Addressing Data Deficiency in Classifying Extinction Risk: a Case Study of a Radiation of Bignoniaceae from Madagascar TATJANA C. GOOD,∗§ MICHELLE L. ZJHRA†, AND CLAIRE KREMEN‡ ∗Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544, U.S.A. †Department of Biology, Georgia Southern University, Statesboro, GA 30460, U.S.A. ‡Department of Environmental Science, Policy, and Management, University of California, Berkeley, CA 94720–3114, U.S.A. Abstract: Of the roughly 12,000 known plant species in Madagascar, only 3% are found in the IUCN ( World Conservation Union) Red List of Threatened Species. We assigned preliminary IUCN categories of threat to the species of a comparatively well-known tribe, Coleeae (Bignoniaceae), which comprises an endemic, species- rich radiation in Madagascar. Because the IUCN Red List Categories and Criteria 3.1 discourage the use of the data-deficient category, we developed a novel method for differentiating between range-limited species and poorly sampled species. We used the Missouri Botanical Garden (MBG) gazetteer to determine where other collection efforts had taken place. We drew buffers around each Coleeae locality and determined how many times the surrounding area had been visited since the last sighting of the specimens by intersecting the buffers with all known botanical localities from the MBG gazetteer. We determined that at least 54% of the Coleeae species are threatened with extinction. Assignments of species to this category were often due to predicted future decline within their current area of occupancy and their lack of inclusion within the protected-area network (only 42% of species are known to occur in protected areas). Three species were presumed extinct, and an additional 12 have not been seen in decades. Among the species threatened with extinction, we “rescued” six of them from the data-deficient category by considering both the sample dates and localities of places where they occurred in relation to additional collections that took place in the immediate area. Due to their recent discovery, 15 species remained in the data-deficient category. If Coleeae is representative of the Malagasy flora, or at least of other endemic-radiated plant groups, then species loss in Madagascar may be even more extreme than is realized. Keywords: biodiversity, endemism, extinction, GAP analysis, IUCN Red List Categories and Criteria, species- distribution mapping Enfrentando Datos Insuficientes en la Clasificaci´on de Riesgo de Extinci´on: un Estudio de Caso de una Radiaci´on de Bignoniaceae de Madagascar Resumen: De las cerca de 12,000 especies conocidas de plantas en Madagascar, solo 3% estan´ en la Lista Roja de especies Amenazadas de la Union´ Mundial de Conservacion´ (IUCN). Asignamos categor´ıas IUCN pre- liminares de amenazas a las especies de una tribu comparativamente bien conocida, Coleeae (Bignoniaceae), que esta´ compuesta de una radiacion´ end´emica y rica en especies en Madagascar. Debido a que las Categor´ıas y Criterios 3.1 de la Lista Roja de IUCN desalientan el uso de la categor´ıa datos insuficientes, desarrollamos un m´etodo novedoso para diferenciar entre especies con rango limitado y especies pobremente muestreadas. Utilizamos el ´ındice topon´ımico del Jard´ın Botanico´ de Missouri ( JBM) para determinar en que otros sitios se han llevado a cabo esfuerzos de recolecta. Trazamos amortiguamientos alrededor de cada localidad de Coleeae §Address for correspondence: Centro Internacional de Ecolog´ıa Tropical—IVIC, Apartado 21827, Caracas 1020-A, Venezuela. email [email protected] Paper submitted January 19, 2005; revised manuscript accepted September 29, 2005. 1099 Conservation Biology Volume 20, No. 4, 1099–1110 C 2006 Society for Conservation Biology DOI: 10.1111/j.1523-1739.2006.00473.x 1100 Data Deficiency and Extinction Risk Good et al. y determinamos cuantas veces hab´ıa sido visitada el area´ desde el ultimo´ registro de los especimenes mediante la interseccion´ de los amortiguamientos con todas las localidades botanicas´ conocidas del ´ındice topon´ımico de JBM. Determinamos que por lo menos 54% de las especies de Coleeae estan´ amenazadas de extincion.´ Las asignaciones de especies a esta categor´ıa se debieron a menudo a la declinacion´ futura pronosticada en su actual area´ de ocupacion´ y su no inclusion´ en la red de areas´ protegidas (se sabe que solo 42% de las especies ocurren en areas´ protegidas). Se considero´ que tres especies estan´ extintas, y 12 mas´ no han sido vistas en d´ecadas. Entre las especies amenazadas de extincion,´ “rescatamos” a 6 de la categor´ıa datos insuficientes al considerar a las fechas y localidades de muestreo en relacion´ con recolectas adicionales que se llevaron a cabo en el area´ inmediata. Debido a su descubrimiento reciente, 15 especies permanecieron en la categor´ıa datos insuficientes. Si Coleeae es representativa de la flora malgache, o por lo menos de otros grupos de plantas radiadas end´emicas, entonces puede que la p´erdida de especies en Madagascar sea aun mas´ extrema de lo que se comprende. Palabras Clave: an´alisis GAP, biodiversidad, categor´ıas y criterios de la Lista Roja de IUCN, endemismo, ex- tinci´on, mapas de distribuci´on de especies Introduction the slow process of getting reassessments done correctly, peer reviewed, and processed for inclusion on the IUCN Conservation biologists require reliable information on Red List. species identities and extents of occurrence to assess Sometimes referred to as an island continent, Mada- the status of species, identify areas of endemism, and gascar combines the evolutionary characteristics of isola- design networks of protected areas (Margules & Pressey tion with the biogeographic opportunities of a continent, 2000; Cabeza & Moilanen 2001). Twenty to fifty percent often resulting in spectacular radiations in many taxa. of the world’s plant species may be threatened with ex- Tribe Coleeae, a species-rich radiation, is a good system tinction (Pitman & Jorgenson 2002; Bramwell 2003), but in which to investigate the patterns and processes of evo- few countries have comprehensive, up-to-date red lists lution, including speciation and extinction (MacArthur & of threatened plants (e.g., Ecuador; Valenzia et al. 2000). Wilson 1967; Sauer 1969; Cox 1990). Efforts to compile these lists are underway in many coun- We asked three questions: (1) According to the IUCN tries, including Madagascar. Red List criteria (IUCN 2004a), what is the risk of extinc- Madagascar is considered one of the world’s hotspots tion for each member of tribe Coleeae? (2) How many of biodiversity, based on its unique and diverse biota and species of Coleeae are protected under the current pro- on the high levels of threat to its forest ecosystems (My- tected area network? and (3) How many localities con- ers et al. 2000). Its flora is among the most species rich taining species of Coleeae still occur in forested areas? (Barthlott et al. 1996) and dense (individuals per area; A difficulty with making such assessments, for this and Phillips & Miller 2002) on Earth. Eighty percent of the other groups on Madagascar and elsewhere, is that sam- plant species found on the island are endemic (Schatz et ple sizes are often small and sampling may be biased (Pe- al. 2000). Madagascar is the world’s second richest center terson et al. 1998; Hijmans et al. 2000; Randrianasolo et of diversity for the plant family Bignoniaceae, exceeded al. 2002). We developed a novel method for differentiat- only by the Neotropics (Gentry 1988). Coleeae (family ing between range-limited species and poorly sampled Bignoniaceae) is a monophyletic tribe endemic to Mada- species, thereby reducing the number of species that gascar and the surrounding islands of the Pacific Ocean would be listed as data deficient. This method can readily (Zjhra 1998, 2003; Zjhra et al. 2004) and is character- be applied to other taxa and regions. ized by high species diversity and local endemism (Gentry 1983, 1988; Zjhra 1998) within forested habitats. Yet, not a single species of Malagasy Bignoniaceae is listed in the 1997 IUCN Red List of Threatened Plants (Walter & Gillet Methods 1998), The World List of Threatened Trees (Oldfield et al. Coleeae 1998), or the 2004 IUCN Red List of Threatened Species (IUCN 2004b). This situation is not unique to Coleeae. Tribe Coleeae traditionally consisted of five genera (Colea, Of the roughly 12,000 species of plants in Madagascar 21 species; Ophiocolea, 9 species; Rhodocolea, 14 spec- (Myers et al. 2000), only 362 species (3%) are on the ies; Phyllarthron, 20 species; and Phylloctenium, 3 spe- 2004 update of the IUCN Red List of Threatened Species cies; Perrier de la Bˆathie 1938a, 1938b) with a total of 67 (IUCN 2004b). This demonstrates the lack of knowledge species. Current molecular results, however, place Phyl- of the status of the majority of Malagasy flora and reflects loctenium within the Phyllarthron clade (Zjhra 1998; Conservation Biology Volume 20, No. 4, August 2006 Good et al. Data Deficiency and Extinction Risk 1101 Zjhra 2003). Species of Coleeae are mostly canopy trees, in the context of assigning IUCN Red List categories to treelets, and, less commonly, shrubs (Zjhra 2003). Al- species. We used the Missouri Botanical Garden gazetteer, though individuals of these species may persist in de- which contains all known collection localities in Madagas- graded areas or secondary forest, reproduction has not car, to assess whether the species ranges are as narrow been observed