Individual differences in aggressiveness of adelie penguins

Anita. Behav.,1974,22, 611-616

INDIVIDUAL DIFFERENCES IN AGGRESSIVENESS OF ADELIE PENGUINS BY E. B. S P U R R

Department of Zoology, University of Canterbury, Christchurch, New Zealand Abstract. The number of pecks per minute given by individual Adelie penguins to an artificial model is used as a measure of aggressiveness. Penguins without eggs or chicks are less aggressive than thoes with eggs or chicks. Aggressiveness increases after egg-laying, and reaches a peak at about chick hatching. Prior to egg-laying, males are more aggressive towards the model than females, but after egg-laying there is no difference between them (on average). Most penguins with above average aggressiveness are located at territories in the centre of a colony, whereas those with below average aggressiveness tend to occur at the periphery. Penguins with high aggressiveness also have a higher breeding success than less aggressive ones. The individuals comprising a community of Adelie penguins (Pygoscelis adeliae) may appear morphologically similar, but are behaviourally quite distinct. Reference has been made elsewhere to differences in date of arrival at the breeding colonies, pair and site tenacity, clutch size, breeding success, and frequency of behaviour patterns among different groups of the community (Spurr 1972). This paper is concerned with differences in the aggressiveness of individual penguins. Aggressiveness may be expressed either by overt aggression (fighting) or by threat displays given to intruders. Penguins may have to fight for a territory during the occupation of the colonies, then defend the boundary against intruders throughout the rest of the season. In any one season, however, most penguins return to the territories without having to fight for them. Furthermore, boundary disputes between established penguins are often initiated not because a neighbour trespasses onto a territory, but because it is moving about near the boundary (Spurt in press). The neighbour may return the threat across the shared boundary, and the ensuing encounter may end as abruptly as it began, with no decisive result. On its own territory, each penguin is dominant. Thus, it is difficult to determine from natural observations any differences between the aggressiveness of individual penguins, even when on adjacent territories. When comparing the responses of residents to strangers approaching the territory, it is necessary to take into account such factors as the way in which the approach was made (e.g. directly or indirectly, slowly or quickly), because these factors affect the responses given. In this

study, however, a model was used to provide a standard stimulus that could be presented in a standard way, and the responses of penguins to this standard stimulus were recorded in an attempt to determine individual diffierences in aggressiveness. Methods Observations were made during the summer of 1969 to 1970, at the University of Canterbury field station, Cape Bird, Ross Island, Antarctica (77 ~ 13' 10" S, 166 ~ 28' 30" E). A total of approximately 200 penguins were presented with an artificial model at 5-day intervals throughout the season. All penguins were banded with aluminium alloy flipper bands, and sex was determined either by observed copulation, or by pairing with another penguin of known sex. Adult penguins were classified into the following categories (see Spurr 1972): (i) mated penguins; these produced eggs, and were sub-divided into (a) successful breeders, when they raised chicks to independence, (b) unsuccessful breeders, when they lost all their eggs or chicks. (ii) unmated penguins; these occupied territories but did not produce eggs. They may be alone or keeping company with another penguin. No difference could be detected in the responses of the test penguins to a stuffed penguin presented in either a resting or a threatening position. Both were strongly attacked. Furthermore, there was no apparent difference between responses to a stuffed penguin and an artificial model of approximately penguin size. The stuffed penguin would have been ideal for this experiment except that the test penguins soon tore through the skin when pecking. The artificial

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model was made from a tough finely woven fabric and mounted in an upright resting posture. The model was attached to a 3-m pole mounted on wheels, so that it could be pushed up to the outside edge of the nest. The number of pecks delivered in 1 min, and notes on behaviour, such as raising or sleeking of the occipital crest, and reaching forward or turning away, were all recorded. It was difficult to present this model to the penguins prior to egglaying because they either moved away from it or attacked it with their flippers. Flipper attacks were dangerous because the penguins could injure their flippers on the wooden back supports of the model. For this reason, the model had to be withdrawn when attacked in this way. Two tests were made to check for habituation to the model. In the first test, three males were presented with the model a total of ten times each, at 5-min intervals. The number of pecks per minute did not decrease in this number of trials. In the second test (about midway through the season) the model was presented to twenty penguins (of unknown sex) from colonies other than the study colonies. The average number of peeks per minute was 73-2 for the non-study penguins, compared to 68.6 for the study penguins at the same stage of the season. The difference is not significant (t-test, P>0.05).

Results Differences in aggressiveness of males and females. Males alone at the nest site before egglaying pecked the model at an average of sixteen pecks per minute (Fig. 1). Females were not normally found alone at nests without eggs or chicks. When a pair were together at the nest prior to egg-laying, males averaged nineteen

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Fig. 1. Responses to a model by the same penguins before and after egg-laying. (White bars represent females; black bars represent males).

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pecks per minute, and females five pecks per minute. The difference is highly significant (t-test, P<0.01). Not only were responses from males of higher intensity (as measured by pecks per minute) but they were also given to more presentations of the model when both members of a pair were together on the territory (males responded on thirteen occasions, females on two; Z 2, P<0-01). Pairs together at the nest soon after the first egg was laid, each averaged twenty-three pecks per minute (Fig. 1). After the second egg was laid, males alone during the first incubation watch averaged fifty-two pecks per minute. Females alone during the second watch averaged fifty-eight pecks per minute. From all trials through the season, the average mated male scored 57.5 pecks per minute, and the average female scored 62.3 pecks per minute. (The difference is not significant; t-test, P>0.05). These results indicate that the early difference in the responses of males and females to the model had disappeared after egg-laying (by which time the female would have been completely accepted as the mate). Although there was no difference, on average, between the model scores of males and females, there were some marked individual differences. In twenty out of a sample of forty-five individual pairs, there was no significant difference between the scores of male and female; but in fourteen the male had a significantly higher score, and in eleven the female had a significantly higher score. Thus, some high scoring males were paired with low scoring females, and vice versa. When both members of a pair were on the territory together after egg-laying, the penguin actually on the nest participated in more of the encounters with the model than the other (thirty-two against twelve; •2, P<0.01). An equal number of males and females participated in the thirty-two encounters by penguins on the nest (sixteen each; Z 2, P>0.05), but males were responsible for ten of the twelve encounters by penguins standing off the nest (Z 2, P<0.05). When females were standing off the nest, they tended to stand back and let the male do the defending.

Aggressiveness of different categories of penguins. Unmated penguins and unsuccessful breeders without eggs or chicks delivered many fewer pecks per minute to the model than penguins with eggs or chicks (Fig. 2). Thus, males without eggs or chicks scored an average of 14.8 pecks per minute; females without eggs

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Fig. 2. Distribution of model scores (pecks per minute) of different categories of penguins (N = number in sample.) or chicks scored an average of 7.2 pecks per minute. These average scores remained fairly constant throughout the season. The scores of penguins that had lost nest contents were similar to the scores of those that had never laid. The scores of successful breeders prior to egg-laying were very similar to those of unmated and unsuccessful breeders without eggs or chicks (see Fig. 1; average male nineteen pecks per minute, and average female five pecks per minute). After egg-laying, however, their average scores increased (see below). Aggressiveness through the season. The average scores of successful breeders increased after egg-laying in early November, and continued to increase until about chick hatching in mid December (Fig. 3(a)). The highest average scores were obtained between 30 and 44 days after egg-laying (Fig. 3(b)). Thereafter, the average scores decreased again. This means that the penguins showed most aggression toward the model at about chick hatching, which at Cape Bird occurs between 31 and 38 days after egglaying (Spurr 1972). The increased aggressiveness at chick hatching is highly significant (anova, P<0.01). Classification of aggressiveness. Individual penguins were classified according to their mean scores for the season. The mean scores of mated males ranged from 9 to 114 (Mean 58, SD 25) and mated females ranged from 15 to 114 (Mean 62, SD 22). Penguins were considered to be of average aggressiveness if the score fell within one standard deviation either side of the

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(b) Fig. 3. Response of penguins to model presented at different times after laying of first egg. (a) Monthly time base. (b) Time corrected to date of laying first egg. (White bars represent females; black bars represent males ) population mean, and above or below average if the score fell more than one standard deviation outside the mean. Distribution of aggressive penguins. The distribution of aggression scores within a colony is shown in Fig. 4. Most penguins (males and females) with above-average scores were located at territories in the centre of the colony. Penguins with below-average scores tended to occur at the periphery of the colony. This difference in the distribution of penguins is statistically significant (Z 2, P < 0 . 0 5 , for each sex). Aggressiveness and breeding success. Breeding success of individual penguins was determined over a period of time, ranging from one to four seasons, during the course of another study (Spurr 1972). Most records were from more than one season, so that the effect of catastrophes is reduced. Breeding success is calculated as the percentage of eggs laid surviving as viable chicks until mid January. Penguins with high aggression scores (as tested with the model) had a significantly higher breeding success than penguins with low scores

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Fig. 4. Distribution of model scores of penguins at different positions in a colony. (Upper colony males, lower colony females.) Black circle represents above average score; dotted circle represents average score; white circle represents below average score; incomplete circle represents unmated male present for part of season only, no female. (Table I). The analysis did not, however, consider other factors known to affect breeding success (clutch size, territory locality, and time of laying: see discussion). Discussion

The isolation of Adelie penguins on individual breeding territories precludes the formation of a definite peck order. Nevertheless, it can be readily established that some penguins are more aggressive than others. An artificial model (as used in this study) provides a standard stimulus, and responses given to it may be regarded as indicative of responses to an intruder. It is often stated that the male Adelie penguin is more aggressive than the female (e.g. Sladen 1958). This type of statement needs clarification. The difference in aggressiveness of males and females is related to their roles in territory selection and pair formation. The territory on which a pair of Adelie penguins breed is invariably selected by the male before pair formation. To be able to enter his territory, a female must first appease the male's aggressiveness. Throughout early pair formation males

F(males) = 98.2(df 1, 74), P<0.001. F(females) = 64.9, (dfl, 60), P<0-001 *This result was due entirely to 100 per cent success by one female which laid only one egg and successfully raised the chick. frequently attack females, and chase them away from the territory. The male is clearly dominant at this stage of pair formation, and this is reflected in the responses to the model. Females that re-unite with previous mates however, are not so strongly dominated as in new pairs; males do not attack them on approach, nor drive them away from the territory. This is largely because individual recognition and mutual behaviour performed at reunion apparently reduce aggression (Spurr in press). As a pair becomes established, the female takes an increasing part in the defence of the territory. After the eggs are laid, when only either the male or female is present, there appears to be no difference in the quality of the male's and female's responses. When they are on t h e territory together, however, the male may still be dominant to the female, as is indicated by his response to the model when he is standing off the nest. Thus, it is possible that the male is always (at least slightly) dominant to the female whenever the two are together, but what has not been made clear before is that when the female is alone at the nest after egg-laying, she defends the territory just as strongly as the male (on

SPURR: INDIVIDUAL DIFFERENCES IN AGGRESSIVENESS OF PENGUINS average). In fact, some females were more aggressive toward the model than their partners, and it would be interesting to determine the dominance relationships of such pairs. The difference between the seasonal number of pecks per minute delivered to the model by mated compared to unmated penguins must not be taken as a direct measure of the difference in aggressiveness of the two groups. Before egglaying (and after losing eggs or chicks) mated penguins had a similar score to unmated penguins. Thus, under similar conditions, there is probably little or no difference in aggressiveness between the two groups of penguins. The increase in aggressive responses to the model by parents after egg-laying is associated with increased attachment to the nest site provided by the presence of eggs or chicks. This increase in aggressiveness of parents from egglaying to chick hatching may be controlled by secretions of progesterone and prolactin, as indicated by Vowles & Harwood (1966) for ring doves, Streptopelia risoria. It is probably not related to the increased incidence of threats, attacks and fights per bird recorded at this time of season (Spurr 1972) which mainly result f r o m the increased numbers of unmated penguins and unsuccessful breeders ashore. The lower number of pecks per minute delivered to the model by penguins at the colony periphery indicates that they are less aggressive than penguins in the colony centre. Peripheral penguins encountered more natural intruders, but they responded no less frequently per intruder than central penguins (Spurr 1972). Furthermore, from the results of tests designed to check for habituation, there was no evidence of any reduction with time of exposure in the intensity of responses elicited. Thus, habituation to intrusion cannot be used to explain the lower aggressiveness of peripheral penguins to the model. One must assume that the differences in aggressiveness are real, and seek an explanation elsewhere. In colonies of kittiwakes, Rissa tridactyla, Coulson (1968) found that males at the periphery were lighter and suffered a higher mortality than those at the centre. He postulated that intense competiton for nest sites resulted in very high selection for vigorous males at the centre of a colony. In Adelie penguin colonies, peripheral sites, because they are more exposed and more disturbed, are known to be less suitable for breeding than central ones (Spurr 1972), so that the distribution of less aggressive penguins at the

615

periphery may be the result of competition. In most cases, only aggressive penguins will be able to establish themselves in the centre. Sometimes, however, less aggressive penguins may become established in the centre because of an opportunistic lack of competition. This may well account for the presence of some males of average aggressiveness in the centre of a colony, as in Fig. 4. Once they are established, mature penguins (especially males) exhibit a high degree of site tenacity (Penney 1968), but to do this they must defend the territory against young penguins seeking to establish themselves. Competition, however, may be expressed in ways other than by brute strength. Thus, successful defence of a territory is greatly assisted by the advantages of previous ownership (Spurr 1972). Also, early return ensures that a territory is regained without first having to fight for it, though date of return may be influenced by competition at sea (see below). Without fighting for a territory, late returning penguins can usually nest only at the colony periphery. Penguins in the centre of a colony tend to be more successful breeders (Spurr 1972) as well as more aggressive than penguins at the colony periphery. Furthermore, the most aggressive penguins in this study had the highest breeding success. The correlation between aggressiveness and breeding success, however, may not be direct, since the two may be associated because of some other factor(s). It is likely that differences in responses to the model of individual penguins at the same point in the breeding cycle are influenced by several factors, such as age, experience, inherent aggressiveness, and physical condition. Thus, in some pairs, males may have been of similar age to females, while in other pairs they may have been either younger or older. Perhaps this may account for some males being less aggressive and others more aggressive than their partners. It is also possible that younger penguins tend to nest at the colony periphery, have smaller average clutches, lay later in the season, are less aggressive, and are less successful breeders than more mature penguins. Certainly, peripheral breeding, single-egg clutches, late laying, and unsuccessful breeding are positively associated (Spurr 1972). Further studies are needed to assess the relation of different factors to one another, especially age and experience to aggressiveness. Thus, inherent differences in aggressiveness can be determined only from penguins of known age.

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Selection will favour aggressiveness because it is advantageous for maintaining a prime (central) breeding site within the colonies, and probably influences feeding rights at sea. When a feeding-flock of penguins discover a swarm of krill (Euphausia spp.), the dominant individuals may be able to feed more efficiently (obtaining more food in a shorter time). Dominance at sea, in fact, may be a prerequisite for dominance in the breeding colonies (Carrick & Ingham t967). Those penguins that obtain sufficient food to come into reproductive condition early in the season, will be able to return early to the breeding colonies, and obtain (and maintain) a prime breeding site. Selection will also prevent 'over-aggressiveness', because it is necessary that penguins remain within aggregated groups, both on land (for successful breeding) and at sea (for feeding and protection against predators). Also, penguins must not spend all their time defending the territory, or be too aggressive to mate.

Acknowledgments This work was done while I was a member of the University of Canterbury Antarctic Research Unit. Field support was provided by the Antarctic Division, D.S.I.R. (Wellington, New Zealand), and logistic support by the U.S. Navy VXE-6 squadron. Penguin bands were supplied by Dr W. J. L. Sladen of the U S A R P bird-banding program.

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I am grateful to Professor E. C. Young for encouragement and assistance in the field, and to Dr V. Benzie and my wife, Barbara, for critically reading the manuscript.

REFERENCES Carrick, R. & Ingham, S. E. (1967). Antarctic sea-birds as subjects for ecological research. Japan Antarctic Research Expedition Scientific Reports Special Issue, 1, 151-184. Coulson, J. C. (1968). Differences in the quality of birds nesting in the centre and on the edges of a colony. Nature, Lond., 217, 478--479. Penney, R. L. (1968). Territorial and social behaviour in the Adelie penguin. Antarctic Research Series, 12, 83-131. Sladen, W. J. L. (1958). The Pygoscelid penguins. I. Methods of Study. II. The Adelie penguin Pygoscelis adeliae (Hombron & Jacquinot). Falkland lslands Dependencies Survey Scientific Reports, 17, 1-97. 9Spurr, E. B. (1972). 'Social Organisation of the Adelie Penguin, Pygoscelis adeliae'. PhD. Thesis, University of Canterbury, Christchurch, New Zealand. 169 pp. Spurt, E. B. (in press). Communication in the Adelie penguin. In: The Biology of Penguins (Ed. by B. Stonehouse). London: Macmillan. Vowles, D. M. & Harwood, D. (1966). The effect of exogenous hormones on aggressive and defensive behaviour in the ring dove (Streptopelia risoria). J. Endocr., 36, 35-51. (Received 10 July 1973; revised 13 November 1973; MS. number: 1236)