Behavioral Ecology Advance Access originally published online on September 10, 2007
Behavioral Ecology 2007 18(6):1082-1084; doi:10.1093/beheco/arm079
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Long-lasting mobbing of the pied flycatcher increases the risk of nest predation
a Institute of Systematic Biology, University of Daugavpils, LV-5401 Daugavpils, Latvia b Institute of Zoology and Hydrobiology, University of Tartu, 51014, Tartu, Estonia
Address correspondence to I. Krams. E-mail: indrikis.krams{at}biology.lv.
Received 18 May 2005; revised 18 July 2007; accepted 5 August 2007.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Mobbing behavior may provide real benefits because mobbing prey individuals often cause a predator to leave the vicinity. However, mobbing calls of prey can attract acoustically oriented predators thus increasing nest predation. Therefore, a real value of mobbing as a type of adaptive behavior may depend on its duration. In this experimental study, we tested whether mobbing duration by the pied flycatcher Ficedula hypoleuca, a small hole-nesting passerine, increases the risk of nest predation. From the top of one nest-box within each of 78 experimental plots, we played back long calls of pied flycatchers, whereas recordings of short mobbing calls were played back from the top of another nearby nest-box. The nest-boxes were arranged in pairs, and each of them contained a quail Coturnix coturnix egg. Long-call nest-boxes were depredated by martens Martes martes significantly more often than short-call nest-boxes. This predator usually hunts by night and may eavesdrop on the calls of their mobbing prey while resting nearby during the day. The results of the present study show that long-lasting conspicuous mobbing calls may carry a significant cost for the breeding birds.
Key words: antipredator behavior, Ficedula hypoleuca, long-lasting mobbing, mobbing costs, pied flycatcher.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Signals emitted by a prey individual in the presence of a predator typically represent an alarm intended to warn others or may be designed to deter the predator from attack (Klump and Shalter 1984
). Breeding prey individuals often mob predators by emitting repeated and loud calls and performing stereotyped movements that recruit the majority of local prey around the predator (Wilson 1975; Curio 1978; Dominey 1983; Hurd 1996; Pavey and Smyth 1998; Desrochers et al. 2002). Mobbing behavior has an adaptive value because mobbing assemblies often cause a predator to vacate its immediate foraging area (Pettifor 1990; Flasskamp 1994). This well-defined behavioral pattern occurs in a wide diversity of vertebrate groups but especially in birds, mammals, and fish (Altmann 1956; Curio 1978; Pitcher et al. 1986).
Despite the benefits, mobbing behavior may also carry costs such as injury or death (Hoogland and Sherman 1976; Denson 1979; Curio and Regelmann 1985, 1986; Pitcher et al. 1986; Sordahl 1990). Additionally, the mobbing calls of prey individuals can be eavesdropped (McGregor 1993) by acoustically oriented predators (Latimer 1977; Shalter 1978; Ryan et al. 1982; Klump and Shalter 1984; Yasukawa 1989; Redondo and Castro 1992; Leech and Leonard 1997; Godfray and Johnstone 2000; Mougeot and Bretagnolle 2000; Krams 2001; Haskell 2002). A recent experimental study revealed that mobbing calls of pied flycatchers can increase nest predation (Krama and Krams 2005). Therefore, the benefits of mobbing may depend on the duration of calling because this may influence the risk of attracting predators.
In this experimental study, we investigated whether the short- and long-lasting vocalizations of mobbing pied flycatchers Ficedula hypoleuca, a small migratory hole-nesting passerine, cause different rates of nest predation. Predators such as the marten Martes martes can locate their mobbing prey while resting nearby during the day (Krama and Krams 2005). Predation by martens often accounts for significantly decreased reproductive success in the pied flycatcher (Mihelsons and Vilka 1974). We predicted that nests from which were broadcast long calls of pied flycatchers would be depredated by martens more frequently than nest-boxes from which short calls were broadcast.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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The field experiment was performed between 28 May and 20 July 2003 at 78 areas located near Kr
slava, southeastern Latvia. To examine the risks associated with mobbing calls, we compared the frequency of nest predation in nest-boxes with playbacks of long-lasting mobbing calls with that in nest-boxes with short-lasting mobbing calls. The duration of long-lasting playbacks was 15 min, and the duration of the short-lasting playbacks was 2 min. Duration of mobbing up to 10–15 min can be often recorded in the pied flycatcher during the breeding season.
While mobbing predators, pied flycatchers use "pik" calls (Bergmann and Helb 1982; Krama and Krams 2005), and we recorded the mobbing calls of 17 pairs of pied flycatchers. The calls were recorded with a Sony W6DC cassette recorder connected to a parabolic microphone. A sonogram of calls was produced using Avisoft-SASLab Light software (Raimund Specht, Berlin, Germany). Experimental tapes consisted of continuous calling without periods of silence, which simulated the natural situation. Each 20-s calling period consisted of records taken from one pair of birds, and the next calling period contained the records taken from another pair of birds. The order of the birds on the tape was random, and the calls played back were never repeated (McGregor et al. 1992). Playback amplitude was standardized to natural sound level. Calls were broadcast using a Soundmax SM-1007 cassette recorder.
The study areas were, on average, 3.0 km apart (range 0.5–38 km). At each area, the nest-boxes were arranged in pairs and were placed 70–85 m apart (74 ± 2.5 m, mean ± standard error, n = 78). This arrangement of the nest-boxes was not unnatural because pied flycatchers provided with nest-boxes often exhibited semicolonial breeding behavior. We used wooden board nest-boxes in all experimental trials. The nest-boxes were mounted on trees 1.5–1.7 m above ground level. Martens can depredate up to 100% of the local population of pied flycatchers breeding in nest-boxes in Latvia (Mihelsons and Vilka 1974), and presumably martens use a nest-box as a search image while hunting for nestlings and adult birds. To avoid this possible attraction of predators, we placed empty nest-boxes at each experimental area 5–9 days before the trials. Just before the beginning of the playbacks, we placed pieces of recently abandoned nests of pied flycatchers and a quail Coturnix coturnix egg into each of the nest-boxes in order to control for any olfactory attractiveness of the experimental nest-boxes. We considered predation to have occurred if the top of the nest-box was opened and the egg was missing or broken. Avian predators such as European jays Garrulus glandarius and great spotted woodpeckers Dendrocopos major cannot open the nest-boxes at the study area, whereas martens readily enter nest-boxes by removing the top. We also dispersed sand around the experimental trees to check for tracks of mammalian predators.
The study was carried out in young (25–50 years old) dry pine plantations with a sparse understorey. The density of the local avian community was low and mostly represented by tree pipits Anthus trivialis, song thrushes Turdus philomelos, mistle thrushes T. viscivorus, crested tits Parus cristatus, willow tits P. montanus, and chaffinches Fringilla coelebs. The nest-boxes were placed in pine plantations about 25–35 m away from 85- to 150-year-old mixed forests. The older forests were with a rich understorey dominated by common spruce Picea abies, Scots pine Pinus sylvestris, and common birch Betula pendula. Martens usually live in older forests and rarely come into less productive pine plantations. To count the number of martens, we conducted snow tracking on the grid of transects (total length 72 km) in winter. In spring, some additional data were obtained by direct observations of martens. The results of the census indicate that the study area was inhabited by at least 40 adult martens. The density of martens in the study was generally higher than elsewhere (Lindström et al. 1995) because of the forestry practice of clear-cutting.
We broadcast the mobbing calls of pied flycatchers from the top of the nest-box, which simulated natural conditions because pied flycatchers often give alarm calls while sitting on their nest-boxes. Within each of the 78 areas, a long-lasting mobbing call was played back from one of a pair of nest-boxes, while short-lasting calls were played back from the other nest-box. Nest-boxes were allocated to each treatment by tossing a coin. Playbacks of both long- and short-lasting mobbing calls were conducted simultaneously in each area (n = 78). The trials with mobbing calls were carried out 1–2 h before sunset in calm, warm, and dry weather. We usually conducted trials at 3–4 areas during one evening. The nest-boxes were inspected the following morning, 2–4 h after sunrise. Nest-boxes were not depredated during the first trial in 18 areas, and thus, the experimental trials were repeated. In these cases, we moved the nest-boxes about 500–800 m and repeated the experimental procedure after 6–10 days. The experimental design suggests that each trial was carried out at the territory of a different predator. Therefore, each test can be treated as an independent data point.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Artificial nests were depredated in 23 trials across all experimental areas. Artificial nests with playbacks of long-lasting mobbing calls of pied flycatchers were depredated significantly more by martens than nests with short-lasting calls (Figure 1,
2 = 19.17, degrees of freedom = 1, P < 0.001). We are certain that martens depredated the 23 artificial nests because we found their tracks in the sand around the trees and the top of the nest-boxes had been removed. In 19 cases, we found the remains of the quail eggshell either in the nest-box or within 5 m of the trees supporting the nest-box.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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The results of this field experiment are consistent with previous data (Krama and Krams 2005
) indicating a substantial increase in predation of artificial nests from which were broadcast lengthy mobbing calls. These data suggest that mobbing calls that persist longer help predators to locate the nests. Thus, individuals engaging in mobbing behavior 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 to the vicinity.
In the case of short-lasting mobbing, predators could perceive these calls as detection–notification signals (Bradbury and Vehrencamp 1998). Predators that stalk their prey rely heavily on surprise (Caro 1995). If prey detect a stalking predator and signal this by giving brief mobbing calls, the predator may give up its current hunt because it is now likely to be unsuccessful. Besides indicating to a stalking predator that has been spotted, prey individuals giving the calls have an opportunity to alarm conspecifics (including offspring and neighbors), thereby recruiting them to a mobbing aggregation (Curio 1978). In this way, mobbing goals can be achieved without attracting the attention of another predator.
During the breeding season, mobbing behavior is a typical component of nest defense (Newton 1998). The level of nest defense generally increases with advanced time in the breeding season as well as with the age of young being defended. Therefore, mobbing is expected to be longer and more intense closer to offspring maturation. In the case of long-lasting mobbing, the calls can be easier to locate than calls of short-lasting mobbing. The results suggest that martens resting nearby during the day used easily locatable long-lasting mobbing calls as cues. The signals of sender were exploited because the mobbing calls eavesdropped by the predators indicated not only a mobbing event but also the location of nests or hiding offspring. In our experimental design, long-lasting mobbing calls served as stimuli whose perception by other animals was not beneficial to the initiator of a mob.
Under natural conditions, the long calls of pied flycatchers are relatively rare in nature (Curio 1975) and their duration may lie between the durations used in this study. There is a group size effect in mobbing (Becker 1984; Robinson 1985), and mobbing may become time consuming when there are only a few prey individuals. Supposedly, many birds stay in patches not only because they are restricted by availability of suitable microhabitats and food resources but also because they are influenced by potential predation risks as well (Mönkkönen et al. 1997; Forsman et al. 1998). In such cases, cooperation among neighboring individuals is of crucial importance for mobbing to be successful (Kruuk 1964; Slagsvold 1980). In particular, cooperative mobbing may reduce the length of time required to evict the predator and thus the likelihood of other predators locating the nest.
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FUNDING |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Latvian Research Council (04.1243 to I.K.); European Union (VPD1/ESF/PIAA/04/NP/3.2.3.1/0003/0065 to K.I.).
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ACKNOWLEDGEMENTS |
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We thank John Quinn, Derek Parsons, Seppo Rytkönen, Ilva Everte, and Gary Ramey for comments on the manuscript.
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