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Simulated courtship interactions elicit neighbour intrusions in the whitethroat, Sylvia communis
ANIMAL BEHAVIOUR, 2005, 69, 161–168 doi:10.1016/j.anbehav.2004.01.021
Simulated courtship interactions elicit neighbour intrusions in the whitethroat, Sylvia communis THORSTEN J. S. BA LSBY & TOR BEN DABELSTEEN
Department of Animal Behaviour, Zoological Institute, University of Copenhagen (Received 11 October 2001; initial acceptance 28 November 2001; final acceptance 22 January 2004; published online 11 November 2004; MS. number: 7092R)
Animals often signal in communication network environments that include nonintended receivers that may constitute a risk to the signalling animals. Unpaired male songbirds, which sometimes intrude into neighbouring territories and interrupt courtship, may be an example of nonintended receivers of vocal courtship signals. We investigated this in the whitethroat, using dyads of unmated territorial males. Each dyad consisted of a resident male, who was part of the experimental treatment, and a neighbouring male, whose responses to the treatment stimuli were tested. Each dyad received two playback treatments: a courtship treatment in which the treatment male was induced to court a remotely controlled calling and jumping stuffed female, and a song duel treatment in which playbacks of male song were used to induce the focal male to countersing. The neighbours responded with more song flights to the courtship treatment than to the song duel treatment, perhaps to achieve an overview of the courtship activity or attract the female. Only the courtship treatment resulted in neighbouring intrusions and immediate chasing of the intruder by the treatment male. The males that suffered intrusions did not sing less than those that did not suffer intrusions. Reduced singing therefore may not be able to explain the intrusions. Every intrusion except one occurred after the first courtship vocalization, making it likely that the courtship per se caused the intrusions. This emphasizes the necessity of restricting the transmission range of courtship vocalizations in a network and therefore also explains why the courtship vocalizations of whitethroat males are relatively short ranging. Ó 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Vocalizations are usually propagated in a communication network environment where several individuals may be potential receivers of the signals (e.g. Dabelsteen 1992; McGregor 1993; McGregor & Dabelsteen 1996). The presence of both intended and nonintended receivers may have acted as a strong selection force in the evolution of the vocalizations, since either restricting or increasing the transmission capability of the vocalizations might have been adaptive in different contexts (e.g. McGregor & Dabelsteen 1996; Dabelsteen et al. 1998). Several species use quiet vocalizations during courtship and in aggressive intrasexual interactions, for example the Eurasian blackbird, Turdus merula (Dabelsteen 1988; Dabelsteen & Pedersen 1990), the common yellowthroat, Geothlypis trichas (Ritchison 1995) and the dark-eyed junco, Junco hyemalis (Titus 1998); see also the review by Correspondence and present address: T. J. S. Balsby, The Macaulay Library, Cornell Laboratory of Ornithology, 159 Sapsucker Woods Road, Ithaca, NY 14850, U.S.A. (email: [email protected]). T. Dabelsteen is at the Department of Animal Behaviour, Zoological Institute, University of Copenhagen, Tagensvej 16, DK-2200 Copenhagen N, Denmark. 0003–3472/04/$30.00/0
Dabelsteen et al. (1998). The use of quiet vocalizations may be an attempt to restrict information transfer to counter disadvantageous information gathering or eavesdropping by nonintended receivers in the network (Dabelsteen et al. 1998). Eavesdropping (McGregor & Dabelsteen 1996) is different from ordinary information gathering in that information is extracted from an interaction between other individuals and therefore may be relative about the interactants. Such relative information cannot be obtained by listening to the signals of the interactants separately. Neighbouring males may use information from courtship to the unambiguous disadvantage of the courting male. In territorial species such as European robins, Erithacus rubecula (Lack 1940), Eurasian blackbirds (Snow 1958) and dunnocks, Prunella modularis (Davies 1992) intruding males disrupt courtship or copulation attempts. In lekking species where information transfer cannot be restricted because of the high density of small territories, disruption of courtship and copulation ¨ glund & is well known (e.g. Foster 1983; Trail 1985; Ho Alatalo 1995; Alatalo et al. 1996). In a number of other species, both territorial and nonterritorial, females may call loudly in the context of courtship, that is, use calls
161 Ó 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
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with a long transmission range relative to the distance to other males (Montgomerie & Thornhill 1990). These calls may be used by females to attract males from the surroundings and thereby induce competition between males (Montgomerie & Thornhill 1990; Pizzari 2001). This could give females an opportunity to compare males through male–male competition or alternatively only the winner of the male–male competition may have access to the females (Wiley & Poston 1996). Female presence on a male’s territory could also be revealed by the behaviour of the male, which may use special displays or intensify the display of sexually selected traits, for instance in the lesser bird of paradise, Paradisaea minor (Beehler 1983), red-winged blackbird, Agelaius phoeniceus (Searcy & Yasukawa 1990), European starling, Sturnus vulgaris (Eens et al. 1993) and whitethroat (Balsby & Dabelsteen 2003a). Both male and female birds are able to eavesdrop on male–male vocal interactions in neighbouring territories (McGregor et al. 1997; Naguib & Todt 1997; Naguib et al. 1999; Otter et al. 1999; Peake et al. 2001, 2002; Mennill et al. 2002). Furthermore, Tobias & Seddon (2002) have shown that neighbouring male robins can gather information from loud female begging calls, which are given especially during the fertile period, and although they are directed at the mate, the neighbouring males will approach the female in response to these calls. Responses of neighbouring males to male–female interactions, that is, courtship interactions, have not yet been investigated although such interactions may have a strong effect. For instance, Lack (1939) mentioned that male black grouse, Tetrao tetrix, would intensify their display rate if a female is being courted inside the neighbouring territory. We investigated the responses of whitethroat males to information gathered from neighbouring territories. We allowed the males to gather information or eavesdrop on courtship and song duels taking place on neighbouring territories. Whitethroat males sing from a perched position (perch song) as well as during song flights (flight song; Balsby & Dabelsteen 2003a). Males typically use perch songs in vocal interactions with other males. Most male–male vocal interactions take place across territory borders, but they sometimes occur inside a territory (personal observation). Courtship usually takes place inside a territory. The unmated females visit several territories of unmated males before choosing a male (personal observation). Male courtship of visiting females is characterized by a special type of display, the diving song display, in which the male dives towards the female while singing a characteristic quiet diving song (Balsby 2000; Balsby & Dabelsteen 2003a). Diving song displays are often given in sequences of several displays. After a sequence of diving song displays, males often give sequences of woid-calls (Bergmann & Helb 1982) and sometimes a song flight before returning to normal singing behaviour, which mainly consists of perch songs at the territory border (Balsby & Dabelsteen 2003a). The behaviour of the female influences the courtship behaviour of the male in different ways. Female dscharp-calls (Bergmann & Helb 1982) can initiate the diving song display, and during courtship females may
respond to this display with short horizontal jumps and quiet ze-calls (Balsby & Dabelsteen 2002). The jumps increase the number of diving songs, whereas the ze-calls may elicit copulation attempts (Balsby & Dabelsteen 2002). Besides the diving song display, which occurs only in the presence of a female, males may also give woid-calls in association with the courtship (Balsby & Dabelsteen 2003a). These woid-calls may be directed towards potential male intruders and are capable of delaying intrusions (Balsby & Dabelsteen 2003b). We compared neighbouring whitethroat males’ responses to two treatments, which were both set up inside the territory of the treatment males: a courtship treatment and a song duel treatment. The courtship treatment allowed the neighbouring males to perceive the vocal signals of a courtship interaction between the treatment male and a simulated female, whereas the song duel treatment allowed the neighbouring males to perceive a song duel between the treatment male and a simulated male. We quantified the singing behaviour of the neighbouring males as well as whether they intruded on to the territories of the treatment males where the treatments were presented. Observations of unmated males showed that most intrusions occur when females are visiting the territory (Balsby & Dabelsteen 2003a). We therefore predicted that neighbouring males would intrude on the territory more often in response to the courtship treatment than to the song duel treatment. METHODS
Test Subjects and Equipment We carried out the experiment at Mols Bjerge, Denmark (56 140 N, 10 350 E), between 16 May and 4 July 2000 and between 13 May and 19 June 2002. All trials were initiated between 0700 and 1300 hours using 23 dyads of neighbouring unmated males of which only 16 dyads (11 in 2000 and five in 2002) of males were successful (see below). We used only unmated males because mated males are much less responsive to both male (Balsby 2000) and female stimuli (personal observation). The unmated males could easily be distinguished from mated males on the basis of their very high song activity (Balsby 2000). In each dyad, one of the males, the treatment male, was part of the treatment, whereas the other male was the neighbouring test subject. Each neighbouring test subject was presented with two treatments, a courtship treatment in which the treatment male was stimulated to court a remotely controlled calling and jumping stuffed female, and a song duel treatment in which the treatment male was stimulated to countersing to a small loudspeaker playing perch songs. The vocalizations used for stimulating the treatment males were all recorded in the experimental area in 1998 with a Sennheiser MKH816T and a SONY TCD10-PRO DAT recorder. All vocalizations were digitized in Avisoft (Avisoft-SASLab, Berlin, Germany). The subsequent sound processing was done in SIGPRO (Pedersen 1998). The digitized vocalizations were filtered and then standardized to the same peak amplitude value.
BALSBY & DABELSTEEN: COURTSHIP INTERACTIONS IN THE WHITETHROAT
The playback part of the song duel treatment was played from the SONY TCD10-PRO DAT in 2000 and from a portable computer by means of Avisoft in 2002, whereas the vocalizations used in the courtship treatment were played from a portable computer (Toshiba Satellite 300 CDS) connected to a Digital Sound Emitter (Dabelsteen 1992). For both treatments, the vocalizations were then amplified by a 35-W Dennon DCA power amplifier and played back through a small speaker (VIFA 1 Neodymium tweeter; Larsen & Dabelsteen 1997). The sound pressure level for the three types of vocalization were adjusted to ¨ el & Kjær Sound Pressure the natural levels using a Bru Level meter type 2236, fast setting. The natural levels were 63 dB (A) at 10 m for perch song (Balsby & Dabelsteen 2001), 46 dB (A) at 12 m for dscharp-calls and 36 dB (A) at 2.7 m for ze-calls (Balsby & Dabelsteen 2002). Whitethroat territory size varies between 0.06 and 1.0 ha (Sell & Odderskær 1990; Halupka et al. 2002), which equals a territory diameter of about 50 to about 155 m. Estimates of the discrimination distances suggest that diving songs, woid-calls and dscharp-calls transmit into neighbouring territories and that perch and flight songs transmit across neighbouring territories (Balsby et al. 2003), whereas zecalls from the centre of the territory would not transmit into the neighbouring territory.
The Song Duel Treatment The songs used to elicit the song duel with the treatment males originated from three different males. We used their songs to construct three playback stimuli each containing song from only one of the males. The three playback stimuli were used in approximately the same number of trials (N Z 4, 6, 6 trials). Each playback stimulus contained a loop of 55–61 perch songs, which was repeated twice. A song duel treatment trial involved playing one of the three stimuli towards a treatment male for 7–9 min. The songs were played from a speaker placed 1–2 m above ground level, and the behaviour of the treatment male and the neighbouring male was quantified for the first 7 min of playback during which the treatment male sang back towards the speaker.
The Courtship Treatment The courtship treatment was more complex than the song duel treatment, since both visual and acoustic female stimuli were necessary to elicit the courtship display of the treatment male. The visual part of the female stimulus consisted of a stuffed female whitethroat mounted on a remotely controlled device. This device allowed the female dummy to simulate the short horizontal jumps that natural females give in response to the dives of the males’ courtship display (Balsby & Dabelsteen 2002). The acoustic part of the female stimulus was played back interactively through a speaker placed on the ground below the stuffed female. It consisted of dscharp- and ze-calls (Balsby & Dabelsteen 2002). Seven sequences of ze-calls originating from two different females were used, but only one of the sequences was played back in a trial
(each of the ze-call sequences were used in one, two or three trials). Five dscharp-calls from two females were played back in pairs with an average rate of three pairs of calls per 2 min, and we used only two calls from one female in each trial, which gave four pairs of calls (each pair of calls was used in four, four and five trials). Two dummy females were each used in eight trials. The set-up, the interactive control of the female and the visual and acoustic stimuli are described in detail in Balsby & Dabelsteen (2002). All courtship treatment trials started with playback of dscharp-calls to initiate diving song displays of the treatment male. Dscharp-calls were also played back in the pauses between the diving song displays to stimulate the treatment males to resume the display. The jumps were given in response to the diving song display immediately after the male had passed the female dummy in a dive. The ze-calls were played during the silent intervals between the diving songs of a sequence of diving song displays and when the male perched within 2 m of the dummy. The stimulation of the treatment male was interactive and hence driven by the treatment male. The resulting courtship treatment therefore varied quantitatively between the trials, but not in quality because all neighbouring males received a complete set of male and female courtship vocalizations. We always attempted to stimulate the courtship of the treatment male maximally with dscharp-calls, jumps and ze-calls in the appropriate contexts. The treatment males did not respond with diving song immediately after the start of the female dscharp-calls. The average latency to diving song G SE was 416 G 104 s (range 12–1271 s). We defined the start of a courtship treatment as the time when the first diving song was given. The neighbouring male’s response to the courtship treatment was quantified from the first diving songs of the treatment male and 7 min onwards for comparison with the song duel treatment. However, we continued the courtship treatment upto 9 min (range 2–21 min) after the 7 min to investigate whether neighbouring males that did not intrude during the first 7 min did so later on.
Procedure and Behavioural Measurements During the experiment, the observers were sitting on the ground approximately 20 m from the set-up. The position of the observers was always chosen so that both the test and the treatment males could approach the setup directly without getting closer than 20 m to them. The treatment males were present and singing while we set up the equipment in their territories before the first treatment. The neighbouring males were also present in their territories and all but one were singing while we set up the equipment. All of the equipment for both treatments was put in position before the first treatment, except for the stuffed female, which was mounted just before the courtship treatment. We started the stimulation of the treatment male as soon as possible after positioning the equipment, when the treatment males were within hearing range of the playback. Approximately 30 min passed between the presentations of the two treatments
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to a test subject. The treatment males and the neighbouring males were similarly present and singing in their respective territories at the start of the second treatment. Seven trials were abandoned because either the neighbouring male did not respond by singing during the treatment or during the postplayback period to either the song duel treatment or the courtship treatment, or natural females entered the territory during the trial. We presented the courtship treatment first in 10 trials and the song duel treatment first in six trials. The slightly skewed proportion was due to several experiments failing during the start of the season when the song duel treatment was played first and attracted unmated females from outside the territory. The playback speaker was located at the same place in the territory of the treatment male during both treatments, that is, approximately halfway between the centre of the territory and the territory border towards the neighbouring male. In neither of the treatments were the neighbouring males likely to have seen the equipment involved in the stimulation of the treatment male, because it was hidden in the vegetation and because the distances between the neighbouring male and the experimental set-up were relatively large, at least initially. The initial decisions of the neighbouring males therefore must have relied solely on their reception of vocal cues from the interactions in the territories of the treatment males. We recorded the vocal behaviour of the neighbouring males and the treatment males with one or two directional microphones (Sennheiser MKH 70 P48 and MKH816T) on a Sony TCD10-pro DAT recorder for the female treatment and a Sony TCM5000 EMV cassette recorder in 2000 and a Sony TCD10-pro DAT recorder in 2002 for the song duel treatment. The visual behaviour of the treatment males and the neighbouring males was narrated on to the tapes. Recordings began at the start of stimulation of the treatment males. From the recordings, we quantified the behaviours of the treatment males to assess our success in completing the two treatments. We recorded the number of diving song sequences and number of diving songs per sequence, number of flight songs, number of perch songs, and percentage time spent woid-calling. We recorded the following responses of neighbouring males: number of flight songs, number of perch songs, time spent woidcalling, and whether they intruded on to the territory of the treatment males. Parametric statistics were calculated in SAS v. 6.12 (SAS Institute Inc., Cary, North Carolina, U.S.A.). However, because some of the data could not fulfil the assumptions of parametric tests, nonparametric statistics were used. Nonparametric tests were calculated in accordance with Siegel & Castellan (1988). All probabilities were two-tailed. Power tests were calculated in S-plus v. 6.1 (Insightful Corp., Seattle, Washington, U.S.A.). RESULTS
Control of the Treatments There were no differences between the 2 years with respect to any of the behavioural measures (t test: all
t14 ! 0.92, P R 0.378) or the proportion of birds that intruded (Fisher’s exact test: P Z 1.00). The data for the 2 years were therefore pooled. In the song duel treatment, the perch song, flight song activity and time spent woid-calling of the treatment male did not differ between the three male playback stimuli (ANOVA: all F2,13 % 1.54, all P R 0.252). In the courtship treatment the two female dummies elicited the same number of intrusions, and the flight song activity and time spent woid-calling of the treatment males did not differ between treatments (t test: both t14 ! 0.72, both P O 0.486); however, the perch song activity tended to be higher although not significantly so (t test: t14 Z 2.01, P Z 0.064). Altogether, the various playbacks did not give rise to biases in the treatments.
Completion of Treatments The song duel treatment was completed in all of the 16 trials, as the 16 treatment males responded almost immediately to the playback of perch song by approaching the speaker and singing back. None of the treatment males left their territories or responded with diving song displays to this treatment. All song duel treatments were maintained for 7 min. The courtship treatment was also completed in all of the trials with respect to the courtship vocalizations. Fifteen of the treatment males gave complete diving song displays to the female dummy. The last male gave only diving songs close to the stuffed female. During the 7-min treatment period, they gave a mean G SE of 3.0 G 0.6 (range 0–10) diving song sequences that each included 8.1 G 1.2 diving songs. Four of the males attempted copulation with the dummy female. In some of the males, the courtship was maintained far beyond the 7-min treatment period. The mean total duration of the males’ courtship G SE was 17 min 3 s G 1 min 29 s (range 9 min 26 s–29 min 39 s). The courtship treatment also differed from the song duel treatment by including fewer perch songs (paired t test: t15 Z 2.65, P Z 0.018; Fig. 1a), and by tending to include more flight songs (t15 Z 2.05, P Z 0.058; Fig. 1b) and more woid-calls (t15 Z 2.67, P Z 0.018; Fig. 1c). Significantly more of the treatment males gave woid-calls during the courtship treatment (12 males) than during the song duel treatment (three males; binomial test: k Z 1, N Z 11, P Z 0.012; five males were excluded because of ties).
Responses of Neighbouring Males In general, the neighbouring males responded with perch songs, flight songs and intrusions into the treatment territory, but almost never with woid-calls. Only one neighbouring male used a few woid-calls, and these were given during the courtship treatment. The neighbouring males responded with more flight song activity to the courtship treatment than to the song duel treatment (paired t test: t15 Z 2.26, P Z 0.039; Fig. 2b), whereas the perch song activity clearly did not vary between the treatments (t15 Z 0.96, P Z 0.353; Fig. 2a).
BALSBY & DABELSTEEN: COURTSHIP INTERACTIONS IN THE WHITETHROAT
Perch songs/min
10 8 6 4 2
Flight songs/min
0
% Time woid-calling
*
(a)
0.7 0.6 (b) 0.5 0.4 0.3 0.2 0.1 0
Song duel
Courtship
Song duel
Courtship
20
*
(c) 15 10 5 0
Song duel
Courtship
Figure 1. Vocal activity of treatment males (XGSE) during the song duel and the courtship treatment. (a) Number of perched songs/ min, (b) numbers of flight songs/min and (c) % time spent woidcalling. Paired t test: *P ! 0.05.
Perch songs/min
The clearest difference in the effect of the two treatments was observed in the neighbouring males’ intrusion behaviour. None of the 16 males intruded during the song duel treatment, whereas six of the 16 males intruded during the 7-min courtship treatment period. This difference between the two treatment periods is significant 7 6 (a) 5 4 3 2 1 0
Song duel
(binomial test: k Z 0, N Z 6, P Z 0.032; 10 trials were excluded because of ties). Furthermore, three other males intruded after the 7-min courtship treatment period where the treatment male continued to court the female dummy with diving song display. Four of the intruders disrupted a copulation attempt, as they appeared while the treatment males were attempting copulation with the dummy female. One of the intruders even managed to peck at the site of the cloaca of the dummy female. All of the nine males that experienced intrusion immediately turned towards the intruder and chased it out of the territory before they resumed courting the female. The intruder was usually silent during these chases, whereas the treatment male would frequently vocalize. The intrusion decisions could not be predicted from the intruders’ song output before intrusions, because their song output during the preintrusion period, measured from playback of the first dscharp-call, did not vary from that of the nonintruders, either with respect to perch songs/min (no intrusion: XGSEZ4:86G0:92; intrusion: 4.90 G 1.02; t test: t14 Z 0.02, P Z 0.984, power Z 0.050), or with respect to flight songs/min (no intrusion: 0.25 G 0.07; intrusion: 29 G 0.09; t14 Z 0.39, P Z 0.698, power Z 0.070). It could be argued that the vocal activity of the treatment males rather than the occurrence of courtship per se determined whether the neighbouring males intruded. We tested this by comparing the vocal output of treatment males experiencing intrusion from the neighbouring males with that of treatment males that did not experience intrusions. We estimated the song outputs of perch and flight song from the first dscharp-call until the first intrusion after the first diving song. The two categories of treatment males did not vary for any of the three song types: diving songs/min, perch songs/min and flight songs/min (diving song: no intrusion: XGSEZ0:014G0:005; intrusion: 0.019 G 0.009; t test: t14 Z 0.46, P Z 0.650, power Z 0.079; perch song: no intrusion: 6.03 G 1.47; intrusion: 7.42 G 3.24; t14 Z 1.04, P Z 0.314, power Z 0.207; flight song: no intrusion: 0.57 G 0.82; intrusion: 0.70 G 0.18; t14 Z 0.67, P Z 0.516, unequal variance, power Z 0.103). However, the treatment males in territories where no intrusion occurred tended to spend more time woid-calling than treatment males that suffered intrusions, although not significantly so (no intrusion: XGSEZ13:17G3:26; intrusion: 4.69 G 2.57; t test: t14 Z 2.07, P Z 0.057, power Z 0.630).
Courtship
DISCUSSION Flight songs/min
0.6
*
0.5 (b) 0.4 0.3 0.2 0.1 0
Song duel
Courtship
Figure 2. Vocal response of neighbouring male (XGSE) to the song duel and the courtship treatment. (a) Number of perch songs/min and (b) number of flight songs/min. Paired t test: *P ! 0.05.
This experiment shows that whitethroat courtship interactions, unlike song duel interactions, frequently elicit intrusion of neighbouring males into the territory where the interaction takes place. The higher frequency of intrusion in the courtship context relative to other contexts is also supported by observations of natural courtship interactions (Balsby & Dabelsteen 2003a). All of the intrusions in this study did in some way result in interference with the courtship or even the copulation of the intruded males, which immediately turned towards the intruder and chased it. One of the consequences of
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intrusions during natural courtship is that males, as in this study, put all their effort into chasing the intruder and that females disappear from the territories while the male is busy with the intruder (personal observations). It is possible that in whitethroats intrusions followed by courtship disruption might also be used to redirect female mate choice, as has been suggested for lek-displaying species (Trail 1985), although there are no observations supporting this in whitethroats. Intrusions can be rather costly for the treatment males in terms of lost opportunities for attracting a female, and maybe even in terms of lost fertilization opportunities if the intruder interrupts copulation or if cloaca pecking results in sperm ejection as in the dunnock (Davies 1983). The decisions to intrude were probably made on the basis of information gathered from the vocalizations of one or both of the individuals involved in the courtship interactions, because visual detection of the female dummy used in the experiment would have been difficult even for the treatment males if no auditory cues were available (Balsby & Dabelsteen 2002). The high song flight activity of neighbouring males could be explained as attempts to facilitate visual location of a female after a change in the vocal activity in the treatment male’s territory. Visual location may be necessary since acoustic ranging would be difficult in an open whitethroat habitat (Balsby et al. 2003). Alternatively, the high song flight activity of the neighbouring males may simply be attempts to match the increased song flight activity of the treatment male as a part of male–male vocal competition in attracting females. Song is used in territorial defence in many species and intrusions may therefore vary with song activity. However, the song activity of the treatment males in this experiment did not vary between males that suffered intrusions and males that never experienced intrusions, and although these tests have low power, they indicate that differences in song activity cannot explain the intrusions. The tendency for males suffering intrusions to give fewer woid-calls than males that did not indicates that woidcalls might play a role in deterring neighbouring males from intruding. This result follows another experiment, which showed that woid-calls can at least delay males’ approaches to a place where courtship takes place (Balsby & Dabelsteen 2003b). Despite the treatment, males using woid-calls at a high rate in between the courtship displays (Fig. 1c), most of them sooner or later proved incapable of deterring neighbouring males from intruding. The only effective way of avoiding intrusions during courtship may therefore be to use signals with limited transmission capability (e.g. McGregor & Dabelsteen 1996; Dabelsteen et al. 1998). The very short transmission ranges of the whitethroat diving songs used during courtship may therefore have evolved as a result of selection for restricted information transfer (Balsby et al. 2003). However, males in neighbouring territories may be able to use alternative cues about potential courtship from both of the sexes involved in precourtship activities. Female cues might include dscharp-calls, which may sometimes transmit into neighbouring territories (Balsby et al. 2003). Whether neighbours should use dscharp-calls solely as a basis for intrusion decisions, however, is doubtful since it is
difficult to distinguish between dscharp-calls from the two sexes and because the call is also used as a contact call between mated individuals and in response to intrusions by mated individuals (Balsby 2000, personal observation). Male acoustic cues may include changes in song activity. For instance, the treatment males in this study showed a very high song flight activity before the courtship treatment period, which, in combination with the female dscharp-calls, may have made the neighbouring males aware that something of potential interest was happening in the territories of the treatment males. However, only one of the nine intrusions occurred before the first diving song, suggesting that the neighbouring males did not have reliable information about courtship until they had somehow perceived the diving song display. The diving song display carries reliable information about courtship and also allows approximate location of the female, since diving songs are usually given only while the male is diving towards the female. However, the diving song display does not in itself seem capable of providing reliable information about the receptiveness of the female and how well the treatment male was able to match the female courtship solicitations such as the dscharp-calls. Such information could require eavesdropping on the courtship interaction where the neighbouring males also extract information from the female part of the interaction. However, the information about female presence and location, which is contained in the diving song display, may still be sufficient for a neighbouring male to decide to intrude and hence create a selection pressure for quieter diving songs and for the associated flying pattern to occur at relatively low heights. Diving songs are very quiet (Balsby et al. 2003) and they always occur close to the vegetation (personal observations). Courtship disruptions have been studied extensively in lek species such as black grouse (Lack 1939; Alatalo et al. 1996), great snipe, Gallinago media (Sæther et al. 1999), Guinean cock-of-the-rock, Chiroxipha linearis (Trail 1985; Trail & Koutnik 1986), buff-breasted sandpiper, Tryngites subruficollis (Lanctot et al. 1998) and several species of grouse (Foster 1983). Direct courtship disruptions have received much less attention in territorial species, although they have been reported in the Eurasian blackbird (Snow 1958) and the dunnock (Davies 1992). Furthermore, the number of intruders peaks in the female’s fertile period for several species (Møller 1987) and extrapair paternity is common in many socially monogamous species (Griffith et al. 2002), indicating that courtship interruptions might occur in several species. However, courtship disruptions may be less frequent in territorial species than in lek species because the relatively large territory sizes may facilitate concealment of courtship activities. The importance of distance is indicated in lek species by a negative relation between the frequency of courtship or copulation disruptions and distance between territory centres (Foster 1983; Alatalo et al. 1996). In the whitethroat, the territory size is much larger at the time of pair formation than during incubation (Sell & Odderskær 1990). The relatively large territory sizes of unmated males may help in reducing the transfer of information about courtship to neighbouring males.
BALSBY & DABELSTEEN: COURTSHIP INTERACTIONS IN THE WHITETHROAT
In conclusion, our study shows that males may try to constrain a neighbour’s detection of their courtship by using quiet vocalizations with short transmission range. However, such detections cannot totally be avoided; when courtship was detected by neighbouring males most of them sooner or later intruded into the courtship territory with the result that the courting male interrupted its courtship or copulation attempt to chase the intruder. Similar detection of song duels did not result in intrusions. Whitethroat males normally respect the territory borders of their neighbours. Only courtship seems capable of diminishing this respect. Acknowledgments We thank the Mols Laboratory, Natural History Museum and Fussingø Statsskovsdistrikt Skovpart Mols for permission to work in the area. John Andersen constructed the jumping female device, Simon Boel Pedersen programmed the Digital Sound Emitter for interactive playback, and Kenneth Bengtson kindly provided one of the stuffed female whitethroats. Lars Holst Hansen assisted in the field during some of the experiments. Centre for Sound Communication and Poul Hansen at the Natural History Museum A˚rhus assisted us with equipment. Peter McGregor, Stephen Nowicki, Marc Naguib, Susannah Buhrman and two anonymous referees gave valuable comments on the manuscript. T.J.S. Balsby was funded by a Ph.D. scholarship from Copenhagen University. References ¨ glund, J., Alatalo, R. V., Burke, T., Dann, J., Hanotte, O., Ho Lundberg, A., Moss, R. & Rintama¨ki, P. T. 1996. Paternity, copulation disturbance and female choice in lekking black grouse. Animal Behaviour, 52, 861–873. Balsby, T. J. S. 2000. The function of song in whitethroats Sylvia communis. Bioacoustics, 11, 17–30. Balsby, T. J. S. & Dabelsteen, T. 2001. The meaning of song repertoire size and song length to male whitethroats Sylvia communis. Behavioural Processes, 56, 75–84. Balsby, T. J. S. & Dabelsteen, T. 2002. Female behaviour affects male courtship in whitethroats Sylvia communis. An interactive experiment using visual and acoustic cues. Animal Behaviour, 63, 251–257. Balsby, T. J. S. & Dabelsteen, T. 2003a. Male singing behaviour and female presence in the territory in whitethroats. Acta Ethologica, 4, 81–88. Balsby, T. J. S. & Dabelsteen, T. 2003b. Male calling between courtship sequences in whitethroats: a way to counter intrusions from neighbouring rivals. Behavioural Processes, 63, 149–157. Balsby, T. J. S., Dabelsteen, T. & Pedersen, S. B. 2003. Degradation of whitethroat vocalisations: implications for song flight and communication network activities. Behaviour, 140, 695–720. Beehler, B. 1983. Lek behaviour of the lesser bird of paradise. Auk, 100, 992–995. Bergmann, H.-H. & Helb, H.-W. 1982. Stimmen der Vo¨gel Europas. Mu ¨ nchen: BLV Verlagsgesellschaft. Dabelsteen, T. 1988. The meaning of the full song of the blackbird Turdus merula to untreated and estradiol treated females. Ornis Scandinavica, 19, 7–16.
Dabelsteen, T. 1992. Interactive playback: a finely tuned response. In: Playback and Studies of Animal Communication (Ed. by P. K. McGregor), pp. 97–109. London: Plenum. Dabelsteen, T. & Pedersen, S. B. 1990. Song and information about aggressive responses of blackbirds, Turdus merula: evidence from interactive playback experiments with territory owners. Animal Behaviour, 40, 1158–1168. Dabelsteen, T., McGregor, P. K., Lampe, H. M., Langmore, N. E. & Holland, J. 1998. Quiet song in song birds: an overlooked phenomenon. Bioacoustics, 9, 89–105. Davies, N. B. 1983. Polyandry, cloaca-pecking and sperm competition in dunnocks. Nature, 302, 334–336. Davies, N. B. 1992. Dunnock Behaviour and Social Evolution. Oxford: Oxford University Press. Eens, M., Pinxten, R. & Verheyen, R. F. 1993. Function of the song and song repertoire in the European starling Sturnus vulgaris: an aviary experiment. Behaviour, 125, 51–66. Foster, M. 1983. Disruption, dispersion, and dominance in lekbreeding birds. American Naturalist, 122, 53–72. Griffith, S. C., Owens, I. P. F. & Thuman, K. A. 2002. Extra pair paternity in birds: a review of interspecific variation and adaptive function. Molecular Ecology, 11, 2195–2212. Halupka, K., Borowiec, M., Karczewska, A., Kunka, A. & Pietrowiak, J. 2002. Habitat requirements of whitethroats Sylvia communis breeding in an alluvial plain. Bird Study, 49, 297–299. ¨ glund, J. & Alatalo, R. V. 1995. Leks. Princeton, New Jersey: Ho Princeton University Press. Lack, D. 1939. The display of the blackcock. British Birds, 32, 290–303. Lack, D. 1940. Observations on captive robins. British Birds, 33, 262–270. Lanctot, R. B., Weatherhead, P. J., Kempenars, B. & Scribner, K. T. 1998. Male traits, mating tactics and reproductive success in the buff-breasted sandpiper, Tryngites subruficollis. Animal Behaviour, 56, 419–432. Larsen, O. N. & Dabelsteen, T. 1997. The VIFA10 Neodymium tweeter: a versatile speaker for playback experiments. Bioacoustics, 8, 323–326. McGregor, P. K. 1993. Signalling in territorial systems: a context for individual identification, ranging and eavesdropping. Philosophical Transactions of the Royal Society of London, Series B, 340, 237–244. McGregor, P. K. & Dabelsteen, T. 1996. Communication networks. In: Ecology and Evolution of Acoustic Communication in Birds (Ed. by D. E. Kroodsma & E. H. Miller), pp. 409–425. Ithaca: Cornell University Press. McGregor, P. K., Dabelsteen, T. & Holland, J. 1997. Eavesdropping in a territorial songbird communication network: preliminary results. Bioacoustics, 8, 253–254. Mennill, D. J., Ratcliffe, L. M. & Boag, P. 2002. Female eavesdropping on male song contests in song birds. Science, 296, 873. Montgomerie, R. & Thornhill, R. 1990. Fertility advertisement in birds: a means of inciting male–male competition. Ethology, 81, 209–220. Møller, A. P. 1987. Intruders and defenders of avian sperm competition. Oikos, 48, 47–54. Naguib, M. & Todt, D. 1997. Effects of dyadic vocal interactions on other conspecific receivers in nightingales. Animal Behaviour, 54, 1535–1543. Naguib, M., Fichtel, C. & Todt, D. 1999. Nightingales respond more strongly to vocal leaders of simulated dyadic interactions. Proceedings of the Royal Society of London, Series B, 266, 537–542. Otter, K., McGregor, P. K., Terry, A. M. R., Burford, F. R. L., Peake, T. M. & Dabelsteen, T. 1999. Do female great tits Parus
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major assess males by eavesdropping? A field study using interactive playback. Proceedings of the Royal Society of London, Series B, 266, 1305–1309. Peake, T. M., Terry, A. M. R., McGregor, P. K. & Dabelsteen, T. 2001. Male great tits eavesdrop on simulated male-to-male vocal interactions. Proceedings of the Royal Society of London, Series B, 268, 1183–1187. Peake, T. M., Terry, A. M. R., McGregor, P. K. & Dabelsteen, T. 2002. Do great tits assess rivals by combining direct experience with information gathered by eavesdropping? Proceedings of the Royal Society of London, Series B, 269, 1925–1929. Pedersen, S. B. 1998. Preliminary Operation Manual for Signal Processor SIGPRO. Odense: Centre for Sound Communication, Odense University. Pizzari, T. 2001. Indirect partner choice through manipulation of male behaviour by female fowl, Gallus gallus domesticus. Proceedings of the Royal Society of London, Series B, 268, 181–186. Ritchison, G. 1995. Characteristics, use and possible functions of the perch songs and chatter calls of male common yellowthroats. Condor, 97, 27–38. Sæther, S. A., Fiske, P. & Ka˚la˚s, J. A. 1999. Pushy males and choosy females: courtship disruption and mate choice in the lekking great
snipe. Proceedings of the Royal Society of London, Series B, 266, 1227–1234. Searcy, W. A. & Yasukawa, K. 1990. Use of the song repertoire in intersexual contexts by male red-winged blackbirds. Behavioral Ecology and Sociobiology, 27, 123–128. Sell, H. & Odderskær, P. 1990. Tornsangerens ynglebiologi i danske læhegn. Dansk Ornithologisk Forenings Tidsskrift, 84, 21–29. Siegel, S. & Castellan, N. J., Jr. 1988. Nonparametric Statistics for Behavioral Sciences. 2nd edn. New York: McGraw-Hill. Snow, D. W. 1958. A Study of Blackbirds. London: British Museum (Natural History). Titus, R. C. 1998. Short-range and long-range songs: use of two acoustically distinct song classes by dark-eyed juncos. Auk, 115, 386–393. Tobias, J. A. & Seddon, N. 2002. Female begging in European robins: do neighbours eavesdrop for extra pair copulations? Behavioral Ecology, 13, 637–642. Trail, P. W. 1985. Courtship disruption modifies mate choice in a lek-breeding bird. Science, 227, 778–780. Trail, P. W. & Koutnik, D. L. 1986. Courtship disruption at the lek in the Guianan cock-of-the-rock. Ethology, 73, 197–218. Wiley, R. H. & Poston, J. 1996. Indirect mate choice, competition for mates, and coevolution of the sexes. Evolution, 50, 1371–1381.
Simulated courtship interactions elicit neighbour intrusions in the whitethroat, Sylvia communis THORSTEN J. S. BA LSBY & TOR BEN DABELSTEEN
Department of Animal Behaviour, Zoological Institute, University of Copenhagen (Received 11 October 2001; initial acceptance 28 November 2001; final acceptance 22 January 2004; published online 11 November 2004; MS. number: 7092R)
Animals often signal in communication network environments that include nonintended receivers that may constitute a risk to the signalling animals. Unpaired male songbirds, which sometimes intrude into neighbouring territories and interrupt courtship, may be an example of nonintended receivers of vocal courtship signals. We investigated this in the whitethroat, using dyads of unmated territorial males. Each dyad consisted of a resident male, who was part of the experimental treatment, and a neighbouring male, whose responses to the treatment stimuli were tested. Each dyad received two playback treatments: a courtship treatment in which the treatment male was induced to court a remotely controlled calling and jumping stuffed female, and a song duel treatment in which playbacks of male song were used to induce the focal male to countersing. The neighbours responded with more song flights to the courtship treatment than to the song duel treatment, perhaps to achieve an overview of the courtship activity or attract the female. Only the courtship treatment resulted in neighbouring intrusions and immediate chasing of the intruder by the treatment male. The males that suffered intrusions did not sing less than those that did not suffer intrusions. Reduced singing therefore may not be able to explain the intrusions. Every intrusion except one occurred after the first courtship vocalization, making it likely that the courtship per se caused the intrusions. This emphasizes the necessity of restricting the transmission range of courtship vocalizations in a network and therefore also explains why the courtship vocalizations of whitethroat males are relatively short ranging. Ó 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Vocalizations are usually propagated in a communication network environment where several individuals may be potential receivers of the signals (e.g. Dabelsteen 1992; McGregor 1993; McGregor & Dabelsteen 1996). The presence of both intended and nonintended receivers may have acted as a strong selection force in the evolution of the vocalizations, since either restricting or increasing the transmission capability of the vocalizations might have been adaptive in different contexts (e.g. McGregor & Dabelsteen 1996; Dabelsteen et al. 1998). Several species use quiet vocalizations during courtship and in aggressive intrasexual interactions, for example the Eurasian blackbird, Turdus merula (Dabelsteen 1988; Dabelsteen & Pedersen 1990), the common yellowthroat, Geothlypis trichas (Ritchison 1995) and the dark-eyed junco, Junco hyemalis (Titus 1998); see also the review by Correspondence and present address: T. J. S. Balsby, The Macaulay Library, Cornell Laboratory of Ornithology, 159 Sapsucker Woods Road, Ithaca, NY 14850, U.S.A. (email: [email protected]). T. Dabelsteen is at the Department of Animal Behaviour, Zoological Institute, University of Copenhagen, Tagensvej 16, DK-2200 Copenhagen N, Denmark. 0003–3472/04/$30.00/0
Dabelsteen et al. (1998). The use of quiet vocalizations may be an attempt to restrict information transfer to counter disadvantageous information gathering or eavesdropping by nonintended receivers in the network (Dabelsteen et al. 1998). Eavesdropping (McGregor & Dabelsteen 1996) is different from ordinary information gathering in that information is extracted from an interaction between other individuals and therefore may be relative about the interactants. Such relative information cannot be obtained by listening to the signals of the interactants separately. Neighbouring males may use information from courtship to the unambiguous disadvantage of the courting male. In territorial species such as European robins, Erithacus rubecula (Lack 1940), Eurasian blackbirds (Snow 1958) and dunnocks, Prunella modularis (Davies 1992) intruding males disrupt courtship or copulation attempts. In lekking species where information transfer cannot be restricted because of the high density of small territories, disruption of courtship and copulation ¨ glund & is well known (e.g. Foster 1983; Trail 1985; Ho Alatalo 1995; Alatalo et al. 1996). In a number of other species, both territorial and nonterritorial, females may call loudly in the context of courtship, that is, use calls
161 Ó 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
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with a long transmission range relative to the distance to other males (Montgomerie & Thornhill 1990). These calls may be used by females to attract males from the surroundings and thereby induce competition between males (Montgomerie & Thornhill 1990; Pizzari 2001). This could give females an opportunity to compare males through male–male competition or alternatively only the winner of the male–male competition may have access to the females (Wiley & Poston 1996). Female presence on a male’s territory could also be revealed by the behaviour of the male, which may use special displays or intensify the display of sexually selected traits, for instance in the lesser bird of paradise, Paradisaea minor (Beehler 1983), red-winged blackbird, Agelaius phoeniceus (Searcy & Yasukawa 1990), European starling, Sturnus vulgaris (Eens et al. 1993) and whitethroat (Balsby & Dabelsteen 2003a). Both male and female birds are able to eavesdrop on male–male vocal interactions in neighbouring territories (McGregor et al. 1997; Naguib & Todt 1997; Naguib et al. 1999; Otter et al. 1999; Peake et al. 2001, 2002; Mennill et al. 2002). Furthermore, Tobias & Seddon (2002) have shown that neighbouring male robins can gather information from loud female begging calls, which are given especially during the fertile period, and although they are directed at the mate, the neighbouring males will approach the female in response to these calls. Responses of neighbouring males to male–female interactions, that is, courtship interactions, have not yet been investigated although such interactions may have a strong effect. For instance, Lack (1939) mentioned that male black grouse, Tetrao tetrix, would intensify their display rate if a female is being courted inside the neighbouring territory. We investigated the responses of whitethroat males to information gathered from neighbouring territories. We allowed the males to gather information or eavesdrop on courtship and song duels taking place on neighbouring territories. Whitethroat males sing from a perched position (perch song) as well as during song flights (flight song; Balsby & Dabelsteen 2003a). Males typically use perch songs in vocal interactions with other males. Most male–male vocal interactions take place across territory borders, but they sometimes occur inside a territory (personal observation). Courtship usually takes place inside a territory. The unmated females visit several territories of unmated males before choosing a male (personal observation). Male courtship of visiting females is characterized by a special type of display, the diving song display, in which the male dives towards the female while singing a characteristic quiet diving song (Balsby 2000; Balsby & Dabelsteen 2003a). Diving song displays are often given in sequences of several displays. After a sequence of diving song displays, males often give sequences of woid-calls (Bergmann & Helb 1982) and sometimes a song flight before returning to normal singing behaviour, which mainly consists of perch songs at the territory border (Balsby & Dabelsteen 2003a). The behaviour of the female influences the courtship behaviour of the male in different ways. Female dscharp-calls (Bergmann & Helb 1982) can initiate the diving song display, and during courtship females may
respond to this display with short horizontal jumps and quiet ze-calls (Balsby & Dabelsteen 2002). The jumps increase the number of diving songs, whereas the ze-calls may elicit copulation attempts (Balsby & Dabelsteen 2002). Besides the diving song display, which occurs only in the presence of a female, males may also give woid-calls in association with the courtship (Balsby & Dabelsteen 2003a). These woid-calls may be directed towards potential male intruders and are capable of delaying intrusions (Balsby & Dabelsteen 2003b). We compared neighbouring whitethroat males’ responses to two treatments, which were both set up inside the territory of the treatment males: a courtship treatment and a song duel treatment. The courtship treatment allowed the neighbouring males to perceive the vocal signals of a courtship interaction between the treatment male and a simulated female, whereas the song duel treatment allowed the neighbouring males to perceive a song duel between the treatment male and a simulated male. We quantified the singing behaviour of the neighbouring males as well as whether they intruded on to the territories of the treatment males where the treatments were presented. Observations of unmated males showed that most intrusions occur when females are visiting the territory (Balsby & Dabelsteen 2003a). We therefore predicted that neighbouring males would intrude on the territory more often in response to the courtship treatment than to the song duel treatment. METHODS
Test Subjects and Equipment We carried out the experiment at Mols Bjerge, Denmark (56 140 N, 10 350 E), between 16 May and 4 July 2000 and between 13 May and 19 June 2002. All trials were initiated between 0700 and 1300 hours using 23 dyads of neighbouring unmated males of which only 16 dyads (11 in 2000 and five in 2002) of males were successful (see below). We used only unmated males because mated males are much less responsive to both male (Balsby 2000) and female stimuli (personal observation). The unmated males could easily be distinguished from mated males on the basis of their very high song activity (Balsby 2000). In each dyad, one of the males, the treatment male, was part of the treatment, whereas the other male was the neighbouring test subject. Each neighbouring test subject was presented with two treatments, a courtship treatment in which the treatment male was stimulated to court a remotely controlled calling and jumping stuffed female, and a song duel treatment in which the treatment male was stimulated to countersing to a small loudspeaker playing perch songs. The vocalizations used for stimulating the treatment males were all recorded in the experimental area in 1998 with a Sennheiser MKH816T and a SONY TCD10-PRO DAT recorder. All vocalizations were digitized in Avisoft (Avisoft-SASLab, Berlin, Germany). The subsequent sound processing was done in SIGPRO (Pedersen 1998). The digitized vocalizations were filtered and then standardized to the same peak amplitude value.
BALSBY & DABELSTEEN: COURTSHIP INTERACTIONS IN THE WHITETHROAT
The playback part of the song duel treatment was played from the SONY TCD10-PRO DAT in 2000 and from a portable computer by means of Avisoft in 2002, whereas the vocalizations used in the courtship treatment were played from a portable computer (Toshiba Satellite 300 CDS) connected to a Digital Sound Emitter (Dabelsteen 1992). For both treatments, the vocalizations were then amplified by a 35-W Dennon DCA power amplifier and played back through a small speaker (VIFA 1 Neodymium tweeter; Larsen & Dabelsteen 1997). The sound pressure level for the three types of vocalization were adjusted to ¨ el & Kjær Sound Pressure the natural levels using a Bru Level meter type 2236, fast setting. The natural levels were 63 dB (A) at 10 m for perch song (Balsby & Dabelsteen 2001), 46 dB (A) at 12 m for dscharp-calls and 36 dB (A) at 2.7 m for ze-calls (Balsby & Dabelsteen 2002). Whitethroat territory size varies between 0.06 and 1.0 ha (Sell & Odderskær 1990; Halupka et al. 2002), which equals a territory diameter of about 50 to about 155 m. Estimates of the discrimination distances suggest that diving songs, woid-calls and dscharp-calls transmit into neighbouring territories and that perch and flight songs transmit across neighbouring territories (Balsby et al. 2003), whereas zecalls from the centre of the territory would not transmit into the neighbouring territory.
The Song Duel Treatment The songs used to elicit the song duel with the treatment males originated from three different males. We used their songs to construct three playback stimuli each containing song from only one of the males. The three playback stimuli were used in approximately the same number of trials (N Z 4, 6, 6 trials). Each playback stimulus contained a loop of 55–61 perch songs, which was repeated twice. A song duel treatment trial involved playing one of the three stimuli towards a treatment male for 7–9 min. The songs were played from a speaker placed 1–2 m above ground level, and the behaviour of the treatment male and the neighbouring male was quantified for the first 7 min of playback during which the treatment male sang back towards the speaker.
The Courtship Treatment The courtship treatment was more complex than the song duel treatment, since both visual and acoustic female stimuli were necessary to elicit the courtship display of the treatment male. The visual part of the female stimulus consisted of a stuffed female whitethroat mounted on a remotely controlled device. This device allowed the female dummy to simulate the short horizontal jumps that natural females give in response to the dives of the males’ courtship display (Balsby & Dabelsteen 2002). The acoustic part of the female stimulus was played back interactively through a speaker placed on the ground below the stuffed female. It consisted of dscharp- and ze-calls (Balsby & Dabelsteen 2002). Seven sequences of ze-calls originating from two different females were used, but only one of the sequences was played back in a trial
(each of the ze-call sequences were used in one, two or three trials). Five dscharp-calls from two females were played back in pairs with an average rate of three pairs of calls per 2 min, and we used only two calls from one female in each trial, which gave four pairs of calls (each pair of calls was used in four, four and five trials). Two dummy females were each used in eight trials. The set-up, the interactive control of the female and the visual and acoustic stimuli are described in detail in Balsby & Dabelsteen (2002). All courtship treatment trials started with playback of dscharp-calls to initiate diving song displays of the treatment male. Dscharp-calls were also played back in the pauses between the diving song displays to stimulate the treatment males to resume the display. The jumps were given in response to the diving song display immediately after the male had passed the female dummy in a dive. The ze-calls were played during the silent intervals between the diving songs of a sequence of diving song displays and when the male perched within 2 m of the dummy. The stimulation of the treatment male was interactive and hence driven by the treatment male. The resulting courtship treatment therefore varied quantitatively between the trials, but not in quality because all neighbouring males received a complete set of male and female courtship vocalizations. We always attempted to stimulate the courtship of the treatment male maximally with dscharp-calls, jumps and ze-calls in the appropriate contexts. The treatment males did not respond with diving song immediately after the start of the female dscharp-calls. The average latency to diving song G SE was 416 G 104 s (range 12–1271 s). We defined the start of a courtship treatment as the time when the first diving song was given. The neighbouring male’s response to the courtship treatment was quantified from the first diving songs of the treatment male and 7 min onwards for comparison with the song duel treatment. However, we continued the courtship treatment upto 9 min (range 2–21 min) after the 7 min to investigate whether neighbouring males that did not intrude during the first 7 min did so later on.
Procedure and Behavioural Measurements During the experiment, the observers were sitting on the ground approximately 20 m from the set-up. The position of the observers was always chosen so that both the test and the treatment males could approach the setup directly without getting closer than 20 m to them. The treatment males were present and singing while we set up the equipment in their territories before the first treatment. The neighbouring males were also present in their territories and all but one were singing while we set up the equipment. All of the equipment for both treatments was put in position before the first treatment, except for the stuffed female, which was mounted just before the courtship treatment. We started the stimulation of the treatment male as soon as possible after positioning the equipment, when the treatment males were within hearing range of the playback. Approximately 30 min passed between the presentations of the two treatments
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to a test subject. The treatment males and the neighbouring males were similarly present and singing in their respective territories at the start of the second treatment. Seven trials were abandoned because either the neighbouring male did not respond by singing during the treatment or during the postplayback period to either the song duel treatment or the courtship treatment, or natural females entered the territory during the trial. We presented the courtship treatment first in 10 trials and the song duel treatment first in six trials. The slightly skewed proportion was due to several experiments failing during the start of the season when the song duel treatment was played first and attracted unmated females from outside the territory. The playback speaker was located at the same place in the territory of the treatment male during both treatments, that is, approximately halfway between the centre of the territory and the territory border towards the neighbouring male. In neither of the treatments were the neighbouring males likely to have seen the equipment involved in the stimulation of the treatment male, because it was hidden in the vegetation and because the distances between the neighbouring male and the experimental set-up were relatively large, at least initially. The initial decisions of the neighbouring males therefore must have relied solely on their reception of vocal cues from the interactions in the territories of the treatment males. We recorded the vocal behaviour of the neighbouring males and the treatment males with one or two directional microphones (Sennheiser MKH 70 P48 and MKH816T) on a Sony TCD10-pro DAT recorder for the female treatment and a Sony TCM5000 EMV cassette recorder in 2000 and a Sony TCD10-pro DAT recorder in 2002 for the song duel treatment. The visual behaviour of the treatment males and the neighbouring males was narrated on to the tapes. Recordings began at the start of stimulation of the treatment males. From the recordings, we quantified the behaviours of the treatment males to assess our success in completing the two treatments. We recorded the number of diving song sequences and number of diving songs per sequence, number of flight songs, number of perch songs, and percentage time spent woid-calling. We recorded the following responses of neighbouring males: number of flight songs, number of perch songs, time spent woidcalling, and whether they intruded on to the territory of the treatment males. Parametric statistics were calculated in SAS v. 6.12 (SAS Institute Inc., Cary, North Carolina, U.S.A.). However, because some of the data could not fulfil the assumptions of parametric tests, nonparametric statistics were used. Nonparametric tests were calculated in accordance with Siegel & Castellan (1988). All probabilities were two-tailed. Power tests were calculated in S-plus v. 6.1 (Insightful Corp., Seattle, Washington, U.S.A.). RESULTS
Control of the Treatments There were no differences between the 2 years with respect to any of the behavioural measures (t test: all
t14 ! 0.92, P R 0.378) or the proportion of birds that intruded (Fisher’s exact test: P Z 1.00). The data for the 2 years were therefore pooled. In the song duel treatment, the perch song, flight song activity and time spent woid-calling of the treatment male did not differ between the three male playback stimuli (ANOVA: all F2,13 % 1.54, all P R 0.252). In the courtship treatment the two female dummies elicited the same number of intrusions, and the flight song activity and time spent woid-calling of the treatment males did not differ between treatments (t test: both t14 ! 0.72, both P O 0.486); however, the perch song activity tended to be higher although not significantly so (t test: t14 Z 2.01, P Z 0.064). Altogether, the various playbacks did not give rise to biases in the treatments.
Completion of Treatments The song duel treatment was completed in all of the 16 trials, as the 16 treatment males responded almost immediately to the playback of perch song by approaching the speaker and singing back. None of the treatment males left their territories or responded with diving song displays to this treatment. All song duel treatments were maintained for 7 min. The courtship treatment was also completed in all of the trials with respect to the courtship vocalizations. Fifteen of the treatment males gave complete diving song displays to the female dummy. The last male gave only diving songs close to the stuffed female. During the 7-min treatment period, they gave a mean G SE of 3.0 G 0.6 (range 0–10) diving song sequences that each included 8.1 G 1.2 diving songs. Four of the males attempted copulation with the dummy female. In some of the males, the courtship was maintained far beyond the 7-min treatment period. The mean total duration of the males’ courtship G SE was 17 min 3 s G 1 min 29 s (range 9 min 26 s–29 min 39 s). The courtship treatment also differed from the song duel treatment by including fewer perch songs (paired t test: t15 Z 2.65, P Z 0.018; Fig. 1a), and by tending to include more flight songs (t15 Z 2.05, P Z 0.058; Fig. 1b) and more woid-calls (t15 Z 2.67, P Z 0.018; Fig. 1c). Significantly more of the treatment males gave woid-calls during the courtship treatment (12 males) than during the song duel treatment (three males; binomial test: k Z 1, N Z 11, P Z 0.012; five males were excluded because of ties).
Responses of Neighbouring Males In general, the neighbouring males responded with perch songs, flight songs and intrusions into the treatment territory, but almost never with woid-calls. Only one neighbouring male used a few woid-calls, and these were given during the courtship treatment. The neighbouring males responded with more flight song activity to the courtship treatment than to the song duel treatment (paired t test: t15 Z 2.26, P Z 0.039; Fig. 2b), whereas the perch song activity clearly did not vary between the treatments (t15 Z 0.96, P Z 0.353; Fig. 2a).
BALSBY & DABELSTEEN: COURTSHIP INTERACTIONS IN THE WHITETHROAT
Perch songs/min
10 8 6 4 2
Flight songs/min
0
% Time woid-calling
*
(a)
0.7 0.6 (b) 0.5 0.4 0.3 0.2 0.1 0
Song duel
Courtship
Song duel
Courtship
20
*
(c) 15 10 5 0
Song duel
Courtship
Figure 1. Vocal activity of treatment males (XGSE) during the song duel and the courtship treatment. (a) Number of perched songs/ min, (b) numbers of flight songs/min and (c) % time spent woidcalling. Paired t test: *P ! 0.05.
Perch songs/min
The clearest difference in the effect of the two treatments was observed in the neighbouring males’ intrusion behaviour. None of the 16 males intruded during the song duel treatment, whereas six of the 16 males intruded during the 7-min courtship treatment period. This difference between the two treatment periods is significant 7 6 (a) 5 4 3 2 1 0
Song duel
(binomial test: k Z 0, N Z 6, P Z 0.032; 10 trials were excluded because of ties). Furthermore, three other males intruded after the 7-min courtship treatment period where the treatment male continued to court the female dummy with diving song display. Four of the intruders disrupted a copulation attempt, as they appeared while the treatment males were attempting copulation with the dummy female. One of the intruders even managed to peck at the site of the cloaca of the dummy female. All of the nine males that experienced intrusion immediately turned towards the intruder and chased it out of the territory before they resumed courting the female. The intruder was usually silent during these chases, whereas the treatment male would frequently vocalize. The intrusion decisions could not be predicted from the intruders’ song output before intrusions, because their song output during the preintrusion period, measured from playback of the first dscharp-call, did not vary from that of the nonintruders, either with respect to perch songs/min (no intrusion: XGSEZ4:86G0:92; intrusion: 4.90 G 1.02; t test: t14 Z 0.02, P Z 0.984, power Z 0.050), or with respect to flight songs/min (no intrusion: 0.25 G 0.07; intrusion: 29 G 0.09; t14 Z 0.39, P Z 0.698, power Z 0.070). It could be argued that the vocal activity of the treatment males rather than the occurrence of courtship per se determined whether the neighbouring males intruded. We tested this by comparing the vocal output of treatment males experiencing intrusion from the neighbouring males with that of treatment males that did not experience intrusions. We estimated the song outputs of perch and flight song from the first dscharp-call until the first intrusion after the first diving song. The two categories of treatment males did not vary for any of the three song types: diving songs/min, perch songs/min and flight songs/min (diving song: no intrusion: XGSEZ0:014G0:005; intrusion: 0.019 G 0.009; t test: t14 Z 0.46, P Z 0.650, power Z 0.079; perch song: no intrusion: 6.03 G 1.47; intrusion: 7.42 G 3.24; t14 Z 1.04, P Z 0.314, power Z 0.207; flight song: no intrusion: 0.57 G 0.82; intrusion: 0.70 G 0.18; t14 Z 0.67, P Z 0.516, unequal variance, power Z 0.103). However, the treatment males in territories where no intrusion occurred tended to spend more time woid-calling than treatment males that suffered intrusions, although not significantly so (no intrusion: XGSEZ13:17G3:26; intrusion: 4.69 G 2.57; t test: t14 Z 2.07, P Z 0.057, power Z 0.630).
Courtship
DISCUSSION Flight songs/min
0.6
*
0.5 (b) 0.4 0.3 0.2 0.1 0
Song duel
Courtship
Figure 2. Vocal response of neighbouring male (XGSE) to the song duel and the courtship treatment. (a) Number of perch songs/min and (b) number of flight songs/min. Paired t test: *P ! 0.05.
This experiment shows that whitethroat courtship interactions, unlike song duel interactions, frequently elicit intrusion of neighbouring males into the territory where the interaction takes place. The higher frequency of intrusion in the courtship context relative to other contexts is also supported by observations of natural courtship interactions (Balsby & Dabelsteen 2003a). All of the intrusions in this study did in some way result in interference with the courtship or even the copulation of the intruded males, which immediately turned towards the intruder and chased it. One of the consequences of
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intrusions during natural courtship is that males, as in this study, put all their effort into chasing the intruder and that females disappear from the territories while the male is busy with the intruder (personal observations). It is possible that in whitethroats intrusions followed by courtship disruption might also be used to redirect female mate choice, as has been suggested for lek-displaying species (Trail 1985), although there are no observations supporting this in whitethroats. Intrusions can be rather costly for the treatment males in terms of lost opportunities for attracting a female, and maybe even in terms of lost fertilization opportunities if the intruder interrupts copulation or if cloaca pecking results in sperm ejection as in the dunnock (Davies 1983). The decisions to intrude were probably made on the basis of information gathered from the vocalizations of one or both of the individuals involved in the courtship interactions, because visual detection of the female dummy used in the experiment would have been difficult even for the treatment males if no auditory cues were available (Balsby & Dabelsteen 2002). The high song flight activity of neighbouring males could be explained as attempts to facilitate visual location of a female after a change in the vocal activity in the treatment male’s territory. Visual location may be necessary since acoustic ranging would be difficult in an open whitethroat habitat (Balsby et al. 2003). Alternatively, the high song flight activity of the neighbouring males may simply be attempts to match the increased song flight activity of the treatment male as a part of male–male vocal competition in attracting females. Song is used in territorial defence in many species and intrusions may therefore vary with song activity. However, the song activity of the treatment males in this experiment did not vary between males that suffered intrusions and males that never experienced intrusions, and although these tests have low power, they indicate that differences in song activity cannot explain the intrusions. The tendency for males suffering intrusions to give fewer woid-calls than males that did not indicates that woidcalls might play a role in deterring neighbouring males from intruding. This result follows another experiment, which showed that woid-calls can at least delay males’ approaches to a place where courtship takes place (Balsby & Dabelsteen 2003b). Despite the treatment, males using woid-calls at a high rate in between the courtship displays (Fig. 1c), most of them sooner or later proved incapable of deterring neighbouring males from intruding. The only effective way of avoiding intrusions during courtship may therefore be to use signals with limited transmission capability (e.g. McGregor & Dabelsteen 1996; Dabelsteen et al. 1998). The very short transmission ranges of the whitethroat diving songs used during courtship may therefore have evolved as a result of selection for restricted information transfer (Balsby et al. 2003). However, males in neighbouring territories may be able to use alternative cues about potential courtship from both of the sexes involved in precourtship activities. Female cues might include dscharp-calls, which may sometimes transmit into neighbouring territories (Balsby et al. 2003). Whether neighbours should use dscharp-calls solely as a basis for intrusion decisions, however, is doubtful since it is
difficult to distinguish between dscharp-calls from the two sexes and because the call is also used as a contact call between mated individuals and in response to intrusions by mated individuals (Balsby 2000, personal observation). Male acoustic cues may include changes in song activity. For instance, the treatment males in this study showed a very high song flight activity before the courtship treatment period, which, in combination with the female dscharp-calls, may have made the neighbouring males aware that something of potential interest was happening in the territories of the treatment males. However, only one of the nine intrusions occurred before the first diving song, suggesting that the neighbouring males did not have reliable information about courtship until they had somehow perceived the diving song display. The diving song display carries reliable information about courtship and also allows approximate location of the female, since diving songs are usually given only while the male is diving towards the female. However, the diving song display does not in itself seem capable of providing reliable information about the receptiveness of the female and how well the treatment male was able to match the female courtship solicitations such as the dscharp-calls. Such information could require eavesdropping on the courtship interaction where the neighbouring males also extract information from the female part of the interaction. However, the information about female presence and location, which is contained in the diving song display, may still be sufficient for a neighbouring male to decide to intrude and hence create a selection pressure for quieter diving songs and for the associated flying pattern to occur at relatively low heights. Diving songs are very quiet (Balsby et al. 2003) and they always occur close to the vegetation (personal observations). Courtship disruptions have been studied extensively in lek species such as black grouse (Lack 1939; Alatalo et al. 1996), great snipe, Gallinago media (Sæther et al. 1999), Guinean cock-of-the-rock, Chiroxipha linearis (Trail 1985; Trail & Koutnik 1986), buff-breasted sandpiper, Tryngites subruficollis (Lanctot et al. 1998) and several species of grouse (Foster 1983). Direct courtship disruptions have received much less attention in territorial species, although they have been reported in the Eurasian blackbird (Snow 1958) and the dunnock (Davies 1992). Furthermore, the number of intruders peaks in the female’s fertile period for several species (Møller 1987) and extrapair paternity is common in many socially monogamous species (Griffith et al. 2002), indicating that courtship interruptions might occur in several species. However, courtship disruptions may be less frequent in territorial species than in lek species because the relatively large territory sizes may facilitate concealment of courtship activities. The importance of distance is indicated in lek species by a negative relation between the frequency of courtship or copulation disruptions and distance between territory centres (Foster 1983; Alatalo et al. 1996). In the whitethroat, the territory size is much larger at the time of pair formation than during incubation (Sell & Odderskær 1990). The relatively large territory sizes of unmated males may help in reducing the transfer of information about courtship to neighbouring males.
BALSBY & DABELSTEEN: COURTSHIP INTERACTIONS IN THE WHITETHROAT
In conclusion, our study shows that males may try to constrain a neighbour’s detection of their courtship by using quiet vocalizations with short transmission range. However, such detections cannot totally be avoided; when courtship was detected by neighbouring males most of them sooner or later intruded into the courtship territory with the result that the courting male interrupted its courtship or copulation attempt to chase the intruder. Similar detection of song duels did not result in intrusions. Whitethroat males normally respect the territory borders of their neighbours. Only courtship seems capable of diminishing this respect. Acknowledgments We thank the Mols Laboratory, Natural History Museum and Fussingø Statsskovsdistrikt Skovpart Mols for permission to work in the area. John Andersen constructed the jumping female device, Simon Boel Pedersen programmed the Digital Sound Emitter for interactive playback, and Kenneth Bengtson kindly provided one of the stuffed female whitethroats. Lars Holst Hansen assisted in the field during some of the experiments. Centre for Sound Communication and Poul Hansen at the Natural History Museum A˚rhus assisted us with equipment. Peter McGregor, Stephen Nowicki, Marc Naguib, Susannah Buhrman and two anonymous referees gave valuable comments on the manuscript. T.J.S. Balsby was funded by a Ph.D. scholarship from Copenhagen University. References ¨ glund, J., Alatalo, R. V., Burke, T., Dann, J., Hanotte, O., Ho Lundberg, A., Moss, R. & Rintama¨ki, P. T. 1996. Paternity, copulation disturbance and female choice in lekking black grouse. Animal Behaviour, 52, 861–873. Balsby, T. J. S. 2000. The function of song in whitethroats Sylvia communis. Bioacoustics, 11, 17–30. Balsby, T. J. S. & Dabelsteen, T. 2001. The meaning of song repertoire size and song length to male whitethroats Sylvia communis. Behavioural Processes, 56, 75–84. Balsby, T. J. S. & Dabelsteen, T. 2002. Female behaviour affects male courtship in whitethroats Sylvia communis. An interactive experiment using visual and acoustic cues. Animal Behaviour, 63, 251–257. Balsby, T. J. S. & Dabelsteen, T. 2003a. Male singing behaviour and female presence in the territory in whitethroats. Acta Ethologica, 4, 81–88. Balsby, T. J. S. & Dabelsteen, T. 2003b. Male calling between courtship sequences in whitethroats: a way to counter intrusions from neighbouring rivals. Behavioural Processes, 63, 149–157. Balsby, T. J. S., Dabelsteen, T. & Pedersen, S. B. 2003. Degradation of whitethroat vocalisations: implications for song flight and communication network activities. Behaviour, 140, 695–720. Beehler, B. 1983. Lek behaviour of the lesser bird of paradise. Auk, 100, 992–995. Bergmann, H.-H. & Helb, H.-W. 1982. Stimmen der Vo¨gel Europas. Mu ¨ nchen: BLV Verlagsgesellschaft. Dabelsteen, T. 1988. The meaning of the full song of the blackbird Turdus merula to untreated and estradiol treated females. Ornis Scandinavica, 19, 7–16.
Dabelsteen, T. 1992. Interactive playback: a finely tuned response. In: Playback and Studies of Animal Communication (Ed. by P. K. McGregor), pp. 97–109. London: Plenum. Dabelsteen, T. & Pedersen, S. B. 1990. Song and information about aggressive responses of blackbirds, Turdus merula: evidence from interactive playback experiments with territory owners. Animal Behaviour, 40, 1158–1168. Dabelsteen, T., McGregor, P. K., Lampe, H. M., Langmore, N. E. & Holland, J. 1998. Quiet song in song birds: an overlooked phenomenon. Bioacoustics, 9, 89–105. Davies, N. B. 1983. Polyandry, cloaca-pecking and sperm competition in dunnocks. Nature, 302, 334–336. Davies, N. B. 1992. Dunnock Behaviour and Social Evolution. Oxford: Oxford University Press. Eens, M., Pinxten, R. & Verheyen, R. F. 1993. Function of the song and song repertoire in the European starling Sturnus vulgaris: an aviary experiment. Behaviour, 125, 51–66. Foster, M. 1983. Disruption, dispersion, and dominance in lekbreeding birds. American Naturalist, 122, 53–72. Griffith, S. C., Owens, I. P. F. & Thuman, K. A. 2002. Extra pair paternity in birds: a review of interspecific variation and adaptive function. Molecular Ecology, 11, 2195–2212. Halupka, K., Borowiec, M., Karczewska, A., Kunka, A. & Pietrowiak, J. 2002. Habitat requirements of whitethroats Sylvia communis breeding in an alluvial plain. Bird Study, 49, 297–299. ¨ glund, J. & Alatalo, R. V. 1995. Leks. Princeton, New Jersey: Ho Princeton University Press. Lack, D. 1939. The display of the blackcock. British Birds, 32, 290–303. Lack, D. 1940. Observations on captive robins. British Birds, 33, 262–270. Lanctot, R. B., Weatherhead, P. J., Kempenars, B. & Scribner, K. T. 1998. Male traits, mating tactics and reproductive success in the buff-breasted sandpiper, Tryngites subruficollis. Animal Behaviour, 56, 419–432. Larsen, O. N. & Dabelsteen, T. 1997. The VIFA10 Neodymium tweeter: a versatile speaker for playback experiments. Bioacoustics, 8, 323–326. McGregor, P. K. 1993. Signalling in territorial systems: a context for individual identification, ranging and eavesdropping. Philosophical Transactions of the Royal Society of London, Series B, 340, 237–244. McGregor, P. K. & Dabelsteen, T. 1996. Communication networks. In: Ecology and Evolution of Acoustic Communication in Birds (Ed. by D. E. Kroodsma & E. H. Miller), pp. 409–425. Ithaca: Cornell University Press. McGregor, P. K., Dabelsteen, T. & Holland, J. 1997. Eavesdropping in a territorial songbird communication network: preliminary results. Bioacoustics, 8, 253–254. Mennill, D. J., Ratcliffe, L. M. & Boag, P. 2002. Female eavesdropping on male song contests in song birds. Science, 296, 873. Montgomerie, R. & Thornhill, R. 1990. Fertility advertisement in birds: a means of inciting male–male competition. Ethology, 81, 209–220. Møller, A. P. 1987. Intruders and defenders of avian sperm competition. Oikos, 48, 47–54. Naguib, M. & Todt, D. 1997. Effects of dyadic vocal interactions on other conspecific receivers in nightingales. Animal Behaviour, 54, 1535–1543. Naguib, M., Fichtel, C. & Todt, D. 1999. Nightingales respond more strongly to vocal leaders of simulated dyadic interactions. Proceedings of the Royal Society of London, Series B, 266, 537–542. Otter, K., McGregor, P. K., Terry, A. M. R., Burford, F. R. L., Peake, T. M. & Dabelsteen, T. 1999. Do female great tits Parus
167
168
ANIMAL BEHAVIOUR, 69, 1
major assess males by eavesdropping? A field study using interactive playback. Proceedings of the Royal Society of London, Series B, 266, 1305–1309. Peake, T. M., Terry, A. M. R., McGregor, P. K. & Dabelsteen, T. 2001. Male great tits eavesdrop on simulated male-to-male vocal interactions. Proceedings of the Royal Society of London, Series B, 268, 1183–1187. Peake, T. M., Terry, A. M. R., McGregor, P. K. & Dabelsteen, T. 2002. Do great tits assess rivals by combining direct experience with information gathered by eavesdropping? Proceedings of the Royal Society of London, Series B, 269, 1925–1929. Pedersen, S. B. 1998. Preliminary Operation Manual for Signal Processor SIGPRO. Odense: Centre for Sound Communication, Odense University. Pizzari, T. 2001. Indirect partner choice through manipulation of male behaviour by female fowl, Gallus gallus domesticus. Proceedings of the Royal Society of London, Series B, 268, 181–186. Ritchison, G. 1995. Characteristics, use and possible functions of the perch songs and chatter calls of male common yellowthroats. Condor, 97, 27–38. Sæther, S. A., Fiske, P. & Ka˚la˚s, J. A. 1999. Pushy males and choosy females: courtship disruption and mate choice in the lekking great
snipe. Proceedings of the Royal Society of London, Series B, 266, 1227–1234. Searcy, W. A. & Yasukawa, K. 1990. Use of the song repertoire in intersexual contexts by male red-winged blackbirds. Behavioral Ecology and Sociobiology, 27, 123–128. Sell, H. & Odderskær, P. 1990. Tornsangerens ynglebiologi i danske læhegn. Dansk Ornithologisk Forenings Tidsskrift, 84, 21–29. Siegel, S. & Castellan, N. J., Jr. 1988. Nonparametric Statistics for Behavioral Sciences. 2nd edn. New York: McGraw-Hill. Snow, D. W. 1958. A Study of Blackbirds. London: British Museum (Natural History). Titus, R. C. 1998. Short-range and long-range songs: use of two acoustically distinct song classes by dark-eyed juncos. Auk, 115, 386–393. Tobias, J. A. & Seddon, N. 2002. Female begging in European robins: do neighbours eavesdrop for extra pair copulations? Behavioral Ecology, 13, 637–642. Trail, P. W. 1985. Courtship disruption modifies mate choice in a lek-breeding bird. Science, 227, 778–780. Trail, P. W. & Koutnik, D. L. 1986. Courtship disruption at the lek in the Guianan cock-of-the-rock. Ethology, 73, 197–218. Wiley, R. H. & Poston, J. 1996. Indirect mate choice, competition for mates, and coevolution of the sexes. Evolution, 50, 1371–1381.