Predators, risks and context for mobbing and alarm calls in black-billed magpies

Anim. Behav., 1991,41, 633-638

Predators, risks and context for mobbing and alarm calls in black-billed magpies

E R I C S T O N E & C H A R L E S H. T R O S T Department o f Biological Sciences, Idaho State University, Pocatello, Idaho 83209, U.S.A.

(Received 9 April 1990; initial acceptance 7 June 1990; final acceptance 5 September 1990; MS. number: A5775)

Abstract. Black-billed magpie, Pica pica hudson&, mobbing and alarm calls were recorded for each of several different predator contexts. These were analysed spectrographically to determine whether the callers used temporal variation to communicate (1) the nature of the danger, (2) the identity of the predator and (3) the risks involved in actions resulting from alertness to the presence of the predator (e.g. fleeing or mobbing). The results support the notion that magpies vary call syllable length to give recipients information about the nature of the danger and to respond to a predator in an appropriate manner. Playback experiments were conducted using recordings of the separate call types as stimuli. The aim of the playback experiments was to determine whether one form of call elicits a more intense reaction from recipients than another call. It was found that magpies responded to calls with longer syllables by approaching the speaker while their response to calls with shorter syllables was aversive.

Over the past decade there has been considerable interest in and debate about the evolution of alarm calls in birds and mammals (reviews in Wittenberger 1981; Barnard 1983). Some of the most pressing questions concern the relative costs and benefits for the three participants: the initiator of an alarm signal (the individual that first spots a predator and gives the initial alarm signal), the recipient(s) of the alarm signal, and the predator (who may also be a recipient). How such behaviour could have evolved, since initiators put themselves at risk by drawing attention to themselves while calling (Melchior 1971; Sherman 1977, 1980), is especially problematic in cases where alarm calls are not of a type or quality that is difficult for predators to locate (Shalter & Schleidt 1977). The initiator and recipient(s) of alarms are not always related to one another. Thus, kin selection is not always sufficient to explain alarm calling in the presence of a predator. The initiator's call may function to prevent attack by signalling to the predator that it has been spotted and that further pursuit by the predator would be fruitless. But this hypothesis has been difficult to support. Callers are often more likely to be attacked than non-calling members of a group (Smythe 1970, 1977; Coblentz 1980).

The question of how alarm-calling behaviour might have evolved can be extended to include predator mobbing (Curioet al. 1978). Shields (1984) found that members of mobbing groups of barn swallows, Hirundo rustica, do not participate

equally in mobbing but instead, some individuals are 'passive' and some are 'active' mobbers. Mobbing a predator may enhance the individual fitness of the initiators ('active' mobbers) if by recruiting others they are able to (1) dilute the attention of the predator on themselves and divert it to other birds, or (2) succeed in driving the predator away. Several hypotheses exist regarding the benefits to individuals recruited to mob (see Curio et al. 1978; Shields 1984). Though not mutually exclusive, these hypotheses assume that recruits have some means of assessing the risks involved when deciding whether to respond to an alarm call. A second assumption is that the initiator of a mobbing can coordinate the actions of the other members of the group. The rationale for this assumption stems from observations that animals will not always mob a predator. Buitron (1983) revealed that responses of black-billed magpies, Pica pica hudsonia, to a predator vary in intensity at different times during the breeding season. She suggested that the degree of parental investment was one of the critical fac- tors determining the intensity of mobbing. Magpies also responded more intensely to predators that posed a significant threat to vulnerable young than to predators that were not a significant threat. For example coyotes, Canis latrans, were mobbed more intensely when young were fledging than when they were nestlings. This seems reasonable in light of the fact that coyotes only prey on fledgling magpies that are learning to fly and are found on the ground,

0003-3472/91/040633+06 $03.00/0 �9 1991 The Association for the Study of Animal Behaviour

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634 Animal Behaviour, 41, 4

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Figure l. Sonagrams of magpie alarm calls (a) staccato call (b) basic call. SL: syllable length, ISL: inter-syllable length.

unable to escape. Buitron's findings imply that something exists within the alarm calls of initiators that yields information concerning the context or risk involved and whether a mobbing is necessary. It appears likely that the type of call that an initiator gives coordinates the flock's response to the presence of a predator�9 Melchior (1971) found similar variability in the alarm calls of small mammals.

Black-billed magpies mob under a variety of circumstances. They have even been observed to mob dead conspecifics. The advantage of this behaviour is unclear, although a dead conspecific may signify the presence of a predator. Moholt 's (1989) investigation of variation in the mobbing response to a model predator and to a dead conspecific suggests that graded mobbing (perhaps alarm) calls were given in each context and that these calls differed with respect to the length of their syllables. Simi- larly, Buitron (1983) states that one variation of the alarm call ('staccato call') was given more often in one predator context, that of a flying hawk, than another call ('basic call'). Figure 1, a sonographic comparison of alarm calls, shows that these two call types differ significantly in the length of the syllables. Moholt (1989) found however that they did not differ in the inter-syllable distance or in the

number of syllables per call. Buitron (1983) also described the temporal variation between these calls.

Recently Ficken (1990) described variability in pitch in the alarm calls of the Mexican chickadee, Parus selateri. Although the results of Ficken's analysis of these calls under different contexts strongly suggest that these birds, as well as other species, are able to vary call structure in a graded fashion to communicate contextual information to conspecifics, they do not indicate that the birds actually do this. Call variability may simply indicate a change in the motivational state of the individual making the call. Without examining the response of individuals receiving these calls, it is difficult to make specific inferences about what types of information these calls actually relay to conspecifics.

Our aims in this study were to determine whether variation in mobbing and alarm calls of black- billed magpies is associated with specific predator contexts and whether magpies discriminate variation in the temporal components of conspecific alarm calls to coordinate an effective and appropriate response to a predator. Our study addresses the following questions. (1) Can variability within alarm or mobbing calls be ascribed to the context in

Stone & Trost: Magpie mobbing and alarm calls 635

which the calls were given? (2) Do magpies discriminate variation in alarm or mobbing calls and respond differently to different calls?

M E T H O D S

Recorded Calls

We recorded calls given under a variety of natural circumstances, including calls given when the presence of real predators had been detected by a flock of magpies. This part of the investigation was carried out prior to and during the breeding season. Magpies gave alarm calls and mobbed when approached by terrestrial predators such as domestic cats, Felis domestieus, and dogs, Canis familiaris, or humans and at the approach of avian predators such as hawks.

Because it was unlikely that all flocks would be recorded mobbing or giving alarm calls in the presence of identical 'natural predators', we attempted to characterize each type of 'encounter'. The categories used were: (1) type of predator: (a) terrestrial or (b) avian; (2) time of breeding seasons: (a) nest building, (b) egg laying, (c) nestling or (d) fledging; and (3) the behaviour of the callers towards the predator: (a) mobbing or (b) alarm. We also estimated the distance from the predator to the bird giving the call when each call was given.

Terrestrial predators pose little threat to adult magpies but are often predators of nests or fledged young that have not yet learned to fly. Some hawks (e.g. red-tailed hawks, Buteo jamaieensis) may occasionally be a threat to young, while larger acci- piters (e.g. northern goshawks, Accipiter gentilis), and falcons (e.g, prairie falcon, Faleo mexicanus) are predators of adult magpies. A flying hawk is considerably more of a threat to magpies than one that is perched at a great distance. However, if the hawk is perched so as to attack, it may be a far more dangerous target to mob (Buitron 1983). We did not attempt to use the activity of a predator as a factor that might influence the type of call given, although it is possible that such an effect existed.

We recorded the calls with a Fostex X-30 cassette- tape deck and a hand-made parabolic microphone by positioning ourselves within 50 m of an active nest and waiting until a predator arrived. Thirteen nests were used at three separate locations. Because we could not be sure that any individual magpie made a particular call, we did not use a paired design in our statistical analysis. Instead, we used a ehi-

squared test after characterizing all calls with regard to the length of their syllables. Recordings were analysed using the calipers ofa Multigon Uniscan II sonagram. Only the first call recorded for each 'predator event' was used in the analysis as responses to predators were expected to change during each encounter with a predator and as calls given in response to the same predator were not independent events. Each call (the mean of all syllables) was described as either 'basic' (mean syllable length > 0' 12 s), 'intermediate' (mean syllable length between 0.112 and 0.093 s), or 'staccato' ( < 0.093 s) after Buitron (1983).

Playback Experiments

Synthetic stimulus calls for each type (basic, intermediate and staccato) were produced using the SOUNDWAVE computer software and digital converter. This computer package digitizes sound and stores it in computer memory allowing the experimenter to edit the sound by altering fre- quencies, decibel levels and temporal components, and to paste sounds together. Thus, we were able to create stimulus tapes of calls that were equivalent in volume, number of syllables per call and the rate at which the entire call was repeated.

The stimulus calls were played on a Panasonic RX-F9 tape deck and speaker to focks of magpies in locations throughout southeast Idaho, western Wyoming and northern Utah. To control for seasonal changes in responses to playbacks, all of the experiments were conducted after magpies in the area had fledged young (June-July). Each trial represented a random sample of subjects. The order of stimuli was rotated among successive tests and two examples of each stimulus were used to control for any incidental effects due to unmeasured components of any particular stimulus. Each test began when at least one magpie was within 50 m of a speaker and consisted of 5 min of calls followed by 10 rain of silence. For each 1-min interval during the playback, we recorded the nearest distance of any bird to the speaker. Because the number of birds present at the beginning of each experiment was expected to determine the eventual number of birds responding to the playback, we used only the distance measure as a means of examining differences in response to each call type. These were used to test for significant differences in response between treatment stimuli using a repeated- measures ANOVA.


Table I. Contexts for call types that were recorded in the presence of natural predators

Call type

Context Staccato Intermediate Basic Z 2 (df) P

Predator Avian 18 15 7 Terrestrial 13 6 9 2.886 (2) NS

Season Nest building 8 0 0 Egg laying 12 7 4 Nestling 8 9 6 Fledging 3 5 6 15.418 (6) <0.05

Behaviour Mobbing 0 5 15 Alarm only 31 16 1 45.135(2) <0.0001

80

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Playback

I I i i I i I t I

I 2 5 4 5 i I ~ I i L a I I ] i I i I i I i I i I i

2 0 0 6 7 8 9 I 0 I I 1 2 1 5 1 4 1 5 1 6

Minute of playback

Figure 2. Response to playback (5 min followed by 10 min of silence, N = 13 per stimulus) of each call type, staccato ( � 9 intermediate (A) and basic ((3). The response was measured as the nearest distance any bird came towards the speaker during each minute interval. F= 1.648, df= 28,504, P < 0.025. Repeated-measures ANOVA.

R E S U L T S

Recorded Cal l s

Sixty-eight encounters were recorded as follows: 18 northern harrier, Circus cyaneus; 14 human; 10 american crow, Corvus brachyrhyncos; seven domestic cat; four raccoon, Procyon lotor; four red-tailed hawk; four northern goshawk; one red fox, Fulpes vulpes; two cooper 's hawk, Accipiter cooperii; one great-horned owl, Bubo virginianus;

one domestic dog; and two unidentified terrestrial predators.

Significant differences were found for two of the three context categories (Table I) . Staccato calls were given more often in the early stages of the breeding season whereas basic calls were given more often late in the breeding season, Staccato calls were given when mobbing did not ensue. Con- versely, when the response was to mob the intruder, basic calls were usually given, suggesting that the

Stone & Trost: Magpie mobbing and alarm calls 637

long-syllable basic call functions to recruit conspecifics to mob a predator. There was a tendency, although it was not a significant one, for avian predators to elicit staccato calls and for terrestrial predators to be responded to with basic calls, which is consistent with the findings of Buitron (1983). We also found that basic calls were given when predators were significantly closer to a caller (staccato: 52.83_ 61.64 m, intermediate: 49.75_ 68'55 m, basic: 7-19_5.5m, F=3.79, df=2,63, P=0.028 one-way ANOVA). Thus, we conclude that the basic call is associated with a mobbing context and may be used to recruit other magpies to mob a predator while the staccato call is a more general alarm signal and may be used to alert others to the presence of a predator.

Playback Experiment

A significant interaction term of the repeated- measures ANOVA, using the nearest distance any bird came within each 1-min interval shows that the responses of magpies to playback of the three stimulus calls were different. Magpies responded to basic calls by moving towards the call (speaker) whereas the response to staccato calls was to increase the distance between the bird and the speaker (Fig. 2). It is evident that the magpies' initial response to the basic call was to investigate or attack. In two cases this resulted in a magpie actually landing on the speaker and attacking it with pecks from its beak. The typical response to a staccato call was to fly further away; the response to the intermediate call was moderate and somewhat inconsistent.

D I S C U S S I O N

Our results suggest a mechanism whereby recipients of alarm and mobbing calls might receive information concerning the context, the relative risks and the benefits to an individual. If magpies responding to an alarm call do indeed assess the relative risk involved in confronting a predator, our results represent a significant improvement in the under- standing of this behaviour. While communication of context or risk is not uncommon in animals, the ability of individuals to discriminate and respond appropriately has been less well examined.

Several of the hypotheses used to explain the advantages to an individual that is recruited to

mob a predator fall into the following three general categories.

The Cultural Transmission of Enemy Recognition Hypothesis

Curio et al. (1978) suggests that recruits benefit by learning to avoid future dangerous encounters with predators by observing other birds mobbing a dangerous object. Shields (1984) showed initiators of mobbings, which he termed 'active' mobbers, were those with dependent offspring or kin nearby, while recruits other than a mate ('passive' mobbers) often stayed at a distance from the predator and rarely put themselves at risk. An assumption of the cultural transmission hypothesis is that young or inexperienced individuals would 'know' to respond to mobbings because they would be obtaining valu- able information. If this were the case, one might expect younger more naive individuals to respond more often in mobbing situations. We know of no direct evidence to support this prediction. Shields (1984) found that recruits were a random sample of the source population.

The Selfish Herd Hypothesis

Hamilton (1971) suggested that recruits respond to danger by aggregating to dilute the attention of the predator on any one individual. The individual benefits, as a member of a flock, because it is less likely to be attacked and more likely to be warned earlier when attack is imminent. The benefits, however, are not evenly distributed among all individuals. Dominant individuals often occupy the least vulnerable positions, such as the centre of a flock, while subordinates are at the periphery. Thus, one could argue that the cohesiveness of social groups could not be based solely on each individual's selfish interest alone. Otherwise, subordinate individuals would not be expected to join a flock unless the risk of predation to the individual was still greater than as a subordinate flock member. Our results suggest a mechanism whereby recruits might assess the contexts and risks of group membership.

The Move-on Hypothesis

Curio et al. (1978) suggests that the benefit to all participants in a mobbing is the prevention of predators remaining within the area. Thus, the mobbing of a predator will deter the predator from


developing a search image for the prey species and continuing predation. This hypothesis assumes that alternative strategies such as cheating (e.g. hiding while other individuals mob the predator) would not exist.

All three hypotheses assume that recruits can assess the relative risks of mobbing while initiators o f a mobbing can coordinate the response of conspecifics. We have shown that a mechanism exists whereby black-billed magpies can accomplish both of these ends.

Magpie basic calls were given in a mobbing context and were similarly responded to during playback. These basic calls were distinguished from staccato calls, which were given in an alarm or alert context only. The response by magpies to the broadcast of the staccato call was typically to flee or hide. As with similar experiments in bird songs, the responses of individuals to variation in alarm calls was shown to correspond to the contexts in which these variations are given. Addit ional evidence of the link between variation in call type and the transfer of information between individuals was obtained using playbacks in which the variation might have otherwise been explained by suggesting that the caller's motivational state gave rise to the observed variation.

A C K N O W L E D G M E N T S

The study was partially funded by a grant in aid of research from Sigma Xi, The Scientific Research Society and a grant from The Graduate Committee for Research and Scholarship at Idaho State University. We are especially grateful to Mike Baker, Deborah Buitron, Millicent Ficken and William Shields for advice and comments made on

an early draft of the manuscript and to Kendrick Mohol t for the original 'brainstorm'.

R E F E R E N C E S

Barnard, C. J. 1983. Animal Behavior. New York: John Wiley.

Buitron, D. 1983. Variability in the response of black- billed magpies to natural predators. Behaviour, 87, 209 236.

Coblentz, B. E. 1980. On the improbability of pursuit invitation signals in mammals. Am. Nat., 115,438-442.

Curio, E., Ernst, V. & Vieth, W. 1978. Cultural transmission of enemy recognition: one function of mobbing. Science, 24, 89~901.

Ficken, M. S. 1990. Acoustic characteristics of alarm calls associated with predation risk in chickadees. Anim. Behav., 39, 400-401.

Hamilton, W. D. 1971. Geometry for the selfish herd. J. theor. Biol., 31,295-3! 1.

Melchior, H. R. 1971. Characteristics of arctic ground squirrel alarm calls. Oecologia (Berl.), 7, 184-190.

Moholt, R. K. 1989. Dominance, predator interactions, and social gatherings of the black-billed magpie. M.S. thesis, Idaho State University, Pocatello.

Shalter, M. D. & Schleidt, W. M. 1977. The ability of barn owls (Tyto alba) to discriminate and localize avian alarm calls. Ibis, 119, 22 27.

Sherman, P. W. 1977. Nepotism and the evolution of alarm calls. Science, 197, 1247-1253.

Sherman, P. W. 1980. The limits of ground squirrel nepotism. In: Sociobiology." Beyond Nature/Nurture? (Ed. by G. W. Barlow & J. Silverberg), pp. 505-544. Boulder, Colorado: Westview.

Shields, W. M. 1984. Barn swallow mobbing: self-defence, collateral kin defence, or parental care? Anim. Behav., 32, 132-148.

Smythe, N. 1970. On the existence of pursuit invitation signals in mammals. Am. Nat:, 104, 491-494.

Smythe, N. 1977. The function of mammalian alarm advertising: social signals or pursuit invitation? Am. Nat., 111, 191-194.

Wittenberger, J. F. 1981. Animal Social Behavior. Boston: Duxbury.

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Predators, risks and context for mobbing and alarm calls in black-billed magpies