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Bionomics of the rainbow lizard Agama agama (L.) in eastern Nigeria during the dry season
Journal of Arid Environments (1981) 4, 235-245
Bionomics of the rainbow lizard Agama agama (L.) in eastern Nigeria during the dry season
J.
L. Cloudsley-Thompson* Accepted 9 March 1981
The distribution, population structure and behaviour of agamid : lizards at Nsukka during January and early February 1981 are described. The animals were almost always found near buildings, trees, rubble and fallen logs etc.: they tended to remain in the same place day after day. Territorial behaviour was most marked in adult males, but individuals of all sizes displayed by 'nodding'. Mating is described. The animals roosted at night in trees and shrubs and on buildings, Activity was greatly influenced by weather. Escape from enemies is described, and it is suggested that, in addition to indicating 'social space', 'nodding' may act as a protean anti-predator strategy. These lizards are omnivorous.
Introduction The observations described below were made on the campus of the University of Nigeria, Nsukka, throughout January and early February 1981 and supplement those of Harris (1963, 1964) who has made an important pioneer study of the rainbow lizard. During most of the time, while the harmattans was blowing, day temperatures averaged about 30°C and the relative humidity fell as low as 10 per cent. Towards the end of the period, however, temperatures and humidities began to increase somewhat, but this did not appear greatly to affect the behaviour of the rainbow lizards (Agama agama (L.), Lacertilia: Agamidae), the objects of investigation, except in so far as fewer females and juveniles were sighted when counts were made while the sun was exceptionally hot. At this time of year, during the dry season, the grass was brown and the soil baked hard by the sun. Few animals were evident, apart from agamid lizards and birds-mainly hooded vultures. The lizards were obviously not distributed evenly throughout the University campus. In some places-especially near buildings and cement-lined drainage ditches--they were common, whereas in open grassland away from trees they were not to be found at all. Even within densely populated habitats, the distribution of the various individuals appeared to remain constant. At the same time, the population structures within these habitats appeared to vary consistently. Some contained mainly adults and large juveniles; in others, smaller juveniles predominated. The observations described below were made in order to elucidate these points.
Methods Daily inspections were made in selected environments: the quadrangle of the Continuing Education Centre (CEC) and the Zoological Gardens of the Department of Zoology (Zoo).
* Department of Zoology, Birkbeck College (University of London), Malet Street, London WCIE 7HX, England. t A seasonal, dust-laden, wind from the Sahara occurring when the north-east trades dominate the area. 014-0-1963/81/030235 + 13 $02.00/0
©
1981 Academic Press Inc. (London) Limited
J. L. CLOUDSLEY-THOMPSON
236
For census purposes, these were both arbitrarily divided into smaller areas within which the numbers of lizards were counted. The order in which the various areas were visited was altered arbitrarily from day to day so that if any lizards were inadvertently driven from one to another and therefore counted twice, this would not bias the results. Numbers of lizards on or at the base of the wall at the west end of Eyoita Hall of Residence were also counted daily. Although adult males in full reproductive coloration and with developed gular folds were clearly recognizable, it was not always possible to distinguish with certainty between immature males and adult females (Harris, 1963, 1964). On the daily counts, therefore, only three categories of lizard were recognized: (a) males in the reproductive phase (6'), (b) females and immature adult males (~) and, (c) juveniles, small females and young of all sizes (juv). Certainly more than half the animals recorded as ~ were, in fact, immature adult males, which began to develop orange-coloured heads and black tips to the tail towards the end of january. If, therefore, the sexes were approximately equal in numbers, some of the larger 'juveniles' must, in fact, have been small females. Total values obtained, therefore, probably somewhat underestimate the ratio of adults to juveniles. Unfortunately, several lizards were collected in the Zoo by members of the Staff of the Department of Zoology for parasitological research and class experiments before the counts had been made on 7,8,9 and 16 January, a total of about 75 individuals of all categories being Croton brushes
Croton brushes
Ditch
i' ....._~ ~ <..,
J"
,,,,,,,,,--
... a.
:! en
Frangipani bushes
iV~?':'~i:r;'rZ;(~j!(%'i~; . . Oleander bushes
Ditch 10 m
Figure 1. Sketch map toshow main basking places, roosting sites and refuges (broken lines) of mature males, female arid juvenile A. agama in the quadrangle of the Continuing Education Centre.
BIONOMICS OF THE RAINBOW LIZARD
237
taken. On those days, unusually low numbers of sightings were recorded. Although the total area of the Zoo was some 20,000 m 2 , and the area surveyed amounted to only 6500 m 2 , the lizards were invariably shy and in hiding everywhere for an hour or two after being hunted. Fewer lizards were sighted on days when the sky was cloudy or the sun obscured by harmattan dust. For example, on 20 January, between 12.00-12.30 h, only 4 0', 5 ~, 22 juv lizards were sighted in the Zoo study areas and 4 0', 1 ~, 3 juv in the CEC quadrangle. The figures for the following day, while the sun was shining, were 7 0', 9 '12, 46 juv and 5 0', 4 ~, 11 juv respectively. Again, fewer sightings were made early in the afternoons on days when the sun was especially hot. On 31 January at 14.15 h, for instance, only 3 0', 2~, 4 juv were recorded in the CEC quadrangle. Distribution
Rainbow lizards appeared almost invariably to live near buildings, cement-lined drains, brick rubble, fallen logs and heaps of leaves. The majority sighted in the Zoo, for example, were seen near the Empty Cage, the south wall of the Monkey House (until 16 January when a number of them must have been caught) and the Central Area (near the Hyena House, Shed and Experimental Animals House) (Fig. 1). Numbers sighted in other parts of the Zoo study area were extremely small (Table 1). Even within the Monkey House and Empty Cage, where the counts were made, the lizards appeared to restrict themselves roughly-tothe same areas, day after day (Table 2). The differences between the numbers in the three sections into both of which these buildings were arbitrarily divided are statistically significant (X 2 test, P > 0·05; P > 0,01), indicating permanent differences in the population sizes. Furthermore, the majority of juveniles sighted in the vicinity of the Empty Cage were nearly full grown, whereas those on the south wall of the Monkey House and within the Central Area were mostly of the smallest size range. Ratios of the three classes of lizards in the CEC quadrangle, Zoo and end wall of Eyoita Hall were also significantly different (X 2 test, P > 0·001). Table 1. Mean (n = 35) and maximum sightings of A. agama in different localities and calculated total population in the areas studied. Further explanation in the text Male
Female
Juvenile
mean max
4·9 6
4·6 8
8·2 13
mean max mean max mean max mean max mean max mean max
0·5 2 3·2 7
0·2 1 6·0
5·6 14 7·6 19 18·6 38 3'7 12 35'3 58 15·0 24
Locality CEC Zoo Monkey House Empty Cage Central Area Elsewhere Zoo totals Eyoita Hall Calculated total population in study areas Calculated mean density per ha
1-6
11
2·8 9 0·3
5 0·5 3 5·8 12 1'3 2
9·2 18 4'3 12
27
65
260
32
78
313
3
r. L. CLOUDSLEY-THOMPSON
238
Table 2. Mean (n = 35) and maximum sightings of A. agama on different sections of the south wall of the Monkey House and in the Empty Cage of the Zoo Monkey House West End ~
mean max
5f
1
Central Area
East End
juv
~
5f
juv
~
5f
juv
0·3 9
1
1
4
0·1
0·3 1
1
4
1·9
Empty Cage Central Area
West End
mean max
~
5f
juv
~
5f
1·0 3
2·1 6
3·3 9
0'7 3
1·6 5
East End juv 1·2
4
~
5f
juv
1·5 3
2·2 6
3·1 10
Territorial behaviour was most marked among males in the reproductive colour phase. In Figs 1 and 2 are shown the positions most often taken up by such males in the CEC quadrangle and the Zoo study area. The roosting places of females and some juveniles are also indicated in Fig. 1. Immature males, females and juveniles were often to be found in the same areas day after day-indeed, it appeared that all individuals were to some extent territorial. At the same time, they all displayed by 'nodding', and this may assist in maintaining a 'social space' around individual lizards. Other explanations of the behaviour pattern will be discussed later.
Population structure The population structure appeared to vary in different places. When the means of the sightings in the CEC quadrangle, the study area of the Zoological Gardens and the end wall of Eyoita Hall were compared (Table 1), it was found that the ratios of adult to juvenile lizards in the CEC quadrangle, the Empty Cage at the Zoo and the wall of Eyoita Hall were higher than elsewhere. If it is assumed that the ratios in the sightings were proportional to the total populations in these areas, the significantly larger number of juveniles in the Central Area of the Zoo may have been related to the extra cover available there, especially in the piles of logs and heaps of dead leaves-which would have afforded shelter from predatory enemies such as kites, pied crows, vultures and so on. Indeed, lizards of the smallest size range (c. 60 mm) were only found in quantity in the Central Area of the Zoo. As already mentioned, it was often impossible to distinguish, in the field, between adult females and males not in breeding coloration. In the CEC quadrangle, however, I learned to recognize every adult lizard individually, because these were more accustomed to people and, consequently, relatively tame. Here there appeared to be a total of six males in reproductive colours, two females and six immature males. Towards the end of the period of observation, some of the immature males began to develop full reproductive colouring. One did so on 28 January, another on 30 January and two more during the first week of February. Nevertheless, I continued to count them as 'imrnatures' in order not to upset the calculations. No doubt some of the larger juveniles would have matured into adult females about the same time, but this could only have been determined by dissection as the coloration of females and juveniles is identical (Harris, 1964). On 28 January, a record of seven adult males was
BIONOMICS OF THE RAINBOW LIZARD
I Monkeys 00
8
239
,0
G o
Boboons
o ~
I
0
0 4> C VI 4> ::J >,0
II
E
o
III
G ,.
G
G 0
(1
~ 6
Kiosk
Figure 2. Sketch map of the Zoological Gardens study area.
observed in the Empty Cage of the Zoo. Previously the greatest number recorded on any one occasion had been five (on 20 January). It therefore seems probable that here, too, some of the immature males had developed rainbow colours. Total numbers It was not possible to assess total population numbers with any high degree of accuracy. After a week or two, I was able to recognize many of the individual males in the reproductive phase by their colour variations and by the fact that they were to be seen in the same place day after day. Until the end of January, when some of the immature males began to adopt rainbow coloration, there were seven adult males in the Empty Cage of the Zoo, two on the wall of the Monkey House (until 16 January when one of them was almost certainly captured), six in the Central Area and three others-a total of 18 in approx. 6500 m 2 (Fig. 1). The CEC quadrangle housed six males in approx. 1600 m 2 (Fig. 2) and the west end of Eyoita Hall, three on approx. 210 m 2 of wall space. Some idea of the total numbers of females, immature males and juveniles can be obtained from the fact that the mean number of individual sightings recorded on or in the Empty Cage of the Zoo was 13,6, whereas at 17.15 h on 12 January I was able to count 33 individuals roosting on the top of the wall-the maximum recorded there at anyone time. This would give a ratio of mean sightings to total numbers of 1 to 2·4. If this ratio was the same in the various study areas, the total number of agamid lizards involved in the survey would have been about 27 males, 65 females, 260 juveniles.
240
J. L. CLOUDSLEY-THOMPSON Behaviour Territorial display and aggression
As Harris (1964) so clearly indicated, A. agama, like other agamids, is a territorial species. The sexual dimorphic coloration of dominant males becomes more brilliant in the breeding season (Carpenter, 1967; Harris, 1964). Individual males in breeding coloration tend to occupy one or two preferred places within a comparatively restricted range where they display themselves, nodding conspicuously. All individuals have the habit of nodding to some extent. but adult males also 'bob'-that is, they nod extremely vigorously, at the same time bending their forelegs as they do so and thus increasing the display (Harris, 1964). If an immature male or female encroaches upon the social space of a cock or rainbow male, the latter either chases it away or nods with extra special vigour, displaying its gular fold. Should this not be sufficient to persuade its rival to leave, the dominant male will move sideways towards it, with a -series of rapid jumps. Any individual, other than another cock male in rainbow coloration, then departs. Sometimes two rainbow males will rest alongside one another as though sizing each other up. They may then display and, if neither gives way, a brief fight ensues in which the two contestants lash each other with their tails .and even struggle briefly. Many of the smaller of the immature male lizards in the CEC quadrangle appeared to have lost the tips of their tails, perhaps in territorial disputes. On one occasion, in the Zoo, I watched a male in breeding coloration jump onto a breeze-block on which a large female (or immature male) was sunning itself. The rainbow male then lashed out once vigorously with its tail, and the other fled immediately from the breeze-block. Adult males did not usually bother to display to juveniles, but merely chased them off. As mentioned above, all rainbow lizards, including the smallest juveniles seen, would display by nodding. This is such a characteristic trait and makes the animals so conspicuous that it is difficult to believe that it can have no function whatsoever. I gained a distinct impression that even the youngest rainbow lizards tend to be solitary and that nodding may be a means of maintaining the social space around them. Harris (1964) concluded that nodding is in no way connected with territorial or reproductive behaviour, nor does it assist in judging distance since it does not take place before snapping up an insect. He thought it might serve to reveal the positions of cryptically coloured females and juveniles (an explanation somewhat similar to that which presented itself to me). The head bobbing and challenge display of cock lizards is a far more intense form of head movement. The main function of a territory for A. agama, according to Harris (1964), is to provide a mate. Heatwole (1976), on the other hand, argued that, in general, territoriality provides a mechanism whereby at least-a proportion of the population can obtain an adequate food supply, although surplus individuals die, rather than the entire population suffering the deleterious effects of inadequate energy resources. In the case of A. agama, although dominant territorial males may tolerate subordinate males within their territory and share food with them, courtship and mating appear to be the prerogative of the dominant animal (Stamps, 1977).
Reproduction
When chased by males in the reproductive phase, other adults usually ran away. Some individuals, however, presumably females, did so with their tails lifted up at an angle of about 45° from horizontal. It seemed probable that this might be a courtship response (Carpenter, 1967; Schmidt & Inger, 1957). The tail is raised in the same way during mating and the male then lies closely alongside the female with his tail pointing forwards beneath her body and his cloaca apposed to hers. The eggs are buried in sand and number not less than five; their size is about that of a large pea (Dr Margaret Anizoba, pers. comm.). Males in the reproductive colour phase are found throughout the year, but oviposition at Nsukka probably only takes placeat the time of the spring rains in April (Dr Uche Onubogu, pers. cornm.). Certainly I found no young less than about 6 cm in length from mouth to vent, and
(c)
(d)
Plate 1. Habitats of A. agama at the University of Nigeria, Nsukka. (a) The CEC quadrangle,
(b) central region of the Zoological Gardens, (c) the Monkey House, (d) the west end of Eyoita Hall of Residence.
[facing page240]
(d)
(e)
(0
Plate 2. Behaviour of A. agama at Nsukka. (a) Rainbow male and female, (b) male climbing borassus palm, (c) juvenile on log heap, (d) male sleeping in croton bush, (e) immature male and juvenile roosting in an hibiscus, (f) roosting female.
BIONOMICS OF THE RAINBOW LIZARD
241
most were considerably larger than this. Presumably they were last year's babies. Harris (1964) describes reproduction in detail. He states that clutches of five or six eggs are most common, but clutches of only three or as many as eight eggs have been found.
Nocturnal roosting
The rainbow lizards in the CEC courtyard roosted at night in various trees and shrubs. Between 17.00-18.00 h, an hour before complete darkness fell, each lizard would begin to make its way towards the tree or bush in which it habitually spent the night. (This was verified in the case of males in the reproductive colour phase, the larger females and immature males which could be recognized individually. At the same time, I gained the impression that the juvenile lizards also roosted nightly always in the same trees and shrubs. Some of these are indicated in Fig. 1.) Movement towards the roosting place was unhurried: a lizard would make a sudden dash for about a metre, stop motionless for 5 min or so, and then make another sudden movement upwards, a metre or so at a time with lengthy intermediate pauses. Finally it would scramble into the branches, or into the fibrous mass at the base of the palm fronds and, after a couple of wriggles, emerge among the leaves to remain motionless for the remainder of the night. When disturbed just before bedtime, the lizards would dart up their regular roosting tree or bush and disappear for good. Individuals that roosted on the branches of frangipani or hibiscus bushes, when they could still be seen before darkness fell, would remain wary, as far as possible keeping on the side away from the observer of the branch to which they were clinging. After nightfall, however, they were reluctant to move, even when a torch was shone directly onto them. They would occasionally allow themselves to be touched without responding but, if excessive liberties were taken in this respect, would jump onto another branch or into the foliage where they were difficult to detect. When forced to leave their roosting bush and take shelter beneath the steps of the CEC quadrangle, they would return to their perch within 10-15 min. The agamids that inhabited the Empty Cage in the Zoo appeared all to roost on the top of the wall under the eaves where their heads could be seen from the ground. Those that frequented the west wall of Eyoita Hall, on the other hand, roosted in a vertical posture, clinging to the roughcast where they were sheltered to some extent from observation by drainpipes, wide open windows, branches and so on. A few roosted against the architrave of the windows, others horizontally on the window sills. When roosting, the normal social spacing appeared to disappear and adult males in the reproductive phase could then be seen in close proximity to females and juvenile animals. Juvenile agamid lizards began to go to bed first, followed by the adult females and finally, somewhat later, by the males in breeding colours-although one female was still on the ground in the CEC courtyard for three nights running at 18.15 h, at least half an hour after all her companions had retired for the night. First to rise, around 09.15 h were the adult males, followed by the females and, finally, the young. By 10.45 h maximum sightings could be recorded. Later in the year, however, when the weather is warmer, basking begins earlier in the morning or, as I was informed, shortly after sunrise. Not only numbers of sightings but also the time of emergence appeared to he influenced by sunshine. A small colony (consisting of two males in breeding coloration and about a dozen other individuals) that occupied a sunny, sheltered site at the south-eastern corner of the CEC building was nearly always up earlier than the colony in the quadrangle. The only exceptions to this were on days such as 29 January when the wind blew strongly from the east. One male, however, sometimes continued to roost on a frangipani tree until quite late in one morning-presumably because there was little human disturbance in this locality. When they descended from their roosting places in the morning even mature males had assumed a dark, cryptic coloration and only brightened as they warmed up in the sunshine. They then began nodding and feeding. Loss of colour after nightfall took several hours; its recovery at dawn was complete within a few minutes.
242
r. L.
CLOUDSLEY-THOMPSON
Avoidance of wind and rain At 11.00 h on 25 January 4 0, 7~, 12juv were counted in the CEC quadrangle in sunshine. An hour later, the sky became overcast and cloudy, a cool breeze sprang up, and there was a light shower of rain. Long before this, however, all the lizards had vanished-indeed their disappearance almost coincided with the appearance of the rain clouds-but they had not retired to their roosting positions. They had taken to their daytime refuges. Some were beneath the steps, others at the bases of the bushes or up the fig tree arid Borassus palm. Two hours afterwards, although the sun had stilI not reappeared, 4 0, 4 ~ and 7 juv had come out and were lying pressed incredibly flat upon the cement and tiles of the lukewarm ground. In the Zoo, only 1 0, 1 ~, 2 juv and 29 roosting animals were to be seen, all on or in the Empty Cage; 1 0, 4~, 10 juv were clustered behind the drainpipe against the wall of Eyoita Hall. Presumably refuges and roosting places coincided for these individuals. The small colony at the south-eastern corner of the CEC building, mentioned above, took refuge mainly in the space beneath some large water tanks, but their roosting places were almost certainly . among the fronds of the talI Borassus palms nearby. On windy days the numbers of females, immature males and juveniles to be seen were much reduced, but adult males in reproductive coloration were less affected. For example on 29 January, eight males in reproductive coloration-the original six plus two others which had previously been immature-were to be seen in the CEC quadrangle, but only two females or immature males and two juveniles. Escape from enemies Although approachable to within 3-4 m, or even less when on the ground, A. agama is more shy after taking refuge in a tree or bush. Invariably it wilI run round to the side of the trunk or branch that cannot be seen by the observer; if two people approach simultaneously from opposite sides, the lizard will climb rapidly into the branches. The lizards in the CEC quadrangle would take refuge in any convenient bush or tree (except for the fan palm and the Phoenix palm, which none of them would climb) and did not restrict themselves to the trees or bushes in which they habitually roosted. The individuals that inhabited the eastern end of the courtyard would also take refuge in the artificial cement-lined ditch beneath the steps and in the tunnel leading beneath the verandah to the lawn on the east. These were usually the only animals to venture on the lawn-perhaps because they had a safe line of retreat: the lizards that inhabited the south-east corner often basked on the edge of the covered path, but seldom went as far as the lawn beyond. Low-level refuges were never used, however, as roosting places during the night. Although relatively tame, rainbow lizards were able to move with surprising speed when the occasion warranted it, and to jump with considerable agility from one branch to another. As mentioned above, none of them roosted or took refuge in the Phoenix palm, apparently because they could not force their way through the mass of fibres beneath the bases of the existing fronds. On one occasion a female was chased up the trunk of this palm, struggled briefly to cross the fibrous barrier, then leapt 3 m to the ground and darted into shelter beneath the north-eastern step. Females were more shy than males or juveniles. Apart from adult males in rainbow colours, A. agama is undoubtedly cryptic. Individuals on an appropriate background are most inconspicuous until they move or nod their heads. When roosting at dusk or dawn, even males in the reproductive phase become dark and are difficult to make out among leafy branches. On open ground, all individuals are alert and aware of the presence of an enemy although they nod most vigorously when one approaches. This, therefore, may be a warning signal to other members of the colony. At the same time, it may, like other types of erratic or protean behaviour, distract the attention of a predator at the critical moment, so that it misses its quarry. Feeding Rainbow lizards are omnivorous. On a number of occasions I saw them eating hibiscus and other flower petals, grass, dead leaves, bread crumbs, fragments of ground-nut, sugar and
BIONOMICS OF THE RAINBOW LIZARD
243
crushed sweets that they licked up from the ground. They also ate ants with alacrity, and would occasionally stand over the hole leading to a nest, licking up the ants one by one as they emerged. I have previously recorded them feeding on termites (Cloudsley- Thompson, 1963). Adults have occasionally been observed to feed cannibalistically on their young, but whether they also feed on geckoes (Hemidactylus brookii) has not yet been determinedalthough this seems unlikely because there is no temporal or spatial overlap between the two species. (It would be interesting if this were the case, because 10 per cent of the agamids were found to be parasitized by Pentastomida. These they might have caught from geckoes which are already known to harbour them; Dr Uche Onubogu, pers. comm.). Juveniles of many species of lizard eat relatively more animal matter than adults (Schoener, 1977).
Discussion This study was completed without my being able to consult The Life of the Rainbow Lizard (Harris, 1964): neither this essential monograph nor The Life of Reptiles (Bellairs, 1969), nor, indeed, any of the references listed in the bibliography was to be found in the Nnamdi Azikiwe Library of the University of Nigeria. Nevertheless, since I was unable to recollect either the topics covered or the conclusions reached in Harris's work, my own observations were completely unbiassed. The main differences between the conclusions reached by Harris (1964) and myself are as follows. Harris recorded an average density among buildings of 16·2 ha- 1 (40 per acre) and a territorial density of2·g ha- 1 (7 per acre). Away from buildings, in districts where the lizards were arboreal, .he recorded 56·7 ha- 1 (140 per acre) and 14·6 ha- 1 (36 per acre) respectively. In contrast, my maximum sightings suggested approximate densities of 78·3 ha- 1 and territorial densities of 11·5 ha- 1 near buildings (CEC, Eyoita Hall and the Empty Cage and Monkey House of the Zoo) and of 40 ha -1 and 15·0 ha -1 in the parts of the Zoo where trees predominated rather than buildings. In other words, territorial densities were slightly lower in arboreal regions, at Nsukka, than found to be the case in Ibadan by Harris (1964), but very much greater near buildings. Harris recorded shikra hawks as being among the main predators. There are, however, no vultures in Ibadan, although kites are plentiful, whereas hawks are scarce and hooded vultures numerous at Nsukka. Possibly vultures are less efficient predators of A. agama than are hawks and kites. The mean density for all the study areas combined was about 400 ha " ! and the territorial density 32 ha -1 (Table 1). These figures, however, are calculated maxima based on an estimation of the ratio of mean sightings to total numbers of 1 to 2,4, as assessed in the Empty Cage of the Zoo. The figures used for comparison with those of Harris (1964) were the maximum numbers recorded at one time in any of the three categories of lizard adopted, and therefore somewhat lower. Western (1974) estimated a population of 187 ± 35·3 ha- 1 on four lava outcrops in a semi-arid environment of northern Kenya. The daily pattern of life differs somewhat at Nsukka from Ibadan (Harris, 1964) and He (Halstead, 1970). It seems likely. that the differences are related to the different climatic regimes in the three places. Fighting seemed to be less common at Nsukka than in Ibadan, while it was not observed at all at He. Like me, Harris (1964) reached the conclusion that A. agama is really a tree-living species although, in rain-forest, lizards are usually to be found only on the walls of buildings. The explanation he gave was that forest is cooler than open country because the sunlight is excluded and only in clearings and along roads are the animals able to raise their body temperature by basking. The mud walls of houses also absorb a considerable amount of heat during the day and, at night, act as heat reservoirs; the lizards are not slow to enjoy this warmth. Where there are no dwellings, however, they sleep high up in trees, usually in crevices at the base of a side limb or the frond of a palm-which would be much cooler and less protected than a roost in the roof of a house. Stomach analysis showed that A. agama is primarily insectivorous at Ibadan, feeding almost entirely on ants. Large males are, however, cannibalistic. Only occasionally is vegetable matter eaten there, and then chiefly by adult males which show a preference for coloured
J. L. CLOUDS LEY-THOMPSON
244
objects. The large amount of vegetable matter eaten by the agamids at Nsukka may reflect the scarcity of insect food available during the dry season. Harris (1964) did not mention the marked avoidance of rain that I observed although throughout he lays stress on the effect of temperature on behaviour. Nor did he place so much emphasis on escape from enemies which appeared to me to be the most reasonable explanation for the differences in population structures observed. Chapman & Chapman (1964) also concluded that vegetable matter is eaten mainly in the months with least rainfall; while Marshall & Hook (1960) found that the sexual cycle in A. agama lionotus is timed not by rainfall but by the seasonal appearance of animal food that appears after the rains.
Summary Agamid lizards were studied in the campus of the University of Nigeria, Nsukka, throughout January and early February 1981. They were almost invariably found near buildings, trees, cement-lined drains, brick rubble, fallen logs and heaps of leaves. Even within these restricted localities, the animals remained in roughly the same places day after day. Territorial behaviour was most marked between adult males in reproductive coloration, but individuals of all sizes displayed by 'nodding', possibly thereby indicating their 'social spaces'. In territorial disputes, adult males displayed their gular folds, jumped sideways at their rivals and lashed with their tails. The courtship response of the female was to raise her tail. During mating, the male lies alongside the female with his tail pointing forwards beneath her body. Oviposition probably takes place at the time of the rains. Juvenile lizards of the smallest size ranges were most common where there was plenty of shelter. The animals roosted at dusk in trees and shrubs, on the walls of buildings where the texture was rough, and under the eaves. Adult males slowly become black after dark, but their colour brightens up rapidly when they begin sun basking in the morning. Activity is markedly affected by weather; wind and rain are avoided at all times. When approached too closely, the lizards took refuge near the roots of shrubs, beneath drains and in other inaccessible places. Such retreats did not necessarily coincide with the nocturnal roosting places of the individuals. Nodding may additionally function as a form of erratic or 'protean' antipredator device. Rainbow lizards are omnivorous at Nsukka, feeding on ants, termites, fallen flowers, breadcrumbs, ground nuts, sugar etc. Large individuals are also reported to be cannibalistic and to eat their own young. Thanks are due to the Inter-University Council for providing the air fare to Nigeria and for financial support under the Short-Term Visitor Scheme, to Dr Mark Eluwa, Head of the Department of Zoology, University of Nigeria, Nsukka for hospitality and accommodation, to the Academic Board of Birkbeck College (University of London) for granting me leave of absence during part of the spring term, 1981, and to Professor A. d'A. Bellairs for commenting on the manuscript.
References Bellairs, A. (1969). The Life of Reptiles. London: Weidenfeld & Nicolson. 2 vols., 590 pp. Carpenter, C. C. (1967). Aggression and social structure in iguanid lizards. In Milstead, W. W. (Ed.), Lizard Ecology. A Symposium, pp. 87-105. Columbia: University of Missouri Press. 300 pp. Chapman, B. M. & Chapman, R. F. (1964). Observations on the biology of the lizard Agama agama in Ghana. Proceedings of the Zoological Society of London, 143: 121-132. Cloudsley-Thompson, J. L. (1963). Some aspects of the fauna of the district around Lake Chad. Entomologist's Monthly Magazine, 98: 180-181. Halstead, L. B. (1970). Some observations of the rainbow lizard, Agama agama (L.), at the University of He. Nigerian Field, 25 (2): 86-89. Harris, V. A. (1963). The Anatomy of the Rainbow Lizard. Agama agama (L.). London: Hutchinson. 104 pp, C
BIONOMICS OF THE RAINBOW LIZARD
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Harris, V. A. (1964). The Life of the Rainbow Lizard. London: Hutchinson. 174 pp. Heatwole, H. (1976). Reptile Ecology. St. Lucia: University of Queensland Press. 178 pp. Marshall, A. J. & Hook, R. (1960). The breeding biology of equatorial vertebrates: reproduction of the lizard Agama agama lionotus Boulenger at Lat. OOOl'N. Proceedings of the Zoological Society of London, 134: 197-205. Schmidt, K. P. & Inger, R. F. (1957). Living Reptiles of the World. London: Hamish Hamilton. 287 pp. Schoener, T. W. (1977). Competition and the niche. In Gans, C. & Tinkle, D. W. (Eds), Biology of the Reptilia. Vol. 7, Ecology and Behaviour A, pp. 35-136. London: Academic Press. 736 pp. Stamps, J. A. (1977). Social behaviour and spacing patterns in lizards. In Gans, C. & Tinkle, D. W. (Eds), Biology of the Reptilia. Vol. 7, Ecology and Behaviour A, pp. 265-334. London: Academic Press. 736 pp. Western, D. (1974). The distribution, density and biomass densities of lizards in a semi-arid environment of northern Kenya. East African Wildlife Journal, 12: 49-62.
Bionomics of the rainbow lizard Agama agama (L.) in eastern Nigeria during the dry season
J.
L. Cloudsley-Thompson* Accepted 9 March 1981
The distribution, population structure and behaviour of agamid : lizards at Nsukka during January and early February 1981 are described. The animals were almost always found near buildings, trees, rubble and fallen logs etc.: they tended to remain in the same place day after day. Territorial behaviour was most marked in adult males, but individuals of all sizes displayed by 'nodding'. Mating is described. The animals roosted at night in trees and shrubs and on buildings, Activity was greatly influenced by weather. Escape from enemies is described, and it is suggested that, in addition to indicating 'social space', 'nodding' may act as a protean anti-predator strategy. These lizards are omnivorous.
Introduction The observations described below were made on the campus of the University of Nigeria, Nsukka, throughout January and early February 1981 and supplement those of Harris (1963, 1964) who has made an important pioneer study of the rainbow lizard. During most of the time, while the harmattans was blowing, day temperatures averaged about 30°C and the relative humidity fell as low as 10 per cent. Towards the end of the period, however, temperatures and humidities began to increase somewhat, but this did not appear greatly to affect the behaviour of the rainbow lizards (Agama agama (L.), Lacertilia: Agamidae), the objects of investigation, except in so far as fewer females and juveniles were sighted when counts were made while the sun was exceptionally hot. At this time of year, during the dry season, the grass was brown and the soil baked hard by the sun. Few animals were evident, apart from agamid lizards and birds-mainly hooded vultures. The lizards were obviously not distributed evenly throughout the University campus. In some places-especially near buildings and cement-lined drainage ditches--they were common, whereas in open grassland away from trees they were not to be found at all. Even within densely populated habitats, the distribution of the various individuals appeared to remain constant. At the same time, the population structures within these habitats appeared to vary consistently. Some contained mainly adults and large juveniles; in others, smaller juveniles predominated. The observations described below were made in order to elucidate these points.
Methods Daily inspections were made in selected environments: the quadrangle of the Continuing Education Centre (CEC) and the Zoological Gardens of the Department of Zoology (Zoo).
* Department of Zoology, Birkbeck College (University of London), Malet Street, London WCIE 7HX, England. t A seasonal, dust-laden, wind from the Sahara occurring when the north-east trades dominate the area. 014-0-1963/81/030235 + 13 $02.00/0
©
1981 Academic Press Inc. (London) Limited
J. L. CLOUDSLEY-THOMPSON
236
For census purposes, these were both arbitrarily divided into smaller areas within which the numbers of lizards were counted. The order in which the various areas were visited was altered arbitrarily from day to day so that if any lizards were inadvertently driven from one to another and therefore counted twice, this would not bias the results. Numbers of lizards on or at the base of the wall at the west end of Eyoita Hall of Residence were also counted daily. Although adult males in full reproductive coloration and with developed gular folds were clearly recognizable, it was not always possible to distinguish with certainty between immature males and adult females (Harris, 1963, 1964). On the daily counts, therefore, only three categories of lizard were recognized: (a) males in the reproductive phase (6'), (b) females and immature adult males (~) and, (c) juveniles, small females and young of all sizes (juv). Certainly more than half the animals recorded as ~ were, in fact, immature adult males, which began to develop orange-coloured heads and black tips to the tail towards the end of january. If, therefore, the sexes were approximately equal in numbers, some of the larger 'juveniles' must, in fact, have been small females. Total values obtained, therefore, probably somewhat underestimate the ratio of adults to juveniles. Unfortunately, several lizards were collected in the Zoo by members of the Staff of the Department of Zoology for parasitological research and class experiments before the counts had been made on 7,8,9 and 16 January, a total of about 75 individuals of all categories being Croton brushes
Croton brushes
Ditch
i' ....._~ ~ <..,
J"
,,,,,,,,,--
... a.
:! en
Frangipani bushes
iV~?':'~i:r;'rZ;(~j!(%'i~; . . Oleander bushes
Ditch 10 m
Figure 1. Sketch map toshow main basking places, roosting sites and refuges (broken lines) of mature males, female arid juvenile A. agama in the quadrangle of the Continuing Education Centre.
BIONOMICS OF THE RAINBOW LIZARD
237
taken. On those days, unusually low numbers of sightings were recorded. Although the total area of the Zoo was some 20,000 m 2 , and the area surveyed amounted to only 6500 m 2 , the lizards were invariably shy and in hiding everywhere for an hour or two after being hunted. Fewer lizards were sighted on days when the sky was cloudy or the sun obscured by harmattan dust. For example, on 20 January, between 12.00-12.30 h, only 4 0', 5 ~, 22 juv lizards were sighted in the Zoo study areas and 4 0', 1 ~, 3 juv in the CEC quadrangle. The figures for the following day, while the sun was shining, were 7 0', 9 '12, 46 juv and 5 0', 4 ~, 11 juv respectively. Again, fewer sightings were made early in the afternoons on days when the sun was especially hot. On 31 January at 14.15 h, for instance, only 3 0', 2~, 4 juv were recorded in the CEC quadrangle. Distribution
Rainbow lizards appeared almost invariably to live near buildings, cement-lined drains, brick rubble, fallen logs and heaps of leaves. The majority sighted in the Zoo, for example, were seen near the Empty Cage, the south wall of the Monkey House (until 16 January when a number of them must have been caught) and the Central Area (near the Hyena House, Shed and Experimental Animals House) (Fig. 1). Numbers sighted in other parts of the Zoo study area were extremely small (Table 1). Even within the Monkey House and Empty Cage, where the counts were made, the lizards appeared to restrict themselves roughly-tothe same areas, day after day (Table 2). The differences between the numbers in the three sections into both of which these buildings were arbitrarily divided are statistically significant (X 2 test, P > 0·05; P > 0,01), indicating permanent differences in the population sizes. Furthermore, the majority of juveniles sighted in the vicinity of the Empty Cage were nearly full grown, whereas those on the south wall of the Monkey House and within the Central Area were mostly of the smallest size range. Ratios of the three classes of lizards in the CEC quadrangle, Zoo and end wall of Eyoita Hall were also significantly different (X 2 test, P > 0·001). Table 1. Mean (n = 35) and maximum sightings of A. agama in different localities and calculated total population in the areas studied. Further explanation in the text Male
Female
Juvenile
mean max
4·9 6
4·6 8
8·2 13
mean max mean max mean max mean max mean max mean max
0·5 2 3·2 7
0·2 1 6·0
5·6 14 7·6 19 18·6 38 3'7 12 35'3 58 15·0 24
Locality CEC Zoo Monkey House Empty Cage Central Area Elsewhere Zoo totals Eyoita Hall Calculated total population in study areas Calculated mean density per ha
1-6
11
2·8 9 0·3
5 0·5 3 5·8 12 1'3 2
9·2 18 4'3 12
27
65
260
32
78
313
3
r. L. CLOUDSLEY-THOMPSON
238
Table 2. Mean (n = 35) and maximum sightings of A. agama on different sections of the south wall of the Monkey House and in the Empty Cage of the Zoo Monkey House West End ~
mean max
5f
1
Central Area
East End
juv
~
5f
juv
~
5f
juv
0·3 9
1
1
4
0·1
0·3 1
1
4
1·9
Empty Cage Central Area
West End
mean max
~
5f
juv
~
5f
1·0 3
2·1 6
3·3 9
0'7 3
1·6 5
East End juv 1·2
4
~
5f
juv
1·5 3
2·2 6
3·1 10
Territorial behaviour was most marked among males in the reproductive colour phase. In Figs 1 and 2 are shown the positions most often taken up by such males in the CEC quadrangle and the Zoo study area. The roosting places of females and some juveniles are also indicated in Fig. 1. Immature males, females and juveniles were often to be found in the same areas day after day-indeed, it appeared that all individuals were to some extent territorial. At the same time, they all displayed by 'nodding', and this may assist in maintaining a 'social space' around individual lizards. Other explanations of the behaviour pattern will be discussed later.
Population structure The population structure appeared to vary in different places. When the means of the sightings in the CEC quadrangle, the study area of the Zoological Gardens and the end wall of Eyoita Hall were compared (Table 1), it was found that the ratios of adult to juvenile lizards in the CEC quadrangle, the Empty Cage at the Zoo and the wall of Eyoita Hall were higher than elsewhere. If it is assumed that the ratios in the sightings were proportional to the total populations in these areas, the significantly larger number of juveniles in the Central Area of the Zoo may have been related to the extra cover available there, especially in the piles of logs and heaps of dead leaves-which would have afforded shelter from predatory enemies such as kites, pied crows, vultures and so on. Indeed, lizards of the smallest size range (c. 60 mm) were only found in quantity in the Central Area of the Zoo. As already mentioned, it was often impossible to distinguish, in the field, between adult females and males not in breeding coloration. In the CEC quadrangle, however, I learned to recognize every adult lizard individually, because these were more accustomed to people and, consequently, relatively tame. Here there appeared to be a total of six males in reproductive colours, two females and six immature males. Towards the end of the period of observation, some of the immature males began to develop full reproductive colouring. One did so on 28 January, another on 30 January and two more during the first week of February. Nevertheless, I continued to count them as 'imrnatures' in order not to upset the calculations. No doubt some of the larger juveniles would have matured into adult females about the same time, but this could only have been determined by dissection as the coloration of females and juveniles is identical (Harris, 1964). On 28 January, a record of seven adult males was
BIONOMICS OF THE RAINBOW LIZARD
I Monkeys 00
8
239
,0
G o
Boboons
o ~
I
0
0 4> C VI 4> ::J >,0
II
E
o
III
G ,.
G
G 0
(1
~ 6
Kiosk
Figure 2. Sketch map of the Zoological Gardens study area.
observed in the Empty Cage of the Zoo. Previously the greatest number recorded on any one occasion had been five (on 20 January). It therefore seems probable that here, too, some of the immature males had developed rainbow colours. Total numbers It was not possible to assess total population numbers with any high degree of accuracy. After a week or two, I was able to recognize many of the individual males in the reproductive phase by their colour variations and by the fact that they were to be seen in the same place day after day. Until the end of January, when some of the immature males began to adopt rainbow coloration, there were seven adult males in the Empty Cage of the Zoo, two on the wall of the Monkey House (until 16 January when one of them was almost certainly captured), six in the Central Area and three others-a total of 18 in approx. 6500 m 2 (Fig. 1). The CEC quadrangle housed six males in approx. 1600 m 2 (Fig. 2) and the west end of Eyoita Hall, three on approx. 210 m 2 of wall space. Some idea of the total numbers of females, immature males and juveniles can be obtained from the fact that the mean number of individual sightings recorded on or in the Empty Cage of the Zoo was 13,6, whereas at 17.15 h on 12 January I was able to count 33 individuals roosting on the top of the wall-the maximum recorded there at anyone time. This would give a ratio of mean sightings to total numbers of 1 to 2·4. If this ratio was the same in the various study areas, the total number of agamid lizards involved in the survey would have been about 27 males, 65 females, 260 juveniles.
240
J. L. CLOUDSLEY-THOMPSON Behaviour Territorial display and aggression
As Harris (1964) so clearly indicated, A. agama, like other agamids, is a territorial species. The sexual dimorphic coloration of dominant males becomes more brilliant in the breeding season (Carpenter, 1967; Harris, 1964). Individual males in breeding coloration tend to occupy one or two preferred places within a comparatively restricted range where they display themselves, nodding conspicuously. All individuals have the habit of nodding to some extent. but adult males also 'bob'-that is, they nod extremely vigorously, at the same time bending their forelegs as they do so and thus increasing the display (Harris, 1964). If an immature male or female encroaches upon the social space of a cock or rainbow male, the latter either chases it away or nods with extra special vigour, displaying its gular fold. Should this not be sufficient to persuade its rival to leave, the dominant male will move sideways towards it, with a -series of rapid jumps. Any individual, other than another cock male in rainbow coloration, then departs. Sometimes two rainbow males will rest alongside one another as though sizing each other up. They may then display and, if neither gives way, a brief fight ensues in which the two contestants lash each other with their tails .and even struggle briefly. Many of the smaller of the immature male lizards in the CEC quadrangle appeared to have lost the tips of their tails, perhaps in territorial disputes. On one occasion, in the Zoo, I watched a male in breeding coloration jump onto a breeze-block on which a large female (or immature male) was sunning itself. The rainbow male then lashed out once vigorously with its tail, and the other fled immediately from the breeze-block. Adult males did not usually bother to display to juveniles, but merely chased them off. As mentioned above, all rainbow lizards, including the smallest juveniles seen, would display by nodding. This is such a characteristic trait and makes the animals so conspicuous that it is difficult to believe that it can have no function whatsoever. I gained a distinct impression that even the youngest rainbow lizards tend to be solitary and that nodding may be a means of maintaining the social space around them. Harris (1964) concluded that nodding is in no way connected with territorial or reproductive behaviour, nor does it assist in judging distance since it does not take place before snapping up an insect. He thought it might serve to reveal the positions of cryptically coloured females and juveniles (an explanation somewhat similar to that which presented itself to me). The head bobbing and challenge display of cock lizards is a far more intense form of head movement. The main function of a territory for A. agama, according to Harris (1964), is to provide a mate. Heatwole (1976), on the other hand, argued that, in general, territoriality provides a mechanism whereby at least-a proportion of the population can obtain an adequate food supply, although surplus individuals die, rather than the entire population suffering the deleterious effects of inadequate energy resources. In the case of A. agama, although dominant territorial males may tolerate subordinate males within their territory and share food with them, courtship and mating appear to be the prerogative of the dominant animal (Stamps, 1977).
Reproduction
When chased by males in the reproductive phase, other adults usually ran away. Some individuals, however, presumably females, did so with their tails lifted up at an angle of about 45° from horizontal. It seemed probable that this might be a courtship response (Carpenter, 1967; Schmidt & Inger, 1957). The tail is raised in the same way during mating and the male then lies closely alongside the female with his tail pointing forwards beneath her body and his cloaca apposed to hers. The eggs are buried in sand and number not less than five; their size is about that of a large pea (Dr Margaret Anizoba, pers. comm.). Males in the reproductive colour phase are found throughout the year, but oviposition at Nsukka probably only takes placeat the time of the spring rains in April (Dr Uche Onubogu, pers. cornm.). Certainly I found no young less than about 6 cm in length from mouth to vent, and
(c)
(d)
Plate 1. Habitats of A. agama at the University of Nigeria, Nsukka. (a) The CEC quadrangle,
(b) central region of the Zoological Gardens, (c) the Monkey House, (d) the west end of Eyoita Hall of Residence.
[facing page240]
(d)
(e)
(0
Plate 2. Behaviour of A. agama at Nsukka. (a) Rainbow male and female, (b) male climbing borassus palm, (c) juvenile on log heap, (d) male sleeping in croton bush, (e) immature male and juvenile roosting in an hibiscus, (f) roosting female.
BIONOMICS OF THE RAINBOW LIZARD
241
most were considerably larger than this. Presumably they were last year's babies. Harris (1964) describes reproduction in detail. He states that clutches of five or six eggs are most common, but clutches of only three or as many as eight eggs have been found.
Nocturnal roosting
The rainbow lizards in the CEC courtyard roosted at night in various trees and shrubs. Between 17.00-18.00 h, an hour before complete darkness fell, each lizard would begin to make its way towards the tree or bush in which it habitually spent the night. (This was verified in the case of males in the reproductive colour phase, the larger females and immature males which could be recognized individually. At the same time, I gained the impression that the juvenile lizards also roosted nightly always in the same trees and shrubs. Some of these are indicated in Fig. 1.) Movement towards the roosting place was unhurried: a lizard would make a sudden dash for about a metre, stop motionless for 5 min or so, and then make another sudden movement upwards, a metre or so at a time with lengthy intermediate pauses. Finally it would scramble into the branches, or into the fibrous mass at the base of the palm fronds and, after a couple of wriggles, emerge among the leaves to remain motionless for the remainder of the night. When disturbed just before bedtime, the lizards would dart up their regular roosting tree or bush and disappear for good. Individuals that roosted on the branches of frangipani or hibiscus bushes, when they could still be seen before darkness fell, would remain wary, as far as possible keeping on the side away from the observer of the branch to which they were clinging. After nightfall, however, they were reluctant to move, even when a torch was shone directly onto them. They would occasionally allow themselves to be touched without responding but, if excessive liberties were taken in this respect, would jump onto another branch or into the foliage where they were difficult to detect. When forced to leave their roosting bush and take shelter beneath the steps of the CEC quadrangle, they would return to their perch within 10-15 min. The agamids that inhabited the Empty Cage in the Zoo appeared all to roost on the top of the wall under the eaves where their heads could be seen from the ground. Those that frequented the west wall of Eyoita Hall, on the other hand, roosted in a vertical posture, clinging to the roughcast where they were sheltered to some extent from observation by drainpipes, wide open windows, branches and so on. A few roosted against the architrave of the windows, others horizontally on the window sills. When roosting, the normal social spacing appeared to disappear and adult males in the reproductive phase could then be seen in close proximity to females and juvenile animals. Juvenile agamid lizards began to go to bed first, followed by the adult females and finally, somewhat later, by the males in breeding colours-although one female was still on the ground in the CEC courtyard for three nights running at 18.15 h, at least half an hour after all her companions had retired for the night. First to rise, around 09.15 h were the adult males, followed by the females and, finally, the young. By 10.45 h maximum sightings could be recorded. Later in the year, however, when the weather is warmer, basking begins earlier in the morning or, as I was informed, shortly after sunrise. Not only numbers of sightings but also the time of emergence appeared to he influenced by sunshine. A small colony (consisting of two males in breeding coloration and about a dozen other individuals) that occupied a sunny, sheltered site at the south-eastern corner of the CEC building was nearly always up earlier than the colony in the quadrangle. The only exceptions to this were on days such as 29 January when the wind blew strongly from the east. One male, however, sometimes continued to roost on a frangipani tree until quite late in one morning-presumably because there was little human disturbance in this locality. When they descended from their roosting places in the morning even mature males had assumed a dark, cryptic coloration and only brightened as they warmed up in the sunshine. They then began nodding and feeding. Loss of colour after nightfall took several hours; its recovery at dawn was complete within a few minutes.
242
r. L.
CLOUDSLEY-THOMPSON
Avoidance of wind and rain At 11.00 h on 25 January 4 0, 7~, 12juv were counted in the CEC quadrangle in sunshine. An hour later, the sky became overcast and cloudy, a cool breeze sprang up, and there was a light shower of rain. Long before this, however, all the lizards had vanished-indeed their disappearance almost coincided with the appearance of the rain clouds-but they had not retired to their roosting positions. They had taken to their daytime refuges. Some were beneath the steps, others at the bases of the bushes or up the fig tree arid Borassus palm. Two hours afterwards, although the sun had stilI not reappeared, 4 0, 4 ~ and 7 juv had come out and were lying pressed incredibly flat upon the cement and tiles of the lukewarm ground. In the Zoo, only 1 0, 1 ~, 2 juv and 29 roosting animals were to be seen, all on or in the Empty Cage; 1 0, 4~, 10 juv were clustered behind the drainpipe against the wall of Eyoita Hall. Presumably refuges and roosting places coincided for these individuals. The small colony at the south-eastern corner of the CEC building, mentioned above, took refuge mainly in the space beneath some large water tanks, but their roosting places were almost certainly . among the fronds of the talI Borassus palms nearby. On windy days the numbers of females, immature males and juveniles to be seen were much reduced, but adult males in reproductive coloration were less affected. For example on 29 January, eight males in reproductive coloration-the original six plus two others which had previously been immature-were to be seen in the CEC quadrangle, but only two females or immature males and two juveniles. Escape from enemies Although approachable to within 3-4 m, or even less when on the ground, A. agama is more shy after taking refuge in a tree or bush. Invariably it wilI run round to the side of the trunk or branch that cannot be seen by the observer; if two people approach simultaneously from opposite sides, the lizard will climb rapidly into the branches. The lizards in the CEC quadrangle would take refuge in any convenient bush or tree (except for the fan palm and the Phoenix palm, which none of them would climb) and did not restrict themselves to the trees or bushes in which they habitually roosted. The individuals that inhabited the eastern end of the courtyard would also take refuge in the artificial cement-lined ditch beneath the steps and in the tunnel leading beneath the verandah to the lawn on the east. These were usually the only animals to venture on the lawn-perhaps because they had a safe line of retreat: the lizards that inhabited the south-east corner often basked on the edge of the covered path, but seldom went as far as the lawn beyond. Low-level refuges were never used, however, as roosting places during the night. Although relatively tame, rainbow lizards were able to move with surprising speed when the occasion warranted it, and to jump with considerable agility from one branch to another. As mentioned above, none of them roosted or took refuge in the Phoenix palm, apparently because they could not force their way through the mass of fibres beneath the bases of the existing fronds. On one occasion a female was chased up the trunk of this palm, struggled briefly to cross the fibrous barrier, then leapt 3 m to the ground and darted into shelter beneath the north-eastern step. Females were more shy than males or juveniles. Apart from adult males in rainbow colours, A. agama is undoubtedly cryptic. Individuals on an appropriate background are most inconspicuous until they move or nod their heads. When roosting at dusk or dawn, even males in the reproductive phase become dark and are difficult to make out among leafy branches. On open ground, all individuals are alert and aware of the presence of an enemy although they nod most vigorously when one approaches. This, therefore, may be a warning signal to other members of the colony. At the same time, it may, like other types of erratic or protean behaviour, distract the attention of a predator at the critical moment, so that it misses its quarry. Feeding Rainbow lizards are omnivorous. On a number of occasions I saw them eating hibiscus and other flower petals, grass, dead leaves, bread crumbs, fragments of ground-nut, sugar and
BIONOMICS OF THE RAINBOW LIZARD
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crushed sweets that they licked up from the ground. They also ate ants with alacrity, and would occasionally stand over the hole leading to a nest, licking up the ants one by one as they emerged. I have previously recorded them feeding on termites (Cloudsley- Thompson, 1963). Adults have occasionally been observed to feed cannibalistically on their young, but whether they also feed on geckoes (Hemidactylus brookii) has not yet been determinedalthough this seems unlikely because there is no temporal or spatial overlap between the two species. (It would be interesting if this were the case, because 10 per cent of the agamids were found to be parasitized by Pentastomida. These they might have caught from geckoes which are already known to harbour them; Dr Uche Onubogu, pers. comm.). Juveniles of many species of lizard eat relatively more animal matter than adults (Schoener, 1977).
Discussion This study was completed without my being able to consult The Life of the Rainbow Lizard (Harris, 1964): neither this essential monograph nor The Life of Reptiles (Bellairs, 1969), nor, indeed, any of the references listed in the bibliography was to be found in the Nnamdi Azikiwe Library of the University of Nigeria. Nevertheless, since I was unable to recollect either the topics covered or the conclusions reached in Harris's work, my own observations were completely unbiassed. The main differences between the conclusions reached by Harris (1964) and myself are as follows. Harris recorded an average density among buildings of 16·2 ha- 1 (40 per acre) and a territorial density of2·g ha- 1 (7 per acre). Away from buildings, in districts where the lizards were arboreal, .he recorded 56·7 ha- 1 (140 per acre) and 14·6 ha- 1 (36 per acre) respectively. In contrast, my maximum sightings suggested approximate densities of 78·3 ha- 1 and territorial densities of 11·5 ha- 1 near buildings (CEC, Eyoita Hall and the Empty Cage and Monkey House of the Zoo) and of 40 ha -1 and 15·0 ha -1 in the parts of the Zoo where trees predominated rather than buildings. In other words, territorial densities were slightly lower in arboreal regions, at Nsukka, than found to be the case in Ibadan by Harris (1964), but very much greater near buildings. Harris recorded shikra hawks as being among the main predators. There are, however, no vultures in Ibadan, although kites are plentiful, whereas hawks are scarce and hooded vultures numerous at Nsukka. Possibly vultures are less efficient predators of A. agama than are hawks and kites. The mean density for all the study areas combined was about 400 ha " ! and the territorial density 32 ha -1 (Table 1). These figures, however, are calculated maxima based on an estimation of the ratio of mean sightings to total numbers of 1 to 2,4, as assessed in the Empty Cage of the Zoo. The figures used for comparison with those of Harris (1964) were the maximum numbers recorded at one time in any of the three categories of lizard adopted, and therefore somewhat lower. Western (1974) estimated a population of 187 ± 35·3 ha- 1 on four lava outcrops in a semi-arid environment of northern Kenya. The daily pattern of life differs somewhat at Nsukka from Ibadan (Harris, 1964) and He (Halstead, 1970). It seems likely. that the differences are related to the different climatic regimes in the three places. Fighting seemed to be less common at Nsukka than in Ibadan, while it was not observed at all at He. Like me, Harris (1964) reached the conclusion that A. agama is really a tree-living species although, in rain-forest, lizards are usually to be found only on the walls of buildings. The explanation he gave was that forest is cooler than open country because the sunlight is excluded and only in clearings and along roads are the animals able to raise their body temperature by basking. The mud walls of houses also absorb a considerable amount of heat during the day and, at night, act as heat reservoirs; the lizards are not slow to enjoy this warmth. Where there are no dwellings, however, they sleep high up in trees, usually in crevices at the base of a side limb or the frond of a palm-which would be much cooler and less protected than a roost in the roof of a house. Stomach analysis showed that A. agama is primarily insectivorous at Ibadan, feeding almost entirely on ants. Large males are, however, cannibalistic. Only occasionally is vegetable matter eaten there, and then chiefly by adult males which show a preference for coloured
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objects. The large amount of vegetable matter eaten by the agamids at Nsukka may reflect the scarcity of insect food available during the dry season. Harris (1964) did not mention the marked avoidance of rain that I observed although throughout he lays stress on the effect of temperature on behaviour. Nor did he place so much emphasis on escape from enemies which appeared to me to be the most reasonable explanation for the differences in population structures observed. Chapman & Chapman (1964) also concluded that vegetable matter is eaten mainly in the months with least rainfall; while Marshall & Hook (1960) found that the sexual cycle in A. agama lionotus is timed not by rainfall but by the seasonal appearance of animal food that appears after the rains.
Summary Agamid lizards were studied in the campus of the University of Nigeria, Nsukka, throughout January and early February 1981. They were almost invariably found near buildings, trees, cement-lined drains, brick rubble, fallen logs and heaps of leaves. Even within these restricted localities, the animals remained in roughly the same places day after day. Territorial behaviour was most marked between adult males in reproductive coloration, but individuals of all sizes displayed by 'nodding', possibly thereby indicating their 'social spaces'. In territorial disputes, adult males displayed their gular folds, jumped sideways at their rivals and lashed with their tails. The courtship response of the female was to raise her tail. During mating, the male lies alongside the female with his tail pointing forwards beneath her body. Oviposition probably takes place at the time of the rains. Juvenile lizards of the smallest size ranges were most common where there was plenty of shelter. The animals roosted at dusk in trees and shrubs, on the walls of buildings where the texture was rough, and under the eaves. Adult males slowly become black after dark, but their colour brightens up rapidly when they begin sun basking in the morning. Activity is markedly affected by weather; wind and rain are avoided at all times. When approached too closely, the lizards took refuge near the roots of shrubs, beneath drains and in other inaccessible places. Such retreats did not necessarily coincide with the nocturnal roosting places of the individuals. Nodding may additionally function as a form of erratic or 'protean' antipredator device. Rainbow lizards are omnivorous at Nsukka, feeding on ants, termites, fallen flowers, breadcrumbs, ground nuts, sugar etc. Large individuals are also reported to be cannibalistic and to eat their own young. Thanks are due to the Inter-University Council for providing the air fare to Nigeria and for financial support under the Short-Term Visitor Scheme, to Dr Mark Eluwa, Head of the Department of Zoology, University of Nigeria, Nsukka for hospitality and accommodation, to the Academic Board of Birkbeck College (University of London) for granting me leave of absence during part of the spring term, 1981, and to Professor A. d'A. Bellairs for commenting on the manuscript.
References Bellairs, A. (1969). The Life of Reptiles. London: Weidenfeld & Nicolson. 2 vols., 590 pp. Carpenter, C. C. (1967). Aggression and social structure in iguanid lizards. In Milstead, W. W. (Ed.), Lizard Ecology. A Symposium, pp. 87-105. Columbia: University of Missouri Press. 300 pp. Chapman, B. M. & Chapman, R. F. (1964). Observations on the biology of the lizard Agama agama in Ghana. Proceedings of the Zoological Society of London, 143: 121-132. Cloudsley-Thompson, J. L. (1963). Some aspects of the fauna of the district around Lake Chad. Entomologist's Monthly Magazine, 98: 180-181. Halstead, L. B. (1970). Some observations of the rainbow lizard, Agama agama (L.), at the University of He. Nigerian Field, 25 (2): 86-89. Harris, V. A. (1963). The Anatomy of the Rainbow Lizard. Agama agama (L.). London: Hutchinson. 104 pp, C
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Harris, V. A. (1964). The Life of the Rainbow Lizard. London: Hutchinson. 174 pp. Heatwole, H. (1976). Reptile Ecology. St. Lucia: University of Queensland Press. 178 pp. Marshall, A. J. & Hook, R. (1960). The breeding biology of equatorial vertebrates: reproduction of the lizard Agama agama lionotus Boulenger at Lat. OOOl'N. Proceedings of the Zoological Society of London, 134: 197-205. Schmidt, K. P. & Inger, R. F. (1957). Living Reptiles of the World. London: Hamish Hamilton. 287 pp. Schoener, T. W. (1977). Competition and the niche. In Gans, C. & Tinkle, D. W. (Eds), Biology of the Reptilia. Vol. 7, Ecology and Behaviour A, pp. 35-136. London: Academic Press. 736 pp. Stamps, J. A. (1977). Social behaviour and spacing patterns in lizards. In Gans, C. & Tinkle, D. W. (Eds), Biology of the Reptilia. Vol. 7, Ecology and Behaviour A, pp. 265-334. London: Academic Press. 736 pp. Western, D. (1974). The distribution, density and biomass densities of lizards in a semi-arid environment of northern Kenya. East African Wildlife Journal, 12: 49-62.