Mobbing behaviour: reciprocity-based co-operation in breeding Pied Flycatchers Ficedula hypoleuca

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1 Ibis (2006), 148, Blackwell Publishing Ltd Mobbing behaviour: reciprocity-based co-operation in breeding Pied Flycatchers Ficedula hypoleuca INDRIKIS KRAMS, 1 * TATJANA KRAMA 2 & KRISTINE IGAUNE 1 1 Department of Sciences, Daugavpils University, LV-5400 Daugavpils, Latvia 2 Institute of Zoology and Hydrobiology, Tartu University, Tartu 51014, Estonia Recent non-experimental evidence suggests that reciprocal altruism may be more common in nature than was previously thought. Here we present experimental evidence for mobbing behaviour as reciprocal altruism in breeding Pied Flycatchers Ficedula hypoleuca, a small migratory passerine. Pied Flycatchers attended mobs initiated by their co-operating neighbours. However, they did not join in mobbing initiated by their conspecific neighbours when not assisted in the test an hour before. The results suggest that birds followed a tit-for-tatlike strategy and that responses of neighbouring Flycatchers may be related to reciprocal altruism. Reciprocal altruism is a form of mutual co-operation in which one individual helps an unrelated individual and then receives the assistance of that individual itself some time later (Trivers 1971). Theory predicts that reciprocity should act to increase the lifetime fitness of another individual at cost to one s own fitness (survival and/or reproduction) (Trivers 1971, Axelrod & Hamilton 1981). Several reviews have concluded that reciprocity is rare or non-existent in nature (Packer 1977, Wilkinson 1984, Milinski 1987, Packer & Ruttan 1988, Clements & Stephens 1995, Hauser et al. 2003). Mobbing is the joint assault on a predator performed by prey individuals in an attempt to disable or drive it from the vicinity (Curio 1978, Curio et al. 1978, Dominey 1983, Shedd 1983, Arnold 2000). This behavioural pattern occurs in a diverse range of vertebrate groups, but particularly in fish, birds and mammals (Altmann 1956, Curio 1978, Pitcher et al. 1986). Recent non-experimental evidence suggests that the mobbing behaviour of breeding birds may be explained in terms of reciprocity (Krams & Krama 2002). Indeed, it suggests that reciprocal altruism may be widespread in nature (Dugatkin et al. 1992, Roberts 1998). The basic paradigm for most evolutionary models of co-operation has been the Prisoner s dilemma, where individuals have only two alternatives: to cooperate or to defect (Axelrod & Hamilton 1981). By definition, mutual co-operation gives a higher payoff *Corresponding author. krams@apollo.lv than mutual defection. However, a defector gains an even higher payoff when paired with a co-operator. The initiator of mobbing may be under an increased risk of predation by attracting the predator s attention (Krams 2001). If neighbours co-operate during mobbing, they have an increased opportunity to drive the predator from their breeding area (Lorenz 1931, Pettifor 1990, Flasskamp 1994). If no neighbour co-operates with the first individual to mob, the lone harasser takes a deadly risk (Hoogland & Sherman 1976, Denson 1979, Curio & Regelmann 1985, 1986, Poiani & Yorke 1989, Sordahl 1990). When the initiator is exposed to a defector, it suffers in the initial encounter but may then punish the defector by not joining in the mobbing initiated by the defector. Assuming that the birds are caught in the prisoner s dilemma and that they are playing some form of reciprocity, they should copy each other s behaviour according to certain rules. We tested whether breeding Pied Flycatchers Ficedula hypoleuca follow a simple strategy called tit-for-tat, showing an initial bias towards co-operation, then copying each of the other Gird s moves (Axelrod & Hamilton 1981). In nestbox areas Pied Flycatchers often exhibit semicolonial breeding behaviour, which could be associated with co-operation (Snow & Perrins 1997). METHODS The field study was carried out in May and June 2002 and 2004 near Kraslava, southeastern Latvia (54 58 N, E). We performed a field experiment

2 Reciprocity-based co-operation in Pied Flycatchers 51 in a population of Pied Flycatchers. We used wooden board nestboxes to attract flycatchers. The nestboxes were placed in dry young pine forests with sparse understorey. During the nestling phase we presented a predator at nestboxes occupied by Pied Flycatchers. A stuffed Tawny Owl Strix aluco served as predator stimulus in all trials. This is a common predator of small birds in Northern Europe. Passerine birds usually react strongly to the presence of Tawny Owls (Bautista & Lane 2000). When Pied Flycatchers detect this predator near their nests, they mob it while uttering characteristic calls that attract other potential hetero- and conspecific prey species (Shalter 1978). The nestboxes were arranged in pairs and placed m apart (n = 68; ± 2.73 m, mean ± se). The distance between neighbouring pairs of nestboxes was at least 350 m. When we presented the owl at one of the nestboxes, Flycatchers from both nestboxes of a box pair interrupted their feeding behaviour. This suggests that Pied Flycatchers breeding in neighbouring nestboxes perceived the situation as risky (Desrochers et al. 2002), but no birds were attracted to the owl mobbing from more distant nestboxes. Seventeen pairs of nestboxes were assigned to the experimental group and another 17 pairs served as a control group. Just before the owl was presented at one of the experimental nestboxes, we captured both parents breeding in another nestbox. A strip of plastic was attached to the entrance inside the nestbox, so that the birds could enter the nestbox but could not leave it. These birds were kept in captivity for 15 min while the owl was presented at the nestbox of their neighbours. One of the birds was kept in a cage in a hide while the second captured bird remained in the nestbox. As the birds were not allowed to assist their neighbours, they automatically behaved like defectors in the eyes of their neighbours. As captured birds were out of their neighbours sight, the defecting was not obvious to the neighbours. To ensure that defecting was recognized, we played back the alarm calls of the caged nest recorded 4 6 days previously. Breeding Pied Flycatchers often give alarm calls near their nestboxes for some minutes before joining their mobbing neighbours. The calls were recorded with a Sony W6DC cassette recorder connected to a parabolic microphone. As soon as the harassment of the predator was over, we released the defectors. One hour later we presented the owl for another 15 min at the nest of the defectors to see the response of those birds that did not receive assistance. In the control group no bird was caught and they could choose whether or not to co-operate. Our aim was to determine whether Pied Flycatchers use tit-for-tat when deciding to join in mobbing. If they do they should (i) join in mobbing initiated by their neighbours if they were assisted by the neighbours during mobbing at their own nestbox, and (ii) not assist their neighbours if the neighbours had not assisted them in the test an hour before. For reciprocal altruism to work, there must be some kind of social control against cheats, i.e. those individuals receiving benefits without reciprocating. In communities in which the individuals are familiar with each other, a cheat will be recognized and quickly punished, e.g. by not participating in mobbing initiated by the non-reciprocator (Axelrod & Hamilton 1981, Clutton-Brock & Parker 1995). The observers of test and control birds responses were not blind to the hypothesis and treatment. We divided the mobbing response of Pied Flycatchers, according to their displays and voice, into four categories: (i) no response to the dummy predator (0 points) birds investigated the predator from a distance usually without alarm calls while continuing activities such as foraging or singing; (ii) weak response with frequent approaching and retreating to/from the predator (1 point); (iii) average response (2 points) the birds tended to be close to the predator, and they moved restlessly around it by bowing, pivoting, tail-flicking or hovered in the air in front of it; (iv) strong response with intense movements and display, which included frequent dive-attacks at the predator (3 points). During weak, average and strong responses Pied Flycatchers used pik calls (Bergmann & Helb 1982). The density of the other nesting passerines was low at our study area. At all 34 study sites the number of passerine birds was similar, with between six and ten individuals, including both pairs of Pied Flycatchers (one-way ANOVA, F 33 = 0.19, ns). Thus, the possible dilution effect during the harassment of predators can be treated as similar across all of the sites. The following heterospecific bird species were breeding at the study sites: Tree Pipits Anthus trivialis, Robins Erithacus rubecula, Song Thrushes Turdus philomelos, Mistle Thrushes T. viscivorus, Willow Warblers Phylloscopus trochilus, Chiffchaffs Ph. collybita, Spotted Flycatchers Muscicapa striata, Crested Tits Parus cristatus, Willow Tits P. montanus and Chaffinches Fringilla coelebs. All the above sedentary and migratory bird species are known to mob predators (Snow & Perrins 1997).

3 52 I. Krams, T. Krama & K. Igaune We observed and evaluated the behaviour of Pied Flycatchers from a hide. The owl was mounted on a small platform 1.2 m above ground at the top of a pole. It was installed when, to the best of our knowledge, no Pied Flycatcher was nearby. The predator was positioned m from the nestbox. The owl was looking towards the nest, being placed between two neighbouring nestboxes. Directly after each 15- min period of presenting the owl, the dummy was moved into the hide. The Flycatchers could not see us because all of the manipulations were done from within the hide. We spent the hour between the first and the second trial in the tent to be sure that the birds were not involved in any other anti-predator activities. At the time when the experiments were performed Pied Flycatchers were feeding nestlings, which were at least 5 days old. The maximum difference in age of nestlings in two neighbouring nestboxes was 5 days. The trials were undertaken mainly during the middle of the day (10:00 16:00 h) in calm, warm and dry weather. All adult Flycatchers were marked with light colours of non-waterproof ink 1 2 days before the trials. The birds marked themselves by touching a piece of ink-saturated foamrubber while entering or leaving the entrance of their nestboxes. Because birds either attended the alarms at neighbouring nestboxes or remained at their own nestboxes, we used a sign-test to evaluate the behaviour of the birds in control and experimental groups. In all analyses, two-tailed statistics were used. RESULTS During the first of the paired trials the predator was detected by one of the nestbox within s (n = 34, control and experimental groups taken together; ± s, mean ± se) after positioning of the owl at the nest. Its mate arrived to join in mobbing s later (n = 24; ± s, mean ± se). Neighbouring Flycatchers appeared within s after the mobbing was initiated by the nest. always arrived in pairs. In the control group all of the 17 neighbouring pairs of Pied Flycatchers arrived during the first trial to mob the owl outside their own territories. One hour later when the owl appeared at the co-operator nestbox all of the 17 supported pairs of control Pied Flycatchers attended mobs initiated by the cooperators. During the first trials with the experimental group assistance by neighbours was prevented. During the second trial only four defector Pied Flycatchers were assisted by their neighbours. The behaviour of birds in control and experimental groups differed highly significantly during the second trial (sign-test, P < ). The alarm intensity of control and experimental nest was mainly scored as average response during the first trials (Table 1). There was no significant difference between the groups (Mann Whitney U-test, U = 5.5, n 1 P = 0.77). The intensity of mobbing behaviour of control and experimental birds was also scored as average response during the second trial. The behaviour did not differ between the first and second trials within either control (Wilcoxon matched-pairs signed-ranks test, z = 0, n P = 0.34) or experimental (experimental individuals vs. defectors ) groups (Wilcoxon matched-pairs signed-ranks test, z = 1, n P = 0.32). Experimental and control nest did not differ in the intensity of alarms during the second trials (Mann Whitney U-test, U = 127.5, n 1 P = 0.28). The mobbing behaviour of neighbouring individuals was less intense than that of nest in the control group during both the first (Mann Whitney U-test, U = 17.5, n 1 P = 0.03) and the second trial (Mann Whitney U-test, U = 20, n 1 P = 0.03). However, neighbouring individuals Table 1. Intensity of alarms of nest and neighbouring individuals in experimental and control groups of Pied Flycatchers. Experimental group Control group First trials Second trials First trials Second trials Type of response No response Weak Average Strong

4 Reciprocity-based co-operation in Pied Flycatchers 53 did not differ in the intensity of mobbing behaviour either between the first and second trials in the control group (Mann Whitney U-test, U = 127.5, n 1 P = 0.20) or during the second trial between the experimental and control groups (Mann Whitney U-test, U = 31, n 1 = 4, P = 0.25). DISCUSSION Males of many monogamous bird species adopt a mixed reproductive strategy. They not only guard their own mate and help her to raise a brood but also attempt to obtain sneaky copulations with other females, especially those of neighbouring males (Birkhead & Møller 1992). If some chicks in neighbouring nests are sired by these extra-pair matings, males may have a genetic interest in protecting neighbouring nests. As we have no information about the occurrence of extra-pair matings, we cannot exclude the possibility that the payoffs associated with mobbing were influenced by kinship. However, no male joined in mobbing at a neighbour s nestbox without its mate, which should have been expected if this were the case. Assuming that our results do not reflect extra-pair paternity, what factors are responsible for the striking differences in behaviour of control and experimental Pied Flycatchers? Our result is clear: Pied Flycatchers attended mobs initiated by their cooperating neighbours while non-cooperators were not assisted in the tests an hour later. This resembles the first move in the tit-for-tat strategy in which only co-operating individuals are supposed to be supported by their neighbour-partners on the next move. Mobbing has the essential feature of a prisoner s dilemma with a scale of pay-offs T, R, P and S (see below), where T is the best and S is the worst outcome. Individuals refusing to assist their neighbours avoid co-operating. Harassment has been shown to entail a risk of injury or even death to the prey individual involved owing to its proximity to the predator (Hoogland & Sherman 1976, Denson 1979, Curio & Regelmann 1985, 1986, Poiani & Yorke 1989, Sordahl 1990). Therefore, the temptation to defect (T) may pay better than co-operation. Although it is risky to harass a predator, the prey animals may profit from a joint defence against predators because mobbing decreases the risk of being attacked (Pavey & Smyth 1998). In addition, the strength of a mobbing response increases with group size (Robinson 1985, Verbeek 1985). Hence, the increased inclusive fitness of breeding neighbours is the reward for mutual cooperation (R). If both neighbours do not call and mobbing is not initiated, the predator may remain in the vicinity. In this case no individual increases its own risk of predation. However, as it is usually impossible to feed offspring while a predator is present, this is costly. This is the punishment (P) for mutual defection. Finally, the initiator of mobbing and its offspring may be under increased risk of predation by attracting the predator s attention, especially if not joined by other neighbouring prey individuals. This case could be treated as the sucker s payoff (S). The breeding season of most migratory birds seems to be too short for them to establish a real co-operation with their territorial neighbours (Curio 1978). However, birds living in breeding communities are not anonymous (Godard 1991) and their social behaviour, such as collective mobbing, is evidently based on temporal stability of the breeding communities (Naguib et al. 1999, Krams & Krama 2002) and the positive relationships with conspecific and heterospecific neighbours (Mönkkönen et al. 1997, Forsman et al. 1998a, 1998b). Because mobbing individuals base their decisions of offspring defence on future benefits (Windt & Curio 1986), neighbouring Flycatchers can engage in co-operative relationships, playing a titfor-tat-like game in which the players copy each of their other bird s moves. During the breeding season individuals may either increase their fitness or lose their offspring. The move-on hypothesis supported by observational (Pettifor 1990) and experimental (Flasskamp 1994) evidence reveals that the risk of being killed or injured by a retaliating predator is only worth taking if the mobbers succeed in driving away the predator from their home area. Owing to the group size effect (Robinson 1985, Verbeek 1985), mobbing neighbours increase the safety of their nests as a reward for mutual co-operation, whereas a lone Flycatcher family has a greater risk of predation. In this study, co-operating Flycatcher families won the reward for mutual co-operation on every encounter. Noncooperators were punished immediately. The results of this study show that the origin and evolution of mobbing behaviour in breeding Pied Flycatchers may be explained in terms of reciprocal altruism. However, more experiments are needed to reveal the exact mechanism of these reciprocal relationships. We thank Peter Marler, Raivo Mänd, Staffan Ulfstrand, Michael Taborsky, Nigel Seymour-Dale, Ilva Everte, Martyn Stenning and an anonymous referee for critically reading the manuscript. Eberhard Curio and Walther Thiede encouraged us to test mobbing as a type of titfor-tat experimentally.

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