1. INTRODUCTION
Human actions driver significant alternation to global nature systems since 1900, making dramatic biodiversity loss and approximately 1 million species face extinction, and unprecedented changes experienced by the nature during the past fifty years (IPBES, 2019). Anthropologic disturbance to wildlife not limited in human residential areas and nearby but also penetrated to protected areas through nature-based visitation and recreation (Geffroy et al., 2015; Marion et al., 2016; Slater et al., 2019), threating wildlife behaviour, abundance, reproduction (Steven et al., 2011) and increasing vulnerability of prey to predators (Geffroy et al., 2015). While conservationists believe that by through exploring indicator behaviours of wildlife, we could understand pressure wildlife experiencing from anthropogenic impacts, advance behavior-based management and achieve sustainable conservation and ecotourism (Berger-Tal et al., 2011; Blumstein et al., 2017). And one of those indicator behaviour is anti-predator vigilance (Berger-Tal et al., 2011).
Animals scan environments around to monitor potential threats from both predators and rivals, regarded as the behavior of vigilance (Caro, 2005; Beauchamp, 2015). Amounts of studies on antipredation behavior revealed that animals gather in large group to decrease individual vigilance, share collective vigilance benefit and avoid being captured (Pulliam, 1973). A great deal of these studies focused on individual vigilance based on the assumption that an individual initiate vigilance bout regardless of behavioral state of other members, named as independent vigilance (Pulliam, 1973; Caro, 2005). Cooperated vigilance behavior patterns of synchronization and coordination, however, were also observed in multiple animal systems when taking time origination of vigilance bout between group companions into consideration (Pays et al., 2007a, b).
Synchronized vigilance indicates individual copy neighbors’ vigilance state by monitoring group companions (Pulliam, 1973) leading to collective vigilance wave (Beauchamp, 2010), also known as the allelomimetic vigilance (Quenette and Gerard, 1992; Pays et al., 2007a, b). Contagious vigilance in group may also induce collective waves of other activities e.g., foraging wave (Quenette and Gerard, 1992) and sleep wave (Beauchamp, 2010). Evidences from case studies and model analysis (Rodríguez-Gironés and Vásquez, 2002; Sirot and Touzalin, 2009) illustrate group members could often synchronize their vigilance in the field.
While coordinated vigilance refers to group member keeping vigilant alternatively in order to avoid scan gap of independent and synchronized vigilance by chance (Bednekoff, 2015). Sentinel behaviour, a well-known form of coordinated vigilance was observed in limited range of vertebrates with cooperative breeding behaviour (Bednekoff, 2015), including mammals (Rasa, 1986; Clutton-Brock et al., 2013), birds (Wickler, 1985; Wright et al., 2001) and fish (Brandl and Bellwood, 2015). Since the likely small potential benefit in most cases, time paying in coordinated vigilance would be less worthy (Ward, 1985) and are seldom occurred in nature (Rodríguez-Gironés and Vásquez, 2002).
So, compared with group vigilance when each individual scan independently, collective vigilance with at least one member is vigilant should be expected higher in coordinated groups and lower in synchronized groups (Pays et al., 2007a, b). Up to date, three vigilance strategies were documented respectively in different study systems and no joint vigilance was reported yet. Ge et al (2011) reported synchronization of collective vigilance of two adult Red-crowned craneGrus japonesis in family groups decreased when birds shifted from core zone with less disturbance to buffer zone with higher disturbance; and common crane Grus grus behaved coordinated vigilance in buffer zones. Basically, smaller common crane showed stronger antipredation vigilance than bigger crane species (Kong et al., 2020), which means common crane could adopt elevated vigilance strategy to red-crowned crane facing similar threats or disturbance, e.g. the buffer zone disturbance in the study of Ge et al (2011). Then, regardless of species, we could make a rational inference that couple cranes may decrease vigilance synchronization with disturbance increase and shift to coordinated vigilance as predation risk or disturbance increase further in small groups (Wickler, 1985). So, we wonder whether synchronized and coordinated vigilance could be detected in nature, for a single species, concerning their common nature of cooperative vigilance and what factors drive the alternation of synchronization and coordination vigilance.
In this study, we tested (1) how environmental and group variables affect both individual and collective vigilance of black-necked cranes; (2) how they response to nature-based recreation through anti-predator vigilance adjusting and (3) moreover, we anticipated to determine an safety observation distance for both visitation and scientific research purpose from vigilance studying, which could also benefit conservation decision-making and management.
We examined the cooperative vigilance temporal pattern (synchronization and coordination) in an exclusively plateau distributed crane species, Black-necked Crane Grus nigricollis , an ideal candidate could be easily observed in distance for testing vigilance cooperation (Li et al., 2017). The birds are facing direct interference from nature-based tourism and indirect threats from climate change and anthropogenic expansion induced wetland loss dramatically (Harris and Mirande, 2013; Li et al., 2014).
Since studies documented synchronization vigilance decreasing between group companies was driven by disturbance (Ge et al., 2011) and predation risk (Podgórski et al., 2016). Coordinated collective vigilance pattern, as a stronger antipredation response against disturbance (Ge et al., 2011) could also be observed for birds under strong disturbing circumstance while synchronized vigilance would be expected facing lower disturbance. We hypothesized that black-necked crane could decrease synchronized vigilance with disturbance and predation risk increase, even shift to coordinated vigilance, if possible. Concerning nature-based recreation in habitats of black-necked cranes are common, we take both disturbance level (categorial variable) and observer distance (continuous variable) into consideration. If vigilance alternation of synchronization to coordination could be detected indeed, then cooperated vigilance of black-necked cranes would vary as a function of the continuous variable of observer distance. Then we could regard the distance (intercept value with X axis) at which cranes alter vigilance from synchronized to coordinated as a control distance keeping tourist away from the birds; and this control distance could be valuable reference in future conservation aimed tourist management.