Securing a Long-term Future for Coral Reefs
Authors: Ove Hoegh-Guldberg, Emma V. Kennedy, Hawthorne L. Beyer, Caleb McClennen, Hugh P. Possingham
Journal: Trends in Ecology & Evolution (2018)

Severe degradation of coral reefs in recent decades has been driven by a range of threatening processes including climate change. Ocean warming is expected to have further severe impacts on reefs unless global warming is restrained well below 2°C (the goals of the Paris Agreement). Not all coral reefs are equally at risk from climate change, however, suggesting the potential for identifying reefs for conservation action that are less vulnerable to climate change and which may be best positioned for regenerating other degraded reefs in the future. There is uncertainty in future conditions. Variance reduction methods from finance (e.g., modern portfolio theory) can be applied to conservation planning to identify a portfolio of coral reefs for which the risk of widespread failure across the portfolio is minimised. Long-term, risk-sensitive planning in the context of the uncertainty of projected climate impacts complements existing conservation strategies. Rapid ocean warming as a result of climate change poses a key risk for coral reefs. Even if the goals of the Paris Climate Agreement are achieved, coral reefs are likely to decline by 70–90% relative to their current abundance by midcentury. Although alarming, coral communities that survive will play a key role in the regeneration of reefs by mid-to-late century. Here, we argue for a coordinated, global coral reef conservation strategy that is centred on 50 large (500 km2) regions that are the least vulnerable to climate change and which are positioned to facilitate future coral reef regeneration. The proposed strategy and actions should strengthen and expand existing conservation efforts for coral reefs as we face the long-term consequences of intensifying climate change. Rapid ocean warming as a result of climate change poses a key risk for coral reefs. Even if the goals of the Paris Climate Agreement are achieved, coral reefs are likely to decline by 70–90% relative to their current abundance by midcentury. Although alarming, coral communities that survive will play a key role in the regeneration of reefs by mid-to-late century. Here, we argue for a coordinated, global coral reef conservation strategy that is centred on 50 large (500 km2) regions that are the least vulnerable to climate change and which are positioned to facilitate future coral reef regeneration. The proposed strategy and actions should strengthen and expand existing conservation efforts for coral reefs as we face the long-term consequences of intensifying climate change. Coral reefs provide habitat to over a million species as well as essential ecosystem services (e.g., food, coastal protection) to hundreds of millions of people throughout the tropics and subtropics [1Cinner J.E. et al.Vulnerability of coastal communities to key impacts of climate change on coral reef fisheries.Glob. Environ. Change. 2012; 22: 12-20Crossref Scopus (304) Google Scholar, 2Pendleton L. et al.Coral reefs and people in a high-CO2 world: Where can science make a difference to people?.PLoS One. 2016; 11: 1-21Crossref Scopus (52) Google Scholar]. Despite their importance, coral reefs are in rapid decline, with the rate accelerating for many coral reefs over the past decade (e.g., Great Barrier Reef, [3Hughes T.P. et al.Global warming and recurrent mass bleaching of corals.Nature. 2017; 543: 373-377Crossref PubMed Scopus (1687) Google Scholar]). Human impacts such as fishing pressure, coastal development, and pollution are combining with rising ocean temperatures to push reefs increasingly into states typified by low coral abundance, reduced biodiversity, and degraded ecosystems services [1Cinner J.E. et al.Vulnerability of coastal communities to key impacts of climate change on coral reef fisheries.Glob. Environ. Change. 2012; 22: 12-20Crossref Scopus (304) Google Scholar, 2Pendleton L. et al.Coral reefs and people in a high-CO2 world: Where can science make a difference to people?.PLoS One. 2016; 11: 1-21Crossref Scopus (52) Google Scholar]. While all threats facing coral reefs need addressing, those associated with global ocean warming are the most serious, with the near total loss of coral reefs across the planet expected by midcentury under current greenhouse gas emission projections [3Hughes T.P. et al.Global warming and recurrent mass bleaching of corals.Nature. 2017; 543: 373-377Crossref PubMed Scopus (1687) Google Scholar, 4Hoegh-Guldberg O. et al.The ocean.in: Press C.U. Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part B: Regional Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, 2014: 1655-1731Google Scholar, 5Hoegh-Guldberg O. Climate change, coral bleaching and the future of the world's coral reefs.Mar. Freshw. Res. 1999; 50: 839Crossref Scopus (2623) Google Scholar]. Within this context, reducing the impact of local threats has the potential to build much needed resilience for coral reefs as they face escalating threats from global climate change. The United Nations Framework Convention on Climate Change (UNFCCC) and its 21st Conference of the Parties (COP21) agreed to hold 'the increase in the global average temperature to well below 2°C above preindustrial levels and pursuing efforts to limit the temperature increase to 1.5°C above preindustrial levels' [6UNFCCC Conference of the Parties (COP) (2015) Paris Climate Change Conference-November 2015, COP 21, 21932Google Scholar]. To date, 180 of the 197 parties have ratified the Paris Agreement on climate change. This agreement is founded upon a scientifically based target under which relatively stable ocean conditions may be achieved by midcentury [4Hoegh-Guldberg O. et al.The ocean.in: Press C.U. Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part B: Regional Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, 2014: 1655-1731Google Scholar]. While current pledges to reduce emissions by the world's nations fall short of what is required to achieve the goals of the Paris Agreement [7Rogelj J. et al.Paris agreement climate proposals need a boost to keep warming well below 2°C.Nature. 2016; 534: 631-639Crossref PubMed Scopus (1787) Google Scholar], there is considerable hope that the international community will continue to work together to ramp up the emission reduction ambitions of its member states over the coming years. While the Paris Agreement was an impressive political achievement, average planetary surface temperature is expected to increase by another 0.5°C, putting further strain on already stressed natural and human systems. Under optimistic projections, the trend of increasing heat stress may render approximately 70–90% of the current distribution of coral reef habitat unsuitable for most corals [8Frieler K. et al.Limiting global warming to 2°C is unlikely to save most coral reefs.Nat. Clim. Change. 2013; 3: 165-170Crossref Scopus (288) Google Scholar, 9Donner S. et al.Global assessment of coral bleaching and required rates of adaptation under climate change.Glob. Change Biol. 2005; 11: 2251-2265Crossref Scopus (461) Google Scholar, 10Donner S.D. Coping with commitment: projected thermal stress on coral reefs under different future scenarios.PLoS One. 2009; 4e5712Crossref PubMed Scopus (162) Google Scholar]. Failure to achieve the Paris Agreement, however, will see the near total loss of coral reefs for the foreseeable future [4Hoegh-Guldberg O. et al.The ocean.in: Press C.U. Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part B: Regional Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, 2014: 1655-1731Google Scholar]. Pressures from global climate change add to the pressures from local factors such as coastal development, pollution, and overfishing to seriously threaten the viability of coral reefs. Here, we argue for a global, long-term strategy for protecting coral reefs that are both least vulnerable to climate change, and which are well positioned to facilitate the regeneration of many coral reefs later this century (Box 1 and Figure 1). Recognizing that the restoration of coral reefs may make sense at some scales of intervention [11Darling E.S. Côté I.M. Seeking resilience in marine ecosystems.Science. 2018; 359: 986-987Crossref PubMed Scopus (50) Google Scholar, 12Haisfield K.M. et al.An ounce of prevention: cost-effectiveness of coral reef rehabilitation relative to enforcement.Conserv. Lett. 2010; 3: 243-250Crossref Scopus (22) Google Scholar, 13Bayraktarov E. et al.The cost and feasibility of marine coastal restoration.Ecol. Appl. 2016; 26: 1055-1074Crossref PubMed Google Scholar], we argue that the future for coral reefs depends mainly on the success of these approaches being used together with large scale conservation initiatives (Box 2). To ensure that coral reefs persist beyond midcentury, strengthened conservation policies [14Hughes T.P. et al.Rising to the challenge of sustaining coral reef resilience.Trends Ecol. Evol. 2010; 25: 633-642Abstract Full Text Full Text PDF PubMed Scopus (741) Google Scholar], innovative and expanded financing [15Anthony K. et al.New interventions are needed to save coral reefs.Nat. Ecol. Evol. 2017; 1: 1420-1422Crossref PubMed Scopus (138) Google Scholar, 16UN Environment (2018) Analysis of International Funding for the Sustainable Management of Coral Reefs and Associated Coastal Ecosystems. Coral Reef Initiative, UN Environment World Conservation Monitoring Centre. wcmc.io/coralbrochureGoogle Scholar], and increased on-the-ground capacity will all be required [17Page G.G. A Synthesis of Issues Affecting the Management of Coral Reefs and Recommendations for Long-Term Capacity Building in U.S. Jurisdictions. National Oceanic and Atmospheric Administration's Coral Reef Conservation Program, 2015Google Scholar].Box 1Using MPT to Inform ConservationMPT [15Anthony K. et al.New interventions are needed to save coral reefs.Nat. Ecol. Evol. 2017; 1: 1420-1422Crossref PubMed Scopus (138) Google Scholar] is a mathematical approach for building portfolios of assets that maximise the expected return for a given level of risk. The idea is built around the concept that the risk to an asset should be assessed in the context of the overall risk and return of all assets in a given portfolio. Variance-reduction methods are widely used in the financial sector, and MPT was part of the work for which Harry Markowitz received the 1990 Alfred Nobel Memorial Prize in Economic Sciences.Conservation planning is also fundamentally concerned with investing limited resources to achieve conservation outcomes (returns) while minimising the risk of failure of those projects. In the case of coral reef conservation, uncertainty in projected long-term conservation outcomes is driven by variation in estimates of climate change impacts. MPT provides a risk-sensitive framework for conservation planning that explicitly accounts for the covariance in expected outcomes among planning units (investment opportunities).Beyer et al. [20Beyer H.L. et al.Risk-sensitive planning for coral reef conservation under rapid climate change.Conserv. Lett. 2018; (Published online June 27, 2018)https://doi.org/10.1111/conl.12587Crossref Scopus (105) Google Scholar] applied MPT to the problem of selecting 50 coral reef areas at a global scale (Figure I) that are among the least vulnerable to climate change impacts, and which have the potential to also foster regeneration in other areas via larval dispersal. There are often complex impacts of climate on biological systems that are difficult to capture with a small number of metrics. Beyer et al. used 174 metrics to quantify past and projected ocean warming impacts and risks of cyclone damage, as well as connectivity to other reefs, thereby ensuring that the solution is robust across a wide range of measures of climate change impact. They found substantial opportunity to reduce risk in the portfolio, while sacrificing only relatively small amounts of performance in expected conservation outcomes. MPT and other variance reduction methods provide important opportunities for improving long-term conservation planning to ensure it is more robust to uncertainty arising from climate change.Figure 1A Global Coral Reef Conservation Portfolio. Location of the 50 coral reef regions or bioclimatic units (BCUs) identified using a modern portfolio theory approach to balance expected conservation returns and risk of poor performance across the portfolio (Box 1). Reef symbol sizes have been exaggerated to improve visibility. The 'Coral Triangle' consists of locations primarily falling with the waters of Indonesia, the Philippines, Malaysia, Papua New Guinea, Solomon Islands, and East Timor. The Red Sea includes reefs falling primarily within the waters of Egypt, Sudan, Saudi Arabia, Eritrea, and Yemen. Further details and on-line resources around the portfolio of BCUs are provided by Beyer et al. [21Markowitz H.M. Portfolio selection.J. Finance. 1952; 7: 77-91Google Scholar].View Large Image Figure ViewerDownload Hi-res image Download (PPT)Box 2Accelerating Conservation Action within BCUsDeveloping conservation plans within the selected BCUs begins with a participatory site assessment to identify actions that are likely to deliver conservation returns in the near to medium term. This assessment should be integrated into local planning processes and institutions where appropriate, but at minimum should provide for: (i) threat assessment, (ii) Institutional capacity assessment, (iii) monitoring and evaluation (M&E), and (iv) policy development and implementation. Protocols for site assessments have been developed by a variety of sources (METT, NOAA, SocMon) [33Bunce L. Pomeroy B. Socioeconomic Monitoring Guidelines for Coastal Managers in Southeast Asia: SocMon SEA. Global Coral Reef Monitoring Network, 2003Google Scholar, 34Pomeroy R.S. et al.How is your MPA doing? A methodology for evaluating the management effectiveness of marine protected areas.Ocean Coast. Manage. 2005; 48: 485-502Crossref Scopus (204) Google Scholar, 35Stolton S. et al.Reporting Progress at Protected Area Sites. World Bank/WWF Alliance for Forest Conservation and Sustainable Use, 2003Google Scholar].Threat assessments are required for all locally relevant drivers, including, but not limited to: fisheries, coastal development, land-based pollution, and climate change. The development of solutions might include: expanding habitat conservation measures (e.g., marine protected areas, multi-use marine parks), regulating and rebuilding fisheries, reducing sedimentation and nutrient run-off, or rehabilitating coral reefs following extreme events such as storms and heat waves.Institutional capacity assessments should evaluate locally appropriate institutions relevant to governance, financial resources, training and education, technical capacity for implementation of conservation measures, and available social and natural scientific information. This capacity assessment will uncover key pathways to deliver threat mitigation strategies, such as new financial mechanisms to improve erosion control in upland agriculture, capacity building programs for park or fisheries enforcement officers, community engagement to increase participation in reef governance, and technical training or data collection.M&E systems are critical to the long-term adaptive management and tracking of changes both within and across BCUs. Initial participatory site assessments should identify existing M&E systems or build a baseline for future evaluations. In this regard, there are growing opportunities for technologies, from automated underwater vehicles, low-altitude drones, and remote sensing (coupled with AI) to strengthen and expend M&E capabilities within many BCU regions [36Roelfsema C. et al.Coral reef habitat mapping: a combination of object-based image analysis and ecological modelling.Remote Sens. Environ. 2018; 208: 27-41Crossref Scopus (80) Google Scholar]. The combined assessment of threats, institutional capacity, and M&E should conclude with a gap and opportunity analysis that identifies key areas for local and global investment to secure the long-term viability of each BCU.Policy development and implementation: facilitating the development of policy aimed at creating effective and lasting regulatory mechanisms is important for the long-term sustainability of coastal resources such as coral reefs. Alongside leadership,and legislative gap analysis, policy development across the many countries involved has the potential to deliver benefits of scale and experience. Adaptive policy development is needed in response to the strong drivers of change likely to be experienced over the coming decades and century. MPT [15Anthony K. et al.New interventions are needed to save coral reefs.Nat. Ecol. Evol. 2017; 1: 1420-1422Crossref PubMed Scopus (138) Google Scholar] is a mathematical approach for building portfolios of assets that maximise the expected return for a given level of risk. The idea is built around the concept that the risk to an asset should be assessed in the context of the overall risk and return of all assets in a given portfolio. Variance-reduction methods are widely used in the financial sector, and MPT was part of the work for which Harry Markowitz received the 1990 Alfred Nobel Memorial Prize in Economic Sciences. Conservation planning is also fundamentally concerned with investing limited resources to achieve conservation outcomes (returns) while minimising the risk of failure of those projects. In the case of coral reef conservation, uncertainty in projected long-term conservation outcomes is driven by variation in estimates of climate change impacts. MPT provides a risk-sensitive framework for conservation planning that explicitly accounts for the covariance in expected outcomes among planning units (investment opportunities). Beyer et al. [20Beyer H.L. et al.Risk-sensitive planning for coral reef conservation under rapid climate change.Conserv. Lett. 2018; (Published online June 27, 2018)https://doi.org/10.1111/conl.12587Crossref Scopus (105) Google Scholar] applied MPT to the problem of selecting 50 coral reef areas at a global scale (Figure I) that are among the least vulnerable to climate change impacts, and which have the potential to also foster regeneration in other areas via larval dispersal. There are often complex impacts of climate on biological systems that are difficult to capture with a small number of metrics. Beyer et al. used 174 metrics to quantify past and projected ocean warming impacts and risks of cyclone damage, as well as connectivity to other reefs, thereby ensuring that the solution is robust across a wide range of measures of climate change impact. They found substantial opportunity to reduce risk in the portfolio, while sacrificing only relatively small amounts of performance in expected conservation outcomes. MPT and other variance reduction methods provide important opportunities for improving long-term conservation planning to ensure it is more robust to uncertainty arising from climate change. Developing conservation plans within the selected BCUs begins with a participatory site assessment to identify actions that are likely to deliver conservation returns in the near to medium term. This assessment should be integrated into local planning processes and institutions where appropriate, but at minimum should provide for: (i) threat assessment, (ii) Institutional capacity assessment, (iii) monitoring and evaluation (M&E), and (iv) policy development and implementation. Protocols for site assessments have been developed by a variety of sources (METT, NOAA, SocMon) [33Bunce L. Pomeroy B. Socioeconomic Monitoring Guidelines for Coastal Managers in Southeast Asia: SocMon SEA. Global Coral Reef Monitoring Network, 2003Google Scholar, 34Pomeroy R.S. et al.How is your MPA doing? A methodology for evaluating the management effectiveness of marine protected areas.Ocean Coast. Manage. 2005; 48: 485-502Crossref Scopus (204) Google Scholar, 35Stolton S. et al.Reporting Progress at Protected Area Sites. World Bank/WWF Alliance for Forest Conservation and Sustainable Use, 2003Google Scholar]. Threat assessments are required for all locally relevant drivers, including, but not limited to: fisheries, coastal development, land-based pollution, and climate change. The development of solutions might include: expanding habitat conservation measures (e.g., marine protected areas, multi-use marine parks), regulating and rebuilding fisheries, reducing sedimentation and nutrient run-off, or rehabilitating coral reefs following extreme events such as storms and heat waves. Institutional capacity assessments should evaluate locally appropriate institutions relevant to governance, financial resources, training and education, technical capacity for implementation of conservation measures, and available social and natural scientific information. This capacity assessment will uncover key pathways to deliver threat mitigation strategies, such as new financial mechanisms to improve erosion control in upland agriculture, capacity building programs for park or fisheries enforcement officers, community engagement to increase participation in reef governance, and technical training or data collection. M&E systems are critical to the long-term adaptive management and tracking of changes both within and across BCUs. Initial participatory site assessments should identify existing M&E systems or build a baseline for future evaluations. In this regard, there are growing opportunities for technologies, from automated underwater vehicles, low-altitude drones, and remote sensing (coupled with AI) to strengthen and expend M&E capabilities within many BCU regions [36Roelfsema C. et al.Coral reef habitat mapping: a combination of object-based image analysis and ecological modelling.Remote Sens. Environ. 2018; 208: 27-41Crossref Scopus (80) Google Scholar]. The combined assessment of threats, institutional capacity, and M&E should conclude with a gap and opportunity analysis that identifies key areas for local and global investment to secure the long-term viability of each BCU. Policy development and implementation: facilitating the development of policy aimed at creating effective and lasting regulatory mechanisms is important for the long-term sustainability of coastal resources such as coral reefs. Alongside leadership,and legislative gap analysis, policy development across the many countries involved has the potential to deliver benefits of scale and experience. Adaptive policy development is needed in response to the strong drivers of change likely to be experienced over the coming decades and century. Given limited resources, effective conservation policy requires both intervention and geographic prioritization [18Iwamura T. et al.A climatic stability approach to prioritizing global conservation investments.PLoS One. 2010; 5Crossref PubMed Scopus (48) Google Scholar, 19Klein C.J. et al.Prioritizing land and sea conservation investments to protect coral reefs.PLoS One. 2010; 5e15103Crossref PubMed Scopus (71) Google Scholar]. Here, we describe a global strategy (see Figure I in Box 1) that focuses on identifying well-connected coral reefs that have the best chance of surviving projected climate change along a 'well below 2°C' pathway, as defined in the Paris Agreement (COP21 2015). Working under the assumption that the goals of the Paris Agreement will be achieved, these reefs (Figure 1) are likely to play important roles in facilitating the persistence of corals as global average temperature increases by another 0.5 °C, and the subsequent regeneration of coral reefs in the broader context as ocean temperatures stabilize. Thus, ensuring that the array of non-climate change related threats do not degrade or eliminate these reefs over this time period is of critical importance. The questions underpinning policy development then become: how does one objectively identify coral reefs that are relatively less vulnerable to climate change yet are better positioned to facilitate the regeneration of other reefs in the future? And, on the conservation side, where must we carry out actions that mitigate near-term threats (Box 2 and Figure 2), especially in the context of uncertainty? A recent study [20Beyer H.L. et al.Risk-sensitive planning for coral reef conservation under rapid climate change.Conserv. Lett. 2018; (Published online June 27, 2018)https://doi.org/10.1111/conl.12587Crossref Scopus (105) Google Scholar] applied modern portfolio theory (MPT, Box 1, [21Markowitz H.M. Portfolio selection.J. Finance. 1952; 7: 77-91Google Scholar]) to solve the problem of identifying a portfolio of reefs (Figure 1) that has a high probability, as a set, of surviving climate change while having a good capacity to repopulate other reefs over time. MPT is a mathematical approach for identifying an optimal portfolio of assets, such that the expected return on investments is maximized for a given level of risk. Up until recently, MPT has not been applied to spatial planning problems, and not at a global scale [22Ando A.W. Mallory M.L. Optimal portfolio design to reduce climate-related conservation uncertainty in the prairie pot-hole region.Proc. Natl. Acad. Sci. U. S. A. 2012; 109: 6484-6489Crossref PubMed Scopus (112) Google Scholar, 23Runting R.K. et al.Reducing risk in reserve selection using modern portfolio theory: coastal planning under sea-level rise.J. Appl. Ecol. 2018; 55: 2193-2203Crossref Scopus (25) Google Scholar]. In the context of long-term conservation planning, risk arises from the substantial uncertainty in the projection of future climate conditions. By accounting for the covariance in conditions among sites, MPT facilitates the selection of a portfolio of sites or bioclimatic units (BCUs, Figure 1) that are likely to provide good return on investment, with a lower risk of catastrophic loss across the entire portfolio. MPT was used in this particular study to optimize the selection of a portfolio of 50 BCUs with respect to the reduced exposure of BCUs to thermal stress in the past and future (i.e., mass coral bleaching and mortality) and storm damage, while also having a high degree of larval connectivity to other coral reefs. The large size of the 50 BCUs (500 km2) reduces the inherent vulnerability associated with selecting small areas, while providing flexibility in the potential conservation interventions that could be implemented given differences in the range, scale, and the immediacy of threats (Figure 2). Risk-sensitive, spatially explicit decision support tools like this can assist decision-makers in identifying objective and transparent solutions (and hence policy) for conservation problems. Importantly, decision support tools like MPT are designed to inform but not prescribe solutions. It is generally not possible to incorporate all dimensions of a problem into a single decision support tool in all but the simplest of problems. For example, some of the BCUs identified by Beyer and colleagues [20Beyer H.L. et al.Risk-sensitive planning for coral reef conservation under rapid climate change.Conserv. Lett. 2018; (Published online June 27, 2018)https://doi.org/10.1111/conl.12587Crossref Scopus (105) Google Scholar] occur in places where governance or local socio-economic conditions for improved conservation are not optimal. In other cases, highly valuable sites may also be too small to be prioritized in a global-scale analysis, but clearly warrant conservation action. Hence, the translation of a theoretically optimal portfolio to one that will be practical to implement requires adjustments based on local conditions and evidence. Innovative science, increased global awareness, political commitment, and resourcing of a global response to the threat that climate change poses to coral reefs are necessary but not sufficient to save coral reefs. Ultimately, the solution to ensure the survival of coral reefs also depends on the success of an array of management systems in place across the world. The 50 large coral reef regions identified [20Beyer H.L. et al.Risk-sensitive planning for coral reef conservation under rapid climate change.Conserv. Lett. 2018; (Published online June 27, 2018)https://doi.org/10.1111/conl.12587Crossref Scopus (105) Google Scholar] (Figure 1) provide a diverse portfolio of reefs that hedges against future climate stress and that urgently requires investment in conservation interventions. Increased global support is needed to facilitate participatory multi-stakeholder reassessment of the conservation needs, socio-economic issues, and biodiversity values across the proposed portfolio (Box 2 and Figure 2). Of critical importance will be the reassessment of localized threats such as declining water quality, over-exploitation, habitat loss, invasive species, as well as the local exposure to increasing climate threats such as heat stress and intense storms. Sustainable conservation requires that the full set of interactions between people, ecosystems, and economic systems be taken into account [22Ando A.W. Mallory M.L. Optimal portfolio design to reduce climate-related conservation uncertainty in the prairie pot-hole region.Proc. Natl. Acad. Sci. U. S. A. 2012; 109: 6484-6489Crossref PubMed Scopus (112) Google Scholar]. Strategies within each BCU might take on a variety of forms, depending on local