Andrew M. Allen, Bruno J. Ens, Martijn van de Pol, Henk van der Jeugd, Magali Frauendorf, Henk-Jan van der Kolk, Kees Oosterbeek, Jeroen Nienhuis, Eelke Jongejans. 2019: Colour-ring wear and loss effects in citizen science mark-resighting studies. Avian Research, 10(1): 11. DOI: 10.1186/s40657-019-0151-z
Citation: Andrew M. Allen, Bruno J. Ens, Martijn van de Pol, Henk van der Jeugd, Magali Frauendorf, Henk-Jan van der Kolk, Kees Oosterbeek, Jeroen Nienhuis, Eelke Jongejans. 2019: Colour-ring wear and loss effects in citizen science mark-resighting studies. Avian Research, 10(1): 11. DOI: 10.1186/s40657-019-0151-z

Colour-ring wear and loss effects in citizen science mark-resighting studies

More Information
  • Corresponding author:

    Andrew M. Allen, Andrew.Allen@science.ru.nl

  • Received Date: 16 Aug 2018
  • Accepted Date: 07 Apr 2019
  • Available Online: 24 Apr 2022
  • Publish Date: 14 Apr 2019
  • Background 

    Ring wear and loss may have important consequences for mark-recapture studies that aim to estimate survival trends. Our study quantifies the rates of wear and loss from a long-running colour-ringing project of the Eurasian Oystercatcher (Haematopus ostralegus) in the Netherlands.

    Methods 

    Our analysis included 8909 colour-ringed oystercatchers with 118,071 resightings,predominantly ringed and observed by citizen scientists. We quantified how ring wear and loss may vary with ring colour and age,and how this may impact resighting probabilities. We then determined how ring loss may impact survival estimates and resighting probabilities of mark-recapture models by simulating four scenarios of how citizen scientists may resight and report birds with lost colour rings.

    Results 

    Annual rates of colour ring loss averaged 2.5% compared with 1% for ring wear,but lost rings also had a higher reporting probability (31.2%) than worn rings (10.3%). Lost rings may not directly impact survival estimates since 50% of oystercatchers with lost rings could still be uniquely identified. Ring wear and loss rapidly increased between 10 and 15 years after ringing. Rates of ring loss were comparable amongst ring colours,but the wear rate appeared higher for red and white rings compared to other colours. Rates of ring wear and loss varied significantly amongst different regions in our study,which were characterised as having different habitat features. Differential rates of ring wear may have important implications for studies conducted over large geographical scales or of multiple species.

    Conclusions 

    Based on simulations of ring loss in our population,estimates of apparent survival may be 0.3-1.2% lower whilst the impact of ring wear was deemed even lower. We developed a table of recommendations containing advice for ring fitting,data collection,study design,and mark-recapture analyses,so that future colour-ringing studies can benefit from our experiences in collecting and analysing data of ring wear and loss through citizen science.

  • Seasonal climatic changes and food availability fluctuations drive many species of animals to migrate between breeding and wintering areas (Alerstam et al. 2003; Newton 2008; Rappole 2013). For inexperienced juveniles, their long-distance migration is incredibly challenging (Klaassen et al. 2014; Oppel et al. 2015; Rotics et al. 2016; Vega et al. 2016) regardless of whether they travel by themselves (McKinnon et al. 2014) or follow adults (Sergio et al. 2014; Hewson et al. 2016; Meyburg et al. 2017). Juveniles may have migration strategies that differ from those of adults (Strandberg et al. 2010; McKinnon et al. 2014), such as choosing different movement patterns (Oppel et al. 2015), spending more time at stopover sites (Mellone et al. 2013), flying with large flocks to escape predators, or exploring new migration paths to accommodate environmental change (Yoda et al. 2017). Although the juvenile migration and wintering destination of several ardeid species have been examined (Jourdain et al. 2008; Geary et al. 2015), further conservation studies addressing the juvenile migration ecology of other species, especially those that are either threatened or depend on particular areas, are still needed (Rotics et al. 2016; Vega et al. 2016).

    The Chinese Egret (Egretta eulophotes) (Pelecaniformes: Ardeidae) is a globally vulnerable species with an estimated population below 10, 000 worldwide (BirdLife International 2020). It is a wetland-dependent bird, usually foraging in coastal wetlands, mainly breeding on offshore islands in eastern China, North Korea, South Korea and eastern Russia, and wintering in coastal regions of southeast Asia, with sightings of banded bird occurring in the Philippines, Indonesia, Malaysia, Singapore, Brunei, Vietnam and Thailand. This egret is a long-distance migrant, likely migrating through coastal South Korea, Japan and China. According to the IUCN, the Chinese Egret has suffered population reductions in recent decades because of the reclamation of tidal mudflats, estuarine habitats, and offshore breeding islands for agriculture and industry (BirdLife International 2020). Although many studies have focused on the breeding behavior, feeding ecology and genetics of the Chinese Egret (Zhou et al. 2010; Huang et al. 2013; Wang et al. 2013; Dai et al. 2015; Lei et al. 2016), and juvenile Chinese Egret migration data were collected from within China from 5 transmitters (Zhang et al. 2018), the transnational migration and wintering areas of this vulnerable species have not been studied.

    In this study, we documented the transnational migration and wintering areas of juvenile Chinese Egrets and aimed to: (1) identify and map juvenile Chinese Egret autumn migration routes with Global Positioning System (GPS) tracking, (2) determine their migration movement traits such as travel distance, migration duration, stopover duration and flight speed, and (3) identify their wintering areas. Our novel juvenile Chinese Egret migration data will provide a fundamental basis for further studies on the population dynamics and habitat conservation of this vulnerable species.

    Juvenile Chinese Egrets were captured on Fantuozi Island (39°9′12.16″ N, 122°18′ 19.84″ E) in Dalian, Liaoning Province, China (Fig. 1). This offshore island is located in the Yellow Sea and near Bohai Bay, and its distance from the mainland is approximately 11.9 km. Fantuozi Island has hosted a large breeding colony of vulnerable Chinese Egrets during April to October in recent years. The area of this breeding island is approximately 0.09 km2 and the island is uninhabited.

    Figure  1.  Migration routes and wintering areas of juvenile Chinese Egrets. Each line represents one individual. Red, blue, and orange lines represent inland, coastal, and oceanic routes, respectively. The dash line represents the route taken by females, and the solid line represents the route taken by males

    In August 2018, 39 fully flighted juvenile Chinese Egrets were captured on the ground near their nests at night using a hand-held net after they fledged, their weights and body length were measured, and some feathers were collected to extract DNA to unambiguously assign sex later in the laboratory (Huang et al. 2013). Then, the juveniles were fitted with solar-charged GPS/GSM transmitters (HQB-2512S, weight 14 g, or HQB-2009P, weight 9 g; Hunan Global Messenger Technology, China). The weight of the transmitter plus backpacks with a Teflon ribbon harness was approximately 2–4% of the average egret's weight (449.10 ± 43.21 g) (Hadjikyriakou et al. 2020). Both types of transmitters included a solar panel with rechargeable batteries, transmitting data at 2-h intervals via the GSM network. All birds were released within 2 h at the site of capture when no abnormal behavior or death was observed after transmitter attachment.

    Departure was considered to have occurred when new locations showed a significant southern movement and directional movements continued to occur (Huschle et al. 2013). The wintering area was based on the IUCN document or determined by both movements not continuing to move south and juveniles surviving through whole wintering period in the reached area during December–February to ensure that the data represent the locations of wintering birds. When a juvenile arrived at a wintering area, its autumn migration was considered complete. The autumn migration of juvenile Chinese Egrets was defined as the last point recorded from the vicinity of its natal island before departure until the first point reached in the wintering area, and using the WGS-84 (World Geodetic System 1984, used by all GPS devices) coordinate system, the migration distance was calculated by summing all the distances of consecutive migration locations between these two points, not including the variation in locations at stopover sites (Li et al. 2020). A stopover site was defined as an area when the speed was 0 km/h and where a juvenile stayed for at least 4 h (two GPS positions and intervals recorded with a transmitter) during the migration journey (Mi et al. 2018; Alonso et al. 2020). The inland and coastal migration routes indicated that more than two thirds of the juvenile stopover sites occurred in freshwater and coastal wetlands, respectively. Migration duration was defined as the total duration between the last date in the vicinity of the natal island before departure and the first date on which successfully arriving individuals reached the wintering area, including the periods spent at stopover sites (Huschle et al. 2013). Migration speed was calculated as the migration distance divided by the migration duration (Monti et al. 2018; Li et al. 2020). Night and day were defined as 6:00 p.m. to 6:00 a.m. and 7:00 a.m. to 5:00 p.m. Beijing time, respectively, depending on the transmitter's transmission at 2-h intervals via the GSM network and according to the closer local times of sunrise and sunset (https://richurimo.51240.com/orwww.timeanddate.com) in October in two time zones, UTC + 8 (China, Philippines, and Malaysia) and UTC + 7 (Vietnam), in which the juvenile Chinese Egrets passed during their autumn migration.

    The death of a tracked juvenile was identified on the basis of three indicators (Monti et al. 2018; Sergio et al. 2019): the transmission data indicated that the transmitter was functioning normally, GPS locations confirmed that the transmitter was stationary or the juvenile was not moving, and terminal temperature values followed the environmental temperature fluctuations. However, this indirect death identification sometimes cannot be distinguished from transmitter loss and hence might overestimate the mortality of juveniles. Therefore, the retrieval of carcasses or transmitters in the field was used to further confirm death and determine the cause of death if possible. Transmitter-failure (signal loss) was assumed to occur when the GPS signal was suddenly interrupted and no new GPS data were further received. This transmitter-failure identification procedure sometimes included death that occurred over the sea, as no carcass or transmitter could be found, and hence might underestimate mortality.

    GPS positions were utilized to map the migration routes of the juvenile Chinese Egrets, visualize their movements with Google Earth remote-sensing images (Google Inc. 2013), and identify their wintering areas (Klaassen et al. 2010; Page et al. 2014; Hadjikyriakou et al. 2020) via ArcGIS 10.3. A-test was used to analyze gender differences and all statistical analyses were conducted in R 3.5.1 (R Core Team 2018).

    Thirty-nine juvenile Chinese Egrets were captured and tracked in the summer of 2018, including 15 females and 24 males. During their first autumn journey, migration information was obtained for 30 tracked juveniles (14 females, 16 males), and 9 tracked juveniles (1 female, 8 males) died before starting migration (Table 1). Finally, 13 tracked juveniles (8 females and 5 males) successfully finished migration and arrived in the wintering area, 13 tracked juveniles unfortunately failed, and 4 lost signals during migration.

    Table  1.  Autumn migration information for juvenile Chinese Egrets
    Id Gender Complete migration Departure date Arrival date Migration route Migration distance (km) Flight speed (km/h) Max flight speed (km/h)
    JE1813 M N 2018/10/10 Coastal 65.0
    JE1814 F Y 2018/10/17 2018/10/22 Coastal 4437.93 50.43 81.8
    JE1815 M Y 2018/10/06 2018/10/10 Coastal 4274.24 57.76 83.9
    JE1816 F Signal lost 2018/10/06 Coastal 74.6
    JE1817 F N 2018/10/10 Coastal 90.2
    JE1818 M Y 2018/10/17 2018/10/21 Coastal 3872.42 56.95 92.2
    JE1819 F N 2018/09/23 Coastal 115.2
    JE1820 F N 2018/10/16 Coastal 74.2
    JE1821 M N 2018/10/17 Inland 79.7
    JE1822 F Y 2018/10/06 2018/10/08 Oceanic 3305.44 55.09 89.0
    JE1823 M Y 2018/10/17 2018/10/22 Coastal 3950.17 56.43 96.9
    JE1824 M N 2018/10/17 Inland 74.2
    JE1825 F Y 2018/09/30 2018/10/03 Coastal 4031.17 57.59 98.3
    JE1826 M N 2018/10/17 Coastal 83.2
    JE1828 M N 2018/10/26 Oceanic 93.5
    JE1829 M N 2018/10/06 Coastal 115.5
    JE1830 M N 2018/10/16 Coastal 88.6
    JE1831 M N 2018/10/16 Inland 71.4
    JE1832 F Y 2018/10/06 2018/10/10 Oceanic 3368.40 54.33 116.8
    JE1834 F Y 2018/10/28 2018/11/01 Coastal 3664.78 63.19 91.5
    JE1835 F Signal lost 2018/10/23 Coastal 92.5
    JE1837 F Y 2018/10/26 2018/10/29 Coastal 4358.56 62.27 106.6
    JE1838 M N 2018/10/26 Inland 87.7
    JE1839 F N 2018/10/01 Inland 76.9
    JE1842 M Y 2018/10/10 2018/10/15 Coastal 4562.74 71.29 95.3
    JE1844 F Y 2018/10/01 2018/10/05 Coastal 3451.76 49.31 100.4
    JE1845 M N 2018/11/16 Coastal 62.1
    JE1847 M Y 2018/10/06 2018/10/10 Coastal 3696.93 56.01 91.7
    JE1851 M Signal lost 2018/10/17 Coastal 79.9
    JE1852 F Y 2018/10/16 2018/10/22 Coastal 4091.75 53.84 89.0
     | Show Table
    DownLoad: CSV

    The juvenile Chinese Egrets departed southward from the vicinity of their natal island and underwent directional movements that continued to occur in a narrow range, with longitude ranging between 128.39° E and 105.76° E and latitude ranging from 40.55° N to 4.71° N. GPS tracking data showed that the juvenile Chinese Egrets migrated via three routes: coastal, inland, and oceanic (Fig. 1).

    The coastal route was most often used by the juvenile Chinese Egrets. Twenty-one of the tracked egrets (11 females, 10 males) migrated along this route, with 11 individuals successfully arriving in the wintering area. The juveniles flew along the eastern coast of Chinese mainland, passed across the Taiwan Strait and South China Sea, and finally arrived in their wintering area. On this journey, there were several stopovers in the coastal wetlands of China, including those in Shandong, Jiangsu, Shanghai, Zhejiang, Fujian, Taiwan, Guangdong, Guangxi, and Hainan.

    The inland route of juvenile Chinese Egrets was via Chinese mainland to the wintering area. On this journey, their stopovers were mainly distributed in the freshwater wetlands of Chinese mainland, including those in Anhui, Jiangxi, Hunan, and Guangxi. Six juveniles (one female, five males) migrated via this route (Fig. 1). Two flew inland but stayed in Guangxi, China, which is not a reported wintering area for the Chinese Egret, and died or lost data there in late winter. The other four juveniles died during inland migration, with one staying near the Poyang Lake in Jiangxi Province, China, for 51 days.

    The oceanic route of juvenile Chinese Egrets was a migration route in which juveniles flew over the Pacific Ocean to the wintering area. Three juveniles (two females, one male) migrated via this route, with two females directly arriving in the wintering area without a stopover. These two females flew over 3305.44 km in 56 h and 3368.40 km in 62 h across the Pacific Ocean. The male migrating via the oceanic route flew along the Korean Peninsula and Japan, and passed over the western Pacific Ocean but unfortunately died at a stopover site in Taiwan.

    The juvenile Chinese Egrets began their migration journeys between September 23rd and November 16th, with a departure peak occurring October 16th to 17th among eight males. Unlike males, females mostly embarked on different dates and most of them (N = 11, approximately 73%) left before October 16th (Table 1). These juveniles arrived in wintering areas between October 3rd and November 1st.

    Juvenile Chinese Egrets mainly migrated during the night. The total flight time for all juveniles (N = 30) was 622 h (79.85%) during the night from 6:00 p.m. to 6:00 a.m. and 157 h (20.15%) during the day. The complete migration duration of 13 juveniles averaged 5.08 ± 1.04 days, with the shortest time being approximately 3 days without stopover, and the longest duration was 7 days with 4 stopovers. There was no significant difference in migration duration between males (N = 5, 5.40 ± 0.55 days) and females (N = 8, 4.88 ± 1.25 days) (p > 0.05). The stopover duration of these 13 juveniles averaged 23.08 ± 19.28 h during the complete migration, ranging from 6 to 66 h. The flight speed during the complete migration averaged 57.27 ± 5.73 km/h, and the maximum speed reached 116.8 km/h. The migratory distance of these juvenile egrets during the complete migration averaged 3928.18 ± 414.27 km, ranging from 3305.44 to 4562.74 km. There was no significant difference in migration distance between males (4071.30 ± 345.35 km) and females (3838.72 ± 449.75 km) (p > 0.05).

    Our data map (Fig. 2) showed that five (three females, two males) juvenile Chinese Egrets arrived and wintered in the Philippines, four (two females, two males) arrived and wintered in Vietnam, and three (two females, one male) arrived and wintered in Malaysia. Two juveniles (one female, one male) stayed in Guangxi in China and died or lost data there in late winter, suggesting that Guangxi might be a newly recorded wintering area of the Chinese Egret. This observation needs to be further confirmed with more evidence, such as adult wintering records or juvenile survival through the whole wintering period. The wintering area covered 4.9127° N to 18.75929° N latitude and 105.76315° E to 122.28246° E longitude (Table 2). Of these juveniles, 12 individuals died while staying in their wintering areas, one (JE1815) lost its signal in January 2019, and only one successfully started its spring migration on June 2020 after staying in the Philippines for 606 days.

    Figure  2.  Wintering sites of juvenile Chinese Egrets. The blue circles represent the wintering sites for males, and the orange circles represent the wintering sites for females
    Table  2.  Wintering areas of juvenile Chinese Egrets
    Id Gender Country First-arrival longitude (°E) First-arrival latitude (°N) Longitude (°E) Latitude (°N) Survival time in wintering area (day)
    JE1814 F Malaysia 120.60222 13.49441 119.44778 4.9127 5
    JE1815 M Malaysia 116.68037 6.86859 116.65495 6.87045 Data lost in 5–5–2019 (207)
    JE1818 M Philippines 120.17426 12.15116 119.87864 12.40801 5
    JE1822 F Philippines 122.28246 13.88808 122.28246 13.88808 23
    JE1823 M Philippines 120.69018 14.95215 121.96769 10.71733 9
    JE1825 F Vietnam 109.42664 12.92982 109.42664 12.92982 35
    JE1832 F Philippines 121.22903 18.56443 120.20459 13.80685 484
    JE1834 F Vietnam 108.48739 15.68706 data lost Data lost Data lost
    JE1837 F Malaysia 116.65784 6.98118 116.65784 6.87118 17
    JE1842 M Vietnam 109.07333 13.89422 106.67048 10.12373 13
    JE1844 F Philippines 120.54535 14.79499 120.61732 13.96882 606 (spring migration in 6–1–2020)
    JE1847 M Vietnam 109.01347 14.89908 108.87021 15.07266 10
    JE1852 F Vietnam 105.79143 18.71875 105.76315 18.75929 10
     | Show Table
    DownLoad: CSV

    This GPS tracking study showed that the autumn migration of juvenile Chinese Egrets migrated southward via three routes: coastal, oceanic, and inland. The oceanic route was the first to be reported for this egret, and the coastal and inland routes were consistent with previous findings of studies tracking juvenile Chinese Egrets in China (Zhang et al. 2018). The oceanic route had a shorter migration distance (3336.92 km on average) and migration duration (59.00 h) than the coastal route (4035.68 km and 70.55 h, respectively). The coastal migration route was the most important for juvenile Chinese Egrets, as it was popular for autumn migration, suggesting that coastal wetlands are critical habitats for the conservation of the vulnerable Chinese Egret. The inland route, such as that used by one individual that stayed for 51 days in Poyang Lake in Chinese mainland, suggests that juvenile egrets might consume prey in freshwater habitats during the autumn migration. Previous nestling diet analyses on offshore breeding islands in southern China indicated that the nestlings depended on prey that only occurred in coastal wetlands (Fang et al. 2011).

    Our tracking data indicated that juvenile Chinese Egrets departed southward in autumn from the vicinity of their natal island to their wintering areas, the Philippines, Vietnam, and Malaysia, after a premigratory stage in early summer. This migration information is highly consistent with the typical pattern of autumn migration in other juvenile ardeid birds, such as Reddish Egrets (Egretta rufescens) (Geary et al. 2015) and Purple Herons (Ardea purpurea) (Jourdain et al. 2008). However, there are some differences in the movement traits of ardeid species. The average migratory distance of juvenile Chinese Egrets (3928.18 ± 414.27 km) was longer than that of juvenile Reddish Egrets (1140.41 ± 179.16 km) (Geary et al. 2015), and the average flight speed of juvenile Chinese Egrets (57.27 ± 5.73 km/h) was faster than that of juvenile Purple Herons (approximately 40 km/h) and juvenile Reddish Egrets (4.87 km/day) (Jourdain et al. 2008; Geary et al. 2015). Analyzing consistency and plasticity in migratory traits between short- and long-distance migrants within the same species is essential to understand the evolution and ontogeny of migratory strategies (Monti et al. 2018). The oceanic route of juvenile Chinese Egrets had a shorter migration distance (3336.92 km on average), fewer stopover (0), and slower flight speed (54.71 km/h) when compared to those of the coastal route (4035.68 km; 1.5; and 57.73 km/h, respectively). A study on short- and long-distance migratory Ospreys (Pandion haliaetus) showed that short-distance migration birds had shorter migratory distances, lower stopover use, and a faster flight speed when compared to long-distance migratory birds, suggesting that migration distance affects stopover use but not flight speed and that the lower flight speed is due to higher stopover use (Monti et al. 2018). Our data support the conclusion that migration distance affects stopover use when juvenile Chinese Egrets use a relatively direct oceanic route across the Pacific Ocean without stopovers but do not correspond with the suggestion that higher stopover use reduces flight speed.

    The mortalities of tracked juvenile Chinese Egrets were 23.08, 38.46, and 23.08% in the stages of premigration, migration and wintering, respectively. The associated high mortality indicates that autumn migration is a more critical time affecting the survival of juvenile Chinese Egrets than both the premigration and wintering periods. The first autumn migration is a crucial time for juveniles because of the combination of their relatively low mobility and inexperience. Juveniles may experience high costs associated with their relatively low flight performance because of their inexperience when using thermals (on land) or choosing favorable air currents (Mitchell et al. 2015). They may spend more time at stopover sites to refuel than older individuals due to their low foraging efficiency (Riotte-Lambert and Weimerskirch 2013). Moreover, juveniles may be more likely to interact naively with predators or venture into suboptimal habitats, decreasing their probability of obtaining adequate refuel and/or survival (Geary et al. 2015). In addition, during migration, the mortalities of our tracked juveniles along the coastal, oceanic, and inland route were 33.33, 33.33, and 83.33%, respectively. The juveniles successfully finished migration had significantly lower stopover use (N = 13; 1.38 ± 1.04) than the unsuccessful individuals (N = 14; 3.86 ± 2.60) (p < 0.01), suggesting that low stopover use may reduce mortality during autumn migration. When migrants increase their use of stopovers during the migratory period, they may experience a longer time over which to encounter harsh environmental conditions, leading to death.

    Our data support that the Chinese Egret is one of the key species making use of the East Asian–Australasian Flyway (EAAFP 2020). The migratory routes taken by juvenile Chinese Egrets stretch from China, southward through East Asia to wintering areas in Southeast Asia including the Philippines, Malaysia, and Vietnam, which could be identified as a part of the East Asian–Australasian Flyway (EAAFP 2020). During the migration journey, Chinese Egrets should rely on a system of healthy wetlands to rest and feed. The habitats along the flyway, ranging from important inland wetlands to coastal and offshore sites, are internationally important in supporting the vulnerable Chinese Egret. Among the three migratory routes used by juvenile Chinese Egrets, the coastal route was most often used, suggesting that coastal wetlands are particularly important for these birds. In the future, it is essential to identify and conserve a network of important wetlands used by the Chinese Egret throughout its migratory routes.

    Juvenile Chinese Egrets were found to migrate southward via three migration routes, coastal, oceanic, and inland, winter in the coastal wetlands of Southeast Asia, including the Philippines, Vietnam, and Malaysia, and begin their spring migration in the third year, which confirms that the Chinese Egret is one of the key species using the East Asian–Australasian Flyway. Among these routes, the oceanic route is newly reported in this study. Moreover, the coastal route is most often used by juveniles during autumn migration, suggesting that coastal wetlands are particularly important. The inland route used by some juveniles indicates that they may rely on freshwater wetland habitats. Our novel autumn migration data collected for the Chinese Egret suggest that international cooperation is important to conserve this vulnerable egret and the wetland habitats on which it depends. These results provide a fundamental basis for further studies to develop conservation plans for this vulnerable species.

    We thank Jingtao Liu, Danxia Xia, Ying Yin, and Yihuang Chen who helped attach transmitters and collect samples in field. We also thank Yuwei Huang, Haoran Luo, and Wei Xu for assistance in laboratory work of this study.

    ZH designed and performed the experiments, completed the analyses, and wrote the manuscript; XC and WF conceived, directed, and coordinated this study, helped with writing, and revised the manuscript. XZ collected some samples, assisted with analyses and lab work. HZ assisted with bird capture and transmitter attachment in field. All authors read and approved the final manuscript.

    The datasets used in the present study are available from the corresponding author on reasonable request.

    The license for this research in the study site was issued by the Forestry and Grassland Administration, Liaoning Province, China (Permission Number: 201810). This research and all procedures were approved by the Animal Ethics Committee in Xiamen University, China. Field work was conducted in the evening, and visits to a breeding colony were restricted to a maximum of two hours per day.

    Not applicable.

    The authors declare that they have no competing interests.

  • Allen AM, Singh NJ. Linking movement ecology with wildlife management and conservation. Front Ecol Evol. 2016;3:155.
    Allen AM, Ens BJ, van de Pol M, van der Jeugd H, Frauendorf M, Oosterbeek K, Jongejans E. Seasonal survival and migratory connectivity of Eurasian Oystercatchers revealed by citizen science. Auk. 2019;136:1-17. .
    Baccetti N, Morelli F. Which ring colour looks best: results of the Antequera 'Ophthalmic' tests. In: Béchet A, Rendón-Martos M, Amat JA, Baccetti N, Childress B, editors. Proceedings of the IVth international workshop on the greater flamingo in the Mediterranean region and northwest Africa. Flamingo Special Publication 1; 2009. pp. 78-9.
    Baylis SM, Drynan D, Clarke N, Van M, Sunnucks P, Clarke RH. Estimates of wear rates in metal bird bands, with applications for survival and movement models of marked individuals. J Field Ornithol. 2018;89:393-406.
    Bearhop S, Ward RM, Evans PR. Long-term survival rates in colour-ringed shorebirds—practical considerations in the application of mark-recapture models. Bird Study. 2003;50:271-9.
    Berthold P, Bauer HG, Westhead V. Bird migration: a general survey [Internet]. Oxford: Oxford University Press; 2001.
    Clark JA, Thorup K, Stroud DA. Quantifying the movement patterns of birds from ring recoveries. Ringing Migr. 2009;24:180-8.
    Clausen KK, Frederiksen M, Madsen J. Measuring neck collar loss of Pink-footed Geese Anser brachyrhynchus. Bird Study. 2015;62:137-40.
    Collins P, Jessop R, Minton C. Fading of colour-bands used on Pied Oystercatchers Haematopus longirostris and Sooty Oystercatchers H. fuliginosus in southeast Australia. Wader Study Gr Bull. 2002;99:50-3.
    Conn PB, Kendall WL, Samuel MD. A general model for the analysis of mark-resight, mark-recapture, and band-recovery data under tag loss. Biometrics. 2004;60:900-9.
    Durell SEALV. Differential survival in adult Eurasian oystercatchers Haematopus ostralegus. J Avian Biol. 2007;38:530-5.
    Duriez O, Sæther SA, Ens BJ, Choquet R, Pradel R, Lambeck RHD, Klaassen M. Estimating survival and movements using both live and dead recoveries: a case study of oystercatchers confronted with habitat change. J Appl Ecol. 2009;46:144-53.
    Duriez O, Ens BJ, Choquet R, Pradel R, Klaassen M. Comparing the seasonal survival of resident and migratory oystercatchers: Carry-over effects of habitat quality and weather conditions. Oikos. 2012;121:862-73.
    Ens BJ, Underhill LG. Synthesis of oystercatcher conservation assessments: general lessons and recommendations. Int Wader Stud. 2014;20:5-22.
    Ens BJ, Kersten M, Brenninkmeijer A, Hulscher JB. Territory quality, parental effort and reproductive success of Oystercatchers (Haematopus ostralegus). J Anim Ecol. 1992;61:703-15.
    Ens BJ, Aarts B, Hallmann C, Oosterbeek K, Sierdsema H, Slaterus R, Troost G, van Turnhout C, Wiersma P, Nienhuis J, van Winden E. Scholeksters in de knel: onderzoek naar de oorzaken van de dramatische achteruitgang van de Scholekster in Nederland. Nijmegen, Netherlands; 2011.
    Harris MP. Loss of weight and legibility of bird rings. Ringing Migr. 1980;3:41-9.
    Juillet C, Choquet R, Gauthier G, Pradel R. A capture-recapture model with double-marking, live and dead encounters, and heterogeneity of reporting due to auxiliary mark loss. J Agric Biol Environ Stat. 2011;16:88-104.
    Kennard JH. Longevity records of North American birds. Bird Band. 1975;46:55-73.
    Koronkiewicz TJ, Paxton EH, Sogge MK. A technique to produce aluminum color bands for avian research. J Field Ornithol. 2005;76:94-7.
    Laake JL. RMark: an R interface for analysis of capture-recapture data with MARK. AFSC Processed Report 2013-01, Seattle; 2013.
    Lyngs P. Wear and loss of rings used on Razorbills Alca torda—further caution in the estimation of large auk survival. Ringing Migr. 2006;23:39-44.
    Meissner W, Bzoma S. Colour rings with individual numbers increase the number of ringing recoveries of small waders. Wader Study Gr Bull. 2011;2:114-7.
    Méndez V, Alves JA, Gill JA, Gunnarsson TG. Patterns and processes in shorebird survival rates: a global review. Ibis. 2018;160:723-41.
    Milligan JL, Davis AK, Altizer SM. Errors associated with using colored leg bands to identify wild birds. J Field Ornithol. 2003;74:111-8.
    Mitchell C, Trinder M. On reading colour rings. Ringing Migr. 2008;24:11-4.
    O'Brien S, Robert B, Tiandry H. Consequences of violating the recapture duration assumption of mark-recapture models: a test using simulated and empirical data from an endangered tortoise population. J Appl Ecol. 2005;42:1096-104.
    Pigniczki C, Kralj J, Volponi S, Žuljević A, Dakhli M-A, Mikuska T, Azafzaf H, Végvári Z. Migration routes and stopover sites of the Eurasian Spoonbill (Platalea leucorodia) between the Carpathian Basin and wintering areas. Ornis Hung. 2016;24:128-49.
    Rees EC, Owen M, Gitay H, Warren S. The fate of plastic leg rings used on geese and swans. Wildfowl. 1990;41:43-52.
    Reynolds TJ, King R, Harwood J, Frederiksen M, Harris MP, Wanless S. Integrated data analysis in the presence of emigration and mark loss. J Agric Biol Environ Stat. 2009;14:411-31.
    Robinson RA, Clark NA, Lanctot R, Nebel S, Harrington B, Clark JA, Gill JA, Meltofte H, Rogers DI, Rogers KG, Ens BJ, Reynolds CM, Ward RM, Piersma T, Atkinson PW. Long term demographic monitoring of wader populations in non-breeding areas. Wader Study Gr Bull. 2005;106(April):17-29.
    Robinson RA, Grantham MJ, Clark JA. Declining rates of ring recovery in British birds. Ringing Migr. 2009;24:266-72.
    Roche EA, Dovichin CM, Arnold TW. Field-readable alphanumeric flags are valuable markers for shorebirds: use of double-marking to identify cases of misidentification. J Field Ornithol. 2014;85:329-38.
    Roodbergen M, van der Werf B, Hötker H. Revealing the contributions of reproduction and survival to the Europe-wide decline in meadow birds: review and meta-analysis. J Ornithol. 2012;153:53-74.
    Runge CA, Martin TG, Possingham HP, Willis SG, Fuller RA. Conserving mobile species. Front Ecol Environ. 2014;12:395-402.
    Rutten AL, Oosterbeek K, Verhulst S, Dingemanse NJ, Ens BJ. Experimental evidence for interference competition in oystercatchers, Haematopus ostralegus. II. Free-living birds. Behav Ecol. 2010;21:1261-70.
    Safriel UN, Harris MP, Brooke MDL, Britton CK. Survival of breeding oystercatchers Haematopus ostralegus. J Anim Ecol. 1984;53:867-77.
    Sandvik H, Erikstad KE, Barrett RT, Yoccoz NG. The effect of climate on adult survival in five species of North Atlantic seabirds. J Anim Ecol. 2005;74:817-31.
    Seber GAF. A review of estimating animal abundance. Biometrics. 1986;42:267-92.
    Senar JC, Carrillo-Ortiz J, Arroyo L. Numbered neck collars for long-distance identification of parakeets. J Field Ornithol. 2012;83:180-5.
    van de Pol M, Bruinzeel LW, Heg D, van der Jeugd HP, Verhulst S. A silver spoon for a golden future: long-term effects of natal origin on fitness prospects of oystercatchers (Haematopus ostralegus). J Anim Ecol. 2006;75:616-26.
    van de Pol M, Vindenes Y, Sæther B-E, Engen S, Ens BJ, Oosterbeek K, Tinbergen JM. Effects of climate change and variability on population dynamics in a long-lived shorebird. Ecology. 2010;91:1192-204.
    van de Pol M, Atkinson PW, Blew J, Crowe O, Delany S, Duriez O, Hötker H, Laursen K, Oosterbeek KH, Petersen A, Thorup O, Tjørve K, Triplet P, Yésou P. A global assessment of the conservation status of the nominate subspecies of Eurasian Oystercatcher Haematopus ostralegus ostralegus. Int Wader Stud. 2014;20:47-61.
    Walker RH, Robinson RA, Leech DI, Moss D, Kew AJ, Barber LJ, Barimore CJ, Blackburn JR, Clewley GD, De Palacio DX, Grantham MJ, Griffin BM, Schäfer S, Clark JA. Bird ringing and nest recording in Britain and Ireland in 2014. Ringing Migr. 2015;30:84-147.
    Ward RM. Darvic colour-rings for shorebird studies: manufacture, application and durability. Int Wader Study Gr Bull. 2000;91:30-4.
    Weiser EL, Lanctot RB, Brown SC, Gates HR, Bentzen RL, Bêty J, Boldenow ML, English WB, Franks SE, Koloski L, Kwon E, Lamarre J-F, Lank DB, Liebezeit JR, McKinnon L, Nol E, Rausch J, Saalfeld ST, Senner NR, Ward DH, Woodard PF, Sandercock BK. Environmental and ecological conditions at Arctic breeding sites have limited effects on true survival rates of adult shorebirds. Auk. 2018;135:29-43.
    White GC, Burnham KP. Program MARK: survival estimation from populations of marked animals. Bird Study. 1999;46:S120-39.
    Wood KA, Nuijten RJM, Newth JL, Haitjema T, Vangeluwe D, Ioannidis P, Harrison AL, Mackenzie C, Hilton GM, Nolet BA, Rees EC. Apparent survival of an Arctic-breeding migratory bird over 44 years of fluctuating population size. Ibis. 2018;160:413-30.
  • Related Articles

  • Cited by

    Periodical cited type(27)

    1. Geng Huang, Wenjia Hu, Jianguo Du, et al. Identification and scenario-based optimization of ecological corridor networks for waterbirds in typical coastal wetlands. Ecological Indicators, 2025, 171: 113147. DOI:10.1016/j.ecolind.2025.113147
    2. Jackson Barratt Heitmann, Travis H. Folk, Lisa J. Lord, et al. Geographically isolated wetlands have higher alpha diversity than surrounding uplands in pine savanna ecosystems. Wetlands Ecology and Management, 2025, 33(1) DOI:10.1007/s11273-025-10035-6
    3. Abdallah Aouadi, Farrah Samraoui, Zineb Bouhala, et al. Macrophyte cover and environmental factors shaping macroinvertebrate diversity in a Mediterranean urban pond. Wetlands Ecology and Management, 2025, 33(1) DOI:10.1007/s11273-024-10025-0
    4. Thomas Pagnon, Clémence Péchinot, Léa Sgro, et al. Structural effects of reedbed grazing and its cessation on reed-nesting songbird densities. Avian Research, 2024, 15: 100182. DOI:10.1016/j.avrs.2024.100182
    5. Jan Giordano, Filippo Moretti, Corrado Battisti. Pattern in water-related birds reveals a shift in biomass between mature and mowed reedbeds: evidence from a coastal wetland. Ethology Ecology & Evolution, 2024, 36(6): 679. DOI:10.1080/03949370.2024.2411508
    6. Jacob G. Davies, Calvin Dytham, Robert A. Robinson, et al. Estimating the distribution of reedbed in Britain demonstrates challenges of remotely sensing rare land cover types at large spatial scales. Scientific Reports, 2024, 14(1) DOI:10.1038/s41598-024-73030-6
    7. Michela Ingaramo, Anna Rita Bernadette Cammerino, Vincenzo Rizzi, et al. Birds as Cultural Ambassadors: Bridging Ecosystem Services and Biodiversity Conservation in Wetland Planning. Sustainability, 2024, 16(23): 10286. DOI:10.3390/su162310286
    8. Giuliana Romero-Mariscal, Pablo A. Garcia-Chevesich, Lino Morales-Paredes, et al. Peruvian Wetlands: National Survey, Diagnosis, and Further Steps toward Their Protection. Sustainability, 2023, 15(10): 8255. DOI:10.3390/su15108255
    9. Pierre Mallet, Arnaud Bechet, Clelia Sirami, et al. Field margins as substitute habitat for the conservation of birds in agricultural wetlands. Peer Community Journal, 2023, 3 DOI:10.24072/pcjournal.299
    10. Qifan Liang, Jun Zhai, Chang Li. From separation to incorporation: Development of a unifying framework that integrated bird habitats with public recreation spaces within the wetland park system. Journal of Cleaner Production, 2023, 430: 139647. DOI:10.1016/j.jclepro.2023.139647
    11. Henrique C. Delfino. A fragile future for pink birds: habitat suitability models predict a high impact of climate change on the future distribution of flamingos. Emu - Austral Ornithology, 2023, 123(4): 310. DOI:10.1080/01584197.2023.2257757
    12. Emanuele Fasola, Fabrizio Stefani, Giovanni Forcina, et al. Exploratory Analyses of Sexual Size Dimorphism (SSD) and Sexual Dichromatism (SD) in Free-Living Adult Purple Herons (Ardea purpurea). Waterbirds, 2023, 45(3) DOI:10.1675/063.045.0314
    13. Mauro Fasola, Daniele Pellitteri-Rosa, Guido Pinoli, et al. Five decades of breeding populations census for 12 species of colonial waterbirds in northwestern Italy. Scientific Data, 2023, 10(1) DOI:10.1038/s41597-023-02072-8
    14. William Higgisson, Adrian Cobb, Alica Tschierschke, et al. The Role of Environmental Water and Reedbed Condition on the Response of Phragmites australis Reedbeds to Flooding. Remote Sensing, 2022, 14(8): 1868. DOI:10.3390/rs14081868
    15. Christian Stratton, Kathryn M. Irvine, Katharine M. Banner, et al. Coupling validation effort with in situ bioacoustic data improves estimating relative activity and occupancy for multiple species with cross‐species misclassifications. Methods in Ecology and Evolution, 2022, 13(6): 1288. DOI:10.1111/2041-210X.13831
    16. D. Scridel, S. Tenan, M. Brambilla, et al. Early-succession secondary forests following agropastoral abandonment are key winter habitats for the conservation of a priority bird in the European Alps. European Journal of Forest Research, 2022, 141(6): 1029. DOI:10.1007/s10342-022-01485-1
    17. Mauro Fasola, Elisa Cardarelli, Luigi Ranghetti, et al. Changes in rice cultivation affect population trends of herons and egrets in Italy. Global Ecology and Conservation, 2022, 36: e02135. DOI:10.1016/j.gecco.2022.e02135
    18. Francesco Pio Tozzi, Marco Varricchione, Maria Carla de Francesco, et al. Vegetation Dynamics on a Restored salt Marsh Mosaic: a Re-Visitation Study in a Coastal Wetland in Central Italy. Wetlands, 2022, 42(8) DOI:10.1007/s13157-022-01627-6
    19. Matteo Anderle, Chiara Paniccia, Mattia Brambilla, et al. The contribution of landscape features, climate and topography in shaping taxonomical and functional diversity of avian communities in a heterogeneous Alpine region. Oecologia, 2022, 199(3): 499. DOI:10.1007/s00442-022-05134-7
    20. Somayeh Alikhani, Petri Nummi, Anne Ojala. Urban Wetlands: A Review on Ecological and Cultural Values. Water, 2021, 13(22): 3301. DOI:10.3390/w13223301
    21. Chukwuemeka Onwuka Martins, Oluwatobi Emmanuel Olaniyi, Mohamed Zakaria. Environmental Factors and Spatial Heterogeneity Affect Occupancy Estimates of Waterbirds in Peninsular Malaysia. Ornithological Science, 2021, 20(1) DOI:10.2326/osj.20.39
    22. Swades Pal, Sandipta Debanshi. Machine learning models for wetland habitat vulnerability in mature Ganges delta. Environmental Science and Pollution Research, 2021, 28(15): 19121. DOI:10.1007/s11356-020-11413-8
    23. C.O Martins, O.E Olaniyi, M Zakaria. Ecological factors and spatial heterogeneity of Terrestrial Birds in Peninsular Malaysia. IOP Conference Series: Earth and Environmental Science, 2021, 736(1): 012035. DOI:10.1088/1755-1315/736/1/012035
    24. Mattia Brambilla, Franco Rizzolli, Alessandro Franzoi, et al. A network of small protected areas favoured generalist but not specialized wetland birds in a 30-year period. Biological Conservation, 2020, 248: 108699. DOI:10.1016/j.biocon.2020.108699
    25. Bruno Pereira Berto, Carlos Wilson Gomes Lopes. Coccidia of Wild Birds as Ecological Biomarkers: Some Approaches on Parasite-Host-Environment Interaction. Journal of Parasitology, 2020, 106(5) DOI:10.1645/19-148
    26. Navid Ghajarnia, Georgia Destouni, Josefin Thorslund, et al. Data for wetlandscapes and their changes around the world. Earth System Science Data, 2020, 12(2): 1083. DOI:10.5194/essd-12-1083-2020
    27. Guido Brusa, Michele Dalle Fratte, Giuseppe Bogliani, et al. [Wetlands in the Continental biogeographical region of Northern Italy: from scenarios of change to conservation perspectives]. Natural History Sciences, 2019, 6(2) DOI:10.4081/nhs.2019.427

    Other cited types(0)

Catalog

    Figures(4)  /  Tables(6)

    Article Metrics

    Article views (197) PDF downloads (8) Cited by(27)

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return