-1—
SCENT AND LIGHT ORIENTATION BY FORAGING
4C.1.' ( HYNENOPTERA FORMICIDAE )
by
C.T. David, B.Sc..
A thesis submitted for the degree of Doctor of Philosophy
of the University of London.
Imperial College of Science and, Technology, Field Station, • Ashurst Lodge,
Ascot, Berkshire. April 1973. -2-
ABSTRACT.
After a brief description of the laboratory maintenance of the ants and of the design of the foraging arena, the method of testing for a light orientation in a foraging ant is given. Two methods of orientation are described; pottering and menotaxis.
The times taken by ants to complete unsuccessful foraging journeys in the arena are given, and these are compared with figures for other species.
The method used by the ants to orient towards the nest is discussed theoretically and experimentally.
Experiments were performed to discover the factors maintaining menotaxis in ants leaving the nest, and to investigate the factors affecting the angle of this orientation to the light.
Ante orient towards food by different mechanisms. These are described and discussed in relation to various theories of klinokinesis.
The method of orienting towards the nest by fed ants is examined, and is found to differ from that of unfed ants. A correlation was found between the distances walked before feeding by an ant, and the distance it subsequently walks towards the nest after feeding. The mechanism of this was investigated.
Ants lay trails from food sources too large to carry to the nest in one journey. Experiments are described dealing with the existence and lifetime of trails; the sensory cues associated with the presence of more food than can be carried to the nest; the absence of any intrinsic orientation in an odour trail; the method of orientation of ants following odour trails; and the
factors influencing the taking up of a menotaxis in trail following ants. -3-
CONTENTS.
Page.
Section 1.
Introduction. 5 Section 2.
Materials and methods.
Menotaxis and pottering. 11 Section 3. Length of foragint trips. 17 Section 4.
Memtaxis in foraging ants, 30 Section 5.
Directions taken by ants leaving the nest. 38 Section 6.
Klinotaxis or Tropotaxis. 54 Section 7.
Klinokinesis. 57 Section 8. The return to the nest,
After feeding on outward menotactic orientation 68
After feeding whilst pottering. 75 Section 9.
Trail laying behaviour. 81
Evidence for the existence of trails. 84 Stimuli necessary to initiate trail laying. 86 Life time of trails 90 -4- Page.
Section 10
Recruitment by odour trails. - 97 Intrinsic orientation of the trails 100
Orientation of ants following trails. 103 Factors affecting menotaxis in trail following ants 111
Section- 11
Summary. 128 Acknowledgements. 131
References 132 -5-
SECTION I. INTRODUCTION.
A critical summary of the more important works on ant orientation is given by MacGregor (1948), later work has been reviewed by Vowles(1955) and Wilson (1971). Three senses have been widely thought to govern the homing of ants; the antennal sense of odour, the sense of sight, and a kinaesthetic sense. The last of these has never been rigorously demonstrated, howeVer in Sections 6 and lb evidence is given that Mvrmica scabrinodis is able to measure the distance it has walked, which might be considered a form of kinaesthetic sense. Much of the work given here has been concerned with studying the interactions between scent and light orientations in foraging ants.
Foraging ants are considered to be those that leave their nest entrance, without carrying any object in their mandibles, and then walk away from the nest entrance for any distance, however small. Ants carrying
objects in their mandibles when they leave the nest entrance are not
considered any further since their behaviour is different from that of ants without a burden. They leave the nest entrance and take up a menotaxis
and walk in a straight line for a few centimetres, then deposit the object
they were carrying on the substrate, and return to the nest entrance by reversing the angle of their orientation to the light. it is shown in Section 5 that foraging ants often show a bias in the directions in which they leave the nest, but no such bias could be detected in the directions
in which these burdened ants left the nest, even when such a bias was detected in foraging ants.
The family Formididae tc which all ants belong has been subdivided
into various subfamilies. The latest classification is given by Wilson (1971).
He recognises nine subfamilies with living representatives,but considers
that these can be divided into two groups, whose common ancestor may not
even have been a social insect, and which certainly did not have typical -6- ant like mandibles or antennae. This implies that many factors of ant behaviour, especially those relating to social life such as reactions to trail pheromones, have probably been independently evolved- by the different groups of ants. Because of this it is a mistake to put too much emphasis on similarities between ants in different groups, Even within the subfamily Myrmicinae, three different organs have been found to produce trail pheromones, the poison gland, the Dufour's gland, and glands in the hind tibiae, and the responses of the ants to the pheromones are probably just as varied.
So that the relevance of work on other species of ant to this work on the behaviour of Myrrnica can be evaluated there follows a list of the genera of ant mentioned in this thesis together with the subfamily to which they belong, and the larger groups,as classified by Wilson.
Group. Subfamily. Genus. Myrmecioid Complex. Dolichoderinae. IIPLE921. Formicinae. Formica.
Lasius(Acanthomyops) Camponotus.
Poneroid Complex. Dorylinae. Eciton.
Neivamyrmex.
Myrmicinae. Manica.
Myrmica.
Pheidole.
Solenopsis.
Monomorium. Atta. Crematogaster.
Pogonomyrmex.
Tetramorium.
Messor
SECTION 2. -7-
MATERIALS AND METHODS ANT COLONIES
Colonies of Myrmica scabrinodis Nyl. were collected from Chobham Common, Surrey; Silwood Park, Berkshire; and Guernsey, Channel Islands. The ants were identified using keys in Collingwood (1964) and Bernard (1968) and by comparison with specimens in the British Museum (Natural History). NESTS AND MAINTENANCE All colonies used had one or more fertile queens and the ratio of queens to workers was kept at about 1 - 100 by removal of surplus workers. This was done in order to try to keep the conditions inside the nest as standard as possible between different colonies. The colonies were housed in glass and plaster of Paris observation nests filled with sand kept damp by a cotton wick. The nests were connected by interlocking plastic tubes to plastic sandwich boxes with a ring of 'Fluon' painted on the inside wall to prevent the escape of the ants. This design of nest proved very successful and some colonies were kept in them for more than three years. The nests were kept in a 20°C constant temperature room with a 16 hour day, 8 hour night light cycle. The ants were fed on 0.5 Molar sucrose solution contained in glass tubes stoppered at the ends with cotton wool, and on flies (Lucilia spp.). FORAGING ARENA The arena consisted of a wooden table 1.8 x 0.65 m covered with a hardboard board that was in turn covered with a replaceable blank newsprint sheet to give an uniform surface that could be changed in a few minutes. This surface wasdivided by pencil lines into 10 cm squares enabling the paths of the ants to be copied accurately onto sheet s of paper marked with a plan of the arena. These marking lines seemed to have no effect on the orienta- tion of the ants, the lines were not followed by the ants which would cross them at all angles with no signs of any change in direction or speed of move- ment. The arena surface was levelled by means of a spirit level. Ants gained access to the table through a hole, lined by a polythene tube,drilled near to the centre of the table. The nests were connected to this tube by interlocking tubes. -8-
Ants did not climb off the table even when it was illuminated from underneath, however there was a considerable edge effect, foraging ants often walking for considerable distances along the edge of the table. The arena was surrounded by fine muslin curtains and covered by a paper roof in order that the movements of the observer would not disturb the ants and that all visual features could be controlled. The arena was lit by two fluorescent tubes above its paper roof, which produced an uniform diffuse light over the arena surface. When these alone were switched on no evidence was found that the ants could orient to any visual features of the arena. Their movements were exactly similar to the movements of ants in dim red light (Page 15 ), so it is unlikely there were any features in the arena by which the ants could orient. There were also light bulbs at each end of the arena in order to provide orienting stimuli for the ants. All these lights were shielded with black paper to reduce light leakage and thus reflections from the walls. The lights could be controlled from the observer's seat beside the table. The arena was housed in a dark room with a minimum temperature of 20°C. All experiments and observations were made at between 20°C and 22°C, though on hot days the temperature in the room sometimes reached 28°C. It is felt that an arena of this size provides a large enough area for most of the natural activities of a Myrmica nest to be carried out. The area 2 of the arena was 1.17 m . Brian (1956) recorded a density of 4.2 nests per square metre for Myrmica scabrinodis in Scotland. These must therefore have had• less than 0.25 square metres each in which to forage. METHOD OF TESTING ANTS FOR THE PRESENCE OF LIGHT ORIENTATION It was important for much of this research to be able to determine whether individual ants were orienting by the light direction. Unless it is possible to correlate some features of an animal's behav- iour, such as straightness of its path, the speed of its movement etc. with its light orientation, the only way to discover if an animal is using the light as an orienting cue is to change the light direction, or to remove the light cue altogether and look for a subsequent change in the behaviour of the animal. This usually involves disturbing the animal's behaviour and can only be done -9- if the behaviour of the animal is sufficiently predictable to allow changes in its behaviour to be correlated with the experimental changes in its environment. Thus an animal might be orienting by a menotaxis, but be changing the angle of the menotaxis at frequent intervals. If this was happening there might be no observable change in the animal's path when the light direction was changed, since the animal would probably have changed its menotactic angle and thus its path at this time anyway. The light orientations recognised in animals are positive and negative phototaxes, and photomenotaxis. There are at least three kinds of positive and negative phototaxis; a klinotaxis, a tropotaxis, and a telotaxis. In a klinotaxis the animal orients towards or away from the light after comparing the intensity of illumination in successive positions; in a tropotaxis the animal orients after comparing the intensity- of illumination simultaneously zs the special case of a menotaxis using two receptors. A telotaxis A where the animal moves straight towards, or directly away from the light. That is the menotactic angle is 00 or 180°. If an animal is performing a menotaxis its path would be expected to turn through 1800 when the light direction at the animal changes by this amount, and similarly at other angles of change in the light direction. The arena was constructed so that the experiment of changing the light o direction by 180 could be easily carried out. The lights at either end of the arena were connected by a two-way switch /so that as one was switched off the other was simultaneously switched on. It was discovered that when the lights were switched when the ants were following a scent trail the ants would act in an lalarmed'mann.er, suddenly running in a straight line at high speed as has been described by Vowles (1954), unless there was little change in light intensity at the position of the ant. When the ants were at a position of little change in light intensity they would reverse their direction of travel along the trail within a few seconds, indicating that the ants on the trail had acquired a menotaxis. By using lights of different Wattages in the lights at either end of the arena, it was possible to switch the lights with no great change in the light intensity at any predetermined point in the arena. Marak and Wolken (1965) used a similar technique to investigate the spectral sensitivity of Solenopsis saevissima (Fr. Smith). They used lights -10-
of different colours on either side of a trail. If the ants behaved in an alarmed manner when the lights were changed over they could detect a difference in the intensity of the two lights. If no alarm reaction was ob- served, and the ants smoothly changed direction, the two different coloured lights appeared to be of the same intensity to the ants. In this way the relative brightness of different coloured lights needed to give the ants the same illusion of brightness could be found, and thus the relative sensitivity of the ants' eyes to light of different wavelengths determined. MENOTAXIS AND POTTERING
An ant in the foraging arena that is not stimulated by food, proximity to the nest, or by odour trails can walk in two different ways. The ant may have a "light compass orientation" or "menotaxis", or it may not orient to the light direction in any fashion, it may be "pottering". "Pottering" in locusts was defined by Ellis (1963) as "walking with frequent changes in direction. Movement was generally relatively slow and the grass, cage walls, and floor were frequently touched by the palps and antennae." The term "pottering" is used in this thesis to describe the behaviour of ants that are not orienting by the light direction, or as far as can be discovered by other stimuli. The ants walk with frequent changes in direction, thus following an irregular, twisting and looping path, with frequent stops. The palps as far as can be seen do not touch the arena surface, but the antennae do so, tapping the substrate at frequent inter- vals. An ant's path showing both types of movement is given in Fig.9. The ant left the nest and took up a menotaxis that was lost about 30 cm from the nest, when the ant started pottering. These activities of pottering and menotaxis can be distinguished by changing the light direction whereupon an ant with a menotaxis changes direction while one that is pottering does not. This procedure is time consuming, and it was hoped to discover some means of diagnosing from the path of an ant whether or not it was light orienting. To that end the paths of light orienting ants were compared with those of pottering ants from an experiment designed originally to discover if ants orienting with a menotaxis were using any straightening cues other than the direction of the light, and if pottering ants were using any cues from the light. The paths of pottering ants were plotted for a one minute period while the arena was illuminated by a light at one end. This light was then switched off and the ants observed by a dim red light. Marak and Wolken (1965) report that Solenopsis saevissima, (Fr. Smith) has a peak of sensitivity to light in the near red region of the spectrum at 620 However no response could be found in Myrmica scabrinodis to the red light used. -32-
Vowles (1954) described a typical straight run from alarmed Myrmica ruginodis Nyl, and showed that this was maintained by a menotaxis. This behaviour was also found in Myrmica scabrinodis, it could be elicited by lighting tapping an ant with a pencil. In the dim red light, the straight run was not elicited when ants were tapped with a pencil, the ants running on a curving path. This indicated that the ants did not take up a menotaxis to the red light, and it was probably not visible to them at all. After the light at the end of the arena was switched off the ants were allowed half a minute to settle down, and then their path was plotted for one minute in the red light. The light at the end of the arena was then switched on, and the path of the ant recorded for a further minute after half a minute to settle down. In this way any influence of the directional light on the path of pottering ants could be detected by comparing the path of the ants in directional light, and in the dim red light. A second group of pottering ants were each given an aphid. It had been shown that ants carrying an aphid took up a menotaxis (Page 6 8 ). Once the ants were successfully carrying the aphid, their paths were plotted in the light, in dim red light, and again in the light as was done for pottering ants.
Each path was projected by means of an epidiascope on to a wall at its original size, (the tracks were recorded on plans of the arena at a scale of 1.5cm to 10cm). The distance the ants had walked between the timing marks at 15 second intervals was then measured using a map-measurer, and the number of degrees that an ant had turned in that time was measured with a protractor. The number of degrees the ants had turned per centi- metre was found by __dividing the degrees turned per 15 Ls.4.40y‘as by the distance walked per 15 ,s-<_e...c.ns . These results are given in Table 1 . Typical paths are shown in Figure 1 for the pottering ants, and in Figure 2 for the light orienting ants. EFFECT OFDIM RED LIGHT ON THE SPEED OF MOVEMENT AND RATE OF CHANGE OF DIRECTION OF POTTERING AND LIGHT ORIENTING ANTS. 2 4 21 20 11 15 28 24.6 16 38 25 11.7 39 28 12 33 Light. '18 . 25 ' 11 ) 21
25.4 21 27 43 29 27 27 24 17. 16 34 29 22 23 28 21 31 27.9 31 ' 40 Dark. R.C.D. 9 0 3 (°/cm. 24 20 17 12.4 15 19 17 29 41 25 46 22 24 19 21 31. 27-1 Light. .
50 35 10 90 290 126 65 296 207 250 136 257 100 3 8 175 3C7 183 190 208 Light. 266 90 90 230 225 340 155 340 220 302 221 160 170 237 188 248 325 213 196 198 215 Dark. R.C.D. ( ° / 15 sec ) ( ° / 15 0 20 20 240 210 270 235 100 175 140 260 370 273 160 290 315 180 233 250 Light. 17 0 • 5.5 6.5 5.0 9.3 8.0 7.0 8.0 8.5 8.5 15.8 14.0 8.9 13.0 11.0 13.7 10.0 15.2 11-7 13.3 12.5. Light. • , 8.3. 5.8 3.3 7.3 9.8 7.5 8-7 975 5.0 4.7 8.7 9-8 8.5 7.2 10.0 11.0 7.7 8.9 13.3
Dark. .7.5 ' ( cmt / 15 sec ) ( cmt / 5 . °9 7.3 6-0 8.3 7.6 10.0 11.5 10 18.5 12.0 11.0 8 10.5 10.0 11.3 10.5 6.0 10.0 13.0 11.0 - Light,. ,8.0 SPEED OF WALKING. SPEED OF J Al. A4. A5. A6. A7. A8. A9. A3. A10. Bl. B2. B4. B3. B5. 36. B8. B10. 39.
. Average Average IANT.NO. IANT.NO. MENOTAXIS ) ANTS WITH APHID. ANTS POTTERING ( WITH -14- FIGURE 1. PATH OF POTTERING ANT IN DIRECTIONAL LIGHT AND IN DIM RED LIGHT.
! ...... 1 . , ...... 4 v
......
-„, ....i...... , I • . -t- P -...... „,4 - -,
•
FIGURE 2, PATH OF LIGHT ORIENTING ANT IN DIRECTIONAL LIGHT AND IN DIM-RED LIGHT.
- -.1 . , _,...._
, 1-----.
1---- k
.... . or • 9-'--1",
I-- 1 Ocrft-1 C) = nest entrance.. <--light off, <—< light on. -15-
As can be seen from Table 1 when a light is present at one end of the arena ants that are orienting by the light direction walk slightly faster and turn less per unit time than do pottering ants, the differences however are insignificant as determined by the Wilcoxon's Sum of Ranks Test (Langley 1956), They turn less per unit distance than pottering ants which is significant at p = <0.02 by the same test. In the dark the speed of ants that were previously light orienting decreases and their rate of turning per unit time increases, these changes are insignificant using the Wilcoxon's Signed Ranks Test. (Langley 1956) The rate of turning per unit distance however increases by a factor of two, which is significant at p = < 0.01 using the Wilcoxon's Signed Ranks Test. This speed, and the rates of turning are not significantly different from those of pottering ants in the same conditions. There is no significant change in the rates of turning or speed in the pottering ants in the two conditions. When the light is again switched on, the menotactically orienting ants revert to their former behaviour. The pottering ants decreased their rate of turning throughout the experiment, but the changes are not significant. From this experiment it would appear that the rate of turning per centimetre is the most constant feature in the walking behaviour of the ants. Their speed, and distance turned per unit time are far less constant, presumably because the antsstop frequently for varying lengths of time, and only turn whilst they are actually walking, and then tend to walk round curves of fairly constant radius. The paths of ants in the dark that were previously orienting by the light direction are indistinguishable from those of ants that were pottering in the dark or from those of ants pottering in the light. This indicates that while an ant is light orienting the only straightening cue to an ant's course since in the dark is the light direction,i\there is no more straightening than in pottering ants. This is evidence against the old theory of the existence of a kinaesthetic sense (Pieron 1904)(1909). This theory explained the return of ants to the nest and limpets to their scars worn in the rocks, to an animal being able to reproduce the twists and turns of its outward path in reverse having recorded them by proprioceptors in the muscles and joints. Since the ant -16- does not straighten its path even slightly in the dark when it would be straightening it in the light, it seems doubtful whether it could reproduce its outward movements in enough detail to return to the nest after a long and complicated foraging journey. However a kinaesthetic sense in the fashion of bees, where the distance the bee travelled to a source of food can be read, if not by the bees, from the bees' dance, is not ruled out by these observations. The return of limpets to their homes is now explained by the animals following polarized, chemical trails radiating out from their home over the rock surface (Cook et al 1969). From this experiment it can be seen that although there are differences between the rate of turning per cent imetre in light orienting and pottering ants, one cannot tell from one track whether an ant is light orienting or pottering, since there is a considerable overlap in the turning rates of ants in these two states. Thus to tell if an ant is light orienting or pottering, one must change the light direction and look for subsequent changes in the ant's path.
LJ -17-
SECTION 3.
LENGTH OF FORAGING TRIPS The time that 164 workers took to complete "unsuccessful" foraging journeys, i.e. those in which no food was found, in an arena they had been using for a long time, is given in Figure 3 The majority of the ants re-enter the nest within one minute of leaving its entrance. If these results are plotted as the numbers of the one hundred and sixty-four ants left foraging after fixed time intervals, Fig. 4 is obtained. The times taken for half of the ants remaining foraging to return to the nest is.not constant, so the likelihood of an ant returning to the nest in each successive minute is not constant. However as a graph of the numbers of ants remaining foraging against the logarithm of the time shows (Fig. 5 ) the ei'id of the curve is almost a straight line which starts about two minutes after the ants have left the nest. This means that the chance of an ant returning to the nest in each successive minute after two minutes have passed, is almost constant. Wilson (1962) found that in Solenopsis saevissima (Fr. Smith) there was never a constant chance for ants to return to the nest in each successive minute. In that case a plot of the logarithm of the numbers of ants remaining foraging against the logarithm of the time was a straight line indicating that the chance of ants returning in each time interval decreased the longer they had been away from the nest. He explained this by the "common sense deduction" that the longer an ant remains foraging, the further it wanders from its nest, and thus the longer is the time it takes to return to its nest when it does turn back. This explanation implied that the Solenopsis workers had a constant chance of turning back in any time interval, and the complex distribution of the lengths of their foraging journeys is caused by the length of time the ants take to find their nest. FIGURE 3. LENGTH OF UNSUCCESSFUL' FORAGING JOURNEYS.
.9
80
70 -
60- Numbers of 50 . journeys completed at 40- given time. 30 -
20
10
0 Ju 1' 15 20+ Length of journey (minutes).
FIGURE 4. NUMBERS OF ANTS REMAINING IN FORAGING ARENA AT VARIOUS TIMES AFTER START OF FORAGING.
180
160
140
320 Numbers of ants remaininglOO in foraging 80 - arena at given • • time. 60
40 -
20
5 10 15 20+
Time after start of iournevs ( mini €R0 -19-
FIGURE 5. NUMBERS OF ANTS REMAINING FORAGING IN THE ARENA AT VARIOUS TIMES AFTER START OF FORAGING PLOTTED AGAINST THE LOGARITHM OF THE TIME ELAPSED.
180
160
140
320 Numbers of ,ants 100 remaining 80 foraging. 60
40
20
0 0.5 1.0 /Log. Time ( minutes)
FIGURE 6. FIGURE ILLUSTRATING THE AREAS FROM WHICH ANTS WOULD BE "DRAINED" INTO THE NEST.
4U cm -20-
This idea of a constant chance for a change in the ants behaviour occurring during any time interval, cannot account for the situation in Myrmica scabrinodis where the chance of an ant returning to the nest in any time interval after the ants have been foraging for two minutes is a constant, unless I. The journey time of ants back to the nest from the position at which the change in their behaviour leading to this return occurs, is a constant no matter how long the ants have been away from the nest, or 2. The journey time back to the nest is of short duration compared to that of the whole foraging trip, but it need not be constant. It is possible to decide which of these hypotheses is not true by following the homeward path of the ants and observing its length. Unfortunately it was not possible to distinguish the homeward path of the ants from .the path of an ant that was still foraging, since both move in an irregular twisting path. To induce homeward movement the ants were presented with an aphid, while they were following this twisting path after they had been foraging' for various lengths of time and the times these ants took to reach the nest are given in Table 2 As can be seen, the length of time for which the ants had been foraging, and likewise the distance they were from the nest when they were presented and likewise the distance they were from the nest when they were presented with the aphid, bear no relation to the length of time the ant takes to return to the nest. It is unlikely that the ants presented with aphids have any more diffi- culty in returning to the nest than do unsuccessful foragers. The carrying of the aphid does not appear to slow their movements; the aphid is only about the size of the ant's head and so leaves the antennae free. Since the average journey time back to the nest was 4 minutes which is long compared with the average foraging time of 3.5 minutes, the 2nd hypothesis, that the journey time back to the nest is short compared with the foraging time LE3 Otitrue. The observed journey times do fit the first hypothesis, since there is little variation in their length no matter how long the ant has been foraging or how far it is from the nest when it was given the aphid. -21-
TABLE 2.
TIMES TAKEN BY ANTS ADTER FORAGING FOR VARIOUS TINES TO RETURN
THREE DISTANCES TO THE NEST ENTRANCE, AFTER BEING GIVEN AN APHID.
Distance from Time spent Time for nest entrance, foraging. return. ( cm) ( min ) ( min )
10 6.5 0.5 IC) 4.5 1.5 10 3.5 6.5 10 2.5 8-0 10 1.0 5.5 3.4 4.4
20 7.0 4.5 20 2.5 2.0 20 2.0 3.5 20 1.5 4.0 3.0 6.0
50 10.5 3.0 5o 8.5 2.0 50 3.0 7.0 50 3.0 1.5 50 2.5 3.5 50 2.0 3.0 50 1.0 4 4.5 4.3 3.6 -22-
However this result does not prove the truth of the first hypothesis. The constant chance for ants to return in any time interval could arise also from two other causes other than a constant chance for a change in the ant. The first of these is that different ants may characteristically forage for different times, and the constant chance of a return could then be due to the relative numbers of ants in the nest that will return at any time. This could not be tested as no method was found for marking individual ants so that the length of their foraging trips could be measured that did not seriously inter- fere with the ants' behaviour. However, it might well be true, since Weir (1958) has shown that some individuals of Myrmica scabrinodis fora ge, and others do not, the difference between the two groups being mainly one of age. So if this can occur it is possible that some ants habitually forage for longer periods than others. The second cause for a constant chance of a return by ants in any time interval might be that after a short period of foraging all the ants are ready to return to the nest, however a few in this short time have wandered so far from the nest that they are unable to orient themselves toward it, and only find it by chance. If it is assumed that the ants are finding their nest by chance, then it is possible, given the speed of the ants, the size of the foraging arena, and the proportion of the ants entering the nest each minute, to calculate the area of the foraging arena surface from which all the ants would in practice be "drained" into the nest in each minute. Once this area has been calculated, one can look on the_arena surface and see whether there is any change in the behaviour of ants inside and outside this hypothetical area. If the size of the area in which ants are in fact changing their behaviour in a fashion leading to their being "drained" from the foraging arena is greatly different from the area calculated, the hypothesis that the ants are finding their nest by chance may be eliminated. The area of the foraging arena is 117,000 sq. cm., 14% of the ants return to the nest in each minute after the first few minutes, and the average speed of the ants is 40 cm min. If the ants were stationary and distributed over the arena at random, then 14% of the ants would be found within a circle of area 1638 sq. cm around the nest entrance. That would be the area from which the ants -23- would be "drained" in the first minute assuming the ants nearest to the nest at any moment are always the first to reach it. As the ants move at 40 cm a minute an area this size would in fact "drain" more than 14% of the ants from the arena surface in a minute. If the ants were all moving in parallel lines from left to right, the area would "drain" all the ants from area A plus the ants from area B in Fig. 6 in the first minute, and all the ants from area B in the second and subsequent minutes. For 14% of the ants to be "drained" each minute, area B must be equal to 14% of the foraging arena in area . The radius of Area A would then be 1638 divided by 80 cm, which is 22 cm. '22 cm is then the radius of the area round the nest entrance which would drain 14% of the ants from the arena each minute. Observations on ants in the foraging arena show that most ants given food and placed 10 cm from the nest entrance can orient towards the entrance. However, ants placed 20 cm from the nest entrance cannot do so. 20 ants were given an aphid at the nest entrance and then placed one at a time on a circle drawn 10 cm from the nest entrance. The ants were placed down facing clockwise round the circle. This procedure could be carried out without unduly alarming an ant by allowing the ant to seize an aphid in its mandibles , and then lifting the aphid using forceps. The ant would not let go of the aphid. The direction taken by the ant was scored 'positive' if it was within the tangent to the circle round the nest entrance at the position of the ant after the ant had walked 10 cm, and 'negative' if it was outside this tangent. The experiment was repeated but the ants were placed on a circle drawn 20 cm from the nest entrance. The results are given in Table 3 This experiment suffers from the same fault as the proceeding one, (Page 20 ) that one is trying to deduce the behaviour of unfed ants from that of fed ones. In this case the behaviour of the fed ants was compared with that of foraging ants selected at random from the arena surface. 20 of these were deposited on circles 10 cm and 20 cm from the nest entrance by allowing them to walk onto pieces of paper that were then moved and the ant allowed to walk off onto the arena surface. The moving of the paper often alarmed the ants, which was surprising as lifting the ants given aphids TABLE 3.
DIRXTIONS TAKEN BY ANTS GIVEN APHIDS AND PLACED 10 AND 20 CM FROM
NEST ENTRANCE.
Distance from + — 1 nest entrance. (No of ants walking (No of ants walking ( cm ) Towards nest entrance). away from nest
10 17 3
20 12 8
TABU', 4.
DIRECTIONS TAKEN BY ANTS TAKEN AT RANDOM FROM THE ARENA SURFACE AND
PLACED 10 AND 20 CM FROM THE 'EST ENTRANCE WITHOUT BEING GIVEN AN APHID.
Distance from +
nest entrance. (No. of ants walking (No. of ants walking
( cm ) towards nest entrance), away from nest.)
10 18 - 2 -
20 9 - 11 -25- off their feet seldom alarmed them. The directions taken by these 40 unfed ants are given in Table 4 As can be seen, at 10 cm both groups of ants oriented toward the nest entrance, the probability of this result occurring by chance is less than 5% by the Binomial Test. At 20 cm there is no significant orienta- tion toward the nest entrance by either group of ants. The differences between the directions taken by the fed and the unfed ants are insignificant. From this experiment no change in the ants' behaviour that would lead to their being "drained" from the arena can be detected at the distance it was predicted. Two major assumptions were made to provide the figure of 22 cm for the radius of this distance. The first was that the ants were distributed at random over the arena. In fact they are not so distributed. The position of every ant in the foraging arena was plotted on five different days, the results are shown in Figure 7. As can be seen the ants are not distributed evenly over the foraging arena but are clustered toward the nest entrance. Evidence for the existence of a mechanism that keeps the ants clustered towards the nest entrance is given in the next section, where it is shown that the ants leave the nest by picking up a menotaxis, which is lost at a distance from the nest when the .ants start pottering. This concentration of the ants towards the nest would reduce the area from which the ants are "drained". The second assumption made was that the ants walked in straight lines, in fact their paths are quite tortuous. This fact would lead to the area of the area from which the ants are "drained" having to be increased to "drain" 14% of the ants in each minute. These two assumptions may balance each other out, so that the "drained" area would be about that calculated. As the area calculated inside which the ants should be "drained" into the nest in each minute is much larger than the observed area in which the ants' behaviour is changed leading them to orient toward the nest entrance, there must be some other cue not immediately affecting the ants placed on the arena, guiding the ants towards the nest. If there is no such cue, not even 14% of the ants present in the foraging arena would be able to reach the nest entrance in each minute. A behaviour of fed ants indicating the presence of such a cue is described in section 8 . Here the fed ants picked up a menotactic FIGURE 7.
THE POSITIONS OF EVERY ANT IN THE FORAGING ARENA AT MIDDAY ON FIVE SUCCESSIVE DAYS WHEN NO FOOD HAD BEEN PLACED IN THE ARENA.
x X x 0.- 1
x x * x x x x . v I r- ..., 4 x x 'S x• it xx. A X :..c A. .. .4' X . V . r. Jc. k Jr ..4 - . 4 I
. I X i X I S L__ I ,t "4__10,_ ..X ---• x i X 1
x= position of ant ie. nest entrance. -27- orientation, the angle of which to the light is changed after the ant has travelled "legs" varying in length from 5 to 35 cm. The orientation of the ant to the nest entrance was determined at the start of each "leg", when the menotactic angle had just been changed. It was found that there was a significant orientation towards the nest entrance at the start of each "leg". This orientation of the "legs" of fed ants towards the nest would probably provide a means for a large enough number of ants getting close enough to the nest entrance for 14% of them to be drained into it each minute. Possibly, the paths of unfed ants proceeding to the nest are similarly biased towards the nest entrance. Thus it is unlikely to be true that the ants remaining foraging in the arena after two minutes have passed in their foraging trip, are all wandering around and returning to the nest by chance when they happen to pass close to it. However this hypothesis can be tested in a more direct fashion by discovering if ants that have been foraging for at least three minutes are all willing to re-enter the nest if they find it. To test this, 25 ants that had been foraging for periods ranging from 4 to 6 minutes were presented with the nest entrance. This was done by leading the ants onto the arena surface from the nest through a long flexible plastic tube that could later be moved over the arena surface till it was next to an ant. 4 ants acted in an alarmed manner when the nest entrance was brought up to them, 12 ants entered the nest entrance and proceeded to the nest, one ant entered the nest entrance and immediately re-emerged, and 8 ants refused to enter the nest entrance at all.
25 ants were given aphids whilst foraging and then had the nest entrance brought up to them as above. 1 ant acted in an alarmed manner, 23 ants entered the nest, 1 ant did not enter the nest. Thus it is unlikely that all the ants foraging two minutes aSter they leave the nest are ready to enter the nest if it is found. In conclusion there are two hypotheses which could account for the observed length of journey times in Myrmica scabrinodis. The first of these is that there is a constant chance for ants to bedome ready to re- enter the nest in any time interval during a foraging journey. After this change has occurred the ants continue walking but now are slightly guided towards the nest entrance. The nest entrance is reached in similar times after the ants have been foraging for different lengths of time because there is little relation between the length of a foraging journey and the distance -28- the ants get from the nest. An ant in the first minute of foraging can get to the furthest point of the foraging arena from the nest entrance, and in any case a mechanism exists that tends to keep the ants closer than this to the nest entrance. This is a similar theory to that of Wilson (1962) concerning Solenopsis saevissima, Wilson implied that there was a constant chance for a change of behaviour leading to a return in these ants, and explained the decreasing chance of an ant reaching the nest entrance in each successive time interval as being due to the increasing time the ants took to reach the nest after longer journeys. However Wilson was using a finite foraging arena, probably smaller than that used here, so it might be expected that the Solenopsis would behave like the Myrmica and have a constant journey time back to the nest. Because of this Wilson's explanation of the situation in Solenopsis cannot be accepted without further study-.
The second hypothesis that can account for the observed foraging trip times in Myrmica scabrinodis is that indiVidual ants have set foraging times. After they have been foraging for this time they become ready to enter the nest if it is reached, and the nest is found as is described for the first hypothesis. The constant chance for ants to return to the nest in any constant time interval is then due merely to the relative numbers of ants with different set foraging times in the colony. The only way to distinguish between these two hypotheses is by timing the foraging journeys of individual ants and seeing if they are constant or vary from trip to trip. As has been already explained, this could not be done as no satisfactory- method for marking the ants could be devised. The times of foraging journeys of ants have been very seldom measured. The only field estimate has been made by Holt (1955) for Formica aquilonia Yarrow in Scotland. These ants forage by radiating out from the nests along set routes which go to trees with aphids on. Hunting ants "leak" out from these routes at a fairly constant rate per metre of route, and forage over the ground between the routes. These ants return to the nest by rejoining one of the routes. Holt marked 50 foragers just as they left the nest along one of the routes and observed the times they took to return to the nest. His results are shown in Fig. B. As can be seen most of the ants returned between 1.5 and 3 hours after they left the nest. In this species the majority -29- of the ants collect honeydew from aphids, only a few hunt insect prey, so one cannot compare this distribution of journey times with that of unfed foragers in Viyrmica. The situation in Formica acuilonia is similar to that in Myrmica when the ants are recruited to a long lasting supply of sucrose solution present in their arena. Then the majority of the journey times would also be of the same length, since most of the ants are walking straight to the sucrose, filling their crops from it and walking straight back, a process that would not be expected to take greatly different times for different ants .
FIGURE . ).‹ LENGTH OF FORAGING JOURNEYS OF FORMICA Aallgia. DATA OF HOLT ( 1955 ).
10
9 a.
Numbers of 7 " journeys 6 completed in given 5 - time interval. 4 -
3
2 1
0 60 120 - 180 Length of journey (minutes ) -30-
SEuTION 4.
MENOTAXIS IN FORAGING ANTS • In a foraging arena that has had ants on its surface for more than about one week, but with no fresh odour trails laid by the ants from food finds to the nest, ants leaving the nest entrance often pick up a menotaxis which is then lost 20 - 30 cm from the nest entrance (Fig. 9 ). About one ant in five does this, but these are .not only the ants which are going to remain foraging for the longer periods of time (see page 17 ), since many of them return to the nest within one or two minutes. The presence of this menotaxis can be demonstrated in the ants as described in the Methods section (Page 8), by changing the light direction: shortly afterward the ants change their direction of movement by a similar amount. MAINTENANCE OF THE MENOTAXIS A paper disc 20 cm in diameter was left flat on the foraging arena surface 20 cm from the nest entrance. After one week ants leaving the nest were observed to pass over this disc with no signs of hesitation at its edge, and to maintain their menotaxis while they crossed the disc (Fig. 10 ). The disc was now removed exposing an area of the arena surface on which the ants had never walked, but continuous with the remainder of the arena surface. Ants passing over the area from which the disc had been removed lost their menotaxis after passing onto the clean exposed area (Fig. 11 ). When the disc was replaced in its original orientation the ants once more passed straight on over it without losing their menotaxis. When the FIGURE 9 .. LOSS OF MENOTAXIS BY ANT LEAVli\G NE;ST AFTER TRAVELLI~G 30 eM.
.. · .. ·1
•
FIGU11E 10. EFFECT OF PAP ER DISC PLACED IN PATti OF ANT LEAVING NEST vlIW b.. NENOTACTIC ORIENTATION !
I I I I i I I I I, f ----- .1 ~~- ----+- 1 I -, I ----.~
• II I ----' -32-
FIGURE U. LOSS OF MENOTAXIS BY ANT LEAVING NEST ON PASSING INTO NEWLY EXPOSED AREA.
t
I
--, -33-
o disc was replaced but rotated through either 90 or 180, ants still passed straight on over it without losing their orientation. The best explanation of these observations is that in an old arena the surface for some distance around the nest entrance is changed by the ants in some fashion. Since no differences could be observed with a binocular microscope between the paper of the foraging arena surface before and after ants had been foraging on it, it is likely that the ants had marked the arena surface with some odour in the absence of which the 'ants lost their menotaxis. There is no evidence to suggest that this odour can cause the ants to pick up a menotaxis, only that it stops the ants from losing their menotaxis once it has been acquired. This is shown by the fact that once ants left an area rendered free of scent by the method of protecting it from the ants with a paper shield, they were never seen to pick up a menotaxis (Fig. 11 ). The odour on the arena surface could be present in many forms. It could be as a field, that is, it is not concentrated in spots or trails, but spread out more or less evenly. It could be present as a series of discrete spots, as is suggested by MacGregor (1948) for the ant Myrmica ruginodis Nyl. MacGregor stated that a single spot of odour was sufficient to change an ant's behaviour from travelling in an irregular looping path to that of travelling in a path with the loops suppressed. As has been said there is no evidence hi Myrmica scabrinodis to suggest that the odour can change the ants' behaviour from pottering and give it a menotaxis. Also the arena foraged on by the ants from one colony, caused ants from a second colony to pick up a menotaxis when they left the nest. MacGregor stated that the odour spots in Myrmica ruginodis were only detectable by ants from the same nest as those that laid them. In light of these two facts it is improbable that the odour causing Myrmica scabrinodis to keep their menotaxis is the same as that found by MacGregor to initiate one. The odour could also be in the form of streaks or trails of odour, as is the case with Monomorium pharaonis L. Sudd (1965), or Pogonomyrmex badius (Latr.) Holldobler and Wilson (1970). In these cases the trails of odour are used by the ants as orienting cues, the ants follow them on the start of their foraging trips, and during their return. In the case of Pogonomyrmex, -34-
Hollclobler (1971) has shown that the ants following these trails of odour do have a menotaxis. It should be emphasised at this point that these trails of odour are distinct from the evanescent trails of odour used by these ants to recruit workers to.food finds. There is no evidence to suggest that these trails are decay products of the recruiting trails, or are deposited at the same time. In Pogonomyrmex the long lasting odour discussed above is a product of the Dufour's gland, while the recruiting trail is produced by the poison gland. Both however are deposited by the sting. (Holldobler&Wilson 1970). No means has been found for determining the form taken by the odour in the foraging arena. It seems that the ants' behaviour is best explained if the odour is in the form of a field rather than as discrete spots or trails. The lack of effect on the ants when the paper disc was turned through 90° implies that if the odour is in the form of trails, the ants are not using this as a cue for their orientation, since they continue to walk across the paper when any trails are presumably at right angles. In any case the scent cannot be in such a narrow trail as is the case in Monomorium or in Pogonomyrmex, where all the ants leave the nest in definite routes. In Myrmica that situation is approached after the ants have been fed from a long lasting sucrose source placed away from their nest in the arena. The ants leave the nest in the direction towards the one they have been fed in, even after the sucrose has been removed for one or two days. But in this case, there is no approach to the narrowness of the routes described in the other two ant species. (This situation of the ants being biased in the direction to which they leave the nest is discussed in the next section). The difference between a wide odour trail and an odour field is non-existent.
SOURCE OF THE ODOUR Ants were allowed to forage over a clean arena surface for three weeks but they were fed by means of a side opening to the tube connecting the arena to the nest. No recruiting odour trails were laid as far as is known on the arena surface. At the end of the three week period no ants leaving the nest entrance were observed to pick up a menotaxis, or if they did, it was lost too soon to be demonstrated by the method of moving the lights. In an arena in which
ants had been fed, and recruiting odour trails had been laid to the nest, -35- ants were observed to leave the nest with a menotaxis after one week. However, the number of ants that had foraged in the foodless arena for the three week period was only about the same as in the arena with the food for the one week period, that is there were only about one third the number of ants present in the arena without the food at any one time as in the arena with the food. So the lack of odour that maintains the meno- taxis in the ants in the foodless arena need not be due to the lack of odour trails in this arena, but might be due to the lesser number of ants depositing this odour. A piece of paper 20 cm square over which ants from a different nest had laid a recruiting trail the day before was plaCed next to the nest entrance in a clean foraging arena. One ant out of 22 leaving the nest over this piece of paper was observed to up a menotaxis while passing over this piece of paper. One week later, 4 ants out of 25 were observed to up a menotaxis while they crossed this sheet of paper. The paper had been left in the arena for that week. From these experiments it is impossible to prove that the odour maintaining the menotaxis in the ants is some product of the recruiting trails of these ants. An experiment that might have yi elded some connection,would have been to have placed the paper which had had the recruiting trail laid over it the day before, away from the nest entrance in an old foraging arena. If ants had then lost their menotaxis when passing over this piece of paper, it would have shown perhaps that a day old recruiting trail was 1\ a sufficient stimulus to enable the ants maintain their menotaxis. However a positive result would not have been proof that the odour present in the arena is a decay product of the recruiting odour trails.
Behaviour similar to that of Myrmica seabrinodis on scented and unscented areas is shown by Eciton sp. (Vowles 1955), where, the army ants turned alternately from side to side on unscented areas, but ran straight on an area scented with their trail pheromone. Price (1970) has shown that female Pleoloplus, Endosys and Mastrus (Hymenoptera Ichneumonidae), when searching the ground cover for their -36- hosts, respond to their own trail pheromone by avoiding researching these areas. Here the response is by orthokinesis, the females move faster in areas with the trail pheromone, which also appears to act as an irritant. The response in Myrmica scabrinodis is a klinokinetic one, there is an increase in the rate of undirected turning in the areas without the odour, which has the effect of concentrating the ants in the odourless areas. (See discussion page 64 ). Wilson (1962), shows that Solenopsis saevissima will lay trails to extensions to their foraging areas. These are presumably distinguished from the original area by odour, which may be a similar phenomenon to that in Myrmica where the ants can distinguish new areas by their odour, though these ants do not lay trails to them.
The behaviour of Myrmica scabrinodis losing their menotaxis in unscented areas may have considerable adaptive value for the ants. It provides a klinokinesis that keeps them in unscented and thus unsearched areas. The actual twisting path followed by the ants is no better a foraging strategy for searching an area than is a straight path of the same length, in fact if the ant crosses its own path it is obviously a worse strategy since the same area is being searched twice. The twisting path however will increase the chance of the ants finding food sources close to its own nest, whereas in the case of a straight course out from the nest and straight back again of the same length as is the twisting path described above, food will on average be found further from the nest. This means that there will be less chance of controlling the food by defending it from ants from other nests/as it will take longer to recruit ants to exploit the food (Brian 1955). More energy will also have to be expended in bringing the food back to the nest. This behaviour of losing the menotaxis in unscented areas may also have the function of lessening the chance of the ants becoming lost, as they will lose their orientation and go little further from the nest once they are in unmarked territory. The behaviour of the ants in not picking up a menotaxis once they have regained a scented area may also be of importance to the ants. A -37-
scented area once found might not belong to the same nest, and picking up a menotaxis in this area might lead to an ant getting lost, or to reaching the nest entrance of the other nest where it would be likely to be killed. -38-
SEC TI ON 5 .
THE DIRECTIONS TAKEN BY ANTS LEAVING THE NEST
It was noticed that the directions in which the ants were leaving the nest in a foraging arena were often clustered towards one direction, even though no recruiting trails had been laid from that direction to the nest for one or two days, and it had been shown that a recruiting trail was effective on the ants for only a period of minutes (page 92 ). The following experiments were devised to investigate the mechanisms controlling this clustering of the ants° paths.
METHODS
The amount of clustering of the ants° paths and the direction to which they were biased was determined by noting for ten minute periods the positions at which individual ants crossed in an outward direction the edge of the area formed by the four ten centimetre squares surrounding the nest entrance. This was done by marking the position at which the ant crossed the boundary on plans of the area. The results were later plotted to produce the circular distributions shown in Figs. 11 to 19 and the distributions were analysed by the techniques given in Batschelet (1965). The edge of the squares was chosen as these were already marked on the arena surface. The corners of a square are further from the centre of a square than are the midpoints of the four sides. Ants spreading out from a point source such as a nest entrance might be expected to have an exponential rather than an even distribution of outward distances, which means that more ants would be passing through the mid points of the sides of the square area than would pass through the corners, since the mid points are closer to the centre where there are more ants. However this does not hold as the majority of the ants getting 10 cm from the nest entrance are orienting menotactically away from the nest entrance even those going the opposite way to the bias and thus the numbers going through each length of the side of the square are only dependent on the angle this -39- subtends at the centre of the square. When no clustering of the ants' paths could be observed in any one direction, there was never any sign of clustering at the four mid points of sides of the square in the records of their tracks. The directions of the ants leaving the nest were recorded for two ten minute periods to determine the initial bias in the direction of the ants leaving the nest. The bias remains the same direction for up to three days in an unfed colony, but the amount of the bias slowly declines till it is undetectable four days after the ants have been fed. (Figs 12 A B. ). The nest direction was then blocked, and all the ants foraging on the surface of the arena were removed and put back into the nest by a side arm to the tube connecting the nest to the arena. Some physical feature of the arena was then changed, the ants released from the nest entrance, and after one hour to allow the ants to settle down, two more ten minute records of the directions in which the ants were leaving the nest were taken. When no feature was changed in the arena but the above procedure carried out, the bias in the directions at which the ants left the nest remained unchanged. When the ants on the arena surface were removed but not replaced inside the nest, the bias in the directions taken by ants emerging from the nest was also present and the same direction as before. Only one record of the effect of changing a feature in the arena was taken on any one day. Before another feature was changed, the bias in the direction at which the ants left the nest was re-established as described in the next section.
THE DIRECTION OF THE BIAS
When the ants showed a bias towards a particular direction of leaving the nest this was always towards the direction in which food had been placed the day before. This was sham by first testing the bias on a clean arena surface, no bias was detectable (Fig. i3 ). The ants were then fed 0.5M sucrose 40 cm from the nest entrance one day, and the direction of the bias noted the next day. -40-
FIGURE 12 A.
DIRECTIONS IN WHICH ANTS LEFT THE VICINITY OF THE NEST ENTRANCE ONE DAY AFTER FEEDING.
Directio in which food placed.
B.
DIRECTIONS IN WHICH ANTS LEFT THE VICINITY OF THE NEST ENTRANCE THREE DAYS AFTER FFFOING.
—Direction in which food placed FIGURE I3.
DIRECTIONS IN WHICH ANTS LEFT THE VICINITY OF THE NEST ENTRANCE ON A NEW FORAGING ARENA SURFACE.
A -42-
This was repeated four times, each time with the sucrose in a different direction from the nest entrance. The results are shown in Fig. 14 . In each case the bias in the direction at which the ants left the nest corresponded with the position the sucrose had been in the day before, so it is very likely that the position of food one day controls the direction of the bias the next.
FACTORS CONTROLLING THE DIRECTION OF THE BIAS
Ants were fed on sucrose as described above and after one day their directions of leaving the nest were recorded, a feature of the arena was changed and the directions recorded again as described on page
1. The paper of the foraging arena surface in a 60 cm circle surrounding the nest entrance was rotated through 1800, but all other features of the arena including a light at one end were left unchanged. This had no effect on the direction in which the ants left the nest. (Fig. 15 ).
2. The light at one end of the arena was switched off, and the arena lit by diffuse top lighting only. In these conditions no menotactic orientation is possible, and any bias in the direction taken by the ants must be due to the arena surface. Far fewer ants left the area around the nest entrance in these conditions than when there was a light at the end of the arena. However a bias was detectable, more of the ants leaving the nest towards the position of the food than.in other directions (Fig. 16 )•
3. The light at one end of the arena was switched off and the:paper of the arena surface was turned through 1800. More of the ants now went off in the direction away from the food than in the other directions (Fig, 17 ). These two experiments, Nos.2 and 3 indicate that the arena surface alone has enough cues to orient the outward paths of the ants in the previous direction of the food.
4. The light at one end of the arena was switched to the other end, no other feature of the arena was changed. The bias in the direction at which the ants left the nest was changed, but not abolished. As many ants left FIGURE 14 . DIRECTIONS iN WHICH ANTS LEFT THE VICINITY OF THE NEST ENTRANCE AFTER FEEDING IN DIRECTION OF ARROW ON THE PRECEEDING DAY. -44-
FIGURE 15
DIRECTIONS IN MICH ANTS LEFT THE VICINITY OF THECNEST ENTRANCE, BEFORE (A) AND AFTER (B) THE PAPER SURROUNDING THE NEST ENTRANCE WAS ROTATED THROUGH 180°.
A.
= 2 ants 0 = I ant
B. -45- •
FIGURE 16. DIRECTIONS IN WHICH ANTS LEFT THE VICINITY OF THE NEST ENTRANCE, BEFORE (A) AND AFTER (B) THE LIGHT AT THE END OF THE ARENA WAS SWITCHED
A.
B. FIGURE 17 . DIRECTIONS IN WHICH ANTS LEFT THE VICINITY OF THE NEST ENTRANCE, BEFORE (A) AND AFTER (B) THE LIGHT AT ONE END OF THE ARENA WAS SWITCHED OFF AND THE PAPER SURROUNDING THE NEST ENTRANCE ROTATED THROUGH 1800.
A.
®= 2 ants. 0 . 1 ant.
B . -47-
FIGURE 18 DIRECTIONS IN WHICH ANTS LEFT THE VICINITY OF THE NEST ENTRANCE, BEFORE (A) AND AFTER (B) THE LIGHT AT ONE END OF THE ARENA WAS SWITCHED TO THE OTHER.
A.
• = 2 ants o ,= 1 ant ) 48-
FIGUPE 19 DIRECTION IN WHICH ANTS TEFT THE VICINITY OF THE NEST ENTRANCE, BEFORE (A) AND AFTER (B) THE LIGHT AT ONE END OF THE ARENA WAS SWITCHED TO THE OTHER, AND THE PAPER SURROUNDING THE NEST ENTRANCE WAS TURNED THROUGH 1800 .
• 2 ants. O. 1 ant.
B. -49- the nest towards the previous position of the food as left the nest away from the previous position of the food. However, the numbers of ants leaving the nest in other directions was still much lower than would be expected if there was no bias in the direction to which the ants left the nest. (Fig. 1E ).
5. The light direction was reversed and the paper of the arena surface was turned through 180°. The bias in the direction of the ants leaving the nest was fully reversed. The same percentage of ants that had previously left the nest in the direction of the previous position of the food, now left in the opposite directior Fig• 19 )
From these results it was evident that the direction the ants left the nest was being affected both by the paper of the arena surface and the light direction, since turning the light direction through 180° had less effect on the direction the ants left the nest, than did both turning the light direction through 180° and turning the paper of the arena surface through 180° at the same time. A most surprising thing about the results of these experiments was that turning the arena surface through 180° had less effect on the ants than turning the light direction through 180°. (Experiments 1 and 4). This result was unexpected as it was thought that since the arena was symmetrical about the nest entrance, and the only visual feature the ants could be shown to orient by was the light at one end or the other of the o arena, turning the arena surface through 180 would have exactly the same effect on an ant as turning the light direction through 180°. This result implied that there was some other feature of the arena by which the ants could orient, though it was felt that this was probably not anything detectable on the surface of the arena such as draughts, as no oriented behaviour could be found with ants in the dark, or in diffuse vertical light. The most likely explanation is that there was some oriented cue inside the tube connecting the nest to the arena surface. This could be scent marks inside the nest entrance, or the direction in which the tube was bent when it entered the nest horizontally after passing vertically through the table. -50-
Even if there is some cue in the nest entrance the results can only be explained if the ants are able to 'carry over' from day to day the menotactic angle at which they left the nest the day before. This can be seen by the results of experiment- 4. With the light direction alone changed, all other features of the arena being unchanged, there is still a change in the direction of the bias at which the ants left the nest. To react to this change in the light direction the ants must have had some carry over of the angle they were orienting by previously. That the ants were carrying over this angle from day to day, and not from foraging trip to foraging trip was proved by shutting the ants into the nest overnight after feeding them with sucrose solution as before. The next day the ants were released and experiment 4 repeated; with the same result. A 'carry over' of this nature has been reported from honeybees, Lindauer (1954), and from Wood ants Formica rufaL. Jander (1957). Ayre (1968) reports that in Myrmica americana Emery, ants recruited by a scent trail, after half an hour are no longer orienting by the trail but by "memory". He showed this by having ants lay a trail from one branch of a 'Y' shaped stand, down the stand and along an arena to the nest. After half an hour he rotated the stand and the recruited ants went up the wrong arm. However he did not show by what stimuli the ants were orienting to the wrong arm, (presumably visual), or that the ants that went up the wrong arm after rotation of the stand had made a previous trip to the food and thus had a "memory" of the direction to turn at the junction. An explanation of the results not given by Ayre might be that on the trail to the stand the ants had picked up a menotaxis, this occurs in Myrmica scabrinodis whilst on a trail, see page 106. The stand may have been arranged so that the branches were in line with the trail. When the ants reached the junction on the 'Y' stand, they turned the way that took them most nearly in line with their previous menotaxis. This would be a similar phenomenon to that of 'Correcting Behaviour' (Dingle 1964) or Centrifugal Swing (Schnetrla 1929 ). In these phenomena an animal after a forced turn in one direction makes a turn in the opposite direction at the first opportunity. It has been discussed in terms of the'optomotor reaction', (Wilson and Hoy 1968), not for menotaxes but Wigglesworth (193p) points out, there is no distinction between optomotor reactions and -51- photomenotaxes. (For fuller discussion, see page 120). Because of these objections, the presence of a 'carry over in My-rmica americana is not shown by these observations by Are.
However a 'carry over' has been demonstrated in Myrmica scabrinodis page 81. If it is accepted that 'carry over' of menotactic orientations can occur from day to day, the way this effects the orientation of the ants is probably as follows. Anant leaving the nest entrance is affected by the directional cues in the nest entrance. If they correspond with the carried over menotactic angle the ant picks up the carried over menotactic angle and walks away from the nest entrance. If the paper arena has been turned, this has little effect on the ant, but if the directional light stimulus is not present, the ant orients by odour cues from the arena surface. (Experiments I, 2, 3). If the light direction has been altered so that it no longer corres- ponds with the cues inside the nest entrance, some ants orient by the carried over menotactic angle, others pick up a new menotaxis from cues on the paper arena surface. (Experiment 4). When both the light direction and the ,paper arena surface have been altered, the ant behaves as above, some orienting by the carried over menotactic angle, others picking up a new menotactic angle from cues on the paper surface, however this time the old and the acquired menotaxis have the same angle (Experiment 5). This hypothesis could be tested by rotating the tube from the nest to the arena by 180°. When the light direction is then also reversed, the ants should all reverse their bias, the situation now being the same as rotating the paper arena only as in Experiment 1. If the ants do not reverse their direction of travel completely as in Experiment 5, the cue cannot be in the nest entrance. Some cue on the arena surface would have to be looked for. A bias in the direction in which ants leave the nest has been reported many times. In Myrmica rubra = (ruginodis Nyl) Brian (1956) found that in Scotland where the areas suitable for nesting were limited in area, many nests occurred close together in suitable places such as -52- rotting logs. The ants from each nest foraged radially outward from each nest away from the other nests, thus each nest was at the end of a large foraging area. Yasuno (1965) reports similar asymmetrical foraging areas in Formica truncorum, Formica exsecta, Formica fusca and Camponotus herculeanus in Japan. Wilson, DiHier and Markin (1971) show that Solenopsis.saevissims richteri Forel also have asymmetrical foraging grounds. The situation described above in Myrmica scabrinodis provides a mechanism which would maintain such asymmetrical foraging areas.
Sudd (1965) shows that Monomorium pharaonis leave the nest along a few odour marked routes from which the ants slowly leak, a situation similar to that of Formica aquilonia except that the latter's routes are probably not marked by odour. Holt (1955), It seems likely that the bias in the direction taken by Myrmica scabrinodis when it leaves the nest, which it has been shown is partly controlled by odour, is very similar to the situation in Monomorium where the bias, wholly controlled by odour, is much greater.
It seems likely that the odour on the arena surface that can guide the ants to leaving the nest in one direction, is the same as the odour on the arena surface which maintained the menotaxis in the ants, that was dis- cussed in the last section. The guiding odour seems definitely to be related to the presence of recruiting t rails, which could not be shown with the odour maintaining the menotaxis. The odour maintaining the meno- taxis is possibly a general field of odour left from many recruiting trails converging on the nest, while the guiding odour may be an increase in the strength of the field in the direction the food lay the day before, and thus where the most recent trails are to be found. It might be possible to test this hypothesis by allowing ants laying trails to approach the nest from only one direction after a colony has been placed in a clean arena, but to allow foraging ants to scatter all over the surface when trails are not being laid. If the hypothesis that the odours with the two different effects are the same is true, ants should only pick up a menotaxis in the direction towards the previous position of the food. -53- instead of in all directions but with a bias towards the previous position of the food, as happens when ants are allowed free access to the arena at all times. -54--
SECTION 6. KLINOTAXIS OR TROP O TAXIS When a drop of 0.5 M sucrose was brought near to the antennae of ants that were either orienting menotactically or pottering; they stopped, and then turned toward the drop and walked slowly toward it. Their antennae were held forward and up from the head towards the sugar solution, and they were waved from side to side. This was quite different from the way the antennae were held whilst foraging, when they are held level with the body of the ant and are tapped against the substrate. Ants with only one antenna could orient toward the sugar droplet just as well as ants with two. The ants are obviously performing either a tropotaxis, or a klino- taxis, but one cannot say which as it is not known whether the stimulus gradient is being along the length of one antenna or both, between the two antennae, or between the successive positions of each antenna. The behaviour of the ants with only one antenna suggest that it need not be detected between two antennae. The stimulus detected by the ants from a drop of sucrose is not known. Ants will orient as above to droplets of distilled water, but once they have been allowed to drink freely from these, significantly more ants orient to droplets of sucrose solution than do to droplets of distilled water. Pottering ants were presented with a droplet of distilled water held on a wire loop, and allowed to drink from this until they left the drop. 20 ants were then presented with a drop of 0.5 M sucrose solution held 5mm away from them, one minute after they had left the distilled water, 20 ants were presented with a drop of distilled water of the same size held 5mm away from them, one minute after they had left the distilled water. The numbers of ants that reacted by orienting to the droplets and walking towards them are given in Table 5 These results were compared using the Chi Squared Test, and are significantly different at the p 0.01 level. Since significantly more ants oriented to the sugar droplet than did to the water droplet, the stimulus detected by the ant cannot be water vapour given off by the droplet, as more of that would be given off by the water droplet which had the same surface area but higher concentration of water than did the sugar droplet. -55-
TABLE 5. RESPONSE OF FORAGING ANTS TO DROPLETS OF 0.5M SUCROSE SOLUTION OR
DISTILLED WATER HELD 0.5 CM FROM THEM ONE MINUTE AFTER FEEDING TO
SATIATION WITH DISTILLED WATER.
Nature of Droplet. No. of ants walking No. of ants not
up to droplet. walking to droplet.
0.5M sucrose 14. 6. solution.
Distilled 5. 15. water. -56-
0.5M and 1M sucrose solutions lose water by evaporation, so there is no chance that the antswe.re detecting the sucrose droplets by any decrease in the water vapour concentration in the air as the sucrose solutions took it up from the air. Since sucrose is almost involatile, and cannot be sensed at a distance, (Dethier, Barton Browne and Smith 1960) it seems likely that the ants are responding to some decay product of the sucrose solution such as alcohols produced by yeasts. However, the sucrose solutions used were freshly made up from a stock of vAnalart sucrose and distilled water, so there can only have been very small quantities of such substances present. More experiments are therefore needed before one can discover the cue that enables the ants to distinguish sucrose solutions from water. Similar tropotactic or klinotactic orientations are performed by the ants to other objects, such as squashed flies, which can be detected from 10 cm away and intact aphids. sW -.57-
SECTION 7,, KL]NOKINESIS
If sucrose solution is removed from the ants after the ants have started to orient towards it, but before they have come into contact with it, or if it is removed from feeding ants before they are sated and have stopped feeding, the turning rate of the ants is increased by a factor of about 4 while their speed of movement is also increased for a period of about one minute. A typical track is shown in Fig. 20 which is the track of a pottering ant which had a drop of 0. 5M sucrose brought into contact with one of its antennae. An ant which had a clean wire touch its antenna showed no such reaction. The mean turning rate of the ants increased from 1Z° to 50° per centimetre. The speed of movement increased from 30 to 45 cm a minute, and the rate of turning per second from 14° to 38°. The relation between rates of turning per centimetre and per second of course depends on the walking speed of the ants. These figures are the average of 10 tracks from pottering ants for half a minute before stimulation with sucrose and for half a minute afterward. This reaction is a klinokinetic one, since the turning rate of the ant is increased without there being any apparent directional bias to the turning. There is also an orthokinetic reaction, as the speed of the ants is increased by the stimulus. See page 62 for a discussion of klinokinesis. This behaviour is similar to that observed by Dethier (Igs-7) in flies after they were fed from drops of sucrose too small to sate them, that is they would drink a second drop if found. It is also performed by Coccinellid (Banks 1964) and Syrphid (Chandler 1969 ) larvae after contact with an aphid. It has been shown by Nurdie and Hassell (1973) that this behaviour is adaptive to animals whose prey or food is clustered, since the animal is more likely to find another food item by intensively searching the area in which it found the first. In flies (Dethier 1957) the rate of turning and the duration of turning are proportional to the strength of the stimulus producing the klinokinesis. That is true also of honeybees where the 'dance' of a returned forager inside the hive appears to be a form of delayed klinokinesis resulting from
the food find. -58- FIGUHE 20.
PATHS OF POTTERI~D ANTS PRESENTED WITH A DRGP or·' o· 5H SUCHOSE FRON \'J1-IICH THEY \'JERE NOT ALLO/JED TO FEED.
-,----
I . -----.~ , I ,___ -'- __-'--_--L-' _._L_._~
~.: - .. - 1-10 cmo.(
~----lO cncnot------I -59—
Hero the dancing is performed more vigorously as the strength of the food find increases, and the nearer the food to the nest, the greater the number of turns and the more hasty the 'waggling'. In Myrmica scabrinodis no correlation could be found between the rate or the aura:lion, of turning, and the strength of the sucrose producing this response, or the amount of sucrose solution ingested, or the distance of the ants from the nest. This emerged from an experiment in which the ants were given a sucrose solution of 0. 1M, 0.5M, and 1.0M for different periods of time; 0 seconds, where the sucrose was touched to their antennae but they were not allowed to feed from it, 1 minute, and 2 minutes, at different distances from the nest, 10,20 and 30cm. After the two minute presentation the ants were often sated and showed no klinokinesis. The results in this section of Table 6 therefore show the mean results for all ants allowed this period of drinking, and also the mean of those that did perform the klinokinesis.
The half life of this period of increased turning was measured from only two observations on each path of the ant. The turning rates were measured for a ten second period immediately the klinokizletic circling was started and again for a ten second period thirty seconds later. A drop was always found in the rate of change of direction between the two figures, and the half life for the decay of the increased turning calculated from this to the nearesthalf minute. The figures in Table 6 are the averages of this figure for the ants in each condition corrected to the nearest half minute.
The figure for the rate of turning of the ants in each condition is obtained from the first 30 seconds of their path after the turning rate increased.
As can be seen from Table 6, there are no significant differences between the results of any treatment, Since it was very time consuming to extract these results from the paths of the ants, and very large replicates would be needed to disprove that klinokinetic circling in Myrmica is an all or none phenomenon, this experiment was carried no further. . Strength of sucrose. 0-1M 0.5M 1.OM
Distance from 20 10 20 30 20 nest.(cm)
Time allowed to drink (min) 0 1 1 0 1 2 1 0 1
Half lfe of decay of 90 60 60 30 60 30/15 90 60 60 increased turning ( sec)(see text)
R.C.D. (° sec ) 41 33 48 35 46 21/42 42 34 33
Number of 5 :5 5 10 11 8 5 5 5 observations. -61.-
Chandler(1969) found that the klinokinetic circling behaviour of
Syrphid larvae was initiated after only a few seconds of contact with an
aphid, and that it increased in strength 0.11, the larva had been in
contact with the aphid for about 5 minutes, then slowly declined.
The larva apeared to start to feed on the aphid. only after it had been in contact with it for more than 2 minutes. So the increased turning rate
after the larva had been in contact with the aphid for shorter periods than
this, must have been initiated through surface receptors on the larva, and
not through any internal change brought on by the presence of food in its
gut. This seems very similar to the situation in Nyrmica where the circling
behaviour is initiated after the antennae alone have sensed the presence
of sucrose solution. -62-
There is a confusion in the literature about the nature, classification, and even existence of klinokinesis. The term was first used by Gunn, Kennedy and Pielou (1937) who defined a kinesis as "Variation in generalised undirected, random locomotory activity due to variations in intensity of stimulation", and a klinokinesis as "changes in rate of change of direction" (R. C.D.) This was based on the:work of Ullyott (1936) on the planarian Dendrocoel um lacteum. This work has however been thrown in doubt by that of Stasko and Sullivan (1971), and Gunn (1966) had already said that the whole concept of klinokinesis was in doubt. Since it cannot be doubted that rates of changes in direction do vary in animals in response to stimuli, Gunn presumably meant that the role of these differing rates of change in direction in concentrating animals in "favourable" areas was in doubt. There appear to be two different mechanisms by which a klinokinesis can concentrate animals in one area rather than another. The fir st iof these was recognised by Frankel and Gunn (1940) and is the situation where the animal has a higher R. C.D. in the "unfavourable" area and a lower R.C.D. in the "favourable" area in which it congregates. Thus the animal walks straighter in the "favourable" area than it does in the "unfavourable" area, which has the effect that the animal is more likely to turn back once it is in the unfavourable area. An example of this type of klinokinesis is the behaviour of the louse Pediculus humanus on smooth and rough surfaces, (Wigglesworth 1941). On the rough surface of unglazed paper the lice walked straighter than they did on the smoother surface of glazed paper, and they were often observed to regain the unglazed paper after crossing the boundary from the unglazed to the glazed paper (Fig,21 ) The second mechanism by which animals may be concentrated in one area rather than another is the opposite of the above, they are concentrated in the area where they have the higher R. C.D. The animals walk straight until they reach a favourable area where their R. C.D. increases, and the animals are trapped inside the area with the higher R. C.D. This is similar to the orthokinetic response, where an animal slows down in the favourable area thus spending more time in these than in the unfavourable areas through which it passed quickly. In the klinokinetic case, the speed of the animal -63-
FIGURE 21. (After Wiggleswobth 1941)
woollen glazed unglazed woollen unglazed silk paper stockine paper paper stockinet
,\
.1.7 --'''`9'-'7' (5 min.) '`"(6 mm.) (8 min.) woollen A cotton cotton blotting C. cotton silk stockinet stockinet stockinet stockinet paper ,,.f-j 'x-,:,.— 1,- -• :•.:7-7' .
Reactions of lice to rough and smooth materials (A-11. Below, the path followed (during three minutes, observation) by a louse in a petri dish with a strip of flannel on a floor of blotting paper; its activities are almost confined to the strip (Wigglesworth ').
FIGURE 22. ( After Davenport et al.)
„.„ . Tracings:of tracks of Pinnixa cliactoptcrana. A. Four tracks made by a single crab, the central stream of water entering through hole at top and leaving at bottom, labelled with fluorescin, fills the area within the clotted line. B. Same crab with host-factor in the stream. C. Track of a crab in a trough filled with host-factor. Marks on tracks at so sec. intervals (Davenport, Camougis and Hickok. ). -64-
is unaffected in the area in which it is concentrated but its velocity, a vector quantity, is reduced because its turning rate is increased. The straight line distance travelled, or the animals net displacement is reduced in the area with the higher R.C.D. Surteeg1964) uses the ratio of the speed of the animal to its velocity in different conditions to discover if animals are orienting by orthokinetic or klinokinetic mechanisms. Examples of animals showings this type of klinokinesis are numerous. Pethier (1947) recorded that Monarch Butterfly caterpillars showed in- creased R. C.D. when on. a screen over a host leaf compared to the R. C.D. of caterpillars on a screen not over a host leaf. In 1957 he showed. that the turning rate of flies was increased after feeding with quantities of sucrose solution insufficient to sate them, and Murdie and Hassell (1973) showed, using a mathematical model, that the observed increases in the R.C.D. of flies after feeding on sugar would keep them in the area in which the sugar droplet was found. Chandler (1969) found that the R. C.D. of first instar Syrphid larvae increased from 80° min to 300° min after contact for 5 minute with an aphid and that this increase in R. C.D. concentrated the larvae in areas where they had found aphids. Davenport, Camougis and Hickok (1960) recorded that the R. C.D. of the parasitic crab Pinnixia chaetopterana was higher in water containing the "host factor" than it was in pure sea water, and the effect of this was the "capture of the crabs inside the areas of host factor (Fig. 22_ ) . In Myrmica scabrinodis a klinokinetic mechanism of this nature concentratesants on odourless areas of substrate (page 36 ) In the odourless area the speed of the ant drops from 44 cm a minute to 36 cm a minute, the R. C.D. increases from 12° per cm to 25° cm. The orthokinetic component in the concentrating mechanism can be ignored by considering only the path lengths of ants in the odourless and scented areas. In Table 7 these are given for an ant in the 4 x 10 cm scented squares adjoining a 4 x 10 square odourless area, and the path length for that ant on passing into the odourless area is also given. As can be seen the path length on the odourless area is significantly longer than that on the scented area, proving that this klinokinetic response does concentrate the ants in the odourless area. Since klinokinesis has been shown to concentrate ants either in the -65-
TABLE 7.
LENGTH OF PATH OF ANTS IN THE BLOCK OF FOUR TtW CENTIMETRE SQUARES
ADJOINING THE NEST ENTRANCE, AND IN A NEWLY EXPOSED BLOCK OF FOUR
TEN CENTIMETRE SQUARES ADJOINING THESE.
Length of path in Length of path in area adjoining nest newly exposed area.
entrance. ( cm) ( cm )
20 44 25 43 23 37 22 51 24 26 23 41 22 38 24 33 42 38 47 49
27.2 40.0 -66-- area with the higher R. C.D. or in the area with the lower R. C.D. it is important to find out what the differences are between the behaviour of the animals in the two cases that lead to such different results. It seems likely that a small change in the behaviour of an animal would be enough to cause a klinokinesis to have these two different effects. For instance, an increase in the reaction time, the time spent in the area where an animal has a higher R.C.D. before its R. C.D. increases, would lead to the animal passing further into the area before its R. C.D. increases. It would then be unlikely to reach the boundary of this area, because of the twistiness of its path. If the reaction time before the increase in the R.C.D. increases is short, the animal is likely to recross the boundary of the area in which the R.C.D. is increased much more quickly and thus will spend more time in the area with the lower R. C. D. With this in mind it is interesting that Myrmica has a long reaction time before the absence of odour initiates a change from menotaxis to pottering (Fig 11 .) It is not claimed that a change in reaction time is the universal mechanism producing these different results from what seems a simple piece of behaviour, other differences are possible and probably exist. Kennedy (1945) divided klinokinesis into two types depending on the stimulus intensity associated with each R.C.D. Thus if there was a high stimulus intensity associated with a high R. C.D. and a lower stimulus intensity associated with a lower R.C.D. this was a "Direct" klinokinesis, if a low stimulus intensity was associated with a high R. C.D. and a higher stimulus intensity with a low R. C.D. it was an "Inverse" klinokinesis. This scheme works for most stimuli, however it is difficult to decide on a physical basis whether the glazed or the unglazed paper is the higher intensity stimulus in the case of the louse. A know- ledge of the method of operation of the receptor of roughness, or smoothness is needed before one can tell. On the other hand a classifica- tion of klinokinesis based on the two mechanisms described above, although necessary, is more difficult to apply since the precise factors leading to the different mechanisms are not known. Thus a klinokinesis could only be classified after a thorough study of its results, whereas the scheme adopted by Kennedy can give a definition of a klinokinesis -67-
ir.nnlecliately the stimuli affecting the R. C.D. are known, and. the effect these have on the R. C.D. The original description of klinokinesis included the gradual adaptation of the higher R. C.D. to a high stimulus intensity, this was necessary as the Dendrocoelium did adapt to high light intensities by decreasing its R. C.D. and this was thought to account for the movement of the animal down light gradients. However it is felt that both mechanisms of klinokinesis will operate, even if there is no adaptation, in confining animals to discrete areas with sharp boundaries. Adaptation may be necessary to account for the movement of animals up gradients by klinokinesis, but such a movement has not been rigorously demonstrated. Most klinokineses described are involved in some sort of "searching" behaviour. It would probably be to the advantage of most animals to temporarily suspend the operation of a klinokinesis, probably by adaptation if this search is unsuccessful, in order to leave the area to which it was confined by the klinokinesis. SECTION 8. THE RETURN TO THE NEST AFTER FEEDING ON OUTWARD MENOTACTIC ORIENTATION
Ants were fed to satiation from 0.5M sucrose solution, or given a portable prey such as an adult Aphis fabae during the menotactically controlled straight journey from the nest. When they left the sucrose, or picked up and carried the aphid, they picked up a menotaxis of opposite sign to the one they had on leaving the nest. This had the effect of taking the ants back towards the nest. (Fig. 23 ). The angle of menotaxis was shown to depend on the angle of previous menotaxis, and not on any odour cues from the paper surface of the arena, by switching the light by which the ants were orienting from one end of the arena to the other just as the ant reached the food. The menotactic angle picked up on leaving the food was then such as to take the ant directly away from the nest (Fig. 24 ). The length of time the ant spent at the food had no effect on the meno- tactic angle picked up. When ants were fed from a sugar source that would deliver the solution only very- slowly (usually a tube with a very tight fitting wick) from which ants took at least 5 minutes to reach a satiated state instead of about 2 minutes, the same menotactic orientation was picked up. In cases where the ants were directed away from the nest by changing the position of the lights as has been described above, the original meno- tactic angle was changed to a new menotactic angle after the ants had travelled from 5 - 30 cm, and was then changed again after legs varying
in length as is described on page- 75. The distances walked by 23 ants after leaving the spot where they were given an aphid before they lost their initial menotactic orientation when directed away from the nest by changing the light direction are given in Table 8 together with the distance each ant was from the nest when it was given the aphid. The correlation coefficient of the two distances is 0.3643 as deter- mined by the Spearman Rank Correlation Test, this is significant at the
p = 0.05 level. -69- FIGURE 21.
CHANGE OF NENOTACTIC ANGLE IN ANTS FED MITE ORIENTING BY THE LIGHT.
.....t..._
F."
....4...... ----
....4
)(= position where fed. -->= position where light direction reversed. O. position of nest entrance. FIGURE 24. THE EFFECT OF CHANGING THE LIGHT DIRECTION WHEN AN ANT IS FED.
1
_L. - -70-
TABLE 8. DISTANCE WALKED BY AN ANT BEFORE FIRST CHANGING THE ANGLE OF TTS MENOTACTIC ORIENTATION AFTER BEING GIVEN AN APHID AT DIFFERENT DISTANCES FROM THE NEST ENTRANCE WHILE ON THE INITIAL OUTWARD MENOTACTIC ORIENTATION.
Distance of ant Distance walked from nest entrance by ant till menotactic when given aphid. angle first changed. ( cm ) ( cm ) 10 15 10 20 10 9 10 5 11 10 15 20 15 20 15 8 25 5 25 . , 25 25 26 25 21 25 30 25 13 25 3 30 23 31 20 31 21 31 23 31 15 31 6 31 19 31 36 -71-
This implies that the further an ant has walked from its nest before being presented with food, the further it walks before losing its orientation after being fed. This might be thought to be evidence for a "kinaesthetic sense" in the ants, recording the distance they have walked, perhaps by the energy expended as in honeybees. However, another explanation is possible so this will be considered first. The ant could be telling from some cues from the odour present in the arena surface that they are getting further away, not nearer to the nest. Suppose the odour field around the nest decreases exponentially in strength with the distance away from the nest. Then the further an ant is from the nest the further it will have to walk to produce the same drop in intensity of the scent field, since the new menotaxis is now taking the ant directly away from the nest entrance (Fig. 25 ). This could be ruled out by giving the ants a piece of clean paper to cross during this initial leg of the menotaxis. If the ants were noticing a decrease in the scent field they would be expected to lose their menotaxis when passing over the paper. This experiment has not been done with ants directed away from the nest, however 10 ants approaching the nest entrance, when the direction of illumination has not been altered during their foraging trip, did not lose their orientation when crossing a piece of clean paper (Fig 26 ). So it is unlikely that the amount of scent present in the arena has any bearing on the distances walked by the ants before losing their initial menotactic angle. Evidence suggesting the presence of a kinaesthetic sense has been been found by Jander (1957) in the ant Formica rufa L. He presented the ants walking along a straight path successively with two lights. The first o was at 135 to their course and was lit for 30 seconds, the second was at 225° to their course and was lit for 10 seconds. This cycle of two lights was repeated several times. When these ants were later presented with a single continuous light, they would orient to it at 159°, near the resultant of the two previous light directions. (135 x 3 + 225)/4 = 157.5. This implies that the ant must either have been measuring the distance it had travelled while each light was
-72-
FIGURE 25.
DISTANCE WALKED BY ANT TO PRODUCE THE SANE DROP iN STRENGTH OF A SCENT FIELD AT DIFFERENT DISTANCES FROM THE NEST, IF THE STRENGTH OF THE FIELD DECREASES EXPONENTIALLY WITH DISTANCE FROM NEST.
Same drop in strength is produced by an ant walking further in position B than in position A. strength of odour field
...•■•••■•••••■••••■••> Distance from nest. FIGURE 26. LACK OF LOSS OF NENOTAXIS, OR OF A CHANGE IN 1TS ANGLE WHEN AN ANT CROSSED A DISC OF CLEAN PAPER PLACED IN ITS PATH.
...■......
...... -...... - ....mm
...... f - .
I 1 ..----■ [
C). nest entrance. '<= position where ant fed. 4....._ ,.position where light direction changed. -73 shining, or the times for which they had been shining. Jander has shown that the ants are able to correct their menotactic angle relative to the sun to within 1°, after being imprisoned in a light tight box for two hours. This means that the ants must be able to measure time intervals as short as 4 minutes since the sun moves through the sky at 15 0an hour. If the ants can do this, they can most probably measure time intervals shorter than this, so there is no need to postulate a "kinaesthetic sense" as in the bee which measures the distance it has travelled by the exertion it has needed to take it that far (Heran & Lindauer). However an experiment has shown that Myrmica scabrinodis has a sense of the distance it has travelled, rather than of the time it has taken to walk that distance (Sec. 10 ) so there may be a "kinaesthetic" sense. (in the simple meaning of naming the distance travelled rather than Pieron's (1904) idea of measuring the turns of the route as well) in this case also. -75-
AFTER FEEDING WHILST POTTERING
After the ants have walked for varying distances from the nest, having picked up a menotactic orientation, this menotaxis is lost and the ants usually start pottering, though some of the ants return to the nest straight away by reversing their original menotactic orientation. One of the stimuli causing the loss of this menotaxis has been shown to be the presence of a clean substrate (see Page 36 ) . Ants that had lost their menotaxis were presented with an aphid within 30 seconds. These ants set off towards the nest with a menotaxis opposite in sign to the one they had had on leaving the nest, and as in the previous section this angle of orientation was shown to be dependent on the original menotactic angle of orientation by reversing the light direction when the ant was presented with the aphid, and the ant would set off in the opposite direction to that of the nest. Ants that had been pottering for about one minute or longer were presented with an aphid. These ants also picked up a menotaxis, but the angle of their orientation to the light was not related to the previous meno- tactic angle, nor apparently to the nest direction (Figs.3.27 ). The angle of this menotaxis was changed after the ants had walked up to 35 cms., and the ants walked on at this new menotactic angle for a further few cms. This behaviour of straight, menotactically controlled "legs", was maintained until the ants reached the nest, sometimes taking up to 20 minutes.. A menotaxis is not detectable by the techniques used in the foraging arena if it is maintained for less than about 5 cm. So the distribution of the length of the "legsucannot be found out. However the average "leg" length observed was 16.5 cm (ii = 48). Ants that returned towards the nest by reversing their original, menotactic orientation, but were unable to find the nest entrance, either because they missed it, or because their path had been directed away from the nest by the experimental movement of the lights of the arena, lost their original menotactic angle, and behaved as did the ants that had been pottering for some time by changing their menotactic angle frequently to produce a path consisting of straight "legs" at angles to each other. -76-
FIGURE 27.
PATH OF ANT FED AFTER IT HAL BEEN POTTERING FOR TWO MINUTES.
I
...-.....4 .-
, r
)< 1 _ o = nest entrance. = position' where ant fed. = position where light direction changed.
FIGURE 28.
METHOD OF MEASURING ORIENTATION OF ANT TO NEST ENTRANCE AT THE START OF EACH LEG..
Nest entrance.
Pat ant.
'x' is the angle measured. -77-
Ants picked up from the nest entrance by giving them an aphid, and when they were grasping it firmly with their mandibles lifting the aphid and the ant together (a procedure which could be carried out without alarming the ant) were then deposited either in the arena or on a clean piece of paper, also behaved as described above. At first sight the angles picked up on each "leg" of the menotaxis appear to be random, however if the direction the ant is aiming at the start of each "leg" is examined this is found not to be so. 15 ants were picked up from the nest entrance by giving them an aphid as is described above, and were then placed at various points in the arena 50 cm from the nest entrance. Their paths were plotted, and the angle relative to, the nest entrance that each ant was facing at the start of each leg was measured. Only legs with a length of more than 10 ems were counted, as these were long enough to be reasonably certain in which direction the ants were orienting. The last leg before an ant reached the nest was not counted as this would have biased the resultS towards a lower value for the average angle of orientation towards the nest. 5 legs were analysed from each ant unless the ants reached the nest entrance on the 6th leg or before. The orientation of therant at the start of each leg in relation to the nest entrance was measured (Fig .28 ). The results are shown in Figure .29 . As can be seen, the distribution of the angles is not even which would be the expected distribution if the legs were randomly oriented with respect o to the nest direction. The average orientation is in fact at 57 to the nest entrance. The distribution of the angles was compared with the distribution expected if there was no bias towards the direction of the nest by using the Chi Squared Test, and it is significantly different at the p = < 0.01 level. The cause of this bias in the orientations of the start of each leg must be some cue in the arena that is related to the position of the nest. This could be either odour cues from the arena surface, or from the nest entrance itself, or it could be due to the position of the nest entrance in the centre of the arena where the ants could orient towards it by aiming for a point equidistant from all four walls„ To try and test which of these possibilities was the correct one, the arena surface was re-covered, and the experiment repeated on the fresh arena surfann Theres li s am crirrAriiYt Figure 0 As can be seen,
FIGURE 29 DIRECTION OF ORIENTATION OF "LEGS" OF RETURNING FORAGERS IN RELATION TO NEST 10 ENTRANCE IN OLD ARENA,
Numbers of legs 8 at given n = 43 6 orientation to nest entrance.
20 /4.0 6b go 160 120 1130
Angle of orientation of ant at start of each leg to nest entrance (0 ) FIGURE 30 . ORIENTATION OF "LEGS" OF RETURNING FORAGERS ON CLEAN ARENA SURFACE.
n=52 10 Numbers of legs at given orientation to 6 nest entrance. 4
0 t 0 20 40 60 80 100 120 140 160 180 Angle of orientation of ant at start of each leg to nest entrance ( ° ) -79- there was then no longer any bias in the orientation of the ants at the start of each leg towards the direction of the nest. Using a CM squared test, this cannot be distinguished from an even distribution. So it seems fairly certain that the bias of the legs towards the nest direction is caused by some cue from the arena surface, since this was the only thing changed between the two experiments. MacGregor (1948) found a similar path of legs with angles between them in foraging Myrmica ruginodis when given food in unfamiliar territory, but the angles between each successive leg of the path of the ant was much greater than is the case in Myrmica scabrinodis. The ants o often turning through more than 360 between each leg, instead of the 30 to 200 0change in Myrmica scabrinodis. A change of less than about o ZO will probably not be detected in a menotactic orientation in the typical short legs of their path. The mechanism for this orientation to the nest is not known. It may be that on the straight legs the ants are able to discover changes in the odour, concentration at different places in their path, and then react to them by a klinotaxis-like mechanism. Sh orey. (1973), discussing chemotactic mechanisms for insects following 'aerial trails' (Butler 1970) says "an increasing molecular concentration on the average, would be encountered as an insect proceeds towards the source. It seems entirely possible that the insect while flying through such a cloud of pheromone, could integrate and compare within its nervous system the various intensities of odour through which it has passed. Steering reactions (chemoklinotaxis) would be made to turn the insect back towards those positions in space where it had previously obtained highest pheromone stimulation." This situation, if it occurs, would be extremely difficult to analyse in a flying insect. However, in the ant, where the odour fields of different strengths, are readily available just by cutting paper from near to, or far away from the nest entrance, it would be much easier. Thus an ant if it were to cross paper from far from the nest, then from near the nest, then from far from the nest, during one leg of a menotactic orientation, would be expected to practically reverse its -80- direction of track on the next leg if the chernoklinotactic theory is true, since this would be equivalent to passing close to the nest but missing it and carrying on past it. SECTION 9, TRAIL LAYING BEHAVIOUR
Foraging workers were fed individually 40 cm from the nest entrance with 0.5 M sucrose solution. They fed from the sucrose and then left it and took up a menotaxis as has been described for fed ants in Section g The behaviour of these ants as they returned to the nest was observed and the effect of contact with these ants and with their trails on the behaviour of other ants was noted. Both of these will be described in this and the following sections. As they walked the fed ants laid an odour trail, (evidence for the existence of this is given on page $4 ). This trail was laid by dragging the tip of the abdomen along the substrate. There is obvious extension of the sting as has been described in Solenopsis Saevissima by Wilson (1962) and in Pogonomyrmex badius by Holldobler and Wilson (1970). In other details the trail laying behaviour of Myrmica scabrinodis is similar to that of Solenopsis. Trail laying ants move at a slower pace (38 cm min, n = 10, sd =5'4 ) to similarly fed ants not laying a trail (44 cm min. n =9 sdr6 ), the front end of the body is occasionally swung from side to side of the line of travel (this may account for the slower speed). , If other ants are met either on the arena surface or in the nest, they are tapped vigorously with the antennae. This may have an alerting function, or stimulate the tapped ant to move, since out of 25 ants so tapped inside the nest by returned, trail laying ants, 19 left the nest and followed the trail, while from 25 ants that were within 0.5 cm of a trail laid into the nest, but were not encountered by the trail laying ant, only 8 ants left the nest and followed the trail. These contacts do not lead, as in Solenopsis, to the trail laying ant reversing its light orientation and thus returning to the origin of the trail. (See i1.84 for further discussion of this behaviour). Once inside the nest ants fed with sucrose solution run around for a short time and then engage in trophollaxis with one or more workers before leaving the nest, and then they do not lay a trail towards the food. Ants laying a trail from food on which they cannot feed, and is too large to carry or drag, (page 88 ), sometimes do leave the nest after a few seconds and -82-
return to the food laying a trail. They do not appear to follow their own trail when doing this, but up a menotaxis immediately they leave the nest. The direction taken by these ants on leaving the nest was found to depend on the angle of the rnanotaxis the ants had used in returning to the nest, and not on cues from the trail they had deposited. If the light direction was reversed while the ants were in the nest, they left it in the wrong direction for the food, at an angle to the light opposite to the menotactic angle held while returning to the nest. (Fig 31 ). This behaviour of a trail laying ant returning to the food laying a trail was presumably that observed by Pickles (1936) in Myrmica ruginodis Nyl in Yorkshire when a group of 12 workers left the nest and proceeded in file to a dead cater- pillar nine feet six inches away. This behaviour was also observed by Wilson (1962) in Solenopsis and by Holldobler and Wilson (1970) in Pogonomyrmex
The behaviour of the ant leaving the nest and returning to the food find by reversing its menotactic orientation, is evidence that a 'carry over' of a menotactic angle can occur over the length of time from one foraging trip to another. On page 50 indirect evidence is presented .that i&yrmica can carry over a - menotactic orientation from one day to the' next. This result helps to confirm that this is possible. -83-
FIGURE 31.
EFFECT OF CHANGING LIGHT DIRECTION WHILST TRAIL LAYING ANT IS INSIDE NEST ON PATH TAKEN BY THAT ANT WHEN IT RE-EMERGES.
O = nest entrance. x = point where ant fed. Iv position where light direction changed. -84-
EVIDENCE FOR THE EXISTENCE OF THE TRAILS
The paths of ants returning from the sucrose solution 40 cm from the nest were plotted (Fig. 32 ) The sucrose was presented to ant foraging apart from others and removed as soon as it was left by an ant to avoid more than one ant laying a trail at one time. The paths of the first few ants to leave the nest entrance after the return of the fed ant were also plotted (Fig. 33 ). It can be seen that the path of the second group of ants largely coincided with that of the fed ant. Ants that crossed the path of the fed ant, without coming into contact with the ant, also followed its path (Fig. 31 ). This indicates that the coincidence of the paths is due to some factor left by th.e fed ant on the foraging arena surface, and not to any contact between the fed and recruited ants as is postulated by Von Frisch (19 67) in the honeybee, (but see Wells and Wenner 1973). Szlep and Jacobi (1967) stated that in Monomorium venustum Smith, Monomorium subopacum phoenicium Emery and two species of Tapinoma, during contact between a fed ant and other workers, an "oscillatory recruitment display" occurred, which they said by itself conveyed information on the food source to the unfed ants. 'However it seems that this behaviour is the same as that described on page $1 for Myrmica scabrinodis, where the fed ant tapped other workers vigorously with its antennae. This behaviour obviously need not impart any information necessary for the receiving ants to find the food, because ants not so treated can follow the trail. Wilson (1962) also found that the vibrating movements of fed Solenopsis in contact with other ants were not essential for trail following. As described on page ei , these movements: seem to serve an alerting function, as a means for getting the tapped ants moving. This behaviour used to be thought one of the most convincing examples of antennal language and was described by Goetsch (1934) from Myrmica laevinodis Nyl ( = rubra L. ? ) and Manica rubida (Latr.) From the observations on the behaviour of recruits following the path of fed a*ts that are behaving as described "on page 81 , there can be no doubt that Myrmica scabrinodis lays odour trails to recruit other workers to food finds. -85- FIGURE 32.
PATH OF TRAIL LAYING ANT FROM SUCROSE SOLUTION TO NEST ENTRANCE.
,
-r---
-.1
FIGURE 33.
PATH OF RECRUITS FROM NEST TO SUCROSE SOLUTION, AND OF AN ANT THAT CROSSED THE PATH OF THE TRAIL LAYER.
I
L.--
,...... a..-...
1 ...... 1 ,,,...,. - ...,, ,...... „. ' ....--..., i'
...... I I-
1 t ...... -. -.86-
STIMULI NECESSARY TO INITIATE TRAIL LAYING IN FORAGERS
It has been shown in many ant species that the main stimulus for trail laying is the finding of more food on a foraging trip that can be carried back to the nest in one journey. (Shorey (1973), Wilson (1962), Ayre (1968), Sudd (1960), Goetsch (1934) ). This appeared to be the case also in Myrmica scabrinodis, and the following experiments were per- formed to identify the sensory cues associated with the presence of more food than could be carried on one trip. 1. SUCROSE SOLUTION. The volume of sucrose solution drunk by foraging ants was measured. Ants were then fed on the average volume of sucrose ingested by foraging workers in the hope that some of these would prove to have been sated by the sucrose they had drunk, and would return to the nest, but not laying a trail as there was no excess sucrose present. Various stimuli could then be given to these ants to discover those that would elicit trail laying. The presence of trail laying could be easily observed by looking for the protruded sting. Ants were fed from on 0.5 M sucrose solution contained in 2 p.1 "Microcaps" with a twist of cotton wool inserted at one end to act as a wick. The position of the meniscus was observed before and after each feeding. The average volume taken at one feeding was 0.3625 Al (n = 20, Sd = 0.106p.1) which was equivalent to a movement of 5.8 mm in the meniscus. "Microcaps" were filled with 5.0mm of sucrose solution and 25 ants fed from these.
8 of the ants did not finish the 5 mm of solution, and of these 8, 7 took up a menotaxis and returned to the nest laying a trail, while 1 took up a menotaxis and returned to the nest but did not lay a trail. 10 of the ants fed from the tubes and finished the 5 mm of solution and then performed a circling behaviour as has been described in Section 7 . 6 of these resumed pottering when the circling was completed, and 4 took up a menotaxis and returned to the nest. None of these 10 ants laid a trail. The 7 remaining ants drank the sucrose solution till it was exhausted, and took up a menotaxis and returned to the nest without laying a trail and -87--
without any circling behaviour. These 7 ants were presumed to be those that had been sated by the sucrose just as it was exhausted. One of these 7 ants was presented with a filled "Microcap" of sucrose, and after examining it for a few seconds with its antennae, but probably without drinking from it, carried on towards the nest, but now laying a trail. A second of these ants was allowed to touch a drop of sucrose solution with its antennae, and this then carried on towards the nest, laying a trail, though it is certain it did not drink from the sucrose. From this it seemd that sugar stimulation of the antennal sense organs alone is sufficient to cause a satiated ant to initiate trail laying. It had already been shown that the antennal sense organs alone are sufficient to initiate circling in unfed or unsatiated ants (Section 7 ). Wilson (1962) found that Solenopsis saevissima would lay trails from sources of a sugar solution, even if these solutions were removed before the ant was allowed to feed (page 136). However (page 142) he says that trail laying was elicited in a certain percentage of the workers that successfully feed. He uses the idea that workers not allowed to feed will not lay trails as an important part of the mechanism of the "Mass Response" that controls the number of ants recruited to baits that, are already saturated. It seems that there is a contradiction here, and Myrmica scabrinodis has never been seen to lay a trail after it was allowed to touch sucrose solutions with its antennae but not to feed from them, an experiment tha. t was repeated many times (Section 7 ). It seems that Myrmica should have a much finer control of its "Mass Response" than Solenoosis_ if the observation, that that ant will lay trails after antennal stimulation only, is true. 2. PORTABLE PREY. The portable prey used in this set of experiments was an adult, apterous, Aphis fabae. In each case, 20 ants were given an aphid whilst they were on the outward menotactic orientation from the nest. After struggling for various lengths of time with the aphid, the ants took up a menotaxis and returned to the nest without laying a trail. Halfway to the nest, each ant was given some stimulus, and whether or not the ants subsequently laid a trail was observed. -88-
The first group of ants were presented with a second aphid held between the ant's antennae. 3 of these ants acted in an alarmed fashion, the remainder briefly examined the aphid with their antennae, and then left the aphid and carried on towards the nest. 8 of these ants laid a trail as they proceeded, 9 did not. The antennae of the next group were lightly touched with a clean needle. 12 carried on towards the nest but did not lay a trail, the 8 others reacted in an alarmed fashion. The antennae of the next group were touched with a needle smeared with the body juices of an aphid. 10 of these ants reacted in an alarmed fashion, 3 ants returned to the nest laying a trail, while 7 returned without so doing. The last group of ants were presented with a drop of 0.5 M sucrose solution.. They did not react to it at all, and none of these ants laid a trail.
From this it seems evident that the presence of more solid food as well as of more liquid food than the ants can carry can also be discovered by the antennal sense organs. The stimulus perceived is_presumably a chemical one as ants laid a trail after stimulation with a needle smeared in aphid blood, while none did so after stimulation with a clean needle. The reason for the ants given aphids not responding to the sucrose solution is unknown. Sucrose is responded to by ants not given aphids and by ants that have been fed on the sucrose. It may be that the smell of an aphid is very strong, and blocks the antennal sense organs that respond to sucrose or the aphid when held in the ant's mandibles may release some honeydew, which provides a stronger stimulus to the ants than the weak sucrose solution used inthe experiment. 3. LARGE PREY. 10 ants were each given a dead House Fly, Musca domestica. They were just able to drag this back to the nest, only one ant laid a trail from a fly. A behaviour pattern observed by McGregor (1948) in Myrmica ruginodis was seen frequently, the ants would leave the fly and walk from 3 to 5 cm from the fly towards the nest orienting menotactically, they would then return to the fly by reversing this menotactic orientation, and drag it a few centimetres further before leaving the fly again. -89-
10 ants were each given a dead house fly pinned to the arena surface. After pulling at it for several minutes, the 10 ants each left the flies, and returned to the nest laying a trail. The ants in this behaviour of leaving the fly differ from Monomorium pharaonis L, Sudd (1960), these ants did not leave a prey the cuticle of which the ants could not penetrate and thus from which they had not fed. However, they would leave the prey and return to the nest as soon as they were able to feed from it after the cuticle was cut, There is no evidence that the Myrmica presented with the flies had fed from them, the only behaviour seen was the ants pulling first at one portion of the pinned down fly, and then at another.
Thus trail laying in Myrmica scabrinodis is similar to that in many ants, in that trails are laid in response to immovable prey, or to the presence of more food than the ants can remove in one trip. This is the first occasion that it has been shown that antennal stimulation along is sufficient to cause trail laying in ants already carrying a burden, or those that have been satiated with sucrose. There is no evidence for or against a hypothesis that the response to flies is mediated through the antenna as well. Trail laying in Myrmica scabrinodis was also observed in the laboratory when ants were given a new nest. Trails were laid from the new nest to the old, and the ants subsequently moved to the new nest along the trail. Wilson (1962) reports that Solenopsis saevissima will lay trails to extensions to its foraging arena, no such behaviour was observed in Myrmica.
Heyde (1924) said that older Myrmica rubra workers were more likely to return to the nest laying a trail, without feeding from a food source than younger, inexperienced workers, which usually did feed first, No evidence was found for this in Myrmica scabrinodis; individuals all seemed to drink from a sucrose source before returning to the nest laying a trail. -90-
LIFE TIME OF TRIALS
To discover the length of time the trail laid by an individual ant was effective in guiding ants, the following experiment was performed. An ant was made to lay a trail over a piece of clean paper by feeding it with sucrose solution. This piece of paper was cut to produce a piece of paper 15 cm long and 7 cm wide on either side of the trail, that is 14 cm x 15 cm. A second ant was then made to lay a trail back to the nest from sucrose solution placed about 40 cm from the nest entrance on the foraging arena. This trail recruited a group of ants from the nest entrance that followed it towards the food. The piece of paper bearing the original trail was then placed across this trail leading from the food so that the trail on its surface was at right angles to the trail the recruits were following. The edge of this piece of paper was placed about 10 cm from the nest entrance. The ants following the trail from the nest entrance passed onto the paper placed in their path and lost their orientation at about the position where the trail crossed their path at right angles. If any ants followed this trail to either end of the paper, it was assumed the trail was still active. Table 10 gives the number of ants that followed the trail to either end, the number of ants that reached the trail but did not follow it, and the age of the trail at the time the ants reached it to the nearest minute. -91—
TABLE 10.
THE RESPONSE OF ANTS TO ODOUR TRAILS OF DIFFERENT AGES PLACED ACROSS
THEIR PATH.
Time since trail No. of ants No. not % laid. (minutes) following. following. following.
1 7 2 80 1 1 0 2 8 3 80 2 4 0 3 3 1 75 4 4 4 4 6 - 1 67 5 2 4 28 5 0 1 6 0 7 •0 0 0 8 0 • -92-
As can be seen the trail is effective on a paper surface for about 5 minutes, and then its activity rapidly declines, at 6 minutes no ants out of 7 respond to the trail, and at 10 minutes, no ants out of 8. Section 5 suggests that a long lasting component of the odour trail may be present as has been found in Pogonomyrmex badiuseHolldobler and Wilson (1970): found that the poison gland secretion of this ant was initially a stronger attractant for the ants than that of the Dufour's gland, but that the attraction faded more rapidly, so that after 20 minutes the secretion of the Dufour's gland was guiding the orientation of the ants. They suggested that the Dufour's gland secretion acted as an orientation cue for the ants whilst foraging, and Holldobler (1969) showed that the gland secretion would guide the ants to their nest if visual stimuli were removed. This is a situation similar to that described in Myrmica scabrinodis (Section 5 ) where the arena surface contains enough information to orient the outward paths of the ants the day after trails were laid. However as can be seen from Table 10 any such product of the recruiting trail in Myrmica does not seem to effect the orientation of ants that have just left the trail, Since a trail has been shown to last five minutes, the distance over which a trail can guide the ants can be calculated once the speed of the ant is known. The average of the speeds of a trail laying ant, and of a trail following ant is 41 cm min, which means that the maximum effective length of a trail is about 100 cm, which is 1 m. The' maximum length of effective trail observed in the foraging arena was 1.1 m, which is very similar to the calculated maximum possible length. The lengths of time that various odour trails of ants are effective in guiding the ants is given in Table 11 . The lengths of time given are usually from laboratory experiments and probably bear little relation to the lengths of time that the trails last in the field. As can be seen the length of life reported from odour trails vary considerably. An explanation for this variability in the time for which the odour trails of ants remain active is discussed below. It seems that odour trails of ants have two different functions. The first of these is as recruitment guides to foragers, these guide the ants -93-
TABLE 11. LIFE TIME OF THE ODOUR TRAILS OF VARIOUS ANT SPECIES.
SPECIES. SUBSTRATE. LIFETIME. REFERENCE.
TetramoriuM aaLaaDAZ non absorbent 168 hr. Blum and Ross ( F.) paper. ( 1965)
Solenopsis saevissima paper 20 min.
(Fr. Smith) glass 85-125 sec Wilson (1962)
Pogonomyrmex badius paper,Poison gland, up to 20 min Wilson and ( Latr.) paper, Dufour's 20 min plus Holldobler gland. (1970) Atta texana (Buckley) paper 5 months Moser and Blum (1963)
Monomorium phamnia 24 hr Elum(1966) L.
Monomorium minimum 2 • 5 hr Blum (1966) (Buckley)
Eciton spp forest floor 3 weeks Schneirla (1963)
Camponotus beebei 15 min. Wilson(1965) Wheeler.
Camponotus modoc paper 24 hr plus (Personal observatiOn.)
Lasius fuliginosus glass 1 hr Carthy (1951) Latr. -95- to sources of food which may be temporary, such as dead insect prey, or to new nest sites when a preferable one is found. Examples of these are the trails of Solenopsis saevissirna. (Wilson 1962), of Monomorium pharaonis (Sudd 1960), and of the poison gland secretion of Pogonomyrmex badius (Holldobler and Wilson 1970). In order to function efficiently for this purpose, a trail should be ephemeral, (Wilson 1962), otherwise ants would continue to be recruited to old food finds that have become exhausted, and the foraging area would rapidly become covered with trails from which the ants would have difficulty in distinguishing the most recent. The second function served by trails is as orientation cues for ants to enable them to move efficiently around their foraging area. Examples of these are the long lasting trails of Lasius fuliginosus (Carthy 1951 )
Camponotus modoc (personal observation), and Atta texana (Moser D)1( 381.um) These trails provide marked routes between nests of these ants, and between the nests and permanent sources of food, such as aphid colonies, or sections of the forests in which leaves are being cut in the case of Atta. To serve this function the trails should be long lasting, or else a short period when they are not in use would be enough to disrupt the ants foraging activities. The routes by which Monomorium pharaonic workers leave the nest, and return to it are probably formed by odour trails of this type, however the similar routes of Formica spp, have not been shown to be marked by odour Sudd (1967). The cue in Monomorium seems very similar to that in Pogonomyrmex badius where the secretion of the Dufour's gland is longer lasting and provides orienting cues after the cues from the poison gland secretion are no longer effective, The longer lasting cues deposited on the arena surface by Myrmica scabrinodis probably serve a similar function, to the routes of Monornerium especially as Sudd (1960) has shown that Myrmica rubra has similar routes to Monomorium. These routes in the different species of Myrmica probably only differ from each other in the extent of the guidance given to the ant. The trails of Army ants, subfamily Dorylinae, seem to provide orientation cues throughout the foraging trip (Schneirla 1933). The ants seem to deposit odour trails continuously as they advance into new territory. Thus the behaviour of these ants seems similar to those of Monomorium at the start of each foraging trip where the ants are confined to chemically -96- marked routes. The behaviour of the Army ants of always depositing an odour trail wherever they forage, may be linked with the absence of compound eyes in this subfamily, which would make visual navigation more difficult. However, it is likely that both following odour trails whilst foraging and the absence of eyes are adaptations for life underground. -97-
SECTION 10. RECRUITMENT BY ODOUR TRAILS
The odour trails of Myrmica scabrinodis have been shown to have a guiding effect on ants leaving the nest or on those that are already foraging. However they also have the effect of causing ants to leave the nest that would not otherwise have done so, a recruiting effect. This was demonstrated by counting the ants leaving the nest as they passed through a glass tube on their way to the foraging arena. The number of ants leaving the nest in unit time remains constant until food is introduced into the arena and the first fed ants return to the nest. As soon as they have arrived the number of ants leaving the nest per unit time increases by a factor of 6 (Fig 34 ) It might be thought that this is due to the odour trails guiding ants already moving inside the nest to the nest entrance, however observations indicate that the majority of the ants that leave the nest were not moving when the trail layer entered the nest and that they start to move when the trail passes close to them. A recruiting as well as a guiding function for the ecent trail has also been reported by Wilson (1962) in Solenopsis, where extracts of the Duiouris gland blown into a nest caused large numbers of workers to leave the nest. Eidmann (1927) shows that in Myrmica rubra the trail appears to give almost no guidance as to direction and to have only a recruiting function. When a second trail is laid to the nest a short time after a previous trail, the number of ants recruited by the second trail is much greater than by the first one, even if no food was found the first time (Table 12 ), the time interval between the two trails can be as much as 30 mins. A similar phenomenon occurs in Monomorium pharaonis Sudd (1960) but here greater numbers of the ants responded to a second trail if they found food on the first one, even after 50 minutes. In Myrmica, the trail alone seems to be enough to cause this effect, no more food need be found than that covering the trail laying ants to lay the trail back to the nest. FIGURE 34
RECORDS OF THE NUMBERS OF ANTS LEAVING A NEST iN HALF HOUR INTERVALS BEFORE AND AFTER A FLY, (LUCILIA) WAS PLACED IN THE ARENA AT 12 HR.
Nos. of ants per half hour. 3oo_
200- WO,
100_ ....••••••
r 12 Time (hr). -99-
TABLE12.
NUTHERS OF ANTS RESPONDING TO TRAILS WITH VARIOUS INTERVALS BETWEEN THEM.
Nos. of recruits Nos of recruits Interval between responding to responding to trails.• first trail. second trail. (minutes)
40 35 5 12 23 5
12 18 5 6 15 - 15 17 32 15 10 12 30
23 29 30 • 14 26 30
11 9 60 21 24 60
7 3 60 -100-
INTRINSIC ORIENTATION OF THE TRAILS
Ants that crossed the path of the trail laying ant turned in either direction along the trail, Out of 27 cases where foragers met a trail, 14 turned towards the nest, 9 away from the nest, and 4 did not follow the trail for 10 cm in either direction. 14 and 9 are not significantly different using the Binomial Test (p = 0.202), so there appears to be no bias in the direction taken by the ants. However in these conditions ants that crossed the trail might be equally likely to have been returning to the nest or to be continuing foraging. To remove this possibility ants as they met the trail were given an aphid, this had been shown to make the ants thus presented willing to enter the nest when they found its entrance. After being given aphids, 11 ants followed the trail away from the nest for more than 10 cm, 9 ants followed the trail towards the nest for more than 10 cm, 32 ants did not follow the trail at all, some of these perhaps because their struggles with the aphid had taken so long the trail had lost its effectiveness in guiding ants before the ants were ready to follow it. 11 and 9 are not significantly different using the Binomial Test (p = 0.412) so in these circumstances there appears to be no bias in the direction the ants take on a trail. It might be possible for ants once travelling on a trail to find from it some cue as to their direction of travel along it. To test this possibility the trail laying ant was made to lay a trail back to the nest over a piece of paper laid flat on the arena surface. The light at the end of the arena was then turned off so that the recruits could only orient by the trail and not by the light direction. This paper was turned round so that the ends of the trail on the paper and on the arena surface coincided, the recruits then passed over the paper with no signs of hesitation. When the paper was turned through a right angle, the ants would pass on to the paper for a short distance and then lose their orientation. Some of these ants then followed the section of trail now going at right angles to its former path. 5 ants were observed to go in the direction previously towards the food, and 7 ants in the direction previously towards the nest. 7 and 5 are not significantly different (p = 0.387) using the binomial test. -101-
Sudd ( 196?) states that in no ant has an intrinsic orientation in a trail been observed to convey information to an ant. Even in Lasius falia_1422fas where the trail is made up of shaped odour spots so that the trail can be seen to have an intrinsic orientation (Carthy 1950,1951) this information can apparently not be used by the ants. Sudd explains
MacGregor's (1948) results where ants found the position of the nest in the dark after running over one spot of scent as being due to gravity orientation. This seems unlikely as MacGregor's apparatus was presumably flat, and the effect was removed by swabbing the spot with ethanol. No observations were made on Myrmica scabrinodis that could confirm MacGregor's results with Myrmica ruginodis.
Since Sudd's(1967) book was published Holldobler and Wilson (1970) showed that in Pogonomyrmex spp.the secretion of the poison gland provides a recruitment pheromone while the secretion of the Dufour's gland provides longer lasting cues that are used for orientation by foraging ants. They have shown not that the ants can distinguish between the two, but merely that the Dufour's gland secretion retains its activity in guiding the ants for longer and that the ants thus orient by this after the poison gland secretions have evaporated. They provide no evidence that the Dufour's gland secretions shows the ants which way to return to the nest; for this they presumably rely on some other sensory modality.
In Holldobler's (1971) experiments visual cues for the homing ants were as far as possible removed. After rotation of the arena , ants went in the wrong direction for the nest entrance implying that the odour cues had been moved with the arena surface. This "wrong" orientation of the ants could be explained by an oriented odour trail from the centre of the arena to the nest at the edge, but it could also be due to an odour trail from the food in the centreof the arena to the nest, which the ants followed from one end to the other in the absence of visual cues. -102-
Vowles (1955) states that there is some intrinsic orientation in Eciton odour trails, he said that Schneirla believed this to be due to the greater concentration of the odour near the bivouac than far from it, which gradient the ants could discover after running a short distance along the trail. To date there is no confirmed case of an ant trail possessing an intrinsic orientation, however Wells and Buckley (1972) show that the snail Physa acuta can determine the polarity of trails left by other individuals or by itself. The trails last about 30 minutes. Cook et al. (1969) produce some evidence that the three common British species of Limpet (Patella sppo also follow trails to their "homes" on the rocks, and that these trails are probably polarised. -103-
ORIENTA TION OF ANTS FOLLOWING TRAILS
Since it had been shown that the trail itself gave no cues as to the direction to travel along it,o. series of experiments were carried out to identify the cues by which ants following the trail were orienting. In each
case an ant worker was fed with 0 0 5M sucrose solution contained in a glass tube 40cm from the nest entrance. The ant then laid a scent trail to the nest. Each trail would recruit from 10 to 25 other workers which followed the trail toward the food source. 10 EFFECT OF REMOVING A PORTION CF THE TRAIL It was arranged that the ant depositing the odour trail from the food source to the nest passed over a paper disc 20 cm in diameter placed flat on the foraging arena between the food and the nest. H this disc was removed and then replaced the recruited ants were still able to follow the trail (Fig ::'5 A). H the disc was removed leaving an area free of the trail pheromone, but wi~ no break in the arena surface over which the ants walked, the recruited ants lost their orientation after pas sing about 10 cm into the trail-free area (Fig 35 B). 2. EFFECT ON RECRUITS OF BENDS IN A SCENT TRAIL When a scent trail had a sharp bend in it, the recruits moving along the trail walked straight on at the bend, thus leaving the trail /,(Fig o 36 ). After continuing for about 10 cm they lost their orientation and pottered until in some cases the trail was refound. H the trail was reached again it was sometimes once more followed, but lost again at a second bend. This indicates that the loss of the trail at a bend was not due to the weakening of the trail as the part laid earlier evaporates, for it is followed again further on where it must be even weaker. However, the trail was not lost at bends within a few cm of the nest, or of where recruits first met it (Fig. 36 ). 3. EFFECT OF REMOVING THE FOOD BEFORE THE RECRUITS REACH IT. When the recruits reached the end of a trail where there was a supply of sucrose solution they drank from it. H the sucrose was removed before the recruits reached it they carried on in a straight line continuous with the end of the trail for about 10 cm before losing their orientation (Fig. 37 ). I . -104-
FIGURE 35.
EFFECT OF REI':GVING A PGRTION OF THE TRAIL ON RECRUITS FOLL0.11I\G
THE TRAlL. A, THAlL COI1PLETE, B, PORTIOI~ RENOVED.
=f 1- I ~-I ! -,--1-----t----l-- i------t A. --+-----~------i----r-- -L- ---j +-+-r---- r-:-----~---· .------~- ~--:::~-:;~I _·-t ti-r--- t -·_- .L- ~ r------1 .--+·---t~--t---t----f ! I Ii: ..-...... -_--'-1 i _ i__ J. .. _. __L~_. ___ L-
o = nest entrance. ,_ --- = path of trail layer. ____ = path of recruits.
! I I I .L B. +--+-·----1------~-- --_ I
I ---r-I--"! --- ~T .-. .---. - !. -_. ;:·.... ,---·--r
I -+- I -1·-·----- +---'---1---- i --I r- -t--r--J '--+---l---- , ~-- ,I I~, I /' ,;: I ,I ______--'- I __----' ,I_____ 1_---' _-__:-----1'._ -' i
-106-
These experiments indicated that ants on a scent trail had some other straightening influence than the scent trail, since they carried on going straight for some distance after they had lost the trail. Tests for menotaxis in the ants were carried out as described in the methods section (page ), on the ants on the trail. When the light direction was changed through 180°, ants on the trail reversed their direction of travel along the trail within a few seconds (Fig. 3 8A). If the angle of change of the light direction was nearer to 90°, the ants left the trail when the change occurred and kept walking at the same angle to the light source (Fig. 3813). This indicated that the ants on the trail had taken a menotaxis holding them in the same direction as the trail. Ants in the first few cm of travel along a trail showed no effect when the light direction was changed, indicating that the menotaxis is not acquired immediately the trail was followed. This explains why the effect of bends on recruits in a trail is different in the first few cm of travel along a trail from what it is later on. The change to a menotaxis can also be observed by a change in the ants' manner of walking. In the first few cm along a trail the ants are more hesitant, walking slower and on a more crooked course than they do later on. In 38 out of the 44 cases observed (Fig. 39) the menotaxis was lost between 7 and 14 cm from the point where the an'ts were no longer on the trail. Sudd (1967) suggests that once a Pheidole crassinoda Emery recruit has"picked up the line of a trail it can continue on that line, relying on its own light compass, and only checking with the trail at intervals." Presumably,he means by this that the ant only needs intermittent stimulation from a trail in order to maintain its light compass orientation. If this is the case in My-rmica the intervals between which the ant responds to the trail must be very short compared with the response time between this checking and the time the menotaxis is lost. This can be shown by distribution of the points at which the menotaxis is lost. Suppose the intervals between the times when the ant responded to the trail were long, and that the ants lost their menotaxis immediately the -107-
r"5 Flr-URE .D <3
EFFECT OF CHANGING THE LIGHT DIRECT,ON THROUGH 180° (A) AND 90° (B) ON ANTS FOLLOWING A TRAIL.
,
A. ... At,-. --
....r.--...... • ..01
o = nest entrance. = path of trail layer path of recruit = position where light direction changed,.
. .--.■ ••
B.
-II -108- FIGURE 351 . POSITIONS AT WHICH ANTS LOST THEIR MENOTAXIS AFTER LOSING TRAIL.
IO
9
7 Numbers of ants losing menotaxis at given distancs..
4 -
3 2- 1-
0 0 10 15 20 Distance walked by ant till menotaxis lost ( cm ) -109- trail was not present when they checked for it, then there would be a continuous distribution of distances beyond the end of the trail at which the ants lost their menotaxis, (Fig. 11-0). If there was a delay before the ants responded to the loss of the trail by losing their menotaxis, this distribution of positions at which the ants lost their menotaxis would be shifted away from the end of the trail (Fig. 41 ). Any variation in the response time of individual ants between checking and finding the trail was missing, and responding to this loss by starting pottering would result in the distribution of positions being spread out. In fact (Fig. 39 ) the cluster of points at which the ants lose their menotaxis is only about the same width as the gap separating the cluster from the end of the trail. This means that the response time after the ants notice the loss of the trail before losing their menotaxis must be about the same as the time between which the ants are checking for the presence or absence of the trail or it must be longer than the checking time. For the first to be true the response time of individual ants to the loss of the trail must all be of the same length. This seems most unlikely, so the best hypothesis is that the checking interval with the trail is short and that the ants response time to the loss of the trail is long. There is in fact no need to postulate that there is any checking interval at which the ants respond to the trail at all:The distribution of points at which the ants lose their menotaxis in Fig. 39 can be explained entirely by the ants having a lag time before they respond to the loss of the trail by losing their menotaxis. The ants are probably continuously responsive tothe presence or absence of a trail, checking continuously for its presence, or responding to its absence having adapted to its presence.
FIGURE 4 3 . HYPOTHETICAL DISTRIBUTION OF POSITIONS AT WHICH ANTS WOULD LOSE THEIR MENOTAXIS ON LOSS OF A TRAIL, IF THEY WERE CHECKING FOR THE PRESENCE OF- A TRAILEVERY 15 CM
Axes of figure as in Figure 39.
FIGURE li 1 • HYPOTHETICAL DISTRIBUTION OF POSITIONS AT WHICH ANTS WOULD LOSE THEIR MENOTAXIS ON LOSS OF A TRAIL, IF THEY WERE CHECKING FOR THE PRESENCE OF A TRAIL EVERY 15 CM, AND HAD A LAG DISTANCE OF 5 CM BEFORE RESPONDING TO THE LOSS OF THE TRAIL
Axes of 7- figure as in 6- Figure 3$7. 5_
4-
3
2
1_
0 10 151 20 FACTORS AFFECTING THE MENOTAXIS IN TRAIL FOLLOWING ANTS
In order to investigate the factors causing the setting up of the menotaxis in trail following ants it was necessary to design an experiment where as many as possible of the conditions that might affect this could be controlled.
APPARATUS (Fig. 42 )
The apparatus consisted of a 'T' shaped bridge -built of card with one arm of the cross bar extendable to different lengths. The structure was supported on corks standing in 10 cm petri dishes with fluon coated sides to prevent the escape of the ants. Ants could climb on to the structure midway along the extendable arm from a plastic tube with a swing door. This tube was connected to their nest. The whole structure was mounted on a heavy baseboard to prevent vibrations alarming the ants and was housed inside muslin curtains to limit the number of visual cues available to the ants.
METHODS
The structure was set up so that the distan ce from the nest entrance to the T junction was fixed at 20 cm. An ant was fed in petri dish tA' with sucrose and it then laid a trail along the bridge back to the nest. Any occasion when the trail laying ant did not make a smooth turn at the junction on the bridge was abandoned and a fresh bridge substituted. Once the ant entered the next entrance this was shut by means of the door, and the bridge was then shortened to a predetermined length. The ants were released from the nest entrance at a predetermined time such that the length of time from the trail laying ant leaving the T junction to the first recruits reaching the junction could be kept constant in spite of the distance varying, or the time could be varied at a set distance. In this way a group of ants following a scent trail could be presented with a right angle bend in the trail either at different distances from the start of the trail, but with the trail having lasted the same time and so presumably being of the same strength, or with the bend being at the same Revolving door at nest entrance
Tube to nest. 111111t 1077///
Extendable portion 20 cni of bridge.
Cork stand.
'Fluon Petri dish 'A'. on inside wall of petri dish. -113- distance from the nest but with different strength trails. If the ants were menotactically orienting they would be expected to go straight on at the junction, while if they had not yet picked up a menotaxis, or had lost it they would follow the trail round the bend. Sudd (1960), reported that Monomorium pharaonis following trails were more likely at a split in a trail to follow the ant in front than they would have been had their choice of route at a split been unaffected by the choice of the ant they were following. No evidence of a similar phenomenon could be found in Myrmica scabrinodis and the results of the following experiments are almost as significant statistically if only the choice of the first ant in each series of recruits is counted.. It was found with clean bridges when no trail was present that 26% of the ants turned the right angle bend when the bend was 18 cm from the nest entrance (N = 29, 23 straight, 6 turned). 28% of the ants turned the right angle bend when the bend was 6 cm from the nest entrance (N = 55, 43 straight, 12 turned). These results are not significantly different using the Chi-Squared Test (P = 0.7 -0.8) so there is no evidence of any straightening effect being produced in the ants by the act of being forced to walk in a straight line along the bridge. However it might be that at 6 cm the bridge has already produced a straightening effect in the ants. That this is probably not so is suggested by the fact that on clean bridges no menotaxis could be demonstrated in the ants at any distance from the start of the bridge; and, on trails, no menotaxis can be demonstrated until the ants have followed them for more than 8 cm.
EXPERIMENT TO DETERMINE THE EFFECTS OF DIFFERENT TRAIL STRENGTHS ON THE MENOTAXIS OF ANTS AT DIFFERENT DISTANCES FROM THE START OF THE TRAIL.
The apparatus was set up as described above, and after a trail was laid the bridge length was shortened to 11 cm. This was a length at which it had been noted that the majority of the ants following a trail had acquired a menotaxis. The ants were released from the nest entrance at times on different runs of 0 or 180 seconds after the trail laying ant had entered the nest -114° entrance. No two runs were performed on the same day. The times taken for the recruits to reach the junction after the ant laying the trail had passed, and the numbers turning the bend or carrying straight on are given in Table 13 The experiment was repeated but the bridge length was altered to 6 cm, a distance at which all the ants are orienting by the trail. The results as above are given in Table 13
As can be seen from Table 13 , the majority of the ants go straight at the junction when this is 11 cm from the start of the trail (N = 21, 20 straight, 1 turning). However, 26% of the ants would be expected to turn the corner if there was no trail, that is 5.5 ants out of 21. 20 - 1 is significantly different from 15.5 - 5.5 using the Chi Squared Test. (p = 0.05 - 0.02). So the bridge plus the trail causes more straightening in the ants at 11 cm, even though the trail is bent, than does the bridge without any scent trail. Any effect of increasing age of the trail is not very marked at 11 cm from the start of the trail. When the trail is more than 3 minutes old, 1 ant turns and 8 go straight, at less than 3 minutes, 0 ants turn and 13 go straight. These sets of figures cannot be compared using a Chi Squared Test, however, using Fisher Exact Probability Test, it can be shown that the difference between the two populations are not significant (p = 0.41)
At 6 cm from the start of the trail the majority of the ants follow the trail at the junction (N = 44, 5 straight, 39 turning). 26% of the ants would be expected to turn the corner if there was no trail, that is 11.5 ants out of 44. 39 - 5 is significantly different from 11.5 - 32.5 using the Chi Squared Test (p = 0.001). This indicates that at 6 cm from the start of a trail the ants are orienting by the trail, and also that the meno- taxis is acquired between 6 and 11 cm from the start of the trail. The effect of increasing the age of the trail is not very marked at 6 cm from the start of the trail, even though with 3 minutes delay, the trail is approaching the time at which it is no longer effective in guiding the ants (see page 90 ). It seems that response to the trail is all or none. The period of time over which they cease to respond to a trail is relatively short compared with the length of life of the trail. -115-
TABLE 13.
DIRECTION TAKEN BY ANTS AT RIGHT ANGLE BEND IN ODOUR TRAIL AT DIFFERENT AGES OF TRAIL.
rt
DISTANCE DELAY TIME TO TIME TO NO. NO. ( CM ) (, SEC ) FIRST RECRUIT LAST RECRUIT TURNING STRAIGHT. ( MIN. ) (MIN.)
11 180 4.50 5030 1 5 11 180 3.40 4.10 0 3 11 0 1.10 1./.0 0 3 11 0 1.40 0 1 11 0 1.50 2.20 0 4 li. 0 1.20 3.30 0 5
6 180 3.50 4.10 3 0 . 6 30 1.20 1.20 6 1 6 0 0.15 0.30 9 0 6 0 0.20 0.46 2 2 6 0 0.20 1.05 7 2 6 0 0.35 0.55 4 0 6 0 0.25 0.50 8 2 -116-
That going straight at the junction is an indication of menotaxis by the ants was proved by testing for a menotaxis at 11 cm from the start of the bridge, by reversing the light direction. When this was done ants at this distance from the start of the bridge reversed their direction of travel along the bridge. This effect was not seen with ants at 6 cm from the start of the bridge.
Thus the switch from scent orientation to a menotaxis on a scent trail depends on the distance walked by the ants along a trail, or the time they have walked along a trail, but not on the strength of the trail, or on the straightening effect produced by the trail in the path of the ant, since ants walked over a narrow bridge and which have thus had their path straightened show no menotaxis (Page 113 ).
The walking speeds of ants on a trail vary considerably, from 0.25 cm sed'to 1.0 cm sec,' so it is possible to find whether the distance walked or the time spent walking by an ant on a trail is the factor which controls the switch to a menotaxis. This can be done by finding whether there is a better correlation between the direction ants take at the right angle bend in the odour trail, which is an indication of the 'presence or absence of a menotaxis, and the distance the ants have walked along the trail, or the time they have spent walking. To discover whether the distance an ant had walked along a trail, or the time that it took to walk a certain distance was the factor most influencing the position at which it took up a menotaxis when following a scent trail, 8 groups of ants were observed in their passage along a trail to a right angle bend in the trail at three different distances from the nest entrance. The number of ants in each group that turned the corner was counted, and the time that the first and last ant in each group took to reach the corner was measured, the direction taken by these two ants was noted. As it had been shown that the length of time since a scent trail was laid had little influence on the taking up of a menotaxis in ants following the trail, no attempt was made to ensure that the trails were of the same age when the ants reached the corner. The trail was obtained as described on page iti by feeding an ant in petri dish 'A' and letting it walk back to the nest over the bridge. When the trail laying ant did not make a smooth turn -117- at the junction on the bridge the bridge was discarded and a clean one used for the next replicate. When the trail laying ant reached the nest a group of recruited ants were allowed out, and then the nest entrance was shut by the rotating door. The lengths of time that the first and last ants of the group took to reach the junction were measured using a stop watch, and the directions taken by all the ants in the group were noted. The first ant to reach the corner always took less time to reach the corner than did the last ant because the bridge was wide enough for the ants to overtake one another and thus the ants that walked the fastest reached the corner first. Table 1 4 gives the numbers of each group turning the corner and the time taken for the first and last ants of that group to reach the corner. In Figure 4 3 , the average of the time taken by the first and last ants in each group to reach the corner is plotted against the percentage of the ants in that group turning the corner. The average of the times taken by the first and last ants to reach the corner is felt to be a fair indication of the speed of the group since as explained above, the ants sort themselves out along the bridge by their speed of movement, thus the first and last ants in a group were usually the fastest and slowest respectively. As can be seen from Figure 43 the points indicating the percentage of the ants in a group turning the corner are clustered into distinct groups at each distance. However there is little difference in the time taken by the groups of ants to reach 6 cm from the start of the bridge and 11 cm from the start of the bridge, in fact many of the groups overlap in time. The average time taken by some of the groups of ants to walk 11 cm was less than the time taken by some of the groups of ants to walk 6 cm. The percentage of each of these groups turning the corner is however quite distinct. At least 50% of each group of ants turn the corner at 6 cm, while at most 14% of the ants do so at 11 cm from the start of the trail but no such correlation can be found with the time spent walking. As the lack of turning the corner has been shown to indicate that an ant has a menotaxis, this result means that the initiation of a menotaxis which occurs between 6 and 11 cm from the start of the trail depends on the distance an ant has walked, rather than on the time it took to walk that distance. -118-
TABLE 1I+ .
THE TIMES TAKEN BY THE FIRST AND LAST ANTS OF A GROUP TO REACH A RIGHT ANGLE BEND IN AN ODOUR TRAIL, AND THE DIRECTIONS TAKEN AT THE BEND By THE ANTS IN THE GROUP.
Distance t.) Time of Time of No. No. % corner (cm) first ant last ant turning straight turning (sec) ( sec ) •
6 7 21 9 0 100 6 8 15 3 0 100 6 15 22 4 0 100 6 12 27 4 1 80 6 18 16 7 2 78 6 25 25 3 1 75 6 11 18 3 3 50 6 25 19 4 4 50
11 11 29 0 3 0 11 11 22 0 2 0 11 15 35 1 9 10 11 18 30 , 0 6 0 11 22 22 1 6 14 11 23 32 0 5 0 11 25 28 0 3 0 11 36 33 0 4 0
18 30 0 1 18 35 51 0 2 0 18 38 58 0 5 0 18 50 •63 0 3 (:) 18 55 59 1 3 25 18 41 52 1 2 33 18 38 49 1 4 30 18 28 53 1 2 33 -U9-
FIGURE 43.
THE PERCENTAGE OF EACH GROUP OF ANTS TURNING THE RIGHT ANGLE
BEND IN AN ODOUR TRAIL, PLOTTED AGAINST THE AVERAGE OF THE TIMES
TAKEN BY THE FIRST AND LAST ANTS IN THE GROUP TO REACH THE BEND.
% of each group turning the bend. 46 0
0 0
V
0 10 20 30 40. 50 60
Average of the times taken by the first and last ants of the group to reach the bend. ( sec )
E right angle bend at 6 cm from nest. ✓right angle bend at 11 cm from nest. O right angle bend at 18 cm from nest. -320-
Table 15 gives the results on the directions taken by the first and last ants in each group to reach the corner in the trail, and the directions taken by these ants.
As can be seen from the table the direction taken by an ant at the corner bears no relation to the time spent walking by that ant to the corner. The average time taken by the last ants of a group to reach the corner when this was 6 cm from the nest entrance (21 seconds) was longer than the average time taken to reach the corner by the fastest ants when this was 11 cm from the nest entrance, 19 seconds. At six centimetres however, 6 ants out of 8 turned the corner and thus were orienting by the trail whereas at 11 cm no ants out of 8 turned the corner, the ants had taken up a menotaxis. It was hoped to further test the hypothesis that it is the distance an ant has walked along a trail rather than the time taken to walk that distance that is the factor that controls the position at which a menotaxis is taken up by ants following the trail, by holding ants still for various lengths of time as they followed the trail before they had taken up a menotaxis, and then to observe the effect this had on the position at which the ants took up a menotaxis. If they took up a menotaxis nearer to the start of the bridge after a period of imprisonment in contact with the trail and with the orienting light visible to them, this would be evidence that the time an ant had been in contact with a trail was important in fixing the position at which an ant took up a menotaxis. This experiment could not be carried out, as holding an ant still invariably alarmed it, so that it would not follow the trail when it was released.
The finding that the distance an ant has walked along a straight trail, not the time for which it has been walking along that trail is the factor that controls the moment of taking up a menotaxis in the trail following ants has bearing on the phenomenon known by various names among which are "Correcting Behaviour" (Dingle 1961), and "Delayed Compensatory Response" (Dingle 1965), which has been observed in many animals including ants (Schneirla 1929) (Dingle 1962). This behaviour is the tendency of the animals after being forced to make a turn in a certain direction, (say left), to make a turn in the opposite direction (right) at the first opportunity. This was -121-
TABLE 15.
THZ, TIMES TAKEN BY THE FIRST AND LAST ANTS OF A GROUP TO REACH A RIGHT
ANTE BEND IN AN ODOUR TRAIL, AND THE DIRECTIONS TAKEN BY THESE ANTS AT
THE BEND.
Distance to Direction Time of Direction Time of right angle taken by first ant second ant second ant bend,(cm). first ant ( sec ) (sec )
6 T 7 T 21 6 T 8 T 15 6 T 15 T 22 6 T 12 T 27 6 S 18 T 20 6 T 25 S 25 6 T 11 S 18 6 T 25 T 19 15.1 20-9 n s 11 S 29 11 S 11 S 22 11 S 15 S 35 11 s 18 s 22 11 S 22 S 30 11 s 23 S 32 ii. S 25 S - - ' 28 11 S 36 S 33 18-8 28-8 18 S 30 18 S 35 S 51 18 S 38 S 58 18 S 50 S 63 18 T 55 S 59 18 S 41 - S 52 le T 38 S 49 . 18 S 28 T 53 39.4 55 -122- explained by Schneirla (1929) by a phenomenon of "Centrifugal Swing"„ in which there were two components, the first being the effect of momentum, which carried an ant making a forced right angle turn against the far wall of the turn, and the second being a thigmotactic response in which the ant then followed this wall at a subsequent choice point round the corner, thus turning against the direction of the preceding forced turn. This explanation of "correcting behaviour" has been shown to,be false for many animals (Dingle 1961) (Grosslight and Harrison 1961) (Wilson and Hoy 1968). and has not been rigorously demonstrated in any species, however it is still quoted in many texts as the mechanism for "correcting behaviour" in ants i.e. Wilson (1971). "Correcting behaviour" has also been explained by Hull's (1943) concept of "Reactive Inhibition". This is a negative motivational tendency which declines with time not to repeat an activity. That is, if an animal has just made a right turn, it would not repeat that right turn immediately, and the tendency not to repeat this right turn would decline with time. Dingle showed that this explanation could not account for the behaviour observed in Boxelder bugs, Leptocoris trivittatus (Say) (Herniptera Coreidae) (Dingle 1964) or in Mealworm larvae, Tenebrio molitor (Coleoptera Tenebrionidae) (Dingle 1964b) for three reasons. First the tendency of these insects to make a "correcting turn" depended on the distance the insect was made to walk in a straight line before the forced turn. If "reactive inhibition" was controlling the tendency to make "correcting turns", events prior to the forced turn should have no effect on the subsequent turning responses. These turning responses were dependent on the distance the animal had walked, not on the time spent walking before the turn. Second that as reactive inhibition decays with time, the tendency of the insect to make a "correcting turn" should decline with time, but Dingle had shown that the tendency to make "correcting turns" declined with the distance, not with the time spent walking between the forced turn and the choice point. Thirdly, that when the insects were forced to make a right turn, the action not to be repeated would be a right turn, but at a choice the animals would make a "correcting turn" rather than carrying straight on thus not simply not repeating the forced turn but actively making the opposite turn. -123
Wilson and Hoy (1968) showed that the "correcting behaviour" in Oncopeltus fasciatus was only shown in the light, and was probably identical with the tOntomotor reactions,. This is probably also the case in Leptocorus, since Dingle showed this bug "corrected" less well in red light than it did in day-light. It seems that Leptocoris, when walked along a straight path, acquires an optomotor straightening tendency. This acquisition seems to depend on the distance walked by the bugs along the path, and not on the time spent walking along the path. This seems to be a very similar mechanism to that of Myrmica which take up a menotaxis after walking for a certain distance along a straight odour trail. Wigglesworth (1939) considers that the optomotor reaction and menotaxis are two aspects of the same phenomenon. The only difference between the two being that the optomotor reaction is a response to movements of the whole visual field, while a menotaxis is a response to the movements of point objects in the visual field. However Jander (1957) has shown that Wood Ants Formica rufa can orient simultaneously to two objects in the visual field, and in the field orient.61 many landmarks simultaneously, which !implies that the distinction between orienting to disturbances in the whole visual field, and just one point in the field, is not valid, as ants can be observed to take up menotaxes to one object or many. A further similarity between the acquisition of an optomotor reaction in Leptocoris and a menotaxis in Myrmica is that the optomotor reaction in Leptocoris appears to be acquired suddenly between 10 and 15 cm from the start of the straight path. However as Dingle says, the standard deviations for the observations on which this hypothesis of a sudden acquisition of a straightening tendency is based are "unfortunately large", and the hypothesis that the optomotor reaction is gradually acquired, cannot be ruled out.
It seems probable that the same mechanism is controlling the position at which ants take up the menotaxis when following a trail, as is controlling the position at which the menotaxis is lost when the trail is lost. Both of these occur in about the same distance. Unfortunately the times that ants -124- took to lose their menotaxis and start pottering or leaving a trail, were not measured so it is not known whether it is the distance the ants have walked after leaving the trail, or the time spent walking, which determines the "lag" time in losing the menotaxis. If it is the distance that is important this would be another similarity with the "correcting behaviour'? of Leptocoris where the decay of the tendency to make a correcting turn has been shown to depend on the distance walked. That is the optomotor reaction leading to straightening is lost at a certain distance from the forced turn, not at a certain time after the turn was made. This behaviour of Myrmica in measuring the distance walked, rather than the length of time spent walking might be thought ,to be evidence for a kinaesthetic sense. In this case there can be no suggestion that it is mediated by responses to odours in the substrate as was the hypothesis in
Section Pj . However another hypothesis is possible, It might be controlled by a time sense, if this time sense was liked to the physiology of the ant in such a way that the lengths of time measured are exactly correlated with the walking speed of the ant. Thus if the time measuring device of one ant was slower than that of a second ant, it would take up a menotaxis later in time than the second ant, but it would only have walked the same distance before the menotaxis was taken up since it was walking slower than the ant with the faster time device. Such a time measuring device that measured different times as the physiology of an animal varied has been found by Fritsch (1959) in Daphnia magna Straus (Crustacea Cladocera), These animals live for a constant number of heart beats, even though the rate of heart beating varies considerably with temperature. However Dingle's (1964) experiment with Leptocoris shows that if there is such a time measuring device present in this insect it functions only when the insect is walking, and not when held stationary. Since this would seem to have to be a very subtle device to take account of all these variables, the hypothesis of a kinaesthetic sense measuring the distance an ant has walked is much simpler, and therefore preferable until one or the other hyp ()thesis can be rigorously tested. -125-
The advantage to an ant in taking up a menotaxis when its path is straightened by a trail is not very clear. When menotaxis is possible, all ants laying trails orient by a menotaxis. Thus the trails laid consist of straight lines, however trail laying ants frequently return to the nest as described on page 75 in a series of menotactically controlled straight legs. When this is the case, recruits are very seldom able to follow a trail back to its origin, as each leg is long enough to enable them to take up a menotaxis, and thus when the trail bends, they lose it. However the greatest distance trails are effective in guiding the ants on the arena was about one metre. This is because a trail only was effective in guiding the ants for five minutes, and the average walking speed of the ants was 40 cm a minute. Thus the effective length of a trail is the distance an ant can walk in 2.5 minutes which is 100 cm. The length of the path of an ant returning to the nest in a series of straight legs is often considerably more than one metre so the ants recruited by a trail of this form would never reach the end of it anyway. In this case a trail probably just serves to recruit ants into the foraging territory after one ant has successfully found food. Eidmann (1927) who found the Myrmica rubra trails gave pra.ctibally no guidance to direction had probably observed a case like this. in If an ant returns to the neste. single good orientation laying a trail, the menotaxis taken up by the ants near the start of the trail serves to take the ants along the length of the trail, and to carry on past its apparent end where it may have evaporated still keeping their good orientation. The menotaxis,up by the ants leaving along a trail may have the function of keeping the ants going in the correct direction along the trail, since it has been shown (page too), that the trail has no intrinsic orientation. However if this is the case, it is peculiar that the menotaxis becomes dominant over the scent orientation, since this means that the trail is lost at bends. It might be thought that the menotaxis taken up, bythe ants is entirely a product of a laboratory situation, where the ants have too few cues to orient by, however Vowles (1951 ) has shown that Myrmica ruginodis in the field do orient by a light compass mechanism, and field observations at Silwood Park indicate that Myrmica scabrinodis following trails in the field also -126- was orienting by the light direction.
it has long been known that ants can simultaneously use several
different stimuli by which to orient. There are many accounts of ants
orienting by light or gravity while following an odour trail.
Lubbock, (1884) found that Lasius niga- carrying larvae to their nest
along an odour trail were orienting by the light of candles beside the
table they were crossing.
Santschi (1911) found that Messor could only make a 'correct' choice of direction on a trail if they were placed on it near the place where they
were captured. This suggeststhat these ants were using nearby landmarks
as orienting cues,
Goetsch (1934) showed that creigast scutellaris 01. workers orient
to gravity when on a trail running vertically up a wall. If the trail was
turned through more than 40° the ants became disoriented, if more than
70° they left the trail and ran straight up the wall. However this last effect was not observed with eats unfamiliar with the trail, or with fresh trails. This implied that some learning process had taken place in the ants,
perhaps similar to that found by Jander(1957) in Wood ants (Page 71 ).
Wilson (1962.) stated that Solenouls saevissima when they find an odour trail whilst foraging tend to walk outward along it, even though as he showed the odour trails themselves have no intrinsic orientation. The ants must therefore have been orienting by some cue other than the trail, and
Wilson implied that this was the light.
Marak and Wolken (1965) stated that Soleno sis saevissima workers after being trained to use a light as an orienting cue would reverse their direction of travel along a trail when the light was moved to the opposite side of the trail. This indicated that this cklit has a light orientation wheh it followed the trail,
Holldobler (1971) stated that when pogonomyrmex badius (Latr.) workers were transferred to the trail of a neighbouring nest they continued to run in the same direction with respect to the sun. In a foraging arena _127_
when the visual cues were removed the ants would follow the trails to the nest, however when visual cues were present, the ants homed with only slightly less accuracy whem the trails were turned away from the nest entrance than when they led to the entrance. This implied that ants on a trail are aso orienting by the light direction, and that this is dominant over the scent orientation in many circumstances.
This behaviour of Pogonomyrmex is very similar to that of Myrmica in that on trails the ant appears to hold a menotactic orientation, while its orientation when returning to the nest appears to be largely controlled by menotactic orientations, the angle of which can be influenced by odour (page IS ). 128-
SECTION 11. SUNNARY.
The times taken by ants to complete unsuccessful foraging journeys were found. It. was shown that the distribution of these times could only be explained if the ants can orient towards the nest entrance,so that it is found more readily than by chance, from at least 20cm. No such orientation could be demonstrated in unfed ants, but . fed ants it was shown could orient towards the nest entrance from more. than 20 cm by the use of odour cues on the arena surface, no such guidance occurring on a clean surface. it is possible that unfed ants can also use these cues.
Odour cues on the arena surface, possibly identical with those above maintain a menotaxis in ants leaving the nest entrance. The angle of the orientation of these ants to the light was shown to depend on an interaction between an unknown cue, prob ably in the nest entrance; odour cues on the arena surface near the nest entrance; and a carried over menotactic orientation. The odour cues on the arena surface may be identical to those maintaining a menotaxis in the ants, and to those guiding the ants to the nest entrance.
When food is found whilst foraging, the ants can orient towards it by a chemoklinotactic or tropotactic mechanism. if there is no odour gradient leading to the food, and if the ants are nor satiated, a klinokinetic circling behaviour is performed. This seems to be an all or none response, no correlation could be found between any component of this behaviour, and the intensity of the stimulus producing the circling behaviour.
This klinokinesis , and that produced by the loss. of menotaxis in areas without odour, are discussed in relation to the various theories of klinokinetic mechanisms.
The finding of food causes the ants to become ready to enter the nest.
If the food is found on the outward menotaxis from the nest entrance, or shortly after this menotaxis is lost, the sign of the menotaxis is reversed, and the -129-
ants thus walk back towards the nest. The distance walked before the
angle of the menotaxis is again changed is related to the distance walked
from the nest to the food.
if the food is found after the ants have ben pottering for some time,
a menotaxis is induced. The angle of this orientation to the light is
changed every few centimetres. The orientation of the ant at the start
of each new period with a menotaxis is in general towards the nest, and this
orientation is produced by odour cues on the arena surface.
If more food is found than can be carried to the nest in one journey this fact is sensed by the antennal sense organs, and the ants return to the nest laying a trail. These trails are active for about 5 minuteson
a paper substrate; have no intrinsic orientation;and serve to recruit ants on to the foraging arena aswell as to guide them to the food.
Ants following the trail take up a menotaxis along the line of the trail if it takes them in a straight line for more than about 8cm.
No such menotaxis is produced in ants whose path is straightened by other means such as by making them walk over narrow bridges.
The initiation of the menotaxis in ants following the trail depends on the distance for which the ants have been following the trail, and not on the strength of the trail, or on the time for which the ants have been follow following the trail. This result is similar to those found on the initiation of optomotor reactions in railroaded bugs.
The loss of the menotaxis on loss of a trail occurs some way from the trail, this can be explained entirely by the lag time in the ants before they respond to the loss of a trail by losing their menotaxis, and there is no need to postulate that the ants have checking intervals between which they are unresponsive to the trail.
Kenotaxis can be initiated in Myrmica by the finding of food; by the following of a trail; and by alarm and it can be maintained by odour cues from the arena surface. The angle of the menotaxis can be set -130-
by carry over from previous foraging trips; by the orientation of a trail; or by other cues from the arena surface.
Pottering is performed when no light orientation is possible, that is in the dark; after loss of a menotaxis through various causes, such as after klinokinetic searching behaviour; or by many ants from the moment the nest is left. -1.31-
AC:KNOW-LEDGE/41.MS
I should like to express my thanks to Professor T.R.E. Southwood for allowing me facilities in his department, and also to Professor J. S. Kennedy, my supervisor,for helpful criticism and discussion. My thanks are also due to the States of Guernsey Education Council for a Research Studentshiplwithout which this work could not have been undertaken. -132-
REFERENCES.
Ayre, G,L., 1968. Comparative studies on the behaviour of three species of ants (.Hymenoptera: Formicidae ) II. Trail formation and group foraging. Can. Ent. 101: 118-128. Banks, C.J., 1964. The behaviour of individual coccinellid larvae on plants. Br. J. Anim Behay., 5: 12-24. Batschelet, E., 1965. Statistical methods fro the analysis of problems in animal prientatj-_cgland certain biological rhythms (American Institute of Biological Sciences, Washington, D.C., U.S.A. ) Bernard, F., 1968. Les fourmis (Tim:S:112a= FOrmicidae ) d'Eurcvle occidentale g septentrionale. Faune, tt d3.1 haN911.L kl&literraneen, ho. 1. Masson et Cie, Paris. Blum, M.S., and Ross, G.N., 19b5. Chemical ,teleasers- of social behaviour. V. Source, specifity and properties of the odour trail pheromone of Tetramorium guineense (F.) (Formicidee: ivrmioinae) J. ins. Lhimaiol., 11: 857-68, Bonnet, C., 1779. Observation XLIII. Sur un procede des fourmis. Oeuvres d'Histoire Naturelle et de Philosophie, 1: 535-536. Brian, N.V., 1955. Food collection by a 'Scottish ant community. J. Anim Ecol., 24: 336-351. Brian, M.V., 1956. The natural density of Myrmica rubra and associated ants in West Scotland. Ins. Soc. III: 473-487. Butler, C.G., 1970. Chemical communication in insects: behavioural and ecologic aspects. Advan. Chemoreceotion 1:35-78. Carthy, J.D., 1951. The orientation of two allied species of British ant. II. Odour trail laying and following in Ac ntho012-as (Lasius) faliginmia. Behaviour, 3:304-318. Carthy, J.D., 1965. The behaviour of arthropods. Oliver and Boyd, London. Chandler, A.E.F., 1969. Locomotory behaviour of first instar larvae of aphidophagous y.,rT2121Liae (Diptera) after contact with aphids. Anim. Behay., 17: 673-678. Collingwood, C.A., 19b4. The identification and distribution of British ants I. A revised key to the species found in Britain. Trans. Soc. Brit. Ent. 16:93-114. Cook, A., Bamford, 0.S., Freeman, J.D.B., and Teidman, J.b., 1969. A study of the homing habit of the limpet. Anim. Behay., 17: 330.9. -133-
Davenport, D., Camougis,G., and Hickok, „i.e. 1960. Analyses of the behaviour of commensals in host-factor. I. A hesionid polychaete and a pinnotherid crab. Anim Behay. 8: 209-218. Dethier, V.G. 1947. Chemical insect attractInts and EtRilitilte. The Blakiston Co., Philadelphia, Pa. Dethier, V.G. 1957. Communication by insects: the physiology of dancing. Science, 125: 331-336. Dethier, V.G., Barton Browne, L., and Smith, Carroll N., 1960. The designation of chemicals in terms of the responses they elicit from insects. J. Econ. Ent. 53:134-136. Dingle, H. 1961. Correcting behaviour in Boxelder bugs. Ecology 42: 207-11. Dingle, H. 1962. The occurrence of correcting behaviour in various insects. Ecology-, 43: 727-728. Dingle, H. 1964. Further observations on correcting behaviour in Boxelder bugs. Anim. Behay. 12: 116-124. Dingle, H. 1964b. Correcting behaviour in mealworms (Tenebrio) and the rejection of a previous hypothesis. Anim. Behay. 12: 137-139. Dingle, H. 1965. Turn alternation by bugs on causeways as a delayed compensatory response and the effects of varying visual inputs and length of straight path. Anim. Behav, 13: 171-177. E,dmann, H., 1927. Rev. Zool. russe 7:39-47. Ellis, P.E., 1963. An experimental Study of feeding, basking, marching and pottering in locust nymphs. Behaviour 20:282-310. Fraenkel, G. and Gunn, D.L., 1961. The orientation of animals. New York: Dover Pubns. Frisch, K. von, 1967. The dance languaatLui orientation of bees (tr Chadwick) Belknap Press , Cambridge, Mass. Fritsch, H.H., 1959. Herzfraquenz, Haulungstadien and Lebensdauer Mannchen von Daphnia magna Strauss. Zwiss Zool 161:266-273. Goetsch, W., 1934. Untersuchungen uber die Zusammenarbeit im Ameisenstaat. Zeitschrift fur Morphologie urd Okologie der Tiere 28:319-401. Grosslight, J.H., and Harrison, P.C., 1961. Variability of response in a determined turning sequence in the mealworm (Tenebrio molitor) an experimental test of alternative hypotheses. Anim Behay. 9:loo-100 Gunn, D.L., 1966. in discussion period Symp. R.Ent Soc Lond. 3: 109-110. -134-
Gunn, D.L., Kennedy, J.S., and Pielou, D.P., 1937. Classification of Taxes and kineses. Nature, 140:1064. Heran, H, and Lindauer, M. 1963. Windkompensation und Seitenwindkorrektur der Beinen beim Flug uber Wasser. Z.vergl.Physiol, 47:39-55. Holldobler, B.,1971. Homing in the harvester ant Pogonomyrmex badius. Science, 171: 1149-51 Holldobler,B., and Wilson, E.O., 1970 Recruitment trails in the harvester ant Pogonomyrmex badius. Psyche 77: 385-99. Holt, S.J., 195. On the foraging activity of the wood ant. Anim Ecol. 24: 1-34. Hull, C-.L., 1943. Principles of EttEllgEL. New York. Appleton Century Crofts. Kennedy, J.S., 1945. Classification and nomenclature of Animal behaviour.
Langley R., 1956. Practical aatiatira. Pan Books, London. Nature 156:754. Lindauer, M., 19514. Dauertanze im Bienenstock und ihre Beziehung zur Sonnenbahn. Naturwissenschaften 41:506-507. Lubbock, Sir J., 1884, Ants, Bees and Wasps. London. Kegan Paul, Trench. MacGregor, E.G., 1948. Odour as a basis for orientated movement in ants. Behaviour 1:267-296, Marak, G.E., and Wolken, J.J., 1965. An action spectrum for the fire ant (Solenopsis saevissima) Nature, 205:1328-1329. Moser, J.C., and Blum, M.S., 1963. Trail marking substance of the Texas leaf cutting ant, source and potency. Science 140: 1228. Murdie G. and Hassell., 1973. Food distribution, Searching success, and predator prey models, in the EathamItigal Theory DI ILt Dynamics of hiolaical populations. Academic Press. Pickles, W. 1936., Populations and terrirories of the ants Formica fusee, Afanhpayso flavus and Myrmica ruginodis at Thornhill Yorks. J.Anim Ecol, 5:262-270. Pieron, H. 1904. Du role du sense musculaire dans l'orientation des fourmis. Bull inst Gen Psych 1V: 168-167, Pieron, H., 1909. Contribution a la bioiogie de la patelle et de la calyptree. Le sens de retour et la memoire topographique. Ali. 21acel. gan..5e ser 1, 19+29. Price, P.W. 1970,. Trail odours; recognition by ineects parasitic on cocoons._aaiaLaa 170: 546-547. Saintschi, F. 1911, Observations et remarques critiques sur le mechanisme de lcorientation chez les fourmis. Ray.Sallaag. LQ,21 15:003-336 Schneirla, T.C., 1929. Learning and orientation in ants. Come Psych moncme, 6:1-43. -135-
Schneirla TX., 1933. Studies on Army ants in Panama. J.Comp Psycho?. 15: 267-299. Schneiria, T.C., 1963. The behaviour and biology of certain Nearctic army ants; Springtime resurgence of cyclic function- S.E.Arizona. Anim Behay. 11:583-595. Shorey, H.H. 1973. Behavioural responses to insect pheromones 6052. Ann. Rev. Ent.18:349-381. Siegel, S. 1956. Nonparametric statistics for the behavioural sciences. McGraw Hill. New York. Stasko A.B., and Sullivan C,M., 1971. Responses of planarians to light, an examination of klinokinesis. Anim 3.61aai. Monogr 4: Sudd, J.H.,1957. Communication and recruitment in Pharoah's ant, Monomorium lharaonis (L.) Anim. Behav, 5: lo4-109. Sudd, J.H.,1960. The foraging method of Pharoah's ant, Monomorium pharaehis (L.) Anim Behay. 8: 67-75. Sudd, J.H., 1965. The transport of prey by ants Behay. 25:234-271. Sudd, J.H., 1959. interaction between ants on a scent trail. Nature 183: 1588. Sudd, J.H., 1967. An introduction to the behaviour of ants. Edward Arnold, London. Surtees G., 1964. Laboratogy studies on dispersion behaviour of adult beetles in grain VIII. Spontaneous activity in three spp. and a new approach to analysis of kinesis mechanisms. Anim Behav 12: 374-388. Szlep R. and Jacobi T. 1967. The mechanism of recruitment to mass foraging in colonies of Monomorium venustum Smith, M. subopacum. phoenicium Emery, IgLLnoml israelis For. and Tali_L„iona._ simrothri phoenicium Em. ins Sec XIV 25-40. Tumlinson J.H., Silverstein , R.M. Moser J.C. Brownlee R.G., Ruth J.M., 1971. identification ofthe trail pheromone of a leaf cutting ant Atta texana Nature 234:34c-349. Ullyott, P. 1936. The behaviour of Dendrocoelium lacteum. I. Responses at dark and light bouridaries,1I, Responses in non directional gradients. J.Exp Biol., 13: 253-264, 265-278. Vowles, D.M. 1951. Sensitivity of ants to polarised light, Nature 165 282-283. Vowles, D.M. 1954. The orientation of ants. 1. The substitution of stimuli. J. Exp. Biol. 31: 341-355. Vowles, D.M. 1955. The foraging of ants. Anim Behav 3: 1-13. -136-
Weir, J.S., 1958. Polyethism in workers of the ant tlyrmica. Ins Soc. 5: 97-128, . Wells, M.J. and Buckley, S.K.L., 1972. Snails and trails. Anim Behay. 20: 345-355.. Wells, P.H., and Wenner, A.M., 1973. Nature 241: 171-175. Wigglesworth, V.G., 1941. Sensory physiology of the human louse, Pediculus humanis. Parasitology 33: 67-169. Wigglesworth, V.G., 1939. The principles of insect plysiologz. 5th. Ed 1961, Methuen, London. Wilson, D.M., and Hoy, R.R., 1968. Optomotor reaction, Locomotory bias, and reactive inhibition in the milkweed bug 212E2.221,122 and the beetle Zophobas. Z. vergl. Lhysiol. 58: 136-152, Wilson, E.O., 1962. Chemical communication among workers of the fire ant, Ci.cler. losivalinja...p. (Fr Smith). 1. The organisation of mass foraging. Anim Behav, 10: 134-147. Wilson, E.O., 19b5. Trail sharing in ants. Psyche, 72: 2-7. Wilson, E.O., 1971 The insect societies. Belknap Press, Cambridge, Mass. Wilson, N.L., Dillier, J.H., and Markin, G.P., 1971. Foraging Territories of imported fire ants. Ann. Ent. Soc. Amer. 64: 660-665. Yasuno, M., 1965. Territory of ants in the Kayano grassland at Mt. Hakkoda. Sci. Rep. Tohoku Univ. ser 4, (Biol) 31: 195-206.