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Plants on the IUCN Red List: setting priorities to inform conservation
Review
Special Issue: Plant science research in botanic gardens
Plants on the IUCN Red List: setting priorities to inform conservation George E. Schatz Missouri Botanical Garden, PO Box 299, Saint Louis, MO 63166-0299, USA
The continuing decline of plant diversity will have a greater impact on human society than any other type of biodiversity loss. It is imperative, therefore, that efforts are increased to assess the conservation status of plants for the IUCN Red List of Threatened Species, the de facto baseline reference for many conservation decisions. As discussed here, a review of plants on the current Red List suggests that priorities for future Red Listing should serve multiple purposes: to inform national conservation policy, to contribute to global conservation analyses, to encompass the phylogenetic diversity of plants and to address the dependence of human societies on plants. Future progress in plant Red Listing requires greater participation by the world’s herbaria and increased support for expert networks. The unknown status of plant conservation Efforts to halt the continuing decline of biodiversity worldwide are currently hampered by inadequate knowledge of the threatened status of the organisms that constitute the fundamental basis for all life on Earth: green plants. As the IUCN Red List of Threatened Species (http:// www.iucnredlist.org/) has increasingly been adopted as the gold standard for information on the conservation status of species [1,2], plants have had a disproportionately minor role in the conservation-planning process. Whereas most species of vertebrates have been assessed globally for their conservation status and, thus, can contribute to prioritization analyses, only 3.2% of plant species currently appear on the IUCN Red List and only two groups of plants (conifers and cycads) have been (nearly) comprehensively assessed. Nevertheless, various estimates of the potential number of plant species threatened with extinction have approached 50% [3,4], a staggering figure given the fundamental role of plants as providers of food, shelter and medicine for human use and/or essential ecosystem services for all biodiversity. Several recent papers and reports have summarized progress on plant Red Listing in the context of the Global Strategy for Plant Conservation (GSPC) [5–7] and will be only briefly recapitulated here. It is clear that the (overly) ambitious GSPC Target 2 goal of ‘a preliminary assessment of the conservation status of all known plant species at national, regional, and international levels’ will not be met by 2010. However, a significant number of plant species have been evaluated over the past decade at both Corresponding author: Schatz, G.E. ([email protected])
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global and national levels, with both the IUCN Red List Categories and Criteria [8,9] (Figure 1) and other systems, and therefore contribute to our overall understanding of their conservation status and the magnitude of threats facing plants worldwide. With 2010 upon us, and a mandate from the United Nations Convention on Biological Diversity (CBD) to reformulate and reinvigorate the GSPC to reflect emerging threats, such as climate change [10], I suggest that priorities for plant Red Listing should be set that will directly inform the conservation of the planet’s green lifeline and ensure that maximum plant diversity is preserved for future generations. Plants on, and not on, the IUCN Red List The current online version of the IUCN Red List of Threatened Species (http://www.iucnredlist.org/) includes 11 995 species of bryophytes, ferns, lycopods, gymnosperms and angiosperms out of an estimated total number of species across those groups of 379 881 [11], or <3.2% (Table 1). In addition, 1016 infraspecies of gymnosperms and angiosperms are listed, as are two green algae and 58 red algae. Unfortunately, not all assessments are equivalent. Among the 13 011 listed taxa, 8505 (65%) were assessed before 2001 under the older version 2.3 of the IUCN Red List Categories and Criteria, whereas 4506 (35%) have been assessed since 2001 using the current version 3.1 of the Categories and Criteria. Therefore, with a recommended 10-year shelf life, assessments of nearly two-thirds of the currently listed taxa have either already expired or are set to expire by the end of 2010. Among those taxa are most of the 8120 tree species currently listed that were originally assessed for The World List of Threatened Trees [12]. Previously, the decision to standardize assessments to at least version 2.3 of Categories and Criteria meant that many of the 34 000 taxa listed in the 1997 IUCN Red List of Threatened Plants [13] were not retained. Numerous other plants that have been globally (or nationally) assessed for their conservation status over the past decade do not, however, appear on the IUCN Red List for a variety of reasons. The low number of only 346 North American taxa currently on the List reflects the use by NatureServe (http://www.natureserve.org/explorer) of a different system to assess the nearly 32 000 taxa native to Canada and the USA. Similarly, the 21 000 vascular plant species of Australia were previously monitored under Rare or Threatened Australian Plants [14], which has now been superseded by the Environment
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Review
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Figure 1. Structure of the IUCN Red List categories. Reproduced with permission from IUCN.
Protection and Biodiversity Conservation Act of 1999 (http://www.environment.gov.au/cgi-bin/sprat/public/ publicthreatenedlist.pl?wanted=flora), and New Zealand has applied its own system to its 2357 indigenous taxa [15]. The Global Tree Campaign has conducted 10 assessments of 2500 species of trees [6], including Magnoliaceae [16], oaks [17] and regional subsets of Ethiopian [18], Guatemalan [19] and Central Asian [20] tree species, very few of which have been incorporated into the Red List. Spanish language assessments of all 5500 Peruvian endemics [21], 46 species from Central and Southern Chile [22] and 8000 Spanish taxa [23] have also not been added to the Red List. The under-resourced and over-taxed Red List Program office simply has not had the capacity to keep pace with the number of submitted assessments, an untenable situation that will only be exacerbated by the increasing volume of plant assessments coming from South Africa (13 000 endemics), Madagascar (2850 endemics), the Critical Ecosystem Partnership Fund (CEPF) projects in the Caucasus (1000 endemics) and the Eastern Arc Mountains/Coastal Forests of East Africa (700 endemics), the Sampled Red List Index (7400 species) [5], seagrasses (60 species) and mangroves (50 species) contributed by the Global Marine Species Assessment, and the newly launched Global Cactus Assessment (1500 species), as well as many other smaller subsets. Given that >50% of countries have completed some form of plant Red List assessment at a national level [7], it is probable that the conservation status of at least 100 000 flowering plant species (28%) has been evaluated at some point during the past 20 years. Priorities for plant Red Listing Selection of plant species for Red Listing has been, and will probably continue to be, an ad hoc process depending upon Table 1. Numbers of plant species on the IUCN Red List of Threatened Species Taxon Bryophytes Ferns/Lycopods Gymnosperms Angiosperms Total a
Data from Ref. [11].
Estimated total spp. a 13 370 12 838 1391 352 282 379 881
Spp. on 2008 Red List 95 211 910 10 779 11 995
% 0.7 1.6 65 3 3.2
individual initiative and enthusiasm, and subject to the vagaries of funding. Nevertheless, renewal of the GSPC would benefit from a set of clearly articulated, strategic priorities for plant Red Listing that would serve multiple purposes: (i) to inform national conservation policy; (ii) to contribute to global conservation analyses and serve as a robust surrogate for all plants; (iii) to encompass the full phylogenetic diversity of plant life; and (iv) to address the fundamental dependence of human societies on plants. National and regional endemics Under the CBD, signatory countries are obligated to ensure the protection of species that occur only within their borders. As implementation of CBD decisions, such as the GSPC, must involve priority-setting at the country level, Red Listing of all national endemics, which by definition are then global assessments, should then form the basis for national conservation policy. Recent assessment projects that have focused on national endemics have revealed that >50% of the 4000 endemic Ecuadoran plant species are known from only one or two populations [24], and that 87% of the 5500 endemic Peruvian plant species are not recorded from within protected areas [21]. Baseline assessment of all national endemics leads directly to the identification of Important Plant Areas (GSPC Target 5) and highlights gaps in the protected areas network for in situ conservation of threatened species (GSPC Target 7). For example, in Madagascar, rare and threatened endemic species of Pandanaceae exposed priority sites for new protection [25]. However, despite the fact that 91% of the 34 000 species listed in the 1997 IUCN Red List of Threatened Plants were single-country endemics [13], much of biodiversity straddles political boundaries, which are often associated with geographical features (river basins or mountain ranges) that also constitute evolutionary hotspots of endemism. One wonders how many more species are endemic to both Ecuador and Peru. In the recent CEPF Caucasus plant assessment project, in addition to assessing all national endemics in Armenia, Azerbaijan, Georgia and the Caucasian areas of Russia and Turkey, a regional approach also targeted taxa endemic to two or three countries for assessment. Similarly, the CEPF Eastern Arc/Coastal Forests project (http://cepf.tfcg.org/) often encountered taxa distributed from the Taita Hills in Kenya to the southern limit of the Eastern Arc Mountains in 639
Review Tanzania, as well coastal forest endemics distributed from Somalia through Kenya and Tanzania to Mozambique. In calling for plant conservation assessments at national and regional levels in addition to international, the GSPC recognized the desire and need for countries to protect and monitor non-endemic species that might nevertheless be rare and of conservation concern within their borders. As governments allocate funds to meet their commitments under the CBD by carrying out assessments of both national endemics and national-level assessments of non-endemics, it is essential that some type of clearinghouse mechanism be developed to track implementation of Target 2 of the GSPC at national and regional levels [26]. Wild plants that contribute directly to human livelihoods and crop wild relatives In contrast to the developed world, where only a small percentage of the human population is engaged in agriculture (in the USA, there are 2.2 million farmers out of a total population of 304 million, or <1%; http://www. ers.usda.gov/StateFacts/US.htm), most of the human population worldwide still rely on subsistence farming and harvest of wild plants to sustain life. With the human population optimistically projected to stabilize at between nine and ten billion by the end of the century, food production will need to double at a minimum, and pressure upon wild plants that are already utilized for food, fuel, housing and medicine will correspondingly increase. It is therefore imperative that the conservation status of all wild plants that contribute directly to human livelihoods be assessed and monitored. National and regional assessments of wild-harvested plants that are deemed threatened because of overexploitation should guide national and international (CITES) legislation and lead to direct involvement of local communities in formulating management plans for their sustainable use. Sites with populations of wild-harvested plants that could be managed sustainably constitute Important Plant Areas for dual protection and use [27]. In addition to wild-harvested plants, non-harvested crop wild relatives should also be given the highest priority for conservation assessment and monitoring insofar as they relate directly to food security. They represent a priceless library of genetic traits potentially conferring disease and pest resistance, drought and salt tolerance, and improved nutritional benefits, which, in the face of environmental change become increasingly important for both traditional breeding and targeted gene insertion. It is essential that crop wild relatives be conserved in situ throughout their range to preserve their maximum genetic variability and, therefore, their response potential to climate change [28,29]. Encompassing phylogenetic diversity: basal, long branches and restricted range higher taxa In terms of evolutionary history, it is misleading to equate all plants with amphibians, birds or mammals in conservation priority-setting exercises. A more apt comparison would juxtapose plants with all vertebrates, but even that would fall short in according appropriate weight to the phylogenetic diversity of green plants. The decision by the Sampled Red List Index (SRLI) to recognize bryophytes, 640
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ferns and fern allies, gymnosperms, monocots and dicots as equivalent sampling units addresses, to some extent, the need to achieve representativeness of photosynthetic organisms in an overall biodiversity indicator but still fails to ensure that the phylogenetic diversity within monocots and dicots is adequately encompassed. At the risk of losing entire evolutionary lineages of flowering plants, it is essential that phylogenetic considerations guide priorities for conducting IUCN Red List assessments and, ultimately, inform conservation decisions on the ground [30,31]. At present, it is difficult to evaluate the extent to which the Red List currently encompasses the phylogenetic diversity of flowering plants insofar as higher taxonomic ranks follow an outdated classification system; adoption of an upto-date classification scheme based on the Angiosperm Phylogeny Group system is needed. An analysis of flowering plants on the current IUCN Red List in relation to the families and orders circumscribed by Stevens on the Angiosperm Phylogeny Website (http://www.mobot.org/ MOBOT/research/APweb) reveals that 8 of 56 orders and 167 (38%) of 445 families have not yet had any species assessed and incorporated in the IUCN Red List. Although circumscription of families and orders is ultimately arbitrary, those higher taxon ranks nevertheless reflect a measure of phylogenetic diversity and, thus, constitute targets to achieve full representation of distinct evolutionary lineages. As an example, the paraphyletic dicots to be sampled in the SRLI will fail to give adequate attention to the basal angiosperms: the ANITA grade (Amborellaceae, Nymphaeales, Illiciaceae, Trimeniaceae and Austrobaileyaceae), Chloranthales and magnoliids. Currently, only four (all Illicium spp.) of 175 species of the ANITA grade have been assessed. Similarly, only 4 of 75 species of Chloranthales have been assessed, whereas 985 (9.8%) of 9978 species of magnoliids (i.e. more than three times more than flowering plants as a whole) have been assessed, albeit with no assessments in six of the families (Atherospermataceae, Calycanthaceae, Eupomatiaceae, Himantandraceae, Hydnoraceae and Saururaceae). Just as these groups represent the basal-most, oldest lineages of flowering plants, many restricted-range families also constitute long, basal branches within the flowering plant tree. An analysis of higher taxon endemism in relation to the WWF Ecoregions revealed that 61 families are restricted to five or fewer ecoregions, with 16 families endemic (or nearly so) to a single ecoregion [32]. Although these 61 families account for only 320 species, they nevertheless represent unique evolutionary lineages on Gondwanan islands and southern hemisphere continents, and in Mediterranean ecosystems and arid deserts. Such higher taxon endemics, including restricted-range genera, have irreplaceable information content and are, therefore, arguably of greater conservation worth [33]; their restricted occurrence and threatened status should thus drive area selection planning processes. Global comprehensive taxonomic assessments Recent global assessments (or reassessments) of amphibians and mammals have received significant international attention [34,35]. Comprehensively assessing an entire clade enables definitive statements on the conservation
Review status of biodiversity to be made and supports numerous analyses on the types and geographical patterns of threat to biodiversity [36]. The Alliance for Zero Extinction (http:// www.zeroextinction.org/), which seeks to pinpoint the epicenters of imminent extinction by identifying those sites harboring the only known occurrence of either Critically Endangered or Endangered species, restricted their initial analysis to comprehensively assessed groups and, therefore, included only the conifers among plants [37]. Assessments of all cycads species have recently been updated, and the SRLI will include assessments of all 1400 gymnosperm species [5,38]. A new Global Cactus Assessment has been launched to assess the 1500 species of cacti, and global assessments of both bamboos and palms have been proposed. Although all of these groups have various merits for comprehensive assessment, including the direct contribution to human livelihoods of many species, they fail to achieve two essential elements of a global assessment: global distribution and representativeness. With the exception of a few African and Malagasy species, cacti are restricted to mostly arid regions of the New World. Conversely, palms are almost entirely restricted to the humid tropics and are particularly depauperate in African tropical forests; bamboos are similarly mostly tropical and subtropical, with highly localized distributions. Moreover, all of these groups exhibit relative homogeneity in habit and/or life form and habitat preference and, thus, do not reflect the tremendous diversity of plants in general. By contrast, and based on all criteria, the Fabaceae are the ideal family to assess comprehensively. The 19 300 species of legumes range from annual desert herbs to rainforest canopy trees and occupy most terrestrial biomes and habitats. A recent analysis exploring global patterns of plant diversity scored 14 724 genera for presence or absence in 52 geographical units and showed that legumes are the single best predictor of generic diversity worldwide [39]. They are also arguably the most documented large family, both in terms of their specimen base and the assimilation of information into databases. For example, the Royal Botanic Gardens, Kew, UK (http://www.kew.org/) have >600 000 specimens of legumes representing all genera, whereas the Missouri Botanical Garden TROPICOS database, Saint Louis, MO, USA (http://www.tropicos.org/) currently has 143 390 specimen records representing 8539 species from the New World alone. The ILDIS (International Legume Database and Information Service; http://www.ildis.org/) database is one of the oldest (>20 years) and most comprehensive biodiversity databases. In addition to the 19 000 accepted legume species included in ILDIS (for each of which all known countries of occurrence are listed), 5118 infraspecific taxa, 28 510 synonyms, 14 087 vernacular names and 5162 uses are recorded, all documented by 57 445 bibliographic references. With its up-to-date taxonomic framework and associated data, ILDIS represents an unparalleled resource upon which to undertake conservation assessments. In addition, legumes have a crucial role in both human livelihoods and ecosystem functioning. They are cultivated on 15% of arable land and account for 27% of total primary crop production. Legumes provide one-third of our dietary nitrogen requirement and, in some developing countries
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where people lack access to animal protein and nitrogen fertilizer, they can provide up to two-thirds of nutritional requirements. In the USA alone, the annual soybean crop is worth US$21 billion, and the alfalfa crop US$7 billion ((http://www.ers.usda.gov/StateFacts/US.htm). More than a dozen other species of legumes are major agricultural grain and forage crops worldwide, and dozens more are minor regional crops. During the late 1970s, a panel convened by the National Academy of Sciences identified >600 species of tropical legumes of promising benefit to society and detailed the status and research needs of nearly 200 of them in Tropical Legumes: Resources for the Future [40], a report that is all the more relevant today. Possibly half of all legume species can be regarded as crop wild relatives and, thus, should be considered as priorities for conservation in their native habitats. Owing to the symbiotic relationship with the Rhizobium bacterium inhabiting nodules on the roots of most of the species in the family, legumes are directly involved in fixing atmospheric nitrogen into the forms essential for plant growth and, thus, ultimately for human consumption. Annually, 40–60 million metric tons of nitrogen are fixed by legume crops worldwide, with an additional 3–5 million metric tons by native legume species. This ability to fix nitrogen can have a substantially increased role in crop rotations, with a potential reduction by 40% of costly and unsustainable petroleum-based nitrogen fertilizer, the equivalent of 800 million metric tons of carbon dioxide sequestration. A Global Legume Assessment would galvanize plant conservation efforts worldwide, providing the missing dimension in global biodiversity conservation planning and serving as a true barometer of the global health of plants. In addition to the 777 species on the current Red List, recent assessment projects in the Caucasus, East Africa, Madagascar and South Africa have resulted in >3000 new assessments of legumes, such that 20% of all legumes have already been assessed. Although a case can be made for the SRLI as representative of plants overall [5], it is questionable whether the 7400 randomly chosen bryophytes, ferns, gymnosperms and flowering plants (1500 species from among 60 100 monocots, plus 1500 species from 292 000 dicots) will adequately represent all habits and/or life forms, biomes and/or habitat types, and geographic regions as well as all legume species would. Concluding remarks: herbaria must get involved Recent assessment projects provide important lessons learned and demonstrate that plant assessments can be achieved in a timely manner with sufficient training and human resources. The success of each project depends upon the formation of a network of local botanists with expertise on both the species themselves and threats to their habitats. These networks serve as either IUCN/SSC Specialist Groups and/or Red List Authorities capable of validating the assessments, formulating regional plant conservation strategies and, ultimately, making recommendations to both governmental and non-governmental organizations to mitigate the loss of plant diversity. National and regional experts take ownership of the assessment process and deliver highly visible results in the form of Red Books, which are illustrated with images 641
Review and maps that serve to personalize biodiversity [22,41–43]. National herbaria provide most of these local botanists to regional assessment networks, creating the necessary bridge between taxonomic collections and conservation, particularly for a group as speciose as plants, in which many species are ‘known’ only in the herbarium. As repositories of the primary occurrence data (i.e. specimens) that document plant diversity and its distribution, the world’s 3000 herbaria have a moral responsibility to participate actively in Red Listing [44,45]. The task of assessing the conservation status of the remaining 300 000 plant species not yet evaluated is eminently doable: each herbarium would be responsible for the assessments of only 100 species on average. Even if only 300 herbaria participated in Red Listing (including all existing national herbaria of the 192 CBD signatory countries, additional regional herbaria in many countries and US herbaria with international research programs), each would still only need to evaluate 1000 species. Recent assessment projects in Madagascar and South Africa suggest that plants can be Red Listed for as little as US$30 per species. The key to future progress in plant Red Listing is to continue assembling the modest funding necessary to support the human networks that lie at the heart of Red List assessments. Acknowledgments I thank Julie Griffin and Craig Hilton-Taylor at IUCN for information, my colleagues on the Biodiversity Assessment and Plant Conservation Sub-Committees of the IUCN/Species Survival Commission from whom I have learned the nuances of Red Listing, and all of my colleagues on the Caucasus, Eastern Arc/Coastal Forests and Madagascar plant assessment projects, funds for which were provided by the Critical Ecosystem Partnership Fund and the Marisla Foundation.
References 1 Hoffman, M. et al. (2008) Conservation planning and the IUCN Red List. Endanger. Species Res. 6, 113–125 2 Rodrigues, A.S.L. et al. (2006) The value of the IUCN Red List for conservation. Trends Ecol. Evol. 21, 71–76 3 Bramwell, D. (2003) On the size of the world’s threatened flora. Plant Talk 32, 4 4 Pitman, N. and Jørgensen, P.M. (2002) Estimating the size of the world’s threatened flora. Science 298, 989 5 Brummit, N. et al. (2008) Applications of the IUCN Red List: towards a global barometer for plant diversity. Endanger. Species Res. 6, 127–135 6 Newton, A.C. and Oldfield, S. (2008) Red Listing the world’s tree species: a review of recent progress. Endanger. Species Res. 6, 137–147 7 UNEP (2008) Plant Conservation Report. A Review of Progress in Implementing the Global Strategy for Plant Conservation (GSPC), UNEP/CBD/COP/9/INF/25 8 IUCN (2001) IUCN Red List Categories and Criteria: version 3.1, IUCN 9 Mace, G.M. et al. (2008) Quantification of extinction risk: IUCN’s system for classifying threatened species. Conserv. Biol. 22, 1424–1442 10 Bomhard, B. et al. (2005) Potential impacts of future land use and climate change on the Red List status of the Proteaceae in the Cape Floristic Region. Global Change Biol. 11, 1452–1468 11 Paton, A.J. et al. (2008) A working list of all known plant species – progress and prospects towards Target 1 of the Global Strategy for Plant Conservation. Taxon 57, 1–10 12 Oldfield, S. et al. (1998) The World List of Threatened Trees, World Conservation Press 13 Walter, K.S. and Gillet, H.J., eds (1998) 1997 IUCN Red List of Threatened Plants, World Conservation Monitoring Center 14 Briggs, J.D. and Leigh, J.H. (1996) Rare or Threatened Australian Plants, (2nd edn), CSRIO 15 de Lange, P.J. et al. (2009) Threatened and uncommon plants of New Zealand (2008 revision). N. Z. J. Bot. 47, 61–96
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Trends in Plant Science Vol.14 No.11 16 Cicuzza, D. et al. (2007) The Red List of Magnoliaceae, Fauna and Flora International 17 Oldfield, S. and Eastwood, A. (2007) The Red List of Oaks, Fauna and Flora International 18 Vivero, J.L. et al. (2005) The Red List of Endemic Trees & Shrubs of Ethiopia and Eritrea, Fauna and Flora International 19 Vivero, J.L. et al. (2006) The Red List of Trees of Guatemala, Fauna and Flora International 20 Eastwood, A. et al. (2009) The Red List of Trees of Central Asia, Fauna & Flora International 21 Leo´n, B. et al., eds (2006) El Libro Rojo de las Plantas Ende´micas del Peru´, Revista Peruana de Biologı´a 22 Hechenleitner, P. et al. (2005) Plantas Amenazadas del Centro-Sur de Chile. Distribucio´n, Conservacio´n y Propagacio´n, Universidad Austral de Chile y Real Jardı´n Bota´nico de Edimburgo ´ . et al. (2007) Atlas y Libro Rojo de la Flora Vascular 23 Ban˜ares, A Amenazada de Espan˜a: Taxones Prioritarios, (2nd edn), Direccio´n General de Conservacio´n de la Naturaleza 24 Valencia, R. et al., eds (2000) Libro Rojo de las Plantas Ende´micas del Ecuador 2000, PUCE editions 25 Callmander, M.W. et al. (2007) Identification of priority areas for plant conservation in Madagascar using Red List criteria: rare and threatened Pandanaceae indicate sites in need of protection. Oryx 41, 168–176 26 Rodrı´guez, J.P. (2008) National Red Lists: the largest global market for IUCN Red List Categories and Criteria. Endanger. Species Res. 6, 193–198 27 Hamilton, A.C. and Radford, E.A. (2007) Identification and Conservation of Important Plant Areas for Medicinal Plants in the Himalaya, Plantlife International and Ethnobotanical Society of Nepal 28 Heywood, V. et al. (2007) Conservation and sustainable use of crop wild relatives. Agric. Ecosyst. Environ. 121, 245–255 29 Jarvis, A. et al. (2008) The effect of climate change on crop wild relatives. Agric. Ecosyst. Environ. 126, 13–23 30 Faith, D.P. et al. (2004) Integrating phylogenetic diversity, complementarity and endemism for conservation assessment. Conserv. Biol. 18, 255–261 31 Mooers, A.O. et al. (2005) Evolutionary heritage as a metric for conservation. In Phylogeny and Conservation (Purvis, A. et al., eds), pp. 120–138, Cambridge University Press 32 Massad, T. et al. The distribution and conservation status of restricted range vascular plant families. In Conservation Without Borders, Society for Conservation Biology Annual Meeting, 24–28 June 2006, San Jose, CA, USA, Abstract Book 33 Crozier, R.H. (1997) Preserving the information content of species: genetic diversity, phylogeny, and conservation worth. Annu. Rev. Ecol. Syst. 28, 243–268 34 Schipper, J. et al. (2008) The status of the world’s land and marine mammals: diversity, threat and knowledge. Science 322, 225–230 35 Stuart, S.N. et al. (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306, 1783–1786 36 Baillie, J.E.M. et al., eds (2004) A Global Species Assessment, IUCN 37 Ricketts, T.H. et al. (2005) Pinpointing and preventing imminent extinctions. Proc. Natl. Acad. Sci. U. S. A. 102, 18497–21850 38 Baillie, J.E.M. et al. (2008) Toward monitoring global biodiversity. Conserv. Lett. 1, 18–26 39 Nic Lughadha, E.N. et al. (2005) Measuring the fate of plant diversity: towards a foundation for future monitoring and opportunities for urgent action. Philos. Trans. R. Soc. B 360, 359–372 40 National Research Council (1979) Tropical Legumes: Resources for the Future, National Academy of Sciences 41 Collar, N. (1996) The reasons for red data books. Oryx 30, 121–130 42 Golding, J., ed. (2002) Southern African Plant Red Lists, Southern African Botanical Diversity Network Report No. 14. SABONET 43 de Montmollin, B. and Strahm, W. (2005) The Top 50 Mediterranean Island Plants. Wild plants at the Brink of Extinction, and What is Needed to Save Them, IUCN/SSC Mediterranean Islands Plant Specialist Group 44 Callmander, M.W. et al. (2005) IUCN Red List assessment and the Global Strategy for Plant Conservation: taxonomists must act now. Taxon 54, 1047–1050 45 Schatz, G.E. (2002) Taxonomy and herbaria in service of plant conservation: lessons from Madagascar’s endemic families. Ann. Miss. Bot. Gard. 89, 145–152
Special Issue: Plant science research in botanic gardens
Plants on the IUCN Red List: setting priorities to inform conservation George E. Schatz Missouri Botanical Garden, PO Box 299, Saint Louis, MO 63166-0299, USA
The continuing decline of plant diversity will have a greater impact on human society than any other type of biodiversity loss. It is imperative, therefore, that efforts are increased to assess the conservation status of plants for the IUCN Red List of Threatened Species, the de facto baseline reference for many conservation decisions. As discussed here, a review of plants on the current Red List suggests that priorities for future Red Listing should serve multiple purposes: to inform national conservation policy, to contribute to global conservation analyses, to encompass the phylogenetic diversity of plants and to address the dependence of human societies on plants. Future progress in plant Red Listing requires greater participation by the world’s herbaria and increased support for expert networks. The unknown status of plant conservation Efforts to halt the continuing decline of biodiversity worldwide are currently hampered by inadequate knowledge of the threatened status of the organisms that constitute the fundamental basis for all life on Earth: green plants. As the IUCN Red List of Threatened Species (http:// www.iucnredlist.org/) has increasingly been adopted as the gold standard for information on the conservation status of species [1,2], plants have had a disproportionately minor role in the conservation-planning process. Whereas most species of vertebrates have been assessed globally for their conservation status and, thus, can contribute to prioritization analyses, only 3.2% of plant species currently appear on the IUCN Red List and only two groups of plants (conifers and cycads) have been (nearly) comprehensively assessed. Nevertheless, various estimates of the potential number of plant species threatened with extinction have approached 50% [3,4], a staggering figure given the fundamental role of plants as providers of food, shelter and medicine for human use and/or essential ecosystem services for all biodiversity. Several recent papers and reports have summarized progress on plant Red Listing in the context of the Global Strategy for Plant Conservation (GSPC) [5–7] and will be only briefly recapitulated here. It is clear that the (overly) ambitious GSPC Target 2 goal of ‘a preliminary assessment of the conservation status of all known plant species at national, regional, and international levels’ will not be met by 2010. However, a significant number of plant species have been evaluated over the past decade at both Corresponding author: Schatz, G.E. ([email protected])
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global and national levels, with both the IUCN Red List Categories and Criteria [8,9] (Figure 1) and other systems, and therefore contribute to our overall understanding of their conservation status and the magnitude of threats facing plants worldwide. With 2010 upon us, and a mandate from the United Nations Convention on Biological Diversity (CBD) to reformulate and reinvigorate the GSPC to reflect emerging threats, such as climate change [10], I suggest that priorities for plant Red Listing should be set that will directly inform the conservation of the planet’s green lifeline and ensure that maximum plant diversity is preserved for future generations. Plants on, and not on, the IUCN Red List The current online version of the IUCN Red List of Threatened Species (http://www.iucnredlist.org/) includes 11 995 species of bryophytes, ferns, lycopods, gymnosperms and angiosperms out of an estimated total number of species across those groups of 379 881 [11], or <3.2% (Table 1). In addition, 1016 infraspecies of gymnosperms and angiosperms are listed, as are two green algae and 58 red algae. Unfortunately, not all assessments are equivalent. Among the 13 011 listed taxa, 8505 (65%) were assessed before 2001 under the older version 2.3 of the IUCN Red List Categories and Criteria, whereas 4506 (35%) have been assessed since 2001 using the current version 3.1 of the Categories and Criteria. Therefore, with a recommended 10-year shelf life, assessments of nearly two-thirds of the currently listed taxa have either already expired or are set to expire by the end of 2010. Among those taxa are most of the 8120 tree species currently listed that were originally assessed for The World List of Threatened Trees [12]. Previously, the decision to standardize assessments to at least version 2.3 of Categories and Criteria meant that many of the 34 000 taxa listed in the 1997 IUCN Red List of Threatened Plants [13] were not retained. Numerous other plants that have been globally (or nationally) assessed for their conservation status over the past decade do not, however, appear on the IUCN Red List for a variety of reasons. The low number of only 346 North American taxa currently on the List reflects the use by NatureServe (http://www.natureserve.org/explorer) of a different system to assess the nearly 32 000 taxa native to Canada and the USA. Similarly, the 21 000 vascular plant species of Australia were previously monitored under Rare or Threatened Australian Plants [14], which has now been superseded by the Environment
1360-1385/$ – see front matter ß 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.tplants.2009.08.012 Available online 19 September 2009
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Figure 1. Structure of the IUCN Red List categories. Reproduced with permission from IUCN.
Protection and Biodiversity Conservation Act of 1999 (http://www.environment.gov.au/cgi-bin/sprat/public/ publicthreatenedlist.pl?wanted=flora), and New Zealand has applied its own system to its 2357 indigenous taxa [15]. The Global Tree Campaign has conducted 10 assessments of 2500 species of trees [6], including Magnoliaceae [16], oaks [17] and regional subsets of Ethiopian [18], Guatemalan [19] and Central Asian [20] tree species, very few of which have been incorporated into the Red List. Spanish language assessments of all 5500 Peruvian endemics [21], 46 species from Central and Southern Chile [22] and 8000 Spanish taxa [23] have also not been added to the Red List. The under-resourced and over-taxed Red List Program office simply has not had the capacity to keep pace with the number of submitted assessments, an untenable situation that will only be exacerbated by the increasing volume of plant assessments coming from South Africa (13 000 endemics), Madagascar (2850 endemics), the Critical Ecosystem Partnership Fund (CEPF) projects in the Caucasus (1000 endemics) and the Eastern Arc Mountains/Coastal Forests of East Africa (700 endemics), the Sampled Red List Index (7400 species) [5], seagrasses (60 species) and mangroves (50 species) contributed by the Global Marine Species Assessment, and the newly launched Global Cactus Assessment (1500 species), as well as many other smaller subsets. Given that >50% of countries have completed some form of plant Red List assessment at a national level [7], it is probable that the conservation status of at least 100 000 flowering plant species (28%) has been evaluated at some point during the past 20 years. Priorities for plant Red Listing Selection of plant species for Red Listing has been, and will probably continue to be, an ad hoc process depending upon Table 1. Numbers of plant species on the IUCN Red List of Threatened Species Taxon Bryophytes Ferns/Lycopods Gymnosperms Angiosperms Total a
Data from Ref. [11].
Estimated total spp. a 13 370 12 838 1391 352 282 379 881
Spp. on 2008 Red List 95 211 910 10 779 11 995
% 0.7 1.6 65 3 3.2
individual initiative and enthusiasm, and subject to the vagaries of funding. Nevertheless, renewal of the GSPC would benefit from a set of clearly articulated, strategic priorities for plant Red Listing that would serve multiple purposes: (i) to inform national conservation policy; (ii) to contribute to global conservation analyses and serve as a robust surrogate for all plants; (iii) to encompass the full phylogenetic diversity of plant life; and (iv) to address the fundamental dependence of human societies on plants. National and regional endemics Under the CBD, signatory countries are obligated to ensure the protection of species that occur only within their borders. As implementation of CBD decisions, such as the GSPC, must involve priority-setting at the country level, Red Listing of all national endemics, which by definition are then global assessments, should then form the basis for national conservation policy. Recent assessment projects that have focused on national endemics have revealed that >50% of the 4000 endemic Ecuadoran plant species are known from only one or two populations [24], and that 87% of the 5500 endemic Peruvian plant species are not recorded from within protected areas [21]. Baseline assessment of all national endemics leads directly to the identification of Important Plant Areas (GSPC Target 5) and highlights gaps in the protected areas network for in situ conservation of threatened species (GSPC Target 7). For example, in Madagascar, rare and threatened endemic species of Pandanaceae exposed priority sites for new protection [25]. However, despite the fact that 91% of the 34 000 species listed in the 1997 IUCN Red List of Threatened Plants were single-country endemics [13], much of biodiversity straddles political boundaries, which are often associated with geographical features (river basins or mountain ranges) that also constitute evolutionary hotspots of endemism. One wonders how many more species are endemic to both Ecuador and Peru. In the recent CEPF Caucasus plant assessment project, in addition to assessing all national endemics in Armenia, Azerbaijan, Georgia and the Caucasian areas of Russia and Turkey, a regional approach also targeted taxa endemic to two or three countries for assessment. Similarly, the CEPF Eastern Arc/Coastal Forests project (http://cepf.tfcg.org/) often encountered taxa distributed from the Taita Hills in Kenya to the southern limit of the Eastern Arc Mountains in 639
Review Tanzania, as well coastal forest endemics distributed from Somalia through Kenya and Tanzania to Mozambique. In calling for plant conservation assessments at national and regional levels in addition to international, the GSPC recognized the desire and need for countries to protect and monitor non-endemic species that might nevertheless be rare and of conservation concern within their borders. As governments allocate funds to meet their commitments under the CBD by carrying out assessments of both national endemics and national-level assessments of non-endemics, it is essential that some type of clearinghouse mechanism be developed to track implementation of Target 2 of the GSPC at national and regional levels [26]. Wild plants that contribute directly to human livelihoods and crop wild relatives In contrast to the developed world, where only a small percentage of the human population is engaged in agriculture (in the USA, there are 2.2 million farmers out of a total population of 304 million, or <1%; http://www. ers.usda.gov/StateFacts/US.htm), most of the human population worldwide still rely on subsistence farming and harvest of wild plants to sustain life. With the human population optimistically projected to stabilize at between nine and ten billion by the end of the century, food production will need to double at a minimum, and pressure upon wild plants that are already utilized for food, fuel, housing and medicine will correspondingly increase. It is therefore imperative that the conservation status of all wild plants that contribute directly to human livelihoods be assessed and monitored. National and regional assessments of wild-harvested plants that are deemed threatened because of overexploitation should guide national and international (CITES) legislation and lead to direct involvement of local communities in formulating management plans for their sustainable use. Sites with populations of wild-harvested plants that could be managed sustainably constitute Important Plant Areas for dual protection and use [27]. In addition to wild-harvested plants, non-harvested crop wild relatives should also be given the highest priority for conservation assessment and monitoring insofar as they relate directly to food security. They represent a priceless library of genetic traits potentially conferring disease and pest resistance, drought and salt tolerance, and improved nutritional benefits, which, in the face of environmental change become increasingly important for both traditional breeding and targeted gene insertion. It is essential that crop wild relatives be conserved in situ throughout their range to preserve their maximum genetic variability and, therefore, their response potential to climate change [28,29]. Encompassing phylogenetic diversity: basal, long branches and restricted range higher taxa In terms of evolutionary history, it is misleading to equate all plants with amphibians, birds or mammals in conservation priority-setting exercises. A more apt comparison would juxtapose plants with all vertebrates, but even that would fall short in according appropriate weight to the phylogenetic diversity of green plants. The decision by the Sampled Red List Index (SRLI) to recognize bryophytes, 640
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ferns and fern allies, gymnosperms, monocots and dicots as equivalent sampling units addresses, to some extent, the need to achieve representativeness of photosynthetic organisms in an overall biodiversity indicator but still fails to ensure that the phylogenetic diversity within monocots and dicots is adequately encompassed. At the risk of losing entire evolutionary lineages of flowering plants, it is essential that phylogenetic considerations guide priorities for conducting IUCN Red List assessments and, ultimately, inform conservation decisions on the ground [30,31]. At present, it is difficult to evaluate the extent to which the Red List currently encompasses the phylogenetic diversity of flowering plants insofar as higher taxonomic ranks follow an outdated classification system; adoption of an upto-date classification scheme based on the Angiosperm Phylogeny Group system is needed. An analysis of flowering plants on the current IUCN Red List in relation to the families and orders circumscribed by Stevens on the Angiosperm Phylogeny Website (http://www.mobot.org/ MOBOT/research/APweb) reveals that 8 of 56 orders and 167 (38%) of 445 families have not yet had any species assessed and incorporated in the IUCN Red List. Although circumscription of families and orders is ultimately arbitrary, those higher taxon ranks nevertheless reflect a measure of phylogenetic diversity and, thus, constitute targets to achieve full representation of distinct evolutionary lineages. As an example, the paraphyletic dicots to be sampled in the SRLI will fail to give adequate attention to the basal angiosperms: the ANITA grade (Amborellaceae, Nymphaeales, Illiciaceae, Trimeniaceae and Austrobaileyaceae), Chloranthales and magnoliids. Currently, only four (all Illicium spp.) of 175 species of the ANITA grade have been assessed. Similarly, only 4 of 75 species of Chloranthales have been assessed, whereas 985 (9.8%) of 9978 species of magnoliids (i.e. more than three times more than flowering plants as a whole) have been assessed, albeit with no assessments in six of the families (Atherospermataceae, Calycanthaceae, Eupomatiaceae, Himantandraceae, Hydnoraceae and Saururaceae). Just as these groups represent the basal-most, oldest lineages of flowering plants, many restricted-range families also constitute long, basal branches within the flowering plant tree. An analysis of higher taxon endemism in relation to the WWF Ecoregions revealed that 61 families are restricted to five or fewer ecoregions, with 16 families endemic (or nearly so) to a single ecoregion [32]. Although these 61 families account for only 320 species, they nevertheless represent unique evolutionary lineages on Gondwanan islands and southern hemisphere continents, and in Mediterranean ecosystems and arid deserts. Such higher taxon endemics, including restricted-range genera, have irreplaceable information content and are, therefore, arguably of greater conservation worth [33]; their restricted occurrence and threatened status should thus drive area selection planning processes. Global comprehensive taxonomic assessments Recent global assessments (or reassessments) of amphibians and mammals have received significant international attention [34,35]. Comprehensively assessing an entire clade enables definitive statements on the conservation
Review status of biodiversity to be made and supports numerous analyses on the types and geographical patterns of threat to biodiversity [36]. The Alliance for Zero Extinction (http:// www.zeroextinction.org/), which seeks to pinpoint the epicenters of imminent extinction by identifying those sites harboring the only known occurrence of either Critically Endangered or Endangered species, restricted their initial analysis to comprehensively assessed groups and, therefore, included only the conifers among plants [37]. Assessments of all cycads species have recently been updated, and the SRLI will include assessments of all 1400 gymnosperm species [5,38]. A new Global Cactus Assessment has been launched to assess the 1500 species of cacti, and global assessments of both bamboos and palms have been proposed. Although all of these groups have various merits for comprehensive assessment, including the direct contribution to human livelihoods of many species, they fail to achieve two essential elements of a global assessment: global distribution and representativeness. With the exception of a few African and Malagasy species, cacti are restricted to mostly arid regions of the New World. Conversely, palms are almost entirely restricted to the humid tropics and are particularly depauperate in African tropical forests; bamboos are similarly mostly tropical and subtropical, with highly localized distributions. Moreover, all of these groups exhibit relative homogeneity in habit and/or life form and habitat preference and, thus, do not reflect the tremendous diversity of plants in general. By contrast, and based on all criteria, the Fabaceae are the ideal family to assess comprehensively. The 19 300 species of legumes range from annual desert herbs to rainforest canopy trees and occupy most terrestrial biomes and habitats. A recent analysis exploring global patterns of plant diversity scored 14 724 genera for presence or absence in 52 geographical units and showed that legumes are the single best predictor of generic diversity worldwide [39]. They are also arguably the most documented large family, both in terms of their specimen base and the assimilation of information into databases. For example, the Royal Botanic Gardens, Kew, UK (http://www.kew.org/) have >600 000 specimens of legumes representing all genera, whereas the Missouri Botanical Garden TROPICOS database, Saint Louis, MO, USA (http://www.tropicos.org/) currently has 143 390 specimen records representing 8539 species from the New World alone. The ILDIS (International Legume Database and Information Service; http://www.ildis.org/) database is one of the oldest (>20 years) and most comprehensive biodiversity databases. In addition to the 19 000 accepted legume species included in ILDIS (for each of which all known countries of occurrence are listed), 5118 infraspecific taxa, 28 510 synonyms, 14 087 vernacular names and 5162 uses are recorded, all documented by 57 445 bibliographic references. With its up-to-date taxonomic framework and associated data, ILDIS represents an unparalleled resource upon which to undertake conservation assessments. In addition, legumes have a crucial role in both human livelihoods and ecosystem functioning. They are cultivated on 15% of arable land and account for 27% of total primary crop production. Legumes provide one-third of our dietary nitrogen requirement and, in some developing countries
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where people lack access to animal protein and nitrogen fertilizer, they can provide up to two-thirds of nutritional requirements. In the USA alone, the annual soybean crop is worth US$21 billion, and the alfalfa crop US$7 billion ((http://www.ers.usda.gov/StateFacts/US.htm). More than a dozen other species of legumes are major agricultural grain and forage crops worldwide, and dozens more are minor regional crops. During the late 1970s, a panel convened by the National Academy of Sciences identified >600 species of tropical legumes of promising benefit to society and detailed the status and research needs of nearly 200 of them in Tropical Legumes: Resources for the Future [40], a report that is all the more relevant today. Possibly half of all legume species can be regarded as crop wild relatives and, thus, should be considered as priorities for conservation in their native habitats. Owing to the symbiotic relationship with the Rhizobium bacterium inhabiting nodules on the roots of most of the species in the family, legumes are directly involved in fixing atmospheric nitrogen into the forms essential for plant growth and, thus, ultimately for human consumption. Annually, 40–60 million metric tons of nitrogen are fixed by legume crops worldwide, with an additional 3–5 million metric tons by native legume species. This ability to fix nitrogen can have a substantially increased role in crop rotations, with a potential reduction by 40% of costly and unsustainable petroleum-based nitrogen fertilizer, the equivalent of 800 million metric tons of carbon dioxide sequestration. A Global Legume Assessment would galvanize plant conservation efforts worldwide, providing the missing dimension in global biodiversity conservation planning and serving as a true barometer of the global health of plants. In addition to the 777 species on the current Red List, recent assessment projects in the Caucasus, East Africa, Madagascar and South Africa have resulted in >3000 new assessments of legumes, such that 20% of all legumes have already been assessed. Although a case can be made for the SRLI as representative of plants overall [5], it is questionable whether the 7400 randomly chosen bryophytes, ferns, gymnosperms and flowering plants (1500 species from among 60 100 monocots, plus 1500 species from 292 000 dicots) will adequately represent all habits and/or life forms, biomes and/or habitat types, and geographic regions as well as all legume species would. Concluding remarks: herbaria must get involved Recent assessment projects provide important lessons learned and demonstrate that plant assessments can be achieved in a timely manner with sufficient training and human resources. The success of each project depends upon the formation of a network of local botanists with expertise on both the species themselves and threats to their habitats. These networks serve as either IUCN/SSC Specialist Groups and/or Red List Authorities capable of validating the assessments, formulating regional plant conservation strategies and, ultimately, making recommendations to both governmental and non-governmental organizations to mitigate the loss of plant diversity. National and regional experts take ownership of the assessment process and deliver highly visible results in the form of Red Books, which are illustrated with images 641
Review and maps that serve to personalize biodiversity [22,41–43]. National herbaria provide most of these local botanists to regional assessment networks, creating the necessary bridge between taxonomic collections and conservation, particularly for a group as speciose as plants, in which many species are ‘known’ only in the herbarium. As repositories of the primary occurrence data (i.e. specimens) that document plant diversity and its distribution, the world’s 3000 herbaria have a moral responsibility to participate actively in Red Listing [44,45]. The task of assessing the conservation status of the remaining 300 000 plant species not yet evaluated is eminently doable: each herbarium would be responsible for the assessments of only 100 species on average. Even if only 300 herbaria participated in Red Listing (including all existing national herbaria of the 192 CBD signatory countries, additional regional herbaria in many countries and US herbaria with international research programs), each would still only need to evaluate 1000 species. Recent assessment projects in Madagascar and South Africa suggest that plants can be Red Listed for as little as US$30 per species. The key to future progress in plant Red Listing is to continue assembling the modest funding necessary to support the human networks that lie at the heart of Red List assessments. Acknowledgments I thank Julie Griffin and Craig Hilton-Taylor at IUCN for information, my colleagues on the Biodiversity Assessment and Plant Conservation Sub-Committees of the IUCN/Species Survival Commission from whom I have learned the nuances of Red Listing, and all of my colleagues on the Caucasus, Eastern Arc/Coastal Forests and Madagascar plant assessment projects, funds for which were provided by the Critical Ecosystem Partnership Fund and the Marisla Foundation.
References 1 Hoffman, M. et al. (2008) Conservation planning and the IUCN Red List. Endanger. Species Res. 6, 113–125 2 Rodrigues, A.S.L. et al. (2006) The value of the IUCN Red List for conservation. Trends Ecol. Evol. 21, 71–76 3 Bramwell, D. (2003) On the size of the world’s threatened flora. Plant Talk 32, 4 4 Pitman, N. and Jørgensen, P.M. (2002) Estimating the size of the world’s threatened flora. Science 298, 989 5 Brummit, N. et al. (2008) Applications of the IUCN Red List: towards a global barometer for plant diversity. Endanger. Species Res. 6, 127–135 6 Newton, A.C. and Oldfield, S. (2008) Red Listing the world’s tree species: a review of recent progress. Endanger. Species Res. 6, 137–147 7 UNEP (2008) Plant Conservation Report. A Review of Progress in Implementing the Global Strategy for Plant Conservation (GSPC), UNEP/CBD/COP/9/INF/25 8 IUCN (2001) IUCN Red List Categories and Criteria: version 3.1, IUCN 9 Mace, G.M. et al. (2008) Quantification of extinction risk: IUCN’s system for classifying threatened species. Conserv. Biol. 22, 1424–1442 10 Bomhard, B. et al. (2005) Potential impacts of future land use and climate change on the Red List status of the Proteaceae in the Cape Floristic Region. Global Change Biol. 11, 1452–1468 11 Paton, A.J. et al. (2008) A working list of all known plant species – progress and prospects towards Target 1 of the Global Strategy for Plant Conservation. Taxon 57, 1–10 12 Oldfield, S. et al. (1998) The World List of Threatened Trees, World Conservation Press 13 Walter, K.S. and Gillet, H.J., eds (1998) 1997 IUCN Red List of Threatened Plants, World Conservation Monitoring Center 14 Briggs, J.D. and Leigh, J.H. (1996) Rare or Threatened Australian Plants, (2nd edn), CSRIO 15 de Lange, P.J. et al. (2009) Threatened and uncommon plants of New Zealand (2008 revision). N. Z. J. Bot. 47, 61–96
642
Trends in Plant Science Vol.14 No.11 16 Cicuzza, D. et al. (2007) The Red List of Magnoliaceae, Fauna and Flora International 17 Oldfield, S. and Eastwood, A. (2007) The Red List of Oaks, Fauna and Flora International 18 Vivero, J.L. et al. (2005) The Red List of Endemic Trees & Shrubs of Ethiopia and Eritrea, Fauna and Flora International 19 Vivero, J.L. et al. (2006) The Red List of Trees of Guatemala, Fauna and Flora International 20 Eastwood, A. et al. (2009) The Red List of Trees of Central Asia, Fauna & Flora International 21 Leo´n, B. et al., eds (2006) El Libro Rojo de las Plantas Ende´micas del Peru´, Revista Peruana de Biologı´a 22 Hechenleitner, P. et al. (2005) Plantas Amenazadas del Centro-Sur de Chile. Distribucio´n, Conservacio´n y Propagacio´n, Universidad Austral de Chile y Real Jardı´n Bota´nico de Edimburgo ´ . et al. (2007) Atlas y Libro Rojo de la Flora Vascular 23 Ban˜ares, A Amenazada de Espan˜a: Taxones Prioritarios, (2nd edn), Direccio´n General de Conservacio´n de la Naturaleza 24 Valencia, R. et al., eds (2000) Libro Rojo de las Plantas Ende´micas del Ecuador 2000, PUCE editions 25 Callmander, M.W. et al. (2007) Identification of priority areas for plant conservation in Madagascar using Red List criteria: rare and threatened Pandanaceae indicate sites in need of protection. Oryx 41, 168–176 26 Rodrı´guez, J.P. (2008) National Red Lists: the largest global market for IUCN Red List Categories and Criteria. Endanger. Species Res. 6, 193–198 27 Hamilton, A.C. and Radford, E.A. (2007) Identification and Conservation of Important Plant Areas for Medicinal Plants in the Himalaya, Plantlife International and Ethnobotanical Society of Nepal 28 Heywood, V. et al. (2007) Conservation and sustainable use of crop wild relatives. Agric. Ecosyst. Environ. 121, 245–255 29 Jarvis, A. et al. (2008) The effect of climate change on crop wild relatives. Agric. Ecosyst. Environ. 126, 13–23 30 Faith, D.P. et al. (2004) Integrating phylogenetic diversity, complementarity and endemism for conservation assessment. Conserv. Biol. 18, 255–261 31 Mooers, A.O. et al. (2005) Evolutionary heritage as a metric for conservation. In Phylogeny and Conservation (Purvis, A. et al., eds), pp. 120–138, Cambridge University Press 32 Massad, T. et al. The distribution and conservation status of restricted range vascular plant families. In Conservation Without Borders, Society for Conservation Biology Annual Meeting, 24–28 June 2006, San Jose, CA, USA, Abstract Book 33 Crozier, R.H. (1997) Preserving the information content of species: genetic diversity, phylogeny, and conservation worth. Annu. Rev. Ecol. Syst. 28, 243–268 34 Schipper, J. et al. (2008) The status of the world’s land and marine mammals: diversity, threat and knowledge. Science 322, 225–230 35 Stuart, S.N. et al. (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306, 1783–1786 36 Baillie, J.E.M. et al., eds (2004) A Global Species Assessment, IUCN 37 Ricketts, T.H. et al. (2005) Pinpointing and preventing imminent extinctions. Proc. Natl. Acad. Sci. U. S. A. 102, 18497–21850 38 Baillie, J.E.M. et al. (2008) Toward monitoring global biodiversity. Conserv. Lett. 1, 18–26 39 Nic Lughadha, E.N. et al. (2005) Measuring the fate of plant diversity: towards a foundation for future monitoring and opportunities for urgent action. Philos. Trans. R. Soc. B 360, 359–372 40 National Research Council (1979) Tropical Legumes: Resources for the Future, National Academy of Sciences 41 Collar, N. (1996) The reasons for red data books. Oryx 30, 121–130 42 Golding, J., ed. (2002) Southern African Plant Red Lists, Southern African Botanical Diversity Network Report No. 14. SABONET 43 de Montmollin, B. and Strahm, W. (2005) The Top 50 Mediterranean Island Plants. Wild plants at the Brink of Extinction, and What is Needed to Save Them, IUCN/SSC Mediterranean Islands Plant Specialist Group 44 Callmander, M.W. et al. (2005) IUCN Red List assessment and the Global Strategy for Plant Conservation: taxonomists must act now. Taxon 54, 1047–1050 45 Schatz, G.E. (2002) Taxonomy and herbaria in service of plant conservation: lessons from Madagascar’s endemic families. Ann. Miss. Bot. Gard. 89, 145–152