Migration is a life-history strategy that animals evolved to explore distant areas with abundant but seasonal food resources (Dingle and Drake 2007). Studies have shown that successful bird migration depends on both genetic and social factors (reviewed in Newton 2008). However, it still remains unknown whether inherent navigation mechanisms or post-natal learning has greater influence on migratory behavior in different bird taxa (Alerstam 2006). Both laboratory and field studies have demonstrated that migratory behavior (e.g., timing, direction, duration of migration) of some nocturnal passerines (e.g., Eurasian Blackcap, Sylvia atricapilla, Berthold and Pulido 1994; Swainson's Thrush, Catharus ustulatus, Delmore et al. 2015) was primarily influenced by genetic factors (Berthold 2004). Using tracking technology, researchers further revealed the importance of non-genetic factors on the migratory behavior of some long-lived birds (e.g., White Stork, Ciconia ciconia, Chernetsov et al. 2004; Whooping Crane, Grus americana, Mueller et al. 2013).

Red-crowned Crane (Grus japonensis) is a long-lived waterbird that distributes in Northeast Asia (mainly China, Russia, Japan, North and South Korea). Due to threatened habitat and low population numbers (∼3,050 individuals), it is classified as Endangered by the International Union for Conservation of Nature (IUCN 2019). Based on different migration habits, Red-crowned Cranes are divided into a migratory continental population (∼1,580 individuals) and a sedentary island population in Hokkaido, Japan (∼1,470 individuals) (BirdLife International 2018). The western migratory population mainly breeds in wetlands of Heilongjiang, Jilin, Liaoning and Inner Mongolia, and migrates to the Yellow River Delta and Yancheng in China during non-breeding seasons (Su and Zou 2012).

In December 2015, four Red-crowned Crane subadults were found in a village near Hulun Lake Nature Reserve in northeast China, which was not the species' normal wintering area. Three of them were fitted with unique identifiable color rings and were later proved to be hand-reared individuals released by Khingansky Nature Reserve on 21 April 2015, another one had an unknown origin. We deployed GPS-GSM transmitters on them as well as on another three wild Red-crowned Cranes in 2015 and 2016 to assess migration routes of both hand-reared and wild Red-crowned Cranes, with the objectives of 1) comparing differences in migration routes between them; 2) determining whether and how migratory behavior of hand-reared individuals would change among years.

Methods

Results

As of September 2018, we received a total of 48,574 locations, of which 46,870 were valid. Six out of fourteen tracked individuals completed at least one migration to and from breeding areas (Table 1 and Fig. 1). For hand-reared individuals, we received 162 valid locations from the first set of transmitters. After release on 21 May 2016, transmitters on three (2K6, 3K1, S43) of four hand-reared cranes functioned well and showed their synchronous eastward migration back to hatching site at KNR. While the fourth crane, 1K7, had a failed transmitter, and we have not received any information from it since transmitter failure. Transmitters of 2K6, 3K1 and S43 lost signals on 14, 21 and 24 June 2016, respectively, at KNR before they could start autumn migration. With the second set of transmitters attached April 2017, a total of 728 valid locations were recorded. After release on 24 April 2017, 2K6, 3K1 and S43 did not move back to KNR synchronously. Individual 2K6 and S43 arrived at KNR on 1 and 15 May respectively, while 3K1 died in Hulunbuir City, Inner Mongolia (49° 27′ 36″ N, 125° 00′ 00″ E; ca. 615.33 km away from release site) due to poisoning on 9 May 2017, on its way back to KNR. We lost signals from S43 on 24 June 2017 at KNR. On 31 October 2017, 2K6 started to follow the traditional migratory route of Red-crowned Cranes and wintered at Yellow River Delta and then successfully returned back to KNR in spring 2018 (Table 1; Fig. 1).

Table 1.

Detailed information on migratory performance of three wild and four hand-reared Red-crowned Cranes (Grus japonensis) tracked using GPS-GSM transmitters in north China between April 2015 and April 2018.

Figure 1.

Migration routes of six Red-crowned Cranes (Grus japonensis) tracked using GPS-GSM transmitters in north China between April 2015 and April 2018; (A) migration of three wild cranes (A02, A14, and A20) along regular migration routes used by the Red-crowned Crane western population between 2015 and 2017; (b) movements of three subadult cranes (2K6 and 3K1 were hand-reared individuals, S43 was with unknown origin) returning to Khingansky Nature Reserve in Russia after releasing on 16 May 2016 (dashed line rectangle in A shows area in b); (C) movements of 2K6, 3K1 and S43 returning to Khingansky Nature Reserve after releasing at Hulun Lake Nature Reserve on 24 April 2017, and subsequent corrected migrations of one hand-reared individual 2K6 in autumn 2017 and spring 2018.

For three natural-born crane individuals (A14, A20, A02), nine migration routes with 3,134 valid locations were recorded between October 2015 and April 2017 (Table 1). After release in 2015, crane A14 migrated north to its breeding ground in China-Russia border, while the other two individuals stayed in Lindian until the breeding season in 2015. Individuals A14 and A20 wintered each year in Yancheng, Jiangsu Province, while A02 wintered in Yellow River Delta where hand-reared 2K6 also wintered after rectifying its migration from previous years (Table 1; Fig. 1).

Discussion

Using tracking technology, we tracked both hand-reared and wild Red-crowned Cranes in this study. While wild individuals used normal north-south migration route, three hand-reared subadults took an abnormal west-east route for the first two years. In the third year, hand-reared individual 2K6 rectified abnormal migration route and traveled to the species' regular wintering site. We speculate that 2K6 either migrated with other subadult groups or its mate after reaching sexual maturity in 2017 (Red-crowned Crane reaches maturity at three to four years of age; Masatomi and Kitagawa 1974). Due to limited sample size, we cannot further explain the causes of their abnormal migratory behavior. However, it is certain that, in addition to promote understanding of bird migration, our findings bear important implications for the protection, re-wilding and reintroduction of cranes or other similar species.

The Red-crowned Crane western population now faces two major threats: high rates of individual loss (poisoning and loss of wild populations due to captivity) and habitat destruction (Wood et al. 2010; Su and Zou 2012; Zhou et al. 2016). Autopsy results showed that 3K1 died of eating seeds mixed with pesticide, which is a common form of poisoning reported (Zhou et al. 2014). The sedentary Red-crowned Crane population is stable but with low genetic variation (Harris and Mirande 2013; Akiyama et al. 2017). Researchers found that if migratory behavior was completely dominated by genetic factors, it was likely to persist, regardless of population size; however, for species relying mainly on learning for their first migration, small migratory populations may face strong “Allee effect (individual fitness tends to decline at low population density)”, which will ultimately lead to loss of migratory behavior (Stephens and Sutherland. 1999; Fagan et al. 2012; Berdahl et al. 2016; Foss-Grant et al. 2018). There has been success in reestablishing migratory behavior of Whooping Cranes using ultralight aircraft, but the process was very costly and labor-intensive (Ellis et al. 2003).

Artificial interventions are encouraged in protecting endangered species with small population size (Wang et al. 2018). Inexperienced migrants of some bird taxa (e.g., passerines and raptors) may rely on inherent navigation system to find correct way to wintering area for their first migration (Berthold 2004; Thorup et al. 2007; Mellone et al. 2016). For birds migrating in flocks (e.g., storks, cranes and bustards), the importance of learning has been proved: inexperienced migrants follow their parents or other elder group members for their first migration, so that correct migration route can be passed on (Palacín et al. 2011). Studies on White Stork and Sandhill Crane (Grus canadensis) also found that if the young failed to migrate with their parents or other members in the first year, they will experience higher rate of mortality during migration (Chernetsov et al. 2004; Hayes 2015). According to our study, when re-wilding captive-bred or reintroducing individuals of some long-lived species, experienced individuals should be included in the group to ensure successful migration (Teitelbaum et al. 2016).