The Ants Chapter 1
CHAPTER 1. THE IMPORTANCE OF ANTS
They are everywhere but only occasionally noticed. They run much of the terrestrial world as the premier soil turners, channelers of energy, dominatrices of the insect fauna--yet receive only passing mention in textbooks on ecology. They employ the most complex forms of chemical communication of any animals and their social organization provides an illuminating contrast to that of human beings, but not one biologist in a hundred can describe the life cycle of any species. The neglect of ants in science and natural history is a shortcoming that should be remedied. They represent the culmination of insect evolution, in the same sense that human beings represent the summit of vertebrate evolution.
During the latter half of the Paleozoic Era a sequence of three events occurred that predestined the character of the modern insect fauna and set the stage for the origin of ants. The first was the invention of flight, the first time this had been achieved by any group of organisms in the history of life. One line out of the many existing in the Paleozoic somehow evolved wings in the adult stage, and it soon afterward enjoyed extensive species formation and diversification. Then a single line within this expanding "paleopterous" group attained the ability to fold the wings back over the body when not in use, giving the adults greater mobility on the ground after alighting. From this "neopterous" group, which also prospered, came still another line that attained complete metamorphosis. Now highly specialized larvae occupying one ecological niche could be transfigured into radically different adult forms occupying another ecological niche. This third, holometabolous group of insects exceeded its predecessors in evolutionary attainment. It radiated extensively to produce the most diverse and abundant insect orders now in existence, namely the beetles (Coleoptera), flies (Diptera), and bees, wasps, and their relatives (Hymenoptera).
The story did not quite end at this point. During Cretaceous times, spanning 140 million to 65 million years before the present, a fourth and wholly different kind of event occurred, the origin of advanced social life. All of the insects in this category, comprising the termites, ants, and some of the bees and wasps, are colonial. More precisely, they are eusocial in their habits. This means that two or more generations overlap in the society, adults take care of the young, and, most importantly, the adults are divided into reproductive and nonreproductive castes, in other words queens and kings versus workers (Michener, 1969, 1974; Wilson, 1971).
To a degree seldom grasped even by entomologists, the modern insect fauna has become predominantly social. Recent measurements suggest that about one-third of the entire animal biomass of the Amazonian terra firme rain forest is composed of ants and termites, with each hectare of soil containing in excess of 8 million ants and 1 million termites. These two kinds of insects, along with bees and wasps, make up somewhat more than 75 percent of the total insect biomass (Beck, 1971; Fittkau and Klinge, 1973). Ants and termites similarly dominate the forests and savannas of Zaïre (Dejean et al., 1986). Although comparable biomass measurements have not yet been made elsewhere, it is our subjective impression that the eusocial insects, ants foremost among them, are comparably abundant in most other principal habitats around the world.
For example, on the Ivory Coast savanna the density of ants is 7000 colonies and 20 million individuals per hectare, with one species alone, Camponotus acvapimensis, accounting for 2 million of the individuals (Lévieux, 1966, 1982). Such African habitats are often visited by driver ants (Dorylus spp.), single colonies of which occasionally contain more than 20 million workers (Raignier and Van Boven, 1955). And the driver ant case is far from the ultimate. A "supercolony" of the ant Formica yessensis on the Ishikari Coast of Hokkaido was reported to be composed of 306 million workers and 1,080,000 queens living in 45,000 interconnected nests across a territory of 2.7 square kilometers (Higashi and Yamauchi, 1979).
The local diversity of ants is substantial, far exceeding that of other social insects and reflecting the manner in which ant species have evolved to saturate a wide range of feeding niches in the soil and vegetation. In lowland rain forest at the Busu River, northeastern Papua-New Guinea, Wilson (1959a) collected 172 species of ants belonging to 59 genera in an area of about one square mile (2.6 km2). Barry Bolton (in Room, 1971) recorded 219 species in 63 genera in a square mile of cocoa plantation and forest at Tafo, Ghana, while Kempf (1964a, and personal communication) found 272 species belonging to 71 genera in a comparable area at Agudos, São Paulo State, Brazil. During two years of field work, Manfred Verhaagh (personal communication) collected at least 350 species belonging to 71 genera at the Rio Yuyapichis, in the larger valley of the Rio Pachitea, Peru; the western Amazon Basin, in which this watershed is located, may have the richest ant fauna in the world. Moving to more limited sample spaces, Room (1971) recorded 48 genera and 128 species from only 250 square meters in a cocoa farm in Ghana. Wilson (1988) identified 43 species in 26 genera in a single tree from the Tambopata Reserve in the Peruvian Amazon. If the terrestrial fauna had been assayed around the tree as well, the total point diversity would probably have rivaled that of Room's Ghanaian sample. Temperate faunas are less rich but often impressive nonetheless: 23 genera and 87 species in 5.6 square kilometers at the E. S. George Reserve in Michigan (Talbot, 1975), and 30 genera and 76 species in 8 square kilometers of the Welaka Reserve, Florida (Van Pelt, 1956).
The impact of the ants on the terrestrial environment is correspondingly great. In most terrestrial habitats they are among the leading predators of other insects and small invertebrates (Wilson, 1971; Jeanne, 1979; Lévieux, 1982; Sörensen and Schmidt, 1987). Leafcutter ants, in other words members of the genera Acromyrmex and Atta, are species for species the principal herbivores and most destructive insect pests of Central and South America (Weber, 1972; Cherrett, 1982). Pogonomyrmex and other harvester ants rank among the principal granivores, competing effectively with mammals for seeds in deserts of the southwestern United States (Davidson et al., 1980). In another adaptive zone, ants are sufficiently dense to reduce the abundance of ground-dwelling spiders and carabid beetles, especially when these arthropods are specialized to live in the soil and rotting vegetation (Darlington, 1971; Cherix, 1980; Wilson, 1986a). Where montane habitats are high enough to be mostly free of ants, such as the summit of Mt. Mitchell in North Carolina and the Sarawaget Mountains of Papua-New Guinea above 2500 meters, carabids and spiders increase markedly in numbers.
It is not surprising to find that ants also alter their physical environment profoundly. In the woodlands of New England, they move approximately the same amount of soil as earthworms, and they surpass them in tropical forests (Lyford, 1963; Abe, 1982). In temperate forests of New York, they are responsible for the dispersal of nearly one-third of the species of the herbaceous plant species, which in turn comprise 40 percent of the aboveground biomass (Handel et al., 1981). They aid in the spread of forest vegetation onto bare rocks in Finland (Oionen, 1956) and foredune vegetation onto salt lakes in the U.S.S.R. (Pavlova, 1977). Because ants transport plant and animal remains into their nest chambers, mixing these materials with excavated earth, the nest area is often charged with high levels of carbon, nitrogen, and phosphorus. The soil surface is consequently broken into a mosaic of nutrient concentrations, and this in turn creates patchy distributions of plant growth, especially during the early stages of succession (Beattie and Culver, 1977; Petal, 1978; Briese, 1982b). The great earthen nests of the leafcutter ants (Atta) have a particularly strong impact on local environments. In tropical rain forests, where less than 0.1 percent of nutrients normally filter deeper than 5 centimeters beneath the soil (Savage, 1982), the leafcutter workers carry large quantities of freshly cut vegetation into nest chambers as deep as six meters. Haines (1978) found that the flow of 13 elements through the underground refuse dumps of A. colombica was 16 to 98 times the flow in undisturbed leaf litter beneath equivalent sample areas. The enrichment of materials resulted in a fourfold increase in the quantity of fine tree roots in the dump. Energy flow through the A. colombica nests was about ten times greater on a per square meter basis than in forest areas away from the nests. Other ants turn and modify the soil in ways that have just begun to be assessed, and to an especially important degree in deserts, savannas, and tropical forests (Lévieux, 1976d; Petal, 1978; Whitford et al., 1986). According to Graedel and Eisner (1987; see also Monastersky, 1987), formicine ants may be responsible for much of the previously unexplained quantities of formic acid found in the atmosphere above the Amazon forest and other habitats rich in these insects. Graedel and Eisner estimate, very roughly, that formicine ants may release 1012 grams of formic acid globally each year.
The abundance and ecological dominance of ants is matched by their extraordinary geographic range. Various of the approximately 8800 known species are found from the Arctic circle to the southernmost reaches of Tasmania, Tierra del Fuego, and southern Africa. The only places free of native species are Antarctica, Iceland, Greenland, Polynesia east of Tonga, and a few of the most remote islands in the Atlantic and Indian Oceans (Wilson and Taylor, 1967b). Four genera (Camponotus, Crematogaster, Hypoponera, and Pheidole) extend individually over most of this vast range (Wilson, 1976e).
Some species of ants have adapted very well to even the most disturbed habitats. Most cities in the tropics are home to "tramp species," forms that have been carried worldwide by human commerce. The little myrmicine Tetramorium simillimum is equally likely to turn up in an alley in Alexandria or a beach in Tahiti. "Crazy ants" (Paratrechina longicornis) swarm under debris in vacant lots; colonies of the tiny dolichoderine Tapinoma melanocephalum nest in abandoned plumbing, dead plant stems, and even soiled clothing. Pharaoh's ant (Monomorium pharaonis) is a worldwide household pest. Its vast, multi-queened colonies thrive in wall spaces and detritus. In hospitals they often visit soiled bandages and track pathogenic microbes onto clean dressings and food. A notorious colony occupied the entire Biological Laboratories of Harvard University during the 1960s and 1970s. An extermination campaign was finally undertaken when workers were discovered carrying radioactive chemicals from culture dishes into the surrounding walls. [The incident was made the basis of the melodramatic scientific novel Spirals, by William Patrick (Houghton Mifflin, Boston, 1983).]
Ants are resistant to hard radiation. Colonies exposed to intense cesium-based irradiation in a French forest suffered no evident decline or change in behavior during eleven months, even when some of the surrounding plants were dying or losing their leaves (Le Masne and Bonavita-Cougourdan, 1972). At least some ant species are also highly resistant to industrial pollution. Near a nitrogen plant in Poland, populations of Myrmica ruginodis and Lasius niger remained robust after other invertebrates became scarce. They actually reduced the concentration of the nitrate, apparently by stimulation of microorganisms that bind the pollutant (Petal, 1978).
Surprisingly, some species are even able to survive under water. Queens and workers of Formica species can live for up to 14 days or longer while submerged, during which time they are in an anesthetized condition and their oxygen consumption falls to between 5 and 20 percent of the usual resting rate. Oxygen consumption under water is highest in Formica uralensis, which lives in bogs and is most likely to suffer periodic flooding of the nest (Gryllenberg and Rosengren, 1984). In preliminary experiments, Wilson (unpublished) found that Cardiocondyla venustula colonies living close to water on islands in the Florida Keys can withstand submergence in salt water for at least several hours.
Ants offer special advantages for some important kinds of basic biological research. The colony is a superorganism. It can be analyzed as a coherent unit and compared with the organism in the design of experiments, with individuals treated as the rough analogs of cells. The aim of much of contemporary research on ants, as well as that on other kinds of social insects, is first to identify more fully the mechanisms by which colony members differentiate into castes and divide labor, and second to understand why certain combinations of these mechanisms have produced more successful products than others. The larger hope is that more general and exact principles of biological organization will be revealed by the meshing of information from insect sociobiology with equivalent information from developmental biology. The definitive process at the level of the organism is morphogenesis, the set of procedures by which individual cells or cell populations undergo changes in shape or position incident to organismic development. The definitive process at the level of the colony is sociogenesis, the procedures by which individuals undergo changes in caste, behavior, and physical location incident to colonial development. The question of interest for general biology is the nature of the similarities between morphogenesis and sociogenesis.
The study of ant social organization is by necessity both a reductionistic and holistic enterprise. The behavior of the colony as a whole can be understood only if the programs and positional effects of the individual members are both specified and explained more deeply at the physiological level. But such accounts are still far from complete. The information makes full sense only when the colonial pattern of each species is examined as an idiosyncratic adaptation to the natural environment in which it lives.
At both the individual and colonial levels, social insects offer great advantages over ordinary organisms for the study of biological organization. Although it is virtually impossible to dissect a higher organism into its constituent parts for study and then put it back together again, alive and whole, this can easily be done with an insect colony. The colony, in other words the superorganism, can be subdivided into any conceivable combination of sets of its members. It can then be manipulated experimentally and reconstituted at the end of the day, unharmed and ready for replicate treatment at a later time. One technique used successfully for the analysis of optimization in social organization is the following: the colony is modified by changing caste ratios, as though it were a mutant. The performance of this "pseudomutant" is compared with that of the untransformed colony as well as other modified versions. The same colony can be turned repetitively into pseudomutants in random sequences on different days, eliminating the variance that would otherwise arise from between-colony differences (Wilson, 1980b). Fragments of colonies can be separated for more intensive short-term studies of many kinds and then either discarded or rejoined. They can be shifted about in various geometric configurations to study position effects, rather like moving the brain or liver to novel locations in order to study the effects on other parts of the body.
At the highest level of explanation, that of the ecosystem, the large numbers of kinds of ants (including more than 1000 species in the ant genus Pheidole alone) give a panoramic view of the evolution of colonial patterns. The very exuberance of diversity makes the correlative analysis of adaptation easier and more rigorous. In a subsequent phase of research, hypotheses concerning the functions of body form, caste systems, and other biological traits can then be subjected to experimental tests in the field and laboratory. This research is rendered easier by the small size of these insects, as well as the ease with which they can be cultured in the laboratory. Finally, ants are extraordinary among social animals in the swiftness with which they adapt to radically altered environments in the laboratory and resume normal behavior under the gaze of the investigator.
Ants are premier organisms for research in behavioral ecology and sociobiology. They exemplify principles in these relatively new disciplines as well as offer exceptional opportunities for the testing and extension of theory. They provide, for example, some of the best documentation of the following phenomena:
• Kin selection and selection at the level of the colony.
• Competition at each of the three levels of organization: among individuals of the same colony, among colonies of the same species, and among species.
• The effects of competition on community structure.
• The shaping of the organization and development of societies by natural selection.
• The shaping of castes by natural selection to create an "adaptive demography," in which the size and age distributions of colony members contribute to the genetic fitness of the colony as a whole.
• The nature of physiological and behavioral regulatory processes in social organization.
• Hierarchy in control processes.
Ants and other social insects have been underutilized in textbooks and the review literature on behavior and ecology, which tend to favor vertebrate examples. This has been true even when, as in the case of pheromones and kin selection, the basic concepts were pioneered during studies on insects. The disproportion has two causes. First, vertebrates attract more enthusiasts among scientists and naturalists simply because they are more nearly human in size. This bias is understandable but is not always a wise research strategy. The strongest efforts by gifted investigators often yield results that could have been achieved in less time and more convincingly with social insects. The second reason for the relative neglect of social insects is that their study seems more "technical." That is, it requires a specialized knowledge of anatomy, physiology, and other topics of entomology not ordinarily acquired by biologists during their basic university education.
We confess to having written this book mainly to celebrate a personal muse, perhaps the least explicable yet most sympathetic reason why any book should be written. But in so doing we have tried to reorganize myrmecology into a form that addresses biological principles while making ants, the paragons of the insect world, more accessible for future study by others.
Hölldobler, B. and Wilson, E. O. 1990. The Ants. Cambridge, Mass. Harvard University Press. Text used with permission of the authors.