- Email: [email protected]
Brood-rearing behaviour in small cultures of the ant Myrmica rubra L
Anim. Behav.,1974,22,879-889
BROOD-REARING
BEHAVIOUR IN SMALL CULTURES OF THE ANT MYRbZICA RUBRA L. BY M. V. BRIAN
Institute
of Terrestrial
Ecology, Furzebrook
Research Station,
Wareham, Dorset
Abstract. The behaviour of individual workers and queens in small spring-type cultures in observation nests has been studied by regular sampling of their activities. Winter larvae of two distinct sizes: (i) small, worker-biased and (ii) big queen-potential, were the only brood present. Workers have been classified behaviourally on a basis of the ratio of time spent on/off brood into nurses (>2), foragers (0*5). With a queen in the culture all types bite the sexual larvae, as does the queen herself occasionally but the time spent doing this declines in the order: foragers, intermediates, nurses, queens. Nurse attack is usually restricted to the later stages of a culture. All workers also feed sexual larvae a little in the presence of queens, mostly before and after the main phase of attack which lasts for 5 or 6 days; these larvae are fed much more frequently if queens are absent. By contrast, small, worker-biased larvae are fed mainly by nurses. Queens thus switch worker behaviour in relation to sexual larvae at an individual, not a group, level. Death and debility of the queen brings foragers in to assist the nurses in feeding big, sexual but not worker-biased larvae. Pale workers usually nurse and dark ones usuallv forage or behave as intermediates but there are exceptions. There is some evidence, too, that nurses a&smaller than others. This paper describes a study of brood treatment by individually recognizable workers of the ant Myrmica rubra L. The main aim was to find out what part workers of different ages and sizes play in blocking the full sexual development of those female larvae that have the capability of forming queens, so that instead they yield adult workers. This only occurs if at least one queen is present and the mechanism involves both starvation of protein, which reduces their size (Brian 1973a), and a form of attack that advances their metamorphosis (Brian 1973b). Two hypotheses have been outlined (Brian 1973a). First, that the brood-rearing behaviour of every worker changes according to whether queens are present or not; second, that a class of workers that is subordmate in the society if queens are present becomes dominant if they are absent. Big workers might be such a class; they are known to increase in numbers as colonies grow and to herald the production of sexual larvae. They might have a stronger atllnity for sexual brood than for queens but be restrained from indulging this in the presence of adult queens. This study was designed to settle which hypothesis is correct: whether the queen switches behaviour in all workers or whether she transfers dominance in the society from one group to another. In other words, whether she acts at the individual or the group level.
Methods Nests of Myrmica were collected in late autumn and stored at 5°C. In all cases adults and brood were warmed at 20°C with full food for 1 or 2 weeks before being used in observation nests. Workers were marked by cutting off the left or the right or both or neither of their two epinotal spines whilst under COz narcosis. This provides an easily seen structural cue reinforced by the black colour of the wound scar. Black marks of a variety of shapes can be made on the thorax of pale workers by wounding but unless accompanied by structural differences they are not easily and certainly recognized. All observations have been made through a stereoscopic microscope with between 10 and 20 magnifications. A useful observation nest consists of a glass tube lying at the bottom of a V formed from two mirrors; the whole is covered with red glass. The glass tube (bore 0.5 to 1 *O cm) is reduced at one end to a pore for ventilation and plugged at the other with a polythene tube containing 10 to 20 per cent sucrose solution for water and energy. About two-thirds is kept under the red glass and one-third in the open. Crushed flies and other prey are inserted daily into the light part, in addition to the sugar. The angle between the mirrors is arranged to provide one clear image of the ants; then, with the aid of a spotlight which can be waxed and waned gradually, it is possible to observe them both from above and from either side. 819
880
ANIMAL
BEHAVIOUR,
Each nest contained four or five workers, a size range of ten larvae and one queen. The workers were deliberately chosen to cover all possible variations of colour, as degree of pigmention has long been known to influence behaviour in this species (Ehrhardt 1931). Size, too, was varied as much as possible, but frequently small dark and big pale workers were rare in the colonies. Workers were not selected behaviourally : by, for example, separating those that came out of the nest readily on disturbance from those more strongly attached to brood. Behaviour was sampled periodically, not observed continuously. At each sampling a culture was watched until the activity of every adult had been noted; this was repeated two or three times a day at intervals of at least an hour during daytime for several weeks. The main activities are : grooming, feeding by regurgitation chewing prey, exploring or collectin material. These are related to specific objects, f ike big or small larvae, workers, or the queen and are performed in or outside the darkened area. Also, much of the time is spent standing still, either on or off the brood. Some thirty or more activities were noted as follows: standing on or off brood, workers or the queen, on the nest fabric or outside; grooming themselves, the queen, other workers, small or big larvae, eggs or pupae or the nest fabric; feeding the queen, other workers, small or big larvae; chewing prey; biting sexual larvae; collecting urine from larvae; laying an egg or attacking other adults; collecting a fly or sugar or water; exploring inside or outside the darkened area; taking rubbish out or ejecting a pellet or faeces. Classification and condensation of the collected data is not easy but some reasonable simplifications help. Thus, grooming is highly associated with liquid regurgitation, and the two actions are grouped together. Grooming and feeding adults (workers and queens) and rare actions, like licking the walls and defecating, are also grouped together as they appear to be unconnected with brood rearing. Important distinctions are related to the size of larva attended, where workers stand whilst inactive and, in general, their degree of attraction to the brood area. By these means the thirty activities can be reduced to nine that are important in brood rearing in spring; these are listed in Table I. In their turn these can be classified into three major groups: one (group A) is a set concerned
22,
4
with feeding and rearing small larvae, which attract some workers strongly in the presence of queens; another (group C) is a set concerned with exploring the nest and environment and standing about away from larvae; finally there is a set (group B) of activities which are neutral, both to small larvae and to exploration, but concerned with the treatment of big sexual larvae and adults. Two main series of observations are reported here. The first is a study of how workers behave with queens present all the time; this illustrates the diversity of behaviour in these circumstances. The second is a study of two cultures between which a queen alternated; this shows the effect of a change in queen status. Results The Behaviour of Workers and Queens To describe all the cultures watched in detail would be tedious; a representative sample will be given first and then the results of other observations summarized. A representative sample. This culture consisted of one queen, two small pale workers (symbolized wl and w2), a large pale worker (W) and two large dark workers (Wl and W2). It was watched for 39 days, during which time a total of 396 records were made; twenty-nine of these involving eggs or pupae have been excluded and the remaining 367 classified into the nine minor and three major groups of activities just described. Three rounds of big sexual larvae were supplied: on days 1, 23 and 36. The queen was closely associated with small larvae but spent a quarter of her time feeding directly on prey. She never fed or bit big sexual larvae. The worker, wl, showed a very high association with small larvae, spending more of its time grooming and feeding them than the queen. She never groomed or fed the queen, nor did she exchange food with other workers. Big sexual larvae were bitten four times but only in the second and third rounds by this worker. She was only once seen away from the brood and is a typical nurse. The next small pale worker, w2, spent less time standing on brood and more time chewing prey and dealing with small larvae. Unlike wl, she was seen feeding and grooming big larvae four times, three in the first and once in the third round. Like WI, she was seen biting big larvae three times in the second and third rounds, not the first. She, too, is classed as a typical nurse.
BRIAN:
BROOD
REARING
BEHAVIOUR
881
IN THE ANT
Table I. Summar y of Activity samples of Five Workem and One Queen Rearing Small and Large Larvae in Spring for Thirty-Nine Days, and a C%ss&ation of Worker Type Bnsed on These Observations. Activities Connehd with Eggs 0rPapaearenotInchded
Classof activity A B
C
Q
wl
w2
W
w2
(1) Stand on brood (2) Groom and feed 1 (3) Chew prey
38 2 16
T:
l4 10 12
‘l 0 8
9
11
l7 12 14
1;; ;r$gn and feed L
0
0
4
:
lf
(3) Groom and feed adults
!
ii
i
8
(1) Stand off brood (2) Explore (3) Collect
2
tl
0
8
0
it
Description of activity
Sum A E Assignmentof behavioural type:
WI
Total
%
109 ::
30 10 17
1:
7
2
4
6
33:
1:
I
22
23
55
15
21
z
121
23 4
71
%i: 49 YE 12 1 2
36 10 11
:‘6 31
2; 36
2;! 82
:: 23
Q
N
I
F
N
N
3
Explanation of symbols: 1 = small larva, L = big larva, Q = queen, w = small pale worker, W = big pale worker, W = big dark worker, N = nurse, I = intermediate, F = forager.
Of the big workers the first (W), which was pale, spent rather less time on brood than the nurses, both standing still and feeding and grooming, but about the same chewing prey. She groomed but never fed a larva in the first round before she started biting. Like wl and w2, she did not bite sexual larvae in the first round but did later on. According to the table she groomed and fed adults nine times and collected a fly once. Her overall pattern of activity, with thirty-six actions in group A and only ten in group C, make it reasonable to classify her as a nurse, but she is less nurse-like than the small pale workers and evidently has a tendency to leave the young brood and explore. The second big worker, WI, was very dark and spent very little time on the brood or chewing prey near it. She was once seen feeding big larvae in the first round after biting had stopped. Her record of biting big larvae covered all three rounds and she was particularly concerned with this in the first. Four out of the six records of grooming and feeding adults were self-grooming. She never fed the queen. This worker spent a great deal of time outside exploring but was only once seen to collect food (a fly). Most of her time standing away from the brood seems to have been spent guarding the others, for she adopted a position facing away from the brood zone towards the nest entrance. She is a typical forager.
The third big worker was also dark (W2) but spent more time on the brood and chewing prey than Wl. Nevertheless, she was never seen to feed small larvae. Like WI, she bit big larvae a lot in all three rounds and she spent a lot of time on guard. In the end she had more records of behaviour under group C than under group A but because she spent so much time with the brood she is classed as an intermediate. Quite probably she was changing from nursing to foraging behaviour but it is possible that Wl interfered when she started exploring though this was never seen. Hence, in this culture there were three nurses (all pale and one big), one intermediate (dark and big) and one forager (dark and big). The activities of the whole culture, summed and expressed as percentages, are given on the right of Table I. It is important at present to note that both nurses and foragers both fed and groomed the big sexual larvae as well as biting them. There was a time trend in this however that will be described shortly. Comparisons of Four Cuhres Data for all individuals of four cultures comprising in all four queens and seventeen workers are summarized in Table II ; this includes the one just described in detail (culture 3). Only the three main groups of activity are shown but group B has been given in more detail to
882
ANIMAL
BEHAVIOUR,
22,
4
Table II. All Individuals Showing Their PhysicalCharacteristicpand Caste,the Freqwney of Activities in Grops, A B and C andtheFrequencyWi~WhichTbeyWereSeentoFeedsndGroom(Bl)orBite(B2)~~e
Frequencyof activity Code
Culture
A
B
C
8
:
56
1:
8
21
:;20
:
wl W
w2
wl
i 3
i 1
w2
Bl
2
NC 28 11
B2
0
0
11 2
*l-8 9.8
04
:2
49
12
:
49
0
4
ii 25
:i 19
2 2 7
5: 13 6.3
2' 4
3" 3
10 l?
;:z
2'6
44
w"
:
W W
;
E 25 31
:
::
;::
:2 0 1
W
t
27
20
20
1.4
z
3
$2 w2
3
1
21 20 11
21 17 18
:: 19
AZ4 0.58
:
1: 3
Wl
:
11
22
2
0.46
5
:
:
; 7
2: 19
ET
0.38 0.19 0.17
: 3
13 7
Zl W
:t
Worker type assigned -
Nurse
:
Intermediate
Forager
+Q died.
show the individual’s behaviour towards sexual larvae. Queens varied somewhat: three spent nearly all their time on the brood; another that died after only 8 days wandered out occasionally. The three normal queens form a homogeneous group (by ~2, P > O-05). The workers have been classified as nurses, intermediates and foragers on a basis of the relative frequency of actions in groups A and C. The distribution of this ratio, on a logarithmic base for compactness, is shown in Table VIII. It has no breaks in its whole range from 50 to O-17 and provides no basis for a natural classification. This is not surprising, for Ehrhardt (1931) has shown that age changes nurses into foragers. The distinction made between nurses, intermediates and foragers is therefore somewhat arbitrary. Moreover, both the nurses and the foragers are, as far as the relative frequency of activities A : B : C are concerned, internally heterogeneous (by ~2, P < @OS). Curiously enough, the only category that is homogeneous in this sense is that of the intermediates (by ~2, P 0.2 to 0.3) but sub-groups of nurses, the first three and the last four listed in Table II, are internally homogeneous. However, the categories used are certainly distinct in their values of A: B : C,
for the last four nurses, if summed and compared with the intermediates, give a high value of ~2 (P < 0401), as do the intermediates and foragers compared (P < 0401). Curiously, the least difference exists between queens and the top three nurses, which give a ~2 with P = 0.02. Seven out of nine nurses were small and eight out of nine were pale, but one small dark worker, though nurse-like in behaviour, spent much less time with small larvae than the average. One small pale worker was even less associated with small larvae. The intermediate types were all big and three were dark. The foragers were all dark and three out of four were big. The one with most outside experience was, however, small and dark. Activities of group B were shown rather less often by queens and nurses than by intermediates and foragers but this varied a lot. After classifying the workers, an average for each type and for queens can be calculated (Table III). This shows that the average queen spends over half her time motionless on the brood, whilst the average nurse spends about one-third of her time this way. A nurse, though she chews prey about as often as a queen, feeds and grooms small larvae more often. A forager does very little nursing but spends quite a lot
BRIAN: BROOD REARING BEHAVIOUR IN THE ANT
883
Table III. The Percentageof Time Spentin the Nine Main Activiti~ by the AverageQueen,Nurse,Intermediate and Forager, and their Rank
Activity group A B C
Queen Description of activity (2) (1) Groom Stand onand brood feed 1 (3) Chew prey
{;j ;rF
and feed L
Nurse
Intermediate % rank
Forager % rank
%
rank
%
rank
::52
:
30 ::
1.5 2.5
:s8
73.5 2
2 8
; 6
4 8 8
i.5 4.5
1; 11
;:: 5
1: 9
i 5
2
3
(3) droom and feed adults
ii
E.5 5
(1) Stand off brood (2) Explore (3) Collect
7
4
‘7
7
20
ii.5
22
2
21
78.5
2
69
1:
6
25 11
:
of time chewing prey; about half as much as nurses. Activities off the brood account for only 10 to 14 per cent of a nurse’s time, 37 per cent of an intermediate’s time and 58 per cent of a forager’s time. The average forager seems to spend 36 per cent of its time exploring and collecting and nearly 22 per cent guarding the nest entrance. Its only other major activity is biting big sexual larvae. The time spent doing this declines as follows : forager-intermediatenurse-queen; the last rarely bites them. Feeding and grooming big larvae is not, on the other hand, related to worker type, nor is feeding and grooming adults. Ranking these activities in order of frequency helps in the comparison. In particular, it shows a striking difference between intermediates and foragers in the rank position of exploratory behaviour (C2): last equal in the former and first in the latter. On the other hand both categories rank very high as regards standing off brood (Cl). These four sets of ranks can be shown to lack concordance, using Kendall’s test ( W = 0.301, P near 0.3). Individual comparisons show no rank correlation between worker types, using Kendall’s T-test: between nurses and intermediates P = 0.24 and between intermediates and foragers P = 0.31. Only queens and nurses show significent rank correlation (T = 0.63, P = O-012), which recalls the near-homogeneity of A : B : C, using the ~2 test. There is evidently more behavioural resemblance between the morphologicallydistinct female castes than between any set of workers. Behaviour Towards Big Larvae Biting. The decline in biting tendency from foragers through intermediates and nurses to
queens has been noted. There is also a time effect in the culture described (number 3), whereas the foragers and the intermediates bit larvae in the first round, the nurses did not join in until the second and third rounds. This is true of all four cultures: whereas only five out of nine nurses bit larvae during the first round, seven out of eight foragers did so; nurses became more hostile in later rounds. Nurses are of course very preoccupied with feeding small larvae at first, whereas the intermediates and foragers have spare time as food is very easy to obtain. However, competition for biting space on these larvae is undoubtedly real and tends to favour the bigger, stronger, more aggressive workers. Two big dark workers were particularly and consistently aggressive and could be seen biting big larvae on the fringe of the brood group for hours at a time and were clearly making it difficult for smaller, younger workers to attack systematically. Table IV illustrates a typical time sequence: cultures three and four have been added together on the basis of worker type, and the frequency of biting and of feeding have been set out (in 2-day periods) over the whole 44 days during which three rounds of big larvae were supplied. Notice again that the nurses did not bite in the first round but that the intermediates and foragers bit in all three. Biting started after 8 days in the first round and after only 4 days in the other two rounds; this is probably because the workers were still recovering from hibernation when the experiment was set up. Feeding. Feeding these big larvae is certainly not the preoccupation of nurses in the same way that feeding small larvae is. In fact, intermediates and foragers feed them slightly more than nurses do. Feeding seems to go on in rather a desultory
884
ANIMAL
BEHAVIOUR,
22,
TaMeIV.TheFreqneacywithwhiehPeedi4gand~~of~~WasRecordedinthe~o~3an84.~ After Group@ Into Queens, Nurses, Intermediat~~~~~ Rods
Queens 2-day classes
Feed
Feed
of J3ig Larvae Were Made AvaiJable to Intermediates and Foragers
NUlWS
Bite
4
Bite
Feed
Days on which L added
Bite
o-2 -4
First L
-6
1
-
2
-8
2
-
1
-10
1
-
-12
3
-
1
-
3 11
1
3
-14
5
-
-16
2
-
1
-
-18
1
-
-20 -22
1
-24
-
-26
-
Fresh L
3
-
12
5
-
4
-28 -30 -32
-
-34 -36
Fresh L -
-38
4
-40
2
-42 -44
way before and after the period of biting but never during its peak. This is not altogether surprising as it would be difficult to feed a larva that was being attacked. These periods of attack last 5 to 6 days and then fade. Some larvae succeed in growing into queens but more mature slowly and metamorphose at a smaller sire, forming workers. At the moment there is no clue as to why some succeed and others fail.
1
Queens Present and Absent In one culture already described the queen died on the eighth day. A striking change in worker behaviour towards big larvae soon followed. Thus, whereas they were actively biting larvae on days 2 and 3, they were feeding and grooming them on days 6 and 7. In this, all four workers were involved.
BRIAN:
BROOD
REARING
BEHAVIOUR
To pursue this further and see what effect queen status had on the activities of the various worker types, two cultures were set up for observation and a queen was switched from one to the other every 7 days. The whole trial was run for 4 weeks, giving each culture two with and two without the queen. There were four workers, chosen to span a range of sizes and colours, and three big and three small larvae
IN THE ANT
885
in each observation nest. All the adults were warmed for 10 days beforehand. Twenty sample observations were taken each week, giving eighty in all, forty with and forty without the queen. The activities have been summarized in the same way as before and collected in Tables V and VI. This time, each of the eight workers has a record of its actions during the period with the queen and during a period with-
Table V. Culture X: Summary of the Activities of Four Workers with a Queen on Alternate Weeks (Weeks 1 and 3 witb, 2 and 4 without). Worker a, Small and PakKoloured; Worker b, Small and Medhun-Coloured; Worker c, Bii and MedhmColoured; Worker d, Big and Median-Coloured Worker individual Class of activity A B C
Description activity
of
(1) (2) (3) {;]
Stand on brood Groom and Feed 1 Chew prey gy?andfeedL
(3) (1) (2) (3)
Grroom and feed adults Stand off brood Explore Collect
SllmA
B C Characterization Explanation
Sum
Q
+Q “-a
3: 4 f 2 0
127 x 1
x 35 ?I
of worker:
4 I 3 4
-
ii
1 N
+Q b-Q
+Q ‘-0
+Q d-O
+Q
-Q
14
7
23
12
28
4
15
27
80
45
:
i!l
;
;: 6 0
1: 5 6
:, 1
17 2
: 0
54 1:
32 15
:: I
1: 23
0” 0
ii
31
:
i
;
zi
23 13 4 N
9 17 12 I
b 0 16
4 1
ii
1: 1 24
10 0 31
ii
124 I
13 10 I
: N
3 N
of symbols: N = nurse, I = intermediate,
1; 1
1: 2
20
:i
98
I52 N
26
::
F = forager.
Table VI. Culture Y: Sumnuuy of the Activities of Four Workers with a Queen on Alternate Weeks (Weeks 2 and 4 with, 1 and 3 without). Worker e, Small and Pale; Worker f, Small and Medium-Coloured; Worker g, Bii and Dark Coloured; Worker h, Bii and Medhun-coloured. Worker individual Class of activity A B
C SumA
Description of activity
Q
(1) (2) (3) (1)
Stand on brood Groom and feed 1 Chew prey Groom and feed L
29 1:
(2) (3) Bite GroomL and feed adults (1) Explore (2) Stand off brood (3) Collect B C
Characterization Explanation
of worker:
of symbols:
:
+Q f-Q
+Q
0
7 8
10 3 7 12
4 3 6 i
2 17
?
10 4
2”
5
x 0 39 tl
s 0
i!l 0 20 14 1 N
N = nurse,
+Qe-Q
ii 2 N
I = intermediate,
i
SUm
L?
-Q
+Q
h-Q
+Q
-Q
2 :
x
:.
:;
3 19
18 :‘o
20 10 15 58
:
15
19”
2; 2 49 62 34
2: 1 45 17 31
4 1 1 loa
10
4 2
6”
2
Y
46
: 0 13 16 4
: 0 2;
182 0 6 2
163 1 6 s
: 2 14 12 8
0 ii ;:
N
I
F
F
I
I
6
F = forager.
5
886
ANIMAL
BEHAVIOUR,
out her; thus, any change in its behaviour due to the queen is apparent. The queen fed on prey more in culture Y than in culture X but showed no other major differences. No explanation can be offered for this except that Y seems to have chewed prey more in general than the first; this might have been because it had a devoted forager. The effect of the queen on the culture as a whole can now be considered. In X the workers were particularly sedentary and the queen reduced the time spent standing on the brood very substantially; Y workers were more active and the queen had no effect. In both cultures the queen increased slightly the time workers spent feeding small larvae and chewing prey. She reduced the time they spent feeding and grooming big larvae to one-third of its value in the queenless group; intensive attack was substituted. Inter change between adults rose in X when the queen was added but fell slightly in Y; this is, perhaps, again due to her greater activating effect on the X workers. She showed no appreciable influence on the time spent standing away from the brood, foraging or simply exploring. To summarize, the queen had her greatest effect on the attitude of workers towards big sexual larvae, inducing attack and reducing feeding. She only had a small effect on the activity and attention paid to small larvae, increasing it slightly. In one culture she reduced the time for which the workers stood on the brood and increased the amount of mutual interchange. The behaviour of each worker can be described individually. a. Small and pale, proved as expected to have strong nursing tendencies. She spent less time standing on the brood when the queen was added and more time feeding and grooming small larvae and adults; she also bit big larvae a little. b. Small, but a little darker-coloured, turned out to be intermediate between nurse and forager. Like a, she spent less time standing on brood when the queen was present and more time grooming and feeding adults and biting big larvae but unlike a she spent very little time at all feeding and grooming small larvae or chewing prey. e. A big and medium-coloured worker, apparently became less nurse-like when the queen was in the culture; she left the brood and explored outside and bit big larvae. However, she was never an active nurse and merely
22,
4
stood passively on larvae so that the queen substituted activity off the brood for inactivity on it. d. Also big and medium-coloured, behaved as a nurse both with and without the queen. She was like a in many ways but showed a very strong reaction to big larvae. e. Small and pale, was a normal nurse. When the queen was added she switched from standing on brood and feeding big larvae to attacking them. f: Small but darker than e, was rather unbiased behaviourally. With a queen she chewed prey more and foraged less and associated with small larvae more though she never fed them. She also fed big larvae less and bit them a little. g. Big and dark, was a typical forager. Though she fed big larvae regularly in queenless conditions she bit them continually otherwise. h. Big and medium-coloured, was an intermediate. She, too, fed big larvae when the queen was absent but did not attack them as wholeheartedly as g or e when the queen was present, though she fed small larvae more. In these cultures, during periods when the queen was present, all the workers bit big larvae, and six out of eight fed them as well; remarkable ambivalence! The frequency of feeding was, however, much less than when the queen was absent; then seven out of eight workers delivered food often. To look for time trends, all the weekly sequences of twenty observations have been summed term by term after separating those periods with queens from those without. This is quite legitimate, for fresh big larvae were given each week at the start of a new series. The results (Table VII), with observations Table VII. Trends in Biting and Feeding Freqmcy of SemalLarvaebyworkerswltb or without a Queen. FourSeziesofTwentyObsemationswithaQueemand FourwitboutHaveBeenSammd.FreshSexnalLmvae WereGivenattbeStartofBachSerltw
Observation sequence
With a queen Feeds
Bites
Without a queen:
F&S
l-4
6
2
3
5-8
2
11
6
9-12
2
19
9
13-16
3
22
7
17-U)
0
22
13
887
BRIAN: BROOD REARING BEHAVIOUR IN THE ANT
(A/C > O-5 < 2.0). The system seems to work well in spite of the fact that the frequency of the ratio shows no natural break and some of the classes are heterogeneous. Moreover, there is a point of interest about the distribution that should be noted though its significance is not clear. On a logarithmic base it is symmetric with a mode at A/C = 2 (Table VIII). It is thus almost exactly bisected into thirteen nurses on one side and twelve other categories on the other side. This is a coincidence, and since workers were not taken at random too much weight should not be attached to it. However, it might mean that the nurses represent a young age group and the rest an older one; the nurses may thus change with time into both intermediates and foragers. In winter the worker population is composed very largely of two age groups: those from the previous summer overwintering for the first time and older ones overwintering for the second time (Brian 1951, 1972). If the two groups are compared for pigmentation (Table IX) it is clear that the nurses are paler than the others (by the x* test for homogeneity P < O-01). As it is well known that workers darken with time they are almost certainly, as would be expected, younger. There is also a less well-marked size difference (by x* P = 0.03); a possible explanation of this is discussed in the next section.
grouped into fours, show that trends exist: thus, with queens the time spent feeding big larvae declines and biting increases, without queens feeding frequency rises. Worker Sii and Colour The behavioural basis of worker classification has already been explained and justified. Those that spend more than twice as much time with brood than elsewhere (A/C > 2) have been classed as nurses. Others have been classed as foragers, (A/C < 0.5) and intermediates, Table VIII. The Frequency Diibution Twenty-Five Workers on a Log&se
Ratio on/off brood behaviour (A/C) FrequencyClasses to 0.125
Frequency distribution of all 25 workers 2
0.25 too-5
3 1
to 1
2
Scale
for
Worker type
0
o-125 to o-25
0.5
of A/C
F
3-l
1 to2 2
to4
5-l
4
to8
3
8
to16
2
Discussion The theory that the worker population is divided into pro- and anti-queen factions, that the latter gain power as the colony grows and the queens’ influence weakens and that as a consequence associate and replacement queens arise, is not supported by these results. Big workers produced as the colony grows in size, though truly precursors of new queens in the population and
16 to32 32 to64
64 to 128 SUm
2 I
OJ 25
Explanation of symbols: N = nurse, I = intermediates, F = foragers.
Table TX. Two Rebaviour-Based Classes of Workers (Nurses and others) Aaalysed in Respect of Size and Coloration. All Twenty-Five Workers Have Been Included NUlXS
Coloration intensity
Foragers and intermediates
Small
Big
SUm
Small
Big
SUm
Total
Pale
8
2
10
0
1
1
11
Medium
0
2
2
2
1
3
5
Dark
1
0
1
1
7
8
9
Sum
9
4
13
3
9
12
25
888
ANIMAL
BEHAVIOUR,
though they must improve the general nutritional status, are not themselves instruments of newqueen production. Indeed, the reverse is the case, for as long as queens are present, these big workers are the first and most persistent attackers of sex-potential larvae. Instead of this population control over sex production there is control at the individual level. All workers are switched by queens from nourishing sexual larvae on protein to starving them of it (thus reducing their size) and biting them (thus advancing their metamorphosis). In this process the bigger, older foragers appear to play a more important part than the smaller, younger nurses. With ample and effective queens they attack sexual larvae vigorously; if without, they help the nurses feed them on undiluted prey, an attention they rarely bestow on small, non-sexual larvae; they are more responsive to sexual larvae than are the workers. This study has also yielded information about the way work is apportioned. This species has been investigated by Ehrhardt (1931) who found that pale young workers were nurses and that they changed into foragers as they darkened and aged; they are pre-adapted to daylight exposure, Weir (1958a, b) confirmed this with the species Myrmica scabrinodis Nylander and Myrmica ruginodis Nylander. In the former species he distinguished six degrees of melanization and found that the darker ones were more easily drawn away from the brood than the paler ones. The latter (nurses) would leave the brood after the dark ones had been taken away but otherwise they stayed close to it. In fact, Brian (1956) found that a proportion of workers, presumably nurses, would struggle towards the brood even when worker density on it was high. If dark foragers are withdrawn some of the nurses move off, presumably in search of food which is normally placed on the periphery by foragers. By testing the nest-building skill of the colour classes Weir found that a group that spent a lot of time standing near but not on the brood were most skilful, and he called them domestics and regarded them as a mobile reserve of foragers. The intermediates identified in these studies seem to correspond very well behaviourally with these domestics. That nurses have a tendency to be smaller than foragers is interesting in view of the fact that Myrmica rubra is undoubtedly a monomorphic species. Weir (1958a, b) found exactly the same in Myrmica scabrinodis but not in the sub-species microgyna of M. ruginodis. Ehrhardt
22,
4
(1931) does not appear to have noticed this in M. rubra though it was conspicuous in the dimorphic Messor. It is also true of Oecophylla,
as Ledoux has shown (1949), but it is not a general rule in ants, for the nurses are larger than foragers in some species of Pheidole (Sudd 1967). Small size would appear to be an advantage to nurses. It brings them down to the scale of their larvae and enables more to be packed into the confined nest spaces; however, large size may not be an advantage to foragers, particularly if they have evolved an effective system of co-operative hunting. If smaller workers changed behaviourally more slowly than bigger ones they might create a population in which nurses were smaller on average than others. They may come from different broods, too. Weir suggested that the small pale workers of M. scabrinodis which were the nurses in spring were rapid brood of the previous summer (the life-cycle is described in Brian 195 1). Medium-coloured workers would then have been formed earlier in the summer from hibernated larvae and the darkest workers would have overwintered twice. This is consistent with what is known of worker longevity (Brian 1951, 1972). Curiously enough, the brood from eggs in one season dies 2 years afterwards, whether it becomes adult in the same season (rapid) or in the next. Thus rapid brood spends a bigger proportion of its life in the adult stage than the brood that hibernates in the larval stage. Larvae age as quickly as the adults do. This might imply slower behavioural change in the small workers formed rapidly and so add to the size effect already suggested. These small workers are formed from larvae that are switched relatively early in their development from the queen-style of growth and development. Larger workers are formed from brood that has followed the queen-style further, hibernated, and even then failed to get the necessary food for growth, either because this is just not available or because it is withheld by workers under the influence of queens. However, though these two ways of producing workers together give a unimodal size frequency distribution, each component in fact follows slightly different ontogenetic routes. These could cause behavioural differences: a worker that was a ‘failed’ queen might tend to forage and a precocious worker to nurse. It would be interesting to enquire whether any of the control systems known to exist in Myrmica could
BRIAN: BROOD REARING BEHAVIOUR IN THE ANT
regulate the ratio nurse-forager efficiently by varying the ratio of rapid-retarded brood. REFERENCES Brian, M. V. (1951). Summer population changes in colonies of the ant Myrmica. Physiologia camp. Oecol., 2, 248-262. Brian, M. V. (1956). Group form and causesof working inefficiencyin the ant Myrmica rubra L. Physiol. Zod., 29, 173-194. Brian, M. V. (1972).Population turnover in wild colonies of the ant Myrmica. In: Proceedings of ZBTIPT Working Group on Social Znsects meeting, Warsaw, June 1970, Ekol. Pofska, 20,43-53.
Brian, M. V. (1973a). Feeding and growth in the ant Myrmica. J. Anim. Ecol., 42, 37-53.
889
Brian, M. V. (1973b). Caste control through worker attack in the ant Myrmica. Znsectes sot., 20, 87-102. Ehrhardt, S. (1931). tfber Arbeitsteil bei Myrmicaturd Messor-Arten. 2. Morph. Y kol. Tiere, 20, 755-812. Ledoux, A. (1949).Recherchesur la biologle de la fourmi tileuse (Oecophyllo Iongitwda Latr.). In: Theses p&sent&s a la Faculte des Sciencesde l’Univemit& de Paris,p. 461. Sudd, J. H (1967) An Introduction to the Behaviour of Ants p. 200. London: Edward Arnold. Weir, J. S. (1958a). Polyethism in workers of the ant Myrmica. Part I. Znsectessot,, 5,97-128. Weir, J. S. (1958b). Polyethism in workers of the ant Myrmica. Part II. Znsectes sot., 5, 315-339. (Received 14 December 1973; revised 4 March MS.
number: 1284)
1974;
BROOD-REARING
BEHAVIOUR IN SMALL CULTURES OF THE ANT MYRbZICA RUBRA L. BY M. V. BRIAN
Institute
of Terrestrial
Ecology, Furzebrook
Research Station,
Wareham, Dorset
Abstract. The behaviour of individual workers and queens in small spring-type cultures in observation nests has been studied by regular sampling of their activities. Winter larvae of two distinct sizes: (i) small, worker-biased and (ii) big queen-potential, were the only brood present. Workers have been classified behaviourally on a basis of the ratio of time spent on/off brood into nurses (>2), foragers (
Methods Nests of Myrmica were collected in late autumn and stored at 5°C. In all cases adults and brood were warmed at 20°C with full food for 1 or 2 weeks before being used in observation nests. Workers were marked by cutting off the left or the right or both or neither of their two epinotal spines whilst under COz narcosis. This provides an easily seen structural cue reinforced by the black colour of the wound scar. Black marks of a variety of shapes can be made on the thorax of pale workers by wounding but unless accompanied by structural differences they are not easily and certainly recognized. All observations have been made through a stereoscopic microscope with between 10 and 20 magnifications. A useful observation nest consists of a glass tube lying at the bottom of a V formed from two mirrors; the whole is covered with red glass. The glass tube (bore 0.5 to 1 *O cm) is reduced at one end to a pore for ventilation and plugged at the other with a polythene tube containing 10 to 20 per cent sucrose solution for water and energy. About two-thirds is kept under the red glass and one-third in the open. Crushed flies and other prey are inserted daily into the light part, in addition to the sugar. The angle between the mirrors is arranged to provide one clear image of the ants; then, with the aid of a spotlight which can be waxed and waned gradually, it is possible to observe them both from above and from either side. 819
880
ANIMAL
BEHAVIOUR,
Each nest contained four or five workers, a size range of ten larvae and one queen. The workers were deliberately chosen to cover all possible variations of colour, as degree of pigmention has long been known to influence behaviour in this species (Ehrhardt 1931). Size, too, was varied as much as possible, but frequently small dark and big pale workers were rare in the colonies. Workers were not selected behaviourally : by, for example, separating those that came out of the nest readily on disturbance from those more strongly attached to brood. Behaviour was sampled periodically, not observed continuously. At each sampling a culture was watched until the activity of every adult had been noted; this was repeated two or three times a day at intervals of at least an hour during daytime for several weeks. The main activities are : grooming, feeding by regurgitation chewing prey, exploring or collectin material. These are related to specific objects, f ike big or small larvae, workers, or the queen and are performed in or outside the darkened area. Also, much of the time is spent standing still, either on or off the brood. Some thirty or more activities were noted as follows: standing on or off brood, workers or the queen, on the nest fabric or outside; grooming themselves, the queen, other workers, small or big larvae, eggs or pupae or the nest fabric; feeding the queen, other workers, small or big larvae; chewing prey; biting sexual larvae; collecting urine from larvae; laying an egg or attacking other adults; collecting a fly or sugar or water; exploring inside or outside the darkened area; taking rubbish out or ejecting a pellet or faeces. Classification and condensation of the collected data is not easy but some reasonable simplifications help. Thus, grooming is highly associated with liquid regurgitation, and the two actions are grouped together. Grooming and feeding adults (workers and queens) and rare actions, like licking the walls and defecating, are also grouped together as they appear to be unconnected with brood rearing. Important distinctions are related to the size of larva attended, where workers stand whilst inactive and, in general, their degree of attraction to the brood area. By these means the thirty activities can be reduced to nine that are important in brood rearing in spring; these are listed in Table I. In their turn these can be classified into three major groups: one (group A) is a set concerned
22,
4
with feeding and rearing small larvae, which attract some workers strongly in the presence of queens; another (group C) is a set concerned with exploring the nest and environment and standing about away from larvae; finally there is a set (group B) of activities which are neutral, both to small larvae and to exploration, but concerned with the treatment of big sexual larvae and adults. Two main series of observations are reported here. The first is a study of how workers behave with queens present all the time; this illustrates the diversity of behaviour in these circumstances. The second is a study of two cultures between which a queen alternated; this shows the effect of a change in queen status. Results The Behaviour of Workers and Queens To describe all the cultures watched in detail would be tedious; a representative sample will be given first and then the results of other observations summarized. A representative sample. This culture consisted of one queen, two small pale workers (symbolized wl and w2), a large pale worker (W) and two large dark workers (Wl and W2). It was watched for 39 days, during which time a total of 396 records were made; twenty-nine of these involving eggs or pupae have been excluded and the remaining 367 classified into the nine minor and three major groups of activities just described. Three rounds of big sexual larvae were supplied: on days 1, 23 and 36. The queen was closely associated with small larvae but spent a quarter of her time feeding directly on prey. She never fed or bit big sexual larvae. The worker, wl, showed a very high association with small larvae, spending more of its time grooming and feeding them than the queen. She never groomed or fed the queen, nor did she exchange food with other workers. Big sexual larvae were bitten four times but only in the second and third rounds by this worker. She was only once seen away from the brood and is a typical nurse. The next small pale worker, w2, spent less time standing on brood and more time chewing prey and dealing with small larvae. Unlike wl, she was seen feeding and grooming big larvae four times, three in the first and once in the third round. Like WI, she was seen biting big larvae three times in the second and third rounds, not the first. She, too, is classed as a typical nurse.
BRIAN:
BROOD
REARING
BEHAVIOUR
881
IN THE ANT
Table I. Summar y of Activity samples of Five Workem and One Queen Rearing Small and Large Larvae in Spring for Thirty-Nine Days, and a C%ss&ation of Worker Type Bnsed on These Observations. Activities Connehd with Eggs 0rPapaearenotInchded
Classof activity A B
C
Q
wl
w2
W
w2
(1) Stand on brood (2) Groom and feed 1 (3) Chew prey
38 2 16
T:
l4 10 12
‘l 0 8
9
11
l7 12 14
1;; ;r$gn and feed L
0
0
4
:
lf
(3) Groom and feed adults
!
ii
i
8
(1) Stand off brood (2) Explore (3) Collect
2
tl
0
8
0
it
Description of activity
Sum A E Assignmentof behavioural type:
WI
Total
%
109 ::
30 10 17
1:
7
2
4
6
33:
1:
I
22
23
55
15
21
z
121
23 4
71
%i: 49 YE 12 1 2
36 10 11
:‘6 31
2; 36
2;! 82
:: 23
Q
N
I
F
N
N
3
Explanation of symbols: 1 = small larva, L = big larva, Q = queen, w = small pale worker, W = big pale worker, W = big dark worker, N = nurse, I = intermediate, F = forager.
Of the big workers the first (W), which was pale, spent rather less time on brood than the nurses, both standing still and feeding and grooming, but about the same chewing prey. She groomed but never fed a larva in the first round before she started biting. Like wl and w2, she did not bite sexual larvae in the first round but did later on. According to the table she groomed and fed adults nine times and collected a fly once. Her overall pattern of activity, with thirty-six actions in group A and only ten in group C, make it reasonable to classify her as a nurse, but she is less nurse-like than the small pale workers and evidently has a tendency to leave the young brood and explore. The second big worker, WI, was very dark and spent very little time on the brood or chewing prey near it. She was once seen feeding big larvae in the first round after biting had stopped. Her record of biting big larvae covered all three rounds and she was particularly concerned with this in the first. Four out of the six records of grooming and feeding adults were self-grooming. She never fed the queen. This worker spent a great deal of time outside exploring but was only once seen to collect food (a fly). Most of her time standing away from the brood seems to have been spent guarding the others, for she adopted a position facing away from the brood zone towards the nest entrance. She is a typical forager.
The third big worker was also dark (W2) but spent more time on the brood and chewing prey than Wl. Nevertheless, she was never seen to feed small larvae. Like WI, she bit big larvae a lot in all three rounds and she spent a lot of time on guard. In the end she had more records of behaviour under group C than under group A but because she spent so much time with the brood she is classed as an intermediate. Quite probably she was changing from nursing to foraging behaviour but it is possible that Wl interfered when she started exploring though this was never seen. Hence, in this culture there were three nurses (all pale and one big), one intermediate (dark and big) and one forager (dark and big). The activities of the whole culture, summed and expressed as percentages, are given on the right of Table I. It is important at present to note that both nurses and foragers both fed and groomed the big sexual larvae as well as biting them. There was a time trend in this however that will be described shortly. Comparisons of Four Cuhres Data for all individuals of four cultures comprising in all four queens and seventeen workers are summarized in Table II ; this includes the one just described in detail (culture 3). Only the three main groups of activity are shown but group B has been given in more detail to
882
ANIMAL
BEHAVIOUR,
22,
4
Table II. All Individuals Showing Their PhysicalCharacteristicpand Caste,the Freqwney of Activities in Grops, A B and C andtheFrequencyWi~WhichTbeyWereSeentoFeedsndGroom(Bl)orBite(B2)~~e
Frequencyof activity Code
Culture
A
B
C
8
:
56
1:
8
21
:;20
:
wl W
w2
wl
i 3
i 1
w2
Bl
2
NC 28 11
B2
0
0
11 2
*l-8 9.8
04
:2
49
12
:
49
0
4
ii 25
:i 19
2 2 7
5: 13 6.3
2' 4
3" 3
10 l?
;:z
2'6
44
w"
:
W W
;
E 25 31
:
::
;::
:2 0 1
W
t
27
20
20
1.4
z
3
$2 w2
3
1
21 20 11
21 17 18
:: 19
AZ4 0.58
:
1: 3
Wl
:
11
22
2
0.46
5
:
:
; 7
2: 19
ET
0.38 0.19 0.17
: 3
13 7
Zl W
:t
Worker type assigned -
Nurse
:
Intermediate
Forager
+Q died.
show the individual’s behaviour towards sexual larvae. Queens varied somewhat: three spent nearly all their time on the brood; another that died after only 8 days wandered out occasionally. The three normal queens form a homogeneous group (by ~2, P > O-05). The workers have been classified as nurses, intermediates and foragers on a basis of the relative frequency of actions in groups A and C. The distribution of this ratio, on a logarithmic base for compactness, is shown in Table VIII. It has no breaks in its whole range from 50 to O-17 and provides no basis for a natural classification. This is not surprising, for Ehrhardt (1931) has shown that age changes nurses into foragers. The distinction made between nurses, intermediates and foragers is therefore somewhat arbitrary. Moreover, both the nurses and the foragers are, as far as the relative frequency of activities A : B : C are concerned, internally heterogeneous (by ~2, P < @OS). Curiously enough, the only category that is homogeneous in this sense is that of the intermediates (by ~2, P 0.2 to 0.3) but sub-groups of nurses, the first three and the last four listed in Table II, are internally homogeneous. However, the categories used are certainly distinct in their values of A: B : C,
for the last four nurses, if summed and compared with the intermediates, give a high value of ~2 (P < 0401), as do the intermediates and foragers compared (P < 0401). Curiously, the least difference exists between queens and the top three nurses, which give a ~2 with P = 0.02. Seven out of nine nurses were small and eight out of nine were pale, but one small dark worker, though nurse-like in behaviour, spent much less time with small larvae than the average. One small pale worker was even less associated with small larvae. The intermediate types were all big and three were dark. The foragers were all dark and three out of four were big. The one with most outside experience was, however, small and dark. Activities of group B were shown rather less often by queens and nurses than by intermediates and foragers but this varied a lot. After classifying the workers, an average for each type and for queens can be calculated (Table III). This shows that the average queen spends over half her time motionless on the brood, whilst the average nurse spends about one-third of her time this way. A nurse, though she chews prey about as often as a queen, feeds and grooms small larvae more often. A forager does very little nursing but spends quite a lot
BRIAN: BROOD REARING BEHAVIOUR IN THE ANT
883
Table III. The Percentageof Time Spentin the Nine Main Activiti~ by the AverageQueen,Nurse,Intermediate and Forager, and their Rank
Activity group A B C
Queen Description of activity (2) (1) Groom Stand onand brood feed 1 (3) Chew prey
{;j ;rF
and feed L
Nurse
Intermediate % rank
Forager % rank
%
rank
%
rank
::52
:
30 ::
1.5 2.5
:s8
73.5 2
2 8
; 6
4 8 8
i.5 4.5
1; 11
;:: 5
1: 9
i 5
2
3
(3) droom and feed adults
ii
E.5 5
(1) Stand off brood (2) Explore (3) Collect
7
4
‘7
7
20
ii.5
22
2
21
78.5
2
69
1:
6
25 11
:
of time chewing prey; about half as much as nurses. Activities off the brood account for only 10 to 14 per cent of a nurse’s time, 37 per cent of an intermediate’s time and 58 per cent of a forager’s time. The average forager seems to spend 36 per cent of its time exploring and collecting and nearly 22 per cent guarding the nest entrance. Its only other major activity is biting big sexual larvae. The time spent doing this declines as follows : forager-intermediatenurse-queen; the last rarely bites them. Feeding and grooming big larvae is not, on the other hand, related to worker type, nor is feeding and grooming adults. Ranking these activities in order of frequency helps in the comparison. In particular, it shows a striking difference between intermediates and foragers in the rank position of exploratory behaviour (C2): last equal in the former and first in the latter. On the other hand both categories rank very high as regards standing off brood (Cl). These four sets of ranks can be shown to lack concordance, using Kendall’s test ( W = 0.301, P near 0.3). Individual comparisons show no rank correlation between worker types, using Kendall’s T-test: between nurses and intermediates P = 0.24 and between intermediates and foragers P = 0.31. Only queens and nurses show significent rank correlation (T = 0.63, P = O-012), which recalls the near-homogeneity of A : B : C, using the ~2 test. There is evidently more behavioural resemblance between the morphologicallydistinct female castes than between any set of workers. Behaviour Towards Big Larvae Biting. The decline in biting tendency from foragers through intermediates and nurses to
queens has been noted. There is also a time effect in the culture described (number 3), whereas the foragers and the intermediates bit larvae in the first round, the nurses did not join in until the second and third rounds. This is true of all four cultures: whereas only five out of nine nurses bit larvae during the first round, seven out of eight foragers did so; nurses became more hostile in later rounds. Nurses are of course very preoccupied with feeding small larvae at first, whereas the intermediates and foragers have spare time as food is very easy to obtain. However, competition for biting space on these larvae is undoubtedly real and tends to favour the bigger, stronger, more aggressive workers. Two big dark workers were particularly and consistently aggressive and could be seen biting big larvae on the fringe of the brood group for hours at a time and were clearly making it difficult for smaller, younger workers to attack systematically. Table IV illustrates a typical time sequence: cultures three and four have been added together on the basis of worker type, and the frequency of biting and of feeding have been set out (in 2-day periods) over the whole 44 days during which three rounds of big larvae were supplied. Notice again that the nurses did not bite in the first round but that the intermediates and foragers bit in all three. Biting started after 8 days in the first round and after only 4 days in the other two rounds; this is probably because the workers were still recovering from hibernation when the experiment was set up. Feeding. Feeding these big larvae is certainly not the preoccupation of nurses in the same way that feeding small larvae is. In fact, intermediates and foragers feed them slightly more than nurses do. Feeding seems to go on in rather a desultory
884
ANIMAL
BEHAVIOUR,
22,
TaMeIV.TheFreqneacywithwhiehPeedi4gand~~of~~WasRecordedinthe~o~3an84.~ After Group@ Into Queens, Nurses, Intermediat~~~~~ Rods
Queens 2-day classes
Feed
Feed
of J3ig Larvae Were Made AvaiJable to Intermediates and Foragers
NUlWS
Bite
4
Bite
Feed
Days on which L added
Bite
o-2 -4
First L
-6
1
-
2
-8
2
-
1
-10
1
-
-12
3
-
1
-
3 11
1
3
-14
5
-
-16
2
-
1
-
-18
1
-
-20 -22
1
-24
-
-26
-
Fresh L
3
-
12
5
-
4
-28 -30 -32
-
-34 -36
Fresh L -
-38
4
-40
2
-42 -44
way before and after the period of biting but never during its peak. This is not altogether surprising as it would be difficult to feed a larva that was being attacked. These periods of attack last 5 to 6 days and then fade. Some larvae succeed in growing into queens but more mature slowly and metamorphose at a smaller sire, forming workers. At the moment there is no clue as to why some succeed and others fail.
1
Queens Present and Absent In one culture already described the queen died on the eighth day. A striking change in worker behaviour towards big larvae soon followed. Thus, whereas they were actively biting larvae on days 2 and 3, they were feeding and grooming them on days 6 and 7. In this, all four workers were involved.
BRIAN:
BROOD
REARING
BEHAVIOUR
To pursue this further and see what effect queen status had on the activities of the various worker types, two cultures were set up for observation and a queen was switched from one to the other every 7 days. The whole trial was run for 4 weeks, giving each culture two with and two without the queen. There were four workers, chosen to span a range of sizes and colours, and three big and three small larvae
IN THE ANT
885
in each observation nest. All the adults were warmed for 10 days beforehand. Twenty sample observations were taken each week, giving eighty in all, forty with and forty without the queen. The activities have been summarized in the same way as before and collected in Tables V and VI. This time, each of the eight workers has a record of its actions during the period with the queen and during a period with-
Table V. Culture X: Summary of the Activities of Four Workers with a Queen on Alternate Weeks (Weeks 1 and 3 witb, 2 and 4 without). Worker a, Small and PakKoloured; Worker b, Small and Medhun-Coloured; Worker c, Bii and MedhmColoured; Worker d, Big and Median-Coloured Worker individual Class of activity A B C
Description activity
of
(1) (2) (3) {;]
Stand on brood Groom and Feed 1 Chew prey gy?andfeedL
(3) (1) (2) (3)
Grroom and feed adults Stand off brood Explore Collect
SllmA
B C Characterization Explanation
Sum
Q
+Q “-a
3: 4 f 2 0
127 x 1
x 35 ?I
of worker:
4 I 3 4
-
ii
1 N
+Q b-Q
+Q ‘-0
+Q d-O
+Q
-Q
14
7
23
12
28
4
15
27
80
45
:
i!l
;
;: 6 0
1: 5 6
:, 1
17 2
: 0
54 1:
32 15
:: I
1: 23
0” 0
ii
31
:
i
;
zi
23 13 4 N
9 17 12 I
b 0 16
4 1
ii
1: 1 24
10 0 31
ii
124 I
13 10 I
: N
3 N
of symbols: N = nurse, I = intermediate,
1; 1
1: 2
20
:i
98
I52 N
26
::
F = forager.
Table VI. Culture Y: Sumnuuy of the Activities of Four Workers with a Queen on Alternate Weeks (Weeks 2 and 4 with, 1 and 3 without). Worker e, Small and Pale; Worker f, Small and Medium-Coloured; Worker g, Bii and Dark Coloured; Worker h, Bii and Medhun-coloured. Worker individual Class of activity A B
C SumA
Description of activity
Q
(1) (2) (3) (1)
Stand on brood Groom and feed 1 Chew prey Groom and feed L
29 1:
(2) (3) Bite GroomL and feed adults (1) Explore (2) Stand off brood (3) Collect B C
Characterization Explanation
of worker:
of symbols:
:
+Q f-Q
+Q
0
7 8
10 3 7 12
4 3 6 i
2 17
?
10 4
2”
5
x 0 39 tl
s 0
i!l 0 20 14 1 N
N = nurse,
+Qe-Q
ii 2 N
I = intermediate,
i
SUm
L?
-Q
+Q
h-Q
+Q
-Q
2 :
x
:.
:;
3 19
18 :‘o
20 10 15 58
:
15
19”
2; 2 49 62 34
2: 1 45 17 31
4 1 1 loa
10
4 2
6”
2
Y
46
: 0 13 16 4
: 0 2;
182 0 6 2
163 1 6 s
: 2 14 12 8
0 ii ;:
N
I
F
F
I
I
6
F = forager.
5
886
ANIMAL
BEHAVIOUR,
out her; thus, any change in its behaviour due to the queen is apparent. The queen fed on prey more in culture Y than in culture X but showed no other major differences. No explanation can be offered for this except that Y seems to have chewed prey more in general than the first; this might have been because it had a devoted forager. The effect of the queen on the culture as a whole can now be considered. In X the workers were particularly sedentary and the queen reduced the time spent standing on the brood very substantially; Y workers were more active and the queen had no effect. In both cultures the queen increased slightly the time workers spent feeding small larvae and chewing prey. She reduced the time they spent feeding and grooming big larvae to one-third of its value in the queenless group; intensive attack was substituted. Inter change between adults rose in X when the queen was added but fell slightly in Y; this is, perhaps, again due to her greater activating effect on the X workers. She showed no appreciable influence on the time spent standing away from the brood, foraging or simply exploring. To summarize, the queen had her greatest effect on the attitude of workers towards big sexual larvae, inducing attack and reducing feeding. She only had a small effect on the activity and attention paid to small larvae, increasing it slightly. In one culture she reduced the time for which the workers stood on the brood and increased the amount of mutual interchange. The behaviour of each worker can be described individually. a. Small and pale, proved as expected to have strong nursing tendencies. She spent less time standing on the brood when the queen was added and more time feeding and grooming small larvae and adults; she also bit big larvae a little. b. Small, but a little darker-coloured, turned out to be intermediate between nurse and forager. Like a, she spent less time standing on brood when the queen was present and more time grooming and feeding adults and biting big larvae but unlike a she spent very little time at all feeding and grooming small larvae or chewing prey. e. A big and medium-coloured worker, apparently became less nurse-like when the queen was in the culture; she left the brood and explored outside and bit big larvae. However, she was never an active nurse and merely
22,
4
stood passively on larvae so that the queen substituted activity off the brood for inactivity on it. d. Also big and medium-coloured, behaved as a nurse both with and without the queen. She was like a in many ways but showed a very strong reaction to big larvae. e. Small and pale, was a normal nurse. When the queen was added she switched from standing on brood and feeding big larvae to attacking them. f: Small but darker than e, was rather unbiased behaviourally. With a queen she chewed prey more and foraged less and associated with small larvae more though she never fed them. She also fed big larvae less and bit them a little. g. Big and dark, was a typical forager. Though she fed big larvae regularly in queenless conditions she bit them continually otherwise. h. Big and medium-coloured, was an intermediate. She, too, fed big larvae when the queen was absent but did not attack them as wholeheartedly as g or e when the queen was present, though she fed small larvae more. In these cultures, during periods when the queen was present, all the workers bit big larvae, and six out of eight fed them as well; remarkable ambivalence! The frequency of feeding was, however, much less than when the queen was absent; then seven out of eight workers delivered food often. To look for time trends, all the weekly sequences of twenty observations have been summed term by term after separating those periods with queens from those without. This is quite legitimate, for fresh big larvae were given each week at the start of a new series. The results (Table VII), with observations Table VII. Trends in Biting and Feeding Freqmcy of SemalLarvaebyworkerswltb or without a Queen. FourSeziesofTwentyObsemationswithaQueemand FourwitboutHaveBeenSammd.FreshSexnalLmvae WereGivenattbeStartofBachSerltw
Observation sequence
With a queen Feeds
Bites
Without a queen:
F&S
l-4
6
2
3
5-8
2
11
6
9-12
2
19
9
13-16
3
22
7
17-U)
0
22
13
887
BRIAN: BROOD REARING BEHAVIOUR IN THE ANT
(A/C > O-5 < 2.0). The system seems to work well in spite of the fact that the frequency of the ratio shows no natural break and some of the classes are heterogeneous. Moreover, there is a point of interest about the distribution that should be noted though its significance is not clear. On a logarithmic base it is symmetric with a mode at A/C = 2 (Table VIII). It is thus almost exactly bisected into thirteen nurses on one side and twelve other categories on the other side. This is a coincidence, and since workers were not taken at random too much weight should not be attached to it. However, it might mean that the nurses represent a young age group and the rest an older one; the nurses may thus change with time into both intermediates and foragers. In winter the worker population is composed very largely of two age groups: those from the previous summer overwintering for the first time and older ones overwintering for the second time (Brian 1951, 1972). If the two groups are compared for pigmentation (Table IX) it is clear that the nurses are paler than the others (by the x* test for homogeneity P < O-01). As it is well known that workers darken with time they are almost certainly, as would be expected, younger. There is also a less well-marked size difference (by x* P = 0.03); a possible explanation of this is discussed in the next section.
grouped into fours, show that trends exist: thus, with queens the time spent feeding big larvae declines and biting increases, without queens feeding frequency rises. Worker Sii and Colour The behavioural basis of worker classification has already been explained and justified. Those that spend more than twice as much time with brood than elsewhere (A/C > 2) have been classed as nurses. Others have been classed as foragers, (A/C < 0.5) and intermediates, Table VIII. The Frequency Diibution Twenty-Five Workers on a Log&se
Ratio on/off brood behaviour (A/C) FrequencyClasses to 0.125
Frequency distribution of all 25 workers 2
0.25 too-5
3 1
to 1
2
Scale
for
Worker type
0
o-125 to o-25
0.5
of A/C
F
3-l
1 to2 2
to4
5-l
4
to8
3
8
to16
2
Discussion The theory that the worker population is divided into pro- and anti-queen factions, that the latter gain power as the colony grows and the queens’ influence weakens and that as a consequence associate and replacement queens arise, is not supported by these results. Big workers produced as the colony grows in size, though truly precursors of new queens in the population and
16 to32 32 to64
64 to 128 SUm
2 I
OJ 25
Explanation of symbols: N = nurse, I = intermediates, F = foragers.
Table TX. Two Rebaviour-Based Classes of Workers (Nurses and others) Aaalysed in Respect of Size and Coloration. All Twenty-Five Workers Have Been Included NUlXS
Coloration intensity
Foragers and intermediates
Small
Big
SUm
Small
Big
SUm
Total
Pale
8
2
10
0
1
1
11
Medium
0
2
2
2
1
3
5
Dark
1
0
1
1
7
8
9
Sum
9
4
13
3
9
12
25
888
ANIMAL
BEHAVIOUR,
though they must improve the general nutritional status, are not themselves instruments of newqueen production. Indeed, the reverse is the case, for as long as queens are present, these big workers are the first and most persistent attackers of sex-potential larvae. Instead of this population control over sex production there is control at the individual level. All workers are switched by queens from nourishing sexual larvae on protein to starving them of it (thus reducing their size) and biting them (thus advancing their metamorphosis). In this process the bigger, older foragers appear to play a more important part than the smaller, younger nurses. With ample and effective queens they attack sexual larvae vigorously; if without, they help the nurses feed them on undiluted prey, an attention they rarely bestow on small, non-sexual larvae; they are more responsive to sexual larvae than are the workers. This study has also yielded information about the way work is apportioned. This species has been investigated by Ehrhardt (1931) who found that pale young workers were nurses and that they changed into foragers as they darkened and aged; they are pre-adapted to daylight exposure, Weir (1958a, b) confirmed this with the species Myrmica scabrinodis Nylander and Myrmica ruginodis Nylander. In the former species he distinguished six degrees of melanization and found that the darker ones were more easily drawn away from the brood than the paler ones. The latter (nurses) would leave the brood after the dark ones had been taken away but otherwise they stayed close to it. In fact, Brian (1956) found that a proportion of workers, presumably nurses, would struggle towards the brood even when worker density on it was high. If dark foragers are withdrawn some of the nurses move off, presumably in search of food which is normally placed on the periphery by foragers. By testing the nest-building skill of the colour classes Weir found that a group that spent a lot of time standing near but not on the brood were most skilful, and he called them domestics and regarded them as a mobile reserve of foragers. The intermediates identified in these studies seem to correspond very well behaviourally with these domestics. That nurses have a tendency to be smaller than foragers is interesting in view of the fact that Myrmica rubra is undoubtedly a monomorphic species. Weir (1958a, b) found exactly the same in Myrmica scabrinodis but not in the sub-species microgyna of M. ruginodis. Ehrhardt
22,
4
(1931) does not appear to have noticed this in M. rubra though it was conspicuous in the dimorphic Messor. It is also true of Oecophylla,
as Ledoux has shown (1949), but it is not a general rule in ants, for the nurses are larger than foragers in some species of Pheidole (Sudd 1967). Small size would appear to be an advantage to nurses. It brings them down to the scale of their larvae and enables more to be packed into the confined nest spaces; however, large size may not be an advantage to foragers, particularly if they have evolved an effective system of co-operative hunting. If smaller workers changed behaviourally more slowly than bigger ones they might create a population in which nurses were smaller on average than others. They may come from different broods, too. Weir suggested that the small pale workers of M. scabrinodis which were the nurses in spring were rapid brood of the previous summer (the life-cycle is described in Brian 195 1). Medium-coloured workers would then have been formed earlier in the summer from hibernated larvae and the darkest workers would have overwintered twice. This is consistent with what is known of worker longevity (Brian 1951, 1972). Curiously enough, the brood from eggs in one season dies 2 years afterwards, whether it becomes adult in the same season (rapid) or in the next. Thus rapid brood spends a bigger proportion of its life in the adult stage than the brood that hibernates in the larval stage. Larvae age as quickly as the adults do. This might imply slower behavioural change in the small workers formed rapidly and so add to the size effect already suggested. These small workers are formed from larvae that are switched relatively early in their development from the queen-style of growth and development. Larger workers are formed from brood that has followed the queen-style further, hibernated, and even then failed to get the necessary food for growth, either because this is just not available or because it is withheld by workers under the influence of queens. However, though these two ways of producing workers together give a unimodal size frequency distribution, each component in fact follows slightly different ontogenetic routes. These could cause behavioural differences: a worker that was a ‘failed’ queen might tend to forage and a precocious worker to nurse. It would be interesting to enquire whether any of the control systems known to exist in Myrmica could
BRIAN: BROOD REARING BEHAVIOUR IN THE ANT
regulate the ratio nurse-forager efficiently by varying the ratio of rapid-retarded brood. REFERENCES Brian, M. V. (1951). Summer population changes in colonies of the ant Myrmica. Physiologia camp. Oecol., 2, 248-262. Brian, M. V. (1956). Group form and causesof working inefficiencyin the ant Myrmica rubra L. Physiol. Zod., 29, 173-194. Brian, M. V. (1972).Population turnover in wild colonies of the ant Myrmica. In: Proceedings of ZBTIPT Working Group on Social Znsects meeting, Warsaw, June 1970, Ekol. Pofska, 20,43-53.
Brian, M. V. (1973a). Feeding and growth in the ant Myrmica. J. Anim. Ecol., 42, 37-53.
889
Brian, M. V. (1973b). Caste control through worker attack in the ant Myrmica. Znsectes sot., 20, 87-102. Ehrhardt, S. (1931). tfber Arbeitsteil bei Myrmicaturd Messor-Arten. 2. Morph. Y kol. Tiere, 20, 755-812. Ledoux, A. (1949).Recherchesur la biologle de la fourmi tileuse (Oecophyllo Iongitwda Latr.). In: Theses p&sent&s a la Faculte des Sciencesde l’Univemit& de Paris,p. 461. Sudd, J. H (1967) An Introduction to the Behaviour of Ants p. 200. London: Edward Arnold. Weir, J. S. (1958a). Polyethism in workers of the ant Myrmica. Part I. Znsectessot,, 5,97-128. Weir, J. S. (1958b). Polyethism in workers of the ant Myrmica. Part II. Znsectes sot., 5, 315-339. (Received 14 December 1973; revised 4 March MS.
number: 1284)
1974;