Social behaviour in animals

Introduction

      actions of animals living in communities. Such behaviour may include the feeding of the young, the building of shelters, or the guarding of territory.

General characteristics

      Social behaviour (Social behaviour in animals) among animals takes many forms. The American naturalist and artist John James Audubon (Audubon, John James) observed one of the largest social groups that man has ever known, in the fall of 1813 near Henderson, Kentucky. The species was the passenger pigeon (Ectopistes migratorius), once incredibly numerous but hunted to extinction by the end of the 19th century. Audubon wrote:

The air was literally filled with pigeons; the light of noonday was obscured as by an eclipse; the dung fell in spots not unlike melting flakes of snow. . . . The people were all in arms. . . . For a week or more, the population fed on no other flesh than that of pigeons. . . . The atmosphere, during this time, was strongly impregnated with the peculiar odour which emanates from the species. . . . Let us take a column of one mile in breadth, which is far below the average size, and suppose it passing over us without interruption for three hours, at the rate mentioned above of one mile in the minute. This will give us a parallelogram of 180 miles by 1, covering 180 square miles. Allowing 2 pigeons to the square yard, we have 1,115,136,000 pigeons in one flock.

Social and nonsocial behaviour

      The largest social organizations ever known are those of desert locusts; the pigeons were second; and present-day China is probably third, although some pelagic fish schools may be next. Persecution by man is reducing all the large social organizations except his own: the bison and the anchovies off California and Peru have fared poorly compared to smaller groups.

      Large numbers or crowding do not in themselves constitute social behaviour. It is usually true, for instance, that a fish that produces a million eggs tosses them out less socially than does a fish that produces a single young and cares for it much more, and that a polygamous bird is less social than a faithfully monogamous one. Overcrowding leads to many social abnormalities. Crowded cats, for instance, develop a “despot” and “pariahs,” and there is an almost continuous frenzy of spiteful hissing, growling, or fighting. Crowded rats display, in addition, hypersexuality, homosexuality, and cannibalism.

      Animals sometimes are brought together by some localized attraction or scarcity, as are moths around an electric light, animals at a water hole in the dry African savanna, birds and bees at a fruit-bearing tree, or iguanas crowding to nest on islands free of predators. To determine whether a grouping is social or not, it is necessary to examine the distribution of the animal within the limits of its needed habitat. Most animals require a certain sort of habitat—woodland for a squirrel, or nearly bare ground for a horned lark. Within the correct habitat, the animal also requires certain resources, such as food and water and nesting or roosting sites. The needed habitats and resources collectively form the “niche” of the animal. If an animal's niche is locally distributed, the animal may be found clumped, even if it is not particularly social. If the niche or habitat is patchily or irregularly distributed and the animal cannot move easily from one patch to another, it is said to live in a “coarse-grain” environment or to have a “coarse-grained” niche. Such animals often seem social when they in reality are not. If the niche or habitat of an animal is rather uniform, so that the animal can move about and find what it needs in many places, it is said to live in a “fine-grain” environment or to have a “fine-grained” niche. Such animals often seem solitary when they actually are reacting to one another and hence are social. These animals tend to be solitary because they do not need to follow others in order to get to the right environment.

      Within a fine-grain environment, or within one “grain” of a coarse-grain environment, animals may occur in groups even when they are not social. A “random” pattern of distribution, in which animals wander without regard to each other, brings asocial animals together at times. An even distribution is much more common, as in territories of many songbirds in which each pair occupies its own plot of ground; these creatures are actually social animals, in the sense that each interacts with its neighbours so as to keep them at a certain long distance. “Clumped” distribution of animals is also common; this situation usually is truly social in the sense that each animal interacts with its neighbours so as to keep them at a certain short distance. Regularity of the short or long distance that an animal keeps from its neighbours is thus as much an indication of sociality as is grouping; only the theoretical (and probably nonexistent) animal that completely ignores its neighbours is truly nonsocial. Time is also a factor in spacing; truly social animals have a tendency to move to the correct distances from each other and to maintain those positions over specifiable time periods, such as for the morning hours each day.

Dominance hierarchies and division of labour

      Social interaction in time and space is sometimes shown to the ethologist by patterns of following and leadership, although neither of these is necessarily social; following occurs in a dog tracking a rabbit, and leading is seen in an anglerfish luring a smaller fish for dinner by dangling a fleshy protuberance on the snout. In the Eurasian red deer (Cervus elaphus), an old female leads the does and fawns about. Spanish merino sheep have been bred to follow each other, while the Scottish highland sheep have been bred to be more independent; following may thus vary within a species according to its needs or to the environmental pressures on it.

      Following need not mean there is a leader. The first bird in a migratory “V” of geese or pelicans is not continually the same, and the leaders of a school of fish change every time the school changes direction.

      Leadership is sometimes, but not always, associated with a dominance hierarchy or peck order, which may or may not be a sign of social behaviour. Peck order, first noted in bumblebees, means that A pecks B, B pecks C, etc., but it does not necessarily mean that A leads C or B or that the three are interacting constructively. The dominant central males of a baboon troop tend to influence the direction taken by the rest of the troop around them; but the bullying dominant stag circling around a herd of red deer has to follow wherever the females decide to go, and his initiative is limited to running straying females back to the herd.

      Dominance hierarchies may occur whether or not there is social behaviour in the usual sense. Among several species of birds that follow swarms of army ants in Panama to catch insects flushed by the ants, the big ocellated antbird (Phaenostictus mcleannani) is dominant, the medium-sized bicoloured antbird (Gymnopithys bicolor) is next, and the small, spotted antbird (Hylophylax naevioides) is chased by all the other members of the flock.

      Crowding almost any two solitary animals together will produce a dominance hierarchy, in which one animal becomes boss or kills the other. This is a major cause of deaths in zoos and aquariums, but it is not necessarily social behaviour. Some biologists even say that dominance hierarchies are evidence of antisocial rather than social behaviour and are expressions of inadequacy in overcrowded social systems. It is certainly true that most peck orders appear in unnatural situations, such as among chickens in a henyard or animals in a cage. In most animals, the absence of a dominance hierarchy, rather than the presence of such, in a crowded context is a sign of a high development of social behaviour.

      A further interaction that the ethologist watches for in social animals is division of labour (labour, division of). Any two animals will, of course, divide up food or any other resource between them. Indeed, no two animals in nature ever have precisely the same niche; (niche) if two species have similar niches, they will tend to develop different ways of doing things, or one will exterminate the other. Ecologists call this the “competitive exclusion principle.” Man attempts to reduce insect competition by various methods of “control.” He kills off other animals by cutting down the trees in which they live. Most animals are less destructive and tend to divide up the world rather than to exterminate other species. Evolution, before the advent of man, seems to have produced continuously more kinds of animals and a greater division of niches, except in periods of environmental disaster. The three antbirds mentioned above tend to specialize in large, medium, and small prey; to the degree that these birds take different foods, they are cooperating better with each other.

      Division of labour also occurs within a species. Males and females of some woodpecker species forage in different places in the trees, taking different types of food. Some animals use the same resource but do different things to get it. The male huia (Heterolocha acutirostris), an extinct bird of New Zealand, apparently used his short straight beak to open logs while the female, with her long curved beak, removed the insect larvae from the long tunnels he exposed. Male and female birds often build nests together, dividing the labour equally in some cases.

      Social insects have more elaborate divisions of labour. Animals that cooperate by division of labour tend to use varied resources and to find more uses for them.

      Division of labour seems to be a passing phase in the evolution of most animals other than man. It is evidently of little advantage to most animal societies. The honeybee, the leaf-cutter ants, and other animals with division of labour nearly always occur only where there is little competition from more specialized animals. Few of the most advanced insects or other animals show division of labour. In habitats such as the coral reef and the tropical forest, division of labour tends to be among different species rather than within a species.

Social interaction

      Social interactions of various types are more important in determining degree of sociality than are most of the above characteristics. The only interactions between animals that are seldom considered social are behaviours in which animals take something needed by others. The question arises, however, as to how to classify the parasitic relationships of a fetus in the mother and the male anglerfish (Photocorynus spiniceps) on his mate, or the fact that killing by predators may help animals to avoid overgrazing their habitats. One could speak of communication of feint and chase in the interaction between moose and wolves. When a bird chases another off its territory, it uses communication and interacts with the other bird very strongly.

      Humans often consider chimpanzees or bees as more social than desert locusts, because the locusts have rather simple interactions. Male hummingbirds and birds of paradise, however, have their elaborate plumages and social displays because the females get together with them so seldom that they might not recognize a suitable mate without the displays. It seems generally true that elaborate rituals evolve where social bonds are most fleeting or likely to be disrupted. To determine sociality, one must look at the total spectrum of social interactions as well as at their diversity and productivity, rather than just at a single feature.

      Altruistic social behaviour is often found among animals. An altruistic animal is one that expends some of its energy helping another without direct benefit to itself, be it a mother bear protecting her cubs against their hungry father or a bird giving an alarm call that warns its neighbours of a hawk. An alarm call may help the bird itself, of course, by startling the predator or warning it that this alert bird will be hard to catch.

      Psychologists have found that a rat or monkey will slow its rate of pressing a lever for food if that lever also gives an electric shock to a nearby rat or monkey. Rats will take turns sitting on a platform so that others can feed without being interrupted by electric shock. Rats or pigeons can be trained to cooperate in getting food.

      Since the altruistic animal always loses something by its behaviour, the question arises why altruism exists. One answer is that, as the evolutionist Charles Darwin (Darwin, Charles) suggested, when an animal protects its offspring, it helps its kind to survive the process of natural selection. When porpoises help an injured relative to the surface where it can breathe, they seem to be following a pattern of behaviour that can be accounted for by evolution. Their altruism clearly helps the group and therefore becomes part of the genetic endowment. Altruism, significantly enough, is usually limited to an animal's relatives. Most social animals, such as penguins, feed only their own young. When the individual animal loses more than it or its relatives gain, as when female seals nurse young not their own, the question arises whether this serves the survival of the larger group or the species. Under some conditions, the survival of the group may be more important even than survival of the individual, as when the honeybee dies defending the hive. The worker honeybee, which is not able to reproduce, is in the biological sense not an individual so much as an extra limb of a collective animal.

      Reciprocal altruism, in which a benefit is later returned to the benefactor, need not be between related animals and may not even seem altruistic. Alarm calls of birds often alert entirely unrelated kinds of birds, which later may return the favour. An act that seems selfish in the short run is sometimes altruistic in the long run, or vice versa, in the case of maladaptation. Wasps, ants and termites that cannibalize or dominate nestmates at times of food shortage may better keep the colony from starving. Individual ants and bees are often lazy, spending most of their time resting or wandering aimlessly, but these unemployed individuals form an easily mobilized reserve in times of danger.

      Individual and group recognition are often important aspects of social structure. Ovenbirds (Seiurus aurocapillus) in North America recognize neighbouring males by their songs and react aggressively mainly to songs of strange males. Animals that have long parental bonds often show individual recognition. Herring gulls (Larus argentatus), for example, recognize chicks or mates by slight differences in voice or appearance. The larger or more ephemeral the society, the less there can be individual recognition between distant individuals and the more important becomes recognition by group characters, such as the “nest odours” of social insects. Ants, bees, and termites often attack strangers, or even members of their own colony that have been experimentally removed for a few days or washed. Many kinds of parasitic insects (beetles, flies, butterfly caterpillars), however, provide food or scents that gain them entry to a nest, then prey on larvae there.

      Other internal characteristics of societies are age structure, birth rates, and death rates. A young wasp or termite colony has few old animals, a mature colony has more, and a declining colony or one that is producing reproductive forms has few young. The old colony has a lower percentage of foraging workers than does the young colony, and has a lower birth rate and higher death rate as a consequence; but only the old colony produces reproductive forms.

      Societies also perform movements, such as nomadism and migration (see migration). Army ants wander nomadically after prey. Wildebeest and locusts of Africa emigrate to green areas of local rains; flocking or solitary birds migrate back and forth to escape winter or drought; anadromous fishes, such as salmon, move to the sea for food and to rivers to spawn; catadromous ones, such as eels, do the reverse.

      Migrants are often placed at a disadvantage compared to residents, for the latter can take the regular food supplies and leave only ephemeral sources for migrants. Migrants that follow army ants for food in Central America are subordinate to residents and succeed only when residents are absent. The migrant can turn its world from a coarse-grained one to a fine-grained or dependable one by migrating from one patch to the next, and by force of numbers migrants sometimes displace residents.

      Societies can make use of seasonal environmental changes by migrating locally, such as sowbugs clustering to estivate in hot weather or ladybugs hibernating in masses. Other societies show food storage; e.g., harvester ants (Messor) and wood or pack rats (Neotoma). Honey ants (Myrmecocystus) have a “replete” caste that bloat their abdomens with stored honey and hang from the roofs of underground chambers until tapped by other workers.

      Societies show population fluctuations, from extinction to explosion. Mass emigrations in some, such as lemmings and squirrels, occur mainly after population explosions or periodic extirpations of food supplies. Some populations, such as many protozoans, worms, and insects, normally undergo violent fluctuations, but are resistant to extinction. These are animals in which the adults emigrate or both adults and young emigrate. Animals in which the adults normally occupy a fine-grained habitat and only the young move, such as most higher animals, normally have relatively stable populations, but are easily killed off by a new predator or temporally unpredictable events.

      A major external characteristic of the more complex societies is that they construct things, or modify their environments. The elaborate air-conditioned castles of some termites, the path systems of feral house cats, and the patterns of singing at dawn among birds of ephemeral or coarse-grain habitats, all are “structures” created by animals.

      Cooperation and competition are major aspects of animal social behaviour. Social facilitation, as when yawning spreads through a pride of lions or chickens eat more rapidly together, shows that cooperative competition can be social. Social animals, which live close together, often interfere and fight more with each other, especially in early stages, than do solitary ones. A fair percentage of the communication between social animals involves “agonistic” or threat–submission behaviour. If this behaviour results in a more adaptive dispersion of the animals, it has been altruistic. Grouped goldfish and other animals survive heat, cold, metallic ions, and other “pollution” better than do isolated animals; but if too many animals aggregate, they pollute each other. Social groups therefore have an optimum size and density, based upon an equilibrium between advantages and disadvantages.

      Linking the internal and external characteristics of social systems are flows of energy and materials. Social systems use energy in building structures, or information-rich systems. Physically, one can measure the success of a social system by how efficiently and extensively it uses energy and materials and converts them to physical, biological, or cultural structures. Success in the short run can lead to disaster in the long run, as when elephants or humans destroy an African forest and then must starve or emigrate. Energy and material flows involve an interspecific web, the ecosystem, and must be measured over the long run and in general as well as locally or in the short run.

      Social behaviour, therefore, must include interactions between different kinds of animals. A flock of sandpipers in flight is not less social if it includes two species rather than one. If species cooperate, a flock of two species can even be more social than a flock of one species. At African waterholes, baboons keep the lookout while associated antelope are good at scenting predators. symbiosis is social, even though the late biologist Traian Savesculu of Romania was half right when he joked “Symbiosis is like marriage—a mutual exploitation.” Like all social organizations, it is both cooperative and competitive.

      Social behaviour may thus be defined as “more or less diverse and constructive interactions among two or more animals.” Social behaviour is usually constructive, productive, and adaptive; but it sometimes persists for a time after the evolutionary basis for it is gone. For instance, many kinds of hawks in the eastern United States have almost disappeared, but the flocks of small birds that were formerly their prey still form as vigilante groups.

Types of animal societies

      To understand social behaviour more fully, it is necessary to examine it throughout the range of animal life. W.C. Allee (Allee, Warder Clyde), in his classic book The Social Life of Animals, distinguishes two major types of animal societies. One is the parental, or familial, society, in which parent and offspring stay together for varying lengths of time. The other is the pair bond, or club, society, composed of individuals that come together from different families. This type was much emphasized by the 19th-century English philosopher Herbert Spencer (Spencer, Herbert) because it corresponded to his social (social Darwinism) Darwinist ideas. The social Darwinist does not like to admit that a weak son can win out if he has powerful parents; but recent work with rhesus monkeys shows clearly that the son of a high-ranking mother tends to be protected by his mother and hence gets to the top of the hierarchy even if he himself is a weakling. Parental societies are very common.

Parental societies

      Parental societies are found at all levels, from the cell to the monkey troupe. All animals provide for their young in some way. In every animal there is a period when the young is part of the parent and receives materials from the parent. Later, the young may partly or completely separate from the parent; in some animals, the more or less separate young is then helped by the parent, or helps it.

Parental behaviour among simple organisms

      Even some of the simplest organisms show colonial aggregations of the parental type. Some viruses form inclusion bodies in the cells they attack; these bodies are thought to be colonies of daughter viral strands. Other viruses form ordered arrays.

       bacteria, only a few steps up the evolutionary scale beyond viruses, also show parent–young colonies. Diplococci, which can cause pneumonia, are dot-shaped bacteria that have two daughter cells in each group. Streptococci form chains, and staphylococci arrange themselves in grapelike clusters. In all of these, and in a large number of other colonial bacteria, the offspring that are produced by a dividing parent generally stay together for some length of time.

      Protozoa (protozoan), a few steps beyond bacteria, also show parental sociality. Many reproduce by simple division and hence give the daughters help only before the split. Under difficult conditions, protozoans commonly form a protective “cyst” and divide within it. In such divided cysts 2, 4, 8, 16, 32, or even more daughter cells may associate until the cyst “hatches.”

      Some protozoans form definite colonies in addition to or in place of cysts. Volvox and many other slow-moving or sedentary colonial protozoans show differentiation or division of labour between cells of a colony. In Volvox, the forward cells have large eyespots and a few rear cells take care of reproduction.

      It is almost certain that sponges (sponge) evolved from colonial flagellate protozoans. Sponges are integrated networks of cells, some of them amoeboid (amorphous) and some flagellate. It has been shown that if a sponge is strained through cloth so that the cells are separated, they will reunite and form new sponges so long as a flagellate collar cell can rejoin an amoeboid cell. The sponge is thus on the border between colonial organization and integrated multicellular organization. One advantage of integrated multicellular organization, with different types of cells performing different functions, was probably that the sponges could become much larger than the largest multinucleate or even colonial protozoans and thus could capture these protozoans. This type of organization also provides strength: some cells can hold on in swift currents, while some can secrete skeletons and others concentrate on food getting. Thus cooperation gave sponges and similar multicellular animals an advantage in competition with even the largest and most aggressive single-celled animals.

      The colonial organization of cells into protozoan colonies or into multicellular animals will be referred to below as the “colonial-1” stage, in contrast to the colonial organization of attached multicellular animals—the “colonial-2” stage. The colonial-2 stage is well developed in successful aquatic animals just above the sponges; the coelenterates (cnidarian) (hydroids, jellyfishes or medusae, sea anemones). coral reefs bear witness to the success of colonial-2 growth in other coelenterates. Many different types of free-swimming colonies, such as the dangerous fish-killing Portuguese man-of-war (Physalia), exhibit huge complexity on the colonial plan. In corals and other colonies, the original individual is linked to its offspring in a network. Food material and chemicals are often exchanged between individuals over the tubes of this network. Often the different individuals in this network show division of labour. Sometimes, as in Obelia, there are only reproductive and feeding individuals. In Physalia, there are swimming individuals, stinging ones, and many others, including one that serves as a gas-filled float. The interdependence and communication in such a colony is so extensive that the colony seems almost to be an individual and is sometimes called a superorganism.

      Despite the great success of sponges and coelenterates, the main line of evolution goes onward through colonial-1 animals. The link was probably wormlike animals somewhat like present-day flatworms. Most flatworms and higher worms show very little association between parents and young.

From flatworms to insects

      The main line of evolution leading from flatworms to insects shows little parent–young cooperation or colonial development. The entoproct Bryozoa, or moss animals (moss animal), form treelike colonies like those of corals and thus show type-2 coloniality; but it is not certain whether the Bryozoa actually belong to the line leading to insects. A few wheel worms or rotifers, such as the free-floating Conochilus volvox, form colonies. A few annelid worms, such as sybellid fan worms, bud off chains of individuals in a manner like the flatworm Catenula. This is a common method of breeding in some annelids; the special rear “worm,” or “epitoke,” breaks off and swims to the surface, where it releases sperm or eggs and dies, often in huge swarms of epitokes as in the Samoan palolo worm (Palola siciliensis).

      Typically such worms as roundworms and earthworms strew their eggs about or attach them to something as soon as they are fertilized or brood the eggs only briefly. A few nemertine worms are viviparous—i.e., they produce live young. The annelid worm Ctenodrilus is said to be truly viviparous, the nutrition of the young coming via maternal blood vessels. Most mollusks take little care of their young. One chiton, Callistochiton viviparus, gives birth to young that have undergone development in the ovary. In a few bivalves such as the European oyster (Ostrea edulis), the eggs develop in the gill filaments. Most squids release single eggs or chains of eggs, but some members of the octopus group stay near their eggs and remove debris from them. The paper nautilus, Argonauta, forms a paper nautilus shell and the mother takes care of her eggs in it. At times the male hides in the shell.

      Peripatus and its relatives, the onychophorans, are intermediate between annelid worms and arthropods and have well-developed parental systems. Some Australian forms lay eggs, but others keep the eggs inside until young hatch; many of these are viviparous, giving the young secretions from the uterus.

      Not until one reaches such jointed-legged animals as crabs (crab) and insects (arthropods (arthropod)) does one find much extended association between young and their parents. A few scattered arthropods still have no parental care other than production of eggs. The female walkingstick casually drops eggs as she moves about. Many ostracods and copepods, and many of the edible shrimps, shed eggs into the ocean waters. Most arthropods, however, care for their young briefly.

      Scorpions (scorpion) are all viviparous or ovoviviparous (eggs developing in the mother), and many carry their young about. The female pseudoscorpion of the leaf litter often builds a little nest, and the young get nourishment from her in a belly pouch. The female solifugid, or sun scorpion, makes a burrow for her eggs and then brings prey to the young after they emerge from the burrow. The female whip scorpion attaches eggs to herself and carries them until the young go through several molts; she dies as soon as they leave. Spiders (spider) generally weave a silken case for eggs and young. The female wolf spider carries her young on her back. Some young spiders build a family or community web together. The harvestmen and mites mostly lay eggs in the environment, but some mites carry eggs until they hatch. Some ticks (tick) deposit egg masses, and hundreds of young seed ticks may stay together, to the dismay of a human when such a mass drops on him and starts to spread. Sea spiders (sea spider) (pycnogonids) are strange, for the male takes the egg mass from the female and cares for the eggs until they hatch, or slightly longer. Most crustaceans briefly brood their eggs, or eggs and young, often in special pouches on the body of the female.

      Millipedes often form a nest; the young Spirobolus later eat the material of that nest. Some female millipedes coil about the eggs for several weeks. Many centipede females brood eggs, but others do not. In symphylans, often considered a link to insects, the female carries eggs in cheek pouches.

Social insects (social insect)

      Insects show the greatest development of family structure among animals. Most so-called insect societies are, strictly speaking, families. Sometimes they are called colonies, but the individuals are not directly attached to each other as in the “colonies-1” of protozoa and multicellular animals or the “colonies-2” of corals. They might be called “colonies-3” because they are “attached” by chemicals as well as by social behaviour. The young stay with both parents or with the mother and form social organizations of high complexity. Social behaviour of this type is known among the thrips (Thysanoptera), Zoraptera, book lice (Psocoptera), web spinners (Embioptera), termites (Isoptera), and roaches (Blattoidea) of the more primitive insects, and in some groups of the higher insects—the aphids and lace bugs of the Heteroptera, and especially, in the ants, bees, and wasps of the Hymenoptera. Some of these groups bear little resemblance to the families of vertebrates. A critical observer might say of insect societies that the parents enslave their first children or their sisters, frequently with “drugs,” and thereby ensure better care of their later ones.

      Societies of lower insects are simple. The female (or male in the case of mole crickets, Gryllotalpa), works hard to build a nest and to protect its first offspring. The offspring may reciprocate by helping to build a colony web under a stone or leaf or under tree bark, as in the web spinners and book lice. In wood roaches, such as Cryptocercus punctulatus of the southeastern United States, the young must stay with the adults, because all have symbiotic protozoans inside them that digest wood cellulose: at every molt the roach loses all its protozoa (because the linings of the fore- and hindgut are also molted) and must eat the feces of another roach or die.

      In termites (termite), the male and female lose their wings after a dispersal flight and dig a cavity in which they raise the first young. These young have their sexual maturation inhibited by chemical secretions from their parents; instead of reproducing themselves, they work hard to make more chambers and get food for the next young. They often get fecal material from each other full of symbiotic protozoa to digest wood and also use the fecal material to build houses. The more advanced forms masticate wood and grow fungus on the pulp produced in that way. The young have a division of labour, some being workers and some soldiers; there are also nasutes, which have snoutlike processes that eject a sticky substance used in warfare to protect the colony. Such colonies may become huge and build houses higher than a man's head. The first parents are not so much the leaders of the colony as egg-producing machines cared for by their first offspring. Eventually some of the slaves achieve their freedom when the chemical secretion from their parents runs short; they develop wings, fly off, and start new colonies of their own.

      Some beetles (coleopteran) show behaviour approaching the social. A British rove beetle defends its eggs and young against intruders. Dung beetles dig burrows and store dung for their larvae. The male and female burying beetle cooperate to dig away the soil underneath small dead animals; the female feeds her larvae on regurgitated food. Bark and ambrosia beetles dig tunnels in wood and grow fungal spores; the female feeds her young on pieces of fungus while the male keeps away other males.

      Some moths (moth) and butterflies (butterfly) associate in the caterpillar stage. Social caterpillars, such as the tent caterpillars (Lasiocampidae) and the larvae of small ermine moths (Yponomeuta padella), make webs similar to those of colonial spiders but use them only to hide in rather than to catch prey.

      The origins of social behaviour can be seen in bees (bee) and wasps (wasp). There are solitary bees and wasps, all of which prepare a protected place for the egg and later the larva. Some “gall wasps”—as in “gall aphids” and some mites—sting plants, which then provide fleshy galls for the young larvae. The parent often provides food for the larva. The tarantula-killer wasp will sting a huge spider and store it in a drugged state by the egg. The “parasitoid” hymenopterans lay an egg on or in a wandering caterpillar to parasitize it. Some bees or wasps return to put a new spider or other food source into the nest after the first food has been eaten, a process called progressive provisioning. From this it is only a short step to having a single female care for several young in a compound nest, as in Polistes wasps, and another short step to having sisters or young stay around the nest and help care for the later young. In some insects, such as wasps of the genus Polistes, this is done by having the first or strongest female harass or dominate the later or weaker ones. Their sexual growth is repressed and they cannot lay eggs as long as the dominant female is there. Chemical dominance, or drugging, is the next step; in the more social bees and ants, chemicals produced by the queen are actually needed by the workers, and exchange of food and drugs (trophallaxis) is regular.

      Division of labour often occurs in ant and bee societies. Ants are often polymorphic (polymorphism), with small individuals working in the nest and medium or medium-large ones working outside; huge-headed individuals become protective soldiers or even use their heads as plugs to stop up the nest entrance to all besides members of the colony. Honeybees (honeybee) have division of labour (labour, division of) by age—the youngest bees feeding larvae, older ones building the comb, and still older ones flying out for nectar and pollen and bee glue. Many of the polymorphic differences are apparently determined by food, as when the new queen bee gets royal jelly regularly, while the smaller workers get royal jelly for only a few days. Other differences are genetic, as in the case of the male ant or bee, which comes from an unfertilized egg.

      These family societies of insects are diverse and successful. Termites and ants are among the most common tropical insects, bees and wasps among the common subtropical and temperate ones. The houses of termites—earth castles with shingled construction to shed rain and porous outer layers to control carbon dioxide and humidity—are equalled in their intricacy only by those of man. The honeybees communicate with chemicals and dances to tell each other the distance and direction of flowers.

      The ferocious defense of the nest by wasps and hornets avails them little, however, against the onslaughts of marauding hordes of army ants (tribe Ecitonini) in the tropical forests of the Western Hemisphere and of hordes of driver ants (tribe Dorylini) in Africa. The army ants do not eat trees or people, as early stories would have it, but they tear apart arthropods. The driver ants, which have scissor-like mandibles that cut flesh, can tear apart humans if given the chance. These are probably the largest of the familial or “colonial-3” societies. A large colony of the army ant Eciton burchelli may include 1,500,000 individuals, and the colonies of the driver ant Anomma wilverthi probably contain up to 22,000,000.

      The leaf-cutter ants of the Western Hemisphere live in huge underground colonies. They, along with termites and a few beetles and moths, are agriculturalists. The leaf-cutter ants cut strips of green leaves and make a paste of them in which they grow fungus. Their underground chambers may reach several yards. It is hard to realize that such huge colonies are extended families.

From bryozoans to humans

      In the other great line of evolution, which leads to man, the social use of the family has taken a different tack. Where the first line began with actively moving, wormlike individuals and ended with drugged, tiny individuals in huge families, the line that leads to humans begins with colonial, attached animals of the general appearance of corals but of the structure of worms and ends with social animals in which families play an important but relatively small role.

      Some early wormlike animals evidently settled down on the floors of ancient oceans, and to protect themselves had to develop shells (as in the lamp shells or brachiopods) or colonies with specialized defensive members (as in the moss animals or bryozoans). Brachiopods are solitary and shed their gametes into the seawater. Moss animals form colonies in which there is direct or partially impeded exchange of body fluids. Their societies show more division of labour than do termite colonies. There are feeding individuals, reproductive individuals, special whiplike individuals (vibracula), and bird-head individuals (avicularia) that hit or bite other animals settling on the colony.

      It seems incongruous to suggest that active vertebrates (vertebrate) developed from tiny wormlike animals living sedentary and colonial lives, but the future does not always belong to the strongest, biggest, or fastest animals of a given age. The moss animals, with their tiny encrustations or filamentous colonies, are internally much advanced over the more abundant corals.

      One major side branch of this line of descent does lead to the nonsocial echinoderms (echinoderm)—starfish, brittle stars, sea cucumbers. Few of these animals take care of their offspring, and even their gametes tend to be shed broadcast into the seawater. Some sea stars, brittle stars, and sea urchins of the Arctic and Antarctic brood their eggs. In some, as the brittle star Amphipholis squamata, the young are attached to the mother and get nourishment from her. Some sea cucumbers, equally divided among cold-water and warm-water forms, brood their eggs externally or, as in Thyone rubra of California, inside. A few sea lilies or crinoids brood eggs or young.

      There is also little parental care in several of the wormlike side branches of this line of descent. Pogonophoran (beardworm) worms, which even lack a digestive tract, sometimes brood eggs in their tubes in the ocean mud. Arrowworms (Chaetognatha) occasionally carry eggs about, but most release them into the ocean waters where they swim. The arrowworms are successful predators, but the line to vertebrates leads for the most part through the colonial or sedentary filter feeders—the pterobranchs (pterobranch), the acorn worms, and the tunicates or sea squirts.

      The pterobranchs are sedentary, colonial wormlike animals, with a central stalk in some colonies but no direct connection in others. The individuals of the latter wander in and out of the colony tubes. Pterobranchs are related to burrowing solitary acorn worms, the hemichordates. All these animals release their eggs and sperm rather casually into the ocean.

      The sea squirts (sea squirt) (Tunicata (tunicate)) are mostly soft spongelike masses that cling to rocks or pilings in the sea. Most shed eggs into the sea, but some brood eggs or young and release them partly grown. The young are either free-swimming tadpole-like animals or are budded from the adult to form a colony.

      The line of descent up to this point is, curiously enough, closely associated with colonial animals, while the line that led to insects produced rather few colonial animals. It has been suggested that advances made during periods of coloniality may produce better free-living individuals and vice versa; the inference is that drastic new changes in a colonial animal can be perpetuated because of feeding by the rest of the colony and later be incorporated in a viable free-living combination.

      Some biologists, including Darwin (with his vested interest in competition), have suggested that the sea squirts and all the other colonial animals are unimportant sidelines in evolution. They suggest that the mainline passed through nonsocial, competitive, free-living, wormlike and, later, tadpole-like animals. Wormlike animals led to animals like arrowworms, to the tunicate tadpole, and then to fishlike animals such as Amphioxus.

      Certainly the next steps were through free-swimming animals with relatively little family life—cephalochordates (lancets) and the jawless fishes. Modern lampreys make a nest for external fertilization, but the hatching larvae make their own way to live as filter feeders in the muddy debris of stream bottoms.

      Many jawed fishes take little care of their eggs or young, but there are some major exceptions. Many sharks, skates, and rays give birth to live young, and some have placentas to nourish them. Some fishes make nests; the Siamese fighting fish (Betta splendens) and others make bubble nests at the surface, while sticklebacks (Eucalia) and a mormyrid fish (Gymnarchus) make weed nests, and such fishes as salmon dig spawning nests in the bottoms of streams. Stickleback males fan their eggs until the young hatch, making sure there is enough oxygen. Other fish, such as the black-chinned mouthbreeder, fan their eggs by keeping them in their mouths. Other mouthbreeder fish periodically spit out the young fry and take them back in until the young are feeding well. Mouthbreeders include a freshwater catfish (Loricaria typus) and some marine catfishes (Galeichthys felis and its relatives), plus cardinal fishes (Apogonidae). There are several fish of a dozen different taxonomic assemblages that bear their young alive, among them the surf perches (Embiotocidae) and the mollies (Poeciliidae). Some have a placenta-like arrangement to nourish the young until birth.

      While care of young by the male is frequent in fishes, it is rare among invertebrates (where the sea spiders are the only major example). Care by the males frees the female to obtain more food and hence raise more young per unit of time, which may be necessary in the event that food is difficult to find.

      Male care of the young is well developed in lungfishes, predecessors of land vertebrates. Most salamanders and frogs, on the other hand, are not very good parents. The male Surinam toad (Pipa pipa) presses the eggs into the back of the female, and the young of Rhinoderma darwinii go through development in the vocal pouch of the male. The live-bearing frog (Nectophrynoides) of Africa, in which the young hatch within the mother and remain with her for protection, is another exception to the general rule that amphibians (amphibian) release their eggs and care for them little.

      Among reptiles (reptile) the best parental care is in alligators (alligator) and some crocodiles (crocodile), where the female makes a mound of dead leaves or sand and stays around to protect the eggs, to release them when they hatch, and to guard the young for perhaps as long as a year.

      Birds are well known for parental care. Most build nests, incubate eggs, and care for young. The males commonly help the females in this. Often young birds stay with their parents a year or more, and numerous examples are known of the young of one brood helping to feed the young of later broods. Often the young help the parents defend a “group territory,” as among Australian bell magpies (Cracticus) and Mexican jays (Aphelocoma ultramarina).

      The most advanced parental society yet recorded among birds is that of the ocellated antbird, which follows swarms of army ants in order to capture insects they flush in the neotropical forests. This bird's young stay with their parents for several months, then go and find mates, but return to their parents periodically for several years. The young bird and its mate are accepted as part of the extended family; they are not chased away as often as are unrelated birds.

      An even greater organization of parental care is found in mammals (mammal), except that the males seldom help care for the young. The young are usually nourished before birth by the placenta of the mother, except in the egg-laying duck-billed platypus, the spiny echidna, and in marsupials. The young of marsupials are born prematurely and grow in the pouch of the mother for long periods. All mammal young, even the platypus and spiny echidna, must lap or suck milk produced by the mammary glands of the mother. This ensures that there is a strong family association between mother and young.

      Commonly, groups develop around a mother and may be joined by other such groups and by males to form bands, troops, and herds. Troops of monkeys and apes are basically families or grouped families. These and wolf bands include males, which may help to raise young. The “extended families” of humans lead to tribes, states, and nations.

      Nationalism as a force in human affairs is commonly related to mother and home and family, as well as to interlocking family relationships even more complex than those of ocellated antbirds or wolf societies.

Societies with sexual bonds

      Nonparental social relationships fall into two categories, sexual bonds and nonsexual bonds. Normally, only the latter can involve members of two or more species. Sexual bonds lead in many animals to parental bonds, of course, but differ in that the bond is normally between offspring of different families. The reason for this is that the main advantage of sexual union is to combine the good genetic features of two different lines. Some young, of course, will have the bad features of both lines and will be eliminated—a wastage tolerated in nature as a necessary expense.

      Most animals depend on elaborate behaviour (reproductive behaviour) patterns to bring the male and female and their gametes together at the appropriate time, rather than using the seemingly more certain processes of asexual reproduction, virgin birth, hermaphroditic self-fertilization, or male parasitism. Many marine animals shed eggs and sperm into the water or into special nests but do so only when chemically stimulated by the presence of substances from the opposite sex. Other animals of this kind use their “internal clocks” to release gametes only at a certain time of day or year. Samoan palolo worms (palolo worm), for example, form special gonadal body sections by budding, and then release them to swarm in very large numbers at the surface of the ocean according to a schedule set by the Moon. The grunion (Leuresthes tenuis), a small Pacific fish of the silversides family, is well known for its males and females meeting to fertilize eggs high on the beach at the highest tide each month and at the highest waves of that tide as well. The synchronization of male and female requires them to have an internal lunar clock, such as that known for the colour changes of fiddler crabs.

       courtship must basically ensure two things: that the correct male and female get together at the right time with as little loss as possible; and that the offspring have the best possible chance to survive. Ensuring these two things has led to elaborate courtship patterns in animals. Where different kinds of animals that look, smell, or feel alike coexist, each individual must be especially careful not to hybridize with the wrong species. Otherwise it will waste its eggs or sperm in a union that will produce no young, or young that are malformed or maladapted for the world into which they emerge. Animals often develop complicated odours, colours, or voices as means of identification. There are many species of fruit flies of the genus Drosophila, and to avoid mismatings, each species has its own pattern of waving the wings by the male. The sight and sound of the wrong pattern of waving is enough to cause a female fruit fly to flee (see reproductive behaviour).

      Where there is only a limited breeding area or a patchy environment in which the good areas are restricted, strong male–female differences are advantageous. In these cases the males have to advertise, often with song, to help females locate good areas. Males of species whose courtship displays are performed in groups usually have to compete more directly with each other and thus tend to develop large size or striking colours, overpowering scents or voices, or other exaggerated features. Female domestic chickens, sage grouse, and baboons tend to copulate mainly with the lordliest and most dominant males. This is not so evident in other animals, in which the females tend to mate with the male holding the best territory. The dominant male is likely to be the oldest one, the one that has proved he can survive and hence is “fittest.”

      The success of the “supermasculine” or lordly males in a few species may be advantageous only to those males. A few lordly males often usurp the few suitable places to breed, as in male sea elephants (Mirounga angustirostris) on Pacific beaches and in male red-winged blackbirds in North American marshes. If the lordly male blackbirds are eliminated, however, other males come in and the females breed with them just as quickly.

      The supermasculine males in these species, full of pomp and strutting, seldom care for their young. Baboon males, it is true, do at times stop fights between lesser animals and drive away leopards or other predators. But usually the female takes care of the young herself. It may even be an advantage if she is “ladylike” and unobtrusive, so that the lordly male may draw predators away from the young. Keeping the male away from the young may also allow the female and her young more food. If environments are limited in food, keeping excess males out of the breeding area clearly is an advantage.

      Supermasculinity, as well as being correlated with female care of the young, is also associated with polygamy. The mating of several animals of one sex with a single individual of the other sex tends to be associated in birds and mammals with great differences between the sexes. Serial polygamy, or the mating of an animal of one sex with several of the other sex at different times, may also occur. Promiscuity, or the mating of each female with several males and each male with several females, tends in supermasculine animals to resemble serial polygamy. monogamy, or the mating of each male with one female, tends to occur mainly in animals with little difference between the sexes.

      Having many mates does not necessarily mean that an animal is more social than if it has only one mate. In most cases, the polygamous male spends much time driving away other males and little time courting his females. His females spend little time with him, because they are busy raising many young—with little care for each. Among African weaver birds (Ploceus), monogamous species of the forest have smaller clutches than do polygamous ones of the savanna.

      The whole system of lordly males, ladylike females, polygamy or serial polygamy, and multiple young tends to occur mainly in animals with restricted and undependable sources of food and other necessities. One investigator found that males of the long-billed marsh wren (Cistothorus palustris) in Washington, where their marshes varied greatly in quality, had several mates; females went to males with good territories and left neighbouring males, with poor territories, mateless. Another investigator found that in Georgia, where the marshes were everywhere about equal in food supply and nesting cover, the long-billed marsh wrens were usually monogamous. The correlation suggested by many recent studies is this: sexual dimorphism and diethism (behavioral differences) arise in animals in which environmental opportunities are restricted due to undependability or local distribution.

Nonfamilial social bonds

      Social behaviour also occurs among animals that are not necessarily related by parental or sexual bonds. A “flock” or “band” of animals may be formed of only one family in some cases, but often several families or individuals join together.

Spacing

      As previously noted, social organization within a species may be shown not only by the presence of clumping or positive movement of individuals but also by even spacing resulting from negative movements away from each other. Sociality is shown more by the presence of a definite spacing than by nearness.

      There is little evidence for social spacing in protozoans and simpler beings, such as viruses and bacteria. Most recorded groups of unicellular or lower animals are probably parental or sexual groups. There seem to be few social interactions among microorganisms, but this apparent dearth of social behaviour may be an artifact introduced by the disturbance of observation.

      Most colonies of sponges (sponge) and coelenterates seem to be parental colonies or aggregations in favourable sites rather than nonfamilial societies. There is little information on nonfamilial social organization among colonial-2 animals, even among those that can move, such as the colonies of Portuguese man-of-wars (Portuguese man-of-war) or the planktonic rotifer or sea-squirt colonies. Most worms and their relatives are not known to react to each other or to form social structures of the “flock” type. Little is known about mollusk organization; but the simple fact that mollusks do not pile up on top of each other suggests that they are capable of negative social reactions.

       barnacle larvae prefer to attach next to another member of their own species or on a place where one of their species has just been removed. They avoid settling on top of another member of their own species, even though they readily settle on a member of another species. They react in part to chemicals that are specific to their species. Barnacles, then, aggregate in colonies but within a colony space themselves out. If the multicellular animal is a colony-1, the coral colony a colony-2, and the bee society a colony-3, the barnacle society may be called a colony-4. Colonies-4, in which the interactions take place between unrelated, unmated, and unattached individuals, are regular in arthropods. In many cases the existence or nature of a colony-4 is not obvious or is problematical. Bees form colonies-3 and perhaps also colonies-4, for colonies of bees space themselves out in the environment and avoid establishing themselves too close to other active colonies; but there is no evidence that bee colonies avoid getting too far apart, although if they did then mating between bees from different colonies would become difficult.

      Colonies-4 are known among other arthropods (arthropod). Tube-dwelling amphipods form colonies but chase each other and avoid getting too close. They show the phenomenon of “personal space,” or “individual distance,” as surely as do swallows sitting on a wire, among whom a new arrival settling will sometimes cause shifting outward by individuals on both sides. Individual distance or personal space is a fairly sharply defined space around each individual that can be penetrated by another individual without hostility only after certain overtures.

      The amphipod colonies also show the phenomenon of territoriality. Territoriality (territorial behaviour) differs from personal space in that a territory is centered on some object outside the body of the animal itself. The male bitterling (Rhodeus sericeus), a European fish that lays its eggs inside a freshwater clam, will chase male intruders away from his clam even if the clam gets up and moves several feet. The male house finch (Carpodacus mexicanus) of North America chases other males away from his female, wherever she moves. More often, however, the external reference for territory is a fixed plot of ground, a nest hole, or some immovable set of objects. The animal may chase out intruders or tolerate them in the territory, but in his territory he is in charge. Work with bicoloured antbirds in Panamanian forests suggests that a territory may be defined as “an external referent in which one animal or group dominates others that become dominant elsewhere.” A pair of bicoloured antbirds permits others on its territory, but as soon as the pair crosses a boundary line into another territory, it becomes subordinate to the pair of that territory.

      Territoriality is known to exist among insects such as dragonflies and ants, some fish, a few frogs, some lizards, most birds, and many mammals. It probably exists, at least in chemical forms, in tube worms of a muddy beach or rocky shore, and perhaps even among sedentary protozoans.

Swarming

      Personal space and territoriality are definite negative signs of coloniality-4, but there are also positive signs. Mutual repulsion is only part of sociality, for mutual attraction must also exist. Mutual attraction is found in many arthropods above the barnacles. Some of the best studied examples are the mating swarms of ants, flies, midges, and, especially, fireflies. Another example of mutual attraction is the migratory horde, of which the African migratory locust (Schistocerca migratoria) is the best studied example.

      The synchronized communal displays of the fireflies (firefly) of Thailand are among the most impressive exhibitions of the insect world. The gatherings of thousands of males on the mangroves of the coastal swamps have been described as a city of pulsating glitter, every male anticipating the flicker of his neighbours and flashing in unison with them. Communal mating displays (display behaviour) of this type are common in birds such as manakins, sage grouse, ruffs, and birds of paradise, and are called lek displays. Presumably, the communal display enables females to find the males more easily. Seldom do bird leks approach the numbers or synchrony of a firefly lek in Thailand, but several male manakins sometimes cooperate in a synchronized cartwheel dance. It is difficult to explain why males competing with each other for mates should help one another, but the phenomenon has been well documented.

      The legendary colonies-4 of the migratory locusts (locust) are far larger and more impressive than the migratory colonies-3 of the army and driver ants. When food is abundant, the locusts disperse widely and grow up in what is called the “solitaria” phase. As the locusts crowd and encounter each other, they begin to change colour and enter the “gregaria” phase, in which they look so different that they were once considered a separate species. The “gregaria” locusts behave differently too, for they are excitable and social. They begin to march over the ground as food supplies diminish. Finally they take wing in huge hordes and fly downwind to a low-pressure area where rains have recently fallen. Here they descend on crops and other vegetation, eating it to the ground before flying to the next low-pressure area. The extinct migratory hordes of passenger pigeons were apparently similar in their effects on vegetation.

      Many other examples of flocks occur in higher animals, especially insects (social insect) and vertebrates. Most show little internal structure. The migratory hordes of armyworms that devastated midwestern corn fields in the United States before the days of synthetic insecticides, the swarms of male and female palolo worms in the ocean, the feeding swarms of sharks, and the dense schools of herring are all examples of flocks with little internal structure. The Austrian ethologist Konrad Lorenz (Lorenz, Konrad) calls them “anonymous flocks,” because it matters little if individuals change places and bonds are seldom individualized. When the fish school turns, it is like an army platoon turning to the flank, for the former side fishes are now the leaders.

      The mating choruses at frog ponds provide an example of an auditory lek. Some salamanders congregate to breed, generally by sight and by odour, in running streams. Snakes form winter dens in which there may be hundreds of individuals rolled up in balls.

      Among birds, pigeons (Columbidae), starlings (Sturnidae), and various blackbirds (Icteridae) form dense flocks that wheel about in the sky or mill along the ground during foraging, the rearmost flying ahead to become briefly the leaders. Shorebirds and gulls gather on mud flats or elsewhere to feed. Such birds as the brown creepers (Certhia familiaris) reduce the winter cold by clumping together at night. Flocks of geese are made of many families of geese. Many birds gather into huge roosts, containing thousands or even millions of individuals in the case of the red-winged blackbirds (Agelaius phoeniceus) of North America. Tricoloured blackbirds (A. tricolor) of California are even more colonial than redwing blackbirds when nesting and by sheer force of numbers push into colonies of the more dominant redwings and displace them. The nesting colonies of queleas (Quelea quelea) in Africa contain millions of nests. There are many such colonies of birds, such as the phenomenal colonies of seabirds that are found on islands throughout the world.

      Mammals often form herds or packs. Many herds are more structured than bird societies, simply because many mammal groups are combined families plus males. Huge migratory herds of wildebeest and zebra wander the African plains. Each herd of zebra includes many familial harems that are held together by individual males. The herd of Scottish red deer is a matriarchal group led by an old female and composed of her extended family plus other extended families like hers.

      Hunting mammals often have even more structured groups. A male and female wolf (Canis lupus) and their offspring form a hunting pack that may fuse with another pack or split apart. African hunting dogs (Lycaon picta) and hyenas (Hyaena and Crocuta) form similarly flexible hunting packs, which are said to be even more effective than lion groups at running down prey.

       primate troops are often as complex as societies of hunting mammals or more so. Superimposed on their parental and sexual bonds is a group organization based on the occupation of a given area. The troop may also accept animals from outside. The society of baboons (baboon), as studied on the plains of Kenya, is very highly organized. Around the edge of the troop as it moves are the subadult males, watching carefully for predators and snatching bites of food when they can. Inside, the playful groups of juveniles stay close to the central hierarchy, a cooperating group of two or three big males that keep the subadult males at the periphery. The males of the central hierarchy are replaced, as they get old and toothless, by brash young males moving in from the periphery. With the central hierarchy march the females and their infants, protected both by the big males and by the peripheral younger males. The society is integrated by mutual grooming sessions, in which the big males get most of the grooming, and by domination by the big males.

Interspecific associations

Individual animal interactions

      Associations of animals often include more than one species. These groups may be called colonies-5 or colonies-0, since there is recent evidence that the nucleus and other parts of the cell were originally symbiotic viruses and bacteria. The most intimate form of interspecific association is that known as symbiosis, or mutualism, in which dissimilar organisms live together.

      Multicellular animals often live on or beside other animals. Small fish live in the tentacles of some jellyfish, sea anemones, and even the Portuguese man-of-war, yet are able to evade or inactivate the stinging cells. Some hydroids and worms live on tubes of other worms or on the shells of other invertebrates. The tubes of worms and shrimp often harbour other worms or fish. At times, the animal will live only on one kind of shell and is found nowhere else. Paleontologists have found some evolutionary sequences in which such an animal first lived on rocks and shells of a wide variety of types, then developed larger forms that lived on one type of animal and probably got food from it.

Complex associations

      Slave making is a kind of social relation that verges on parasitism. Certain kinds of ants raid colonies of other kinds of ants, carry off their young, and raise them as slaves. The slaves are perfectly socialized members of the colony and probably do not even realize that their social behaviour is misdirected. They exchange food and drugs with their captors as willingly as they would have with their own species, had they been reared by their own workers.

      One of the most complex associations is that of animals around army and driver ants. In the huge colonies of army ants live dozens of other kinds of insects, millipedes, and mites. Some help clean debris below the nests; some have chemicals that allow them to fool the ant security guards and enter the colony. Mites, beetles, and others ride on the ants or march in their columns. Some may help the ants by cleaning them or by giving them chemicals they crave. Others are like wolves in the fold, eating the food of the ants or even their larvae. The swarms of ants are also waited upon by many kinds of flies and birds. The flies lay eggs on insects and spiders fleeing from the ants. The birds capture animals flushed by the ants. In the tropics of the Western Hemisphere, nearly 50 kinds of birds follow the army ants persistently and would probably die without them.

      Some of these associations may not be social in any accepted sense of the word. Humans are not social with rats and fleas merely because they live with them. Some interspecific associations, however, are definitely social. These include the mixed flocks of antelope, zebra, and wildebeest on the African plains, for example, and mixed flocks of birds throughout the world.

      One can travel for hours across the African plains or through a tropical forest scarcely seeing an animal and suddenly be surrounded by a herd or flock of many kinds of animals. Usually each animal eats a different kind or type of grass or fruit or insect, although sometimes there is overlap in the foods taken or ways of feeding. The flock moves along together, not spending much time at each concentrated food source. Often it includes parental groups (colonies-2 in the case of mothers carrying young, or colonies-3 after the young separate).

      The fact that forest flocks are usually of several species rather than one probably reflects the fact that forests have more species of animals, and hence each species has less of a food supply and must not allow competitors of its own species about it, even its own offspring. In less complex habitats, there are usually very few species, and the animals can tolerate their own young even though these are competitors. They may even use their young—to detect predators (in the case of baboons) or to build a “city” (in the case of bees and ants).

      When a forest (ecosystem) is destroyed and begins to grow back, the first animals that come in tend to be kinds that are solitary and very antagonistic or uncommunicative. Later, flocking animals become more common, although they still resist groups of outsiders. Finally, as the mature forest re-establishes itself, one finds mostly paired animals that do not keep their young with them. These paired animals tend to associate with pairs of other species to form mixed flocks. Eventually, every animal links itself with every other in the system, forming what ecologists call a complex “food web,” “ecosystem,” or “web of life.” It is gradually being recognized that such a web is socially cooperative as well as socially competitive. The ecosystem eventually approaches a stage of “colony-6,” or what the French biologist and philosopher Teilhard de Chardin called the noosphere.

Dynamics of social behaviour

Costs and gains

      Social behaviour among humans is often regarded as an end in itself, the expression of a basic drive that has no necessary purpose. Biologists doubt that any animal has social tendencies without some adaptive advantage.

The costs

      Social behaviour and communication not only take an animal's substance and energy; they impede feeding, drinking, and other inputs necessary for life. The first cells that associated with other cells to form multicellular filaments lost the ability to absorb on the side by which they were attached. Perhaps the reason most multicellular filaments occur among animals that are attached to the ground or to some other surface is that such animals lose less proportionately than members of free-floating aggregations; attachment on one side to the ground already limits their input. Locomotion is impaired if animals must stay together. The single-celled ciliates could not readily have evolved into higher organisms, because dividing them into many joined cells would have slowed down these fast-moving predators. A speedy golden plover trying to stay with other shorebirds in a mixed flying group near shore constantly turns back to keep with them; it is impeded by its social tendency.

      Social behaviour also attracts enemies. Groups of animals have epidemics, while solitary animals seldom do. Many disease-carrying parasites spread much more easily at times when animals are together. Some rabbit fleas are even adapted to the hormonal cycles of the rabbits, so that they reproduce at the times of year the rabbits are reproducing and hence are social.

      Predators, like parasites, often have an easier time if animals are crowded together; the animals are often busy reacting to each other and the predator can sneak up without being observed. Their communicatory systems may even attract predators. Tuna prey specifically on fish in schools; a small hawk in tropical America (Accipiter superciliosus) mainly on mixed bird flocks.

      Social behaviour increases the number of interactions between animals and thus the chances of conflict. The conflicts may be solved by fighting, by patterns of dominance and submission (peck orders (dominance hierarchy)), or by mutual avoidance. Mutual fighting and mutual avoidance have the same result—a partitioning of resources for which the animals are competing.

The gains

      Against these disadvantages of being social, it is possible to set a number of clear advantages. They fall into six broad categories, corresponding to the six possible kinds of animal behaviour. By social behaviour animals gain: (1) food and other resources, (2) reproductive advantages, and (3) shelter and space. They are enabled to avoid (4) physical and other small hazards, (5) competitors, and (6) predators or other large dangers. The first and third of these gains are reactions to desirable things of small (1) and medium to large size (3) respectively; the fourth and sixth are reactions to undesirable things of these sizes.

food

      The value of being social in getting food is obvious in the case of hunting bands. Cooperative hunting has been found among wolves and African hunting dogs, hyenas, lions, killer whales, porpoises, cormorants, white pelicans, pairs of eagles and of ravens, tuna when chasing small fish, army ants, primitive and modern men, and many other animals. Animals that hunt cooperatively can trap, chase, and tear apart prey that would otherwise be too fast, strong, or large for them. In African hunting dogs the chase is run by the leader of the pack, but the rest keep the antelope or other prey from dodging left or right and also help fall on it when the leader catches it. Flocks of wattled starlings (Creatophora cinerea) fly after African migratory locusts and surround one group after another, eating every trapped locust from each group. In army ants, the individuals are bound to each other by chemical “trail substances” so that no individual gets far from the group; when one finds prey, it grabs it and emits an “alarm” chemical that causes nearby ants to grab, bite, and sting so that the prey is overwhelmed within seconds. They then tear the prey, usually insects or other arthropods, limb from limb and carry it back to the nest.

      Interspecific groups of birds are sometimes food-getting societies. Drongos (Dicrurus species) of Africa flush much food, and other birds follow them to get it. Honey-guides (Indicator species) of Africa lead honey badgers or men to bee nests and eat wax after the mammals break open the nests for honey. Hawks have been known to follow railroad trains for the same reason, and hornbills and hawks follow monkeys. The birds, lizards, flies, and other animals that associate with army ants offer other examples of interspecific food-providing associations. One animal may steal food from another, as American widgeons (Anas americana) steal grass from redheads (Aythya americana).

      In addition to hunting and flushing food cooperatively, animals sometimes lead others to food or teach them to use it. Parents, especially among mammals, often teach their young to hunt or lead them to food. Animals that must migrate or depend upon seasonally available resources often depend on others to show them what foods are good and where. Vultures and jackals flock to carcasses on the African plains. American robins (Turdus migratorius) in California have been observed learning to use certain berries after flocks of cedar waxwings (Bombycilla cedrorum) came through and started eating the berries. Tests with a tape recorder show that the recorded calls of some birds that follow army ants will attract unrelated kinds of birds that also follow ants. In the laboratory, some animals learn to push a lever for food by watching others get food that way and learn to avoid distasteful foods by watching others cough it up. In studies of Japanese monkeys (Macaca fuscata), the habit of washing potatoes before eating spread from the younger to older monkeys of a troupe. In Britain, a few titmice learned to open milk bottles and drink cream; the habit spread much too rapidly to be a genetic change.

Reproduction

      The reproductive (reproductive behaviour) advantages of social behaviour have mostly been discussed earlier. It was noted that sex is a way of combining desirable genes from different lines, genes that otherwise might slowly or never get together. In many lines of animals, parental behaviour is clearly useful in protecting or teaching the young. This normally requires the adult to have fewer young. The careful parent loses in time and energy and number of offspring but comes to prevail in evolution if it has more descendants than does a careless parent that lets its young die. The careless parent prevails if it can get more young out by caring for each one less; some parasites are careless parents because each of the young needs little care and a large number must be produced to get to an extremely distant host.

Shelter

      Social behaviour is often used in habitat selection and shelter selection, even to the extent of making it possible for the animal to improve the environment it finds. Male birds that later will fight with each other over territorial boundaries gather first at areas where they hear another bird singing, rather than hunting for a more isolated (and probably unsuitable) place. Certain beetles that attack pines put out a scent that attracts other beetles; only as a result of concerted attack by all beetles can the protective pitch of the tree be reduced so that all may enter. Movement to a flock is a good way to find a patch of habitat or a shelter. It has been suggested that flocking increases the accuracy of migration, since the average direction taken by a flock is more correct than the individual directions taken by individual birds. Small flocks of European starlings returning to a California roost were less accurate in their direction than large flocks. Cooperative building of structures is well known in humans, prairie dogs, rats (whose tunnel systems rival the catacombs in complexity), beavers, certain weaver finches, wasps, bees, termites, and many others; symbiotic use of structures occurs in many animals.

Hazards

      Social behaviour can also help animals avoid small hazards. This includes avoiding heat or cold and wet or dry situations as well as preening or grooming to keep off dirt, parasites, and other small environmental hazards. A goose cleaving the air for its companions at the front of a V-shaped flock, a parent bird brooding its young or sheltering it from the Sun, a group of creepers roosting together to help each other survive the cold winter night, and a group of baboons grooming each other to pick off ticks furnish other examples.

Competitors

      Dangers from competition are avoided by agonistic behaviour (agonism). The five basic types of agonistic behaviour are aggressive display (threat), submissive display (appeasement), attack, avoidance, and fighting.

      Social aggressive display is not common. Males of a troupe of howler monkeys all yell at a neighbouring troupe to make them keep their distance. Baboon males in the “central hierarchy” cooperate to keep aggressive young males from winning, backing each other up with threats. Social attack occurs in some birds and mammals that keep group territories and may lead to fighting if the other group attacks or threatens.

      Highly social submissive display and escape also are not common. A baboon troupe may retreat as another moves in at a water hole. But even when a single animal retreats from a competitor it is a social act. Territoriality is (territorial behaviour) certainly a system in which an animal defends its right to be dominant in part of its home range. The basic feature of territoriality, however, is not aggression in a certain area but submission outside that area. The common idea that strong animals survive and the weak do not is true only in the short run, for in a few generations all reproducing animals are equally strong. Strong animals will begin to lose if they keep on chasing others. An animal that keeps too large a territory will spend more time chasing away intruders than it will in eating or reproducing, unless it can get others to help it. Bees get help by drugging the nonreproductive members of their colony. Most animals limit themselves so that the territory of the most dominant animal or group of animals never exceeds about twice the size of the least dominant animal or group of animals of that species. Most often the young animal has a small territory but defends a larger one as he gains experience, then gradually loses it as he reaches old age.

Predators

      The final reason for social behaviour, and one of the most important, is to avoid predators or other large dangers. Just as animals can sometimes overcome large prey by grouping to attack it, so they can sometimes overcome large predators by grouping to defend against them. Cooperative and spirited attacks upon predators occur in most animals that protect their young and are a regular phenomenon in gull and tern colonies, in baboon troupes, in bees and wasps, and many others. “Mobbing” is a similar phenomenon in which the attack is not carried all the way to the predator but so harasses it that it departs or at least is prevented from getting its prey. The massed effect of many mobbing birds is more intimidating to a predator than is mobbing by one or two birds.

      Grouping also helps against predators because a predator is distracted by the “confusion effect” of so many shapes, sounds, or smells. Human hunters know that one cannot shoot a duck out of a flock by aiming at the flock; the shot is more likely to pass between the birds than if the hunter aims at one of them. Similarly, hawks have been seen to drive through a flock and miss every bird. Successful predators either dive to break up a flock and then grab a separate animal or pick off an outlying one at the start. Butterflies on tropical trails also swirl up in a confusion effect from a mud puddle. The phenomenon is caused by the difficulty the eye or other sense organ has in analyzing or following very complex motions that cross each other.

      Another advantage of the group or flock is that many eyes can see a predator more quickly than can one pair of eyes. Ornithologists have found that social birds are nervous outside of a flock and must spend too much time watching to be able to forage effectively. Certain species that forage by peering in dense vegetation are especially in danger and must associate with other species that look about more actively in open foliage. The peering species often are good at yelling and perhaps help the other birds by scaring or disturbing predators. This suggests that a social organization may have many reasons for being.

Development factors

      As noted above, behaviour changes somewhat in the course of evolution. Biologists commonly call the genetic determinants of behaviour in a line of organisms instinct. Every behaviour pattern, however, can be changed somewhat by the individual animal in the course of its experience. The old view that instinct and learning are two different types of behaviour is seldom accepted today, even though some kinds of behaviour certainly have little learning superimposed.

      The real question is how social behaviour develops. It is possible to breed animals for aggressiveness or nonaggressiveness, and by further crosses to study the inheritance of behaviour. Mouse strains that show different degrees of aggressiveness are easy to develop. Biochemical imbalances also affect behaviour: in many animals an oversupply of male hormones causes aggressive and antisocial behaviour. Pituitary hormones, especially luteinizing hormone, have the same effect in other animals, such as starlings.

      Stimulation of the brain or removal of part of it gives evidence of a structural basis for behaviour; stimulation of the hypothalamus produces many social behaviour patterns, such as sexual activity and aggression. There are even “pleasure centres” that the animal will stimulate on its own, if given a bar to press that sends a shock to its head. Sexual centres are one of the “pleasure centres” that rats are fond of stimulating.

      Another approach is to isolate the animal and see if it still develops a particular behaviour. Young pigeons reared in cardboard tubes will fly soon after release, showing that practice is not necessary. Some young songbirds reared in isolation develop normal songs, and many develop normal calls. Many songbirds must listen to songs of their own species at a particular age, however, to learn them.

      An animal may develop social behaviour while still in the egg or mother. Baby ducklings peep to the calling mother from the egg. An animal may develop social behaviour soon after it emerges or at some critical period later. A young duckling follows the first object it sees, be it a duck or a duckling or the hand of the experimenter. Young birds, ants, and some mammals “imprint” on the first object they see to such an extent that they may court it or show agonistic behaviour to it later. A mother goat given a lamb in exchange for her kid soon after birth will adopt the lamb and drive away her own kid when it is returned to her.

      Later learning also influences social behaviour. Mice that experience defeat learn to run rather than fight; the opposite holds for mice that win. Most animals, however, start at the bottom of a peck order and take defeats in stride, later becoming the dominant animals if they manage to survive. It has been found that association with other young monkeys helps a monkey to behave properly in sexual activity later, although many learn to copulate properly without this opportunity.

The evolution of sociality

      The fact that bees and ants form complex societies, more complex in some ways than those of apes, shows that social behaviour occurs in small animals as well as in large ones, in animals with small brains or large ones, and in both major lines of evolution. If bacteria can be rather social and humans rather solitary, there is no reason to suppose sociality is more advanced in evolution than is solitary life.

      Social behaviour is instead an adaptation to certain environmental opportunities. The evolution of sociality can be glimpsed in the line that leads from the earwig through wood-eating cockroaches to termites, or in the line from solitary bees to social ones. Communication systems also evolve, as may be seen in the line leading from dully coloured monogamous crows to brightly coloured birds of paradise and plain bowerbirds in New Guinea. In this system, the male bird of paradise is brightly coloured to attract the crowlike female. The bright male also attracts predators. The bowerbirds have lost the bright plumage; instead they make elaborate maypoles or bowers decorated with flowers to attract females. One bowerbird even paints the walls of his bower, using a mashed berry or a straw stained in berry juice. These bowerbirds have become safely coloured, for they have replaced bright plumage with bright objects.

      The ecological maturity and regularity of a habitat seem to determine to some extent how social its inhabitants will be. Among African weaver finches, for instance, the forest-living ones are solitary and monogamous; birds of savannas and marshes flock and nest polygamously; and those of very dry habitats tend to be relatively solitary. The same phenomenon has been noted for cats; leopards of the forest and cheetahs of very open country tend to be less social than lions of open savanna areas. Antelope, deer, monkeys, and apes exhibit similar differences. The general rule is that, as an environment grows up from the level of bare ground to that of savanna and finally forest, the solitary animals are replaced by social ones and then by solitary ones again. In the forest, however, single-species societies decline in importance and societies of several species form. The same things happen as a marine community proceeds from bare rock to the complexity of a coral reef.

      Societies of the same species, therefore, seem adapted for intermediate habitats that are in transition between bare ground and forest. It may be that the reason for this is that most intermediate habitats are unstable, likely to be limited in space or time.

Edwin O. Willis Ed.

Additional Reading

General works that deal with social behaviour include W.C. Allee, The Social Life of Animals (1938, reprinted 1976), a readable classic emphasizing peck order and social facilitation at the expense of other aspects of social behaviour; Niko Tinbergen, Social Behaviour in Animals, with Special Reference to Vertebrates (1953, reissued 1990), a popular account by a founder of ethology concentrating on birds, fish, and insects; John Tyler Bonner, Cells and Societies (1955, reissued 1966), a readable account of social life from the howler monkeys down to the cell; William Etkin (ed.), Social Behaviour and Organization Among Vertebrates (1964), a set of moderately technical articles on social behaviour; John F. Eisenberg, “The Social Organizations of Mammals,” Handbuch der Zoologie, 10:1–92 (1965), a review of mammalian social behaviour that shows it derives mostly from maternal societies; Peggy E. Ellis (ed.), Social Organization of Animal Communities (1965), a useful set of rather technical articles, concentrating on social behaviour in insects; John Hurrell Crook (ed.), Social Behaviour in Birds and Mammals (1970), several excellent technical summaries of research in social behaviour, including a discussion of habitat and society; Stuart J. Dimond, The Social Behaviour of Animals (1970), a discussion of experiments on the learning of social behaviour in domestic and caged animals; E.S.E. Hafez (ed.), The Behaviour of Domestic Animals, 3rd ed. (1975), an excellent sourcebook, containing chapters on patterns and mechanisms of behaviour and the specific behaviour of cattle, sheep, swine, horses, dogs, cats, and poultry; Trevor B. Poole, Social Behaviour in Mammals (1985), a condensed source of information on mammalian sociobiology for advanced readers; Andrew Cockburn, Social Behaviour in Fluctuating Populations (1988), a critique of hypotheses and ideas concerning the influence of demography on the evolution of social behaviour in animals; Thomas D. Brock et al., Biology of Microorganisms, 7th ed. (1994); and Robert D. Barnes, Invertebrate Zoology, 6th ed. (1994).Texts that cover particular types of behaviour are V.C. Wynne-Edwards, Animal Dispersion in Relation to Social Behaviour (1962, reissued 1972), a polemic reviewing much of social behaviour to support the view that animals practice birth control by means of social behaviour—but control is usually by agonistic reactions; Harriet L. Rheingold (ed.), Maternal Behaviour in Mammals (1963), a set of moderately technical articles on the mother-infant relationship in mammals; and Edward C. Simmel, Ronald A. Hoppe, and G. Alexander Milton (eds.), Social Facilitation and Imitative Behaviour (1968), scientific articles on imitative learning in animals and humans.Symbiosis is examined in S. Mark Henry (ed.), Symbiosis, 2 vol. (1966–67), informative summaries of a few of the many symbioses known to occur, from viruses to humans; and Lynn Margulis, Origin of Eukaryotic Cells (1970), a discussion of the origin of cells by symbiosis.Studies on the social behaviour of various specific animals include Niko Tinbergen, The Herring Gull's World: A Study of the Social Behaviour of Birds, rev. ed. (1961, reprinted 1989); David Lack, Ecological Adaptations for Breeding in Birds (1968, reissued 1972), a demonstration that the social behaviour of nesting birds depends on their habitats and their foraging; Martin L. Cody (ed.), Habitat Selection in Birds (1985), an excellent collection of review articles; F. Fraser Darling, A Herd of Red Deer (1937, reissued 1967), one of the earliest field studies of a wild society, establishing that deer are matriarchal; John Paul Scott and John L. Fuller, Genetics and the Social Behaviour of the Dog (1965), a scientific analysis of heredity and learning that shows how they interact; Irven Devore (ed.), Primate Behavior (1965), one of the best collections of relatively nontechnical articles on the behaviour of free-living monkeys and apes; Frans de Waal, Chimpanzee Politics: Power and Sex Among Apes (1982; originally published in Dutch, 1982), an entertaining and perhaps humbling look at coalition building, power plays, deception, and manipulation in a species other than our own; and Gisela Kaplan and Lesley Rogers, Orang-utans in Borneo (1994), covering the debates surrounding the orangutan and questions relating to communication, the use of tools, and learning abilities, based on the authors' fieldwork observations and incorporating all previous fieldwork results as well as past laboratory tests.

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