These insurance
companies then ask clients such as Wal-Mart, Toyota, and
Honda to buy their bond in return for a reduced premium
for insurance against the losses associated with the closure
of the canal (Economist 2005). In this case, the framework implicitly assigned who had those rights and how
those rights could be used to generate value in the system
(figure 2).
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Case 2: The closed-loop production metaphor in Hawaii. Kamehameha Schools, an educational trust and the largest private
landowner in Hawaii, undertook a comprehensive landplanning process on the island of Oahu that was intended to
balance environmental, economic, cultural, and community
values (Kamehameha Schools 2000). Kamehameha Schools
and local stakeholders considered a range of future scenarios
for the use of the land. They considered restoration activities, such as invasive species removal, restoring degraded
agricultural lands for biofuel production, diversified agriculture and forestry, and residential development. This
suite of options encompassed their goals of maintaining
and enhancing the environmental and cultural resources in
the region (exemplifying a closed-loop view of the human–
environment relationship). They used a spatially explicit
modeling tool to quantify changes in the delivery of services
such as carbon storage and water quality and the financial
return from the land (Goldstein et al. 2012). The scenarios
would lead to varying degrees of trade-offs among water
quality and carbon storage.
In spite of the fact that residential development was projected to yield the greatest financial returns, Kamehameha
Schools and the local stakeholders chose a plan in which
diversified agriculture and forestry were emphasized instead.
They were concerned that selling and developing the lands
could lead to potentially irreversible losses of cultural assets.
Consequently, they strived to close the loop in the human–
environment interaction by incorporating diverse human
activities, including restoration and extraction activities,
into local land-use planning. The ecosystem services model
provided a quantitative way for stakeholders and decision­
makers to consider the environmental, economic, and
cultural implications of alternative land-use scenarios and
provided a pathway for understanding how ecosystem services could be replaced by equivalent natural or humanmade
services.
Case 3: The stewardship metaphor in South Australia. Researchers
in the South Australian Murray–Darling Basin region of
South Australia investigated the influence of values, place
attachment, beliefs, and norms on the conservation of
native vegetation by rural landholders. The results indicated
that the strength of landholder connections with nature
was a significant predictor of the landholders’ environmental concerns (e.g., awareness of the consequences of
environmental problems), which in turn influenced their
personal norms about conservation and their self-reported
planting behavior (Raymond et al. 2011). The connection to
nature was measured by asking a random and representative sample of rural landholders (n = 1300) to respond to
a set of items about the strength of their bonds to natural
features (e.g., to native plants and animals) found in different areas of rural South Australia. In this case, a strict
focus on the economic benefits would have been too limiting; the research revealed the need for resource managers
to consider the influence of connections to nature if the
www.biosciencemag.org goal is to better understand how humans interact with
ecosystems, such as the extent to which landholders have
planted native vegetation on private land. Consistent with
the stewardship metaphor, the study findings highlighted
that humans’ moral concerns partially drive the protection
of ecosystems.
Case 4: The web-of-life metaphor in British Columbia. On the
west coast of Vancouver Island, British Columbia, Canada,
the reintroduction of a well-known keystone predator, the
sea otter, has caused the decline of multiple shellfish on
which coastal communities had come to rely. The narrow
conceptions of sea otters as directly good (e.g., for tourism)
or bad (e.g., for mussel production) were arguably limiting
and adversarial, given the diverse direct and indirect impacts
that otters have on a range of species in these marine ecosystems. Sea otter predation of sea urchins has led to increased
kelp production (Watson and Estes 2011). Kelp forests
are among the most productive ecosystems on the planet
(Mann 1973), so greater kelp growth is hypothesized to
lead to increased ecosystem productivity (through nutrient
­sub­sidies to secondary producers and increased habitat for
fish and invertebrates) to nearshore systems (Duggins et al.
1989, Tallis 2009). Markel (2011) revealed that such contributions of expanded kelp forests appear to have a dramatic
positive effect on some ecosystem functions, including rockfish production. Meanwhile, the effects on mussel growth
appear to be minor—even though kelp-derived nutrients
constitute a majority of mussel tissue in many sites (Singh
2010). Clearly, the ways of nature are varied and complex, as
is implied by the web-of-life metaphor. Humans are but one
node in a complex network of interactions. Recognizing and
articulating these diverse connections is an essential component of effective ecosystem management.
Case 5: The ecocultural-community metaphor in the Tsawout First
Nation community, on Vancouver Island. Tsawout, one of five
Saanich communities of southern Vancouver Island, British
Columbia, has about 1000 residents. The Tsawout, like other
Northwest Coast peoples, rely heavily on salmon and other
marine life for their sustenance. For many centuries, they
practiced sustainable reef-net fishing of migrating salmon
within kelp beds along the rocky shorelines of the Gulf
and San Juan islands (Claxton and Elliott 1994, Turner and
Berkes 2006). The bay, lagoon, and sandy spit adjacent to
their main village have also provided key resources, including clams, seals, game birds, and food and medicine plants.
The entire area plays an integral role in Tsawout economic,
social, and spiritual life. These areas have been threatened
by outside development, including the establishment of a
regional district sewage treatment plant near the spit and
a proposed commercial marina adjacent to the reserve,
which the Tsawout Nation contested successfully in court
(Claxton v. Saanichton Bay Marina 1987). The Tsawout continue to foster a belief system of kinship and responsibility
to their lands and resources, exemplified by their caretaking
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role of the newly formed Tsawout Land Stewardship Society,
registered in June 2012. Their beliefs (Tsawout First Nation
2012) include the notions that “the origin of the living
things of this world are our ancient relatives and that they
must be treated with respect, and… the islands, the salmon,
and the living things can be called upon for help to survive in this life.” The inextricable relationship and oneness
between humans and all the other entities of the environment, including those concerning spirituality, are embodied
in these beliefs and reflected in the stories, ceremonies,
and resource management actions of the Tsawout, as they
are in those of many other indigenous peoples.
Conclusions
In this article, we have explored some of the ways in
which humans conceptualize human–environment relationships. We surmise that ecosystem researchers and managers
use different types of metaphors for understanding those
relationships, such as the economic production, closedloop production, web-of-life, stewardship, and ecocultural­community metaphors. Each metaphor reveals different
parts of the human–environment dynamic and is aligned
with different management objectives and indicators of
­success. Researchers will not find perfect metaphors; the
validity and potential applicability of each metaphor will
vary from one context to another.
Using the economic production metaphor provides for a
simple and systematic assessment of the goods and services
that ecosystems provide to human beings, which can inform
the cost–benefits analysis of different policy options for
managing global markets; however, doing so does not foster
consideration of the complex interactions between humans
and nature (table 1). These feedbacks are inherent to the
closed-loop production metaphor but principally within
the context of stocks of natural capital and material flows.
Applying the stewardship metaphor takes into account
a broader suite of values and drivers of behavior from
moral, ethical, and ecosystem-health perspectives, which can
broadly be categorized as nonmarket perspectives. However,
this metaphor is arguably focused on humans (an anthropocentric perspective) and emphasizes a unidirectional
­relationship of care (not a network of feedback processes
among entities and collectives; table 1). This metaphor may
be appropriate if researchers are examining land management practices from the perspective of individual land
managers but may be inappropriate if the land management
practice under investigation affects multiple landholders or
a regional community. The web-of-life metaphor emphasizes the complex interactions among humans and nature at
larger scales (from individual to community and ecosystem
scales) and can therefore highlight indirect pathways of
interaction that affect things of value. However, the interconnections among the physical, social, and spiritual worlds
are missing from this metaphor, and it is difficult to translate the metaphor into practical decisionmaking. Implicit
in the ecocultural-community metaphor is the recognition of the inextricable relationship and oneness between
humans past, present, and future and all the other entities
of the environment. These entities include those related to
spirituality, which are embodied in beliefs and reflected in
the stories, ceremonies, and actions of indigenous peoples.
How to add in these additional dimensions is difficult
to explain, and it is challenging to measure or quantify
the interactions that this metaphor promotes (table 2).
Nevertheless, the use of this metaphor will be necessary in
order to engage both indigenous and nonindigenous groups
who have land management practices, customs, or rituals
that are not directly aligned with the economic production
metaphor. For example, the application of an ecoculturalcommunity metaphor is salient to managing mining claims
and associated land management disputes in parts of
Australia and Canada in which there can be conflict both
within and between indigenous and nonindigenous groups
about the economic benefits of mining royalties versus the
need to retain existing cultural practices and rights over
resource use and management.
Given the strengths and weaknesses of each metaphor
(table 3), we encourage ecosystem researchers and ­managers
to systematically consider multiple metaphors to understand
human–environment relationships and adopt an appropriate metaphor to suit the land management context. In
­reality, individuals engage with multiple metaphors implicitly, and the challenge is to develop systematic processes
for making them explicit. We therefore encourage a deliberative approach whereby ecosystem researchers actively
engage conservation practitioners and local resource users
Table 1. Comparison of the economic production and closed-loop production metaphors.
Prominence and role of
valuation in that context
Contributions to
decisionmaking
Human–environment relationships
can be quantified in monetary
terms
Focused on the monetary
benefits that humans derive
from ecosystems and is the
main decision criterion
Informs the cost–benefits
analysis of different policy
options
Production pathways (stocks and
flows) allow for an assessment of
the impact that humans have on
the ecosystem
Modified by the extent to
which human actions degrade,
maintain, restore, or enhance
ecosystem function
Identifies pathways through
which ecosystems provide
for human well-being and
vice versa
Metaphor
Main context for application
Assumptions
Economic
production
Monetary valuation for the
services that ecosystems
provide for human well-being
Closedloop
production
Quantification of the services
that ecosystems provide to
humans and those that humans
provide to ecosystems, not
necessarily in monetary terms
542 BioScience • July 2013 / Vol. 63 No. 7
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Table 2. Comparison of the stewardship, web-of-life, and ecocultural-community metaphors.
Metaphor
Main context for application
Assumptions
Prominence and role of
valuation in that context
Contributions to
decisionmaking
Stewardship
Explores or explains the
factors that contribute to
conservation (nonmarket)
behavior
A combination of economic,
moral, and instrumental
factors influence conservation
behavior and can be
anthropocentric or ecocentric,
depending on school of ethics
Behavior may be related to
nonmarket values; instead,
the antecedents (drivers) of
stewardship may be explored
or explained using multiple
methods
This metaphor identifies the
factors that enable or constrain
conservation behavior for
targeted policy development
Web of life
Helps represent the interand intraspecific relationships
among humans and other
species
Human–environment
interactions can be reduced
to and quantified within
their component parts; the
metaphor is ecocentric
Valuation may not be directly
considered; instead, the
understanding of complex
ecology can lead to
unforeseen outcomes that
can inform valuation (using
multiple methods)
This metaphor helps identify
what components of the natural
world are the most important
drivers of change and through
what pathways
Ecocultural
community
Explores the interrelationships
among social, physical, and
spiritual connections to land
and resources
Complex interdependencies
exist among humans, land,
and spirituality that cannot be
quantified; the metaphor is
kincentric and includes human
and nonhuman relatives
Valuation is implicit within the
connections between humans,
land, and spirituality
Network diagrams describe the
relationships among cultural
and spiritual practices and
ecosystem management;
documentation of oral histories
informs legislation and land
rights
Table 3. Strengths and limitations of the economic production, closed-loop production, stewardship, web-of-life, and
ecocultural-community metaphors.
Metaphor
Strengths
Limitations
Economic production
This metaphor includes a valuation comparison across
sites and aligns with existing economic and policy
paradigms.
It only involves half of the loop in human–environment
relationships and from a production perspective; it does not
account for the importance of diverse human–environment
linkages.
Closed-loop production
This metaphor includes quantified feedback processes.
It is focused on feedbacks within a production metaphor;
intangible services tend not to be incorporated because of
the difficulty in quantifying them.
Stewardship
This metaphor can quantify the nonmarket drivers of
conservation decisions that are beyond the scope of the
production metaphor.
It generally explains only a small portion of the relevant
behavior; theory development is limited to the body of ideas
held by a research community in what has been defined
as a top-down view of reality; it is often considered an
anthropocentric metaphor.
Web of life
This metaphor can highlight indirect pathways of interaction
that affect things of value and points out nonintuitive and
unforeseen aspects of the environment that are important.
It is often constrained to system interactions within the
biophysical world and this metaphor, alone, does not
translate into practical decisionmaking.
Ecocultural community
Theory development is guided by conservation
practitioners; this metaphor includes interactions among
the human, physical, and spiritual realms.
It is difficult to quantify the interactions among humans, land,
and spirituality and to translate these values into practical
decisionmaking, particularly in relation to the management of
ecosystems by nonindigenous communities.
to make explicit, through open deliberation, the types of
metaphors salient to their conservation problem and how
each metaphor can be systematically considered as part of
ecosystem research or management. A deliberative approach
would involve (a) appreciating the importance of the social
context of ecosystem research and management; (b) respecting a diverse set of knowledge cultures, values, and beliefs;
(c) actively engaging multiple types of communities (e.g.,
rural landholders, urban residents, conservation practitioners, indigenous peoples) in ecosystem research and management decisions; (d) respecting that each metaphor has
different assumptions and contexts for application and can
contribute to decisionmaking in a unique way (table 1); and
(e) more generally respecting the notion that humans are
part of nature rather than separate from it.
www.biosciencemag.org There is an empirical literature that indicates substantial
advantages of a deliberative approach, including greater
buy in by participants (e.g., Sabatier et al. 2005). However,
we acknowledge that there are drawbacks associated with
this deliberative approach to ecosystem management. They
include the opportunity costs associated with the time
required to engage multiple communities in ecosystem
management and to systematically consider the multiple
metaphors, the ideological conflicts among those who
espouse different metaphors and models for valuating
ecosystems, the challenges associated with the commensurability of the different valuation systems associated with
different metaphors, and the potential for some groups to
feel marginalized if the metaphors to which they subscribe
are not integrated into environmental planning or policy.
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In some cases, good economic accounting of the services
provided by the environment may be all that is necessary,
and therefore, a monistic approach may be appropriate. In
other cases, there may be no common ground among stakeholders and no scope for deliberation.
In this light, both monistic and deliberative approaches
to metaphor use have their advantages and disadvantages.
We believe that the deliberative approach may be most
applicable when key stakeholders in the conservation problem have different types and levels of knowledge about
human–environment relationships (Raymond et al. 2010)
and when there is evidence that stakholders are navigating among multiple metaphors of human–environment
relationships to address their interests or concerns. For
example, the same person may seek to maximize revenues
from forests when operating in his or her day-to-day office
environment while simultaneously supporting forest conservation for the intrinsic value of forests when interacting
with friends and family—two behaviors that are not necessarily incompatible. We discuss the policy implications of
this deliberative approach below.
Most metaphors are used implicitly or unconsciously but
are not made explicit in research or among management
teams. The goal of a deliberative approach is to make these
implicit metaphors explicit. When a new project is commenced, we encourage that opportunities be provided for
individuals and groups to articulate and share their metaphors explicitly with respect to the environmental problem
and decisionmaking context of the project. The deliberative
approach may benefit from the following elements:
Innovative ways of communicating and eliciting multiple
metaphors from different stakeholder groups will methodologically require adopting and improving on participatory
methods that effectively identify and engage with multiple
stakeholder groups (Reed 2008) and ways of communicating
multiple metaphors. These stakeholder processes may result
in the development of simplified metaphors that resonate
with both local citizens and scientists. Understanding of
context, including explicit understanding of the relevant
metaphors, to whom they are important, and how the
involved groups navigate among metaphors, would be
likely to benefit efforts to employ and encourage multiple
metaphors.
An effective facilitation process is necessary, given that
valuations and translations are usually made in power-laden
contexts (Gómez-Baggethun and Ruiz-Pérez 2011). The
framework proposed by Chan and colleagues (2012b) could
be adopted by facilitators to address potential power imbalances and to direct research in order to make more effective decisions. This framework involves obtaining consent;
determining the decisionmaking context of the management
problem; characterizing the components of the social–­
ecological context; determining the ecosystem services,
benefits, and values, both tangible and intangible; and synthesizing information from the process into influence diagrams and scenarios that reflect the different perspectives.
544 BioScience • July 2013 / Vol. 63 No. 7
A deliberative approach also requires the development of
new institutional arrangements that are flexible and responsive to local contexts and that are applicable at a variety of
scales of management. The international arena is currently
dominated by a global monetary system that treats natural
resources as largely fungible, even when science suggests
­otherwise (Koellner 2011). Creative institutional contexts
that are buffered, to a degree, from the overriding logic that
characterizes the broader global system could be encouraged
in order to balance the single logic of the dominant metaphor.
Norgaard (2010) noted, “Fully thinking through ecosystem
service projects from multiple perspectives means [that]
society must establish standing institutional mechanisms for
bringing out, sorting through, and using complex, contradictory insights in environmental management” (p. 1220). To
harness these insights, we encourage institutions supporting
ecosystem management to be network builders and facilitators of dialogue across multiple stakeholder groups, not just
regulatory arms. It will be important to support local organizations that represent the perspectives of multiple ecosystem
management groups (e.g., conservation nongovernmental
organizations, farm system groups) and other community
members with diverse values and ethics. Support can come in
many forms and may include arranging regional forums that
enable these organizations to share their perspectives and
ideas with scientists and policymakers (building on the community engagement pathways proposed by Raymond and
Robinson [2013]). Boundary organizations that operate at
the interface of science, policy, and community groups may
be well positioned to help decisionmakers navigate complex
interactions and conflicting metaphors at these forums.
At the ecosystem project level, the deliberative approach
could inform the problem-orientation phase (otherwise
known as the scoping phase) of conservation planning. In
an exploration of options for improved conservation and
management policy, Clark and colleagues (2009) suggested
that effective problem orientation requires key stakeholders
to determine goals, identify problems, determine alternatives, and evaluate those alternatives from the standpoints of
different stakeholders. We encourage that effort be directed
to understanding each stakeholder’s standpoint, including the dominant metaphors expressed by that individual.
During this sharing phase, some metaphors raised by the
stakeholders will complement one another, whereas others
will collide. A useful way to address conflicts is to discuss the
different perspectives with respect to the different process
activities related to addressing the conservation problem,
such as agreement on standards for prescription (laws,
actions, norms), management goals, asset management,
enforcement, implementation, monitoring and evaluation,
and succession (see Clark and colleagues [2009] for a further
discussion about each of these activities). To account for the
diversity of metaphors, environmental researchers and managers could benefit from learning to employ different types
of metaphors on the basis of their strengths and weaknesses
within the decisionmaking context.
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Tools that can be used to describe human–environment
relationships from different perspectives are crucial to
such decisionmaking processes. Research could be directed
to the development of innovative tools that incorporate
ecological, social, and economic values for ecosystems at
specific ­locations and that account for the costs and benefits
of different management strategies and process activities
(building on Smith et al. 2011). The outputs of these tools
could be used at different points of the deliberative decision
process, particularly in the identification of shared goals for
management and the monitoring and evaluation of conservation successes. We also encourage research on the kinds of
changes in practice that could result from sharing metaphors
and the benefits of these changes for improving our overall
approaches to ecosystem research and management. These
changes may include an understanding of a broader set of
values that guide environmental decisionmaking; a new set
of ideas or perspectives to guide an approach to ecosystem
valuation; a new language for communicating ecosystem
management principles that is understood by scientists and
citizens; and changes to the relationships among scientists,
policymakers, and citizens (e.g., building trust between
scientists and citizens by creating opportunities for open
dialogue and knowledge sharing).
The ecosystem services concept has received significant
attention from researchers and policymakers worldwide, but
engagement of diverse groups in the concept remains challenging. This limited engagement can be partly ­attributed
to an overemphasis on the economic production metaphor, which frames human–environment relationships as
a unidirectional productive relationship in which nature
provides for people only in concrete, measurable, and quantifiable ways. A more diverse set of metaphors of human–
environment relationships is rarely applied. We presented
the conceptual basis for five diverse metaphors of human–
environment relationships and showed how they have
been applied in practice. Each is naturally associated with
a different resource management ethic, as well as different
objectives, indicators of success, decisionmaking outputs,
strengths, and limitations. We encourage researchers to systematically consider the validity and potential applicability
of multiple metaphors of human–environment relationships and, where it is possible, apply a deliberative approach
to ecosystem research and management in which researchers, conservation practitioners, and local resource users
work together to address complex conservation problems.
Such a deliberative approach will require the active creation
and support of contexts that allow researchers, conservation
practitioners, and stakeholders to negotiate, understand, and
apply multiple metaphors.
Acknowledgments
This article originated from the Peter Wall Institute for
Advanced Studies Exploratory Workshop “Ecosystems:
Services, stewardship, and sustainability” held in Vancouver,
Canada, in June 2012. We thank the Peter Wall Institute for
www.biosciencemag.org Advanced Studies at the University of British Columbia for
funding the workshop (led by KMAC and Terre Satterfield)
and all participants for their contribution to the ideas
presented here. We would also like to thank three internal
reviewers, Anne Salomon, Sarah Klain, and Rachelle Gould,
for their valuable insights and edits.
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Christopher M. Raymond ([email protected]) is affiliated with Enviroconnect, in Stirling, South Australia, and with the Institute
for Land, Water and Society, at Charles Sturt University, in Albury, New
South Wales, Australia. Gerald G. Singh, Jordan Levine, Jordan Tam, and
Kai M. A. Chan are affiliated with the Institute for Resources, Environment,
and Sustainability; Joanna R. Bernhardt is affiliated with the Department
of Zoology and Biodiversity Research Centre; and Harry Nelson is affiliated
with the Department of Forest Resources Management at the University of
British Columbia, in Vancouver, Canada. Karina Benessaiah is affiliated
with the School of Geographical Sciences and Urban Planning at Arizona
State University, in Tempe. Nancy J. Turner is affiliated with the School of
Environmental Studies at the University of Victoria, in Victoria, British
Columbia, Canada. Bryan Norton is affiliated with the School of Public Policy
at the Georgia Institute of Technology, in Atlanta.
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