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Group effect in nest defence behaviour of breeding pied flycatchers, Ficedula hypoleuca
Animal Behaviour 77 (2009) 513–517
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Group effect in nest defence behaviour of breeding pied flycatchers, Ficedula hypoleuca rzinxsˇ a, Tatjana Krama b,1 Indrikis Krams a, *, Arnis Be a b
Institute of Systematic Biology, University of Daugavpils Institute of Life and Earth Sciences, University of Tartu
a r t i c l e i n f o Article history: Received 12 April 2008 Initial acceptance 19 June 2008 Final acceptance 13 November 2008 Published online 27 December 2008 MS. number: 08-00229 Keywords: antipredator behaviour Ficedula hypoleuca group effect mobbing pied flycatcher
Many group-living animals approach and mob nest predators, since grouping can increase the effectiveness of defence against predators. Some nonexperimental evidence shows that the intensity of harassment of predators increases with increasing mob size, indicating a group size effect for mobbing. In this field study we tested whether the intensity of mobbing depends on breeding group size in semicolonially breeding pied flycatchers. We recorded nest defence by parents when chicks were at least 8 days old and again 4 days later. When group size decreased naturally between the first and second trials, the intensity of mobbing a stuffed owl by the nest owners decreased. In contrast, when the number of neighbours remained unchanged the intensity of mobbing by nest owners increased significantly in the second trial. These results reveal the importance of group size in mobbing, indicating that the mobbing behaviour of the first individuals to mob is influenced by the presence of other mobbing conspecific individuals. Ó 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Prey individuals may cooperate to decrease the probability of being attacked because cooperating allows them to adapt their response to the changing risk of predation (Krause & Ruxton 2002; Caro 2005). Mobbing is an antipredator behaviour that occurs when prey individuals harass a predator by cooperatively attacking it, during which the predator is usually unable to attack the individual that initiated the mob (Wilson 1975). This communal defence has an adaptive value since mobbing assemblies often cause a predator to vacate its immediate foraging area so that prey individuals can decrease the risk to their offspring and resume their daily activities (Pettifor 1990; Flasskamp 1994). Mobbing behaviour is most frequently seen in birds (Curio 1978; McLean & Rhodes 1991; Naguib et al. 1999; Desrochers et al. 2002; Krams & Krama 2002; Maklakov 2002; Olendorf et al. 2004; Griesser & Ekman 2005; Templeton et al. 2005), although it is also known to occur in other social animals such as mammals, fish (Altmann 1956; Dominey 1983; Pitcher et al. 1986; Kirkwood & Dickie 2005; Solo´rzano-Filho 2006) and some invertebrates (Mori & Saito 2004; Ken et al. 2005). Several studies have demonstrated that larger groups of prey individuals are more effective at detecting approaching predators
* Correspondence: I. Krams, Institute of Systematic Biology, Daugavpils University, LV-5401 Daugavpils, Latvia. E-mail address: [email protected] (I. Krams). 1 T. Krama is currently at the Institute of Systematic Biology, Daugavpils University, LV-5401 Daugavpils, Latvia.
(Pulliam 1973; Godin et al. 1988; Cresswell 1994). Safety in numbers is another important benefit of antipredator grouping (Krause & Ruxton 2002; Caro 2005): an individual stands little chance against a larger predator, but when a group is involved, the risk to each group member may be reduced or diluted (Curio 1978; Krause & Ruxton 2002; Caro 2005). The dilution effect proposed by Hamilton (1971) is a way of explaining the benefits of cooperation by selfish individuals. In addition, members of larger groups have more chances of confusing the predator when they behave similarly in an unpredictable way (Hoogland & Sherman 1976; Owens & Goss-Custard 1976; Driver & Humphries 1988). In natural populations of birds, individual fitness depends on the number of their offspring at fledging. Pairs producing more fledglings have a better chance of recruiting offspring as future breeders in the local population (Alatalo & Lundberg 1986; Linde´n et al. 1992). By cooperating to drive away predators successfully, all individuals involved may increase their chances of survival and reproduction (Krams et al. 2006a, b, 2008). Some evidence suggests that the intensity of mobbing usually increases with decreasing distance of the predator from the offspring, which correlates with decreased predation success on them (Kruuk 1964). Mobbing individuals have a greater chance of driving the predator from the neighbourhood than those that are not mobbing (Pettifor 1990; Flasskamp 1994; Pavey & Smyth 1998; Zuberbu¨hler et al. 1999), in addition to reducing the chances of a future attack. Andersson & Wiklund (1978) found that an artificial nest placed near a colony of fieldfares, Turdus pilaris, was less likely to be preyed upon than one
0003-3472/$38.00 Ó 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.anbehav.2008.11.007
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placed beside a solitary active fieldfare nest. This was suggested to be the result of the effective predator mobbing by fieldfares which is more intense in colonies (Wiklund & Andersson 1994). All these nonexperimental data suggest a direct link between group size (Hoogland & Sherman 1976; Becker 1984; Robinson 1985; Mori & Saito 2004) and mobbing intensity which may result in successful expulsion of the predator; however, experimental evidence is still missing (but see Wiklund & Andersson 1994). If there is such a relationship, one may predict that, conversely, a decreased group size may lead to decreased offspring defence. Our aim in this study was to test whether the intensity of predator harassment of the first individuals to mob depends on the size of the group formed by neighbouring conspecifics. If no neighbours assist the initiators of mobbing, the lone harassers may be under an increased risk of predation by attracting the predator’s attention (Hoogland & Sherman 1976; Denson 1979; Curio & Regelmann 1985, 1986); therefore prey individuals in this situation should be selected to mob less. We studied the group size effect in breeding pied flycatchers while they mobbed predators in the presence of other breeding conspecifics, and when the offspring of neighbouring pied flycatchers fledged and the neighbouring adults had disappeared from the vicinity. If the dilution of risk is important in mobbing, one may predict that the intensity of mobbing will decrease as the group size of prey individuals decreases; therefore the first individual to mob should be aware of its social environment. METHODS slava, southThe field experiment was performed near Kra eastern Latvia, in June of 2007. To attract pied flycatchers we used wooden board nestboxes placed in young (25–50 years old) dry plantations of Scots pine, Pinus sylvestris, with a sparse understorey. They were arranged in pairs and placed 39–50 m apart. The distance between the neighbouring pairs of nestboxes was at least 350 m and sufficient not to attract other flycatchers from distant nestboxes to mobbing of owls. This arrangement of nestboxes was not unnatural, because pied flycatchers provided with nestboxes often breed semicolonially. During the nestling phase we presented a stuffed tawny owl, Strix aluco, as a predator near nestboxes occupied by pied flycatchers. The tawny owl is a common predator of birds in northern Europe whose presence strongly affects the behaviour of passerine birds (Bautista & Lane 2000). Our first inclusion criterion was that both nestboxes of a box pair were occupied by pied flycatchers. The age of nestlings was the next requirement for inclusion. We monitored egg and fledgling ages to identify box pairs where nestlings in one box were 1–2 days older than in the neighbouring box. The chicks of pied flycatchers fledge within 14–16 days of hatching (Lundberg & Alatalo 1992). Since parents are predicted to take higher risks while defending larger broods (e.g. Curio 1987; Lambrechts et al. 2000), we included in the study only nestboxes containing six nestlings, which was the average egg and nestling number in the study area in 2007. A total of 40 pairs of nestboxes (80 individual nestboxes) met the requirements. We assigned 20 pairs of nestboxes to the changed size group and another set of 20 pairs to the stable size group. We conducted the study within one breeding season since changing proximate constraints such as food availability or predator pressure may cause behavioural differences between years (Dale et al. 1996; Sasva´ri & Hegyi 1998; Lind & Cresswell 2005). We took advantage of natural variation and scheduled the trials so that the group size decreased from two pairs to one pair in the changed size group during the study, while the group size did not vary in the stable size group. In both groups the predator was placed near the nestbox of the youngest brood of a box pair. The first trial was performed when the offspring in the youngest brood were at least 8 days old (Bogliani et al. 1999). The trials were
repeated 4 days later so that chicks in the older broods of the changed size group had already left their nests while the chicks in the older broods of the stable size group were still in their nestboxes. By showing the predator only twice at each nestbox we reduced the risk of the free-living birds habituating to predators (Knight & Temple 1986a, b; Listøen et al. 2000). We observed and scored the mobbing behaviour of each individual bird in both pairs (i.e. four adults). Since the mobbing intensity of males and females was similar (Kruskal–Wallis test: H2 ¼ 2.00, P ¼ 0.546), we calculated the mean value and assigned it to each pair of adult pied flycatchers. Our scale of pied flycatcher mobbing response consisted of four categories of displays and vocalizations: (1) no response to the dummy predator (0 points): birds investigating the predator from a distance (>10 m) usually without alarm calls while continuing activities such as foraging or singing; (2) weak response (1 point): with frequent approaching and retreating to/from the predator within 5–10 m; (3) average response (2 points): birds close to the predator (3–5 m), and moving restlessly around it by bowing, pivoting, tail flicking or hovering in the air in front of it; and (4) strong response (3 points): intense movements and display close to the predator (0.5–3 m), including dive-attacks at the predator (Krams et al. 2008). Since the perches suitable for mobbing birds varied in distance from the predator at each location, we only scored behaviour and not the specific distance of a mobbing bird’s approach to the predator. Although we do not know whether our ranking system is linear in terms of risk and energy expenditure, it corresponds to the speciesspecific, step-by-step, increasing intensity of mobbing behaviour observed in several species under field conditions (Creutz 1955; Curio 1959, 1961a, b, 1975; Shalter 1978). During weak, average and strong responses, the pied flycatchers used a combination of ‘pik’ and ‘tck’ calls (Bergmann & Helb 1982). The predator was mounted on a small platform 1.2 m above the ground, between the two neighbouring nestboxes about 1.5 m from the younger brood nestbox and facing the nest. We observed and evaluated the behaviour of the adult pied flycatchers from a hide. The owl was installed when, to the best of our knowledge, no pied flycatcher was nearby. As soon as the owl was discovered we started documenting the mobbing response of the nest owners and their neighbours. After 10 min of mobbing we moved the decoy back into the hide. All manipulations were done from within the hide, concealing the observers from view. The trials were undertaken during the middle of the day (1100–1500 hours) in calm and dry weather. The adult flycatchers were not trapped or affected in any other way. They had marked themselves with nonwaterproof ink 1–4 days before the trials by touching a piece of ink-saturated foam-rubber while entering or leaving the entrance of their nestboxes. Hole-nesting birds were the most common avian species in the dry pine plantations. The density of the other passerines such as tree pipits, Anthus trivialis, crested tits, Lophophanes cristatus, willow tits, Poecile montanus, and chaffinches, Fringilla coelebs, was low. All of the heterospecific birds had fledglings at the time of the experimental trials and they sometimes attended mobbings during trials just for predator inspection from a distance. There could have been effects of heterospecific mobbing but we were not able to quantity these data and thus we can only speculate that the presence of the heterospecific individuals did not influence the behaviour of pied flycatchers. Statistical Analyses The data obtained allowed the use of parametric statistics for summed ranks. However, we used nonparametric tests because of the sampling procedure which was inexact and cannot be improved mathematically. We used Mann–Whitney U tests and Wilcoxon signed-ranks tests. All of the analyses were two tailed.
I. Krams et al. / Animal Behaviour 77 (2009) 513–517
Ethical Note We checked nestboxes to record clutch size and nestling age three to four times before the experimental trials. Since we checked the nestboxes mainly in the absence of adult birds, our activities did not cause any significant disturbance leading to desertion or abnormal behaviour. The study was approved by the Science Council of the Republic of Latvia. RESULTS In the changed size group the alarm intensity of parents of the younger nestlings was scored as ‘weak/average response’ ðX SD ¼ 1:80 0:62Þ during the first trials. In the stable size group the mobbing intensity of the parents of younger nestlings was also scored as ‘weak/average response’ ðX SD ¼ 1:65 0:67Þ during the first trials. The groups did not differ in alarm intensity (Mann–Whitney U test: U ¼ 173, N1 ¼ N2 ¼ 20, P ¼ 0.42). As soon as the offspring of neighbours fledged and abandoned their nestboxes, the parents of younger nestlings significantly decreased their intensity of mobbing from ‘weak/average’ to ‘weak response’ ðX SD ¼ 1:25 1:12Þ in the changed size group (Wilcoxon signed-ranks test: Z ¼ 2.08, N ¼ 20, P ¼ 0.038), whereas the intensity of nest defence increased from ‘weak’ to ‘strong response’ ðX SD ¼ 2:4 0:60Þ in the stable size group during the second trial (Z ¼ 3.26, N ¼ 20, P ¼ 0.01). The intensity of mobbing behaviour of the parents of younger nestlings was significantly different between changed and stable size groups during the second trials (Mann–Whitney U test: U ¼ 83.5, N1 ¼ N2 ¼ 20, P ¼ 0.001; Fig. 1). In the changed size group 19 neighbouring pairs arrived during the first trial to mob the tawny owl. In the stable size group 18 neighbouring pairs assisted the parents of younger nestlings during the first trial. During the second trials 17 pairs of pied flycatchers of the stable size group were assisted by their neighbours but none of the birds of the changed size group were assisted by neighbours since the neighbouring offspring had already fledged and the neighbouring adults had already left the area. DISCUSSION Theoretical models of life history evolution predict that the resolution to the parental dilemma whether to place their offspring at greater risk of mortality when under threat of predation instead of themselves will vary among species, depending on offspring
Strong response Weak response
Average response No response
Number of responses
20
10
0
First trial
Second trial
Stable size group
First trial
Second trial
Changed size group
Figure 1. The intensity of mobbing responses to a life-like tawny owl shown to breeding pied flycatchers with ‘younger’ nestlings during the first trial and a second trial 4 days later.
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number and the probability of survival for the parents (Trivers 1972; Dawkins & Carlisle 1976; Maynard Smith 1977; Andersson et al. 1981; Redondo 1989; Rytko¨nen & Soppela 1995). Many studies have documented a temporal increase in nest defence during the breeding cycle indicating that parents increase their fitness by investing more in older than younger offspring (Harvey & Greenwood 1978; Lazarus & Inglis 1986; Montgomerie & Weatherhead 1988; Redondo 1989; Clutton-Brock 1991; Onnebrink & Curio 1991; Rytko¨nen et al. 1995a, b; Halupka & Halupka 1997; Michl et al. 2000; Pavel & Buresˇ 2001; Rytko¨nen 2002). Our results show that this pattern might depend on specific circumstances. Parent pied flycatchers mobbed the stuffed owl equally intensely during the first trials in the stable size and the changed size groups. During the course of the breeding season, the parents of younger nestlings generally increased their mobbing intensity in the stable size group, while birds avoided taking greater risks (Zuk & Kolluru 1998; Krama & Krams 2005; Zuk et al. 2006; Krams et al. 2007) associated with nest defence in the changed size group at the end of the nesting cycle. These opposing changes in nest defence of the parent flycatchers were observed with the offspring number remaining constant in all the trials. Our approach was not to manipulate or control the presumed causal factor experimentally but to take advantage of natural variation in studying effects of group size on mobbing behaviour. Since we did not experimentally control the causal factor, our conclusions are limited and there might be other explanations for the effects of group size on the nest defence behaviour such as possible changes in hormone levels of adult pied flycatchers. Nest defence can be related to the elevated testosterone levels in males (Alonso-Alvarez & Velando 2001) which can increase in the presence of other potential mating partners such as neighbouring females. Therefore the intensity of nest defence of males in the changed size groups might be reduced in the absence of potential extrapair partners. However, such a hormone effect has not been revealed so far and this explanation is highly unlikely especially in the middle of the breeding season. In some earlier nonexperimental studies, mobbing has been shown to be more effective in larger groups of yellow-rumped caciques, Cacicus cela (Robinson 1985). Similar effects were demonstrated by Hoogland & Sherman (1976) for bank swallows, Riparia riparia. In these studies the more intense mobbing in larger groups could be a result of some self-reinforcement by some of the prey individuals. Our study suggests that the social context of nest defence in terms of the number of neighbours can have a significant effect on the intensity of predator mobbing by the initiator individuals. Although a single prey individual may take the risk to mob predators, mobbing is usually performed by a group. This study clearly shows that the first individuals to mob are aware of the presence of other conspecific mobbers in addition to their mate. While pied flycatchers increased the mobbing intensity between trials in the stable size group, the birds of the changed size group decreased their nest defence efforts from the first trial to the second trial as soon as their neighbours left the area. By assembling in a group, mobbers may protect themselves simply by virtue of selfishly dividing the risk as a sheer function of numbers (Hamilton 1971). The benefit of mobbing is obvious for the initiator, but not always for those it attracts since it is potentially dangerous. However, in our study the predator was always placed so that it affected both pairs of neighbouring flycatchers. Even though the predator was not placed near their nestbox, the neighbouring flycatchers were not able to feed offspring while the predator was present. Owing to the group size effect, the mobbing individuals increased the safety of their offspring by cooperating. As proposed by Curio (1963), the more intensely a predator is molested, the sooner it should leave an area. The ‘move-on’ hypothesis is supported by observational (Pettifor 1990; Pavey &
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Smyth 1998) and experimental (Flasskamp 1994) evidence of potential prey driving predators away. Our results show that a pair of flycatchers initiated weaker mobbing when left alone than when the neighbours were present. Why then did the birds decrease the intensity of mobbing? Curio (1963) also suggested that a predator could be equally affected not only by intense mobbing but also by longer harassment. A possible reason why parent flycatchers mobbed weakly is that intense long-lasting mobbing calls help acoustically oriented predators to locate the nests (Yasukawa 1989; Zuberbu¨hler et al. 1997, 1999; Zuk & Kolluru 1998; Krams 2001; Krama & Krams 2005; Bernal et al. 2006; Zuk et al. 2006; Krams et al. 2007). Thus, individuals engaging in mobbing behaviour that includes making calls may face a trade-off between the benefits of removing predators from the territory and the costs of attracting other predators (Krama & Krams 2005; Krams et al. 2007). In the case of weaker mobbing, predators could perceive these calls as detection notification signals (Bradbury & Vehrencamp 1998). Besides indicating to a stalking predator that it has been noticed, prey individuals giving the calls have an opportunity to silence offspring and warn conspecific and heterospecific neighbours (Curio 1978). In this way some mobbing goals may be achieved without attracting the attention of another predator. Theory predicts that the resolution to the parental dilemma may vary depending on offspring number, their quality, age and the probability of survival for parents (Maynard Smith 1977; Kokko & Jennions 2003). However, the empirical results are often equivocal (e.g. Rytko¨nen et al. 1995a, b; Rytko¨nen 2002). Our study reveals the role of the social environment in defending offspring which may be as important as offspring age. This is especially important because of recent census and monitoring techniques suggesting using playback of mobbing calls to census bird abundance (Hutto et al. 1986; Gunn et al. 2000; Turcotte & Desrochers 2002; Fichtel & Hammerschmidt 2003). Our results show that studies using this methodology should exercise caution in using mobbing calls for surveying birds since mobbing intensity does not always allow for direct insights into reproductive behaviour.
Acknowledgments We thank Gary Ramey, Mikus Abolin xsˇ-Abols and Inese Kivleniece for helpful comments on the manuscript. Funding for this project was provided by the Science Council of Latvia (07.2100).
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Group effect in nest defence behaviour of breeding pied flycatchers, Ficedula hypoleuca rzinxsˇ a, Tatjana Krama b,1 Indrikis Krams a, *, Arnis Be a b
Institute of Systematic Biology, University of Daugavpils Institute of Life and Earth Sciences, University of Tartu
a r t i c l e i n f o Article history: Received 12 April 2008 Initial acceptance 19 June 2008 Final acceptance 13 November 2008 Published online 27 December 2008 MS. number: 08-00229 Keywords: antipredator behaviour Ficedula hypoleuca group effect mobbing pied flycatcher
Many group-living animals approach and mob nest predators, since grouping can increase the effectiveness of defence against predators. Some nonexperimental evidence shows that the intensity of harassment of predators increases with increasing mob size, indicating a group size effect for mobbing. In this field study we tested whether the intensity of mobbing depends on breeding group size in semicolonially breeding pied flycatchers. We recorded nest defence by parents when chicks were at least 8 days old and again 4 days later. When group size decreased naturally between the first and second trials, the intensity of mobbing a stuffed owl by the nest owners decreased. In contrast, when the number of neighbours remained unchanged the intensity of mobbing by nest owners increased significantly in the second trial. These results reveal the importance of group size in mobbing, indicating that the mobbing behaviour of the first individuals to mob is influenced by the presence of other mobbing conspecific individuals. Ó 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Prey individuals may cooperate to decrease the probability of being attacked because cooperating allows them to adapt their response to the changing risk of predation (Krause & Ruxton 2002; Caro 2005). Mobbing is an antipredator behaviour that occurs when prey individuals harass a predator by cooperatively attacking it, during which the predator is usually unable to attack the individual that initiated the mob (Wilson 1975). This communal defence has an adaptive value since mobbing assemblies often cause a predator to vacate its immediate foraging area so that prey individuals can decrease the risk to their offspring and resume their daily activities (Pettifor 1990; Flasskamp 1994). Mobbing behaviour is most frequently seen in birds (Curio 1978; McLean & Rhodes 1991; Naguib et al. 1999; Desrochers et al. 2002; Krams & Krama 2002; Maklakov 2002; Olendorf et al. 2004; Griesser & Ekman 2005; Templeton et al. 2005), although it is also known to occur in other social animals such as mammals, fish (Altmann 1956; Dominey 1983; Pitcher et al. 1986; Kirkwood & Dickie 2005; Solo´rzano-Filho 2006) and some invertebrates (Mori & Saito 2004; Ken et al. 2005). Several studies have demonstrated that larger groups of prey individuals are more effective at detecting approaching predators
* Correspondence: I. Krams, Institute of Systematic Biology, Daugavpils University, LV-5401 Daugavpils, Latvia. E-mail address: [email protected] (I. Krams). 1 T. Krama is currently at the Institute of Systematic Biology, Daugavpils University, LV-5401 Daugavpils, Latvia.
(Pulliam 1973; Godin et al. 1988; Cresswell 1994). Safety in numbers is another important benefit of antipredator grouping (Krause & Ruxton 2002; Caro 2005): an individual stands little chance against a larger predator, but when a group is involved, the risk to each group member may be reduced or diluted (Curio 1978; Krause & Ruxton 2002; Caro 2005). The dilution effect proposed by Hamilton (1971) is a way of explaining the benefits of cooperation by selfish individuals. In addition, members of larger groups have more chances of confusing the predator when they behave similarly in an unpredictable way (Hoogland & Sherman 1976; Owens & Goss-Custard 1976; Driver & Humphries 1988). In natural populations of birds, individual fitness depends on the number of their offspring at fledging. Pairs producing more fledglings have a better chance of recruiting offspring as future breeders in the local population (Alatalo & Lundberg 1986; Linde´n et al. 1992). By cooperating to drive away predators successfully, all individuals involved may increase their chances of survival and reproduction (Krams et al. 2006a, b, 2008). Some evidence suggests that the intensity of mobbing usually increases with decreasing distance of the predator from the offspring, which correlates with decreased predation success on them (Kruuk 1964). Mobbing individuals have a greater chance of driving the predator from the neighbourhood than those that are not mobbing (Pettifor 1990; Flasskamp 1994; Pavey & Smyth 1998; Zuberbu¨hler et al. 1999), in addition to reducing the chances of a future attack. Andersson & Wiklund (1978) found that an artificial nest placed near a colony of fieldfares, Turdus pilaris, was less likely to be preyed upon than one
0003-3472/$38.00 Ó 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.anbehav.2008.11.007
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placed beside a solitary active fieldfare nest. This was suggested to be the result of the effective predator mobbing by fieldfares which is more intense in colonies (Wiklund & Andersson 1994). All these nonexperimental data suggest a direct link between group size (Hoogland & Sherman 1976; Becker 1984; Robinson 1985; Mori & Saito 2004) and mobbing intensity which may result in successful expulsion of the predator; however, experimental evidence is still missing (but see Wiklund & Andersson 1994). If there is such a relationship, one may predict that, conversely, a decreased group size may lead to decreased offspring defence. Our aim in this study was to test whether the intensity of predator harassment of the first individuals to mob depends on the size of the group formed by neighbouring conspecifics. If no neighbours assist the initiators of mobbing, the lone harassers may be under an increased risk of predation by attracting the predator’s attention (Hoogland & Sherman 1976; Denson 1979; Curio & Regelmann 1985, 1986); therefore prey individuals in this situation should be selected to mob less. We studied the group size effect in breeding pied flycatchers while they mobbed predators in the presence of other breeding conspecifics, and when the offspring of neighbouring pied flycatchers fledged and the neighbouring adults had disappeared from the vicinity. If the dilution of risk is important in mobbing, one may predict that the intensity of mobbing will decrease as the group size of prey individuals decreases; therefore the first individual to mob should be aware of its social environment. METHODS slava, southThe field experiment was performed near Kra eastern Latvia, in June of 2007. To attract pied flycatchers we used wooden board nestboxes placed in young (25–50 years old) dry plantations of Scots pine, Pinus sylvestris, with a sparse understorey. They were arranged in pairs and placed 39–50 m apart. The distance between the neighbouring pairs of nestboxes was at least 350 m and sufficient not to attract other flycatchers from distant nestboxes to mobbing of owls. This arrangement of nestboxes was not unnatural, because pied flycatchers provided with nestboxes often breed semicolonially. During the nestling phase we presented a stuffed tawny owl, Strix aluco, as a predator near nestboxes occupied by pied flycatchers. The tawny owl is a common predator of birds in northern Europe whose presence strongly affects the behaviour of passerine birds (Bautista & Lane 2000). Our first inclusion criterion was that both nestboxes of a box pair were occupied by pied flycatchers. The age of nestlings was the next requirement for inclusion. We monitored egg and fledgling ages to identify box pairs where nestlings in one box were 1–2 days older than in the neighbouring box. The chicks of pied flycatchers fledge within 14–16 days of hatching (Lundberg & Alatalo 1992). Since parents are predicted to take higher risks while defending larger broods (e.g. Curio 1987; Lambrechts et al. 2000), we included in the study only nestboxes containing six nestlings, which was the average egg and nestling number in the study area in 2007. A total of 40 pairs of nestboxes (80 individual nestboxes) met the requirements. We assigned 20 pairs of nestboxes to the changed size group and another set of 20 pairs to the stable size group. We conducted the study within one breeding season since changing proximate constraints such as food availability or predator pressure may cause behavioural differences between years (Dale et al. 1996; Sasva´ri & Hegyi 1998; Lind & Cresswell 2005). We took advantage of natural variation and scheduled the trials so that the group size decreased from two pairs to one pair in the changed size group during the study, while the group size did not vary in the stable size group. In both groups the predator was placed near the nestbox of the youngest brood of a box pair. The first trial was performed when the offspring in the youngest brood were at least 8 days old (Bogliani et al. 1999). The trials were
repeated 4 days later so that chicks in the older broods of the changed size group had already left their nests while the chicks in the older broods of the stable size group were still in their nestboxes. By showing the predator only twice at each nestbox we reduced the risk of the free-living birds habituating to predators (Knight & Temple 1986a, b; Listøen et al. 2000). We observed and scored the mobbing behaviour of each individual bird in both pairs (i.e. four adults). Since the mobbing intensity of males and females was similar (Kruskal–Wallis test: H2 ¼ 2.00, P ¼ 0.546), we calculated the mean value and assigned it to each pair of adult pied flycatchers. Our scale of pied flycatcher mobbing response consisted of four categories of displays and vocalizations: (1) no response to the dummy predator (0 points): birds investigating the predator from a distance (>10 m) usually without alarm calls while continuing activities such as foraging or singing; (2) weak response (1 point): with frequent approaching and retreating to/from the predator within 5–10 m; (3) average response (2 points): birds close to the predator (3–5 m), and moving restlessly around it by bowing, pivoting, tail flicking or hovering in the air in front of it; and (4) strong response (3 points): intense movements and display close to the predator (0.5–3 m), including dive-attacks at the predator (Krams et al. 2008). Since the perches suitable for mobbing birds varied in distance from the predator at each location, we only scored behaviour and not the specific distance of a mobbing bird’s approach to the predator. Although we do not know whether our ranking system is linear in terms of risk and energy expenditure, it corresponds to the speciesspecific, step-by-step, increasing intensity of mobbing behaviour observed in several species under field conditions (Creutz 1955; Curio 1959, 1961a, b, 1975; Shalter 1978). During weak, average and strong responses, the pied flycatchers used a combination of ‘pik’ and ‘tck’ calls (Bergmann & Helb 1982). The predator was mounted on a small platform 1.2 m above the ground, between the two neighbouring nestboxes about 1.5 m from the younger brood nestbox and facing the nest. We observed and evaluated the behaviour of the adult pied flycatchers from a hide. The owl was installed when, to the best of our knowledge, no pied flycatcher was nearby. As soon as the owl was discovered we started documenting the mobbing response of the nest owners and their neighbours. After 10 min of mobbing we moved the decoy back into the hide. All manipulations were done from within the hide, concealing the observers from view. The trials were undertaken during the middle of the day (1100–1500 hours) in calm and dry weather. The adult flycatchers were not trapped or affected in any other way. They had marked themselves with nonwaterproof ink 1–4 days before the trials by touching a piece of ink-saturated foam-rubber while entering or leaving the entrance of their nestboxes. Hole-nesting birds were the most common avian species in the dry pine plantations. The density of the other passerines such as tree pipits, Anthus trivialis, crested tits, Lophophanes cristatus, willow tits, Poecile montanus, and chaffinches, Fringilla coelebs, was low. All of the heterospecific birds had fledglings at the time of the experimental trials and they sometimes attended mobbings during trials just for predator inspection from a distance. There could have been effects of heterospecific mobbing but we were not able to quantity these data and thus we can only speculate that the presence of the heterospecific individuals did not influence the behaviour of pied flycatchers. Statistical Analyses The data obtained allowed the use of parametric statistics for summed ranks. However, we used nonparametric tests because of the sampling procedure which was inexact and cannot be improved mathematically. We used Mann–Whitney U tests and Wilcoxon signed-ranks tests. All of the analyses were two tailed.
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Ethical Note We checked nestboxes to record clutch size and nestling age three to four times before the experimental trials. Since we checked the nestboxes mainly in the absence of adult birds, our activities did not cause any significant disturbance leading to desertion or abnormal behaviour. The study was approved by the Science Council of the Republic of Latvia. RESULTS In the changed size group the alarm intensity of parents of the younger nestlings was scored as ‘weak/average response’ ðX SD ¼ 1:80 0:62Þ during the first trials. In the stable size group the mobbing intensity of the parents of younger nestlings was also scored as ‘weak/average response’ ðX SD ¼ 1:65 0:67Þ during the first trials. The groups did not differ in alarm intensity (Mann–Whitney U test: U ¼ 173, N1 ¼ N2 ¼ 20, P ¼ 0.42). As soon as the offspring of neighbours fledged and abandoned their nestboxes, the parents of younger nestlings significantly decreased their intensity of mobbing from ‘weak/average’ to ‘weak response’ ðX SD ¼ 1:25 1:12Þ in the changed size group (Wilcoxon signed-ranks test: Z ¼ 2.08, N ¼ 20, P ¼ 0.038), whereas the intensity of nest defence increased from ‘weak’ to ‘strong response’ ðX SD ¼ 2:4 0:60Þ in the stable size group during the second trial (Z ¼ 3.26, N ¼ 20, P ¼ 0.01). The intensity of mobbing behaviour of the parents of younger nestlings was significantly different between changed and stable size groups during the second trials (Mann–Whitney U test: U ¼ 83.5, N1 ¼ N2 ¼ 20, P ¼ 0.001; Fig. 1). In the changed size group 19 neighbouring pairs arrived during the first trial to mob the tawny owl. In the stable size group 18 neighbouring pairs assisted the parents of younger nestlings during the first trial. During the second trials 17 pairs of pied flycatchers of the stable size group were assisted by their neighbours but none of the birds of the changed size group were assisted by neighbours since the neighbouring offspring had already fledged and the neighbouring adults had already left the area. DISCUSSION Theoretical models of life history evolution predict that the resolution to the parental dilemma whether to place their offspring at greater risk of mortality when under threat of predation instead of themselves will vary among species, depending on offspring
Strong response Weak response
Average response No response
Number of responses
20
10
0
First trial
Second trial
Stable size group
First trial
Second trial
Changed size group
Figure 1. The intensity of mobbing responses to a life-like tawny owl shown to breeding pied flycatchers with ‘younger’ nestlings during the first trial and a second trial 4 days later.
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number and the probability of survival for the parents (Trivers 1972; Dawkins & Carlisle 1976; Maynard Smith 1977; Andersson et al. 1981; Redondo 1989; Rytko¨nen & Soppela 1995). Many studies have documented a temporal increase in nest defence during the breeding cycle indicating that parents increase their fitness by investing more in older than younger offspring (Harvey & Greenwood 1978; Lazarus & Inglis 1986; Montgomerie & Weatherhead 1988; Redondo 1989; Clutton-Brock 1991; Onnebrink & Curio 1991; Rytko¨nen et al. 1995a, b; Halupka & Halupka 1997; Michl et al. 2000; Pavel & Buresˇ 2001; Rytko¨nen 2002). Our results show that this pattern might depend on specific circumstances. Parent pied flycatchers mobbed the stuffed owl equally intensely during the first trials in the stable size and the changed size groups. During the course of the breeding season, the parents of younger nestlings generally increased their mobbing intensity in the stable size group, while birds avoided taking greater risks (Zuk & Kolluru 1998; Krama & Krams 2005; Zuk et al. 2006; Krams et al. 2007) associated with nest defence in the changed size group at the end of the nesting cycle. These opposing changes in nest defence of the parent flycatchers were observed with the offspring number remaining constant in all the trials. Our approach was not to manipulate or control the presumed causal factor experimentally but to take advantage of natural variation in studying effects of group size on mobbing behaviour. Since we did not experimentally control the causal factor, our conclusions are limited and there might be other explanations for the effects of group size on the nest defence behaviour such as possible changes in hormone levels of adult pied flycatchers. Nest defence can be related to the elevated testosterone levels in males (Alonso-Alvarez & Velando 2001) which can increase in the presence of other potential mating partners such as neighbouring females. Therefore the intensity of nest defence of males in the changed size groups might be reduced in the absence of potential extrapair partners. However, such a hormone effect has not been revealed so far and this explanation is highly unlikely especially in the middle of the breeding season. In some earlier nonexperimental studies, mobbing has been shown to be more effective in larger groups of yellow-rumped caciques, Cacicus cela (Robinson 1985). Similar effects were demonstrated by Hoogland & Sherman (1976) for bank swallows, Riparia riparia. In these studies the more intense mobbing in larger groups could be a result of some self-reinforcement by some of the prey individuals. Our study suggests that the social context of nest defence in terms of the number of neighbours can have a significant effect on the intensity of predator mobbing by the initiator individuals. Although a single prey individual may take the risk to mob predators, mobbing is usually performed by a group. This study clearly shows that the first individuals to mob are aware of the presence of other conspecific mobbers in addition to their mate. While pied flycatchers increased the mobbing intensity between trials in the stable size group, the birds of the changed size group decreased their nest defence efforts from the first trial to the second trial as soon as their neighbours left the area. By assembling in a group, mobbers may protect themselves simply by virtue of selfishly dividing the risk as a sheer function of numbers (Hamilton 1971). The benefit of mobbing is obvious for the initiator, but not always for those it attracts since it is potentially dangerous. However, in our study the predator was always placed so that it affected both pairs of neighbouring flycatchers. Even though the predator was not placed near their nestbox, the neighbouring flycatchers were not able to feed offspring while the predator was present. Owing to the group size effect, the mobbing individuals increased the safety of their offspring by cooperating. As proposed by Curio (1963), the more intensely a predator is molested, the sooner it should leave an area. The ‘move-on’ hypothesis is supported by observational (Pettifor 1990; Pavey &
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Smyth 1998) and experimental (Flasskamp 1994) evidence of potential prey driving predators away. Our results show that a pair of flycatchers initiated weaker mobbing when left alone than when the neighbours were present. Why then did the birds decrease the intensity of mobbing? Curio (1963) also suggested that a predator could be equally affected not only by intense mobbing but also by longer harassment. A possible reason why parent flycatchers mobbed weakly is that intense long-lasting mobbing calls help acoustically oriented predators to locate the nests (Yasukawa 1989; Zuberbu¨hler et al. 1997, 1999; Zuk & Kolluru 1998; Krams 2001; Krama & Krams 2005; Bernal et al. 2006; Zuk et al. 2006; Krams et al. 2007). Thus, individuals engaging in mobbing behaviour that includes making calls may face a trade-off between the benefits of removing predators from the territory and the costs of attracting other predators (Krama & Krams 2005; Krams et al. 2007). In the case of weaker mobbing, predators could perceive these calls as detection notification signals (Bradbury & Vehrencamp 1998). Besides indicating to a stalking predator that it has been noticed, prey individuals giving the calls have an opportunity to silence offspring and warn conspecific and heterospecific neighbours (Curio 1978). In this way some mobbing goals may be achieved without attracting the attention of another predator. Theory predicts that the resolution to the parental dilemma may vary depending on offspring number, their quality, age and the probability of survival for parents (Maynard Smith 1977; Kokko & Jennions 2003). However, the empirical results are often equivocal (e.g. Rytko¨nen et al. 1995a, b; Rytko¨nen 2002). Our study reveals the role of the social environment in defending offspring which may be as important as offspring age. This is especially important because of recent census and monitoring techniques suggesting using playback of mobbing calls to census bird abundance (Hutto et al. 1986; Gunn et al. 2000; Turcotte & Desrochers 2002; Fichtel & Hammerschmidt 2003). Our results show that studies using this methodology should exercise caution in using mobbing calls for surveying birds since mobbing intensity does not always allow for direct insights into reproductive behaviour.
Acknowledgments We thank Gary Ramey, Mikus Abolin xsˇ-Abols and Inese Kivleniece for helpful comments on the manuscript. Funding for this project was provided by the Science Council of Latvia (07.2100).
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