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Biological Conservation
journal homepage: www.elsevier.com/locate/biocon
Creating a conservation network: Restoration of the critically endangered
Chinese crested tern using social attraction
Yiwei Lu
a,b
, Daniel D. Roby
c
, Zhongyong Fan
a,b
, Simba Chan
d
, Donald E. Lyons
c,e
,
Chung-Hang Hong
f
, Siyu Wang
a,b
, Jia Yang
a,b
, Xiao Zhou
g
, Dongdong Chen
g
, Hsiao-Wei Yuan
f
,
Shuihua Chen
a,h,⁎
a
Zhejiang Museum of Natural History, Hangzhou, China
b
Zhejiang Biodiversity Research Center, Hangzhou, China
c
Department of Fisheries and Wildlife, Oregon State University, Corvallis, OR, USA
d
Birdlife International –Asia Division, Tokyo, Japan
e
National Audubon Society Seabird Restoration Program, Corvallis, OR, USA
f
Department of Forestry and Resource Conservation, National Taiwan University, Taipei, China
g
Department of Chemistry and Life Science, Zhejiang Normal University, Jinhua, China
h
Zhejiang Provincial Museum, Hangzhou, China
ARTICLE INFO
Keywords:
Seabird restoration
Tern breeding colony
Island conservation
Seabird conservation in China
East China Sea
Greater crested tern
ABSTRACT
Social attraction techniques have been demonstrated effective in restoring seabird breeding colonies, especially
colonies of terns (Subfamily: Sterninae). The Chinese crested tern (Thalasseus bernsteini) is a critically en-
dangered seabird with a global population of about 100 breeding adults and a breeding range restricted to the
East China Sea and the Yellow Sea. In order to restore a breeding colony of Chinese crested terns in an archi-
pelago where a former colony had been abandoned, social attraction (decoys and audio playback systems) was
deployed on a small, uninhabited island with no history of seabird nesting. The objective was to establish a
breeding colony of greater crested terns (T. bergii), a closely-related common species, in the hope that Chinese
crested terns would follow. Thousands of greater crested terns and at least 19 Chinese crested terns colonized the
island during the first breeding season after deployment of social attraction. After three years of successful
breeding, the colony was abruptly abandoned early in the fourth breeding season because of invasive king rat
snakes (Elaphe carinata), which consumed all tern eggs. Following removal of all snakes from the colony, terns
resumed nesting the subsequent year. Recovery of this critically endangered seabird depends on repeating this
process at multiple islands. Careful planning, in conjunction with habitat management, close colony monitoring,
and deployment of social attraction, can establish a conservation network of suitable, secure colony sites where
most breeding adults can reproduce successfully. This approach can be used to restore a variety of declining
seabird species along the Chinese coastline.
1. Introduction
Nearly one-third of seabird species are threatened with extinction
due to entanglement with fishing gear, reduction in marine food sup-
plies, environmental contaminants, oil spills, overharvest, and in-
troduction of invasive species that prey on breeding seabirds or destroy
their nesting habitat (IUCN, 2017). Restoration of historical populations
and the protection of seabirds from further threats are the major con-
servation goals for seabirds worldwide. Over the long-term, it has been
assumed that if suitable nesting habitat and protection from anthro-
pogenic disturbance could be provided, populations of threatened birds
would recover (Ahlering and Faaborg, 2006). But this strategy may be
inadequate in some cases, especially for colonial species, including most
seabirds, whose selection of nesting habitat is largely determined by
social cues whose absence may delay recovery, even when suitable
habitat is available (Clout, 2001;Doligez et al., 2002).
Since the 1970s, new techniques have been developed and im-
plemented to actively enhance seabird restoration efforts (Jones and
Kress, 2012). These techniques, which can be classified into two major
categories: social attraction and chick translocation, have been used in
at least 171 different seabird restoration projects conducted in 16
countries/regions in an attempt to restore 64 seabird species (Zhou
https://doi.org/10.1016/j.biocon.2020.108694
Received 31 January 2020; Received in revised form 15 May 2020; Accepted 24 June 2020
⁎
Corresponding author at: Zhejiang Museum of Natural History, Hangzhou, China.
E-mail address: chensh@zmnh.com (S. Chen).
Biological Conservation 248 (2020) 108694
0006-3207/ © 2020 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/BY-NC-ND/4.0/).
T
et al., 2017). With social attraction, decoys (models of adults, chicks,
and eggs), playback of recordings of vocalizations, mirrors, scent, and
artificial burrows are used to lure adult seabirds to restoration sites
with the goal of establishing breeding colonies (Jones and Kress, 2012).
More than 95% of seabird species, especially terns (Sterninae), can be
attracted to breeding sites by the presence of conspecifics and other
seabirds (Rolland et al., 1998). Also, terns feed their young and provide
other parental care for extended periods post-fledging, suggesting that
chick translocations would likely not result in fledged young that would
survive to recruit into the breeding population.
To assure the success of a restoration project using social attraction,
some important procedures should be followed, including nesting ha-
bitat enhancement, deploying social attraction before the nesting
season, close monitoring of the incipient colony, and control of pre-
dators that may threaten the colony. A full understanding of the
breeding biology of the targeted species is also crucial, especially social
factors such as colony size, nesting density, and nesting synchrony,
which can play key roles in restoration success (Kress, 1983;Roby et al.,
2002). Jones and Kress (2012) listed 82 seabird restoration projects
using social attraction techniques worldwide, and 44 of these projects
(54%) were confirmed to have been successful. Restoration of a
breeding colony of an endangered species using social attraction tech-
niques, however, would likely face particular challenges due to small
population size.
The Chinese crested tern (Thalasseus bernsteini) is perhaps the most
threatened seabird species in the world. It was rediscovered in 2000
after a 63-year period with no confirmed sightings, when the species
was presumed extinct (Liang et al., 2000). Total population size was
estimated at no more than 50 individuals, and it was listed by the IUCN
as Critically Endangered (BirdLife International, 2017). The most ser-
ious immediate threat to the survival of the species was exploitation –
illegal harvest of eggs by fishermen (Chen et al., 2009). Beyond the
direct take of eggs, the disturbance associated with fishermen landing
on breeding islands to collect eggs or shellfish apparently caused
breeding terns to abandon suitable nesting sites. Another documented
cause of nest failure in Chinese crested terns is ill-timed summer ty-
phoons (Chen et al., 2015). Long-term issues of conservation concern
for the species include nesting habitat loss due to development on is-
lands, the introduction of mammalian predators (e.g., rats [Rattus
spp.]), and the degradation of foraging habitat in coastal areas due to
sewage discharge, agricultural chemical runoff, and industrial pollu-
tion. These threats to the Chinese crested tern have not been adequately
evaluated due to the lack of close monitoring and research since the
species was rediscovered.
Considering the extremely small population size and severe threats
to survival, the primary conservation action following rediscovery was
safeguarding all Chinese crested terns. But fluctuations in population
counts since rediscovery of the species implied that there might be
other breeding adults besides those nesting at the two know breeding
colonies. While the extensive known breeding range of the species made
it extremely difficult to find additional breeding colonies, the frequent
shifts among colony sites led to severe challenges in safeguarding the
breeding population (Chen et al., 2011). If Chinese crested terns could
be attracted to a site with suitable nesting habitat that is continuously
monitored and secured against egg harvest and other human dis-
turbances, however, the most serious immediate threats to the species
might be quickly addressed, and the species could reverse recent de-
clines and climb back from the brink of extinction.
In 2013, a tern restoration project was initiated in the Jiushan
Islands (Fig. 1), the location of a former breeding colony of Chinese
crested terns that was abandoned in 2007 after breeding failure due to
illegal egg harvest. Tiedun Dao, which was selected for the restoration
project, is near the original breeding island (Jiangjunmao), but was not
known to have been occupied by breeding seabirds. Social attraction
techniques were considered essential for establishing a breeding colony
of Chinese crested terns on Tiedun Dao; however, these techniques had
never before been used to restore a breeding colony of such an extra-
ordinarily rare species. To improve the chances for success, we used
social attraction techniques to try to establish a new breeding colony of
greater crested terns (T. bergii). Since their rediscovery, Chinese crested
terns had only been found nesting in large colonies of greater crested
terns (Chen et al., 2011); therefore, we hoped that Chinese crested terns
would subsequently recruit to a new breeding colony of greater crested
terns.
Using this approach, and monitoring the restoration site closely, we
sought to achieve three objectives: (1) attract greater crested terns to
nest at a new breeding site by using social attraction techniques; (2)
establish a new colony of Chinese crested terns within a colony of the
common sympatric congener; (3) provide a more robust estimate the
global population of Chinese crested terns; if the successful restoration
of a mixed breeding colony of greater crested terns and Chinese crested
terns in the Jiushan Archipelago did not negatively affect the size of the
other two known breeding colonies for Chinese crested terns, it would
indicate that there are other breeding-age Chinese crested terns and as
yet undiscovered breeding colonies for the species somewhere in the
northwestern Pacific. Achieving these objectives is a crucial first step
for the longer-term goal of establishing a well-protected and closely-
monitored network of breeding islands for greater crested terns and
Chinese crested terns, which would address the difficulties in the con-
servation of this critically endangered species and save it from extinc-
tion.
2. Methods
2.1. Study species and area
The Chinese crested tern has been a poorly-known species since it
was first described in 1863. Following the collection of 21 specimens in
1937 along the coast of Shandong Province, China, there were no
confirmed records until four adults and four chicks were found among a
large colony of greater crested terns in the Matsu Islands, Taiwan, along
the Fujian Province coast of China in 2000 (Liang et al., 2000). Prior to
this discovery, many ornithologists had presumed the Chinese crested
tern was extinct.
Since rediscovery in 2000, breeding has now been confirmed in five
locations. Three of these locations were found before 2013 and are
along the Chinese coast: the Matsu Islands (Liang et al., 2000;Hung
et al., 2019), the Jiushan Islands, and the Wuzhishan Islands (Chen
et al., 2010;Fig. 1). In 2016, two other small breeding colonies of
Chinese crested terns were confirmed for the first time: an uninhabited
island offthe southwestern coast of South Korea (Song et al., 2017), and
the Penghu Islands of Taiwan (Liu and Hetherington, 2016).
The continental coastline of Zhejiang Province extends over
2200 km from 27°06′N to 31°11′N, and there are 3061 islands offthe
coast of Zhejiang Province, 2886 of which are uninhabited. The Jiushan
Archipelago (29°26′N, 122°10′E) is situated 19 km offthe coast of
Xiangshan County, eastern Zhejiang Province (Fig. 1) and consists of 76
uninhabited islands that were included in the Jiushan Islands National
Nature Reserve in 2011. In 2004, a breeding colony of Chinese crested
terns, the first to be discovered after the rediscovery of the species
nesting in the Matsu Islands, was found on Jiangjunmao Island in the
Jiushan Archipelago. About 10–20 adult Chinese crested terns were
found nesting among ca. 4000 greater crested terns (Chen et al., 2009).
In 2005 and 2006, no Chinese crested terns were found nesting in the
Jiushan Islands, but in 2007 eight Chinese crested terns were again
observed breeding among nesting greater crested terns on Jiangjunmao
Island. Illegal egg harvest apparently caused all crested terns to
abandon the Jiushan Islands after the 2007 breeding season.
Tiedun Dao is a 2.58-ha island with a maximum elevation of 26.8 m
asl that was chosen as a tern colony restoration site in the Jiushan
Archipelago. Tiedun Dao is located about 1 km from Jiangjunmao
Island, the site where nesting by Chinese crested terns was first detected
Y. Lu, et al. Biological Conservation 248 (2020) 108694
2
in the Jiushan Islands, and is within the core protected area of the
Nature Reserve (Fig. 1). It was selected based on several criteria, in-
cluding (1) absence of human occupation and mammalian predators,
(2) accessibility for site preparation and monitoring, (3) presence of
dense vegetation on top of the island, allowing colony monitors to live
on the island without disturbing nesting seabirds, and (4) proximity to
Jiangjunmao Island, the former site of a mixed species tern colony.
The Wuzhishan Archipelago (30°13′N, 121°50′E) is located at the
mouth of Hangzhou Bay, 7 km offshore of the largest island in the
Zhoushan Group (Fig. 1). It consists of 7 uninhabited islands that were
included in the Wuzhishan Islands Provincial Nature Reserve in 2001.
Since 2008, two to six pairs of Chinese crested terns have been observed
nesting among greater crested terns at large colonies in the Wuzhishan
Islands (Chen et al., 2011). The tern colony shifted among four islands,
depending on the breeding season, including Mantoushan, Yaqueshan,
Longdongshan, and Wumaoshan. In 2014, however, this mixed-species
breeding colony disappeared. In 2015, we chose Yaqueshan as a second
restoration site where social attraction would be deployed in an effort
to stabilize the breeding colony there. Yaqueshan is a 1.08-ha island
with a maximum elevation of 18.5 m asl; the island is relatively flat and
covered by short grass compared to the other islands in the Wuzhishan
Archipelago.
2.2. Social attraction techniques
Social attraction aims to lure adult birds to restoration sites with the
goal of establishing or re-establishing breeding colonies where none
currently exists. Most seabird species are gregarious colonial nesters,
excellent candidates for restoration because they can be lured using
social attraction techniques that seek to replicate features of an estab-
lished colony (Kress, 1983;Roby et al., 2002;Jones and Kress, 2012).
Most tern species are amenable to the use of social attraction to lure
them to a site where suitable nesting habitat is available. Decoys are
deployed across a prospective colony site and recordings of calls are
played using automated audio playback systems. The visual and audio
cues cause prospecting adult terns to investigate the site and remain
until other potential mates are also attracted. This technique, coupled
with intensive monitoring and management of any problems that arise
(e.g., predators) has been successful in restoring breeding colonies of
nearly 50 different seabird species around the globe (Jones and Kress,
2012;Zhou et al., 2017).
In early 2013, before the breeding season, we used bait stations and
track plates to survey for potential mammalian predators at Tiedun
Dao. Lesser rice field rats (Rattus losea) were detected on Tiedun Dao;
consequently, we used the rodenticide Bromadiolone dispensed at bait
stations to eradicate rats from the island. According to Chen et al.
(2011), the preferred nest substrate of mixed colonies of greater and
Chinese crested terns includes grassy areas, bare rock, and a zone of
interspersed bare rock and low grass devoid of tall vegetation. We
identified the eastern part of Tiedun Dao as having substrate most
suitable for nesting terns and the prospective site for a new tern
breeding colony; this part of the island includes an extensive area of
bare rock that slopes down to the shoreline, providing access to the
water's edge for older chicks.
In late April of 2013, one month before the tern breeding season
started, we dispensed rodenticide to eradicate rats from the island.
Then we cleared vegetation, uprooted tall grasses, and cut shorter
grasses in a rectangular area about 60 m × 200 m as the predetermined
site for the prospective tern colony. To provide social attraction at the
new colony site, we securely installed 350 plastic greater crested tern
decoys and 50 Chinese crested tern decoys. We also deployed three
audio playback systems (Murremaid Music Boxes, South Bristol, Maine,
USA) on the prospective colony site, each including two patio speakers
and powered by solar panels. The audio playback systems broadcast
Fig. 1. The study area, including the two sites in Zhejiang Province where Chinese crested tern restoration projects have used social attraction techniques: Tiedun
Dao in the Jiushan Archipelago and Yaqueshan in the Wuzhishan Archipelago.
Y. Lu, et al. Biological Conservation 248 (2020) 108694
3
digital recordings of the calls of greater crested terns that had been
recorded at a breeding colony on the Wuzhishan Islands. After the
breeding season, we removed all decoys, audio playback systems, and
solar panels from the tern colony site for cleaning, maintenance, and
storage during the non-breeding season. We followed this procedure
each year during 2014–2018.
2.3. Monitoring and data collection
In 2013, the first year of the restoration effort in the Jiushan Islands,
we set up a video surveillance system at the restoration site on Tiedun
Dao, and the colony monitors lived on a nearby island, Jigushan, and
monitored the colony site with binoculars and spotting scopes from a
distance of about 600 m. Because of the difficulty of closely monitoring
the restoration site from such a distance, beginning in 2014 the colony
monitors lived in tents or portable buildings set up on the opposite side
of Tiedun Dao from the tern colony site and separated by a dense patch
of vegetation.
The resident colony monitors monitored the restoration site and
breeding colony from observation blinds that were installed at the
periphery of the nesting area. Ingress and egress from the observation
blinds was via concealed pathways cut in dense vegetation adjacent to
the area cleared as nesting habitat. This set-up facilitated the close
monitoring of the breeding colony without disturbing nesting terns. The
tasks of the resident colony monitors included (1) deterring disturbance
to the tern colony due to illegal egg harvest or other human visitation to
the island; (2) detecting other potential factors that might limit colony
restoration, such as disturbance from predators; (3) monitoring use of
the island by greater and Chinese crested terns, including visitation,
breeding behavior, egg-laying, incubation, and chick-rearing; and (4)
responding to any factors that might limit colony restoration as ap-
propriate (e.g., predator removal).
Fig. 2. Numbers of Chinese crested terns and greater crested terns attending the Tiedun Dao colony restoration site in the Jiushan Islands and the Yaqueshan colony
restoration site in the Wuzhishan Islands, Zhejiang Province, China during the 2013–2018 breeding seasons. Restoration efforts were initiated on Tiedun Dao in 2013
and on Yaqueshan in 2015.
Y. Lu, et al. Biological Conservation 248 (2020) 108694
4
At the Wuzhishan Islands, the colony monitors did not live on the
nesting island, but visited Yaqueshan, the nesting island, during the day
via watercraft, weather permitting. The colony monitors observed the
nesting area and tern colony from an observation blind set up on the
northeastern side of Yaqueshan.
Data on the estimated number of greater and Chinese crested terns
present on each colony and the causes of any tern nesting failure were
collected daily on Tiedun Dao and, weather-permitting, on Yaqueshan.
The numbers of greater crested terns on the breeding colonies were
estimated from the blinds by counting the numbers of incubating and
non-incubating terns in plots (3 m × 3 m) that were marked on the
nesting area prior to the breeding season. Because the entire breeding
colony could not be observed from the blinds, these estimates were
extrapolated to the entire colony area by adjusting the plot counts
based on the ratio of terns in plots to the total number of active tern
nests counted during walk-throughs on each colony in mid-June, late in
the incubation period, when peak numbers of breeding pairs were in-
cubating eggs.
To count the total number of tern nests on-colony, 6–8 team
members walked through the entire colony and took photographs of all
eggs in each nesting plot. From the photography, we could distinguish
active nests from abandoned ones because unattended eggs were gen-
erally covered in mud and rolled together in windrows. By comparing
photography taken during mid-June with photography taken in late
August, once all terns had finished nesting and left the breeding colony,
we could also estimate the number of eggs that hatched in each plot and
throughout the entire colony as well. This estimate is likely a minimum
because a few eggs were laid on the colony after mid-June by adults
that had lost eggs earlier in the season. The numbers of hatched eggs
minus those taken by predators and those addled on the nesting area
were considered the best estimate of the numbers of young greater
crested terns raised to fledging age at each tern colony. The number of
Chinese crested terns was accurate to the nearest individual, while the
number of greater crested terns was considered accurate to the nearest
100 individuals.
3. Results
3.1. Size and productivity of breeding colonies
The estimated numbers of adult Chinese crested terns and greater
crested terns on the two colony restoration sites during the study period
are shown in Fig. 2. In 2013, two colony monitors began monitoring the
Tiedun Dao colony site on 7 May. On 1 June, five greater crested terns
were first observed on the colony site near the social attraction. From 3
June to 19 June, 2–8 greater crested terns were occasionally observed
on the Tiedun Dao colony site, but a breeding colony failed to form.
One month later, on 18 July, about 50 greater crested terns suddenly
appeared on the Tiedun Dao colony site and, in the following days, the
numbers of terns increased rapidly and egg-laying was initiated. The
numbers of greater crested terns continued to increase throughout
much of August, peaking at an estimated 3300 individuals on 27 Au-
gust. By 23 July at least six Chinese crested terns had joined the newly
formed colony of greater crested terns, and the number of Chinese
crested terns counted on Tiedun Dao peaked at 19 individuals on 27
August (Fig. 2). More than 800 pairs of greater crested terns and at least
two pairs of Chinese crested terns laid eggs. Ultimately, this newly es-
tablished tern colony successfully produced over 600 greater crested
tern fledglings and at least one Chinese crested tern fledgling by early
October.
In 2014, terns arrived at Tiedun Dao in early May and most laid
their eggs by the end of May. At its peak, the Tiedun Dao colony in-
cluded about 4000 greater crested terns and 43 Chinese crested terns
(Fig. 2), and at least 13 young Chinese crested terns and about 1000
young greater crested terns were fledged by the end of the 2014 nesting
season. At the Wuzhishan Islands in 2014, as many as 500 greater
crested terns appeared in May, but all abandoned the nesting ground
later in the month. This was the first year that the mixed species
breeding colony of crested terns abandoned the colony in the Wuz-
hishan Islands since the colony was first discovered in 2008.
In 2015, in an effort to restore a crested tern breeding colony at the
Wuzhishan Islands and stabilize it, we deployed social attraction on
Yaqueshan in the Wuzhishan Archipelago. Yaqueshan had been the site
of a mixed species breeding colony of greater and Chinese crested terns
in 2008, 2010, and 2012; in 2009, 2011, and 2013 the tern colony was
on a different island in the Wuzhishan Archipelago. The social attrac-
tion at Yaqueshan consisted of installing 300 greater crested tern de-
coys and two audio playback systems distributed over the former
nesting area. At the peak of the nesting season about 3200 greater
crested terns and 10 Chinese crested terns were attracted to the colony
site on Yaqueshan (Fig. 2), and about 1200 young greater crested terns
and 4 young Chinese crested terns were fledged by the end of the 2015
nesting season. During the same nesting season, a total of about 2500
greater crested terns and 52 Chinese crested terns attempted to nest on
Tiedun Dao in the Jiushan Islands (Fig. 2). About 1000 young greater
crested terns and 16 young Chinese crested terns were fledged from the
Tiedun Dao colony in 2015.
In 2016, as many as 100 greater crested terns appeared at the colony
site on Tiedun Dao in early May, but the Tiedun Dao colony was un-
expectedly abandoned by the end of the month (Fig. 3). The earliest
arriving greater crested terns laid two small batches of eggs, 15 and 7
eggs each, but these eggs disappeared soon after they were laid, and
adult terns did not attend the colony overnight. Using video surveil-
lance equipment, we discovered that the tern eggs were being con-
sumed by king rat snakes (Elaphe carinata) at night, and that this pre-
dator disturbance was likely the cause of colony abandonment early in
the 2016 breeding season. Meanwhile at Yaqueshan in the Wuzhishan
Islands, a total of about 4000 greater crested terns and at least 14
Chinese crested terns were counted during the peak of the nesting
season (Fig. 2), and the colony at Yaqueshan produced about 1200
greater crested tern fledglings and 6 Chinese crested tern fledglings by
the end of the 2016 breeding season.
In 2017, after 18 king rat snakes were trapped and removed from
Tiedun Dao before the tern breeding season, the mixed species tern
colony reformed on Tiedun Dao amidst the deployed social attraction.
About 2500 greater crested terns and 26 Chinese crested terns were
counted on the Tiedun Dao colony during the peak of the breeding
season, and about 1100 greater crested tern fledglings and 6 Chinese
crested tern fledglings were produced by the end of the 2017 nesting
season. Concurrently at Yaqueshan, about 2600 greater crested terns
and at least 12 Chinese crested terns nested amidst and near social
Fig. 3. Timeline of attendance by greater crested terns of the colony restoration
site on Tiedun Dao, Jiushan Islands during the 2016 breeding season, when
invasive king rat snakes were detected on and removed from the colony site.
The numbers of greater crested tern eggs present on the colony restoration site
each day are also shown.
Y. Lu, et al. Biological Conservation 248 (2020) 108694
5
attraction, and about 1000 greater crested tern fledglings and 4 Chinese
crested tern fledglings were produced by the end of the nesting season.
In 2018, the tern breeding colonies formed at the colony sites in the
two island groups in early May, as in 2017. About 4200 greater crested
terns and 42 Chinese crested terns were counted at the Tiedun Dao
colony by mid-June, and about 5300 greater crested terns and 35
Chinese crested terns were counted concurrently at the Yaqueshan
colony (Fig. 2). By late August, about 1600 greater crested tern chicks
and 13 Chinese crested tern chicks had fledged at Tiedun Dao, and
about 1900 greater crested tern chicks and 12 Chinese crested tern
chicks had fledged at Yaqueshan.
3.2. Threats to breeding Chinese crested terns
Illegal egg harvest and associated disturbance to breeding adults
have been identified as the greatest threat to Chinese crested terns
(Chen et al., 2015); however, no tern egg collection occurred at either
the Tiedun Dao or the Yaqueshan colonies during the 6-year restoration
period. During the breeding seasons of 2013–2018, the colony monitors
for the Tiedun Dao restoration site prevented a total of 13 attempts by
fishermen to land on the island, including one instance in 2014 when a
fisherman fled the island just after entering the breeding colony and
noticing a colony monitor was in an observation blind. The colony
monitors also deterred an additional 28 vessels from approaching the
colony site so closely as to flush adult terns.
On 11 July 2015, a Super Typhoon named Chan-hom (Category 4
storm with 210 km/h winds) passed near both Tiedun Dao and
Yaqueshan, killing at least six greater crested tern chicks at Tiedun Dao
and at least 184 greater crested tern chicks at Yaqueshan, but no
Chinese crested terns were known to have been killed during this ty-
phoon.
A single lesser rice field rat was detected on Tiedun Dao in both
2015 and 2016, and three lesser rice field rats were detected at
Yaqueshan in 2015 and 2016. Despite the presence of small numbers of
this widespread and omnivorous rat species on Tiedun Dao and
Yaqueshan, no harm to the tern breeding colonies on these islands from
invasive rats was detected or documented during our study.
One or more peregrine falcons (Falco peregrinus) were observed
visiting the tern breeding colony on Tiedun Dao during the breeding
seasons of 2014, 2015, 2017, and 2018, and falcons were documented
depredating at least six adult greater crested terns on or near the
colony. No Chinese crested terns were observed being depredated by
peregrine falcons during the study period, however.
King rat snakes were observed on Tiedun Dao during both the 2014
and 2015 breeding seasons, but this common and widespread species
was not documented to eat tern eggs until 2016. The first 23 eggs that
were laid by greater crested terns on the Tiedun Dao colony in 2016
were all apparently eaten by king rat snakes, and the breeding colony
was subsequently abandoned during the 2016 nesting season (see
Fig. 3). Only after 18 king rat snakes had been trapped and removed
from Tiedun Dao before the 2017 nesting season did the mixed-species
tern breeding colony reform on Tiedun Dao. No king rat snakes were
subsequently detected on Tiedun Dao during the 2017 nesting season.
However, snake trapping early in the 2018 nesting season revealed that
at least four king rat snakes had re-colonized Tiedun Dao.
4. Discussion
4.1. Social attraction and the conservation challenges for the Chinese
crested tern
Since Chinese crested terns were rediscovered in the Matsu Islands
in 2000, the species was regarded for 13 years as breeding in only two
large colonies of greater crested terns, and the global population of
Chinese crested terns was considered very low, likely less than 50 in-
dividuals (Chen et al., 2009;Chen et al., 2015). Small population size
and severe threats to reproductive success from illegal egg harvest and
typhoons apparently drove the species to the very brink of extinction
(Chen et al., 2015). Although alarm over the species' status has at-
tracted worldwide conservation attention, saving this critically en-
dangered species still faces many challenges.
On the one hand, the breeding range of the Chinese crested tern is
large and extensive, across most of the East China Sea, making it ex-
traordinarily difficult to detect and monitor all breeding attempts by
the species. Even for the three known larger breeding colonies in the
Matsu, Jiushan, and Wuzhishan archipelagos, large fluctuations in
numbers of breeding individuals have been recorded among years, and
frequent shifts occur among different islands within each archipelago
(Chen et al., 2009;Hung et al., 2019; this study). These nesting char-
acteristics make it very difficult to monitor and safeguard the very few
known breeding individuals.
On the other hand, two major threats to the species' persistence, egg
harvest and human disturbance, are still widespread at islands along
the coast of the East China Sea. Elimination of these threats depends on
increased public awareness of the conservation needs of the species,
which requires a long-term effort toward public education and out-
reach. In the short term, however, saving such a critically endangered
seabird requires a more immediate and active restoration effort. Our
results indicated that social attraction techniques can provide an im-
portant tool to address the immediate challenges for conservation of the
Chinese crested tern.
First, it is possible to attract Chinese crested terns to nest at selected
islands. Even so, the Chinese crested tern is so rare that the success of
social attraction depends on using the technique to restore large
breeding colonies of greater crested terns, which then lure Chinese
crested terns to recruit to those colonies.
Second, the use of social attraction techniques to establish or restore
mixed species tern colonies on particular islands provides an opportu-
nity for close monitoring of those colonies, if the islands are selected
carefully to facilitate monitoring efforts. Close monitoring of active tern
colonies can effectively deter illegal egg harvest and other human dis-
turbance, enhancing the prospects for breeding success at the colony.
Furthermore, close monitoring provides an opportunity to identify
those factors that limit colony size and nesting success. For example,
close monitoring at Tiedun Dao allowed the detection and elimination
of a major threat to that colony, the invasion of king rat snakes, which is
a widely-distributed species on islands along the coast of the East China
Sea (Huang, 1990) that can cause abandonment of tern colonies.
Third, through the use of social attraction, we obtained a more
accurate understanding of the size of the population of Chinese crested
terns. Using a relatively complete survey of potential nesting islands
along the coast of Shandong, Zhejiang, and Fujian provinces, the total
number of Chinese crested terns was estimated to be no more than 50
individuals in 2008 (Jiang et al., 2005;Liu et al., 2009;Chen et al.,
2009;Hung et al., 2019). Because these surveys were conducted over
multiple breeding seasons, however, the accuracy of this population
estimate was somewhat in question. The number of breeding in-
dividuals that were recorded during the six-year restoration project
(2013–2018) was considerably more than the previous estimate
(Fig. 4). For example, in 2015 the minimum total number of breeding
adult Chinese crested terns reached 75 individuals, based on data col-
lected during monitoring at the Matsu (Hung et al., 2019), Wuzhishan,
and Jiushan archipelagos. The dramatic increase in the census number
of breeding adults since 2012 implies that restoration projects at the
Jiushan and Wuzhishan archipelagos attracted breeding individuals
from colonies other than the three known colonies. Two new breeding
sites that were discovered in 2016 support our hypothesis that other
previously undetected breeding colonies of Chinese crested terns were
the source of the unprecedented numbers of adults counted in 2015. In
2016, five Chinese crested terns were discovered nesting in a large
black-tailed gull colony on a small island offthe southwest coast of
South Korea, and two pairs of Chinese crested terns were discovered at
Y. Lu, et al. Biological Conservation 248 (2020) 108694
6
the Penghu Islands in Taiwan (Song et al., 2017;Liu and Hetherington,
2016). Regardless, the breeding colonies at the Jiushan, Wuzhishan,
and Matsu archipelagos still included most of the known breeding in-
dividuals of Chinese crested terns.
Finally, the success of the restoration projects using social attraction
at the Jiushan and Wuzhishan archipelagos generated considerable
public attention. A four-episode documentary film on this tern re-
storation project was televised by China Central Television (China
Central Television, 2016). This publicity greatly enhanced the aware-
ness of this conservation project by governmental agencies, scientists,
and the general public in a short period of time, and contributed en-
ormously to the conservation of the Chinese crested tern in China and
its prospects for future recovery. The seabird breeding colonies in the
Jiushan Islands Nature Reserve were frequently subjected to illegal egg
harvest and human disturbance before 2013 (Fan et al., 2011;Chen
et al., 2015), but intrusion by boats into the protected area decreased
significantly following the initiation of tern colony restoration and il-
legal egg harvest has not been reported since then.
The recorded number of adult Chinese crested terns has increased
dramatically since we initiated the restoration project in 2013 (Fig. 4).
In 2018, we attracted a total of 77 breeding adult Chinese crested terns
to the Tiedun Dao and Yaqueshan colony sites, or 88.5% of the known
number of breeding adults in the global population in that year. Also in
2018, 25 Chinese crested tern chicks fledged from the Tiedun Dao and
Yaqueshan colonies, which accounted for 96.2% of the known number
of Chinese crested tern fledglings produced range-wide in that year.
Consequently, we now know for the first time in history that the global
population of Chinese crested terns exceeds 100. The population in-
crease from less than 50 to more than 100 individuals is a cautiously
hopeful sign that this critically endangered species can be brought back
from the very brink of extinction.
A new threat to the Chinese crested tern has, however, been re-
vealed based on molecular studies (Yang et al., 2018). Evidence from
this study indicates that hybridization between Chinese crested terns
and greater crested terns has occurred, and that the hybrid descendants
are likely fertile. Genetic introgression may represent a serious threat to
such a critically endangered species. That hybridization has occurred is
perhaps not surprising given the very small population size of Chinese
crested terns and their habit of nesting in large greater crested tern
colonies. For this and other reasons (avoiding genetic drift and in-
breeding depression), rapid population expansion is fundamental to the
conservation of Chinese crested terns and survival of the species in the
long-term.
4.2. Conservation networks: a restoration approach for Chinese crested
terns and other breeding seabirds in China
An effective population recovery plan for an endangered species
relies on complete knowledge of its life history, ecology, and genetics
(Campbell et al., 2002). For some critically endangered species, direct
management intervention, such as artificial propagation and ex situ
conservation, are necessary (Fiedler & Groom, 2006). Among terns in
general, and Chinese crested terns in particular, extended post-fledging
parental care is a life history trait that poses nearly insurmountable
obstacles for captive breeding programs. In the case of the Chinese
crested tern, whose breeding population is so small and widely dis-
tributed over an extensive breeding range, and the severity of the
threats still facing the species, creating a conservation network of
monitored breeding sites to safeguard all nesting attempts is regarded
as the best immediate conservation action.
Our results indicated that it is possible to establish new mixed
species breeding colonies of greater and Chinese crested terns using
social attraction techniques. Close monitoring and safeguarding of these
new colonies can protect the colonies from most major threats and
thereby enhance breeding success. Although the use of social attraction
at one colony site might impact the numbers of breeding adults at an-
other site, it is possible to achieve balanced colony sizes through co-
operation and coordination of social attraction efforts. This approach
was successfully used to sustain mixed species breeding colonies on
both Tiedun Dao and Yaqueshan in 2015 and 2017. With the popula-
tions of both greater crested terns and Chinese crested terns apparently
increasing, more new breeding colonies could be created using social
attraction. By persisting in this approach, a well-protected, closely-
monitored, and extensive conservation network of tern breeding islands
Fig. 4. Counts of individual adult and fledgling Chinese crested terns at extant breeding colonies during the 2000–2018 breeding seasons. Data from the Matsu
Islands is courtesy of Hung (2018), data from the Penghu Islands is courtesy of Qianxun Zheng, and data from Korea is courtesy of Yunkyoung Lee.
Y. Lu, et al. Biological Conservation 248 (2020) 108694
7
could be developed in the East China Sea, and potentially in the Yellow
Sea as well, where the Chinese crested tern was originally described.
Such an extensive conservation network of protected colony sites would
help spread the risk from major typhoons in the East China Sea during
the nesting season, typhoons whose strength, frequency, and overlap
with the tern nesting season are known to be increasing with climate
change (Chen et al., 2015).
In the future, a conservation network should include migratory
stopover sites and wintering sites across the Australasian-East Asia
Flyway, as well as breeding sites in the East China Sea and Yellow Sea.
Currently, there is still only a very limited understanding and knowl-
edge of the migratory stopover sites and wintering range of the Chinese
crested tern, and more research efforts are needed to elucidate the
species' habitat requirements during the non-breeding period. Although
restoration of a critically endangered species is usually a difficult, long-
term, and systematic mission with many risks of failure along the way,
creating a conservation network through social attraction offers an
opportunity to consolidate conservation achievements step by step, and
enhance the prospects of saving the Chinese crested tern from extinc-
tion.
Managing a conservation reliant species like the Chinese crested
tern in the long term will always be a major challenge, especially sus-
taining the funding support for crucial research and conservation ef-
forts. In recent years, however, as social attraction has been applied to
more sites in an effort to restore the population of Chinese crested terns,
the funding streams from governmental and non-governmental orga-
nizations for the conservation of this critically endangered species have
increased substantially. We remain optimistic that as the public be-
comes more aware of the plight of Chinese crested terns and as con-
servation awareness increases in China generally that the resources to
sustain this restoration effort will be available.
There are various ways to create a new breeding colony for different
species depending on their specific breeding ecology. It could be
achieved through social attraction, or chick translocation, or even by a
combination of these two techniques. It could also be achieved by fo-
cusing on just one species independently or, as in the case of Chinese
crested terns, by focusing on species that are closely-related or colony
associates. Nevertheless, we have shown that establishing a well-mon-
itored and protected network of breeding sites has widespread con-
servation implications for most seabirds. Among the 171 active seabird
restoration projects conducted in 16 countries/regions, at least 75
projects were determined to be successful in helping restore 34 different
seabird species (Zhou et al., 2017). Through the use of active restora-
tion techniques, robust conservation networks of breeding sites have
gradually been developed for some seabird species, including Atlantic
puffins (Fratercula arctica), Caspian terns (Hydroprogne caspia), roseate
terns (Sterna dougallii), common terns (Sterna hirundo), and Arctic terns
(Sterna paradisaea)(Roby et al., 2002;Kress et al., 2009;Jones and
Kress, 2012;Zhou et al., 2017).
China's coastline extends over 18,000 km, spanning temperate,
subtropical, and tropical regions. It includes rocky coasts and islets,
rapidly accreting soft shorelines, mangroves, and coral reefs. There are
a total of ca. 6500 uninhabited islands along the China coast within the
Bohai, Yellow, East China, and South China seas in 13 different pro-
vinces or districts. These islands provide a wide variety of potential
breeding habitats for seabirds. Currently, a total of 77 seabird species
have been recorded along the China coast. Among these species, 37
(48%) have been documented as breeding (Chen et al., 2018). As with
those of the Chinese crested tern, most breeding habitats and colonies
are facing severe threats, including illegal egg harvest, human dis-
turbance, habitat degradation and loss, marine pollution, declining food
availability, and increasing frequency and severity of typhoons. These
threats have resulted in the widespread loss of breeding colonies and
population declines (Chen et al., 2009;Fan et al., 2011;Chen et al.,
2015;Chen et al., 2018). The restoration project for the critically en-
dangered Chinese crested tern is the first attempt in China at active
restoration of a seabird population. It promises to provide much in-
valuable experience for the conservation of breeding seabirds and fa-
cilitate seabird restoration throughout China.
CRediT authorship contribution statement
Yiwei Lu: Conceptualization, Investigation, Data curation,
Writing - original draft. Daniel D. Roby: Conceptualization,
Methodology, Writing - review & editing. Zhongyong Fan:
Conceptualization, Methodology, Investigation, Data curation.
Simba Chan: Conceptualization, Investigation, Funding acquisition.
Donald E. Lyons: Conceptualization, Methodology. Chung-Hang
Hong: Investigation, Data curation. Siyu Wang: Investigation, Data
curation, Resources. Jia Yang: Investigation, Data curation,
Resources. Xiao Zhou: Investigation, Data curation. Dongdong
Chen: Investigation, Data curation. Hsiao-Wei Yuan: Supervision.
Shuihua Chen: Conceptualization, Methodology, Writing - review &
editing, Supervision, Project administration, Funding acquisition.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ-
ence the work reported in this paper.
Acknowledgments
We are grateful to Yunkyoung Lee and Qianxun Zheng from the
National Institute of Ecology in the Republic of Korea, and the Penghu
Wild Bird Society for providing data, and to the administration of the
Zhejiang Jiushan Archipelago Provincial Marine Ecological Nature
Reserve and the administration of the Zhejiang Wuzhishan Archipelago
Provincial Bird Nature Reserve for their assistance. We thank Stefanie
Collar, Qin Huang, Peng Ding, Chao Chen, Ho nam Leung, Andy Lee,
Chun Fai Lo, Liwei Liu, Xinjie Jin, Xiaojian Yu, Yining Chen, Jiang
Wang, Peng Zhang, Xiaosong Zhuang, Xudong Jiang, Yanhao Tian,
Huaizhen Ding, Qianmeng Guo, Kun Tan, Jie Gen, Zhiwen Yan, Vivian
Fu, Yat Tung Yu, Kirsten Bixler, Yasuko Suzuki, Zhongde Wang, Tingke
Lu, Juncheng Yang, Ankang Zhang, Zhijun Lou, and Guan Chen for
assistance with field work, and to Stephen Kress and Ping Ding for
advice. This study was funded by the National Natural Science
Foundation of China (grant nos. 30570251 and 31572291), the
Zhejiang Technological Research Project for Public Welfare
(LGN18C030001), the National Key R&D Program of China
(2017YFC1403500), the Biodiversity Investigation, Observation and
Assessment Program (2019-2023) of the Ministry of Ecology and
Environment of China, Zhejiang Rare and Endangered Wildlife Rescue
and Conservation Project (2017-2020), the Endangered Species
Monitoring Fund from the State Forestry Administration of China, the
Ocean Park Conservation Foundation (Hong Kong), the popular science
fund from the China Association for Science and Technology, the Japan
Fund for Global Environment, the Critically Endangered Animals
Conservation Fund of the US Fish and Wildlife Service (Wildlife
Without Borders), and a small grant from the Craig Harrison
Conservation Fund of the Pacific Seabird Group.
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