Behavioral plasticity in soldiers of Atta mexicana and its adaptive significance in urban environments

- by A Sunjian and Li H.

Sunjian A and Li H. (2005) Behavioral plasticity in soldiers of Atta mexicana and its adaptive significance in urban environments. Notes from Underground 11 (1)

(en español)

(revision date: February 10, 2004)

The major workers of many ant species have evolved as specialists for various tasks, including that of seed milling, food storage, and colony defence. In the highly polymorphic leaf-cutting genus Atta, the larger workers have been termed soldiers because it is widely acknowledged that these individuals are specialized solely for colony defence (Weber 1972; Wilson 1980a; Whitehouse and Jaffe 1996; Hughes and Goulson 2001). Nevertheless, there have been sporadic reports of cases where the soldiers engaged in other activities. Atta colombica majors are known to forage alongside smaller workers and cut the tough skin of fallen fruit (Wetterer 1995), Mintzer notes that Atta mexicana soldiers are "used to keep the foraging trails and tunnels clear by (re)moving large heavy twigs and pebbles, and they also are recruited to cut a few very tough food items" (per. comm), and even A. cephalotes soldiers may at times be used to carry very large berries (Slosberg 2004).
Majors clear a seed while a minor worker tries to hitch a ride. No minor workers were seen to ride on the very smooth seeds once they were being transported back to the nest.

A. mexicana is primarily present in Central and Northern Mexico, but this far-flung species can be found as far north as Arizona. During a ten day stay in Puerto Vallarta and Nuevo Vallarta, two beach resort towns on the western edge of central Mexico, the authors encountered numerous colonies of A. mexicana and filmed various colonies as they foraged and engaged in other daily activities. This article provides the first detailed reports on an extraordinary instance of behavioral plasticity in the soldiers of an A. mexicana colony filmed in the old downtown area of Puerto Vallarta, and discusses its significance with regards to the adaptation of Atta leafcutters to live in human-created habitats.

On the night of December 6, 2003, the authors encountered a foraging trail of A. mexicana at the intersection of Ignacio Vallarta and Francisa Rodriguez streets. Hundreds of ants were issuing from a crack on a very tall stone wall that rose up against a nearby hill, and massing around the fallen fruits of a nearby huamuchil tree (Pithecellobium dulce).

The fruit of this tree from the Legume family takes the form of an irregularly swollen, strongly twisted greenish pod, and usually carries 6-10 seeds. The flat black seeds are buried in an inner sweetish white pulp, are about 1 cm in diameter, and are oval to irregular in shape. The leafcutter ants were clustered around the fallen pods in dense masses, and the authors noted that the ants were intensely attracted to the black seeds. Workers of all sizes, including very large majors (those with head widths greater than 4mm), were involved in stripping the surrounding pulp from the seeds.

A black seed, once stripped from the pulp, was then surrounded by workers, all of whom tried to grasp the smooth surface of the seed in order to carry it back to the nest. However, because of its relatively heavy weight, irregular shape, and very smooth surface, the seed presented a difficult, if not impossible challenge, for most of the smaller workers. Although some small workers, including foragers with head widths less than 3mm, started to grasp and pull on the seeds, they did not persist in their efforts. On the other hand, the larger workers persisted for longer periods of time, and almost all the seeds were carried towards the nest by large foragers or large-headed majors, whose much greater head sizes allowed them to lift and balance the bulky seeds on their massive mandibles.
Five major workers trying to lift a seed. Smaller workers were frequently "squeezed out" by the mobs of majors that surrounded the seeds.

The method used by the majors to position and lift the seeds was identical to that used by foragers attempting to lift cut leaf pieces. An ant first tucked her head downwards and angled against the underside of the thorax, slid her mandibles down the object, then grasped it firmly and lifted her head, swinging the item above her. Even with their oversized heads (two sampled laden soldiers had head widths greater than 4.6 mm), some of the majors had difficulty carrying their burdens back to the nest. Several of the carriers walked slowly and stiffly on splayed legs, their smaller nestmates swirling around them like fast flowing current against flotsam, and once or twice, a laden major would stumble forwards or sideways.

The development of large urban and suburban environments is in evolutionary terms a very recent consequence of humanity's encroachment on tropical nature. Leafcutter ants in general seem to have greatly benefited from these human activities. For example, Atta cephalotes nest densities are much greater in human cleared environments than in primary forests (Jaffe and Vilela 1988). Densities of A. mexicana nests are also very high in the rapidly developing resort community of Nuevo Vallarta in Mexico (Sunjian and Li, 2005).

These man-made environments are in many ways simpler and less biologically diverse than natural habitats. However, at the same time, it could be argued that they represent areas with challenges and opportunities that are more rapidly fluctuating and patchy than those in nature. For example, a colony may stumble upon food thrown away by a passing pedestrian. This is an occurrence which will not occur regularly, nor would it necessarily happen in the same location.

Leafcutters may also face new challenges in these urban and suburban areas that are not normally present in natural environments. The lower trunks of many of the public trees in Puerto Vallarta and its environs have been decorated with a white, lime-containing paint. According to the locals, this serves to prevent the ants and other pests from damaging the trees, and there is some evidence that leafcutter ants are wary about foraging on these "protected" plants, at least when freshly-painted (pers obs). If effective, this would result in a severe narrowing of the potential targets for A. mexicana, and may force the colonies to adapt by seeking alternative sources of forage for their fungus gardens. Indeed, in addition to the seed-collecting A. mexicana colony, the authors also discovered another colony in the city's Isla Cuale that was rapidly mobilizing its large soldiers to haul in very large cereal pieces.
A major worker struggles to carry a bulky, smooth seed. Even with their oversized heads, some of the majors had difficulty carrying their burdens back to the nest.

Seen in this light, the expanded behavioral repertoire of A. mexicana soldiers in urbanized Puerto Vallarta is strongly adaptive in that it allows colonies with this phenotype to effectively exploit a much wider range of resources that typical foragers cannot easily handle. Unlike some myrmicines like Pheidologeton, a generalist swarm raider that forages on an extremely wide range of food items, Atta leafcutters have not mastered very efficient and rapid group transport and instead seem to emphasize the use of individual retrieval of leaf pieces and other vegetable material, although there is a strong correlation between the size of a leafcutter forager and the size and density of the loads it will carry, such that efficiency is maximized (Van Breda and Stradling 1994; Wetterer 1994).

If viewed from the perspective of the allometric space model postulated by Oster and Wilson (1978), the rapid encroachment of human civilization represents a significant increase (or at least reorganization) of the tasks faced by a leafcutter colony, and the greater behavioral flexibility of the soldiers is a very positive trait in this light. Holldobler and Wilson (1990) postulated that a colony can increase its coverage of all the potential tasks in the local environment via three paths: (1) by changing the allometric curve that describes the worker force and thus create new castes to deal with additional tasks; (2) by expanding the range of tasks that a worker can perform; and (3) by adding specific communication and cooperative behavior that allows the colony to accomplish tasks beyond the capabilities of individual members. Clearly in this case, the colony was able to exploit an unusual resource (large, bulky, smooth-skinned seeds) by the second route. Whether or not this behavioral plasticity represents an adaptive response to urbanization is very doubtful, and further studies of A. mexicana under more natural conditions is advisable.

Finally, there are several questions that derive from these observations and may be amenable to future studies.

  1. Is this behavioral plasticity in the majors and soldiers of the Puerto Vallarta colony a widespread phenomenon present in many other colonies?

    The authors observed another A. mexicana colony in the Rio Cuale area whose major workers also engaged in bringing large cereal pieces back to a foraging hole. Thus, this plasticity in behavior may be widespread in at least this species. The authors also observed what may be an instance of group transport in this colony, with media workers cooperating to bring back extremely large pieces of cereal. Unfortunately, no documentation of this remarkable phenomenon was undertaken.

  2. What is the mechanism that elicits this foraging behavior in the soldiers of this species?

    The authors observed that these workers were extremely attracted to the seeds and fallen pods, and that they frequently even tried to wrest away seeds that were already being carried by their nestmates. In many ant species, the behavioral repertoire of the majors are minimized when they are excluded from certain work by the presence of other castes, but this range of behavioral acts can be expanded by removal of the minor and media workers (Wilson,1984). In the case of A. mexicana, although some smaller workers participated in trying to lift the seeds, they did not persist and were frequently "squeezed out" by the mobs of majors that surrounded the seeds.

  3. Did the broadening of the behavioral repertoire of A. mexicana soldiers also result in a proportionate increase in the ratio of majors to smaller workers when compared to other Atta species?

    One of the results of the ergonomic theory of caste optimization is that the more specialized a caste, the less its numerical representation in the colony (Holldobler and Wilson 1990). Thus, A. mexicana colonies which have evolved a soldier caste with an expanded behavioral repertoire should have a corresponding increase in the proportion of soldiers compared to other smaller workers. For example, A. cephalotes majors seem to be more specialized than A. mexicana in that they primarily serve as defenders of the nest (Wetterer 1995). Thus, we would expect the proportion of major workers in A. mexicana in the colony to be greater than that of A. cephalotes soldiers.

QuickTime movie of majors foraging

A shortened and reduced movie segment that shows majors foraging is presented here. The movie is 16 MB in size and so it would be best to right click on the link and save it to your local hard drive before viewing with Apple's QuickTime viewer. High resolution and extended segments are available from the authors.

Literature Cited

Holldobler B and EO Wilson (1990) The ants. Belknap, Cambridge, Mass

Hughes WOH and D Goulson (2001) Polyethism and the importance of context in the alarm reaction of the grass-cutting ant, Atta capiguara. Behav Ecol Sociobiol 49:503-508

Jaffe K and E Vilela (1988) On nest densities of the leaf-cutting ant Atta cephalotes in tropical primary forests. Biotropica 21(3):234-236

Oster GF and EO Wilson (1978) Caste and Ecology in the Social Insects (Monographs in Population Biology, no. 12) Princeton University Press, Princeton, NJ

Sunjian A and H Li (2005). Atta mexicana in the resort community of Nuevo Vallarta, Mexico. Notes from Underground 11(1).

Slosberg P. (2004). Cybereef's Leafcutter Ants of Costa Rica . cybereef.com/leafcutters/

Van Breda J M and DJ Stradling (1994) Mechanisms affecting load size determination in Atta cephalotes L. (Hymenoptera: Formicidae). Insectes Sociaux. 41(4):423-434

Weber NA (1972) Gardening Ants: The Attines. Mem Am Phil Soc 92:1-146

Wetterer, J. K. (1995) Forager polymorphism and foraging ecology of the leaf-cutting ant, Atta colombica. Psyche 102: 133-147.

Wetterer JK (1994) Forager polymorphism, size-matching and load delivery in the leaf-cutting ant, Atta cephalotes. Ecological Entomology. 19(1):57-64.

Whitehouse MEA and K Jaffe (1996) Ant wars: combat strategies, territory and nest defense in the leaf-cutting ant Atta laevigata. Anim Behav 51:1207-1217

Wilson EO (1980) Caste and division of labor in leaf-cutter ants (Hymenoptera: Formicidae: Atta). I. The overall pattern in A.sexdens. Behav Ecol Sociobiol 7:143-156

Wilson EO (1984) The relation between caste ratios and division of labor in the ant genus Pheidole. Behav Ecol Sociobiol 16(2):89-98