Insects manipulate their environment for a variety of purposes: to trap prey, attract mates, and provide shelter from the elements and protection from predators and parasites. Nests are a special category of environmental manipulation. A nest may be defined as any modification of the environment by adult insects that provides shelter for the rearing of their offspring. In most nest-building insects, the nests are simple excavations or small constructions that provide temporary protection for eggs or larvae, with or without the adult parent(s) in attendance to provide continuing parental care. In the numerous lineages of nest-building insects, an increase in parental care has generally been accompanied by the evolution of more elaborate nesting behavior. The trend has climaxed numerous times in the eusocial insects such as termites, ants, wasps, and bees, whose nests may be very large and architecturally complex and may house the colony for many years under homeostatically controlled physical conditions.
TAXONOMIC DISTRIBUTION OF NEST BUILDING
Nest building has evolved in only a handful of mandibulate insect orders. In this brief survey, only a few selected examples of nest-building species are given for each.
True nests have evolved in a few species of locusts and crickets. In the burrowing cricket, Anurogryllus muticus (Gryllidae), nesting behavior reaches the highest point found in the order. The female of this species excavates a brood chamber in the soil and then seals herself inside and lays her eggs. When the nymphs hatch, the mother feeds them with special trophic eggs and later with grass that she gathers outside and brings into the nest.
A number of beetles manipulate the environment so as to provide shelter and/or food for their young. The female of the leaf roller, Deporaus betulae (Attelabidae), cuts across a leaf along a precise trajectory, then rolls the leaf into a tube, inside of which she lays her eggs. The larvae feed on the inner layers of the leaf roll, while being protected by the outer layers. The dung beetles (Scarabaeidae) excavate nests in the ground and provision them with balls of dung rolled to the site. Some of the carrion beetles (Silphidae) form the body of a dead mouse or other small mammal into a ball, drop it into an excavated chamber, then lay eggs on it. In some species, the female remains in the nest and feeds the young larvae by regurgitation until they are large enough to feed on the carrion directly.
Both sexes of webspinners, adults as well as nymphs, produce silk from the swollen metatarsal glands in the forelegs, which they use to spin a network of galleries on tree trunks or in leaf litter. Not only do the galleries serve as a center for brood-rearing, but they also provide a shelter within which the family of webspinners grazes on bark, dead leaves, moss, or lichens.
All the termites are eusocial (reproductive division of labor, cooperation in brood care, and overlap of at least two generations capable of contributing labor to the colony) and all live in nests. In the more primitive species, the colony nests in the wood source it feeds on. Such “single-site nesting” is exemplified by the small colonies formed by species of Termopsidae, most genera of Kalotermitidae, and the less-derived members of Rhinotermitidae. The colony spends its entire life in its log, the nest consisting simply of the irregular galleries excavated by the feeding termites. The “higher” termites, belonging to the family Termitidae and others, have evolved the ability to nest independently of their food source, in the soil or arboreally. Dissolving the identity between food source and nest freed these species to evolve larger colony size and to exploit a wider range of cellulose sources, including wood fragments of all sizes, grass, seeds, leaf litter, and humus.
Nesting behavior in the Hymenoptera is limited to three super-families: Sphecoidea, Vespoidea, and Apoidea. The ancestors of nest-building aculeates were non-nesting parasitoids of other arthropods. Nesting behavior probably got its start when a female para-sitoid dragged her paralyzed prey into a crudely excavated nest in the ground and laid an egg on it, much as some sphecoids do today. Many of the solitary sphecoids and vespoids (sand wasps, digger wasps, spider wasps) excavate a subterranean nest and stock it with one or more paralyzed prey, on which an egg is laid; others (mud daubers, potter wasps) construct aerial nests of mud. A few sphecids nest in hollow stems or other natural cavities.
Except for the parasitic “cuckoo bees,” all bees (Apoidea) make nests. Most are solitary, the female excavating a nest in the ground or using hollow stems or other natural cavities. Carpenter bees excavate burrows in solid wood. Some solitary bees construct nests of resin or a mixture of resin and pebbles, leaf pulp, or mud on rocks, stems, or leaves.
Eusocial behavior has arisen in all three superfamilies. Nesting behavior, a prerequisite, was already established well in advance of the numerous origins of eusociality in these taxa. In the ants (Formicidae) and bees (Apidae), the evolution of eusocial behavior occurred in subterranean nests, while in the wasps (Sphecidae, Vespidae) it took place in constructed, aerial nests of naked brood cells. In each group, as social life became more elaborate, nests increased in size and complexity and adapted to new nesting sites. Although many species of ants nest in the ground, many others, especially in the tropics, construct arboreal nests or nest intimately with plants. Many of the eusocial bees construct their nests in cavities, whereas others construct aerial nests, either with combs exposed or enclosed in a heavy involucrum. With larger colony size in the wasps came the evolution of protective nest envelopes and/or the move to cavities in the soil or in trees.
Materials and Tools
For the majority of social species that excavate nests in soil or wood, the nest consists merely of the cavity left after the removal of material. In contrast, constructed nests, which have evolved in all four eusocial groups, require a combination of exogenous structural material and adhesive to bind the particles of material together. Various materials are used: termites use soil or wood particles cemented together with saliva and/or fecal material. Ants use wood or other vegetable fiber or mud. Lasius fuliginosus, for example, fills its nest cavity with an irregular carton meshwork glued together with honeydew. The matrix is strengthened by the network of hyphae of a symbiotic fungus. Social wasps (Vespidae) are known as “paper wasps” because familiar species use wood pulp as a structural material, although many tropical species use plant hair and some even use mud. The fibers are chewed and mixed with a proteinaceous secretion of the labial gland that dries into a plastic-like matrix, giving the finished carton strength and a modicum of water repellency. Wasps that build exposed, pedicellate combs construct the pedicel primarily of this secretion, giving it toughness and a dark, shiny appearance (Fig. 1). Honey bees are unusual in using wax, secreted by wax glands on the abdomen, rather than collected material to construct their brood and storage cells. Other social bees also use wax, but mix it with exogenous materials, including pollen, plant resins (propolis), vegetable material, mud, or even feces. Microstigmus wasps (Sphecidae) produce silk from glands at the tip of the abdomen and use this to glue together the leaf pubescence from which their delicate nests are sculpted. Weaver ants (Oecophylla spp.) sew living leaves together with strands of larval silk to create multiple arboreal nesting chambers in which the young are reared.
In all nest-building insects the mandibles are chisel and trowel, the primary tools used to excavate, collect, carry, and mix materials and shape them into the nest. In paper wasps, there is evidence that mandibular morphology has evolved along with changes in nesting material. Other tools are important in a few species: sand wasps use the legs to kick excavated sand out of the burrow, and paper wasps use the forelegs to help manipulate wads of nest material during chewing and mixing with oral secretion. Sensory feedback is critical for precision construction. Wasps use the antennae as calipers to control the size of brood cells in the comb. Honey bees measure brood cell diameter with the prothoracic tarsi and sense the thickness of wax in the cell walls via pressure receptors on the antennae.
FIGURE 1 Newly founded nest of the social wasp, Mischocyttarus drewseni, from Brazil. The founding female is shown wiping an ant-repelling secretion (the gland opens at the base of the terminal abdominal sternite) onto the pedicel of the nest, where it reduces the likelihood that ants will discover the comb of brood cells while the queen is away on a foraging trip.
The information required to construct the nest ultimately resides in the genome of individuals, not as a blueprint of the finished nest, but as a set of one or more kinds of construction acts combined with a set of decision rules. The decision rules determine the location and orientation of material added in relation to environmental cues that include gravity, the current structure of the nest, and the location and state of brood and food stores in the nest. It is the interaction of innate rules of behavior and feedback from external cues that results in the species-typical form of the nest.
The simplest nests of solitary species are constructed by following a linear (nonbranching) sequence of steps. A sand wasp digging her nest, for example, need only decide when to switch from extending the burrow to excavating a brood cell. In contrast, nonlinearity characterizes the construction behavior of all social insects. Rather than following a programmed linear sequence, workers make choices among several types of building behavior according to the current state of construction of the nest. Thus, a Polistes wasp can use her load of pulp to thicken the pedicel, lengthen a brood cell, initiate a new brood cell, or cover the silken cap of a cell containing a pupa. A social insect worker in a large colony may, in the course of her entire lifetime, perform only one or a small subset of the kinds of construction acts and decision rules in her species’ repertory.
Social Organization of Building
In the eusocial insect colony, workers specialize on different elements of nest construction. Older Polybia wasp workers collect materials, some specializing in water, others in wood pulp. Back at the nest, these materials are turned over to younger workers, the builders, who keep the pulp moist with water as they add it to the appropriate places on the nest. The builders regulate the overall rate of activity, for it is they who have direct contact with the construction site and can determine the level of demand for materials. Foragers gain information about demand for their material as they seek builders to unload to.
Nest Architecture and Expansion
Termites and ants tend their brood in loose piles in nursery chambers. In contrast, eusocial bees and wasps rear their offspring individually in cylindrical cells (bumble bees rear several immatures per cell). In all but the simplest bee and wasp societies, brood cells are grouped into combs of various sizes, shapes, and orientations (Fig. 1). The most space-efficient way to close-pack cylindrical cells is to surround each cell with six others. Since adjoining cells share walls, this results in the familiar “honeycomb” pattern of hexagonal cells.
From the core of the nest outward, the typical arrangement is brood, then stored food, and finally the defensive structures. In the honey bee hive, for example, the central brood cells are surrounded by a concentric layer of pollen-storage cells and then an outer layer of honey-storage cells. The entrance to the nest cavity (or a hive box) is secured by guard bees against intrusion by predators and parasites. A similar arrangement is also seen in the nests of termites (Fig. 2) and wasps.
Most social insects are able to expand their nests to accommodate colony growth. In some species, such as yellowjacket wasps, growth is continuous throughout the life in the colony, whereas in others it occurs in bouts separated by periods of no growth. Honey bees expand the combs in the hive when there is a strong nectar flow coupled with a shortage of honey storage cells. In ants and termites, nest expansion may occur opportunistically after rains soften the soil.
FUNCTIONS OF NESTS
The nest is the information center of the colony. It is here that information is communicated about resource supply and demand and about the status of the queen. The nest itself is involved in the distribution of information about colony membership. Each colony has a unique mix of chemicals that labels every individual as belonging to that colony. This “colony odor” resides on the cuticle of each individual as well as in the nest material, and it has been shown for wasps and honey bees that newly emerging workers learn to recognize their colony odor from the nest.
Bumble bees construct specialized wax pots in which they store honey and pollen during periods of good foraging. Stingless bees and honey bees store pollen and enough honey to sustain the adult
FIGURE 2 Simplified diagram of the nest of the termite, Macrotermes bellicosus, from the savanna of Ivory Coast. The front half of the nest is cut away, except for the lower left quarter, which shows the external surface. In the lower part of the mound, just at ground level, is the nest proper, a construction consisting of the central royal cell (containing the queen, king, and attending workers), surrounded by chambers containing brood, fungus gardens, and stored food. Surrounding this is the ridged outer nest, whose design enables it to function as a giant air conditioner. During the day in the dry season, ventilation within the nest is externally driven by the sun, which warms the air in the peripheral air channels, causing it to rise. This sets up a convective circulation within the mound (arrows). CO2 produced in the central nest diffuses out through the walls of the ridges. Air temperatures are highest and CO2 levels lowest in the upper portions of the peripheral air channels. Air temperature within the fungus gardens is kept within 29-31°C.
population through the unfavorable season. The “honey wasps” (Brachygastra spp.) of the Neotropics also store large amounts of honey in their brood cells for the same purpose. Many other species of social wasps store enough honey as droplets in empty brood cells to get the colony through several days of poor foraging. Desert seed-harvester ants stockpile seeds in chambers in their nests, and honey ants (Myrmecocystus and others) store large amounts of honey in the crops of specialized workers called repletes. The fungus ants and higher termites in the subfamily Macrotermitinae (Termitidae) grow specialized fungus as food in chambers in their nests (Fig. 2 ).
Nests often incorporate or accommodate some means of defense against natural enemies. The broods of small, newly initiated colonies are especially vulnerable when the founding queen must leave the nest to forage. Wasps in the genera Polistes and Mischocyttarus suspend their uncovered combs from a narrow, tough pedicel, which they coat with an ant-repelling secretion produced by an exocrine gland at the base of the terminal sternite (Fig. 1). Among the swarm-founding wasps of the tropics are several species that surround the access to the nest with “ant traps” made of carton bristles several millimeters long, each tipped with a sticky droplet.
Bees and wasps that nest in cavities or construct protective outer covers reduce access by ants and parasitoids to a narrow entrance that can be guarded by a few defending workers. Some stingless bees cover the entrance tube with sticky propolis as a barrier against ants, whereas others pull the soft, waxy tube closed each night. The outer layer of the involucrum of arboreal nests of Trigona corvina and T. spinipes is thin and easily broken by an intruder, allowing defending bees to swarm out through passageways in the tough, inner layer and launch an attack.
Social species that form small colonies can exert little control over temperature, humidity, or atmospheric gas concentration in the nest, but some compensate by placing their nests in favorable micro-habitats. By building their nests where sun-warmed air collects, such as under eaves on the sunny sides of outbuildings, Polistes wasps at higher latitudes achieve shorter egg-to-adult development times than they would at ambient temperatures.
By virtue of a larger metabolizing biomass and lower nest surface/volume ratios, social species with larger colonies are better able to regulate nest conditions, and nest architecture is often adapted to enhancing homeostatic control. Large colonies produce considerable amounts of metabolic heat, raising nest core temperature well above ambient. Thick nest-cavity walls or insulating envelope reduce the loss of this heat to the environment. By combining metabolic heating with evaporative cooling, honey bees can regulate the temperature in the core of the nest to within half a degree of 35°C, even if the outside temperature is many degrees lower or higher. The multiple layers of paper envelope of yellowjacket wasps (Vespula) enclose dead air spaces that insulate the nest against heat loss, enabling the colony to maintain the nest temperature well above ambient.
Subterranean-nesting termites and ants have less control over the temperature in the chambers of their nests, but they can construct the nest to take advantage of solar heating. Some ground-nesting ants of temperate regions excavate chambers under flat rocks lying on sunny ground. As the rock warms in the sun during the day, heat is conducted downward to the ground below. By moving the brood up into these warm but moist chambers during the day, the ants accelerate the development of their immatures. At night, as the rock loses its heat, the brood is moved down to relatively warmer chambers deeper in the soil.
Some ants in higher latitudes build honeycombed mounds of soil or plant detritus. In some of the Formica species these can be over 2 m in height. The sun warms the mound to several degrees above ambient, and the colony incubates pupae by moving them up into chambers in the mound during the day.
The most spectacular examples of homeostatic control of nest conditions are the large epigeal (aboveground) mounds built by termites in the savannas of the tropics. Homeostatic mechanisms vary across species, habitat, season, and even time of day. One example is Macrotermes bellicosus, found on the savannas of western Africa, whose colonies can reach 2 million workers living inside large, cathedral-like towers that are 3 m or more in height. Air circulation within the mound during the day in the dry season is shown in Fig. 2 .