Nigel J. Collar

Quantification of Extinction Risk: IUCN's System for Classifying Threatened Species

The International Union for Conservation of Nature (IUCN) Red List of Threatened Species was increasingly used during the 1980s to assess the conservation status of species for policy and planning purposes. This use stimulated the development of a new set of quantitative criteria for listing species in the categories of threat: critically endangered, endangered, and vulnerable. These criteria, which were intended to be applicable to all species except microorganisms, were part of a broader system for classifying threatened species and were fully implemented by IUCN in 2000. The system and the criteria have been widely used by conservation practitioners and scientists and now underpin one indicator being used to assess the Convention on Biological Diversity 2010 biodiversity target. We describe the process and the technical background to the IUCN Red List system. The criteria refer to fundamental biological processes underlying population decline and extinction. But given major differences between species, the threatening processes affecting them, and the paucity of knowledge relating to most species, the IUCN system had to be both broad and flexible to be applicable to the majority of described species. The system was designed to measure the symptoms of extinction risk, and uses 5 independent criteria relating to aspects of population loss and decline of range size. A species is assigned to a threat category if it meets the quantitative threshold for at least one criterion. The criteria and the accompanying rules and guidelines used by IUCN are intended to increase the consistency, transparency, and validity of its categorization system, but it necessitates some compromises that affect the applicability of the system and the species lists that result. In particular, choices were made over the assessment of uncertainty, poorly known species, depleted species, population decline, restricted ranges, and rarity; all of these affect the way red lists should be viewed and used. Processes related to priority setting and the development of national red lists need to take account of some assumptions in the formulation of the criteria.

Value of the IUCN Red List

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How many bird extinctions have we prevented

Considerable resources and efforts have been directed at biodiversity conservation in recent years, but measures of the success of conservation pro- grammes have been limited. Based on information on population sizes, trends, threatening processes and the nature and intensity of conservation actions imple- mented during 1994-2004, we assessed that 16 bird species would have probably become extinct during this period if conservation programmes for them had not been undertaken. The mean minimum population size of these 16 species increased from 34 to 147 breeding individuals during 1994-2004. In 1994, 63% of them had declining populations but by 2004, 81% were increasing. Most of these species (63%) are found on islands. The principal threats that led to their decline were habitat loss and degradation (88%), invasive species (50%) and exploitation (38%), a pattern similar to that for other threatened species, but with exploitation and invasive species being relatively more important. The principal actions carried out were habitat protection and management (75% of species), control of invasive species (50%), and captive breeding and release (33%). The 16 species represent only 8.9% of those currently classified as Critically Endangered, and 1.3% of those threatened with extinction. Many of these additional species slipped closer to extinction during 1994-2004, including 164 that deteriorated in status sufficiently to be uplisted to higher categories of extinction risk on the IUCN Red List (IUCN, 2006). Efforts need to be considerably scaled up to prevent many more extinctions in the coming decades. The knowledge and tools to achieve this are available, but we need to mobilize the resources and political will to apply them.

The reasons for Red Data Books

The late Sir Peter Scott, a former President of Fauna and Flora International, proposed the idea of Red Data Books as conservation tools more than 30 years ago. Today, the international Red Data Book programme appears to be effectively at an end, with priority being given to Action Plans and Conservation Assessment Management Plans for groups oftaxa. These, however, cannot entirely replace Red Data Books, and the author of this paper argues that Red Data Books have many vital roles to play in species conservation and makes a plea for their renascence.

Museum DNA reveals the demographic history of the endangered Seychelles warbler

The importance of evolutionary conservation – how understanding evolutionary forces can help guide conservation decisions – is widely recognized. However, the historical demography of many endangered species is unknown, despite the fact that this can have important implications for contemporary ecological processes and for extinction risk. Here, we reconstruct the population history of the Seychelles warbler (Acrocephalus sechellensis) – an ecological model species. By the 1960s, this species was on the brink of extinction, but its previous history is unknown. We used DNA samples from contemporary and museum specimens spanning 140 years to reconstruct bottleneck history. We found a 25% reduction in genetic diversity between museum and contemporary populations, and strong genetic structure. Simulations indicate that the Seychelles warbler was bottlenecked from a large population, with an ancestral Ne of several thousands falling to <50 within the last century. Such a rapid decline, due to anthropogenic factors, has important implications for extinction risk in the Seychelles warbler, and our results will inform conservation practices. Reconstructing the population history of this species also allows us to better understand patterns of genetic diversity, inbreeding and promiscuity in the contemporary populations. Our approaches can be applied across species to test ecological hypotheses and inform conservation.

Distribution, status and conservation of the Bengal Florican Houbaropsis bengalensis in Cambodia

Summary The Bengal Florican is a ‘Critically Endangered’ bustard (Otididae) restricted to India, Nepal and southern Indochina. Fewer than 500 birds are estimated to remain in the Indian subcontinent, whilst the Indochinese breeding population is primarily restricted to grasslands surrounding the Tonle Sap lake, Cambodia. We conducted the first comprehensive breeding season survey of Bengal Florican within the Tonle Sap region (19,500 km 2 ). During 2005/06 and 2006/07 we systematically sampled 1-km squares for territorial males. Bengal Florican were detected within 90 1-km squares at a mean density of 0.34 males km � 2 which, accounting for unequal survey effort across grassland blocks, provides a mean estimate of 0.2 males km � 2 . Based on 2005 habitat extent, the estimated Tonle Sap population is 416 adult males (333–502 6 95% CI), more than half of them in Kompong Thom province. Tonle Sap grasslands are rapidly being lost due to intensification of rice cultivation and, based on satellite images, we document declines of 28% grassland cover within 10 grassland blocks between January 2005 and March 2007. Based on mean 2005 population densities the remaining grassland may support as few as 294 adult male florican, a decline of 30% since 2005. In response to these habitat declines almost 350 km 2 of grassland have been designated as protected areas, set aside for biodiversity and local livelihoods. Conservation activities in these areas include participatory land-use zoning, patrols reporting new developments to government officials, awareness-raising and incentive-led nest protection schemes.

The impact of translocations on neutral and functional genetic diversity within and among populations of the Seychelles warbler

Translocations are an increasingly common tool in conservation. The maintenance of genetic diversity through translocation is critical for both the short‐ and long‐term persistence of populations and species. However, the relative spatio‐temporal impacts of translocations on neutral and functional genetic diversity, and how this affects genetic structure among the conserved populations overall, have received little investigation. We compared the impact of translocating different numbers of founders on both microsatellite and major histocompatibility complex (MHC) class I diversity over a 23‐year period in the Seychelles warbler (Acrocephalus sechellensis). We found low and stable microsatellite and MHC diversity in the source population and evidence for only a limited loss of either type of diversity in the four new populations. However, we found evidence of significant, but low to moderate, genetic differentiation between populations, with those populations established with fewer founders clustering separately. Stochastic genetic capture (as opposed to subsequent drift) was the main determinant of translocated population diversity. Furthermore, a strong correlation between microsatellite and MHC differentiation suggested that neutral processes outweighed selection in shaping MHC diversity in the new populations. These data provide important insights into how to optimize the use of translocation as a conservation tool.

Rapid declines in habitat quality and population size of the Liben (Sidamo) Lark Heteromirafra sidamoensis necessitate immediate conservation action

The Critically Endangered Liben Lark (formerly Sidamo Lark) is known only from the Liben Plain of southern Ethiopia, where rapid grassland deterioration is driving the species towards extinction. Fieldwork on the Liben Plain in May 2009 to assess changes in habitat and population since June 2007 recorded a significant deterioration in habitat and decline in numbers. In both 2007 and 2009, birds were associated with areas with greater than average grass cover, and in 2007 with areas of higher grass. However, between 2007 and 2009 there was a significant decline in grass cover and height, a 40% decline in number of birds recorded along repeated transects, and a contraction of 38% in the occupied area of the Liben Plain. Moreover, the cover of bare ground increased more in areas where the species was recorded in 2007 than at random points, suggesting a more rapid degradation of the best sites. There was also a loss to arable agriculture of 8% of the grassland present in 2007. Invading fennel plants increased in number and area on the plain but did not appear to influence the distribution of the lark. An analysis of NDVI showed that grassland deterioration could not be explained by drought, and the most likely explanation is that grassland quality is suffering from overgrazing. Predictive modelling suggests that, apart from a smaller and politically insecure area some 500 km to the north-east near Somalia, there is no suitable habitat for this species elsewhere in the Horn of Africa. As a matter of extreme urgency, cattle exclosures need to be established on the Liben Plain to allow grassland regeneration. This may require the ploughing of land to reduce soil compaction and re-sowing with local grass species. In the longer term, further degradation of the plain should be prevented by, for example, clearing encroaching scrub to increase grassland area and reduce grazing pressure, and by developing sustainable rangeland management practices. These actions have the full and active support of local pastoralists.

Assessment mismatches must be sorted out: they leave species at risk

Sir — Although Rodríguez et al. are correct that nationally endemic taxa should be classified identically on national and global Red Lists, they provide no evidence to support their inferences that national Red Lists “are more accurate” than global Red Lists, or that global lists ignore a “wealth of local data”. Moreover, we see certain problems with the national Red Lists they analyse which suggest these inferences may be mistaken. Only nine of the 70 different assessments tabulated by Rodríguez et al. are due to different information about species. Thirty-two result from differences between IUCN assessors and the national assessors over the choices of taxa for consideration — especially taxa from groups such as reptiles, amphibians, bony fishes and invertebrates, which IUCN has only partially considered — and the inclusion of subspecies, which have not been a major focus of the IUCN Red List. Seven species were listed as Data Deficient on the national lists, whereas for the global list the same information was considered adequate to place them in a threatened category. Of particular concern are the cases resulting from inconsistent use in the national lists of the IUCN Red List Criteria (see Table 1). Many of these inconsistencies are compounded by national Red List assessments not making their use of the Red List Criteria explicit for each taxon, as required, and/or failing to provide supporting information (despite the claim that national Red Lists utilize a “wealth of local data”, the Argentine and Ecuador lists contain no supporting data whatsoever). At present IUCN recommends that experts making assessments for the global Red List should consult national authorities in reaching a decision. IUCN would like to move rapidly towards a situation where the national assessments could be used without any intermediate steps to ensure standardization of approaches. To this end IUCN has established two key initiatives. First, to improve information flow and quality, IUCN is appointing Red List Authorities (RLAs) who will ensure that all assessments are done in a fully consultative manner and are well documented and peer reviewed (a model established by BirdLife International). The RLAs will have access to shared databases of species information that will be based in part on interactive web technologies (see http://www.iucn.org/ themes/ssc/programs/sis. htm). Second, IUCN aims to improve consistency in the use of the Red List Criteria. It is running a series of regional Red List workshops around the world: the first, held in Sri Lanka in September 1999, involved participants from 12 Asian countries. Other workshops are planned for Mesoamerica, South America, southern Africa and east Africa. IUCN is also recommending and distributing standard computer software that takes assessors systematically through the categorization process. Progress in all this is constrained only by resources. Craig Hilton-Taylor*, Georgina M. Mace†, David R. Capper‡, Nigel J. Collar‡, Simon N. Stuart§, Colin J. Bibby‡, Caroline Pollock*, Jørgen B. Thomsen|| *IUCN/SSC UK Office, 219c Huntingdon Road, Cambridge CB3 0DL, UK †Institute of Zoology, Zoological Society of London, Regent’s Park, London NW1 4RY, UK ‡BirdLife International, Wellbrook Court, Girton Road, Cambridge CB3 0NA, UK §IUCN/SSC, Rue Mauverney 28, Gland CH-1196, Switzerland ||Conservation International, 2501 M Street, NW, Suite 200, Washington, DC 20037, USA

The science of bird conservation

Colin Bibby (1948–2004) was the quintessential bird conservation biologist. Over his career, he served as lead scientist at two of the world’s largest bird conservation organizations, the Royal Society for the Protection of Birds, and BirdLife International. His contributions encompassed detailed autecological studies of rare bird species such as the Dartford Warbler Sylvia undata (e.g. Bibby 1978) and Fuerteventura Stonechat Saxicola dacotiae (e.g. Bibby and Hill 1987), a sweeping synthesis of the techniques of bird conservation science (Bibby et al. 1992, 2000), and pioneering contributions in conservation planning such as the Endemic Bird Areas concept (ICBP 1992). This memorial volume of Bird Conservation International seeks to reflect the breadth of Colin’s legacy by presenting papers illustrating the role of ornithological science in saving threatened birds, reviews of novel field and analytical techniques, and syntheses of progress with the development of bird conservation strategies. In the first category, we include studies of albatrosses (Croxall et al.), South Asian vultures (Pain et al.), migratory species (Kirby et al.), and the Northern Bald Ibis Geronticus eremita (Bowden et al.). In the second, we have reviews of surveying bird abundance (Buckland et al.), bird-habitat associations (Lee and Marsden), fluctuating asymmetry (Lens and Eggermont), camera trapping (O’Brien et al.), automated sound recording (Brandes), stable isotopes (Hobson), and socio-economic surveys (MacMillan and Leader-Williams). Finally, we document progress in three key tools for bird conservation planning: atlases (Pomeroy et al.), population indices (Gregory et al.), and the IUCN Red List of threatened bird species (Butchart). We hope that this span from the specifics to the generalities of bird conservation science provides a fitting tribute to Colin’s life and work. To set the context for this tribute, however, we take advantage of our editorial privilege to reflect on the state of bird conservation science, and to assess its future potential. The urgency of the task faced by bird conservation science should not be underestimated. No fewer than 1,226 species of birds, out of 9,856 extant species, are threatened with extinction, almost one eighth of the total (BirdLife International 2008a). However, rates of endangerment for other vertebrate classes are worse (Baillie et al. 2004). To what extent is conservation science delivering the scientific knowledge necessary to save those 1,226 threatened birds—and indeed, biological diversity more generally? In this essay, we tackle five aspects of this question. First, we use information from the Handbook of the birds of the world to assess the prevalence of threatened species studies. Because the intensity of study varies greatly across threatened species, we then explore some factors that correlate with and might help explain this variation. Third, we switch data source to this very journal, specifically manuscripts published in Bird Conservation International over the last five years, to ask where conservation ornithologists come from. We continue this line of enquiry to examine the kinds of questions being pursued concerning threatened bird species. Finally, we speculate on the importance of bird conservation science as a pioneer and model for conservation science in general. We conclude with some suggestions for future priorities for bird conservation science as a discipline.