This study aims to test if there are differences in nest defence behaviour in single and in groups of Yellow-legged Gulls Larus michahellis during two stages of the breeding season: incubation and early chick-rearing period. When a human intruder wearing a mask approached and stood still next to the target nest during incubation, the gulls took part in passive mobbing and helped the ‘attacked’ gull, thereby showing altruistic behaviour. In contrast, during the early chick-rearing period, decreased altruistic behaviour was observed: the individuals that took part in the passive mobbing tended to remain on their own nests, in order to look after their own chicks. In this stage, a reduction of the size of passive mobbing was also noted. Furthermore, gulls from disturbed nests increased the intensity of nest defence by increasing the number of dives directed at the heads of the human intruders. Again, those gulls whose nests were directly affected by an approaching human intruder left their nests quickly to begin an aerial defence, encouraging the chicks to leave the nest and hide among rocks and shrubs. The adult gulls came back to their nests only after the danger had ceased and the chicks had come back to their nests, in agreement with the Parental Investment Theory.

Coloniality in nesting birds represents an important life-history strategy to maximize reproductive success (Herring & Ackerman 2011). Efficient anti-predator behaviour is crucial for the survival of animals (Lima & Dill 1990; Graw & Manser 2007). In this context, nest defence has been studied in a large number of bird species as an example of anti-predator behaviour (e.g. Kruuk 1964; Shields 1984; Sibley & McCleery 1985; Stone & Trost 1991). The reduction of predation risk through direct defence by group members has been suggested to play a primary role in group survival (Kazama & Watamuki 2011). The animals that vigorously defend against predators may experience a decrease in predation risk (Dugatkin & Gudin 1992). When colonial nesting birds are threatened by predators, group mobbing or attacks reduce nest predation risk by chasing the predator away (Montevecchi 1979; Whittam & Leonard 2000).

In fact, many animals display increased risk-taking behaviour during the mating season resulting in increased reproductive success (e.g. Kruuk 1964; Horn 1968; Dill et al. 1999; Berzins et al. 2010). Mobbing has been well documented in a variety of animals and this conspicuous anti-predator strategy quickly recruits both conspecifics (Anderson & Wiklund 1978; Krams et al. 2010) and heterospecifics (Hurd 1996; Krams & Krama 2002).

However, mobbing behaviour has some costs including risks of injury and death to the mobber (Poiani & Yorke 1989) as well as a waste of time and energy (Collias & Collias 1978). Several studies have documented an increase in time in mobbing as a part of nest defence during the breeding period. In contrast, mobbing may be rarely performed either during nest building or in the egg-laying phase (Montgomerie & Weatherhead 1988; Redondo 1989). Theoretical models and life-history evolution predict that in resolving the parental dilemma, an animal’s decision on whether to take care of themselves or of their offspring depends on the offspring value and their own probability of survival (Trivers 1971, 1974; Anderson et al. 1981; Redondo 1989; Berzins et al. 2010). Parents can increase their fitness by investing more in older rather than young offspring, which explains the increase in the intensity of mobbing as the breeding season advances (Carlisle 1985; Montgomerie & Weatherhead 1988). Moreover, mobbing often includes swoops at a potential predator and it may involve direct attack, with physical contact made by the mobber (e.g. Hartley 1950; Kruuk 1964; Gramza 1967; Curio 1978). The notion of mobbing as parental care implies that it will reduce the predation rate on the mobber’s progeny (Greig-Smith 1980; Biermann & Robertson 1982). If this is true, mobbing would provide direct benefits by increasing the reproductive portion of the personal component of the mobber’s inclusive fitness (Brown & Brown 1981; Shields 1984) as the primary beneficiaries of mobbing are the offspring (Shields 1984).

When a predator or an intruder steps into a breeding colony of gulls, animals near to it fly off performing alarm calls. Alarm calls alert other individuals that fly off and join the other birds. This group flies in a circle round the predator and some animals, normally the owners of the directly threatened nests, perform dives against the predator or intruder (Shields 1984). Dives are flights starting from the sky in the direction of the predator’s head, usually without contact. Subjects performing dives against the predator are called ‘active mobbers’ and the meaning of this behaviour is an active offspring defence. Active mobbing is directly involved with nest defence and is measured by the number of gulls flying high and around the head of the intruder. Passive mobbers are a random sample of the local population (Shields 1984). If passive mobbers leave the nest, they face an increased risk of their chicks being preyed on by other predators. From a merely adaptive point of view, passive mobbing is apparently profitless.

Passive mobbing is usually less risky than active mobbing, but the costs of becoming a passive mobber include an energetic and time cost as well as an increased risk of personal injury due to mid-air collisions with other gulls (Conover 1987). Moreover, other gulls are potentially dangerous predators of gull chicks. Cannibalism is a frequent behaviour in gulls (Burger & Gochfeld 1985). Kruuk (1964, 1976), Curio (1978), Shields (1984), Conover (1987) and Ostreiher (2003) have proposed an interpretation of the adaptive value of passive mobbing; this circular flight aims to frighten and ‘study’ the intruder to evaluate its level of danger (e.g. predator of adults, predator of chicks, predator of eggs, where it comes from), study its strategies of attack and so on. Obviously, predators of adult animals are considered the most dangerous. Therefore, passive mobbing has a social purpose. In fact, the intruder can be frightened by a large number of gulls flying and making alarm calls above its head. Once the gulls have studied the intruder, they go back to their nests (Kruuk 1976; Curio 1978; Conover 1985). Accordingly, researchers usually divide the period of exposition to intruders into sub-periods in order to observe the decrease of mobbing animals (habituation to the human).

Parental investment reflects the effort that parents make to increase the survival of their offspring as a trade-off with their own future prospect of survival and reproduction (Trivers 1974). Studies of parental investment suggest that individual parents are consistent in the intensity of their defence of offspring within and among reproductive events (Montgomery & Weatherhead 1988). The intensity with which parents defend their offspring, and the risk they expose themselves to, should reflect the reproductive value (Fisher 1930; Williams 1966). The intensity of defence of offspring peaks at an intermediate age (2 years) followed by decrease into old age and senescence (Møller & Nielsen 2014). Several researchers developed the Parental Investment Theory (Trivers 1971, 1974; Dawkins & Carlisle 1976; Maynard Smith 1977). Parental investment behaviour is related to the mating system (monogamy and polygamy) and the characteristics of offspring (age, vulnerability, quality, number). This theory accounts for the seasonal trend in the defensive behaviour by assuming an increasing value of the offspring for the parents during the rearing season (Siderius 1993). Therefore, both male and female adults defend chicks with increasing intensity during their growth (Jones et al. 2002). Several authors studied the risk run by parents during nest defence (Fisher 1930; Williams 1966; Møller & Nielsen 2014). In this context, some studies show an increasing nest defence behaviour with the age of offspring. Montgomerie & Weatherhead (1988) suggested that the nest defence should increase with offspring age because they become more valuable to their parents. According to these authors, the intensity of defence should increase gradually as long as the probability that eggs will hatch increases. The intensity of nest defence should decrease as soon as chicks are able to defend themselves from predators. Knight & Temple (1986) suggested that this change in nest defence with the age of offspring depends on the experimental situation. According to these authors, the increase in offspring value during the first period of life may depend on two different reasons: (i) replacing an older offspring with a new brood is more expensive than replacing a younger one (Barash 1975); (ii) the probability of a successful nest-building decreases as the season progresses (Buitron 1983).

Framed into these theoretical and experimental contexts, this research aims to study the modifications of nest defence behaviour in relation to two different reproductive sub-periods: incubation (from two weeks after the egg is laid) and early chick rearing (from one to three days after hatching). Different behaviours were measured for individuals and groups. In the case of single gulls, the following behaviours were measured: (i) alert; (ii) escape; (iii) flight, with a human intruder approaching, or staying still beside the target nest; (iv) landing and (v) return to the nest with a human intruder going away from the target nest. Moreover, active mobbing in parents from the target nest was measured with the human intruder staying still beside the nest.

In the case of groups, the size of passive mobbing was measured with a human intruder staying still beside the target nest.

From a methodological point of view, this study follows an ethological approach combined with a typical experimental set up under laboratory conditions. In this line, the human intruder operated under strictly controlled conditions: the step pace while approaching the nest as well as the distance and the position of the human intruder from the target nest during a two-minute stay beside the nest. In this experimental approach, a strict control of variables as well as the internal validity were guaranteed by randomizing the following variables: trials, target gulls, days and time of the day. Likewise, external validity was guaranteed by studying the animals in their own habitat during the reproductive period.

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