Trophallaxis

From The Ants, Chapter 7:

One of the elementary bonds of insect colonies is the sharing of food among nestmates. Prey objects and seeds brought into the nest by a few individuals are usually freely consumed by many other individuals. Liquid food, stored in the forager's crop (the “social stomach”) is regurgitated to nestmates and thus distributed over large portions of the colony. This latter form of food transmission is called stomodeal (or oral) trophallaxis. The crops of most ant species that feed on nectar and homopteran-secreted honeydew are capable of considerable distention. Individual foragers are consequently able to carry home large loads of carbohydrates. Some groups of workers serve as living reservoirs during lean periods. The storage of liquid food in the crop has been carried to great heights by the repletes of certain ant species, individuals whose abdomens are so distended they have difficulty moving and are forced to remain permanently in the nest as “living honey casks” (see Chapter 8, Figure 8-41). The liquid, digested only to a limited extent while held in the crop, is freely passed from one ant to another. Thus the crops of all the workers taken together serve as a social stomach from which the colony as a whole draws nourishment. Eisner (1957), adding extensively to the original discoveries of Forel (1878), showed how the proventriculus has evolved in ants to facilitate this communal function. The proventriculus forms a tight constriction at the anterior end of the crop (see Figure 7-1). It regulates the flow of liquid back to the midgut where the food is digested, and thus serves to segregate the communal supply in the crop from the personal supply in the midgut. The proventriculus of Myrmecia (Figure 7-69) is typical of primitive ants, while that of Camponotus represents an advanced form found in formicine ants. So distinctive are the structures that they provide useful characters for the study of phylogeny at the generic and tribal levels (Eisner and Brown, 1958). The peculiar infrabuccal pocket, a sizable cavity located just beneath the tongue of worker ants, filters out and compacts most of the solid material that would otherwise clog the narrow, rigid proventriculus channels (Eisner and Happ, 1962; Figure 7-70). From time to time workers of most ant species disgorge the infrabuccal waste material in the form of a pellet (see Febvay and Kermarrec, 1981). This waste material is then carried out of the nest and discarded. In arboreal ants of the genus Pseudomyrmex, it is routinely fed to the larvae (Wheeler and Bailey, 1920). Typically, a soliciting ant elicits regurgitation from a nestmate by stimulating it with stereotyped tactile signals with the antennae and forelegs. During this episode the mechanical stimulation of the donor's mouthparts, especially her labium, serves as the important releaser of the regurgitator reflex (see pages 7-61 to 7-62 and Figures 7-42, 7-43, 7-71, and 7-72).

Liquid food exchange by regurgitation is a highly evolved form of behavior. It distributes food through colonies with remarkable rapidity. It is much more common among species belonging to phylogenetically advanced subfamilies (Wilson, 1971). A likely precursor exists in the distinctive mode of liquid food transport practiced by some ponerine species. Most ponerine ants are primarily predators and scavengers, but some species collect liquid material as well. Evans and Leston (1971) discovered that workers of a West African species of Odontomachus gather honeydew from aphids and coccids, and carry the liquid homeward as droplets between their mandibles. Other large ponerines transport liquid in a similar manner. They include Ectatomma tuberculatum (Weber, 1946b) and Paraponera clavata (McCluskey and Brown, 1972; Hermann, 1975). The giant Paraponera workers appear to gather most of the liquid from extrafloral nectaries, standing water, and fruit, and this material composes a substantial portion of the harvested food (Hermann, 1975; Young, 1977).

Recent studies have revealed not just the transport but also the transmission of the liquid droplets in species of the ponerine species Pachycondyla obscuricornis and Neoponera villosa, which are large ponerines found in the New World tropical forests (Hölldobler, 1985). When a forager enters the nest laden with liquid food, it stands still for a period of time, swinging its head from side to side while waiting for a nestmate to approach; or else it moves directly toward nestmates and presents them with the food droplet held between its widely opened mandibles. If the colony is well fed, a forager may have to wait as long as 30 minutes before a nestmate responds. Sometimes it is wholly ignored and is not able to share its booty. In this case it imbibes a portion of the droplet itself and wipes off the residue on the floor and walls of the nest. Most of the time, however, nestmates readily accept the liquid food and even actively solicit it from the forager. While jerking its head rapidly up and down, the solicitor approaches the food carrier head on and intensively antennates the front of its head and mandibles (see Figure 7-73). It makes a “spooning” or licking motion with the labium, and slowly transfers part of the standing drop to the space between its own mandibles. All the while it continues to antennate the head and mandibles of the donor. When about a fourth to three-fourths of the liquid has been transferred, the ants pull apart. After the separation, the solicitor appears to imbibe a small fraction of the liquid. The remainder it shares with other nestmates, until as many as ten or more have received a portion.

In short, the Pachycondyla workers do not share food by regurgitation in the characteristic manner of most other ants. Rather they employ a “social bucket” system in which they first collect liquid food, then spoon portions into the gaping mandibles of nestmates. The bucket itself is formed by the mandibles on the side and by inwardly curving setae and the extruded labium underneath. The liquid is held in place by surface tension.

The whole social-bucket procedure, while crude, nevertheless bears a striking similarity to liquid food exchange by regurgitation as it is employed by the Formicinae and other phylogenetically advanced ants (see Figure 7-71). In the latter case the food is collected in the crop. In response to very similar antennal signals and the mechanical stimulation of its labium, the food carrier regurgitates a droplet of liquid from its crop. Simultaneously it opens its mandibles widely, extrudes the labium, and folds the antennae backwards. Occasionally, when a large droplet is regurgitated all at once, it is held between the mandibles in the ponerine manner (Figure 7-74). In contrast to the typical ponerine exchange, however, the soliciting ant imbibes all the food it receives and stores it in the crop. Small amounts of this food pass through the proventriculus into the midgut, where it is digested. The major portions, however, are nevertheless distributed by regurgitation to nestmates.

With this evidence at hand, it is quite reasonable to suppose that the social bucket method of liquid food exchange is a precursor to stomodeal regurgitation. It is not the only evolutionary entrée conceivable but for the moment seems the most plausible one. The hypothesis gains further support from the fact that Ectatomma and Paraponera, which employ the social bucket, are members of the tribe Ectatommini. This taxonomic group is generally considered to be close to the stock that gave rise to the Myrmicinae, among the master users of regurgitation.

It is interesting to take one more step back in time and inquire about the evolutionary origin of the antennal signals used in both the social bucket and regurgitation. A clue is provided by the similarity of the antennal signals used in widely different behavioral categories within the Ponerinae. They include food begging, recruitment initiation, and social greeting, in which nestmates are recognized and alerted into examining the greeter. For example, when a patrolling worker of the African ponerine Paltothyreus tarsatus meets a stray nestmate, both ants first engage in mutual antennation. This behavior closely resembles the antennation pattern preceding food exchange in many other ant species, but no trophallaxis or liquid food exchange of any kind occurs. In fact, Paltothyreus apparently never practices liquid food exchange. In this species the stereotyped antennation is part of a greeting and invitation behavior, by which the nestmate is solicitated to follow in tandem back to the nest (Hölldobler, 1984b). The invitation behavior is even more striking in an Australian species of the ponerine genus Hypoponera (Hölldobler, 1985). After a pair of workers meets face to face, the recruiter tilts its head sideways almost 90 degrees and strikes the upper and lower surfaces of the nestmate's head with its antennae. Often the solicited ant responds with similar antennation. The recruiting ant then turns around and tandem running starts (Figure 7-75). Similar behavior also occurs inside the nest, but it has never been observed to elicit food exchange--only the enticement of nestmates to travel from one nest site to another.

In addition to antennation, the head-jerking movements often associated with food solicitation in Pachycondyla villosa have been found to be part of the invitation behavior in other species of Pachycondyla (Maschwitz et al., 1974; Traniello and Hölldobler, 1984).

In summary, solicitation signals employed by ponerine ants in recruitment are similar if not identical to those employed during food exchange. Because the signals are employed by many ponerine species exclusively for invitation, yet no species is known of their exclusive use in food soliciting, invitation is reasonably interpreted to be the more primitive of the two functions. It would appear that the repertory of some ponerine phylogenetic lines was expanded by ritualization of invitation signals to encompass food soliciting signals.

A very different form of exchange that has been reported in adult workers of several myrmicine genera is abdominal trophallaxis, the extrusion of a droplet of rectal liquid that is consumed by nestmates. In general form it resembles the donation of anal droplets from larvae to workers. The phenomenon was discovered in Zacryptocerus varians, an arboreal cephalotine species from the West Indies and Florida (Wilson, 1976a; Cole, 1980). Corn (1980) was not able to observe abdominal trophallaxis in the giant species Cephalotes atratus, but Diana Wheeler (1984) found it in the cephalotine Procryptocerus scabriusculus. In Procryptocerus scabriusculus the behavior is usually initiated by newly eclosed workers, which seek out older workers and solicit the droplets by licking their abdominal tips. Abdominal trophallaxis was also observed between older workers and between a worker and a queen, but the bouts were much shorter than those occurring between callows and older workers. The function of the behavior remains unknown. However, Wheeler has pointed out its similarity to proctodeal feeding in termites, by which symbiotic protozoans and bacteria are transferred from older to younger colony members. There may be a connection with a second striking peculiarity associated with digestion in cephalotine ants: a mushroom-shaped, sclerotized cap on the proventriculus, an organ that intervenes between the crop and midgut and is thought to filter food as part of the social function of crop storage (Eisner, 1957).

Outside the Cephalotini, abdominal trophallaxis has been observed between the myrmicine slavemaker Harpagoxenus americanus and its hosts species, Leptothorax ambiguus and Leptothorax longispinosus (Stuart, 1981). Workers and queens of the Harpagoxenus occasionally assume a stereotyped posture, standing quietly with the abdomen raised, and extrude a droplet of liquid which is eaten by the slaves. This behavior is doubly remarkable because it is a rare instance of a social parasite donating something to its host. Its function remains unknown, and may prove to be a form of dominance or other exploitative behavior.