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BiologzcalJoumal ofthe Linnean So&& (1999), 66: 305-331. With 2 figures Article ID: bijl. 1998.0279, available online at http://wwv.idealibrary.com on 10 E);L Diversity, evolutionary specialization and geographic distribution of a mutualistic ant-plant complex: Macaranga and Crematogaster in South East Asia BRIGITTE FIALA’*, ARMIN JAKOB‘, ULRICH MASCHWITZ’ AND K. EDUARD LINSENMAIRI I <oologie 111, Biozentrum, ?heodor-Boveri-Institut, Universitat Wurzburg, A m Hubland, 0-97074 Wurzburg, Germany ‘~oologischesInstitut, J. W Goethe-Universitat, Siesmayerstrasse 70, D- 60054 Frankfurt am Main, Germany Received 4 February 1998; acceptedfor publication 23 June 1998 The most conspicuous and species-rich ant-plant mutualism in the Malesian region is found in the important pioneer tree genus Macurungu, yet little is known about the identities or community ecology of the species involved. Our studies have revealed a far more complex system than previously thought. This paper presents the first extensive investigation in the whole distribution area of myrmecophytic Mucarungu. All ant-inhabited species were restricted to the moister parts of SE Asia: Peninsular Malaysia, South and East Thailand, Sumatra and Borneo. We found a rather strict and similar altitudinal zonation of myrmecophytic Macaranga species in all regions. Here we focus on the majority of the 19 Mucaranga species obligatorily associated with ants of the genus Crematogater. We identified a total of 2163 ant queens which belonged to at least eight (morpho)species of the small subgenus Decacraa as well as to one non-Decacrau @robably from Atopogyne). The ant species were not randomly distributed among the Mucuranga species but distinct patterns of associations emerged. Despite common sympatric distribution of Mucurangu species, in most cases a surprisingly high specificity of ant colonization was maintained which was, however, often not species-specific but groups of certain plant species with identical ant partners could be found. These colonization patterns usually but not always mirror existing taxonomic sections within the genus Macaranga. Possible mechanisms of specificity are discussed. The results are compared with other ant-plant mutualisms. 0 1999 The Linnran Socirtv of Ixlndon ADDITIONAL KEY WORDS:-biogeography Malesia - myrmecophyte. ~ co-evolution - Decucremu - host specificity ~ CONTENTS Introduction . . . . . . . . . . . . . . . . . . . . . . . Natural history of the symbiotic partners . . . . . . . . . . . . . 306 307 * Corresponding author. Email: [email protected] 0024-4066/99/030305+27 $30.00/0 305 0 1999 The Linnean Society of London 306 B. FIALA E T A L . The plants . . . . . . . . . . . . . . . . . . The ants . . . . . . . . . . . . . . . . . . Methods . . . . . . . . . . . . . . . . . . . . Study sites . . . . . . . . . . . . . . . . . . . Results . . . . . . . . . . . . . . . . . . . . Diversity and colonization patterns of iMacaranga-associated ants Geographic distribution of plants . . . . . . . . . . Geographic distribution of ants . . . . . . . . . . . Discussion . . . . . . . . . . . . . . . . . . . Specificity . . . . . . . . . . . . . . . . . . Comparisons with other ant-plant systems . . . . . . . Altitude . . . . . . . . . . . . . . . . . . . Possible basis of specificity . . . . . . . . . . . . Geographic distribution . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 307 308 308 309 3 10 310 315 320 32 1 32 1 323 324 325 326 328 329 INTRODUCTION Ecological interactions between competitors or mutualists probably belong to the principal forces driving diversification and specialization in many lineages of organisms. In mutualism research, taxon specificity and degree of obligateness of associated partners are issues of special significance (Buckley, 1982; Thompson, 1994). A broad variety of mutualistic associations exists between ants and plants which are therefore especially suited for studies on evolutionary specialization. The ants benefit from food and partly also nest sites supplied by the host, and the plants benefit from protection against herbivores and vines (e.g. Beattie, 1985; Huxley, 1986; Davidson & McKey, 1993a). Ant-plant mutualisms in the Neotropics have received much more attention than in Oriental regions. Therefore, our knowledge about the community ecology of these relationships is still very fragmentary. The most prominent such system in SE Asia consists of the important pioneer tree genus Macaranga (Euphorbiaceae) and its manifold associations with ants. Macaranga is the only plant genus in the Oriental region with such a substantial radiation of myrmecophytes (with 23( +) known myrmecophytic species in the Malay Archipelago). When we began our studies 10 years ago, this system seemed to be rather uniform, consisting of about 20 Macaranga species, two Crematogaster (Decacrema) partner ants and six trophobiotic scale insects of the genus Coccus (Takahashi, 1952; Ong, 1978; Tho, 1978). In the meantime our investigations have revealed a far more complex system concerning life types and species diversity (Fiala, Linsenmair & Maschwitz, 1994a; Fiala, Jakob & Maschwitz, 1996). For an understanding of the ecology and evolution of this system, studies on the distribution and specificity of the associations are of central importance. The aim of this paper is to provide an extensive overview on the SE Asian myrmecophytic Macaranga-complex, covering the whole distribution area. It is, to our knowledge, the first summarizing survey of this kind. We have compiled data about the distribution of ant and plant species involved in different regions and habitats. T o assess the specificity of the relationships between myrmecophytic Macaranga trees and their ant associates, we examined the occupancy by ants of large specimen bases of more than 2000 Macaranga plants in the tropical forests of SE Asia. We present here data on diversity, abundance, biogeography, and patterns 3UC.IMVGrl-ANT ASSOCIATIONS IN SE ASIA 307 of species associations of one of the most complex and ecologically important antplant mutualisms in the Asian tropics. NATURAL HISTORY OF T H E SYMBIOTIC PARTNERS T h e plants Macaranga is one of the world’s largest genera of pioneer trees (Whitmore, 1984). It comprises 280 species with a range stretching from West Africa through Asia to the Fiji Islands (Whitmore, 1969). In Asia, at least, Macaranga are trees mainly of humid forest with the centre of their distribution in the lowland dipterocarp rainforest areas. Following the anthropogenic destruction of the forest, species of Macaranga now dominate the tropical landscape along roadsides and have become one of the most conspicuous trees in cleared areas. The original habitat of most Macaranga species seems to be gaps in the forest (Whitmore, 1969) as well as forest edges and stream banks. The genus Macaranga comprises the full range from species not ant-inhabited but myrmecophilic, to occasionally colonized species, to obligate ant-plants (review in Fiala, 1996). Most myrmecophytic Macaranga species offer nesting space for ants inside internodes which become hollow by themselves due to degeneration of the pith. Their seedlings can already be colonized by ants when they are only about l 0 c m tall (then possessing but one internode suitable for colonization). In some species, however (Macarangapearsonii Merr., M. hosei King ex Hook f., and M. pruinosa (Miq.) Muell.Arg.), the stem’s interior does not become hollow but remains solid. The pith, however, is soft and dry, and ants can remove it, thus forming internal cavities (Fiala, Maschwitz & Tho, 1991; Fiala & Maschwitz, 1992a, b). (We have formerly called these true myrmecophytes ‘intermediate’ or ‘transitional’, which caused some misunderstanding since this was understood to mean ‘evolutionary intermediate’. However, with this expression, which we will not longer use, we always meant only morphological differences between these species and those with selfhollowing domatia, which we termed ‘obligate myrmecophytes’.) The colonizing queen must be able to find and recognize a host plant, sometimes in very dense undergrowth and isolated gaps in the forests. When she finds an unoccupied plant, she sheds her wings and chews an entrance hole into an internode, which she then seals from inside. Colony foundation is thus claustral and we do not yet know whether the queen uses any food resources inside the plant during that time (such as pith). When the first small workers emerge, they reopen the entrance or chew new holes. The ants live mainly on food bodies produced by the plants, and from honeydew produced by scale insects cultivated inside the stem (extrafloral nectaries do not play a role in most obligate myrmecophytic Macaranga species, Fiala & Maschwitz, 1990, 1991, 1992a, b). The scale insects colonize the plant only after the emergence of the first workers (details about associated coccids see Heckroth et al., 1998). The most important ecological function of the ants for the plant is protection against herbivore damage and climbers (Fiala et al., 1989, 1994a, b; Heil et al., submitted). (For further details on ecology and biology of ant-associated Macaranga see work of Fiala and colleagues, e.g. Fiala, 1996 and refs. therein, as well as Federle et al., 1997; 1998a,b; Heil et al., 1997a, b). 308 B. FIALA ETAL. ?he ants Ant-associations in Macaranga have been proved to be much more diverse and complicated than previously thought. Most occupants are ants of the genus Crematogaster (subfamily Myrmicinae). What in the beginning of studies on a few Macaranga species appeared to be a single ant species-named Crematogaster borneensis Andrt (Ong, 1978; Tho, 1978; Fiala, 1988)-in the meantime has turned out to be a large number of similar species. With one exception (see Results) they belong to the subgenus Decacrema, which is easily identified by its 10-segmented antennae. Within this subgenus, however, the taxonomic relationships are still obscure (as it is also the case within the genus Macaranga. We have only recently started a phylogenetic analysis). The cosmopolitan genus Crematogaster is one of the largest ant genera, and no revision of this genus has been carried out. A large number of species, especially in Asia, remain undescribed. The only available information is a brief checklist of Asian Crematogaster species from Chapman & Chapco (195 1). Bolton (1 995) may be considered for an enumeration of described Crematogaster species. The earlier taxonomic literature on Macaranga ants is scarce and scattered, containing descriptions of various species, ‘subspecies), and ‘varieties’ based on only few individuals, mainly workers which are mostly unsuitable for species identification. Neither identification keys nor cladistic analyses have yet been developed. We have therefore worked on the taxonomy of the ants and are producing a key for identification of the Crematogaster species that are obligate Macaranga inhabitants, which will be reported in detail elsewhere. The ants are at present being described but since this is still incomplete, we will use morphospecies numbers here. Besides the associations with the dominant Crematogaster only few Macaranga species are known to be inhabited by specialized ants from other taxa (all from the subfamily Formicinae): (1) Macaranga puncticulata Gage on the Malay Peninsula is specifically colonized by a Camfonotus (subgenus Colobopsis) (Federle et al., 1998a, b) (2) One species from Borneo, Macaranga lamellata Whitmore, and one from East Thailand, M. motlgana (Muell. Arg.) Whitmore is also associated with two (different) Camponotus species, the first a non-Colobopsis, the second a further Colobopsis (Maschwitz et al., 1996, and unpubl. results) (3) In one species, Macaranga caladi$lia Becc., the domatia open by themselves (in contrast to all other myrmecophytic Macaranga species observed until now) and give access to a great number of unspecific, opportunistic arboreal ants (Fiala, Maschwitz & Linsenmair, 1996) (4) Macaranga pruinosa, which grows in secondary peat swamp forests of WestMalaysia and Sumatra, is a case apart. This species can be inhabited by specialized plant-ants and by generalist species which forage or nest on the tree (Federal et al., 1998a). In this survey we will concentrate on the Macaranga species inhabited by ants of the genus Crematogaster. METHODS Distribution and occupancy data were gathered during field work from 1984 to 1998. Additional information was obtained from collections in museums and herbaria. ILIACARRVGA-ANT ASSOCIATIONS IN SE ASIA 309 Figure 1. Main study sites in SE Asia. In addition, samples were also obtained in other places, e.g. along roadsides or in small forest patches between these sites. Ant specimens were obtained from plants of all sizes, from saplings to mature trees. Inhabiting ants were examined in the field or collected and identified later. The results presented here rely almost entirely on the identification of queen ants. Most Crematogaster species involved can only be identified to species by queens, partly by criteria identifiable through the use of a hand lens, partly only by morphometric measurements. Workers are very variable in colour and size, and often indistinguishable between different species. Queens, however, can mostly be interspecifically differentiated and are obtained rather easily, especially from young saplings or as winged sexuals from branches of large trees. STUDY SITES Surveys took place mainly in Malaysia (Malay Peninsula, Sabah and Sarawak) and in Indonesian Borneo (Kalimantan), but also in parts of Thailand, Sumatra and on some of the islands east and west of Sumatra (Riau and Lingga Archipelago as well as Nias, Siberut and Banyak Islands; see Fig. 1 and Table 1 for information on main collection sites). In addition, parts of (West and East) Java, Bali, northern Sulawesi and northern Palawan (Philippines) were searched for myrmecophytic Macaranga. The plants were sampled randomly as they were encountered, but we always 310 B. FIALA ETAL. obtained samples from all species present in a local population. We collected in primary forests as well as in secondary habitats with different degrees of disturbance. T o sample the entire altitudinal range of ant-Macaranga associations we visited most of the hill regions in Peninsular Malaysia (Genting Highlands, Bukit Fraser, Bukit Larut, Cameron Highlands; elevation up to 1800 m) as well as the Gunung Kinabalu Park (Sabah, Borneo; up to 4000 m). In total, 21 myrmecophytic Macaranga species were surveyed, of which 19 were found to be colonized by Crematogaster ants. These 19 species will be treated in detail in this paper. RESULTS Diuersip and colonization patterns of Macaranga-associatedants Whole distribution area A total of 2163 ant queens were identified from 19 Macaranga species. Twelve species ( + one subspecies) occur only on Borneo (M. aetheadenia Airy Shaw, M. beccariana Merr., M. calcicola Airy Shaw, M. depressa Muell. Arg. and M. depressa ssp., M. havilandii Airy Shaw, M. indistincta Whitmore, M. kingii var. plapphylla Airy Shaw, M. lamellata, M. pearsonii, M. petanaspla Airy Shaw, M. trachyp/ylla Airy Shaw, and M. winkleri Pax & H o h . ) . Six species occur in Borneo, Peninsular Malaysia and Sumatra (M.hosei, M. hullettii King Ex Hook.f., M. bpoleuca Muell. Arg., M. motleyana, M. pruinosa, and M. triloba Muell. Arg., (M. triloba might change its name to M. bancana (T.C. Whitmore and SJ. Davies, pers. comm.), but since this is not yet published, we will use the present name.) We found one species only in Peninsular Malaysia (M. constricta Whitmore et Airy Shaw) and one subspecies only in Sumatra (M. kingii ssp. kingii Hook.f., which was reported also from southern Peninsular Malaysia (Whitmore, 1973). Some Macaranga species have very local distributions; therefore it was not possible to obtain equal-sized samples of all collected plant species and sites (see Table 1 for number of sites). However, from 13 Macaranga species we have >50 samples and only from one very rare species we could obtain less than 20 samples. Sample sizes of trees therefore reflect the natural abundances of these species. No field collections were possible from the following rare species with very restricted distribution: M. kingzi var. kingii from Peninsular Malaysia, and M. rostrata Heine, M. sarcocarpa Airy Shaw, M. winkleriella Whitmore, and M. puberula Heine (all Borneo). For the last two species we could check one ant sample each from herbarium specimens. According to our results, at least eight Crematogaster species of the subgenus Decacrema are involved in regular colonization of these Macaranga species. In addition, a further Crematogaster species which does not belong to the subgenus Decacrema (probably Atopogyne) also occurs as a regular Macaranga ant-partner (Fig. 2). Given the present state of taxonomic knowledge of the SE Asian ant fauna, determination of ants to named species is rarely possible. This is especially true for the genus Crematogaster as explained above. We have therefore sorted our samples to distinct morphospecies, based mainly on queen morphology. Almost all (98%) of the myrmecophytic Macaranga plants collected contained at least one Crematogaster queen. Often multiple colonization of saplings occurred, but in larger plants usually only one monogynous colony was found and also no species ,ZWC4R;FWGA-ANT ASSOCIATIONS IN SE ASIA 31 1 TABLE 1. Occurrence of the different species and number of study sites in the main regions of the whole distribution area of myrmecophytic Mucurungu. Abbreviations: = species does not occur in this region, 0 = no sample could be obtained, Pen. Mal. = Peninsular Malaysia, Sab = Sabah, Sar = Sarawak, Kal = Kalimantan, Sum = Sumatra including islands of the Riau and Lingga Archipelago ~ hfacarunga species Pen. hlal. aetheadenia beccariuna calcicola' constricta' depressa hauilandii hosei hullettii lypoleuca indirtinch kingii var. kingii' kingii var. plap. lamellata' motlgana pearsonii petanosplaj pruinosa truclyplylla triloba winkleri number of main sample sites in different regions Sab Sar Kal 2 4 1 5 I 0 1 Sum 2 7 117 I 0 1 2 l? 9 0 3 * 3 9 1 4 4 3 4 3 -? I 1 4 3 4 ' M calcicola is rare and restricted to limestone; ' ,2f. constricta occurs on a few hillsides in eastern Pen. Mal.; ',W. kingii var. kinpii is a very rare species with a disjunct distribution in the Riau province in east Sumatra and in the state Johore in south eastern Pen. Mal.; ',V.lamellata had been known from a single specimen from Sabah (Whitmore 1975, but was found to be abundant in Lambir Hills, Sarawak. However, we found only one more plant at Santubong, near Kuching). 'M. petanospla was only reported from the Kinabalu area, Sabah PVhitmore 1975). * M . pruinosa in Sarawak differs morphologically from the plants in Pen. hlal., and was never found ant-inhabited in Borneo. becomes polygynous later. Macaranga saplings sometimes (about 4%) also contained nests of other ants from a wide range of genera. Most of these were common arboreal species gaining access through shoot-borer holes or other injuries. These ants were found only rarely in mature trees. An exception was M. pruinosa, which is inhabited by specialized plant-ants but on which generalist species may also forage or nest. Chi-square tests show highly significant non-random distributions of distinct Decacrema species in Macaranga plants (all values of all combinations P<O.OOO 1). Also, when comparing distributions at sites with several sympatric Macaranga we found clear numerical dominance of several species on different Macaranga plants. This picture becomes even clearer, when we differentiate between values for seedlings with only foundresses, and larger plants with established colonies or even with production of female alates (i.e. for which colonies in Macaranga grow to sexual maturity). Most of those species which were still colonizing saplings were absent from larger plants. In larger plants ant species were associated with a maximum of seven Macaranga species whereas a single Macaranga species maximally had three ant occupants. Some species which we rarely found as colonizing queens, however, never were recorded to establish large colonies or even produce sexuals. This is no bias based on larger samples sizes for saplings since for most species we have similar proportions from all size classes. B. FIALA E T A L . 312 250 A 200 % 100 50 n " hul< 600m hul> 600m tri < 600m hyp tri > con 600m Macaranga sp. hos mot pru U El 2 100 $ 80 E 60 40 20 0 cal dep hul ind kin pet tra tri bec hau hyp aet hos pea lam win Macaranga sp. Figure 2. Colonization patterns of Macaranga species by Crematogaster Msp. 1-9 in our main study areas Peninsular Malaysia (A) and Borneo (B). Plant species are arranged within sections according to Whitmore (see Table 7) and within the sections to their main ant colonizers (exception: M. lamellata due to its differing colonization also by Camponotus sp.), Key to abbreviations: aet: M . aetheadenia, bec: M. beccariana, cal: M. calcicola, con: M. constrirta, dep: M. depressa and M. depressa ssp., hav: M. hauilandii, hos: M. hosei, hul: M. hullettii, M. hypoleuca, ind M. indistincta, kin: M. kingii var. plappyphylla, lam: M. lamellata, mot: M. motlqana, pea: M. pearsonii, pet: M. petanosbla, pru: M. pruinosa, tra: M. tracbphylla, tri M. triloba, win: M. winkleri. (Morphospecies numbers are different from those used in Fiala et al., 1994b). In general, specificity must be examined from two viewpoints: that of the plant and that of the ants. In single Macaranga species we found between one and seven ant species, while queens of single ant species colonized up to 12 Macaranga species IZULXRAAGA-ANT ASSOCIATIONS IN SE ASIA 3 13 TABLE 2. Frequency of occupancy for the whole distribution area: (A) view from the ant side, (B) view from the plant side. Percentages indicate the proportion of each ant/iWucaranga species found associated with the respective Macaranga/ant species. The highest values are given in bold letters. A is to be read vertically following columns. Example: from 151 queens collected of species Msp. 1, 47.68% were found on M. motlqana and 22.52% on M. pruinosa. B is to be read horizontally following rows; example: from 49 ant queens collected on M. aetheadenia, 91 3 4 % belonged to Msp. 2 and 4.08% to Msp.4. Key to abbreviations see Fig. 2. (In addition: kin var kin = M. kingii var. kingii, kin var plag = M. kingii var. plagpyphylla) A n Msp.1 151 Msp.2 309 act 0.66 14.56 bec cal con deP hav - - hul - - - - - - - ind kin var kin kin var pLaQ Lam mot Pea Pet - 0.66 47.68 1.32 - 15.2 1 tra - - tri - 0.65 win - - B n aet 49 96 26 39 90 72 145 176 343 108 15 42 27 157 60 24 81 68 358 187 bec cal con deP hav hos hul hrP ind kin var kin kin var pLag lam mot pea Pet P" trfl Iri win Msp.2 2.04 91.84 - 2.56 - 5.52 6.71 8.33 - 3.70 45.86 3.33 - 41.98 - - - 23.28 - 11.48 - 10.82 - - - 94.48 1.14 1.46 0.93 13.33 2.38 7.41 4.46 96.67 - 7.21 0.36 - - hIsp.3 0.56 - 10.3 1 48.82 Msp.4 4.08 100.00 - - 25.56 78.57 Msp.8 0.24 - - - - 5.44 67.38 - - - 0.47 16.3'3 51.70 - 0.24 - - - - - 12.24 0.24 Msp.5 ~ - - 53.85 - hlsp.6 2.04 100.00 58.52 0.58 44.44 86.67 14.29 - 0.64 - - 50.00 - - 2.33 - 83.09 - - 88.89 48.41 - - 91.67 8.33 - 16.18 18.44 83.82 75.42 - ~ 2.56 - Msp.9 - - 50.00 - 32.41 Msp.7 - - 40.34 Msp.8 189 - - - Msp.7 62 0.24 22.70 - - 58.02 ~ 18.63 0.36 8.68 2.35 1.08 ~ 3.61 21.64 Msp.6 423 8.51 0.18 74.44 - - - - - - - Msp.5 147 14.29 4.16 - - 1Lzsp.l - 4.70 - 2 1.97 - 22.52 P" - - 15.23 5.96 hrP 0.36 - 0.66 44.34 0.65 1.62 0.32 0.65 0.32 0.65 2.27 18.77 Msp.4 553 - - 5.30 has Msp.3 305 - - 3.50 12.96 - 4.76 - - 0.64 - - ~ - 5.03 - 0.28 100.00 - - - (although with very differing abundances; Table 2). Regarding the whole distribution area, plants in general were more specific than the ants. Even when sometimes alate production occurred this still does not mean that the ant species in question was a regular inhabitant. When we exclude all frequencies with rates below 10% then we find maximally two main colonizers per Macaranpa species (with one exception in M. indica) and at most five main plant partners per ant species (Table 2). To allow B. FIALA ETAL. 314 TABLE 3. Diversity of partners for all ant and plant species (expressed as Shannon-Wiener index H’) and evenness of frequency of different partners. (A) Mucurungu species, (B) Cremutoguster species. Key to abbreviations see Fig. 2 .4 aet bec cal con dep hav has hul lyp ind n 49 0.530 0.265 96 0 26 0 1 39 1.279 0.640 90 0.820 0.820 72 1 145 0.308 0.308 176 1.054 0.665 343 1.038 0.370 108 3.853 0.717 kin v. kin v. plag lam mot pea pet prui tra tn‘ =#in kin Shannon-Wiener (H’) Evenness 15 0.567 0.567 42 1.012 0.506 27 0.605 0.382 157 1.315 0.567 60 0.211 0.211 24 0.414 0.414 81 0.981 0.981 68 0.639 0.639 358 1.063 0.41 1 187 0 I B Msp.1 Msp.2 Msp.3 Msp.4 Msp.5 Msp.6 Msp.7 Msp.8 Msp.9 n Shannon-Wiener (H’) Evenness 151 2.101 0.663 309 2.253 0.629 305 2.600 0.926 553 2.301 0.642 147 1.920 0.827 423 1.291 0.430 62 1.399 0.882 189 0.095 0.600 24 0.918 0.918 Shannon-Wiener (H’) Evenness n 1 1 TABLE 4.Number of host plants of Mucurungu-colonizing Cremutoguster morphospecies in different regions. Geographical range (GR) gives information on endemic occurrence in either Borneo or Peninsular Malaysia; all = species occur in Peninsular Malaysia, Sumatra and Borneo. Numbers in parentheses: records of host plant species, where the respective ant species was found only once or twice, have been omitted. No. host plants Msp.1 all and GR Msp.2 all Msp.3 all Msp.4 all Msp.5 all Msp.6 all Pen. Mal. only Sumatra only Borneo only all regions 5 (3) 4 (3) 8 (3) 12 ( 2 ) 2 (2) 3 (2) 2 (2) 10 (7) 12 (8) 4 (3) 2 (2) 3 (1) 5 (5) 3 (1) 1 6 (3) 8 (4) 4 4 6 9 (3) (3) (2) (5) 1 7 (7) 7 (7) Msp.7 Borneo Msp.8 Bornco ~ ~ ~ 3 (3) 3 (3) ~ 3 (1) 3 (I) Msp.9 Pen. Mal. 2 (2) ~ ~ 2 (2) a clear comparison of the data, Table 3 provides a summary statistics giving indices of diversity and evenness for each species of ants and plants. Local populations The asymmetry patterns reported for the whole distribution area are probably due to a more widespread distribution of the ant species compared to the plant species (see Table 4 for host plant numbers in different regions). This picture becomes even clearer when local populations are compared. Since there is rather little overlap in the local species pool of the different sites, it was not possible to gain really comparable data sets with the same species from various regions. In the following we will exemplarily provide data from single sites from all major study regions. All sites were in still rather well-preserved forest areas, mostly old secondary forest. Patches of comparatively pristine primary forest as well as freshly logged parts could also be included in the sites in Sabah, Sarawak, Kalimantan and Sumatra. To allow comparison with the association patterns from the whole distribution area (Table 2), specificity from the standpoints of the two partners at ,!-IACARrlVGA-ANT,ZSSOCIATIONS IN SE ASIA 315 the local-population level is presented from five sites (Table 5, further data on local communities can be obtained from the authors upon request). It becomes obvious that the asymmetry of colonization patterns between ant and plant species is reduced in local populations. In single Macaranga species we found between one and three ant species (with one exception of five ant partners, see Table 5), while queens of single ant species colonized also only up to four Macaranga species. When we again exclude all frequencies with rates below loyo, we then find three main colonizers per Macaranga species and also three main plant partners per ant species. In local communities we did also often find a high frequency of exclusive colonization of only one plant species (see Table 5 for frequencies of 100 YO values). Taxonomic groupings That most ants were not specific colonizers of a single host plant did not mean, however, that they colonized plants in an arbitrary way. Some regular patterns could be revealed. In a correlation analysis we found that certain ant species were associated with groups of certain plant species (Table 6). Significant similarities of ant colonization were found in the following groupings: (a) M. aetheadenia, M. hosei, M. pearsonii, M. pruinosa (Msp. 2); (b) M. beccariana, M. havilandii, M. hypoleuca (mostly Msp. 6 and Msp. 7); (c) M. depressa, M. petanosbla, M. kingii var. pla&phylla (mostly Msp. 3); (d) M. calcicola, M. hullettii, M. indistincta, M. kingii var kingii, M. trachyphylla, M. triloba (Msp. 4). Some overlap (based on common occurrence of Msp. 5) occurred in M. constricta, M. lamellata and M. motleyana. M. winkleri did not match any other Macaranga species in its colonization pattern. Species of Macaranga can be grouped into sections (Whitmore, 1975) by different degrees of morphological similarity (possibly reflecting relatedness). The colonization pattern found often, but not always, mirrors these taxonomic sections. As some of them comprise a large number of species colonized by different ants, we separate these sections according to their ant colonization (Table 7). Geographic distribution ofplants All ant-inhabited Macaranga species were found in Peninsular Malaysia (=Pen. Mal.), Borneo and Sumatra. Despite through searches in the last rainforest remnants in West (Ujung Kulon), Central and East Java (mainly Meru Betiri N.P.) as well as in northern Palawan, we could not find any myrmecophytic plants there. This was also the case in Thailand (north of the Isthmus of Kra). Only in the extreme east of Thailand near the Cambodian border (Chantaburi pocket area, Whitmore, 1984), in a rather disturbed area, were a few individuals of M. motleyana found in a small forest path along a river (they were inhabited by a Camponotus species). We never saw any myrmecophytic Macaranga species in the drier parts of Indonesia, such as East Java, Bali and Lombok. Myrmecophytic Macaranga species also did not occur in the three areas visited west of Sumatra (Nias, Siberut, and Banyak islands), although non-myrmecophytic species were abundant (such as the widely distributed M. tanarius (L) Muell. Arg.; unpubl. survey of our student R. Kern, 1997). Nias has become extremely densely populated and it was impossible for us to find any-even badly disturbed-forest habitat, since all has been converted to agricultural use. We found inhabited myrmecophytic species on some smaller islands which are rather near the Pen. Mal. B. FIALA E'TAL. 316 TABLE 5. Frequency of occupancy for local populations in five different sites: (A) Poring (Sabah, Borneo); (B) Lambir Hills (Sarawak, Borneo); (C) Bukit Soeharto (Kalimantan, Borneo); (D) Bukit Tigapuluh (Sumatra); (E) Ulu Gombak (Pen. Mal.).The upper tables provide the view from the ant side, the lower from the plant side. Percentages indicate the proportion of each ant/Macaranga species found associated with the respective Macaranga/ant species. The highest values are given in bold letters. The upper tables are read vertically following columns; the lower tables are read horizontally following rows (see also explanations in Table 2). Key to abbreviations see Fig. 2. (In addition: kin var kin = M. kingti var. kin@, kin var plaQ=M. kin@ var. pla~pyphylla).Further data on local communities can be obtained from the authors upon request A Msp.1 5 n __ bec deP hav hyP ind Pea Pet Msp.2 16 Msp.3 96 - - - - - - - - - - 100.0 - - 100.0 - 68.75 10.42 ~ Msp.4 67 Msp.6 41 Msp.7 23 24.39 - - - - - 43.48 - 75.61 56.52 - - - 0.99 - - - 32.84 52.24 - - - tri - - win - - Msp.1 Msp.2 Msp.3 - - - - - 75.00 - - - - - - - - - 100.0 7.82 - - 100.0 n bec deP hau hrP ind Pea Pet tri win 10 88 10 31 64 16 16 14 101 B n 15.62 5.21 - 15.62 - - - 93.75 - - 26.31 - - - Msp.1 4 Msp.2 31 Msp.3 52 bec hav has hul - hrP Msp.8 101 1.49 13.43 - Msp.4 - 25.00 54.69 - 6.25 73.68 - - - - - - - 99.01 Msp.6 Msp.7 Msp.8 100.0 - - - - - - 100.0 - - 20.31 1.56 - - - - - - - - - - - 100.0 Msp.4 35 Msp.5 25 Msp.6 85 Msp.7 2 Msp.8 32 Msp.4 Msp.5 Msp.6 Msp.7 Msp.8 ~ 7.69 5.71 - - kin var plag 7.69 lam tra - 23.08 85.71 tri 53.84 8.57 Msp.2 Msp.3 ~ win Msp.1 n bec hau has hul hrP kin var pla& lam tra tn' win 57 22 33 6 8 4 27 42 32 30 - 9.37 - 90.62 - - - - - - - - 100.0 - 3.70 7.41 - - - 66.67 33.33 - 28.57 71.43 - 87.50 9.37 - - - - - 3.12 100.0 iWAURRVGA-ANT ASSOCIATIONS IN SE ASIA 317 TABLE 5. continued C Msp.1 Msp.2 Msp.4 Msp.6 Msp.7 Msp.8 n 2 18 19 31 14 14 29.03 78.58 hau - hul 100.00 - 70.97 88.89 11.11 - - 89.47 - 7.14 - - - - - 100.00 Msp.1 Msp.2 hlsp.4 hisp.6 Msp.7 - - 4500 55.00 - - tri win - n bJP Pea tn win 20 2 26 16 20 14 D n ~ 769 - - 100.0 1000 - - Msp 1 5 hisp 2 22 68.18 hos 80.00 - - bJP - - kin v. kin mot tri - hul bJP kin u. kin mot tri 20.00 - 19 2 26 16 20 14 9.09 13.64 - n hlsp. 1 21.05 78.94 100.0 - 10.00 - 20.00 - 100.0 - hul has - 13.33 60.00 - 85.00 - Msp 4 30 - 26.67 - 43.33 3.33 26.67 - - - - - 450 - 100.0 - Msp 6 18 - - 100.0 - - - - Msp.6 - 90.00 - E n hl~p.1 3 Msp.2 38 Msp.3 20 hlsp.4 78 Msp.6 44 hos - 100.0 - - - hul - - 75.00 hvP 100.0 - - - - 25.00 43.59 1.28 55.13 n Msp.1 Msp.2 Msp.3 Msp.4 38 49 48 48 - 100.0 - - - - 30.61 6.25 - - - - 69.38 2.08 89.58 hul bJP tri 10.42 Msp.8 769 - hos ~ - - 86.67 20.00 100.0 - 84.62 Msp.4 - - - Msp.2 ~ 14.28 - tn - - - - bJP hul 10.53 - P" hau - - - 100.0 -- hlsp.6 - 91.67 mainland (Pulau Pangkor (four species), Pulau Tioman (two species) (but none on Pulau Langkawi in the north of Pen. Mal.) as well as in the Riau Archipelago between Sumatra and Pen. Mal. (Pulau Bintan (with two species and Pulau Lingga with four). A number of Macaranga species had a very limited distribution. M. constricta is endemic to forest hillsides in central Pen. Mal. (Whitmore, 1973) and was only found in two primary forest sites (with slightly disturbed parts) west of Kuantan (east coast). M . petanaspla, M. depressa, and M. depressa ssp. (treated as one species below), B. FIALA E'TAL. 318 ** f : f :: * I * ** * * I ** ** I 1 ** 1 : I * I * ** ** * * ** * * ** * * : ** ** I * * I * I * * ** ** $ * I ** f I * * * ** ; * I : I I : * I I I ** I * * ** ** *: ** * ** * * * MAUM.NGA-ANT ASSOCIATIONS IN SE ASIA 319 TABLE 7. Colonization patterns of ants in regard to taxonomic sections (small capitals) of Mucurungu plants (sections after Whitmore, 1975) SECTION PACHYSTEMON SE~VSUSTRICTO (a) inhabited mainly by Crematogaster (Decacrema) Morphospecies 3 & 4: M. calcicola, M. depressa, M. hullettii, M. indistincta, M. kin@ (both ssp.) M. petanos$u, M. trachyph$la, M. triloba. (b) inhabited mainly by C. (Decacrema) Msp. 6 & 7: M.hypoleuca, M. beccariana and M. hauilandii. (c) inhabited mainly by C. (Decacrema) Msp. 5 (as well as by Camponotus in primary forest): M. lamellata (d) inhabited mainly by C. (Decacrema) Msp. 9 and 5: M. conJtricta (e) inhabited mainly by C. (Decacrema) Msp. 1 and Msp. 5: M. motlgana (f) inhabited mainly by C. (Decacrema)Msp. 2: M. aetheadenia PRUINOSA GROUP M. hosei, M. pearsonii, A4. pubmla, M prninosa : inhabited mainly by Crematogaster (Decacrema)Msp. 2 (and partly Msp. I ) SECTION WINKLER~ANAE M. winkleri, M. winkleriella inhabited by Crematogmter (Non-Decacrema) Msp. 8. were found only in the Kinabalu Park (Sabah). Specimens of M. kingii var. kingii could only be obtained from one remote site in east Sumatra. The population in Pen. Mal. recorded by Whitmore (1969) seems to have vanished due to habitat destruction. Especially widespread and abundant species are M. triloba, M. hosei, M. hpoleuca, and M. hulletti from which more than 100 or even 300 samples were obtained, in Borneo also M. winkleri was also locally very common. Habitat restrictions Macaranga motleyana and M. pruinosa are restricted to rather swampy areas. M. calcicola grows only on limestone (Borneo) and could be collected only from one site near Bau (Sarawak), M. winkleriella is also a very rare limestone species of which only herbarium specimens were available. Macaranga lamellata, M. kingii, M. depressa, and M. PetanosQla were mainly found in rather closed forest. Macaranga hosei, M. pearsonii, and M. winkleri establish almost exclusively in open places, whereas M. triloba, M , hyioleuca and M. hullettii originally grew along rivers or in relatively small gaps in forests but nowadays also occur in rather disturbed secondary forests or along roadsides. In Borneo it was not uncommon to find seven sympatric antinhabited species. Altitude Most myrmecophytic Macaranga species seem to be confined to lowland areas; only a few occurred at higher altitudes. An uninterrupted transect from lowland to mountain forests was not possible in the areas surveyed in Pen. Mal. and Sabah. Either lowland forest was already destroyed, or the hilly regions had been transformed and were very disturbed and no continuous natural vegetation cover existed. In Pen. Mal. only three species were abundant enough for detailed study of altitudinal zonation: M. triloba, M. hullettii, and M. bpoleuca (M.hullettii is the only myrmecophytic species found above 900m). All other species never or rarely (M. hosez) occurred above 700m. At Gunung Kinabalu three abundant species could be checked: M. depressa, M. PetanosQla and M. lypoleuca. Only the first two grew above 900 m. 320 B. FIALA ETAL We found a rather strict and similar altitudinal zonation of myrmecophytic Macaranga species in all regions. A rather sharp boundary seems to occur at about 900m. In all areas studied the borderline of occurrence (of, for example, the abundant species M. hypoleuca and M. triloba) was below this elevation. Interestingly, we found a turnover of the ant colonists at about this altitude (see below). The highest records of all species were at about the same elevation (1255 m for M. hullettii at Bukit Larut in Pen. Mal., 1235 m for M. depressa at Gg. Kinabalu, Borneo). Plants were always colonized by ants up to their altitudinal border; we found no uninhabited plants in higher altitudes. In contrast, two non-myrmecophytic species were found up to almost 1900 m (M. rostrata at 1890 m (Borneo), M. indica Wight at 1880 m (Pen. Mal.). Geographic distribution of ants The distribution of ants matches that of their host plants. Crematogaster species also varied in their distribution, obviously correlated with their several host plant occurrence. So far we have not found them outside the ranges of their host plants. Numbers of queen samples obtained reflect abundance of the respective host plants (see above). Patterns of ant and plants species were partly correlated and they will not therefore again be discussed in detail. However, distributional ranges of ants were usually broader than those of plants. Endemic to Borneo were only two ant species (Msp. 7 and Msp. 8) but 12 Macaranga species; endemic to Pen. Mal. was only one ant species (Msp. 9, which was obviously restricted to the eastern parts of central Pen. Mal.). All other ant species were found throughout all regions, however, with different abundances, Msp. 4 and Msp. 6 being especially widespread. The very patchy and disjunct distribution pattern of Msp. 5 is still rather obscure, with specimens found in Lambir Hills (Sarawak), the east coast of Pen. Mal., and on some islands of the Riau Archipelago between Pen. Mal. and Sumatra. Habitat pr&erences We could not find a clear dependence of an ant species on a specific habitat type which could be disentangled from host plant affinity. Msp. 9 was mainly found in closed forest. However, this habitat preference cannot easily be separated from its restriction to the main host plant species growing in this habitat. The same is true for Msp. 8 and M , winkleri for open areas. Msp. 1 was especially abundant in plants growing in swampy areas (M.pruinosa, M. motleyana) but was also present in species on dry ground (M. hypoleuca, M. indistincta). However, it was usually limited to rather light-rich environments and was found mostly in rather disturbed areas along roadsides. When this species was encountered away from its main host plants, it was often found with alates in rather large trees. This is in contrast to all other species occurring only in low abundance on other than their main host plants: they were usually found only as colonizing foundresses in saplings. Msp. 2 was found more often in light-rich, slightly disturbed sites-its main host plants rarely grew in other habitats. Msp. 3 occurs in two forms, sometimes with differing degree of pilosity. These could not be separated morphometrically but may, nevertheless, represent two ecotypes or even sibling species. One was found in the lowlands, especially in Sarawak (‘lowland type’); the other occurred in higher altitudes, particularly in Sabah and Pen. Mal. (‘mountain typ’). Msp. 3 was found’on ridges M C 4 U G A - A N T ASSOCIATIONS IN SE ASIA 32 I in closed forest as well as along logging roads, but perhaps preferred less disturbed areas. Also Mspp. 4, 6 and 7 occurred in closed forests as well as on logging roads. Only the rather rare and scattered Msp. 5 can probably be regarded as being replaced on their host species in a different habitat: in Lambir Hills (Sarawak) it was very abundant on M. lamellata in disturbed areas. Inside the primary forest, however, M. lamellata was mainly colonized by Camponotus sp. (see also Maschwitz et al., 1996). Msp. 5 was also found on saplings of M. hypoleuca, M. motleyana, and M. constricta, always in rather disturbed areas. Altitude Like their host plants, most ant species seem to be restricted to lowland areas, with the exception of the ‘mountain type’ of Msp. 3 which sharply increased in abundance in higher elevations (above about 600 m a.s.1). Especially remarkable was a transition zone which could be surveyed especially well in Pen. Mal., where a species turnover occurred in those species which reach a higher altitude, M. hullettii and M. triloba. Both species are in Pen. Mal. lowland areas usually inhabited by Msp. 4. However, from about 500m upwards, Msp. 3 occurs and becomes increasingly dominant (Fig. 2). It was the only species found above 900 m in Pen. Mal. A similar phenomenon was found for M. depressa at Mt. Kinabalu. In this transition zone single saplings can be found colonized by queens of Msp. 3 as well as by Msp. 4. The proportion of colonization of these species changes with increasing elevation until only Msp. 3 remains. M , petanosgla, also inhabited by this species, rarely occurred below 900 m but was in one case reported with Msp. 4., The ‘lowland type’ of Msp. 3 was especially abundant in M. triloba and M. kingii var. plapphylla in Sarawak. DISCUSSI 0N The results of our survey demonstrate that myrmecophytic Macaranga are usually colonized very specifically by a small group of obligate ant partners dominated by Crematogaster species of the subgenus Decacrema. It now appears that the CrematogasterMucurangu system, like plant-ant associations from the Neotropics (e.g. Longino, 1991; Davidson & McKey, 1993a, b), is a diverse and complex community of superficiallysimilar species. In SE Asia at least nine species of Crematogaster are obligate inhabitants of Macaranga trees. During our studies on SE Asian myrmecophytes we came across a great number of other potential host plants (also from other plant families) for ants but we have never found any of the Macaranga-associated Crematogaster on them. We know of only one record of a C. borneensis from the ant-fern Lecanopteris > 1300 m at Kinabalu Park (Gay & Hensen, 1992). However, taking into account the very difficult taxonomy of this group especially when using only workers, we consider misidentification a likely possibility. This is also indicated by other factors such as the high altitude, the (totally atypical) presence of carton runways in the nests, and the authors’ opinion that the ant in question was very similar to C. treubi Emery, which is not a Decacrema. 322 B. FIALA ETAL. Our survey could not cover all regions and habitats. For instance, there was little material from primary forests on limestone and from remote swamp forests in Sumatra and Indonesian Borneo. Furthermore the few myrmecophytic Macaranga species that could not be included in the study might be colonized by different ant species. Nevertheless, we have extensively sampled the regularly occurring ant inhabitants of Macaranga all over its distribution range and these include the species especially interesting as to questions of specificity. The nine ant and 19 plant species were not associating at random. Despite the sympatric distribution of different Macaranga-Crematogaster associations on a small spatial scale, in most cases rather high specificity was maintained, although some overlap did exist. Especially remarkable is M. winkleri and its partner ant Msp. 8, where both sides seem to be extremely specific. Based on observations from at least 10 different sites M. winkleri was never colonized by any other ant species and Msp. 8 was only found twice on another Macaranga plant, despite through checks of all other species at the sites (and additional checks of about 300 saplings which are not included in the list of identified samples). O n the ant side, no other species had such high specificity. We could not obtain equal sample sizes and equal numbers of sites surveyed for each Macaranga species. Therefore the question may arise as to whether the number of partners recorded for an ant or a plant is likely to increase with increased sampling effort. Analysing the data set, however, the number of ant species recorded for each host-plant species is not closely correlated with the sample size for the host plants. This implies that conclusions would not change with increasing sample size. The two species with the highest sample size actually had the highest numbers of ant species recorded; however, some very abundant species such as M. winkleri, M , hosei and M. hullettii were nevertheless found with only one or two partners. From the ant’s point of view there does appear to be a stronger correlation between the total number of queens collected and the number of records from different host plants. However, since the number of ant species per plant was well estimated by the existing sample size, this correlation is probably better explained by the assumption that the more common ant species have more hosts, which is supported by our data of number of host plants in different regions (Table 4). In addition, our results from surveys of local communities support our assumption. We usually found the general pattern of host specificity very well represented at single sites, although numbers of partners of both ant and plants were in general lower at single sites compared to the whole distribution area. Therefore we regard the pattern found as a real existing geographical one. Besides, we have to consider that this discussion so far was based on the complete records for each species. However, the high number of associated species is mainly due to inclusion of records of species found only once or twice on this respective Macaranga plant. The larger the absolute species number per host plant, the higher the proportion of records of less than 5% occupancy on this species (Table 2). Over the whole distribution area patterns of ant inhabitation seem to be more specific from the plant than from the ant side (a maximum of three species was found to reproduce in each Macaranga plant, whereas winged females of the ant Msp. 4 were found on seven Macaranga species). However, this pattern is modified when regarding local populations form a single site, so this asymmetry is partly a result of the fact that the ant species have a more widespread distribution than each of the plant species. .\ZACARrtVGA-ANT ASSOCIATIONS IN SE ASIA 323 An even more specific picture emerges if one analyses which ant species were found on which Macaranga species. The host species occupied by a given ant species tend to be morphologically similar and probably closely related, reflected in part by their placement in taxonomic sections of the genus (Whitmore, 1975). Some of them can be regarded as sister species (e.g. M. beccariana, and M. hypoleuca, Davies, 1996). Our first molecular analyses (Blattner et al., unpublished) confirm that some of our groupings (Table 7 and Fig. 2) match probable phylogenetic relationships very well. This is especially true for the Section winklerianae, the pruinosa-group (mainly inhabited by Msp. 2), and the group comprising M. beccariana, M. havilandii and M. hypoleuca (inhabited by Msp. 6 and Msp. 7). Surprisingly, other myrmecophytic members of the section Pachystemon show comparatively little genetic variation, which may indicate rather recent radiation in this section. This would be in accordance with the relatively high numbers of host plants of Msp. 3 and Msp. 4, which mainly colonize species from this large group. We do not yet know much about the relationships within the subgenus Decacrema. However, considering morphological similarity of the ants, some patterns emerged which partly fit the association patterns found very closely (e.g. in Msp. 6 and 7). However, we will not speculate about this aspect here, but leave that discussion to our detailed study on the taxonomic relationships of Macaranga-inhabiting Crematogaster ants. Comparisons with other ant-plant system5 Although both lifelong association and the absolute requirement for a partner are thought to favour species-specificity (Schemske, 1983), few obligate myrmecophytes are known to have monophilic associations with ants (see reviews by Davidson & McKey, 1993a,b). Some plant-ants dwell in a number of unrelated plants, others inhabit several related host-species. However, few genera include large numbers of myrmecophytic species and little detailed information on their colonization patterns exists. We will look at three of the most prominent. The most pertinent myrmecophytic association for comparison with Macaranga (and one a the few with a comparable degree of information on diversity and species richness) is its Neotropical analogue, Cecropia. Here, the majority of the myrmecophytic species are inhabited by ants of the dolichoderine genus Azteca, but a few additional ant genera (Pachyconajla, Crematogaster, Camponotus) are found, though less frequently (Longino, 199l), a pattern we also find (with different genera or species)in Macaranga. In both systems, the queen ants ofthe main colonizers show the greatest morphological differentiation between species whereas workers are intraspecifically variable, and cannot always be identified to species. However, in contrast to the Crematogaster plant-ants, the AZteca species on Cecropia have in recent times been intensively studied and extensive information on taxonomy, phylogeny, ecology and host specificity exists (e.g. Davidson & Fisher, 1991; Longino, 1991; Ayala et al., 1996; Folgarait & Davidson, 1994, 1995; Yu & Davidson, 1997). Another diverse system occurs in central America between swollen thorn acacias and obligate ant species of the genus Pseudomyrmex. Ward (1993) pointed out that only 3/ 1 1 common colonizers were confined to one host plant species. It seems that most species occupy any swollen thorn acacia species available to them. The very abundant Pferrugineus F. Smith was even found on 10 acacia species. 324 B. FIALA E T A L . Investigations of the SE Asian plant associations with the ant genus Cladomyrma revealed 18 plant species from nine different genera and eight families as host plants (Moog et al., in press). In Pen. Mal. one species inhabits six host plants from six different genera, although in Borneo there also exist species which are at present known only from one or two host plants (Agosti, 1991;J. Moog, pers. comm.) Mono- and oligophily are not necessarily a consequence of strong evolutionary co-speciation. As in other mutualisms (Jordano, 1987) they may be the outcome of ecological species-sorting, whereby environmental factors produce specific patterns of association. Support for this assumption comes from recent studies on the Cecropia(Ayala et al., 1996) and Leonardoxa-ant associations (Chenuil & McKey, 1996), and on the Pseudomymzex ant partners of Acacia (Ward, 1991, 1993). For other myrmecophytic systems no phylogenetic analyses exist, although available data, reviewed by Davidson & McKey (1993a, b) so far suggest that specific ant-plant associations originated by ecological fitting rather than through direct co-evolution. Our data on the rather habitat-independent regularity of Macaranga-ant associations, however, make the assumption of a closely coevolved system an alternative that cannot be easily discarded and, therefore, merit close scrutiny in the future. Phylogenetic analyses of the complex are not yet available. A cladistic analysis of the myrmecophytic section Pachptemon was conducted by Davies (1996). Not all his plant groupings matched ant-colonization patterns. So far, we can only conclude in agreement with Davies that ant colonizers in the genus Macaranga are a polyphyletic group, i.e. that ant-plant associations arose several times since ant partners of two different ant subgenera (and even different subfamilies) are involved. Whether the eight Decacrema species associated with Macaranga represent a monophyletic clade or indicate multiple independent colonization of Macaranga cannot be answered at the moment but further studies are underway. Altitude No information at all has existed in the literature about the altitudinal zonation of the ant inhabitation of Macaranga, which has now for the first time been surveyed in this paper. Our investigations in the mountains of Pen. Mal. and Sabah revealed an upper limit for myrmecophytic Macaranga at about 1250 m. This is not a boundary of ant occurrence in general-facultative associations of unspecialized ants with non-myrmecophytic Macaranga species which attract ants by extrafloral nectaries, for example, were still found up to about 1900 m. Not much information about the altitudinal distribution is available from other non-epiphytic ant-plant systems. In Malaysia we found two other specific ant-plants at comparable altitudes: (a) the liana Spatholobus cf. bracteolatus Prain ex King (Fabaceae) was found to be colonized by its Cladomyrma spp. partners also only up to 1300 m in Pen. Mal. (J. Moog, pers. comm.); (b) inhabited plants of Xeonauclea gigantea (Valeton) Merr. (Rubiaceae), which is also associated with Cladomyrma ants, occurred at Kinabalu National Park again up to 1300 m. In contrast to Macaranga, here we found a zone of uninhabited plants up to 1600 m. In the Neotropics, inhabited plants of Cecropia have been reported (as exceptional) from up to 2000 m (Longino, 1989), but Janzen (1 973) states but very few ants occur above 1600 m in Costa Rica. At least at one site three ecologically similar Azteca species have ranges corresponding to three Cecropia species, with the ant-plant pairs hfACAR4VGA-ANT ASSOCIATIONS IN SE ASIA 325 spatially segregated along an elevational gradient (Longino, 1991). However, as in Macaranga-ants the diversity and abundance drops with increasing elevation. Pseudomynnex-inhabitedAcacia have been found mostly in lowland habitats but records from 1360 m exist (Ward, 1993). In general we can conclude that in all tropical regions there seems to be a upper borderline of inhabited myrmecophytic trees which is rather similar at about 1250-1 400 m. At this height only a few myrmecophytic species and colonizing ants can be found. Most such associations are restricted to lowland areas up to about 900m, and some are even found exclusively at low elevations up to 300m. A detailed discussion about possible reasons for this pronounced altitudinal zonation of ant-plant associations goes beyond the framework of this paper. Possible basis ojspec$ci& It is not the aim of this paper to focus on determinants of species-specificity. This question will be treated in detail in a later article including experimental studies. We will, however, briefly discuss a few important aspects relevant for the present survey, even if we know only very little about the biological basis of the specificity of ant colonization-on the level of proximate mechanisms as well as on the level of the ultimate reasons. Specificity of association can be a result of host selection and recognition by the ants, as well as at a later stage involving differential host use and performance. Young saplings are colonized by a number of ant species but only a few species were found to make up the majority of colonies in larger plants. However, certain ant species did dominate the saplings of certain plant species. The increasing specificity of species pairing with the increasing age of the plant points to a stochastic component in colony establishment and to secondary, non-random processes of elimination. These could either be direct effects (plant-mediated reduced survival probability) or indirect consequences of non-optimal matching of the two species (higher competitive ability through special adaptations of a certain ant species to its specific host plant). Most Decacrema ant queens search for and colonize their host at night and must locate smallMucaranga saplings among sometimes dense vegetation. Specificity ofcolonization in myrmecophytic Macaranga was also maintained at rather isolated sites, such as forest gaps, despite rather distant and hidden occurrence of individuals. This requires differentiated and very effective mechanisms of host plant location and points to use of chemical cues in the first phase of orientation. The ability of queens to locate and colonize specific hosts, and their absence from others, provide some of the strongest evidence of evolutionary specialization to symbiosis with particular plants (Davidson &McKey, 1993a).Some ants can learn the odour oftheir nest tree speciesby imprinting (Holldobler & Wilson, 1990; Dejean, Djieto & Ngokam, 1992),so that queens possibly prefer to found colonies on the same tree species on which they grew to maturity. However, genetic fixation could also play a role. The mechanisms of host recognition are not yet known from any myrmecophyte-specialist ant. Mechanical properties can play an important role in close-range orientation. A previous study has already reported on one plant feature which seems to restrict the spectrum of colonizers, i.e. a waxy layer on the stem surface. Ants differ strongly with respect to their capacity to move on the glaucous stems, suggesting a mechanism which may restrict host-switching and promote host-specificity (Federle et al., 1997). 326 R . F I A W ETAL. The final ultimate causes which prevent the ants from colonizing plants other than their ‘usual’ hosts are even less known than the proximate factors. The ant species could have special adaptations to a particular plant species which might decrease their competitive ability or their survival on the ‘wrong’ host plant. We do not yet know the factors that might influence the outcome of competition. Factors which might be involved in causing and maintaining the diversity and specificity of the relationships might include features that influence ant colonization, such as differences in the structure of domatia, or may lie in the food resources offered by the plants. Presence or absence of essential compounds as well as relative proportions of main nutrients or production rates could favour a single or few species and discourage all other potential dwellers. For example, ants of the genus Azteca predominate on fast-growing hosts in sunny habitats, whereas only trees in shaded environments seem to be occupied by specialized ants from other genera (Davidson et al., 1989, 1991; Davidson & McKey, 1993a, b). Some Cecropia are dominated by Azteca australis Wheeler, which tends to prefer hosts with especially high production of pearl bodies (Yu & Davidson, 1997). Myrmecophytic Macaranga species can also differ largely in the numbers of food bodies produced (Menke, 1996, and other unpublished results of our team). Our first chemical analyses in several species indicate differences also in the chemical composition of food bodies especially in the sugars (Heil et al., 1997a, b) which reflect taxonomic relations within the genus Macaranga. Whether these differences play a role in either host plant recognition or performance of the colony (growth rates and reproduction) remains to be studied, and we are continuing to assess determinants of specificity in the Macaranga-ant associations, which provide an excellent experimental system for these questions. One central question in studies of specificity is whether the colonization patterns found are due to extreme host specificity of the ants and high evolutionary specialisation, or an outcome of habitat restriction of both plants and ants and therefore due to ecological ‘species sorting’ (sensuJordano, 1987 and Davidson et al., 1991). Evidence for host specialization by ants is often confused due to habitat specialization by hosts. Even when ants were restricted to specific habitats this pattern could be interpreted as a result of an adaptation to either the habitat or the host plant, or perhaps as an effect ofpatchy distribution. This can only be disentangled by further experimental work. However, we can draw at least some conclusions from our studies on host plants which occur in different habitats. With the exception perhaps of Msp. 5, which seems to occur in especially disturbed habitats, and a few Macaranga species like M , indistincta, our data do not provide much evidence for habitat specificity which has been reported to be much more obvious in Cecropia (summarizing discussion in Yu & Davidson, 1997). We have many examples from forest gaps as well as from secondary habitats of species occurring side by side which were hosting distinct ant species. However, if one regards altitudinal zonation also as a habitat effect, we can certainly provide a number of examples for such habitat dependence in the patterns of species associations. Much more experimental work will be necessary to answer these questions, therefore we will not focus on this aspect in this study. Geographic distribution The genus Macaranga is unique among non-epiphytic ant-plants in the Palaeotropics in having developed considerable species richness of myrmecophytes. In SE Asia ~2UCARAVGA-AN7'ASSOCIATIONS IN SE ASIA 327 only Neonauclea (Rubiaceae) with 17 myrmecophytic species (Moog et al., in press) is comparable to Mucarungu. In the Neotropics we find at least seven genera with more than 10 ant-plant species, four of them having even more than 20 species (Davidson & McKey, 1993a). For an interpretation of the evolutionary development of the Macaranga-ant associations, specialization processes and possible trends in host-switching and secondary colonizations, information on the biogeography (including historical factors) in this region is required. Some distribution patterns of myrmecophytic Macaranga in SE Asia are summarized below. (1) The myrmecophytic Macaranga and their ant partners in the Oriental region are restricted to the moist tropics of the Malay Archipelago within the floristic boundaries of West Malesia (sensu Steenis, 1950) and do not extend into monsoon forest regions. The associated ant fauna is rather similar in the different areas. Only two species confined to Borneo (Msp. 7 and Msp. 8), and one to Peninsular Malaysia (Msp. 9) suggest a historical geographical barrier, probably one only recently effective after the last glacial period. (2) The western border: myrmecophytic Macaranga were found neither on the Mentawei nor the Banyak Islands which have been separated from the Sunda shelf by a deep (1500 m) sea and have therefore been isolated for a long time. We have records ofM. triloba from the Nicobar islands (Chakrabarty, 1987)but no confirmation of the identification and no information about ant inhabitation. (3) The eastern and southern border is not identical with the Sunda shelf line. The section Pachysternon, which comprises most of the myrmecophytic species, is restricted to West Malesia. Whitmore regards it as a very aberrant group in the genus with nothing like it east of the Sunda shelf ipers. comm.). M. triloba seems to be the most widespread myrmecophytic Macaranga species. In spite of records of M. triloba from Java (Backer & Bakhuizen van den Brink, 1963) we did not find any in Java, Bali (east of the Wallace line) and northern Sulawesi. (As already briefly mentioned in the introduction, what hitherto to has been considered to be M. triloba might comprise different species. The original M. triloba is probably not even myrmecophytic because most of the collections from Java have solid stems. The myrmecophytic species might have its name changed to M. bancana; T.C. Whitmore and S.J. Davies, pers. comm.). We also found no myrmecophytic Macaranga-associationseven in the moister parts of northern Palawan, an island very close to the centre of diversity of myrmecophytic Macaranga in Borneo. Like Java and Bali, Palawan is situated on the Sunda shelf, which was partly exposed during the last glacial maximum (Whitmore, 1987) about 18 000 years ago (and perhaps also during earlier glacial maxima) so that the separate islands became connected. It is speculated, however, that the exposed shelf areas were covered by mangroves or saline soils and would have resisted the establishment of forest (Chappell & Thom, 1977). Other larger islands of the Malay Archipelago, e.g., the Riau Islands, as well as Pulau Pangkor and Pulau Tioman, are colonized by ant-inhabited Macaranga species. O n Langkawi in the extreme north of Malaysia (which already has semi-deciduous forest) as well as on the small islands Pulau Perhentian and Pulau Gaya (offshore Sabah), no myrmecophytic Macaranga was found. In discussion of the biogeographical distribution of the myrmecophytic symbioses 328 B. FIALA ETAL. it must be kept in mind that almost all systems involving Decucremu ants (and trophobiotic coccids) are obligate associations, and ants and plants as well as associated coccids are not able to survive without each other. Although some birddistributed Mucarungu seeds may have been capable of travelling considerable distances, the lack of Mucurungu on a number of islands led us to assume that other factors than seed distribution may play an important role. The plants usually do not become mature without their ant partners. Searching young ant queens are lost if they do not come across a suitable plant within several hours (pers. obs.). Also the trophobiotic coccids must find an established colony. Thus migration of such a system is in fact only possible in direct contact to already existing intact populations of the partner system. This phenomenon we have also often observed in very disturbed areas in Malaysia: despite a constant seed rain all over the landscape, successful growth of myrmecophytic Macurungu plants can only be found near intact populations. This means that myrmecophytic Mucurungu associations can be very sensitive to all sorts of processes that can cause local extinction, such as geographic or biotic isolation, climatic change, drought, fire or other barriers. The sensitivity to fragmentation and local extinction may explain the lack of myrmecophytic species on small islands or islands strongly influenced by monsoon climate (recently or in the past as on Langkawi or parts of Palawan) and on islands far from the centre of diversity of Mucurungu-myrmecophytism. In addition we still have no idea about the evolutionary age of this symbiotic complex, another important consideration in understanding its distribution patterns. Our data give first hints that the degree of disturbance, as in Cecropia (Longino, 1991), could be a major factor affecting contemporary communities. In primary forests ‘false’ colonization by the ‘wrong’ species occurs rather rarely (pers. obs.) whereas in largely disturbed habitats along roadsides and in clearings host specificity is more often obscured. Some Mucarungu species have remained restricted to forest gaps, but others have followed in the wake of large scale anthropogenic habitat disturbances. Their populations have increased and enlarged their distribution and populations and species originally separated have thus come into contact. The tremendous changes in patterns and abundances of potential host plants confronts the colonizing queens with a new situation which might influence their host selection behaviour. This may in turn lead to change in colonization patterns and the competitive ability of different Mucarungu species and their ant partners. ACKNOWLEDGEMENTS The former director of the Forest Research Institute Malaysia (FRIM) Dato Dr Salleh Mohd. Nor generously gave permission to work at FRIM. The late Dr Tho Yow Pong (FRIM) always took a very active part in the studies and provided support in many ways. We acknowledge the help of the FRIM staff, especially at the herbarium. The Department of Zoology, Universiti Malaya, granted permission to use their field station in Ulu Gombak. In particular, we thank Dr Azarae Hj. Idris for his kind cooperation. We are grateful to the Director of Sabah Parks, Datuk Lamri Ali, for providing facilities and excellent opportunities to work in Kinabalu National Park. We also thank Francis Liew, Rajibi Hj. Aman, Dr Jamili Nais and Kasitah Karim. We are grateful to EPU (and former SERU) for permission to conduct research in Malaysia. M4C4WGA-ANT ASSOCIATIONS IN SE ASIA 329 Over the years, many people have contributed to the studies. Special thanks are due to Dr J. Longino who first shed light on the puzzling diversity of Macaranga ants and helped us tremendously with a first sorting of some of the Crematogaster morphospecies. He also commented on the manuscript. We are very grateful to Dr D. McKey for very valuable suggestions and thorough corrections. which greatly improved the manuscript. Dr T.W. Whitmore provided helpful information on taxonomy and distribution of Macaranga species. We also thank Dr S.J. Davies for his friendly cooperation. Finally we thank our collegues and students in Germany and all of the many people in South East Asia whom we cannot individually name here for contributing to the studies in one way or another. Our colleagues T. Drude, W. Federle, H.P. Heckroth, and R. Kern kindly provided specimens and ant identification and distribution data. We gratefully acknowledge financial support of our studies by the Deutsche Forschungsgemeinschaft. We are also thankful for research grants from the DAAD (German Academic Exchange Service) to B.F. and additional funds of the University of Wurzburg, Zoology 111, to support AJ. REFERENCES Agosti D. 1991. Revision of the oriental ant genus Cladomyma, with an outline of the higher classification of the Formicinae (Hymenoptera: Formicidae). $sternatic Entomology 16: 293-3 10. Ayala FJ, Wetterer JK, Longino JT, Hart1 DL. 1996. Molecular phylogeny of Azteca ants (Hymenoptera: Formicidae) and the colonization of Cecropia trees. Molecular Phylagenetics and Evolution 5: 423-428. Backer CA, Bakhuizen van den Brink RC. 1963. Flora of]ava, Vol. 1. Groningen: Nordhoff Beattie AJ. 1985. ?he evolutionary ecology ofant-plant mutualisms. Cambridge: Cambridge University Press. Bolton B. 1995. A new general catalogue ofthe ants of the world. Cambridge, Mass.: Harvard University Press. Buckley RC. 1982. Ant-plant interactions in Australia. The Hague: W. Junk. Chakrabarty T. 1987. Notes on some Asiatic Euphorbiaceae. 30umal gEconomic and Taxonomic Botany 11: 21-24. Chappell J, Thom BG. 1977. Sea levels and coasts. In: Allen J et al., eds. Sunda and Sahul: Prehistoric studies in South-East Asia, Melanesia, and Australia. London: Academic Press, 275-29 1. Chapman JW, Capco SR. 1951. Checklist of the ants (Hymenoptera, Fomicidae) of Asia. Manila: Bureau of Printing. Chenuil A, McKey DB. 1996. Molecular phylogenetic study of a myrmecophyte symbiosis: did Lonardoxa/ant associations diversify via cospeciation? Molecular Phylogenetics and Evolution 6: 270-286. Davidson DW, Fisher BL. 1991. Symbioses of ants with Cecropia as a function of light regime. In: Huxley CR, Cutler DF, eds. Ant-plant interactions. Oxford: Oxford University Press, 289-309. Davidson DW, Foster RB,Snelling RR, Lozada PW. 1991. Variable composition of some tropical ant-plant symbioses. In: Price PW, Lewinsohn TM, Fernandes GW, Benson WW, eds. Plant-animal interactions: Evolutionary ecology in tropical and temperate regions. New York: John Wiley & Sons, 145-1 62. Davidson DW, McKey D. 1993a. The evolutionary ecology of symbiotic ant-plant relationships. Journal of Hymenoptera Research 2: 13-83. Davidson DW, McKey D. 199313. Ant-plant symbioses: stalking the Chuyachaqui. Trends in Ecology and Evolution 8: 326-332. Davidson DW, Snelling RR, Longino JT. 1989. Competition among ants for myrmecophytes and the significance of plant trichomes. Biotmpica 21: 64-73. Davies SJ. 1996. The comparative ecology of Macaranga (Euphorbiaceae). Unpublished D. Phil. Thesis, Harvard University. Dejean A, Djieto CC, Ngnokam S. 1992. Les relations plantes-fourmis. Nouvel aperGu. Memoires Societe' Royale Belge d'Entomologie 35: 563-567. 330 R. FIALA E T d L . Federle W, Fiala B, Maschwitz U. 1998a. Camponotus (Colobopsis) and Macaranga: A specific two partner ant-plant system from Malaysia. Tropical ~ o o l o g v11: 83-94. Federle W, Maschwitz U, Fiala B. 1998b. The two-partner ant-plant system of Camponotus (Colobopsis) sp. 1 and Macaranga puncticulata (Formicidae: Formicinae; Euphorbicaceae): Myrmecophytic traits of the partner ant. Insectes Sociaux 45: 1-16. Federle W, Maschwitz U, Fiala B, Riederer M, Holldobler B. 1997. Slippery ant-plants and skillful climbers: Selection and protection of specific ant partners by epicuticular wax blooms in Macaranga (Euphorbiaceae). Oecologia 112: 2 17-224. Fiala B. 1988. Biologie, Funktion und Evolution eines malaysischen Myrmekophytiesystems. Unpublished D. Phil. Thesis, University of Frankfurt. Fiala B. 1996. Ants benefit pioneer trees: The genus Macaranga as an example of ant-plant associations in dipterocarp forest ecosystems. In: Schulte A, Schone D, eds. Dipterocarp forest eco.pstems: lowards sustainable management. Singapore: World Scientific, 102-1 23. Fiala B, Grunsky H, Maschwitz U, Linsenmair KE. 1994a. Diversity of ant-plant interactions: Protective efficacy in Macaranga species with different degrees of ant-association. Oecologia 97: 186-1 92. Fiala B, Linsenmair KE, Maschwitz U. 199413. Diversitat von Ameisen-Pflanzen-Interaktionen im siidostasiatischen Regenwald. Andrias Sonderband 13: 169-1 78. Fiala B, Jakob A, Maschwitz U. 1996. Diversity, specificity and geographical distribution of ants inhabiting myrmecophytic Macaranga species in South-east Asia. Global Biodiversity Research in Europe. International Senckenberg-Conference Frankfurt a.M. 9.- 13.12.1996, Abstract volume, 19. Fiala B, Maschwitz U. 1990. Studies on the South East Asian ant-plant association Crematogaster borneeusis/Macaranga: Adaptations of the ant partner. Insectes Sociaux 37: 2 12-23 1. Fiala B, Maschwitz U. 1991. Extrafloral nectaries in the genus Macaranga (Euphorbiaceae) in Malaysia: comparative studies of their possible significance as predispositions for myrmecophytism. Biological Journal ofthe Linnean Socieg. 44: 287-305. Fiala B, Maschwitz U. 1992a. Domatia as most important preadaptations in the evolution of myrmecophytes in a paleotropical tree genus. Plant Systematics and Evolution 180: 53-64. Fiala B, Maschwitz U. 199213. Food bodies in the genus h'acaranga and their significance for the evolution of myrmecophytism. Botanical Journal ofthe Linnean Society 110: 6 1-75. Fiala B, Maschwitz U, Linsenmair KE. 1996. Macaranga caladi$olia Beccari (Euphorbiaceae), a new type of ant-plant among South East Asian myrmecophytic Macaranga species. Biotropica 29: 408-4 12. Fiala B, Maschwitz U, Tho YP. 1991. The association between Macarangu and ants in South East Asia. In: Huxley CR, Cutler DF, eds. Interactions bekoeen ants andplants. Oxford: Oxford University Press, 263-270. Fiala B, Maschwitz U, Tho YP, Helbig AJ. 1989. Studies of a South East Asian ant-plant association: protection of Macaranga trees by Crematogaster borneensis. Oecologia 79: 463-470. Folgarait PJ, Davidson DW. 1994. Antiherbivore defences of myrmecophytic Cecropia under different light regimes. Oikos 71: 305-320. Folgarait PJ, Davidson DW. 1995. Myrmecophytic Cecropia: antiherbivore defences under different nutrient treatments. Oecologia 104: 189-206. Gay H, Hensen R. 1992. Ant specificity and the behaviour in mutualisms with epiphytes: the case of Lxcanopteris (Polypodiaceae). Biological Journal ofthe Linnean Society 47: 26 1-284. Heckroth IEP, Fiala B, Gullan PJ, Maschwitz U, Azarae I Hj. 1998. The soft scale (Coccidae) associates of Malaysian ant-plants. Journal of Tropical Ecologv 14: 1-18. Heil M, Fiala B, Kaiser W, Linsenmair KE. 1997a. Chemical contents of Macaranga food bodies: Physiological adaptations to their role in ant attraction and nutrition. Functional Ecologv 11: 1 17-122. Heil M, Fiala B, Linsenmair KE, Zotz G, Menke P, Maschwitz U. 199713. Food body production in h'iacaranga triloba (Euphorbiaceae): a plant investment in anti-herbivore defence via symbiotic ant partners. 3ournal of EcoloD 85: 847-86 1. Holldobler B, Wilson EO. 1990. Host tree selection by the Neotropical ant Paraponera claoata (Hymenoptera: Formicidae). Biotropica 22: 2 13-2 14. Huxley CR. 1986. Evolution of benevolent ant-plant relationships. In: Juniper B, Southwood RS, eds. Insects and the plant surface. London: Edward Arnold, 258-282. Janzen DH. 1973. Dissolution of mutualism between Cecropia and its AZteca ants. Biotropica 5: 15-28. Jordan0 P. 1987. Patterns of mutualistic interactions in pollination and seed dispersal: Connectance, dependence asymmetries, and coevolution. American Naturalist 129: 657-677. .ZL-lGlIUZ%A-AN'I'ASSOCI.4TIONS IN SE ASIA 33 I Longino JT. 1989. Geographic \variation and community structure in an ant-plant mutualism: Azteca and Crcmbia in Costa Rica. Biotropica 21: 126- 132. LonginoJT. 1991. Taxonomy of Cecropia-inhabiting Aztera ants.Journal OfAaturalHistory 25: 157 1Ll602. Maschwitz U, Fiala B, Davies SJ, Linsenmair KE. 1996. Camponotus and Creniatogaster as partners of one myrmecophytc: A new three-partner association in the genus Mucaranga from Borneo (including description of Camponotus macarangae, new species by K. Dumpert). Erotropica 2: 29-40. Menke P. 1996. Vcrgleichende Untersuchungen zur Futterkorpcrchen Produktion in der sudostasiatischen Ameisenpflanzengattung Macaranga (Euphorbiaceae). Unpublished Diploma Thesis, University of Frankfurt/h4ain. Moog J, Agosti D, Saw LG, Azarae I Hj., Maschwitz U. in press. Host plants of the plant-ant genus Cladomjvma \.$'heeler in Malaysia. MalayJian Journal of Science. Ong SL. 1978. The ant-association in ibi'. triloba. Unpublished D. Phil. Thesis, Kuala Lumpur. Schemske DW. 1983. Limits to specialization and rocvolution in plant-animal mutualisms. In: Nitccki A4H, ed. Coroobtion. Chicago: University of Chicago Press, 67-1 09. Steenis CCGJ, van. 1950. The delimitations of Malaysia and its main plant geographical divisions. Flora Malesiana sr1: I, 1: Ixxx-lxxv. Takahashi R. 1952. Some species of nondiaspinc scale insects from thc Malay Peninsula. Znsecta matsumurana 18: 9-1 7. Tho YP. 1978. Living in harmony. khture .\Ialaysiana 3: 34-39. Thompson JN. 1994. 77ze coeuolutionary proceu. Chicago: University of Chicago Press. Ward PS. 1991. Phylogenetic analysis of pseudomyrmecine ants associated with domatia-bearing plants. 111: Huxley CR, Cutler DF, eds. Ant-plant interactionJ. Oxford: Oxford University Press, 335-352. Ward, PS. 1993. Systematic studies on Pseudomyrmex acacia-ants. Journal of Hymenoptera Research 2: 117-168. Whitmore TC. 1969. First thoughts on the species evolution in Malayan L21acaranga.Biologiral Journal ofthe Linnean Socieb 1: 223-231. Whitmore TC. 1973. Trrejora Of,\lalaya. Vol. 2. Kuala Lumpur, London: Longman. Whitmore TC. 1975. .\lacaranga. In: Airy-Shaw HK, ?'he Euphorbiaceae of Borneo. Kew Bulletin. Additional Series 4: 140-~159. Whitmore TC. 1984. Tropical rainforeJts ofthe Far East, 2nd Edition. Oxford: Clarendon Press. Whitmore TC. 1987. Biogrographical evolution of the Alalgy archipelago. Oxford: Clarendon Press. Yu DW, Davidson DW. 1997. Experimental studies of species-specificityin Cecropia-ant relationships. Ecological I\lonographs 67: 2 7 3-294.