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.