SBC711 Philip Sanders 1

Discuss the features and diversity of ant-plant mutualisms in tropical

rainforests.
“the struggle for existence would be insufficient to explain the progress of
organic life, if another law, that of sociability and of mutual help did not
powerfully work for the improvement of the organisms and for strengthening the
species” Anon., 1880, cited in Boucher 1985, p17

Introduction

Mutualism is one of the main driving forces behind the decline in, as Boucher put it
in 1985, Newtonian ecology. Post-world war ecology has seen the subject more
unified with no defined split between plant and animal facets. The mathematical
approaches and models that aided the rapid growth of ecology, moving it into so
called Newtonian ecology compartmentalised the subject. Boucher states mutualism
as one of the main reasons for the growth of dissatisfaction in the 1970’s in this type
of research; a cognitive dissonance generated by increased popularity of the concept
that nature is an integrated whole but, the research focused on its compartments
(Boucher, 1985). The resurrection of the realised significance of symbiosis and
mutualism in ecology that saw the burst of research in the area during the 1970’s,
contributed massively to the above view. However, no reduction in the mathematical
approach (as Boucher seems to predict) occurred, rather it evolved in refinement by
either inclusion or exclusion of variables in order to get a more specific information
on systems depending on the precise focus of attention (see McDonald and Amstrup,
2001 and de Vries et al., 2006 for examples respectively). This does not detract from
an intergraded nature but increases its resolution. Research in ecology endeavours to
get a picture of nature and how it works and each focused piece of work acts like a
pixel in a digital photo, the greater number of pixels the better the resolution becomes
and more detail is observed. However, similar pixels appear more than once in the
same picture or appear in a completely different picture. This is again is observed in
ecology, the same ecological processes appear in completely different biomes or
different evolutionary versions of the same biomes. One of the best examples of this
is in the ant-plant mutualisms seen on all continents containing tropical rain forest
(Central and South America - Clement et al., 2008 and Machado et al., 2008; Africa -
Gaume and McKey, 1999; India - Shenoy and Borges, 2008; SE Asia -Cannicci et al.,
2008; Australia - Andersen and Morisson, 1998 ) and in most major biomes including
temperate (Whittaker, 1991) and savanna (Palmer et al., 2008).
Ant-plant mutualism has long been considered a classic model of coevolution
(Edwards et al., 2007) as well as mutualism (Bronstein, 1998), with pioneering work
highlighting its importance by D.H. Janzen in the 1960’s (Paracer and Ahmadijian,
2000). As a consequence of its vast geographic distribution, differences in habitats,
and complexities within those habitats there is a diverse array of interactions and
adaptations associated to the various relationships at different ecological levels. Ant-
plant mutualisms can be based on four main themes, 1) defence, 2) seed dispersal, 3)
provision nutrients, and 4) pollination (Paracer and Ahmadijian, 2000). In return
plants provide ants with food and sometimes nest sites. Food provided for the ants
occurs as either food bodies (FBs) which are generally developed in stipulates on the
plants twigs and shoots or extrafloral nectaries (EFN) usually located openly on the
leaf blade (Linsenmair et al., 2001). If the intimacy of the relationship extends to
housing the ants it usually occurs in hollowed out stems and twigs called the domatia.
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As ants dominate arthropod fauna in terms of biomass and numbers in tropical

ecosystems, largely as a result of their relationships with plants (Davidson, 1997), the
levels of ant-plant mutualism can be extraordinarily high, reports document up to 377
myrmecophytic plant/ha in Brazilian rainforest and one third of woody plants on
Barro Colorado Island offer ant rewards so are likely to be ant defended (Bronstein,
1998). Other biological interactions have evolved extending to third parties.
Trophobiosis adds further types of mutualism and species also exploit the ant-plant
relationships.
This essay will concentrate primarily on the first of the themes highlighted above,
defence. Ant defence includes herbivorous insects and vertebrates, pathogenic fungus,
and competitive creeping or epiphytic plants Two main strategies exist in plants that
buy defence with nutrition, obligate myrmecophytes, photobionts that house ant
zoobionts as well as supplying food, and facultative interactions with myrmecophillic
plants that attract ants (and other orders of insects) using FBs and/or EFPs (Paracer
and Ahmadijian, 2000, Bronstein, 1998; Linsenmair et al., 2001). For the purpose of
this essay they will be referred to an obligate or facultative myrmecophytes. Both
strategies will be explained and their diversity highlighted using examples form
different geographical regions. Diversity across ant-plant interactions will be
discussed broadly with examples from aspects other then defence and the inclusion of
other insects. Lastly, the relationship between nourishing plants and there defending
ant colonies have been instrumental in our understanding of the underlying ecological
principles of mutualism. Most of which is derived from analysis of costs, benefits, and
net outcomes of their interactions (Bronstein, 1998). This will be discussed which in
turn will display the subjects importance in increasing ecological resolution in regards
to the pixel metaphoric.

Obligate myrmecophytes of the neotropics

Mutualism between the Acacia and the ants from the genus Pseudomyrmex in
Central America are one of the first and most studied as a result of Janzen’s series of
ant exclusion experiments (Bronstein, 1998). The same type of experiments have been,
and are still being used as a template for looking at ant-plant ecology. Ants of the
genus Pseudomyrmex are aggressive and have predictable behaviour, the genus
contains 10 monophyletic species exclusive to mutualisms with obligate acacias, 4
unrelated species considered parasitic or commensals and 6 generalist species that
occasionally colonise Acacia thorns. The absolute dependence of 10 species and the
reliance of some acacia plants makes this one of the most impressive mutualisms
known (Ward, 1993). The levels of aggression drive of vertebrate and invertebrate
herbivores as well as smothering plants and even fires (Raine et al., 2002). There are
11 species of swollen thorn acacias, most of which are unlikely to survive to
reproductive maturity without a species of obligate ants (Janzen, 1975). The guard
ants are housed in stipular thorns or pseudogalls (Raine et al., 2002), which may or
may not house FBs. The ants burrow a hole in the tip of one thorne in each pair and
live in the resulting cavity (Paracer and Ahmadijian, 2000). All ant-acacia reward
guard ants with EFN on leaf rachis and petiole and neotropic species also provide
protein-rich Beltian bodies on young leaf pinnule-tips. The chemical composition of
the nectar currency affects the type of animal harvesting it, it is this that is thought to
create the strong link between these two obligate guilds. The nectar of the 11 acacia
species contains no sucrose, attractive to non-mutualistic ants, due to high invertase
activity. Pseudomyrmex have vertially no invertase activity in their digestion tracts
SBC711 Philip Sanders 3

and therefore prefer sucrose free EFN. The ratio amount of sucrose, fructose, and
glucose, along with amino acid concentration are all important and costly in attracting
zoobionts. However, some acacia not only use resources to attract and maintain ant
colonies but also allocate resources to enforce spatial segregation between the
protective ants and potential pollinators. As the ants may drive pollinators away
through predation and protection, A. hindsii produces ant repelling chemicals on its
young flowers as well as developing flowers on its less guarded older shoots (Raine et
al., 2002). One species P. nigrophilosa parasitize the Acacia trees, exploiting the
housing from the swollen thorns but not protecting the plant from herbivores or
encroaching vines. They exist on the host tree until evicted by a more competitive
species or the host tree dies (Tillberg, 2004). A number of zoobiont and photobiont
can attain relationships, creating differing combinations of mutualism, which can
change temporally. This combined with variation driven by geographic (Rico-Gray et
al., 1998) and resource availability (Bronstein, 1998) heterogeneity enables this
diversity to occur on such a local scale.
The interactions between the photobiont Cecropia and its zoobiont Azteca were first
described 100 years ago. The Cecropia are indicative of disturbed neotropic forest
and all lowland species are ant associated. The most specialised of this association it
with that of ants in the genus Azteca, which live in the young hollow stems. The stems
are separated into chambers by septa which are accessed by a fertilised queen through
a week point in the steam called the prostoma to lay her eggs. The offspring worker
ants’ boar out and defend their host and as the colony matures the initial chambers
become filled with fass, insect carcasses, and other debris, a hole is then bored in the
apical septum and the colony migrates. The old chambers are left filled with nutrient
rich debris which the opportunist plant utilises for a competitive edge. As well as
housing the colony, the plant also provides two FBs different from that of the Acacia;
Müllerian bodies and Pearl bodies. Costly Müllerian bodies, are similar to Beltian
bodies, rich in protein, carbohydrates, lipids, and amino acids, produced on the leaf
base. The pearl bodies are richer in lipids and produced on the abaxial surface of the
leaves. Isotopic analysis of the tissues of each partner species indicates that the food
bodies are fed preferentially to the larvae and that the adult workers feed on the
herbivorous insects they defend the plant from. Conversely to most obligate
mutualistic relationships, this is thought not to be driven by conflict of reciprocal
exploitation but of neutral to low cost for the combined benefit for each species
(Sagers et al., 2000). Such is the intimacy of the relationship, that food body
production does not reduce even at 40% defoliation, and the ants will increase in
numbers by five times in the presence of volatiles produced after leaf damage (Mayer
et al., 2008). However, nutrient levels and light have shown to have an effect on the
production of food bodies in green house conditions, although effect on colony size is
unknown (Heil et al., 2001), presumably, providing the mutualism starts the combined
factors of patrol of ants keeping competitors clipped and providing 93% of nitrogen
(Sagers et al., 2000) to the plant, a possible of reduction in the probability of light and
nutrient limitation occurring. It has been stated that for ground dwelling trees like
Cecropia nutrient gain is not of great importance (Fiala et al., 1989).

Obligate myrmecophytes of the paleotropics

As was found in the neotropics, there are many ant-plant associations but some
genus are more mutualistic then others. The genus Macaranga, containing 14 SE
Asian myrmecophytes (Fiala et al., 1989), associates with ants mostly from the genus
SBC711 Philip Sanders 4

Crematogaster. However, unlike the genus Azteca, obligate Crematogaster, rely

solely on the FBs produced by the species specific Macaganga. Every potential threat
to the plant is removed and thrown off the leaf surfaces, including insect eggs and
small larvae. The FBs provided for the colonies reflect this with high levels of
polymetric proteins and lipds and high carbon to nitrogen ratios, giving bodies of high
nutritious value. In fact in the species M. triloba, 5% of the plants total energy budget
goes to the production of FBs and 39% of carbohydrates, lipids, proteins and amino
acids invested in overall above ground growth is directed to FB production. Defence
from ants is an indirect method and could be considered relatively inefficient, none
the less the trees obviously rely heavily on this strategy in regards to allocation costs
of FBs. In support of this are the low chitinase activities, a chemical associated to
plant resistance to pathogenic fungi, recorded in Macaranga trees, a trait also
observed in the neotropical Acacia. Linsermair et al., came to the conclusion that the
costs are less for the plant to exchange food bodies for animal-specific defence, than
to produce intrinsic plant defences; the ants defences are the equivalent of a number
of different chemical substances. However, it seems that the Macaranga plants can
regulate the production of FBs in relation to both the presence of an ant colony and
also the presence of herbivore damage (Linsenmair et al., 2001), although unlike the
Cecropia which utilise ant fess for nutrient source the Macaranga appears to be
nutrient limited (Heil et al., 2001). Interestingly the Crematogaster adopt a
polygynous population structure on large mature trees to enable the success of the
colony. On young trees, more then one queen may inhabit different domatia but when
the workers emerge only one queen and its colony will survive. If this colony dies out
and the plant is re-colonised quickly, the damage is usually none lethal. On larger
trees the re-colonisation of sufficient numbers will take too long, in this circumstance
polygyny is tolerated. In addition, several breeding females may inhabit a large tree
after the loss of the founding queen for several weeks or perhaps months, until one
succeeds its parents in maintaining the colony. This enables the colony to continue the
mutualism beyond the relatively short life of the queen and endure through to the end
of the Macaranga’s life (Feldhaar et al., 2000).

Facultative myrmecophytes

The genus Macaranger also has facultative associations with a number of species of
ant, wasps, and flies. This type of myrmecophytes, use external feeding points usually
located on the leaf only; EFNs. As they serve a different purpose, attraction rather
than support, of the mutualistic species there are fundamental differences in the
chemical make up. ‘Taste’ or chemosensory stimulus appears to be more important
than nutritional benefit. The FBs of EFNs found in facultative plants had higher levels
of carbohydrates and were lower in lipids and significantly in protein, then obligate
species. In addition higher relative concentrations of soluble monomeric or dimeric
sugars were higher. As a result less energy is directed to the production of the plants
feeding points, with only 4% of overall energy budget used for EFNs and FBs.
Although the strategy is different and the benefits of the association not as
pronounced as with obligate species (to be expected as the costs are lower),
similarities exist. For example, the species M. tanarius shows significant increase in
nectar flow under greenhouse conditions and artificial leaf damage. Also reductions in
nectar productions occur if plants are protected from nectar feeding insects, therefore,
showing regulation abilities, just as the model obligate species does (Linsenmair et al.,
2001).
SBC711 Philip Sanders 5

Returning to the Central American Acacia genus we can look at diversity in an

aspect of community structure in ant-plant mutualisms. 2006 saw Guimarães et al.,
explore the degree of nestedness across four communities of differing properties.
Predominantly looking at species richness as the ecological frame work as to apply
predicted models on nestedness in mutualistic associations, the paper uncovered
additional ecological effects which also contribute to the degree of nestedeness. The
study worked across four different types of tropical landscapes exploring community-
level patterns in mutualism enabling the bridging of the two main areas of the study of
the organisation of multispecies mutualism; geographic mosaic theory and complex
network theory. The authors discovered that smaller less species rich communities did
not display nestedness the same way communities with high levels of species richness
did. Beyond this biogeographical properties and altitude affected the specialisation
fount in mutualistic communities (Guimarães et al., 2006).

Third party mutualisms and other diverse relationships

Ants aid plants other then just defence, pollination has been recorded but very few
solid reports have been made on it, a more frequently reported phenomenon is ant
seed dispersal. Both in the neotropical (Davidson, 1988) and palotropical (Kaufmann
and Maschwitz, 2006) forests exhibit these features. Kaufmann and Maschwitz (2006)
report finding 18 ant species and 51 plant species in the region they searched and
Davidson reports 10 epiphytic plant species and 3 ant species after his 1988 census in
Peru’s Manu National park. Both are papers report associations with Hemipteran,
trophobionts and fungi.
Trophobiotic relationships exist between many species in the orders Hemiptera,
Heteroptera, and Lepidoptera. Any attempt to exhaustively report these obligate and
facultative associations are deemed to remain fragmented, with several volumes
needed to condense the extensive literature published, so much is the diversity and
numerous the interactions. Most ant-attended species of Hemiptera feed from the
plant phylum and the insertion, feeding and extraction time needed exposes them to
threat of predation. Most species excrete ‘honeydew’ from the anus as high volumes
of liquid get passed through the body during condensing of the nutrients the
individual needs. This honey dew is high in sugar and can be seen as ecological
equivalent to EFNs, it is an additional source for nutrition for both obligate and
facultative associated ant-plant relations. As long as the trophobiosis levels remain
low then it can be seen as beneficial to both plant and ant specie,s as it aid the colony
size (discussed above) and, therefore, indirectly plant defence with little cost (Delabie,
2001).
Species form other orders also exploit ant-plant mutualisams, the semi-
myrmecophytic plant Humboldtia brunonis houses several types of ant species that
allow access to their domatia as breeding sites. This aids the pollen restricted species
in reproductive success but it is not known what effect it has on the plants defences
(Shenoy and Borges, 2008).

Conclusion

“Mutualisms (cooperative interactions between species) have had a central role in

the generation and maintenance of life on earth.” (Bronstein et al., 2006). This is
shown by the different aspects of research discussed above. Without these mutualistic
relationships the most numerous and abundant arthropod may not be the success it is,
SBC711 Philip Sanders 6

and without these associations and the niches that they opened up the diversity in the
tropics might not accumulate to the levels that they currently display. A dacade and a
half ago symbiotic ant–plant mutualisms were reported from over 100 genera of
angiosperms species and 40 genera of ants species (Davidson & McKey 1993). With
this diversity across a relatively local geographical mosaic and a global one, these
relationships provide the perfect platform for the development of robust ecological
models, that can be testes and refined across a range of different circumstances.
Although the initial stages of models appear to show throughout the literature, a lake
of solidarity between studies is present. Despite numerous reviews and many
publications, only recently does some sort of direction and comparison of the models
application appear. In Bronstein’s 1998 and 2006 reviews he states the importance in
the testing and application of ecological concepts extrapolated from the ant-plant
mutualisms to other to communities. With extensive literature as a foundation and an
immense diversity in the features of these mutualisms, the models that do exits can be
developed to include and combine the aspects discussed above. It is necessary to try
to develop predictive models from each variable, limiting nutrients, hebivory rates,
colony size, FB/EFN availability, community interactions, effects of trophobiosis etc...
and then combine them in order to give higher resolution of the picture science
already has. Once this is in place we can use the information to predict possible
outcomes when these areas are disturbed.
SBC711 Philip Sanders 7

References

ANDERSEN, A. N. & MORISSON, S. C. (1998) Myrmecochory in Australia's

seasonal tropics: Effects of disturbance on distance dispersal. Austral Ecology,
23, 483-491.
BOUCHER, D. H. (1985) The Idea Of Mutualism, Past and Future. IN BOUCHER, D.
H. (Ed.) The Biology of Mutualism: Ecology and Evolution. Beckenham,
Croom Helm Ltd.
BRONSTEIN, J. L. (1998) The Contribution of Ant-Plant Protection Studies to Our
Understanding of Mutualism. Biotropica, 30, 150-161.
BRONSTEIN, J. L., ALARCÓN, R. & GEBER, M. (2006) The evolution of plant &
insect mutualisms. New Phytologist, 172, 412-428.
CANNICCI, S., BURROWS, D., FRATINI, S., SMITH III, T. J., OFFENBERG, J. &
DAHDOUH-GUEBAS, F. (2008) Faunal impact on vegetation structure and
ecosystem function in mangrove forests: A review. Aquatic Botany, 89, 186-
200.
CLEMENT, L., KÖPPEN, S., BRAND, W. & HEIL, M. (2008) Strategies of a
parasite of the ant– Acacia mutualism. Behavioral Ecology and Sociobiology,
62, 953-962.
DAVIDSON, D. W. (1988) Ecological Studies of Neotropical Ant Gardens. Ecology,
69, 1138-1152.
DAVIDSON, D. W. (1997) The role of resource imbalances in the evolutionary
ecology of tropical arboreal ants. Biological Journal of the Linnean Society,
61, 153-181.
DE VRIES, H., STEVENS, J. M. G. & VERVAECKE, H. (2006) Measuring and
testing the steepness of dominance hierarchies. Animal Behaviour, 71, 585-
592.
DELABIE, J. H. C. (2001) Trophobiosis Between Formicidae and Hemiptera
(Sternorrhyncha and Auchenorrhyncha): an Overview. Neotropical
Entomology, 30, 501-516.
EDWARDS, D. P., ARAUCO, R., HASSALL, M., SUTHERLAND, W. J.,
CHAMBERLAIN, K., WADHAMS, L. J. & YU, D. W. (2007) Protection in
an ant-plant mutualism: an adaptation or a sensory trap? Animal Behaviour, 74,
377-385.
FELDHAAR, H., FIALA, B., BIN HASHIM, R. & MASCHWITZ, U. (2000)
Maintaining an ant-plant symbiosis: secondary polygyny in the Macaranga
triloba-Crematogaster sp. association. Naturwissenschaften, 87, 408-411.
FIALA, B., MASCHWITZ, U., PONG, T. Y. & HELBIG, A. J. (1989) Studies of a
South East Asian ant-plant association: protection of Macaranga trees by
Crematogaster borneensis. Oecologia, 79, 463-470.
GAUME, L. & MCKEY, D. (1999) An ant-plant mutualism and its host-specific
parasite: activity rhythms, young leaf patrolling, and effects on herbivores of
two specialist plant-ants inhabiting the same myrmecophyte. Oikos, 84, 130-
144.
GUIMARÃES, P. R., RICO-GRAY, V., REIS, S. F. D. & THOMPSON, J. N. (2006)
Asymmetries in specialization in ant–plant mutualistic networks. Proceedings
of the Royal Society B: Biological Sciences, 273, 2041-2047.
HEIL, M., HILPERT, A., FIALA, B. & LINSENMAIR, K. E. (2001) Nutrient
availability and indirect (biotic) defence in a Malaysian ant-plant. Oecologia,
126, 404-408.
SBC711 Philip Sanders 8

JANZEN, D. H. (1975) Pseudomyrmex nigropilosa: A Parasite of a Mutualism.

Science, 188, 936-937.
KAUFMANN, E. & MASCHWITZ, U. (2006) Ant-gardens of tropical Asian
rainforests. Naturwissenschaften, 93, 216-227.
LINSENMAIR, K. E., HEIL, M., KAISER, W. M., FIALA, B., KOCH, T. &
BOLAND, W. (2001) Adaptations to biotic and abiotic stress: Macaranga-ant
plants optimize investment in biotic defence. J. Exp. Bot., 52, 2057-2065.
MACHADO, S. R., MORELLATO, L. P. C., SAJO, M. G. & OLIVEIRA, P. S.
(2008) Morphological patterns of extrafloral nectaries in woody plant species
of the Brazilian cerrado. Plant Biology, 10, 660-673.
MAYER, V., SCHABER, D. & FRANZ HADACEK (2008) Volatiles of
myrmecophytic Piper plants signal stem tissue damage to inhabiting Pheidole
ant-partners. Journal of Ecology, 96, 962-970.
MCDONALD, T. L. & AMSTRUP, S. C. (2001) Estimation of Population Size Using
Open Capture-Recapture Models. Journal of Agricultural, Biological &
Environmental Statistics, 6, 206-220.
PALMER, T. M., STANTON, M. L., YOUNG, T. P., GOHEEN, J. R., PRINGLE, R.
M. & KARBAN, R. (2008) Breakdown of an Ant-Plant Mutualism Follows
the Loss of Large Herbivores from an African Savanna. Science, 319, 192-195.
PARACER, S. & AHMADIJIAN, V. (2000) Symbiosis: An Introduction to Biological
Associations, New York, Oxford University Press.
RAINE, N. E., WILLMER, P. & STONE, G. N. (2002) SPATIAL STRUCTURING
AND FLORAL AVOIDANCE BEHAVIOR PREVENT ANT &
POLLINATOR CONFLICT IN A MEXICAN ANT-ACACIA. Ecology, 83,
3086-3096.
RICO-GRAY, V., GARCÍA-FRANCO, J. G., PALACIOS-RIOS, M., ÍZ-
CASTELAZO, C., PARRA-TABLA, V. & NAVARRO, J. A. (1998)
Geographical and Seasonal Variation in the Richness of Ant-Plant Interactions
in Mexico. Biotropica, 30, 190-200.
SAGERS, C. L., GINGER, S. M. & EVANS, R. D. (2000) Carbon and nitrogen
isotopes trace nutrient exchange in an ant-plant mutualism. Oecologia, 123,
582-586.
SHENOY, M. & BORGES, R. (2008) A novel mutualism between an ant-plant and
its resident pollinator. Naturwissenschaften, 95, 61-65.
TILLBERG, C. V. (2004) Friend or foe? A behavioral and stable isotopic
investigation of an ant–plant symbiosis. Oecologia, 140, 506-515.
WARD, P. S. (1993) Systematic studies on Pseudomyrmex acacia-ants
(Hymenoptera: Formicidae: Pseudomyrmecinae). Journal of Hymenoptera
Research, 2, 117 - 168.
WHITTAKER, J. (1991) Effects of ants on temperate woodland trees. IN HUXLEY,
C. R. & CUTLER, D. F. (Eds.) Ant-plant interactions. Oxford, Oxford
University Press.