The Ants Chapter 10

CHAPTER 10. FORAGING STRATEGIES, TERRITORY, AND POPULATION REGULATION

Ant colonies exploit the environment by wholly social means. They deploy aging workers into the field as expendable probes to blanket the terrain around the nest in a near continuous and instantaneous manner. In many species scouts that encounter a large food supply recruit nestmates in numbers appropriate to the size and richness of the discovery. When they meet enemies, they can recruit defenders or else withdraw, closing the nest entrance and lasting out the danger with the aid of food that has been conveniently stored in the crops and fat bodies of the younger workers.

In the formal framework of a theoretical ecologist an ant colony resembles a plant as much as it does a solitary animal. It is sessile, in other words rooted to a nest site. Its growth is indeterminate, so that under stress it can revert to the size and caste composition of younger colonies. As a consequence the size and age of colonies are only weakly correlated. As Rayner and Franks (1987) have pointed out, close parallels also exist between ant colonies and mycelia of fungi. “Both are collectives of genetically related or identical semi-autonomous units, consisting respectively of discrete multicellular individuals and hyphae.” The patterns created by the growing hyphae are remarkably similar in geometric design to the foraging columns and swarms of army ants and trunk trail systems of wood ants. In both cases the probes of genetically different cultures avoid one another, creating an interdigitating pattern that thoroughly exploits the available resources.

To continue the comparison, many ant colonies adjust to environmental change like plants more by flexibility of response than by movement from place to place. They attain this adaptability by a broad range of social behaviors, including adjustable alarm and recruitment, differential clustering, alterations of nest architecture, and shifts in foraging pattern.

Foraging theory
Foraging theory can be said to have begun, at least in mathematical metaphor, with Emlen (1966) and MacArthur and Pianka (1966). It has been extended greatly by Schoener (1971), Pyke et al. (1977), Orians and Pearson (1979), Stephens and Krebs (1986) and others. The special case of social insects has been theoretically treated by Oster and Wilson (1978) and advanced by many investigators through excellent field and laboratory studies.

Foraging theory is composed mostly of optimality models. The marginal value utilized, or “currency,” is usually energy. The modelers visualize the organism as seeking to maximize its net energetic yield. Evolution by natural selection, they reason, has modified behavior in one or the other of four basic ways so as to increase this currency: (1) choice of food items (optimum diet); (2) choice of food patch (optimum patch choice); (3) allocation of time invested in different patches (optimum time budget); and (4) regulation of the pattern and speed of movement. In the case of ants and other animals with a nest or other permanent retreat, the foraging patterns are analyzed in terms of sallies from a central location. This special case is the subject of “central-place foraging theory,” about which we will say more later.

Optimal foraging patterns are generally thought to be constrained by two forces, one external to the organism and the other internal. The external constraint is mortality due to accidents, disorientation, and attacks by predators and competitors. Many field studies have shown that worker populations of ant colonies are subject to terrible losses through predation and battles with competing colonies. It is also clear that the foraging patterns of individual species are profoundly influenced by these pressures. The internal constraints, on the other hand, are particular physiological constraints and the limited sensory and psychological capacities of organisms. Animals, and especially small-brained creatures like ants, can rarely if ever maximize their net energy yield by calculating exact costs, benefits, and mortality risks for each new situation in turn (of course, even human beings are hard put to accomplish that much). Instead, they are more likely to employ “rules of thumb,” which are quick decisions triggered by relatively simple stimuli or stimulus configurations. The rules of thumb work adequately for individual worker ants most of the time, and they may result in considerable precision when added up across multiple workers during the process of mass communication. Rules of thumb used by fire ants that we introduced earlier to illustrate colony homeostasis (Chapter 9) include the following: “continue hunting for a certain foodstuff if the present foraging load is accepted by nestmates” (it will probably satisfy the needs of the colony); “follow a trail if enough pheromone is present” (it will probably lead to food); and “feed the queen more if final-instar larvae are present” (this means that the colony developmental pipeline is in good working order).

In adapting foraging theory to the social insects, Oster and Wilson (1978) treated risk of worker mortality not as a constraint but as an energy cost that must be born to varying degrees by the colony. When a worker is killed in action, the game is far from over; the colony has merely lost a packet of energy that had been invested earlier through the processes of egg laying, larva rearing, and pupa care. The ultimate pay-off in colony-level selection is the summed production of reproductives over a colony generation. In general, ant colonies appear to act so as to build as large a population of workers as possible during the ergonomic phase, then “cash in” with a partial or full conversion to reproductives during the breeding season. Consequently, a reasonable measure of fitness for a colony in its ergonomic phase of growth is energy, with the growth rate of the adult biomass expressed as calories/unit-of-time and the full colony biomass achieved at the end of the ergonomic phase expressed in net caloric accumulation. The analytic advantage of employing energy as the basic currency is that it can be folded one way or the other into all colony processes. The key particulars are as follows:

• The biomass and biomass growth of the colony or any portion of it can be translated to energy units.

• Foraging success, brood care, and other nurturent activities can be translated into energy gained.

• Protective activities, including nest defense and construction, can be converted into calorie equivalents saved because of the reduction in mortality and impaired colony functions that such activity avoids.

• Metabolism and mortality can be converted directly into caloric loss.

It is of course an oversimplification to measure ergonomic success entirely by the energy equivalents of biomass. Reproductive success depends not just on colony size at the end of the ergonomic phase but also on the proportion of immature and mature forms as measured by the relative frequency of castes at this critical time. It also depends on the forms and kinds of “capital” at the disposal of the colony, particularly the amount of stored resources and the structure and location of the nest. Nevertheless, energy equivalence is probably the overriding determinant of reproductive success. The optimal caste frequency distribution and nest structure at the onset of the reproductive phase are unlikely to differ from those built up during the ergonomic phase, while few species store large amounts of food materials near the end of the ergonomic phase. In addition to such an audit of the total life span, analyses of particular components of foraging appear to be energy-efficient in the case of ants. As we shall see shortly, the time spent selecting food items and the degree of selectivity are consistent with the models of central place foraging theory, which are based on the postulate of net energy maximization. Also, in the case of leafcutting ants, net energy yield appears to be the key function among all those that might have influenced the evolutionary choice of leafcutting ant medias as foraging specialists over minors and majors (Wilson, 1980b).

Foraging behavior has two principal interlocking components: the search and retrieval of food items, often accompanied by the recruitment of nestmates, and the avoidance or defeat of enemies. It is feasible in theory at least to assess the relative importance of the two components by equating them in terms of energetic cost and gain.

The temperature-humidity envelope
Every ant species operates within ranges of temperature and humidity that can be depicted as a two-dimensional space; in other words, every species has a temperature-humidity envelope. Also, the tolerance of an isolated foraging worker is very different from that of an entire colony. The forager is more swiftly affected by the preexisting ambient temperature and humidity of the microenvironment, whereas the colony can control the microenvironment by shifting into deeper reaches of the nest or by the retention of metabolic heat and moisture through clustering. Thus no nuptial flights of the fire ant Solenopsis invicta occur when morning temperatures of the soil (from the surface to 10 cm deep) are below 18°C, and colony founding by newly inseminated queens occurs only if the soil temperatures at 5 to 7 cm below the surface are equal to or greater than 24°C. In addition, young colonies survive winter poorly even in southern Mississippi (Rhoades and Davies, 1967; Markin et al., 1973, 1974). As a consequence the imported fire ant appears already to have reached its geographic range limit in the northern part of the coastal states. To the west, the colonies are likely to be able to spread across desert areas only by colonizing stream beds, irrigated agricultural fields, and urban areas. Foraging fire ant workers, on the other hand, have even less tolerance for extreme cold, heat, and low relative humidity, and they are unable to survive in ambient conditions in which colonies as a whole do well (Francke and Cokendolpher, 1986). The main point to consider is that if fire ants were solitary insects, the geographic distribution of the species would be far more restricted than it is in fact.

A large portion of the available data on temperature tolerances by foraging workers is summarized in Table 10-1. Not surprisingly, a rough correlation exists between the tolerances and the environment, with desert species at the upper end and some (but not all) species from cold temperate forests at the lower end. The extreme thermophiles of the world fauna belong to the myrmicine genera Ocymyrmex of southern Africa and Cataglyphis of North Africa and Eurasia. The two are biogeographic vicariants of each other. In particular, both are specialized in similar manner for diurnal foraging on extremely hot desert terrain. The workers hunt singly for the corpses of insects and other arthropods that have succumbed from the heat (Harkness and Wehner, 1977; Marsh, 1985a,b; Wehner, 1987). Their behavior and even outward physical appearance are remarkably similar. Ocymyrmex barbiger forages in the sun at surface temperatures up to 67°C, which must be close to the record for insects generally. Cataglyphis fortis is a specialist of the extremely hot, dry, and food-impoverished terrain of the Saharan salt pans. At the opposite end, the cryophilic (cold-loving) species Camponotus vicinus and Prenolepis imparis start foraging at just above freezing and cease when the temperature reaches about 20°C. Similarly, the Australian species Nothomyrmecia macrops forages exclusively after dusk, and the workers seem to be more active at times when temperatures are low (5-10°C). Hölldobler and Taylor (1983) suggested that low temperatures hamper the escape of potential prey encountered in the tree tops increasing the hunting success of the Nothomyrmecia foragers (Plate 12).

Most diurnal desert ants pass through two periods in the day when their preferred temperatures occur, in the morning and late afternoon. As a consequence they have a bimodal distribution of foraging activity, with a period of decline around midday. In mesic temperature habitats, such as northern coniferous woodland, the reverse pattern occurs among diurnal species, with foraging peaking in the middle of the day. These patterns are probably determined by external environmental cues. Hunt (1974) was able to shift the desert bimodal pattern of the Chilean dolichoderine Dorymyrmex antarcticus to a mesic unimodal pattern merely by shading the nest at midday.

While the temperature tolerances of ant species are correlated with climate and major habitat, the relation is only loose. Added variance comes from two sources, microhabitat specialization and competition avoidance. Forest species, such as Aphaenogaster rudis and Paratrechina melanderi, have lower tolerance than other species, such as Monomorium minimum and Tetramorium caespitum, which are adapted to clearings in the same immediate area. It is also of advantage for ants to use unusual activity regimes to escape competitors. The thermophilic species of Cataglyphis and Ocymyrmex have the desert terrain virtually to themselves at midday. In the grassy meadows of Massachusetts, the little black ant Monomorium minimum recruits at higher temperatures than does its three closest competitors, Lasius neoniger, Myrmica americana, and Tetramorium caespitum. It combines this specialization with an effective form of venom dispersal to appropriate a substantial fraction of dead insects and other food finds (Adams and Traniello, 1981).

The subtle differences in microhabitat that characterize species are very well illustrated in Formica perpilosa and Trachymyrmex smithi, two ant species common in the Chihuahuan desert of southern New Mexico. As illustrated in Figure 10-1, Formica perpilosa is active in a much broader area around its nest than is T. smithi. The reason is that the [[Formica'' are more resistant to water loss, and they also tend to forage on mesquite and other forms of vegetation, where the relative humidity is higher (Schumacher and Whitford, 1974).

Quantitative studies of humidity preference by foraging ants of the kind conducted by Schumacher and Whitford are rare in the literature, but abundant anecdotal evidence exists to show that the higher the relative humidity, the greater the temperature tolerance. An increase in foraging activity when humidity rises at high temperatures has been observed in Pheidole militicida (Hölldobler and Möglich, 1980), Formica polyctena (Rosengren, 1977b), Prenolepis imparis (Talbot, 1943b, 1946), and a wide range of semi-desert ant genera in Australia (Briese and Macauley, 1980); and it is probably a general phenomenon in ants as a whole. Another source of differential foraging in the face of varying humidity is simple physiological resistance to desiccation, a phenomenon that has been observed in Tetramorium caespitum by Brian (1965b), Pogonomyrmex by Hansen (1978), and diurnal ant species in Australia by Briese and McCauley (1980).

On the other hand, rain halts most foraging in places where the drops pelt the ground and form small puddles and rivulets (Hodgson, 1955; Lewis et al., 1974b; Skinner, 1980a). Every collector is familiar with this phenomenon, to his frequent frustration and especially during tropical wet seasons. On the other hand, there are a few long-legged ants, including the species of the dolichoderine genus Leptomyrmex of Australia and New Guinea and the myrmicine “giraffe ants” Aphaenogaster phalangium of Central America, that use their unusual stature to navigate water films. As a result they are among the first insects to forage after the rain has ceased.