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Two conflicting needs affecting predator mobbing by great tits, Parus major
Anim. Behav., 1988, 36, 926-932
Two conflicting needs affecting predator mobbing by great tits, Parus major UWE ZIMMERMANN & EBERHARD CURIO Arbeitsgruppe f~r Verhaltensforschung, Fakultiit fiir Biologie, Ruhr-Universitiit Bochum, D-4630 Bochum, West German),
Abstract. Predator mobbing by great tits, Parus major, was studied by manipulating two contextual
variables: the proximity of danger to the nest hole (close versus far), and breeding condition (non-breeding versus nest building versus care of nestlings). In five experiments pitting these contextual variables against each other, great tits were presented with a multi-species mobbing chorus signalling danger to which they responded by typical predator harassment. Based on the 'move on' hypothesis of harassment and on context manipulation, harassment levels specific for each of the five experiments could be predictably ordered; the ensuing rank order of scores reflected, by its nature, a series of four strong inference tests. Whereas two latency measures supported the move on hypothesis, two distance-from-danger measures suggested nest hole concealment to be an opposing need; a fifth measure of harassment, comprising both latency and distance, held an intermediate position, thus tying in with the compromise nature of harassment. Considering the 'phantom' nature of the unseen danger stimulus applied, the defence levels observed must be regarded as moderately conservative. There are natural danger stimuli (e.g. cats) that more effectively prevent great tits displaying predator harassment.
When harassing a predator animals run the risk of being injured or killed (reviewed in Curio & Regelmann 1985) and lose time and opportunities to engage in other activities (Curio 1978). What advantages do harassers gain in return? One answer could be the 'move on' hypothesis: a predator should leave an area the sooner, the more intensely and/or the longer it is molested (Curio 1963; Thielcke 1970; Vogel 1975; Cully & Ligon 1976; evidence: Bildstein 1982; Shedd 1982), and should be less likely to attack again (Curio 1978). The move on hypothesis should hold mainly for birds defending a localized resource, especially in the breeding season. Otherwise the prey bird might more easily move away from the site of an encounter. Many authors have emphasized that harassment may protect vulnerable offspring from predators (Toenhardt 1935; Robertson & Biermann 1979; Shalter 1979; Andersson et al. 1980; Barash 1980; Curio 1980; Shedd 1982) although the main avian predators of European hole-nesting birds, the sparrowhawk, Accipiter nisus, and the pygmy owl, Glaucidium passerinum, pose a threat primarily to the parents. Yet offspring would starve to death if a parent were killed by the raptor. Moreover, the pygmy owl is known to pull out young from nest holes on occasion (Scherzinger 1970; Mrckel & Mrckel 1984), while stoats, Mus926
tela erminea, pose a common threat to nestlings and brooding females alike (Perrins 1979). Furthermore, by mobbing intensely parents might disclose their nests to a searching predator (Thurow & Black 1981). There is a lot of indirect evidence that protection of the young is the major determinant of the strength of parental mobbing behaviour. When threatened, great tits and blue tits, Parus caeruleus, mob vocally only at their own nest but silently at their neighbour's nest (Curio 1980; see also Shalter 1979). Similarly, some birds engage in predator harassment only when owning a nest (Horn 1968). Furthermore, in several species the intensity of parental mobbing increases with the age of the young (Curio 1975; Andersson et al. 1980; GreigSmith 1980; Regelmann & Curio 1983), or, with the progression from non-breeding to breeding conditions (Shedd 1982). The critique by Knight & Temple (1986a) who suggested that the age-related increase is due to habituation of fear from the predator stimulus does not apply in the many cases where parents have been tested only once. Great tits stay in and defend their territories more or less during the whole year and leave it only when food is becoming scarce during winter (Drent 1983). Accordingly, great tits mob at a source of danger the whole year round (Hinde 1952; Zim-
Zimmermann & Curio: Conflicting needs in mobbing mermann, unpublished data). In the present study we set out to examine to what extent predator harassment by great tits is influenced, first, by the effect of season and, second, by the proximity of a potential predator to their nest sites. By pitting these contextual variables against each other, we wanted to find out whether great tits solely strive at moving on the predator, with no other need compromising the defence.
M E T H O D S AND S T U D Y AREAS Great tits were lured and induced to mob at a playback of a mixed mobbing tape-recording from a Uher Stereo Report 4200 at 19 cm/s. Similarly, other songbirds were lured inadvertently. The sound stimulus consisted of 2 min of mixed species mobbing chorus (including great tit 'churring'), 1 min of mixed mobbing paired with an artificial 800 Hz sine tone (patterned after the song of the pygmy owl, which did not occur in the study areas), 2 min of the pure sine sound alone and 3 min of mixed mobbing again. (For a more detailed description, technical details and the irrelevance of other species see Regelmann & Curio 1983; for the rationale see Curio et al. 1978.) All individuals were tested only once. The ensuing behaviour was recorded by one of one to three observers from a distance of 15-30 m from the loudspeaker (for details see Regelmann & Curio 1983). The behaviour provoked did not differ qualitatively from that elicited by a live pygmy owl, although in the former case the tits were more cautious (Curio 1979). Five experiments were carried out. Experiment I was conducted at the start of the breeding season (March) during incipient nest building, prior to egg laying. The loudspeaker was positioned 3 m from the nest box and 1 m above ground. Experiment II was conducted at the same time (March) as experiment I, with the speaker positioned at least 20 m away from the nest box. Experiment III was conducted during the breeding season (26 May through 9 June) when great tit pairs were feeding first broods, with the speaker positioned as in experiment I, thus constituting the most immediate threat to the brood. Experiment IV was conducted during the nestling stage (23 April through 26 May, when some broods were still to hatch) at locations selected at
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random, i.e. without prior knowledge of great tit nest sites, but at least 20 m away from potential great tit nest boxes. Experiment V was conducted during the whole year with the exception of the periods in experiments I-IV without knowledge of great tit territories and at least 20 m from possible roosting holes, thus constituting the least threat to the tits. Experiments of type III with great tit pairs feeding first brood nestlings were performed in Lower Saxony near Wolfsburg in study plots of the AuBenstation ffir Populations/Skologie of the 'Vogelwarte Helgoland' in 1977, 1978 and 1980 (for a description see Regelmann & Curio 1983). The other experiments (I, II, IV, V) were conducted in forest and park areas of the Ruhrgebiet in 1979, 1980 and/or 1983. Both the homogeneity of data from different years and the homogeneity of monthly data pooled from trials in the nonbreeding season were tested with a Kruskal-Wallis H-test. For three out of five parameters the trials of two non-breeding season months had to be excluded in order to maintain homogeneity (details of monthly variation in Zimmermann, unpublished data). The following variables which have been described in detail previously (Regelmann & Curio 1983) were compared across different experimental groups. (1) Latency of Approach is the time from the onset of the playback to when a great tit was first seen approaching the speaker. A short latency tends to reflect a greater risk since the number of mobbers joining the party and thus sharing the (apparent) risk always increases as the trial goes on (Wolf, personal communication). (2) Latency of Calling is the time from the start of the tape until the first mobbing call of a great tit. (3) Latency of Attaining Minimum Distance is measured from the onset of the playback until a great tit approached the speaker the closest, compared to all of its other vantage points. (4) Median Distance is the median of at least five distance values from all great tits recorded during a trial. (5) Minimum Distance (MD) should reflect best the risk taken (Regelmann & Curio 1983). These behavioural variables were scored only for the first or the nearest great tit independent of its sex and for males and females separately. If more than one great tit of one sex appeared, the scores of the earliest or the nearest bird were processed and the data were pooled for that sex. During the
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Animal Behaviour, 36, 3
breeding season, only one or two great tits usually came to the experimental site (for example in experiment IV in 80% of 35 trials). Overall, however, great tits other than the territorial bird(s) also tended to approach the speaker though more cautiously. In the non-breeding season (experiment V), when flocks of great tits responded to the stimulus, a male and a female approaching most closely were scored as pair mates. By invariably selecting the strongest responses we attempted to process territory owners only.
PREDICTIONS Evidence is accumulating that harassment serves to move on the predator (Dyrcz et al. 1981; Bildstein 1982; Shedd 1982; Klump & Shalter 1984) and thus deny sustenance to it in the harasser's home range. It is reasonable to assume that the more closely the harasser homes in on the predator and the longer it does so the more effective will be any move on effect (Curio & Regelmann 1985). Accordingly shorter latencies and shorter distances up to which mobbers approach the interloper will be more effective, all other things being equal. In fact latencies, distance measures and the inverse of the call repetition rate all covary, thus underpinning the premise of the move on hypothesis (Regelmann & Curio 1983). Given that the brood is a major beneficiary of predator harassment (Regelmann & Curio 1983, 1986; see also Discussion), and given that nestlings are worth more to the parents than a newly started nest or an empty hole, the following predictions appear reasonable. Among the stages tested, harassment should decline in the order Breeding (nestling stage), Start of Breeding (nest building), Non-breeding. Among the stimulus sites tested, harassment should also decline in the order Near (nest) hole, Away from (nest) hole. Incidentally, the parents would benefit too by increasing their harassment when threatened at their nest site where their travel routes converge and where they would, hence, expose themselves most often to a lurking predator (Gibb 1960; Perrins 1979). This would add to the value of the nest environment as a defended area and, hence, would accrue an additional advantage to defence near the hole, apart from any consideration of offspring protection. Response levels (latencies, distances) of the five experiments should therefore increase in the order
III < I < IV < II < V (see Table I, Results), i.e. in an order of decreasing risk, or effect on the predator (see above). There is some ambiguity in the ordering of experiments I and IV since it is uncertain whether the incremental 'Near hole' condition together with the decremental 'Start breeding' condition in experiment I would, on balance, enhance the response more, as seems likely, than the combination of the decremental 'Away from hole' plus incremental 'Breeding' conditions in experiment IV. We settled the ambiguity as stated prior to an analysis of the data in Table I. The predictions about the outcome of experiments I-V represent the transitive ordering of the cumulative effects of two contextual variables on harassment behaviour. The component inequalities in this ordering would all appear to permit strong inference tests, i.e. tests in which a difference in treatment conditions is expected to translate into a difference in response strength of the same sign.
RESULTS When looking at both sexes together, two latency variables showed that great tits approached danger and called significantly earlier during the breeding season ( = nestling phase) near their nest hole (Fig. 1, experiment III) than in trials away from the hole when nest building starts (experiment II), or during the non-breeding season (experiment V). The two distance variables yielded the most homogeneous results, although in most cases they ran counter to our predictions. Great tits remained significantly farther away from the source of danger when threatened near their (nest) hole (Fig. 1). Away from the hole, they took their shortest Median Distance in trials during nest building and, regarding Minimum Distance, they approached danger more closely during breeding than during the non-breeding season. The Latency of Attaining Minimum Distance from danger presented the fewest differences across experiments (Fig. 1). Away from their hole, great tits approached their Minimum Distance earlier during breeding (experiment IV) than while starting to build nests (experiment II). The predicted ordering of response strength of harassment across experiments is given in Table I (for the derivation see Predictions). To ease comparison, we have lumped each two of three latency measures (Approach, Calling) and the two distance
Zimmermann & Curio." Conflicting needs in mobbing Exp. I Exp II Exp. II[ 500 - Exp. IV Exp V "~ ~.00-
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I
Start Breeding, near hole Start Breeding, away from hole m Breeding, near hole ~ Breeding, away from hole F---] Non-breeding, away from hole Q
I
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11
Latency of Coiling
Median Distance
Latency of Attaining Minimum Distance
= i5
71
lS
Latency of Approach
0
Minimum Distance
Figure 1. Medians (columns) and non-parametric standard e r r o r s vertical bars inside columns, after Sachs 1978) for five behavioural parameters of the first or nearest great tit per trial. Five columns per behavioural variable represent different experimental conditions (see inset). The total number of trials ( = individuals) is given inside or below each column. Significant differences between experimental groups are indicated by solid lines; P-values are two-tailed (Mann-Whitney U-test), *P<0.05; **P<0.01; ***P<0.001.
Table I. Predictions on harassment behaviour measures and their observed outcome in five experiments (I-V) manipulating season and distance of danger from (nest) hole Results Predicted by 'move on' hypothesist II i
III
IV
V
>
<
<
>
>
<
<
<
<
II Ill
Iv For/against prediction
Two latency measures II (+)/+
III
IV
= -/+ (+) (+)/+ =/+
< Male Female Male + female
Latency of attaining minimum distance V
II
III
+/= -/(-) (+)/+ (+)/-
-/+
+ +/(+)
IV
Two distance measures V
(-)/- (-)/+/(+) - / ( - ) -/(+) -/+ +/-
I1
(-)
IlI
IV
(+) ( - ) (-) (-) (-)
6/2
4/6
2/8
6/2
6/4
1/8"
12/4
I0/10
V
(-) +/= (-) (-)/-
3/16"*
Predictions based on 'move on' hypothesis of predator harassment. Results reflect medians of measures (see Fig. 1). Symbols in cells of results: + consonance with prediction, - reverse of prediction, = the two variables concerned point in opposite directions; bracketed symbols denote statistical significance for at least one variable (P < 0.05, one-tailed). One symbol per cell ( + , - , = ) is used where male and female have been found to differ in the same direction, otherwise symbols correspond to male/female. Ratios o f cell totals/matrix for and against the move on hypothesis tested for significance by Dixon & Mood sign test (one-tailed), t Left-hand matrix reads: behaviour measure at start of row < or > behaviour measure at column head. * P < 0.025; **P < 0.005. Because testing of both single comparisons in ceils and o f comparisons across experiments is inferential P-values are one-tailed.
Animal Behaviour, 36, 3
930
measures because they correlate positively within individual trials (Regelmann & Curio 1983; Curio et al. 1985), such that there are three groups of response variables to be compared (Table I). The pairwise comparisons of experiments demonstrate that the two latency measures combined conform most closely to the predictions (in 12 of 16 cases, falling just short of significance), while the reverse holds for the two distance measures (in 16 of 19 cases, Po,o<0"005). The variable Latency of Attaining Minimum Distance holds an intermediate position in that the cases for and against the predictions balance each other (10: 10). In addition there seems to be a subtle difference between the two lumped-variables matrices in that harassment expressed by the two distance-fromdanger variables is more consistent in its direction; this is indicated by both the number of cells displaying significance and by the concordance between the sexes.
DISCUSSION Whereas two latency measures (Approach, Calling) combined largely conform to the move on hypothesis of harassment behaviour, the two distance measures (Minimum and Median Distance) argue against it (Table I). A fifth variable, Latency of Attaining Minimum Distance, does not permit one either to accept or to reject the basic hypothesis since response inequalities for and against it match. This intermediate position lends confidence to the discrepant results concerning the latency and distance measures; the Latency of Attaining Minimum Distance appears to combine ingredients of both the latency and distance variables. Thus, the results do not permit us clearly to reject or to accept the move on hypothesis of harassment. Since there is clear, multi-level evidence for this premise of the predictions being basically correct (Regelmann & Curio 1983, 1986) confounding variables, possibly reflecting a different need, must be looked for. Great tits probably try to minimize the danger of disclosing the presence of their young to the unseen 'phantom' predator by staying farther away from it than predicated by the need to move it on. Far away from the hole, the need to conceal the nest is clearly much smaller so that homing in on the predator gains priority. In some species of concealed nesters there is a rising gradient of the mobbing call repetition rate with
decreasing predator distance from the nest. One avian nest predator, the gymnogene, Polyboroides typus, increases its search efforts once the parent birds increase their mobbing behaviour (Thurow & Black 1981), and some predators appear to home in on the nest site along that gradient (see references in Curio 1976). Great tits increase their vocal mobbing rate as they approach an owl close to the nest with nestlings (Curio & Regelmann 1985). This gradient of calling may serve either of two goals, to add to threatening the interloper or to mitigate the risk to the caller that is inherent in its hom!ng in more closely (Curio & Regelmann 1985). At present, it seems difficult to tell apart this behaviour gradient from one focusing on the nest and thus potentially betraying its position. In other respects great tits seem to employ a compromise between trying to make the predator leave and not betraying the whereabouts of their brood or the centre of their own activities (see Latency of Attaining Minimum Distance in Table I). This interpretation is in line with experiments employing predators of different searching (cognitive) abilities. Great tits keep away from a live cat near their nest with young much farther than from a live owl under the same conditions (median Minimum Distance = 7"5 m (range 3-30 m) versus 1 m (range 0.1-7.5 m), Curio, unpublished data). The distance is in fact by far longer than necessitated by a cat's threat to the parents. Both findings together then would indicate the ability of some predators to infer from harassment the site of the brood at stake and, hence, a novel cost of predator harassment (see Curio & Regelmann 1985). To counter this cost, some concealed nesters appear to distract attention of the searching predator onto themselves by increasing the calling rate each time the predator is following the caller instead of approaching the nest (Knight & Temple 1986b). In the present case the unseen 'phantom' predator remains unclassified. Since only some of the natural predators threaten the brood and since their abilities to locate a nest surely vary, the defence behaviour of great tits must be regarded as conservative. For nest concealment it is less cautious than dictated by a live cat, yet it is much more cautious than if defence was the only priority. Once the nest is discovered, harassment increases (Knight & Temple 1986c). This suggests that harassment of a predator near the nest remains moderate as long as crypticity is maintained. Yet
Zimmermann & Curio: Conflicting needs in mobbing h a r a s s m e n t increases, as a last resort, once the threat has climaxed a n d active defence has gained priority. This interpretation still needs to be more fully examined.
ACKNOWLEDGMENTS We are extremely grateful to all w h o facilitated o u r field work: the AuBenstation fiir P o p u l a t i o n s 6 k o logic, Institut fiir Vogelforschung 'Vogelwarte Helgoland', especially D r R. Berndt, D r W. Winkel, H. Spr6tke, a n d the late O b e r f o r s t r a t G. Raschke improved o u r logistics a n d w o r k i n g facilities. M a n y students a n d guests helped with the experiments: A. Bars, H.-W. B6cking, U. Ernst, G. Ewan, D r E. F r a n k e n b e r g (Jerusalem), C. U b e r h o r s t , W. Vieth, E. Z i m m e r m a n n a n d I. Z i m m e r m a n n . A. Bassaris a n d I. Z i m m e r m a n n helped with the data processing. D r G. K l u m p a n d T. R a d e n b e r g provided us with i n f o r m a t i o n a n d m a p s a b o u t great tit pairs occupying territories in M a r c h 1983. Professor D r J. E. R. S t a d d o n kindly i m p r o v e d o u r English a n d pointed o u t a flaw in the Discussion. T h e zoo ' W i l h e l m a ' a n d D r W. Scherzinger each generously loaned us a p y g m y owl. The Deutsche F o r s c h u n g s g e m e i n s c h a f t f u n d e d p a r t o f the experiments (grants Cu 4/19, 20, 24 a n d 25/3).
REFERENCES Andersson, M., Wiklund, C. G. & Rundgren, H. 1980. Parental defence of offspring: a model and an example. Anita. Behav., 28, 536 542. Barash, D. P. 1980. Predictive sociobiology: mate selection in damselflshes and brood defense in whitecrowned sparrows. In: Soeiobiology: Beyond Nature/ Nurture? (Ed. by G. W. Barlow & J. Silverberg), pp. 209-226. Washington D.C.: American Association for the Advancement of Science. Bildstein, K. L. 1982. Responses of northern harriers to mobbing passerines. J. Field Ornithol., 53, 7-14. Cully, J. F. & Ligon J. D. 1976. Comparative mobbing behavior of Scrub and Mexican jays. Auk, 93, 116-125. Curio, E. 1963. Probleme des Feinderkennens bei Vrgeln. Proc. Xlllth lnt. Ornithol. Congr., 206-239. Curio, E. 1975. The functional organization of antipredator behaviour in the pied flycatcher: a study of avian visual perception. Anita. Behav., 23, I-115. Curio, E. 1976. The Ethology of Predation. Berlin: Springer. Curio, E. 1978. The adaptive significance of avian mobbing. I. Teleonomic hypotheses and predictions. Z. TierpsychoL, 48, 175-183. Curio, E. 1979. Fehlen eines optischen Verst/irkers verst/irkt eine Lautdressur von Kohlmeisen: Ein nichtklassifizierbares Risiko? Verh. dr. zool. Ges., 221.
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Curio, E. 1980. An unknown determinant of a sex-specific altruism. Z. Tierpsychol., 53, 139-152. Curio, E., Augst, H. J., Bfcking, H. W., Milinski, M. & Ohguchi, O. 1978. Wie Singv6gel auf Feindrufe hassen lernen. J. Ornithol., 119, 231-233. Curio, E. & Regelmann, K. 1985. The behavioural dynamics of great tits (Parus major) approaching a predator. Z. Tierpsychol., 69, 3-18. Curio, E., Regelmann, K. & Zimmermann, U. 1985. Brood defence in the great tit (Parus major): the influence of life-history and habitat. Behav. Ecol. Sociobiol., 16, 273-283. Drent, J. P. 1983. The functional ethology of territoriality in the great tit (Parus major L.). Ph.D. thesis, University of Groningen. Dyrcz, A., Witkowski, J. & Okulewicz, J. 198 I. Nesting of 'timid' waders in the vicinity of "bold' ones as an antipredator adaptation. Ibis, 123, 542-545. Gibb, J. A. 1960. Populations of tits and goldcrests and their food supply in pine plantations, lbis, 102, 163 208. Greig-Smith, P. W. 1980. Parental investment in nest defence by stonechats (Saxicola torquata). Anita. Behav., 28, 604-619. Hinde, R. A. 1952. The behaviour of the great tit (Parus major) and some other related species. Behav. SuppL, 2, 1 201. Horn, H. S. 1968. The adaptive significance of colonial nesting in the Brewer's blackbird Euphagus eyanocephalus. Ecology, 49, 682-694. Klump, G. & Shalter, M. D. 1984. Acoustic behaviour of birds and mammals in the predator context. I. Factors affecting the structure of alarm signals. II. The functional significance and evolution of alarm calls. Z. Tierpsychol., 66, 189-226. Knight, R. L. & Temple, S. A. 1986a. Nest defence in the American goldfinch. Anita. Behav., 34, 887-897. Knight, R. L. & Temple, S. A. 1986b. Methodological problems in studies of avian nest defence. AnOn. Behav., 34, 561-566. Knight, R. L. & Temple, S. A. 1986c. Why does intensity of avian nest defense increase during the nesting cycle? Auk, 103, 318-327. Mrckel, R. & Mrckel, W. 1984. Sperlingskauz, Glaucidium passerinum, pl/indert Kohlmeisenbrut in einem Holzbetonnistkasten. Beitr. Vogelk., 30, 29-32. Perrins, C. M. 1979. British Tits. London: Collins. Regelmann, K. & Curio, E. 1983. Determinants of brood defence in the great tit, Parus major L. Behav. Ecol. Sociobiol., 13, 131-145. Regelmann, K. & Curio, E. 1986. Why do great tit (Parus major) males defend their broods more than females do? Anita. Behav., 34, 1206-1214. Robertson, R. J. & Biermann, G. C. 1979. Parental investment strategies determined by expected benefits. Z. Tierpsyehol., 50, 124-128. Sachs, L. 1978. Angewandte Statistik. Berlin: Springer. Scherzinger, W. 1970. Zum Aktionssystem des Sperlingskauzes (Glaucidium passerinum L.). Zoologica, 118, 1120. Shalter, M. D. 1979. Responses of nesting passerines to alarm calls. Ibis, 121, 362-368. Shedd, D. H. 1982. Seasonal variation and function of
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mobbing and related antipredator behaviors of the American robin (Turdus migratorius). Auk, 99, 342346. Thielcke, G. 1970. Vogelstimmen. Berlin: Springer. Thurow, T. L. & Black, H. L. 1981. Ecology and behaviour of the gymnogene. Ostrich, 52, 25 35. Toenhardt, H. 1935. Beitriige zu dem Problem des "Hassens'" der SingvOgel auf die Eulen. Berlin: Triltsch &
Huther. Vogel, C. 1975. Okologie, Lebensweise und Sozialverhalten der Grauen Languren in verschiedenen Biotopen Indiens. Z. Tierpsychol. Suppl., 17, 1 160. Berlin: Paul Parey.
(Received 12 May 1987; revised 18 September 1987; MS. number: 3015)
Two conflicting needs affecting predator mobbing by great tits, Parus major UWE ZIMMERMANN & EBERHARD CURIO Arbeitsgruppe f~r Verhaltensforschung, Fakultiit fiir Biologie, Ruhr-Universitiit Bochum, D-4630 Bochum, West German),
Abstract. Predator mobbing by great tits, Parus major, was studied by manipulating two contextual
variables: the proximity of danger to the nest hole (close versus far), and breeding condition (non-breeding versus nest building versus care of nestlings). In five experiments pitting these contextual variables against each other, great tits were presented with a multi-species mobbing chorus signalling danger to which they responded by typical predator harassment. Based on the 'move on' hypothesis of harassment and on context manipulation, harassment levels specific for each of the five experiments could be predictably ordered; the ensuing rank order of scores reflected, by its nature, a series of four strong inference tests. Whereas two latency measures supported the move on hypothesis, two distance-from-danger measures suggested nest hole concealment to be an opposing need; a fifth measure of harassment, comprising both latency and distance, held an intermediate position, thus tying in with the compromise nature of harassment. Considering the 'phantom' nature of the unseen danger stimulus applied, the defence levels observed must be regarded as moderately conservative. There are natural danger stimuli (e.g. cats) that more effectively prevent great tits displaying predator harassment.
When harassing a predator animals run the risk of being injured or killed (reviewed in Curio & Regelmann 1985) and lose time and opportunities to engage in other activities (Curio 1978). What advantages do harassers gain in return? One answer could be the 'move on' hypothesis: a predator should leave an area the sooner, the more intensely and/or the longer it is molested (Curio 1963; Thielcke 1970; Vogel 1975; Cully & Ligon 1976; evidence: Bildstein 1982; Shedd 1982), and should be less likely to attack again (Curio 1978). The move on hypothesis should hold mainly for birds defending a localized resource, especially in the breeding season. Otherwise the prey bird might more easily move away from the site of an encounter. Many authors have emphasized that harassment may protect vulnerable offspring from predators (Toenhardt 1935; Robertson & Biermann 1979; Shalter 1979; Andersson et al. 1980; Barash 1980; Curio 1980; Shedd 1982) although the main avian predators of European hole-nesting birds, the sparrowhawk, Accipiter nisus, and the pygmy owl, Glaucidium passerinum, pose a threat primarily to the parents. Yet offspring would starve to death if a parent were killed by the raptor. Moreover, the pygmy owl is known to pull out young from nest holes on occasion (Scherzinger 1970; Mrckel & Mrckel 1984), while stoats, Mus926
tela erminea, pose a common threat to nestlings and brooding females alike (Perrins 1979). Furthermore, by mobbing intensely parents might disclose their nests to a searching predator (Thurow & Black 1981). There is a lot of indirect evidence that protection of the young is the major determinant of the strength of parental mobbing behaviour. When threatened, great tits and blue tits, Parus caeruleus, mob vocally only at their own nest but silently at their neighbour's nest (Curio 1980; see also Shalter 1979). Similarly, some birds engage in predator harassment only when owning a nest (Horn 1968). Furthermore, in several species the intensity of parental mobbing increases with the age of the young (Curio 1975; Andersson et al. 1980; GreigSmith 1980; Regelmann & Curio 1983), or, with the progression from non-breeding to breeding conditions (Shedd 1982). The critique by Knight & Temple (1986a) who suggested that the age-related increase is due to habituation of fear from the predator stimulus does not apply in the many cases where parents have been tested only once. Great tits stay in and defend their territories more or less during the whole year and leave it only when food is becoming scarce during winter (Drent 1983). Accordingly, great tits mob at a source of danger the whole year round (Hinde 1952; Zim-
Zimmermann & Curio: Conflicting needs in mobbing mermann, unpublished data). In the present study we set out to examine to what extent predator harassment by great tits is influenced, first, by the effect of season and, second, by the proximity of a potential predator to their nest sites. By pitting these contextual variables against each other, we wanted to find out whether great tits solely strive at moving on the predator, with no other need compromising the defence.
M E T H O D S AND S T U D Y AREAS Great tits were lured and induced to mob at a playback of a mixed mobbing tape-recording from a Uher Stereo Report 4200 at 19 cm/s. Similarly, other songbirds were lured inadvertently. The sound stimulus consisted of 2 min of mixed species mobbing chorus (including great tit 'churring'), 1 min of mixed mobbing paired with an artificial 800 Hz sine tone (patterned after the song of the pygmy owl, which did not occur in the study areas), 2 min of the pure sine sound alone and 3 min of mixed mobbing again. (For a more detailed description, technical details and the irrelevance of other species see Regelmann & Curio 1983; for the rationale see Curio et al. 1978.) All individuals were tested only once. The ensuing behaviour was recorded by one of one to three observers from a distance of 15-30 m from the loudspeaker (for details see Regelmann & Curio 1983). The behaviour provoked did not differ qualitatively from that elicited by a live pygmy owl, although in the former case the tits were more cautious (Curio 1979). Five experiments were carried out. Experiment I was conducted at the start of the breeding season (March) during incipient nest building, prior to egg laying. The loudspeaker was positioned 3 m from the nest box and 1 m above ground. Experiment II was conducted at the same time (March) as experiment I, with the speaker positioned at least 20 m away from the nest box. Experiment III was conducted during the breeding season (26 May through 9 June) when great tit pairs were feeding first broods, with the speaker positioned as in experiment I, thus constituting the most immediate threat to the brood. Experiment IV was conducted during the nestling stage (23 April through 26 May, when some broods were still to hatch) at locations selected at
927
random, i.e. without prior knowledge of great tit nest sites, but at least 20 m away from potential great tit nest boxes. Experiment V was conducted during the whole year with the exception of the periods in experiments I-IV without knowledge of great tit territories and at least 20 m from possible roosting holes, thus constituting the least threat to the tits. Experiments of type III with great tit pairs feeding first brood nestlings were performed in Lower Saxony near Wolfsburg in study plots of the AuBenstation ffir Populations/Skologie of the 'Vogelwarte Helgoland' in 1977, 1978 and 1980 (for a description see Regelmann & Curio 1983). The other experiments (I, II, IV, V) were conducted in forest and park areas of the Ruhrgebiet in 1979, 1980 and/or 1983. Both the homogeneity of data from different years and the homogeneity of monthly data pooled from trials in the nonbreeding season were tested with a Kruskal-Wallis H-test. For three out of five parameters the trials of two non-breeding season months had to be excluded in order to maintain homogeneity (details of monthly variation in Zimmermann, unpublished data). The following variables which have been described in detail previously (Regelmann & Curio 1983) were compared across different experimental groups. (1) Latency of Approach is the time from the onset of the playback to when a great tit was first seen approaching the speaker. A short latency tends to reflect a greater risk since the number of mobbers joining the party and thus sharing the (apparent) risk always increases as the trial goes on (Wolf, personal communication). (2) Latency of Calling is the time from the start of the tape until the first mobbing call of a great tit. (3) Latency of Attaining Minimum Distance is measured from the onset of the playback until a great tit approached the speaker the closest, compared to all of its other vantage points. (4) Median Distance is the median of at least five distance values from all great tits recorded during a trial. (5) Minimum Distance (MD) should reflect best the risk taken (Regelmann & Curio 1983). These behavioural variables were scored only for the first or the nearest great tit independent of its sex and for males and females separately. If more than one great tit of one sex appeared, the scores of the earliest or the nearest bird were processed and the data were pooled for that sex. During the
928
Animal Behaviour, 36, 3
breeding season, only one or two great tits usually came to the experimental site (for example in experiment IV in 80% of 35 trials). Overall, however, great tits other than the territorial bird(s) also tended to approach the speaker though more cautiously. In the non-breeding season (experiment V), when flocks of great tits responded to the stimulus, a male and a female approaching most closely were scored as pair mates. By invariably selecting the strongest responses we attempted to process territory owners only.
PREDICTIONS Evidence is accumulating that harassment serves to move on the predator (Dyrcz et al. 1981; Bildstein 1982; Shedd 1982; Klump & Shalter 1984) and thus deny sustenance to it in the harasser's home range. It is reasonable to assume that the more closely the harasser homes in on the predator and the longer it does so the more effective will be any move on effect (Curio & Regelmann 1985). Accordingly shorter latencies and shorter distances up to which mobbers approach the interloper will be more effective, all other things being equal. In fact latencies, distance measures and the inverse of the call repetition rate all covary, thus underpinning the premise of the move on hypothesis (Regelmann & Curio 1983). Given that the brood is a major beneficiary of predator harassment (Regelmann & Curio 1983, 1986; see also Discussion), and given that nestlings are worth more to the parents than a newly started nest or an empty hole, the following predictions appear reasonable. Among the stages tested, harassment should decline in the order Breeding (nestling stage), Start of Breeding (nest building), Non-breeding. Among the stimulus sites tested, harassment should also decline in the order Near (nest) hole, Away from (nest) hole. Incidentally, the parents would benefit too by increasing their harassment when threatened at their nest site where their travel routes converge and where they would, hence, expose themselves most often to a lurking predator (Gibb 1960; Perrins 1979). This would add to the value of the nest environment as a defended area and, hence, would accrue an additional advantage to defence near the hole, apart from any consideration of offspring protection. Response levels (latencies, distances) of the five experiments should therefore increase in the order
III < I < IV < II < V (see Table I, Results), i.e. in an order of decreasing risk, or effect on the predator (see above). There is some ambiguity in the ordering of experiments I and IV since it is uncertain whether the incremental 'Near hole' condition together with the decremental 'Start breeding' condition in experiment I would, on balance, enhance the response more, as seems likely, than the combination of the decremental 'Away from hole' plus incremental 'Breeding' conditions in experiment IV. We settled the ambiguity as stated prior to an analysis of the data in Table I. The predictions about the outcome of experiments I-V represent the transitive ordering of the cumulative effects of two contextual variables on harassment behaviour. The component inequalities in this ordering would all appear to permit strong inference tests, i.e. tests in which a difference in treatment conditions is expected to translate into a difference in response strength of the same sign.
RESULTS When looking at both sexes together, two latency variables showed that great tits approached danger and called significantly earlier during the breeding season ( = nestling phase) near their nest hole (Fig. 1, experiment III) than in trials away from the hole when nest building starts (experiment II), or during the non-breeding season (experiment V). The two distance variables yielded the most homogeneous results, although in most cases they ran counter to our predictions. Great tits remained significantly farther away from the source of danger when threatened near their (nest) hole (Fig. 1). Away from the hole, they took their shortest Median Distance in trials during nest building and, regarding Minimum Distance, they approached danger more closely during breeding than during the non-breeding season. The Latency of Attaining Minimum Distance from danger presented the fewest differences across experiments (Fig. 1). Away from their hole, great tits approached their Minimum Distance earlier during breeding (experiment IV) than while starting to build nests (experiment II). The predicted ordering of response strength of harassment across experiments is given in Table I (for the derivation see Predictions). To ease comparison, we have lumped each two of three latency measures (Approach, Calling) and the two distance
Zimmermann & Curio." Conflicting needs in mobbing Exp. I Exp II Exp. II[ 500 - Exp. IV Exp V "~ ~.00-
929
I
Start Breeding, near hole Start Breeding, away from hole m Breeding, near hole ~ Breeding, away from hole F---] Non-breeding, away from hole Q
I
~
/ 6o0
t,O0
3o0
~t
•,
'~j c
300"
ww
Q
..
F''"]
~-2oo g
200"
lo0 g
100L
O.
11
Latency of Coiling
Median Distance
Latency of Attaining Minimum Distance
= i5
71
lS
Latency of Approach
0
Minimum Distance
Figure 1. Medians (columns) and non-parametric standard e r r o r s vertical bars inside columns, after Sachs 1978) for five behavioural parameters of the first or nearest great tit per trial. Five columns per behavioural variable represent different experimental conditions (see inset). The total number of trials ( = individuals) is given inside or below each column. Significant differences between experimental groups are indicated by solid lines; P-values are two-tailed (Mann-Whitney U-test), *P<0.05; **P<0.01; ***P<0.001.
Table I. Predictions on harassment behaviour measures and their observed outcome in five experiments (I-V) manipulating season and distance of danger from (nest) hole Results Predicted by 'move on' hypothesist II i
III
IV
V
>
<
<
>
>
<
<
<
<
II Ill
Iv For/against prediction
Two latency measures II (+)/+
III
IV
= -/+ (+) (+)/+ =/+
< Male Female Male + female
Latency of attaining minimum distance V
II
III
+/= -/(-) (+)/+ (+)/-
-/+
+ +/(+)
IV
Two distance measures V
(-)/- (-)/+/(+) - / ( - ) -/(+) -/+ +/-
I1
(-)
IlI
IV
(+) ( - ) (-) (-) (-)
6/2
4/6
2/8
6/2
6/4
1/8"
12/4
I0/10
V
(-) +/= (-) (-)/-
3/16"*
Predictions based on 'move on' hypothesis of predator harassment. Results reflect medians of measures (see Fig. 1). Symbols in cells of results: + consonance with prediction, - reverse of prediction, = the two variables concerned point in opposite directions; bracketed symbols denote statistical significance for at least one variable (P < 0.05, one-tailed). One symbol per cell ( + , - , = ) is used where male and female have been found to differ in the same direction, otherwise symbols correspond to male/female. Ratios o f cell totals/matrix for and against the move on hypothesis tested for significance by Dixon & Mood sign test (one-tailed), t Left-hand matrix reads: behaviour measure at start of row < or > behaviour measure at column head. * P < 0.025; **P < 0.005. Because testing of both single comparisons in ceils and o f comparisons across experiments is inferential P-values are one-tailed.
Animal Behaviour, 36, 3
930
measures because they correlate positively within individual trials (Regelmann & Curio 1983; Curio et al. 1985), such that there are three groups of response variables to be compared (Table I). The pairwise comparisons of experiments demonstrate that the two latency measures combined conform most closely to the predictions (in 12 of 16 cases, falling just short of significance), while the reverse holds for the two distance measures (in 16 of 19 cases, Po,o<0"005). The variable Latency of Attaining Minimum Distance holds an intermediate position in that the cases for and against the predictions balance each other (10: 10). In addition there seems to be a subtle difference between the two lumped-variables matrices in that harassment expressed by the two distance-fromdanger variables is more consistent in its direction; this is indicated by both the number of cells displaying significance and by the concordance between the sexes.
DISCUSSION Whereas two latency measures (Approach, Calling) combined largely conform to the move on hypothesis of harassment behaviour, the two distance measures (Minimum and Median Distance) argue against it (Table I). A fifth variable, Latency of Attaining Minimum Distance, does not permit one either to accept or to reject the basic hypothesis since response inequalities for and against it match. This intermediate position lends confidence to the discrepant results concerning the latency and distance measures; the Latency of Attaining Minimum Distance appears to combine ingredients of both the latency and distance variables. Thus, the results do not permit us clearly to reject or to accept the move on hypothesis of harassment. Since there is clear, multi-level evidence for this premise of the predictions being basically correct (Regelmann & Curio 1983, 1986) confounding variables, possibly reflecting a different need, must be looked for. Great tits probably try to minimize the danger of disclosing the presence of their young to the unseen 'phantom' predator by staying farther away from it than predicated by the need to move it on. Far away from the hole, the need to conceal the nest is clearly much smaller so that homing in on the predator gains priority. In some species of concealed nesters there is a rising gradient of the mobbing call repetition rate with
decreasing predator distance from the nest. One avian nest predator, the gymnogene, Polyboroides typus, increases its search efforts once the parent birds increase their mobbing behaviour (Thurow & Black 1981), and some predators appear to home in on the nest site along that gradient (see references in Curio 1976). Great tits increase their vocal mobbing rate as they approach an owl close to the nest with nestlings (Curio & Regelmann 1985). This gradient of calling may serve either of two goals, to add to threatening the interloper or to mitigate the risk to the caller that is inherent in its hom!ng in more closely (Curio & Regelmann 1985). At present, it seems difficult to tell apart this behaviour gradient from one focusing on the nest and thus potentially betraying its position. In other respects great tits seem to employ a compromise between trying to make the predator leave and not betraying the whereabouts of their brood or the centre of their own activities (see Latency of Attaining Minimum Distance in Table I). This interpretation is in line with experiments employing predators of different searching (cognitive) abilities. Great tits keep away from a live cat near their nest with young much farther than from a live owl under the same conditions (median Minimum Distance = 7"5 m (range 3-30 m) versus 1 m (range 0.1-7.5 m), Curio, unpublished data). The distance is in fact by far longer than necessitated by a cat's threat to the parents. Both findings together then would indicate the ability of some predators to infer from harassment the site of the brood at stake and, hence, a novel cost of predator harassment (see Curio & Regelmann 1985). To counter this cost, some concealed nesters appear to distract attention of the searching predator onto themselves by increasing the calling rate each time the predator is following the caller instead of approaching the nest (Knight & Temple 1986b). In the present case the unseen 'phantom' predator remains unclassified. Since only some of the natural predators threaten the brood and since their abilities to locate a nest surely vary, the defence behaviour of great tits must be regarded as conservative. For nest concealment it is less cautious than dictated by a live cat, yet it is much more cautious than if defence was the only priority. Once the nest is discovered, harassment increases (Knight & Temple 1986c). This suggests that harassment of a predator near the nest remains moderate as long as crypticity is maintained. Yet
Zimmermann & Curio: Conflicting needs in mobbing h a r a s s m e n t increases, as a last resort, once the threat has climaxed a n d active defence has gained priority. This interpretation still needs to be more fully examined.
ACKNOWLEDGMENTS We are extremely grateful to all w h o facilitated o u r field work: the AuBenstation fiir P o p u l a t i o n s 6 k o logic, Institut fiir Vogelforschung 'Vogelwarte Helgoland', especially D r R. Berndt, D r W. Winkel, H. Spr6tke, a n d the late O b e r f o r s t r a t G. Raschke improved o u r logistics a n d w o r k i n g facilities. M a n y students a n d guests helped with the experiments: A. Bars, H.-W. B6cking, U. Ernst, G. Ewan, D r E. F r a n k e n b e r g (Jerusalem), C. U b e r h o r s t , W. Vieth, E. Z i m m e r m a n n a n d I. Z i m m e r m a n n . A. Bassaris a n d I. Z i m m e r m a n n helped with the data processing. D r G. K l u m p a n d T. R a d e n b e r g provided us with i n f o r m a t i o n a n d m a p s a b o u t great tit pairs occupying territories in M a r c h 1983. Professor D r J. E. R. S t a d d o n kindly i m p r o v e d o u r English a n d pointed o u t a flaw in the Discussion. T h e zoo ' W i l h e l m a ' a n d D r W. Scherzinger each generously loaned us a p y g m y owl. The Deutsche F o r s c h u n g s g e m e i n s c h a f t f u n d e d p a r t o f the experiments (grants Cu 4/19, 20, 24 a n d 25/3).
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Curio, E. 1980. An unknown determinant of a sex-specific altruism. Z. Tierpsychol., 53, 139-152. Curio, E., Augst, H. J., Bfcking, H. W., Milinski, M. & Ohguchi, O. 1978. Wie Singv6gel auf Feindrufe hassen lernen. J. Ornithol., 119, 231-233. Curio, E. & Regelmann, K. 1985. The behavioural dynamics of great tits (Parus major) approaching a predator. Z. Tierpsychol., 69, 3-18. Curio, E., Regelmann, K. & Zimmermann, U. 1985. Brood defence in the great tit (Parus major): the influence of life-history and habitat. Behav. Ecol. Sociobiol., 16, 273-283. Drent, J. P. 1983. The functional ethology of territoriality in the great tit (Parus major L.). Ph.D. thesis, University of Groningen. Dyrcz, A., Witkowski, J. & Okulewicz, J. 198 I. Nesting of 'timid' waders in the vicinity of "bold' ones as an antipredator adaptation. Ibis, 123, 542-545. Gibb, J. A. 1960. Populations of tits and goldcrests and their food supply in pine plantations, lbis, 102, 163 208. Greig-Smith, P. W. 1980. Parental investment in nest defence by stonechats (Saxicola torquata). Anita. Behav., 28, 604-619. Hinde, R. A. 1952. The behaviour of the great tit (Parus major) and some other related species. Behav. SuppL, 2, 1 201. Horn, H. S. 1968. The adaptive significance of colonial nesting in the Brewer's blackbird Euphagus eyanocephalus. Ecology, 49, 682-694. Klump, G. & Shalter, M. D. 1984. Acoustic behaviour of birds and mammals in the predator context. I. Factors affecting the structure of alarm signals. II. The functional significance and evolution of alarm calls. Z. Tierpsychol., 66, 189-226. Knight, R. L. & Temple, S. A. 1986a. Nest defence in the American goldfinch. Anita. Behav., 34, 887-897. Knight, R. L. & Temple, S. A. 1986b. Methodological problems in studies of avian nest defence. AnOn. Behav., 34, 561-566. Knight, R. L. & Temple, S. A. 1986c. Why does intensity of avian nest defense increase during the nesting cycle? Auk, 103, 318-327. Mrckel, R. & Mrckel, W. 1984. Sperlingskauz, Glaucidium passerinum, pl/indert Kohlmeisenbrut in einem Holzbetonnistkasten. Beitr. Vogelk., 30, 29-32. Perrins, C. M. 1979. British Tits. London: Collins. Regelmann, K. & Curio, E. 1983. Determinants of brood defence in the great tit, Parus major L. Behav. Ecol. Sociobiol., 13, 131-145. Regelmann, K. & Curio, E. 1986. Why do great tit (Parus major) males defend their broods more than females do? Anita. Behav., 34, 1206-1214. Robertson, R. J. & Biermann, G. C. 1979. Parental investment strategies determined by expected benefits. Z. Tierpsyehol., 50, 124-128. Sachs, L. 1978. Angewandte Statistik. Berlin: Springer. Scherzinger, W. 1970. Zum Aktionssystem des Sperlingskauzes (Glaucidium passerinum L.). Zoologica, 118, 1120. Shalter, M. D. 1979. Responses of nesting passerines to alarm calls. Ibis, 121, 362-368. Shedd, D. H. 1982. Seasonal variation and function of
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(Received 12 May 1987; revised 18 September 1987; MS. number: 3015)