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Individual differences in aggressiveness and food stealing among wintering oystercatchers, Haematopus ostralegus L
Anita. Behav., 1982, 30, 917-928 INDIVIDUAL STEALING
DIFFERENCES AMONG
IN AGGRESSIVENESS
WINTERING
HAEMATOPUS
AND
FOOD
OYSTERCATCHERS,
OSTRALEGUS
L.
BY J. D. GOSS-CUSTARD, S. E. A. LE V. DIT D U R E L L & B. J. ENS*
Institute of Terrestrial Ecology, Furzebrook Research Station, Wareham, Dorset BH20 5AS Abstract. Oystercatchers feeding on mussels foraged in small, overlapping areas and aggressive encounters were common amongst all birds irrespective of their method of opening mussels. Individuals varied consistently in aggressiveness. The more aggressive birds were more frequently present on the mussel bed, fed in those parts where food was most abundant, and were more successful in stealing mussels from other birds. Only the more aggressive birds stole more mussels than they had stolen from them, and stealing increased their rate of food intake. Aggressive encounters between oystercatchers (Haematopus ostralegus L.) feeding on mussels (Mytilus edulis L.) in winter are very common, and mostly concerned with food (Vines 1980). Usually, the encounters involve attempts by one bird to steal a mussel that has been found, and perhaps partly opened, by another. Vines (1980) showed that the risk of a bird being robbed declined as its distance from an aggressor increased, and suggested that oystercatchers spaced themselves out over the mussel bed in order to reduce their chances of being robbed. However, the birds were not individually marked in this study so it was not possible to test for consistent individual differences in social or spatial behaviour. Although the observations suggested that most birds attempted to steal mussels, the extent of the individual variations and the possibility that some birds specialized in stealing mussels (Brockmann & Barnard 1979) could not be examined. This paper describes a study on the individual differences in the behaviour of oystercatchers foraging on a mussel bed on the Exe estuary, South Devon. It describes the spatial behaviour of a sample of colour-marked individuals and compares their aggressiveness, particularly food stealing. Though it is usually assumed that stealing does increase the intake rate of the aggressor, and losing mussels decreases the intake rate of the victim, this may not be so. For instance, stealing food may simply be an alternative to searching for achieving a particular rate of intake. While Caldwell (1980) showed that egrets increased their intake rate by displacing other birds from feeding sites, this has not been shown for birds stealing food items. *Department of Zoology, University of Groningen, Haren (Gr.), The Netherlands.
The contribution that stealing mussels made to the intake rate of different oystercatchers was therefore measured, and the profitability of stealing assessed. A complicating factor in this study was that mussels were opened in three ways and individuals almost invariably used one method (NortonGriffiths 1967). Since we were primarily interested in individual differences and could only study a small sample of birds using each feeding method, we first tested whether the data from all birds could be treated together. Therefore, the behaviour of birds from the three feeding groups is compared before the individual comparisons are made. Methods The mussel beds of the Exe estuary are described by Goss-Custard et al. (in press a). Our studies onbehaviour were made on bed 4 near Cockwood (Fig. 1) because of its ease of access. This bed was quickly occupied as the birds returned in the autumn and high densities (40 birds per ha) were recorded there. Though not the most preferred bed, it was a highly favoured feeding area. Approximately 1 0 ~ of the oystercatchers on the bed were individually colour-marked using the ringing scheme described in GossCustard et al. (1980). The bed was marked out with stones in 50-m squares and the observer sat on the sea-wall overlooking it. Birds were watched throughout 21 low-water periods between 1 November 1979 and 15 February 1980, after which birds began to leave the estuary. Five further watches were made before 31 March, by which time all but one of the marked birds had left. A further eight watches were made during August and September 1980. Observations were often made as the tide
917
918
ANIMAL
BEHAVIOUR,
ebbed and flowed. The bed was searched regularly and the positions of any marked bird recorded. This was done so often that most birds present would have been seen. In addition, we also tried to watch each bird for 5 or 10 rain to record its feeding rate and encounters with other birds, but tended to concentrate on the regular visitors to the bed. The position of the birds at the beginning and end of each 5- or 10min period was noted. The bed was also watched for short periods on a number of other occasions during the winter and the positions of some of the birds noted. All the sightings of each bird during a season were mapped and the outermost ones joined up to describe its feeding area. The size of the area drawn this way depends on the numbers of observations made. However, four birds were seen on at least 35 occasions in 1979/80 and the size of the area used by each one had reached its asymptote by 30 sightings. An average of 60 % of the maximum was obtained after 10 sightings and 80% by 20. Since the position of most birds was recorded on at least 10 occasions and the mean was 19 in 1979/80 and 13 in 1980/81, most feeding areas were reasonably well defined. In a more detailed study, a smaller number of individuals was watched in a limited area of the bed almost daily for 3 months during autumn
Fig. 1. The mussel beds in the lower reaches of the Exe estuary.
30,
3
1980. These observations were made from a hide on a tower 3 m high situated in the middle of the area. The area was subdivided into 25 x 25-m quadrats with b a m b o o sticks. The amount of time spent by each of 10 individuals in each square was recorded regularly. The proportion of a bird's total foraging time spent in each quadrat could then be calculated, providing a more precise description of feeding range. Ten samples of mussels were taken at random from each 50 x 50-m square in December 1979. Each sample measured 20 x 20 cm, and all the mussels over 20 m m long were measured. The ash-free dry weights of a sub-sample of 30 mussels covering a wide size range were determined for each square. The regression of log length on log dry weight was calculated and used to estimate the weight of a mussel 55 m m long, a typical size eaten by oystercatchers on the Exe (Goss-Custard et al. 1980). The thickness of the shells on the ventral side was measured in a further 30 mussels from each square and, from the regression line relating length to shell thickness, the thickness of the shell of a mussel 50 m m long was calculated. The density of mussels was calculated for those over 30 m m long, the size range from which oystercatchers obtained most of their food. Mussel size was measured as volume of flesh by calculating length in millimetres to the power 2.85, the average exponent relating length to weight for mussels on the Exe.
Results General Features of Behaviour A total of 61 colour-marked individuals were seen during the first winter, but almost half only once or twice (Fig. 2). The remainder were seen on up to 21 days, but there was no clear peak in frequency of occurrence. The birds cannot be divided simply into those that occurred only once or twice and those that were present on m o s t occasions: all degrees of attendance were recorded. We could not collect an adequate sample of data from individuals that occurred only occasionally on the bed, so most of our analysis is restricted to the 28 birds that were seen on five or more occasions. For convenience we call these 'regular visitors', the remainder being classed as transients. Although 54 % of the birds seen throughout the winter were transients, on average only 19% of those present on any one tide were in this category. Feeding method and feeding site. Oystercatchers opened mussels in three ways. One was to stab into gaping mussels, and another to pull the
GOSS-CUSTARD ET AL.: FOOD STEALING IN OYSTERCATCHERS 25
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Fig. 2. The frequency of occurrence of individual birds on bed 4 during 21 low-tide watches in the winter 1979/80. mussel from the clump and hammer the shell on the ventral side until it cracked. Both methods were described by Norton-Griffiths (1967). On the Exe, oystercatchers also hammered into mussels in situ and therefore cracked the shell on the dorsal side, usually at the point where the adductor muscle is attached to the mussel shell. We called these methods stabbing, ventral hammering and dorsal hammering, and found that in winter 27 individuals used only one technique while the other bird almost invariably hammered mussels dorsally. Ten regulars on bed 4 used ventral hammering, nine used dorsal hammering and nine used stabbing. Individuals foraged in restricted areas for the whole winter (Fig. 3). Birds which returned in the second year and were studied by us usually fed near where they had been in the previous winter. The detailed observations in the autumn of 1980 show that some birds restricted most of their foraging to very small areas indeed. Despite this, i t is clear that the areas used by individuals overlapped considerably. They did not feed in mutually exclusive territories. As Norton-Griffiths (1967) also showed, birds using different techniques fed in different places. The ventral hammerers fed downshore where the substrate was firm and hammering was easiest, whereas stabbers fed in the wetter and muddier areas upshore. The area used by the dorsal hammerers overlapped with that used by the stabbing birds, presumably because
919
mussels in a clump could be hammered without being driven too deep into the substrate. Comparison of feeding groups. The behaviour of regular visitors feeding by each method was compared by analysis of variance of the rates at which particular activities were performed. The data were collected at low tide throughout the winter of 1979/80 (1 November-28 February). In many cases a particular behaviour was so rare that it was more a p p r o p r a t e to analyse the proportion of 5-rain periods in which it occurred than to deal directly with mean rates. This applied particularly to encounters between birds. Table I compares the rates at which birds clearly found mussels themselves or stole them from other birds and the rates at which mussels were given up, lost to other birds or swallowed. Mussels labelled 'given up' were those that were picked up and carried before being rejected. We realize that many others might be attempted and rejected quickly, but it was difficult to measure this. Consequently, we simply noted the ones which were carried first, as these were clearly identifiable and wasted most searching time. The category 'found' included mussels like this which were eventually rejected. Ventral hammerers found more than dorsal hammerers which in turn found more than stabbers. However, ventral hammerers carried and rej e c t e d considerably more than dorsal hammerers while stabbers carried and rejected very few. There was no significant difference between groups in the numbers stolen from or lost to other birds. T h e overall result was that there were no significant differences between groups in the rates at which mussels were swallowed. The handling times did differ between groups: ventral hammerers t o o k over twice as long to deal with a lrmssel than did stabbers, while dorsal hammerers were intermediate. The percentage of encounters involving mussels was similar in each group of regular visitors, being 52 • 8 in the ventral hammerers, 57 :k I0 in the dorsal hammerers and 65 -4- 7 in the stabbing birds. The rates at which birds were involved in encounters with Other oystercatchers f o r mussels or for other reasons did not differ between groups either (Table II). However, ventral hammerers were attacked more often by crows (Corvus corone) than were either dorsal hammerers or stabbers, perhaps because of their longer handling time or because more crows fed where the ventral hammerers did.
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GOSS-CUSTARD ET AL.: FOOD STEALING IN OYSTERCATCHERS
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Table II. Mean Rates at which Birds Using Each Feeding Method were Involved in Encounters of Various Types (Means 4- SE: all tests of significance by analysis of proportions) Ventral hammerers (V) s~ Numbers of times per 5 min: Attacked by crow: Attacked by oystercatchers: (i) for mussels (ii) for other reasons (iii) for all reasons Attacks of oystercatchers: (i) for mussels (ii) for other reasons (iii) for all reasons
Dorsal hammerers(D) R sB
(N = 159) 0.189 4- 0.039
(N = 168) 0.077 4- 0.02I
0.176 -_Jz0.037 0.088 4- 0.033 0.258 4- 0.051
0.214" 4- 0.057 0.060 4- 0.020 0.274 4- 0.041
0.170 4- 0.039 0.195"** 4- 0.084 0.359*** 4- 0.118
0.167" 4- 0.072 0.131 4- 0.027 0.298***4- 0.085
Stabbers (S) R sE
Significance of differencebetween groups
(N = 149) 0.094 4- 0.042 V > S V>D 0.107"* 4- 0.049 0.114 4- 0.028 0.215 4- 0.068 0.242*4-0.086 0.141"'4-0.056 0.389"*'4-0.143
(P<0.01) (P<0.05) Ns NS NS Ns NS NS
Significance of differences between individuals within a group: *P < 0.05, **P < 0.01, ***P < 0.001. Birds using different methods of feeding attacked each other regularly and there is no evidence that a bird's feeding method influenced its choice of victim. Of the 65 encounters in which the feeding method of both participants was known, only 40 % involved birds belonging to the same feeding group. Table III compares the success with which birds of known feeding method either attacked others or defended themselves against others, whose feeding methods were not usually known. There were no significant differences in the proportions between groups, whether or not mussels were involved. Most attacks which did not involve mussels resulted in the victim running away. The possible outcomes are more varied in the case of encounters over mussels, and these are detailed for all encounters, irrespective of feeding method, in Table IV. The victim retained the mussel in over half of encounters, almost always by carrying it away so the attacker gave up. Often the victim dropped the mussel but the attacker failed to locate it afterwards. In only 21% of encounters did the attacking bird actually steaI the mussel, and in some cases much of the flesh would already have been consumed by the victim. The regular visitors in each group were seen on the bed on a similar number of occasions. The mean q- SE number of tides on which birds were seen were 10.7 ~: 1.6 (N = 10) for ventral hammerers, 14.9 • 1.70 ( N = 9) for dorsal hammerers and 12.6 • 1.79 (N : 9) for stabbers, none of the comparisons being significant at 5 % level (t-test). Thus the behaviour of the groups was similar in most respects, both when feeding rates and social behaviour were compared. The main
differences are that hammerers took longer to open their mussels, found more but gave up on a higher proportion, and lost more to crows. But in every other respect, the behaviour of the regular visitors in the groups was similar, and data from all groups were combined for the analysis of individual variations in behaviour. IndMdual Variations in the Behaviour of Regular Visitors A striking feature of the results is the differences between individuals in the rates at which many o f the social and feeding activities were performed. These could be due either to basic features of the bird, such as its age or genetic characteristics, or to environmental factors, such as food supply, population density, weather, tidal conditions or season. The last three can be ruled out because the differences between individuals were clearly consistent whatever the weather, tide or season. Bird density was not measured in this study. Accordingly, the observations made in the winter 1979/80 at low tide when bird density was lowest and least variable are mainly considered in this paper. Genetic characteristics were not studied and 21 of the 28 residents were adult when ringed so their age was not known exactly. Consequently, only relationships between food supply and a bird's social and feeding activities can be examined here. Frequency of occurrence on file bed. The number of times birds were seen on the bed varied between individuals (Fig. 2). The numbers of low-tide periods during which birds were seen were regressed against the density, size, ash-free dry weight and shell-thickness of the
GOSS-CUSTARD ET AL. : FOOD STEALING IN OYSTERCATCHERS
923
Table Ill. The Outcome of Attacks amongst Oystercatchers in Each Feeding Group (Figures show percentages where N is the total number of encounters seen. ? : outcome uncertain) (i) Attacks involving mussels
Subject bird attacks others and: SteMs N mussel ? Ventral hammerer Dorsal hammerer Stabber All
Subject bird is attacked and: Keeps
N
mussel
?
35 42 57
22.9 11.9 21.1
0 0 1.8
30 72 41
40.0 58.3 56.1
0 4.2 0
134
18.7
0.8
143
53.9
2.1
(ii) Attacks not involving mussels
Ventral hammerer Dorsal hammerer Stabber All
Subject attacks and other: N runs away ?
Subject is attacked and it N runs away
37 38 36
100 95 90
0 5 5
22 22 29
100 96 100
115
94
4
73
99
mussels a n d the softness a n d flatness o f the substrate in the localities where birds fed t h r o u g h o u t the winter. O n l y the density, size a n d shellthickness o f the mussels were selected b y stepwise multiple regression, giving a multiple correlation coefficient o f 0.685. T h e p a r t i a l correlation coefficients for each variable were: mussel density, r = + 0.631, P < 0.01; mussel size, r = + 0.475, P < 0.05; shell thickness, r - - - 0 . 6 3 2 , P < 0.01. Birds t h a t occurred frequently on bed 4 h a d feeding areas where the mussels were n u m e r o u s , large a n d thin-shelled. A g g r e s s i v e encounters. T h e rates at which birds a t t a c k e d others, w h e t h e r f o r mussels o r for o t h e r reasons, often differed significantly between individuals (Table If). However, the rates at which individuals a t t a c k e d others for mussels a n d for other reasons were c o r r e l a t e d with each o t h e r (r = + 0.576, P < 0.01, N = 28). Consequently, the rate at which a b i r d initiated attacks against others for all reasons, i.e. b o t h rates combined, was used as a m e a s u r e o f its aggressiveness, a n d highly significant differences a m o n g individuals were f o u n d (Table II). O f course, this m e a s u r e o f aggressiveness correlated closely with b o t h o f its constituents, i.e. rates o f a t t a c k i n g for mussels (r = + 0.841) a n d for other reasons (r = + 0.863). T h e rate at which a bird a t t a c k e d others was n o t correlated with a n y aspect o f the f o o d supply or with h o w m a n y mussels it f o u n d or gave up,
o r on h o w long it t o o k to open each o f t h e m or h o w m u c h time it spent p e r 5 m i n o p e n i n g mussels. This a p p l i e d w h e t h e r simple o r p a r t i a l coefficients were calculated. However, aggressiveness was correlated with h o w m a n y times a b i r d was seen on the bed (r = + 0.430, P < 0.02, N = 28). T h e m o r e frequently a b i r d occurred on b e d 4, the m o r e aggressive it was (Fig. 4). There were n o significant differences between individuals in the rate at which they were a t t a c k e d by o t h e r oystercatchers when mussels were n o t involved, o r when all encounters were c o m b i n e d (Table II). However, individuals often differed in the rate at which they were a t t a c k e d f o r mussels. This was n o t correlated, using either simple or p a r t i a l correlation analysis, with h o w often the birds occurred on b e d 4 o r t h e f o o d supply, b u t only on h o w m a n y mussels they f o u n d per 5 rain Table IV. Outcome of 277 Encounters Over Mussels
Percentage of encounters Attacker steals mussel and eats it Victim drops mussel but attacker fails to locate it Victim drops mussel but outcome unknown Victim defends mussel and keeps it Victim runs away with mussel and keeps it
20.6 19.5 4.3 1.1 54.5
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(r = + 0.363, P < 0.05). Birds which found more mussels were attacked more often, presumably because they were thereby more often in a position to have food stolen. We think that the rate birds found mussels was partly related to the sizes they took. Handling time and feeding rate were negatively correlated amongst ventral hammerers (r = --0.742, P < 0.02, N = 10) and stabbers (r = --0.824, P < 0.01, N = 9), though not significantly in dorsal hammerers (r = --0.324, N = 9). Birds that fed fast had short handling times, probably because they ate small mussels. This probably depended on the sizes of mussels available in the exact places the birds were feeding. We expected that the more aggressive birds would be attacked less often themselves by other birds, but none of the correlations between the aggressiveness of a bird and how often it was attacked by other oystercatchers reached statistical significance. However, all the relationships were negative: for attacks involving mussels, r = --0.073; for attacks made for other reasons, r = --0.155; for both kinds of attacks combined, r = - - 0 . 2 4 1 ; and for the number of mussels actually stolen, r = - - 0 . 1 0 7 . Similarl.y, the correlations between a bird's aggressweness and how often it was attacked by crows (r = --0.245) and had mussels stolen from it by them ( r = - - 0 . 2 3 2 ) were both negative but not
3
significantly so (N = 28 in all cases). Clearly there is a suggestion that aggressive birds were attacked least often, as confirmed by later studies on a smaller number of individuals (Ens & Goss-Custard, in preparation). Aggressiveness and success in encounters. There were not enough data from the 28 individuals studied in the winter of 1979/80 to test whether aggressive birds were more successful in encounters than the less aggressive ones. However, the detailed studies in autumn 1980 allowed this possibility to be examined. A bird was considered to be successful when: (I) it succeeded in driving away a bird it had attacked or did not flee when it was itself attacked in encounters in which mussels were not involved; or (II) it succeeded in stealing a mussel from another or defended its own mussel either by fighting or by running away. The proportion of encounters in which a bird was involved where it was successful, was highly correlated with aggressiveness in the 10 birds studied in the autumn of 1980 (Fig. 5). Since the aggressiveness of birds in the autumn of 1980 and during the preceding winter were highly correlated (r = +0.864, P < 0.01, N = 8), it can be safely assumed that a bird's aggressiveness in 1979/80 was a good indication of its success in encounters in that year as well. Effect of robbing on profitability. Stealing a mussel from another oystercatcher is likely to enhance the rate of food intake of the aggressor because time does not have to be spent in search-
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Fig. 5. T h e aggressiveness o f an individual in relation to
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GOSS-CUSTARD ET AL.: FOOD STEALING IN OYSTERCATCHERS ing for, and perhaps opening, the mussel. Conversely, the victim is likely to suffer a reduced rate of intake. This was tested by comparing the intake rate of a bird during a 5rain period in which it was involved in an encounter of one kind or another with its intake rate during an adjacent 5-rain period in which no encounter occurred. The data from all birds were combined and are summarized in Table V. Birds which stole a mussel increased their intake rate, yet unsuccessful attacks did not decrease it by much. Even though 80 % of attacks resulted in failure to obtain a mussel (Table IV), there was little penalty for failure as attacks were executed so quickly and successes were beneficial. Birds which were attacked did not suffer a significant reduction in rate of intake unless the mussel was actually lost. Attacks which did not involve mussels had little effect on intake rate. The conclusion is that stealing mussels was profitable and, since the rate of attacking other oystercatchers for mussels was not related to how many mussels the aggressor was finding, it was a genuine gain and not simply an alternative way of obtaining the same number of mussels. The rate of stealing mussels was closely correlated with a bird's aggressiveness (r = 0.669, P < 0.001), whereas the rate it lost mussels was only poorly related (r = - - 0 . 1 0 7 ) . Because of this the difference between stealing and losing mussels, the net gain from encounters over mussels, was correlated with aggressiveness (r = +0.401, P < 0.02, N =: 28: Fig. 6). Stealing mussels more than compensated for those lost by the most aggressive birds, but not in the case of the least aggressive ones. Contribution of robbing to overall intake rate.
Even though individuals differed significantly in how often they attacked other birds and this affected the net gain in encounters over mussels, there were few significant differences between
925
individuals in the rates at which they stole from or lost mussels to other oystereatchers (Table I). This may have been because the contribution which stealing and losing mussels made to total intake was small, and therefore variations in them difficult to detect. On average across all 28 birds, only 3.8 % of mussels were stolen and 4.3 % lost in encounters with oystercatchers and 7.3% with crows. Stealing and losing mussels involved only a small minority of the prey items handled by oystercatehers. However, there was considerable variation among individuals, and some obtained a considerable proportion of their food by stealing. Two obtained over 20 of their mussels by stealing, three obtained 1020% and four obtained 5-10%. Furthermore, the numbers stolen and lost, and therefore the net gain, made a significant contribution to individual variations in feeding rate (Table VI). By expressingthe contribution of each as standard partial regression coefficients, it is clear that the major source of variation between individuals was in how many they found rather than in the number they stole or lost. Though the rate of net gain of mussels made a significant contribution to total intake, it was small compared with the numbers found. Comparison of Regular Visitors and Transients
The relationship between how frequently a bird occurred on the bed and its behaviour is confirmed by comparing the behaviour of transients, which fed all over the bed, with that of regular visitors. Each feeding record on a transient was compared with the nearest record of a resident feeding with the same technique in the same place on the same day, so that all other factors would be held constant. Regulars found and swallowed significantly more mussels than transients (Table VII), but the agonistic behaviour of the groups was not significantly different. However, the largest
Table V. Intake Rate of Mussels in 5-rain Periods in which Various Encounters Occurred, Compared with Control Periods where No Encounters Occurred
Encounter 27 sE
.~"
Control SE
t
P (one.tailed)
Kind of encounter
N
Fails to steal mussel
Steals mussel successfully
16 18
1.44 0.57
0.15 0.12
0.81 0.67
0.16 0.16
2.81 0.55
< 0.01 NS
Loses mussel
Attacked but keeps mussel
19 37
0.53 1.14
0.16 0.10
1.00 1.19
0.19 0.13
1.95 0.33
< 0.05 Ns
Attacks another or is attacked but no mussel involved
21
0.91
0.28
0.81
0.18
0.29
NS
926
ANIMAL
"Jr-
BEHAVIOUR,
30,
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9 9 1"0 ATTACKS/5 MIN
NET GAiN
.3
Fig. 6. The net gain or loss from stealing and losingmussels in relation to the aggressiveness of a bird. t-values were obtained in those activities which, amongst residents, varied significantly according to period of residency, Regulars attacked others and stole more mussels than did transients in this sample. In contrast, the rates at which birds were attacked by other oystercatchers were similar. These comparisons parallel the trends found amongst the regulars. Discussion
Individuals varied in how often they occurred on bed 4 during the winter. Some birds were present on virtually all the low-tide periods we searched for them, but others were not. The missing birds would have been feeding on other mussel beds on the Exe because (1) most oystercatchers remained on this estuary throughout the winter (Goss-Custard et al., in press b), and (2) m o s t birds that fed on mussels ate almost nothing else (Goss-Custard & Durell, in press).
We did not study the factors which determined whether or not a bird would be present on bed 4. We suspect that disturbance by people on other beds was important. Several of our regular visitors were seen on the adjacent bed 3 and were only seen on bed 4 when that bed was disturbed. The height of the tide may also have been important. Some mussel beds were not exposed even at low water on neap tides yet many birds fed there on spring tides. Some birds may also have been displaced by other oystercatchers from more preferred mussel beds (Goss Custard et al., in press a). Most of the birds on bed 4 restricted their foraging to small areas irrespective of how frequently they occurred on the bed. Furthermore, most of the birds that returned in the second winter fed in almost the same place and, as already shown by Norton-Griffiths (1968), used the same method for opening mussels.
Table VI. Standard Partial Regression Coefficients between the Numbers of Mussels Swallowed per 5 rain and the Numbers Found (excluding those given up), Stolen and Lost to Oystereatchers or Crows ( N = 28)
Standard partial t regression coefficient value (1) Numbers found (2) Numbers stolen (3) Numbers lost to oystercatchers (4) Numbers lost to crows (2)--(3) Net gain
+ 1.105 +0.166 --0.238 --0.320 +0.378
22.0 3.59 5.68 6.86 2.25
P < < < < <
0.001 0.001 0.001 0.001 0.05
927
GOSS-CUSTARD ET AL.: FOOD STEALING IN OYSTERCATCHERS Table VII. Comparison of the Behaviour of Regulars and Transients on Bed 4 (N = 49 except for handling time where N = 25)
Regulars X
No. found and opened or stolen by others No. stolen from others No. lost to oystercatchers No. swallowed Handling time No. times attacked others No. times attacked by oystercatchers
sE
1.286 =L0.127 0.082 -t- 0.040 0.031 4- 0.017 1.225 -t- 0.102 118.6 :t: 13.8 0.225 • 0.079 0.225 -t- 0.067
Although aggressive encounters were common, birds did not defend exclusive feeding territories. There was a considerable overlap in the area used by different regular visitors and transient birds also fed in areas used by the regulars. The considerable amount of overlap in feeding areas and the high densities of oystercatchers on bed 4 no doubt contributed to the high incidence of aggression that occurred there. As in Vines' (1980) study, a majority of the encounters were attempts to steal mussels. However, a mussel was not obviously involved in 35-48% of the encounters, depending on the feeding group. In some cases, we may not have realized that a mussel was actually involved. In others, the aggressor may have attacked to gain a feeding site rather than a particular mussel (Vines 1980). However, neither mussels nor feeding sites s e e m e d to be involved in some encounters, because the victim was not actually dealing with a mussel when attacked and, after the encounter, the aggressor did not feed where the victim had been previously. Piping displays (Heppleston 1970) were also common, and mussels were seldom involved in these. We think that encounters of these kinds were either concerned with attempts to establish dominance over another bird or with driving it from the area altogether. Neither possibility has yet been tested. Most of the birds attacked others and were themselves frequently attacked. There is no evidence that certain individuals specialized in stealing mussels, as has been suggested for some kleptoparasitic birds (e.g. Brockmann & Barnard 1979). However, there were considerable individual differences. Some birds were particularly aggressive and successful in stealing, and perhaps also in defending, mussels. These differences were consistent throughout the winter and, indeed, from one winter to the next. We have
Transients X
sE
0.918• 0.127 0.020i 0.020 0.123_-4=0.054 0.888~ 0.123 124.2 :t= 13.6 0.102• 0.044 0.204~ 0.065
t
P
2.05 1.38 1.63 2.10 0.30 1.36 0.22
< 0.05 NS NS < 0.05 NS NS NS
not studied the characteristics of the birds which affected their aggressiveness and success in encounters, but did show that birds that were most frequently on bed 4 were generally the most aggressive. This might suggest that familiarity with an area was important, but it is difficult to distinguish cause from effect, because only birds that were already aggressive may have been able to maintain themselves in one area for long periods. Similarly, adults were in general dominant to immatures (Goss-Custard e t al., in press a), but we cannot separate the effect of familiarity with the Exe Estuary and some other attribute associated with age in determining dominance. There were striking similarities between the results of this study on one bed and those of another in which all the mussel beds were compared (Goss-Custard et al., in press a). In that study, immature oystercatchers were less aggressive, less successful in encounters over mussels, and avoided other birds much more frequently than adults. In the summer, most birds were immatures and fed on a few beds which were preferred because they had a firm substrate and were close to the highwater roost. As the adults returned from the breeding areas, most of the immatures left the preferred beds and so were found in winter on less-preferred areas. T h e s e were not only further from the roost and with a softer substrate, but also contained fewer mussels which were, in general, smaller and thickershelled (Goss-Custard et al. 1981). In other words, the more aggresNve adult birds fed disproportionately on mussel beds where the mussels were dense, large and thin-shelled, in just the same way as did the aggressive individuals within bed 4. Adults also changed beds less often than did immatures and were more likely to return to the same mussel bed in successive winters, just as aggressive birds on
928
ANIMAL
BEHAVIOUR,
bed 4 were faithful to their feeding ranges a n d m a n y birds returned to the same p a r t o f the b e d in 1980. Therefore, the b e h a v i o u r o f birds o f different aggressiveness over the whole estuary was consistent with the results o f the m o r e detailed studies carried o u t on bed 4. H i g h aggressiveness was correlated with several benefits. T h o u g h the direction o f cause a n d effect is unclear, the m o s t aggressive birds fed in those parts o f the bed where mussels were large, dense a n d thin-shelled. W e suspect that one o r all o f these factors affected rate o f intake, t h o u g h the picture was c o m p l i c a t e d by the presence o f three different feeding m e t h o d s which c o u l d be affected b y different factors. The most aggressive birds also o c c u r r e d m o s t often in their feeding a r e a a n d so h a d m o r e chance to l e a r n h o w best to exploit it. F a m i l i a r i t y with the area m a y be one reason w h y regular visitors found, a n d swallowed, m o r e mussels t h a n transients feeding in the same place. Second, the m o s t aggressive birds were m o r e likely to be in credit in encounters with o t h e r birds over mussels. Aggressive birds were often a t t a c k e d b u t they stole m o r e t h a n they lost to others a n d this increased their rate o f i n t a k e significantly. Indeed, the m o s t aggressive birds o b t a i n e d 20 ~ o f their mussels this way. Finally, some encounters were very vigorous a n d feathers were lost. T h o u g h the cost o f this was n o t measured, it m a y have h a p p e n e d least a m o n g the m o s t aggressive i n d M d u a l s .
Acknowledgments W e w o u l d like to t h a n k the m e m b e r s o f the D a w l i s h W a r r e n N a t u r e Reserve M a n a g e m e n t C o m m i t t e e for permission to ring birds, and D r D. Jenkins, D r S. M c G r o r t y a n d D r C. J. R e a d i n g for c o m m e n t i n g on the manuscript. W e are very grateful to R. J. Clarke for help
30,
3
with the statistical analysis. W e are also i n d e b t e d to D r C. Perrins for p r o v i d i n g space a n d facilities f o r one o f us (B. J. Ens) to analyse some o f the results at the E d w a r d G r e y Institute.
REFERENCES Brockmann, H. J. & Bamard, C. J. 1979. Kleptoparasitism in birds. Anim. Behav., 27, 487-514. Caldwell, (3. S. 1980. Underlying benefits of foraging aggression in egrets. Ecology, 61, 996. Gess-Custard, J. D. & Durell, S. In press. Individual and age differences in the feeding ecology of oystercatchers, Haematopus ostralegus, wintering on the Exe Estuary, S. Devon. Ibis. Goss-Custard, J. D., Durell, S., McGrorty, S., Reading, C. J. & Clarke, R. T. 1981. Factors affecting the occupation of mussel )14ytilns edulis beds by oystercatchers, Haematopus ostralegus on the Exe Estuary, Devon. In: Feeding andSurvivalStrategies of Estuarine Organisms (Ed. by N. V. Jones & W. J. Wolff), pp. 21%229. London: Plenum Press. Goss-Custard, J. D., Durell, S., McGrorty, S. & Reading, C. J. In press a. Use of mussel Mytilus edutfs beds by oystercatchers Haematopus ostraIegus according to age and population size. J. Anita. Ecol. Goss-Custard, J. D., Durell, S., Sitters, H. P. & Swinfen, R. In press b. Age-structure and survival of a wintering population of oystercatchers, Haematopus ostralegns. Bird Study. Goss-Custard, J. D., McGrorty, S., Reading, C. J. & Durell, S. 1980. Oystercatchers and mussels on the Exe Estuary. Devon Ass., Special Vol. 2, 161-185. Heppleston, P. B. 1970. The function of oystercatcher piping behaviour. Br. Birds, 63, 133-135. Norton-Griffiths, M. 1967. Some ecological aspects of the feeding behaviour of the oystercatcher, Haematopus ostralegus, On the edible mussel, Mytilus edulis. Ibis, 109, 414-424. Norton-Griffiths, M. 1968. The feeding behaviour of the oystercatcher, Haematopus ostralegus. Unpublished Ph.D. thesis, University of Oxford. Vines, G. 1980. Spatial consequences of aggressive behaviour in flocks of oystercatchers, IIaematopus ostralegns L. Anita. Behav., 28, 1175-1183. (Received 29 October 1981; revised 7 December 1981; MS. number: 2187)
DIFFERENCES AMONG
IN AGGRESSIVENESS
WINTERING
HAEMATOPUS
AND
FOOD
OYSTERCATCHERS,
OSTRALEGUS
L.
BY J. D. GOSS-CUSTARD, S. E. A. LE V. DIT D U R E L L & B. J. ENS*
Institute of Terrestrial Ecology, Furzebrook Research Station, Wareham, Dorset BH20 5AS Abstract. Oystercatchers feeding on mussels foraged in small, overlapping areas and aggressive encounters were common amongst all birds irrespective of their method of opening mussels. Individuals varied consistently in aggressiveness. The more aggressive birds were more frequently present on the mussel bed, fed in those parts where food was most abundant, and were more successful in stealing mussels from other birds. Only the more aggressive birds stole more mussels than they had stolen from them, and stealing increased their rate of food intake. Aggressive encounters between oystercatchers (Haematopus ostralegus L.) feeding on mussels (Mytilus edulis L.) in winter are very common, and mostly concerned with food (Vines 1980). Usually, the encounters involve attempts by one bird to steal a mussel that has been found, and perhaps partly opened, by another. Vines (1980) showed that the risk of a bird being robbed declined as its distance from an aggressor increased, and suggested that oystercatchers spaced themselves out over the mussel bed in order to reduce their chances of being robbed. However, the birds were not individually marked in this study so it was not possible to test for consistent individual differences in social or spatial behaviour. Although the observations suggested that most birds attempted to steal mussels, the extent of the individual variations and the possibility that some birds specialized in stealing mussels (Brockmann & Barnard 1979) could not be examined. This paper describes a study on the individual differences in the behaviour of oystercatchers foraging on a mussel bed on the Exe estuary, South Devon. It describes the spatial behaviour of a sample of colour-marked individuals and compares their aggressiveness, particularly food stealing. Though it is usually assumed that stealing does increase the intake rate of the aggressor, and losing mussels decreases the intake rate of the victim, this may not be so. For instance, stealing food may simply be an alternative to searching for achieving a particular rate of intake. While Caldwell (1980) showed that egrets increased their intake rate by displacing other birds from feeding sites, this has not been shown for birds stealing food items. *Department of Zoology, University of Groningen, Haren (Gr.), The Netherlands.
The contribution that stealing mussels made to the intake rate of different oystercatchers was therefore measured, and the profitability of stealing assessed. A complicating factor in this study was that mussels were opened in three ways and individuals almost invariably used one method (NortonGriffiths 1967). Since we were primarily interested in individual differences and could only study a small sample of birds using each feeding method, we first tested whether the data from all birds could be treated together. Therefore, the behaviour of birds from the three feeding groups is compared before the individual comparisons are made. Methods The mussel beds of the Exe estuary are described by Goss-Custard et al. (in press a). Our studies onbehaviour were made on bed 4 near Cockwood (Fig. 1) because of its ease of access. This bed was quickly occupied as the birds returned in the autumn and high densities (40 birds per ha) were recorded there. Though not the most preferred bed, it was a highly favoured feeding area. Approximately 1 0 ~ of the oystercatchers on the bed were individually colour-marked using the ringing scheme described in GossCustard et al. (1980). The bed was marked out with stones in 50-m squares and the observer sat on the sea-wall overlooking it. Birds were watched throughout 21 low-water periods between 1 November 1979 and 15 February 1980, after which birds began to leave the estuary. Five further watches were made before 31 March, by which time all but one of the marked birds had left. A further eight watches were made during August and September 1980. Observations were often made as the tide
917
918
ANIMAL
BEHAVIOUR,
ebbed and flowed. The bed was searched regularly and the positions of any marked bird recorded. This was done so often that most birds present would have been seen. In addition, we also tried to watch each bird for 5 or 10 rain to record its feeding rate and encounters with other birds, but tended to concentrate on the regular visitors to the bed. The position of the birds at the beginning and end of each 5- or 10min period was noted. The bed was also watched for short periods on a number of other occasions during the winter and the positions of some of the birds noted. All the sightings of each bird during a season were mapped and the outermost ones joined up to describe its feeding area. The size of the area drawn this way depends on the numbers of observations made. However, four birds were seen on at least 35 occasions in 1979/80 and the size of the area used by each one had reached its asymptote by 30 sightings. An average of 60 % of the maximum was obtained after 10 sightings and 80% by 20. Since the position of most birds was recorded on at least 10 occasions and the mean was 19 in 1979/80 and 13 in 1980/81, most feeding areas were reasonably well defined. In a more detailed study, a smaller number of individuals was watched in a limited area of the bed almost daily for 3 months during autumn
Fig. 1. The mussel beds in the lower reaches of the Exe estuary.
30,
3
1980. These observations were made from a hide on a tower 3 m high situated in the middle of the area. The area was subdivided into 25 x 25-m quadrats with b a m b o o sticks. The amount of time spent by each of 10 individuals in each square was recorded regularly. The proportion of a bird's total foraging time spent in each quadrat could then be calculated, providing a more precise description of feeding range. Ten samples of mussels were taken at random from each 50 x 50-m square in December 1979. Each sample measured 20 x 20 cm, and all the mussels over 20 m m long were measured. The ash-free dry weights of a sub-sample of 30 mussels covering a wide size range were determined for each square. The regression of log length on log dry weight was calculated and used to estimate the weight of a mussel 55 m m long, a typical size eaten by oystercatchers on the Exe (Goss-Custard et al. 1980). The thickness of the shells on the ventral side was measured in a further 30 mussels from each square and, from the regression line relating length to shell thickness, the thickness of the shell of a mussel 50 m m long was calculated. The density of mussels was calculated for those over 30 m m long, the size range from which oystercatchers obtained most of their food. Mussel size was measured as volume of flesh by calculating length in millimetres to the power 2.85, the average exponent relating length to weight for mussels on the Exe.
Results General Features of Behaviour A total of 61 colour-marked individuals were seen during the first winter, but almost half only once or twice (Fig. 2). The remainder were seen on up to 21 days, but there was no clear peak in frequency of occurrence. The birds cannot be divided simply into those that occurred only once or twice and those that were present on m o s t occasions: all degrees of attendance were recorded. We could not collect an adequate sample of data from individuals that occurred only occasionally on the bed, so most of our analysis is restricted to the 28 birds that were seen on five or more occasions. For convenience we call these 'regular visitors', the remainder being classed as transients. Although 54 % of the birds seen throughout the winter were transients, on average only 19% of those present on any one tide were in this category. Feeding method and feeding site. Oystercatchers opened mussels in three ways. One was to stab into gaping mussels, and another to pull the
GOSS-CUSTARD ET AL.: FOOD STEALING IN OYSTERCATCHERS 25
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Fig. 2. The frequency of occurrence of individual birds on bed 4 during 21 low-tide watches in the winter 1979/80. mussel from the clump and hammer the shell on the ventral side until it cracked. Both methods were described by Norton-Griffiths (1967). On the Exe, oystercatchers also hammered into mussels in situ and therefore cracked the shell on the dorsal side, usually at the point where the adductor muscle is attached to the mussel shell. We called these methods stabbing, ventral hammering and dorsal hammering, and found that in winter 27 individuals used only one technique while the other bird almost invariably hammered mussels dorsally. Ten regulars on bed 4 used ventral hammering, nine used dorsal hammering and nine used stabbing. Individuals foraged in restricted areas for the whole winter (Fig. 3). Birds which returned in the second year and were studied by us usually fed near where they had been in the previous winter. The detailed observations in the autumn of 1980 show that some birds restricted most of their foraging to very small areas indeed. Despite this, i t is clear that the areas used by individuals overlapped considerably. They did not feed in mutually exclusive territories. As Norton-Griffiths (1967) also showed, birds using different techniques fed in different places. The ventral hammerers fed downshore where the substrate was firm and hammering was easiest, whereas stabbers fed in the wetter and muddier areas upshore. The area used by the dorsal hammerers overlapped with that used by the stabbing birds, presumably because
919
mussels in a clump could be hammered without being driven too deep into the substrate. Comparison of feeding groups. The behaviour of regular visitors feeding by each method was compared by analysis of variance of the rates at which particular activities were performed. The data were collected at low tide throughout the winter of 1979/80 (1 November-28 February). In many cases a particular behaviour was so rare that it was more a p p r o p r a t e to analyse the proportion of 5-rain periods in which it occurred than to deal directly with mean rates. This applied particularly to encounters between birds. Table I compares the rates at which birds clearly found mussels themselves or stole them from other birds and the rates at which mussels were given up, lost to other birds or swallowed. Mussels labelled 'given up' were those that were picked up and carried before being rejected. We realize that many others might be attempted and rejected quickly, but it was difficult to measure this. Consequently, we simply noted the ones which were carried first, as these were clearly identifiable and wasted most searching time. The category 'found' included mussels like this which were eventually rejected. Ventral hammerers found more than dorsal hammerers which in turn found more than stabbers. However, ventral hammerers carried and rej e c t e d considerably more than dorsal hammerers while stabbers carried and rejected very few. There was no significant difference between groups in the numbers stolen from or lost to other birds. T h e overall result was that there were no significant differences between groups in the rates at which mussels were swallowed. The handling times did differ between groups: ventral hammerers t o o k over twice as long to deal with a lrmssel than did stabbers, while dorsal hammerers were intermediate. The percentage of encounters involving mussels was similar in each group of regular visitors, being 52 • 8 in the ventral hammerers, 57 :k I0 in the dorsal hammerers and 65 -4- 7 in the stabbing birds. The rates at which birds were involved in encounters with Other oystercatchers f o r mussels or for other reasons did not differ between groups either (Table II). However, ventral hammerers were attacked more often by crows (Corvus corone) than were either dorsal hammerers or stabbers, perhaps because of their longer handling time or because more crows fed where the ventral hammerers did.
920
ANIMAL
BEHAVIOUR,
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GOSS-CUSTARD ET AL.: FOOD STEALING IN OYSTERCATCHERS
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922
ANIMAL
BEHAViOUR,
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Table II. Mean Rates at which Birds Using Each Feeding Method were Involved in Encounters of Various Types (Means 4- SE: all tests of significance by analysis of proportions) Ventral hammerers (V) s~ Numbers of times per 5 min: Attacked by crow: Attacked by oystercatchers: (i) for mussels (ii) for other reasons (iii) for all reasons Attacks of oystercatchers: (i) for mussels (ii) for other reasons (iii) for all reasons
Dorsal hammerers(D) R sB
(N = 159) 0.189 4- 0.039
(N = 168) 0.077 4- 0.02I
0.176 -_Jz0.037 0.088 4- 0.033 0.258 4- 0.051
0.214" 4- 0.057 0.060 4- 0.020 0.274 4- 0.041
0.170 4- 0.039 0.195"** 4- 0.084 0.359*** 4- 0.118
0.167" 4- 0.072 0.131 4- 0.027 0.298***4- 0.085
Stabbers (S) R sE
Significance of differencebetween groups
(N = 149) 0.094 4- 0.042 V > S V>D 0.107"* 4- 0.049 0.114 4- 0.028 0.215 4- 0.068 0.242*4-0.086 0.141"'4-0.056 0.389"*'4-0.143
(P<0.01) (P<0.05) Ns NS NS Ns NS NS
Significance of differences between individuals within a group: *P < 0.05, **P < 0.01, ***P < 0.001. Birds using different methods of feeding attacked each other regularly and there is no evidence that a bird's feeding method influenced its choice of victim. Of the 65 encounters in which the feeding method of both participants was known, only 40 % involved birds belonging to the same feeding group. Table III compares the success with which birds of known feeding method either attacked others or defended themselves against others, whose feeding methods were not usually known. There were no significant differences in the proportions between groups, whether or not mussels were involved. Most attacks which did not involve mussels resulted in the victim running away. The possible outcomes are more varied in the case of encounters over mussels, and these are detailed for all encounters, irrespective of feeding method, in Table IV. The victim retained the mussel in over half of encounters, almost always by carrying it away so the attacker gave up. Often the victim dropped the mussel but the attacker failed to locate it afterwards. In only 21% of encounters did the attacking bird actually steaI the mussel, and in some cases much of the flesh would already have been consumed by the victim. The regular visitors in each group were seen on the bed on a similar number of occasions. The mean q- SE number of tides on which birds were seen were 10.7 ~: 1.6 (N = 10) for ventral hammerers, 14.9 • 1.70 ( N = 9) for dorsal hammerers and 12.6 • 1.79 (N : 9) for stabbers, none of the comparisons being significant at 5 % level (t-test). Thus the behaviour of the groups was similar in most respects, both when feeding rates and social behaviour were compared. The main
differences are that hammerers took longer to open their mussels, found more but gave up on a higher proportion, and lost more to crows. But in every other respect, the behaviour of the regular visitors in the groups was similar, and data from all groups were combined for the analysis of individual variations in behaviour. IndMdual Variations in the Behaviour of Regular Visitors A striking feature of the results is the differences between individuals in the rates at which many o f the social and feeding activities were performed. These could be due either to basic features of the bird, such as its age or genetic characteristics, or to environmental factors, such as food supply, population density, weather, tidal conditions or season. The last three can be ruled out because the differences between individuals were clearly consistent whatever the weather, tide or season. Bird density was not measured in this study. Accordingly, the observations made in the winter 1979/80 at low tide when bird density was lowest and least variable are mainly considered in this paper. Genetic characteristics were not studied and 21 of the 28 residents were adult when ringed so their age was not known exactly. Consequently, only relationships between food supply and a bird's social and feeding activities can be examined here. Frequency of occurrence on file bed. The number of times birds were seen on the bed varied between individuals (Fig. 2). The numbers of low-tide periods during which birds were seen were regressed against the density, size, ash-free dry weight and shell-thickness of the
GOSS-CUSTARD ET AL. : FOOD STEALING IN OYSTERCATCHERS
923
Table Ill. The Outcome of Attacks amongst Oystercatchers in Each Feeding Group (Figures show percentages where N is the total number of encounters seen. ? : outcome uncertain) (i) Attacks involving mussels
Subject bird attacks others and: SteMs N mussel ? Ventral hammerer Dorsal hammerer Stabber All
Subject bird is attacked and: Keeps
N
mussel
?
35 42 57
22.9 11.9 21.1
0 0 1.8
30 72 41
40.0 58.3 56.1
0 4.2 0
134
18.7
0.8
143
53.9
2.1
(ii) Attacks not involving mussels
Ventral hammerer Dorsal hammerer Stabber All
Subject attacks and other: N runs away ?
Subject is attacked and it N runs away
37 38 36
100 95 90
0 5 5
22 22 29
100 96 100
115
94
4
73
99
mussels a n d the softness a n d flatness o f the substrate in the localities where birds fed t h r o u g h o u t the winter. O n l y the density, size a n d shellthickness o f the mussels were selected b y stepwise multiple regression, giving a multiple correlation coefficient o f 0.685. T h e p a r t i a l correlation coefficients for each variable were: mussel density, r = + 0.631, P < 0.01; mussel size, r = + 0.475, P < 0.05; shell thickness, r - - - 0 . 6 3 2 , P < 0.01. Birds t h a t occurred frequently on bed 4 h a d feeding areas where the mussels were n u m e r o u s , large a n d thin-shelled. A g g r e s s i v e encounters. T h e rates at which birds a t t a c k e d others, w h e t h e r f o r mussels o r for o t h e r reasons, often differed significantly between individuals (Table If). However, the rates at which individuals a t t a c k e d others for mussels a n d for other reasons were c o r r e l a t e d with each o t h e r (r = + 0.576, P < 0.01, N = 28). Consequently, the rate at which a b i r d initiated attacks against others for all reasons, i.e. b o t h rates combined, was used as a m e a s u r e o f its aggressiveness, a n d highly significant differences a m o n g individuals were f o u n d (Table II). O f course, this m e a s u r e o f aggressiveness correlated closely with b o t h o f its constituents, i.e. rates o f a t t a c k i n g for mussels (r = + 0.841) a n d for other reasons (r = + 0.863). T h e rate at which a bird a t t a c k e d others was n o t correlated with a n y aspect o f the f o o d supply or with h o w m a n y mussels it f o u n d or gave up,
o r on h o w long it t o o k to open each o f t h e m or h o w m u c h time it spent p e r 5 m i n o p e n i n g mussels. This a p p l i e d w h e t h e r simple o r p a r t i a l coefficients were calculated. However, aggressiveness was correlated with h o w m a n y times a b i r d was seen on the bed (r = + 0.430, P < 0.02, N = 28). T h e m o r e frequently a b i r d occurred on b e d 4, the m o r e aggressive it was (Fig. 4). There were n o significant differences between individuals in the rate at which they were a t t a c k e d by o t h e r oystercatchers when mussels were n o t involved, o r when all encounters were c o m b i n e d (Table II). However, individuals often differed in the rate at which they were a t t a c k e d f o r mussels. This was n o t correlated, using either simple or p a r t i a l correlation analysis, with h o w often the birds occurred on b e d 4 o r t h e f o o d supply, b u t only on h o w m a n y mussels they f o u n d per 5 rain Table IV. Outcome of 277 Encounters Over Mussels
Percentage of encounters Attacker steals mussel and eats it Victim drops mussel but attacker fails to locate it Victim drops mussel but outcome unknown Victim defends mussel and keeps it Victim runs away with mussel and keeps it
20.6 19.5 4.3 1.1 54.5
924
ANIMAL
BEHAVIOUR,
u~
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oo
z
o @
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NUMBER OF DAYS BEEN ON BED
Fig. 4. T h e aggressiveness o f a n individual in relation to h o w often it was seen on bed 4.
(r = + 0.363, P < 0.05). Birds which found more mussels were attacked more often, presumably because they were thereby more often in a position to have food stolen. We think that the rate birds found mussels was partly related to the sizes they took. Handling time and feeding rate were negatively correlated amongst ventral hammerers (r = --0.742, P < 0.02, N = 10) and stabbers (r = --0.824, P < 0.01, N = 9), though not significantly in dorsal hammerers (r = --0.324, N = 9). Birds that fed fast had short handling times, probably because they ate small mussels. This probably depended on the sizes of mussels available in the exact places the birds were feeding. We expected that the more aggressive birds would be attacked less often themselves by other birds, but none of the correlations between the aggressiveness of a bird and how often it was attacked by other oystercatchers reached statistical significance. However, all the relationships were negative: for attacks involving mussels, r = --0.073; for attacks made for other reasons, r = --0.155; for both kinds of attacks combined, r = - - 0 . 2 4 1 ; and for the number of mussels actually stolen, r = - - 0 . 1 0 7 . Similarl.y, the correlations between a bird's aggressweness and how often it was attacked by crows (r = --0.245) and had mussels stolen from it by them ( r = - - 0 . 2 3 2 ) were both negative but not
3
significantly so (N = 28 in all cases). Clearly there is a suggestion that aggressive birds were attacked least often, as confirmed by later studies on a smaller number of individuals (Ens & Goss-Custard, in preparation). Aggressiveness and success in encounters. There were not enough data from the 28 individuals studied in the winter of 1979/80 to test whether aggressive birds were more successful in encounters than the less aggressive ones. However, the detailed studies in autumn 1980 allowed this possibility to be examined. A bird was considered to be successful when: (I) it succeeded in driving away a bird it had attacked or did not flee when it was itself attacked in encounters in which mussels were not involved; or (II) it succeeded in stealing a mussel from another or defended its own mussel either by fighting or by running away. The proportion of encounters in which a bird was involved where it was successful, was highly correlated with aggressiveness in the 10 birds studied in the autumn of 1980 (Fig. 5). Since the aggressiveness of birds in the autumn of 1980 and during the preceding winter were highly correlated (r = +0.864, P < 0.01, N = 8), it can be safely assumed that a bird's aggressiveness in 1979/80 was a good indication of its success in encounters in that year as well. Effect of robbing on profitability. Stealing a mussel from another oystercatcher is likely to enhance the rate of food intake of the aggressor because time does not have to be spent in search-
1"0-
Q:
30,
o
z tt3 "C..t2
o
CO
Q)
9
9
o p-
<
o o
2~
4'o
PERCENT OF
6"0 ENCOUNTERS
8"o
1bo
WON
Fig. 5. T h e aggressiveness o f an individual in relation to
its success on encounters,
GOSS-CUSTARD ET AL.: FOOD STEALING IN OYSTERCATCHERS ing for, and perhaps opening, the mussel. Conversely, the victim is likely to suffer a reduced rate of intake. This was tested by comparing the intake rate of a bird during a 5rain period in which it was involved in an encounter of one kind or another with its intake rate during an adjacent 5-rain period in which no encounter occurred. The data from all birds were combined and are summarized in Table V. Birds which stole a mussel increased their intake rate, yet unsuccessful attacks did not decrease it by much. Even though 80 % of attacks resulted in failure to obtain a mussel (Table IV), there was little penalty for failure as attacks were executed so quickly and successes were beneficial. Birds which were attacked did not suffer a significant reduction in rate of intake unless the mussel was actually lost. Attacks which did not involve mussels had little effect on intake rate. The conclusion is that stealing mussels was profitable and, since the rate of attacking other oystercatchers for mussels was not related to how many mussels the aggressor was finding, it was a genuine gain and not simply an alternative way of obtaining the same number of mussels. The rate of stealing mussels was closely correlated with a bird's aggressiveness (r = 0.669, P < 0.001), whereas the rate it lost mussels was only poorly related (r = - - 0 . 1 0 7 ) . Because of this the difference between stealing and losing mussels, the net gain from encounters over mussels, was correlated with aggressiveness (r = +0.401, P < 0.02, N =: 28: Fig. 6). Stealing mussels more than compensated for those lost by the most aggressive birds, but not in the case of the least aggressive ones. Contribution of robbing to overall intake rate.
Even though individuals differed significantly in how often they attacked other birds and this affected the net gain in encounters over mussels, there were few significant differences between
925
individuals in the rates at which they stole from or lost mussels to other oystereatchers (Table I). This may have been because the contribution which stealing and losing mussels made to total intake was small, and therefore variations in them difficult to detect. On average across all 28 birds, only 3.8 % of mussels were stolen and 4.3 % lost in encounters with oystercatchers and 7.3% with crows. Stealing and losing mussels involved only a small minority of the prey items handled by oystercatehers. However, there was considerable variation among individuals, and some obtained a considerable proportion of their food by stealing. Two obtained over 20 of their mussels by stealing, three obtained 1020% and four obtained 5-10%. Furthermore, the numbers stolen and lost, and therefore the net gain, made a significant contribution to individual variations in feeding rate (Table VI). By expressingthe contribution of each as standard partial regression coefficients, it is clear that the major source of variation between individuals was in how many they found rather than in the number they stole or lost. Though the rate of net gain of mussels made a significant contribution to total intake, it was small compared with the numbers found. Comparison of Regular Visitors and Transients
The relationship between how frequently a bird occurred on the bed and its behaviour is confirmed by comparing the behaviour of transients, which fed all over the bed, with that of regular visitors. Each feeding record on a transient was compared with the nearest record of a resident feeding with the same technique in the same place on the same day, so that all other factors would be held constant. Regulars found and swallowed significantly more mussels than transients (Table VII), but the agonistic behaviour of the groups was not significantly different. However, the largest
Table V. Intake Rate of Mussels in 5-rain Periods in which Various Encounters Occurred, Compared with Control Periods where No Encounters Occurred
Encounter 27 sE
.~"
Control SE
t
P (one.tailed)
Kind of encounter
N
Fails to steal mussel
Steals mussel successfully
16 18
1.44 0.57
0.15 0.12
0.81 0.67
0.16 0.16
2.81 0.55
< 0.01 NS
Loses mussel
Attacked but keeps mussel
19 37
0.53 1.14
0.16 0.10
1.00 1.19
0.19 0.13
1.95 0.33
< 0.05 Ns
Attacks another or is attacked but no mussel involved
21
0.91
0.28
0.81
0.18
0.29
NS
926
ANIMAL
"Jr-
BEHAVIOUR,
30,
3
.1
9
9 9 1"0 ATTACKS/5 MIN
NET GAiN
.3
Fig. 6. The net gain or loss from stealing and losingmussels in relation to the aggressiveness of a bird. t-values were obtained in those activities which, amongst residents, varied significantly according to period of residency, Regulars attacked others and stole more mussels than did transients in this sample. In contrast, the rates at which birds were attacked by other oystercatchers were similar. These comparisons parallel the trends found amongst the regulars. Discussion
Individuals varied in how often they occurred on bed 4 during the winter. Some birds were present on virtually all the low-tide periods we searched for them, but others were not. The missing birds would have been feeding on other mussel beds on the Exe because (1) most oystercatchers remained on this estuary throughout the winter (Goss-Custard et al., in press b), and (2) m o s t birds that fed on mussels ate almost nothing else (Goss-Custard & Durell, in press).
We did not study the factors which determined whether or not a bird would be present on bed 4. We suspect that disturbance by people on other beds was important. Several of our regular visitors were seen on the adjacent bed 3 and were only seen on bed 4 when that bed was disturbed. The height of the tide may also have been important. Some mussel beds were not exposed even at low water on neap tides yet many birds fed there on spring tides. Some birds may also have been displaced by other oystercatchers from more preferred mussel beds (Goss Custard et al., in press a). Most of the birds on bed 4 restricted their foraging to small areas irrespective of how frequently they occurred on the bed. Furthermore, most of the birds that returned in the second winter fed in almost the same place and, as already shown by Norton-Griffiths (1968), used the same method for opening mussels.
Table VI. Standard Partial Regression Coefficients between the Numbers of Mussels Swallowed per 5 rain and the Numbers Found (excluding those given up), Stolen and Lost to Oystereatchers or Crows ( N = 28)
Standard partial t regression coefficient value (1) Numbers found (2) Numbers stolen (3) Numbers lost to oystercatchers (4) Numbers lost to crows (2)--(3) Net gain
+ 1.105 +0.166 --0.238 --0.320 +0.378
22.0 3.59 5.68 6.86 2.25
P < < < < <
0.001 0.001 0.001 0.001 0.05
927
GOSS-CUSTARD ET AL.: FOOD STEALING IN OYSTERCATCHERS Table VII. Comparison of the Behaviour of Regulars and Transients on Bed 4 (N = 49 except for handling time where N = 25)
Regulars X
No. found and opened or stolen by others No. stolen from others No. lost to oystercatchers No. swallowed Handling time No. times attacked others No. times attacked by oystercatchers
sE
1.286 =L0.127 0.082 -t- 0.040 0.031 4- 0.017 1.225 -t- 0.102 118.6 :t: 13.8 0.225 • 0.079 0.225 -t- 0.067
Although aggressive encounters were common, birds did not defend exclusive feeding territories. There was a considerable overlap in the area used by different regular visitors and transient birds also fed in areas used by the regulars. The considerable amount of overlap in feeding areas and the high densities of oystercatchers on bed 4 no doubt contributed to the high incidence of aggression that occurred there. As in Vines' (1980) study, a majority of the encounters were attempts to steal mussels. However, a mussel was not obviously involved in 35-48% of the encounters, depending on the feeding group. In some cases, we may not have realized that a mussel was actually involved. In others, the aggressor may have attacked to gain a feeding site rather than a particular mussel (Vines 1980). However, neither mussels nor feeding sites s e e m e d to be involved in some encounters, because the victim was not actually dealing with a mussel when attacked and, after the encounter, the aggressor did not feed where the victim had been previously. Piping displays (Heppleston 1970) were also common, and mussels were seldom involved in these. We think that encounters of these kinds were either concerned with attempts to establish dominance over another bird or with driving it from the area altogether. Neither possibility has yet been tested. Most of the birds attacked others and were themselves frequently attacked. There is no evidence that certain individuals specialized in stealing mussels, as has been suggested for some kleptoparasitic birds (e.g. Brockmann & Barnard 1979). However, there were considerable individual differences. Some birds were particularly aggressive and successful in stealing, and perhaps also in defending, mussels. These differences were consistent throughout the winter and, indeed, from one winter to the next. We have
Transients X
sE
0.918• 0.127 0.020i 0.020 0.123_-4=0.054 0.888~ 0.123 124.2 :t= 13.6 0.102• 0.044 0.204~ 0.065
t
P
2.05 1.38 1.63 2.10 0.30 1.36 0.22
< 0.05 NS NS < 0.05 NS NS NS
not studied the characteristics of the birds which affected their aggressiveness and success in encounters, but did show that birds that were most frequently on bed 4 were generally the most aggressive. This might suggest that familiarity with an area was important, but it is difficult to distinguish cause from effect, because only birds that were already aggressive may have been able to maintain themselves in one area for long periods. Similarly, adults were in general dominant to immatures (Goss-Custard e t al., in press a), but we cannot separate the effect of familiarity with the Exe Estuary and some other attribute associated with age in determining dominance. There were striking similarities between the results of this study on one bed and those of another in which all the mussel beds were compared (Goss-Custard et al., in press a). In that study, immature oystercatchers were less aggressive, less successful in encounters over mussels, and avoided other birds much more frequently than adults. In the summer, most birds were immatures and fed on a few beds which were preferred because they had a firm substrate and were close to the highwater roost. As the adults returned from the breeding areas, most of the immatures left the preferred beds and so were found in winter on less-preferred areas. T h e s e were not only further from the roost and with a softer substrate, but also contained fewer mussels which were, in general, smaller and thickershelled (Goss-Custard et al. 1981). In other words, the more aggresNve adult birds fed disproportionately on mussel beds where the mussels were dense, large and thin-shelled, in just the same way as did the aggressive individuals within bed 4. Adults also changed beds less often than did immatures and were more likely to return to the same mussel bed in successive winters, just as aggressive birds on
928
ANIMAL
BEHAVIOUR,
bed 4 were faithful to their feeding ranges a n d m a n y birds returned to the same p a r t o f the b e d in 1980. Therefore, the b e h a v i o u r o f birds o f different aggressiveness over the whole estuary was consistent with the results o f the m o r e detailed studies carried o u t on bed 4. H i g h aggressiveness was correlated with several benefits. T h o u g h the direction o f cause a n d effect is unclear, the m o s t aggressive birds fed in those parts o f the bed where mussels were large, dense a n d thin-shelled. W e suspect that one o r all o f these factors affected rate o f intake, t h o u g h the picture was c o m p l i c a t e d by the presence o f three different feeding m e t h o d s which c o u l d be affected b y different factors. The most aggressive birds also o c c u r r e d m o s t often in their feeding a r e a a n d so h a d m o r e chance to l e a r n h o w best to exploit it. F a m i l i a r i t y with the area m a y be one reason w h y regular visitors found, a n d swallowed, m o r e mussels t h a n transients feeding in the same place. Second, the m o s t aggressive birds were m o r e likely to be in credit in encounters with o t h e r birds over mussels. Aggressive birds were often a t t a c k e d b u t they stole m o r e t h a n they lost to others a n d this increased their rate o f i n t a k e significantly. Indeed, the m o s t aggressive birds o b t a i n e d 20 ~ o f their mussels this way. Finally, some encounters were very vigorous a n d feathers were lost. T h o u g h the cost o f this was n o t measured, it m a y have h a p p e n e d least a m o n g the m o s t aggressive i n d M d u a l s .
Acknowledgments W e w o u l d like to t h a n k the m e m b e r s o f the D a w l i s h W a r r e n N a t u r e Reserve M a n a g e m e n t C o m m i t t e e for permission to ring birds, and D r D. Jenkins, D r S. M c G r o r t y a n d D r C. J. R e a d i n g for c o m m e n t i n g on the manuscript. W e are very grateful to R. J. Clarke for help
30,
3
with the statistical analysis. W e are also i n d e b t e d to D r C. Perrins for p r o v i d i n g space a n d facilities f o r one o f us (B. J. Ens) to analyse some o f the results at the E d w a r d G r e y Institute.
REFERENCES Brockmann, H. J. & Bamard, C. J. 1979. Kleptoparasitism in birds. Anim. Behav., 27, 487-514. Caldwell, (3. S. 1980. Underlying benefits of foraging aggression in egrets. Ecology, 61, 996. Gess-Custard, J. D. & Durell, S. In press. Individual and age differences in the feeding ecology of oystercatchers, Haematopus ostralegus, wintering on the Exe Estuary, S. Devon. Ibis. Goss-Custard, J. D., Durell, S., McGrorty, S., Reading, C. J. & Clarke, R. T. 1981. Factors affecting the occupation of mussel )14ytilns edulis beds by oystercatchers, Haematopus ostralegus on the Exe Estuary, Devon. In: Feeding andSurvivalStrategies of Estuarine Organisms (Ed. by N. V. Jones & W. J. Wolff), pp. 21%229. London: Plenum Press. Goss-Custard, J. D., Durell, S., McGrorty, S. & Reading, C. J. In press a. Use of mussel Mytilus edutfs beds by oystercatchers Haematopus ostraIegus according to age and population size. J. Anita. Ecol. Goss-Custard, J. D., Durell, S., Sitters, H. P. & Swinfen, R. In press b. Age-structure and survival of a wintering population of oystercatchers, Haematopus ostralegns. Bird Study. Goss-Custard, J. D., McGrorty, S., Reading, C. J. & Durell, S. 1980. Oystercatchers and mussels on the Exe Estuary. Devon Ass., Special Vol. 2, 161-185. Heppleston, P. B. 1970. The function of oystercatcher piping behaviour. Br. Birds, 63, 133-135. Norton-Griffiths, M. 1967. Some ecological aspects of the feeding behaviour of the oystercatcher, Haematopus ostralegus, On the edible mussel, Mytilus edulis. Ibis, 109, 414-424. Norton-Griffiths, M. 1968. The feeding behaviour of the oystercatcher, Haematopus ostralegus. Unpublished Ph.D. thesis, University of Oxford. Vines, G. 1980. Spatial consequences of aggressive behaviour in flocks of oystercatchers, IIaematopus ostralegns L. Anita. Behav., 28, 1175-1183. (Received 29 October 1981; revised 7 December 1981; MS. number: 2187)