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J. HYM. RES. 
2(1), 1993 pp. 13-83 

The Evolutionary Ecology of Symbiotic 
Ant - Plant Relationships 

Diane W. Davidson and Doyle McKey 

(DWD) Department of Biology, University of Ulah, Salt Lake City. Utah 84112; 

(DM) Department of Biology, Universily of Miami, Coral Gables. Florida 33124 


Abstract . — A tabular survey of ant-plant symbioses worldwide summarizes aspects of the evolutionary ecology of 
these associations. Remarkable similarities between ant-plant symbioses in disjunct tropical regions result from 
convergent and parallel evolution of similarly preadapted ants and plants. Competition among ants has driven 
evolutionary specialization in plant-ants and is the principal factor accounting for parallelism and convergence. As 
habitat specialization accompanied the evolutionary radiation of many myrmecophytes, frequent host shifts and de 
novo colonizations by habitat-specific ants both inhibited species-specific coevolution and co-cladogenesis, and 
magnified the diversity of mutualistic partners. 

The comparatively high species diversity of neotropical plant-ants and myrmecophytes probably results from 
two historical factors. Most importantly, influenced by Andean orogeny, greater habitat disturbance by fluvial 
systems has created a mosaic of habitat types unparalleled in other tropical regions; both myrmecophytes and plant- 
ants have diversified across habitat boundaries. Second, the arrival of a new wave of dominant ants (especially 
Crematogaster) may have condensed the diversity of relatively timid plant-ants to a greater degree in Africa and 
Asia than in the more isolated Neotropics. Regular trajectories in the evolutionary histories of plant-ants appear 
to be driven principally by competition, in a manner analogous to the taxon cycles or pulses proposed for other 
groups. 


“In all the plants I have seen bearing sacs on the leaves, to whatever order they belong, it is remarkable that the 
pubescence consists of long hairs having a tubercular base; and although I do not see what connection that peculiarity 
can have with the ants’ choice of a habitation, it is probable they find some advantage in it.” .... “Ants’ nests in 
swellings of the branches are found chiefly in soft-wooded trees of humble growth, which have verticillate or quasi- 
verticillate branches and leaves, and especially where the branches put forth at the extremity a whorl or fascicle of 
three or more ramuli; then, either at each leaf-node or at least at the apex of the penultimate (and sometimes of the 
ultimate) branches, will probably be found an ant-house, in the shape of a hollow swelling of the branch...” (Spruce 
1908). 


INTRODUCTION 

A synthetic overview of the evolutionary ecol- 
ogy of mutualism has been disappointingly slow to 
develop (Bronstein 1991). In large part, this short- 
coming may reflect the composite nature of 
mutualisms, which often arise as parasitisms (Th- 
ompson 1 982), and frequently convey benefits con- 
tingent on physical environments, population den- 
sities, and third or multi-species interactions (re- 
viewed in Howe 1984, Addicott 1985, Law and 
Koptur 1 986, Schemske and Horvitz 1 988, Thomp- 
son 1988, Cushman and Addicott 1991). The lack 
of a conceptual organization for such complex and 
variable associations inhibits a search for patterns 


in historical and ecological factors shaping the 
evolution of mutualism. Complicating this en- 
deavor still further is that most studies of mutualism 
focus on pollination and dispersal systems, which 
account for 80 % of the articles on mutualism in 
Bronstein’ s ( 1991) survey. Despite excellent treat- 
ments available for taxonomically and/or geographi- 
cally restricted suites of such interactions (e.g., 
Heithausetal. 1975, Feinsinger and Colwell 1978, 
Janson 1983, Herrera 1984, Gautier-Hion et al. 
1985, Moermond and Denslow 1985, Gottsberger 
1990, Bronstein 1992), both the overwhelming 
numbers and the taxonomic and ecological diver- 
sity of these interactions magnify the difficulty of 


14 


Journal of Hymenoptera Research 


identifying single or few organizing processes or 
principles. 

Symbiotic associations between ants and 
myrmecophytic plants offer a useful counterpoint. 
Sufficiently small in number to be summarized in a 
single table (Appendix 1 ), they nevertheless occur 
in numbers adequate to provide fertile substrate for 
hypothesis testing. Their presence in tropical re- 
gions throughout the world facilitates comparisons 
among taxonomic and ecological equivalents 
evolved in isolation on different continents (McKey 
and Davidson, in press). Despite their considerable 
diversity and widespread distribution, these rela- 
tionships are relatively uniform in structure. Thus 
all myrmecophytic plants provide permanent hous- 
ing and food to ants which are known or (more 
often) presumed to protect their hosts from her- 
bivory or competition, or to provision them with 
nutrients ( reviewed recently in Beattie 1 985, Huxley 
1986, Jolivet 1986, Holldobler and Wilson 1990). 

Here we provide an overview of the symbiotic 
ant-plant relationships, focusing principally on trees, 
shrubs and hemiepiphytes of the American and 
African tropics. (The epiphytic ant-plants have 
been reviewed recently elsewhere by Davidson and 
Epstein 1989.) This geographic specialization re- 
flects our comparatively poor understanding of ant- 
plant relationships in the Oriental and Australian 
tropics where, with the exception of ant-epiphytes 
(Jebb 1985, Huxley and Jebb 1991 ), investigations 
are fewer in number and less detailed (but see the 
recent proliferation of work by Fiala and Maschwitz 
1990 and 1991, Fiala et al. 1989 and 1991, 
Maschwitz et al. 1989 and 1991). For 
myrmecophytes overall, existing evidence is often 
too meagre for a convincing assessment of the 
fitness consequences of particular associations. We 
therefore avoid using the terms “mutualism” and 
“facilitation” in favor of less restrictive words like 
“association”, “interaction”, or “relationship”. For 
similar reasons, the terms “myrmecophyte”, 
“myrmecophytic” and “ant-plant” are used here 
only to describe plants regularly inhabited by ants, 
without implying that plants either benefit from the 
ants or possess traits evolved principally as ant 
attractants. On occasion, we also refer to 
“myrmecophilic” plants, those which are not sym- 
biotic with ants but produce obvious ant attractants 


such as extrafloral nectaries (EFN’s) and/or pearl 
bodies. 

Our principal themes here are the factors which 
have predisposed particular ants and plants toward 
symbiotic association, and the ecological forces 
which have driven evolutionary specialization in 
each of these taxa. We also summarize the pro- 
cesses generating and maintaining diversity within 
each of these groups, as well as the factors limiting 
species specificity and co-cladogenesis. Finally, 
we speculate about particular evolutionary trajec- 
tories which appear to have occurred regularly 
across independent lineages of plant-ants and ant- 
plants. As a prelude to all the above, we briefly 
review the way in which historical context appears 
to have influenced the evolution of ant-plant sym- 
bioses in the American and African tropics. 

DIVERSITY, BIOGEOGRAPHY AND HISTORY 

Both plant-ants and myrmecophytes achieve 
their greatest richness in the American tropics 
(McKey and Davidson, in press). Among ants, the 
proportion of neotropical and African genera con- 
taining specialized plant-ants is approximately the 
same, whether calculated by biogeographic region 
(respectively, 10 % and 12 % of genera) or for 
mesic tropical environments (12.8 % and 14.5 %, 
respectively). Although the mesic Neotropics hold 
approximately 1 .3 times as many ant genera as does 
mesic tropical Africa (Brown 1973), the latter land 
mass has slightly more genera which contain at 
least one plant-ant. Nevertheless, two of these gen- 
era are monotypic and, based on present knowl- 
edge, the species richness of plant-ants appears to 
be about 3.5-fold greater in the Neotropics than in 
Africa (current estimates of 85 species versus 24, 
including one species in Madagascar). Differences 
in diversity occur principally due to the prolifera- 
tion of plant-ant species within endemic neotropical 
genera. In the New World, significant radiations of 
plant-ants occur in endemic Pseudomyrmex 
(N = 32 species), Azteca (N probably > 20), 
Myrme/achista (N > 6), and Allomems (N 8), as 
well as in cosmopolitan Pheidole (N 6) and 
Pachycondyla (N 4). In contrast, significant 
radiations of African plant-ants are limited to 
Tetraponem (N 5) and Technomynnex (N 6), 


Volume 2, Number 1, 1993 


15 


both widely distributed in the Old World tropics, 
and even these radiations are comparatively small. 

Relative to the ant faunas of both the American 
and African tropics, those of the Oriental and Aus- 
tralian regions appear to be poor in plant-ant genera 
(McKey and Davidson, in press); respectively, only 
5.6 % and 7.3 % of regional ant genera, and 7.3 % 
and 9. 1 % of mesic tropical genera, contain plant- 
ants. Moderate to large radiations of plant-ants in 
the Oriental region include only cosmopolitan 
Crematogaster{ N 8 species) and Compouotus ( N 
7), as well as endemic Cladouiynua (N 5), and 
current estimates of plant-ants are only 24 species 
overall. In the Australian region, encompassing 
northern Australia, New Guinea and associated 
islands, such radiations are limited to endemic 
Anonychomynna (probably > 3 species), and the 
species richness of plant-ants presently stands now 
at only about 1 2 species. Although the numbers of 
plant-ants may increase slightly in these regions 
due to increased sampling effort (cf. Dorow and 
Maschwitz 1990, Maschwitz et al. 1991 ) and taxo- 
nomic revision (e.g., S. Shattuck, 1 99 1 , 1 992b), the 
relative poverty of plant-ants at the generic level is 
likely real. 

Myrmecophytes probably constitute a similar 
fraction of all plant genera in the American and 
African tropics, but their species richness is dis- 
tinctly greater in the Neotropics (McKey and 
Davidson, in press). Again unmatched in Africa, 
major radiations of ant-plants within (mainly) en- 
demic, neotropical genera largely account for this 
difference. Neotropical plant genera with signifi- 
cant radiations of myrmecophytes include endemic 
Cecropia (N 50-60 ant-plant species), Tachigali 
(N 20), Triplaris (N = 17), Tococa (N = 40-45), 
Clidemia (N = 1 5-20) and Maieta (N 15), as well 
as non-endemic Acflc/n(N 12 species), Ocotea( N 
6) and Hirtella (N = 6). In contrast, in Africa only 
Acacia (N 15) and, to a lesser extent, Cuviera 
(N = 8+). Cambium (N = 3-6) and Clerodendrum 
(N 3) contain moderate to large numbers of ant- 
plants, and of these genera only Cuviera is re- 
stricted to the Ethiopian region. Estimates of 
myrmecophyte species richness are about three- 
fold greater in the American than the African trop- 
ics, and maximum local (alpha) diversity may be 
twice as high. Although it is not yet possible to 


estimate the frequency of myrmecophytes in the 
tropical floras of Oriental and Australian regions, 
substantial radiations of myrmecophytes within 
genera are comparatively limited (references in 
McKey and Davidson [in press]). These probably 
include only Macaranga(N 23), Korthalsia{ N = 
7+) and Neonauclea (N = 4+) in the Oriental 
tropics, and Chisocheton (N = 6), Kibara, 
Steganthera , and Semecarpus (each with N = 4) in 
the Australian tropics. Altogether, the Oriental and 
Australian tropics likely hold slightly more than 
100 myrmecophyte species. 

At the generic level, the determinants of ant- 
plant and plant-ant diversity in the American and 
African tropics are probably similar to those regu- 
lating species richness of the floras and ant faunas 
overall (McKey and Davidson, in press). Radia- 
tions of myrmecophytes and plant-ants in both 
areas appear to have been strongly affected by both 
the climatic and geologic histories of the continents 
and to have been correlated with diversification in 
habitat use. As may be common for neotropical 
plants in general (Gentry 1986, 1989 and in press, 
but see Simpson and Todzia [1990] for the high 
Andean flora), generic radiations of ant-plants may 
often be comprised of neoendemics with compara- 
tively recent origins. Frequently geographically or 
edaphically restricted, such species may be prod- 
ucts of a “species pump”, postulated to have gener- 
ated new species through habitat specialization 
during range reexpansions within interglacial inter- 
vals of the Pleistocene (Colinvaux, in press). Al- 
though the diversity of tropical ant species has not 
previously been related explicitly to any similar 
mechanism, a possible link between speciation and 
habitat specialization is evidenced by the observa- 
tion that many plant-ants show greater specificity 
to habitats than to host species (Benson 1985, 
Davidson etal. 1989 and 1991;Longino 1989a and 
1991a). 

Given historical and contemporary differences 
in geological activity, and in correlated rates of 
habitat disturbance on the two continents, the Ameri- 
can tropics should have provided greater opportu- 
nity than did tropical Africa for habitat specializa- 
tion and speciation (McKey and Davidson, in press). 
Topographically, the mesic African tropics occupy 
a comparatively flat and featureless plain, much 


16 


Journal of Hymenoptera Research 


more homogeneous than mesic tropica] America. 
In the Neotropics, orogenic activity in the Andes 
has not only influenced the montane and submontane 
areas directly, but has given rise to the fluvial 
disturbances that helped to create a spectacular 
mosaic of landscapes over the vast Amazonian 
region. No less than 26 % of modem lowland 
forests of Western Amazonia give evidence of 
recent erosional and depositional activity, and ap- 
proximately 12 % of these lands are currently in 
some stage of succession (Salo et al. 1 986, Rasanen 
et al. 1 987). In addition to their role in creating and 
maintaining a landscape mosaic conducive to rapid 
speciation, the Andes also appear to have protected 
the mesic Neotropics from the severe and frequent 
droughts which could have magnified species ex- 
tinctions in Africa, as mesic forests were repeatedly 
reduced and fragmented during Pleistocene times 
(Raven and Axelrod 1974, Axelrod and Raven 
1978). 

Finally, neotropical species should also have 
received greater protection than their African coun- 
terparts from Pleistocene temperature variation. 
Lowland Africa is approximately 500m higher in 
elevation than is lowland Amazonia, and would 
have provided fewer refugia for plants and animals 
during glacial periods. Current evidence (e.g., 
Bengo and Maley [1991]) indicates that montane 
forest, including elements now restricted to the 
cool, moist conditions of the Afromontane zone, 
extended to low elevations (600 m or perhaps 
lower) in Central Africa during several periods 
over the last 135,000 years. Judging from the 
dramatic drop in ant diversity and abundance with 
elevation on humid tropical mountains (Janzen 
1973), the conditions suggested for these periods 
would not have been conducive to the success of 
much of the contemporary ant fauna of lowland 
African forests. To the extent that climatic fluctua- 
tions in Africa exceeded those in the American 
tropics, these could have led to the dissolution of 
mutualisms, even without species extinctions, as 
the fitness consequences of association shifted (e.g., 
to parasitism) with fluctuations in the abiotic and 
biotic environments. 


SIMILARITIES BETWEEN ANT-PLANT 
RELATIONSHIPS OF DIFFERENT 
TROPICAL REGIONS 

In the context of the aforementioned differences 
in species richness, and in the climatic and geologic 
histories of ant-plants on different tropical land 
masses, certain similarities in the form and ecology 
of ant-plant relationships of different continents 
appear all the more striking. For example, across 
tropical land masses, large colonies of active and 
aggressive ants occupy fast-growing and light- 
demanding pioneer trees (neotropical Cecropia and 
Old World Macaranga). In contrast, timid ants 
inhabit small, slow-growing understory shrubs or 
treelets with hairy domatia (e.g., American Hirtella, 
Duroici, and many melastomes, and African 
Magnistipula, Delpydora, Cola, and Scapho- 
petalum). Finally, myrmecophytic trees of second- 
ary forests and forest light gaps (neotropical Triplaris 
and African Barteria) grow in circular clearings 
made by pseudomyrmecine ants, which attack veg- 
etation in the neighborhood of their hosts. McKey 
and Davidson (in press) have amassed evidence 
against common ancestry as a general explanation 
for these remarkable commonalities. While some 
comparisons between Africa and Asia suggest com- 
mon descent of ant-plants, plant-ants or both, 
myrmecophytes and specialized plant-ants appear 
to have evolved largely independently in America 
and Africa. No ant-plants of Africa and the 
Neotropics have apparently shared a myrmecophytic 
common ancestor. In contrast, the plant-ant habit 
may be ancient in the sub-family Pseudomyrmecinae 
and in tribes Myrmelachistini and Tapinomini, and 
might possibly have preceded the splitting of South 
America and Africa. However, with these possible 
exceptions, resemblances between symbiotic asso- 
ciations in the American and African tropics are not 
due to common descent of one or both partners from 
an association that predated continental separation 
or other vicariance events, or which migrated intact 
from one continent to the other (McKey and 
Davidson, in press). 

The remarkable correspondences between ant- 
plant associations in the American and African 
tropics must therefore be due to some combination 
of: ( 1) parallel evolution of ants and/or plants from 


Volume 2 , Number 1 , 1 993 


17 


similar starting material, (2) evolutionary conver- 
gence, and (3) the matching of symbiotic partners 
according to a set of shared rules. The task then is 
to identify the preadaptations which have been 
pressed into service and evolutionarily modified in 
symbiotic ants and plants, and to recognize the 
selection pressures which have led repeatedly to the 
correspondences noted above. 

PREADAPTATIONS OF PLANTS AND ANTS 

Parallel and convergent evolution are usually 
regarded as evidence that selection pressures have 
acted in similar ways on organisms of different 
lineages. Selection, however, is only part of the 
explanation for these phenomena. Different lin- 
eages may follow similar evolutionary trajectories 
because they share similar developmental con- 
straints which channel the action of selection along 
a limited number of paths. 

Preadaptations for Myrmeeophytism 

The evolutionary antecedents of specialized 
myrmecophytic traits are poorly explored. How- 
ever, comparative studies of myrmecophytes and 
their less specialized relatives are begining to sug- 
gest plausible and testable hypotheses about the 
origins of these traits (Benson 1985, McKey 1989 
and 1991, O' Dowd and Willson 1989, Fiala and 
Maschwitz 1991, Schupp and Feener 1991). For 
example, in various plant taxa, a few similar struc- 
tures have repeatedly provided the raw materials 
transformed by selection into myrmecophytic struc- 
tures. An understanding of the origins of these 
traits may help to identify constraints which have 
pressed ant-plants of diverse lineages and biogeo- 
graphic regions into a limited number of molds. It 
may also indicate developmental patterns which 
have facilitated the evolution of myrmeeophytism, 
and suggest why myrmecophytes have evolved 
repeatedly in some lineages, but rarely or never in 
others. 

Provision of Food for Plants. — Discussion of 
the evolutionary background of myrmecophytes 
has tended to emphasize the provision of food for 
ants. Indeed, there is evidence from many lineages 
that the ancestors of ant-plants possessed extrafloral 


nectaries, pearl bodies, or other traits, which pro- 
vided food for ants in loose non-symbiotic interac- 
tions. The large, complex nectary glands of some 
ant-plants (e.g.. Acacia, Endospermum, and some 
Macaranga ), and the elaborate food bodies of oth- 
ers (e.g., Mullerian bodies of Cecropia, and 
Beccarian bodies of Asian Macaranga) are readily 
accounted for as outgrowths of these traits. As ant- 
plant interactions intensified into symbiosis, such 
attributes should have been easily modified by 
selection acting on the composition and rate of 
supply of food for ants. The Beltian bodies of 
Central American ant-acacias may be the only case 
in which a specialized food-producing structure of 
a myrmecophyte lacks an obvious antecedent among 
unspecialized but related plants. 

Provision of food ensures that ants are a regular 
component of the plant’s biotic environment, and 
doubtless facilitates the evolution of more intense 
interactions. However, myrmecophytes have 
evolved in only a small subset of the numerous 
plant lineages whose members are engaged in op- 
portunistic myrmecophilic interactions; other plant 
traits must also play a role in facilitating or con- 
straining the evolution of symbiotic interactions. 
Furthermore, in many cases, neither the 
myrmecophytes nor their close relatives provide 
food directly to ants. In many cases, EFN’s and 
food bodies are lacking, and scale insects 
(Coccoidea, Homoptera) are a major source of 
colony nutrition (Appendix 1). Following Ward 
( 1 99 1 ), we suggest that many myrmecophytic rela- 
tionships evolved not from pre-existing 
myrmecophilic relations, but from parasitisms in 
which stem-nesting ants began to inhabit live plant 
cavities and to tend Coccoidea. 

Structures for Housing Ants. — We must thus 
explore plant traits that facilitated the production of 
cavities that could be modified by selection into 
specialized structures for housing ants. The evolu- 
tionary antecedents of myrmecodomatia, the defin- 
ing feature of specialized myrmecophytes, have 
received little attention. Preadaptations and devel- 
opmental constraints in the evolution of 
myrmecodomatia will be discussed in detail else- 
where (McKey, in preparation) and are summa- 
rized only briefly here. 


18 


Journal of Hymenoptera Research 


Table 1 Taxa in which at least some myrmecophytes have long, dense hairs which inhibit insect movements on 
stems, domatia or both. 


Region 

Family 

Genus 

ETHIOPIAN 


Chrysobalanaceae 

Magnistipiila 


Dichapetalaceae 

Dichapetalum 


Ebenaceae 

Diospyros 


Rubiaceae 

Canthium 

Cuviera 


Sapotaceae 

Delpydora 


Sterculiaceae 

Cola 

Scaphopetalinn 

NEOTROPICAL 

Boraginaceae 

Cordia 


Chrysobalanaceae 

Hirtella 


Fabaceae 

Platymiscium 

Tachigali' 


Gesneriaceae 

Besleria 


Melastomataceae 

Allomaieta 1 2 
Blakea 3 
Clidemia 4 
Conostegia 
Henriettea 5 
Maieta 
Sagraea 6 
Toeoca 7 


Cecropiaceae 

Pourouma 


Polygonaceae 

Trip laris 


Rubiaceae 

Duroia 8 

Hoffmannia 

Remijia 

ORIENTAL 


Melastomataceae 

Medinilla 


Verbenaceae 

Callicarjja 


Piperaceae 

Piper 

AUSTRALIAN 


Monimiaceae 

Steganthera 


1 At least one species, collected from a hillside over the junction of the Rio Sotileja and the Rio Manu, in southeastern Peru 
(D. Davidson, unpublished). 

Closely related to Maieta (A. Gentry, personal communication) 

3 Benson ( 1 985) considers the leaf pouches of B. fonnicaria to be in transition from acarodomatia to ant-domatia. Among 
the melastomes listed here, Blakea is unique in not belonging to the Miconieae. 

4 At least three independent origins of domatia in Clidemia sensu strictu; includes Myrmidone (Judd and Skean 1991 ) 

s Includes Henriettella (Judd 1989) 

6 Includes Ossaea p.p. (Judd 1989) 

7 Includes Microphysca (Judd and Skean 1991) 

8 Two independent origins of domatia (foliar domatia and swollen intemodes) 


Volume 2 , Number 1 , 1 993 


19 



Fig. 1. Paired leaf-pouch domatia, covered with dense, erect trichomes, at the base of a leaf of Delpydora 
macrophylla Pierre (Sapotaceae) in southern Cameroon. These pouches are formed by downward folding and 
rolling of the expanded base of the blade on either side of the midrib. The domatia are usually occupied by timid 
Technomyrmex species. 


Stipules have been modified into ant-domatia in 
a few myrmecophytes; known examples are all 
from the Old World tropics (Appendix 1 ). (The 
only apparent exception is Acacia, in which thorns, 
themselves highly specialized stipules, have been 
modified into domatia in both neotropical and Old- 
World representatives.) In many tropical plants, 
large stipules function as mechanical protection for 
the growing bud. In some cases, stipules possess 
ant-attractive structures which provide biotic de- 
fense as well. Where stipules are persistent, rather 
than being shed soon after maturation of associated 
nodes, ants may find suitable shelter for tending 
homopterans, nesting, or both. Although ants and 
their associated debris are observed frequently be- 
neath large stipules, only rarely have these stipules 
become evolutionarily modified to house ants. 
Specializations include recurving or inflating of the 


stipule to form a more enclosed structure (as in New 
Guinea Psychotrio and perhaps African Docty- 
Jodenio), location of specialized food bodies on the 
lower surface of the stipule (Asian Mocaranga), 
and possibly the evolution of persistent stipules. In 
an analogous case, African Diospyros conocorpo 
Giirke & K. Schumann has specialized, hairy 
domatia formed from persistent cataphylls 
(Letouzey and White 1970). These structures are 
leaf-like appendages, usually rapidly deciduous, 
and formed on the first few nodes of young expand- 
ing twigs in many tropical trees with rhythmic 
growth patterns (Halle et al. 1978). They are func- 
tionally analogous to stipules. In D. conocorpo , the 
cataphylls are folded to form a structure completely 
enclosed, except for a small opening near the base 
of the blade, and they are persistent, rather than 
deciduous, as in related species. These structures 


20 


Journal of Hymenoptera Research 


are occupied by Technomyrmexkohlii ( Forel), which 
also inhabits several leaf-pouch ant-plants in the 
same forests. 

In Asia, Africa, and the Neotropics, leaf-pouch 
domatia of strikingly similar form have evolved in 
numerous myrmecophyte lineages (Appendix 1 ). 
Formed near the leaf base, and typically paired on 
either side of the midrib (but single in some spe- 
cies), they are usually covered with long, dense 
trichomes (Table 1 ). Restricted to understory treelets 
and shrubs, these ant-plants typically are occupied 
by small, timid ants. Leaf-pouches seem to be 
formed in one of two ways. In some taxa (e.g., 
neotropical Melastomataceae, and African 
Sterculiaceae), invagination occurs in the internal 
portion of the leaf blade, in a region flanking the 
base of the midrib. This invagination produces 
single or paired inflated pouches, each with an 
entrance on the abaxial leaf surface. In at least four 
plant families, including most frequently and vari- 
ably in the Rubiaceae, paired leaf pouches form in 
a different manner. At the bases of leaf blades, 
(revolute) leaf margins curl downward, as in Afri- 
can Delpydora (Fig. 1), Magnistipula, Dichape- 
tahwi gassitae Bret., and I.xora hippoporifera 
Bremek., neotropical Hirtella and Remijia , and 
Asian Callicarpa saccatci Steen. Less frequently, 
(involute) leaf margins curl upward, as in neotropical 
Duroia sacciferci Benth. and Hook. Pouches may 
be bubble-like invaginations (Gardenia imperialis 
L. Pauwels) or, more often, scroll-like hollow tubes. 

It has long been postulated that the leaf-pouch 
domatia of ant-plants evolved from acarodomatia 
(Schnell 1966, Schnell et al. 1968), presumably by 
intermediate stages in which domatia could be 
occupied either by mites or by small ants. Selection 
led to increased size of domatia with progressive 
transference of protective function from mites to 
ants (O’Dowd and Willson 1989). Benson (1985) 
also argues that leaf-pouch domatia evolved in 
myrmecophytes from small depressions in leaf 
surfaces. The original function of these depres- 
sions was to shelter ant-tended homopterans. The 
two hypotheses are not mutually exclusive, as ants 
may also have used acarodomatia to shelter ho- 
mopterans (Benson 1985). Hypotheses implicat- 
ing acarodomatia in the origin of leaf-pouch ant- 
domatia receive strong support from cases like 


Cola tnarsupiwn K. Schumann, in which a single 
leaf presents a graded series of domatia increasing 
in size from typical acarodomatia at the leaf apex to 
large inflated pouches at the leaf base (Schnell and 
Beaufort 1966). 

Why have leaf-pouch domatia evolved repeat- 
edly in certain groups, for example, at least nine 
times in the tribe Miconieae in the Melastomataceae 
(Table I)? Leaves of many Miconieae have strongly 
arcuate venation with sections of the leaf blade 
vaulted and curved upward between major veins. 
Even before selection intervened to enlarge these 
structures, this waffle-like leaf organization may 
have fortuitously provided invaginations large 
enough to shelter ant nests. In African Sterculiaceae, 
where similar domatia have evolved twice, vena- 
tion is also palmate, with three large veins converg- 
ing at the leaf base. 

The largest group of myrmecophytes is that in 
which domatia are located in stems, or in stem-like 
structures such as petioles or inflorescence stalks 
(Appendix 1). Increasing evidence supports the 
hypothesis that ants originally colonized cavities 
created in twigs and petioles by wood-boring in- 
sects (Ward 1 99 1 , also Appendix 1 ). Together with 
cavities formed by spontaneous drying of pith ca- 
nals, these cavities provided ants with shelter and 
substrate for brood and symbiotic Coccoidea. When 
the presence of ants conferred net benefit (e.g., by 
protection against phytophagous insects, including 
wood-borers, and any diseases transmitted by these 
insects), selection acted on the plant to evolve 
features facilitating its occupancy by ants (Ward 
1991). Such traits include specialized swollen 
twigs and a prostoma, or relatively unlignified spot 
through which ants gain easy access to the domatia. 

What traits may have predisposed plants to 
evolve symbiotic association with ants via this 
mechanism? Wood-boring insects usually attack 
soft, pithy portions of stems. The larger the primary 
diameter of a stem, the thicker its pithy central 
section. Thus thick-twigged plants offer greater 
opportunities than do thin-twigged taxa for wood- 
boring insects, and for ants which nest secondarily 
or primarily in the cavities of living plants. Al- 
though much poorly understood interspecific varia- 
tion in stem structure affects the relationship be- 


Volume 2 , Number 1 , 1993 


21 


tween the primary diameters and pith diameters of 
twigs, myrmecophytes are most likely to evolve in 
plants with thick twigs. 

This observation gains importance when we 
consider the plant-architectural correlates of stem 
primary diameter. The best known of “Corner’s 
rules,” and one confirmed by quantitative studies 
(White 1 983 ), states that there is a positive correla- 
tion between the primary diameter of a stem axis 
and the size of appendages (e.g., leaves) borne by it 
(Halle et al. 1978). This correlation means that 
selection acting on leaf size (Givnish 1987) also 
drives evolutionary change in stem diameter 
( McKey 1991). Thus, the evolution of stem domatia 
may be facilitated by an evolutionary increase in 
leaf size, driven for example, by climatic change, 
by range extension into more mesic environments 
(Givnish 1987), or by selection to minimize meta- 
bolic cost of woody leaf-support tissues (White 
1983). If disparities in leaf size were related to 
habitat, myrmecophyte frequencies could be corre- 
lated with habitat, independently of and perhaps 
even despite any habitat-related differences in se- 
lection imposed by symbiotic ants (McKey, unpub- 
lished). 

Corner’s Rule may help account for several 
groups of ant-plants with domatia in thickened 
support structures (Appendix 1 ). First, myrmeco- 
phytism has evolved often in genera whose moist, 
shaded, understory environments have favored com- 
paratively large, broad leaves and thick stems (e.g., 
African Leonardoxa, and Oriental or Australian 
Tapeinosperma, Steganthera , Kibara, and 
Myristicci). Ants also live symbiotically with mem- 
bers of the Meliaceae, Sapindaceae, and 
Anacardiaceae, whose leaves are not only large, but 
compound. In the Meliaceae, myrmecophytes ap- 
pear to have evolved independently in four genera, 
including three Asian taxa ( Aphanamixis , 
Chisocheton and Aglaia) with massive stems sup- 
porting large compound leaves. Even within 
Aphanamixis, myrmecophily characterizes forms 
with relatively large leaves and twigs (Mabberley 
1985). Second, thick support structures for large 
leaves may also have facilitated the frequent evolu- 
tion of ant-plants in fast-growing pioneer trees, 
whose large leaves and sparse branching allow 
them to support a considerable leaf surface area 


with minimum investment in woody framework 
(White 1983). Examples are neotropical Cecropia, 
Asian Macanmga and Australian Endospermum , 
which almost surely converged due to selection on 
leaf size and tree architecture prior to the evolution 
of myrmecophytism. Other myrmecophytic pio- 
neers of riverine and forest light gaps include 
neotropical Triplaris, Australian Nauclea and Afri- 
can Barteria and Vitex grandifolia Giirke. In all of 
the plants in these two categories, ant protection 
might be especially advantageous, because the large 
and parenchyma-rich meristems are especially sus- 
ceptible to damage by wood-boring insects. Since 
most of these plants produce one-to-few large mer- 
istems at any one time, the material and opportunity 
costs of losing even one meristem could be very 
high. 

Finally, two smaller groups of ant-plants house 
ants in either false nodes, thickened to support 
multiple leaves (e.g., two Cordia species and Diiroia 
hirsuta Poepp. and Endl.), or in stout petioles 
{Piper, Pourouma and Tachigali). Although peti- 
oles might often be too short-lived to function as 
domatia, they are likely to be comparatively long- 
lived for both the compound leaves of Tachigali 
and the simple leaves of myrmecophytic under- 
story Piper species (in which ant cavities also 
extend into the stem itself). 

Preadaptations and Pathways to 
Specialization in Ants 

Specialized plant-ants are represented dispro- 
portionately in particular taxonomic categories of 
ants, and shared characteristics of these taxa pro- 
vide evidence of factors predisposing ants to evolve 
symbiotic relationships with plants. Worldwide, 
plant-ants have evolved in five of 1 2 subfamilies in 
the Formicidae (Appendix 1 ). They are absent only 
from subfamilies of specialized legionary and other 
predatory ants (Cerapachyinae, Dorylinae, 
Ecitoninae, Leptanillinae, and Myrmeciinae), and 
from the monotypic Aneuretinae and Nothomy- 
rmeciinae. Until recently, they were also deemed 
absent from the Ponerinae, the most predatory of 
five subfamilies containing at least some species 
that depend directly and substantially on plant 
resources. However, at least four species of 


22 


Journal of Hymenoptera Research 



Fig. 2. Leaves bound together with carton to form the ephemeral nests of Dolichoderus (= Hypoclinea) bidens (L.) 
in southeastern Peru. 


Pachycondyla now appear to be specialized sym- 
bionts of Cecropia ( Davidson et al . 1991, Davidson 
and Fisher 1 99 1 , J. Longino, personal communica- 
tion). Still, plant-ants are poorly represented in the 
Ponerinae and among predatory ants in general. 

The evolution of obligate plant-ants in five sub- 
families, approximately 30 genera (Appendix 1 ), 
and multiple clades of at least Psendomyrmex (Ward 
1991) and Azteca (Benson 1985, Longino 1991a 
and b) confirms the frequency and facility with 
which plant-ants have evolved, and provides abun- 
dant opportunity to find commonalities in lifestyles 
and traits that may have promoted evolutionary 
specialization on plants. For example, three of the 
six principal generic radiations of South American 
endemics have arisen (one each) in the sub-family 
Pseudomyrmecinae, and in the tribes Tapinomini 
(Dolichoderinae) and Myrmelachistini (Formi- 
cinae). These ants share the habit of regularly 
tending homopterans inside (all three taxa) or out- 
side (especially tapinomines) of cavities in live 
plants. Within each of these groups, common 
ancestors of contemporary plant-ants likely had 
additional traits which predisposed them to evolve 
symbiotic (parasitic as well as mutualistic) associa- 


tions with homoptera and plants. Because the 
relative competitive abilities of ants form an impor- 
tant part of the story, we turn now to consider 
various ecological differences among ants with 
different competitive abilities. 

Competitive Dominants . — Ecological limita- 
tions on populations of arboreal ants in lowland 
tropical forests add insight into probable origins, 
correlates and consequences of arboreal nesting 
habits, including stem-nesting. Colony popula- 
tions appear to be limited principally by food and 
nest sites (Wilson 1959b, Carroll 1979, Davidson 
and Epstein 1989). Because most arboreal ants are 
generalized foragers of plant and homopteran exu- 
dates, and of carrion, interspecific food require- 
ments are strongly overlapping, and competition 
can be intense. The competitive dominants of each 
tropical biogeographic region are species which 
have evolved means of nesting in areas of abundant 
food. They include Old World Oecophylla, 
Crematogaster, Tetramorium, Philidris and 
Polyrachis, some Austral ian Anonychomyrma, and 
New World Crematogaster, Camponotns, Azteca 
and Dolichoderus (including Hypoclinea , Shattuck, 
1 992a). These ants either bind leaves together into 


Volume 2, Number 1, 1993 


23 


temporary nests, or construct potentially more per- 
manent carton homes in the canopy where food is 
abundant (Fig. 2). Like species which occupy the 
top of the competitive hierarchy at high temperate 
latitudes (Vepsalainen and Pisarski 1982), these 
species defend not only their nest sites and tempo- 
rary, localized food patches, but their entire forag- 
ing areas, as absolute territories. Although a certain 
threshold of aggressiveness may have been re- 
quired before these ants could defend their some- 
what exposed nests successfully against vertebrate 
enemies (e.g., monkeys and woodpeckers; J. 
Longino, personal communication), an eventual 
capacity to nest near abundant food almost cer- 
tainly contributed to the escalation of aggressive- 
ness and dominance. 

Most competitive dominants tend populations 
of Homoptera, whose exudates form a steady and 
predictable source of colony nutrition and help to 
fund high worker activity and aggression. These 
ants lack functional stings, but all possess elaborate 
chemical weaponry (Blum and Hermann 1978, 
Attygalle and Morgan 1984, Buschinger and 
Maschwitz 1984, Merlin et al. 1992). Expended in 
use, these exocrine products should be character- 
ized by more rapid turnover and greater cost than is 
associated with longer-lived stings and sturdy ex- 
oskeletons. Nevertheless, if chemical defenses are 
supported by the requisite resource base, they ap- 
pear to be more effective than stings in contests 
among ants (Davidson et al. 1988). With their rich 
sources of homopteran exudates, dominants should 
often experience an excess of dietary carbon in 
relation to protein, so that colony expansion is 
protein-limited. If so, this could explain the “high 
tempo” lifestyle (sensu Oster and Wilson 1978) 
characteristic of these ants and help to resolve the 
enigma of their seeming “inefficiency” in foraging 
(Oster and Wilson 1978; Holldobler and Wilson 
1990). By spending relatively “cheap” carbon 
resources on aggression and seemingly extravagant 
levels of activity, these ants secure dominance over 
territories whose protein resources fund colony 
growth. 

Chemical weaponry and high activity levels are 
not the only traits determining dominance in these 
ants. Abundant food and freedom from nest site 
limitation appear also to have led to larger colony 


sizes and longer life expectancies. If the resource 
environments of ants have helped to shape the 
evolution of life history attributes (e.g., rates of 
egg-laying, worker turnover, etc.), a correlated 
evolved dependency on rapid rates of resource 
acquisition may restrict some dominants to the 
most productive sites in lowland rain forests 
(Davidson and Epstein 1989). Arboreal dominants 
are preeminent in monopolizing high quality re- 
sources at exposed sites such as EFN’s, and 
Homoptera positioned on flowering and fruiting 
peduncles, where a plant's phloem resources are 
frequently most concentrated. As evidence of their 
competitive impact in one rainforest ant commu- 
nity as a whole, Wilson (1959b) noted that a num- 
ber of arboreal ant species regularly forage on the 
ground, whereas only a few exceptional ground 
nesters forage even in the low arboreal zone, and 
possibly none of these reaches the upper canopy. 

( In the Neotropics, terrestrially nesting Paraponera 
and Ectatomma are obvious counter-examples, but 
both genera are exceptional among ponerines for 
their heavy reliance upon plant exudates, carried as 
large droplets in the mandibles.) Dominants can 
restrict the local diversity of other ants, as do the 
parabiotic associates of neotropical ant-gardens 
(Davidson 1988). Thus, the diversity of arboreal 
but not terrestrial ant species is lower inside the 
territories of Ccnnponotus femoratus Fab. and 
Crematogasterc f. linmta parabiotica (Forel), than 
in adjacent areas lacking these ants. Because the 
species composition and diversity of subordinate 
species often varies markedly with the identity of 
dominants, patchiness in the territories of domi- 
nants determines a mosaic of ant communities 
within many tropical forests (Leston 1973, re- 
viewed in Holldobler and Wilson 1990). 

Competitive dominance may be context depen- 
dent, e.g., differing in relation to the identities of 
plant species which form the substrate for ant 
nesting and foraging (Davidson and Epstein 1 989). 
Thus, host plant associations of Oecophylla 
longinoda (Latr.) (Dejean and Dijicto 1990) and 
Tetramorimn aculeatum (Mayr) (Dejean et al. 1 992), 
two widespread dominants in African forests, are 
correlated with worker preferences for foliage types 
offered in laboratory experiments. 


24 


Journal of Hymenoptera Research 


Weak Competitors. — For competitively subor- 
dinate ants, the benefits of combining nesting and 
foraging locations are conditional on locating nests 
and resources in sites which are protected from 
invasion by dominants. Nests in dead or live twigs, 
stems, and larval insect borings can be defended if 
the cavity size is not much larger than the head 
diameters of workers, soldiers, or queens. By 
sealing a stem nest with her head, a single worker 
can protect her whole colony or colony fragment 
from invasion by enemy ants. Thus, along a Pacific 
Ocean beach at Corcovado National Park in Costa 
Rica, the many dead twigs of Coccoloba 
(Polygonaceae) trees were occupied by more than 
nine ant species (six of Pseudomyrmex alone), 
whose head widths were roughly equal and propor- 
tional to the internal diameters of their twig cavities 
(D. Davidson, personal observation). At least some 
African Tetraponera also appear not to nest in 
stems whose diameter exceeds a threshold value 
(Terron 1970). For small-bodied ants like the timid 
Wasmannia scrobifera Kempf in Costa Rica, other 
protected sites may include carton shelters beneath 
leaves of plants whose dense stem trichomes ex- 
clude larger bodied workers (see below). 

For comparatively docile and subordinate ants, 
the advantage of locating their resources inside 
stem cavities is clear. The evolutionary transition 
from nesting in dead twigs to nesting in live twigs 
and other cavities of live plants conveyed the addi- 
tional opportunity to obtain uncontested resources 
from phloem-feeding Homoptera (especially 
Coccoidea), which either invaded such cavities on 
their own or were brought there by the ants. More- 
over, nests in live wood were potentially habitable 
over much longer time periods than those in dead or 
decaying twigs and branches, obviating a need for 
frequent and dangerous nest moves. Longer tenure 
of living nest sites, which grew rather than decay- 
ing with time, may secondarily have allowed the 
evolution of larger colony sizes and increased op- 
portunities for local monopolization of resources, 
as well as the selective advantage of aggressive 
behavior and allelochemicals. Traits conferring a 
capacity to nest in live plants are not well studied, 
but they probably involve evolutionary adjustment 
to an increased threat from nest pathogens. Thus, 
Ward (1991 ) points out the tendency for hypertro- 


phy of metapleural glands in domatia-inhabiting 
pseudomyrmecines. Where studied, the function 
of metapleural secretions has been tied to the sup- 
pression of microbial pathogens (e.g., Maschwitz 
1974, Holldobler and Engel-Siegel 1984). 

In summary, plant-ants are most frequent in taxa 
which depend directly or indirectly, but substan- 
tially, on plant resources. They are most likely to 
have evolved in competitively subordinate ants, 
selected to live in close proximity to food re- 
sources, but to nest and feed in comparatively 
protected and permanent sites which reduce dan- 
gerous contact with competitive dominants. Within 
this subset of ant taxa, selection for evolutionary 
specialization of plant-ants might have been less 
likely in groups where potent defensive exocrine 
compounds (e.g., many Dolichoderus species), and 
worker armor or specialized diets (e.g.,cephalotines) 
diminished the hazards of encounters with domi- 
nants. 

The transition from more generalized ancestors 
to specialized plant-ants would not have been dif- 
ficult. Founding queens should have evolved greater 
efficiencies in locating hosts that provided superior 
food or housing or were more easily accessed. By 
consuming or deterring insect herbivores, ants might 
then have enhanced their own fitness indirectly by 
promoting the vigor or prolonging the lifespans of 
their hosts. However, host specialization by ants, 
as well as consumption of eggs and larvae of insect 
herbivores, could have been favored in ants whether 
the ants and Homoptera had a net positive or nega- 
tive effect on these hosts. Longino (1987), for 
example, discusses the case of Leptothorax obtura- 
tor Wheeler, which nests only in cynipid galls of 
oaks and probably has no fitness effect on the host 
tree. Selection pressures on ants and plants should 
often have been asymmetric, leading to the expec- 
tation that ant-attractive traits would have evolved 
in only a subset of the host plants on which obligate 
plant-ants reside. 

Expectations based on this brief review of com- 
petitive interactions among arboreal ant species can 
now be compared with actual patterns in the distri- 
bution and ecology of specialized plant-ants. 


Volume 2, Number 1 , 1 993 


25 


THE MATCHING OF ANTS AND PLANTS 

Appendix 1 is a worldwide summary of all 
symbiotic ant-plant relationships known to us. To 
facilitate comparisons among ants of differing 
lifestyles and competitive abilities (see below), we 
organize the data by ant genus. Also evident in this 
summary is the basic asymmetry in the degree to 
which relationships are obligate for ants versus 
plants. The vast majority of the ants in the table are 
thought to be obligate plant-ants (column 7, though 
these are not necessarily host-specific). However, 
a substantial fraction of their host genera have no 
obvious myrmecophytic traits (column 6), despite 
their regular association with specialized (usually) 
or unspecialized ants (cf., African Musanga and 
Neotropical Tetrathylaciwn). Few plants with con- 
spicuous myrmecophytic traits (e.g., obvious 
domatia, or naturally hollow stems with prostomas) 
lack specialized plant-ants altogether, though some 
may occur principally with unspecialized ants in 
marginal habitats, or at the edges of their distribu- 
tions (see below). 

Almost certainly. Appendix 1 includes a mix of 
relationships in which ants are parasitic, 
commensalistic, or mutualistic with their hosts, and 
the net outcome of the interactions might even vary 
with habitat or ecological context. These outcomes 
are not wholly predictable from myrmecophytic 
traits, since even in mutualistic associations, plants 
need have no obvious specializations to attract ants. 
Clearly most of the relationships are poorly known, 
and many of the table entries are incomplete. Yet 
the table clarifies the types of data which will 
eventually be essential to describe pattern in these 
relationships, and we hope it will stimulate the 
collection of such data in future studies. 

Despite limited data, patterns in relationships of 
ants and host plants correspond roughly to those 
noted for tropical forest ant faunas as a whole. 
Across genera, the fastest growing myrmecophytes 
of disturbed forest edge (i.e., hosts with rapid rates 
of resource supply to ants) tend to be inhabited by 
ants from aggressive, dominant, carton-building 
genera (column 1), e.g., the Azteca of neotropical 
Cecropia, and Crenmtogaster of ecologically simi- 
lar Old World (especially Asian) Mcicaranga. Less 
aggressive and competitively subordinate ant spe- 


cies tend to persist by employing one or more of 
several strategies likely to reduce interactions with 
the dominants. We deal with each of these in turn. 

Ant Pruning of Host-plant Neighbors 

The most common and significant natural en- 
emies of ants are other ants (Haskins 1 939). Species 
with sting defenses, usually inferior to chemical 
defenses in contests among ants, are disproportion- 
ately likely to attack and prune vegetation sur- 
rounding their hosts (Davidson et al. 1988, also 
column 4, Appendix I). In both Africa and South 
America, this behavior is most widespread in 
pseudomyrmecine plant-ants, where pruning has 
evolved multiple times in independent lineages 
(Ward 1990). The potent stings of 
pseudomyrmecines may be an effective deterrent 
of vertebrates ( Janzen 1 972 ), but they are inferior to 
chemical defenses in repelling colonies of invading 
ants. Although the Pseudomyrmex of Triplaris and 
Acacia , and the Tetraponera of Bacteria, do not 
forage extensively off their host plants, they regu- 
larly leave these hosts to sever the petioles of leaves 
on neighboring plants (Fig. 3). Eventually these 
neighbors die, leaving the host trees in starkly 
defined clearings within the forest. 

Such clearings have been hypothesized to re- 
ward resident colonies by enhancing host-plant 
vigor or, in drier environments, acting as natural 
fire breaks (Janzen 1967a). However, experimen- 
tal evidence suggests that a more immediate selec- 
tive advantage for attacks on neighboring vegeta- 
tion is the reduction of threats from more dominant 
arboreal ants. When permanent wire bridges were 
made between myrmecophytic Triplaris and neigh- 
boring trees, the frequency of invasions by domi- 
nant Crenmtogaster increased, and whole hosts or 
portions of these hosts were eventually usurped by 
Crenmtogaster or Azteca species (Davidson et al. 
1988). The broad taxonomic distribution of obli- 
gate and facultative pruning behavior (the latter 
occurring only in the presence of enemy ants. 
Appendix 1, column 4) suggests that dominant 
competing and predatory ants constitute a major 
threat to many or most specialized plant-ants. Its 
prominence in neotropical ants is evidence against 
the hypothesis that a paucity of dominants charac- 


26 


Journal of Hymenoptera Research 


terizes that region (Carroll 1979, see also Me Key 
and Davidson, in press). Presumably, pruning be- 
havior could also serve to defend resident colonies 
against invasions by leafeutter (Morawetz et al. 
1 992) and legionary ants, which could devastate the 
resource base or the colony itself. 

Pruning behavior is not strictly limited to ants 
with functional stings (Appendix 1). Most 
neotropical Cecropia and Old World Macaranga 
and Endospemntm establish in disturbed second 
growth vegetation, where vines are particularly 
abundant and troublesome to both plants and ants, 
and where weedy dominant ants are a constant 
threat (Benson 1985). Not surprisingly, the com- 
mon ant associates of these host genera ( Azteca , 
Crematogaster and Camponotus, respectively) will 
attack encircling vines (Appendix 1, Janzen 1969, 
Fiala et al. 1989; Davidson personal observation, 
Letourneau et al. 1993), though pruning is not 
typical for these genera as a whole. The compara- 
tively unbranched growth forms of these hosts may 
also help to limit contact with vines and neighbor- 
ing plants (Putz and Holbrook 1988) and, therefore, 
with enemy ants (Benson 1985). In contrast to 
chemically defended ants, in which pruning is 
restricted to species inhabiting hosts of secondary 
forest, species defended principally by strong or 
weak stings (Pachycondyla, Tetraponera, 
Pseudomynnex, and Allomerus) also tend to prune 
around hosts in primary forests, where threats from 
vines and dominant ants are not so severe. Not all 
plant-ants in these genera prune, but some species 
benefit from other forms of protection (see below). 

Worldwide, the most dramatic case of allelopa- 
thy by ants may be that of Mynnelachista 
(Formicinae) species inhabiting myrmecophytes in 
the intriguing western Amazonian “Supay chacras” 
(Quechua for “Gardens of the Devil”). Dominance 
of lowland forest stands (to > 1 0,000 nr in size ) by 
multiple species of myrmecophytes, most promi- 
nently Duroia hirsutci [Poeppig and Endl.] K. 
Schunr, but also Cordio nodosa Lam. and Miconia 
nen’osa Triana, suggests that the ants kill non- 
myrmecophytes selectively (Campbell et al. 1989). 
In a similar phenomenon, at somewhat higher el- 
evations of western Amazonia (700-1200 m), a 
different Mynnelachista species creates monospe- 
cific stands of myrmecophytic Tococa occulentalis 


Naudin (Morawetz et al. 1992). The two conge- 
neric ants share a similar behavioral ecology (D. 
Davidson, personal observation, for supay chacras, 
and Morawetz etal. 1992, for Tococa). Workersdo 
not appear to forage off their hosts, but do leave 
their hosts to attack other plants. When seedlings or 
saplings of plants other than the host species are 
placed in the vicinities of these hosts, workers gnaw 
at the vascular bundles of leaves of the introduced 
plants, and can kill them in a matter of hours to days. 
Morawetz and colleagues describe the extraordi- 
nary capacity of these ants to single out especially 
vulnerable plant tissues for attack. Thus, workers 
bite and poison palmate leaves at the base of lami- 
nae, where all vascular bundles join, pinnately 
nerved leaves at nerve bases of the first and second 
order, and monocots (e.g., palms), nerve by nerve, 
along the entire leaf. Necrosis originating at the 
attack sites spreads rapidly over the entire lamina. 
Within a few hours to a few days, inhabitants of the 
Tococa can successfully kill seedlings and saplings 
within a radius of 4 m and damage trees up to 10 m 
in size. Light gaps created by ant activities are 
subsequently colonized by vegetative propagation 
of the host. 

Although Morawetz and colleagues discount 
the hypothesis that the killing of host plant neigh- 
bors by Mynnelachista has evolved principally to 
exclude enemy ants, several observations suggest 
that the hypothesis should not be ruled out. First, 
leaf-cutter ants, an important enemy of the Tococa , 
invade principally by contact with the branches of 
other plants, not via the main trunk. Second, no 
generalized arboricolous ants appear to forage within 
the territories of these specialized Mynnelachista. 
Furthermore, large worker forces may be needed to 
assure the safety of ants which have left their hosts. 
Attacks on neighbors of Tococa begin when the ant 
population of one or a few individual hosts is at 
least 1500 workers in size. Similarly within supay 
chacras, smaller fragments of the extended colo- 
nies show extreme fidelity to their individual hosts, 
and only workers of the largest trees leave their 
hosts to swarm over seedlings and other vegetation. 
Moreover, the latter activities appear to be re- 
stricted to hot and sunny conditions (D. Davidson, 
personal observation), which may allow maximum 
worker activity and performance levels. To date. 


Volume 2 , Number 1 , 1 993 


27 



Fig. 3. Pseudomyrmex dendroicus Forel on branches of neighboring plants, whose leaves have been pruned by the 
ants. The long, thin body shape of workers in Pseudomyrmex spp. may preclude their use of plants with long, dense 
trichomes. 


there have been no experimental tests of the effects 
of creating artificial and unseverable bridges be- 
tween neighboring intact trees and hosts of these 
Myrmelachista. Such experiments would greatly 
aid in assessing the evolutionary significance of the 
extraordinary behavior of these ants. 

Hiding among Trichomes 

The long, dense and erect trichomes on stems 
and domatia of many myrmecophytic plants form 
mechanical barriers to the movements of large- 
bodied ants and create safe havens for colonies of 
obligate plant-ants with timid and diminutive work- 
ers (Davidson et al. 1 989; Fig. 4, Appendix 1 ). Ant- 
plants with inhibitory hairs on stems, domatia or 
both, occur in at least 18 neotropical genera (eight 
within Melastomataceae alone), and eight families, 
and appear to have evolved independently on at 
least 21 separate occasions (Table 1). In Africa, 
such hairy ant-plants occur in at least eight genera 
and six families, with each generic occurrence 
representing a single independent origin. Trichome- 


myrmecophytes have also evolved in at least four 
genera in the Oriental and Australian tropics (Table 
1 ), though the symbiotic associates of these plants 
remain unknown. In many or most genera of hairy 
ant-plants, long, erect pubescence also occurs in 
non-myrmecophytic congeners. It therefore seems 
likely that docile, small-bodied ants initially sought 
safe nesting and foraging sites on hairy plants prior 
to the evolution of myrmecophytism in these lin- 
eages. A possible contemporary example of such a 
relationship is that between Wasmannia scrobifera 
and a non-myrmecophytic hairy Piper species in 
Costa Rica (D. Davidson, personal observation). 
These ants build small fragile carton nests on abaxial 
leaf surfaces, where they feed on pearl bodies. 
Nests are not limited to individual host plants, nor 
are the ants likely to be obligate plant-ants. In some 
cases, ant dependency on plant trichomes may be 
restricted to the early stages of colony foundation. 
Thus, certain Azteca species regularly initiate colo- 
nies on pubescent ant-plants like Cordia and Tococa 
but later prune runways through host-plant tri- 
chomes and form carton satellite nests on neighbor- 
ing trees lacking protective trichomes (“i” in col- 


28 


Journal of Hymenoptera Research 



Fig. 4. Tiny Pheidole minutula Mayr workers travel easily among the erect trichomes of this myrmecophytic 
Clidemia. Numerous ant species with tiny workers use such “trichome myrmecophytes” as protected feeding and 
nesting sites, where they are safe from larger-bodied competitors and predators. 


umn 4 of Appendix 1 ; D. Davidson, personal obser- 
vation, Benson 1985). 

Contemporary distributions of ants across 
myrmecophytes in Africa and the Neotropics illus- 
trate the influence of plant trichomes on the match 
between ants and plants (Appendix 1). First, in both 
regions, worker ants of pubescent myrmecophytes 
are short-bodied (<3 mm), with short turning radii, 
and do not include longer-bodied pseudomyr- 
mecines. Included here are two neotropical genera 
with functional stings ( Allomenis and Solenopsis), 
and docile African dolichoderines in the genus 
Technomyrmex (species formerly placed in 
Eii gramma, Shattuck, 1992a). All known hosts of 
Allomenis and Solenopsis possess long erect pu- 
bescence. Allomenis is particularly conspicuous in 
its association with a diversity of pubescent host 
genera, seven in total. Of the recorded hosts of 
African Technomyrmex , species in five (and possi- 
bly six) of eight genera are hairy; only two, 
Leonardoxa and Ixora hippoporifera, definitely 
lack trichomes. To the extent that members of 
competitively dominant ant genera depend on pu- 


bescent ant-plants beyond the incipient colony stage, 
the particular species represented in these associa- 
tions are unusually timid for their genera (e.g., the 
Crematogaster cf. victima group on melastomes, 
the tiny Crematogaster sp. on Delpydora , and the 
Azteca species inhabiting hairy Triplaris 
poeppigiana Weddell). Second, the body sizes of 
plant-ants tend to be correlated with trichome spac- 
ing (Davidson et al. 1989). This suggests that 
ancestral ants may have nested preferentially not 
only on pubescent plants but specifically on those 
where mean distances between trichomes were no 
larger than required by their own body sizes. The 
parallels with nest selection by stem diameter in 
generalized stem-nesting ants are obvious (see 
above). 

Third, if ants compete for host plants (see 
Davidson et al. 1989), and if small, timid species 
persist only where protected by trichomes from 
larger dominants (> 3 mm, e.g., Crematogaster and 
Azteca ), then the dominants should prevail on 
myrmecophytes lacking inhibitory trichomes. This 
hypothesis is supported not only across ant-plant 


Volume 2, Number 1, 1993 


29 


genera (Appendix 1), but within several genera 
which are interspecifically variable in pubescence. 
In neotropical Cordia , for example, glabrous C. 
alHodora (R. and P.) Oken is regularly occupied by 
aggressive Azteca, but smaller and more timid 
Allomerus ants inhabit densely hairy C. nodosa. As 
noted above, a small-bodied and timid Azteca spe- 
cies inhabits the hirsute stems of Triplaris 
poeppigiana, though the vast majority of 
myrmecophytic Triplaris species are glabrous and 
occupied by long and narrow-bodied pseudomyr- 
mecines. Third, dominant Crematogaster ants oc- 
cupy glabrous African Canthium, whereas hairy 
congeneric hosts are associated with timid 
Teclinomyrmex species (Bequaert 1922, pp. 474- 
475). The same may perhaps be true in African 
Cuviera , which contains both glabrous and hirsute 
myrmecophytes. Both Teclinomyrmex and 
Crematogaster are recorded as associates of ant- 
plants in this genus, but the distribution of different 
ants in relation to plant pubescence cannot be 
discerned from existing literature. Finally, as noted 
above, some ants 3 mm in body length occasion- 
ally occupy trichome myrmecophytes but regularly 
prune trail systems, which facilitate their move- 
ments (Davidson et al. 1989). 

Association of Camponotus ants with spiny 
palms in the genus Korthalsia may also have had its 
origins in the tendency of ants to feed and nest 
where the plant's growing tips are protected from 
the ants’ natural enemies. Among the 12 Korthalsia 
species which Dransfield (1984) lists for Sabah, 
Malaysia, seven have armed ocrea and five do not. 
Of the species with spiny ocrea, all but K. ferox 
Becc. also show regular associations with ants, 
whereas this is true for none of the species with 
unarmed ocrea. Both the long, sharp and compara- 
tively dense spines of species K. echinometra Becc., 
K. hispida Becc. and K. robusta Blume, and the 
scattered, short, triangular spines of K. cheb Becc., 
K. furtadoana J. Dransf. and K. rostrata Blume are 
more likely to protect the ants from vertebrate 
predators than from other ants. Dransfield (1981) 
found greater herbivory by vertebrates (perhaps 
squirrels) on growing tips of K. rigida Blume (with 
unarmed ocrea and sparsely armed leaf sheaths) 
than on those of K. echinometra and K. rostrata. 
Although he attributed this result to protection that 


ants might afford to the latter species, an alternative 
hypothesis is that both the plants’ growing tips and 
the ant nests benefit from the armature of ocrea and 
leaf sheaths. This would not rule out some addi- 
tional benefit to the plant from its ants. Unfortu- 
nately, phylogenetic relationships remain unde- 
fined for both plants and ants, and it is not yet 
possible to determine the extent to which the vari- 
ous relationships between ants and armed Korthalsia 
evolved independently. However, Dransfield’s 
(1981) observation that Calamus species of New 
Guinea and the Philippines show parallel evolution 
of armed ocrea and relationships with ants suggests 
that myrmecophytism could have evolved more 
than once within Korthalsia as well. Similarly, 
myrmecophytic rattans in the genera Calamus and 
Daenionorops exhibit parallel evolution of ant gal- 
leries formed by interlocking combs of spines, 
forming collars on the leaf sheaths (Dransfield and 
Manokaran 1978). 

Rates of Resource Supply from Plants 

The impact of rates of resource supply on the 
match between ants and plants is best compared 
within host genera, holding food type approxi- 
mately constant. Within western Amazonia, for 
example, the rate of food body production by Ce- 
cropia varies across both species and habitat types 
(Davidson et al. 1991, Davidson and Fisher 1991, 
Folgarait and Davidson 1992). Faced with compe- 
tition from fast-growing pioneer species of similar 
stature, more light-demanding species of large riv- 
erine disturbances defer costly defense in favor of 
rapid growth. Because comparatively shade-toler- 
ant species of small forest light gaps experience 
light competition from much larger neighbors, di- 
version of limiting carbon from defense to growth 
might confer little benefit, and even jeopardize the 
persistence required to take advantage of later 
canopy openings. Thus, the more shade-tolerant 
Cecropia species produce swollen stems, prostomas, 
and trichilia much earlier in development than do 
their light-demanding close relatives (Fig. 5), as 
well as producing a greater dry weight of Mullerian 
bodies per unit leaf area. Despite this greater 
investment (proportional to the plant’s resource 
budget) in biotic defenses by small gap Cecropia, 


30 


Journal of Hymenoptera Research 


there are at least three reasons why the absolute 
rates of food provisioning to ants are greater in 
light-demanding pioneers than in closely related 
but more shade-tolerant gap species. First, and 
perhaps foremost, the smaller sizes of forest gap 
species at the time of colonization by ants are 
associated with fewer leaves (sources of food re- 
wards ) and slower pi ant growth rates. Second, even 
with plant size or light environment held constant, 
small gap Cecropia have intrinsically slower growth 
and leaf production rates than do their more light- 
demanding counterparts. Finally, comparatively 
low light intensities in their typical habitats further 
limit the capacity of the forest gap plants to produce 
ant rewards. 

Ants appear to respond to these quantitative 
differences in food production rates of Cecropia 
(Davidson et al. 1991, Davidson and Fisher 1991). 
For example, in southeastern Pern, patterns of ant 
associations are more closely tied to habitats than to 
host identities. Although the closest taxonomic 
relationships appear to be between Cecropia in 
different habitats (C. C. Berg, personal communi- 
cation), Aztecao\'aticeps¥oxc\ inhabits only intrin- 
sically fast-growing pioneers of riverine and stream- 
side habitats. In contrast, specialized Camponotus, 
Pacliycondyla and Crematogaster species, and 
Azteca australis Wheeler are the typical residents 
of relatively slow-growing and congeneric hosts of 
small light gaps. Although the latter ants frequently 
colonize riverine Cecropia , they seldom establish 
colonies there, and they may usually be outcompeted 
by rapidly developing colonies of A. ovaticeps. 
This pattern holds both within and across host 
species, and it suggests that ant species may coexist 
locally by virtue of their “included niches”. Spe- 
cies with rapidly growing colonies may dominate 
higher quality hosts, but be unable to tolerate low 
rates of resource supply. On the other hand, ants 
with relatively slow-growing colonies tolerate both 
high and low quality resources, but are usually 
excluded by competitors from fast-growing hosts. 

A similar pattern of niche differentiation is ap- 
parent within plant-ant guilds of other 
myrmecophyte taxa (including epiphytes) of both 
the New and Old World (Davidson and Epstein 
1989, Davidson et al. 1989 and 1991). For ex- 
ample, specialized Tetraponera are the typical resi- 


dents of Barteria fistulosa Masters growing in 
small forest treefall gaps, but Crematogaster domi- 
nate in large clearings (D. McKey, personal obser- 
vation). In Barteria nigritana J. D. Hooker, mostly 
restricted to light-rich coastal shrub vegetation, 
Crematogaster is the only recorded associate. In 
Leonardoxa africana Aubrev., Petalomyrmex is 
the typical associate of adult trees, and of a large 
proportion of juveniles. However, juveniles grow- 
ing in deeply shaded sites are usually occupied by 
Cataulacus (McKey 1984). The effects of insola- 
tion on resource quality can also be apparent within 
host species, as in the observation that Polyracliis 
species specializing on broad-leaved bamboos build 
their pavilions only in sunny areas of bamboo 
clumps (Dorow and Maschwitz 1990). 

At present, factors underlying interspecific dif- 
ferences in the resource demands of ants are poorly 
studied. However, just as the evolutionary diversi- 
fication of plants has been influenced by tradeoffs 
in allocation and life history strategies (e.g.. Grime 
1974), similar tradeoffs are likely to have contrib- 
uted to a proliferation of divergent ecological tac- 
tics in plant-ants (and ants in general, Tschinkel 
1991, A. N. Anderson 1991). Included among 
these life histories may be: 1) opportunistic (rud- 
eral) species with rapid colony growth rates, high 
worker turnover, high resource demands, small (or 
moderate) colony sizes with correspondingly weak 
colony defense, short colony lifespans, and early 
reproduction; 2) “tolerant” species with slow-grow- 
ing colonies, low worker turnover, low resource 
demands, high longevity, deferred reproduction, 
and effective defense of the nest site, and 3) com- 
petitive species with rapid colony expansion, low 
worker turnover, and large, long-lived, aggres- 
sively territorial and well-defended colonies. The 
evolution of such divergent ecological strategies is 
likely to have been influenced also by phylogenetic 
constraints, such as preexisting uses of exocrine 
glands (Blum and Hermann 1978, Buschinger and 
Maschwitz 1984), or the form of the proventricu- 
lus, which controls the capacity for and efficiency 
of liquid food storage and transport (Eisner 1957). 
Such phylogenetic constraints might help to ex- 
plain why the competitive rankings and strategies 
of ants are often well-defined (though not perfectly 
so) at the generic level. 


Volume 2, Number 1, 1993 


31 



Fig. 5. Tiny seedling of Cecropia 
“ tessmcnmii ”, whose myrmecophytic traits 
appear approximately with the fifth through 
seventh leaves past the cotyledon stage, and 
when plants are < 10 cm tall. Because of its 
extreme morphological similarity to C. 
membrcaiacea, C. (prov.) "tessmannii" is still 
technically lumped with that species (C. C. 
Berg, personal communication). However, 
C. membranacea , a pioneer of large, riverine 
disturbances, grows more rapidly and ac- 
quires its myrmecophytic traits at substan- 
tially and significantly later leaf nodes 
(Davidson and Fisher 1991). 


Other Traits of Weakly Competitive Ants 

Appendix 1 reveals numerous exceptions 
whereby the generic affiliations of ants are imper- 
fect predictors of subordinate or dominant status, as 
reflected by pruning behavior and association with 
trichome myrmecophytes or uncontested host plants. 
Nevertheless, some of these exceptions are consis- 
tent with the general principles developed here. For 
example, despite their chemical defenses, ants in 
some subgenera of Camponotus (especially 
Colobopsis and Pseiulocolobopsis) can behave as 
subordinates, living secretive lives inside their hol- 
low stem nests. Y et Camponotus of this description 
occur on a diversity of hosts that lack protective 
trichomes and, with one exception, they do not 
prune or attack vegetation around their hosts. At 
least two factors may explain the capacity of these 
species to persist on their hosts. First, major work- 
ers use their large and often modified heads to seal 


stem entrances effectively and to protect nests from 
invaders. Where ants obtain the majority of their 
resources from Coccoidea inside stems or domatia 
(e.g., under ocrea of Korthalsia), foraging occurs in 
seclusion and entails little risk. (A similar explana- 
tion may apply to the timid Plieidole colonies from 
myrmecophytic pipers and melastomes, which sup- 
ply food bodies inside domatia.) 

On the other hand, the extrafloral nectar of 
Endospennum and the Mullerian bodies of Cecro- 
pia , are produced on external plant surfaces. Here, 
the exclusivity of ant resources is protected in part 
by the temporary nature or temporal pattern of their 
production. For example, in the northern coastal 
forests of Papua New Guinea, Endospennum labios 
Schodde produces almost all of its extrafloral nec- 
tar in a brief pulse at about 3:00 AM, likely coincid- 
ing with the diel maximum in relative humidity 
there (Fig. 6). In contrast to myrmecophytic E. 
labios, a myrmecophilic congener, Endospennum 
uiedullosum L.S. Smith produces a greater fraction 


32 


Journal of Hymenoptera Research 


of its nectar during other periods of the diel cycle 
(D. Davidson, unpublished). Although many Ce- 
cropia species release Mullerian bodies slowly all 
day long, they also flush large numbers of these 
bodies just after nightfall (Davidson and Fisher 
1991). Moreover, ants with generalized diets are 
usually not attracted to the bodies (Rickson 1977, 
D. Davidson, personal observation). Camponotus 
associates of Endospenmtm and Cecropia both 
forage on leaf surfaces principally at night, and 
workers of Anoplolepis (not a plant-ant) can range 
freely over Endospennum during daylight hours 
(D. Davidson, personal observation). (See also A. 
N. Anderson’s [ 1991 ] discussion of noctumality in 
Australian Camponotus.) Cladomyrma of 
Neonauclea are nocturnal as well (D. Davidson, 
personal observation), though the object of worker 
foraging on Neonauclea has yet to be identified. 
Finally, some plant-ants in the genera My nnelachista 
and Allomerus are apparently restricted to their 
hosts diumally, but make nocturnal forays to the 
forest floor (J. Longino, personal communication). 
Together, these observations suggest that competi- 
tion may be reduced somewhat at night, though the 
nature of any restrictions on nocturnal activity in 
dominants is not readily apparent. While activity 
schedules of temperate and arid zone ants are 
strongly related to diel variation in temperature and 
humidity regimes, biotic selection pressures could 
be equally important or more important determi- 
nants of foraging times in ants of moist tropical 
forests. 

ANCESTRAL VERSUS MODERN 
RELATIONSHIPS 

We have argued that the matching of ants and 
myrmecophytic plants is convergently alike in dif- 
ferent tropical regions, and that this convergence 
arises from the presence of similarly preadapted 
plants and ants within the respective biotas. In 
concentrating on the associations as they exist 
today, we have neglected the pathways by which 
they may have reached their present form. Ant- 
plant symbioses have undoubtedly evolved from 
more casual and opportunistic relationships be- 
tween plants and ants. In their initial phases, many 
of these associations would likely have resembled 


modern-day relationships in which plants lack ob- 
vious speci al izations for hou si ng ants ( Appendi x I , 
“N” in column 6). Like most other forms of 
mutualism (reviewed in Thompson 1982), many 
symbiotic ant-plant mutualisms probably began as 
parasitisms. What factors may have facilitated the 
transition from parasitism to mutualism, and what 
character transformations could have accompanied 
this change? 

For plants hosting ants inside primary domatia 
(live stems and intemodes), ancestral relationships 
probably consisted of ants tending scale insects 
within natural plant cavities or in insect borings 
(cf.. Ward 1991). From the start, ants must have 
benefitted from access to exclusive resources in 
these protected environments. However, to have 
remained entirely in the sanctity of the host plant, 
ants would have needed a well-balanced diet. Ho- 
mopteran exudates contain not only carbohydrates, 
but some amino acids and lipids (reviewed in 
Buckley 1987), and ant colonies are known to 
harvest and eat Homoptera to meet their protein 
requirements (e.g.. Way 1954, Pontin 1978). Fur- 
thermore, in both New and Old World tropics, as 
well as in Australasia, some plant-ants have evolved 
means of obtaining added protein and fats from 
elaborated calluses or heteroplasias caused by trau- 
matic injury to either the inside ( Tetraponera on 
African Vitex, Bequaert 1922) or outside of host 
plant stems (South American Pseudomyrmex on 
Triplaris , and New Guinea Camponotus on 
Endospennum [D. Davidson, personal observa- 
tion], and possibly Central American Mynnelachista 
on Ocotea [J. Longino, personal communication]). 
In large part then, coccoid-tending residents of live 
stems and cavities could probably have depended 
on hosts to satisfy most or all of their nutritional 
needs, even from the earliest stages of their rela- 
tionships with these plants. 

In contrast, the impact of symbiotic ants on their 
host plants would have depended on the balance 
struck between resource losses to scale insects and 
ants, and any anti-herbivore protection the ants may 
have originally afforded. Although the majority of 
ants would probably have provided at least some 
protection against stem and leaf parasites, the 
Coccoidea would surely have been a liability. 
Substantial carbohydrate losses sustained by the 


Volume 2, Number 1, 1993 


33 



Fig. 6. This large drop of extrafloral nectar was produced in a brief pulse at 3:00 AM on the petiolar nectaries of 
Endospenmun labios, at the Christensen Research Station near Madang in Papua New Guinea. (Screenhouse plant 
courtesy of M. Jehb.) 


plants should have been most debilitating to car- 
bon-limited (light-limited) plants. Thus, in habitats 
of low light intensity, natural selection on plants 
may have acted mainly to exclude both ants and 
Homoptera. However, where light was abundant, 
the benefits of ant defense could have outweighed 
carbohydrate losses (on average). Natural selection 
on these plants should have favored attraction of 
ants, rather than resistance to them. In this way, the 
propensity of ant-parasitized plants to evolve to- 
ward myrmecophytism could have been facilitated 
by high availability of carbon (light) in relation to 
limiting mineral nutrients, and impeded when such 
ratios were low. Furthermore, if herbivore pres- 
sures are generally more intense in comparatively 
productive, sunny environments (see Davidson and 
Fisher [1991] for Cecropia), this trend could have 
reinforced selection for ant attraction in such habi- 
tats. 

Although our data set lacks the resolution to test 
this hypothesis, the hypothesis is consistent with 
the central result of Schupp and Feener’s (1991) 
recent survey of the distribution of ant attractants 
(EFN’s and pearl bodies) within the flora of Barro 
Colorado Island, Panama. While the occurrence of 


such rewards was clearly correlated with phylog- 
eny, it also appeared to depend on the light environ- 
ment. Plant families characteristic of forest light 
gaps were overrepresented among ant-defended 
families. (See also the frequency of superscripts 
“e” and “g” in column 2 of Appendix 1.) Schupp 
and Feener hypothesized that the high frequency of 
ant defenses among forest gap plants may be ex- 
plained by the comparatively low costs of produc- 
ing carbohydrate ant rewards in these light-rich 
habitats, as well as by the tendency for relatively 
continuous growth and leaf production in gap spe- 
cies. The latter explanation meshes well with 
McKey’s (1989) interpretation of biotic defenses 
as an alternative to phenological escape from her- 
bivory (i.e., escape from detection, due to variable 
and unpredictable new leaf production). Pheno- 
logical escape would be unavailable to plants with 
continous leaf production. 

There are some indications that the absence of 
scale insects may be the derived condition in rela- 
tionships involving pseudomyrmecines (P. Ward, 
personal communication). Thus, although 
Coccoidea can be found at the bases of spines on 
African and Indian Acacia housing Tetraponera, 


34 


Journal of Hymenoptera Research 


PseudomyrmexAnhsfoited Central American Aca- 
cia lack scale insects but supply protein-rich Beltian 
bodies. Moreover, the gnawing of internal stem 
walls by Tetraponera tessmannii (Stitz)on African 
Vitex, to produce tunnels with terminal nutritional 
heteroplasias, could have had its origins in the 
excavation of pits to increase the feeding efficien- 
cies of coccoids, now absent from this system (see 
Bailey 1922 for Cuviera). 

For plants that continued to be inhabited by ants 
and scale insects, natural selection would be ex- 
pected to favor a reduction in the ratio of coccoid to 
ant biomass. Although many obviously specialized 
ant-plants still harbor Coccoidea (Appendix 1), 
there is considerable variation across all the ant- 
plants in the densities of scale insect populations 
(D. Davidson, personal observation). At one ex- 
treme are the comparatively unspecialized relation- 
ships between Anonychomyrma (previously 
Iridomyrmex [Shattuck, 1 992b]) and Crenuitogaster 
ants, and a number of pachycaulous understory 
New Guinea trees. Here, the biomass and density 
of Cryptostigma scales are so great that their popu- 
lations may well be limited by either plant re- 
sources or the availability of feeding sites (D. 
Davidson, personal observation). In contrast, in its 
more specialized relationship with Triplaris 
americana L., Pseudomyrmex dendroicus Forel 
maintains only approximately one scale insect per 
leaf junction, and similarly low coccoid densities 
are apparent in Cecropia stems inhabited by Azteca 
ovaticeps and A. australis. 

By what proximate mechanisms might plants 
have responded to selection for reducing losses to 
Homoptera? For myrmecophilic plants, Becerra 
and Venable (1989) have argued that EFN produc- 
tion could have arisen as a means of paying ants 
directly and eliminating parasitic homopteran in- 
termediates. Even if EFN’ s provided ant rewards 
comparable to or lower in value than homopteran 
secretions, reduced resource handling times might 
have induced ants to feed at nectaries and to aban- 
don their Homoptera. In turn, plants would have 
benefitted from lower rates of infection with ho- 
mopteran-mediated diseases and possibly lower 
resource losses. One difficulty with applying this 
theory to the evolution of myrmecophytes is that it 
ignores an important distinction between coccoids 


(the usual homopteran associates of plant-ants) and 
EFN’s. While EFN’s are relatively promiscouous 
resources, accessible to many ants, coccoids tended 
inside cavities can be used exclusively by symbi- 
otic ant associates. If the latter ants are the most 
effective mutualists of the plant, and provide better 
protection in the absence of opportunistically for- 
aging competitors, selection may favor loss of 
EFN’s. There is evidence for such a scenario in 
myrmecophytic Asian Macaranga, which, in con- 
trast to their non-myrmecophytic congeners, al- 
most completely lack EFN’s (Fiala and Maschwitz 
1991). 

A second difficulty with the hypothesis of 
Becerra and Venable (1989) is that it ignores the 
possibility that colonies might keep pace with the 
added resources (EFN) through short-term rede- 
ployment of workers or long-term growth. If so, 
ants might continue to tend Homoptera while also 
feeding from EFN’s. A plausible alternative hy- 
pothesis is linked to the assumption that growth of 
ant colonies (like that of plants. Bloom et al. 1 985) 
is limited by the ratio of carbon and nitrogen re- 
sources. By rewarding ants with abundant carbo- 
hydrate but starving them for protein (Carroll and 
Janzen 1973), plants might have induced colonies 
to consume the majority of their Homoptera. In 
support of this argument, Oecophylla longinoda is 
known to consume more coccoids when given a 
supplemental sugar source (Way 1954). Moreover, 
M. Anderson (1991) attributes “switching” be- 
tween predation and mutualism in ant-homopteran 
relationships (see also Pontin 1958 and 1978) to 
changes in the nutritional status of the ant colony. 
If homopteran populations are regulated in re- 
sponse to ratios of carbon and nitrogen availablity 
to ants, colonies might be expected to maintain 
their associates at densities which supply these 
resources at optimal ratios for colony growth. Cur- 
rently, a lack of data prevents further speculation as 
to how the relative availability (to ants) of carbohy- 
drate and protein might vary with homopteran 
densities. Future investigations might profitably 
focus on natural or experimentally induced varia- 
tion in the relative biomasses of ants and Homoptera 
in particular ant-plant systems. 


Volume 2, Number 1, 1993 


35 


PLANT FITNESS IN RELATION TO ANT 
SPECIES 

In many ecological studies of ant-plant symbio- 
ses, investigators have focused principally on the 
question of whether or not a given ant associate 
benefits its host species. With recently renewed 
appreciation for the diversity of ants colonizing 
individual myrmecophytes comes the realization 
that ants may differ in the protection afforded their 
hosts (e.g.,Janzen 1975, Oliveira et al. 1987, Rico- 
Gray and Thien 1989, Davidson etal. 1991,Longino 
1991a and b, but see Vasconcelos 1990, for a 
counterexample), and that associations must be 
studied in the context of community-wide interac- 
tions. While existing data are too meager to corre- 
late protection with specific ant traits, some conjec- 
tures are warranted. Rapid colony development, 
large colony size, and high levels of worker activity 
should enhance host-plant defense. Large insect 
herbivores (Coleoptera and Orthoptera) may be 
best deterred by active, large bodied workers 
(Davidson and Epstein 1989). In contrast, division 
of colony biomass among numerous small foragers 
may promote fine-grained searching and facilitate 
the detection of small prey, for example, lepi- 
dopteran eggs (Letourneau 1983, Vasconcelos 
1991). Some authors have suggested that small and 
timid ants provide little protection against herbi- 
vores, but augment the nutrient reserves of their 
hosts through deposits of feces and refuse (e.g., 
Janzen 1974b, Beattie 1985). However, at least two 
studies have confirmed the effectiveness of small, 
docile Pheidole ants in defending against either 
insect eggs (Letourneau 1983), or herbivorous lepi- 
dopteran larvae (Vasconcelos 1991). While nutri- 
ent enhancement has been demonstrated convinc- 
ingly in myrmecophytic epiphytes and palms 
(Rickson 1979, Rickson and Rickson 1986), tests 
have disputed the theory for the symbiotic associ- 
ates of Macarcmga (Fiala et al. 1989) and Maieta 
(H. Vasconcelos and B. Forsberg, personal com- 
munication). On reflection, possibilities for nutri- 
ent enhancement are limited by the infrequency of 
foraging off the host (Appendix 1, column 4) and, 
consequently, by the inability of ants to concentrate 
materials from the broader environment. 

Two other cases are likely candidates for nutri- 


ent augmentation by ants (D. Davidson, personal 
observation). First, certain Azteca species center 
their carton nests on Tococa and Hirtella species 
and contribute to a steady rain of carton and refuse 
at the base of the host tree trunk. Second, as a 
rheophyte of stream beds and rocky river beaches, 
Mynneconauclea strigosa (Korth.) Merrill grows 
with its roots anchored in rock crevices. The 
Crematogaster ants, which are its dominant associ- 
ates in forests west of Lahad Datu, Sabah, pack 
refuse and feces into domatia at the distal branch 
tips, from which new swollen internodes arise. The 
absence of any obvious food reward (including 
Homoptera) suggests that ants might leave their 
hosts to forage. If such is the case, workers could 
concentrate nutrients which enhance fitnesses of 
hosts growing in extremely nutrient-poor environ- 
ments. 

In some cases, myrmecophytism actually con- 
tributes to host-plant damage by destructive verte- 
brate predators of ant larvae (especially by wood- 
peckers [Carroll 1983] and monkeys [Freese 1976, 
and J. Terborgh, personal communication, for Ce- 
cropia). Damage by primates may be less common 
for hosts of ants with powerful stings. First, in 
Peruvian Amazonia, Pachycondyla luteola Roger 
(the “pungara”) is an obligate symbiont of Cecro- 
pia , and its painful barbed stings reinforce verte- 
brate learning for a period of seven to ten weeks ( D. 
Davidson, personal observation). Avian prefer- 
ences for nesting in this (Koepcke 1972) and other 
myrmecophytes with stinging ants (Young et al., 
1990) may be at least partly attributable to the 
protection which ants afford against primates. Sec- 
ond, the Tetraponera of African Barteria fistulosa 
also impressed Janzen (1972) as effective deter- 
rents of vertebrates, and a black colobus monkey 
avoided ant-occupied Barteria , while feeding on an 
unoccupied individual nearby (McKey 1974). Gray- 
cheeked mangabey monkeys ( Cercocebus albigena 
[Gray] ) rip open the branches of this host to prey on 
Tetraponera brood, but only if this can be accom- 
plished by reaching from a perch in a different tree 
(D. McKey, personal observation). Even large, 
stinging plant-ants may not affect some vertebrates, 
however. Gorillas in the Central African Republic 
feed on B. fistulosa leaves and branches apparently 
undeterred by healthy, active colonies of 


36 


Journal of Hymenoptera Research 


Tetraponera (M. Fay, personal communication). 
Finally, because plant-ants with functional stings 
also usually prune the vegetation surrounding their 
hosts, crowns inhabited by such ants are usually 
sufficiently isolated in forest gaps to avoid the 
attacks of primates which visit neighboring trees. 

TRENDS IN SPECIALIZATION, SPECIFICITY 
AND COEVOLUTION 

Because the evolutionary histories of symbiotic 
ant-plant systems have been largely independent in 
biogeographically disjunct tropical regions (Me Key 
and Davidson, in press), intercontinental compari- 
sons may provide general insights into the evolu- 
tionary dynamics of such systems. In this section, 
we discuss evolutionary interactions between ants 
and plants, focusing on three questions: (1) Has 
specialization of ants and plants followed similar 
evolutionary pathways due to parallel and/or con- 
vergent evolution in organisms from different con- 
tinents? (2) Have evolutionary interactions be- 
tween ants and plants contributed to the generation 
of diversity in plant-ants and ant-plants? (3) If so, 
are these interactions a partial cause of interconti- 
nental differences in diversity of ant-plants and 
plant-ants? Again we focus mainly on the Ameri- 
can and African tropics, whose ant-plant associa- 
tions are best known. 

The Nature and Causes of Specificity 

Symbiotic ant-plant systems are in general more 
species-specific than are nonsymbiotic ant-plant 
interactions (e.g., Schemske 1983). All tropical 
regions contain examples of ant-plants that are 
obligately associated with one or a small number of 
plant-ant species, which in turn have comparably 
restricted host-plant ranges. In such cases, speci- 
ficity is doubtless a product of intense evolutionary 
interaction. However, much of the seeming speci- 
ficity in ant-plant symbioses may be maintained by 
ecological processes that require no evolutionary 
specialization in ant or plant. We have argued that 
characteristic and repeatedly observed plant-ant 
matches are the result of species sorting (Jordano 
1987) of plants and ants which are mutually pre- 
adapted in many attributes related to the interaction 
(Davidson et al. 1989 and 1991, Davidson and 


Fisher 1991). Driven by the strong competitive 
interactions that structure communities of 
arboricolous ants, the matching of plants and ants is 
determined by plant and ant traits which modify ant 
access to plant resources. 

In a growing number of ant-plant systems, we 
now recognize that seemingly specialized plant- 
ants may be capable of living on any of several 
hosts, and that many or most myrmecophytes can 
persist in association with any of several plant-ants. 
Nevertheless, some relationships are more frequent 
and/or more durable than others. Understanding 
the ecological processes which reduce broad poten- 
tial niches of plant-ants and ant-plants to narrower 
realized niches is a prerequisite to an evolutionary 
investigation of such systems (Davidson and Fisher 
1991). First, ecological studies suggest simpler 
alternatives which must be excluded before hy- 
potheses of evolutionary specialization and coevo- 
lution can be entertained. Second, if ecological 
causes of specificity can be defined, these will 
suggest the likely selective environments in which 
any evolutionary specialization may have taken 
place. Third, studies of unusual associations may 
give clues about the origin of both host-plant speci- 
ficity and host switches, which seem to have taken 
place frequently in symbiotic ant-plant systems 
(Ward 1991). 

Evolutionary Specialization of Ants and Plants 

If competitive interactions among ants are suffi- 
ciently strong and constant, ecological sorting will 
produce predictable patterns of ant-plant associa- 
tions and a selective environment conducive to 
evolutionary specialization (Schemske 1983). Evi- 
dence from various tropical regions suggests that 
evolutionary specialization of ant-plants and plant- 
ants may have been driven largely by competition 
among ant species. Even strong pairwise ant-plant 
mutualisms, it appears, owe many of their traits to 
an evolutionary background of multispecies an- 
tagonistic interactions. Whether these character 
states were evolved in the context of the symbioses, 
or merely fine-tuned from pre-existing traits, often 
cannot be argued confidently from existing data. 
Nevertheless, many traits of both plant-ants and 
their hosts may have been elaborated because of 


Volume 2, Number 1, 1993 


37 


their selective value in the context of symbiotic 
association. 

Ants . — Because ants actively choose their hosts, 
selection should strongly favor specializations for 
rapid and efficient host location by queens. In 
addition to minimizing exposure to predation and 
other environmental hazards, such adaptations could 
help to assure priority of access to contested re- 
sources. Indeed, competitively inferior ants might 
even usurp the hosts of more dominant species by 
evolving rapid means of finding and entering these 
plants. First, almost nothing is known about the 
kinds of information that queens employ to locate 
suitable hosts, but a variety of chemical, visual and 
other cues may be used at different stages of host 
identification. Whatever the mechanisms of host 
identification, the abilities of queens to locate and 
colonize specific hosts, and their absence from 
other hosts and habitats ( Davidson et al. 1 989, Fiala 
and Maschwitz 1990, Morawetz et al. 1992), pro- 
vide some of the strongest evidence of evolutionary 
specialization to the symbiosis. Second, the ex- 
treme dorsiventral flattening of the head, thorax 
and abdomen of Petalomyrmex queens could have 
arisen due to selection for rapid entry of 
myrmecophytes in the face of intraspecific and 
interspecific competition for hosts (McKey 1991). 
Alternatively, however, specialized queen shapes 
might have evolved first in generalized stem-nest- 
ing ants (Longino 1989b), preadapting such ants to 
become specialized plant-ants. Without additional 
phylogenetic analysis, adaptations in body shapes 
remain indistinguishable from preadaptations. 

Once foundresses have safely entered a host, 
their success on plants of different growth rate, 
maximum size, or lifespan, will likely depend on 
key energetic, demographic, and life history fea- 
tures of the colony. Intrinsically rapid rates of egg 
production and development of incipient colonies 
could be favored on fast-growing plants, and 
pleometrosis might substitute for this in at least 
some ant species (Davidson etal. 1991). However, 
before evolutionary specialization can be inferred 
from an apparent matching of colony attributes and 
plant growth rates, careful phylogenetic analysis 
must exclude the alternative hypothesis that ant 
traits evolved prior to the origin of the symbiosis. In 
the case of the Azteca and Cecropia , this caution is 


reinforced by the likelihood that A. ovaticeps and its 
relative A. alfari , may have originated from a weedy 
species which was typical of second growth vegeta- 
tion (Longino 1991b), and whose life histories 
could have preadapted it for occupation of rela- 
tively fast-growing hosts of riverine succession. In 
contrast, A. australis and its relative A. xantliochroa 
Roger, are probably derived from carton-building 
ancestors (Longino 1991b), whose comparatively 
permanent homes may have predisposed them to 
evolve life history traits typical of modern-day 
descendants on slower-growing and, in most cases, 
longer-lived, forest gap Cecropia. 

Many or most specialized plant-ants appear to 
have been relatively weak competitors, in which 
aggressive behavior could well have been maladap- 
tive. Nevertheless, within the limited spheres of 
their host plants, a number of these ants appear to 
have evolved greater similarity to dominants, de- 
fending absolute territories defined by the bound- 
aries of individual trees. Thus, one scenario appar- 
ent in several plant-ant lineages is that of increased 
colony size and aggression in response to symbiotic 
association with myrmecophytes (e.g., Janzen 
1966). For example, the extended colonies of 
Myrmelachista ants on pure stands of Tococa 
occidentalis (see above) reach an estimated worker 
population 1-2 million ants (Morawetz et al. 1992). 
Moreover, on Peruvian Cecropia, Pachycondyla 
luteola exhibits the largest and most aggressive 
colonies achieved by any ponerine ant. Host trees 
>30 m tall literally seeth with aggressive, stinging 
workers, and populations almost certainly range 
into tens or hundreds of thousands of workers (D. 
Davidson, personal observation). Even if rigorous 
phylogenetic analysis confirms that closest rela- 
tives of these ants have much smaller and less 
aggressive colonies (as do Pachycondyla sp. nov. 
on Panamanian Cecropia hispidissima Cuatracasas, 
Davidson and Fisher 1991 ), ecological studies will 
be necessary to determine whether the purportedly 
evolved demographic responses of P. luteola are 
examples of evolutionary accommodation or only 
plasticity in colony structure. For colonies nesting 
and feeding in the comparative security of 
myrmecophytes, increasing worker life spans, and 
nest sites which grow, rather than decaying (like 
dead twigs), could lead automatically to larger 


38 


Journal of Hymenoptera Research 


worker populations, and greater aggression might 
follow as a behavioral response to colony size. 
Similarly, the polygyny and/or pleometrosis noted 
as typical or occasional in some purportedly highly 
specialized plant-ants (Janzen 1966 and 1973, 
McKey 1984, Davidson and Epstein 1989,Longino 
1989b, Vasconcelos in press) may be a plastic 
response to resource availability or competition, 
since queen number can vary similarly in other ant 
species (Ward 1 989b, Holldobler and Wilson 1990). 
Although queens of Azteca australis found their 
colonies individually on isolated hosts in small 
light gaps, they often cooperate to initiate colonies 
on the faster growing plants of riverine distur- 
bances, where both rates of food supply and com- 
petition from other incipient colonies are greater 
(Davidson et al. 1991). At present it is unclear 
whether pleometrosis in the latter environment 
arises from evolutionary adaptation to competition 
or merely from greater numbers of alates produced 
and available in that habitat. 

Pruning of vines and other vegetation in the 
vicinities of hosts is one trait which provides less 
ambiguous evidence for evolutionary accommoda- 
tion to competition for hosts. Facultative pruning, 
requiring the presence of enemy ants, may eventu- 
ally prove to be widespread among unspecialized 
close relatives of obligate plant-ants. However, 
both obligate pruning, and the maintenance of 
vegetation-free zones at the host-plant base, appear 
to occur predominantly in ants whose highly spe- 
cialized diets (Janzen 1966, Davidson et al. 1989, 
Fiala and Maschwitz 1990, Morawetz et al. 1992) 
and unitary host genera (but see Ward 1991) pro- 
vide independent evidence for specialization. 

A final category of specialized ant traits may 
have little or no relevance to competitive ability but 
nonetheless serve as useful indicators of degree of 
evolutionary specialization in plant-ants. For ex- 
ample, Ward’s (1991) phylogenetic analysis of 
pseudomynnecines points to trends for plant-ants 
to have reduced eye size and palpal segmentation, 
as well as hypertrophied metapleural glands (ex- 
cept in cacia-ants). Palpal segmentation is also 
reduced in African Engramma (now included in 
Technomyrmex , Shattuck, 1992a), in comparison 
to other dolichoderines from the Ethiopian region 
(Holldobler and Wilson 1990). Reduction in anten- 


nal segmentation occurs in some lineages of 
Allomerusi Wheeler 1 942), and arboreal stem-nest- 
ing Cladomyrma have fewer antennal segments 
than do most other formicines (Holldobler and 
Wilson 1990). Although 1 0-merous antennae are 
characteristic of more generalized Myrmelachista 
species (subgenus Hincksidris) which nest in dead 
stems, specialized Central American Mynnelachista 
plant-ants have antennae with only 9 segments. 
Lastly, barbed stings are probably derived in both 
Pseudomyrniex ants (Janzen 1966) and 
Pachycondyla luteola (D. Davidson, personal ob- 
servation). In general, sting defenses may be more 
effective against solitary vertebrates than against 
social insect enemies (Davidson et al. 1988), and 
barbed stings may have evolved under selection to 
reinforce learning by vertebrate enemies. 

Plants. — In myrmecophytes, domatia and vari- 
ous food rewards offer clear support for evolution- 
ary specialization, all the more so since the produc- 
tion of such structures can entail obvious costs. 
Ecological costs of myrmecophytic traits may be 
evident in both the presence of ants, as when ant 
predators open the nests (see above), and in their 
absence, e.g., when herbivores invade and inhabit 
foliar or stem domatia (Jolivet 1991, Vasconcelos 
1991). Costs are most evident, however, when 
myrmecophytic traits are lost in the absence of 
symbiotic ants. For example, though Cecropia 
peltata L. is myrmecophytic throughout most of its 
distribution, conspecifics in Caribbean island popu- 
lations lack Mullerian bodies and have trichilia 
reduced or absent (Janzen 1973; Rickson 1977). 
(Non-myrmecophytic Cecropia schreberiana 
Miquel might have been mistaken for C. peltata on 
some of these islands [C. Berg, personal communi- 
cation].) In more recent history, introduced Cecro- 
pia obtusifolia Bertoloni of Hawaii, and C. peltata 
imported to both Asia and Africa have either lost 
their Mullerian bodies or trichilia, or are polymor- 
phic for these characters and exhibit a range of 
trichilia sizes (D. Davidson, personal observation, 
Putz and Holbrook 1988). Although it could be 
argued that such losses are determined environ- 
mentally, rather than genetically, African popula- 
tions of Cecropia peltata lacked trichilia even when 
grown from seed in greenhouses, where progeny of 
myrmecophytic congeners from their native habi- 


Volume 2, Number 1, 1993 


39 


tats have never failed to produce trichilia (Davidson, 
unpublished). 

Selection may also act on plant characteristics 
which influence the outcome of ant-ant competi- 
tion for the resources offered. In so doing, evolu- 
tion might enhance traits which favor the most 
effective mutualists (at levels of defense invest- 
ment optimal for the plant) over their competitors. 
Perhaps most remarkable. Piper ant-plants appar- 
ently produce food bodies only when stimulated to 
do so by the appropriate Pheidole ants (Risch and 
Rickson 1981), or by specialized parasites of the 
ant-plant mutualism (Letoumeau 1990 and 1991). 
The persistence of Mullerian bodies on Cecropia 
trees lacking specialized ants (Rickson 1977, D. 
Davidson, personal observation) provides evidence 
that these bodies are not recognized by unspecialized 
ants as suitable food. Moreover, Mullerian bodies 
of at least Cecropia (prov.) “ tessmann', Cecropia 
hispidissima , and possibly Cecropia ficifolia 
Snethlage appear to have been modified evolution- 
arily to favor their usual resident ants (Davidson 
and Fisher 1991 ). 

In a variety of ways, selection might modify the 
quality, rate, timing or position of the food reward 
to encourage either fine-grained or coarse-grained 
foragers, large or small workers, and aggressive, 
energy-intensive competitive dominants or timid, 
energy -conservative subordinates (see above). As 
an extreme example, plants which provision ants 
with complete diets may facilitate the persistence 
of weakly competitive species, whose foraging can 
then be restricted to the host itself (Appendix I, 
column 4). At least some species of Triplaris 
induce fine-grained foraging by ants with highly 
specialized foraging behaviors. These hosts pro- 
duce pearl bodies which are unique in their yellow 
color (perhaps indicative of some distinctive nutri- 
tional quality) and. are distributed in patches on 
adaxial leaf surfaces. Perhaps pre-adapted for this 
behavior by prior dietary specialization on pollen 
and fungal spores (Wheeler and Bailey 1920), the 
Pseudomyrmex residents of these myrmecophytes 
accumulate these tiny food bodies on their append- 
ages while constantly traversing leaf surfaces. They 
groom the material frequently onto their sting 
sheaths, which serve as storage sites until workers 
return to their nests (Davidson et al. 1988). 


In a number of ant-plant genera, food rewards 
for ants are often produced in more localized and 
defensible sites on true myrmecophytes than on 
myrmecophilic relatives with more promiscuous 
rewards. Thus, in the Endospennwn of New Guinea 
(Airy-Shaw 1980), myrmecophilic E. wedidlosum 
has moderately sized EFN’s scattered across abaxial 
leaves along primary and secondary veins. Petiolar 
nectaries are only slightly larger. In comparison, 
myrmecophytic congeners have greatly enlarged 
petiolar EFN’s and all other EFN’s greatly reduced 
in size and number. Similarly, in the genus 
Macaranga , at least some myrmecophilic species 
have scattered pearl bodies used by a number of 
unspecialized ants (D. Davidson, personal observa- 
tion in New Guinea), whereas the most highly 
evolved myrmecophytes restrict access to food 
bodies by hiding them beneath recurved stipules. 
In incipient myrmecophytes, A/. hosei King ex Hk. 
f. and M. pruinosa (Miq.) Muell.Arg., whose stems 
are not naturally hollow and are only partially 
occupied, accessibility of food bodies appears to be 
intermediate (Fiala et al. 1991). Thus, although 
food bodies are locally concentrated on stipules, the 
stipules are horizontal, leaving them exposed. 
Experimental studies might focus profitably on the 
outcome of ant-ant competition in relation to the 
spatial patterning, accessibility and defensibility of 
ant rewards. Similar relationships are well ac- 
cepted for other plant-animal mutualisms (e.g., 
Feinsinger and Colwell 1978). 

Restrictive entrances to domatia (Fig. 7) may 
render these structures more readily habitable by 
some ants than others, as well as limiting access to 
stem-dwelling Coccoidea. Prostomas of myrme- 
cophytic Leonardoxa are matched to the shapes and 
sizes of their associated ants (McKey 1991), 
Urticating hairs on the prostoma of Cecropia (prov.) 
“ tesswannii" favor large-bodied queens of 
Pachycondyla luteola over smaller-bodied Azteca 
queens (Davidson and Fisher 1991). In general, 
neither the selective effects of these traits on differ- 
ent ant associates, nor their consequences for plant 
fitness are well documented. Nor is it often clear 
where “preadaptation” stops and adaptation be- 
gins. For example, the thin pith cavities of 
myrmecophytic Vitex lianes are easily exploited by 
the plant’s specialist associate, the slender 


40 


Journal of Hymenoptera Research 


Tetraponera tessmannii , but not by stouter ants of 
similar body length. At present, however, there is 
no evidence to suppose that either plant or ant has 
evolved to produce or enhance such a match. Even 
the long, elliptical prostoma of Leonardoxa africana , 
matched to the flattened queens of Petalomynnex 
(McKey 1991), might be explained as preadapta- 
tion. As in numerous other ant-plants with stem- 
domatia, this myrmecophyte’s prostoma occurs at 
the node, opposite the leaf insertion, where a reduc- 
tion in xylem leaves the stem wall relatively thin 
(Bailey 1922). In future studies, both field experi- 
ments and careful phylogenetic analyses of plant 
and ant lineages will be required to determine how 
frequently myrmecophytes may have evolved to 
influence ant-ant competition. 

Limits to Specialization 

The forces leading to specialization in ant-plant 
symbioses are both clear and consistent with theo- 
retical arguments predicting greater specialization 
in mutualistic systems where strong antagonistic 
interactions occur among competing mutualists 
(Law and Koptur 1986). What factors then limit 
species specificity and account for the persistence 
of systems in which multiple ants coexist on the 
same host, or a single ant occupies several hosts? 
What are the limits to specialization? First, the 
matches produced by ecological sorting do not 
necessarily result in mutualistic interactions. A 
plant may be fortuitously 'preadapted’ to harbor a 
persistent parasite, as well as an effective mutualist. 
Depending on the match, an association might 
engender strong reciprocal specialization (when 
most effective mutualists are paired), asymmetrical 
specialization, or even antagonistic interactions in 
which specialization in ants and plants proceeds in 
opposite directions. 

Even when ant-plant associations are funda- 
mentally mutualistic, there may be both genetic and 
ecological limits to specialization and coevolution 
(Schemske 1983, Kiester et al. 1984, Howe and 
Westley 1988). The nature of any genetic con- 
straints is purely a matter for speculation. By and 
large, we do not know the extent of heritable 
variation for relevant ant and plant traits, nor whether 
such variation might limit specialization. Like- 


wise. population structure of ant-plants, and espe- 
cially that of plant-ants, is too poorly understood to 
support much discussion of how specialization and 
species origination might take place in these sys- 
tems. Since sexual selection can drive rapid evolu- 
tionary specialization and coevolution in mutual- 
ists, added information on ant mating sites and 
behaviors or data from genetic markers might be 
especially interesting in helping to determine 
whether mating could be non-random with respect 
to the host species where alates originated. 

More can be said about potential ecological 
limits on the intensity of selection for specializa- 
tion. Most significantly, the outcome of an ant- 
plant interaction may often depend not only on the 
specific identities of associates but also on habitat 
type and plant size. As summarized above, habitat 
may influence the match between plants and ants 
through both ecological and evolutionary variation 
in rates of resource supply to ants. The effects of 
habitat heterogeneity could also be mediated through 
other mechanisms that are still poorly understood. 
For example, on isolated plants, or where nutrient 
poverty limits productivity and alate production, 
low frequencies of host plant colonization may 
reduce the intensity of ant-ant competition for hosts 
(Vasconcelos, in press, D. Davidson, personal ob- 
servation). Herbivore pressures on at least some 
myrmecophytes appear to differ with habitat and 
plant size (Davidson and Fisher 1 99 1 , Janzen 1 974a, 
Letoumeau 1983), as does the probability that 
overgrowing vines will threaten both the host and 
resident ant colony (Rickson 1977, Davidson and 
Fisher 1991). Perhaps also varying with habitat are 
the densities of queen and brood parasitoids, which 
either kill incipient colonies, or prolong their devel- 
opment (Davidson and Fisher 1991). Finally, the 
outcome of competition among ants for host plants 
may be influenced by habitat-correlated physi- 
ological effects on colony development. In Azteca 
ovaticeps , queen mortality prior to first worker 
production is much higher on shaded hosts at the 
forest edge than on hosts of large, sunny and hot 
riverine disturbances (Davidson et al. 1991). In 
both the Azteca of South American Cecropia and 
myrmelachistines of African Leonardoxa , inter- 
specific variation in queen color correlates with 
habitat in a manner consistent with the hypothesis 


Volume 2, Number 1, 1993 


41 



Fig. 7. Restrictive entrance to domatia of the African myrmecophyte Leonardoxa africana (Baill.) Aubrev. 
(Fabaceae: Caesalpinioideae). The plant's mutualistic ant associate, Petalomyrmex phylax Snelling, makes these 
slit-like entrances at the site of the prostoma, which is of similar shape. The entrance allows access by the specialized 
dorsoventrally flattened foundresses of P. phylax, but not by other ants of similar size. Workers of P. phylax are 
of normal shape, but can easily pass through these entrances because they are much smaller than dealate queens of 
Petalomyrmex or workers of other ant species associated with the plant. 


that black queen coloration could be adaptive on 
fast-growing hosts, possibly because of a positive 
effect on physiological rates. Queens are black in 
A. alfari , which dominates Cecropia of roadsides 
and pastures in many disturbed regions, and yel- 
lowish brown in A. ovaticeps , the typical resident of 
fast-growing riverine Cecropia (Longino 1989b). 
Occurring mainly on Cecropia of small forest light 
gaps, A. australis has yellow queens, and may have 
comparatively slow rates of egg-laying (Davidson 
et al. 1991). Similarly in Leonardoxa , black-bod- 
ied queens (and workers) of Aphomomynnex tend 
to occur in more exposed riverine situations, whereas 
reddish yellow Petalomyrmex are typical of more 
shaded forest understory. 


Within myrmecophyte species, host size-de- 
pendent variation in the relative abundances of 
alternative plant-ants may be determined in some 
cases by the match between colony resource de- 
mands and rates of resource provisioning by the 
plants. However, other causal mechanisms might 
also produce correlations between plant sizes and 
the identities of ant inhabitants. For example, such 
correlations could occur if ant species differed in 
the capacity to protect their hosts from herbivory 
(suggested by Longino 1991a and b, for Central 
American Azteca on Cecropia). Additionally, a 
form of ecological succession may take place, with 
regular changes in ant inhabitants through indi- 
vidual plant lifespans. Turnover of ant species 



42 


Journal of Hymenoptera Research 


through time has been observed on hosts in the 
genera Acacia (Janzen 1 975), Leonardoxa (McKey 
1984), Taclngcili (Benson 1985), and Maieta 
(Vasconcelos 1990). Just as successional mecha- 
nisms may vary across plant communities (Connell 
and Slatyer 1977), they may also vary across ant- 
plant systems. One possible explanation for spe- 
cies replacements is that early colonists are eventu- 
ally replaced by superior competitors (Janzen 1 975, 
McKey 1984, Davidson et al. 1989). In this 
context, coexistence of multiple ant species on a 
single host population requires that competitive 
abilities be inversely proportional to colonizing 
abilities, with poor competitors making a living as 
“fugitive species”. 

Even in the absence of direct interspecific inter- 
actions, disparate ant life histories might lead to 
successional changes among the ants of individual 
hosts. On Central American Acacia, for example, 
Pseudomyrmex nigropilosa Emery is an opportu- 
nistic colonist and short-term resident after prior 
residents have died from fire and other causes 
(Janzen 1975). A similar mechanism has been 
proposed by Vasconcelos ( 1 990) to account for the 
coexistence of Pheidole winutula Mayr and 
Crematogaster sp. on Maieta guianensis Aublet 
near Manaus, Brazil . Although the two ant species 
provide equivalent protection for their hosts, the 
frequency of Pheidole occupancy increases with 
plant size. Comparatively early death or desertion 
of hosts by Crematogaster (for unknown reasons) 
leaves plants to be colonized again. Whatever the 
average relationship between the colonizing abili- 
ties of the two ants, larger plants should eventually 
accumulate Pheidole colonies, due to the frequent 
abandonment of hosts by Crematogaster. 

To summarize, both the species composition of 
ant-plant symbioses, and the fitness consequences 
of particular associations, can vary markedly in 
space and time. Just as such inconsistencies are 
postulated to have limited evolutionary specializa- 
tion in non-symbiotic ant-plant relationships 
(Schemske 1983, Beattie 1985), they have likely 
been the predominant obstacles to the evolution of 
species-specificity in symbiotic associations. 


Evolutionary Dynamics of Ant-plant Symbiosis 

Given these limitations to species specificity, 
what are the implications for coevolution? Coevo- 
lution has two aspects. The first is co-accommoda- 
tion, reciprocal evolutionary responses of interact- 
ing organisms (Mitter and Brooks 1983). Co- 
accommodation is most easily recognized when it 
involves functionally matched characters of associ- 
ated organisms or coupled character coevolution 
(Schemske 1983). Several ant-plant systems in 
both Africa and South America offer examples 
suggestive of reciprocal specialization of function- 
ally matched characters in plants and associated 
ants. In this category are matches between the 
dimensions of ants and the prostomas of their plant 
associates (McKey 1991, Davidson and Fisher 
1991), and between food provisioning by plants 
and the foraging and pruning behaviors of their ants 
(Davidson et al. 1988). Though suggestive, the 
data are not usually sufficient to pass arigorous test, 
especially in view of our poor knowledge of phylo- 
genetic relationships (McKey 1991). 

The second aspect of coevolution is association 
by descent (Mitter and Brooks 1983). If ant-plant 
relationships have persisted and diversified as the 
associated lineages underwent successive specia- 
tional events, their phylogenies should be congru- 
ent. If, on the other hand, events such as host- 
switching and secondary exploitation of preexist- 
ing ant-plant mutualisms are frequent, there will be 
no close correspondence between ant and plant 
phylogenies. Interspecific hybridization of plants 
and/or ants will produce yet a third pattern, reticu- 
late evolution. Janzen (1974a) concludes (without 
rigorous phylogenetic analysis) that the neotropical 
ant-acacias do not form a tight phyletic group, and 
postulates that one species may capture ant-adapted 
traits from another via introgression. Ross (1981) 
came to similar conclusions regarding African ant- 
acacias. Aside from the two groups of Acacia, there 
is little information to evaluate the possible role of 
hybridization in the diversification of ant-plants. 
Moreover, Janzen’s observations might beexplained 
alternatively by genotype-environment interactions. 
Thus, evolved associations of ants with one acacia 
lineage could have increased the selection intensity 
for myrmecophytism in other (possibly preadapted) 


Volume 2, Number 1, 1993 


43 


lineages, perhaps because ants occasionally colo- 
nized these unspecialized hosts. 

Of the relatively small number of taxa which 
have produced modest to extensive radiations of 
ant-plants or plant-ants, taxonomic uncertainty pre- 
cludes any examination of the question of associa- 
tion by descent in all but a few cases. And in no case 
do we have equally robust phylogenies in both ants 
and plants. By far the best example is Ward’s 
(1991) study of associations between plants and 
pseudomyrmecine ants, represented by Pseudo- 
myrmex and Myrcidris (Ward 1990) in the 
Neotropics, and by Tetraponera in Africa, Asia and 
Australasia. Specialist plant-ants appear to have 
arisen at least 1 2 times in this sub-family, on a wide 
range of hosts. Most of these events have produced 
only one or a few species of plant-ants, associated 
with a comparably small number of host species. 
Such small radiations offer limited opportunity for 
association by descent. In some cases, apparently 
secondary pseudomyrmecine colonizations of pre- 
existing ant-plant mutualisms have given rise to a 
small number of species on Cordia, Pleurothyrium 
and possibly Cecropia (Ward 1991), all of which 
are predominantly associated with other ants 
( Allomerus , Mynnelachista and Azteca, respec- 
tively). 

The hosts of pseudomyrmecines do include, 
however, three plant genera with large numbers of 
ant-plant species. Each of these (neotropical Aca- 
cia, Tachigali, and Triplaris) is associated with a 
different monophyletic group of Pseudomyrmex. 
Do these more extensive radiations offer evidence 
of association by descent? Ward (1991) concludes 
that at the species level, they do not. First, within 
each of these groups there is no pairwise specificity 
of ant and plant species. Not surprisingly, there is 
no clear pattern of cospeciation. Although in each 
of these three cases, the plant lineage seems to have 
evolved in concert with the ant lineage, the pattern 
of associations suggests host shifts within a taxo- 
nomically restricted guild of ants and plants, rather 
than cospeciation. Furthermore, each of these plant 
groups also harbors ants from at least one other 
lineage of Pseudomyrmex. Even in these extensive 
radiations from associated ancestors, coevolution 
seems to have been diffuse, corresponding to the 
guild coevolution or ecological replacement hy- 


potheses (Howe and Westley 1988), rather than to 
a hypothesis of pairwise coevolution. 

Relationships of various plant-ants to neotropical 
Cecropia paint a somewhat similar picture. Within 
ponerines of the genus Pachycondyla , four prob- 
able Cecropia specialists represent at least three 
separate origins of specialization on this host ge- 
nus. Independent origins include species near both 
P. villosa (Fabricius) and P. unidentata Mayr (J. 
Longino, personal communication) as well as 
Pachycondyla sp. nov. in Panama. Of these, the 
first two species appear to be stem parasites. Their 
small, secretive colonies show little activity on host 
surfaces, though workers of at least the species near 
P. villosa harvest Mullerian bodies and locate en- 
trances at prostomas ( J. Longino, personal commu- 
nication). At present, no data suggest specificity of 
host range within the genus Cecropia. In contrast, 
Pachycondyla sp. nov. appears to have a highly 
specialized relationship with C. hispidissima , which 
produces especially large, hard and purple Mullerian 
bodies (Davidson and Fisher 1991 , B. Fisher, per- 
sonal communication). A close phylogenetic rela- 
tionship between this ant and the Peruvian P. luteola 
cannot yet be ruled out (W. L. Brown, personal 
communication). Colonies of the latter ant occur 
only on C. (prov.) “ tessmannii' , whose relation- 
ship to C. hispidissima is currently uncharacterized. 
The affiliations of Pachycondyla sp. nov. and P. 
luteola with their respective hosts are the most 
likely candidates for pairwise coevolution between 
ants and Cecropia trees, and the evidence is still 
weak. Even if ant and plant phylogenies turn out to 
be congruent here, and if speciation events are 
determined to have been synchronous in ant and 
plant lineages, any postulated cospeciation would 
appear to have been minimal, based on the small 
number of Pachycondyla specialized to Cecropia. 

Three other ant genera provide support for mul- 
tiple independent colonizations of Cecropia. The 
genus Camponotus includes at least two host gen- 
eralists, C. balzani Emery in southeastern Peru, and 
an unnamed species of Camponotus sub-genus 
Pseudocolobopsis in northern Peru( Davidson, un- 
published; R. Snelling, personal communication). 
Multiple radiations of specialized A zteca (Longino 
1989b, 1991a and b) were mentioned above. Al- 
though phylogenies are not yet defined within ei- 


44 


Journal of Hymenoptera Research 


ther ant genus, the overlapping and generalized 
host ranges of closely related ant species argue 
against cospeciation as the major mechanism by 
which diversity is generated. Finally, at least one 
Crematogaster species (near C. cun’ispinosa Mayr, 
J. Longino, personal communication) appears to be 
a specialist on Cecropia in northeastern Peru (vie. 
Genaro Herrera), but inhabits at least several differ- 
ent hosts within the genus (D. Davidson, personal 
observation). With specialized symbionts repre- 
senting four of the five sub-families of plant-ants, 
and multiple origins within at least three ant genera, 
Cecropia presents a strong case for the ease with 
which taxa of generalized stem-nesting ants have 
colonized myrmecophytes over evolutionary time. 

Like Pseudomynnex and Tetraponera, many 
other plant-ant genera are associated with numer- 
ous, unrelated plant hosts (Appendix 1). Of 31 
plant-ant genera (including various subgenera of 
Camponotus ), only 1 1 are known from a single host 
genus, and three of these are records for species 
whose specialization as plant-ants (column 7) re- 
mains in doubt. As in pseudomyrmecines, these 
broad generic host ranges are probably due both to 
multiple independent origins of the plant-ant habit 
within the ant genus, and to secondary colonization 
of additional hosts by plant-ant species. However, 
the taxonomic information necessary to distinguish 
between these possibilities is lacking. Allomems is 
a particularly intriguing case. All known species 
are specialist plant-ants. Unless we assume that 
non-specialist Allomerus once existed but are now 
all extinct (the genus has no fossil record [Holldobler 
and Wilson 1 990] ), then the host range of this genus 
(seven plant genera in five families) is due to 
secondary colonizations and host shifts. 

Perhaps the clearest evidence against 
cospeciation is offered by those cases in which a 
prerequisite for cospeciation, host-specificity, is 
not fulfilled. Several plant-ant species are associ- 
ated with two or more quite unrelated hosts. At 
least three specialist plant-ant species of 
Pseudomynnex occupy more than one plant genus 
(Ward 1991), with P. vidiius F. Smith recorded 
from 5 genera in as many families. Aphomomynnex 
afer Emery is associated with Vitex (Verbenaceae) 
and Leonardoxa (Fabaceae) (R. Snclling, personal 
communication). Technomyrmex (formerly 


Engramma) kohlii is associated with five genera 
(Cola, Scaphopetalum, Cantliimn, Diospyros and 
Delpydora ) belonging to four families (Bequaert 
1 922; R. Snelling, personal communication). These 
appear to be cases in which secondary colonization 
of ant-plants has occurred several times. 

At least one other case, however, does suggest 
association by descent. African Leonardoxa in- 
cludes two myrmecophytes, which cladistic analy- 
sis has shown to be sister species (McKey 1991). 
They are inhabited by Aphomomynnex afer and 
Petalomynnex phylax Snelling, respectively, the 
only two African representatives of the formicine 
tribe Myrmelachistini. Though these two ants are 
obviously closely related (Agosti 1991), further 
taxonomic work will be required to determine 
whether they are sister species or relicts of formerly 
diverse genera in which all congeners have gone 
extinct. 

Habitat Specialization and the Generation of 
Diversity in Ant-plant Synibioses 

Our analysis indicates that cospeciation in lin- 
eages of plants and of host-specific ants has been 
infrequent at best. Ant-plant pairs may be co- 
evolved, but associations seem to be shuffled or 
broken frequently, rather than diversified in con- 
cert via cospeciation. Pairwise coevolution thus 
can account for little of the diversification of these 
symbioses. How then have symbiotic ant-plant 
associations diversified? Mounting evidence sug- 
gests that evolutionary interactions in these sys- 
tems, in both Africa and the Neotropics, correspond 
more closely to two other models of coevolution, 
not mutually exclusive, the guild coevolution hy- 
pothesis and the ecological replacement hypothesis 
(Howe and Westley 1988). These hypotheses en- 
visage diffuse evolutionary interactions among 
sympatric guilds of associated organisms. Specia- 
tion may be accompanied by shifts in patterns of 
host associations, producing new mixes and 
matches. In these guilds, one member may replace 
another as the predominant associate of a particular 
member of the other guild. Guilds are also open. 
New ants may colonize pre-existing ant-plant 
mutualisms, perhaps displacing or completely re- 


Volume 2 , Number 1 , 1993 


45 


placing other ants, and new plants may join a guild 
of ant-plants. 

We postulate that habitat-dependence in the 
outcome of different ant-plant interactions has been 
the principal force driving host shifts and ecologi- 
cal replacements within these guilds. Thus, the 
main obstacle to species-specificity and pairwise 
coevolution of ants and plants has at the same time 
facilitated diversification by other mechanisms. 

Host plant quality, as recognized by ants, may 
vary more with habitat than with host species. Thus, 
Janzen (1966) has called attention to disparities in 
the habitat associations of P. nigrocinctus (Emery) 
and P. spinicola Emery (= P. ferruginea), though 
the two closely related (Ward 1991) species coexist 
locally. In some parts of their ranges, these two 
species also coexist with P.flavicornis F. Smith (= 
P. belti), which has yet a different pattern of habitat 
association (Janzen 1983). In another example, 
distributions of obligate Cecropia ants, both within 
and across genera, are usually more responsive to 
habitats than to host species (Harada and Benson 
1 988, Longino 1 989b, 1991a and b, Davidson et al. 
1991). As is the case for acacia-ants, the conse- 
quent mixing and matching of ants and Cecropia 
species may favor diffuse rather than pairwise 
coevolution. Likewise, effects of different ants on 
plant fitness may vary with habitat, for example, if 
the quality of defense against herbivores mattered 
less under favorable than unfavorable resource 
regimes. 

Thus, genetic differentiation may be associated 
more frequently with habitat specialization, both in 
plants (Davidson and Fisher 1991 ) and in ants, than 
with specific identities of associates. However, 
habitat-dependence may still drive a type of 
cospeciation. For example, a plant and an associ- 
ated ant may have parallel genetic responses to 
environmental variation, both of them diverging 
from conspecifics in a different habitat. Or, genetic 
differentiation in one symbiont, driven by habitat 
specialization, may induce divergence in its associ- 
ate (Thompson 1987). The likelihood of such 
events, in which both ant and plant remain associ- 
ated while undergoing habitat-related divergence, 
may depend on guild diversity. Thus, when an ant- 
plant colonizes a novel environment, poor success 
of the usual ant associate certainly provides selec- 


tive pressure for adaptation of the ant to the new 
habitat. But it also provides opportunities for the 
establishment of other ant species. The richer the 
local guild of plant-ants, the greater the likelihood 
that a member of the guild will establish success- 
fully, replacing the usual associate and preventing 
its specialization for the novel habitat. In depauper- 
ate guilds, preadapted ants are fewer, and the usual 
associate may be more likely to persist and adapt to 
the novel environment. A possible example is the 
relationship between Leonardoxa spp. and their 
Petalomynnex and Aphomomyrmex ants. Plausi- 
bly a case of cospeciation, this system involves a 
small number of ant and plant species (McKey 
1991 ). Neither the two plants nor the two ants ever 
occur sympatrically , and few other myrmecophytes 
and domatia-inhabiting ants share their habitats. 
Perhaps pairwise specificity and cospeciation are 
more likely to occur in modest and geographically 
limited radiations such as these, where taxonomic 
poverty of sympatric guilds of ant-plants and plant- 
ants offers little scope for host-switching and sec- 
ondary colonization. The latter processes may 
dominate in species-rich guilds. If our hypothesis 
is correct, it would suggest that diversity begets 
diversity due to genotype-environment interactions 
in tropical ant-plant symbioses. 

EVOLUTIONARY TRENDS IN SPECIES 
REPLACEMENTS WITHIN PLANT-ANT GUILDS 

Host-switching, secondary colonization, and eco- 
logical replacement seem to be the predominant 
modes by which ant-plant associations are modi- 
fied. Once a new association is forged, it is likely 
to engender selection on one or both partners, and 
to give rise to evolutionary diversification. But 
how do new associations form and spread? What is 
their effect on preexisting associations? Can we 
recognize patterns in the radiation of plant-ants and 
ant-plants? Once again, it may be possible to 
understand the evolutionary dynamics of ant-plant 
associations in the context of competitive interac- 
tions among ants, and habitat-dependence in the 
outcome of ant-ant and ant-plant interactions. While 
many species replacements may have occurred 
without perceptible trace, contemporary systems in 
which ant-plants are associated with multiple unre- 


46 


Journal of Hymenoptera Research 


Table 2. Earliest fossil records of ants for genera (worldwide) in which specialized plant-ants 
have evolved (summary excerpted from Holldobler and Wilson 1990): A = Arkansas amber 
(USA, middle Eocene); Ba = Baltic amber (northern Europe, early Oligocene); Br = Britain 
(Oligocene); Do = Dominican amber (Dominican Republic, late Miocene 3 ); F = Florissant 
shales, Colorado, USA, Oligocene); Sh = Shanwang shales (China, Miocene); Si = Sicilian 
amber (Sicily, Miocene). 


Sub-family and tribe 

Genus 

Earliest fossil find 

PONER1NAE 

Tribe Ponerini 

Pacliycondyla 

Early 01igocene Ba ' r- 

PSEUDOMYRMEC1NAE 

Mwcidris 

No fossil record 


Pseudomyrmex 

01igocene DF 


Tetraponera 

Early Oligocene 63 

MYRMICINAE 

Tribe Cephalotini 

Zacryptocems 

Late Miocene 0 

Tribe Crematogastrini 

Crenuitogaster 

Miocene Sl 

Tribe Leptothoracini 

Leptothorax 

Early 01igocene Ba 

Tribe Pheidolini 

Pheidole 

01igocene D ' F 

Tribe Solenopsidini 

Allomenis 

No fossil record 


Solenopsis 

Late Miocene 0 

Tribe Tetramoriini 

Tetramorinm 

No fossil record 

Tribe Dacetini 

Stmmigenys 

No fossil record 

Tribe unclassified 

Cataidacus 

Miocene Sl 


Podomyrma 

No fossil record 


Atopomyrmex 

No fossil record 

DOL1CHODER1NAE 

Tribe Tapinomini 

Anonychomyrma 

No fossil record 


Axinidris 

No fossil record 


Azteca 

Early Miocene 0 


Tapinoma 

Miocene Sl 


Technomyrmex 

Miocene Sl 

FORMIC1NAE 


Early Ohgocene Ba ’ Si 

Tribe Plagiolepidini 

Plagiolepis 

Tribe Myrmelachistini 

Aphomomyrmex 

No fossil record 


Ctadomynna 

No fossil record 


Myrmelac/iista 

No fossil record 


Petalomyrmex 

No fossil record 

Tribe Camponotini 

Camponotus 

Early Oligocene 8 J,Sl 


a 

Note added in proof. Although Holldobbler and Wilson (1991) date the Baltic amber as late Oligocene, 
more recent work summarized by Kirsshna and Grimaldi ( 1991 ) suggests an earlier estimate. We use 
the latter date because it is conservative in relation to our hypothesis. 


Volume 2, Number 1, 1993 


47 


lated plant-ants may offer examples of species 
replacements in progress. The various ant associ- 
ates of myrmecophytes usually occupy different 
places in a competitive hierarchy. An understand- 
ing of their competitive relationships, and how they 
coexist today, should provide insights into the 
ecological mechanisms that have driven their evo- 
lutionary histories. 

Without more phylogenetic evidence than exists 
today, we have only a snapshot of a process in 
motion, and cannot know its direction with cer- 
tainty. Nevertheless, we attempt a provisional 
distinction between original associates and second- 
ary colonists of several ant-plant associations. First, 
we focus on two ant lineages which seem to have 
played predictable and frequent roles in the eco- 
logical replacement of primary associates. We then 
examine likely causes of such pattern, based on 
what is known of the biology and competitive 
relationships of the ants involved. Generalizing 
from these examples, and referencing the fossil 
record, we propose a hypothesis of taxonomic 
progressions within lineages of plant-ants. This 
hypothesis, combined with information on the geo- 
logical history of mesic-forest environments in 
different tropical regions, leads to new interpreta- 
tions of intercontinental differences among ant- 
plant symbioses. 

Directionality of Species Replacements 

The primary and secondary associates of many 
myrmecophytes can be very difficult to distinguish 
(Ward 1991 ). Nevertheless, patterns in the biogeo- 
graphic and taxonomic distribution of host associa- 
tions in some ant-plant systems suggest that 
myrmecophytes have been colonized recently by 
unspecialized arboreal ants or by host-shifting plant- 
ants, resulting in partial or complete replacement of 
a prior ant associate. In none of the examples that 
follow is the evidence for directionality conclusive. 
Nevertheless, taken together the evidence is strongly 
suggestive, and the approach has enabled us to 
propose testable hypotheses and to define critical 
points where data required to test these hypotheses 
are lacking. 

Crematogaster as Secondary Associates of 
Myrmecophytes. — Several ant-plant relationships 


provide indications that ants of the genus 
Crematogaster have partially or completely re- 
placed prior ant associates of the host plant. First, 
the pattern of ant associations with the two African 
Barteria species suggests that ancestral host rela- 
tionships may have involved Tetraponera ants. For 
T. aethiops (F. Smith) and T. latifrons (Emery), two 
host-specific associates of B.fistulosa Mast. (Janzen 
1972), taxonomic isolation from other sections of 
the genus suggests comparatively ancient origins 
for the association (P. Ward, personal communica- 
tion). Tetraponera has not been found to inhabit the 
other described species of Barteria , B. nigritana 
Hook, f., which instead houses an apparently 
unspecialized Crematogaster. The latter associa- 
tion may have arisen via secondary colonization of 
hosts in the more disturbed, light-rich, coastal scrub 
sites frequented by this plant species. Interestingly, 
while B. fistulosa is occupied by its specialist 
Tetraponera in forest light gaps, it too occurs with 
unspecialized Crematogaster in large, human-made 
clearings in coastal forests of Cameroon (D. McKey, 
personal observation). 

Second, although Crematogaster spp. are pres- 
ently the numerically dominant associates of East 
African ant-acacias, Tetraponera ants may have 
been the original inhabitants. Invasion of East 
African acacias by Crematogaster , which gener- 
ated two new specialists on Acacia , may have 
largely pushed the weakly competitive 
pseudomyrmecine into marginal high-elevation sites 
(Hocking 1970). At lower elevations (ca. 900 m), T. 
penzigi (Mayr) appears to be competitively subor- 
dinate to Crematogaster mimosae (Santschi) and 
C. uigriceps Emery, and has exclusive possession 
of only 0.7 % of the trees. At higher elevations, it 
maintains control of up to 8.5 % of host trees. In 
sites where it cooccurs with the two Crematogaster , 
the pseudomyrmecine appears to persist mainly in 
unoccupied parts of Crematogaster-occupied trees. 
There it ensures exclusive occupancy of stipular 
swellings by boring entrance holes too small to 
accomodate Crematogaster, and by plugging or 
protecting these entrances with carton baffles. 

Asian Macaranga may be another case where 
contemporary numerically dominant Crew wrogfl.ster 
ants have largely replaced the original inhabitants. 
Poorly known associations occur between two 


48 


Journal of Hymenoptera Research 


Camponotus species [provisionally subgenus 
Colobopsis ] and both Macciranga griffithiana M. A. 
and Macarcinga puncticulata Gage (Fiala et al. 
1990). Each of these hosts grows principally in 
swamplands (Whitmore 1973 and 1975), marginal 
habitats where rates of plant growth and supply of 
ant resources are likely to be reduced. Finally, one 
Crematogaster lineage may also have replaced 
another. Thus, Macarcmgci hosts in some undis- 
turbed primary forests are occupied by a species 
with black workers and 11 -segmented antennae, 
whereas hosts of forest and riverine edge typically 
contain any of an unrelated complex of species with 
yellowish workers and 10-merous antennae (D. 
Davidson, personal observation). Despite habitat 
segregation under natural conditions, a mixture of 
the two ant lineages occurs in the extensive 
Macarcmgci forests left after logging. Clearly, in 
view of the habitat specificity of both 
myrmecophytes and their ants, the rapid conver- 
sion of primary forests can be expected to alter 
these symbiotic associations greatly in future years. 

In the Neotropics, unspecialized Crematogaster 
are recorded as clear newcomers and secondary 
associates of several older ant-plant relationships, 
including those between Pseudomyrmex and 
Triplaris (Davidson et al. 1988; Oliveira 1987), 
Pseudomyrmex and Acacia (Janzen 1983), and 
Azteca and Zacryptocerus with Cordia alliodora 
(R. Carroll, personal communication). These Neo- 
tropical examples include no obvious case in which 
colonization by Crematogaster has led to complete 
replacement of a prior associate, and American 
Crematogaster have only rarely evolved into spe- 
cialist plant-ants. Included in the latter category are 
only the Crematogaster cf. victima of many 
neotropical leaf-pouch myrmecophytes, and a de- 
rivative of the opportunistic and widespread C. 
curvispinosa on Cecropia in northeastern Peru (D. 
Davidson, personal observation). 

Azteca as Secondary’ Associates of Neotropical 
Myrmecophytes. — In species richness, Azteca are 
the preeminent competitive dominants among New 
World plant-ants (Appendix 1 ), and play ecological 
roles analogous to those of Crematogaster in many 
Old-World systems (Carroll 1983). Like 
Crematogaster, they may be displacing subordi- 
nate species in many relationships. For example. 


both Crematogaster and Azteca ants displaced 
Pseudomyrmex deudroicus when permanent wire 
bridges were made between the host trees and 
neighboring vegetation (Davidson et al. 1988). 
Moreover, as we also suspect for Old-World 
Crematogaster , some displacements of primary 
associates by Azteca may have been so thorough 
that distinguishing contemporary from prior asso- 
ciations is fraught with uncertainty. For example, 
ants of the genus Azteca are the numerically pre- 
dominant associates of myrmecophytic Cecropia 
today, but associations of Cecropia with other ants, 
such as Camponotus and Pachycondyla, may be 
older. Each of these latter genera includes species 
which are Cecropia specialists, and in both cases 
ongoing competition with Azteca may exclude them 
from riverine and other riparian habitats, where 
Cecropia is most abundant and fast-growing (see 
above, Davidson and Fisher 1991). 

Replacements may also be occurring within the 
genus Azteca. In Amazonian Peru, Azteca ovaticeps 
and its relative, A. alfari appear to be relative 
newcomers, dominating contemporary Cecropia 
populations along riverine and forest edge. The 
two species are closely allied to ants of other early 
successional ant plants (Longino 1991b). These 
ants include A. foreli Emery, which inhabits live 
stems of a variety of rainforest trees, and A. longiceps 
Forel, from mid-elevation Triplaris of the Costa 
Rican Pacific coast. Still other representatives of 
this species-group occur on Cordia alliodora. Thus, 
A. ovaticeps and A. alfari may have originated 
during a comparatively recent host switch onto 
Cecropia. In support of this conjecture are rare 
observations of apparent mistakes in colony found- 
ing behavior. Queens of A. ovaticeps occasionally 
attempt to enter Cecropia membrauacea by bur- 
rowing into the trichilia, rather than into prostomas, 
even though suitable prostomas are available in 
uncolonized intemodes (D. Davidson, personal ob- 
servation). The arrival of A. ovaticeps may have 
driven A. australis out of riverine environments and 
deeper into the forest, where it persists on a variety 
of forest light-gap Cecropia species (see above; 
Davidson and Fisher 1991). 

Azteca australis could itself be a secondary 
colonist. A member of the A. muelleri species 
complex, it is likely descended from generalized 


Volume 2 , Number 1 , 1993 


carton-building ancestors with well-defended cen- 
tral nest sites (Longino 1991a and b). Members of 
this group still maintain carton masses inside the 
boles of their hosts (Longino 1991a). Ants in this 
species complex may have gotten their first foot- 
hold on myrmecophytic Cecropici by building 
external carton nests on hosts whose prior residents 
(possibly Camponotus and Pcichycondyla species) 
had died. 

Analogously and in contemporary times, Azteca 
may be invading other myrmecophytic associa- 
tions. In the Manu National Park and Tambopata 
Reserve of southeastern Peru, at least two carton- 
building species (probably A. ulei Forel var. cordiae 
Forel and A. traili [Emery] var. tococae Forel) are 
residents of trichome myrmecophytes Cordia 
nodosa and Tococa spp. (Appendix 1 ). Queens of 
both ants initiate their colonies inside domatia 
covered by protective hairs, and their incipient 
colonies exhibit host-plant fidelity. Nevertheless, 
larger, established colonies not only leave their 
hosts regularly to forage, but build satellite nests 
(often as ant-gardens) on neighboring trees. These 
ants also prune trail systems through the protective 
stem trichomes. On Cordia, Azteca ants occur 
mainly on hosts in environments of unusually high 
light intensity, and conspecific trees in the primary 
forest understory are occupied by Allomerus. If we 
are correct in assuming that plants with long, dense 
and erect pubescence became myrmecophytes in 
the context of persistent occupation by tiny and 
competitively subordinate ants, then larger-bodied, 
aggressive and dominant Azteca appear to have 
both restricted the distribution of Allomerus, and 
perhaps eliminated the former residents of Tococa. 
Although Tococa is colonized occasionally by timid 
Crematogaster cf. victima and a species of 
Solenopsis, we have never found established colo- 
nies of these ants on the Tococa of southeastern 
Peru. 

Identifying and Characterizing Dominants 

Crematogaster and Azteca are the two genera 
for which biogeographical and phylogenetic infor- 
mation is most suggestive of a frequent role as 
secondary colonists in species replacements among 
plant-ant guilds. They are also the preeminent 


competitive dominants in the arboreal ant faunas of 
Africa and Asia, and New World tropics, respec- 
tively. Isolated from these continents, the Austra- 
lian tropics (including New Guinea and associated 
islands) contains a unique set of competitive domi- 
nants and relative newcomers to ant-plant symbio- 
ses. Among these ants (all dolichoderines) are two 
genera previously classified as Iridomyrmex 
(Shattuck 1 992b), but now considered to be distinct 
taxa and endemics of either the Australian 
(Anonychomynna) or Oriental and Australian re- 
gions (Philidris). Also included are pantropical 
Technomynnex (a single species of which is appar- 
ently native to the New World, Shattuck, 1992a). 

Several other kinds of evidence substantiate the 
inferential evidence about the relative competitive 
abilities of ants involved in ant-plant symbioses. 
Field experiments have demonstrated that 
Crematogaster and Azteca are the principal formicid 
enemies of New World Pseudomyrmex on Triplaris 
(Davidson et al. 1988, see also Oliveira 1987). 
Furthermore, both host-plant fidelity and pruning 
of host-plant neighbors are indicative of weak com- 
petitive ability (Davidson et al. 1988, 1989) and 
occur with some frequency in Pseudomyrmex, 
Tetraponera, Pheidole, Camponotus, and in vari- 
ous myrmelachistines. In contrast, these behaviors 
are atypical of Crematogaster, Anonychomynna, 
Azteca, and Technomynnex (Appendix 1, column 
4). Rare occurrences are limited to early succes- 
sional environments where vines and competitors 
are particularly threatening, as for the Azteca of 
New World Cecropia, and Crematogaster of Asian 
Macaranga. They can also characterize ants which 
are unusually timid for their genera, as are the 
Azteca exhibiting host-plant fidelity on pubescent 
species of Triplaris. 

Implicit in their capacity to invade 
myrmecophytes previously dominated by other ants, 
secondary colonists likely owe their success to 
evolutionary novelties which have enhanced their 
colonizing and/or competitive abilities. The genera 
listed above as competitive dominants are alike in 
possessing potent exocrine products which help to 
convey competitive superiority in interactions with 
other ants (Blum and Hermann 1978, Buschinger 
andMaschwitz 1984). Structural characteristics of 
waists and gasters permit workers to elevate gasters 


50 


Journal of Hymenoptera Research 


and direct toxins toward enemy ants. The same 
adaptations can be effective against potential nest 
raiders, as when Crematogcister workers seal hol- 
low stem nests with protruding gasters bearing 
poison droplets on modified spatulate stings (Forel 
1928). Many dominants are also carton-builders, 
which monopolize resources in the arboreal zone 
by constructing primary or ancillary nests over 
Homoptera and other localized food sources such 
as extrafloral nectaries. 

These traits contribute to the capacity of domi- 
nant ants to monopolize “promiscuous” plant re- 
wards such as EFN’s and surface-feeding 
Homoptera, which are either totally unprotected or 
only partly secluded beneath clasping or folded 
stipules of myrmecophiles. Thus in Borneo, 
Crematogcister species dominate the exposed EFN’s 
of most individuals of myrmecophilic 
Endospermum (Euphorbiaceae), Ryparosa 
(Flacourtiaceae), andMacciranga aetheadenia Airy 
Shaw (D. Davidson, personal observation). 
Crematogaster are also preeminent among visitors 
to other myrmecophilic Malaysian Macarangaspp. 
(Fiala and Maschwitz 1991). In New Guinea, 
scale-tending Crematogaster are the numerically 
predominant inhabitants of the stout hollow stems 
of weedy Nauclea (D. Davidson, personal observa- 
tion). Myrmecophiles with nectaries partly se- 
cluded beneath folded or clasping stipules include 
New Guinea A rchidendron (Fabaceae) and Orien- 
tal Shorea (Dipterocarpaceae), both often domi- 
nated by Technomyrme.x ants (D. Davidson, per- 
sonal observation, Tho, fide Maschwitz and Fiala, 
in press). By sealing off the folded stipules with 
carton, these ants may restrict their competitors’ 
access to EFN. An ability to monopolize externally 
located food resources may also confer a competi- 
tive advantage to dominants on myrmecophytes 
which produce such resources. This result would 
be especially likely if evolutionary interactions of 
the plants with prior ant associates had led to 
increased size and/or number of EFN’s and food 
bodies, or otherwise increased the rate of food 
production to a level at which the plant becomes 
attractive to competitive dominants requiring high 
rates of resource supply. 


Processes of Species Replacements 

How have secondary colonists managed to re- 
place primary associates with highly evolved mecha- 
nisms for locating and exploiting hosts? Even very 
aggressive and dominant ants may have difficulty 
evicting weakly competitive ants, once the latter 
have established their colonies. Thus it seems 
likely that many secondary colonists first achieved 
access to myrmecophytes by occupying hosts whose 
usual partners were absent for one reason or an- 
other. For example, like the Azteca discussed 
above, some Crematogaster could have gained a 
preliminary foothold on myrmecophytes by build- 
ing carton nests on plants which had outlived their 
ant colonies. Early stages of this scenario may be 
represented in the New World associations of 
Crematogaster with myrmecophytic acacia spe- 
cies in second growth environments ( Janzen 1 983). 
Although Crematogaster are apparently unable to 
replace Pseudomyrmex on smaller acacias, they 
can resist colonization by the latter species on 
larger acacias which have lost their former 
Pseudomyrmex colonies. 

The more characteristic ant associates may be 
absent for other reasons. First, by opening domatia 
to feed on ant larvae, vertebrate predators of ants 
may make these domatia unsuitable for continued 
habitation by weakly competitive species. For 
example, after swollen internodes of Cordia 
alliodora are opened by woodpeckers, unspecialized 
Crematogaster often move in and employ carton 
baffles to seal breaks in the domatia (R. Carroll, 
personal communication). Second, older domatia 
are frequently abandoned by the usual residents, as 
colonies move to follow new growth and produc- 
tivity. In Cecropia (Davidson et al. \99\),Remijia 
(Benson 1985), Leonardoxa (D. McKey, personal 
observation ), Endospermum, Korthalsia, and other 
genera (D. Davidson, unpublished), such aban- 
doned domatia are often occupied by unspecialized 
ants, which gain at least protected nest sites if not 
food (Davidson and Fisher 1991, Longino 1991a). 
A possible case of progressive specialization in 
such ants may be seen in the unnamed 
Crematogaster species which occupies Cecropia 
near Genaro Herrera in Loreto, Peru (D. Davidson, 
personal observation). Related to C. curvispinosa 


Volume 2, Number 1, 1993 


51 


(J. Longino, personal communication), it is appar- 
ently descended from generalized stem-nesters, 
rather than from a carton-building lineage. Special- 
ization on Cecropia could have been favored by 
selection sharpening the host-finding abilities of 
foundresses which occasionally colonized the 
woody bases of forest-gap plants, and eventually 
evolved to recognize Mullerian bodies as food. 

Third, the typical ant associates may fail to 
either colonize or to persist on hosts in inappropri- 
ate habitats. Small forest light gaps are marginal for 
western Amazonian Cecropia , and comparatively 
low colonization rates on isolated and inconspicu- 
ous gap plants appear to have provided safety for 
refugees from riverbanks, as well as opportunities 
for in situ colonization of this host genus. All four 
little-known genera of Cecropia ants persist princi- 
pally in forest light gaps. Both Camponotns balzani 
and Pacltycondyla luteola colonize riverine plants, 
but rarely persist there, being excluded by Azteca. 
In contrast, species of Crematogaster and 
Camponotns ( Pseudocolobopsis ) occur on several 
light gap species at Genaro Herrera, but apparently 
do not even colonize plants of riverine and forest 
edge. Their relationships with Cecropia may have 
evolved in situ. Alternatively, past competition 
with Azteca may have led to a shift in their habitat 
preferences. 

Finally, colonists may also gain a foothold at the 
latitudinal or elevational limits of ant-plant asso- 
ciations. Latitudinally, the genus Triplaris ranges 
northward into Mexico; in southwestern Chiapas 
near Mapastepec, it is occupied by a variety of 
apparently unspecialized species of Azteca , 
Crematogaster and Pseudomyrmex , rather than by 
the more typical specialized pseudomyrmecine as- 
sociates (D. Davidson, personal observation). At 
least one specialized Cecropia ant, dry forest A. 
coentleipennis Emery, may have evolved in situ in 
Central America (Longino 1989a and b), a periph- 
eral and comparatively species-poor region within 
the overall distribution of Cecropia. These events 
might well have resulted from independent second- 
ary colonizations of a host which reached Central 
America from South America in advance of its 
typical ant symbionts, or which colonized habitats 
unsuited to the usual associates. 


Elevational segregation among plant-ants of par- 
ticular hosts suggests that new colonizations might 
occur at the elevational limits of species distribu- 
tions. In the lowlands of Cameroon, myrmecophytic 
Leonardoxa consistently house one of two closely 
related myrmelachistine ants, Petalomyrmexphylax 
or Aphomomyrmex afer, depending on host species 
(McKey 1991). However, in submontane forests of 
the Rumpi Hills (500-1700 m), where neither of 
these ants occurs in association with Leonardoxa , 
the plants are inhabited by a bewildering array of 
other ants, including at least two species each of 
Crematogaster, Axinidris and Technomyrmex, and 
one species each of Tapinoma and Leptothorax (R. 
Snelling, personal communication). Some of these 
ants are known not to be host-specific, and they 
may be secondary colonists of a preexisting asso- 
ciation of Leonardoxa with myrmelachistine ants, 
although firm conclusions on directionality of this 
shift must await further work. Finally, in the 
Neotropics, altitudinal replacements should be com- 
mon at the periphery of the Andes. Although we 
know of no published data to test this prediction, 
Longino (1991b) relates that the ranges of some 
Azteca residents of Cecropia segregate altitudinally, 
with some species occurring as high as 2000 m in 
elevation. 

As secondary colonists of myrmecophytes be- 
come increasingly specialized for exploiting their 
new hosts, selection should enhance the host-find- 
ing abilities of these species. With their priority-of- 
colonization eroded, primary associates may even- 
tually be displaced to marginal habitats or replaced 
altogether. 

Taxonomic Progressions Within 
Plant-Ant Lineages 

Since ant-plant symbioses have been shaped by 
repeated evolutionary colonizations and strong com- 
petition among ants, major taxa of plant-ants might 
be expected to exhibit regular taxonomic progres- 
sions in species distributions and characteristics. 
Similar progressions have been described for adap- 
tive radiations in several well-studied animal groups, 
including ants (Wilson 1959a and 1961), carabid 
beetles (Erwin 1985), and birds (Ricklefs and Cox 
1972; Diamond 1986). These accounts are related 


52 


Journal of Hymenoptera Research 


in their emphasis on competition as the force driv- 
ing evolutionary trajectories in animal lineages. 
Wilson’s seminal exposition of the “taxon cycle” in 
Melanesian ants proposes that ants invade new 
geographic areas principally via marginal habitats 
where competition from other ants is reduced. 
From this tenuous foothold, and driven by arrivals 
of new and more dominant species, they diversify 
and evolve competitive strategies which eventually 
enable their invasion of more species-rich forest 
habitats. In apparent contrast, Erwin’s recent ac- 
count of “taxon pulses” in carabid beetles proposes 
that young carabid taxa first appear in productive 
and central moist equatorial habitats. There, they 
force the specialization and migration of older taxa 
into less competitive peripheral latitudes and habi- 
tats. Apparent disparities in the phrasing of Wilson’ s 
and Erwin’s theories obscure theircommon ground. 
Both ideas have their roots in Darlington’s (1957) 
“centrifugal speciation”, whereby intense biotic 
interactions drive waves of species and higher taxa 
from tropical to temperate regions. Moreover, 
whether species originate in new and permissive 
environments, or as evolutionary novelties in 
biotically restrictive environments, young species 
are those with “r-selected” life histories, and gener- 
alized and expanding distributions. Older, progres- 
sively “K-selected” species are driven by biotic 
interactions to increasing specialization and more 
circumscribed distributions. There they persist by 
either unique strategies for evading natural en- 
emies, or by tolerance of unfavorable conditions. 
Vermeij (1978) has argued cogently for similar 
evolutionary trajectories in various marine inverte- 
brate taxa. 

The evolutionary history of plant-ants strongly 
suggests similar taxonomic progressions. Three 
types of evidence support such an interpretation. 
First, as discussed above, taxonomic and biogeo- 
graphic patterns in some ant-plant symbioses sug- 
gest directionality in species replacements, and 
particular taxa occupy predictable roles as victims 
(e.g., Pseudomyrmecinae) and agents (e.g., 
Crematogaster and Azteca) of such replacements. 
Second, and also discussed above, field experi- 
ments and observations strongly support interspe- 
cific competition among ants, often habitat-depen- 
dent in its outcome, as the principal mechanism of 


species replacements. Furthermore, roles of differ- 
ent ants in postulated replacements are consistent 
with their status (independently determined) in 
competitive hierarchies. Third, within ant-plant 
guilds, the postulated replacements of subordinate 
genera, such as Pachycondyla, Plcigiolepis, 
Camponotus, Pseiidomyrmex, and Tetraponera , by 
dominant genera such as Crematogaster, 
Technomyrmex, and Azteca, are consistent with the 
historical sequence in which these taxa are repre- 
sented in the fossil record (Table 2, based on 
Holldobler and Wilson 1990, and see below). 

The diversification of ant taxa began in earnest 
no later than the beginning of the Tertiary Period 
(Holldobler and Wilson 1990), and it eventually 
made ants the most important natural enemies of 
one another. At protected nests and feeding sites, 
timid, twig-inhabiting myrmelachistines and 
pseudomyrmecines, probably among the earliest 
plant-ants, sought out pubescent plants or insect 
borings and other cavities of live plants. But in the 
background, competition was escalating. Evolu- 
tionary advancements in offensive and defensive 
weaponry intensified the pressures on timid and 
secretive plant-ants. As discussed above, evolu- 
tionary novelties and secondary colonizations ap- 
pear to have arisen differentially in environments 
where disturbance favored weedy species with early 
and high reproductive allocation, superior coloniz- 
ing abil ity , and thus priority of access to ant domatia. 
Here also, high productivity (associated with high 
light intensities) subsidized rapid colony growth 
and the evolution of costly chemical weaponry. 
Individually or in combination, these traits made 
their bearers formidable enemies of existing plant- 
ants, driving them into ever more restrictive spe- 
cialization on one or a few hosts, into marginal 
habitats, and in some cases into extinction. Eventu- 
ally, many secondary colonists appear to have 
partly or completely replaced the primary associ- 
ates of several myrmecophyte lineages. These 
secondary associates were often pressured in turn 
by successive waves of newly evolved dominants. 

What examples support such a scenario? 
Myrmelachistine ants provide perhaps the best il- 
lustration of the fate of an old group of competi- 
tively subordinate ants, whose members have been 
driven to suboptimal habitats, to extreme special- 


Volume 2 , Number 1 , 1993 


53 


ization, or to extinction, by dominant ants. As 
circumscribed by Holldobler and Wilson (1990), 
following Wheeler (1920), this tribe is pantropical 
and includes six genera, two of which are endemic 
to each of the major tropical regions (the New 
World, tropical Africa and the Oriental tropics). In 
a recent and still incomplete analysis of generic 
relationships in Formicinae, Agosti (1991) casts 
doubt on the monophyly of the tribe, placing 
Cladomyma in a different informal genus-group 
from all the others. We follow the usual treatment 
of the tribe, but acknowledge the need for further 
work to resolve phylogenetic relationships of these 
ants. 

Myrmelachistine genera have no fossil record 
(Table 2), possibly because most have long been 
specialist plant-ants with restricted ecological dis- 
tributions. However, they are likely to have been 
widespread prior to Miocene times, since two ant 
genera from a tribe (Gesomyrmecini), considered 
by Wheeler (1920) to be closely related (but see 
Agosti 1991), are represented in early Oligocene 
Baltic amber (Holldobler and Wilson 1990). One 
of these, Gesomyrmex , is represented by four extant 
species of the Oriental region (Wheeler 1929a). 
They share with the Oriental myrmelachistine 
Cladomynna certain similarities, such as reduced 
antennal segmentation (believed to be a derived 
character) and worker polymorphism with major, 
media, and minor workers. Furthermore, G. 
kalshoveni Wheeler of Java, is recorded as nesting 
in twig cavities of Artocarpus in primary forest 
(Wheeler 1929b). These bits of information on an 
ant genus regarded by Wheeler (1929a) as “living 
fossils which have undergone no significant modi- 
fication since the Early Tertiary” suggest that the 
plant-ant habit may have a long evolutionary his- 
tory in the Formicinae, currently regarded as hav- 
ing diverged very early from the basal lineage of the 
Formicidae (Holldobler and Wilson 1990). 

In all parts of their pantropical distribution, 
myrmelachistines appear to have experienced eco- 
logical contraction. Although no phylogeny is 
available for the New World genus Mynnelachista , 
interspecific patterns in its distribution and ecology 
reveal the likely imprint of past competition. 
Mynnelachista are often conspicuous leaf foragers 
in montane forests of Central and South America, 


where dominant Crematogaster and Azteca ants 
are largely missing (J. Longino, personal commu- 
nication). In sharp contrast, congeners of tropical 
lowlands are stem-nesters with a relatively incon- 
spicuous presence on leaf surfaces. Among resi- 
dents of Costa Rican Ocotea, workers of a 
Mynnelachista plant-ant at 500-700 m elevation (at 
Rara Avis) do not attack vines (B. Fisher, personal 
communication), though those of a congener at 50 
m in nearby La Selva Biological Station do prune 
(D. Davidson, personal observation). Finally, in 
western Amazonia, perhaps the center of neotropical 
ant diversity (Wilson 1987), Mynnelachista resi- 
dents of Duroia hirsuta and Cordia nodosa appear 
to protect themselves not only by pruning vegeta- 
tion other than potential host plants, and by main- 
taining extensive clearings (“supay chacras”), but 
by effectively hiding from larger-bodied ants amid 
the dense stem hairs of these two hosts. (Morawetz 
et al. [ 1 992] argue that creation of similar clearings 
by a Mynnelachista species on Tococa is not a 
product of past competition. However, this asser- 
tion is based strictly on the probably valid assump- 
tion that clearings enhance the light environment 
and productivity of host plants; it did not stem from 
any direct test for the effects of competition from 
other ants [see, e.g., Davidson et al. 1988]). Over- 
all, the pattern reveals that increasing specializa- 
tion for resisting dominant ants may have been 
required for persistence in highly competitive and 
diverse lowland rainforest faunas. 

The evolutionary fortunes of myrmelachistines 
also appear to have declined in the Old World 
tropics. In Africa, they are represented by only two 
monotypic genera ( Petalomynnex and 
Aphomomynnex). The former is restricted to a 
single host species and confined to a very small area 
of Lower Guinea coastal forest. Both species are 
plant-ants, though interestingly, neither prunes nor 
inhabits pubescent myrmecophytes. Cladomynna 
is one of two myrmelachistine genera known from 
Asia (with the status of Pseudaphomomyrmex re- 
maining uncertain), and all five described species 
are specialized plant-ants (Agosti 1991). Some of 
their hosts (e.g., Saraca) are shared with 
Crematogaster , suggesting the potential for com- 
petitive interactions with this group of dominant 
ants. Furthermore, patterns of host association indi- 


54 


Journal of Hymenoptera Research 


cate that Crematogaster may have replaced 
Cladomyrma in some systems. Thus Cladomynna 
persists on Asian Neonauclea, but Crematogaster 
dominates closely related Myrmeconauclea. Too 
little is known of phylogenetic relationships among 
representatives of any of these lineages to draw 
firm conclusions. 

Pseudomyrmecines appear to be another rela- 
tively old group in which the plant-ant habit may be 
ancient, and in which competitively subordinate 
plant-ants have been restricted or replaced by more 
recently evolved, competitive dominants. 
Tetraponera first appears in fossil deposits in the 
early Oligocene and Pseudoinynnex in the Oli- 
gocene (Table 2). The monotypic Myrcidris, a 
plant-ant whose specializations indicate a long his- 
tory of association with plants, may be a relict that 
is the sister group to all other pseudomyrmecines, 
though other interpretations are possible (Ward 
1990). As discussed above, plant-ants of this rela- 
tively old subfamily are among the most frequent 
apparent victims of the expansion of younger groups 
such as Crematogaster and Azteca. 

Other groups of competitively subordinate ants 
tor which there is circumstantial evidence of re- 
placement by more recently evolved dominants 
also occur relatively early in the fossil record. 
These include Pachycondyla, Camponotus, and 
Plagiolepis , all of which appear in the early Oli- 
gocene. Cecropia specialists derived from widely 
distributed Pachycondyla villosa and P. unidentata 
(J. Longino, personal communication) are prob- 
ably more recent secondary colonists, inhabiting 
mainly older and woody stems abandoned by other 
ants. At present, no evidence indicates that these 
are replacing former inhabitants. Allomerus, an- 
other genus being pressured by contemporary domi- 
nants, has no fossil record, perhaps because all of 
these ants have been plant-ants with highly re- 
stricted distributions. 

In contrast to these weakly competitive groups, 
genera implicated as dominant ants and^ secondary 
or tertiary colonists of existing associations appear 
to be more recent arrivals. The first fossil records 
of Crematogaster and Technomyrmex are in the 
Miocene, and Azteca appears in the early Miocene 
(Table 2). 


Taxonomic Progressions and Intercontinental 
Comparisons of Ant-Plant Symbioses 

If taxonomic progressions such as those postu- 
lated above play major roles in transforming ant- 
plant symbioses over evolutionary time, then long- 
term evolutionary history assumes an added di- 
mension as an important factor shaping interconti- 
nental differences in the nature of ant-plant sym- 
bioses. Contemporary patterns will reflect the 
point to which taxonomic progressions in plant- 
ants have proceeded in a region. The location of 
this point should depend on the ages of regional 
mesic-forest communities (to which most ant-plant 
symbioses are restricted), the traits of the particular 
dominant and subordinate ants evolved there dur- 
ing this period, and the degree to which the region 
is isolated from the products of taxonomic progres- 
sions begun elsewhere. 

West Gondwanaland, today represented by its 
derivative continents Africa and South America, 
has been considered the cradle of the angiosperms 
(Raven and Axelrod 1974). Mesic tropical forest 
and its typical constituents, including plant-ants, 
have had a long history on both these continents. In 
Africa, for example, despite climatic vicissitudes 
and shifts in continental position, a large area of 
lowland tropical rain forest has persisted unbroken 
since the Late Cretaceous-Paleocene (75-55 my 
B.P.) up to the present (Axelrod and Raven 1978). 
That taxonomic progressions in Africa and South 
America began with similar starting material, and 
have continued for about the same amount of time, 
may account for many of the striking similarities in 
ant-plant symbioses of these two regions (McKey 
and Davidson, in press). Interestingly, these two 
continents share old, competitively subordinate ant 
groups like myrmelachistines and pseudo- 
myrmecines. Although these taxa would respond 
in analogous ways to the later onslaught of domi- 
nants, the dominants are derived from different 
genera on the two continents. Whereas in the 
Neotropics, the preeminent competitive dominants 
consist of endemic Azteca, Crematogaster domi- 
nate in the Old World, where they are much more 
prevalent than in the American tropics (Appendix 
1). 


Volume 2, Number 1 , 1993 


55 


During virtually all the Tertiary, South America 
was an island continent (Barron et al., 1 98 1 , Gentry 
1982). Perhaps the later appearing dominants, 
Crematogaster and Azteca , evolved long after di- 
rect exchange between the two continents (via 
overland connections or island filter bridges) be- 
came impossible. Evidence suggests that 
Crematogaster could be an Old World genus which 
arrived relatively late in the New World, possibly 
as part of a widespread tropical Laurasian biota, 
elements of which could have reached the Neotropics 
via North America. First recorded in Sicilian 
amber in the Miocene, the genus is represented in 
Dominican amber (late Miocene), and might con- 
ceivably have invaded South America via Panama, 
a connection in place since the Pliocene (Keigwin 
1978, Barron et al. 1981, Marshall et al. 1982). 
Moreover, species richness of Crematogaster is 
greater in the African and Oriental tropics than in 
the Neotropics (Brown 1973), and the genus has 
evolved numerous specialized plant-ants in the 
former two regions, but only two such described 
species in the American tropics. From our sum- 
mary in Appendix 1, relationships involving 
Crematogaster account for only 7.6 % of all 66 
symbiotic ant-plant relationships listed for the 
Neotropics, but 39.5 % of 43 associations and 27.3 
% of 33 relationships in Africa (including Mala- 
gasy) and the Oriental tropics, respectively. Based 
on analyses at the generic level, our calculations fail 
to take into account the substantial radiations of 
species within the genus Crematogaster on Asian 
Macaranga (Appendix 1 ), as well as the nine spe- 
cies of Crematogaster occurring on African 
Mnsanga (though probably none is a specialized 
plant-ant). No parallel radiations occur in the 
American tropics. 

During the Tertiary, while the South American 
biota was evolving in isolation, there were repeated 
opportunities for biotic exchange between tropical 
Africa and tropical Laurasia. The latter region has 
long harbored mesic tropical forests, though opin- 
ions vary on whether these forests are as ancient as 
those of West Gondwanaland (Raven and Axelrod 
1 974). At the very least, the Oriental tropics were 
an area of moist, equable climate relatively re- 
moved from the major vicissitudes of Neogene and 
later climatic change (Raven and Axelrod 1974). 


Biotic connections of tropical alliances, at least 
through the early Tertiary, may account for simi- 
larities in taxonomic composition of both subordi- 
nate and dominant plant-ants of the African and 
Oriental regions (e.g., Tetraponera as well as 
Crematogaster and Oecophylla). They may also 
help to explain some possible cases of common 
ancestry among ant-plant associations of the Afri- 
can and Oriental tropics (McKey and Davidson, in 
press). 

Of the major tropical regions, the Australian 
tropics (northern Australia, New Guinea, and asso- 
ciated islands) are outstanding for the geologic 
youth of their tropical mesic-forest environments. 
By the Paleocene, Australia was connected with the 
rest of the world only by a cool-temperate pathway 
to South America via Antarctica (Raven and Axelrod 
1 974). At the start of its northward movement 45- 
49 my B.P., what is now tropical northern Australia 
was all well south of the Tropic of Capricorn, and 
was still 1 0 degrees south of its present position by 
the Miocene, when direct migration from the Asian 
tropics first became possible (Axelrod and Raven 
1972). As for New Guinea, neither it nor its 
principal antecedents existed prior to about 40 my 
B.P. Only by the Miocene did it lie close enough to 
the proto-Indonesian arc to begin receiving large 
numbers of immigrants from tropical Asia. (How- 
ever, as vertebrate distributions illustrate, such 
migration was never directly overland [Axelrod 
and Raven 1982]). Thus tropical northern Australia 
and mesic-forest portions of New Guinea have 
been populated to a large degree by taxa derived 
from the Asian tropics via intervening islands (Wil- 
son 1961; Raven and Axelrod 1 974). Nevertheless, 
the contemporary distributions of at least some 
plant-ants (e.g., Anonychomynna, see Shattuck, 
1 992b) reveal an almost certain origin in Australasia. 

Tropical forests of northern Australia and New 
Guinea provide uniquely little evidence for re- 
placement of older and competitively subordinate 
ant genera by contemporary dominants. The ori- 
gins of tropical rain forests in the Australian region 
have apparently been too recent to have allowed 
significant radiations of specialized plant-ants in 
more ancient and weakly competitive ant genera 
prior to the arrival and expansion of the dominants. 
If so, this could help to explain why the fraction of 


56 


Journal of Hymenoptera Research 


ant-plants obviously specialized as myrmecophytes 
is so low in the Australian region (column 6 in 
Appendix 1 ). Compared to 5 1 .2 % of 39 Neotropi- 
cal ant-plant genera, 59.4 % of 32 African genera, 
and 4 1 .4 % of 29 Oriental myrmecophyte genera, 
only 10.7 % of 28 such genera in the Australian 
region have conspicuous specializations to attract 
ants. In the last of these areas, only Endospermitm, 
Ccmthium and Calamus have convincingly ant- 
attractive traits (Appendix 1). Present day plant- 
ants of this region consist principally of dominant 
species of Anonychomyrma (formerly included in 
Iridomyrmex, Shattuck 1992b), Teclinomyrmex and 
Crematogaster, as well as Philidris on epiphytic 
myrmecophytes (Shattuck 1992b). These ants oc- 
cupy only a small number of variously preadapted 
host genera, where they maintain scale insects at 
remarkably high biomass, possibly limited by stem 
volume. Consistent with their status as dominants, 
they do not exhibit host fidelity in foraging. Neither 
pruning of host-plant neighbors, nor hiding among 
dense trichomes is required for persistence of such 
capable competitors. Two associations with weakly 
competitive ant genera may also be comparatively 
recent in origin. The Camponotus of Endospermum 
obtain their protein not from specially evolved 
plant structures, nor from protected sources within 
the stem (e.g., homoptera or the heteroplasias of, 
e.g., Vitex ), but through a form of parasitism of 
external stem walls, i.e., the induction of 
heteroplasias from cambium (D. Davidson, per- 
sonal observation). Moreover, at least one pro- 
posed myrmecophyte in this genus often occurs 
without its ants (Airy-Shaw 1980). Similarly, Ward 
(1991) notes that the unnamed Tetraponera tend- 
ing coccids in terminal branches of Cupaniopsis 
has a much narrower geographic range than does its 
host, and that the symbiosis is apparently young. 

In attempting to explain intercontinental differ- 
ences in diversity, it will be extremely difficult to 
distinguish the relative importances of two major 
historical factors. These are regional differences in 
1) the condensation of diversity through competi- 
tion; and 2) the magnification of diversity, as af- 
fected by habitat diversity and its effects on rates of 
evolutionary host shifts and de novo evolutionary 
colonizations (see above and McKey and Davidson, 
in press.). 


CONCLUSIONS 

Similar selection pressures acting on correspond- 
ingly preadapted ants and plants have produced 
strikingly parallel and convergent evolution in the 
symbiotic ant-plant relationships of different tropi- 
cal regions. Although current concepts of ant-plant 
coevolution focus on the pairwise interaction be- 
tween ant and host plant, these alone cannot ac- 
count for the patterns we observe. Even in relation- 
ships where pairwise interactions are undoubtedly 
strong, multispecies interactions appear to have 
determined many features of present-day symbio- 
ses. The most important force driving the evolu- 
tionary biology of ant-plant symbioses is interspe- 
cific competition among arboricolous ants. Plants 
differ in the kinds of resources which they offer to 
ants, in the rates at which they supply these re- 
sources, and in traits which influence the relative 
competitive abilities of foraging and nesting ants. 
As in other communities structured by competition, 
plant-ants sort out across plants in ways that are 
predictable from their particular resource require- 
ments and competitive abilities and the spectrum of 
available resources (see also Bristow 1991). In the 
American, African and Asian tropics, competi- 
tively dominant ants are associated with the most 
light-demanding and fast-growing hosts, which 
supply resources at the rates required to fuel rapid 
colony growth, interspecific aggression and other 
traits required for dominance. In contrast, competi- 
tively subordinate ants are restricted to plants which 
supply resources at rates too low to support domi- 
nant ants, or to those from which dominant ants can 
be excluded by long, dense plant hairs, pruning of 
neighboring vegetation, or by other ant and plant 
traits which favor competitively subordinate spe- 
cies. Competitive interactions among ants deter- 
mine whether patterns of ant-plant association are 
sufficiently predictable for strong interactions to 
shape the evolution of ants and plants. When 
competitive interactions in plant-ant guilds result 
in constancy in the pairing of particular ants and 
plants, reciprocal evolutionary interactions may 
occasionally give rise to pairwise coevolution. 

Parallel and convergent selection pressures acted 
on similar biological material on different tropical 
land masses. In American, African, Asian and 


Volume 2 , Number 1 , 1993 


57 


Australian regions, the same important 
preadaptations facilitated evolution of the plant-ant 
habit in several lineages of arboricolous ants. Fore- 
most among these traits were the habit of tending 
Coccoidea, and the differential competitive abili- 
ties determined by generically typical offensive 
and defensive weaponry, or by inherent colony 
growth rates and other life-history attributes. Like- 
wise, similar sets of plant traits facilitated the 
evolution of myrmecophytes on different conti- 
nents. Structures evolved independently of ant- 
related selective pressures were co-opted repeat- 
edly as myrmecophytic traits in plant lineages that 
eventually produced ant-plants. These traits in- 
cluded both the long, dense hairs typical of many 
myrmecophyte stems and domatia, and stems 
strongly thickened as support structures for large 
leaves, and available as nest sites for opportunistic 
ants. These similarities in starting material have 
rendered even more pronounced the striking paral- 
lel and convergent evolution of ant-plant symbio- 
ses in the New World and Old World tropics. 

Diversity of both myrmecophytes and their at- 
tendant ants appears to accumulate mainly across 
habitats, rather than biogeographical regions 
(McKey and Davidson, in press). Among ant- 
plants, evolutionary diversification across habitat 
boundaries often appears to reflect the conflicting 
selection pressures imposed by different plant re- 
source environments. Like other tropical plants 
(McKey etal. 1978, Coley 1983), myrmecophytes 
have responded evolutionarily to particular resource 
regimes by altering their relative investments in 
defense versus growth and, perhaps, their relative 
allocation of different kinds of resources to defen- 
sive function (Davidson and Fisher 1991, Folgarait 
and Davidson 1992). In turn, ecological and evolu- 
tionary responses of plants to different resource 
environments determine the quantity and quality of 
resource supply to ants. On the whole, then, both 
partners in ant-plant associations may be more 
sensitive to habitat than to taxonomic differences 
among symbiotic partners. 

Strong competition among mutualists has been 
proposed as a major factor driving the evolution of 
specialization in mutualisms (Law and Koptur 
1 986), and it could help to account for the origins of 
many specialized ant-plant symbioses. Neverthe- 


less, where sufficiently well-studied, phylogenies 
of plant-ants, together with host distributions of 
these ants, suggest that pairwise coevolution and 
cospeciation have been rare. Rather than simple, 
pairwise ant-plant systems, guilds of interacting 
ants and plants seem to be the most frequent arena 
of ant-plant evolutionary interaction. Perhaps as a 
consequence, plant-switching and secondary colo- 
nization (rather than cospeciation or some other 
form of association by descent) may have been the 
usual processes by which these mutualisms diver- 
sified. Repeated colonization of myrmecophyte 
taxa has occurred as unspecialized ants have ex- 
ploited preexisting mutualisms and specialized 
plant-ants have switched hosts. Habitat-depen- 
dence in the effect of associations on fitness of the 
participants seems to have been the principal force 
leading to the evolution of new associations. The 
motor driving such evolutionary opportunities was 
likely the climatically induced range expansion 
that placed ants or plants into habitats sufficiently 
novel to change selection regimes, and to increase 
encounters with new associates (McKey and 
Davidson, in press). 

Regardless of how species originate, a complex 
mosaic of habitats should help to maintain higher 
local diversity, with greater species richness of 
myrmecophytes and/or specialist plant-ants, and a 
greater number of ant/plant combinations. Since 
the potential for evolution of new associations via 
host shifts and secondary colonization depends in 
part on the sizes of locally interacting ant and plant 
guilds, high local diversity may lead to higher rates 
of species origination. Thus, independently of 
distributional changes driven by varying climates, 
beta-diversity is likely to have enhanced alpha- 
diversity. 

As summarized here, the determinants of diver- 
sity of plants and ants in these symbiotic mutualisms 
will likely generalize to other components of tropi- 
cal floras and faunas. In particular, we expect that 
diversification of tropical plants has often involved 
evolutionary adjustments in the amounts and kinds 
of defenses, in response to habitat differences in 
absolute and relative availabilities of essential re- 
sources. Consequently, habitat mosaics related to 
edaphic factors and incident solar radiation should 
often determine mosaics in the primary productiv- 


58 


Journal of Hymenoptera Research 


ity available to consumer organisms. Habitat spe- 
cialization to different productivity regimes has 
likely been important to both the generation and 
maintenance of diversity in many tropical con- 
sumer guilds whose member species have strongly 
overlapping resource requirements (cf., Terborgh 
1983 for primates, and S. Robinson and J. Terborgh, 
personal communication, for birds). 

Habitat specialization may frequently also rep- 
resent the intermediate and final stages of a taxon 
pulse, in which new, opportunistic, abundant, and 
widespread species are driven to progressively 
greater specialization, finer niche differentiation, 
diminished distribution and abundance, and per- 
haps even eventual extinction (Wilson 1959a and 
1961, Ashton 1969, Erwin 1985, Diamond 1986). 
If taxon cycles or pulses are general features of 
animal and plant lineages, they might aid in ex- 
plaining patterns in the relative abundance distribu- 
tions of taxa within higher taxa. Dial and Marzluff 
(1989) have discussed the frequency of “hollow 
curve distributions”, or the overdominance of par- 
ticular minor taxa within major taxa (subunits/ 
unit). Thus, the degree of dominance of most 
dominant taxa is greater than that predicted by a 
variety of null models based on Poisson processes, 
random cladogenesis, and simultaneous or sequen- 
tial resource subdivision, and it is compounded at 
lower levels of the taxonomic hierarchy. Taxon 
pulses might regularly give rise to such patterns if 
the enumeration of taxa at successively lower lev- 
els of the taxonomic hierarchy (where taxa are more 
numerous) were more likely to pick up compara- 
tively rare groups which had recently acquired 
evolutionary novelties, and which represented in- 
termediate stages of a taxon pulse. 

Our analyses of the evolutionary dynamics of 
ant-plant symbioses here and elsewhere (McKey 
and Davidson, in press) lead us to propose new 
hypotheses to explain differences in the diversity of 
ant-plants and plant-ants across different tropical 
regions. Such disparities are quite pronounced 
between the American and African tropical re- 
gions, where ant-plant symbioses are best under- 
stood. Previous explanations for differences in the 
biodiversity of species-rich Neotropical and depau- 
perate African rain forests have emphasized the 
contrasting climatic histories of these two regions. 


Focusing on range contractions during periods of 
unfavorable climate, these explanations attribute 
Africa’s lower diversity to greater extinction dur- 
ing the Pleistocene, as Africa’s climate became 
drier, and refugia were fewer than in Amazonia 
(Raven and Axelrod 1974). We propose that differ- 
ences between the two regions in the rates of 
species origination may be at least as important as 
extinction rates. The relatively stable geological 
history of most of Africa, including the rainforest 
zone, has created a landscape with relatively little 
elevational relief (hence few sharp spatial contrasts 
in temperature and rainfall), comparatively little 
edaphic variation, and relatively infrequent and 
spatially limited fluvial disturbance. In contrast, 
the Andean orogeny, and subandean tectonic activ- 
ity, have helped to create a landscape of great 
elevational, climatic, and edaphic complexity, es- 
pecially in western Amazonia. This has resulted in 
a complex and dynamic mosaic of habitats. 
Colinvaux (in press) suggests that species origina- 
tion usually takes place when ranges are re-expand- 
ing during periods of climatic amelioration. If this 
is so, then in the Neotropics, especially in western 
Amazonia, range expansion would be much more 
likely than in the African forest zone to place ants 
and plants into novel habitats, leading to speciation, 
the formation of new associations, or both. 

Although poorly known by comparison, Asian 
rain forests occur in regions (especially Borneo) 
where topography is substantially more variable 
than that of tropical Africa. Aided by forest frag- 
mentation on numerous island land masses, this 
topography has contributed to the diversification of 
several myrmecophyte lineages here. 
Myrmecophyte diversity in Asia appears to be 
intermediate between that of the African and Ameri- 
can tropics. On the other hand, both regions of the 
Old World tropics may have had the generic diver- 
sity of their plant-ant faunas condensed, relative to 
that of the New World, by the comparatively early 
arrival of a new wave of competitively dominant 
Cremalogcister. The relatively recent origin of rain 
forests in the Australian tropics (including New 
Guinea and associated islands) appears to have 
limited the diversification of myrmecophytes in all 
but the epiphytic Hydnophy tinae ( Jebb 1991, Huxley 
and Jebb 1991). In addition, the elaboration of 


Volume 2, Number 1, 1993 


59 


myrmecophytic traits, which have evolved so fre- 
quently elsewhere in associations with weakly com- 
petitive ants, may have been limited in Australia by 
the cooccurrence of contemporary dominant and 
subordinate ants at the time when rain forests were 
evolving. 

ACKNOWLEDGEMENTS 

This work was supported by the NSF grants RI1- 
8310359 and BSR-9003079, the Guggenheim Founda- 
tion, the Christensen Research Institute and the Univer- 
sity of Utah’ s Faculty Research Committee (to Davidson) 
and the Swiss Natural History Society, the National 
Geographic Society, and the University of Miami (to 
McKey). We thank R. Snelling for numerous ant iden- 
tifications, graciously fit into an overburdened schedule, 
and for helpful conversations about ants. J. Longino and 
P. Ward made invaluable comments on several previous 
drafts of the manuscript, and they and R. Snelling made 
available many of their unpublished observations. Any 
mistakes remaining are our own. We are also very 
grateful to M. Hossaert for facilitating our extensive E- 
Mail correspondence. The manuscript benefitted im- 
measurably from consultations over recent years with 
myrmecologists and botanists specializing in particular 
taxa or floras. These include: C. C. Berg, W. L. Brown, 
Jr., W. Burger, J. Dransfield, A. H. Gentry, W. Judd, J. 
Longino, J. Miller, T. Musthak Ali, S. Renner, S. O. 
Shattuck, J. C. Solomon, C. M. Taylor, H. van der Werff, 
P. S. Ward, and J. L. Zarucchi. Finally, since ant-plant 
symbioses are being drastically altered by habitat de- 
struction around the world, we are particularly grateful 
for the natural parks and reserves that have permitted us 
and others to study these interactions in their pristine 
form. 

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68 


Journal of Hymenoptera Research 


Appendix 1 . Summary of ants living regularly in symbiotic association with one or more 
host species. Questionable or massing data are indicated by question marks. Columns: 

(1) Ant genera (superscript indicates carton-building typical of the genus, though not 
necessarily of plant-ant species) in biogeographic regions (N) = Neotropical, (E) = Ethiopian, 
(M) = Malagasy, (O) = Oriental, and (A) = Australian regions. 

(2) Host taxa have growth forms: T = tree; U = treelet or understory tree; S = shrub; L = 
liana or vine, R = rattan, B = bamboo and H = hemiepiphyte. Habitats include: b = mountain 
brooks; e = edge, second growth, riparian environments; g = forest light gaps; 1 = littoral 
scrub; p = primary forests; s = savannahs or dry forest, and a = aguajals or swamps. 

(3) Ants nest in domatia comprised of: L = leaf pouches; S = naturally hollow stems; Sp = 
pithy stems, hollowed by ants; I = swollen intemodes; P = swollen petioles or bases of 
petioles; Ps = petiolar sheath; R = swollen rachi and petioles; St = persistent stipules (in- 
flated or folded); Sh = persistent spathe; Th = swollen thorns; F = swollen flowering shoots; 
G = gall-like swellings; C = carton shelters around domatia, folded leaves, and/or hairs or 
spines; Cl = cavity formed by leaf base clasping stem; B = insect borings; O = inflated ocrea 
(proximal extension of leaf sheath beyond the petiole), A = erect, narrow auricles on each 
side of petiole, at the terminus of the sheath; Ac = acanthophylls, or basal pinnae reflexed 
backward to form a secluded cavity at the base of a palm frond; Ga = galleries enclosed by 
interlocking combs of spines, forming collars on leaf sheaths, and T = vast chambers exca- 
vated inside tree trunks by ants and partitioned by carton. Plant pubescence: y = domatia and 
stems bear long, dense hairs or spines, likely to inhibit movements of larger bodied ants; n = 
such hairs or spines lacking, or s = only a subset of plants have these hairs. 

(4) Ants prune vines and vegetation around their hosts: Y = obligate for plant-ants in this 
genus; S = in at least some ant associates of the host genus; F = where known, pruning is 
facultative, i.e., in the presence of enemy ants; N = not yet reported for the ant genus on this 
host genus. Host fidelity (foraging predominantly or entirely on the host): y = yes; n = no; i 
= for young (incipient) but not established colonies. 

(5) Food types include: P = pearl bodies; B = other specialized food bodies; H = exudates 
and bodies of homoptera (Coccoidea); E = extrafloral nectar; N = floral nectar; G = 
uncharacterized exudates of tiny glands; F = fungi; VV = lipid-rich and/or protein-rich plant 
wounds, or heteroplasias caused by traumatic injury by ants; O = pollen; T = glandular 
trichome. 

(6) Plants have evolved apparently specialized structures to house ants: Y = yes; N = no. 

(7) Estimated number of congeneric ant species found regularly on the host genus; prob- 
ability of more (+) or several more (++) indicated parenthetically. Square brackets denote 
ants known to be unspecialized, or whose specialization is in doubt. 

(8) References for data on ants or plants: Bq = Bequaert 1922; W = Wheeler 1942; S&B 
= Schnell and Beaufort 1966; B = Benson 1985; H = Huxley 1986; J = Jolivet 1986; H&W 
= Holldobler and Wilson 1990; I) = Davidson et al. 1989; IP = in press; PC = personal 
communication, I)D and DM = respective author’s observations. 


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Macaranga Tes S,n ?,? ? Y 2 Fiala & al. 1990; F. Rickson PC 

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f Daemonorops Rjp Ga,? ?,? H N? 4 Ridley 1910; DD; Rickson & 

Rickson 1986; Dransfield & 
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