Distribution, status, and conservation needs of the golden-crownedsifaka (Propithecus tattersalli)

Astrid Vargasa, Ignacio Jimeneza,*, Francisco Palomaresb, Marıa Jesus Palaciosc

aSpecies and Spaces International, Carlota Alessandri 69, Apt. 10, Montemar 29620, Malaga, SpainbDepartment of Applied Biology, Donana Biological Station, Avda. de Maria Luisa s/n, Pabellon del Peru, Sevilla 41013, SpaincConsejerıa de Medio Ambiente, Direccion General de Medio Ambiente, Avda. Virgen de Guadalupe 42, Caceres 10001, Spain

Abstract

The golden-crowned sifaka is considered one of the world’s most endangered primates. To evaluate the species’ current con-servation status we established its actual distribution and abundance, and assessed current threats that affect its survival. Studymethods involved direct sifaka observations and interviews to local villagers. Propithecus tattersalli’s distribution is restricted to the

region comprised between the Loky and Manambato rivers. Throughout its range, the species is abundant and it can even be foundin small forest fragments, although it was never observed at elevations above 700 m.a.s.l. Major threats to the species includehabitat destruction through slash-and-burn agriculture, grass fires, wood and gold extraction, and poaching. Total population

estimates range from 6100 to 10,000 individuals, with an effective population size of approximately 2500–4000 sifakas. Thoughsensitive to forest destruction, the species seems to be resilient to current levels of landscape fragmentation. We recommend theestablishment of a system of protected areas throughout the Loky-Manambato region and the implementation of a ‘‘Flagship

Species Program’’ utilizing the golden-crowned sifaka as a catalyst for a regional Conservation Management Plan. # 2002 ElsevierScience Ltd. All rights reserved.

Keywords: Golden-crowned sifaka; Propithecus tattersalli; Distribution; Abundance; Flagship species

1. Introduction

Madagascar is considered one of the world’s bio-diversity hotspots due to its high level of endemisms(Mittermeier and Goettsch, 1999). Among the uniquefauna found in the island, lemurs represent a completeadaptive radiation of non-human primates (Mitterme-ier et al., 1992, 1994). Of the existing lemur taxa, thefamily Indriidae contains the largest and, perhaps,the most spectacular lemur species. Within thisfamily, the genus Propithecus comprises nine differenttaxa, of which only one species, Propithescus tattersalli,is monotypic (Mittermeier et al., 1994). This primatewas first noted by Tattersall in 1974 (Tattersall, 1982)but it was not scientifically described until 14 yearslater (Simons, 1988).The golden-crowned sifaka is one of the smallest

representatives of the genus Propithecus, with an aver-age adult weight of 3.5 kg and a total body length ofapproximately 90 cm (Meyers, 1993; Mittermeier et al.,1994). The species is primarily diurnal, although it can

also display early morning and crepuscular activitybouts during the rainy season (Meyers, 1993). Duringdry season, it also tends to feed and rest on higher partsof the canopy (Meyers, 1993), which makes it morevisible from observation points outside of the forest.Group size ranges from 3 to 10 individuals that occupyterritories of 9–12 ha (Meyers, 1993).Previous studies estimated that the geographic dis-

tribution of Propithecus tattersalli was limited to forestfragments between the Loky and the Manambato Riv-ers, in northeast Madagascar (Meyers and Ratsirarson,1989; Randrianarisoa et al., 1999). These surveysfocused mainly on the three largest forest patches pres-ent in the region (Meyers and Ratsirarson, 1989; Mit-termeier et al., 1992; Meyers, 1993; BIODEV-FANAMBY, 1998), with the community of Darainabeing the center point of surveyed fragments. Almost nosurveys had taken place on smaller, neighboring pat-ches. Given the highly fragmented and limited distribu-tion of P. tattersalli, this species has been classified asone of the 25 most critically endangered primates inthe world (IUCN, 1997). The golden-crowned sifaka isalso listed as highest priority rating (6) by the Prim-ate Specialist Group, Species Survival Commission,

0006-3207/02/$ - see front matter # 2002 Elsevier Science Ltd. All rights reserved.

PI I : S0006-3207(02 )00117-9

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www.elsevier.com/locate/biocon

* Corresponding author. Tel./fax: +34-96-360-33-85.

E-mail address: i_jimenez_perez@yahoo.es (I. Jimenez).

International Union for the Conservation of Nature(Mittermeier et al., 1992).Throughout the last decade, there have been multi-

ple—yet unsuccessful—efforts and recommendations totry to establish a 20,000–30,000 ha protected area withinthe Daraina region to help protect the golden-crownedsifaka (Meyers and Ratsirarson, 1989; Mittermeier et al.1992, 1994; Randrianarisoa et al., 1999; BIODEV-FANAMBY, 1998; ANGAP, 2000). However, there hasbeen no systematic evaluation of the actual conservationstatus of the golden-crowned sifaka. This information isthe first step towards the development of a ConservationPlan for the species, ultimately supporting ongoingefforts towards establishing a protected area in the regionof Daraina. In this study, we evaluated the conservationstatus of P. tattersalli, focusing on the following twoobjectives: (1) to establish the species’ actual distributionand abundance, (2) to assess current threats that canaffect the species’ survival. Results from earlier-mentioned objectives were later used to evaluate thegolden-crowned sifaka Red List status based on IUCNcurrent criteria (IUCN, 2001), and to provide manage-ment recommendations to ensure its long-termprotection.

2. Methods

2.1. Study area

The Daraina region (12�500–13�190 S and 49�250–49�550 E) lies within the subregion of Vohemar (Ihar-ana), in the Tsaratanana hydrogeographic region, prov-ince of Antsiranana, northeast Madagascar. Previousinformation suggested that P. tattersalli occurred inforest patches delimited by the Loky and the Mana-mbato Rivers, within the Daraina region (Fig. 1;Simons, 1988; Meyers and Ratsirarson, 1989). Theregion comprises approximately 245,000 ha and it con-tains a mosaic of anthropogenic savanna, dry scrub,agricultural land, gallery forests, and forest fragmentsthat vary on degree of deciduousness. Four types of for-est (ranging in size between 1 and 14,000 ha) are found inthe region: dry deciduous forest covering the lower hills,semi-evergreen forest and pre-montane evergreen forestcovering hills and mountain tops, respectively, and thecoastal forest of Sahaka, within the region of Nosy Be.Throughout the region, an extensive network of galleryforests, which appear highly degraded in some areas,connects many forest fragments. Altitude ranges from100 m in the lowlands of Bekaraoka up to the 1170 mof Binara, the highest point in the region. Climate isseasonal, with a dry period that lasts an average of 8months—April through November—and a 4-month wetseason, from December to March, that coincides withthe Austral summer (Meyers, 1993). No forest within theregion enjoys a legal protection status.

The study area includes 18 rural communities, eachcomposed of small villages that vary between 6 and2000 people (Rajaobelina, personal communication),which primarily depend on a subsistence economydominated by slash-and-burn agriculture, cattle-raising,extraction of forest products, as well as fishing aroundthe coastal and lake areas of Sahaka. The most intensiveform of agriculture is dry rice cultivation in the interiorforests and wet rice farming around Lac Sahaka (Saf-ford, 2000). Gold mining also plays a role in the localeconomy, being mostly exploited by immigrant miners(Meyers and Ratsirarson, 1989). In spite of the region’ssevere fragmentation, the important levels of biologicaldiversity encountered between the Loky and the Mana-mbato Rivers explain why the Daraina region has beenrepeatedly designated as a high priority area for biodi-versity conservation (Ganzhorn et al., 1997; ZICOMA,1999; ANGAP, 2000).

2.2. Geographic distribution

To determine the presence of P. tattersalli in forestfragments we used two main methods: interviews anddirect observations. These techniques were usedthroughout the region comprised between the Loky andthe Manambato Rivers and in bordering forestsand villages located on opposite sides of both riverdrainages. Interviews aimed at obtaining preliminaryinformation on the presence of sifakas in the area aswell as at acquiring knowledge regarding human activ-ities in the surrounding forests and, most importantly,at increasing local awareness and pride regarding theimportance of the golden-crowned sifaka as a unique,endemic species to the region. Interviews to local villa-gers always preceded forest surveys, and target groupsmostly included local middle-aged and young men thatworked in the forests who, therefore, were knowledge-able of the surrounding wooded areas and the possiblepresence of sifakas. Interviews were carried out in abrief, unstructured, and informal fashion covering thethree following issues: (1) presentation of a poster withall the sifakas of Madagascar to ensure proper species’identification and, inquiries about the existence of sifa-kas in nearby forest fragments, (2) inquiries about therelative abundance of the species in those fragments,and (3) activities carried out in the surrounding foreststhat could threaten this primate (slash and burn agri-culture, wood extraction, mining, and hunting).Actual distribution of the golden-crowned sifaka was

subsequently confirmed through surveys of individualforest fragments, which were identified a priori using aLANDSAT TM 1:50,000 image of the region taken in1994 and FTM 1:100,000 maps based on aerial flightstaken in 1949. A forest fragment was defined as anypiece of forested landscape with an area larger than 4 haand a minimum width greater than 50 m. When a forest

326 A. Vargas et al. / Biological Conservation 108 (2002) 325–334

of these characteristics presented areas narrower than50 m, these tracts were considered part of the samefragment only if their length did not exceed 100 m.Longer, narrow areas with trees were not consideredforest fragments if isolated, but they were classified ascorridors when they served as a connection betweenforest patches.Forest fragments were surveyed using two methods:

observation points and forest transects. For any sur-veyed fragment we established an observation point athigh and/or medium altitude sites that allowed maximum

visibility of the area. Distances from each observationpoint to the targeted forest fragment ranged between200 and 1500 m. Once an observation point was estab-lished, each survey team—composed of one to twopeople—searched for sifakas with binoculars for amaximum period of two hours or until the first indivi-dual was detected. Three factors converged to allow ahigh detectability of the species from distant areas: (1)local landscape is rugged, allowing for visual access oflarge forested areas from specifically chosen high andmedium altitude points, (2) our study was conducted

Fig. 1. Golden-crowned sifaka presence throughout its distribution range.

A. Vargas et al. / Biological Conservation 108 (2002) 325–334 327

during the dry season, when most forests within thestudy area had lost a significant number of leaves, and(3) golden-crowned sifakas have a bright white coat thatprovides a sharp contrast with other forest featureswhen observed from afar. Our fragment survey-schemeprevented the possibility of counting the same group ofsifakas in different fragments. Preliminary observationsindicated that the times of highest activity levels, andthus the optimal observation periods to detect golden-crowned sifakas, was between 8:00 and 12:00 and 15:00to 17:30 h.Transects were established in forest fragments where

the existence of sifakas could not be verified fromobservation points. This method was used mostly insmall fragments (4–20 ha) located on flat areas, andwith limited visibility from distant points. In such cases,the forest was transected along its two main axes. Eachsurveyed fragment was given one of the following valuesregarding the occurrence of P. tattersalli: present,absent, and undetermined. Golden-crowned sifakaswere considered present in a forest when at least oneindividual of the species was observed by a member ofour team. The species was considered absent when itspresence could not be confirmed through direct obser-vations and the following criteria where met: (1) morethan 2 h of observation were dedicated to the fragmentand the whole fragment was transected at least along itslongest axis, (2) weather conditions during observationswere appropriate (i.e. absence of rain), and (3) nointerviewees reported having ever observed the speciesin the forest patch. When no sifakas were seen in afragment and at least one of the previous criteria wasnot met, such forest was classified as undetermined.

2.3. Species abundance

Density estimates were obtained from five repre-sentative sampling areas covering sections of forestfragments where the species had been previously detected.These five areas included two lowland dry forest (Cen-tral Bekaraoka and Andasibe), a semievergreen forestfragment (Andrainginala), and two premontane ever-green forests (Binara and Antsahabe; Fig. 1). To deter-mine number of groups per site, a minimum of fourreplicate counts were carried out for two consecutivedays in each sampling area (i.e. two counts from 8:00 to12:00 h and two counts from 15:00 to 17:30 h). Theserepeated counts allowed us to ensure that our groupmeasures were consistent. Densities at each samplingarea were estimated as number of groups sighted divi-ded by the total visible area from such points. Totalobserved area was calculated from a 1:100,000 topo-graphic map that included altitude lines. Comparisonsbetween the different forest types allowed us to obtainminimum and maximum number of groups per unit ofarea (km2).

Area of occupancy and extent of occurrence werecalculated by digitizing each positive forest fragmentfrom the LANDSAT TM image on MAPINFO GIS.Extent of occurrence was measured by a minimumcomplex polygon that included all the known sites ofpresent occurrence of the P. tattersalli. Area of occu-pancy is commonly defined as the area within a speciesextent of occurrence, which is occupied by a taxon,excluding cases of vagrancy (IUCN, 2001). We calcu-lated area of occupancy by adding the areas of all posi-tive fragments in the GIS database and subtractingthose mountain areas whose altitude precluded thepresence of the species. To estimate species abundance,we multiplied minimum and maximum density estimatesby the area of occupancy of P. tattersalli.

2.4. Threats to the species

We provide a descriptive evaluation of threats, whichwas conducted through interviews to local leaders,guides, ad hoc interviews with villagers (young andmiddle-aged men working in the forest), and directobservations. Besides questions regarding the presenceand relative abundance of the species (see earlier), weinquired about activities carried out in forests fragmentsthat could threaten P. tattersalli, such as hunting, slash-and-burn agriculture (tavy), firewood production, goldmining, and logging activities. When talking to villageelders, we also posed questions relative to changes thatmight have taken place overtime in the surroundingarea. In addition, we took notes of the various humanpressures (tavy, wood extraction, etc.) that we encoun-tered while surveying forest fragments and their sur-rounding matrix.

2.5. IUCN Red List status

In order to classify P. tattersalli into the IUCN RedList Categories we used the latest criteria established bythe IUCN Species Survival Commission, version 3.1,approved in February 2000 (IUCN, 2001). Input dataincluded all updated information on golden-crownedsifaka’s geographic distribution (including actual extentof occurrence and area of occupancy), estimated abun-dance, effective population size, number of subpopula-tions, threats to the species, fragmentation patterns,population trends, and estimates of potential declines(Table 1).

3. Results and discussion

3.1. Geographic distribution

Throughout the 6 weeks of fieldwork, a total of 948man-hours were invested in searching for P. tattersalli.

328 A. Vargas et al. / Biological Conservation 108 (2002) 325–334

We carried out a total of 83 interviews, with an averageof four interviews per group of neighboring forestpatches. In general, if P. tattersalli existed within thevicinity of an area, local villagers were able to identify itfrom poster drawings. Information provided by localvillagers regarding the presence or absence of sifakas innearby forests was found to be accurate, and only onthree occasions we found sifakas in small fragments thatlocal villagers had regarded as negative. Golden-crowned sifakas are highly conspicuous and widespreadthroughout their distribution range. While searching forthe species, we were frequently able to establish theirpresence in a fragment before even settling in a specificobservation point. In general, sightings occurred withinthe first 15 min of observation and, if there were sifakasin the targeted forest fragment they could be usuallylocated within the first hour of observation (authors,unpublished data).Ground surveys resulted in sightings of 108 sifaka

groups, including a total of 334 observed individuals. Ofthe 74 surveyed fragments, 66 were located within thelimits established by the Loky and the ManambatoRivers, while eight fragments were selected north andsouth of both river margins, respectively. Actual pres-ence or absence of sifakas was confirmed in 65 of the74 surveyed fragments, of which 44 (59.5%) were posi-tive and the remaining 21 were negative (Fig. 1). Ninefragments where we could not find sifakas were classi-fied as undetermined, since they did not meet the criteriato be classified as negative (Fig. 1). Data analyses showthat the area, where we confirmed sifaka presence,comprises approximately 44,125 ha of forest fragmentsthat vary in size and degree of encroachment. A mini-mum convex polygon that included all known sites ofspecies presence resulted in an overall extent of occur-rence of 88,240 ha (Table 1).

During surveys, we found presence of golden-crownedsifakas outside the geographic limits that were pre-viously suggested for the species (Meyers and Ratsir-arson, 1989; Mittermeier et al., 1994). Presence ofsifakas outside the western edge of the Loky River—inthe three-patch cluster centered around Antanimar-azoko (3�10 S–49�270 E, Fig. 1), was first suggested bylocal villagers during interviews and afterwards it wascorroborated by onsite surveys. Since these patches areisolated from other forests to the west they represent thewesternmost distribution of P. tattersalli. The north andsouth distribution of P. tattersalli is marked by theLoky (12�500 S) and the Manambato (13�190 S) Rivers,respectively, while the furthest East where we verifiedpresence of sifakas was within patches of the Amporahamountain (13�40 S–49�490 E). These geographic bound-aries represent one of the most restricted distributionsof any lemur species (Fig. 1).

3.2. Species abundance

Density estimates were obtained from five sites thatrepresented different forest types. Repeated counts onBinara and Antsahabe, the two highest forests in theregion, yielded no positive observations of sifakas onthe high areas of both forests, and only two sightingson the lowest foothills of Antsahabe. Also, out of the334 sifakas sighted during our study, only two groups(n=6 individuals) were spotted at altitudes between 600and 700 m, with no animals being detected above 700m.a.s.l. Binara and Antsahabe are the only fragments inDaraina that have forested areas above 700 m, and arecent biodiversity survey of Binara also resulted in nosifaka sightings above 700 m.a.s.l. (A.V., personalobservation). Pending further research, our data impliesthat sifakas show a negative selection towards high

Table 1

Criteria met by Propitheus tattersalli based upon IUCN’s Red List Categories and Criteria: version 3.1

Critically endangered Endangered Vulnerable Comments

A. Population reduction

Past decline No decline in the past 10 years

Future decline >80% In three generations Criterion A2ca

B. Geographic range

Extent of occurrence 880 km2 Criterion B1.ab

Area of occupancy 360 km2 Criterion B2.ab

C. Population size �6,100 to 10,000

D. Number of mature individuals �6,100 to 10,000 (Ne�2500 to 4000) Criteria D2b

E. Quantitative analyses N/A

a IUCN, 2001.b This study.

A. Vargas et al. / Biological Conservation 108 (2002) 325–334 329

altitude forests. Therefore, to obtain estimates of spe-cies’ abundance, we only considered data obtained atthree representative sites of deciduous and semi-evergreen forests of altitudes below 700 m.a.s.l. Repe-ated counts yielded consistent results regarding thenumber of groups present in a given area, allowing us todetermine that golden-crowned sifakas occurred at den-sities that varied between 0.18 and 0.29 km2/group.Considering an average of five individuals per group

(Meyers, 1993; Jimenez and Vargas, 2000), minimumand maximum density estimates ranged between 17 and28 ind/km2, respectively. These density estimates arehigher than those reported for P. diadema edwardsi(Glander et al., 1992; Wright, 1995) and P. verreauxiverreauxi (Richard, 1978). Taking into account that,throughout the region, there are approximately 440 km2

of forests available to the species (i.e. forests where weconfirmed the species’ presence), of which approxi-mately 80 km2 are above 700 m.a.s.l., we estimated thatthe potential area of occupancy for the golden-crownedsifaka is 360 km2 (Table 1). Minimum and maximumdensity estimates multiplied by total area of occupancyresulted in total population estimates of 6120–10,080individuals, respectively. Given that only one male andone female reproduce per year in each group (Meyers,1993), effective population size for the species fallsbetween 2520 and 3960 individuals. Our estimates ofoverall abundance are consistent with those presentedby Meyers (1996), who reported a total estimatedpopulation of 8000 golden-crowned sifakas.

3.3. Threats to the species

Interviews and direct observations indicated thatmajor threats to the golden-crowned sifaka includedslash-and-burn agriculture, uncontrolled grass fires,wood extraction for housing and firewood production,logging of precious woods, gold mining, and hunting.This is consistent with previously listed threats to thisspecies (Meyers and Ratsirarson, 1989; Mittermeier etal. 1992, 1994; Randrianarisoa et al., 1999). Slash-and-burn agriculture (tavy), or shifting cultivation, is acommon practice throughout the Daraina region. Plotsfor farming generally yield crops for 2 or 3 years, andneed approximately 10–15 years of fallow in order toreplenish nutrients and become productive again. Tavyin primary forests is more productive than in secondaryforests, and new rice plots need to be progressively cre-ated to meet people’s needs, thus encroaching steadilyon remaining habitat.Uncontrolled grass fires, presumably aimed to clear

pasture and provide forage for cattle, are widespread inMadagascar (Phillipson, 1994). In Daraina, ‘‘fire sea-son’’ takes place primarily in November, and frequentlyoccurs under uncontrolled conditions. Since there is noregulation on distance to forest fragments, fires set to

clear vegetation and promote the growth of pasture canalso destroy natural flora and forest edges, thereforereducing the size of remaining forests overtime. Weobserved significant damage due to tavy and grass fires.Ground proofing of forest fragments that appeared inthe 1994 LANDSAT image revealed that at least 5.5%(n=4) of the forest fragments selected for surveys haddisappeared within the last 6 years. In addition, a sig-nificant portion of surveyed forests fragments presentedvarious degrees of damage due to tavy and grass fires,indicating that these activities pose a significant threatto habitat availability for P. tattersalli.Wood extraction is mostly carried out to build house

frames, pirogues, and for fencing rice fields. Coal andkitay (firewood for cooking) are traditionally producedfrom live and dead wood, respectively, gathered fromthe forest. Throughout the region, the use of kitay ismore commonplace than that of coal, although the lat-ter is preferred when family income permits its acquisi-tion. Information provided by villagers indicated that inmany forest fragments, naturally occurring dead woodis gradually being depleted and the extraction of youngtrees to produce kitay is becoming more common.Freshly cut tree stumps were observed in the majority ofsurveyed fragments, although patches that were close toestablished villages seemed to be subject to greaterimpact. The degree to which exploitation of preciouswoods affects the Daraina region is not well established,but illegal logging of large trees has been occurring inthe forests of Bekaraoka and Binara (authors, personalobservation). Presently, there are no reforestationefforts to counter resource exploitation. A thoroughevaluation of current levels of wood extraction withinthe region, including viable alternatives to amelioratepresent pressures, should be conducted as part of theultimate objective of establishing a protected areawithin the region of Daraina.Gold mining is an activity that mostly takes place

outside forested areas, although it may also occur alongriverbeds within forested areas. Throughout the region,gold mining occurs as small-scale operations, and withinforests it involves digging out large pits near and underthe roots of large trees, an activity that ultimatelydestroys the tree. This has already caused notabledamage to certain riparian forests. During the past dec-ades, most migrants that arrived into the Darainaregion were itinerant gold miners, though apparentlysuch migrations have decreased in the past few years(Rajaobelina, personal communication). But previousattempts to establish a protected area in the region weredenied, partially because they were perceived as apotential obstacle to uncontrolled mining in the region(Meyers, 1996). At current levels of exploitation, goldmining ‘per se’ does not seem to pose a significant threatto P. tattersalli’s survival (Meyers, 1996; this study).Yet, we believe that gold mining actually remains a

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significant potential threat to the region, since it is notpossible to ascertain if new hordes of miners will arrivein the area or if a large commercial company will decideto set up an industrial endeavor in the region.Hunting of P. tattersalli appears to be of limited

extent. Regional beliefs dictate that it is fady (taboo) toeat this species and, although respect for this fady isgenerally honored, immigrant miners do not alwaysrespect local traditions (Meyers, 1996). In general,targeted lemur species for hunting are Eulemur fulvussanfordi, Eulemur coronatus, and Lepilemur spp. (Ran-drianarisoa et al., 1999), and we found lemur traps insome of the surveyed fragments. Interviews revealedthat the species is rarely hunted. In addition, mostsifaka groups encountered during our study seemedunwary of human presence, indicating that respect forthe fady against eating them appears to predominate.Through a multivariate analysis, Jimenez and Vargas

(2000) determined that P. tattersalli was more likely tobe found in large forest fragments (>1000 ha) and thatproximity to large, positive fragments and connectivitybetween patches were important predictors of speciespresence. These results follow classic predictions fromisland biogeography theory regarding the effects ofhabitat fragmentation on wildlife distribution (MacAr-thur and Wilson, 1967; Schafer, 1990). However, a fewdetails indicate that the golden-crowned sifaka might beespecially well adapted to survive in a fragmentedlandscape. For instance, four groups were observed inriparian corridors comprised of single lines of trees ateach side of a creek, and three other groups wereobserved feeding or resting in small clusters of trees(<1 ha) unconnected to nearby forests. One of thesegroups jumped to the ground and crossed more than200 m of savanna to reach the closest forest afternoticing our presence. This, together with similaraccounts reported by local people, suggested that P.tattersalli might be able to cross long distances throughunforested habitat. In addition, the golden-crownedsifaka is not restricted to undisturbed forests, beingalso found around gold-mining villages, inside degra-ded forests and showing, in some cases, a tamedbehavior towards humans. All this information indi-cates that, although P. tattersalli is sensitive to forestdegradation and fragmentation, it is fairly resilient tohuman presence and associated activities, allowing forconservation strategies in a landscape where both,humans and sifakas, can exist together.Illegal logging, tavy, gold mining, and grass fires have

led to habitat destruction and, consequently, to severefragmentation between the Loky and the ManambatoRivers. A recent evaluation of deforestation patterns inthe Daraina region shows that shapes and sizes of mostforest fragments have remained stable during the past50 years (Jimenez and Vargas, 2002). Yet, approxi-mately 5% of small to medium-sized forests have

disappeared during the past 6 years (Jimenez and Var-gas, 2000), indicating a growing increase in humanencroachment. Upon such scenario, P. tattersalli’s pre-sent status quo could rapidly change and, if no efficientprotection action is rapidly taken, the species couldeasily slip into an extinction vortex.

3.4. IUCN Red List status

During the past decade, the golden-crowned sifakahas been classified as a critically endangered species(Mittermeier et al., 1992; IUCN, 1994, 2001). Under thenew IUCN criteria, the species continues to be classifiedas critically endangered based on a potential populationreduction (IUCN criteria A2c), as well as on its limitedgeographic range (criteria B1+2bcd; Hilton-Taylor,2000). Our data show that the species’ present extent ofoccurrence is 880 km2 and, thus, greater than the 100km2 established by the new criteria. Area of occupancyis 360 km2—also significantly greater than the 10 km2

established to meet the critically endangered status(Table 1). In addition, population numbers are wellbeyond the established maximum of 250 animals. Eventhough the golden-crowned sifaka has a very restrictedgeographic distribution in a severely fragmented habi-tat, our data indicate that the species’ classification ascritically endangered under the IUCN ‘‘B’’ criterion isnot warranted (Table 1).Classification as critically endangered under criteria

A2c entails that the species could suffer a ‘‘populationreduction of at least 80%, suspected to be met withinthe next three generations (approximately 27 years forP. tattersalli, P. Wright, personal communication),based on a decline in area of occupancy, extent ofoccurrence and/or quality of habitat’’ (IUCN, 2001;CBSG, 2001). Although fragmentation patterns in theDaraina region have remained stable during the past 50years (Jimenez and Vargas, 2002), the existence of goldand precious stones in the region makes Daraina apotentially dangerous target for mining operations. Inaddition, logging pressures have been continuouslyincreasing since 2001 (authors, personal observation).Recently, the Malagasy NGO Fanamby began toimplement a ‘‘Conservation and Natural ResourceManagement Program for the Daraina Region’’, a pro-gram ultimately conceived to grant protection to thegolden-crowned sifaka and the habitat upon which itdepends, while improving the quality of life of the peo-ple that inhabits the area. At present, however, no for-ests in the area enjoy a legal protection status and, givenMadagascar’s political unrest, the region’s future pro-tection remains uncertain. Considering all availableinformation, we support the IUCN classification of thegolden-crowned sifaka as a critically endangered speciesuntil effective protection measures are in place to ensureits conservation. Yet, we recommend a revision of

A. Vargas et al. / Biological Conservation 108 (2002) 325–334 331

current IUCN categorization of this species in order tore-catalogue it under criterion A2c only.

4. Management recommendations

1. To ensure conservation and long-term survivalof P. tattersalli in such fragmented and complexlandscape, it is important to establish—in thenear future—a Network of Protected Areas.Three forest complexes stand out as the mostrelevant for golden-crowned sifaka conservation:(A). Bekaraoka and neighboring connected frag-ments to the west (Ambilondamba) constitutethe species’ central reservoir (Fig. 1). These for-ests probably harbor the largest and most con-tinuous extension of optimal dry-lowland habitatfor the golden-crowned sifaka, and are currentlyexperiencing the highest impact from humanpopulations living around the village of Daraina.(B). The large forest tracts of Binara-Antsahabe-Ambohitsitondroina, along with the network ofconnected forests north of the Manambato Riverconstitute P. tattersalli’s southern reservoir(Fig. 1). This complex includes the largest tractsof undisturbed forests within the region, butmuch of this area seems to hold suboptimalhabitat for P. tattersalli due to its high elevation.The southwest fragments of Bobankora, Amp-oetany, and Ankaramy constitute a smaller net-work of forests that harbor excellent low- tomid-altitude semievergreen forest, which con-stitute prime habitat for the species. In addition,these forests are transitional between dry andhumid domains, and harbor a unique vegetationassemblage with no analog in Madagascar. (C)The northern forest complexes of Antsaharaingy,Ampondrabe, Antanifotsy, and Benanofy con-stitute the species’ northern reservoir (Fig. 1).Their vegetation communities are also distinctand they should be included as part of the net-work of protected areas.

2. The existence of a highly fragmented landscape,lacking large forest tracts and surrounded bysignificant human presence, precludes the designof a single large reserve. Thus, any regionalstrategy directed to conserve local forests andgolden-crowned sifakas should include what wedefine as ‘‘Conservation Gradients’’. Such con-cept implies the design and enforcement of dif-ferent degrees of protection throughout variousforests fragments present in the region. Accord-ingly, some areas of the earlier mentioned forestscomplexes should be included within a NationalPark or Nature Reserve, while other forestsshould be designated as Foret classe or Regional

Reserve, where sifakas can share their habitatwith some human activities. Conservation ofsmall riparian forests (corridors) could rely oncommunity agreements and incentives, whilesome forests that have low potential for con-servation could be used for extraction purposes.

3. We recommend the implementation of a FlagshipSpecies Program utilizing the golden-crownedsifaka as a catalyst for regional biodiversity con-servation. This program should be implementedas support to the ongoing ‘‘Initiative for Con-servation and Natural Resource Management inthe Daraina Region’’, a program established bythe Malagasy Association FANAMBY sinceJune 2001. The Flagship Species Program shouldinclude management, education/outreach, andresearch actions, with management actionsfocusing primarily on the design and imple-mentation of a Protected Areas Program and theuse of incentives for conservation. Education andoutreach activities should promote the golden-crowned sifaka’s endemic condition as a sourcefor local pride and the species’ ecotourism poten-tial as a reason for local involvement in its con-servation. Finally, research activities should focuson metapopulation studies. Priority questionsthat need to be addressed in order to implementappropriate management actions include: meta-population dynamics, demography, potentialgenetic effects due to geographic isolationbetween populations, and the importance oflarge, undisturbed forest tracts on the speciessurvival.

5. Summary and conclusions

1. Propithecus tattersalli’s distribution is restrictedto the region comprised between the Loky andManambato Rivers, with the exception of a fewgroups residing in a small forest cluster on theother side of the Loky River. Golden-crownedsifakas dwell in forest types that vary from dry-deciduous to semi-evergreen and pre-montaneevergreen forests, and they have never beenreported at elevations above the 700 m.a.s.l.

2. Throughout the 360 km2 of forests available tothe species, the golden-crowned sifaka is abun-dant and found in fragments of variable sizes.Total population estimates range from 6100 to10,000 individuals, with an effective populationsize of �2500 to 4000 sifakas.

3. The species appears to be distributed as a com-plex metapopulation, with three large popula-tions that contain smaller subpopulations withinthem (Fig. 1).

332 A. Vargas et al. / Biological Conservation 108 (2002) 325–334

4. P. tattersalli seems to be fairly resilient to humandisturbance. This adaptable behavior is likely toallow the species to survive in a fragmentedlandscape as long as human disturbance does notincrease significantly and that large forests tracts(i.e. larger than 1000 ha) are not destroyed.

5. The golden-crowned sifaka can be classified as acritically endangered species under criterion A2cof the IUCN’s new Red List Categories andCriteria. Its long-term survival depends on aprecarious status quo, and major potentialchanges in local land use (e.g. beginning ofindustrial gold-mining) could lead the entirepopulation into an extinction vortex.

6. The golden-crowned sifaka is both a reason anda resource to start a regional process for bio-diversity conservation in the Loky-Manambatoregion. It is a reason because it is endangeredand endemic to a small area in northeast Mada-gascar. And it is a potential conservationresource because it is charismatic and can easilyattract ecotourism attention.

Acknowledgements

This project would not have been possible without thesupport and enthusiasm of Serge Rajaobelina andthe FANAMBY crew, who laid the ground to allow usto conduct research in Madagascar. We thank the pro-ject’s field assistants Rindra Andriambola, EmilienneRasoazanabary, Romule Rakotondravony, Abel Razo-najaona, Margarida Fernandes, and Luka Clarke fortheir dedication while searching for golden-crownedsifakas. Financial support for this project was providedby Conservation International, through a grant fromthe Margot Marsh Biodiversity Foundation. Additionalfunding was granted by the Society for the Conserva-tion and Study of Endangered Species and Populations(Germany), Conservation des Especes et des Popula-tions Animales (France), Idea Wild (USA), and theOregon Zoo Conservation Foundation (USA). The‘‘Project D’Appui de Gestion de L’Environnement’’supported the costs of two Malagasy students, TafitaAndriamanantena and Setra Andriamanaitra. We wantto express our gratitude to Bill Konstant, who believedin this project from the beginning and supported ourefforts every step of the way.

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