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\begin{document}

\title{Synchronization or Coordination? Context dependent anti-predator
vigilance to nature-based ecotourism}



\author[1]{Dejun Kong}%
\author[2]{Anders Møller}%
\author[3]{Yan-Yun Zhang}%
\affil[1]{Kunming University}%
\affil[2]{Université Paris-Saclay}%
\affil[3]{School of Life Sciences, Beijing Normal University}%


\vspace{-1em}



  
  \date{May 08, 2024}


\begingroup
\let\center\flushleft
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\endgroup





\selectlanguage{english}
\begin{abstract}
Prey monitor surrounding dangers independently or cooperatively
(synchronized and coordinated vigilance), with independent and
synchronized scanning being prevalent. Coordinated vigilance, including
unique sentinel behaviour, is rare in nature, since it is time-consuming
and benefit-limited. Evidence does not indicate animals adopting
alternative vigilance strategies during antipredation scanning.
Considering the cooperative nature of both synchronization and
coordination, we assessed whether group members could keep alert
synchronously or coordinatedly under different circumstances,
determining whether cooperative vigilance is context dependent. Under
the framework of conservation behavior, we studied how human behaviour
and species-specific variables impacted individual and collective
vigilance of globally threatened Black-necked Cranes (Grus nigricollis)
and explored behaviour-based wildlife management. We tested both
predation risk (juveniles in group) and human disturbance (level and
distance) effects on individual and collective antipredation vigilance
of black-necked crane families. Adults spent significantly more time
(proportion and duration) on scanning than juveniles, and parents with
juveniles behaved more vigilant. Observer distance affected individual
vigilance of adults while juveniles were influenced by none of these
variables. With the number of juveniles and disturbance increased, crane
couples decreased synchronization of vigilance and they shifted to
coordination, which has so far never been reported yet. Similarly, with
observer approaching, adults shift vigilance from synchronization to
coordination. The collective vigilance shift from synchronization to
coordination as a function of observer distance could help us
determining a safe distance of c. 400m for the most vulnerable family
groups with two juveniles, so as no obvious interference with the
threatened birds by human proximity. We argue that vigilance behaviour
could be a reliable indicator in future nature-based tourist management
and decision-making, which can be derived from conservation solutions in
nature.%
\end{abstract}%



\sloppy


\textbf{Synchronization or Coordination? Context dependent anti-predator
vigilance to nature-based ecotourism}

Dejun Kong\textsuperscript{1, 2, *}, Anders Pape
M\selectlanguage{ngerman}øller\textsuperscript{2, 3}, Yanyun Zhang\textsuperscript{2}

\begin{enumerate}
\tightlist
\item
  \emph{Key Laboratory of Special Biological Resource Development and
  Utilization of Universities in Yunnan Province, College of Agronomy
  and Life Sciences, Kunming University, Kunming 650214, Yunnan, China.}
\item
  \emph{Ministry of Education Key Laboratory for Biodiversity Science
  and Ecological Engineering, College of Life Sciences, Beijing Normal
  University, Beijing 100875, China.}
\item
  \emph{Université Paris-Saclay, CNRS, AgroParisTech, Ecologie
  Systématique et Evolution, 91405, Orsay, France.}
\end{enumerate}

\emph{*} Corresponding author: Dejun Kong, kongdj05@hotmail.com.

Full postal address: No. 2 Puxin Road, Jingkai District, Kunming 650223,
Yunnan, China.

Word number without Appendix: 5754.

\textbf{Highlights:}

\begin{enumerate}
\tightlist
\item
  Synchronization to coordinated vigilance was first reported from
  behavioural spectrum analysis in birds.
\item
  Synchronization of vigilance decreased and shifted as coordination
  increased with disturbance and predation risk.
\item
  Families with more juveniles were more vigilant.
\item
  Vigilance could constitute a prime indicator in behaviour-based
  tourist management.
\item
  We recommend to keep tourists at least a distance of 400m away from
  cranes.
\end{enumerate}

\textbf{Abstract:} Prey monitor surrounding dangers independently or
cooperatively (synchronized and coordinated vigilance), with independent
and synchronized scanning being prevalent. Coordinated vigilance,
including unique sentinel behaviour, is rare in nature, since it is
time-consuming and benefit-limited. Evidence does not indicate animals
adopting alternative vigilance strategies during antipredation scanning.
Considering the cooperative nature of both synchronization and
coordination, we assessed whether group members could keep alert
synchronously or coordinatedly under different circumstances,
determining whether cooperative vigilance is context dependent. Under
the framework of conservation behavior, we studied how human behaviour
and species-specific variables impacted individual and collective
vigilance of globally threatened Black-necked Cranes (\emph{Grus
nigricollis} ) and explored behaviour-based wildlife management. We
tested both predation risk (juveniles in group) and human disturbance
(level and distance) effects on individual and collective antipredation
vigilance of black-necked crane families. Adults spent significantly
more time (proportion and duration) on scanning than juveniles, and
parents with juveniles behaved more vigilant. Observer distance affected
individual vigilance of adults while juveniles were influenced by none
of these variables. With the number of juveniles and disturbance
increased, crane couples decreased synchronization of vigilance and they
shifted to coordination, which has so far never been reported yet.
Similarly, with observer approaching, adults shift vigilance from
synchronization to coordination. The collective vigilance shift from
synchronization to coordination as a function of observer distance could
help us determining a safe distance of \emph{c.} 400m for the most
vulnerable family groups with two juveniles, so as no obvious
interference with the threatened birds by human proximity. We argue that
vigilance behaviour could be a reliable indicator in future nature-based
tourist management and decision-making, which can be derived from
conservation solutions in nature.

\textbf{Keywords:} Anthropogenic disturbance; Collective vigilance;
Ecotourism; Nature visitation; Predation risk.

\textbf{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
crane\emph{Grus japonesis} in family groups decreased when birds shifted
from core zone with less disturbance to buffer zone with higher
disturbance; and common crane \emph{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 \emph{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.

\textbf{2. MATERIALS AND METHODS}

\textbf{2.1 Study species}

Black-necked cranes are a vulnerable species in the IUCN Red List,
endemic to the western plateaus of China (including the Qinghai-Tibet
and Yunnan-Guizhou Plateau) with less than 5\% population inhabited in
wetlands of Bhutan and India (Li, 2014). Breeding pairs occupy relative
constant territories while nonbreeding sub-adults wander across vast
areas in flocks (Zhang et al., 2017); they aggregate into flocks or in
small family groups in winter (Liu et al., 2008). Family groups usually
consist of parents and 0, 1 or 2 juveniles. It is easy to distinguish
juveniles from adults from blocky brownish feathers, smaller body size
and whistles like calls. While adults have a distinct black neck, flight
feathers and tail compared with white plumages. However, telling males
from females apart is hardly achieved except from appearance of unison
call.

\textbf{2.2 Study area}

This study was conducted in the Dashanbao National Nature Reserve
(Dashanbao, N27°18\selectlanguage{english}'38 \selectlanguage{english}" -27deg29\selectlanguage{english}'15\selectlanguage{english}", E103deg14\selectlanguage{english}'55\selectlanguage{english}"-103deg23\selectlanguage{english}'49\selectlanguage{english}"), SW China.
Covering an area of 19,200 ha, Dashanbao was first established in 1993
and upgraded to national level in 2003 for protecting the global
threatened Black-necked Crane and plateau wetlands on which waterfowl
depend. Dashanbao was famous not only for its role as an important
wintering ground for black-necked cranes, but also a vital staging and
stopover site for the eastern population of the bird (Kong et al.,
2014b). Each year there are nearly 1,500 individuals wintering at
Dashanbao, constituting 40\% of their eastern population and
\textasciitilde{}14\% of the world population (Yang and Zhang, 2014). In
2004, Dashanbao was designated as a Ramsar wetland of international
importance as the contribution in black-necked crane conservation. There
are four roosting sites, named Dahaizi, Xiaohaiba, Changhuikou and
Yinjiabeihaizi, located along the lakeside of Dashanbao reserve (Fig.
1). Dahaizi is the most famous site as supporting the largest number of
600-900 black-necked cranes each year (Kong et al., 2014b).

Gathering of the gorgeous cranes attracted massive influx of people
there for bird-watching, photography and also landscape viewing. The
local authority started nature-based tourism program in 2009. According
to reports of Dashanbao administration bureau, over 10,000 tourists,
more than 10 times before tourism was implemented, went to Dashanbao at
the end of 2009, with a yearly increasing rate of \textgreater{}30\%.
Over 60,000 people were recorded in 2013-2014 (Yang and Liu, 2014),
sixty times of increase in abundance after entrance permit to the
public. Sharp increase in tourism caused great threats to the
black-necked crane population and other wildlife there. As the Dashanbao
ecotourism overall plan indicated four discrete areas (named Dahaizi
lake area, Tiaodunhe lake area, Jigong mountain and valley area, and
Yanmaidi lake area) opened to the public, where three of the four
black-necked roosting sites were located in two of these areas (Figure
1). People went to Dashanbao visit Dahaizi Lake area (for crane
observation and photograph) and Jigong mountain and valley area the most
(Yang and Liu, 2014), occasionally they drove around the Tiaodun Lake,
but seldom to Yanmaidi lake where cranes were occasionally present.
Thus, cranes were distributed in the Dahaizi and Jigong area and along
the roadside to these areas facing high levels of disturbance, and
cranes in Tiaodunhe area are facing intermediate disturbance while
cranes in the other areas encountered the lowest disturbance from local
native people (Figure 1).

INSERT FIGURE 1 HERE

\textbf{2.3 Data collection}

We conducted behavioral observations of black-necked cranes during
09:00-18:00 in the winter 2013-2014. Cranes were firstly detected along
a 96 km long line transect by vehicle (Figure 1). Once cranes were
located one observer walked to the focal flock and collected behaviour
data of the birds with a digital video recorder (Sony HDR-XR260E with
55x optical zoom) set on a tripod. Meanwhile distance to the birds was
measured with a laser rangefinder monocular (Newcon Optik LRM 2200SI
with a maximum range of 2,200 meters). We aimed to take 10 minutes
(mins) film for each family group encountered, because it is
sufficiently long to get sufficient vigilance bouts for black-necked
cranes (Li et al., 2017). In order to get time series data of each
family member, we made sure each individual was in the picture at the
same time; film recording ceased as long as one bird was out of sight or
flew away (Ge et al., 2011). Vigilant and non-vigilant behavior were
extracted in second (s) from videos taken in the field. We defined
head-up scanning with neck stretched while standing, walking or even
laying down as vigilance (Kong et al., 2020), otherwise as non-vigilant.

\textbf{2.4 Data processes}

All our filmed pictures are sufficiently stable to distinguish each
behavioural state and long enough to meet at least 5 samples of
vigilance/non-vigilance bouts for statistical effectiveness, even for
our shortest video sampling of 2.2 min, as scan and inter-scan duration
for black-necked crane are 4s and 20s on average (Li et al., 2017). So,
all our data were taken into subsequent analysis. Vigilance behaviour
was evaluated by both vigilance proportion and duration for each group
member. Vigilance proportion was calculated as percentage of time spent
on vigilance during the observation secession while vigilance duration
as the average time span (seconds) of each vigilance bout (Li et al.,
2017). Studies documented that group members could coordinate individual
vigilance in order to increase group collective vigilance (Rasa, 1986;
Bednekoff, 2015), and in small crane groups (Ge et al., 2011). We
focused on the collective vigilance time pattern (time serials) of two
adults in family groups, as no vigilance interactions between juveniles
and adults were detected (Ge et al, 2011; Che et al., 2018).

We classified the areas where cranes occurred into low, intermediate and
high disturbance levels according to tourist accessibility. Cranes
distributed along the road to Dahaizi lake and Jigong mountain where
nearly 90\% tourist visited facing the highest disturbance, moderate
disturbance in the areas around Tiaodunhe lake with less 30\% public
visitation, and lowest disturbance in the other areas. We considered the
observer (data collector) as proxy of potential tourists, the distance
from observer to cranes is another effect variable on vigilance. Only
one observer approached crane without aggressive behaving e.g.,
shouting, chasing, means the lowest disturbance from tourist. Because
inexperience always correlated with high predation vulnerability, a
higher proportion of juveniles in groups usually indicated higher
predation risk (Xu et al., 2013; Beauchamp, 2015). We considered our
study objectives of three family typs with two adults and 0-2 juveniles
as three levels of predation risk; and adults without juveniles endure
the lowest predation risk while families with two juveniles have the
highest predation risk.

We found that our data sets deviated from normality in a one-way
Kolmogorov-Smirnov test, and arcsine square root transformation for
vigilance proportion and logarithmic transformation for vigilance
duration were subsequently conducted in order to get normalized data for
parametric tests. Comparisons of vigilance difference between adults and
juveniles and observed to expected collective vigilance of two adults
were accomplished with t-test. One-way ANOVA was used to test both
individual and collective vigilance difference of adults in three family
types. We selected general linear model to distinguish effects of
disturbance level (categorical variable of three levels), observer
distance (continuous variable) and predation risk (categorical variable
of three family types) on both individual and collective vigilance
deviation of black-necked crane (Ge et al., 2011). Collective vigilance
deviation was used to determine collective vigilance pattern
(synchronization or coordination) by considering the deviation between
expected (independent vigilance) and observed collective vigilance (Pays
et al., 2007a, b). Expected collective vigilance was calculated with the
equation of 1-{[}(1-\emph{p\textsubscript{1}} ) *
(1-\emph{p\textsubscript{2}} ){]}, where \emph{p} represents vigilance
proportion of two adults in a family (Pays et al., 2007a, b; Ge et al.,
2011). Statistics were accomplished with IBM SPSS 20.0 software with a
two-tailed significant level of p\textless{}0.05.

\textbf{3. RESULTS}

\textbf{3.1 Individual vigilance}

In total, we obtained 870 mins observations from 34 family groups. For
each family the observation lasted for 10.2 mins on average (range:
2.2-23.5 mins), which met our expectation of 10 min.

Adults spent significantly more time on vigilance (adults:
27.30-31.28\%\emph{vs} juvenile: 8.74-16.65\%; \emph{p} \textless{}0.05)
and relatively longer vigilant bout (adults: 17.4-12.8s \emph{vs}
juvenile: 8.4-11.8s; \emph{p} \textgreater{}0.05) than juveniles (Table
1). No significant difference in adult vigilance proportion (\emph{F}
=0.106,\emph{df} =2, \emph{p} =0.899) and duration (\emph{F} =0.833,
\emph{df} =2,\emph{p} =0.440) among three family groups existed.

Vigilance behavior of adults was closely related to observer distance
(vigilance proportion: \emph{F} =3.139, \emph{df} =24, \emph{p} =0.001;
vigilance duration: \emph{F} =1.804, \emph{df} =24, \emph{p} =0.053)
while juvenile vigilance was not significantly correlated with any of
the variables of family type, disturbance level and observer distance
(\emph{p} \textless{}0.05, Appendix table 1).

INSERT TABLE 1 HERE

\textbf{3.2 Collective vigilance of adults}

For the three family groups, there were no collective vigilance
difference of adults (\emph{F} =0.382,\emph{df} =24, \emph{p} =0.685).
Collective vigilance of adults was significantly related to interactive
effects of observer distance and family type (\emph{F} =25.372,
\emph{df} =1, \emph{p} =0.037).

\textbf{3.3 Collective vigilance pattern}

The deviation of observed and expected collective vigilance did not
differ significantly from zero (\emph{t} =-1.127, \emph{df} =31,\emph{p}
=0.268); and deviation between expected and observed collective
vigilance did not differ significantly among family type (\emph{F}
=1.940, \emph{df} =2, \emph{p} =0.340), disturbance level (\emph{F}
=0.699, \emph{df} =1, \emph{p} =0.491) or observer distance (\emph{F}
=0.740, \emph{df} =20, \emph{p} =0.718).

However, we found, in family group, two adults behaving synchronized
collective vigilance in low disturbance areas when juveniles were
absent, synchronization decreased with increased disturbance and
predation risk (more juveniles in group) to independent vigilance, and
then to coordinated collective vigilance at high level of disturbance
with two juveniles (Figures. 2, 3).

We also found that collective vigilance deviation varied as a function
of observer distance, that crane couples shifted synchronously to
coordinate vigilance with observer approach (Figure 4). On average,
adults shifted collective vigilance from synchronization to coordination
when observers were 400m away for the most vulnerable family with two
juveniles, while two adult birds with 0-1 juveniles kept synchronized
vigilance (Figure 4). While black-necked cranes could endure human
approach to about averagely 100m at population level (Appendix Figure
1).

INSERT FIG. 2-5 HERE

\textbf{4. DISCUSSION}

\textbf{4.1 From synchronization to coordination}

With spectral analysis of vigilance behaviour that takes time sequences
of vigilant and non-vigilant state into consideration, we reported the
first evidence of group vigilance shift from synchronization to
independence and to coordination. As expected from theory, coordination
is evolutionarily unstable (Rodriguez-Girones and Vasquez, 2002; Sirot
and Touzalin, 2009), less important time-expenditure (Ward, 1985),
sentinels are at great risk of getting depredated (Ridley et al., 2013),
unless significant benefit could be met to enhance survive and foraging
odds (Santema and Clutton-Brock, 2013; Brandl and Bellwood, 2015) or to
help coping with frequent disturbances (Ge et al., 2011) of family
members within small groups (Wickler, 1985; Rasa, 1986;
Rodriguez-Girones and Vasquez, 2002). Although coordinated vigilance is
a kind of time-waste behaviour, it leaves fewer alert gaps for foraging
groups (Pulliam, 1973; Sirot and Touzalin, 2009).

\textbf{4.2 Collective vigilance and affecting factors}

Our study indicated that cooperative vigilance shift was disturbance and
predation risk dependent. Many studies demonstrated that cooperative
sentinel activity (one form of coordinated vigilance) increase when pups
are present (Santema and Clutton-Brock, 2013) and when predation risk
becomes greater (Ridley et al., 2010; Rauber and Manser, 2017). These
findings support our findings that cranes coordinate vigilance pattern
when more young birds are present, in high disturbance areas and when
humans show proximity. In our study, we considered the number of
juveniles in a family as predation vulnerability or risk (Xu et al.,
2013), as predators prefer hunting those left behind (Sirot and
Touzalin, 2009), more juveniles cost more individuals and collective
alert time of adults (Table 1). Leading parents to adopt time-consuming
coordinated vigilance strategy (Figure 2) as our study indicated.
Significant interactive effects of family type and observer distance on
adult collective vigilance indicate that cranes with juveniles are more
vulnerable to human disturbance. Our study also emphasizes that
coordinated vigilance or sentinel behaviour may actually exist in
relatively vast systems in small family groups (Ward, 1985; Wickler,
1985), under circumstances with significant disturbance and predation
risk (Rauber and Manser, 2017), even for monogamous breeding systems
(Mainwaring and Griffith, 2013) as in black-necked cranes.

\textbf{4.3 Discovering cooperative vigilance pattern by spectral
analysis}

Different from a recent vigilance synchronization study on black-necked
crane wintering at Lhasa, Tibet, Che et al. (2018) did not detect
significant deviation between observed and expected collective
vigilance. They concluded that no synchronized vigilance occurred for
family members. However, it is difficult to figure out which cooperative
anti-predator behavioural strategy group members adopted regardless of
vigilance spectrum (Pays et al., 2007a, b). As our study indicated no
significant difference between expected and observed collective
vigilance of two adults, revealing independent scan of two adults. When
compared collective vigilance deviation with zero (when collective
vigilance deviation above the value of zero, coordination occurs; in
contrast, synchronization occurs) as spectral analysis suggested (Pays
et al., 2007a, b; Ge et al., 2011), we found parent cranes cooperating
their vigilance bouts in different situations (Figures. 2-4). When the
family is facing great threats e.g., more juveniles, higher disturbance
and more proximity to human observers, adults shift collective scan from
synchronous to asynchronous ways, so as to ensure less scan gap left
(Pulliam, 1973; Sirot and Touzalin, 2009). Just as our results proved
that families with 2 juveniles performed stronger vigilance than
families with 0-1 juvenile.

\textbf{4.4 Increased individual vigilance with tourism}

Our study confirmed former studies (Wang et al., 2009; Che et al., 2018)
that adults took the responsibility of anti-predator scanning with
significant higher alert time expenditure and duration. Wildlife
decrease individual vigilance and benefit from foraging by gathering in
big flocks (Pulliam, 1973; Kong et al., 2020), but interspecific
conflicts also increase with group size (Pulliam, 1973; Caro, 2005), and
juveniles are more vulnerable to conflicts. So, in winter, we could
observe many family groups (2 adults with 1-2 juveniles) forage
separately from other large groups (Liu et al., 2008), so as to keep
\textgreater{}80\% of time in foraging for young birds (Wang et al.,
2009). Whereas adults in family groups have to spent
\textasciitilde{}6\% more time than adults in large groups in vigilance
instead of foraging (Wang et al., 2009). Interestingly, in order to
conquer high predation risk faced by family groups, both individual
vigilance sequence organization and inter-scan intervals of black-necked
cranes are randomly distributed throughout the year (Li et al., 2017),
making vigilance bouts more unpredictable than predators could not
initiate successful attack. Compared with other wintering grounds of
black-necked cranes in China, including those at Caohai wetlands in
Guizhou province (vigilance: 12.59-16.52\%; Li and Ma, 1992), Napahai
wetlands in Yunnan (vigilance: 11.74-17.05\%) and Lhasa in Tibet
(vigilance: 17.8-21.0\%; Che et al., 2018), black-necked cranes in
Dashanbao spent most time allocation to vigilance (27.30-31.28\%); even
higher than former research conducted here in 2008 (vigilance:
15.6-21.4\%; Kong et al., 2008) before visitation opens for public
tourists. Black-necked cranes in our study area are facing equivalent
disturbance to the birds in Daqiao wetland (vigilance: 27.9+-16.5\%; Kong
et al., 2020) with a large human density of 135 residents per square
kilometers, about 80km away from Dashanbao. Similarly, individual
vigilance of cranes in our study (observer distance) and in Daqiao are
significantly affected by human disturbance (Kong et al., 2020). We
believe that the predominant landscape of vast marshes in Napahai and
Caohai wetlands, which the help of avoidance of human access to crane
habitats contributed the lower anti-predator scans. Wintering habitats
utilized by cranes in Dashanbao and Daqiao are farmland (Kong et al.,
2018). From a historical view, our study also demonstrated that the
explosive expands of nature-based tourism cause new threats to the
threatened black-necked cranes (Li et al., 2014). So, we argue that it
is likely that there is strong interference from tourism caused
coordinated vigilance in black-necked cranes in our study.

\textbf{4.5 Conservation and management implications}

In our study, we found that collective vigilance of two adults varied as
a linear function of observer distance, which helps us determining a
distance at which cranes change vigilance from synchronized to
coordinated behaviour. As vigilance of synchronization usually occurred
under lower disturbance or predation risk circumstance as our results
and former studies indicated, we named this distance from observer to
black-necked cranes the least safe distance. From the function, we
quantified the least safe distance for black-necked cranes and most
vulnerable group of 2-2 family was \emph{c.} 100m and 400m respectively.
The 100m safe distance for black-necked crane population is very close
to the flight initiation distance (FID) of 76m for the bird (our
unpublished data). Since cranes benefit from large group sizes (Pays et
al., 2007a), 2-2 families actually were the most vulnerable group for
black-necked cranes. Then, for the black-necked crane, we suggest to
keep at least 400m distance from tourists in order to create the lowest
disturbance, which is valuable in conservation and management. Moreover,
our study lets us determine the solution in nature.

\textbf{AUTHOR CONTRIBUTION:} D. Kong: Conceptualization, Methodology,
Formal analysis, Original draft preparation, Reviewing and Editing. A.P.
Moller: Writing, Reviewing and Editing. Y. Zhang: Software, Formal
analysis, Writing, Reviewing.

\textbf{FUNDING:} This work was supported by the National Natural
Science Foundation of China (Grant number: 31201725, 31760624). The
funders had no role in study design, data collection and analysis,
preparation of the manuscript, or decision to publish.

\textbf{DECLARATIONS} : All authors declare that they have no competing
interests.

\textbf{DATA AVAILABILITY STATEMENT} : All datasets in the present study
are available at Dryad doi: 10.5061/dryad.5mkkwh73j.

\textbf{ACKNOWLEDGMENT}

We thank staff from the Dashanbao National Nature Reserve for their
field assistance. Many thanks to Mr. Xibao Chen, Dongming Li and Miss
Yanxu Dong who helped compiling behavioural data. We would like to thank
Dr. Wanting Peng for her assistance in map construction and drafting
comments.

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TABLES AND FIGURES

TABLE 1. Vigilance (proportion and duration) difference between adults
and juveniles in three family groups of \emph{Grus nigricollis} . The
first figure for each family type is the number of adult and the latter
is the number of juveniles in a family group. Bold figures indicate
significant level of \emph{p} \textless{}0.05.\selectlanguage{english}
\begin{longtable}[]{@{}llllllll@{}}
\toprule
Family types & Age & N & Vigilance proportion & Vigilance proportion &
Collective vigilance & Vigilance duration / Second & Vigilance duration
/ Second\tabularnewline
\midrule
\endhead
& & & Mean \selectlanguage{ngerman}± SD & T-test & Mean \selectlanguage{ngerman}± SD & Mean \selectlanguage{ngerman}± SD & T-test\tabularnewline
F2-0 & Adults & 12 & 28.29\selectlanguage{ngerman}±25.15\% & --- & 34.03\selectlanguage{ngerman}±30.51\%, n=10 &
17.36\selectlanguage{ngerman}±29.52 & ---\tabularnewline
F2-1 & Adults & 33 & 27.30\selectlanguage{ngerman}±20.00\% & t=2.212, df=47, \textbf{p=0.032} &
43.92\selectlanguage{ngerman}±32.18\%, n=16 & 12.05\selectlanguage{ngerman}±14.34 & t=-0.039, df=47,
p=0.969\tabularnewline
& Juveniles & 16 & 16.65\selectlanguage{ngerman}±16.69\% & & --- & 11.78\selectlanguage{ngerman}±10.81 &\tabularnewline
F2-2 & Adults & 21 & 31.28\selectlanguage{ngerman}±21.45\% & t=4.354, df=32.024,
\textbf{p=0.000} & 36.53\selectlanguage{ngerman}±26.89\%, n=11 & 12.81\selectlanguage{ngerman}±10.28 & t=1.471, df=36,
p=0.150\tabularnewline
& Juveniles & 20 & 8.74\selectlanguage{ngerman}±8.72 & & --- & 8.41\selectlanguage{ngerman}±5.70 &\tabularnewline
Total & Adults & 66 & 28.75\selectlanguage{ngerman}±21.18\% & t=4.711, df=100, \textbf{p=0.000}
& 39.05\selectlanguage{ngerman}±29.74\%, n=37 & 13.26\selectlanguage{ngerman}±16.89 & t=0.565, df=97,
p=0.574\tabularnewline
& Juveniles & 36 & 12.26\selectlanguage{ngerman}±13.29\% & & --- & 9.91\selectlanguage{ngerman}±8.40 &\tabularnewline
\bottomrule
\end{longtable}\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image1/image1}

\end{center}
\end{figure}

FIGURE 1. Study area of Dashanbao National Nature Reserve, Yunnan, SW
China. The four dash line regulars numbered 1-4 is four area visited by
tourists named Dahaizi lake area, Jigong mountain and valley area,
Tiaodunhe lake area, and Yanmaidi lake area respectively. ``R''
indicates roosting sites.\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image2/image2}

\end{center}
\end{figure}

FIGURE 2. Comparison of observed and expected collective vigilance of
two adults in three family groups. The figure of ``2'' in group
composition indicates two adults in a family group and the latter figure
of ``0-2'' indicates juvenile number in a family. Positive value of
collective vigilance deviation means coordinated vigilance while
negative is synchronized vigilance. The box plots show median, quartiles
5- and 95- percentiles.\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image3/image3}

\end{center}
\end{figure}

FIGURE 3. Comparison of observed and expected collective vigilance of
two adults under different disturbance. Positive value of collective
vigilance deviation means coordinated vigilance while negative is
synchronized vigilance. The box plots show median, quartiles 5- and 95-
percentiles.\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image4/image4}

\end{center}
\end{figure}

Fig. 4 Collective vigilance function of two adults in family groups to
observer distance. Positive value of collective vigilance deviation
means coordinated vigilance while negative is synchronized vigilance.
F2-0, F2-1 and F2-2 indicate family groups of two adults with 0-2
juveniles.

\textbf{SUPPORTING INFORMATION}

APPENDIX TABLE 1. General linear model outputs of effect variables on
individual vigilance of adults and juveniles.\selectlanguage{english}
\begin{longtable}[]{@{}llllllll@{}}
\toprule
\begin{CJK}{UTF8}{gbsn}　\end{CJK}\selectlanguage{english}Response variables & Effect variables & Adults & Adults & Adults &
Juveniles & Juveniles & Juveniles\tabularnewline
\midrule
\endhead
& & df & F & P & df & F & P\tabularnewline
Vigilance proportion & flock & 1 & 0.051 & 0.823 & 1 & 0.046 &
0.833\tabularnewline
& disturbance & 2 & 0.216 & 0.807 & 2 & 2.517 & 0.122\tabularnewline
& distance & 24 & 3.139 & \textbf{0.001} & 19 & 1.038 &
0.487\tabularnewline
& disturbance * distance & 1 & 0.754 & 0.391 & 1 & 2.678 &
0.128\tabularnewline
Vigilance duration & flock & 1 & 0.408 & 0.527 & 1 & 1.526 &
0.245\tabularnewline
& disturbance & 2 & 0.382 & 0.685 & 2 & 1.012 & 0.398\tabularnewline
& distance & 24 & 1.804 & \textbf{0.053} & 19 & 1.775 &
0.177\tabularnewline
& disturbance * distance & 1 & 0.196 & 0.660 & 1 & 0.097 &
0.762\tabularnewline
\bottomrule
\end{longtable}\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image5/image5}

\end{center}
\end{figure}

APPENDIX FIGURE 1. Collective vigilance function of two adults in family
groups with two juveniles to observer distance. Positive value of
collective vigilance deviation means coordinated vigilance while
negative is synchronized vigilance.

\selectlanguage{english}
\FloatBarrier
\end{document}

