Abstract

Behaviors range greatly in their complexities. Many animals also show types of social organization and just like the behaviors, social organization varies in it's complexity. Most social organization is an intricate web of complex behaviors which arose through years of existence, continually shaped by natural selection. Often social structure is associated with higher animals. However, insect behavior and social organization has formed and evolved to become extremely established. Of insect socialization, ants have proved to be masters of division of labor, cooperative interaction and cohesiveness. The behavior of the ants, which is the foundation of their social structure, has allowed them to radiate and occupy many different environmental niches. In connection with their widespread occurrence, ants have formed relationships with other living organisms. Along with some species of plants, specifically trees, ants have formed cooperative relationships. These mutualistic existences have helped both ant and plant species to further flourish. Ant-plant interactions allow both to benefit. Ants provide protection against a number of threats to the plant and in return the plant provides a home and often food sources for the ants. Furthermore, ants often provide other services for the plant such as natural grooming and can also provide food sources for the plant. The ant-plant interaction has existed for so many years that often the species become dependent upon each other in order to exist.

Ant-plant interactions have been widely studied over the years. Much work has been put into understanding the relationships of the ants and plants. Also, a great deal of research has been done on the exact consequences that result from such mutualistic interactions. The association of ants and plants is a long standing one. This association
has been acted upon by natural selection to give both ant and plant optimal chances of survival. Ant-plant interactions are extremely complex. A single tree can be inhabited by one or multiple species of ants, obligates and non-obligates, with each species exhibiting different and often unique behavior. Just like the variation among inhabitants, there is a variation in benefits and costs for each mutualist. I will discuss 1) the evolution of the ant-plant mutualism, 2) the benefits to each mutualist, 3)herbivory and leaf age as an important indicator to plant-ant attention, 4) spatial and temporal variation in defensive behavior, and 5) the vulnerability of the ant-plant mutualism.

Evolution of ant-plant mutualisms

The evolution of the ant-plant interaction has been selected for as a way to increase the fitness of both ant and plant species. Research suggests that Acacia cornigera evolved traits from purely morphological (e.g., swollen thorns) to purely behavioral and physiological (e.g., aggressiveness, year-round leaf production), with these traits all being passed on phenotypically (Janzen 1966). Furthermore, the coevolution of the ant-plant interaction is the product of an evolutionary feedback system. This system has two basic requirements. One of the organisms must supply the other with a provision, and the receiving organism must possess the ability to favor the donating genotype of the donor organism (Janzen 1966). An example might be the ant removing an insect and receiving a provision, by increasing the number of insects removed the ant receives more provisions and the behavior becomes more induced, passing on the insect-removing behavior genotypically. Furthermore, the trait of extreme susceptibility to insect herbivory is transmitted genotypically by the acacia. Thus complete and thorough occupance by ants is necessary (Janzen 1966). The obligation of acacia to be infested by the ant Pseudomyrmex ferruginea for survival, is yet another example of the extended and clear coevolution between ants and plants.

Benefits of Mutualism

Many benefits arise through ant-plant interactions, but there are some costs that each mutualist must pay in order to interact with the other. The benefits and costs vary across the many ant and plant species. Ant-Acacia trees provide the Psuedomyrmex ants with shelter in the form of large hollow thorns and nutrition from the enlarged foliar nectaries and Beltian bodies (Cronin 1998, Janzen 1966). The year round leaf production enables the plant to produce Beltian bodies for ant consumption. The Beltian bodies are rich in proteins and lipids. The ant colony often feeds exclusively on the food bodies and use the nectaries to feed the ant brood. The swollen thorns of the acacias are normally occupied by the ants where they raise their brood (Janzen 1966). The ants, in return for the plants provisions, vigorously defend their host and colony from most herbivores and neighboring vegetation (Cronin 1998, Janzen 1966, 1969). Furthermore, the aggressiveness on both herbivores and neighboring plant species is dependent on which Psuedomyrmex ant species are inhabiting the acacias. Interestingly, acacias often have multiple species of Psuedomyrmex ants inhabiting them at any particular time (Cronin 1998). The Ant-Cecropia trees produce Mullerian bodes which the Azteca ants feed on (Agrawal 1998, Downhower 1975, Janzen 1969,1973). The ants again feed on the protein-lipid rich food body. The Cecropia trees also provide the ants hollowing within the tree trunks (Agrawal 1998, Janzen 1969, 1973). Within these hollows Azteca ants, like Psuedomyrmex ants and Acacia trees, use the area to raise and house their broods. The plants benefit from the ants in that the ants protect the Cecropia trees from herbivores and defend the host plant and colony from neighboring vegetation (Janzen 1969). Furthermore, the association between the Cecropia trees and the Azteca ants is an obligate relation-
ship. Removal of the ants seriously reduces the fitness of the plant an ultimately the plant dies (Agrawal 1998).

Ant-Piper trees also produce food bodies which Peidole ants feed on. These food bodies like the ones found in Acacia and Cecropia , are rich in proteins and lipids (Letourneau 1990, Risch 1981). Interestingly, the production of the food bodies only occur when ants are present. In contrast, the Acacia and Cecropia food bodies are produced in the presence and absence of their perspective ant species. However, once again the Peidole ants are provided a domicile in which they can raise their brood (Risch 1981). The Peidole ants provide protection against herbivory and neighboring vegetation (Letourneau 1990, Risch 1981).

Ant-Tachigali trees differ from all the other ant-plants in that Tachigali do not produce food bodies for the ants which inhabit them. Instead of food bodies the trees have coccids which suck the phloem contents transferring nutrients indirectly from the host plant to the ant colony. The Psuedomyrmex ants are limited in colonial size by the amount of domatia the trees provide. In return for the plants provisions, the ants protect the trees against herbivores and neighboring vegetation. Research indicates that the Psuedomyrmex ants are an important aspect of the Tachigali trees and that in the ants absence the fitness of the trees diminishes greatly (Fonseca 1994).

The ant defenses sequestered by all the plant species with ant-plant interactions is a relatively uncostly behavior. Often the ant-plant species have relatively mild secondary compounds or lack them completely. With the reduction in secondary compounds the plants do not suffer from self-intoxication nor do they expend the energy and resources to keep secondary compounds readily available. The ant defense of the ant-plant is an inducible defense (Agrawal 1998, Cronin 1998). Inducible defenses allow costs of defenses to be deferred until enemies have been detected, at which time the costs of the defense are offset by the protection received (Cronin 1998). The ant defenses are functionally analogous to the secondary compounds of other plants (Agrawal 1998, Cronin 1998, Janzen 1969).

Herbivory and leaf age as an important indicator to plant-ant attention

Leaf age is of major importance when herbivory and plant life history are considered. The amount of photosynthate that is produced is proportional to the fitness of young leaves. Furthermore, the life expectancy for a sapling or young plant is much lower than the life expectancy of an older plant. Mature leaves are expected to have a lower grazing rate than young leaves. The lower grazing rate of the mature leaves can be associated with toughness which decreases digestibility. Some substances that reduce digestibility are tannins and resins. Young expanding leaves are nutritious and presumably are not heavily defended by chemicals especially not substances which weaken digestibility (Coley 1980).

Often younger plants are occupied by multiple colonies of plant-ants. In comparison older trees are often inhabited by a single colony of plant-ants. The fragility of the saplings and young trees requires a large investment in defense to increase the plants fitness. The high occupancy of saplings and young trees is an indicator of the importance of younger plants being thoroughly infested by the mutualistic ants (Longino 1989).

Cecropia peltata is an ant-plant that associates with ants from the genera Crematogaster or Azteca . Vertical growth is proportional to the surface area of the leaves occurring in the crown of the plant. Research suggests that the majority of the ants which occur in Cecropia peltata are found patrolling the crown of the trees. Furthermore, herbivory appears to be less intense on the top one third of the crown. Ant accumulation is greatest in the top one third of the crown when herbivory is occurring. In addition, the leaves of the top one third of the crown, which are the youngest, are of most value in amount of photosynthate produced (Downhower 1975).

Tachigali myrmecophila is an Amazonian canopy tree inhabited by the stinging ant Psuedomyrmex concolor . The trees are habituated by herbivores. The herbivores can display extensive damage on the trees. Research has indicated the importance of infestation of the mutualist Psuedomyrmex concolor . Tachigali myrmecophila saplings are shade-tolerant, surviving in a suppressed state for several years. Coley et al . (1985) formulated the availability hypothesis. The availability hypothesis predicts that upon resource shortage the plants should invest strongly in defense. The consequences of such an investment in defense would be increased leaf longevity and limited growth rate. The research suggests just that. The interaction between leaf maturity and the group suggests that Psuedomyrmex concolor pushes herbivores from the top to the lower portions of the plant. This behavior helps to support the valuable young leaves. Upon the removal of the ants, herbivory of the plant's young leaves doubled (Fonseca 1994). The aggressive defense of saplings and young leaves is important to the inclusive fitness of both ant and plant.

Spatial and Temporal variation in defensive behavior

Because many ant-plants are inhabited by multiple species of ants, spatial and temporal variation in defensive behavior is important when considering herbivory. Ant-Cecropia trees are typically inhabited by at least four species of Azteca , each of them well represented in terms of relative abundance. This phenomenon is most likely caused by the plants being a limited resource for the ants. However, this condition is favorable for the Cecropia plants (Longino 1989). Each species of ant preforms any number of unique behaviors. Such behaviors can help diminish herbivory by adding to the unpredictability of the ant-plant defense.

The ant-plant Acacia collinsii has a mutualistic relationship with three species of stinging ants, Psuedomyrmex spinicola, P. nigrocinctus, and P. flavicornis . Psuedomyrmex spinicola/P. nigrocinctus are more active in the morning while P. flavicornis is more active in the afternoon. Such research suggests that P. spinicola/P. nigrocinctus ants are the better mutualists in the morning hours while P. flavicornis ants are the better mutualists in the evening. Furthermore, each species of plant-ant patrolled the younger leaves of their perspective areas the most. The three species of Psuedomyrmex ants have similar levels of patrolling activity and post-disturbance activity. The ants respond to the presence of a herbivore with similar swiftness, and attack the herbivore with similar aggressiveness. The research suggests that the traits of spatial and temporal variation reduce the likelihood of plant defenses undergoing manipulation by herbivores thus increasing the fitness of the plants and ants.

Vulnerability of the ant-plant mutualism

The mutualistic interaction of ants and plants is not an impenetrable fortress. There are other arthropods, herps, aves and mammals which prey on ant species including plant-ants. One such example is the case of a beetle that not only feeds on a plant-ant but the beetle's mimicry can stimulate food body production by the ant-plant. Phyllobaenus beetles are parasites of the Piper ant-plant mutualism. Research shows that when Pheidole bicornis ants are present, the predatory Phyllobaenus beetles eventually destroy the colony and feed on the brood. Because Piper -ant plants only produce the protein-lipid rich food bodies in the presence of ants, trees without an established ant colony would be expected to be void of any food body production. However, the research shows that in the absence of the ants the predatory beetles feed on the food bodies and that the plant continues to produce the morsels. Some virgin Pipers , trees never before inhabited by ants, had food body production. In such cases Phyllobaenus larvae were found inhabiting the tree, evidence suggesting Phyllobaenus' ability to stimulate food production in the absence of Pheidole bicornis ants. Whether the beetles destroy ant colony and feed on the food bodies or the beetles parasitize and feed only on food bodies, the fitness of both Pheidole bicornis and Piper trees are greatly diminished (Letourneau 1990).

In a few rare instances, the ant-plant mutualism has disassociated. Plants which were once mutualistic no longer interact with the ants. Some high elevation mainland, one low elevation mainland and many island Cecropia trees lack ant association. Complex mutualisms can evolutionarily disintegrate without the loss of both partners if the proper habitats are available. All of the antless Cecropia trees lack food bodies and the ability to produce them. The inability to produce food bodies to facilitate ant-plant interactions was most likely caused by reduced competition and herbivory in island and high elevation populations. There is also the possibility of increased secondary compounds in the antless Cecropia plants. The one low elevation mainland antless species is expected to have originated in the higher elevations and then reinvaded the lower elevations (Janzen 1973).

The ant-plant mutualism is an interaction that is in continual flux. The fitness of both species are dependent on both internal and external influences. The interaction only exists because of the increase in both species fitness. When either species can increase it's fitness without the association, the mutualism degrades. The complexity of the an-plant mutualism is vast. Multiple species of ants and plants take part in such interactions. The benefits that each species experience are simple and necessary. What seems logical for the spatial and temporal differences in defense are clearly essential for the overall fitness of both species. The mutualism of ants and plants is not the end of the road for the species involved, but rather the current spectacular result of the constant influence of evolutionary processes.

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