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Behaviour patterns of the ant, Formica fusca
BEHAVIOUR PATTERNS O1 THE ANT, Forndca fusca* By D . I . WALLISt Department of Zoology, Cambridge
The wide variety of responses which may be shown by social insects such as the ant makes it worth while to attempt a brief description and classification of these . Without such a description quantitative studies are not possible This "ethogram" may be divided into categories on the basis of function, e.g . cleaning, fighting, feeding, etc ., while differences in motor pattern allow subdivisions of the functional categories . Where function is not clear a more purely descriptive term is used, e .g . jerking . Only the responses of workers are described . Sexual behaviour is not shown by the workers but only by males and queens during the mating flight . No elaborate courtship behaviour is reported in the literature . Larvae show very few responses, chief of which are the head swinging movements and the cocoon spinning behaviour described by Wallis (1960) .
A
B
Methods Observations were made on 20 different colonies housed in plaster of Paris nests divided into 2 main chambers (Wallis, 1961b) . One chamber was covered with red glass (the nestcell), the other with plain glass (the foraging arena) . The ants confined themselves to the nestcell, an area relatively dark to them as their eyes are insensitive to red light, except when foraging . Each nest contained from 40-45 workers and in only 3 nests were queens present. However, responses to the queen did not seem to differ in kind from responses to other individuals . In general, brood was absent from the colonies, but the responses observed towards brood are summarized. The Behaviour Repertoire In culture, some worker ants are typically inactive for a part of the time . During longer bouts of inactivity, e .g. over one minute, a typical inactive posture is adopted-see Fig . IB . The ant gradually "sags" into this posture, which contrasts sharply with the alert posture characteristic of alert but immobile ants-see Fig . 1 A . *This work was carried out while the author held a Research Studentship from the Agricultural Research Council in the Department of Zoology, Cambridge . tPresent address : Dept . of Physiology, Marischal College, Aberdeen .
Fig . 1 . Active and inactive ants . A. An alert individual . B. The inactive posture . In the inactive posture, the head generally rests on the ground and the antennae are held limp and well in towards the body . The body as a whole is prostrate. In the alert posture, the head and body are raised, making an angle with the ground of 30° or so, and the antennae are held outstretched . Intermediate postures may be observed . When active, the ant may perform various sorts of behaviour which may conveniently be divided into (a) behaviour not involving other individuals and (b) behaviour involving other individuals . Heyde (1924) refers to (a) as "individual instincts" and (b) as "social instincts ." I. Behaviour not Involving Another Individual (A) Running-the antennae are held at a small angle above the horizontal, often outstretched from the body . This is typical of a species which is primarily visual outside the nest, and not an odour trail follower (Carthy, 1951) . 105
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ANIMAL BEHAVIOUR, X, 1-2
Fig. 2 . The 3 cleaning postures . A. Foreleg and antennal cleaning. B . Leg cleaning . C . Adbominal cleaning. (B) Feeding-sugar solutions or water are ingested by lapping movements of the tongue. The mandibles are held closed or nearly closed . Typically, the antennae are held in a W-shaped position and their tips rest on the surface of the fluid food . The labial palps also rest on the surface of the food, but the maxillary palps are held back away from the surface . Occasionally, the forelegs may perform movements similar to those seen in food-sharing but in slow;motion. Heyde (1924) states that this is most often seen in individuals inexperienced in social feeding . (C) Cleaning-Cleaning has the function of removing particles of soil, etc ., from the body surface and may serve to invest the body surface with a coat of oleaginous saliva. Wheeler (1910) suggests that this protects the surface from moisture and may be sufficiently antiseptic to prevent the growth of lethal moulds and bacteria. The cleaning movements are described in some detail for Formica rufa by Jung (1937) . The cleaning behaviour of fusca is essentially the same as that of rufa and also as that of Formica sanguinea . Jung, however, tends to subdivide cleaning movements, observed in the animal as a complex but complete sequence of movements, into cleaning of certain parts of the
body . Cleaning is more conveniently analysed in terms of the 3 main postures adopted for cleaning different regions of the body . In each posture a sequence of cleaning movements is performed, but the component movements are not usually performed in isolation . Thus, there is a behavioural justification for classification by posture . Posture 1 . Foreleg and antennal cleaning (Fig . 2A) . The fore-part of the body is raised, its axis making an angle of 30° with the horizontal . The middle and hind-legs support the body, while the antenna and foreleg of a particular side are normally cleaned alternately. A typical sequence is as follows (a) the right foreleg wipes down the antenna of the same side, which is drawn through the strigil of the foreleg . There is normally no active movement of the head, except inclination of the
WALLIS : BEHAVIOUR OF THE ANT
head towards the side cleaned at the beginning of the movement . The antenna is usually wiped once, but may be wiped 2 or 3 times successively. At the same time, the left foreleg is drawn through the mouthparts on the left side between the maxilla and the labium, where the maxillary comb and probably the tongue as well play a part in cleaning the foreleg . (b) secondly, the right foreleg is drawn through the mouthparts and the left foreleg wipes down the left antenna . (c) the sequence is repeated . Before the antenna is wiped, the foreleg may first brush over the dorsal part of the head including the eye of that side. This movement is usually continuous with the sweep down the antenna. Also, the mandibles may be brushed downwards before the foreleg is drawn through the mouthparts . Thus, there is a general pattern of cleaning one antenna while the contralateral foreleg is cleaned . It is probable that the details of this complex sequential pattern may be altered as a result of localised stimuli from soiling particles, etc . (Jung, 1937) . On occasions a part, only, of the sequential pattern may be shown . Posture II. Leg cleaning (Fig . 2B) . The hind-leg and the middle-leg of one side and both the forelegs take part in the cleaning movements . The ant leans over away from the side where the middle and hind-legs are being cleaned and is supported by the middle and hind-legs of the opposite side and by the abdomen . In cleaning the legs of the left side, the hindleg is cleaned by the left middle-leg brushing down it. The forelegs may assist in this . The left middle-leg is cleaned by both the forelegs brushing down it in succession, the contralateral foreleg often initiating cleaning . Apparently only the lower part of the leg (mainly the tarsi) is cleaned . Foreign particles tend to be moved progressively forwards from hind -* middle -* forelegs, and finally to mouthparts when leg cleaning is followed by antennal and foreleg cleaning. Brushing of the forelegs down each other may occur in this posture or in Posture I . One foreleg is pulled up through the strigil of the other, which actively moves down the leg being cleaned . The legs alternate as cleaning or cleaned legs . A further cleaning movement which may occur in
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this posture is brushing of the side of the gaster with the hind-leg of the side being cleaned, which may precede cleaning of the hind-leg . Posture III . Abdominal cleaning (Fig. 2C) . This cleaning response occurs least often . The body is raised and held well clear of the ground by all 6 legs . The head bends under the thorax, while the gaster is bent forward towards it. In this position the ant is able to lick the terminal region of the abdomen . The antennae are usually directed towards the area licked, as Fig . 2C shows . Brushing down the abdomen with the hindleg is sometimes seen while the ant is standing normally. (D) Digging, Carrying Debris, etc. (Nestbuilding responses) . Digging is carried out by 2 types of movement :(i) Pawing movements of the forelegs. The forelegs are moved backwards against the soil or sand, lifted and brought forward again when a further backward movement is made against the soil . Soil is passed backwards and beneath the ant . (ii) Sand grains and other particles are carried in the mandibles . Digging by carrying particles in the mandibles is virtually identical with carrying debris out of the nest, etc .
II . Behaviour Involving Another Individual (A) Examining (Fig. 3). The head and antennae are oriented towards another ant . The antennae often "focus" on this ant and touch it . Crawley (1910) describes similar behaviour for various species, including F. fusca and F. sanguinea, although he seems to confuse mere orientation, plus moving of the antennae over the ant examined, with palpation with the antennae . The term "examining" is not meant to imply any intention on the part of the ant, but it probably gives information about the other ant through the chemoreceptors on the antennae. It is doubtful whether any important tactile information is gained since the antennae may not touch nor move over the surface of the examined ant . Orientation of the antennae, etc ., may accompany other behaviour such as licking, threatening or seizing another ant, but behaviour is classified as examining only when these other elements are absent .
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ANIMAL BEHAVIOUR, X, 1-1
(B) Licking (Fig. 3) The cleaning of certain areas of the body has to be undertaken by other ants (Jung, 1937), who lick with their labial mouthparts. McCook (1879) has described licking in some detail in
Pogonomyrmex barbatus.
away. A passivity is induced, apparently by the tactile stimulus afforded by being licked .
(C) Aggressive Behaviour Aggressive behaviour may consist of adoption of a threat posture, or attack on another ant . The ant attacked may show aggressive behaviour or a flight response .
(i) "Threat" (Fig. 4) Threat is classified as such because it is shown in association with the aggressive responses seizing and dragging ; it appears to share causal factors with them . It may be regarded as an intention aggressive movement . The head is raised, both head and antennae being directed towards the other ant . The mandibles are held wide open with the labial mouthparts tightly withdrawn-see Fig. 4 . The position of the mouthparts is diagnostic of threat . Threat may be directed towards ants from other colonies, other species or inanimate objects .
(ii) Seizing (Fig .5) Seizing consists of gripping part of the ant attacked between the mandibles. Short, sharp rushes followed by seizing are often observed . Frequently the attacked ant is seized by mandible, antenna or limb . Puncture of the head or epinotum, or loss of a limb or antenna, may result from the encounter .
Fig . 3 . An ant from another colony (stippled spot) being examined by Ant A and licked by Ant B . The licking ant has a foreleg resting on the abdomen of the alien ant . It is doubtful, however, whether cleaning of the individual is the only function of licking since, for instance, much licking occurs of areas that the ant can clean for itself . Other functions may be (a) coating of the ant with saliva and (b) removal of exudates from the body surface which are the basis of the specific odour of the ant and of the colony . Odour is, at a gross level anyhow, specific to a colony, but within a colony minor differences of odour between individuals almost certainly exist . Licking reduces such differences by removing some of the exudates ; by ingestion of these the individual property of an exudate might possibly be incorporated into a number of individuals by some trophic mechanism. Thus, a sharing-out of individual differences might be achieved . Areas frequently licked are the mouthparts, abdomen (particularly dorsal surface and the posterior tip), and the limb joints . The antennae of the licking ant play over the surface being licked, while the licked ant rarely tries to move
(iii) Dragging Dragging consists of seizing plus a locomotory element. The attacked ant is usually dragged out of the nest . F. furca does not show the behaviour of bringing the gaster forward between the legs and squirting acid, as for instance does F. rufa .
(iv) Flight Flight consists of a turning away from the individual or object inducing the response and very swift running, often apparently undirected . Sudd (1957) reports a flight response, in Monomorium pharaonis (L) and Hunt (1957) reports the response in fusca. (D) Food-sharing Behaviour (Fig. 6) Food-sharing behaviour is perhaps the most
WALLIS : BEHAVIOUR OF THE ANT PLATE XI
Fig. 4 . Ant showing threat (on left) towards an ant from another colony (white spot) .
Fig . 5 . Seizing an ant from another colony by the leg . Anim. Behav., 10, 1-2
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109
complex behaviour shown by these ants (Wallis, 1961a) . There has been a tendency to oversimplify elements of the pattern as a result of failure to examine behaviour under various conditions of motivation. For instance, Vowles (1952) seems not to have investigated this activity under conditions of hunger in his work on
parts, including the tongue, are extruded and a drop of regurgitated fluid appears . The appearance of this drop is associated with rhythmic movements of the labial mouthparts . There are 2 types of palpation which may accompany either accepting or donating (Wallis, 1961a).
Camponotus.
(i) Palpation by the antennae
Fig. 6. Food-sharing behaviour. The ant on the left is
Antennal palpation may precede and sometimes accompany accepting food or it may precede but rarely accompany regurgitation . The antennae are palpated alternately and they are so directed as to beat down onto the clypeal and frontal region of the head and onto the antennae of the other ant . Other parts of the body may be palpated on occasions, in attempts to induce the palpated ant to respond . Antennal palpation may be shown without being followed by feeding or regurgitation, usually because the other ant fails to respond . Whether the palpation is associated (motivationally) with acceptor or donor behaviour can be established by reference to the behaviour immediately preceding or following the palpation (see Wallis, 1961 a) .
feeding with foreleg palpation from the ant on the rightthe donor. Note position of mandibles and antennae in the two ants . The antennae of the acceptor are lightly moving over the head of the donor. The two basic responses are soliciting or accepting food, and regurgitating or donating food . In accepting (ant A in Fig. 6), the acceptor raises the head and fore-part of the body out of the horizontal so that the forelegs are often off the ground. The angle from the horizontal may be small, or large so that the body axis is almost vertical . The head may be held at an angle to the body and frequently is held out of the horizontal . The antennae are directed towards, and converge on, the head or mouthparts of the ant donating food . Normally, the mandibles are more or less closed while feeding, as in feeding from a food dish . Food is taken by lapping movements of the tongue, and the maxillary palps are held back with the forelegs often poised in mid-air . In donating (ant B in Fig. 6), the donor raises its head but does not normally hold the head at an angle to the body . Again, the forelegs are frequently raised off the ground . The angle the body axis makes with the horizontal may be small or large . The mandibles are generally opened wide and the antennae held passive, bent more or less at right angles but not directed towards the acceptor ant, The labial mouth-
(ii) Palpation by the Forelegs plus Palpation (ant A in Fig. 6) .
Antennal
Foreleg plus antennal palpation may precede or accompany accepting or donating . Accompanying accepting, the antennal component may drop out or become a gentle sweeping motion . Foreleg plus antennal palpation is only shown accompanying donating at the very highest levels of motivation . The forelegs are palpated so quickly that it is difficult to see how they beat, but observations on very sluggish palpation indicate that the forelegs are alternately raised and lowered . The forelegs do not palpate the head on its upper surface ; in fact, they may oscillate without touching the other ant at all . More usually, however, they touch the other ant on the underside of the cheek region or on the forelegs . Sometimes the 2 food-sharing ants are at an angle to each other so that one foreleg may palpate the underside of the cheek on one side, while the other foreleg palpates the dorsal part of the cheek on the other side. This form of palpation may also be shown by itself because the other ant fails to respond .
(iii) Offering When an ant makes regurgitation movements (raising head, opening mandibles wide and extruding the labial mouthparts on which a drop
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ANIMAL BEHAVIOUR, X, 1-2
may appear), which are not evoked by a potential acceptor stimulating the mouthparts or head, this is designated "offering" . It may be followed eventually by regurgitation or may be terminated if no acceptor responds . (iv) Gaping
This response is sometimes observed in an ant that has fed a long time . The head is bent down, the mandibles are opened to their fullest extent and the labial mouthparts extruded . Sometimes a pellet is extruded from the infra-buccal pouch . This behaviour seems to have the mechanical property of facilitating the regurgitation of food, perhaps by getting rid of particles filtered off during feeding and accumulated in the infrabuccal pouch . (E) Jerking or Lunging
Crawley (1910) describes a greeting ceremony for rufa, sanguinea and fusca, where "one of the ants will make a rapid jerk of the whole body forward towards the other . No striking of heads occurs, as has sometimes been said ; the only parts touching are the antennae ." This behaviour can be observed frequently in fusca. It is of very short duration and no movement of the feet relative to the ground occurs, as far as can be seen . Jerking is not as a rule directed straight at another ant, although it is normally evoked by another ant so that various parts of the body (often the legs) may be struck . The response seems to have the function of exciting other ants .
(F) Carrying other Ants and Being Carried by Them
In fusca, ants are normally carried by the mandible (Wheeler, 1910) . The carrying ant grasps the mandible of the other in her mandibles and walks off. Thus, carrying an ant involves the same motor-pattern as carrying debris and brood, etc. The carried ant is lifted from the ground and shows "tonic immobility" (Haskins & Haskins, 1950) . The head points downwards, so that the ant is held up in the air . Its body is curled over, so that the gaster is brought towards the underside of the head. The legs are held in . In this posture the ant freezes into immobility and allows itself to be carried as a rigid object . The carrying ant carries the other in front of it . Possibly this response is evoked by being seized by the mandible and pushed backwards . Occasionally it is seen in fighting ants ; normally, however, fighting ants seize a mandible and drag
in the opposite direction and then curling-up and tonic immobility do not occur . III. Behaviour Associated with Brood Le Masne (1953) has described at length worker/brood responses for a number of species . The responses which may be shown by fusca can be summarized briefly as follows (a) Feeding brood-consists of regurgitation to the brood and is similar to regurgitation to adults. (b) Licking brood-similar to licking of adults . (c) Brood-carrying and the retrieving of brood . Brood-retrieving in Myrmica ruginodis is described by Vowles (1952) . (d) Behaviour associated with the cocoon spinning of the larva (see Wallis, 1960) . This consists of piling debris over the larva in the early stages and freeing the imago from the cocoon after metamorphosis . IV. Summary of the Behavioural Repertoire 1 . Behaviour not involving other ants . A . Running ; B . Feeding ; C . Cleaning (i) Foreleg and antennal, (ii) Leg, (iii) Abdomen ; D. Digging, carrying debris . 2 . Behaviour involving other individuals . A . Examining ; B . Licking ; C . Aggressive behaviour (i) Threat, (ii) Seizing, (iii) Dragging ; D . Flight response ; E . Food-sharing behaviour (i) Accepting : with no palpation, with antennal palpation, with foreleg plus antennal palpation, antennal or foreleg plus antennal palpation not followed by feeding, (ii) Donating : with no palpation, with antennal palpation, with foreleg plus antennal palpation, antennal or foreleg plus antennal palpation not followed by donating, offering ; (iii) Gaping ; F. Jerking ; G . Carrying other ants or being carried . 3 . Behaviour associated with brood . A . Feeding ; B . Licking ; C . Carrying and retrieving ; D . Behaviour associated with the cocoon . Acknowledgments I should like to express my thanks to Dr . W . H. Thorpe, F .R .S ., and Dr . R . A . Hinde, for their advice and encouragement throughout this work, and also to Prof . Sir James Gray, F .R .S ., for permission to work in his department . REFERENCES Carthy, J . D . (1951) . The orientation of two allied species of British ant . Behaviour, 3, 275-303, 304-318 . Crawley, W . C. (1910) . How ants of the same colony greet each other . Ent . Rec., 22, 43 .
WALLIS : BEHAVIOUR OF THE ANT Haskins, C. P. & Haskins, E . F. (1950) . Notes on the biology and social behaviour of the archaic Ponerine ants of the genera Myrmecia and Promyrmecia. Ann. ent. Soc . Amer., 43,461-491 . Heyde, K. (1924) . Die Entwicklung der psychichen Fahigkeiten bei Ameisen and ihr Verhalten bei abgeanderten biologishen Bedingungen . Biol. Zentralbl., 44, 623-654 . Hunt, T. J . (1957) . A response of worker ants to dead ants of their own species . Nature, 179 B, 875 . Jung, K. (1937) . Die Sauberungshandlungen der Ameisen. Zool. Jahrb. Syst., 69, 373-416 . Le Masne, G. (1953) . Observations sur les relations entre le couvain et les adultes chez les formis . Ann . Sci. Nat. Zool. series II, 15, 1-55. McCook, H . C. (1879) . The natural history of the agri-
Sudd, J. H. (1957). Response of ants to dead of their own species . Nature, 179, 431 . Vowles, D. M. (1952) . Individual behaviour patterns in ants. Adv. Sci. X, 37, 18-21 . Wallis, D . I . (1960) . Spinning movements in the larvae of the ant, Formica fusca . Ins . Soc ., 7, 187-199 . Wallis, D . I. (1961a) Food-sharing behaviour of the ants Formica sanguinea and Formica fusca . Behaviour, 17,2-47 . Wallis, D. I . (1961) . Activity in an ant colony . Proc . zool. Socy ., Lond., (in press) . Wheeler, W . M . (1910). Ants : their structure, development and behaviour. New York .
cultural ant of Texas (Pogonomyrmex barbatus) .
London .
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Accepted for publication 1st July, 1961) .
The wide variety of responses which may be shown by social insects such as the ant makes it worth while to attempt a brief description and classification of these . Without such a description quantitative studies are not possible This "ethogram" may be divided into categories on the basis of function, e.g . cleaning, fighting, feeding, etc ., while differences in motor pattern allow subdivisions of the functional categories . Where function is not clear a more purely descriptive term is used, e .g . jerking . Only the responses of workers are described . Sexual behaviour is not shown by the workers but only by males and queens during the mating flight . No elaborate courtship behaviour is reported in the literature . Larvae show very few responses, chief of which are the head swinging movements and the cocoon spinning behaviour described by Wallis (1960) .
A
B
Methods Observations were made on 20 different colonies housed in plaster of Paris nests divided into 2 main chambers (Wallis, 1961b) . One chamber was covered with red glass (the nestcell), the other with plain glass (the foraging arena) . The ants confined themselves to the nestcell, an area relatively dark to them as their eyes are insensitive to red light, except when foraging . Each nest contained from 40-45 workers and in only 3 nests were queens present. However, responses to the queen did not seem to differ in kind from responses to other individuals . In general, brood was absent from the colonies, but the responses observed towards brood are summarized. The Behaviour Repertoire In culture, some worker ants are typically inactive for a part of the time . During longer bouts of inactivity, e .g. over one minute, a typical inactive posture is adopted-see Fig . IB . The ant gradually "sags" into this posture, which contrasts sharply with the alert posture characteristic of alert but immobile ants-see Fig . 1 A . *This work was carried out while the author held a Research Studentship from the Agricultural Research Council in the Department of Zoology, Cambridge . tPresent address : Dept . of Physiology, Marischal College, Aberdeen .
Fig . 1 . Active and inactive ants . A. An alert individual . B. The inactive posture . In the inactive posture, the head generally rests on the ground and the antennae are held limp and well in towards the body . The body as a whole is prostrate. In the alert posture, the head and body are raised, making an angle with the ground of 30° or so, and the antennae are held outstretched . Intermediate postures may be observed . When active, the ant may perform various sorts of behaviour which may conveniently be divided into (a) behaviour not involving other individuals and (b) behaviour involving other individuals . Heyde (1924) refers to (a) as "individual instincts" and (b) as "social instincts ." I. Behaviour not Involving Another Individual (A) Running-the antennae are held at a small angle above the horizontal, often outstretched from the body . This is typical of a species which is primarily visual outside the nest, and not an odour trail follower (Carthy, 1951) . 105
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ANIMAL BEHAVIOUR, X, 1-2
Fig. 2 . The 3 cleaning postures . A. Foreleg and antennal cleaning. B . Leg cleaning . C . Adbominal cleaning. (B) Feeding-sugar solutions or water are ingested by lapping movements of the tongue. The mandibles are held closed or nearly closed . Typically, the antennae are held in a W-shaped position and their tips rest on the surface of the fluid food . The labial palps also rest on the surface of the food, but the maxillary palps are held back away from the surface . Occasionally, the forelegs may perform movements similar to those seen in food-sharing but in slow;motion. Heyde (1924) states that this is most often seen in individuals inexperienced in social feeding . (C) Cleaning-Cleaning has the function of removing particles of soil, etc ., from the body surface and may serve to invest the body surface with a coat of oleaginous saliva. Wheeler (1910) suggests that this protects the surface from moisture and may be sufficiently antiseptic to prevent the growth of lethal moulds and bacteria. The cleaning movements are described in some detail for Formica rufa by Jung (1937) . The cleaning behaviour of fusca is essentially the same as that of rufa and also as that of Formica sanguinea . Jung, however, tends to subdivide cleaning movements, observed in the animal as a complex but complete sequence of movements, into cleaning of certain parts of the
body . Cleaning is more conveniently analysed in terms of the 3 main postures adopted for cleaning different regions of the body . In each posture a sequence of cleaning movements is performed, but the component movements are not usually performed in isolation . Thus, there is a behavioural justification for classification by posture . Posture 1 . Foreleg and antennal cleaning (Fig . 2A) . The fore-part of the body is raised, its axis making an angle of 30° with the horizontal . The middle and hind-legs support the body, while the antenna and foreleg of a particular side are normally cleaned alternately. A typical sequence is as follows (a) the right foreleg wipes down the antenna of the same side, which is drawn through the strigil of the foreleg . There is normally no active movement of the head, except inclination of the
WALLIS : BEHAVIOUR OF THE ANT
head towards the side cleaned at the beginning of the movement . The antenna is usually wiped once, but may be wiped 2 or 3 times successively. At the same time, the left foreleg is drawn through the mouthparts on the left side between the maxilla and the labium, where the maxillary comb and probably the tongue as well play a part in cleaning the foreleg . (b) secondly, the right foreleg is drawn through the mouthparts and the left foreleg wipes down the left antenna . (c) the sequence is repeated . Before the antenna is wiped, the foreleg may first brush over the dorsal part of the head including the eye of that side. This movement is usually continuous with the sweep down the antenna. Also, the mandibles may be brushed downwards before the foreleg is drawn through the mouthparts . Thus, there is a general pattern of cleaning one antenna while the contralateral foreleg is cleaned . It is probable that the details of this complex sequential pattern may be altered as a result of localised stimuli from soiling particles, etc . (Jung, 1937) . On occasions a part, only, of the sequential pattern may be shown . Posture II. Leg cleaning (Fig . 2B) . The hind-leg and the middle-leg of one side and both the forelegs take part in the cleaning movements . The ant leans over away from the side where the middle and hind-legs are being cleaned and is supported by the middle and hind-legs of the opposite side and by the abdomen . In cleaning the legs of the left side, the hindleg is cleaned by the left middle-leg brushing down it. The forelegs may assist in this . The left middle-leg is cleaned by both the forelegs brushing down it in succession, the contralateral foreleg often initiating cleaning . Apparently only the lower part of the leg (mainly the tarsi) is cleaned . Foreign particles tend to be moved progressively forwards from hind -* middle -* forelegs, and finally to mouthparts when leg cleaning is followed by antennal and foreleg cleaning. Brushing of the forelegs down each other may occur in this posture or in Posture I . One foreleg is pulled up through the strigil of the other, which actively moves down the leg being cleaned . The legs alternate as cleaning or cleaned legs . A further cleaning movement which may occur in
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this posture is brushing of the side of the gaster with the hind-leg of the side being cleaned, which may precede cleaning of the hind-leg . Posture III . Abdominal cleaning (Fig. 2C) . This cleaning response occurs least often . The body is raised and held well clear of the ground by all 6 legs . The head bends under the thorax, while the gaster is bent forward towards it. In this position the ant is able to lick the terminal region of the abdomen . The antennae are usually directed towards the area licked, as Fig . 2C shows . Brushing down the abdomen with the hindleg is sometimes seen while the ant is standing normally. (D) Digging, Carrying Debris, etc. (Nestbuilding responses) . Digging is carried out by 2 types of movement :(i) Pawing movements of the forelegs. The forelegs are moved backwards against the soil or sand, lifted and brought forward again when a further backward movement is made against the soil . Soil is passed backwards and beneath the ant . (ii) Sand grains and other particles are carried in the mandibles . Digging by carrying particles in the mandibles is virtually identical with carrying debris out of the nest, etc .
II . Behaviour Involving Another Individual (A) Examining (Fig. 3). The head and antennae are oriented towards another ant . The antennae often "focus" on this ant and touch it . Crawley (1910) describes similar behaviour for various species, including F. fusca and F. sanguinea, although he seems to confuse mere orientation, plus moving of the antennae over the ant examined, with palpation with the antennae . The term "examining" is not meant to imply any intention on the part of the ant, but it probably gives information about the other ant through the chemoreceptors on the antennae. It is doubtful whether any important tactile information is gained since the antennae may not touch nor move over the surface of the examined ant . Orientation of the antennae, etc ., may accompany other behaviour such as licking, threatening or seizing another ant, but behaviour is classified as examining only when these other elements are absent .
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ANIMAL BEHAVIOUR, X, 1-1
(B) Licking (Fig. 3) The cleaning of certain areas of the body has to be undertaken by other ants (Jung, 1937), who lick with their labial mouthparts. McCook (1879) has described licking in some detail in
Pogonomyrmex barbatus.
away. A passivity is induced, apparently by the tactile stimulus afforded by being licked .
(C) Aggressive Behaviour Aggressive behaviour may consist of adoption of a threat posture, or attack on another ant . The ant attacked may show aggressive behaviour or a flight response .
(i) "Threat" (Fig. 4) Threat is classified as such because it is shown in association with the aggressive responses seizing and dragging ; it appears to share causal factors with them . It may be regarded as an intention aggressive movement . The head is raised, both head and antennae being directed towards the other ant . The mandibles are held wide open with the labial mouthparts tightly withdrawn-see Fig. 4 . The position of the mouthparts is diagnostic of threat . Threat may be directed towards ants from other colonies, other species or inanimate objects .
(ii) Seizing (Fig .5) Seizing consists of gripping part of the ant attacked between the mandibles. Short, sharp rushes followed by seizing are often observed . Frequently the attacked ant is seized by mandible, antenna or limb . Puncture of the head or epinotum, or loss of a limb or antenna, may result from the encounter .
Fig . 3 . An ant from another colony (stippled spot) being examined by Ant A and licked by Ant B . The licking ant has a foreleg resting on the abdomen of the alien ant . It is doubtful, however, whether cleaning of the individual is the only function of licking since, for instance, much licking occurs of areas that the ant can clean for itself . Other functions may be (a) coating of the ant with saliva and (b) removal of exudates from the body surface which are the basis of the specific odour of the ant and of the colony . Odour is, at a gross level anyhow, specific to a colony, but within a colony minor differences of odour between individuals almost certainly exist . Licking reduces such differences by removing some of the exudates ; by ingestion of these the individual property of an exudate might possibly be incorporated into a number of individuals by some trophic mechanism. Thus, a sharing-out of individual differences might be achieved . Areas frequently licked are the mouthparts, abdomen (particularly dorsal surface and the posterior tip), and the limb joints . The antennae of the licking ant play over the surface being licked, while the licked ant rarely tries to move
(iii) Dragging Dragging consists of seizing plus a locomotory element. The attacked ant is usually dragged out of the nest . F. furca does not show the behaviour of bringing the gaster forward between the legs and squirting acid, as for instance does F. rufa .
(iv) Flight Flight consists of a turning away from the individual or object inducing the response and very swift running, often apparently undirected . Sudd (1957) reports a flight response, in Monomorium pharaonis (L) and Hunt (1957) reports the response in fusca. (D) Food-sharing Behaviour (Fig. 6) Food-sharing behaviour is perhaps the most
WALLIS : BEHAVIOUR OF THE ANT PLATE XI
Fig. 4 . Ant showing threat (on left) towards an ant from another colony (white spot) .
Fig . 5 . Seizing an ant from another colony by the leg . Anim. Behav., 10, 1-2
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complex behaviour shown by these ants (Wallis, 1961a) . There has been a tendency to oversimplify elements of the pattern as a result of failure to examine behaviour under various conditions of motivation. For instance, Vowles (1952) seems not to have investigated this activity under conditions of hunger in his work on
parts, including the tongue, are extruded and a drop of regurgitated fluid appears . The appearance of this drop is associated with rhythmic movements of the labial mouthparts . There are 2 types of palpation which may accompany either accepting or donating (Wallis, 1961a).
Camponotus.
(i) Palpation by the antennae
Fig. 6. Food-sharing behaviour. The ant on the left is
Antennal palpation may precede and sometimes accompany accepting food or it may precede but rarely accompany regurgitation . The antennae are palpated alternately and they are so directed as to beat down onto the clypeal and frontal region of the head and onto the antennae of the other ant . Other parts of the body may be palpated on occasions, in attempts to induce the palpated ant to respond . Antennal palpation may be shown without being followed by feeding or regurgitation, usually because the other ant fails to respond . Whether the palpation is associated (motivationally) with acceptor or donor behaviour can be established by reference to the behaviour immediately preceding or following the palpation (see Wallis, 1961 a) .
feeding with foreleg palpation from the ant on the rightthe donor. Note position of mandibles and antennae in the two ants . The antennae of the acceptor are lightly moving over the head of the donor. The two basic responses are soliciting or accepting food, and regurgitating or donating food . In accepting (ant A in Fig. 6), the acceptor raises the head and fore-part of the body out of the horizontal so that the forelegs are often off the ground. The angle from the horizontal may be small, or large so that the body axis is almost vertical . The head may be held at an angle to the body and frequently is held out of the horizontal . The antennae are directed towards, and converge on, the head or mouthparts of the ant donating food . Normally, the mandibles are more or less closed while feeding, as in feeding from a food dish . Food is taken by lapping movements of the tongue, and the maxillary palps are held back with the forelegs often poised in mid-air . In donating (ant B in Fig. 6), the donor raises its head but does not normally hold the head at an angle to the body . Again, the forelegs are frequently raised off the ground . The angle the body axis makes with the horizontal may be small or large . The mandibles are generally opened wide and the antennae held passive, bent more or less at right angles but not directed towards the acceptor ant, The labial mouth-
(ii) Palpation by the Forelegs plus Palpation (ant A in Fig. 6) .
Antennal
Foreleg plus antennal palpation may precede or accompany accepting or donating . Accompanying accepting, the antennal component may drop out or become a gentle sweeping motion . Foreleg plus antennal palpation is only shown accompanying donating at the very highest levels of motivation . The forelegs are palpated so quickly that it is difficult to see how they beat, but observations on very sluggish palpation indicate that the forelegs are alternately raised and lowered . The forelegs do not palpate the head on its upper surface ; in fact, they may oscillate without touching the other ant at all . More usually, however, they touch the other ant on the underside of the cheek region or on the forelegs . Sometimes the 2 food-sharing ants are at an angle to each other so that one foreleg may palpate the underside of the cheek on one side, while the other foreleg palpates the dorsal part of the cheek on the other side. This form of palpation may also be shown by itself because the other ant fails to respond .
(iii) Offering When an ant makes regurgitation movements (raising head, opening mandibles wide and extruding the labial mouthparts on which a drop
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ANIMAL BEHAVIOUR, X, 1-2
may appear), which are not evoked by a potential acceptor stimulating the mouthparts or head, this is designated "offering" . It may be followed eventually by regurgitation or may be terminated if no acceptor responds . (iv) Gaping
This response is sometimes observed in an ant that has fed a long time . The head is bent down, the mandibles are opened to their fullest extent and the labial mouthparts extruded . Sometimes a pellet is extruded from the infra-buccal pouch . This behaviour seems to have the mechanical property of facilitating the regurgitation of food, perhaps by getting rid of particles filtered off during feeding and accumulated in the infrabuccal pouch . (E) Jerking or Lunging
Crawley (1910) describes a greeting ceremony for rufa, sanguinea and fusca, where "one of the ants will make a rapid jerk of the whole body forward towards the other . No striking of heads occurs, as has sometimes been said ; the only parts touching are the antennae ." This behaviour can be observed frequently in fusca. It is of very short duration and no movement of the feet relative to the ground occurs, as far as can be seen . Jerking is not as a rule directed straight at another ant, although it is normally evoked by another ant so that various parts of the body (often the legs) may be struck . The response seems to have the function of exciting other ants .
(F) Carrying other Ants and Being Carried by Them
In fusca, ants are normally carried by the mandible (Wheeler, 1910) . The carrying ant grasps the mandible of the other in her mandibles and walks off. Thus, carrying an ant involves the same motor-pattern as carrying debris and brood, etc. The carried ant is lifted from the ground and shows "tonic immobility" (Haskins & Haskins, 1950) . The head points downwards, so that the ant is held up in the air . Its body is curled over, so that the gaster is brought towards the underside of the head. The legs are held in . In this posture the ant freezes into immobility and allows itself to be carried as a rigid object . The carrying ant carries the other in front of it . Possibly this response is evoked by being seized by the mandible and pushed backwards . Occasionally it is seen in fighting ants ; normally, however, fighting ants seize a mandible and drag
in the opposite direction and then curling-up and tonic immobility do not occur . III. Behaviour Associated with Brood Le Masne (1953) has described at length worker/brood responses for a number of species . The responses which may be shown by fusca can be summarized briefly as follows (a) Feeding brood-consists of regurgitation to the brood and is similar to regurgitation to adults. (b) Licking brood-similar to licking of adults . (c) Brood-carrying and the retrieving of brood . Brood-retrieving in Myrmica ruginodis is described by Vowles (1952) . (d) Behaviour associated with the cocoon spinning of the larva (see Wallis, 1960) . This consists of piling debris over the larva in the early stages and freeing the imago from the cocoon after metamorphosis . IV. Summary of the Behavioural Repertoire 1 . Behaviour not involving other ants . A . Running ; B . Feeding ; C . Cleaning (i) Foreleg and antennal, (ii) Leg, (iii) Abdomen ; D. Digging, carrying debris . 2 . Behaviour involving other individuals . A . Examining ; B . Licking ; C . Aggressive behaviour (i) Threat, (ii) Seizing, (iii) Dragging ; D . Flight response ; E . Food-sharing behaviour (i) Accepting : with no palpation, with antennal palpation, with foreleg plus antennal palpation, antennal or foreleg plus antennal palpation not followed by feeding, (ii) Donating : with no palpation, with antennal palpation, with foreleg plus antennal palpation, antennal or foreleg plus antennal palpation not followed by donating, offering ; (iii) Gaping ; F. Jerking ; G . Carrying other ants or being carried . 3 . Behaviour associated with brood . A . Feeding ; B . Licking ; C . Carrying and retrieving ; D . Behaviour associated with the cocoon . Acknowledgments I should like to express my thanks to Dr . W . H. Thorpe, F .R .S ., and Dr . R . A . Hinde, for their advice and encouragement throughout this work, and also to Prof . Sir James Gray, F .R .S ., for permission to work in his department . REFERENCES Carthy, J . D . (1951) . The orientation of two allied species of British ant . Behaviour, 3, 275-303, 304-318 . Crawley, W . C. (1910) . How ants of the same colony greet each other . Ent . Rec., 22, 43 .
WALLIS : BEHAVIOUR OF THE ANT Haskins, C. P. & Haskins, E . F. (1950) . Notes on the biology and social behaviour of the archaic Ponerine ants of the genera Myrmecia and Promyrmecia. Ann. ent. Soc . Amer., 43,461-491 . Heyde, K. (1924) . Die Entwicklung der psychichen Fahigkeiten bei Ameisen and ihr Verhalten bei abgeanderten biologishen Bedingungen . Biol. Zentralbl., 44, 623-654 . Hunt, T. J . (1957) . A response of worker ants to dead ants of their own species . Nature, 179 B, 875 . Jung, K. (1937) . Die Sauberungshandlungen der Ameisen. Zool. Jahrb. Syst., 69, 373-416 . Le Masne, G. (1953) . Observations sur les relations entre le couvain et les adultes chez les formis . Ann . Sci. Nat. Zool. series II, 15, 1-55. McCook, H . C. (1879) . The natural history of the agri-
Sudd, J. H. (1957). Response of ants to dead of their own species . Nature, 179, 431 . Vowles, D. M. (1952) . Individual behaviour patterns in ants. Adv. Sci. X, 37, 18-21 . Wallis, D . I . (1960) . Spinning movements in the larvae of the ant, Formica fusca . Ins . Soc ., 7, 187-199 . Wallis, D . I. (1961a) Food-sharing behaviour of the ants Formica sanguinea and Formica fusca . Behaviour, 17,2-47 . Wallis, D. I . (1961) . Activity in an ant colony . Proc . zool. Socy ., Lond., (in press) . Wheeler, W . M . (1910). Ants : their structure, development and behaviour. New York .
cultural ant of Texas (Pogonomyrmex barbatus) .
London .
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Accepted for publication 1st July, 1961) .