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 Clasificación de Riesgo de Extinción: un Estudio de Caso de una Radiación 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´ endémica 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 método 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 décadas. 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 endémicas, entonces puede que la pérdida de especies en Madagascar sea aun mas´ extrema de lo que se comprende.

Palabras Clave: análisis GAP, biodiversidad, categor´ıas y criterios de la Lista Roja de IUCN, endemismo, ex- tinción, mapas de distribución 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;

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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 outside primary forest habitat (M. Zjhra, as they seem (i.e., the result of true range restriction) personal observation). Species of Coleeae are concen- or appear narrow due to incomplete and/or biased geo- trated in the tropical rainforests of Madagascar, with a graphical coverage. peripheral distribution in Madagascar’s western dry de- ciduous forests and the arid spiny scrub forest of the Mapping of Distributions and Ranges south. We omitted four species (Ophiocolea floribunda, Phyl- The ranges and distributions of all species with more larthron bernierianum, Phyllarthron madagascaren- than three localities were mapped and analyzed using sis, and Phylloctenium bernieri) from the analysis be- ArcView 3.3 Geographic Information System (GIS) soft- cause they probably comprise multispecies complexes. ware (ESRI 1999), following conversion from decimal de- The conservation status of these species will be assessed grees to UTM 38S. To assess the status of threat and assign once morphological and molecular analyses are com- IUCN Red List categories for each species, we derived the pleted (M.L.Z., unpublished data). following information by mapping primary occurrence data: (1) number of subpopulations, (2) number of pro- Distributional Data tected areas that contain ≥1 subpopulation, (3) extent of occurrence, (4) area of occupancy, and (5) their pre- We compiled a database that included all specimens for dicted future decline, as described below (c.f. Schatz et al. which locality information was available from the Mu- 2000). For species with ≤3 localities, we also determined seum National de Histoire Naturelle, Paris, the Royal whether these localities were in remaining patches of for- Botanic Garden at Kew, and Missouri Botanical Garden, est in the year 2000. St. Louis. This database contains 748 accessions, includ- The number of subpopulations was estimated by plac- ing types, with collections dating from 1835 to 1998. Each ing a 10-km2 grid over the layer of the species localities specimen was examined by one of us (M.L.Z.) to deter- and then considering that each occupied cell constituted mine whether the identification was correct. When pos- a distinct subpopulation, except in the cases of occu- sible, we used the Missouri Botanical Garden gazetteer pied adjacent cells for which all such contiguous cells to georeference old records (Schatz et al. 2000; Schatz were then considered to represent a single subpopulation & Lescot 2003). The specimen labels of modern collec- (Schatz et al. 2000). We utilized an ArcView extension, tions (before 1980) included latitudes and longitudes de- Species Range Analyst (Fay et al. 2002), to calculate the termined from maps (1:50,000 or 1:100,000 series) or ge- minimum convex polygon (MCP) for every species based ographic positioning systems. Of the recently discovered on its occurrence points. The area within each polygon (after 1990) Coleeae species, 12 of 15 were collected by represented the extent of occurrence (IUCN 2001). one of us (M.L.Z.). Plant specimens were available from Because Coleeae appear to be dependent on primary 342 localities. These occurrence data formed the basis forest for reproduction, the extent of occurrence may for mapping and analyzing species distributions across not necessarily be a reliable measure of threat. The nega- Madagascar (collection locations in Fig. 1). tive consequences of large-scale deforestation, which has taken place in Madagascar over the last 50 years (Green & Sources of Bias Sussman 1990), on the loss of biodiversity are well known There were two sources of bias in primary occurrence (Brown & Gurevitch 2004). As a result, a species with data taken from herbarium collections. First, collections a large extent of occurrence is still threatened if most are incomplete and often have a biased geographical cov- of the primary forest within its extent of occurrence is erage. Collectors tend to return to known sites, and sam- gone. A much better measure is that of area of occupancy, pling occurs more frequently along roadsides, close to which is defined as “the area within its extent of occur- villages, streams, airports, or established base camps. Sec- rence, which is occupied by a taxon, excluding cases of ond, older records have larger geographical error than re- vagrancy. The measure reflects the fact that a taxon will cent records because latitudes and longitudes were rarely not usually occur throughout the area of its extent of oc- included in the collection data. Although others have currence, which may contain unsuitable or unoccupied touched on these difficulties (Randrianasolo et al. 2002), habitats” (IUCN 2001). But rather than counting the num- only a few have attempted to correct for them (e.g., Hij- ber of occupied grid cells and multiplying them by the cell mans et al. 2000; Peterson et al. 2004). size (IUCN 2001), we defined the area of occupancy as Here we present a novel approach to addressing the the remaining area of primary forest in year 2000 within issue of incomplete and/or biased geographical coverage each species’ minimum convex polygon.

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Figure 1. Collection localities of Coleeae in Madagascar: shaded areas, forest cover; closed circles, Coleeae collection localities; open circles, reassessed data-deficient Coleeae species. Inset shows 5000-km2 buffers surrounding the collection localities of Phyllarthron megapterum (open circles); closed triangles, collection localities of the Missouri Botanical Garden gazetteer; arrow, buffer that was visited four times.

The 2000 layer of forest cover was derived from not represented in the network of protected areas) that Steininger et al. (2003) and modified by adding data may be filled through establishment of new protected ar- from other sources to improve classification of the highly eas. The predicted future decline of a species’ area of oc- clouded regions of the image (e.g., Antongil Bay). We then cupancy was calculated as area of occupancy outside pro- simplified the original land-cover classifications into pri- tected areas/total area of occupancy (Schatz et al. 2000). mary forest, nonprimary forest, cloud, and water classes. This calculation assumes that all the forest outside pro- Because some cloud cover still remained over certain ar- tected areas will be deforested in the near future, which eas of Madagascar, we calculated for each species its area is not unrealistic based on the history of deforestation in of occupancy based on forest area alone and forest area Madagascar (Green & Sussman 1990; Nelson & Horning plus cloud cover area (because areas under persistent 1993; DeFries et al. 2005). clouds often are forested; unpublished observations) and then averaged the two values. IUCN Red List Categories We performed a GAP analysis (Scott et al. 1993) to determine the presence or absence of all species of Coleeae We used the following IUCN categories to assign extinc- in protected areas and to calculate the number of pro- tion risk for each species: extinct, extinct in the wild, crit- tected areas that contained ≥1 population of a Coleeae ically endangered, endangered, vulnerable, near threat- species. Such analyses identify gaps (i.e., species that are ened, least concern, data deficient, and not evaluated.

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Due to lack of information on generation length in many any particular buffer by the same collector in 1 year were tropical trees, including Coleeae, generation length for counted as one visit. The more visits a buffer received criteria A is estimated to be 50 years (WCMC 2004). the more supporting evidence we have that the species indeed has a small extent of occurrence or the species may be extinct if its known localities are now deforested Reassessment of IUCN Status and/or the species has not been observed elsewhere in According to IUCN Red List Criteria and Categories: Ver- over 30 or 50 years (Fig. 2). sion 3.1 (IUCN 2001), the liberal use of the data deficient category is discouraged. Thus, we used additional information such as number of subpopulations occur- ring in protected areas, number of subpopulations oc- curring in forested areas, and number of return visits to the area to assign a threat category to the otherwise data- deficient species. Additionally, we reassessed the status of other Coleeae species that had small extents of occurrence (<5000 km2) to see whether certain species’ extents of occurrence are as small as they seem (i.e., the result of “true absences”) or whether they instead appear small due to incomplete and/or biased geographical coverage. We used a similar approach to reassess the status of species that had not been seen in over 30 or 50 years. To reassess the status of these species, we used the MBG gazetteer to determine where other collection efforts had taken place. We assumed that botanical collection expeditions collected everything that was in fruit or flower at the time and that Coleeae would have been part of the collection had they occurred at those specific locations. The locations where no records of Coleeae were obtained were then assumed to represent true absences. These as- sumptions about collecting habits are reasonable because early collectors (before 1980) were general collectors (i.e., they collected all specimens in fruit and flower), and while modern collectors (post 1980s) tend to spe- cialize on specific families, they also collected Coleeae. It is possible that species of Coleeae that occurred in a locality were not in fruit or flower at the time of a collecting event, which would result in a false absence. Nonethe- less, Coleeae flower and fruit during the same predomi- nant period (November–February) as other trees in the Malagasy forest, so in theory they should be detected over repeated visits because most botanical collectors tended to visit forests in Madagascar during this period. For these three categories of species (data deficient, not observed in 30 or 50 years, or extent of occurrence <5000 km2) we drew buffers of 5000-km2 area around each specimen, corresponding to IUCN’s criteria of extent of occurrence for the category EN (endangered). Next we intersected the buffers with the MBG collection localities and our own Coleeae localities to see how Figure 2. Map of species localities not protected under many times each area had been revisited since the last the current protected-area network (shaded areas, sighting of a specimen. We calculated the average number national parks, special reserves, and nature reserves; of visits per buffer for each species, discarding the ones closed circles, unprotected Coleeae species). that had taken place before the recording of the particu- Phyllarthron megapterum provides an example of a lar specimen in the buffer. If buffers of the same species species with localities that did not occur within a overlapped by >50%, the visits in the overlapping areas protected area but for which its extent of occurrence were only counted once. Furthermore, multiple visits to (depicted by the polygon) included protected areas.

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Results the sparse data associated with these eight species (five of which were DD) truly reflects restricted ranges. Of Preliminary Assignment of IUCN Status these eight species Colea alba, Colea lutescens, Colea A preliminary assignment of extinction risk based on rubra, Rhodocolea linearis (formerly DD), and Ophio- IUCN criteria for the 67 species comprising endemic colea decaryi (formerly EN) have only one specimen per subpopulation that was recorded in forested and pro- tribe Coleeae is given in Table 1. Forty-one percent of ≥ the species are threatened with extinction based on pre- tected areas (based on records 50 years old). There- dicted future decline (20 species, critically endangered fore, we assigned these species the threat category CR. [CR]; 5, endangered [EN]; 1, vulnerable [VU]). Three per- Rhodocolea macrocalyx (formerly DD) has no known cent of the species are threatened with extinction based specimen in forested or protected areas and was assigned on their small extent of occurrence and area of occu- the category EX. Although Colea barbatula has two spec- pancy (2 species, EN). For 56% of the species, there is in- imens/subpopulations in forested and protected areas, its adequate information to make an assessment of their risk predicted future decline of more than 80% allowed it to re- of extinction (DD) either because they have been discov- main in the category CR. Phyllarthron laxinervium has ered recently (after 1990; 15 species), are known from <3 two specimens/subpopulations in forested and protected subpopulations (which does not permit the calculation of areas and therefore retained the category EN. extent of occurrence or area of occupancy, 18 species), or Two species were reassessed based on their small ex- < 2 have only been collected in a very restricted area (≤100 tent of occurrence ( 5000 km , Table 2). Because they km2, 2 species) and there is still too little information had only one specimen per subpopulation in forested or to assess their extinction threat. The four species com- protected area and because their buffers had been revis- plexes (Ophiocolea floribunda, Phyllarthron bernieri- ited on average 11 times since the last sighting of the anum, Phyllarthron madagascarensis, and Phyllocte- species, Phyllarthron megaphyllum and Phyllarthron nium bernieri) were not evaluated (NE). schatzii (formerly EN) were assigned the threat category The known localities of 16% of the species have been CR. deforested. Unless other subpopulations are found else- The revised number of species threatened with extinc- where these species are presumably extinct (Table 1). tion was 34 (29 CR, 4 EN, 1 VU), or 54% (20 species initially assigned CR, 4 DD species not seen in over 50 years reassessed and assigned CR, 2 DD species not seen GAP Analysis in over 30 years reassessed and assigned CR; 7 initially as- A GAP analysis was performed against Madagascar’s cur- signed EN, of which 3 were reassessed and assigned CR, rent protected-area network for 63 species of Coleeae. and 1 initially assigned VU). Furthermore, 3 DD species Twenty-four species (38%) have only one subpopulation were reassessed and assigned EX. The remaining 26 DD in a protected area. The known localities of 28 of the 63 species could not be reassessed with this method because species (44%) do not occur within the protected-area sys- not all of their buffers had been revisited. tem, even though for 20% of them, the area of occupancy intersects parts of the protected-area system (Table 1, Fig. 2). Discussion

Refinement of IUCN Status and Final Assignment IUCN Categories: Current versus Future Threat Four species (all initially DD) have not been recorded Our major finding was that 54% of the species of Coleeae in ≥30 years even though their surroundings (5000 km2 are threatened with extinction, with 51% of those being buffers) have been revisited on average 13 times since the under criteria A (predicted future decline). We believe last sighting of the species (Table 2). Based on records the threat associated with the predicted future decline is ≥30 years old, Ophiocolea velutina and Rhodocolea an appropriate measure: the calculated predicted future campanulata have only one specimen per subpopulation decline is based on the assumption that undisturbed for- in forested and protected areas and were therefore also est will ultimately only be entirely restricted to protected assigned the threat category CR. Phyllarthron sp. nov. areas (Schatz et al. 2000; DeFries et al. 2005), and pro- Vatovavy and Phyllarthron sp. nov. Vohemar are both jections of forest loss in Madagascar are not encouraging known from a single locality, and that locality has been (Green & Sussman 1990; Sussman et al. 1994; Agarwal et deforested. Therefore, we assigned these two species the al. 2005). Critics will argue that this represents a worse- threat category extinct (EX) (Table 2). case scenario. However, we believe this is a conservative Eight species have not been recorded in ≥50 years estimate for two reasons: (1) we were conservative in even though the 5000-km2 area around each locality has our calculations of extent of occurrence and area of oc- been revisited on average 19 times since the last sight- cupancy and have, if anything, overestimated the size of ing of the species (Table 2). We therefore judged that both these areas, and (2) we have only incorporated one

Conservation Biology Volume 20, No. 4, August 2006 Good et al. Data Deficiency and Extinction Risk 1105 d continued & B2a,b(ii) subcriteria c risk b 001). occupancy (%) b ) 2 (km b ) 2 Number of Predicted Number of subpopulations future IUCN IUCN 1928 2 1 1 ? ? ? DD 1992 1 0 1 ? ? ? DD 1923 1 1 1 ? ? ? DD Time subpopulations in forested Extent of Area of decline in category of criteria frame of Number of in protected area occurrence occupancy area of extinction and collections subpopulations areas (2000) (km 1907–19221912–19931911–19851901–1955 31879–1991 71912–1990 171882–1990 41840–1997 41890–1990 41905–1974 101830–1997 2 81882–1974 2 3 51937–1998 41936–1984 1 501905–1995 2 101922–1989 0 14 01912–1963 2 61932–1973 0 13 31898–1996 0 2 71933–1998 0 7 1 71911–1990 3 1 31908–1922 14,000 2 1 91950–1998 2 14 60,0001908–1949 87,000 0 4 3 41908–1970 2,000 36,000 2 20,000 31950–1991 0 10,000 4 14 7 7,000 1 74,000 3 1 2 4,000 5,000 6 1 5 0.81 1 3,000 0.83 13,000 3 0.95 600 1 230,000 1 3 12,000 200 400 1 0.90 2 15,000 2 45,000 370,000 1 0.81 0.93 CR 2 5,700 CR 90 1 CR 0 12,000 26,000 127,000 20 1 45,000 0.98 1 4 CR 0.85 2 A3c; D 0.87 2,500 2,500 45,000 CR CR 0.99 400 1 A3c 0.89 A3c 1.00 7 0.87 170,000 920,000 600 2 CR 10,000 A3c; D 0 CR 1.00 0.89 A3c; A3c; 50,000 D D 90 1 9,000 14,000 CR CR CR 150 CR 14,000 A3c; CR 200 0.89 D 8,000 2,000 56,000 A3c 1.00 0.93 0.91 A3c; CR CR D 5,000 A3c; D A3c; 0.88 D A3c; D 90 200 1,200 A3c 0.79 6,500 CR 0.66 CR A3c A3c CR CR 100 0.28 0.74 CR 0.79 A3c EN A3c; D A3c A3c EN 0.70 A3c; D EN EN A3c; EN D A3c EN A3c; D A3c; D D A3c; B1a,b(ii) 1996–19971966–19941850–1991 1 2 2 0 1 1 1 2 1 ? ? ? ? ? ? ? ? ? DD DD DD 1950–19541928–19901948–1984 3 4 2 1 0 0 1 1 0 12,000 300 ? 600 180 0.37 0.14 ? VU EN ? A3c; B2a,b(ii) D DD ∗ ∗ . Andohahela a sp. nov Table 1. Preliminary assessment of extinction risk for species of the tribe Coleeae according to IUCN Red List Categories and Criteria: Version 3.1 (2 Colea barbatula Colea fusca Colea lantziana Colea muricata Colea myriaptera Colea nana Colea obtusifolia Colea tetragona Ophiocolea delphinensis Rhodocolea boivinii Rhodocolea racemosa Rhodocolea telfairiae Phyllarthron articulatum Phyllarthron bilabiatum Phyllarthron humblotianum Phyllarthron ilicifolium Phyllarthron multiflorum Phyllarthron suarezense Phyllarthron subumbellatum Phylloctenium decaryanum Colea alata Ophiocolea decaryi Rhodocolea nobilis Phyllarthron laxinervium Phyllarthron megapterum Phyllarthron schatzii Colea hirsuta Colea lutescens Colea purpurascens Colea gentryi Species Phyllarthron megaphyllum Rhodocolea involucrata Colea alba Colea asperima Colea

Conservation Biology Volume 20, No. 4, August 2006 1106 Data Deficiency and Extinction Risk Good et al. d subcriteria c NE NE NE risk b ion of the criteria and subcriteria, occupancy (%) b ) 2 1 1.00 DD 1 1.00 DD 1 1.00 DD 1 1.00 DD 1 1.00 DD < < < < < (km b ) 2 1 1 1 1 1 < < < < < Number of Predicted Number of subpopulations future IUCN IUCN 1997199719181997 11993 1 11987 1 11998 01991 1 01926 1 1 01992 2 0 1 1 1 1 1 1 0 1 11996 01998 11960 ?1966 1 ? 11998 ? 11995 1 ? 1 1 1 ? 1 ? 1 ? 1 ? 1 ? 1 0 ? 0 ? 0 ? ? ? 1 ? 0 ? ? 0 ? 1 DD ? 1 ? DD 0 DD ? 0 DD 1 ? 0 ? ? DD ? ? ? DD ? ? ? DD ? ? DD ? ? ? ? ? ? DD DD DD DD DD Time subpopulations in forested Extent of Area of decline in category of criteria frame of Number of in protected area occurrence occupancy area of extinction and collections subpopulations areas (2000) (km 1899–1998 1880–1998 1846–1998 species complexes NE 1988–19921967–19971926–1974 2 21953–1962 11949–1950 1 1 0 2 1 1 2 0 0 1 ? 11847–1994 ? 0 ? ? ? ? ? ? ? ? ? ? DD DD ? DD DD DD 1996–1997 1 01997–1998 1 1 0 1 1988–19981966–19891988–19901953–1991 21967–1984 3 2 1 1 1 0 2 1 0 2 0 1 1 0 3 27 ? ? ? 3 2 ? ? ? 0.17 1.00 ? ? DD DD ? DD DD DD ∗ ∗ ∗ ∗ ∗ ∗ ∗ . ∗ cauliflorous ∗ Vatovavy Vohemar Manongarvivo Ankaviensis Itremo ∗ ∗ sp. nov. ∗ ) indicates recently discovered species (post-1990). sp. nov. sp. nov. ∗ sp. nov. sp. nov. sp. nov. ∗ a Little is known about generation length in tropical trees. For criterion A, the generation length used was 50 years ( WCMC 2004). For detailed descript An asterisk ( A question mark (?) indicates insufficient information. IUCN categories of extinction risk: CR, critically endangered; EN, endangered; VU, vulnerable; DD, data deficient; NE, not evaluated. Table 1. (continued) Colea ramiflora a b c d please consult IUCN (2001) Phyllarthron bernierianum Phyllarthron madagascariensis Phylloctenium bernieri Colea rubra Colea sytsmae Ophiocolea Ophiocolea ornithophila Ophiocolea punctata Ophiocolea schatzii Ophiocolea velutina Ophiocolea vokoanensis Rhodocolea campanulata Rhodocolea linearis Rhodocolea macrocalyx Rhodocolea Rhodocolea multiflora Phyllarthron sahamalazens Phyllarthron Phyllarthron Phyllarthron vokoanensis Ophiocolea floribunda Colea resupinata Rhodocolea Phylloctenium Colea rosea Rhodocolea lemuriphila Rhodocolea perrieri Rhodocolea schatzii Phyllarthron antongiliense Phyllarthron cauliflorum Phyllarthron nocturnum Species

Conservation Biology Volume 20, No. 4, August 2006 Good et al. Data Deficiency and Extinction Risk 1107 . ents. Of the species that fell into one or 50 years (D50, i.e., since 1954), we ≥ consult footnotes in Table 1 Total number Range a 30 years (D30, i.e., since 1974) and isk and IUCN criteria and subcriteria ≥ Number of of visits of visits Range of Final reviations of categories of extinction r 50%; the visits in the overlapping areas were only counted once. ) and for species that had not been sighted in > 2 subpopulations in PA (2000) sighting sighting buffers risk subcriteria c 5000 km ≤ EOEO 3 3 1 1 1 1 22 10 11–15 7–11 1908–1998 1949–1997 CR CR D D D50D50D50D30D30D50 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 14 12 14 6 14 8 12 4 14 1937–2001 1950–2001 6 1937–2001 8 CR 4 CR 1974–1993 CR 1962–1996 1967–1987 CR D CR D CR D D D D D50 3 2 2 38 2–33 1924–1993 CR D D50 2 0 0 15 15 1950–1989 EX (date Number of subpopulations area since last since last revisited extinction and D50 & EOD50 & EO 3 3 1 2 1 2 34 55 7–23 9–18 1937–2001 1937–1998 CR EN D D Reason for subpopulations over all over all collection IUCN IUCN and/or EO) reassessment Number of in forested buffers buffers dates for all category of criteria ∗ ∗ ) had two buffers overlapping by ∗ ∗ ∗ sp. nov. Vatovavysp. nov. Vohemar D30 D30 1 1 0 1 0 0 30 7 30 7 1960–1993 1966–1993 EX EX DD EN CR = = = b Phyllarthron laxinervium Phyllarthron megaphyllum Colea alba Colea lutescens Colea rubra Ophiocolea velutina Rhodocolea campanulata Rhodocolea linearis Rhodocolea macrocalyx Ophiocolea decaryi Colea barbatula Phyllarthron Phyllarthron Phyllarthron schatzii Abbreviations: EO, extent of occurrence; PA, protected areas. For abb Species with an asterisk ( For species with small extent of occurrence (EO assessed whether the assigned threatmore categories of in these Table 1 categories were only based those on whose lack buffers of have sampling all effort been in revisited the were area considered. or due truly to small ranges or extinction ev Table 2. Use of “absence data’’ from other botanical collections to assess threat status of species in the tribe Coleeae. Prior status a b c Prior status Prior status Species

Conservation Biology Volume 20, No. 4, August 2006 1108 Data Deficiency and Extinction Risk Good et al. of the many drivers of biodiversity loss in our analysis and Ten species of Coleeae are from the Masoala Penin- species extinctions are likely to be compounded by sev- sula and are new to science (Zjhra 2006). Although these eral changes, in particular climate changes (Thomas et al. species appear to be endemics restricted to a single wa- 2004). tershed, more collecting expeditions are needed to determine the extent of their distributions. These species were Significance for Other Malagasy Plants discovered after the delineation of the Masoala National Park boundaries (Kremen et al. 1999), and it is not yet As of 2004, only 3% of the 12,000 described Mala- known whether they also occur within the park bound- gasy plant species had been assessed according to IUCN aries. Red List Criteria and Categories: Version 3.1 (2001). Of these, 267 species (74%) were threatened with extinction mainly due to habitat loss (IUCN 2004). Several re- Reassessed Species cent studies reveal similar results. A preliminary assessment of the risk of extinction facing 32 species from the Slightly more than half of the species in this study could endemic families Asteropeiaceae, Melanophyllaceae, and not initially be evaluated due to data deficiency. Roughly Sphaerosepalaceae demonstrates that 62% are threatened half of these were newly discovered species (after 1990) with extinction (Schatz et al. 2000). In the family Pan- on the Masoala Peninsula, whereas the other half were danaceae, 91% of the 95 assessed species are considered species known from two or fewer collections. The IUCN at risk of extinction (M. W. Callamander, G. E. Schatz, T. Red List Categories and Criteria: Version 3.1 (IUCN 2001) Consiglio, and P. Lowry, unpublished data). Every one of discourages designating species as “Data Deficient” and the 15 species (100%) within the family Anacardiaceae, suggests several ways to deal with species with limited for which data are available, is considered threatened data, stating “If the range of a taxon is suspected to be rel- with extinction (Randrianasolo et al. 2002). The 54% of atively circumscribed, and a considerable period of time Coleeae species in our study that face extinction fall on has elapsed since the last record of the taxon, threatened the lower end of the spectrum, but the percentage is status may well be justified.” Thus, we “rescued” 9 out of surely an underestimate of the number of Coleeae species the 35 species from the data-deficient category by con- at risk because we lacked information to assess the risk sidering (1) whether or not the occurrence localities of of extinction for half of the species. In fact, some IUCN the species were still forested and/or protected and (2) practitioners would move several, if not all, DD species how many additional collections took place within the 2 into the category VU according to criteria D1 or D2 (pop- 5000-km area surrounding each Coleeae specimen. Fur- ulation size fewer than 1000 mature individuals or re- thermore, we applied the same information to reassess stricted in area of occupancy or number of locations), species with small extents of occurrence and those that which would mean all assessed species are threatened had not been seen in 30 and 50 years, respectively. We be- with extinction. lieve this information provides grounds for moving three If these assessed species are representative of the Mala- species formerly assigned as EN to CR. gasy flora, then species loss is possibly more extreme than With three species presumed extinct, and an additional previously thought. Endemism of vascular plants in Mada- 12 not seen in decades, this is probably a conservative gascar (not including ferns) is 92% (Goodman & Benstead estimate of Coleeae extinctions. Early collections proba- 2005), and the majority of these plants are facing the same bly represent only a fraction of what originally existed, major threat—deforestation. Thus, it seems likely that for whereas recent collections have unveiled new described any given family 50–100% of the species will be threat- species that have persisted despite rapid habitat loss. ened with extinction in the near future. Molecular work (Zjhra 1998, 2003) suggests repeated regional radiations and habitat diversification (e.g., inva- GAP Analysis sion of dry forests, reinvasion of wet forests) in Coleeae. Pollination studies (Zjhra 1998, 2003) demonstrate that It is clear that the protected-area network in Madagas- 11 or more species of Coleeae may coexist via differential car is inadequate for the protection of Coleeae and many use of reproductive niches. Localized habitat destruction other taxa, including tiger beetles (Andriamampianina et therefore may affect entire clades of a taxonomic group, al. 2000) and butterflies (Kremen et al. 2003). Twenty- not only depleting the region of a portion of its diversity, eight species of Coleeae (42%) are not known to occur in but also impeding our understanding of the historical re- the current protected area network (although for 20% of lationships of these groups. these, the area of occupancy intersects parts of the protected area system; Fig. 2). These species are therefore Concluding Remarks ideal candidates for future survey work. An additional 24 species are only known from a single subpopulation in Analyses such as ours are essential for setting taxon- a protected area, raising questions about the long-term specific conservation priorities and for designing and viability of these presumably “protected” species. managing protected areas. They help identify areas that

Conservation Biology Volume 20, No. 4, August 2006 Good et al. Data Deficiency and Extinction Risk 1109 have been undercollected or areas that need to be revis- ESRI. 1999. Arcview 3.1 GIS. Environmental Systems Research Insti- ited to confirm the existence of species of concern. Our tute, Inc., New York. results together with model outputs of potential species Fay, J., C. Kremen, D. Lees, and L. Andriampianiana. 2002. Species range analyst: an ArcView extension for predicting species ranges distributions (Phillips et al. 2004) allow one to exam- from presence data. Stanford University, Stanford, California. Avail- ine more efficient target areas to inventory and to test able from http://www.stanford.edu/group/CCB/GIS/SRA (accessed and refine species distribution models (Raxworthy et al. December 2005). 2003). Although the outlook for biodiversity in general, Gentry, A. H. 1983. Dispersal and distribution in Bignoniaceae. 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