AM. ZOOLOGIST, 12:589-594 (1972).
Behavioral Regulatory Mechanisms in the Social Homeostasis of Termites
(Isoptera)
ALASTAIR M. STUART
Department of Zoology, University of Massachusetts,
Amherst, Massachusetts 00102
SYNOPSIS. Recent progress in the elucidation of the behavioral mechanisms responsible
for maintaining the steady state in a termite colony is discussed. It is pointed out that
various homeostatic mechanisms have common behavioral mechanisms. The mechanisms involved in nest repair and construction, foraging, defense, and general mass
movements within nests are explained. An experiment is described in which differential responses to a discrete simple stimulus (heat) are made by two different castes of
Nasulitermes corniger and the homeostatic significance emphasized. The factors involved in foraging behavior in Reticuliterm.es are described. An hypothesis for the
significance of the behavioral phenomenon of head-banging in termites is put forward:
it is considered to be connected with the maintenance of accelerated activity in a
colony after "General Alarm."
The idea of social homeostasis was a
logical extrapolation of the concept of superorganism proposed and elaborated on
by Wheeler (1911) and later by Emerson
(1939). Emerson (1956) was especially impressed by the regulatory function of the
termite nest and he showed, with the superorganism analogy as his basis, how the
term "homeostasis" could be applied logically to events at' the level of the insect
colony.
Recently, the concept of superorganism
has been criticized by Wilson (1971) as
having no heuristic value, but it is noteworthy to observe that its derivative "social homeostasis" has been retained as a
viable term and some time is devoted to its
discussion by Wilson. The application of
Cannon's (1932) term homeostasis to social situations is of course, eminently
reasonable even without the context of the
superorganism hypothesis. Indeed, in a
symposium of the Society for Experimental
Biology (S.E.B.) published in 1964, and
dealing in large part' with homeostasis, the
term was extended even though neither social insects nor the superorganism concept
was discussed. Hughes (1964) reported
The support of studies from the author's laboratory through research grants from the N.S.F. (GB
8356X and GB 32536X) is gratefully acknowledged.
589
that there was agreement amongst the numerous participants that the concept could
be applied to organizations at the cellular, organ system, individual, and social
levels. In the present paper, the definition
of the S.E.B. is used (see Hughes, 1964)
and the underlying feedback mechanisms
involved in social homeostasis are emphasized.
Since Emerson's (1956) account of social
homeostasis emphasising nest' climate,
many of the underlying behavioral
mechanisms have become better understood and many more are under active investigation. The present paper will attempt to discuss recent progress in such
behavior and to show that in termites
homeostatic mechanisms at the colony
level need not always occur over long time
intervals.
Behavioral mechanisms involved in the
construction and maintenance of nests.
In many termites the nest is an obvious
and discrete structure. It is not surprising
that it has been remarked on many times
and that the homeostatic nature of the final
form has been emphasized. Emerson
(1956) showed how the structure of the
nest can regulate temperature and humidity and prevent incursions of other insect's
590
ALASTAIR M. STUART
and the entry of water. The temperature
regulation capacity of a nest was further
studied by Liischer (1961a) who pointed
out how the nest' of the African Macrolerrnes natalensis is virtually air-conditioned
and that even in some less elaborate forms
the nest construction was responsible for
damping the daily oscillations in temperature occurring outside the nest and maintaining a relatively constant temperature
within the nest.
Emerson (1956) went on to analogize
how when the nest was damaged its structure was "regenerated" by workers coming
to the breach to repair the damage, while
the soldiers found in such situations were
likened to phagocytes. Such behavior can
be explained without the need of the analogy as will be seen below.
In the building of a nest many factors
are involved, but basically, the site must be
selected by the imagos, the initial nuptial cell excavated, the cell extended by
building, and the primary construction enlarged on and perhaps modified. During
this time the colony size and composition
changes, and this and environmental factors such as gravity, heat, and water will
ultimately affect" the size and form of the
structure. No one has followed such a sequence from start to finish, but nonetheless
some idea of the behavior of the individual termites is known and to what stimuli
they are reacting. On observing a termite
actively building, it can be seen that it
deposits fluid fecal material ("anal cement") into which it will place a piece of
frass or debris with a characteristic rocking
movement of its head; or it may place
malaxated wood in position with the same
characteristic head movements. The sequence of these events changes from species to species, and even within the same
species; also the three actions may occur
independently of each other. In analysing
one component of the building reaction,
that of the deposition of the fecal cement,
it can be seen that this can be produced by
exciting the insect by a stimulus. The deposition ot the fluid fecal material is a
common reaction of a termite on encount-
ering the residue from a drop of odiferous
material or when it is exposed to any
discrete minor environmental perturbation. The former behavior is quite obviously homeostatic in that by covering the
spot with fecal material, the odor of the
spot is masked. In other words the excitatory stimulus has disappeared in response
to behavioral feedback. Again, the positioning of malaxated wood or the placing
of debris on a spot of fecal cement after its
deposition is often the response of a termite to an irregular structure or surface.
Here the results of the behavior smooth
out such irregularities. This type of behavior is clearly seen when the interstices in
wire gauze placed in an experimental nest
are quickly filled by the termites wit'h debris and fecal cement (Stuart, 1967).
These, then, are reactions in which the
steady state of the colony is maintained
while the immediate environment' is being
changed. It should be noted that homeostasis is not incompatable with change,
but does mean that any changes that do
occur are under close control.
It has been pointed out that the building reaction of termites to irregularities
support's the second sequence of events in
the stigmergy hypothesis of Grasse (1959)
if it is considered that surface irregularities
caused initially by a previous response to
some stimulus produce a further building
response (Stuart, 1969). In such a circumscribed situation, it can be seen that an
alternation of stimuli could cause various
structures to take shape through the building reactions. When no more environmental stimuli, self created or otherwise, are
forthcoming, then building will stop. The
first part of Grasses theory that initially
building is random is at variance with the
current observations (Stuart, 1967). The
idea of building being a homeostatic
mechanism explains why building can
cease (Stuart, 1967; Wilson, 1971).
Another phenomenon is present during
building behavior. At stages during the
construction activity, more or less termites
will be recruited to the work depending on
the intensity of the stimuli to which the
TERMITE BEHAVIOR IN SOCIAL HOMEOSTASIS
termites at the building site are exposed.
This recruitment phenomenon can be seen
more clearly by considering the building
reactions connected with the repair of an
established nest or gallery, rather than by
considering new building. Around an
opening in a nest or gallery the building
reactions described above occur as before,
as well as the recruitment, but usually the
reactions occur at a faster rate. In such a
situation the excitatory stimuli caused by
the breach (air movements, humidity differential, light, etc.) are usually at a high
intensity. The recruitment can be accounted for by the fact that an initially
excited termite will run off laying a trail,
and actively passing on the excitation by
mechanically contacting another termite
while exhibiting a zig-zag movement
(Stuart, 1963). The recruited termites deposit fecal cement' and actively build so
repairing the breach. When this is done
the initial excitatory stimulus no longer
exists and the activity of the termites is
reduced at the site of the breach. Again, a
feedback mechanism is present, and it is
obvious that the behavioral acts involved
are homeostatic at the social level.
Mechanisms involved in foraging
Foraging, the communal seeking out and
gathering of food, is as homeostatic at' the
social level as at the organismic. The
colony does not constantly forage, and in
some species the activity is cyclical and in
others connected with the nutritive requirements of the colony at any one time.
The behavior behind foraging in some
species of termites has been studied and
studies on others are underway at this
time. There is no doubt that in the different families of termites many different
mechanisms will be found to be involved
in the finding and exploitation of food.
One mechanism, however, appears basic to
many members of the Rhinotermitidae
and Termitidae. In these families foraging
has been studied under laboratory conditions (Stuart, 1967; Stuart and Samson,
unpublished). In Reticulitermes flavipes,
591
a Rhinotermitid, aggregations of termites
were allowed to congregate and acclimatize
for at least 24 hours under an upturned
15 cm diameter petri dish on a 24 X 36 in
glass plate; the individuals were provided
with fine debris and soil. During the acclimatization time the insects constructed irregular galleries, roughly outlining the petri dish. Moist wads of filter paper were
positioned at' 0, 90, 180, and 270 degrees
from the center of the petri dish and at
distances of 20 cm from the circumference
of the dish. The petri dish was removed
and the behavior noted. The termites wandered over the plate and when any came in
contact with the filter paper they moved
faster and layed a trail back to the workings. They transmitted their excitation to
other individuals by exhibiting the zig-zag
movement in the same way as when they
are excited by stimuli occurring at a breach
in a gallery, and so recruited them to the
food source. Building also occurs during
this behavior along the trail which soon
becomes a covered arcade. The excitatory
stimulus is eventually eliminated by the
termites exhausting the food supply. When
this happens the arcade then becomes disused or it may be extended to a new food
source.
The homeostatic behavioral mechanism
in foraging thus involves similar reactions
to that found in general building and in
repairs to constructions of the colony. The
main points of difference are in the source
of the excitatory stimulus, the intensity of
the response (this will also depend on the
physiological state of the individual insects) , the initial random wandering, the
covering of the trail, and the method by
which the stimulus is eliminated. The
method of transmission of the excitation
and the method of recruitment of further
individuals is, however, the same.
Defense against intruders
When termites are confronted by small
intruders in a nest or gallery, (he intruder
will elicit excitation, and again the same
method of recruitment as was seen in
building and foraging is used to concen-
592
ALASTAIR M. STUART
trate numbers of termites around the point
of disturbance. Usually the excitation is
very high and the soldiers found in most
species of termites are recruited. This soldclier recruitment even occurs in the primitive termites as such an excitation usually
spreads to the inner portions of the galleries where these termites normally rest.
The soldiers and sometimes the workers or
nymphs attack the intruder and if successful immobilize it by piercing it with their
mandibles, or, in the case of the highly
specialized soldiers of some families, by
chemical means. The net result in a succesful defense is the cessation of movement
in the intruder. When this occurs the excit'ation is lowered and the main response
is now that of depositing fecal material on
the immobilized intruder and this is carried out by the workers. Once the intruder
has been so buried the colony once again
returns to a steady state.
The excitation response as a generalized
horneostalic mechanism
From the above considerations it can be
seen that similar mechanisms operate to
maintain homeost'asis in various situations
where the steady state is altered by external perturbations. There is no doubt that
the termites respond to many different' excitatory stimuli in a similar manner. To
the termites, the additional behavioral responses are in a large part responses to
higher or lower orders of excitatory stimuli. The act'ual response to excitation concerned with the recruitment of other individuals to the certain area which is the
focus of the perturbations will be directly
proportional t'o the intensity of the stimulation, the duration of the stimulation, and
the number of termites initially excited,
and inversely proportional to the distance
of the focus from the center of the nest (or
main galleries in wood dwelling species),
and to the number of competing perturbations occurring elsewhere in the colony.
Movements in nests
Greaves (1964) has shown that tempera-
tures in termite nests in Australia vary at
certain times of the day and that this is
correlated with mass movements of termites within the nest. Such movement to
avoid extremes of temperature is again
homeostatic. A most striking example of
what is considered to be the results of such
behavior is seen in the nests of Amitermes
meridionalis which are lamellar like in
shape with their long axes pointing north
and south. Gay and Calaby (1970) have
postulated that the "magnetic" configuration is a response to temperature where
the termites are unable to descend downwards into the ground because of the
swampy nature of the terrain. In other
species of Amitermes in well-drained areas, the termites can respond to temperature by moving vertically up or down.
The experiments of Greaves were made
in the field and the temperatures in the
nests recorded there. Experiments on the
effects of temperature have also been conducted in the laboratory, however, by the
author (unpublished) using workers and
soldiers of Nasutitermes corniger confined
in Wilson nests. In a situation where the
numbers coming t'o a certain area could be
counted, a heat stimulus was presented.
Worker termites rapidly aggregated in the
area, while the numerous soldiers ignored
the stimulus. When the stimulus was removed the workers left the area at' approximately the same rate as they had aggregated. Some deposition of fecal material
occurred. Such movements tend to substantiate the field work of Geaves. It should
also be noted that this is a clear example
of a differential behavioral response (polyethism) by two different castes to a single
simple stimulus. It should also be pointed
out that if the trail plus excitation method
of recruitment were operating here, it
would be expected that the numbers of
workers and soldiers congregating in the
area would reflect their respective proportions in the experiment (a ratio of approximately 2:1 based on naturally occurring ratios in the field). The responses of
the soldiers were, however, quite negative.
TERMITE BEHAVIOR IN SOCIAL HOMEOSTASIS
Other homeostatic mechanisms having behavioral components
One of the most spectacular instances of
social homeostasis in termites is to be
found in the regulation of castes. This regulation is partly behavioral as well as
being physiological. The behavioral components involve the mutual recognition of
individuals in different castes and the
elimination of excess individuals in some
castes by cannibalism. As this aspect of
social homeostasis has been reviewed many
times (Liischer, 1961 b; Stuart, 1970;
Barth, 1971) it will not be further discussed here. Much, however, still remains
to be known of the details of caste regulation.
Another behavioral mechanism whose
function is possibly homeostatic, or at least
functions to modulate other reactions, is
that of head-banging. This is the response
of many termite colonies to maximal stimulations; the "General Alarm" of Stuart
(1963) . On such stimulation a majority of
the individuals produce sound by hit'ting
their heads against the roof and substratum of their galleries and nests. This behavior in Zootermopsis has been thought
(Howse, 1964) to be responsible for the
communication of alarm through the substratum vibrations that are produced being
received by other individuals. This view
has been disputed by Stuart (1969). It is
suggested here that what such a reaction
may do is to keep the level of excitation in
a colony high and so produce accelerated
responses to stimuli that would normally
elicit a lesser response. The time for the
completion of behavioral responses involved in homeostasis would thus be reduced. In a laboratory colony of Zootermopsis angusticollis that was maximally
disturbed, the author noted that head banging among the nymphs ceased after approximately 10 minutes when most had
begun accelerated building, while the two
soldiers in the absence of any directed stimulus continued to head-bang for approximately 70 minutes.
593
Concluding remarks
More research will undoubtly show that
many more mechanisms are involved in
social homeostasis than have been discussed above, and also that different strategies must have evolved in making use of
the basic behavioral mechanisms. It is
hoped that it may be possible one day to
accurately describe the various interacting
mechanisms at the social level in terms of
system analysis, while at the same time
enlarging our knowledge of the behavior
of single termites at the physiological
level.
REFERENCES
Barth, R. H. 1971. Pheromone-endocrine interactions in insects. Mem. Soc. Endocrinol. 18:373404.
Cannon, W. B. 1932. The wisdom of the body.
Kegan Paul, London.
Emerson, A. E. 1939. Social coordination and the
superorganism. Amer. Midland Natur. 21:182209.
Emerson, A. E. 1956. Regenerative behavior and
social homeostasis in termites. Ecology 37:248258.
Gay, F. J., and J. H. Calaby. 1970. Termites of the
Australian region, p. 393-448. In K. Krishna and
F. M. Weesner [ed.], Biology of termites,
Vol. 2. Academic Press, New York.
Grasse, P. P. 1959. La reconstruction du nid et les
coordinations interindividuelles chez Bellicositermes nalalensis et Cubitermes sp. La theorie de la
stigmergie: essai d'initerpretacion du comportement des termites constructeurs Insectes sociaux 6:41-83.
Greaves, T. 1964. Temperature studies of termite
colonies in living trees. Aust. J. Zool. 12:250-262.
Howse, P. E. 1964. The significance of sound produced by the termite Zootermopsis augusticollis
(Hagen) . Anim. Behav. 12:284-300.
Hughes, G. M. 1964. Preface. In Homeostasis and
feedback mechanisms. Symp. Soc. Exp. Biol.
18:vii-viii.
Liischer, M. 1961a. Air-conditioned termite nests.
Sci. Amer. 205 (1) :138-145.
Liischer, M. 19616. Social control of polymorphism
in termites. Symp. Roy. Entomol. Soc. London
1:57-67.
Stuart, A. M. 1963. Studies on the communication
of alarm in the termite Zootermopsis nevadensis
(Hagen), Isoptera. Physiol. Zool. 36:69-84.
Stuart, A. M. 1967. Alarm, defense and construction behavior relationships in termites (Isoptera) Science 156:1123-1125.
Stuart, A. M. 1969. Social behavior and communication, p. 193-232. In K. Krishna and F. M.
594
ALASTAIR M.
Weesner [ed.], Biology of termites, \'ol. 1.
Academic Press, New York.
Stuart, A. M. 1970. The role of chemicals in termite communication, p. 79-106. In J. W.
Johnston, D. G. Moulton, and A. Turk [ed.],
Advances in chemoreception. Vol. 1. Communica-
STUART
don by chemical signals. Appleton-CeiituryCrofts, New York.
Wheeler, W. M. 1911. The ant-colony as an organism. J. Morphol. 22 307-325.
Wilson, E. O. 1971. The insect societies. Harvard
Univ. Press, Cambridge, ^fassachusetts.