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Biological Conservation 246 (2020) 108559

Contents lists available at ScienceDirect

Biological Conservation
journal homepage: www.elsevier.com/locate/biocon

Policy analysis

More than just a (red) list: Over a decade of using South Africa's threatened T
ecosystems in policy and practice

Emily Anne Bottsa, Andrew Skownob,c, , Amanda Driverc, Stephen Holnessd, Kristal Mazee,
Tammy Smithc, Fahiema Danielsc, Philip Desmetd, Kerry Sinkc,d, Mark Bothaf, Jeanne Nelg,h,
Jeffrey Manuelc
a
Independent consultant, South Africa
b
Department of Biological Sciences, University of Cape Town, South Africa
c
South African National Biodiversity Institute, South Africa
d
Nelson Mandela University, South Africa
e
South African National Parks, South Africa
f
Conservation Strategy, Tactics and Insight, South Africa
g
Wageningen Environmental Research, the Netherlands
h
Sustainability Research Unit, Nelson Mandela University, South Africa

A R T I C LE I N FO A B S T R A C T

Keywords: One of the stated applications of the IUCN Red List of Ecosystems (RLE) is to influence government policy and
Biodiversity indicators decision-making. We share 15 years' experience in integrating an independently developed indicator of eco-
Biodiversity targets system threat status into government policies and practice. South Africa's ecosystem threat status indicator was
Ecosystem risk assessment conceptualised in the early 2000s and progressed from a project-based indicator to listing of threatened eco-
Environmental Impact Assessment
systems in terms of national legislation in 2011. We show the range of applications of the indicator, from its use
Spatial planning
Red List of Ecosystems
as a headline indicator in the National Biodiversity Assessment to its role as a direct trigger for Environmental
RLE Impact Assessment. The strong link between threatened ecosystems and systematic conservation planning in
Science-policy interface South Africa also enabled ecosystem threat status to inform multi-sectoral development planning and decision-
South Africa making. We show how bridging products, data availability, persistent mainstreaming and stakeholder engage-
Systematic conservation planning ment have encouraged the use of the indicator in government policy. The advantages and disadvantages of
Threatened ecosystems legislative listing are shared. Sound scientific foundations, combined with pragmatism, have provided a policy-
Threshold relevant tool for focussing management on threatened ecosystems. We make active recommendations that will
facilitate the policy uptake of the IUCN RLE in other countries.

1. Introduction in general, and the IUCN RLE in particular, aim to: i) improve general
awareness and gain public attention about biodiversity loss; ii) provide
Biodiversity indicators have been gaining attention due to an in- a measure for international reporting requirements (e.g. Aichi Biodi-
creasing need for action to slow global losses of biodiversity, including versity Targets); iii) monitor and evaluate conservation actions; and iv)
species and ecosystems (Nicholson et al., 2012; Tittensor et al., 2014; inform government policy and decision-making (Nicholson et al., 2012;
Geijzendorffer et al., 2016). Biodiversity indicators are metrics, based Keith et al., 2013; Geijzendorffer et al., 2016; Keith et al., 2015;
on verifiable data, that convey the state of biodiversity in a way that is Nicholson et al., 2015; Tanentzap et al., 2017; Bland et al., 2019).
relevant to decision-making (Addison et al., 2018). The International While use of indicators for international reporting is relatively more
Union for Conservation of Nature (IUCN) in 2014 adopted the cate- straightforward (Nicholson et al., 2012), their use to inform govern-
gories and criteria for the Red List of Ecosystems (RLE) as the global ment policy has been slower to develop, and evidence for policy ap-
standard for ecosystem risk assessment (Bland et al., 2017). Indicators plications of the IUCN RLE is only recent (Bland et al., 2019). There are,


Corresponding author at: South Africa National Biodiversity Institute, Kirstenbosch Research Centre, Rhodes Drive, Newlands, Cape Town, South Africa.
E-mail addresses: emily.rsa@gmail.com (E.A. Botts), a.skowno@sanbi.org.za (A. Skowno), m.driver@sanbi.org.za (A. Driver),
holness@mandela.ac.za (S. Holness), kristal.maze@sanparks.org (K. Maze), t.smith@sanbi.org.za (T. Smith), f.daniels@sanbi.org.za (F. Daniels),
drphil@ecosolgis.com (P. Desmet), k.sink@sanbi.org.za (K. Sink), mark@ecological.co.za (M. Botha), jeanne.nel@wur.nl (J. Nel),
j.manuel@sanbi.org.za (J. Manuel).

https://doi.org/10.1016/j.biocon.2020.108559
Received 29 November 2019; Received in revised form 19 March 2020; Accepted 31 March 2020
Available online 11 May 2020
0006-3207/ © 2020 Elsevier Ltd. All rights reserved.
E.A. Botts, et al. Biological Conservation 246 (2020) 108559

however, a range of opportunities for the IUCN RLE to be incorporated Table 1


into policy, including through economic, regulatory, informational and A summary of lessons and recommendations from the integration of threatened
preventative policy instruments (Alaniz et al., 2019). ecosystems into South African policy and legislation.
The development of biodiversity indicators that are intended to Lessons and recommendations
influence decision-making involves communication across the challen-
ging knowledge-action boundary (Cook et al., 2013; Game et al., 2015). Developing foundational maps of ecosystem types
Standard national classifications and maps of ecosystem types, preferably with a
This requires a reciprocal relationship between decision-makers com-
recognised custodian, provide a strong foundation for ecosystem risk assessment.
mitted to evidence-based policy (Carroll et al., 2017) and conservation Mapping ecosystem types at a fine enough scale to inform site-level decision-
scientists delivering policy-relevant science (Cook et al., 2013; Game making is ideal, but may not be possible at first and need not be seen as essential.
et al., 2015). For science to be effective in the policy arena, it must be A seamless national map of ecosystem types integrated across all realms is ideal,
but is unlikely to be achievable in initial iterations, so a separate map per realm is
founded on trustworthy methodology (credible), be relevant to specific
workable.
decision-making processes (salient) and consider decision-makers' Establishing formal update protocols for classifications and maps of ecosystem
needs (legitimate) (Cook et al., 2013). Even when these ideals are met, types is an ultimate aim.
integrating science into policy is complex and depends on a host of Addressing data limitations and laying the basis for improvements
socio-political factors and a degree of opportunism (Geijzendorffer There is no need to wait for perfect data; use the best data available and
acknowledge limitations.
et al., 2016). Therefore, information on how and where indicators have
Specifying data gaps that need to be filled to strengthen future assessments can
already been successfully incorporated into policy is useful when ap- provide direction for the scientific community.
plying new indicators. Undertaking the assessment
South Africa was one of several countries to independently develop Comprehensive ecosystem assessment (i.e. covering all ecosystem types) is more
achievable than comprehensive species assessment.
indicators of ecosystem threat status prior to the IUCN RLE (Keith et al.,
It is useful to conduct trial assessments of the criteria to better understand the data
2015; www.iucnrle.org). These indicators met a recognised need for an options, methods and results.
indicator similar to the IUCN Red List of Species that could identify risk Pragmatic judgement calls about operationalising the criteria may be needed to aid
for higher-levels of biodiversity organisation such as ecological com- implementation, but need not compromise scientific integrity.
munities (Noss, 1990; Rodríguez et al., 2007; Keith et al., 2013; Bland Presenting the assessment results
Summary statistics drawn from a comprehensive national assessment of ecosystems
et al., 2017). The numbers of species, including those undescribed, and
can be a powerful reporting tool.
the level of data needed to assess individual species, made red-listing of A simple colour-graded map of ecosystem threat status linked to a clear message is
species piecemeal rather than comprehensive (Rodríguez et al., 2007). an easily understood communication tool.
While there are some conceptual challenges in red-listing ecosystems Maps of threatened ecosystems and associated data and information should be
(Boitani et al., 2015), it was appreciated that ecosystems are more than conveniently accessible from a recognised data server, for a wide range of users.
Linking to bridging products
just assemblages of species and that they reflect ecological processes Ecosystem risk assessment can provide the basis for a legislated list of threatened
and habitat structure (Noss, 1990; Hoekstra et al., 2005; Nicholson ecosystems which can enhance policy uptake.
et al., 2009). It was also apparent that the scale of human modification Ecosystem threat status can provide a headline indicator that features in national
of landscapes was evident at the level of ecosystems (Hoekstra et al., biodiversity monitoring and reporting.
The list of threatened ecosystems and systematic conservation plans can reinforce
2005). South Africa has been using ecosystem types within its estab-
one another if the same underlying spatial datasets are used in both.
lished systematic conservation planning protocols for many years Preparing to list under legislation
(Lombard et al., 2003; Botts et al., 2019) and threat status of these Should the option of listing threatened ecosystems in terms of legislation exist,
ecosystem types has been incorporated into conservation prioritisation consider both the potential advantages and disadvantages of such a step.
and planning for over a decade. The legal and administrative implications should be thoroughly understood prior
to legislative listing of threatened ecosystems.
There is currently much international interest in how the IUCN RLE Stakeholders who will be involved in implementation should be consulted, to draw
could be effectively integrated into national policy (Alaniz et al., 2019). on their practical experience and insight into likely implications.
South Africa is one of the few countries with established policy for Once the list is written into law, consistent information and clear communication
ecosystem risk assessment that pre-dates the IUCN RLE (Bland et al., should be made readily available for implementers, to ensure regulatory
certainty.
2019). In this paper, we give a brief background to how the South
Encouraging policy uptake
African indicator was developed (providing methodological details in A comprehensive assessment of all ecosystem types across the country is easier to
Appendix A1). We then summarise how the indicator has been in- integrate into national policy than piecemeal assessments of individual
crementally integrated into government policy. Finally, in the discus- ecosystem types.
sion we broaden the learning achieved from South Africa to make A spatially explicit list of threatened ecosystems is likely to have greater policy
uptake than a list that is simply descriptive, especially for informing spatial
practical recommendations for the policy uptake of the IUCN RLE that planning and site-based authorisation processes.
are relevant to other countries (Table 1). Mainstreaming the list of threatened ecosystems and ensuring its integration in
policy across a range of sectors takes persistence over a long period of time.
2. Development of South Africa's indicator of ecosystem threat Policies and regulations, both in the environmental sector and in sectors whose
activities rely on or impact on ecosystems, should be urged to explicitly mention
status
threatened ecosystems.

South Africa's indicator of ecosystem threat status has a 15-year


history. Over a series of developmental stages, the methodology and 10 of 2004).
input data (Appendix A1) have been successively refined based on The impetus for an ecosystem-based indicator came from con-
practical experience. servation practitioners, who had existing experience in systematic
conservation planning and established government partnerships. At this
2.1. Origins of the South African indicator of ecosystem threat status stage, an indicator of ecosystem threat status was largely conceptual, its
proposal based on the fact that similar legal provisions were being
South Africa's indicator of ecosystem threat status was first con- made for the more established IUCN Red List of Species. Nevertheless,
ceptualised during discussions relating to new biodiversity legislation. there was rigorous discussion around the rationale for legislative listing
In the early 2000s, recommendations were made that the new law of threatened ecosystems (Botha et al., 2003).
should make provision for the listing of threatened ecosystems (Botha
et al., 2003; Cowling et al., 2003). These recommendations were taken
up into the National Environmental Management: Biodiversity Act (Act

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E.A. Botts, et al. Biological Conservation 246 (2020) 108559

2.2. Sub-national application 2.4. List of Threatened Terrestrial Ecosystems

An indicator of ecosystem threat status was first tested at sub-na- An extensive consultation process was conducted to develop the first
tional level by the Subtropical Thicket Ecosystem Programme (Cowling list of threatened ecosystems under the Biodiversity Act. Through a
et al., 2003). Vegetation types were already being used as surrogate series of expert and stakeholder workshops (2006–2009) consensus was
units for ecosystem types in systematic conservation planning (Lombard reached on six assessment criteria and associated thresholds (Appendix
et al., 2003). A method was developed to set ecosystem-specific con- A1). Two of the six criteria were left dormant since suitable data were
servation targets based on species-area curves (Desmet and Cowling, lacking at the time. The South African framework and IUCN RLE both
2004, Appendix A1). A single criterion was used to assess ecosystem take the IUCN Red List of Species as a conceptual departure point and
threat status, based on the proportion of intact vegetation remaining, consequently have many similar criteria, such as historical and ongoing
relative to a series of thresholds (Appendix A1). Vegetation types with habitat loss or degradation, and rate of loss. Principal differences are
less remaining area than required to achieve their conservation targets that the size of ‘limited extent’ is substantially smaller in the South
were considered Critically Endangered (CR), as below this target, spe- African framework, and it also includes a criterion that allows for in-
cies representation would be compromised. Thresholds for Endangered clusion of ecosystems prioritised in systematic conservation plans
(EN) and Vulnerable (VU) were loosely aligned with theoretical eco- (Appendix A1).
system fragmentation thresholds (Pierce et al., 2005; Desmet, 2018; Based on the criteria that could be implemented, the List of
Appendix A1). This initial criterion is conceptually equivalent to cri- Threatened Terrestrial Ecosystems was officially published in 2011
terion A3 (historical loss of habitat) in the IUCN RLE framework, but (RSA, 2011). The initial list was limited to terrestrial ecosystems, since
the thresholds, though similar, are ecosystem specific. the published National Vegetation Map provided an agreed set of na-
Sub-national application was a testing ground for the indicator. It tional terrestrial ecosystem types (Appendix A1). While the science
was an opportunity to debate the assessment methodology, develop remained central, this stage of development revealed the fundamental
technical skills, and explore feasible data sources. These early appli- importance of stakeholder consultation, including ecologists, con-
cations highlighted the synergies between systematic conservation servation practitioners, and government officials. Stakeholders working
planning and ecosystem risk assessment. Both conservation planning within government, who would be tasked with implementation,
and ecosystem assessment could use the same input maps of ecosystem brought a constant awareness of the possible consequences of the listing
types and the same conservation targets (Table 1). As a result, CR (Table 1). Testing of the criteria was done to ensure that the outcomes
ecosystems are, by definition, identified as priorities in systematic would be implementable. Adjustments were made to some thresholds
conservation plans, and EN ecosystems are also included among the so as to reduce possible administrative burden (e.g. requiring many
portfolio of conservation priorities. onerous permitting applications and authorisations) and thereby
strengthen uptake (Table 1).
2.3. National Spatial Biodiversity Assessment 2004
2.5. National Biodiversity Assessment
In 2004, ecosystem threat status was assessed nationally for the first
time in the National Spatial Biodiversity Assessment (NSBA) (Driver The NSBA 2004 was updated in the National Biodiversity
et al., 2005). The NSBA had a strong focus on developing products that Assessment (NBA) of 2011 (Driver et al., 2012) and 2018 (Skowno
would clearly convey the state of the country's biodiversity to policy- et al., 2019) (Appendix A1). In the NBA 2018, the decision was made to
makers (Reyers et al., 2007). Ecosystem threat status was selected as a transition to the IUCN RLE framework, which had recently been fina-
headline indicator, along with ecosystem protection level (an indicator lised, with full adoption in the terrestrial realm, and progress towards
of how much of each ecosystem type falls within formal protected alignment in the aquatic realms (Skowno et al., 2019, Appendix A1).
areas) (Driver et al., 2005). One of the primary reasons for focussing on Adoption of the internationally accepted IUCN RLE framework will
ecosystems was that in a megadiverse country, species risk assessments strengthen the credibility of threatened ecosystems in national pro-
were unlikely to be comprehensive, whereas it was possible for an cesses and allow for national-level reporting on a host of international
ecosystem assessment to be conducted systematically for all ecosystem processes. Updated classification systems and maps were used to assess
types across the country (Table 1). ecosystem threat status in the terrestrial, marine, estuarine, and inland
Again, a single criterion was used to assess ecosystem threat status, aquatic realms (Appendix A1). For the first time, all of these maps were
but the thresholds were modified (Driver et al., 2005; Reyers et al., seamlessly aligned into a single integrated map of ecosystem types
2007; Appendix A1). The assessment for the terrestrial realm used ac- (Fig. 1a; Harris et al., 2019; Skowno et al., 2019).
cepted national vegetation types as ecosystem types (Appendix A1). The successive assessments in 2004, 2011 and 2018 provided on-
This approach was then extended to rivers, estuaries and the marine going impetus for the improvement in data. In each assessment, data
realm, where concepts and thresholds were broadly equivalent, but gaps were deliberately identified and strategically addressed during the
broad-scale input maps were newly developed, and in some cases were intervening years (Table 1). For example, the coarse map of marine
largely expert-based (Driver et al., 2005, Appendix A1). ecosystem types from the first NSBA has since been considerably im-
The NSBA provided proof-of-concept for assessing threatened eco- proved using increasingly accurate and fine-scale bathymetry, remote
systems at a national scale. It showed that it was possible to mean- sensing, seabed, and biological survey data (Appendix A1). Over the
ingfully assess ecosystems across the country despite data limitations. years, increasingly standardised data update protocols have emerged
Even though some of the data were admittedly coarse-scale, the results for maps of ecosystem types, with formalised expert committees to
proved to be a useful assessment of the relative threat to ecosystems. It ensure that refinements are transparent and scientifically-grounded
also highlighted the value of a systematic assessment across all eco- (Table 1, Dayaram et al., 2019).
system types, allowing for the reporting of summary statistics at a na-
tional level, as well as comparisons between realms and biomes. For 3. Integrating ecosystem threat status into policy and planning
example, it revealed that ecosystems of the Forest, Fynbos and
Grassland biomes were relatively more threatened than other terrestrial South Africa's threatened ecosystems have been increasingly in-
biomes (Driver et al., 2005). Ecosystem threat status became one of the tegrated into legislation, policy, planning and management (Fig. 1;
most popular products of the NSBA, not least due to the visual power of Table A2). This was achieved through ongoing mainstreaming efforts
a simple map linked to a clear message (as in Fig. 1b, Table 1, Reyers focussed around three bridging products: systematic conservation plans
et al., 2007). (Botts et al., 2019; Nel et al., 2016), the legislated list of threatened

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E.A. Botts, et al. Biological Conservation 246 (2020) 108559

Fig. 1. The process of integrating risk assessment of ecosystems into policy showing (a) mapping ecosystem types and their condition; (b) identifying threatened
ecosystems (in this case showing the most recent South African threatened ecosystems; Skowno et al., 2019, Appendix A1); (c) feeding these into systematic
conservation plans, legal listing and national biodiversity assessment; and (d) integrating the products across a range of policy processes. Table items in grey text
summarise the South African policy instruments that explicitly reference threatened ecosystems (details are provided in Table A2). Weight of lines indicates strength
of the linkages.

ecosystems, and the National Biodiversity Assessment (Fig. 1c). Use of are afforded an array of defensive and protective actions against further
threatened ecosystems now ranges from laws intended to regulate threat.
specific activities, through forward-looking spatial plans, to monitoring
and reporting, and even voluntary use within the private sector
(Fig. 1d). Through these avenues, ecosystems facing serious pressure

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E.A. Botts, et al. Biological Conservation 246 (2020) 108559

3.1. Environmental authorisation 3.3. Protected area expansion

In many countries, a primary instrument to inform decision-making The strongest protection that can be given to threatened ecosystems
on the environmental consequences of development projects is is inclusion in the formal protected area network. Protecting ecosystems
Environmental Impact Assessment (EIA). Integrating an indicator of most at risk will prevent further destruction and contribute to their
ecosystem threat status into EIA processes ensures that due considera- persistence. In South Africa, systematic conservation planning (Fig. 1c)
tion is given to mitigating negative impacts on threatened ecosystems at is used as a basis for protected area expansion strategies, which identify
the site-level. In South Africa, EIA regulations state that conversion of sites that should be added to the protected area estate over defined
habitat within CR or EN ecosystems triggers the requirement for an EIA timeframes (Table A2). Through seeking to achieve conservation tar-
(Fig. 1d; Table A2). If residual impact remains, threatened ecosystems gets for representation of all ecosystem types (Appendix A1), systematic
can also be used to determine biodiversity offset requirements. South conservation plans inherently incorporate threatened ecosystems,
African biodiversity offset policies set high ratios for threatened eco- which thus inform priorities for protected area expansion. The need to
systems, requiring for example an offset as large as 30 times the area protect threatened ecosystems can be a persuasive motivator for the
impacted in a CR ecosystem (Table A2). Such measures compel thor- declaration of new protected areas, as was the case for the recent de-
ough application of the mitigation hierarchy, in which impacts are claration of 20 new marine protected areas in South Africa (Table A2).
preferably avoided or minimised and, only where this is impossible, are
offset in a manner that contributes meaningfully to the protection of the 3.4. Monitoring and reporting
ecosystem type that is impacted (Brownlie et al., 2017).
In addition to EIAs, there are numerous other permitting and li- One of the fundamental purposes of biodiversity indicators is
censing processes through which development may be regulated, such monitoring and reporting, and this is one of the more common uses of
as mining, agricultural and water-use authorisations. In South Africa, an RLE (Nicholson et al., 2012). This is especially relevant if ecosystem
even where threatened ecosystems are not directly mentioned in these types are systematically and regularly assessed across a country. The
regulations, they often still form part of the ‘best available evidence’ resulting summarised statistics of CR, EN and VU ecosystems are a
that must be consulted (RSA, 2011, Table A2). Many best-practice powerful reporting tool that draws attention to at-risk ecosystems, their
guidelines and administrative protocols regularly include threatened major threats, and trends in status over time (Table 1). In South Africa,
ecosystems in decision-making (Table A2). For example, the govern- the NBA has used ecosystem threat status as a headline indicator since
ment-endorsed Mining and Biodiversity Guideline identifies CR and EN 2004. The maps and summarised statistics of threatened ecosystems per
ecosystems as falling within the category of “highest biodiversity im- realm and biome from the NBA have been used across many of South
portance/highest risk to mining” (Table A2). A systematic and spatially Africa's biodiversity strategies and reports (Fig. 1c; Table A2).
explicit list of threatened ecosystems, mapped at a fine enough scale to
be applied in site-level decisions, provides other sectors with a con-
3.5. Proactive ecosystem management
venient dataset through which to incorporate environmental sensitivity
into their own regulatory processes (Table 1).
Management plans for individual threatened ecosystems can ad-
dress threatening processes specific to those ecosystems. Identifying an
3.2. Multi-sectoral spatial planning
ecosystem as CR or EN can encourage a wide range of stakeholders to
take action towards improved management. In South Africa, such ac-
Multi-sectoral spatial planning refers broadly to the intended future
tions may be co-ordinated through an official Biodiversity Management
distribution of people and development, integrated from the priorities
Plan for Ecosystems (Table A2). However, even without formal man-
of many different sectors. Threatened ecosystems can be afforded more
agement plans, both government and non-governmental organisations
strategic consideration if they are included in such plans. Rather than
have taken practical action to conserve particular threatened ecosys-
the reactive stance of environmental authorisation, this proactive ap-
tems. For example, eThekwini Municipality has put in place land-use
proach allows appropriate uses for threatened ecosystems to be de-
planning, regulation, formal protection, property rates incentives, fire
termined, and then incorporated alongside other development prio-
management, rehabilitation, and more, to manage and protect the EN
rities. In South Africa, threatened ecosystems most directly influence
KwaZulu-Natal Sandstone Sourveld (Boon et al., 2016).
spatial planning through the legal requirement that municipalities must
take threatened ecosystems into account in their integrated develop-
ment plans (Fig. 1c; Table A2). 3.6. Broader voluntary application
A less direct way of incorporating threatened ecosystems into spa-
tial planning is through systematic conservation planning (Fig. 1c), Outside of the formal policy environment, the IUCN RLE can be used
whereby threatened ecosystems are included together with other bio- in a variety of ways as a planning and decision-support tool (Table A2).
diversity features to identify an efficient and representative set of Corporate use of the IUCN Red List of Species to inform supply chain
spatial priorities. This allows the biodiversity sector to present a single sustainability planning and project management is an emerging trend
contribution to multi-sectoral spatial plans. In South Africa, methodo- globally (Bennun et al., 2017). Anecdotal evidence in South Africa
logical links between threatened ecosystems and systematic conserva- shows that ecosystem threat status is used for sustainability planning in
tion planning ensure that CR and EN ecosystems are identified as the private sector, and in several eco-certification processes (Fig. 1;
priorities. Provision is made for conservation plans to be formalised as Table A2). Industry has begun to recognise that environmental impacts
legal instruments known as Bioregional Plans (Table A2). However, constitute business risks that may prompt costly regulatory require-
even where these have not yet been formally published, conservation ments, or create reputational risk with shareholders and consumers
plans have been increasingly operationalised into government through (Addison et al., 2018).
a number of mainstreaming actions that have facilitated their uptake
(Botts et al., 2019). 4. Discussion
Threatened ecosystems may also be incorporated into Strategic
Environmental Assessments for future large infrastructure develop- South Africa's ecosystem threat status indicator has become a well-
ments, which can thereby consider threatened ecosystems at earlier established, legislated national indicator of the status of biodiversity.
stages of planning. An example is the South African SEA for renewable Below we draw from this national experience to distil lessons pertinent
energy infrastructure (Table A2). to adoption and policy uptake of the IUCN RLE globally.

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E.A. Botts, et al. Biological Conservation 246 (2020) 108559

4.1. Balance between scientific robustness and pragmatism South African VU category has been omitted from triggering EIAs, given
the relatively extensive land area listed as VU. It is acknowledged that
The South African indicator of ecosystem threat status was guided such omission may preclude actions that prevent further decline in
from the outset by a pragmatic perspective. A stated principle within status. However, EIAs are inherently reactive, and there are other
the List of Threatened Terrestrial Ecosystems was that “the identifica- proactive policy tools, such as spatial planning processes, that can
tion of ecosystems to be listed must be based on scientifically credible, better fill a preventative role.
practical and simple criteria” (RSA, 2011). This acknowledges the re-
quirements for policy relevant science: balancing credibility with sal- 4.3. Systematic conservation planning as a framework
ience and legitimacy (Game et al., 2015; Geijzendorffer et al., 2016).
Likewise, the IUCN RLE has rightly given much consideration to bal- Since South African threatened ecosystems are so closely linked
ancing the need for generality, which is essential in a global indicator, with systematic conservation planning, these two spatial planning tools
with scientific robustness (Keith et al., 2015). are complementary and mutually reinforcing. Conservation plans have
The South African indicator of ecosystem threat status has always been increasingly operationalised into government policy and planning
been based on sound science, but the complexities of science were (Fig. 1c, Botts et al., 2019). Tanentzap et al. (2017) propose that con-
sometimes moderated with practical considerations. The best available servation prioritisation can provide a framework that links the gath-
data were used, with gaps identified for improvement in future itera- ering of biodiversity information, biodiversity reporting and decision-
tions (Table 1). Thresholds were based as far as possible on scientific making. The South African experience supports this, as conservation
principles but were adjusted where necessary in subsequent assess- planning has helped to take the indicator beyond a reporting tool, to
ments. Not all the criteria that were developed were used during the achieve some of the other aims of biodiversity indicators, including
first legislative listing of threatened ecosystems. This concession may influencing government policy (Fig. 1d).
have resulted in underestimation of the number of threatened ecosys- Similar links have been found between the IUCN Red List of Species
tems. However, when listing under legislation confidence in the as- and conservation planning (Hoffmann et al., 2008). However, there is
sessment becomes more important, as the onus may be placed on the greater potential for identifying a comprehensive set of spatial priorities
conservation authority to justify these listings in a legal process. Thus, it using ecosystem-level data than with the incomplete species data that is
is better to underestimate than to identify ecosystems as threatened common in most countries. A valued feature of South Africa's indicator
based on low confidence data. of ecosystem threat status is that it is systematically assessed across all
The indicator was developed to be useful before it was perfected, terrestrial and aquatic ecosystems. The foundational input layers are
and has been refined over several iterative assessments. The relatively maps of ecosystem types with complete national coverage, supported
stable community of conservation practitioners maintained a deliber- by an established national ecosystem classification system. South Afri-
ately pragmatic perspective, acknowledging limitations but working ca's national biodiversity agency took the lead in creating and dis-
around them, and recognising that improvements would necessarily be seminating these national datasets (Table 1). The complete spatial
ongoing (Table 1). The same pragmatic use of data and phased im- coverage of the indicator has been fundamental in achieving nationally-
plementation will be necessary as South Africa transitions towards applicable policy integration across sectors (Table 1).
using the IUCN RLE. Refinements to the indicator and the foundational
data mean that trends in ecosystem threat over time cannot be directly 4.4. Acceptance and integration into policy
assessed (although refinements could be applied retrospectively if
warranted). It is expected that with the adoption of the IUCN RLE the The South African indicator has become an oft-quoted measure of
indicator of ecosystem threat will stabilise over time, similar to the the state of biodiversity in the country, echoing the experience of var-
IUCN Red List of Species, which was revised several times before sta- ious ecosystem threat indicators developed around the world, which
bilising with the current categories and criteria (Mace et al., 2008). experienced rapid acceptance (Nicholson et al., 2009; Keith et al.,
2015). One reason for this is their similarity to the well-known IUCN
4.2. Benefits and implications of listing in terms of legislation Red List of Species, with aligned naming conventions and colours. It is
intuitive that an increasing severity of threat can be applied to eco-
There are advantages and disadvantages to legislative listing of systems as well as species. In addition, ecosystem threat status can be
threatened ecosystems. A notable disadvantage is that the flexibility of visually presented on a single colour-graded map (Table 1). This ease of
an ecosystem threat indicator is constrained by legal processes. If used presentation and interpretation has encouraged the use of the indicator
simply as a monitoring tool, threat status can be updated as frequently for communication and reporting (Reyers et al., 2007), which are
as new data is available. Once the list is written into law, more care among the more commonly achieved purposes of indicators (Nicholson
must be taken to ensure sufficient regulatory certainty and consistency et al., 2012; Keith et al., 2015).
of information provided to the public domain (Table 1). Up-listing or In South Africa, the ecosystem threat indicator has gone beyond a
down-listing an ecosystem due to improved data can complicate reg- communication tool and has been embedded into policy, planning and
ulatory compliance. The major advantage of a legislated list, based on regulation (Fig. 1). This deeper policy integration required ongoing
criteria that have been accepted through a scientific and stakeholder engagement with legal processes in the country. The development of
participation process, is that threatened ecosystems are taken more new legislation created the opportunity to conceptualise a new biodi-
seriously during spatial planning and regulatory processes. Experiences versity indicator (Botha et al., 2003). Once enacted, the Biodiversity Act
from Australia, Finland and Norway, where RLE assessments from part established tools and processes that referenced threatened ecosystems.
of legislative tools (Bland et al., 2019), corroborate that decision-ma- However, policy uptake was a gradual process that required persistent
kers are empowered to enforce stronger action to prevent impacts on support and capacity building. Thus, the integration of the ecosystem
threatened ecosystems when the lists are legally recognised. threat indicator into policy was achieved through the combination of
During the legislative listing process, it was important to consider well-timed opportunities and ongoing mainstreaming efforts.
the various legal and administrative consequences that a listed eco-
system would trigger in terms of restrictions on land-use change or 4.5. Conclusion
development activities (Table 1, RSA, 2011). This was essential to
identify potential unintended negative consequences, such as increased According to Keith et al. (2015), the IUCN RLE should “…be judged
bureaucratic load or excessive development restrictions that would by whether it achieves its conservation ends and improves environ-
cause opposition towards the listing process. For these reasons, the mental management…”. While direct conservation outcomes are

6
E.A. Botts, et al. Biological Conservation 246 (2020) 108559

difficult to measure, the South African indicator of ecosystem threat is J.R., Herrera, B., Kontula, T., Lindgaard, A., Pliscoff, P., Skowno, A., Valderrábano,
being widely used to inform environmental management and con- M., Zager, I., Keith, D.A., 2019. Impacts of the IUCN Red List of Ecosystems on
conservation policy and practice. Conserv. Lett. 2019 (e12666).
servation, and has been integrated into a range of policies for spatial Boitani, L., Mace, G.M., Rondinini, C., 2015. Challenging the scientific foundations for an
planning and decision-making by government. The broad range of IUCN Red List of Ecosystems. Conserv. Lett. 8, 125–131.
policy applications achieved by the South African indicator provides Boon, R., Cockburn, J., Douwes, E., Govender, N., Ground, L., Mclean, C., Roberts, D.,
Rouget, M., Slowtow, R., 2016. Managing a threatened savanna ecosystem (KwaZulu-
other countries with an understanding of the opportunities available to Natal Sandstone Sourveld) in an urban biodiversity hotspot: Durban, South Africa.
incorporate threatened ecosystems into policy. We anticipate that such Bothalia 46, a2112.
policy integration will become increasingly widespread as the IUCN Botha, M., Driver, A., Maze, K., 2003. Introducing ecosystem conservation status: BotSoc
contributes to the Biodiversity Bill. Veld & Flora(June 2003).
RLE matures into a robust global indicator. Botts, E.A., Pence, G., Holness, S., Sink, K., Skowno, A., Driver, A., Harris, L.R., Desmet,
Appendix A1 provides details of the methodology applied during P., Escott, B., Lotter, M., Nel, J., Smith, T., Daniels, F., Sinclair, S., Stewart, W.,
various stages in the development of the South African indicator of Manuel, J., 2019. Progress through thirty years of conservation planning practice in
South Africa. Conserv. Biol. https://doi.org/10.1111/cobi.13321. Early view online.
ecosystem threat, including the full categories and criteria for South
Brownlie, S., von Hase, A., Botha, M., Manuel, J., Balmforth, J., Jenner, N., 2017.
Africa's 2011 List of Threatened Terrestrial Ecosystems. Appendix A2 Biodiversity offsets in South Africa – challenges and potential solutions. Impact
gives a list of laws, policies and formal guidance that explicitly re- Assess. Proj. Apprais. 35 (3), 248–256.
ference threatened ecosystems in South Africa. Supplementary data to Carroll, C., Hartl, B., Goldman, G.T., Rohlf, D.J., Treves, A., Kerr, J.T., Ritchie, E.G.,
Kingsford, R.T., Gibbs, K.E., Maron, M., Watson, J.E.M., 2017. Defending the scien-
this article can be found online at https://doi.org/10.1016/j.biocon. tific integrity of conservation-policy processes. Conserv. Biol. 31, 967–975.
2020.108559. Cook, C.N., Mascia, M.B., Schwartz, M.W., Possingham, H.P., Fuller, R.A., 2013.
Achieving conservation science that bridges the knowledge-action boundary.
Conserv. Biol. 27, 669–678.
CRediT authorship contribution statement Cowling, R.M., Lombard, A.T., Rouget, M., Kerley, G.I.H., Wolf, T., Sims-Castley, R.,
Knight, A., Vlok, J.H.J., Pierce, S.M., Boshoff, A.F., Wilson, S.L., 2003. A conservation
Emily Anne Botts: Conceptualization, Investigation, Writing - ori- assessment for the subtropical thicket biome. In: Terrestrial Ecology Research Unit,
Report 43. University of Port Elizabeth.
ginal draft, Writing - review & editing, Visualization. Andrew Skowno: Dayaram, A., Harris, L., Grobler, B., van der Merwe, S., Rebelo, A., Powrie, L.W., Vlok,
Conceptualization, Writing - original draft, Writing - review & editing, J.H.J., Desmet, P., Qabaqaba, M., Hlahane, K., Skowno, A., 2019. Vegetation map of
Visualization, Supervision. Amanda Driver: Conceptualization, South Africa, Lesotho and Swaziland 2018: a description of changes since 2006.
Bothalia 49. https://doi.org/10.4102/abc.v49i1.2452.
Writing - review & editing, Supervision. Stephen Holness: Desmet, P., 2018. Using landscape fragmentation thresholds to determine ecological
Conceptualization, Writing - review & editing. Kristal Maze: process targets in systematic conservation plans. Biol. Conserv. 221, 257–260.
Conceptualization, Writing - review & editing. Tammy Smith: Desmet, P., Cowling, R., 2004. Using the species-area relationship to set baseline targets
for conservation. Ecol. Soc. 9 (11 pages).
Conceptualization, Resources, Writing - review & editing, Project ad-
Driver, A., Maze, K., Rouget, M., Lombard, A.T., Nel, J., Turpie, J.K., Cowling, R.M.,
ministration. Fahiema Daniels: Conceptualization, Writing - review & Desmet, P., Goodman, P., Harris, J., Jonas, Z., Reyers, B., Sink, K., Strauss, T., 2005.
editing. Philip Desmet: Conceptualization, Writing - review & editing. National Spatial Biodiversity Assessment 2004: priorities for biodiversity conserva-
Kerry Sink: Conceptualization, Writing - review & editing. Mark tion in South Africa. Strelitzia 17.
Driver, A., Sink, KJ., Nel, JN., Holness, S., Van Niekerk, L., Daniels, F., Jonas, Z., Majiedt,
Botha: Conceptualization, Writing - review & editing. Jeanne Nel: PA., Harris, L., Maze, K. (2012) National Biodiversity Assessment 2011: an assess-
Conceptualization, Writing - review & editing. Jeffrey Manuel: ment of South Africa's biodiversity and ecosystems. Synthesis Report. South African
Conceptualization, Writing - review & editing. National Biodiversity Institute and Department of Environmental Affairs, Pretoria.
Game, E.T., Schwartz, M.W., Knight, A.T., 2015. Policy relevant conservation science.
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Declaration of competing interest Geijzendorffer, I.R., Regan, E.C., Pereira, H.M., Brotons, L., Brummitt, N., Gavish, Y.,
Haase, P., Martin, C.S., Mihoub, J.B., Secades, C., Schmeller, D.S., Stoll, S., Wetzel,
F.T., Walters, M., 2016. Bridging the gap between biodiversity data and policy re-
The authors declare that they have no known competing financial porting needs: an essential biodiversity variables perspective. J. Appl. Ecol. 53,
interests or personal relationships that could have appeared to influ- 1341–1350.
Harris, L.R., Bessinger, M., Dayaram, A., Holness, S., Kirkman, S., Livingstone, T.C.,
ence the work reported in this paper. Lombard, A.T., Lück-Vogel, M., Pfaff, M., Sink, K.J., Skowno, A.L., 2019. Advancing
land-sea integration for ecologically meaningful coastal conservation and manage-
Acknowledgements ment. Biol. Conserv. 237, 81–89.
Hoekstra, J.M., Boucher, T.M., Ricketts, T.H., Roberts, C., 2005. Confronting a biome
crisis: global disparities of habitat loss and protection. Ecol. Lett. 8, 23–29.
We thank the community of practice for biodiversity planning in Hoffmann, M., Brooks, T.M., Da Fonseca, G.A.B., Gascon, C., Hawkins, A.F.A., James,
South Africa, who were instrumental in developing the South African R.E., Hoffmann, M., Brooks, T.M., Da Fonseca, G.A., Gascon, C., Hawkins, A.F.,
ecosystem threat indicator and championing its integration into policy. James, R.E., Langhammer, P., Mittermeier, R.A., Pilgrim, J.D., Rodrigues, A.S., Silva,
J.M., Silva, J.M.C., 2008. Conservation planning and the IUCN Red List. Endanger.
Special thanks are given to the team who supported SANBI and the Species Res. 6, 113–125.
Department of Environmental Affairs during the 2011 process of listing Keith, D.A., Rodríguez, J.P., Rodríguez-Clark, K.M., Nicholson, E., Aapala, K., Alonso, A.,
threatened ecosystems in terms of legislation, including those from the Asmussen, M., Bachman, S., Basset, A., Barrow, E.G., Bishop, M.J., Bonifacio, R.,
Brooks, T.M., Burgman, M.A., Comer, P., Comin, F.A., Essl, F., Faber-Langendoen, D.,
provincial governments of KwaZulu-Natal, Mpumalanga and Gauteng, Fairweather, P.G., Holdaway, R.J., Jennings, M., Kingsford, R.T., Lester, R.E.,
and the national Department of Agriculture, Forestry and Fisheries, MacNally, R., McCarthy, M.A., Moat, J., Oliveira-Miranda, M.A., Pisanu, P., Poulin,
who were involved in comprehensively testing the criteria. E.A.B was B., Regan, T.J., Riecken, U., Spalding, M.D., Zambrano-Martıinez, S., 2013. Scientific
foundations for an IUCN Red List of Ecosystems. PLoS One 8, e62111.
compensated by SANBI for writing and co-ordinating this paper. Keith, D.A., Rodríguez, J.P., Brooks, T.M., Burgman, M.A., Barrow, E.G., Bland, L., Comer,
P.J., Franklin, J., Link, J., McCarthy, M.A., Miller, R.M., Murray, N.J., Nel, J.,
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