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McAney C.M., Fairley J.S. 1989. Analysis Nature Research reports, Peterbo- ALTITUDINAL DISTRIBUTION OF FRUIT of the diet of the lesser horseshoe rough, 47. Rhinolophus hipposideros, in the West Robinson M.F., Stebbings R.E. 1993. Food (PTEROPODIDAE) IN LORE LINDU NATIONAL PARK, of Ireland. J. Zool. Lond. 217: 491- of the serotine bat, Eptesicus serotinus CENTRAL , INDONESIA 498. - is faecal analysis a valid qualitative Menaker M. 1964. The free running period and quantitative technique? J. Zool. 1 2 1 of the bat clock; seasonal variations at Lond. 231: 239-248. IBNU MARYANTO , MUHAMAD YANI , SITI NURAMALIATI PRIJONO , 1* low body temperature. J. Cell. Comp. Shiel C., McAney C., Sullivan C., Fairley SIGIT WIANTORO Physiol. 57: 81-86. J. 1997. Identification of arthropod Møller A.P. 2001. The effect of dairy farm- fragments in bat droppings. The Received 25 August 2010; accepted 7 March 2011 ing on barn swallow Hirundo rustica Society, London. abundance, distribution and reproduc- Skidmore P. 1991. Insects of the British 1Museum Zoologicum Bogoriense-LIPI, Jl. Raya Jakarta-Bogor KM. 46, Cibinong, Bogor, tion. J. Appl. Ecol. 38: 378-389. Cow-dung Community. Occasional Indonesia; Corresponding author, E-mail: [email protected] Park K.J., Jones G., Ransome R.D. 2000. Publication No. 21. Field Studies Co- 2Jl. Gotong Royong, Pajeruk Lombok Mataram-NTB, Indonesia. Torpor, arousal and activity in hiber- uncil. Richmond Publishing, Slough. nating bats: a telemetric study of free- Sommer C., Steffansen B., Overgaard Niel- ABSTRACT - Between March 2000 and July 2001, we studied the distribution of fruit bats living greater horseshoe bats (Rhino- sen B., Gronvold J., Vagn Jensen in Lore Lindu National Park, Central Sulawesi, Indonesia. Vegetation types and elevation lophus ferrumequinum). Funct. Ecol. K.M., Brochner Jespersen J., Spring- belts between 350 and 2100 m a.s.l. were combined to characterize 17 habitat types, which 14: 580-588. borg J., Nansen P. 1992. Ivermectin were surveyed using standardized mist netting. Sixteen of Pteropodidae (fruit bats) Rabinowitz A.R., Tuttle M.D. 1982. A test excreted in cattle dung after subcuta- were identified in the park. Using an Euclidian distance dissimilarity index (EDD), the 16 of the validity of two currently used neous or pour-on treatment: concentra- species were clustered into four main groups. The results of cluster analysis were supported methods of determining bat prey prefe- tions and impact on dung fauna. Bull. by Principle Component Analysis, PC1 and PC2 accounting for 71.94% and 27.39% of rences. Acta Theriol. 27: 283-293. Entomol. Res. 82: 257-264. total variance, respectively. We suggest that PC2 primarily implies an altitudinal gradient, Racey P.A., Speakman J.R. 1987. The Stone E.L., Jones G., Harris S. 2009. Street while PC1 is probably related to the gradient of humidity. energy costs of pregnancy and lacta- lighting disturbs commuting bats. tion in heterothermic bats. Symp. Curr. Biol. 19:1-5. Key words: Chiroptera, elevation, diversity, habitat preferences Zool. Soc. Lond. 57: 107-125. Strong L., James S. 1992. Some effects of Ransome R.D. 1971. The effect of ambient rearing the yellow dung fly, Scatopha- RIASSUNTO - Distribuzione altitudinale dei pipistrelli frugivori (Pteropodidae) nel Par- temperature on the arousal frequency ga stercoraria, in cattle dung contain- co Nazionale di Lore Lindu, Sulawesi, Indonesia. Tra Marzo 2000 e Luglio 2001, abbia- of the hibernating greater horseshoe ing ivermectin. Entomol. Exp. Appl. mo studiato la distribuzione dei pipistrelli frugivori del Parco Nazionale di Lore Lindu (Su- bat, Rhinolophus ferrumequinum, in 63: 39-45. lawesi, Indonesia). Il tipo di vegetazione e le fasc di quota individuate tra 350 e 2100 m relation to site selection and the hiber- Unwin D.M. 1991. A key to the Families of s.l.m. sono state combinate ad identificare 17 habitat, che sono stati monitorati tramite mist- nation state. J. Zool. London 164: 353- British Diptera. Field Studies Council, nets. Sono state identificate 16 specie, che, tramite analisi dei cluster (EDD), sono state 371. Shrewsbury, UK. raggruppate in 4 gruppi principali. I risultati ottenuti sono stai confermati dall’Analisi delle Ransome R.D. 1990. The Natural History Whitaker J.O. 1988. Food habitat analysis Componenti Principali, per la quale PC1 e PC2 hanno spiegato, rispettivamente, il 71,94% of Hibernating Bats. Christopher of insectivorous bats. In: Kunz T.H. e 27,39% della varianza complessiva. Riteniamo che PC2 sia legata ad un gradiente altitu- Helm, Kent, UK. (Ed.). Ecological and behavioural me- dinale, mentre PC1 probabilmente riflette un gradiente di umidità. Ransome R.D. 2000. Monitoring diets and thods for the study of bats. Smithso- population changes of greater horse- nian Institution Press, Washington, Parole chiave: Chiroptera, altitudine, diversità, preferenze ambientali shoe bats in Gloucestershire and pp.171-189. Somerset. English Nature Research Williams C.A. 2001. The winter ecology of DOI: 10.4404/Hystrix-22.1-4480 Reports, Peterborough, 341: 1-55. Rhinolophus hipposideros, the lesser Ransome R.D. 2002. Winter feeding stu- horseshoe bat. PhD thesis, Open Uni- INTRODUCTION Musser 1984; Musser 1991), and even dies on greater horseshoe bats. English versity, Cornwall, U.K. for more mobile , such as pte- Sulawesi Island (Indonesia) retains ropodids, levels of ca. 10% have been high levels of endemism, particularly reported (Maryanto and Higashi in for mammals. As much as 30 % of the prep.). Furthermore, Sulawesi has been island’s are endemic (Carleton and divided into several areas based on the

167 Maryanto et al. distribution of endemic mammals, for al. (2005) showed that species asso- instance (Musser and Dagosto ciated with disturbed habitats tend to be 1987; Corbet and Hill 1992), squirrels widely distributed and show higher (Musser et al. 2010), macaques (Foo- rates of gene flow between populations den 1969; Supriatna 1996) and tarsiers than species associated with rain fo- (Shekelle and Laksono 2004), but not rests, which tend to be endemic. This for Chiroptera. The geological history study was designed to provide detailed of the island probably played a major information on the distribution and ha- role in determining the high endemism bitat preferences of fruit bats in a rates of Sulawesi (Shekelle and Lakso- mountainous region of Central Sulawe- no 2004). si. Sulawesi and neighbouring smaller isl- ands are known to be rich in pteropodid MATERIALS AND METHODS (fruit bat) species. Bergmans and Ro- zendaal (1988) reported 21 species of Lore Lindu National Park is the largest Pteropodidae in Sulawesi and San- protected area on the island (ca. 231000 ha; gihe/Sangir islands, to which, in their Fig.1). The Park has a rugged topography, checklist of Indonesian mammals, altitude ranging from 250 to 2340 m a. s. l. Suyanto et al. (2002) added six further The area is mainly mountainous, 90% of the park being above 1000 m, while lower species, recorded on Selayar and Ta- areas occur only next to the north-western laud islands ( humilis K. An- park boundaries (Wirawan 1981). Ten land dersen, 1909; minutus Mil- system use types and 11 major vegetation ler, 1906; C. sphinx (Vahl, 1797); Pte- types have been distinguished (Maryanto ropus speciosus K. Andersen, 1908; P. and Yani 2001). According to Watling and pumilus Miller, 1911). A new species, Mulyana (1981), in Lore Lindu lowland linduensis Maryanto and Ya- forest species grow up to 1500 m a.s.l., the ni, 2003 has been recently described transition to mountain forest occurring at from the Lore Lindu area. However, about 1000 m a.s.l. In contrast, Musser and none of these studies provided any in- Dagosto (1987) reported that, in Central Sulawesi, above 1300 m a.s.l. the lowland formation on the habitat preferences of evergreen forest gives way to the lower these bats. In other parts of Southeast mountain rain forest, and that this transition Asia, Medway (1972) and Heaney et al. entails a reduction in mean canopy height, (1989) reported that pteropodid species number of buttressed trunks and creepers, richness typically decreases with height and ambient temperature. Biological diver- above sea level. The same pattern has sity generally decreases with increasing been reported for Lombok Island and elevation (Whitmore, 1984). the Lesser Sunda Islands of Indonesia According to Maryanto and Yani (2001), (Gunnel et al. 1996; Kitchener 1998). vegetation cover was divided into 11 types: The distribution and diversity of bats cloud forest (Cf), upper mountain forest (Um), mountain forest (Mo), lower moun- are influenced by microclimate, eleva- tain forest (Lm), lower mountain moist tion, habitat types and food resources forest (Lmm), marsh (Ma), mixed garden (Maryanto and Yani 2003; Hodgkison (Mg), monsoon forest (Ms), swamp forest et al. 2004; Campbell et al. 2007). In (Sf), lowland forest (Lf), and degraded low- the Philippine archipelago, Heaney et land forest (Df). We divided the study area

168 Maryanto et al. Fruit bats in Indonesia distribution of endemic mammals, for al. (2005) showed that species asso- instance Muridae (Musser and Dagosto ciated with disturbed habitats tend to be 1987; Corbet and Hill 1992), squirrels widely distributed and show higher (Musser et al. 2010), macaques (Foo- rates of gene flow between populations den 1969; Supriatna 1996) and tarsiers than species associated with rain fo- (Shekelle and Laksono 2004), but not rests, which tend to be endemic. This for Chiroptera. The geological history study was designed to provide detailed of the island probably played a major information on the distribution and ha- role in determining the high endemism bitat preferences of fruit bats in a rates of Sulawesi (Shekelle and Lakso- mountainous region of Central Sulawe- no 2004). si. Sulawesi and neighbouring smaller isl- ands are known to be rich in pteropodid MATERIALS AND METHODS (fruit bat) species. Bergmans and Ro- zendaal (1988) reported 21 species of Lore Lindu National Park is the largest Pteropodidae in Sulawesi and San- protected area on the island (ca. 231000 ha; gihe/Sangir islands, to which, in their Fig.1). The Park has a rugged topography, checklist of Indonesian mammals, altitude ranging from 250 to 2340 m a. s. l. Suyanto et al. (2002) added six further The area is mainly mountainous, 90% of the park being above 1000 m, while lower species, recorded on Selayar and Ta- areas occur only next to the north-western laud islands (Acerodon humilis K. An- park boundaries (Wirawan 1981). Ten land dersen, 1909; Cynopterus minutus Mil- system use types and 11 major vegetation Figure 1 - Study area: Lore Lindu National Park, Central Sulawesi, Indonesia. ler, 1906; C. sphinx (Vahl, 1797); Pte- types have been distinguished (Maryanto ropus speciosus K. Andersen, 1908; P. and Yani 2001). According to Watling and into seven altitudinal zones: 300-599 m ity coefficient (EDD; Krebs 1989) was pumilus Miller, 1911). A new species, Mulyana (1981), in Lore Lindu lowland (L2), 600-899 m (L1), 900-1199 m (M2), used and dendrograms were clustered by Rousettus linduensis Maryanto and Ya- forest species grow up to 1500 m a.s.l., the 1200-1499 m (M1), 1500-1799 m (H2), the Unweighted Pair Group Method with ni, 2003 has been recently described transition to mountain forest occurring at 1800-2099 m (H1) and above 2100 m a.s.l. Arithmetic Mean (UPGMA). Cluster ana- from the Lore Lindu area. However, about 1000 m a.s.l. In contrast, Musser and (T). From the combination of the 11 vege- lyses and dendrograms of dissimilarity none of these studies provided any in- Dagosto (1987) reported that, in Central tation types and 7 altitudinal zones, we were produced using NTSYSpc 2.10. Prin- Sulawesi, above 1300 m a.s.l. the lowland formation on the habitat preferences of obtained 17 habitats (Tab. 1). As an exam- ciple Component Analysis (PCA) was em- evergreen forest gives way to the lower ple, L2Ms is monsoon forest at 300-599 m ployed to group bats according to habitat these bats. In other parts of Southeast mountain rain forest, and that this transition a.s.l. Between March 2000 and July 2001, a preferences (Tab. 1). Asia, Medway (1972) and Heaney et al. entails a reduction in mean canopy height, total of 40 sampling sites were set up in the (1989) reported that pteropodid species number of buttressed trunks and creepers, different habitats. Each sampling site was RESULTS richness typically decreases with height and ambient temperature. Biological diver- sampled for four nights by using four mist above sea level. The same pattern has sity generally decreases with increasing nets (lengths of 6, 9, 12, 18 m, each with a 1. Composition and diversity of bat been reported for Lombok Island and elevation (Whitmore, 1984). height of 2.7 m and four shelves). Mist nets assemblages the Lesser Sunda Islands of Indonesia According to Maryanto and Yani (2001), were set up among the lower tree canopies

(Gunnel et al. 1996; Kitchener 1998). vegetation cover was divided into 11 types: and checked at 21:00 and 06:00 the follow- A total of 3799 fruit bats were cap- The distribution and diversity of bats cloud forest (Cf), upper mountain forest ing day. Survey data were entered into a (Um), mountain forest (Mo), lower moun- tured. The sample included 16 species are influenced by microclimate, eleva- Geographical Information System (GIS) tain forest (Lm), lower mountain moist and 11 genera (Tab. 1), 62% of Sula- tion, habitat types and food resources (Arcview 3.2). Shannon-Wiener’s index forest (Lmm), marsh (Ma), mixed garden and Evenness (Krebs 1989) were used to wesian fruit bat species. Dominant spe- (Maryanto and Yani 2003; Hodgkison (Mg), monsoon forest (Ms), swamp forest compare bat assemblages. To define differ- cies (90.8% of the whole bat assem- et al. 2004; Campbell et al. 2007). In (Sf), lowland forest (Lf), and degraded low- ent clusters of species in relation to habitat blage) included nigrescens the Philippine archipelago, Heaney et land forest (Df). We divided the study area variables, the Euclidian distance dissimilar- (Gray, 1870) (2075 individuals), Rou-

169 Maryanto et al. settus celebensis K. Andersen, 1907 tion in the abundance of dominant and (1309 individuals), mi- eurytopic species. Shannon-Weiner’s nimus (E. Geoffroy, 1810) (200 indi- diversity curve was rather stable be- viduals), and Cynopterus luzoniensis tween 300 and 1500 m a.s.l. and then (Peters, 1861) (187 individuals). Two progressively decreased down to 0.18 species, Rousettus (Boneia) bidens at the highest elevations, while even- (Jentink, 1879) and R. linduensis were ness ranged between 0.2 and 0.4 at rarely netted and were represented by 300-1800 m a.s.l. and then increased up only nine and four (0.241% and 0.11%) to 0.53 at the highest elevations (Fig. individuals each. Seven of the 16 spe- 2). The decrease in Shannon-Weiner cies (44%), C. luzoniensis, index at the summit of the mountain exoleta K. Andersen, 1909, R. (Boneia) mainly depended on low species rich- bidens, R. celebensis, R. linduensis, ness, bat assemblages being sharply wallacei (Gray, 1866), dominated by Thoopterus nigrescens and celebensis Miller (Tab. 1). and Hollister, 1921 are endemic to Su- lawesi and adjacent islands (Kitchener 2. Habitat preferences and Maharadatunkamsi 1991; Corbet and Hill 1992). The 16 species were clustered into The number of individuals captured for groups at EDD =1.9, subgroups at EDD each altitudinal zone ranged from 48 = 1.4 and subsets at EDD = 1.2 (Fig. (L2Ms) to 627 (M2Lm), due to varia- 3).

Figure 2 - Variation in both Shannon-Wiener’s evenness indexes for fruit bat assemblages in different habitats in relation to the height a.s.l. (see the methods for habitat abbrevia- tions).

170 Maryanto et al. Fruit bats in Indonesia

settus celebensis K. Andersen, 1907 tion in the abundance of dominant and R. (1309 individuals), Macroglossus mi- eurytopic species. Shannon-Weiner’s nimus (E. Geoffroy, 1810) (200 indi- diversity curve was rather stable be- viduals), and Cynopterus luzoniensis tween 300 and 1500 m a.s.l. and then (Peters, 1861) (187 individuals). Two progressively decreased down to 0.18 species, Rousettus (Boneia) bidens at the highest elevations, while even- (Jentink, 1879) and R. linduensis were ness ranged between 0.2 and 0.4 at R. celebensis (Rc), rarely netted and were represented by 300-1800 m a.s.l. and then increased up Macroglossus minimus only nine and four (0.241% and 0.11%) to 0.53 at the highest elevations (Fig.

individuals each. Seven of the 16 spe- 2). The decrease in Shannon-Weiner (Hc), cies (44%), C. luzoniensis, Dobsonia index at the summit of the mountain

exoleta K. Andersen, 1909, R. (Boneia) mainly depended on low species rich- ) bidens (Rb), Cynopterus brachyotis (Cb), C. luzo- bidens, R. celebensis, R. linduensis, ness, bat assemblages being sharply Styloctenium wallacei (Gray, 1866), dominated by Thoopterus nigrescens ( Boneia and Harpyionycteris celebensis Miller (Tab. 1). (Chm), and Hollister, 1921 are endemic to Su- R. lawesi and adjacent islands (Kitchener 2. Habitat preferences (Ra), and Maharadatunkamsi 1991; Corbet and Hill 1992). The 16 species were clustered into Harpyonycteris celebensis The number of individuals captured for groups at EDD =1.9, subgroups at EDD each altitudinal zone ranged from 48 = 1.4 and subsets at EDD = 1.2 (Fig. (L2Ms) to 627 (M2Lm), due to varia- 3).

Chironax Chironax melanocephalus Rousettus amplexicaudatus spelaea (Es), (Pa), (De), mistnet/four nights captured in different habitats (see methods for abbreviations) at Lore Lindu 2 (Tn). (* = endemic species of Sulawesi and adjacent islands). (Sw), Thoopterus nigrescens Pteropus alecto Dobsonia exoleta

C. minutus (Cm), Figure 2 - Variation in both Shannon-Wiener’s evenness indexes for fruit bat assemblages in different habitats in relation to the height a.s.l. (see the methods for habitat abbrevia- Nyctimene cephalotes (Nc), tions). Table 1. Number Table of bat species for 100 m linduensis (Rl), Styloctenium wallacei National Park, Central Abbreviations Sulawesi. of species names: niensis (Cl), (Mm),

171 Maryanto et al.

Figure 3 - Clustering of bats species captured at Lore Lindu National Park, Central Sulawe- si by Euclidian dissimilarity index and UPGMA.

Group B1: Upper mountain association Group B3: included only one individual (1800-2100 m a.s.l.): consisted of R. Pteropus alecto, a migrant species, (Boneia) bidens and T. nigrescens. The which was captured in a marsh using first is a rare and probably stenotopic mistnets that were set up about 9 m species, while T. nigrescens is a eury- above the ground. topic species. However, both of them Group B4: Lowland and lower- are associated with the upper mountain mountain association (300-1200 m forest. a.s.l.): consisted of two Subgroups, Group B2: Lowland & mountain forest B4a: frugivores (C. brachyotis, C. lu- association (600-1800 m a.s.l.): con- zoniensis, C. minutus, R. celebensis, D. sisted of two Subgroups. Subgroup exoleta and N. cephalotes); and B4b: B2A: Nectarivores, included M. mini- nectarivores (R. amplexicaudatus and mus, S. wallacei and R. linduensis. In E. spelaea), mainly associated with particular, M. minimus (Subset B2Aa) lowland forests at 300-600 m a.s.l. is a more specialized nectarivore than (Corbet and Hill 1992). Except for R. the other two species. R. linduensis was celebensis, the eight species of Group also captured in swamp forest at 930 m B4 are widespread, indicating that en- a.s.l. Subgroup B2B: included of H. demic species are mainly distributed at celebensis and C. melanocephalus high altitudes. which are mainly frugivores (Corbet The results of clustering analysis are and Hill, 1992). supported by PCA (Fig. 4, Tab. 2), for

172 Maryanto et al. Fruit bats in Indonesia

Figure 4 - Principle Component Analysis. PC1 and PC2 explain 71.94%, and 27.39% of total variance. Species name abbreviations are as in Table 1. Figure 3 - Clustering of bats species captured at Lore Lindu National Park, Central Sulawe- si by Euclidian dissimilarity index and UPGMA. Table 2 - Factors’ scores of Principle Component Analysis (see methods for abbreviations).

Group B1: Upper mountain association Group B3: included only one individual Habitat Factor 1 Factor 2 Factor 3 (1800-2100 m a.s.l.): consisted of R. Pteropus alecto, a migrant species, TCf -0.64449 -0.64143 -0.79372 (Boneia) bidens and T. nigrescens. The which was captured in a marsh using H1Cf -0.62667 0.63681 -0.91862 first is a rare and probably stenotopic mistnets that were set up about 9 m species, while T. nigrescens is a eury- above the ground. H1Um -0.74569 2.85406 -0.42391 topic species. However, both of them Group B4: Lowland and lower- H2Um -0.6208 0.84672 -0.48849 are associated with the upper mountain mountain association (300-1200 m H2Mo -0.78214 1.03824 0.57678 forest. a.s.l.): consisted of two Subgroups, M1Mo -0.74557 -0.54158 0.4933 Group B2: Lowland & mountain forest B4a: frugivores (C. brachyotis, C. lu- M1Mo -0.57096 -0.09283 0.35539 association (600-1800 m a.s.l.): con- zoniensis, C. minutus, R. celebensis, D. M2Sf -0.00731 -0.07363 2.69962 sisted of two Subgroups. Subgroup exoleta and N. cephalotes); and B4b: M2Lm 2.47036 0.88395 -0.28367 B2A: Nectarivores, included M. mini- nectarivores (R. amplexicaudatus and M2Lmm -0.47871 -0.97322 -1.14078 mus, S. wallacei and R. linduensis. In E. spelaea), mainly associated with particular, M. minimus (Subset B2Aa) lowland forests at 300-600 m a.s.l. M2Dl 0.6102 -0.36647 0.20854 is a more specialized nectarivore than (Corbet and Hill 1992). Except for R. M2Ma -0.98804 -0.7665 1.57638 the other two species. R. linduensis was celebensis, the eight species of Group M2Mg 0.82951 -0.35562 -0.20075 also captured in swamp forest at 930 m B4 are widespread, indicating that en- L1Ms -0.20684 -1.08587 -1.06841 a.s.l. Subgroup B2B: included of H. demic species are mainly distributed at L1Lf 1.7756 -0.19181 0.52512 celebensis and C. melanocephalus high altitudes. L1Lm 1.04591 -0.10739 -0.30729 which are mainly frugivores (Corbet The results of clustering analysis are L2MS -0.31436 -1.06344 -0.80949 and Hill, 1992). supported by PCA (Fig. 4, Tab. 2), for

173 Maryanto et al. which the inspection of the eigenvalues important trees in tropical rain forests revealed that PC1, PC2 and PC3 ac- are associated with bats (Marshall, counted for 71.94%, 27.39% and 1985; Fujita and Tuttle, 1991), which 0.34% of total variance, respectively. are considered to play a major role in PC3 was subsequently excluded from the maintenance of many forest ecosys- the analysis. On PC1, the two dominant tems. Shilton (1999) studied seed dis- species, T. nigrescens and R. celeben- persal and pollination by bats in the sis, are positioned on opposite margins, Krakatau Islands and demonstrated rap- suggesting that PC1 was associated id transit times, generally less than 30 with some factor which is very differ- minutes, whilst Tidemann et al. (1990) ent between mountain and lowland reported that in Cynopterus sphinx gut areas. It should be noted that the group retention of food, including viable fig of T. nigrescens and R. (Boneia) bidens seeds, can be more than 12 hours. Ma- is joined by P. alecto which was cap- croglossus, Eonycteris and Rousettus tured only in a marsh. Humidity being bats mainly feed at flowers (Maryati et higher in mountain forests than in low- al. 2008; Soegiharto et al. 2010) and land forests, PC1 may be related to the may play a major role in the pollination gradient of humidity. For PC2, moun- of several tree species in Sulawesi. tain species such as T. nigrescens, R. Six fruit bats species found in Lore bidens and H. celebensis are positioned Lindu National Park are widespread on the positive margin, while lowland throughout Southeast Asia (C. brachyo- species, R. amplexicaudatus, C. minu- tis, C. minutus, M. minimus, C. mela- tus, P. alecto and R. celebensis are on nocephalus, R. amplexicaudatus and E. the negative one, suggesting that PC2 spelaea). Heaney et al. (2005) sug- primarily describes an altitudinal gra- gested that widespread species occur dient. also in disturbed habitats, whilst en- demic species are rarely found far from DISCUSSION primary rain forest. Accordingly, in our study area R. amplexicaudatus, C. bra- Our results agree with previous studies chyotis, C. minutus were strongly asso- of fruit bats in suggesting that species ciated with disturbed lowland habitats. richness decreases with altitude (Hea- In contrast, the ability of these species ney et al. 1989; Medway 1972; Azlan to tolerate disturbed habitats and low 2003), although in the Rinjani Moun- humidity in highland habitats may be tain area of Lombok richness declined quite limited (Abdullah et al. 1997; between 200-400 m (Gunnel 1998). Bat Azlan 2000; 2003). abundance is thought to be influenced In Sri Lanka, C. brachyotis has been by habitat types and, consequently, reported to be rare and restricted to for- food availability. Accordingly, the di- est habitat (Mapatuna et al. 2002), versity of fruit trees decreases from therefore this species is potentially lowland areas to mountain peaks threatened by deforestation. In contrast, (Whitmore 1984). in Peninsular Malaysia and Sarawak, C. Over 450 species of fruit-bearing brachyotis has two ‘morphs’: one plants, including many economically usually found in forest and the other in

174 Maryanto et al. Fruit bats in Indonesia which the inspection of the eigenvalues important trees in tropical rain forests disturbed habitats (Campbell et al. cedures adopted in the field. We are in- revealed that PC1, PC2 and PC3 ac- are associated with bats (Marshall, 2004; 2006; 2007). In Lore Lindu, C. debted to R. A. How (Western Australian counted for 71.94%, 27.39% and 1985; Fujita and Tuttle, 1991), which brachyotis and C. minutus are sympa- Museum), S. Higashi (Hokkaido Universi- 0.34% of total variance, respectively. are considered to play a major role in tric with the endemic R. celebensis and ty), M. Struebig (Queen Mary-University PC3 was subsequently excluded from the maintenance of many forest ecosys- C. luzoniensis in lowland or open habi- of London) and Alan T. Hitch (University the analysis. On PC1, the two dominant tems. Shilton (1999) studied seed dis- tats. of California Davis) who commented on species, T. nigrescens and R. celeben- persal and pollination by bats in the M. minimus has been reported to be a analyses and critically read the manuscript. Finally, grateful thanks are due to TNC and sis, are positioned on opposite margins, Krakatau Islands and demonstrated rap- strong flier with wide distribution, from USAID for funding this study. suggesting that PC1 was associated id transit times, generally less than 30 lowlands to upper mountain elevations with some factor which is very differ- minutes, whilst Tidemann et al. (1990) (Suyanto 1994). In Lore Lindu, it was REFERENCES ent between mountain and lowland reported that in Cynopterus sphinx gut usually found in open secondary forests areas. It should be noted that the group retention of food, including viable fig and was rather common in marsh and Abdullah M.T., Siswanto H., Widiyanto A., of T. nigrescens and R. (Boneia) bidens seeds, can be more than 12 hours. Ma- swamp forest. It is sympatric with the Setiabudi A., Firmansyah M. 1997. is joined by P. alecto which was cap- croglossus, Eonycteris and Rousettus Sulawesian eurytopic species R. cele- Abundance, diversity and distribu- tured only in a marsh. Humidity being bats mainly feed at flowers (Maryati et bensis and T. nigrescens. R. bidens oc- tional records of bats in disturbed higher in mountain forests than in low- al. 2008; Soegiharto et al. 2010) and curred at high elevations, R. linduensis habitats in Kalimantan Barat. Sarawak land forests, PC1 may be related to the may play a major role in the pollination and M. minimus at middle elevations Museum Journal 51(72): 75-84. gradient of humidity. For PC2, moun- of several tree species in Sulawesi. and R. amplexicaudatus and E. spelaea Azlan J., Maryanto I., Kartono A.P., Ab- tain species such as T. nigrescens, R. Six fruit bats species found in Lore in lowlands. In contrast, Bergmans and dullah M.T. 2003. Diversity, relative bidens and H. celebensis are positioned Lindu National Park are widespread Rozendaal (1988) recorded R. (Boneia) abundance and conservation of Chi- on the positive margin, while lowland throughout Southeast Asia (C. brachyo- bidens in lowland forests, between 200 ropterans in Kayan Mentarang Na- species, R. amplexicaudatus, C. minu- tis, C. minutus, M. minimus, C. mela- and 500 m a.s.l., of Tambun and Lem- tional Park East Kalimantan, Indone- tus, P. alecto and R. celebensis are on nocephalus, R. amplexicaudatus and E. beh Island. Pteropus alecto has so far sia. Sarawak Museum Journal 58(79): the negative one, suggesting that PC2 spelaea). Heaney et al. (2005) sug- been reported also for Bawean, Maluku 251-265. primarily describes an altitudinal gra- gested that widespread species occur and Irian (West Papua). Azlan J., Sharma R.S.K., Zakaria M. 2000. Species diversity and relative abun- dient. also in disturbed habitats, whilst en- Based on this survey, habitat overlap dance of understory bats at Air Hitam demic species are rarely found far from and niche breadth deserve additional Forest Reserve, Selangor, Malaysia. DISCUSSION primary rain forest. Accordingly, in our future studies to clarify the ecology and Malay. Nat. J. 54(1): 69-75. study area R. amplexicaudatus, C. bra- biogeography of bats in Sulawesi. Bergmans W., Rozendaal F.G. 1988. Notes Our results agree with previous studies chyotis, C. minutus were strongly asso- on collections of fruit bats from Sula- of fruit bats in suggesting that species ciated with disturbed lowland habitats. ACKNOWLEDGEMENTS wesi and some off-lying islands richness decreases with altitude (Hea- In contrast, the ability of these species (Mammalia, Megachiroptera). Zool. ney et al. 1989; Medway 1972; Azlan to tolerate disturbed habitats and low We would like to express to our thanks to Verhandel. 248: 1-74. 2003), although in the Rinjani Moun- humidity in highland habitats may be Ir. Banjar Yulianto Laban, the Director of Campbell P., Schneider C.J., Adnan A.M., tain area of Lombok richness declined quite limited (Abdullah et al. 1997; Lore Lindu National Park, who provided us Zubaid A., Kunz T.H. 2004. Phyloge- between 200-400 m (Gunnel 1998). Bat Azlan 2000; 2003). with very substantial assistance in the field, ny and phylogeography of Old World abundance is thought to be influenced In Sri Lanka, C. brachyotis has been as did a number of park staff. We are also fruit bats in the Cynopterus brachyotis by habitat types and, consequently, reported to be rare and restricted to for- grateful to Duncan Neville, The Nature complex. Mol. Phylogenet. Evol. 33: food availability. Accordingly, the di- est habitat (Mapatuna et al. 2002), Conservancy Program Manager at Palu, 764–781. and Darrell J. Kitchener, The Nature Con- versity of fruit trees decreases from therefore this species is potentially Campbell P., Schneider C.J., Adnan A.M., servancy Director of Conservation, for or- Zubaid A., Kunz T.H. 2006. Compara- lowland areas to mountain peaks threatened by deforestation. In contrast, ganizing of the mammal survey in Lore tive population structure of Cynopte- (Whitmore 1984). in Peninsular Malaysia and Sarawak, C. Lindu National Park. Thanks are extended rus fruit bats in peninsular Malaysia Over 450 species of fruit-bearing brachyotis has two ‘morphs’: one to our field assistants Mohamad Annas, and southern Thailand. Mol. Ecol. 15: plants, including many economically usually found in forest and the other in who helped in developing mist netting pro- 1-19.

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