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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 . . . . . . . . . . . . . . . . . . .
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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.
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