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Biological Conservation 180 (2014) 84–96

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Biological Conservation

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Accounting for conservation: Using the IUCN to evaluate the impact of a conservation organization ⇑ R.P. Young a,b, , M.A. Hudson a, A.M.R. Terry a, C.G. Jones b,c, R.E. Lewis a, V. Tatayah c, N. Zuël c, S.H.M. Butchart d a Durrell Trust, Les Augres Manor, Trinity, Jersey, Channel Islands, UK b Department of Life Sciences, Imperial College London, Silwood Park Campus, Buckhurst Road, Ascot, Berkshire SL5 7PY, UK c Mauritian Wildlife Foundation, Grannum Road, Vacoas, Mauritius d BirdLife International, Wellbrook Court, Girton Road, Cambridge, UK article info abstract

Article history: Global and project-level indicators have received considerable attention, but indicators of Received 31 March 2014 the conservation actions and impacts of programmes and institutions appear to be under-developed. Received in revised form 22 September The IUCN Red List Index (RLI) has potential to be a useful indicator at an organizational-level to evaluate 2014 long-term impact of conservation on the risk of , thereby supporting institutional Accepted 27 September 2014 decision-making and communications. However, it has not yet been tested for its utility in tracking changes in extinction risk of a set of species targeted specifically by an individual conservation agency. Here, we examine the feasibility of using the RLI as one metric of the conservation impact of the Durrell Keywords: Wildlife Conservation Trust, a conservation charity which runs multi-decadal programmes on a modest IUCN Red List Durrell Wildlife Conservation Trust number of globally threatened terrestrial species. Of 17 target , and Conservation impact species, eight underwent improvements in Red List category (reductions in extinction risk) owing to Evaluation conservation. This drove a 67% increase in the value of the Red List Index between 1988 and 2012. This Biodiversity indicators contrasts with a 23% decline in a counterfactual RLI showing projected trends if conservation had been Counterfactual withdrawn in 1988. For organizations that target sets of species with circumscribed geographic distribu- tions and that are regularly assessed by the IUCN Red List, the RLI is a useful indicator for measuring and demonstrating long-term conservation impact to technical and non-technical audiences. Ó 2014 Elsevier Ltd. All rights reserved.

1. Introduction at) different levels of conservation implementation such as projects, programmes and institutions, nationally and globally Monitoring and evaluation is an increasingly integral compo- are particularly valuable. Whilst the development of indicators at nent of biodiversity conservation practice and policy. It enables global and project-levels has received much attention (e.g. Conser- the setting of management and policy objectives, adaptation of vation Measures Partnership’s Open Standards for the Practice of interventions, measurement of effectiveness and demonstration Conservation (CMP, 2004); Cambridge Conservation Forum’s of results to donors, supporters and other stakeholders (Yoccoz Harmonizing Measures of Conservation Success (Kapos et al., et al., 2001; Stem et al., 2005; Sutherland et al., 2010; Jones 2008)), indicators of conservation actions, outputs and impacts at et al., 2013). It requires the development of individual and sets of programme and institutional-levels appear to be particularly indicators, the desirable properties of which depend on the moni- under-developed. toring objectives (Jones et al., 2013). In general terms, however, An important suite of policy-relevant indicators (Walpole et al., indicators should be scientifically robust, objectively verifiable, 2009) was developed to measure biodiversity status, threats and practical to implement, cost-effective and easy to communicate responses at the global-level in response to the Convention of Bio- to non-technical as well as technically-minded audiences. logical Diversity’s target to reduce the rate of by Indicators that are scalable between (and therefore informative 2010 (and these indicators were used to demonstrate that it was not met: Butchart et al., 2010). These formed the basis for a revised set (CBD, 2010a) recommended for tracking progress against the ⇑ Corresponding author at: Durrell Wildlife Conservation Trust, Les Augres 20 ‘Aichi Targets’ in the CBD’s Strategic Plan on Biodiversity Manor, Trinity, Jersey, Channel Islands, UK. (CBD, 2010b). Among these, Target 12 states that ‘‘By 2020, the E-mail address: [email protected] (R.P. Young). http://dx.doi.org/10.1016/j.biocon.2014.09.039 0006-3207/Ó 2014 Elsevier Ltd. All rights reserved. R.P. Young et al. / Biological Conservation 180 (2014) 84–96 85 extinction of known has been prevented and their extinction risk. The magnitude of this difference underestimated , particularly of those most in decline, has been the impact of conservation as it does not take into account species improved and sustained’’ (CBD, 2010b). The principal indicator used which would have deteriorated in status without conservation to report on progress towards this target is the IUCN Red List Index efforts (Hoffmann et al., 2010). To fully evaluate the impact of con- (RLI), which shows trends over time in the aggregate extinction servation actions, it is necessary to ask what would have happened risk of sets of species (Butchart et al., 2004, 2005, 2007). if there had been no intervention, i.e. a counterfactual outcome The RLI is calculated from data in the IUCN Red List of Threa- that is not observed (Ferraro and Pattanayak, 2006). A counterfac- tened Species (IUCN, 2013a), which is considered the most author- tual approach to programme impact evaluation has been broadly itative and objective system for categorizing the extinction risk of lacking within the conservation sector, hampering efforts to prop- taxa (Hambler, 2004; de Grammont and Cuarón, 2006; Rodrigues erly assess the outcomes of conservation funding programmes, et al., 2006). Species are assessed against criteria with quantitative intervention types, projects and institutions (Ferraro and thresholds for geographic range and population size, structure and Pattanayak, 2006). trends (IUCN, 2012) and then assigned to categories of extinction A number of impact evaluation methods are available to risk (ranging from Least Concern through to disentangle the effects of the intervention from the wider and Extinct) . The RLI is based on the proportion of species that dynamics of the system, including randomized controlled trials move through the IUCN Red List categories between periodic and quasi-experimental designs such as ‘‘natural’’ experiments assessments, either away from or towards extinction, as a result (e.g. Rosenzweig and Wolpin, 2000), instrumental variable meth- of genuine improvements or deterioration in status. It excludes ods (e.g. Edmonds, 2002) and matching (e.g. Clements et al., changes in category resulting from taxonomic revisions, changes 2014). However, many barriers to implementing such experimen- to the IUCN Red List criteria, or improvements in knowledge tal approaches often exist, including programme resource levels, (Butchart et al., 2004, 2006b, 2007). Index trends therefore relate ethical considerations, non-random allocation of treatment units, to how survival probability of a set of particular species changes lack of available controls, lack of data, among many others (see over time. Ferraro and Pattanayak, 2006). An alternative when these Global RLIs showing trends in extinction risk for all species experimental options are not possible is to construct counterfac- within a particular taxonomic group have been calculated for the tual scenarios based on target species population histories, threat world’s (Butchart et al., 2004, 2010; BirdLife International, levels and the socio-economic and management context of the pro- 2013b), (Stuart et al., 2004), (Schipper gramme just before the intervention commenced to predict the et al., 2008), and warm water reef-building corals (Carpenter counterfactual outcomes for species in the absence of conservation et al., 2008), bringing global attention to the concerning declines (e.g. Butchart et al., 2006a). in amphibians and corals in particular. However, there are no other Given its scalability and objectivity, the RLI has potential to be a groups in which all species have been assessed against the IUCN useful indicator at an institutional level to help assess organiza- Red List criteria at least twice, although reassessments of all coni- tional conservation impact, inform institutional decision-making, fers, cycads, mangroves, seagrasses, cartilaginous fishes, lobsters, and to provide evidence to donors and other institutional stake- crayfish and freshwater crabs are planned or underway (IUCN, holders of the ‘return on their investment’. However, the RLI has 2013b). Further, hyperdiverse orders such Coleoptera, not yet been used to track extinction risk in a set of species tar- Diptera and are particularly under-represented geted specifically by an individual conservation agency, or with within the Red List (Cardoso et al., 2012), although regionally com- reference to a counterfactual scenario in this way. Here, we aim prehensive assessments are now underway for some groups within to test the feasibility of employing the RLI on a modestly sized the latter, and for other invertebrate groups. To account for the set of species as a metric of institutional-level conservation impact, under-representation of these and other highly speciose and using Durrell Wildlife Conservation Trust as a case study. This poorly known taxonomic groups a sampled approach to red listing international charity focuses on the conservation of globally threa- has been developed (Baillie et al., 2008; Lewis and Senior, 2011), tened terrestrial vertebrate species and is characterized by running through which a representative sample of species have been intensive multi-decadal conservation programmes on a relatively assessed for , fishes, butterflies, dragonflies, and small number of species. We discuss the benefits and limitations (monocots, legumes, and ferns), with other inverte- of using the RLI for this purpose and examine in what contexts brate assessments underway. Repeated assessments will allow the approach may be effective. sampled RLIs to be developed in due course (IUCN, 2013b). National RLIs have also been developed based on repeated application of the Red List categories and criteria at a national scale 2. Materials and methods in order to assess national extinction risk, including for Australia (Szabo et al., 2012), Sweden (Gärdenfors, 2010), Finland (Juslen 2.1. The institution and species selection et al., 2013) and Paraguay (López, 2011). Global RLIs have been disaggregated to show trends in different biogeographic realms The Durrell Wildlife Conservation Trust (Durrell) is a non-profit (Butchart et al., 2004, 2005), for different taxonomic groups organization based in Jersey, Channel Islands, whose mission is (BirdLife International, 2013a), in relation to different international ‘saving species from extinction’. It runs long-term field agreements (e.g. Ramsar Convention on Wetlands, the Agreement programmes targeting globally threatened terrestrial vertebrate on the Conservation of and Petrels: BirdLife species on island (www.durrell.org). For example, International, 2013a; UN Millennium Development Goals: UN, Durrell has been running programmes in Madagascar for over 2013), to show the contribution of different threats (Butchart, 25 years and in Mauritius for over 35 years. Over its history, Dur- 2008; McGeoch et al., 2010; Almond et al., 2013), to assess the rell has led, or supported a national-level partner organization to effectiveness of protected areas (Butchart et al., 2012), and to conduct, species-specific conservation interventions on 53 verte- quantify the impact of conservation action (Hoffmann et al., 2010). brate species, including fish (n = 1), amphibians (n = 2), reptiles The latter study contrasted RLIs for birds, mammals and (n = 17), birds (n = 16) and mammals (n = 17), for which detailed amphibians with alternative ‘counterfactual’ RLIs that excluded documentation exists. Durrell has also previously run field-based those improvements in status driven by conservation interventions programmes on approximately 10 other species which are insuffi- that led to species being downlisted to lower categories of ciently documented to consider in this study. 86 R.P. Young et al. / Biological Conservation 180 (2014) 84–96

Here, we define species-specific interventions as: (1) providing technical support and/or strategic and scientific protection, management and restoration (that explicitly accounts guidance to help deliver conservation actions. These field for the conservation needs of a target species, e.g. by establishing trips are supplemented by remote technical assistance in or zoning a protected area based on the distribution of a target spe- the intervening periods. cies); (2) invasive alien species management (when conducted to (b) Durrell has provided significant levels of training to multi- directly benefit a target species to e.g. reduce nest predation rates ple members of staff from the national-level partner(s) over by ); (3) anti- patrols to reduce rates of a multi-year period where the newly acquired skills will poaching of target species; (4) reintroduction back to the wild clearly benefit effectiveness of conservation actions on the and translocation from wild populations to new sites; (5) supple- ground. mental feeding of target species; (6) nest site provision/manage- (c) Durrell has run a conservation breeding programme (as part ment through the establishment and maintenance of nest boxes; of a wider conservation strategy for a species) that has pro- (7) disease management where individuals of target species are vided for release back into the wild. captured, examined and treated for infection if required; (8) ‘head-starting’, i.e. harvesting eggs or young individuals and cap- Of the 53 species, interventions were considered too short-term tive rearing them through a risky life stage before release back to for 17 species and were insufficiently intensive or sustained for 6 the wild; and (9) captive breeding programmes (if animals are species. Thirteen of the remaining 30 species are reptiles and could released back into the wild as part of multi-annual releases com- not be included in the RLI as the majority had been assessed only plemented by long-term in-situ management actions). More infor- once for the IUCN Red List, or were listed as . There- mation on the different conservations actions conducted for each fore 17 species (1 amphibian, 7 mammals and 9 birds) were of the species included in this analysis is given in Table A1. included in the ‘Durrell RLI’ (see Table 1) from the countries of For the purposes of this study, we only included those species Mauritius ( Psittacula eques; ; Mauri- for which Durrell or a national-level partner organization has tius Falco punctatus; white eye Zosterops chloronothos; implemented long-term (>10 years), intensive and sustained con- Nesoenas mayeri; Foudia flavicans; servation efforts across all or the majority (>50%) of the species’ Rodrigues fruitbat rodricensis; Acro- range. National-level partners were either national NGOs or gov- cephalus rodericanus), Madagascar (Alaotran gentle Hapale- ernment departments with which Durrell forms a long-term stra- mur alaotrensis; Madagascar teal Anas bernieri; Malagasy giant tegic partnership to assist in the leadership and delivery of jumping rat Hypogeomys antimena; Meller’s duck Anas melleri; conservation programmes and to develop institutional capacity. Narrow-striped Mungotictis decemlineata; Meller’s duck The period of >10 years was chosen to be in line with the minimum A. melleri), Brazil (Black ; Golden Leontop- time period over which population trends are assessed under IUCN ithecus rosalia), (Pygmy hog Porcula salvania), and Spain (Mal- Red List criteria (i.e. 10 years or 3 generations, whichever is lorcan midwife toad Alytes muletensis) (see Fig. 1). The main threats longer). We chose a standard threshold for determining long-term, to the target species were invasive species, habitat loss driven by rather than using species-specific periods of three generation agriculture and logging, and , with the relative importance lengths because, for the longer-lived species, programmes would of these threats varying between locations (see Fig. 2a and Table A1 have to be run for nearly 30 years to be considered long-term. Fur- for more information on the different threat types). The main ther, because trends from 10 years can be extrapolated to a rate national-level partners (or international partners with permanent over three generations for application to the Red List criterion national-level programmes) for each species are given in Table 1. thresholds, following IUCN (2012). The species in the study have a mean generation length of 5.7 years, ranging between 3.6 (e.g. 2.2. Calculating the Red List Index Mauritius fody Foudia rubra) and 9.9 years (e.g. Leontopithecus chrysopygus) years. Although the time period ideally Red List categories and the associated documentation were would be matched to a species’ life history, thereby allowing taken from IUCN (2013a) and BirdLife International (2013b). The enough time for population recovery that could be then reflected RLIs were calculated following the methodology outlined in detail in potential changes in Red List category, clearly there is a trade- by Butchart et al. (2007). In summary, index values were calculated off between these biological factors and the reality and challenges from the number of species in each IUCN Red List category in a of running programmes for multiple decades. We also only particular assessment year multiplied by a category weight (5 – included species for which Durrell or national-level partner(s) Extinct/; 4 – Critically Endangered; 3 – Endan- intervened across the majority of the species’ range to ensure we gered; 2 – Vulnerable; 1 – Near Threatened; 0 – Least Concern). can practically attribute any recovery to the conservation actions The sum of the scores is then expressed as a fraction of the maxi- implemented by Durrell and/or national-level partner. Here, we mum possible sum (the score obtained if all species had gone define long-term, intensive and sustained conservation efforts as extinct) such that an overall score of 0 on the RLI would mean that one or more of the following: all species in the set are extinct, whereas a score of 1.0 equates to all species being Least Concern, i.e. that none are expected to 1. A field conservation programme where Durrell staff are become extinct in the near future. The numbers of species in each based permanently on the ground leading the implementa- category for years prior to the most recent assessment were tion of conservation actions for at least 10 years to reduce calculated based on the number of species that underwent genuine directly the main threats to a species and thereby enable status changes in each time period between assessments. its recovery. We followed Hoffmann et al. (2010) in determining which of 2. A field conservation programme led by a national-level part- Durrell’s target mammal, bird and amphibian species have under- ner(s) implementing conservation actions for more than gone Red List category changes owing to genuine improvements or 10 years to reduce directly the main threats to a species deteriorations in status. Hoffmann et al. (2010) used the current and thereby enable its recovery, where two or more of the Red List criteria and retrospectively applied them to all mammal, following criteria are met: bird and amphibian species back to the year in which they were (a) Durrell members of staff spend extended periods of time first assessed. This effectively excluded changes in the Red List - (typically several weeks a year) on an annual or near-annual egory of species and therefore the RLI trends that were as a result basis on the ground with the national-level partner of changes in Red List criteria rather than the changes to the status Table 1 Species targeted by Durrell with information on the duration of the conservation intervention, Durrell’s role within the programme and the national-level partners. The current Red List category along with the estimated counterfactual 2012 Red List category, which assumes all Durrell-led or supported conservation actions had ceased in 1988, are indicated. For those species undergoing a genuine status change the relevant previous Red List categories are also given (from Hoffmann et al. (2010)).

Species, programme duration and role of Durrell within partnership Current and counterfactual Red List categories. For Reasons for 2012 counterfactual Red List category species undergoing status change the adjusted Red List category history is given (from Hoffmann et al., 2010) ‘80 ‘88 ‘94 ‘96 ‘00 ‘04 ‘08 ‘12 ‘12 CF Mallorcan midwife toad Alytes muletensis. 1985–2011. Partner in collaborative CR VU VU CR Captive breeding and release programmes would either not have happened or recovery programme, leading captive breeding programme. Main local partner: occurred much later through another agency. Despite impacts from invasive Conselleria d’Agriculture i Pesca (CDAP) of the Government of Mallorca predators at several isolated populations, the species was found in 13 gorge locations (Buley and Garcia, 1997) and is predicted to have persisted in the wild until 2012. Probable criteria met: B2ab (iv) Mauritius fody Foudia rubra. 1989-ongoing. Strategic, technical and financial CR EN EN CR Ceasing invasive predator control in Black River Gorges NP is likely to have led to support to main local partner, Mauritian Wildlife Foundation (MWF). Other local elevated nest predation rates and lower productivity. Captive breeding and release partner: National Parks and Conservation Services of the Government of onto Ile aux Aigrettes would not have happened. In 1988, the wild population was

Mauritius (NPCS) estimated at 100–200 pairs and so we predict the population would have persisted 84–96 (2014) 180 Conservation Biological / al. et Young R.P. until 2012 Safford and Jones (1998). Probable criteria met: D Falco punctatus 1976-ongoing. Programme partner focusing on in- CR EN VU VU EX Ceasing invasive predator control, nest site protection and nest box provision situ population management, captive breeding, research and capacity building; would have resulted in high juvenile mortality and low productivity in remaining provision of strategic, technical and financial support to MWF. Other local Black River Gorges population. Ceasing captive breeding and release programme partner: NPCS means the reestablishment of a population in Bambous Mountains in eastern Mauritius would not have happened. In 1988, an estimated 60 individuals were in the wild (C. Jones, pers. comm.) and therefore we predicted it would have become EX by 2012 Echo parakeet Psittacula eques. 1986-ongoing. Programme partner focusing on in- CR EN EN EX Ceasing invasive predator control, provision of next boxes, and supplementary situ population management, captive breeding, research and capacity building; feeding in Black River Gorges and stopping the captive breeding and release provision of strategic, technical and financial support to MWF. Other local programme would have resulted in very low productivity and downward partner: NPCS population trends. Only 25 birds were left in the wild in 1988 (C. Jones, pers. comm.) and therefore we predicted the species would have become EX by 2012 Madagascar teal Anas bernieri. 1992-ongoing. Lead implementing agency. Main EN EN Captive breeding would not have happened but this would not have affected wild local partner: Regional Direction for Environment and Forests of the population as no animals released back to wild (from Durrell or any other Government of Madagascar (DREF) institution). No site protection and development of local management plans is likely to have led to losses of local populations but no clear evidence the species would have met any CR criteria. Probable criteria met: C2a (ii) Meller’s duck Anas melleri. 1988-ongoing. Lead implementing agency. Main local VU EN EN EN Captive breeding would not have happened but this would not have affected wild partner: DREF population as no animals released back to wild (from Durrell or any other institution). No site protection and development of local management plans is likely to have led to losses of local populations but no clear evidence the species would have met any CR criteria. Probable criteria met: C2a (ii) Olive white eye Zosterops chloronothos. 1990-ongoing. Strategic, technical and CR CR Rat control in Black River Gorges would not have happened which may have led to financial support to MWF. Other local partner: NPCS increased nest predation rates and decreased productivity in this single remaining population. Captive breeding and release programmes would not have happened and therefore a new population in Ile aux Aigrettes would not have been established. In 1988 there were approximately 200 pairs in the wild and therefore we predict the species would have persisted until 2012. Probable criteria met: C2aii Pink pigeon Nesoenas mayeri. 1982-ongoing. Programme partner focusing on in-situ CR EN EN Ew Ceasing invasive predator control, supplementary feeding, Durrell-supported population management, captive breeding, research and capacity building; captive breeding and release programmes would have resulted in very low provision of strategic, technical and financial support to MWF. Other local productivity in the single Black River Gorges population and downward trends. partner: NPCS Only 9–10 birds left in the wild in 1990 (Swinnerton, 2001; Swinnerton et al., 2004) and therefore we predicted it would have become EW before 2012. By 1988, the species was well established in captivity in at least seven zoological institutions other than Durrell and Mauritius and so we assume it would have persisted in captivity until 2012 (continued on next page) 87 Table 1 (continued) 88

Species, programme duration and role of Durrell within partnership Current and counterfactual Red List categories. For Reasons for 2012 counterfactual Red List category species undergoing status change the adjusted Red List category history is given (from Hoffmann et al., 2010) ‘80 ‘88 ‘94 ‘96 ‘00 ‘04 ‘08 ‘12 ‘12 CF Rodrigues fody Foudia flavicans. 1982-ongoing. Programme partner focusing on EN VU NT Ew Ceasing habitat protection and restoration would have significantly jeopardized the captive breeding, research and capacity building; provision of strategic, population recovery. Only 5–6 pairs left in wild in 1968 (Impey et al., 2002) and technical and financial support to MWF. Other local partner: NPCS probably not significantly above 100 birds in 1988 (C. Jones, pers. comm.) and therefore we predicted it would have become EW before 2012. By 1988, it was held by one zoological institution other that Durrell and so we assume it would have persisted in captivity until 2012 Rodrigues warbler rodericanus. 1982-ongoing. Programme partner CR EN NT EX Ceasing habitat protection and restoration would have significantly jeopardized the focusing on research and capacity building; provision of strategic, technical and population recovery. 8 Pairs were known to exist in 1979 (C. Jones, pers. comm.) and financial support to MWF. Other local partner: NPCS probably not significantly above 100 birds in 1988 (C. Jones, pers. comm.) and therefore we predicted it would have become EX before 2012 Alaotran gentle lemur Hapalemur alaotrensis. 1990-ongoing. Lead implementing CR CR Site protection, conservation payments, and local policies and regulations would ..Yuge l ilgclCnevto 8 21)84–96 (2014) 180 Conservation Biological / al. et Young R.P. agency. Main local partners: DREF; WWF Madagascar; Madagascar Wildlife and not have happened probably leading to significantly increased habitat loss through Conservation burning and agricultural encroachment, and continuation of poaching. However, 2 and a population size of possibly 1000– with an AoO of approximately 300 km 2500 in 1988 we predicted the population would have persisted until 2012. Probable criteria met: B1ab (iii, v) Malagasy giant jumping rat Hypogeomys antimena. 1998-ongoing. Lead EN CR Site protection, site management, conservation payments, compliance and implementing agency. Main local partners: DREF; Fanamby; National Centre for enforcement, and local policies and regulations would not have happened leading Training in Environment, Research and Forestry (CNFREF) of Madagascar to continuation of high rates in Menabe Antimena dry forest, the only site at which the species exists. A PHVA model (Sommer et al., 2002) predicted rapid population declines and extinction within 24 years if rates of deforestation and feral predation continued unabated. Probable criteria met: E Narrow-striped mongoose Mungotictis decemlineata. 2002-ongoing. Lead VU VU Site protection, site management, conservation payments, compliance and implementing agency. Main local partners: DREF; Fanamby; CNFREF enforcement, and local policies and regulations would not have happened leading to continuation of high deforestation rates in Menabe Antimena, representing approximately 30% of species’ AoO (Woolaver et al., 2006). Species has persisted in other areas of its range with little effective habitat conservation and no clear evidence the species would have met any EN or CR criteria. Probable criteria met: B1ab (ii–v) Rodrigues fruitbat Pteropus rodricensis. 1982-ongoing. Programme partner focusing CR CR Ceasing Durrell’s captive breeding would not have affected wild population as no on captive breeding, research and capacity building; provision of strategic, animals were released back to wild (from Durrell or other institution). Ceasing site technical and financial support to MWF. Other local partner: NPCS management and habitat restoration is likely to have led to some habitat loss. We assume the moratorium on hunting would have remained in place. By 1988, this species had recovered from a low of 70 individuals in 1979 to around 800 (C. Jones, pers. comm.) and therefore we predicted its population would have persisted until 2012. Probable criteria met: B1ab (iii) Pygmy hog Porcula salvania. 1996-ongoing. Lead implementing agency. Main local CR CR Captive breeding and release programme would not have happened and therefore partners: Ecosystems India; Assam Forest Department new populations in Sonai Rupai Wildlife Sanctuary and Orang National Park would not have been established. Work to improve site management in Manas National Park to ensure the grasslands are more suitable for pygmy hogs would not have happened which could have led to further declines in the last remaining wild population. Probable criteria met: C2a (ii) Black lion tamarin Leontopithecus chrysopygus. 1985-ongoing, Partner in EN EN Ceasing Durrell’s captive breeding programme, technical support and training of collaborative recovery programme focusing on captive breeding and release, national-level partner staff is likely to have jeopardized the first releases in Morro and training staff from national-level partners. Main local partner: Instituto de do Diabo NP in 1999–2001. Financial support to main national-level partner would Pesquisas Ecológicas (IPÊ); International Committee for the Conservation and not have happened, which helped fund habitat corridor restoration. However, no Management of Lion (ICCM) clear evidence the species would have met any CR criteria without this support. Probable criteria met: B2ab (iii) Leontopithecus rosalia. 1975-ongoing. Partner in collaborative CR EN EN Ceasing Durrell’s captive breeding programme would not have had a significant recovery programme focusing on captive breeding and release, and training staff impact on the wider ex-situ programme with the species held by many 10s of other from national-level partners. Main local partner: University of Brasília; zoological institutions by 1988. Training of staff from national-level partners would International Committee for the Conservation and Management of Lion have ceased. However, we predicted the work of the many other national- and Tamarins (ICCM) international-level partners would still have led to the recovery to EN. Criteria met: B1ab (iii) R.P. Young et al. / Biological Conservation 180 (2014) 84–96 89

Fig. 1. Locations of long-term species conservation programmes operated by Durrell and its national-level partners. of species in the wild. The genuine status changes given by the series). Each ‘run’ produced an RLI for the complete time period Hoffmann et al. (2010) were updated using the latest information for each taxonomic group, incorporating extrapolation and tempo- in BirdLife International (2013b) to account for any further cate- ral uncertainty. Following Butchart et al. (2010), ten thousand such gory changes that occurred after 2010. Due to differences in the runs were generated for each taxonomic group, and the mean was timing of Red List assessments for these three groups, we modelled calculated. The aggregated RLI was calculated as the arithmetic an RLI for each taxonomic class separately with an aggregated RLI mean of modelled RLIs for each taxa and the 2.5% estimate (lower) calculated as the arithmetic mean of the three modelled RLIs. The and 97.5% (upper) values were used to generate the 95% confidence RLIs for each taxonomic group were interpolated linearly for years interval displayed in Fig. 3. between data points and extrapolated linearly (with a slope equal The counterfactual RLI was calculated by predicting what Red to that between the two closest assessed points) back to 1988 List category each of the 17 species would have qualified at in (eight years before the first assessment for mammals, following 2012 if all Durrell-led or -supported conservation actions had Butchart et al., 2010) and forwards to 2012 for years for which esti- ceased in 1988 and if threats at the time had continued unabated, mates were not available (with a slope equal to that between the following the logic of Butchart et al. (2006a) (see below). These two closest assessed points), following the method of Butchart 2012 counterfactual categories were used to calculate a counter- et al. (2010). Rather than extrapolating deterministically, this factual RLI value for 2012, and a line fitted back to the observed method incorporates extrapolation uncertainty by selecting the RLI value in 1988. For Critically Endangered bird species, we fol- slope used for extrapolation from a normal distribution with a lowed the criteria of Butchart et al. (2006a) to establish the likeli- probability equal to the slope of the closest two assessed points, hood of whether a species would not have survived as extant if and standard deviation equal to 60% of this slope (i.e. the CV is conservation had been withdrawn in 1988. Butchart et al. 60%). Given that only one amphibian species was included in the (2006a) drew up a list of bird species that had a minimum popula- Durrell RLI, and therefore only one species contributed to the RLI tion estimated to be fewer than 100 individuals in 1994 or had a trend between 1980 and 1988 we set the starting point of the current population that was estimated to be fewer than 200 indi- aggregated RLI at 1988, when all the birds were first assessed. viduals and estimated, inferred or suspected to be declining at a The ‘true’ RLI likely changes from year to year, whereas assess- rate of more than 80% over 10 years or three generations (which- ments are repeated only at multi-year intervals, meaning the pre- ever was longer). They then determined whether each species cise value for any particular year is uncertain. To make this explicit, was likely to have gone extinct during 1994–2004 if conservation a final RLI value was assigned to each taxonomic group for each action had ceased in 1994, using published and expert-based infor- year from a 5 year moving window, centred on the focal year (with mation on the population size, trends, severity of threats and the window set as 3–4 years for the first two and last two years in intensity and effectiveness of conservation interventions. In their 90 R.P. Young et al. / Biological Conservation 180 (2014) 84–96

(a) Benefited from conservation No detected benefit from conservation there was clear evidence that the species would have deteriorated further or still improved without this conservation. Agriculture & aquaculture Finally, for the species that were downlisted to a lower category Invasive species Logging & wood harvesting of extinction risk during 1988–2012, we calculated the mean & severe weather number of years between the start of the intervention and the date Hunting the species first qualified for downlisting (according to the data Urban development presented in Hoffmann et al., 2010). For all species, Durrell either Fire instigated the conservation programmes or was involved from the time when significant conservation interventions were initi- Water management ated. To account for species that may have recovered sufficiently 012345678 to merit downlisting to a lower Red List category between the start Number of species of the intervention and 1988 (the year Red List categories were first assigned) we examined the population histories of each downlist- Benefited from conservation No detected benefit from conservation (b) ed species prior to 1988. All qualified as Critically Endangered in Species management 1988 except the Rodrigues fody which qualified as Endangered Land protection (see Table 1). At the start of the intervention for this species in Invasive species control 1982, its population was likely over 100 individuals and not declin- Land management ing and therefore probably would have still qualified as Endan- Habitat restoration gered (under criterion D) at that date. External capacity building Education & awareness 2.3. Threats and conservation actions Livelihood & other incentives For each species in the RLI, we coded the threats operating dur- Law & policy ing the intervention period and the conservation actions imple- 012345678 mented (see Table A1). We used data available for birds (at Number of species www.birdlife.org/datazone/species) on the impact of threats,

Fig. 2. Number of species (a) impacted by different threat types and (b) receiving based on their timing, scope and severity, to exclude any of low different actions that ‘benefited from conservation’ (i.e. they qualified for down- or negligible impact. For mammals and amphibians, there is no listing on the IUCN Red List since 1988 owing to conservation action according to data source on the impact scores for current or historical threats Hoffmann et al. (2010) or they were predicted to have avoided a status deterio- and therefore we made judgements based on the BirdLife Interna- ration due to conservation; dark grey bars), compared with species that showed ‘no tional threat scoring system on their likely impact so as to only detected benefit from conservation’ (no change in Red List category compared with the counterfactual or qualified for uplisting to a higher category of extinction risk consider threats of a medium or high impact. We coded the threats since 1988; light grey bars). following the ‘1st Level of Classification’ of the IUCN-CMP Unified Classification of Direct Threats Version 3.1 (2011; Salafsky et al. (2008)). Given the very broad definition of the Biological Resource Use and Natural System Modification categories and their preva- lence among the species considered, for these threat types we used the 2nd Level of Classification sub-categories. We coded the conservation actions following the ‘1st Level of Classification’ from the IUCN – CMP Unified Classification of Conservation Actions Needed Version 2.0 (Salafsky et al. (2008). Given the very broad definition of the Land/Water Management category, and its importance in Durrell’s conservation pro- grammes, for this conservation action we used the 2nd Level of Classification sub-categories, which importantly allowed us to dis- tinguish between 2.1. Site/Area Management (hereafter referred to as Land Management); 2.2. Invasive/Problematic Species Control (hereafter referred to as Invasive Species Control; and 2.3. Habitat and Natural Process Restoration (hereafter referred to as Habitat Restoration). For each different threat or action type, we then calculated the number of species that were downlisted on the Red List or avoided Fig. 3. Trends in the Red List Index of Species Survival for Durrell’s target species (solid black line with 95% confidence interval) and for the counterfactual scenario uplisting compared with the counterfactual (hereafter referred to (dashed black line). as species that ‘benefitted from conservation’), and the number that remained unchanged compared with the counterfactual or were uplisted on the Red List (hereafter referred to as species that analysis Butchart et al. (2006a), predicted that the pink pigeon N. experienced ‘no detected benefit from conservation’, recognizing mayeri and Echo parakeet P. eques would have been likely to have that some or many probably did benefit, but to a degree that did gone extinct during 1994–2004 in the absence of conservation, and not affect their Red List categorization) (Fig. 2a and b). To investi- that the Mauritius kestrel F. punctatus, Rodrigues warbler A. roder- gate ability to mitigate different threats and the potential effective- icanus and Rodrigues fody F. flavicans would have gone extinct ness of conservation actions we used a ’s Exact Test (Fisher, prior to 1994. 1922) on a series of 2 Â 2 contingency tables to test for an unequal To determine the counterfactual 2012 Red List categories for all distribution of species between the benefit and the no benefit cat- other species in the Durrell RLI, we assumed that the earliest Red egories in the presence versus absence of each of the threats and List category would have remained unchanged if the conservation conservation actions. All statistical analyses were conducted in R activities led or supported by Durrell had ceased in 1988, unless 2.11.1 (R Development Core Team, 2008). R.P. Young et al. / Biological Conservation 180 (2014) 84–96 91

3. Results logging and wood-harvesting (13), and invasive alien species (11) (Fig. 2a). Invasive species was the only threat that showed a differ- 3.1. Red List Index ence between the ratio of numbers of species that benefited versus did not experience a detectable benefit from conservation when Across the 17 species included in the Durrell RLI, 12 ‘genuine the threat was present versus when it was absent (Fishers Exact category changes’ relating to nine species occurred between 1988 Test, odds ratio = 11.1, P = 0.049). Of 11 species impacted by and 2012 (Table 1, some species moved categories in more than invasive species, eight experienced a benefit from conservation one time period between assessments), 11 of which were improve- compared to three for which we did not detect any benefit. ments (downlisting to lower Red List categories) in eight species Species management (15 species), land protection (13) and land and all were the result of conservation actions (Hoffmann et al., management (13) were the top three most commonly imple- 2010). For example, the Mallorcan midwife toad A. muletensis mented actions (Fig. 2b). Invasive alien control was the only con- was downlisted from Critically Endangered to Vulnerable under servation action for which there was a difference in the ratio of criterion D2 between 1996 and 2004 as a result of captive breeding species that benefited and did not benefit from conservation (- and reintroduction combined with invasive species control. This ers Exact Test, odds ratio = 18.8, P = 0.015). Of eight species for led to the re-establishment of populations and the recovery of which invasive alien control was implemented as a conservation established populations (Table 1). The twelfth status change was action, seven species benefitted whereas only one species did not the deterioration in the status of the Meller’s duck A. melleri during experience a detected benefit. This compared with a corresponding 1988–1994, driven mainly by the conversion of wetlands to rice ratio of two and seven species when invasive species control was production and hunting which is estimated to have caused the not implemented. population size to fall below 2500 mature individuals, qualifying the species for uplisting from Vulnerable to Endangered under cri- terion Red List criterion C2aii by 1994. Overall, the category 4. Discussion changes equate to a net mean rate of 0.44 species per year moving one Red List category away from extinction. These status improve- In this study, we tested for the first time the practicality of the ments drove a positive trend in the Durrell RLI (Fig. 3) which RLI for evaluating institutional-level conservation impacts. By con- increased from a mean index value of 0.31 (95% CI: 0.29–0.32) in trasting an observed RLI with a counterfactual scenario we show it 1988 to 0.52 (95% CI: 0.51–0.52) in 2012, an increase of 67.1% is possible to measure trends in the impact of an organization’s (2.7% per year). conservation efforts on the relative survival probability of a mod- Of the eight species that were downlisted to lower categories of estly sized set of bird, mammal and amphibian species. We also extinction risk between 1988 and 2012, the mean number of years show that the length of time required for a detectable recovery between the start of the conservation intervention and the year of in this group of globally threatened vertebrate species, as mea- the first downlisting was 16.3 years (±1.2 SE; range: 11–25 years; sured by an improvement in Red List category, is on average just n = 8). over 16 years. Table 1 gives the predicted Red List categories for all 17 species The main driver of the positive trend observed in the Durrell RLI in 2012 under the counterfactual scenario of Durrell-led or is the successful efforts in Mauritius since the late 1970s to con- supported conservation actions ceasing in 1988, along with infor- serve highly threatened birds. The downlisting of six of these bird mation on the duration of the intervention, main threats and species (Mauritius kestrel, echo parakeet, pink pigeon, Mauritius actions implemented. We predicted that Red List categories for fody, Rodrigues fody and Rodrigues warbler) represents a globally 10 species would have remained unchanged from their original significant species conservation success story. It has been brought category, whereas six species would have deteriorated and one about through intensive hands-on management of wild popula- would still have improved. Five Mauritian birds were predicted tions including captive breeding and release, clutch and brood to have moved from Critically Endangered to Extinct (or Extinct manipulations, nest site enhancement and the provisioning of nest in the Wild) and the Malagasy giant jumping rat would have been boxes, supplemental feeding, translocations as well as controlling uplisted from Endangered to Critically Endangered. A population invasive predators and restoring forest through weeding viability model produced prior to the conservation intervention and planting. The other downlistings resulting from genuine was implemented predicted severe and rapid population declines improvements in status related to golden lion tamarin L. rosalia sufficient to have likely met Criterion E of the CR category, assum- (which was downlisted from Critically Endangered to Endangered ing rates of deforestation and feral dog predation had continued in 2004 following a long-term programme of captive breeding, unabated (see Table 1). We predicted the golden lion tamarin how- reintroduction, site management and habitat restoration) and Mal- ever would have still have improved in status, from Critically lorcan midwife toad (which was downlisted from Critically Endan- Endangered to Endangered, due to the number of international gered to Vulnerable in 2004 after a long-term captive breeding and and national-level organizations involved in this recovery pro- reintroduction programme). gramme and the relatively small role played by Durrell. The 17 species included in this study faced nine main threats The counterfactual RLI declined by 23.4% during 1988–2012 with nine different main conservation actions implemented in (0.9% per year) to a value of 0.24 in 2012. Overall, this represents response. Most notable was the difference in the ratio of the a mean rate of 0.18 species per year moving one Red List category numbers of species benefitting versus not experiencing a towards extinction. The absolute difference in 2012 between index detected benefit from conservation when invasive species control values in the Durrell and counterfactual RLIs is therefore 0.29, was and was not implemented. This result suggests that in the which can be attributed to the conservation efforts of Durrell and geographic regions and conservation contexts involved in this its national-level partners. study, invasive species was the most tractable threat in terms of enabling species recovery. This is unsurprising as of seven spe- cies benefitting from conservation, six were Mauritian birds, 3.2. Threats and conservation actions where invasive species was often the primary threat through pre- dation of eggs, nestlings or adults, and where invasive species The principal threats to the 17 species in terms of proportion of management has been successfully implemented and sustained species affected were agriculture and aquaculture (16 species), since 1985 (Jones and Hartley, 1995). This finding is in line with 92 R.P. Young et al. / Biological Conservation 180 (2014) 84–96 the well-documented impacts of invasive mammalian species in As it may require a substantial increase in population or geo- particular on oceanic island faunas (see Courchamp et al., 2003; graphic range size, or a major reduction in the rate of decline, for Simberloff et al., 2013 for reviews). These analyses, however, a globally threatened species to move into a lower Red List cate- are based on very small sample sizes and did not attempt to gory of extinction risk, the RLI is best suited to tracking changes quantify the magnitude of the impact of the different threats in the status of species over at least moderate time periods (4– types which is necessary to understand better the ability to mit- 5 years or more). While deteriorations in status, and hence igate different threats and the relative effectiveness of different uplistings on the Red List can happen very rapidly (e.g. Indian conservation actions. white-backed Gyps bengalensis and long-billed Gyps indicus vul- In order to evaluate fully the impacts of a conservation pro- tures, Prakash et al., 2003; spoon-billed sandpiper Eurynorhynchus gramme it is necessary to ask what would have happened if there pygmeus, Zockler et al., 2010; and , Milner-Gulland had been no intervention, a process of making inferences about an et al., 2001), for the eight study species that improved in status it unobserved counterfactual event that is rarely applied in conserva- took on average 16.3 years from the start of the intervention to tion programme evaluation (Ferraro and Pattanayak, 2006). In the the year of the first downlisting, with a range of 11–25 years. current study, we predicted what would have happened to the tar- The 16 year period reflects the time needed for actions to be get species by 2012 if conservation had been withdrawn in 1988 implemented sufficiently to mitigate threats allowing population (the start date of the RLI). We considered an alternative approach recovery of a magnitude to merit downlisting. It also reflects the to evaluating the impact of conservation actions on the target spe- periodicity of the assessment schedule, which at its most fre- cies by contrasting them with a set of comparator species, matched quent takes place every 4 years (for birds). There is a clear mis- for a range of biological traits but subject to no or much reduced match between the average time to first downlisting shown conservation effort. However, the types of species targeted by Dur- here and the typical conservation funding time-frames of rell essentially represent unique treatment units without obvious 2–4 years. For the many globally threatened species with longer comparators, a common barrier to such quasi-experimental generation lengths than species in this study Pacifici et al. designs (Ferraro, 2009). Many of the target species in this study (2013) and therefore often longer population recovery times, are from restricted island faunas with very few or no biologically the time from initiation of conservation interventions to first similar species with comparable population histories but contrast- downlisting is likely to be significantly longer than the 16 years ing conservation efforts. reported here. This also emphasizes the challenge of meeting Predicting counterfactual Red List categories for the Mauritian the CBD Aichi Target 12, under which the world’s governments birds was relatively straightforward, as the population histories, have committed to improving the status of known threatened threats and conservation actions are well known, and several had species by 2020 (CBD, 2010a). been documented by a previous study examining the number of prevented by conservation interventions (Butchart et al., 2006a). In the 1980s, five of the Mauritian bird species were 5. Conclusion at extremely low population sizes (<100 individuals), with a strong likelihood of high-impact threats returning should conservation As an indicator of institutional impact, the RLI is most practical actions be withdrawn, and therefore a high likelihood that they for organizations with a relatively small set of target species that would have gone extinct (Butchart et al., 2006a). Assessing have restricted distributions (and therefore for which the institu- ‘avoided category changes’ requires detailed information on popu- tion’s interventions can impact a large proportion of the population lation sizes and trends, and threats and effectiveness of conserva- of each species). For example, during 2008–2012, the BirdLife tion actions, which are often not available for taxa other than International Partnership undertook conservation action for 537 birds. For this reason, predicting counterfactual 2012 categories threatened bird species in over 140 countries worldwide for amphibian and mammal species in the current study was not (BirdLife International, 2013c). Determining the counterfactual sta- as straightforward. For the Malagasy giant jumping rat, the avail- tus in the absence of conservation for each of these species would ability of a population viability model (Sommer et al., 2002) pro- be a significant challenge, as would ascribing the impact of actions duced prior to a major forest conservation intervention enabled by BirdLife Partners or Species Guardians for species that span us to judge that conservation had led to an ‘avoided uplisting’ of multiple countries (which is the case for 37% of threatened bird this species. A set of standard criteria and levels of evidence for species: BirdLife International, 2013b) and which may receive con- estimating counterfactual RLIs for a range of taxa would be needed servation actions implemented by multiple organizations and to ensure consistency in impact measurement performed by differ- agencies. ent institutions and across different conservation programme Using the RLI to track the impact of an institution has a further structures. limitation. It relies on target species being periodically assessed for Determining the counterfactual modern-day Red List categories the IUCN Red List which in turn relies on the activities of IUCN Spe- for the target species was also challenging given all of the pro- cies Survival Commission Specialist Groups, IUCN Red List Partners grammes are implemented as part of partnerships of national and Red List Authorities, which often operate voluntarily. The and international conservation organizations. As part of its opera- number of species assessments in the Red List now exceeds over tional strategy, Durrell works in close long-term partnerships with 70,000 species (IUCN, 2013a) but RLIs are only currently available national-level organizations (or national-level programmes of for birds, mammals, amphibians and corals. Substantially greater international outfits) to deliver and build capacity for conservation funding and more efficient processes are required to scale up the actions. These partnerships are so intertwined that for the majority taxonomic coverage and frequency of reassessments (Stuart of species in this study we found it impossible to sensibly disaggre- et al., 2010; Rondinini et al., 2013). gate the relative contributions of the institutions involved. We also The action-focused RLI indicator is well-suited for raising did not consider the impact of any other agencies external to these awareness for public and policy makers, auditing management partnerships that may have implemented actions benefitting the actions and informing policy decisions (Jones et al., 2013). Like target species, mainly because these were extremely difficult to macroeconomic indicators, such as the FTSE 100 or Dow Jones quantify and rare in occurrence. The conservation impacts reported Index, it is intuitively understandable to non-technical audiences here therefore are acknowledged as shared between Durrell and its despite its underlying technical complexity (Jones et al., 2013). national-level partners. Therefore, the RLI is a useful tool in demonstrating and R.P. Young et al. / Biological Conservation 180 (2014) 84–96 93 communicating medium to long-term conservation impacts of Acknowledgements institutions and programmes to a range of non-technical but influ- ential audiences such as trustees, supporters and donors. To con- The authors would like to thank the many people whom have clude, by contrasting an observed with a counterfactual RLI this contributed to the IUCN Red List assessments upon which these study provides scarce but vital quantitative evidence that, given analyses are based. We are also grateful to Nik Cole, Glyn Young, time, intensive and sustained conservation efforts can significantly Lance Woolaver, Herizo Andrianandrasana, Matthew Morton and improve the status of threatened species. With widespread uncer- Dominic Wormell for their useful information and insights in the tainty about the effectiveness of conservation investments (Ferraro design and drafting of the manuscript. The research was funded and Pattanayak, 2006), and the need to show progress towards CBD by the institutions to which the authors are affiliated. Aichi Target 12 at global, national and sub-national levels, this study suggests the RLI can make an important contribution to eval- Appendix A uating the performance of species-focused conservation institu- tions and programmes. Supplementary Table A1.

Table A1 Historical and current threats, and conservation actions for species targeted by Durrell. For species that qualified for a genuine Red List category change since 1988 (both down and uplisting) or have avoided being downlisted, the main threats driving the change or mitigated by the conservation action are highlighted in bold.

Species Threats to species Species and site-based conservation actions implemented by Durrell and/or national-level partners Mallorcan midwife toad Alytes muletensis Housing and urban areas Invasive species control Commercial and industrial areas /translocation Dams and water management/use Captive breeding Invasive species Training Droughts Mauritius fody Foudia rubra Annual and perennial non-timber Site/area protection crops Invasive species Invasive species control Logging and wood harvesting Habitat and natural process restoration Species recovery Species re-introduction/translocation Captive breeding Mauritius kestrel Falco punctatus Annual and perennial non-timber Site/area protection crops Logging and wood harvesting Invasive species control Invasive speciose Species recovery Agricultural and forestry effluents Species reintroduction/translocation Captive breeding Training Institutional and civil society development Conservation finance Echo parakeet Psittacula eques Wood and pulp plantations Site/area protection Logging and wood harvesting Invasive species control Invasive species Habitat and natural process restoration Problematic native species Nest protection Species reintroduction/translocation Captive breeding Training Institutional and civil society development Conservation finance Madagascar teal Anas bernieri Annual and perennial non-timber Site/area protection crops Marine and freshwater aquaculture Captive breeding Hunting and trapping terrestrial Training animals Logging and wood harvesting Meller’s duck Anas melleri Annual and perennial non-timber Site/area protection crops Hunting and trapping terrestrial Captive breeding animals Logging and wood harvesting Training Invasive species Agricultural and forestry effluents Olive white eye Zosterops chloronothos Annual and perennial non-timber Site/area protection crops Logging and wood harvesting Invasive species control Invasive species Habitat and natural process restoration Species recovery Captive breeding Pink pigeon Nesoenas mayeri Annual and perennial non-timber Site/area protection

(continued on next page) 94 R.P. Young et al. / Biological Conservation 180 (2014) 84–96

Table A1 (continued)

Species Threats to species Species and site-based conservation actions implemented by Durrell and/or national-level partners crops Logging and wood harvesting Invasive species control Invasive species Habitat and natural process restoration Storms and flooding Species recovery Species reintroduction/translocation Captive breeding Training Institutional and civil society development Conservation finance Rodrigues fody Foudia flavicans Annual and perennial non-timber Site/area protection crops Livestock farming and ranching Site/area management Invasive species Invasive species control Storms and flooding Habitat and natural process restoration Captive breeding Rodrigues warbler Acrocephalus Annual and perennial non-timber Site/area protection rodericanus crops Invasive species Site/area management Invasive species control Habitat and natural process restoration Alaotran gentle lemur Hapalemur Annual and perennial non-timber Site/area protection alaotrensis crops Livestock farming and ranching Site/area management Hunting and trapping terrestrial Species management animals Fire and fire suppression Captive breeding Awareness and communications Legislation Policies and regulations Compliance and enforcement Linked enterprises and livelihood alternatives Conservation payments Institutional and civil society development Malagasy giant jumping rat Hypogeomys Annual and perennial non-timber Site/area protection antimena crops Livestock farming and ranching Site/area management Hunting and trapping terrestrial Captive breeding animals Logging and wood harvesting Awareness and communications Invasive species Training Legislation Policies and regulations Compliance and enforcement Livelihood, economic and other incentives Conservation payments Institutional and civil society development Narrow-striped mongoose Mungotictis Annual and perennial non-timber Site/area protection decemlineata crops Livestock farming and ranching Site/area management Logging and wood harvesting Legislation Policies and regulations Compliance and enforcement Livelihood, economic and other incentives Conservation payments Institutional and civil society development Rodrigues fruitbat Pteropus rodricensis Annual and perennial non-timber Habitat and natural process restoration crops Hunting and trapping terrestrial Captive breeding animals Logging and wood harvesting Legislation Problematic native species Training Storms and flooding Institutional and civil society development Conservation finance Pygmy hog Porcula salvania Annual and perennial non-timber Site/area management crops Wood and pulp plantations Habitat and natural process restoration Livestock farming and ranching Species management Hunting and trapping terrestrial Species re-introduction/translocation animals Logging and wood harvesting Captive breeding Fire and fire suppression Training Awareness and communications Linked enterprises and livelihood alternatives Institutional and civil society development R.P. Young et al. / Biological Conservation 180 (2014) 84–96 95

Black lion tamarin Leontopithecus Annual and perennial non-timber Site/area protection chrysopygus crops Wood and pulp plantations Site/area management Livestock farming and ranching Habitat and natural process restoration Logging and wood harvesting Species re-introduction/translocation Captive breeding Awareness and communications Conservation finance Golden lion tamarin Leontopithecus rosalia Housing and urban areas Site/area management Annual and perennial non-timber Habitat and natural process restoration crops Livestock farming and ranching Species reintroduction/translocation Hunting and trapping terrestrial Captive breeding animals Logging and wood harvesting Fire and fire suppression

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