American Journal of Primatology 18285-301 (1989) Population Survey of Macaques in Northern Sulawesi J. SUGARDJITO', C.H. SOUTHWICK', J. SUPRIATNA3z4,A. KOHLHAAS', S. BAKER5, J. ERWIN', J. FROEHLICH3, AND N. LERCHE7 'Centre for Research in Biology, LZPZ, Kotak Pos 110, Bogor, Indonesia; 'Department of Environmental, Population and Organismic Biology, University of Colorado, Boulder; 3Department of Anthropology, University of New Mexico, Albuquerque; 4Department of Biology, University o Indonesia, Jakarta, Indonesia; 5Department of Psychology, University of Georgia, Athens; bfDepartment of Biology, American University, Washington, D.C.; 7CaliforniaPrimate Research Center, Davis A field survey of 25 sites in Sulawesi Utara (north Sulawesi) in 1987 and 1988 found macaques in 16 of these sites. The most viable population of Macaca nigra was found in the Tangkoko reserve a t an estimated density of 76.2 monkeys/km2,which is less than one-third the abundance reported in the late 1970s by the MacKinnons. The adjacent reserves of Batuangus and Duasudara had only 22 monkeys/km2,yielding a population estimate for these three contiguous reserves of only 3,655 individuals. Macaca nigrescens were found in the central and western portions of Dumoga-Bone National Park in densities of 15.5 and 16.4 monkeys/km2, significantly below the density of 27/km2 reported by the MacKinnons. The more peripheral areas of Dumoga-Bone had only 8.15 monkeys/km2, yielding a population estimate of M. nigrescens in Dumoga-Bone of less than 34,000. Our total population estimate for M. nigra and M. nigrescens combined is less than 50,000 individuals, which is considerably below that reported in recent literature. M . hecki were observed in only two locations, Tangale and Panua Reserves, at low densities of 3.3 to 5.2 monkeys/km2, suggesting its range and abundance have declined since the observations of Groves (Pp.84-124 in THE MACAQUES: STUDIES IN ECOLOGY, BEHAVIOR AND EVOLUTION. D.G. Lindburg, ed. New York, Van Nostrand Reinhold, 1980). Several factors have contributed to population decline in these species: habitat shrinkage, increasing human population pressure, and drought conditions. Group sizes were significantly smaller in our study than in previous ones, and we found a shortage of juveniles and infants. Key words: Indonesia, populations, conservation INTRODUCTION This paper presents field census data on the abundance and distribution of three species of macaques (Macaca nigra, the Celebes crested or black macaque; M. Received for publication November 29, 1988; revision accepted May 31, 1989. Address reprint requests to Dr. Charles H. Southwick, Department of EPO Biology, Box B-334, University of Colorado, Boulder, CO 80309. 0 1989 Alan R. Liss, Inc. 286 I Sugardjito et al. TABLE I. The Sulawesi Macaques Species Common name M. hecki Crested macaque or black macaque or Celebes ape Gorontalo macaque or Celebes ape Heck‘s macaque M. tonkeana M . maura M. ochreata M . brunnescens Tonkean macaque Moor macaque Booted macaque Muna-Butung macaque Macaca nigra M . nigrescens General distribution Eastern North Sulawesi Central North Sulawesi Western North Sulawesi and Central Sulawesi Central and South Sulawesi South Sulawesi Southeast Sulawesi Muna and Buton Islands, Southeast Sulawesi nigrescens, the Gorontalo macaque; and M. hecki, Heck’s macaque) in northern Sulawesi, Indonesia. Forest surveys were conducted from October 1987 to June 1988, and were concentrated in the geographic ranges of M . nigra and M . nigrescens. The macaques of Sulawesi are endemic and highly speciated in a relatively small geographic area. The most thorough taxonomic studies by Fooden [19691and Albrecht [1977, 19781 divide the Sulawesi macaques into seven distinct species of Macaca (Table I). This classification is accepted by more recent studies of Brotoisworo 119821, Kawamoto et al. [19821, Takenaka et al. l1987a,bl, and Hamada et al. . Collectively these studies involve genetic analyses of population differences in morphology, blood hemoglobin patterns, and enzyme biochemistry. Groves [19801, however, classifies the Sulawesi macaques into only four species, with nigra and nigrescens as subspecies of nigra, and brunnescens and ochreata as subspecies of ochreata. Older classification systems place the Sulawesi macaques into two genera, Macaca and Cynopithecus [Laurie & Hill, 1954; Napier & Napier, 1967; and Hill, 19741, with the genus Cynopithecus applied to M. niger. Our own observations, while not taxonomically definitive, are compatible with the seven-species classification of Fooden , with all seven species in the genus Macaca. We feel more taxonomic work is needed, however, in areas of potential sympatry and hybridization. Regardless of which classification is finally accepted, there are more species of macaques in Sulawesi than in any comparable land area [Eudey, 19871. If the seven-species system is accepted, Sulawesi has 37% of the species in the genus Macaca on less than 1%of the land area occupied by the genus. The macaques of Sulawesi are also unique in being more highly derived than any other members of the genus. This is especially true of M. nigra and M . nigrescens. Not only are they virtually tailless (a condition which led to their popular designation as the “Celebes Apes”), but they have a more prognathic and baboonlike craniofacial structure than any of the other macaques (Fig. 1).They also show in captivity a prevalence of human-like adult diabetes [Howard, 19881. Despite these unique morphological and physiological features, the Sulawesi macaques have received relatively little field study. The taxonomic studies of Fooden  and Albrecht [1977, 19781 were done primarily on captive and museum specimens. Groves’s [19801 work involved only 2 months of field studies. Investigations by Bismark , Brotoisworo , and Watanabe and Brotoisworo 119821 were also short-term, and those by Kawamoto et al. , Takenaka et al. [1987a,bl involved only studies of blood chemistry on captive animals. Hamada et al. 119881 have recently continued studies in comparative morphology. Populations of Sulawesi Macaques I 287 Fig. 1. Macaca nigra female and infant in the Surabaya zoo John and Kathy MacKinnon undertook extensive population surveys in the late 1970's, and their work forms an excellent baseline on population distribution and abundance, especially of M. nigra and M . nigrescens. Kathy MacKinnon also did more detailed studies on the ecology and behavior of M. nigra at the Tangkoko Reserve, but this work is largely unpublished (MacKinnon, pers. commun.). Since the population surveys of the MacKinnons were done 8-10 years ago and the ecology of Sulawesi has changed rapidly [Whitten et al., 19871, the purpose of this study was t o obtain a current view of monkey populations in north Sulawesi. This research is part of a larger program involving field research in central, southern and southeastern Sulawesi to study M. maura, M . tonkeana, M . ochreata, and M . brunnescens. METHODS Site North Sulawesi, also known as Sulawesi Utara, is the northeastern peninsula of Sulawesi, formerly known as the Celebes. It is just above the equator, extending from 0.4" to 1.8"North latitude, and 121.1' to 125.5' East longitude (Fig. 2). The peninsula is approximately 50 to 100 km in width, extending approximately 450 km from west to east. The topography is volcanic with elevations reaching 2,207 m interspersed with broad valleys and dissected by many rivers. The climate is moist 288 I Sugardjito et al. 1 1 1 - 2- N TangkokoBotuangusDuasudara A \ 0 Lout Sulowesi 80 hrn M ' U 8, Manemba- Nemba SKALA l2.000.000 Pondas Tongale Tulabolo Panua Dumcqa- Bow-Taraut Tambun Dumoga-Bone Hdqs Pinolosian Matayangan Molibagu Equator I 1220 _ _ _ Fig. 2. Elusan 124' 123' _ _ _ ~ ~ ~ 125' ~ Northern Sulawesi (Sulawesi Utara) showing study sites. tropical, with typical annual rainfall amounts varying from 1,000 to 4,000 mm. Heaviest rainfalls occur from November to May. The original vegetation is tropical forest, with a rich assemblage of more than 300 species of trees. Primary forest is characterized by a high (40-50 m) semiclosed canopy, a high percentage of buttressed trees, many lianas, and a relatively open or sparse understory (Fig. 3). Secondary forest, occurring in cut-over areas and natural gaps, has an open or sporadic canopy, dense intermediate layer, and abundant ground cover. Sulawesi has a rich flora and fauna containing elements of both Asian and Australian biota and a high component of endemic animals. The most notable large animals include the anoa (Bubalus depressicornis and B . quarles), a small forest bovid; the babirusa (Babyrousa babirussa), a unique wild pig; the cus-cus (Phalanger ursinus and P. celebensis), an arboreal marsupial; the maleo fowl (Macrocephalon maleo); several species of large hornbills; and the macaques. Ninetyeight percent of the mammals, excluding bats, are endemic. The human population of Sulawesi Utara numbered 2,234,508 in 1984, an increase of 68%since 1961. The population growth rate exceeds 2% per annum, and 41.2% of the population is under 18 years of age. The predominant occupation is farming, with coconuts, cloves, and rice as major crops. Data Collection From October 1987 to June 1988 we conducted forest surveys in 25 locations, 20 of which were in national parks or nature reserves (Table 11; Fig. 2). In each location, we conducted systematic walks in forest habitat, mostly on trails, but also on cross-country compass bearings. These were done with local field guides who knew the terrain and wildlife. Field observations were made from 6:OO A.M. to 6:OO P.M., concentrating in early morning and late afternoon. Field sites were selected based on the best chances of finding monkeys, as ascertained from opinions of local guides and existing scientific reports. Special emphasis was given to the Tangkoko- Populations of Sulawesi Macaques I 289 Fig. 3. Primary forest habitat of M. nigru in Tangkoko Reserve. Batuangus-Duasudara Reserves and Dumoga-Bone National Park (Fig. 2) since these sites had been the focus of previous studies. Field methods followed the procedures of Southwick and Cadigan  in Malaysia, and those recommended by the primate field manual of the U S . National Academy of Science [Eisenberg et al., 19811. These are essentially the same field survey methods used by the MacKinnons in the late 1970s. This involved slow, quiet walking, with frequent stops to scan and listen for sounds. Most of the walking survey was on forest trails, but about 25%was forest cross country without established trails. Our average detection distance in this study was 51.2 m (measured in direct line of sight), which we rounded to 50 m, thereby covering a transect strip 100 m wide on either side of the trail. This varied locally depending on vegetation and terrain, but 50 m represented the typical range of primate detection. Hence, 100 m of trail walking was the equivalent of surveying 1 ha; 1 km of forest survey equated to 10 ha, and 10 km equated to 1 km2. Only monkeys seen were counted, and when a monkey or a group was spotted, an effort was made to obtain a count or best possible estimate of group size or party size. It was usually difficult or sometimes impossible to get a completely accurate count of total group size due to the flight distance of the monkeys (often 30 to 40 m), their relatively shy behavior, and their tendency to hide or disappear in dense foliage. The term “party” is more vague than “group,” and does not imply that a total group was counted. Throughout this paper, the term “group” will be used, but this is not intended to imply that we always measured total group size and structure in these species. In a few areas, especially the Toraut area of Dumoga-Bone National Park, the monkeys were not so shy, and could be observed often from 15 to 20 m. Even in shy groups a good progression count was sometimes obtained when a group moved or 290 I Sugardjito et al. TABLE 11. Forest Sites Surveyed in North Suiawesi, October 1987-May 1988 Field site Tangkoko Batuangus Duasudara Manembo-nembo (N) Manembo-nembo (S) Gn. Ambang Dumoga-Bone-Hdqs Dumoga-Bone-Toraut Dumoga-Bone-Tapaku-Lintang Dumoga-Bone-Tambun Dumoga-Bone-Lombongo Dumoga-Bone-Tulabolo Dumoga-Bone-Boneponte Tangale Panua Batuputih Danowudu Gn. Klabat Elusan Pondos Modayaq Bedaro Pinolosian Matayangan Bunbungon Monkeys observed" +++ ++ ++ ++ ++ 0 ++ +++ + + ++ + t t + Species M . nigra M . nigra M . nigra M . nigra M . nigra M . nigrescens M . nigrescens M . nigrescens M . nigrescens M . nigrescens M . nigrescens M . nigrescens M . hecki M . hecki 0 0 0 0 + 0 + 0 0 0 M . nigra M . nigra Protected or unwotected Protected Protected Protected Protected Protected Protected Protected Protected Protected Protected Protected Protected Protected Protected Protected Protected Protected Unprotected Unprotected Unprotected Unprotected Unprotected Unprotected Unprotected Unprotected a + + + , monkeys abundant, over 50/km2; + + , monkeys common, but not abundant, 10-40km2; +, monkeys present but rare, less than 10/km2;0, monkeys not seen. jumped across a critical crossing from one tree to another. Group size estimates were facilitated and cross-checked by the presence of three or four observers in most of our field parties. We accomplished 415 km of original forest survey. This did not include returning on the same route, or walking the same trail unless a t least one month separated the surveys. Also, it did not include walking through secondary scrub or semi-cultivated areas enroute to good forest habitat. After taking a 4-wheel drive track as far as possible, we often had to walk 5 to 10 km to get to suitable forest. Our total footwork in this study exceeded 1,200 km, and our total 4-wheel drive travel exceeded 5,000 km. RESULTS Of the 25 sites visited (Fig. 2, Table 11)monkeys were found in 16 of these sites: they were seen in 14 of 17 protected sites (82%),but in only 2 of 8 unprotected sites (25%) (Fig. 4). The 25 sites visited are logically grouped into 11locations by virtue of habitat or proximity (Table 111). Monkeys were found in 10 of these locations-all except Gunung Klabat near Manado. In Gn. Klabat monkeys were reported by reliable eyewitness observers, but we did not see them there in three visits totalling 19.5 km of forest walking. This mountain is a reserve forest, and although wildlife is Populations of Sulawesi Macaques I 291 loo r 135 N 30 80 125 f 0 60 40 20 d: U 0 P U P P = PROTECTED FORESTS U = UNPROTECTED FORESTS Fig. 4. hevalence and density of macaques in protected and unprotected forests in northern Sulawesi, 198788. Densities for only those forests containing macaques. TABLE 111. Forest Locations, Area Surveyed, and Population Densities, 1987-1988 Location Tangkoko [central] Batuangus, Duasudara Gn. Klabat Manembo-nembo Gn. Ambang and Modayaq Pondos and Elusan Dumoga-Bone [Toraut, Hdqs.] Dumoga-Bone [East. Peripheral] Dumoga-Bone [Gorontalo] Panua [Marisal Tangale km km2 Groups Groups/ x group Population surveyed surveyed seen km2 size km2 82.5 30.9 19.5 6.5 8.25 3.09 1.95 0.65 42 4 0 3 5.1 1.3 0 4.6 15.0 16.7 0 8.3 22.5 20.0 2.25 2.0 1 1 0.4 0.5 16 1 131.6 13.2 28 2.1 7.3 27.0 2.7 1 0.4 22 22.5 31.0 21.0 2.25 3.1 2.1 6 1 2 2.7 0.3 0.95 6.2 16 3.5 Species 76.2 22.0 0 38.5 nigra nigra 7.1 0.5 nigra nigra 15.5 8.15 16.4 5.2 3.3 nigra nigrescens nigrescens nigrescens hecki hecki legally protected, we classified Gn. Klabat as an unprotected area since it does not have resident rangers or forest guides who patrol the area. M . nigra were found in eastern Sulawesi Utara, east of Kotamobagu and Modayaq; M . nigrescens in central Sulawesi Utara, from Tambun to Lombongo and Gorontalo; and M. hecki west of Gorontalo. These distribution patterns agree in general with those described by Fooden  and Groves [19801, although Groves reported sympatric zones of species overlap which no longer seem to exist. We 292 / Sugardjito et al. TABLE IV. Patterns of Abundance and Total Population Estimates General population status High population density Moderate population density Low population density Location Tangkoko (central) Batuangus, Duasudara Manembo-nembo Dumoga-Bone, (Toraut, Hdqs.) Dumoga-Bone (Gorontalo) Dumoga-Bone (peripheral) Gn. Ambang and Modayaq Pondos and Elusan Panua (Marisa) Tangale Size of area (ha) Population density (No./km2) Maximum potential population (individuals) 3,196 76.2 2,435 5,549 6,500 22.0 38.5 1,220 2,502 69,675" 69,675 15.5 16.4 10,800 11,427 139,350 8,638 100,000b 45,000 125 8.15 7.1 0.5 5.2 3.3 11,357 613 500 2,340 7 "Dumoga-BoneNational Park is 278,700 ha. The figures in this line and the next two lines are based on the assumption that 25% of this area is central (Toraut),25% is western (Gorontalo), and 50% peripheral. bEstimate. found a gap of approximately 30 km separating M . nigrescens and M . hecki in the Gorontalo region. The boundary of M . nigra and M . nigrescens is not clear, but apparently occurs somewhere near the Kotamobagu-Modayaq-Bedaro region or between Kotamobagu and Pinolosian. We found M. nigra near Kotamobagu, and some villagers described monkeys resembling M. nigra, whereas others described M. nigrescens. We also found an M . nigra pet monkey outside Molibagu which the owner said had been captured near Molibagu, but the only wild monkeys we saw near Motayangan or Molibagu were M. nigrescens. There is still the possibility of species overlap between M . nigra and M . nigrescens distributions, and even of hybrid animals, but we could not confirm this. In general, we found scattered and isolated populations of one or the other species with no specific forests containing more than one species. Population Abundance and Densities Only one location (Tangkoko) showed an abundant population with a density of more than 50 monkeys/km2 (Table 111). In 82.5 km of forest survey, we observed groups or parties on 42 occasions at Tangkoko, a density of 5.1 groups/km2and 76.2 individuals/km2 (Table 111). The Toraut site in Dumoga-Bone National Park also showed an abundant population, approximately 5 groups or parties and 50 individuals/km2,but only in a very limited area of 2 km2. When combined with other adjacent sites near the park headquarters, the overall density in the main portion of Dumoga-Bone was only moderate (2.1 groups and 15.5 individuals/km2). Table IV shows the general distribution of population density, with only Tangkoko showing high density (>50 individuals/km2),4 locations showing moderate densities (10-40 individuals/km2), 5 locations showing low density (<10 individuals/km2), and one location with no monkeys found in our survey (Gn. Klabat). In areas where monkeys were found, group or party density varied from 0.32 groupsLkm2in Panua Reserve f M . hecki) to 5.1 groups/km2in Tangkoko f M . nigra). Average group or party sizes varied from 15.0 in Tangkoko (range, 2 to 58) to 3.5 Populations of Sulawesi Macaques I 293 121 N E Y 8 \ v) a 3 x Group Frequency - 0 in M nigro 0 M nigrexens % CHANGE -49.0 +23.5 % CHANGE -49.3 -54.4 z 0 Z Group Size P 3 0 m 5 llL 0 10 0 > .U C 1978 n 1988 Fig. 5. Group frequencies and average group sizes of M . nigru and M . nigrescens, 1988 compared to 1978. (1978 data from MacKinnon 1198311. in Tangale (range, 2 to 5). In general, group sizes were small. They were largest in the Tangkoko-Batuangus-DuasudaraReserves, averaging 15-16, but were only 6-8 monkeys/group in Manembo-nembo and Dumoga-Bone except for single groups of 16-22 individuals. In the major areas of monkey abundance, TangkokoBatuangus for M . nigra, group size averaged 15.0; and in the major area of abundance for M . nigrescens, Dumoga-Bone, group size averaged only 7.3. These are small groups compared to earlier data (Fig. 5), and compared to other macaque species. Population distribution in the two major areas of monkey abundance, Tangkoko and Dumoga-Bone, also showed patchiness, with central or core areas near the Reserve Headquarters showing the highest population densities, whereas peripheral areas showed lower lower population densities. In Tangkoko, the central area near the site known as “MacKinnon’s Cottage” had an estimated population density of 5.1 groups and 76.2 individuals/km2 (of M. nzgra), while the peripheral areas of Batuangus and Duasudara, even though they were adjacent and contiguous forest, had an estimated population density of only 1.3 groups/km2 and 22.0 individuals/km2 (Table 111). In Dumoga-Bone National Park, the central area near the park headquarters and the Toraut Biological Research Station had 2.1 groups and 15.5 individuals/km2 (of M. nigrescens). In contrast, peripheral areas of contiguous forest had only 0.4groups and 8.15 individuals/km2. There was considerable evidence that peripheral areas had less ranger patrol- 294 I Sugardjito et al. 1978 1988 Tangkoko Macaco nigfo = Dumoga-Bone M nigfescens Panua M heck; Fig. 6. Estimated population densities at Tangkoko, Dumoga-Bone, and Panua, 1978-1988 (1978data from MacKinnon [19831). ling and more disturbances than central areas near reserve headquarters. Disturbances included logging, rattan collecting, hunting, and small-animal trapping. Population Composition Age and sex ratio data were obtained on only a few groups because fleeting views of many individuals did not permit completely accurate classifications. Data on a sample of 131 individuals of M. nigra and M . nigrescens show an adult malefemale ratio of k2.1 (i.e., 32.1% of the adult population was male; 67.9% was female). The age ratio of 174 individuals showed 75.3% of the population as adult; 24.7% as immature. The infanttadult female ratio showed only 14.6% of the adult females with infants. Many groups had no infants, and some groups had neither infants or juveniles. Population estimates of the maximum potential populations in 1988 are 3,655 M. nigra for the Tangkoko-Batuangus-DuasudaraReserves, 2,502 M. nigra for Manembo-nembo; 33,584 M. nigrescens for the whole of Dumoga-Bone National Park; 2,347 M. hecki in Panua and Tangale Reserves; and finally, only small and scattered populations of all three species outside the reserves (Table IV). DISCUSSION Substantial monkey populations were found only in the largest and best-protected reserves: Dumoga-Bone, Tangkoko-Batuangus-Duasudara (grouped together because they represent one contiguous forest area), Panua, and Manembonembo. We are not confident of the Manembo-nembo population estimate, however, because of its small sample size and large extrapolation. We fear that, by chance, we may have found groups easily in a short distance. We have greater confidence in the Dumoga-Bone and Tangkoko estimates, based on five separate visits each, and more adequate survey samples. From surveys in Tangkoko-Batuangus-Duasudara and Dumoga-Bone, several major conclusions emerged. The population density of macaques was high in Tangkoko, but less than one-third of that observed by the MacKinnons 10 years ago [WWF, 1980; MacKinnon, 19831 (Fig. 6). Our field methods and population estimates were the same as those used by the MacKinnons. MacKinnon found 10 Populations of Sulawesi Macaques I 295 groupskm' with an average group size of 30; hence, a population density of 300 individuals/km'. In the same area, we found only 5.1 groups/km2,with an average group size of 15.2, hence, a total population density of 76.2 (Fig. 6). In two completely independent surveys in 1987, Supriatna and a team of 5 first estimated 80 monkeyskm', and Sugardjito, Southwick, and a team of 5 others first estimated 87 monkeydkm'. Only in 3 subsequent visits in 1988 did we have to revise these estimates downward to 76.2 monkeys/km'. We do not believe that we missed monkeys, nor did we have any seasonal bias since we sampled before, during and after the rainy season. Hence, we believe there has been a true population decline in the past 10 years. There is a special problem of interpreting group size data in these species, but this does not affect our total population density estimates. Since our average group sizes were only 7-15 monkeys, but we occasionally saw groups as large as 58, we do not know if true group size is large and we were usually seeing only small foraging parties, or, conversely, if true group size is small, and we occasionally saw large feeding aggregations that happened to come together for short periods. We suspect the latter, but this will require further work. In other words, we believe it is likely that these species show a fission-fusion type of group organization. This would not affect our total population density estimates since we were counting parties of monkeys seen, and these would either represent many small groups, or fewer large groups. The population decline observed in Tangkoko was even more evident in Batuangus and Duasudara. These areas are continuous with, but peripheral to, Tangkoko. They lack frequent patrolling by forest rangers, however, and they are also fringed by greater human population density. These peripheral areas have greater human disturbance in the form of hunting, wood cutting, rattan collecting, and small animal trapping. As a result, they have fewer monkeys, only 22.0/km2. The total population estimate of M. nigra for Tangkoko-Batuangus-Duasudara is only 3,655 individuals, a very different figure than the estimate of 26,235 which would be obtained by extrapolating the MacKinnon density estimate to the entire Tangkoko-Batuangus-Duasudarareserve. This type of extrapolation has been done by Whitten et al. [19871 when he estimated a total population figure of 144,000 for Macaca nigra. This same figure has also been republished by the MacKinnons [19871 based on their own data taken nearly 10 years ago. Both Whitten et al. and the MacKinnons combined M. nigra and M . nigrescens in their estimate, however. Our own population estimate for M . nigra is under 6,000, and for M . nigrescens it is under 40,000. This will be discussed later under conservation status and needs. In the central headquarters area of Dumoga-Bone, we found more groups (2.lkm') of M. nigrescens than the MacKinnons (1.69 groups/km'), but we found a much smaller average group size (7.3 compared to 16.0) (Fig. 5). Hence, population density was only 15.5/km2in our study in the Toraut and Headquarters area of Dumoga-Bone compared to 27.0km' in the MacKinnon's study (Fig. 6). Although we could not obtain sex and age counts on all groups in DumogaBone, we could readily detect a shortage of infants and juveniles. Seventy-five percent of all monkeys seen were adults. Populations of Macaca rnulatta and M. fascicularis with normal reproduction and survivorship should have 50% of the population as infants and juveniles [Southwick et al., 1980; Wheatley, 19801. The implication of this finding is that either reproduction of the Sulawesi monkeys has been reduced in recent years or mortality of infants has increased. The population decline in Dumoga-Bone has affected group size rather than the numbers of groups. This is reminiscent of the population decline of howler monkeys on Barro Colorado Island, Panama, in the late 1940s where a population 296 I Sugardjito et al. stress (in that case, a yellow fever epidemic) resulted in a sharp decline of group size, but no change in the number of groups [Collias and Southwick, 19521. These two examples illustrate the traditional stability of primate groups in face of ecological stress, but they also show vulnerability to loss. We believe that two types of factors are involved in the decline of M . nigra and M. nigrescens populations in the past 10 years. First of all, hunting and other forms of disturbance are clearly decreasing monkey populations. Although these macaques are protected by Indonesian law, trapping and hunting continues for the pet trade and for food. Pet monkeys are common in north Sulawesi-they may be seen in virtually every town and many villages. We found traps for monkeys in several areas, even within Tangkoko reserve. Monkeys are also trapped and shot for food by many local people. This is especially true of crop-raiding monkeys which live along forest edges and move out to neighboring gardens and plantations to feed on bananas, papayas, mangoes, and garden crops. Local people who kill these monkeys have no concept of their scientific importance. Secondly, we believe that recent droughts have been a factor in population decline. Sulawesi has had two drought years in the 1980s-1982 and 1987. Since 1982, the rainfall at Bitung and Airtembaga, the two closest weather stations to the Tangkoko-Batuangus-Duasudarareserves, was 49.7% below the 23-year average for the Manado area (Figs. 7,s). The average rainfall for Manado over the past 23 years was 3,120 mm (taken at Manado Airport), whereas in 1982, the Bitung Station registered only 1,069 mm (65.7% below normal), and in 1987, the Airtembaga Station, which is on the edge of Bitung slightly closer to Tangkoko, registered only 527 mm of rain (83.1% below normal). These drought conditions were part of the broad El Niiio drought effect from 1982 to 1987 which affected the western Pacific region from Australia to Borneo. A plantation owner near Manado told us that 1987 was the driest year he could remember in 45 years of agricultural work. In October 1987, forest conditions were extremely dry, and fires were common. We were delayed in entering Tangkoko in mid-October because numerous forest fires were still burning. These were of both natural origin from lightning strikes, and of human origin from slash and burn agriculture around the edges of the parks. Since these macaques are primarily frugivorous, extremely dry conditions could have impacted monkey populations unfavorably by reducing fruit yields of forest trees. Although we have no direct data to prove this, very dry forest conditions were obvious. Shortages of natural food could have reduced either birth rates or infant survival rates. Both processes occurring in 1982 and 1987 would have resulted in the very low numbers of juveniles and infants which we observed. Low infant numbers might also result from selective trapping since infants are favored as pets. However, infants are obtained by trapping or even killing the mother, so this should not be responsible in itself for the low infant to female ratios seen. Also adults are most often shot for food, so this would further reduce the number of adults. Although the drought remains only a hypothetical explanation of the population decline, it suggests the need for more detailed ecological studies of monkey populations in relation to weather conditions, forest ecology, and fruit production. Population Status and Conservation Needs The population status of the macaques of north Sulawesi is now more endangered than indicated by the previous reports of the MacKinnons [1983,1987], and by the review of Whitten et al. 119871. We believe that M. nigra is particularly Populations of Sulawesi Macaques I 297 + - n E E Y .-mr CT -cp Ir !jooo 4000 t b MANADO -0- AERTEMBAGA i = 3120 n 2000 3 1000 U 0 1960 b + MANADO -0- AERTEMBAGA 1970 1980 1990 Year Fig. 7. Annual rainfall at Manado and Airtembaga,near Tangkoko-Batuangus-Duasudarareserves from 1965 through 1987. (Data courtesy of Mulyadi Susanto, Head, PHPA Office, Manado.) vulnerable. If it is indeed a separate species, as proposed by Fooden [19691, Albrecht , and Takenaka et al. [1987a,b], and as we believe it to be from our own ecological observations, it is in a precarious position. Its largest population is in the Tangkoko-Batuangus-Duasudarareserves, but even here we estimate less than 3,700 individuals. This area is subject to increasing human encroachment, and it is an isolated area surrounded on two sides by the ocean and on all other boundaries by human habitations and/or cultivation. It is clearly vulnerable to increasing ecological stress such as drought or forest fires. A volcanic eruption from any one of its three mountain peaks, or even a shift in forest ecology, could imperil its monkey populations. Yet these reserves are absolutely essential for the continued survival of M. nigra. M . nigra occur elsewhere in Sulawesi Utara, but the populations are small, scattered, and isolated. Most are hunted and survive in shrinking habitats. The only other significant population shown by our data occurs in Manembo-nembo 298 I Sugardjito et al. reserve, but we feel our extrapolations from a small sample may give an overly optimistic picture. On just two visits to Manembo-nembo, we found monkeys near the forest edges. These edges were difficult to reach after several kilometers of cultivation and slash. Hunting and trapping of monkeys is common around Manembo-nembo as it is in most unprotected parts of Sulawesi Utara. Since trapping of monkeys is common in Sulawesi Utara, especially if they are caught raiding crops at forest edges, and these monkeys are often eaten, a conservation program to save these monkeys and reimburse farmers would be highly desirable. The Forestry Department of Sulawesi in Manado has suggested that confiscated monkeys, and monkeys trapped as crop raiders be taken to forest areas such as Gn. Klabat, if their protection could be assured, or they could be released on an island reserve such as the remaining forest on Lembeh Island just offshore from Tangkoko-Batuangus. In this latter location, they could be protected and provisioned for conservation. We believe that every effort must be made to protect the Tangkoko-BatuangusDuasudara reserves, and Manembo-nembo as well. It would be desirable to expand them if at all possible, and, in any case to increase their protective surveillance. M . nigrescens is in a somewhat safer population status than M. nigra because it inhabits a larger protected area, Dumoga-Bone National Park. With the vast size of this park (278,700ha), we estimate a total population of M . nigrescens in the park as slightly under 34,000 (Table IV). As with M . nigra, populations outside the parks are small, scattered, and not necessarily viable. In terms of survival into the 21st century, none of these unprotected populations can be counted on for continued existence. Even Dumoga-Bone National Park faces several threats. Many of the usual problems of wood-cutting, rattan collecting, hunting, and animal trapping occur within the boundaries of Dumoga-Bone. In addition, a new road is being built along the park’s eastern boundary from Dumoga to Inobonto, and this will bring increased disturbance to this part of the park. Furthermore, gold has been discovered in the center of the park, and this raises the threat of new settlements within the park. There already is one village enclave of nearly 2,000 people 28 km within the western boundary of the park (Pinogu), and this creates considerable human traffic through the forest. During our visits to both eastern and western boundaries of Dumoga-Bone park we saw helicopter flights into the center of the park. Mining engineers associated with these flights told us these were only exploratory trips, but on one afternoon we saw seven flights carrying heavy construction equipment. These flights in themselves are disruptive to monkeys, and any major development, especially if it involved a road and semipermanent mining camp, would be potentially very damaging to the wildlife populations of Dumoga-Bone. Primate populations would be reduced not only by direct habitat loss for roads, mining operations, and settlements, but also by the secondary activities of hunting, agricultural incursions, and poaching of forest products. Our surveys of M . hecki populations in the western parts of Sulawesi Utara are too limited to make definite judgements of the population status of this species. The results we do have are not encouraging, however. M . hecki were found in both reserves visited, Tangale and Panua, but Tangale is so small (125 ha) that it probably contains only 2 or 3 small groups. We found a total of 7 monkeys there, and we were able to walk completely through and around the entire reserve in 5 hours. It is an important reserve, but too small to guarantee the survival of primates. Brotoisworo [19821expressed the view that M . hecki is inadequately protected, and additional reserves are highly recommended. We agree with this recommen- Populations of Sulawesi Macaques / 299 dation. Panua is a large reserve (45,000 ha), but it has extensive disturbance around its boundaries, and according to our surveys, it has only a small population of M. hechi (Table IV). Western Sulawesi Utara is an area of rapid population growth and many timber-cutting concessions. The new Trans-Sulawesi highway will bring more people into this area. Gn. Ambang is an example of a nature reserve that was started too late to be an effective protector of wildlife. Although it contains excellent forest, hunting has virtually eliminated primates in Gn. Ambang. In two visits there and 16 km of forest survey we did not find monkeys. The forest ranger at Gn. Ambang told us he had seen monkeys only once in the past year despite almost daily patrols. The only monkeys we found in the Kotamobagu-Ambang-Modayaq area were outside the Ambang reserve near Bedaro village south of Modayaq. The Kotamobagu area has been a government transmigration site, bringing in people from Java, and it has had the greatest population increase of any area in Sulawesi Utara (36.2%for the Kotamobagu area in 10 years, compared to 23.7% for the Gorontalo area, and 18.9% for the Manado area). This provides further evidence of the link between rapid population growth and the loss of wildlife unless vigorous protection is applied. CONCLUSIONS 1. Field studies in 1987-88 on the macaques of north Sulawesi show a more discouraging picture of their population status than that in the existing literature. 2. Populations are smaller, more scattered, and isolated, and population density is less than in the late 1970's. 3. Both the numbers of groups and average group sizes of M. nigra and M . nigrescens are less than in the 1970's. A relative shortage of infants and juveniles indicates recent periods of either increased infant mortality or less successful reproduction. 4. The Tangkoko-Batuangus-Duasudarareserves contain the only sizeable and well-protected population of M . nigru. These reserves are essential for the survival of this species. 5. Dumoga-Bone National Park is essential for the survival of M. nigrescens. 6. M . hechi needs additional reserves, and all three species need more effective protection. ACKNOWLEDGMENTS We are indebted to Professor Karl Somadikarta of the University of Indonesia for serving as our scientific counterpart in Indonesia. Drs. Mulyadi Susanto, Head of the Direktorat Jenderal Perlindungan Hutan dan Pelestarian Alam (PHPA) office in Manado, and Ubus Wardju Maskar, Director of the Dumoga-Bone National Park, granted permission to enter the parks and reserves of Sulawesi Utara. They also provided transportation and logistic support for some of our field work. We are grateful to Mr. T. Hainald of the Indonesian Academy of Sciences (LIPI) for approval of U.S. participation in our project. At each field location we enjoyed the support of local rangers and forest guides, especially Lende, Yunus Masala, and Reol Welua a t Tangkoko; Hamzah Hamid and Nikko a t Dumoga-Bone; Syamsi Antula and Lely Swalang in Gorontalo; and many others. Many students of the University of Indonesia and the National University of Indonesia participated in our field work, including Edy Hendras, Yacob Muskita, Eddy Rachmat, Yopie, Akbar, Basuki, Titien, Nashrudin, and Erma. Field work was supported by a grant to Dr. J. Erwin from the National Geographic Society, a Faculty Fellowship and Grant-in-Aid to Dr. Southwick from the 300 I Sugardjito et al. University of Colorado Council for Research and Creative Work, and a grant to Ja t na Supriatna from the World Wildlife Fund U S . Follow-up work in 1988 has been supported by USPHS Grant RR 04391-01 to the University of Colorado. REFERENCES AND TAXONOMY. CYNOPITHECIDAE, CERCOCEBUS, MACACA, CYNOPITHEAlbrecht, G.H. Methodological approaches GUS. Edinburgh, University Press, 1974. to morphological variation in primate pop- Kawamoto, Y.; Takenaka, 0.; Brotoisworo, ulations: The Celebesian macaques. YEARE. Preliminary Report on genetic variation BOOK OF PHYSICAL ANTHROPOLOGY within and between species of Sulawesi 201290-308, 1977. macaques. KYOTO UNIVERSITY OVERAlbrecht, G.H. THE CRANIOFACIAL SEAS RESEARCH REPORT 2:23-38, MORPHOLOGY OF THE SULAWESI MA1982. CAQUES: MULTIVARIATE APPROACH- Laurie, E.M.O.; Hill, J.E. LIST OF LAND ES TO BIOLOGICAL PROBLEMS. ContriMAMMALS OF NEW GUINEA, CELEbutions to Primatolom, Vol. 13. Basel. BES AND ADJACENT ISLANDS, 1758Karger, 151 pp., 1978.-1952. London, British Museum of Natural Bismarck. M. Ecolom and behavior of M . niHistory, 1954. grescens’ in DumGa-Bone Reserve, North MacKinnon, K. REPORT OF A WORLD Sulawesi. LAP BALEN PENELITEN 392: HEALTH ORGANIZATION (WHO) CON1-30, 1982. SULTANCY TO INDONESIA TO DETERBrotoisworo, E. Conservation of Sulawesi MINE POPULATION ESTIMATES OF macaques. KYOTO UNIVERSITY OVERTHE CYNOMOLGOUS OR LONG-TAILSEAS RESEARCH REPORT 2:39-50, ED MACAQUE, Mucaca fusciculuris (AND 1982. OTHER PRIMATES) AND THE FEASICollias, N.E.; Southwick, C.H. A field study BILITY OF SEMI-WILD BREEDINGPROof population density and social organizaJECTS OF THIS SPECIES. WHO PRItion in howling monkeys. PROCEEDINGS MATE RESOURCES PROGRAMME AMERICAN PHILOSOPHICAL SOCIFEASIBILITY STUDY: PHASE 11. Mimeo. ETY 96:143-156, 1952. Rep., 67 pp. + 7 appendices, 1983. Eisenberg, J.F.; Dittus, W.P.J.; Fleming, MacKinnon, K. Conservation status of priT.H; Green. K.; Struhsaker. T.: Thorinamates in Malesia with special reference to ton, R.W., Jr. TECHNIQUES FOR THE Indonesia. PRIMATE CONSERVATION 8: STUDY OF PRIMATE POPULATION 175-183,1987. ECOLOGY. Washinpton. D.C.. NAS-NRC Napier, J.; Napier, P. HANDBOOK OF LIVCommittee on Primate Conservation, 233 ING PRIMATES: MORPHOLOGY, ECOLpp., 1981. OGY AND BEHAVIOR. New York, AcaEudey, A.A. ACTION PLAN FOR ASIAN demic Press, 1967. PRIMATE CONSERVATION: 1987-1991. Southwick, C.H.; Cadigan, F.C., Jr. PopulaIUCN/SSC Primate Specialist Group. tion studies of primates in Malaysia. PRIMATES 13:l-13,1972. UNEP and WWF Publication, 65 pp., 1987. Fooden, J. Taxonomy and evolution of the Southwick, C.H.; Richie, T.; Taylor, H.; Teas, monkeys of the Celebes (Primates: CerH.J.; Siddiqi, M.F. Rhesus monkey populacopithecidae). BIBLIOTHECA PRIMATOtions in India and Nepal: Patterns of LOGICA 1O:l-147, 1969. Growth, Decline, and Natural Regulation. Groves, C.P. Speciation in Macaca: The view Pp. 151-170 in BIOSOCIAL MECHAfrom Sulawesi. Pp. 84-124 in THE MANISMS OF POPULATION REGULACAQUES: STUDIES IN ECOLOGY, BETION. M.N. Cohen, R.S. Malpass, H.G. HAVIOR AND EVOLUTION. D.G. LindKlein, eds. New Haven, Yale University burg, ed. New York, Van Nostrand Press, Chap. 7, 1980. Reinhold, 1980. Takenaka, 0.; Hotta, M.; Takenaka, A.; Hamada, Y.; Watanabe, T.; Takenaka, 0.; Kawamoto, Y.; Suryobroto, B.; BrotoisSuryobraoto, B.; Kawamoto Y. Morphologworo, E. Origin and evolution of the Suical studies on the Sulawesi macaques. I. lawesi macaques: 1. Electrophoretic analyPhyletic analysis of body color. PRIMATES sis of hemoglobins. PRIMATES 28:87-97, 29:65-80, 1988. 1987a. Howard, Charles F., (ed.) NONHUMAN Takenaka, 0.; Hotta, M; Kawamoto, Y.; PRIMATE STUDIES ON DIABETES, Suryobroto, B.; Brotoisworo, E. Origin and CARBOHYDRATE INTOLERANCE, AND evolution of the Sulawesi macaques: 2. OBESITY. Monographs in Primatology, Complete amino acid sequences of seven B Vol. 12. New York, Alan R. Liss, Inc., 1988. chains of three molecular types. PRIHill, W.C.O. COMPARATIVE ANATOMY MATES 28:99-109, 1987b. Populations of Sulawesi Macaques I 301 Watanabe, K.; Brotoisworo, E. Field observation of Sulawesi macaques. KYOTO UNIVERSITY OVERSEAS RESEARCH REPORT 2:3-9,1982. Wheatley, B.P. Feeding and ranging of East Bornean Mmaca fuscicularis. Pp.215-246 in THE MACAQUES: STUDIES IN ECOLOGY, BEHAVIOR AND EVOLUTION. D.G.Lindburg, ed. New York, Van Nostrand Reinhold, 1980. Whitten, A.J.; Mustafa, M.; Henderson, G.S. THE ECOLOGY OF SULAWESI. Yogyakarta, Indonesia: Gadjah Mada University Press, (Distributed in the United States by Sinauer Associates, Sunderland, Massachusetts), 1987. World Wildlife Fund. CAGAR ALAM GN. TANGKOKO-DUA SAUDARA, SULAWESI UTARA. WWF REPORT FOR THE DIRECTORATE OF NATURE CONSERVATION, REPUBLIC OF INDONESIA. WWF, Bogor, 1980.