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Alarm calling by individual willow tits, Parus montanus
Anim. Behav., 1990, 40, 437442
Alarm calling by individual willow tits, Parus montanus RAUNO
V. A L A T A L O * & P E K K A
HELLEt$
*Department of Biology, University of Jyviiskylii, Yliopistonkatu 9, SF-40100 Jyvdskylii, Finland t Meltaus Game Research Station, Finnish Game and Fisheries Research Institute, and Konnevesi Research Station, University of Jyviiskyld, SF-97340 Meltaus, Finland
Abstract. Alarm responses of wild-captured individual willow tits to model sparrowhawks, Accipiter nisus, flying over a test chamber were studied. Tits did not usually give alarm calls if the apparent predator was passing nearby (at a height of 10 m), while over half of the individuals responded by alarm calling for a more distant predator (40 m). This suggests that alarm calling involves a risk to the caller. Second, there was individual variation in the responses, with older males giving the call more frequently than females or young males. The greater responsiveness of adult males may indicate that different individuals in a flock gain different benefits by warning the others. The tendency to give alarm calls increased over the autumn, which could be related to the establishment of cohesive flocks at that time.
The evolution of alarm calls has attracted numerous theories and speculations (see Harvey & Greenwood 1978; Klump & Shalter 1984; Smith 1986). Among these, the idea that animals take the risk of alarm calling for the benefit of their kin (Hamilton 1964) is perhaps the only one that has been verified (Sherman 1977; Hoogland 1983). Other explanations include direct benefits for the caller through predator distraction (Charnov & Krebs 1975), informing the predator that it has been observed, or retaining group companions (e.g. Smith 1986). Reciprocal altruism, where individuals that alert others would gain when these other individuals give alarm calls in the next predator context, is open to cheating (Trivers 1971; Tamachi 1987). Various group-selection arguments have also been proposed (Wilson 1975). Surprisingly little work has been devoted to test these hypotheses, even though experimental studies of alarm calling are feasible (Klump & Curio 1983; Gyger et al. 1986; Klump et al. 1986a). We have studied the willow tit, a common holarctic forest passerine. During the winter individuals stay in small flocks of four to eight birds (Ekman & Askenmo 1984; Hogstad 1987), where individuals are not related because they disperse during the autumn of their first year (Ekman 1979; Ekman et al. 1981). For breeding, the flock separates and pairs usually form between flock members. There is a clear dominance hierarchy in flocks (Ekman & Askenmo 1984; Hogstad 1987; Koivula & Orell ~To whom correspondence should be addressed. 0003-3472/90/090437 + 06 $03.00/0
1988), with older (age over 1 year) males at the top and young (born in the previous summer) females at the bottom, with older females and young males having an intermediate position. Older individuals forage higher in trees, and the experimental removal of these older birds allows young birds to move from lower to upper sites (Ekman & Askenmo 1984). Upper sites in the trees are better since they are safer from predators (Ekman 1986, 1987; Hogstad 1988), and arthropods are more abundant there than in the lower half of spruce (R. V. Alatalo, unpublished data). Given that different individuals have different roles in the flocks, it is possible that they benefit from alarm calling in different ways (Cheney & Seyfarth 1985; Smith 1986). Subdominants might actually benefit from the death of a dominant individual, giving them better access to the limited food resources in feeding sites that are safe from predators, or other resources such as roosting cavities, nesting territories and mates. Under these circumstances, if there are no direct benefits of giving alarm calls such as predator distraction, subdominants might do best by keeping silent, even if there were no cost for calling. Dominants, instead, have more to gain from alerting the others if there are any future benefits such as companion retention or reciprocity in alarm calling at least by some of the other individuals. Willow tits usually mate with members of their flock, and because there is a 5-30% surplus of unmated males (Ekman & Askenmo 1986), the survival of females may be important for males, increasing the benefit to them
9 1990 The Association for the Study of Animal Behaviour 437
Animal Behaviour, 40, 3
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from calling. To test this hypothesis we looked at the responses of different individuals in a standardized presentation of sparrowhawk, Accipiter nisus, models. If, on the other hand, individuals give alarm calls irrespectively of sex and age, it would suggest that there are instant benefits of alarm calling for all of the individuals or that it involves reciprocal altruism. The explanations involving direct benefits of alarm calling, such as predator distraction or informing the predator that it has already been observed, do not necessarily imply any risk from alarm calling. If alarm calling is costly, increasing the risk of being observed and captured by the predator, animals should be less willing to give the alarm call when the possibilities of escaping the predator are reduced. It is possible to test between these alternatives by varying the risk of being caught by a predator, and for this purpose we varied the perceived distance of a hawk model flying overhead.
METHODS
The experiments were performed at the Konnevesi Research Station in Central Finland (63~ We tested 33 individuals during February-March 1987, when birds are still in stable flocks, and 31 individuals in October-November 1987, when stable flocks have just formed (see Ekman 1979; Ekman et al. 1981). We used individuals that were captured with mist nets from feeding tables within 5 km of the station, and released with colour bands after the experiments. We separated first-year birds from older individuals by the abrasion and shape of the tail, which is a reliable indicator particularly in early winter (Laaksonen & Lehikoinen 1976). For sexing we used the wing length (see Haftorn 1982; Hogstad 1987; Koivula & Orell 1988). Individuals with a maximum wing-chord length (Svensson 1975) of less than 64 mm were defined as females and those with a wing chord of 64 mm or longer as males. The error in sexing the birds by this criterion is just over 5%. We carried out the experiments within 2 h of capturing the birds, which were kept separately in dark boxes in the interim. To avoid problems with changes in temperature, the study chamber was situated outdoors. The birds were placed one at a time in a small (20 x 30 cm) cage on the bottom of a chamber measuring 2 x 1 m with 1 m high closed
walls. The hawk model was attached to a fishing line that was placed 2 m above the cage, and we used an electric motor to move the hawk at a given steady speed over the chamber (see Klump & Curio 1983). Apart from the moving hawk model, the tits could see only the sky above the chamber walls. Each bird was tested once with each model with a 10-rain interval between the two tests. The order of presentations was systematically alternated between consecutive individuals tested. As a close predator, we used the perceived minimum distance of 10 m (model wing span 7.2 cm, speed 120cm/s). The distant predator flew at a simulated height of 40 m (1.8 cm, 30 cm/s). These speeds correspond to a hawk flying at 8.4 m/s (30 km/h), and since the line was visible for a distance of 3'5 m, the distant hawk was visible for 11.7 s and the near hawk for 2'9 s. Our models mimicked a gliding hawk with wings partly folded. Apart from direct observation through a small hole in the chamber wall, we also filmed the experiments on 41 individuals with a video camera to measure the time it took for the tits to notice the hawk model (to the nearest 0.1 s), and to study the responses of tits more carefully in slow motion. However, when the tits were perching it was easy to see when they noticed the hawk model, as they froze with the head typically slightly turned and the bill pointed slightly upwards while they looked at the model. We also recorded on videofihns how long the birds looked at the hawk and their activity (perching or moving around the cage). We recorded some of the alarm calls with a Sony TC-D5M casette recorder and Telinga-pro microphone placed within the test chamber 1 m from the bird. The recordings were analysed with a UNISCAN II Spectrograph.
RESULTS Behaviour of Test Birds
The birds looked at the hawk for on average
(4-SD) 6'5 _+2-9 s ( N = 58, range 2-15 s). There was a slight, but non-significant tendency for individuals giving an alarm call to look longer (7.4 4- 3.15, N-= 20) than the silent ones (6.0 4- 2.6 s, N = 38, t = 1'83, P < 0.10). However, there was no correlation between how long a test bird followed the hawk and the time it took to notice the model and start looking after the appearance of the model (r s= 0'009,
Alatalo & Helle: Alarm calls o f willow tits
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Table I. Characteristics of alarm calling and alarm calls of willow tits in the experiment
Latency to notice the hawk model (s) Time between first observation and alarm response (s) Duration of alarm call (s) Call characteristics Maximum frequency of major band Frequency range (kHz) Harmonics (no. of separate bands)
Mean
sn
N
2.2
1.5
18
1.3 1.2
1.2 0.8
17 19
8.7 1.4
0.7 0.7
17 17
5.5
2.1
13
N = 47, P > 0-10). Whether the test bird was perching or actively moving around did not influence the time it took from the appearance of the hawk model above the bird to the moment when it responded to its appearance by freezing, raising the bill and beginning to look at it. The birds habituated between the two tests. In the first test the alarm call was elicited from 37.5% and in the second test from 18.8% of the 64 test birds (/~2 = 5'56, P < 0'05). There was no significant difference between tests in the time from the model's appearance to the time the birds started looking at it (first run: X'___SD = 0 ' 8 _ 1' 1 S, N = 25; second run: 0'4_+0"4, N = 2 1 , M a n n - W h i t n e y Utest, z = 1.30, P=0.19), or in the duration of looking (first run: 7-1_+3-1s, N = 2 7 ; second run: 6.1 _+2.6 s, N = 2 7 , t = 1.38, P = 0-17). When the tits did give an alarm call, they did so on average 2.2 s after the appearance of the hawk and 1.3 s after the start of freezing (Table I). The duration of the call varied greatly: the shortest one, including only one element, lasted 0.2 s and the longest one with 10 elements in three bouts went on for 3'0 s. The maxim u m frequency of the major band was 8'7 kHz, but the harmonics were pronounced in m a n y cases. Distance of the Hawk The size of the hawk model had a marked influence on the percentage of tits alarm calling (Fig. 1). Only 10% of tits gave alarm calls when the simulated distance to the hawk was only 10m, while nearly half of them responded by alarm calling when the hawk was 40 m away. The percentages are somewhat higher, 16 and 59% respectively, if
50
I00
5O
Large
Small Model
Figure 1. Percentage of willow tits giving an alarm call ( 9 and keeping silent ([]) in response to the large and small hawk models in (a) the first and (b) the second run.
only the first runs are included, eliminating the effect of habituation. There was a non-significant tendency for tits to notice the 10-m hawk sooner after its appearance (X'+SD=0.4+0-3 s, N = 2 8 ) than the 40-m hawk (1.0+ 1.1 s, N = 2 2 , U-test, P<0.10). Hence, with regard to observability one would expect the 10-m hawk to elicit a greater response. Since the 10-m hawk moved faster it was visible for 2.9 s, whereas the 40-m hawk was visible for 11.7 s. Consequently following the 10-m hawk was somewhat shorter (5.5+2.5s, N = 3 1 ) than for the 40-m hawk (7.7+2"9s, N = 2 7 , t = 3 ' 1 7 , P<0"01). One could speculate that the shorter period of visibility might prevent tits from alarm calling at the 10-m hawk. However, 75% ( N = 16) of the alarm responses to the 40-m hawk were given within the 2.9-s period for which the 10-m hawk was visible. Furthermore, alarm calling was not restricted to the period when the hawk was visible, and in two of the seven alarm calls given in response to the close hawk the tit clearly waited until the hawk was no longer visible before it gave the alarm call. There were no observable differences in the alarm calls that were given to close or distant hawk models, but we had only two recordings of the few alarm calls for the close hawk. The two calls were
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5O
Adult male 2,24
Adult female
1-33
Juvenile male Juvenile female 0-85 1.00
Figure 2. Percentageof willowtits givingan alarm call to the small ([] ) and large ( 9 ) modelsand the percentage keeping silent ([2) by sex and age. Sample sizes are: adult male 21, adult female 12, juvenile male 13 and juvenile female 18. Numbers show the mean alarm score (see text for details). typical alarm calls with the maximum frequency of the main band 8"8 kHz in both cases and the maximum frequency range 1-1 and 1.3 kHz. Individual Differences Since the distance of the model and the order of presentation influenced the probability of eliciting the alarm call we used an index of alarm call tendency (alarm score) to standardize the effect of the run order. The index is highest if an individual gave an alarm call for the 10-m hawk and if the alarm response also appeared in the second test; we thus weighted in particular the response to the 10-m hawk since only few individuals responded to it. The alarm scores given were as follows ( - = no alarm call; + = alarm call given): large model first, first/second run: - / - = 0; + / - = 2; - / + = 3; + / + = 5 ; small model first, first/second run: - / - =0; + / - = 4 ; - / + =5; + / + =6. The validity of the index can be tested by comparing the average index for the two run orders, which is exactly the same (1.44, U-test, z = 0.01, P = 0-99). Statistical tests below are based on this alarm index. Among adult males two-thirds gave the alarm call at least once, and a quarter gave the alarm call even for the 10-m hawk (Fig. 2). Half of the old females gave an alarm call in some of the tests. Among the young birds over 60% of individuals did not give an alarm call in any of the tests. With respect to age there was a significant difference, old tits having a higher alarm index than young birds (U-test, z = 1.97, P<0.05), but with respect to sex there was no significant difference (U-test, z = 1-01, P>0.10). According to other studies (Ekman & Askenmo 1984; Hogstad 1987; Koivula & Orell 1988) old males are always at the top of the dominance rank in willow tit flocks and young females are at the
bottom. The relationship between old females and young males is less clear, and in the Finnish study (Koivula & Orell 1988), carried out closest to our study area, they had, on average, about the same dominance rank. Using this dominance rank (3=adult male; 2 = a d u l t female, young male; 1 = young female) there is a significant correlation between dominance rank and the alarm index (rs = 0.26, N=64, P<0"05). However, the correlation coefficient is rather small, indicating only a weak tendency for dominant individuals to be more prone to give alarm calls. Many (33%) old males refrained from giving an alarm call while many (39%) of the young females did give one. Individual tits might react in different ways to the stress caused by their capture, which could affect their tendency to give an alarm call. However, there was no correlation between the estimated dominance rank (three categories, see above) and the time taken to notice the model after its appearance (r~= -0"11, N = 4 6 , P>0.10) or the latency to give the alarm call (rs=0.20, N = 17, P>0.10) or the duration of looking (r~=0.12, N=54, P>0-10). Neither was there any correlation between the activity of the individual (1 =perching in both experiments; 1'5 = moving actively in one test; 2 = moving actively in both tests) and the dominance category ( r s = - 0 . 0 9 , N=41, P>0.10). The lack of correlation suggests that it is how likely the bird is to give an alarm call that varies between individuals. Seasonal Variation During late autumn (October-November), when the winter flocks have just formed, only 39 % of the test birds gave the alarm call in at least one of the tests (Fig. 3). In late winter 61% did so, and the tendency to give an alarm call was higher according
Alatalo & Helle: Alarm calls o f willow tits
Autumn
Winter
Figure 3. Percentage of willow tits giving an alarm call to the small ([]) and large (11) models and the percentage keeping silent ([]) in the autumn (N = 31) and winter (N = 33) samples. Mean alarm score: autumn 1.00; winter 1.86 (see text for details). to the alarm index (U-test, z = 1.99, P<0.05). This increase is not due to differences in the composition of the sample with respect to age and sex, since a similar tendency was observable in all the four sexage categories, even though it was not significant in any specific category alone: old males: from 56% (N=9) to 75% (N=12); old females: from 43% (N= 7) to 60% (N= 5); young males: from 25% (N= 8) to 60% (N= 5); and young females: from 29% ( N = 7) to 46% (N= 11). In autumn, during October and early November, the tendency to give an alarm call increased with date (rs=0-40, N=31, P<0-05). In fact, by early November the response was as intense as in late winter. DISCUSSION Willow tits usually remained silent if the hawk was only 10 m away. This indicates that there may be a risk to the caller itself in giving the alarm call. It is likely that hawks flying 40 m away do not hear the alarm call at all, as indicated by the study by Klump et al. (1986a) of the auditory threshold for highfrequency calls of the sparrowhawk. Furthermore, the alarm calls of willow tits are weak. In the closely related North American species, the black-capped chickadee, P. atricapillus, the sound pressure level of the alarm call at a distance of 1 m is only 55-6 dB, less than that of other calls of this species (Ficken & Witkin 1977; Witkin & Ficken 1979). Observations under natural conditions have indicated for many bird species, such as the robin, Erithacus rubecula (East 1981), that birds give alarm calls only if they are in cover (see Klump & Shalter 1984). A similar type of experiment with blue tits, P. caeruleus (Klump & Curio 1983) also revealed that high-frequency alarm calls are given in response to distant (60-m) hawks. Blue tits use another call, scolding, if the hawk is very close
441
(5 m). Scolding has a much wider frequency range suggesting that its function is different to that of an ordinary alarm call, and it has also been reported for great tits, P. major, in similar situations (Klump & Shalter 1984). In our experiments willow tits never scolded. It is worth mentioning that individual tits might have responded differently if they had been tested in a group. It is likely that the characteristics of the alarm call, with its narrow high-frequency band, also serve to reduce the risk that the predator will see and locate the caller (see Klump & Shalter 1984; Klump et al. 1986a). Willow tit alarm calls usually have several weaker overtones and undertones. These harmonics may increase the audibility and localization of the calls to some degree. The fact that old males, highest in the dominance rank in the willow tit flocks, were most likely to give an alarm call suggests that the benefit of doing so is highest for them. In fact, we expected that subordinate young males or females might keep silent because they might benefit from the death of the dominants. This might allow them access to better and safer foraging sites (Ekman 1986). However, the correlation between dominance and tendency to give an alarm call is not very strong and females and young tits do frequently give alarm calls, it may well be that the greater tendency of old males to give alarm calls lies in the importance for them of having a female alive for the next breeding season; the costs of competition with flock members may also be less for them than for the subordinates. Deception or manipulation with alarm calls to an individual's own benefit has been described in other groups of animals (Cheney & Seyfarth 1985; Munn 1986). Great tits have also been observed to use alarm calls deceptively to gain access to a feeding site held by another great tit (Matsuoka 1980; Moiler 1988). The fact that subordinates do give alarm calls suggests that alarm calling in these flocks may involve some kind of reciprocal altruism. The cost of giving an alarm call may be small when it is done only if the predator is far away, and then even small benefits may be sufficient to overcome this cost. The increasing tendency to give alarm calls during the autumn when the flocks stabilize suggests that alarm calling is a feature of stable flocks where the evolution of reciprocal altruism is most likely. Tamachi (1987) presented a model that predicts polymorphism in altruistic alarm calling, suggesting that only some individuals would be callers.
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Animal Behaviour, 40, 3
Superficially our d a t a fit this prediction as half o f the individuals did not give a l a r m calls. However, a l a r m calling is likely to be a b e h a v i o u r p a t t e r n that is d e p e n d e n t on circumstances, in particular on the distance to the predator. It m a y well be t h a t noncallers in o u r study would have given a n a l a r m call if the distance of the model were greater, or if the model were more like a true hawk.
ACKNOWLEDGMENTS W e t h a n k J. Jokim~iki a n d J. S u h o n e n for their help in the field a n d D. Eriksson a n d J. Sorjonen for their help in sound recordings. A g r a n t from the A c a d e m y o f F i n l a n d (to R.A.) is gratefully acknowledged.
REFERENCES Charnov, E. L. & Krebs, J. R. 1975. The evolution of alarm calls: altruism or manipulation? Am. Nat., 109, 107-112. Cheney, D. L. & Seyfarth, R. M. 1985. Selective forces affecting the predator alarm calls of vervet monkeys. Behaviour, 76, 25-61. East, M. 1981. Alarm calling and parental investment in the robin Erithacus rubecula. Ibis, 123, 223-230. Ekman, J. 1979. Coherence, composition and territories of winter social groups of the willow tit Parus montanus and the crested tit P. cristatus. Ornis Scand., 10, 56-68. Ekman, J. 1986. Tree use and predator vulnerability of wintering passerines. Ornis Scand., 17, 261-267. Ekman, J. 1987. Exposure and time use in willow tit flocks: the cost of subordination. Anim. Behav., 35, 445-452. Ekman, J. & Askenmo, C. 1984. Social rank and habitat use in willow tit groups. Anita. Behav., 32, 508-514. Ekman, J. & Askenmo, C. 1986. Reproductive cost, agespecific survival and a comparison of the reproductive strategy in two European tits (genus Parus). Evolution, 40, 159-168. Ekman, J., Cederholm, G. & Askenmo, C. 1981. Spacing and survival in winter groups of willow tit Parus montanus and crested tit P. cristatus: a removal study. J. Anim. Ecol., 50, I-9. Ficken, M. S. & Witkin, S. R. 1977. Responses of black-capped chickadee flocks to predators. Auk, 94, 156-157. Gyger, M., Karakashian, S. J. & Marler, P. 1986. Avian alarm calling: is there an audience effect? Anim. Behav., 34, 1570-1572. Haftorn, S. 1982. Variation in body measurements of the willow tit Parus montanus, together with a method for sexing live birds and data on the degree of shrinkage in size after skinning. Fauna norv. Set. C, Cinclus, 5, 16-26. Hamilton, W. D. 1964. The genetical theory of social behavior. I, II. J. theor. Biol., 7, 1-52.
Harvey, P. H. & Greenwood, P. G. 1978. Anti-predator defence strategies: some evolutionary problems. In: Behavioural Ecology: an Evolutionary Approach (Ed. by J. R. Krebs & N. B. Davies), pp. 129-151. Oxford: Blackwell Scientific Publications. Hogstad, O. 1987. Social rank in winter flocks of willow tits Parus montanus. Ibis, 129, 1-9. Hogstad, O. 1988. Social rank and antipredator behaviour of willow tits Parus montanus in winter flocks. Ibis', 130, 45-56. Hoogland, J. L. 1983. Nepotism and alarm calling in the black-tailed prairie dog, Cynomus ludovicianus. Anim. Behav., 31,472-479. Klump, G. M. & Curio, E. 1983. Reactions of blue tits Parus eaeruleus to hawk models of different sizes. Bird Behav., 4, 78-81. Klump, G. M. & Shalter, M. D. 1984. Acoustic behaviour of birds and mammals in the predator context. I. Factors affecting the structure of alarm calls. II. The functional significance and evolution of alarm signals. Z. Tierpsychol., 66, 189-226. Klump, G. M., Kretzschmar, E. & Curio, E. 1986a. The hearing of an avian predator and its avian prey. Behav. Ecol. Soeiobiol., 8, 317-323. Klump, G. M., Windt, W. & Curio, E. 1986b. The great tit's (Parus major) auditory resolution in azimuth. J. comp. Physiol., 158, 383 390. Koivula, K. & Orell, M. 1988. Social rank and winter survival in the willow tit Parus montanus. Ornisfenn., 65, 114-120. Laaksonen, M. & Lehikoinen, E. 1976. Age determination of willow and crested tit Parus montanus and P. cristatus. OrnisJenn., 53, 9-14. Matsuoka, S. 1980. Pseudo warning call in titmice. Tori, 29, 87-90. Moller, A. P. 1988. False alarm calls as a means of resource usurpation in the great tit Parus major. Ethology, 79, 25-30. Munn, C. A. 1986. Birds that 'cry wolf'. Nature, Lond., 319, 143-145. Sherman, P. W. 1977. Nepotism and the evolution of alarm calls. Science, 197, 1246-1253. Smith, R. J. F. 1986. Evolution of alarm signals: role of benefits of retaining group members or territorial neighbors. Am. Nat., 128, 604-610. Svensson, L. 1975. Identification Guide to European Passerines. Stockholm: Svensson. Tamachi, N. 1987. The evolution of alarm calls: an altruism with nonlinear effect. J. theor. Biol., 127, 141-153. Trivers, R. L. 1971. The evolution of reciprocal altruism. Q. Rev. Biol., 46, 35-56. Wilson, D. S. 1975. A theory of group selection. Proc. natn Acad. Sei. U.S.A., 72, 143-146. Witkin, S. R. & Ficken, M. S. 1979. Chickadee alarm calls: does mate investment pay dividends? Anim. Behav., 27, 1275-1276. (Received 7 October 1988; initial acceptance 11 January 1989; final acceptanee 25 May 1989; MS. number: 3299)
Alarm calling by individual willow tits, Parus montanus RAUNO
V. A L A T A L O * & P E K K A
HELLEt$
*Department of Biology, University of Jyviiskylii, Yliopistonkatu 9, SF-40100 Jyvdskylii, Finland t Meltaus Game Research Station, Finnish Game and Fisheries Research Institute, and Konnevesi Research Station, University of Jyviiskyld, SF-97340 Meltaus, Finland
Abstract. Alarm responses of wild-captured individual willow tits to model sparrowhawks, Accipiter nisus, flying over a test chamber were studied. Tits did not usually give alarm calls if the apparent predator was passing nearby (at a height of 10 m), while over half of the individuals responded by alarm calling for a more distant predator (40 m). This suggests that alarm calling involves a risk to the caller. Second, there was individual variation in the responses, with older males giving the call more frequently than females or young males. The greater responsiveness of adult males may indicate that different individuals in a flock gain different benefits by warning the others. The tendency to give alarm calls increased over the autumn, which could be related to the establishment of cohesive flocks at that time.
The evolution of alarm calls has attracted numerous theories and speculations (see Harvey & Greenwood 1978; Klump & Shalter 1984; Smith 1986). Among these, the idea that animals take the risk of alarm calling for the benefit of their kin (Hamilton 1964) is perhaps the only one that has been verified (Sherman 1977; Hoogland 1983). Other explanations include direct benefits for the caller through predator distraction (Charnov & Krebs 1975), informing the predator that it has been observed, or retaining group companions (e.g. Smith 1986). Reciprocal altruism, where individuals that alert others would gain when these other individuals give alarm calls in the next predator context, is open to cheating (Trivers 1971; Tamachi 1987). Various group-selection arguments have also been proposed (Wilson 1975). Surprisingly little work has been devoted to test these hypotheses, even though experimental studies of alarm calling are feasible (Klump & Curio 1983; Gyger et al. 1986; Klump et al. 1986a). We have studied the willow tit, a common holarctic forest passerine. During the winter individuals stay in small flocks of four to eight birds (Ekman & Askenmo 1984; Hogstad 1987), where individuals are not related because they disperse during the autumn of their first year (Ekman 1979; Ekman et al. 1981). For breeding, the flock separates and pairs usually form between flock members. There is a clear dominance hierarchy in flocks (Ekman & Askenmo 1984; Hogstad 1987; Koivula & Orell ~To whom correspondence should be addressed. 0003-3472/90/090437 + 06 $03.00/0
1988), with older (age over 1 year) males at the top and young (born in the previous summer) females at the bottom, with older females and young males having an intermediate position. Older individuals forage higher in trees, and the experimental removal of these older birds allows young birds to move from lower to upper sites (Ekman & Askenmo 1984). Upper sites in the trees are better since they are safer from predators (Ekman 1986, 1987; Hogstad 1988), and arthropods are more abundant there than in the lower half of spruce (R. V. Alatalo, unpublished data). Given that different individuals have different roles in the flocks, it is possible that they benefit from alarm calling in different ways (Cheney & Seyfarth 1985; Smith 1986). Subdominants might actually benefit from the death of a dominant individual, giving them better access to the limited food resources in feeding sites that are safe from predators, or other resources such as roosting cavities, nesting territories and mates. Under these circumstances, if there are no direct benefits of giving alarm calls such as predator distraction, subdominants might do best by keeping silent, even if there were no cost for calling. Dominants, instead, have more to gain from alerting the others if there are any future benefits such as companion retention or reciprocity in alarm calling at least by some of the other individuals. Willow tits usually mate with members of their flock, and because there is a 5-30% surplus of unmated males (Ekman & Askenmo 1986), the survival of females may be important for males, increasing the benefit to them
9 1990 The Association for the Study of Animal Behaviour 437
Animal Behaviour, 40, 3
438
from calling. To test this hypothesis we looked at the responses of different individuals in a standardized presentation of sparrowhawk, Accipiter nisus, models. If, on the other hand, individuals give alarm calls irrespectively of sex and age, it would suggest that there are instant benefits of alarm calling for all of the individuals or that it involves reciprocal altruism. The explanations involving direct benefits of alarm calling, such as predator distraction or informing the predator that it has already been observed, do not necessarily imply any risk from alarm calling. If alarm calling is costly, increasing the risk of being observed and captured by the predator, animals should be less willing to give the alarm call when the possibilities of escaping the predator are reduced. It is possible to test between these alternatives by varying the risk of being caught by a predator, and for this purpose we varied the perceived distance of a hawk model flying overhead.
METHODS
The experiments were performed at the Konnevesi Research Station in Central Finland (63~ We tested 33 individuals during February-March 1987, when birds are still in stable flocks, and 31 individuals in October-November 1987, when stable flocks have just formed (see Ekman 1979; Ekman et al. 1981). We used individuals that were captured with mist nets from feeding tables within 5 km of the station, and released with colour bands after the experiments. We separated first-year birds from older individuals by the abrasion and shape of the tail, which is a reliable indicator particularly in early winter (Laaksonen & Lehikoinen 1976). For sexing we used the wing length (see Haftorn 1982; Hogstad 1987; Koivula & Orell 1988). Individuals with a maximum wing-chord length (Svensson 1975) of less than 64 mm were defined as females and those with a wing chord of 64 mm or longer as males. The error in sexing the birds by this criterion is just over 5%. We carried out the experiments within 2 h of capturing the birds, which were kept separately in dark boxes in the interim. To avoid problems with changes in temperature, the study chamber was situated outdoors. The birds were placed one at a time in a small (20 x 30 cm) cage on the bottom of a chamber measuring 2 x 1 m with 1 m high closed
walls. The hawk model was attached to a fishing line that was placed 2 m above the cage, and we used an electric motor to move the hawk at a given steady speed over the chamber (see Klump & Curio 1983). Apart from the moving hawk model, the tits could see only the sky above the chamber walls. Each bird was tested once with each model with a 10-rain interval between the two tests. The order of presentations was systematically alternated between consecutive individuals tested. As a close predator, we used the perceived minimum distance of 10 m (model wing span 7.2 cm, speed 120cm/s). The distant predator flew at a simulated height of 40 m (1.8 cm, 30 cm/s). These speeds correspond to a hawk flying at 8.4 m/s (30 km/h), and since the line was visible for a distance of 3'5 m, the distant hawk was visible for 11.7 s and the near hawk for 2'9 s. Our models mimicked a gliding hawk with wings partly folded. Apart from direct observation through a small hole in the chamber wall, we also filmed the experiments on 41 individuals with a video camera to measure the time it took for the tits to notice the hawk model (to the nearest 0.1 s), and to study the responses of tits more carefully in slow motion. However, when the tits were perching it was easy to see when they noticed the hawk model, as they froze with the head typically slightly turned and the bill pointed slightly upwards while they looked at the model. We also recorded on videofihns how long the birds looked at the hawk and their activity (perching or moving around the cage). We recorded some of the alarm calls with a Sony TC-D5M casette recorder and Telinga-pro microphone placed within the test chamber 1 m from the bird. The recordings were analysed with a UNISCAN II Spectrograph.
RESULTS Behaviour of Test Birds
The birds looked at the hawk for on average
(4-SD) 6'5 _+2-9 s ( N = 58, range 2-15 s). There was a slight, but non-significant tendency for individuals giving an alarm call to look longer (7.4 4- 3.15, N-= 20) than the silent ones (6.0 4- 2.6 s, N = 38, t = 1'83, P < 0.10). However, there was no correlation between how long a test bird followed the hawk and the time it took to notice the model and start looking after the appearance of the model (r s= 0'009,
Alatalo & Helle: Alarm calls o f willow tits
439
Table I. Characteristics of alarm calling and alarm calls of willow tits in the experiment
Latency to notice the hawk model (s) Time between first observation and alarm response (s) Duration of alarm call (s) Call characteristics Maximum frequency of major band Frequency range (kHz) Harmonics (no. of separate bands)
Mean
sn
N
2.2
1.5
18
1.3 1.2
1.2 0.8
17 19
8.7 1.4
0.7 0.7
17 17
5.5
2.1
13
N = 47, P > 0-10). Whether the test bird was perching or actively moving around did not influence the time it took from the appearance of the hawk model above the bird to the moment when it responded to its appearance by freezing, raising the bill and beginning to look at it. The birds habituated between the two tests. In the first test the alarm call was elicited from 37.5% and in the second test from 18.8% of the 64 test birds (/~2 = 5'56, P < 0'05). There was no significant difference between tests in the time from the model's appearance to the time the birds started looking at it (first run: X'___SD = 0 ' 8 _ 1' 1 S, N = 25; second run: 0'4_+0"4, N = 2 1 , M a n n - W h i t n e y Utest, z = 1.30, P=0.19), or in the duration of looking (first run: 7-1_+3-1s, N = 2 7 ; second run: 6.1 _+2.6 s, N = 2 7 , t = 1.38, P = 0-17). When the tits did give an alarm call, they did so on average 2.2 s after the appearance of the hawk and 1.3 s after the start of freezing (Table I). The duration of the call varied greatly: the shortest one, including only one element, lasted 0.2 s and the longest one with 10 elements in three bouts went on for 3'0 s. The maxim u m frequency of the major band was 8'7 kHz, but the harmonics were pronounced in m a n y cases. Distance of the Hawk The size of the hawk model had a marked influence on the percentage of tits alarm calling (Fig. 1). Only 10% of tits gave alarm calls when the simulated distance to the hawk was only 10m, while nearly half of them responded by alarm calling when the hawk was 40 m away. The percentages are somewhat higher, 16 and 59% respectively, if
50
I00
5O
Large
Small Model
Figure 1. Percentage of willow tits giving an alarm call ( 9 and keeping silent ([]) in response to the large and small hawk models in (a) the first and (b) the second run.
only the first runs are included, eliminating the effect of habituation. There was a non-significant tendency for tits to notice the 10-m hawk sooner after its appearance (X'+SD=0.4+0-3 s, N = 2 8 ) than the 40-m hawk (1.0+ 1.1 s, N = 2 2 , U-test, P<0.10). Hence, with regard to observability one would expect the 10-m hawk to elicit a greater response. Since the 10-m hawk moved faster it was visible for 2.9 s, whereas the 40-m hawk was visible for 11.7 s. Consequently following the 10-m hawk was somewhat shorter (5.5+2.5s, N = 3 1 ) than for the 40-m hawk (7.7+2"9s, N = 2 7 , t = 3 ' 1 7 , P<0"01). One could speculate that the shorter period of visibility might prevent tits from alarm calling at the 10-m hawk. However, 75% ( N = 16) of the alarm responses to the 40-m hawk were given within the 2.9-s period for which the 10-m hawk was visible. Furthermore, alarm calling was not restricted to the period when the hawk was visible, and in two of the seven alarm calls given in response to the close hawk the tit clearly waited until the hawk was no longer visible before it gave the alarm call. There were no observable differences in the alarm calls that were given to close or distant hawk models, but we had only two recordings of the few alarm calls for the close hawk. The two calls were
Animal Behaviour, 40, 3
440
5O
Adult male 2,24
Adult female
1-33
Juvenile male Juvenile female 0-85 1.00
Figure 2. Percentageof willowtits givingan alarm call to the small ([] ) and large ( 9 ) modelsand the percentage keeping silent ([2) by sex and age. Sample sizes are: adult male 21, adult female 12, juvenile male 13 and juvenile female 18. Numbers show the mean alarm score (see text for details). typical alarm calls with the maximum frequency of the main band 8"8 kHz in both cases and the maximum frequency range 1-1 and 1.3 kHz. Individual Differences Since the distance of the model and the order of presentation influenced the probability of eliciting the alarm call we used an index of alarm call tendency (alarm score) to standardize the effect of the run order. The index is highest if an individual gave an alarm call for the 10-m hawk and if the alarm response also appeared in the second test; we thus weighted in particular the response to the 10-m hawk since only few individuals responded to it. The alarm scores given were as follows ( - = no alarm call; + = alarm call given): large model first, first/second run: - / - = 0; + / - = 2; - / + = 3; + / + = 5 ; small model first, first/second run: - / - =0; + / - = 4 ; - / + =5; + / + =6. The validity of the index can be tested by comparing the average index for the two run orders, which is exactly the same (1.44, U-test, z = 0.01, P = 0-99). Statistical tests below are based on this alarm index. Among adult males two-thirds gave the alarm call at least once, and a quarter gave the alarm call even for the 10-m hawk (Fig. 2). Half of the old females gave an alarm call in some of the tests. Among the young birds over 60% of individuals did not give an alarm call in any of the tests. With respect to age there was a significant difference, old tits having a higher alarm index than young birds (U-test, z = 1.97, P<0.05), but with respect to sex there was no significant difference (U-test, z = 1-01, P>0.10). According to other studies (Ekman & Askenmo 1984; Hogstad 1987; Koivula & Orell 1988) old males are always at the top of the dominance rank in willow tit flocks and young females are at the
bottom. The relationship between old females and young males is less clear, and in the Finnish study (Koivula & Orell 1988), carried out closest to our study area, they had, on average, about the same dominance rank. Using this dominance rank (3=adult male; 2 = a d u l t female, young male; 1 = young female) there is a significant correlation between dominance rank and the alarm index (rs = 0.26, N=64, P<0"05). However, the correlation coefficient is rather small, indicating only a weak tendency for dominant individuals to be more prone to give alarm calls. Many (33%) old males refrained from giving an alarm call while many (39%) of the young females did give one. Individual tits might react in different ways to the stress caused by their capture, which could affect their tendency to give an alarm call. However, there was no correlation between the estimated dominance rank (three categories, see above) and the time taken to notice the model after its appearance (r~= -0"11, N = 4 6 , P>0.10) or the latency to give the alarm call (rs=0.20, N = 17, P>0.10) or the duration of looking (r~=0.12, N=54, P>0-10). Neither was there any correlation between the activity of the individual (1 =perching in both experiments; 1'5 = moving actively in one test; 2 = moving actively in both tests) and the dominance category ( r s = - 0 . 0 9 , N=41, P>0.10). The lack of correlation suggests that it is how likely the bird is to give an alarm call that varies between individuals. Seasonal Variation During late autumn (October-November), when the winter flocks have just formed, only 39 % of the test birds gave the alarm call in at least one of the tests (Fig. 3). In late winter 61% did so, and the tendency to give an alarm call was higher according
Alatalo & Helle: Alarm calls o f willow tits
Autumn
Winter
Figure 3. Percentage of willow tits giving an alarm call to the small ([]) and large (11) models and the percentage keeping silent ([]) in the autumn (N = 31) and winter (N = 33) samples. Mean alarm score: autumn 1.00; winter 1.86 (see text for details). to the alarm index (U-test, z = 1.99, P<0.05). This increase is not due to differences in the composition of the sample with respect to age and sex, since a similar tendency was observable in all the four sexage categories, even though it was not significant in any specific category alone: old males: from 56% (N=9) to 75% (N=12); old females: from 43% (N= 7) to 60% (N= 5); young males: from 25% (N= 8) to 60% (N= 5); and young females: from 29% ( N = 7) to 46% (N= 11). In autumn, during October and early November, the tendency to give an alarm call increased with date (rs=0-40, N=31, P<0-05). In fact, by early November the response was as intense as in late winter. DISCUSSION Willow tits usually remained silent if the hawk was only 10 m away. This indicates that there may be a risk to the caller itself in giving the alarm call. It is likely that hawks flying 40 m away do not hear the alarm call at all, as indicated by the study by Klump et al. (1986a) of the auditory threshold for highfrequency calls of the sparrowhawk. Furthermore, the alarm calls of willow tits are weak. In the closely related North American species, the black-capped chickadee, P. atricapillus, the sound pressure level of the alarm call at a distance of 1 m is only 55-6 dB, less than that of other calls of this species (Ficken & Witkin 1977; Witkin & Ficken 1979). Observations under natural conditions have indicated for many bird species, such as the robin, Erithacus rubecula (East 1981), that birds give alarm calls only if they are in cover (see Klump & Shalter 1984). A similar type of experiment with blue tits, P. caeruleus (Klump & Curio 1983) also revealed that high-frequency alarm calls are given in response to distant (60-m) hawks. Blue tits use another call, scolding, if the hawk is very close
441
(5 m). Scolding has a much wider frequency range suggesting that its function is different to that of an ordinary alarm call, and it has also been reported for great tits, P. major, in similar situations (Klump & Shalter 1984). In our experiments willow tits never scolded. It is worth mentioning that individual tits might have responded differently if they had been tested in a group. It is likely that the characteristics of the alarm call, with its narrow high-frequency band, also serve to reduce the risk that the predator will see and locate the caller (see Klump & Shalter 1984; Klump et al. 1986a). Willow tit alarm calls usually have several weaker overtones and undertones. These harmonics may increase the audibility and localization of the calls to some degree. The fact that old males, highest in the dominance rank in the willow tit flocks, were most likely to give an alarm call suggests that the benefit of doing so is highest for them. In fact, we expected that subordinate young males or females might keep silent because they might benefit from the death of the dominants. This might allow them access to better and safer foraging sites (Ekman 1986). However, the correlation between dominance and tendency to give an alarm call is not very strong and females and young tits do frequently give alarm calls, it may well be that the greater tendency of old males to give alarm calls lies in the importance for them of having a female alive for the next breeding season; the costs of competition with flock members may also be less for them than for the subordinates. Deception or manipulation with alarm calls to an individual's own benefit has been described in other groups of animals (Cheney & Seyfarth 1985; Munn 1986). Great tits have also been observed to use alarm calls deceptively to gain access to a feeding site held by another great tit (Matsuoka 1980; Moiler 1988). The fact that subordinates do give alarm calls suggests that alarm calling in these flocks may involve some kind of reciprocal altruism. The cost of giving an alarm call may be small when it is done only if the predator is far away, and then even small benefits may be sufficient to overcome this cost. The increasing tendency to give alarm calls during the autumn when the flocks stabilize suggests that alarm calling is a feature of stable flocks where the evolution of reciprocal altruism is most likely. Tamachi (1987) presented a model that predicts polymorphism in altruistic alarm calling, suggesting that only some individuals would be callers.
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Animal Behaviour, 40, 3
Superficially our d a t a fit this prediction as half o f the individuals did not give a l a r m calls. However, a l a r m calling is likely to be a b e h a v i o u r p a t t e r n that is d e p e n d e n t on circumstances, in particular on the distance to the predator. It m a y well be t h a t noncallers in o u r study would have given a n a l a r m call if the distance of the model were greater, or if the model were more like a true hawk.
ACKNOWLEDGMENTS W e t h a n k J. Jokim~iki a n d J. S u h o n e n for their help in the field a n d D. Eriksson a n d J. Sorjonen for their help in sound recordings. A g r a n t from the A c a d e m y o f F i n l a n d (to R.A.) is gratefully acknowledged.
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