The Ants Chapter 16

CHAPTER 16. THE ARMY ANTS

No spectacle of the tropical world is more exciting and mystifying than that of a colony of army ants on the march. In his book, Ants, Their Structure, Development and Behavior, Wheeler expressed its poetry in the following way: "The driver and legionary ants are the Huns and Tartars of the insect world.  Their vast armies of blind but exquisitely coöperating and highly polymorphic workers filled with an insatiable carnivorous appetite and a longing for perennial migrations, accompanied by a motley host of weird myrmecophilous camp-followers and concealing the nuptials of their strange, fertile castes, and the rearing of their young, in the inaccessible penetralia of the soil--all suggest to the observer who first comes upon these insects in some tropical thicket, the existence of a subtle, relentless and uncanny agency, directing and permeating all their activities."

The swarm raiders
Eciton burchellii is one of the best understood of the army ants. This big, conspicuous species is abundant in humid lowland forests from Brazil and Peru north to southern Mexico (Borgmeier, 1955). Its marauding workers, together with those of other species of Eciton, are well known to native peoples by such local names as padicours, tuocas, tepeguas, and soldados. In English they are called army ants, as well as foraging ants, legionary ants, soldier ants, and visiting ants. These insects have understandably been a prime target for study by naturalists for a long time, from Lund (1831) through Bates, Belt, von Ihering, Müller, and Sumichrast in the last century to Beebe, Wheeler, and many others in more recent times. But it was T. C. Schneirla (1933-1971) who, by conducting patient studies over virtually his entire career, first unraveled the complex behavior and life cycle of this and other species of Eciton. His results were confirmed and greatly extended in rich studies conducted by C. W. Rettenmeyer (1963a).

A day in the life of an Eciton burchellii colony seen through the eyes of Schneirla and Rettenmeyer begins at dawn, as the first light suffuses the heavily shaded forest floor. At this moment the colony is in “bivouac,” meaning that it is temporarily camped in a more or less exposed position. The sites most favored for bivouacs are the spaces between the buttresses of forest trees and beneath fallen tree trunks (see Figure 16-1 and Plate 20) or any sheltered spot along the trunks and main branches of standing trees to a height of twenty meters or more above the ground. Most of the shelter for the queen and immature forms is provided by the bodies of the workers themselves. As they gather to form the bivouac, they link their legs and bodies together with their strong tarsal claws (Figure 16-2), forming chains and nets of their own bodies that accumulate layer upon interlocking layer until finally the entire worker force comprises a solid cylindrical or ellipsoidal mass up to a meter across. For this reason Schneirla and others have spoken of the ant swarm itself as the “bivouac.” Between 150,000 and 700,000 workers are present. Toward the center of the mass are found thousands of immature forms, a single mother queen, and, for a brief interval in the dry season, a thousand or so males and several virgin queens. The entire dark-brown conglomerate exudes a musky, somewhat fetid odor.

When the light level around the ants exceeds about 0.5 lux, the bivouac begins to dissolve. The chains and clusters break up and tumble down into a churning mass on the ground. As the pressure builds, the mass flows outward in all directions. Then a raiding column emerges along the path of least resistance and grows away from the bivouac at a rate of up to 20 m an hour. No leaders take command of the raiding column. Instead, workers finding themselves in the van press forward for a few centimeters and then wheel back into the throng behind them, to be supplanted immediately by others who extend the march a little farther. As the workers run on to new ground, they lay down small quantities of chemical trail substances from the tips of their abdomens, originating in the hindgut and probably also in the pygidial gland (Hölldobler and Engel, 1978), guiding others forward. Workers encountering prey lay extra recruitment trails that draw nestmates differentially in that direction (Chadab and Rettenmeyer, 1975). A loose organization emerges in the columns, based on behavioral differences among the castes. The smaller and medium-sized workers race along the chemical trails and extend it at the point, while the larger, clumsier soldiers, unable to keep a secure footing among their nestmates, travel for the most part on either side. The location of the Eciton soldiers misled early observers into concluding that they are the leaders. As Thomas Belt put it, “Here and there one of the light-colored officers moves backwards and forwards directing the columns.” Actually the soldiers, with their large heads and exceptionally long, sickle-shaped mandibles, have relatively little control over their nestmates and serve instead almost exclusively as a defense force. The minimas and medias, bearing shorter, clamp-shaped mandibles, are the generalists. They capture and transport the prey, choose the bivouac sites, and care for the brood and queen. Workers often work in teams, with large medias serving as porters. These specialists initiate the transport of large prey items and are joined by workers of equal or smaller size. The teams accomplish their task with greater energetic efficiency than if they cut the prey into small pieces and carried them individually (Franks, 1986; see Figure 8-48).

Eciton burchellii has an unusual mode of hunting even for an army ant. It is a “swarm raider,” which means that the foraging workers spread out into a fan-shaped swarm with a broad front. Most other army ant species are “column raiders,” pressing outward along narrow dendritic odor trails in the pattern exemplified in Figure 16-3. Schneirla (1956b) has described a typical raid as follows:

For an Eciton burchellii raid nearing the height of its development in swarming, picture a rectangular body of 15 meters or more in width and 1 to 2 meters in depth, made up of many tens of thousands of scurrying reddish-black individuals, which as a mass manages to move broadside ahead in a fairly direct path. When it starts to develop at dawn, the foray at first has no particular direction, but in the course of time one section acquires a direction through a more rapid advance of its members and soon drains in the other radial expansions. Thereafter this growing mass holds its initial direction in an approximate manner through the pressure of ants arriving in rear columns from the direction of the bivouac. The steady advance in a principal direction, usually with not more than 15° deviation to either side, indicates a considerable degree of internal organization, notwithstanding the chaos and confusion that seem to prevail within the advancing mass. But organization does exist, indicated not only by the maintenance of a general direction but also by the occurrence of flanking movements of limited scope, alternately to right and left, at intervals of 5 to 20 minutes depending on the size of the swarm.

The huge sorties of burchellii in particular bring disaster to practically all animal life that lies in their path and fails to escape. Their normal bag includes tarantulas, scorpions, beetles, roaches, grasshoppers, and the adults and broods of other ants and many forest insects; few evade the dragnet. I have seen snakes, lizards, and nestling birds killed on various occasions; undoubtedly a larger vertebrate which, because of injury or for some other reason, could not run off, would be killed by stinging or asphyxiation. But lacking a cutting or shearing edge on their mandibles, unlike their African relatives the “driver ants,” these tropical American swarmers cannot tear down their occasional vertebrate victims. Arthropods, such as ticks, escape through their excitatory secretions, stick insects through repellent chemicals, as tests show, as well as through tonic immobility. The swarmers react to movement in particular as well as to the scent of their booty, and a motionless insect has some chance of escaping them. Common exceptions, which may enjoy almost a community invulnerability in many cases, include termites and Azteca ants in their bulb nests in trees, army ants of their own and other species both on raiding parties and in their bivouacs, and leaf-cutter ants in the larger mound communities; in various ways these often manage to fight off or somehow repel the swarmers.

The approach of the massive burchellii attack is heralded by three types of sound effect from very different sources. There is a kind of foundation noise from the rattling and rustling of leaves and vegetation as the ants seethe along and a screen of agitated small life is flushed out. This fuses with related sounds such as an irregular staccato produced in the random movements of jumping insects knocking against leaves and wood. This noise, more or less continuous, beats on the ears of an observer until it acquires a distinctive meaning almost as the collective death rattle of the countless victims. When this composite sound is muffled after a rain, as the swarm moves through soaked and heavily dripping vegetation, there is an uncanny effect of inappropriate silence.

Another characteristic accompaniment of the swarm raid is the loud and variable buzzing of the scattered crowd of flies of various species, some types hovering, circling, or darting just ahead of the advancing fringe of the swarm, others over the swarm itself or over the fan of columns behind. To the general hum are added irregular short notes of higher pitch as individuals or small groups of flies swoop down suddenly here or there upon some probable victim of the ants which has suddenly burst into view. . . No part of the prosaic clatter, but impressive solo effects, are the occasional calls of antbirds. One first catches from a distance the beautiful crescendo of the bicolored antbird, then closer to the scene of action the characteristic low twittering notes of the antwren and other common frequenters of the raid.

If you wish to find a colony of swarm raiders in Central or South America, the quickest way is to walk quietly through a tropical forest in the middle of the morning, listening. For long intervals the only birds you might hear are in the distance and mostly in the canopy. Then, as Johnson (1954) has expressed it, comes a “chirring, twittering, and piping” of antbirds close to the ground. Mingled in is the murmur or hissing caused by the frantic movements of countless insects trying to escape the raiders, and the buzzing of parasitic flies. Very soon you will see the ants themselves marching in a broad front, hundreds of thousands streaming forward as though drawn toward some goal just out of sight in the forest shadows. Also present may be ithomiine butterflies, which fly over the leading edge of the swarm. First noticed by Drummond (1976), the butterflies are now known to feed on the droppings of the antbirds (Ray and Andrews, 1980; Andrews, 1983).

On Barro Colorado Island, Panama, where Schneirla conducted most of his studies, the antbirds normally follow only the raids of Eciton burchellii and those of another common swarm-raider, Labidus praedator. They pay no attention to the less conspicuous forays of Eciton hamatum, Eciton dulcium, Eciton vagans, and other column-raiding army ants. There are at least ten species of antbirds on Barro Colorado Island, all members of the family Formicariidae. They feed principally on the insects and other arthropods flushed by the approaching burchellii swarms (Johnson, 1954; Willis, 1967). Although a specimen of Neomorphus geoffroyi has been recorded with its stomach stuffed with burchellii workers, most species appear to avoid the ants completely or at most consume them by accident while swallowing other food.

As one might anticipate from these accounts, the burchellii colonies and their efficient camp followers have a profound effect on the faunas of those particular parts of the forest over which the swarms pass. E. C. Williams (1941), for example, noted a sharp depletion of the arthropods at spots on the forest floor where a swarm had struck the previous day. On Barro Colorado Island, which has an area of approximately 17 km2, there exist only about 50 burchellii colonies at any one time. Since each colony travels at most 100 to 200 m every day (and not at all on about half the days), the collective population of burchellii colonies raids only a minute fraction of the island's surface in the course of one day, or even in the course of one week. But the strikes are probably frequent enough during the course of months to have a significant effect on the composition and age structure of the colonies of ants and social wasps.

The food supply is quickly and drastically reduced in the immediate vicinity of each colony. Early writers, especially Müller (1886) and Vosseler (1905), jumped to the reasonable conclusion that army ant colonies change their bivouac sites whenever the surrounding food supply is exhausted. At an early stage of his work, however, Schneirla (1933b, 1938) discovered that the emigrations are subject to an endogenous, precisely rhythmic control unconnected to the immediate food supply. He proceeded to demonstrate that each Eciton colony alternates between a statary phase, in which it remains at the same bivouac site for as long as two to three weeks, and a nomadic phase, in which it moves to a new bivouac site at the close of each day, also for a period of two to three weeks. (The nomadic phase is better called the migratory phase, since army ants are migratory hunters rather than nomads in the strict sense. That is, they move periodically to areas of fresh prey, rather than guide herds to fresh pastures in the manner of true nomads.  True nomadism is known among ants only in certain Malaysian species of Hypoclinea [see Chapter 13].)  The basic Eciton cycle is summarized in Figure 16-4. Its key feature is the correlation between the reproductive cycle, in which broods of workers are reared in periodic batches, and the behavior cycle, consisting of the alternation of the statary and migratory phases. The single most important feature of Eciton biology to bear in mind in trying to grasp this rather complex relation is the remarkable degree to which development is synchronized within each successive brood. The ovaries of the queen begin developing rapidly when the colony enters the statary phase, and within a week her abdomen is greatly swollen by 55,000 to 66,000 eggs (Figure 16-5). Then, in a burst of prodigious labor lasting for several days in the middle of the statary period, the queen lays from 100,000 to 300,000 eggs. By the end of the third and final week of the statary period, larvae hatch, again all within a few days of each other. A few days later the “callow” workers (so called because they are at first weak and lightly pigmented) emerge from the cocoons. The sudden appearance of tens of thousands of new adult workers has a galvanic effect on their older sisters. The general level of activity increases, the size and intensity of the swarm raids grow, and the colony starts emigrating at the end of each day's marauding. In short, the colony enters the migratory phase. The migratory phase itself continues as long as the brood initiated during the previous statary period remains in the larval stage. As soon as the larvae pupate, however, the intensity of the raids diminishes, the emigrations cease, and the colony (by definition) passes into the next statary phase.

The emigration is a dramatic event requiring sudden complex behavioral changes on the part of all adult members of the Eciton colony. At dusk or slightly before workers stop carrying food into the old bivouac and start carrying it, along with their own larvae, in an outward direction to some new bivouac site along the pheromone-impregnated trails (Figure 16-6). Eventually, usually after most of the larvae have been transported to the site, the queen herself makes the journey. This event usually transpires between 8:00 and 10:00 p.m., well after nightfall. Just before the queen emerges from the bivouac, the workers on the trail nearby become distinctly more excited, and the column of running workers thickens beyond its usual width of 2 to 3 cm, soon widening to as much as 15 cm. Suddenly the queen appears in the thickest part. As she runs along she is crowded in by the “retinue,” a shifting mob consisting of an unusual number of soldiers and darkly colored, unladen smaller workers. The members of the retinue jostle her, press in underfoot, climb up on her back, and at times literally envelop her body in a solid mass. But, even with this encumbrance, the queen moves along easily to the new bivouac site. She is guided by the odor trail and can follow it all by herself even if the surrounding workers are taken away. After passage the emigration tapers off, and it is usually finished by midnight. If the column is disturbed near the queen, she stops and is swiftly covered by a blanket of protecting workers. All New World army ants employ retinues during emigrations ready to react this way. The largest are formed by Eciton burchellii and other species that travel aboveground and hence are most exposed to predators (Rettenmeyer et al., 1978).

The activity cycle of Eciton colonies is truly endogenous. It is not linked to any known astronomical rhythm or weather event. It continues at an even tempo month after month, in both wet and dry seasons throughout the entire year. Propelled by the daily emigrations of the migratory phase, the colony drifts perpetually back and forth over the forest floor (Figure 16-7). The results of experiments performed by Schneirla indicate that the phases of the activity cycle are determined by the stages of development of the brood and their effect on worker behavior. When he deprived Eciton colonies in the early migratory phase of their callow workers, they lapsed into the relatively lethargic state characteristic of the statary phase, and emigrations ceased. Migratory behavior was not resumed until the larvae present at the start of the experiments had grown much larger and more active. In order to test further the role of larvae in the activation of the workers, Schneirla divided colony fragments into two parts of equal size, one part with larvae and the other without. Those workers left with larvae showed much greater continuous activity.

These results, while provocative, are not decisive and at best solve only half the problem. For if the activity cycle is controlled by the reproductive cycle, what controls the reproductive cycle? The logical place to look would seem to be the queen. By her astonishing capacity to lay all of her eggs in one brief burst, she creates the synchronization of brood development, which is the essential feature for the colonial control of the activity cycle. At first Schneirla (1944) concluded that this reproductive effort by the queen is the “pace-maker,” thus implying that the queen herself is the seat of an endogenous rhythm. Later, however, Schneirla (1949b, 1956b) modified his hypothesis by viewing the queen and her colony as reciprocally donating elements in an oscillating system:

When each successive brood approaches larval maturity, the social-stimulative effect upon workers nears its peak. The workers thus energize and carry out some of the greatest raids in the nomadic phase, with their by-product larger and larger quantities of booty in the bivouac. But our histological studies show that, at the same time, more and more of the larvae (the largest first of all) soon reduce their feeding to zero as they begin to spin their cocoons. Thus in the last few days of each nomadic phase a food surplus inevitably arises. At this time the queen apparently begins to feed voraciously. It is probable that the queen does not overfeed automatically in the presence of plenty, but that she is started and maintained in the process by an augmented stimulation from the greatly enlivened worker population. Within the last few days of each nomadic phase, the queen's gaster begins to swell increasingly, first of all from a recrudescence of the fat bodies, then from an accelerating maturation of eggs. The overfeeding evidently continues into the statary phase, when, with colony food consumption greatly reduced after enclosure of the brood, smaller raids evidently bring in sufficient food to support the processes until the queen becomes maximally physogastric. These occurrences, which are regular and precise events in every Eciton colony, are adequate to prepare the queen for the massive egg-laying operation which begins about one week after the nomadic phase has ended.

While this interpretation makes a pretty story, it is constructed with fragments of very circumstantial evidence. The crucial question is unanswered as to whether the queen really is stimulated to feed in excess by the greater abundance of food or at least by the higher intensity of worker activity associated with the food, as Schneirla posited, or whether her increased feeding is timed by some other, undetermined physiological event. Since work on Eciton physiology is still virtually nonexistent, and experimental evidence of any kind very sparse, one can do no more than reflect on these possibilities as competing hypotheses.

Another question of considerable interest, added to the inducement of queen oogenesis, is the stimulus that triggers the onset of the migratory phase. According to Schneirla's theory of brood stimulation (actually a hypothesis), the migratory phase is initiated when workers become excited by the near-simultaneous eclosion of new, callow workers from the pupae. Migration is sustained thereafter by stimulation from the growing larvae. As illustrated in Figure 16-4, the mass eclosion at the start of the migratory phase coincides with the hatching of the egg mass. We may then ask which event, adult eclosion from the pupa or egg hatching, triggers the migratory phase? In an ingenious experiment conducted on Neivamyrmex nigrescens, Topoff et al. (1980) removed the larval brood of an early migratory colony and replaced it with the pupal brood of an early statary colony. As a result, the pupae eclosed well before the next batch of eggs laid by the host colony hatched, with the result that for several days the host colony was occupied by newly eclosed, callow workers but no larvae. It commenced its next migratory phase nonetheless, demonstrating that newly emerged adults are sufficient by themselves to drive this segment of the army-ant cycle.

Very little is known concerning the actual communicative stimuli that mediate the activity cycles. In his voluminous theoretical writings on the subject, Schneirla often spoke of “trophallaxis” as the driving force of the cycles of army ants, but it is clear that he meant this term to be virtually synonymous with “communication” in the broadest sense. Apparently he had no clear ideas about the nature of the signals utilized. In earlier articles he attributed much of the stimulative effect of the larvae to their “squirming”; later he stressed the probable existence of pheromones as well. But these speculations were based almost entirely on observations of the more obvious outward signs of communication, a level of study usually inadequate to distinguish even the sensory modalities employed in communication with insect colonies and unlikely to identify the signals employed. Lappano (1958) discovered that the labial glands of burchellii larvae become fully functional on the eighth or ninth migratory day, about the time raiding activity reaches its peak. She concluded that the labial glands are “probably” producing a pheromone that excites the worker. But again, the only evidence available is the stated coincidence in time of the two events. Our lack of knowledge of the semiotic basis of the Eciton cycle is due simply to the lack of any serious attempt to obtain it. This interesting subject does not seem likely to resist sustained experimental study; any such effort in the future is likely to yield exceptionally interesting results.

In his classic writings Schneirla was inadvertently misled by his failure to distinguish consistently between the ultimate causation and the proximate causation of the army-ant cycle. It is possible and even likely that the adaptive value, hence the ultimate causation, is the additional food made available to the colony when it emigrates frequently. However, biological systems often evolve so as to rely on endogenous rhythms to make the needed changes, rather than on a close reading of the environment from day to day. Put another way, the flush of callow workers becomes the token signal to the workers to initiate daily emigrations. They are the proximate cause of the emigrations, but the ultimate cause--the advantage emigrations give to emigration-prone genotypes in the ant population--remains the improved food supply. Although Schneirla occasionally mentioned that food availability might have been an important factor in the evolution of emigrations (1944, 1957b), the idea played no important role in his theoretical interpretation. After he had demonstrated the endogenous nature of the cycle, and its control by synchronous brood development, he dismissed the role of food depletion. The emigrations, he repeatedly asserted, are caused by the appearance of callow workers and the older larvae; they are not caused by food shortage. He meant only that food shortages are not the proximate cause.

In his culminating synthesis, however, Schneirla (1971) provided a more balanced view of evolution and physiological mechanisms. Toward the end of his life, he also learned that food shortages are in fact among the proximate controls, at least to a minor degree in some army ant species. In his last field study, on the small Asian army ant Aenictus, he discovered that short-term variation in colony activity depends on the “alimentary condition prevalent in the brood” (Schneirla and Reyes, 1969). To be specific, the ants appear to emigrate more often when their food supply runs low. Topoff and Mirenda (1980a,b) later tested the impact of food supply on emigrations in Neivamyrmex nigrescens by a series of experiments. This was made possible by their feat of culturing army ant colonies in the laboratory long enough to follow the brood cycle under controlled conditions. Two colonies overfed with prey emigrated on only 28 percent of the days during the migratory phase of the cycle, while two underfed colonies emigrated on 62 percent of the migratory days. It is now clear that although Neivamyrmex colonies follow an endogenous cycle of roughly the Eciton type (see Table 16-2), the tempo of their migratory phase is strongly affected by the amount of food they harvest. The complex interactions mediating raiding and emigrations in ecitonine army ants have been reviewed by Topoff (1984).

To summarize very briefly to this point, the colonies of Eciton and at least some other army ant species follow an endogenous cycle as Schneirla described it. The migratory phase is triggered at least in part by the emergence of new, callow adult workers. It is quite possible that the cycle was put in place genetically and is kept there through natural selection by the advantage it gives in overcoming food shortages. The frequency of raids is also fine-tuned in at least one species (Neivamyrmex nigrescens) by the day-to-day availability of food.

Colony multiplication in Eciton, first elucidated by Schneirla and R. Z. Brown (1950, 1952), is a highly specialized and ponderous operation. Through most of the year the mother queen is the paramount center of attraction for the workers, even when she is in competition with the mature worker larvae toward the close of each migratory phase. By serving as the focal point of the aggregating workers, she literally holds the colony together. The situation changes drastically, however, when the annual sexual brood is produced early in the dry season. This kind of brood contains no workers, but, in Eciton hamatum at least, it consists of about 1,500 males and 6 new queens. Even when the sexual larvae are still very young, a large fraction of the worker force becomes affiliated with the brood as opposed to the mother queen. By the time the larvae are nearly mature, the bivouac can be found to consist of two approximately equal zones: a brood-free zone containing the queen and her affiliated workers, and a zone in which the rest of the workers hold the sexual brood. The colony has not yet split in any overt manner, but important behavioral differences between the two sections do exist. For example, if the queen is removed for a few hours at a time, she is readily accepted back into the brood-free zone from which she originated, but she is rejected by workers belonging to the other zone. Also, there is evidence that workers from the queen zone cannibalize brood from the other zone when they contact them.

The young queens are the first members of the sexual brood to emerge from the cocoons. The workers cluster excitedly over them, paying closest attention to the first one or two to appear (see Figure 16-8). Several days later the new adult males emerge from their cocoons. This event energizes the colony, sets off a maximum raid followed by emigration, and at last splits the bivouac. Raids are conducted along two radial trails from the old bivouac site. As they intensify during the day, the young queens and their nuclei of workers move out along one of the trails, while the old queen with her nucleus moves out along the other. When the derivative swarm begins to cluster at the new bivouac site, only one of the virgin queens is able to make the journey to it. The others are held back by the clinging and clustering of small groups of workers. They are, to use Schneirla's expression, “sealed off” from the rest of the daughter colony. Eventually they are abandoned and left to die. Now there exist two colonies: one containing the old queen; the other, the successful virgin, daughter queen. In a minority of cases the old queen is also superseded. That is, the old queen herself falls victim to the sealing-off operation, leaving both of the two daughter colonies with new virgin queens. This presumably happens most often when the health and attractive power of the old queen begin to fail prior to colony fission. The maximum age of the Eciton queen is not known, but is believed to be relatively great for an insect; a marked queen of Eciton burchellii, for example, was recovered by Rettenmeyer after a period of four and a half years. The males, in contrast, enjoy only one to three weeks of adult existence. Shortly after their emergence they depart on flights away from the home bivouac in search of other colonies. Their bodies are heavily laden with exocrine glands resembling those of the queens. The new queens are fecundated within a few days of their emergence, and almost all of the males disappear within three weeks after that. Rettenmeyer (1963a) has described an actual mating, and he has presented evidence that a queen sometimes mates more than once in her lifetime and may even mate annually. Two other matings were observed by Schneirla (1971) after the ants had been removed for laboratory observation. The copulations lasted two and ten hours respectively.

Recently Franks and Hölldobler (1987) proposed that in army ants an unusual form of sexual selection exists, in which the workers play a major role in selecting their sister's mate. Outbreeding appears to be the rule in army ants; Schneirla (1971) has suggested that Eciton males must fly before they can mate. Thus, males have to enter alien colonies and break the worker barrier to get to the females. Under these circumstances workers are in a position to choose both the mother and father of their future nestmates. Franks and Hölldobler argued that the reason why workers should be involved in choosing mates for their queen is that they will later invest in the progeny of these males. Therefore the principle of sexual selection and female choice should apply to their preferences. In order to maximize their own inclusive fitness, the workers should actively choose the males that are most fertile. Sexual selection theory suggests that males may demonstrate that they will be donors of highly viable gene combinations, for example by being themselves large, robust and vigorous. It is possible that worker involvement in sexual selection has favored males that are superficially similar in size and shape to their conspecific queen. Such is in fact the case in the polyphyletic lineages of army ants. The unusual robustness of army ant males is well known. In Africa they are called sausage flies, and elsewhere they are commonly mistaken for wasps. It is possible that during evolutionary history, the gaster of the male became elongated and enlarged to house the massive sperm vesicles (Gotwald and Burdette, 1981) together with the ever increasing glandular equipment needed to impress the workers. Recently, Hölldobler and Engel-Siegel (1982) discovered that ecitonine males are unusually well endowed with abdominal glands, especially between the tergites of the gaster. Such glands, which do not occur in workers, closely resemble those of the queen (Whelden, 1963). Fierce sexual competition is made likely by the highly skewed numerical sex ratio in army ants. Where only a few males succeed, the resulting selection has probably led to the evolution of the rich glandular equipment in males, because only the most attractive males were successful. In fact males have retinues of workers that accompany them like the entourage of queens.

There is one further feature of the army ant syndrome that can be explained in terms of this unusual form of sexual selection and sexual competition. In many army ant species males lose their wings upon entering an alien colony (Figure 16-9). Dealate males have been found in the Old World army ants, including Dorylus rubellus (Savage, 1847, cited in Gotwald, 1982), as well as in the New World Labidus praedator (Rettenmeyer, 1963a) and species of Eciton (Schneirla, 1971).

The phylogeny of the doryline and ecitonine army ants
The genus Eciton represents one of the furthest extensions of an evolutionary trend that began independently within each of many different groups of ants. According to Gotwald (1982), the “true” army ants of the subfamilies Dorylinae and Ecitoninae are triphyletic, or triple-origined. Specifically, the combination of army-ant behavior and the dichthadiigyne queen has arisen separately in the genera Aenictus and Dorylus, which compose the subfamily Dorylinae, and a third time in Eciton and its relatives (Cheliomyrmex, Labidus, Neivamyrmex, and Nomamyrmex), which compose the subfamily Ecitoninae. The division between the two subfamilies is supported by a number of strong morphological differences, including even the Dufour's gland epithelium (Billen, 1985a).

On the basis of a phenetic study of Dorylus, Barr et al. (1985) recognized three groupings within that genus: Dorylus (including the “subgenera” Anomma, Dichthadia, and Typhlopone), Alaopone, and Rhogmus. These authors (and Gotwald, 1985) took the conservative position of placing all of the species under the single genus Dorylus, noting that “whether to recognize these groupings at the generic or subgeneric level must await the broader consideration which will be accorded the group in a complete revision.” The higher taxonomic status of Aenictus is in similar limbo. If the genus is truly independent, having arisen out of a stock entirely separate from those of Dorylus and the ecitonines, it should logically be placed either in the same subfamily as the ancestral stock or accorded a subfamily of its own. But again, this decision awaits a full analysis of the Dorylinae and candidate ancestral groups, particularly the Ponerinae. Meanwhile, Gotwald has provided sound biogeographic data to support his belief (1979) that Dorylus arose in Africa and spread into Tropical Asia, while Aenictus arose in Asia and spread to Africa and Australia.

In the New World, Cheliomyrmex is the phylogenetically most interesting genus. It is distinguished by a single waist segment, as opposed to the two waist segments possessed by all the other New World army ants. (Among Old World forms, Dorylus also has a single segment.) Cheliomyrmex is otherwise anatomically close to the remainder of the New World army ants (Gotwald, 1971). Wheeler, and later Gotwald and Kupiec (1975) and Gotwald (1978), considered the single-jointed waist primitive, and thus Cheliomyrmex itself primitive. Cheliomyrmex workers also have a median tooth on the tarsal claws and a simple pygidium (as opposed to a longitudinally impressed pygidium with terminal spines). Both of these traits are probably primitive (see Figure 16-10). However, Cheliomyrmex remains a rarely seen and enigmatic genus and needs to be examined in much more detail before its phylogenetic position can be ascertained with confidence. Its biology and life cycle might also shed light on its position within the Ecitoninae.

The phylogenetic origins of the three army ant groups (Aenictini, Dorylini, Ecitonini plus Cheliomyrmecini) are more generally very poorly understood. A favorite view, originating with Emery (1895) and entertained more recently by Brown (1975) and Gotwald (1982), is that the army ants arose from the tribe Cerapachyini of the subfamily Ponerinae. One of the cerapachyine traits favorable to this hypothesis is the widespread habit of raiding other species of ants. But again, both the anatomy and the behavior of the cerapachyines could be merely convergent to those of the doryline and ecitonine army ants.

The time of the origin of the three doryline and ecitonine lines is also unknown. A single species, Neivamyrmex ectopus, has been described from the Dominican Republic amber, which is late Oligocene or early Miocene in age (Wilson, 1985d). The two type workers are quite modern in aspect and closest in overall anatomy to species now living in Mexico and the southern United States than to the much richer Central and South American faunas. It is of special interest that army ants are today completely absent from the Dominican Republic and the remainder of the Greater Antilles. In other words they have retreated from this part of the world since no later than Oligocene times.