J Ornithol (2009) 150:569–576 DOI 10.1007/s10336-009-0384-4
ORIGINAL ARTICLE
Adjustment of incubation according to the threat posed: a further signal of enemy recognition in the Blackcap Sylvia atricapilla? Milica Pozˇgayova´ Æ Petr Procha´zka Æ Marcel Honza
Received: 10 April 2008 / Revised: 11 November 2008 / Accepted: 9 January 2009 / Published online: 13 February 2009 Ó Dt. Ornithologen-Gesellschaft e.V. 2009
Abstract Nest predation and brood parasitism are costly for nest owners, and natural selection should therefore favour the evolution of parental counterdefences. We addressed the question of whether Blackcaps Sylvia atricapilla change their incubation behaviour in response to various nest intruders and whether this adjustment matches the intensity of mobbing exhibited towards these intruders. Near focal nests, we successively exposed a dummy of a brood parasite, nest predator and an innocuous species. After the parents had responded, we removed the dummy and filmed their incubation. The most aggressive response towards the Common Cuckoo Cuculus canorus and high nest attendance after its disappearance indicated recognition of the brood parasite. Low-intensity response to the Jay Garrulus glandarius, together with reduced subsequent parental care, suggested that Blackcaps perceived it either as less deleterious at the egg stage than the Cuckoo or as a danger to themselves. Almost no aggression towards the Turtle Dove Streptopelia turtur, along with the resumption of incubation after its removal, implied that Blackcaps recognised it as harmless. In addition, we found that the level of aggression positively correlated with nest attendance, suggesting a link between the intensity of
Communicated by T. Friedl. M. Pozˇgayova´ (&) P. Procha´zka M. Honza Department of Avian Ecology, Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, v.v.i., Kveˇtna´ 8, 60365 Brno, Czech Republic e-mail:
[email protected] M. Pozˇgayova´ Institute of Botany and Zoology, Faculty of Science, Masaryk University, Kotla´rˇska´ 2, 61137 Brno, Czech Republic
mobbing and subsequent parental care. Altogether, our results demonstrate that the issue of enemy recognition may be viewed as a complex of both aggressive and postpresentation behaviours. Keywords Aggression Brood parasitism Nest attendance Nest defence Nest predation
Introduction Predation and brood parasitism are important causes of nest failures in birds (Rothstein 1990; Ricklefs 2000) and therefore act as strong selective agents responsible for the evolution of nest defence. In a particular breeding attempt, the consequences of nest predation and brood parasitism may be rather similar, because both often lead to a nesting success close to 0 (Øien et al. 1998; Schmidt and Whelan 1999). However, after nest depredation, parents may still have enough time to renest and produce some offspring in a given breeding season. After a successful act of parasitism, hosts often lose all their progeny. Furthermore, they are forced to foster a parasitic young for a prolonged period, which precludes their further reproduction. In addition, some brood parasites are also known as predators of host eggs and/or nestlings (Ga¨rtner 1981; Soler et al. 1995; Clotfelter and Yasukawa 1999). In such cases, and in host populations under heavy rates of parasitism, brood parasites may affect host breeding success as much as or even more than nest predators, thus imposing strong selective force on host defences (Rothstein 1990; Baraba´s et al. 2004). Generally, it is assumed that nest defence is beneficial for the defender’s reproductive success, but it may also represent costs for future parental survival in terms of reduced foraging time and extra energy expenditure
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(Komdeur and Kats 1999), risks of injury or even death (McLean 1987; Sordahl 1990). On the other hand, aggressive behaviour may attract further enemies (Martin et al. 2000; Banks and Martin 2001) and operate as a nest location cue for an intruder (Uyehara and Narins 1995; Gill et al. 1997; Krams et al. 2007). Therefore, the intensity of defence in a given situation should be optimised according to the balance between these costs and benefits (Montgomerie and Weatherhead 1988). Studies on adaptive significance of enemy recognition have shown that nest defence would be far more effective if parents were able to differentiate among threats (e.g. McLean and Rhodes 1991). Moreover, birds may respond appropriately not only during direct encounter with an intruder, but also after its disappearance—by adjusting their further incubation behaviour according to the threat posed. In this context, increased nest attendance may be viewed as nest guarding, because it enables quicker responses towards various stimuli (Davies et al. 2003). The sight of a brood parasite, for example, may put hosts on alert and lead to increased nest attendance (Davies et al. 2003), which may, in turn, significantly promote the probability of egg rejection (Moksnes et al. 2000; Ba´rtol et al. 2002). Checking the nest contents by parents may facilitate spotting of damaged eggs, rapid removal of which has been shown to be highly adaptive for survival chances of the remaining clutch (Sealy and Neudorf 1995). Moreover, only recently, M. Honza et al. (in preparation) found that a high proportion of time spent nest checking significantly accelerates the ejection of a parasitic egg. Therefore, specific aggression combined with high levels of nest attendance may increase the effectiveness of nest defence and, in this way, some hosts may successfully deter nest predators or escape brood parasitism (Arcese and Smith 1988; Mermoz and Ferna´ndez 1999). In this study, we investigated whether parents adjust their nest attendance in response to the intruder type, and if such changes are in accordance with specific enemy recognition demonstrated during dummy experiments. We tested the Blackcap Sylvia atricapilla, since it exhibits high aggression towards the Common Cuckoo Cuculus canorus, hereafter Cuckoo, and perceives it as a specific threat (Moksnes et al. 1991; Røskaft et al. 2002; Grim 2005). The retention of Cuckoo-specific aggression (together with high egg rejection rates; e.g. Moksnes and Røskaft 1992; Honza et al. 2004b) from the past when the species was commonly parasitised (Moksnes and Røskaft 1995; Honza et al. 2001) is therefore the most likely explanation why it is currently parasitised only rarely (Benecke 1982; Berthold et al. 1995). Moreover, Blackcaps suffer from high nest predation (Weidinger 2000; Remesˇ 2003), and the Jay Garrulus glandarius is the
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major avian predator of their nests (Schaefer 2004; Weidinger 2006). Because of the diverse risks posed by various intruders, parents should respond specifically to the type of the threat presented. As nest defence may be viewed as a complex, we further hypothesised that there should be a relationship between the intensity of mobbing and subsequent nest attendance. Assuming Blackcaps’ enemy recognition abilities and the fact that Cuckoo parasitism is most dangerous in the egg stage, we predicted the most aggressive responses towards the Cuckoo dummy and the most intense nest attendance after its disappearance. As the intensity of reactions towards nest predators increases progressively with the breeding attempt and culminates shortly before nestlings fledge (Pavel and Buresˇ 2001; Fisher et al. 2004; Pavel 2006), we predicted low-intensity response towards the Jay (however, more pronounced than towards the control). Because the Jay may be perceived as dangerous to the parents (Duckworth 1991; Buresˇ and Pavel 2003), we expected a lower nest attendance after the Jay presentation than after the control. Finally, because of higher proportion of incubation in female Blackcaps (Bairlein 1978; Honza et al. 2007), we predicted quicker and more intense responses towards the dummies in females than in males.
Methods Study site and experimental procedures We conducted the field work from 25 April to 25 May 2006 in a deciduous forest near Dolnı´ Bojanovice (48°510 N, 17°020 E), Czech Republic. The nesting Blackcaps were successively presented with taxidermic mounts of three avian intruders in a random order: Cuckoo, Jay and Turtle Dove (Streptopelia turtur; hereafter Dove), the last one as a control. M.P. attached the mount to the shrubs 0.5–1 m from the nest, retreated to an approximately 20-m-distance vegetation cover and timed the birds’ latency to the first arrival (in seconds). The mobbing behaviour was then observed for 5 min or until a direct contact attack on the dummy, when it was withdrawn to avoid its destruction. After dummy removal, the incubation behaviour of the nest owners was filmed for 90 min using a Sony DCRTRV125E or DCR-TRV320E video camera mounted on a tripod, sheltered and camouflaged by foliaged twigs, and placed 5–10 m from the nest. After that period, M.P. returned to the nest to present the next mount. Before the first dummy experiment, the nest owners were habituated to the camera set-up for 1.5 h. Experiments were done within 3 days after the clutch completion and each nest contained four or five eggs.
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Variables and statistical analyses During dummy presentations, Blackcaps uttered several well distinguishable types of calls (reviewed in Cramp 1992). The most common call was the hard scolding ‘tak’ (it sounded like two pebbles struck together) which was rapidly repeated when the birds were excited or alarmed. In high-intensity alarm, the tak-call became a very rapid rhythmic series, e.g. ‘te´tte´tt’ or ‘tette´rett’. The variability in alarm calling during the dummy experiments enabled us to record the intensity of vocalisation on a scale (0—no vocalisation, 1—tak-calls, 2—high-intensity alarm, 3—takcalls and high-intensity alarm). Furthermore, we recorded the intensity of behaviour: 0—no reaction, 1—watching from distance, 2—approaching (hopping on twigs progressively towards the dummy), 3—very close passes with flight-overs, diving or hovering but without contact attacks, 4—contact attacks. For the ordinal characteristics (vocalisation and behaviour) the maximum value on the scale observed during each dummy test was taken into account. If both parents reacted, we summed the scores obtained for each parent. Additionally, we recorded the minimum distance from the dummy (in metres) and latency to the first arrival (in seconds) for each parent. If both parents reacted, the lower values for the minimum distance and latency were used in the analysis. From the videotapes, we extracted the latency of the first arriving bird (female/male) and for each mate the latency to the first sitting (in seconds), percentage of the time spent on the nest (from each 90-min filming period) and the time spent nest checking (in seconds). Nest checking was clearly identifiable: the parent stood in the nest or on the nest rim looking into the nest and/or turning the eggs (see also Moksnes et al. 1993 for the definition). For the analysis of overall post-presentation behaviour, time variables of both parents were summarised and the shorter latency was taken into account. For sex-specific analyses of incubation behaviour, the male/female latencies to the first arrival were not taken into account, because these are not mutually independent (i.e. the first arriving parent starts incubation and thus causes the delay in arrival of the alternating parent). We recorded mobbing behaviour at 17 nests and in 15 of them we also succeeded in filming nest attendance after dummy removals. In general, we carried out principal component analysis (PCA) of (1) aggressive behaviour during dummy experiments, and (2) post-presentation nest attendance. Because some of the behavioural characteristics obtained during dummy presentations were measured as categories on ordinal scales (vocalisation, behaviour), for the first data set we applied a more adequate variant of PCA, i.e. categorical PCA (CATPCA). Both CATPCA and PCA were computed in SPSS 15.0.
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For further analyses, we selected and presented only principal components complying with Kaiser’s criterion (eigenvalue [1). Blackcap behaviour towards the dummies was best expressed by CATPC1 (65% of the total variance; Table 1), which represented the overall aggression of both parents. The sex-specific CATPC1 for females explained 92% of variance and expressed aggression, while CATPC1 in males explained 62% of variance and represented nonaggression (Table 1). Blackcap post-presentation behaviour was best expressed by PC1 (65% of the total variance; Table 1), which represented overall nest attendance. In females, it explained 60% of variance and represented nest attendance, while in males it explained 83% of variance and expressed absence from the nest (Table 1). The component scores (CATPC1 or PC1) and individual behavioural characteristics were compared using Friedman ANOVA and nonparametric Wilcoxon matched pairs test (the latter used also as post hoc tests). All these further analyses and Spearman rank correlations were computed in Statistica 8.0.
Results Blackcap overall aggression differed significantly in intensity with respect to the dummy type (Fig. 1). Sexspecific aggression to the three intruders differed significantly in females (Friedman ANOVA: v22,17 = 13.45, P = 0.001; Wilcoxon matched pairs tests Cuckoo vs Dove: Z = 1.76, P = 0.078; Cuckoo vs Jay: Z = 2.86, P = 0.004; Dove vs Jay: Z = 1.44, P = 0.149), however, Table 1 Blackcap Sylvia atricapilla overall and sex-specific aggression/nest attendance Variable
Overall aggression
M nonaggression
F aggression
Vocalisation
0.64
-0.91
Behaviour
0.93
-0.98
0.89
Minimum distance
-0.78
0.97
-0.87
Latency to 1st arrival
-0.73
0.97
-0.63
Number of birds reacting Percentage of total variance
0.91 64.89 Overall attendance
–
0.72
–
91.63 M absence
61.55 F attendance
Latency to 1st arrival
-0.86
–
Latency to 1st sitting
-0.86
0.86
-0.81
–
Percentage of time on nest Time spent checking
0.90 0.57
-0.96 -0.91
0.86 0.64
Percentage of total variance
65.37
83.02
60.27
CATPC1 and PC1 loadings, % of total explained variance are given M male, F female
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J Ornithol (2009) 150:569–576 1.0
1.0 P = 0.005
0.8 P = 0.013
0.6
P = 0.140
P = 0.011
0.6
P = 0.463
0.4
Nest attendance
0.4
Aggression
P = 0.233
0.8
0.2 0.0 -0.2 -0.4
0.2 0.0 -0.2 -0.4
-0.6
-0.6
-0.8
-0.8
-1.0
-1.0 -1.2
-1.2 Cuckoo
Dove
Cuckoo
Jay
Dove
Jay
Fig. 1 Blackcap Sylvia atricapilla overall aggression (CATPC1 scores) towards the three dummies (Friedman ANOVA: v22,17 = 14.00, P = 0.001; mean, SE, 1.96 9 SE, significance of post hoc tests given)
Fig. 2 Blackcap overall nest attendance (PC1 scores) after dummy presentations (Friedman ANOVA: v22,15 = 8.93, P = 0.011; mean, SE, 1.96 9 SE, significance of post hoc tests given)
in males the difference was not significant at all (Friedman ANOVA: v22,17 = 0.93, P = 0.629). Moreover, in all dummy experiments, females were more responsive than males (Table 2) and in 35 of 51 (68.6%) cases they responded as the first. Blackcaps significantly differed in their overall nest attendance with respect to the dummy (Fig. 2). The overall time the parents spent nest checking did not significantly differ among the three mounts (v22,15 = 3.29, P = 0.193); however, the latency to the first arrival differed significantly (v22,15 = 17.19, P = 0.001). It was longest after the Jay dummy removal (Cuckoo vs Jay: Z = 3.29, P = 0.001, n1,2 = 15 and Dove vs Jay: Z = 3.29, P = 0.001, n1,2 = 15, respectively), but did not differ between the Cuckoo and Dove (Z = 0.09, P = 0.925, n1,2 = 15). Neither the females nor the males differed significantly in their nest attendance in response to the three mounts (males: v22,15 = 1.13, P = 0.569; females: v22,15 = 4.13, P = 0.127). Females were significantly more attentive than males, but only after the Dove presentation (Z = 2.44, P = 0.015), while after the Cuckoo and Jay presentation the nest attendance did not differ between the mates
(Z = 0.34, P = 0.733 and Z = 0.06, P = 0.955, respectively). Overall and female aggression towards the Cuckoo positively correlated with subsequent nest attendance, while male non-aggression correlated positively with their absence from the nest (Table 3). The latency to the first sitting decreased with overall aggression, while time spent nest checking marginally significantly increased with aggression. Female aggression marginally significantly correlated with the time spent on the nest. Male nonaggression positively correlated with the latency to the first sitting and negatively with the time spent on the nest and checking. In addition to the responses towards the Cuckoo, the overall latency to the first arrival decreased with aggression to the Dove (Table 3).
Table 2 Sex differences in mobbing behaviour Variable
Cuckoo
Dove
Jay
Vocalisation
2.29 (0.022)
2.67 (0.005)
1.89 (0.033)
Behaviour
2.31 (0.012)
2.31 (0.013)
2.67 (0.005)
Minimum distance
3.01 (0.002)
2.71 (0.007)
3.06 (0.002)
Latency to 1st arrival
3.05 (0.002)
2.60 (0.006)
2.90 (0.003)
Wilcoxon matched pairs tests: Z and (P) given; n1,2 = 17 for each dummy; females—more responsive
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Discussion Blackcaps showed the highest level of aggression towards the Cuckoo dummy (Fig. 1). This is in accordance with Grim’s (2005) finding that this suitable host recognises the Cuckoo as a specific threat despite the current lack of parasitism. Nevertheless, it is theoretically assumed that when the host is no longer under selection pressure from the brood parasite, it should respond to it as to other nest intruders (generalised response; Rothstein 1990). Thus, high and directed Blackcap aggression towards the Cuckoo may be plausibly explained as a relic behaviour from the past when this species was commonly parasitised. Such counteradaptation may be retained in a host population for long periods because its adaptive value is close to neutral. The scenario has been suggested by Rothstein (2001) for the maintenance of egg recognition abilities in the absence
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Table 3 Spearman rank correlations of aggression (CATPC1 scores) with post-presentation behaviour Variable
Overall
Male
Cuckoo
Dove
Jay
Latency to 1st arrival
-0.41 (0.132)
-0.55 (0.036)
Latency to 1st sitting
-0.78 (0.001)
Percentage of time on nest
Female
Cuckoo
Dove
Jay
-0.30 (0.274)
–
–
-0.24 (0.380)
-0.31 (0.255)
0.78 (0.001)
0.15 (0.589)
0.26 (0.357)
-0.37 (0.170)
-0.16 (0.562)
0.25 (0.374)
0.44 (0.105)
-0.02 (0.934)
0.45 (0.096)
-0.56 (0.030)
0.19 (0.503)
-0.48 (0.068)
0.50 (0.058)
-0.14 (0.610)
0.02 (0.955)
Time spent checking
0.50 (0.056)
0.18 (0.532)
-0.21 (0.462)
-0.56 (0.030)
0.39 (0.149)
-0.44 (0.098)
0.41 (0.131)
0.24 (0.386)
-0.03 (0.904)
PC1 (attendance)
0.63 (0.011)
0.34 (0.221)
0.43 (0.109)
0.55 (0.034)
-0.30 (0.274)
0.45 (0.094)
0.62 (0.014)
0.07 (0.805)
-0.13 (0.652)
–
Cuckoo –
Dove –
Jay –
rs and P given; n = 15 for each dummy; significant values are in bold
of brood parasitism and, by analogy, we propose the same for the maintenance of the nest defence behaviour. Aggressiveness together with high rejection rates of foreign eggs may then prevent Cuckoos from re-colonising the Blackcap as a host (see also Lova´szi and Moska´t 2004). In comparison with the highest Blackcap aggression towards the Cuckoo, its nest attendance after the Cuckoo removal was intermediate and did not significantly differ from that exhibited after the Jay or Dove presentation (Fig. 2). Moreover, tested birds did not spend more time nest checking after their encounter with the Cuckoo than after their encounters with the other two intruders. Similarly, Honza et al. (2004a) found that Reed Warblers Acrocephalus scirpaceus in a regularly parasitised population in the same area did not change their incubation behaviour after Cuckoo dummy withdrawal. However, Reed Warblers did not recognise the Cuckoo as a specific threat, because they responded to it similarly weakly as to the control (Honza et al. 2004a). Furthermore, Moksnes et al. (1993) found that Meadow Pipits Anthus pratensis that were exposed to a dummy Cuckoo beside their nests did not show any specific change in subsequent nest attendance: birds confronted with the Cuckoo spent the same amount of time incubating as those that were not presented with it. Distributions of the time spent nest checking and preening were also similar (Moksnes et al. 1993). The apparent absence of an obvious threat-specific change in post-presentation behaviour, however, need not necessarily imply weak recognition abilities, because incubation may physically block a parasite’s access to the host eggs and thus work as nest protection. Such behaviour (immediate settling on eggs) as a specific response towards a brood parasite has been described in the Yellow Warbler Dendroica petechia. The species recognises the threat of being parasitised and evolved this ‘nest-protection behaviour’ perhaps because other commonly used nest defences may be insufficient to deter the parasite (Hobson and Sealy
1989; Gill and Sealy 1996). As Cuckoos are known to make several inspection visits to the host’s nests before parasitic laying, or partially predate them (Honza et al. 2002), nest attendance could serve as an adaptation against such repeated visits. The sight of a Cuckoo may put hosts on alert for parasitism, increase nest attendance and lead to increased egg rejection and, in turn, increased attendance may enable quicker spotting of the Cuckoo (Davies et al. 2003). Although not significantly higher than after the Dove presentation, nest attendance after Cuckoo removal may still represent nest guarding, because Blackcaps recognised the Cuckoo as a specific threat in the dummy experiments. Furthermore, returning to the nest as soon as possible and continuing with incubation may significantly enhance survival chances of a clutch in terms of the ‘harm to offspring’ hypothesis, which states that parental investment is related to the harm that offspring would suffer during the period of no parental care (Dale et al. 1996). Contrary to intense Blackcap responses towards the Cuckoo, its aggression towards the Jay and Dove was of lower intensity and did not differ significantly from one another (Fig. 1). However, the nest owners were more silent when confronted with the Jay compared to the Dove (Wilcoxon matched pairs test: Z = 2.27, P = 0.023, n1,2 = 17), while in three cases during the Dove presentation they even resumed incubation. Moreover, after the Jay disappeared, the birds were less attentive (in comparison to the Dove; Fig. 2) and significantly delayed their first arrival (in comparison to the other two dummies). As the responses towards nest predators increase with the time and culminate shortly before nestlings fledge (Fisher et al. 2004; Pavel 2006), Blackcaps may perceive the Jay as a more serious threat to their young than to their eggs. Alternatively, we suggest that the birds may have been wary of the Jay, because they can perceive it as dangerous to themselves (for similar explanation of parental responses towards the Jay, see Duckworth 1991; Buresˇ and Pavel
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2003; Davies et al. 2003). This explanation is supported by the longer latency to arrival after the Jay presentation compared both to the Cuckoo and the control. Exploring possible associations between parental nest defence exhibited during and after dummy presentations, we found that parents more aggressive towards the Cuckoo showed more pronounced nest attendance. The stronger the mobbing, the sooner the birds sat on the clutch and the more time they devoted to nest checking (Table 3). This may suggest that more aggressive individuals recognised the brood parasite as a specific threat and adjusted their subsequent nest-attendance behaviour accordingly. Likewise, Honza et al. (2004a) found that Reed Warblers which quickly responded towards the Cuckoo mount also quickly arrived at nests after its removal. Thus, it seems that some individuals are inherently more responsive to the Cuckoo than others, which may be connected to their personality (Hollander et al. 2008) and/or previous experience with nest intruders (e.g. Smith et al. 1984; Knight and Temple 1986). Hollander et al. (2008) found an association between avian personality and nest defence: more assertive Great Tits Parus major produced a higher rate of alarm calls towards a human intruder than less assertive. This may be also the case in our study. ‘Bolder’ Blackcaps may have been more aggressive towards the Cuckoo, and afterwards had shorter latency times and checked the clutch more. In addition, such individuals returned earlier to the nest after the Dove presentation. This demonstrates certain individual consistency in behavioural responses in the context of nest defence and brood care, pointing to the possible fitness consequences of variation in behavioural decisions. In all dummy experiments, female Blackcaps were more aggressive than males and, during the majority of presentations, they also responded first. In species with biparental care, both sexes are expected to defend the nest either equally (Nealen and Breitwisch 1997) or proportionately to the sex-specific costs and benefits, parental duties and/or experience with nest intruders (reviewed by Montgomerie and Weatherhead 1988). Female Blackcaps spend more time incubating in comparison to their mates (Bairlein 1978; Cramp 1992 and quotations therein) and therefore are more involved in rejection of parasitic eggs than males (Honza et al. 2007). By analogy, this may be the reason for the higher female aggressiveness documented in our study. However, as we tested nest owners only at the beginning of the incubation period, we cannot rule out greater male investment or even sex role reversal in nest defence later in the course of the nesting cycle (Rytko¨nen et al. 1993; Hogstad 2005). Instead of conducting only dummy experiments, we have broadened the common view of nest defence and enemy recognition. We propose the nest defence to be a complex behaviour exhibited both during encounters with
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various intruders and carried-over after their disappearance. For nest owners, it may be therefore vital to adjust not only their aggression, but also the subsequent incubation according to the threat posed. Thus, both aggressive and nest-attendance behaviours could have substantial fitness consequences for parents.
Zusammenfassung Anpassung des Brutverhaltens in Abha¨ngigkeit von einer akuten Gefahr: ein weiterer Hinweis auf Feinderkennung bei der Mo¨nchsgrasmu¨cke? Nestpra¨dation und Brutparasitismus stellen Kosten fu¨r die Inhaber eines Nestes dar und daher sollte die natu¨rliche Selektion die Entwicklung von elterlichen Gegenmaßnahmen bevorzugen. Wir untersuchten die Frage, ob Mo¨nchsgrasmu¨cken (Sylvia atricapilla) ihr Brutverhalten als Antwort auf verschiedene Eindringlinge a¨ndern, und ob ¨ nderung zur Intensita¨t des Hassens auf den Eindiese A dringling passt. In der Na¨he der untersuchten Nester pra¨sentierten wir nacheinander Attrappen von Brutparasiten, Nestpra¨datoren und einer harmlosen Art. Nach der Reaktion der Elternvo¨gel entfernten wir die Attrappen und filmten deren Brutverhalten. Die heftigste Reaktion gegenu¨ber dem Kuckuck (Cuculus canorus) und eine folgende stetige Anwesenheit am Nest wiesen auf die Erkennung des Brutparasiten hin. Eine Antwort geringer Intensita¨t auf Eichelha¨her (Garrulus glandarius) zusammen mit einer nachfolgend verringerten elterlichen Sorge legen nahe, dass Mo¨nchsgrasmu¨cken Eichelha¨her entweder als weniger scha¨dlich fu¨r die Eier ansahen als den Kuckuck oder ihn als Gefahr fu¨r sich selbst einstuften. So gut wie keine Aggression gegenu¨ber der Turteltaube (Streptopelia turtur) und eine sofortige Wiederaufnahme des Brutgescha¨fts nach ihrer Entfernung legen nahe, dass Mo¨nchsgrasmu¨cken sie als harmlos erkannten. Daru¨ber hinaus fanden wir, dass das Maß der Aggression positiv korrelierte mit der Anwesenheit am Nest, was fu¨r einen Zusammenhang spricht zwischen der Sta¨rke des Hassens und der darauf folgenden elterlichen Sorge am Nest. Zusammengenommen zeigen unsere Ergebnisse, dass das Feld der Feinderkennung als ein Komplex gesehen werden ko¨nnte aus dem Aggressionsverhalten gegenu¨ber dem Feind und dem darauf folgenden Verhalten. Acknowledgments We are indebted to T. Grim, I. Krams, V. Sˇicha and anonymous referees for their helpful comments on earlier versions of the manuscript. Experiments were conducted following the ASCR Animal Care Protocol (licence number 0008/98-M103) and complied with the current Czech Law on the Protection of Animals against Mistreatment. The study was supported by GAAV (A600930605), GACˇR (524/05/H536) and MSM (LC06073).
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References Arcese P, Smith JNM (1988) Effects of population density and supplemental food on reproduction in song sparrows. J Anim Ecol 57:119–136 ¨ ber die Biologie einer su¨dwestdeutschen PopuBairlein F (1978) U lation der Mo¨nchsgrasmu¨cke (Sylvia atricapilla). J Ornithol 118:14–51 Banks AJ, Martin TE (2001) Host activity and the risk of nest parasitism by brown-headed cowbirds. Behav Ecol 12:31–40 Baraba´s L, Gilicze B, Takasu F, Moska´t C (2004) Survival and antiparasite defense in a host metapopulation under heavy brood parasitism: a source-sink dynamic model. J Ethol 22:143–151 Ba´rtol I, Karcza Z, Moska´t C, Røskaft E, Kisbenedek T (2002) Responses of great reed warblers Acrocephalus arundinaceus to experimental brood parasitism: the effects of a cuckoo Cuculus canorus dummy and egg mimicry. J Avian Biol 33:420–425 Benecke HG (1982) Zur Bedeutung verschiedener Wirtsvogelarten fu¨r die Reproduktion des Kuckucks in der DDR. Falke 29:153–155 Berthold P, Fiedler W, Querner U (1995) Die Mo¨nchsgrasmu¨cke (Sylvia atricapilla) als Kuckucks (Cuculus canorus)-Wirt. Charadrius 31:11–17 Buresˇ S, Pavel V (2003) Do birds behave in order to avoid disclosing their nest site? Bird Study 50:73–77 Clotfelter ED, Yasukawa K (1999) Impact of brood parasitism of brown-headed cowbirds on red-winged blackbird reproductive success. Condor 101:105–114 Cramp S (1992) The birds of the Western Palearctic, vol VI. Warblers. Oxford University Press, Oxford Dale S, Gustavsen R, Slagsvold T (1996) Risk taking during parental care: a test of three hypotheses applied to the pied flycatcher. Behav Ecol Sociobiol 39:31–42 Davies NB, Butchart SHM, Burke TA, Chaline N, Stewart IRK (2003) Reed warblers guard against cuckoos and cuckoldry. Anim Behav 65:285–295 Duckworth JW (1991) Responses of breeding reed warblers Acrocephalus scirpaceus to mounts of sparrowhawk Accipiter nisus, cuckoo Cuculus canorus and jay Garrulus glandarius. Ibis 133:68–74 Fisher RJ, Poulin RG, Todd LD, Brigham RM (2004) Nest stage, wind speed, and air temperature affect the nest defence behaviours of burrowing owls. Can J Zool 82:707–713 Ga¨rtner K (1981) Das Wegnehmen von Wirtsvogeleiern durch den Kuckuck (Cuculus canorus). Ornithol Mitt 33:115–131 Gill SA, Sealy SG (1996) Nest defence by yellow warblers: recognition of a brood parasite and an avian nest predator. Behaviour 133:263–282 Gill SA, Grieef PM, Staib LM, Sealy SG (1997) Does nest defence deter or facilitate cowbird parasitism? A test of the nesting-cue hypothesis. Ethology 103:56–71 Grim T (2005) Host recognition of brood parasites: implications for methodology in studies of enemy recognition. Auk 122:530–543 Hobson KA, Sealy SG (1989) Responses of yellow warblers to the threat of cowbird parasitism. Anim Behav 38:510–519 Hogstad O (2005) Sex-differences in nest defence in fieldfares Turdus pilaris in relation to their size and physical condition. Ibis 147:375–380 Hollander FA, Van Overveld T, Tokka I, Matthysen E (2008) Personality and nest defence in the great tit (Parus major). Ethology 114:405–412 Honza M, Moksnes A, Røskaft E, Stokke B (2001) How are different common cuckoo Cuculus canorus morphs maintained? An evaluation of different hypotheses. Ardea 89:341–352 Honza M, Taborsky B, Taborsky M, Teuschl Y, Vogl W, Moksnes A, Røskaft E (2002) Behaviour of female common cuckoos,
575 Cuculus canorus, in the vicinity of host nests before and during egg laying: a radiotelemetry study. Anim Behav 64:861–868 Honza M, Grim T, Cˇapek M, Moksnes A, Røskaft E (2004a) Nest defence, enemy recognition and nest inspection behaviour of experimentally parasitized reed warblers Acrocephalus scirpaceus. Bird Study 51:256–263 Honza M, Procha´zka P, Stokke BG, Moksnes A, Røskaft E, Cˇapek M, Mrlı´k V (2004b) Are blackcaps current winners in the evolutionary struggle against the common cuckoo? J Ethol 22:175– 180 Honza M, Pozˇgayova´ M, Procha´zka P, Tkadlec E (2007) Consistency in egg rejection behaviour: responses to repeated brood parasitism in the blackcap (Sylvia atricapilla). Ethology 113:344–351 Knight RL, Temple SA (1986) Why does intensity of avian nest defense increase during the nesting cycle? Auk 103:318–327 Komdeur J, Kats RKH (1999) Predation risk affects trade-off between nest guarding and foraging in Seychelles warblers. Behav Ecol 10:648–658 Krams I, Krama T, Igaune K, Ma¨nd R (2007) Long-lasting mobbing of the pied flycatcher increases the risk of nest predation. Behav Ecol 18:1082–1084 Lova´szi P, Moska´t C (2004) Break-down of arm race between the redbacked shrike (Lanius collurio) and the common cuckoo (Cuculus canorus). Behaviour 141:245–262 Martin TE, Scott J, Menge C (2000) Nest predation increases with parental activity: separating nest site and parental activity effects. Proc R Soc Lond B 267:2287–2293 McLean IG (1987) Response to a dangerous enemy: should a brood parasite be mobbed? Ethology 75:235–245 McLean IG, Rhodes G (1991) Enemy recognition and responses in birds. Curr Ornithol 8:173–211 Mermoz ME, Ferna´ndez GJ (1999) Low frequency of shiny cowbird parasitism on scarlet-headed blackbirds: anti-parasite adaptations or nonspecific host life-history traits? J Avian Biol 30:15–22 Moksnes A, Røskaft E (1992) Responses of some rare cuckoo hosts to mimetic model cuckoo eggs and to foreign conspecific eggs. Ornis Scand 23:17–23 Moksnes A, Røskaft E (1995) Egg-morphs and host preference in the common cuckoo (Cuculus canorus): an analysis of cuckoo and host eggs from European museum collections. J Zool 236:625–648 Moksnes A, Røskaft E, Braa AT, Korsnes L, Lampe HM, Pedersen HC (1991) Behavioural responses of potential hosts towards artificial cuckoo eggs and dummies. Behaviour 116:64–85 Moksnes A, Røskaft E, Korsnes L (1993) Rejection of cuckoo (Cuculus canorus) eggs by meadow pipits (Anthus pratensis). Behav Ecol 4:120–127 Moksnes A, Røskaft E, Hagen LG, Honza M, Mørk C, Olsen PH (2000) Common cuckoo Cuculus canorus and host behaviour at reed warbler Acrocephalus scirpaceus nests. Ibis 142:247–258 Montgomerie RD, Weatherhead PJ (1988) Risk and rewards of nest defence by parent birds. Q Rev Biol 63:167–187 Nealen PM, Breitwisch R (1997) Northern cardinal sexes defend nests equally. Wilson Bull 109:269–278 Øien IJ, Moksnes A, Røskaft E, Honza M (1998) Costs of cuckoo Cuculus canorus parasitism to reed warblers Acrocephalus scirpaceus. J Avian Biol 29:209–215 Pavel V (2006) When do altricial birds reach maximum of their brood defence intensity? J Ethol 24:175–179 Pavel V, Buresˇ S (2001) Offspring age and nest defence: test of the feedback hypothesis in the meadow pipit. Anim Behav 61:297–303 Remesˇ V (2003) Effects of exotic habitat on nesting success, territory density, and settlement patterns in the blackcap (Sylvia atricapilla). Conserv Biol 17:1127–1133 Ricklefs RE (2000) Density dependence, evolutionary optimization, and the diversification of avian life histories. Condor 102:9–22
123
576 Røskaft E, Moksnes A, Stokke BG, Bicˇ´ık V, Moska´t C (2002) Aggression to dummy cuckoos by potential European cuckoo hosts. Behaviour 139:613–628 Rothstein SI (1990) A model system for coevolution: avian brood parasitism. Annu Rev Ecol Syst 21:481–508 Rothstein SI (2001) Relic behaviours, coevolution and the retention versus loss of host defences after episodes of avian brood parasitism. Anim Behav 61:95–107 Rytko¨nen S, Orell M, Koivula K (1993) Sex-role reversal in willow tit nest defense. Behav Ecol Sociobiol 33:275–282 Schaefer T (2004) Video monitoring of shrub-nests reveals nest predators. Bird Study 51:170–177 Schmidt KA, Whelan C (1999) The relative impacts of nest predation and brood parasitism on seasonal fecundity in songbirds. Conserv Biol 13:46–57 Sealy SG, Neudorf DL (1995) Male northern orioles eject cowbird eggs: implications for the evolution of rejection behavior. Condor 97:369–375
123
J Ornithol (2009) 150:569–576 Smith JNM, Arcese P, McLean IG (1984) Age, experience, and enemy recognition by wild song sparrows. Behav Ecol Sociobiol 14:101–106 Soler M, Soler JJ, Martı´nez JG, Møller AP (1995) Magpie host manipulation by great spotted cuckoos: evidence for an avian mafia? Evolution 49:770–775 Sordahl TA (1990) The risks of avian mobbing and distraction behavior: an anecdotal review. Wilson Bull 102:349–352 Uyehara JC, Narins PM (1995) Nest defense by willow flycatchers to brood-parasitic intruders. Condor 97:361–368 Weidinger K (2000) The breeding performance of blackcap Sylvia atricapilla in two types of forest habitat. Ardea 88:225–233 Weidinger K (2006) Validating the use of temperature data loggers to measure survival of songbird nests. J Field Ornithol 77:357–364
