Migration strategies of Swan Geese Anser cygnoides from ... · toward a staging area at the Yalu River Estuary on the China-North Korea border. After staging for several weeks, the

90

© Wildfowl & Wetlands Trust Wildfowl (2011) 61: 90–109

Migration strategies of Swan Geese Anser

cygnoides from northeast Mongolia

NYAMBAYAR BATBAYAR1,6*, JOHN Y. TAKEKAWA2, SCOTT H. NEWMAN3, DIANN J. PROSSER4,

TSEVEENMYADAG NATSAGDORJ5 & XIANGMING XIAO1

1Department of Botany and Microbiology, College of Arts and Sciences, Earth Observation and Modeling Laboratory, University of Oklahoma, Norman,

OK 73019-5300, USA. 2U.S. Geological Survey, Western Ecological Research Center, 505 Azuar Drive Vallejo,

CA 94592, USA. 3Food and Agriculture Organization of the United Nations, EMPRES Wildlife Unit,

Viale delle Terme di Caracalla, Rome 00153, Italy. 4U.S. Geological Survey, Patuxent Wildlife Research Center, BARC-East Bldg 308,

10300 Baltimore Ave, Beltsville, Maryland, 20705, USA.5Mongolian Academy of Sciences, Institute of Biology, Zukov Ave., Ulaanbaatar 210351,

Mongolia.6Wildlife Science and Conservation Center of Mongolia, Undram Plaza 404 toot,

Ulaanbaatar 210351, Mongolia.*Correspondence author. E-mail: [email protected]

Abstract

In 2006–2008, 25 Swan Geese Anser cygnoides were marked with solar-powered GPSsatellite transmitters in northeast Mongolia to examine the timing and pathways oftheir migration. Most geese began their autumn migration in August, flying southeasttoward a staging area at the Yalu River Estuary on the China-North Korea border.After staging for several weeks, the Swan Geese continued to their wintering groundsat wetlands along the Yangtze River Basin of eastern China in December. Springmigration commenced in late February, and the birds following either a same-route orloop migration to arrive at the breeding grounds in mid April. Swan Geese used alarger number of staging areas for a longer duration when they were north of 42°N latitude; they seemed to avoid staging for extended periods in the highlyurbanised areas of eastern China. Further research should examine threats anddisturbances to the geese in relation to human population growth and increasingurbanisation.

Key words: Anser cygnoides, East Asian Flyway, migration, satellite telemetry, SwanGoose.

Swan Goose migration strategies 91


Understanding local movements andmigration across large landscapes is criticalfor identifying the factors that influence thesurvival of migratory birds and for devisingeffective conservation strategies (Berger2004; Newton 2007). Migration dataprovide insights into specific areas used,migratory connectivity, timing, stopoversites, migratory behaviour and physiology(Berthold et al. 2003; Robinson et al. 2010).In addition, use of satellite tracking data has improved our understanding of theecology of diseases such as avian influenzaand the connectivity between outbreak areas and wild bird locations (Gaidet et al.

2010; Newman et al. 2009; Takekawa et al.

2010). The Swan Goose Anser cygnoides is a

globally threatened species listed as“vulnerable” in the latest Red List ofThreatened Species of the InternationalUnion for Conservation of Nature andoccurs only in East Asia (BirdLifeInternational 2009). Recent counts madeboth at the breeding grounds in Mongoliaand Russia (Goroshko 2003; Goroshko et al.

2004; Tseveenmyadag et al. 2007) and atwintering sites in China (Zhang et al. 2010)indicate a dramatic decline in numberswhich has been attributed to: drought-induced wetland loss, disturbance of nestingbirds by livestock, competition withlivestock for grazing areas, illegal hunting,egg collection, reduction in the abundanceof submerged vegetation (i.e. the birds’ food supply) due to water pollution and dam water regulation, and wetlandconversion for agriculture and developmentprojects (Goroshko 2003; Goroshko et al.

2004; Poyarkov 2001; Poyarkov 2006;

Tseveenmyadag et al. 2007; Zhang et al. 2010;Fox et al. 2011). The decreasing populationsize may also be related to habitat change ordegradation at stopover sites along themigration flyway. Furthermore, the highlypathogenic avian influenza H5N1 virus,which has been reported across the SwanGoose wintering range, poses a significantthreat to this species.

In 2006 and 2008, moulting geese werefitted with satellite transmitters and trackedfrom their breeding sites on the MongolDaguur in northeast Mongolia to theirwintering grounds in the Yangtze RiverBasin of eastern China. Global positioningsystem (GPS) location data were used todescribe their annual migration in detail,including identifying stopover and winteringsites, documenting the timing of migration,and delineating migration corridors alongthe East Asian Flyway. In addition toproviding the first documentation of thecomplete migration cycle of the SwanGoose, a major focus of this study was todetermine how the birds used the landscapein relation to human populations. We hope that the greater knowledge andunderstanding of how Swan Geese use thelandscape, provided by tracking themovements of individual birds, will help toimprove the prospects of conservationefforts directed at this species.

Study area and methods

The Mongol Daguur region can becharacterised as a vast temperate grasslandsteppe, with low mountains and rolling hills,and with numerous small and medium sizedsteppe lakes and wetlands. Nomadic herdersand their livestock are the main populations

92 Swan Goose migration strategies


in the area. Most lakes in this region are fedby rain water; only a few are fed by runningrivers and streams. The lake and wetlandsteppe landscape extends north intoneighbouring Russia and east into China;this border region of the three countries isan important area for the Swan Goose andmany other wetland-dependent species innortheast Asia (BirdLife International2005).

Swan Geese were captured during theirmoulting period by herding them into adrive-trap or by capturing them in dip-netsfrom boats. A total of 25 Swan Geese were caught at the Khaichiin Tsagaan Lake(49.683°N, 114.684°E) in the MongolDaguur of northeast Mongolia in July 2006(Fig. 1), and a further 41 geese at KhaichiinTsagaan Lake, Khorin Tsagaan Lake(49.661°N, 114.606°E), and Khokh Lake(49.540°N, 115.585°E), in the same regionof northeast Mongolia, in 2008. Allcaptured geese were tested for the avianinfluenza virus, but none were found to bepositive (authors’ unpubl. data). Geese weremeasured and marked with aluminium metalleg rings and plastic neck collars forindividual identification, using orange neckcollars with black alphanumeric codes (withone letter and two numbers) in 2006 andgreen neck collars with white alphanumericcodes in 2008.

We fitted 45 g or 70 g solar-poweredArgos-GPS platform transmitter terminals(PTTs: Microwave Telemetry, Inc., Columbia, MD, USA) to the backs of selected adults,using a teflon-ribbon harness (Bally RibbonMills, Bally, PA, USA). Ten 70 g transmitterswere fitted in 2006 and fifteen 45 gtransmitters in 2008. Backpack harnesses for

the transmitters were reinforced to preventloss, because Swan Geese have very strongbills and their lower mandibles are serratedfor cutting plants and grasses. The weight ofthe transmitter and harness was < 3% of thebirds’ body mass. Birds were released assoon as possible after marking, typicallywithin an hour, back at their capturelocations. Procedures for capture, handlingand marking were reviewed and approved by the U.S. Geological Survey PatuxentWildlife Research Center Animal Care and Use Committee, and also by theUniversity of Maryland Baltimore CountyInstitutional ACUC (Protocol EE070200710). Transmitters were programmed to recordGPS locations every 2 h and Argos locationsdownloaded every 2–3 days. Only geese thathad complete migration routes wereincluded in analyses, and only GPS datawere used, which are typically accurate todistances of < 10 m.

The annual cycle of the Swan Goose was divided into five different periods: 1) autumn (southbound) migration, 2)wintering, 3) spring (northbound) migration, 4) breeding season, and 5) moulting or post-breeding. We examined the location dataand used specific areas, duration of stay, andscale of movements to estimate the durationof these periods. Movement from themoulting and wintering areas was used toindicate the onset of migration. Geese wereclassified as breeding if the GPS fixes werefound to be in very close proximity to eachother at a site over more than a one-weekperiod during the breeding season (Ely et al.

2007). The arrival time was defined as thefirst date that Swan Geese were detected onthe breeding grounds. Swan Geese prefer



to use larger lakes for moulting because they provide more safety when flightless(authors’ pers. obs.). We assumed thatmovements of several kilometres frombreeding areas on smaller lakes to largerlakes indicated that the birds had moved to moulting grounds. Staging areas, where migrating birds store fuel formigration, were identified as sites wherebirds remained in the vicinity (i.e. no large-scale movements to or from the siteoccurred) over a period of ≥ 7 days duringthe migration period (Warnock 2010). Visualinspection of locations in close proximityand limited movements at the southern endof the migration were used as cut-off datesfor the autumn migration and to determinearrival at the wintering grounds (Oppel et al.

2008). Various factors such as food supply, local

environment, weather, proximity to mainwintering areas, and hunting pressure maydisturb and eventually influence the timingof bird migration (Berthold et al. 2003). Inthis study, the linear distance from stopoverlocations to the nearest urban area was usedas an indicator of potential disturbance toSwan Geese along the migration route(Benitez-Lopez et al. 2010). Furthermore,we examined the flight speeds and distancestravelled by birds between consecutivelocations to see whether flights north andsouth of 42°N differed significantly, withthe density of urban areas in the SwanGoose flyway generally being higher southof this latitude (Fig. 1). A Wilcoxon signed-rank test was used to test whether there wasa significant difference in the average speedsand flight distances recorded for individualbirds during spring and autumn migration.

Analyses were conducted and box plotsproduced using R statistical software (RDevelopment Core Team 2011). Mean flightduration and distances are given with s.d.values throughout.

The European Space Agency’s GlobCover land cover map with 300 m spatialresolution (Bicheron et al. 2008) producedfor the period December 2004 – June 2006was used to determine land cover types atstopover and staging locations along theSwan Goose migration route in East Asiaand for calculating distances between townsor villages and stopover locations. Locationdata were plotted within ArcGIS 9.3 (ESRI2008) to determine the migration route andstopover sites, and to calculate the flightdistances of Swan Geese. The 50%, 95%and 99% fixed kernel home ranges werecalculated using Hawth’s Analysis Tools(Beyer 2004) in ArcGIS 9.3 to determine the areas used by Swan Geese staging at theYalu River Estuary (39.869°N, 124.301°E)and wintering at Poyang Lake (29.217°N,115.960°E), including defining theboundaries of movements by individualgeese in these areas.

Results

Ten geese were fitted with satellitetransmitters in 2006 and 15 geese in 2008.Overall, 17 (68%) birds provided satellitetracking data useful for evaluatingmigration. Fourteen of the useful trackswere from the 2008 deployment, but onlythree of 10 geese from 2006 yielded data.Although the other seven birds appearednormal upon release, they did not swim well,and five were recaptured by the next day. Wefound that they had been adversely affected



by capture myopathy, because for shortperiods they had entangled their wings orfeet in the small-mesh fishing net used as a holding pen that year (a different type of holding pen was used in subsequentyears).

A total of 15,458 GPS fixes wereobtained with an average of 858 locationsper individual, ranging from 14–2,420locations per bird. Such large individualvariation was influenced primarily by theduration over which signals were received

Figure 1. Migration paths, locations, and important stopover sites of Swan Geese marked with satellitetransmitters in northeast Mongolia. Swan Geese were captured at the Mongol Daguur, and many usedthe Yalu River Estuary as a major staging site. Poyang Lake was the main wintering area along theYangtze River Basin. White circles = major stopover locations; black shading = urbanised areas.



Tab

le 1

.M

orph

olog

ical

dat

a fo

r Sw

an G

eese

fitt

ed w

ith s

atel

lite

tran

smitt

ers

and

a su

mm

ary

of th

e pe

rfor

man

ce o

f th

e tr

ansm

itter

s.

Sa

tell

ite

Sex

Ag

eW

eig

ht

Cu

lmen

T

ars

us

Sta

rt d

ate

of

Da

te l

ast

T

ota

l T

ota

l

ID(g

)(m

m)

(mm

)tr

an

smis

sio

nsi

gn

al

da

ys

wit

h

nu

mb

er

of

receiv

ed

sig

na

lsG

PS

fix

es

67578

FA

d35

5040

.583

530

-Jul

-06

17-S

ep-0

650

378

67585

FA

d26

00–

986

30-J

ul-0

613

-Nov

-07

472

1618

67697

FA

d25

00–

–30

-Jul

-06

30-N

ov-0

612

472

182101

FA

d27

0098

.684

.529

-Jul

-08

2-D

ec-0

812

781

182102*

MA

d29

0010

3.4

89.6

29-J

ul-0

84-

Nov

-08

9914

82103

FA

d29

2084

81.9

27-J

ul-0

89-

Dec

-08

135

437

82104

MA

d38

0089

.292

.627

-Jul

-08

24-A

ug-0

829

134

82105

FA

d34

9095

.391

.526

-Jul

-08

18-A

ug-0

938

92,

302

82106

FSu

bad

2550

84.7

75.4

27-J

ul-0

827

-Sep

-08

6341

882107

FA

d31

0090

.580

.527

-Jul

-08

27-N

ov-0

948

91,

534

82108

FA

d28

5092

.779

.927

-Jul

-08

18-A

ug-0

938

82,

420

82109

MA

d31

5089

84.6

27-J

ul-0

823

-Sep

-08

5946

882110

MA

d17

0089

.980

.527

-Jul

-08

20-D

ec-0

814

731

482111

FA

d27

5088

.275

.827

-Jul

-08

13-M

ay-0

929

11,

954

82112

MA

d–

80.7

77.7

27-J

ul-0

810

-Dec

-08

137

1,10

082113

FA

d27

2088

.180

.527

-Jul

-08

5-N

ov-0

810

230

682114

MA

d27

0083

.876

.429

-Jul

-08

5-Se

p-08

3922

782115

MA

d31

0055

.450

.327

-Jul

-08

3-Se

p-08

3930

2

*Not

incl

uded

in th

e an

alys

is



(range = 29–489 days; Table 1). Departurefrom the post-breeding area wasdocumented for 17 birds, five of whichprovided complete autumn and springmigration histories, and twelve birds hadpartial migration histories. Two geese withworking transmitters made autumnmigrations in the second year after capture.All birds migrated within the East AsianFlyway.

Autumn migration

The route and timing of the autumnmigration was documented for six male andeleven female geese (Table 2). Autumnmigration started between 3 August and 16 September (median date = 8 August,

n = 19). Most birds started their migration inAugust, but two birds (transmitter numbers82103 and 82108) started in September in 2008. Signals for five birds (#67578,82104, 82110, 82114 and 82115) that startedtheir autumn migration ended beforereaching the Hinggan Mountains in InnerMongolia, China. Ten Swan Geeseprogressed across eastern Mongolia and theManchurian Plain to the Yalu River Estuaryon the border of China and North Korea,but from here they flew southwest towintering areas in east China. Two SwanGeese migrated to areas at the same latitudeas the Yalu River Estuary but flew directlysouth to the wintering grounds (#67585,82113).

Table 2. Chronology and movements of satellite-tracked Swan Geese during their annualcycle.

Migration periods Autumn Winter Spring Breeding Post-

migration migration breeding

No. of geese tracked 17 5 5 5 3

Start or arrival date (range) 3 Aug– 23 Oct– 25 Feb– 13 Apr– 16 Jun– 16 Sep 1 Jan 5 Apr 4 Jun 22 Jun

Start or arrival date 8 Aug 7 Dec 14 Mar 9 May 21 Jun(median date)

Min–Max duration (days) 74–146 56–155 30–66 43–70 61–65

Average duration ± s.d. 107 ± 29 104 52 ± 15 53 63(days)

Linear distance travelled 2,580–3,170 – 2,570–2,700 – –(km)

Average linear distance 2,900 ± 272 – 2,630 ± 54 – –travelled ± s.d. (km)



The Yalu River Estuary on the borderbetween China and North Korea was a keystaging area for Swan Geese (Figs. 1 and 2a).Two birds tracked in 2006 arrived after midOctober, whereas five birds tracked in 2008arrived at the end of September, and twoarrived around at the end of October. Allbirds stayed at this staging area until the endof December when air temperatures sharplydecreased and freezing conditions likelyreduced availability of food resources. The99% fixed kernel home ranges for SwanGeese in this location during the autumnand spring migration were 176 km2 and 190 km2, respectively.

Swan Geese arrived at the winteringgrounds in December, although one birdarrived on 1 January (Table 2). Five birds(#67585, 82105, 82107, 82108, and 82111)that successfully completed the southboundmigration travelled 2,580–3,170 km (mean =2,900 ± 272 km, n = 5) to reach theirwintering grounds in eastern China.Autumn migration for these birds took74–146 days (mean = 107 ± 29 days, n = 5).Individual variation in the autumn migrationperiod was largely due to the different lengthof time geese spent at the staging areas.

Wintering

Poyang Lake, located in the Jiangxi Provincealong the Yangtze River and the largestfreshwater lake in China, was an importantwintering area for the Swan Geese trackedfrom northeast Mongolia (Fig. 2b). Fourgeese (#67585, 82105, 82107 and 82111)arrived first at the northwest region of thelake. Later, geese moved to the south of thelake for most of the remaining winteringperiod and returned to the northwest just

before the spring migration began. Anothergoose (#82108) spent the winter at FengshaLake (30.927°N, 117.630°E) in AnhuiProvince located within the Yangtze RiverBasin 240 km northeast of Poyang Lake andknown to be another important wintering sitefor Swan Geese (Fox et al. 2008). Arrival datesat wintering areas ranged from 23 October to1 January with a median date of 7 December(n = 5). Swan Geese spent 56–155 days (mean= 104 ± 37 days) at the wintering grounds.The 50%, 95%, and 99% fixed kernel homerange of Swan Geese in this location duringtheir winter stay were of 60 km2, 370 km2 and580 km2, respectively (Fig. 2b).

Spring migration

Swan Geese departed for their springmigration between 25 February and 5 April(median = 14 March, n = 5 birds).Northbound travel lasted for 30–66 dayswith an average of 52 days (s.d. = 15 days).The spring migration routes for three of theSwan Geese were similar to those takenduring the autumn migration. Two geesefollowed different routes, flying directly tothe north without staging at the Yalu RiverEstuary. Geese which followed a same-routespring migration took 30–66 days to reachthe breeding grounds, with many shorterstopovers between staging areas, whereasthe two geese following a loop migrationtravelled for 43 and 60 days respectively,differing from geese following the same-route migration by having longer non-stopflights with fewer staging periods. The fivegeese completed the spring migration aftertravelling 2,570–2,700 km (mean = 2,630 ±54 km) to reach the breeding grounds innortheast Mongolia.



Arrival at breeding and post-breeding

areas

The first bird arrived at the breedinggrounds on 13 April and the last arrived on4 June (median = 9 May, n = 5). The geesestayed on the breeding grounds for 43–70days (mean = 53 ± 15 days). Four birdsarrived at the same area where they werecaptured in the previous year, the fifth(#82105) probably bred at Tsagaan Lake(47.911°N, 119.604°E) in China. SwanGeese arrived at their moulting sitesbetween 16–22 June. Post-breeding areaswhere geese typically moult were on lakeswith grassy meadows. Swan Geese remained

at these post-breeding areas for two monthsprior to the beginning of autumn migrationin August. Two birds were tracked on asecond autumn migration beginning on 23 August 2007 (#67585) and on 18 August2009 (#82105). Migration routes of thesebirds were similar to the previous year up tothe time their transmitter signals ended inmid migration.

Staging areas

A total of 54 staging areas were used by the17 Swan Geese after they left the breedingand moulting grounds. Five female SwanGeese that had complete migration cycleshad similar numbers of stopover areas

A B

Figure 2. Foraging and roosting locations of Swan Geese at major staging and wintering areas.Contours represent 99% fixed kernel home ranges in three different seasons. Yellow contours showareas used during autumn migration (September–December), red contours indicate spring migrationlocations (March–April), and green contours show wintering locations (January–February). Blue dotsshown are locations for five birds that made a complete migration cycle. A. Yalu River Estuary at theborder area between China and North Korea. B. Poyang Lake, Jiangsu Province, China.



during the migration (ANOVA test: F4, 49 =0.17, P = 0.95, n.s.). The number of stagingareas where birds spent on average morethan 10 days ranged from 4–9 sites per bird.Birds were spending 8–70 days per site(mean = 23 days; 95% UCI = 41, LCI = 4).We also obtained detailed information onlocation and habitat for selected majorstaging and stopover sites (Table 3).

The Yalu River Estuary was a key stagingarea or pre-wintering area. Eight SwanGeese spent 16–70 days there (mean = 34days) from 16 September to 20 December.The Swan Geese did not use adjacentagriculture fields to forage during thisperiod. Instead, they used mostly mud flatareas and habitats along the coastline (Fig. 2a).

In general, the number of stopover andstaging areas and the duration Swan Geesespent at important staging areas were greaterwhen geese were north of 42°N (Fig. 1).There was some preliminary evidence thatthe distance from a stopover location tourban areas decreased as the birds flewsouth, with the smallest distances involvedbeing close to the wintering grounds (Fig. 3).Few Swan Geese used Buir Lake, which isone of the largest lakes in the region, as astopover site, although 24,000 Swan Geesehave been recorded there previously(Goroshko 2004). Only one of our markedgeese stopped at this lake, for 1–2 daysduring autumn migration. There were noobvious major changes in flight speed anddistance during migration along the directroute (Fig. 4).

Seventy-eight locations were useful forestimating flight speeds and successivedistances during migration. Overall, the Swan

Geese migrated on average at 31 ± 1.8 km/h(n = 78; range = 11–77 km/h for individualflights), at 31 ± 2.2 km/h in autumn (n = 38;range = 12–66 km/h) and at 32 ± 2.8 km/hin spring (n = 40; range = 11–77 km/h forindividual flights). A Wilcoxon signed-ranktest found no significant difference in averageflight speeds recorded during the autumn andspring migration (Z = –0.24, P < 0.82, n.s.).The average distance travelled by individualbirds also did not differ markedly betweenautumn and spring (Z = 0.37, P < 0.72, n.s.)(Fig. 4). Non-stop flights of > 24 h durationwere observed for three occasions, whengeese with transmitters #82105, #82107 and #82111 flew for 26, 29 and 30 h inSeptember and December 2008. Theseflights were of 977 km, 1,053 km and 1,395km, at speeds of 38, 36 and 47 km/hrespectively.

Discussion

Two distinct flight paths were used duringautumn migration by the Swan Geesetracked in our study: 1) an indirect flightbetween Mongol Daguur in northeastMongolia and Poyang Lake in eastern Chinathrough the Yalu River Estuary on theChina-North Korean border, and 2) a directflight between the Mongol Daguur and thePoyang Lake. Geese flying through the YaluRiver Estuary during their migration flewmore than 300 km farther than those flyingstraight from the Mongol Daguur to PoyangLake, but more marked geese used thisroute. In terms of maximising energy andminimising time, migration along thispathway appears more costly than the directflight. Many migratory species make detoursto avoid hazardous and inhospitable land



Tab

le 3

.L

ocat

ion,

hab

itat,

and

dura

tion

of s

tay

of S

wan

Gee

se a

t sel

ecte

d m

ajor

sto

pove

r site

s (i.

e.w

here

bird

s sp

ent o

n av

erag

e m

ore

than

10

days

). A

fter

mou

lting

, gee

se s

pent

ove

r a

wee

k at

54

diff

eren

t mig

ratio

n lo

catio

ns.

Co

un

try

Lo

ca

tio

nC

oo

rdin

ate

sH

ab

ita

tS

ea

son

Da

teN

um

ber

of

Ave

rag

e

Ra

ng

e

PT

T m

ark

ed

D

ays

bir

ds

Mo

ng

oli

aK

havt

sgai

t Lak

eN

49.

347°

L

ake

Aut

umn

13 A

ug–3

Sep

122

22E

114

.416

°

Mo

ng

oli

aSh

andi

n L

ake

and

N 4

8.50

4°

Lak

e an

d A

utum

n25

Aug

–24

Sep

610

2–18

Khe

rlen

Riv

erE

116

.333

°rip

aria

n m

eado

w

Mo

ng

oli

aO

lziit

iin S

hava

r N

47.

200°

L

ake

and

Aut

umn

15 S

ep–1

0 O

ct1

2626

Lak

eE

117

.275

°rip

aria

n m

eado

w

Ch

ina

Bay

an H

ushu

Lak

eN

47.

913°

L

ake

Aut

umn

10 S

ep–

6 Se

p1

1717

E 1

19.6

06°

Ch

ina

Dal

ai H

u L

ake

N 4

3.37

7°

Lak

eA

utum

n10

Sep

–12

Oct

220

13–2

7E

116

.705

°

Ch

ina

Ajil

a G

acha

Lak

eN

44.

331°

Sm

all l

akes

Aut

umn

22 S

ep–2

Nov

210

8–13

E 1

21.0

65°

Ch

ina

Sulis

hi L

ake

N 4

2.79

5°

Smal

l lak

eA

utum

n20

Sep

–23

Oct

134

34E

122

.439

°



Tab

le 3

(cont

inue

d)

Co

un

try

Lo

ca

tio

nC

oo

rdin

ate

sH

ab

ita

tS

ea

son

Da

teN

um

ber

of

Ave

rag

e

Ra

ng

e

PT

T m

ark

ed

D

ays

bir

ds

Ch

ina

Huo

jia L

ake

N 4

3.62

8°

Smal

l lak

eA

utum

n8

Oct

–5 N

ov1

2727

E 1

22.8

17°

Ch

ina

an

d

Yal

u R

iver

Est

uary

N 3

9.86

9°

Est

uary

Sprin

g15

Mar

–14

Apr

222

19–2

6N

ort

h K

ore

aE

124

.301

°A

utum

n16

Sep

–20

Dec

834

16–7

0

No

rth

Ko

rea

Cha

ngp’

oN

39.

530°

Se

asho

reA

utum

n1

Oct

–4 D

ec2

3813

–63

E 1

25.3

67°

Ch

ina

Yel

low

Riv

er d

elta

N 3

7.80

9°

Seas

hore

Aut

umn

4 O

ct–5

Nov

130

30E

119

.185

°

Ch

ina

Chi

shan

Lak

eN

31.

824°

Po

nds

and

Aut

umn

6 D

ec–3

0 D

ec1

2424

E 1

19.0

96°

irrig

atio

n ch

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masses or water bodies, and thus reduce therisks encountered during migration(Newton 2007). However, there are nomajor physical barriers such as a largemountain range or body of water that wouldprevent Swan Geese flying directly south toPoyang Lake from Mongolia. In fact, geeseflying to the Yalu River Estuary must crossBohai Bay en route to the Yangtze RiverBasin.

One possible explanation for theintensive use of this estuary by Swan Geeseis that weather and climate patternsinfluenced their migration (Gordo 2007).Prevailing winds and favourable conditions

may favour stopovers by migratory birdsalong the Yellow Sea (van de Kam 2010).Alternatively, the Swan Geese may havebeen avoiding interior areas with highestdensities of human, agriculture, andinfrastructure development while exploitingnatural areas as much as possible beforearriving at Poyang Lake. Furthermore, flyingvia Yalu River could be a traditionalmigration route to Japan and South Koreawhere Swan Geese commonly used towinter (Brazil 1991).

Swan Goose migration between the YaluRiver Estuary and Poyang Lake was brief,with fewer stopovers compared to flights

Figure 3. Changes in linear distance from stopover sites to the nearest urban area in relation to latitude(n = 5 birds). Size of the dark circles indicates the duration of stay (in days) at stopover sites; each circlerepresents a location and duration is illustrated in the legend.



Figure 4. Consecutive flight distance and groundspeed of migration for Swan Geese relative tobreeding and wintering locations (latitude). Latitude is represented by the midpoint of 4 degree intervalson the x-axis. Outliers indicate the ability of some individuals to cover long flight distances at rapidspeeds during non-stop flights. Seasons are indicated as (a) autumn migration, (b) spring migration and(c) both seasons combined.



between Mongol Daguur and the Yalu RiverEstuary. In general, we did not see majorchanges in average flight speeds anddistances along the migration route inautumn and spring (Fig. 4), although there were some substantial maximumgroundspeed and flight distances recordedduring autumn migration prior to the geesearriving on the Yalu River Estuary. The datashow that Swan Geese can cover c. 1,400 kmwithin 30 h, but the ecological andenvironmental factors influencing suchflights are not known.

Availability of stopover sites and durationof stay are important parts of the annualcycle and influence birds’ migrationstrategies (Berthold et al. 2003; Newton2007). Marked Swan Geese made morestopovers in the areas north of 42°Nlatitude, which may indicate the presence ofmore suitable sites in the north that wereprimarily natural wetlands. There arecurrently few large human concentrations inthe areas intersecting northeast Mongolia,Russia, and China where Swan Geese breedand moult. Thus, the region is mostlyundisturbed or underdeveloped. SwanGeese exhibited longer stopover durationsin the north of 42°N latitude during both the autumn and spring migration.Furthermore, our data suggest that theproximate distance from a stopover locationto urban areas decreased as birds flew south,and the distance was least near the winteringarea (Fig. 3). Swan Geese may prefer to uselandscapes with lower human densities andless urbanisation while exploiting areas withrich in food supply.

The scale of urbanisation in easternChina, home to 10% of the world’s

population (van de Kam 2010) and themajority of the population in China, is veryintensive. As a result, human developmenthas dramatically changed land cover and land use practices in eastern China (Deng et al. 2008). Avian species oftenrespond dramatically to urbanisation anddevelopment depending on spatial scalesand local food, available habitats, anddisturbance levels (Clergeau et al. 1998;Garaffa et al. 2009; Klein 1993; Marzluff2001; Traut & Hostetler 2003). Large scalechanges at a landscape level in east Chinamay have affected migratory behaviour ofthe Swan Geese historically, but there aretoo few historical data available to analysethis hypothesis.

Nonetheless, eastern China is the mostimportant wintering area for the SwanGoose, and nearly 95–100% of the geesefrom the Dauria region are found winteringthere (Cao et al. 2008a; Zhang et al. 2010). In the last four decades, the wintering range of Swan Geese has graduallycontracted coincident with a decline in theirpopulations likely related to increasedpoaching, water-level control for irrigationand industrial use, habitat degradation ofcoastal and inland wetlands, and pollution(Barter et al. 2007; Cao et al. 2010; Quan et al.

2002; Zhang et al. 2010). Expansion ofurbanisation and economic development in east Asia has caused large-scale change in ecosystems of the region. Also, degradation of wetlands in easternChina has contributed to distribution range shifts, contraction, and northwardexpansion for many waterbird species (Caoet al. 2008b; Cao et al. 2010; de Boer et al.

2011).



Extensive use of mud flats by SwanGeese has been documented during the non-breeding season. Swan Geese were commonly observed grubbing onunderground rhizomes of Vallisneria asiatica

in mud flat habitats at wintering sites inShengjin Lake (Fox et al. 2008; Zhang & Lu1999) and in the Han River Estuary (Han etal. 2003). It is unclear what constitutes themain food supply for staging Swan Geese inthe Yalu River Estuary mud flats and whygeese do not use grassland habitats andagricultural fields. However, it could berelated to the availability of foraginghabitats in that region and easy access tonutrient-rich food.

In addition, Poyang Lake is one of themajor wintering areas for the Swan Gooseand many other waterbirds but has beencalled the potential epicenter of HPAIH5N1 (Cao et al. 2008a; Prosser et al. 2009;Takekawa et al. 2010). Outbreaks of highlypathogenic avian influenza H5N1 haveoccurred along the migration route fromnortheast Mongolia through the Yalu RiverEstuary to Poyang Lake (Sakoda et al. 2010;Takekawa et al. 2010). The density ofwetlands along this migration route is sparsein northern compared to southern regionswhere man-made wetlands are abundant(Bicheron et al. 2008). Thus, in stopoverareas north of 42°N, Swan Geese may have greater chances of interactions withwaterbirds originating from different parts of south and east Asia, increasing the potential for H5N1 transmission.Consequently, potential spread andpersistence of HPAI H5N1 in this regionmay pose a threat to the Swan Goosepopulation.

It remains unclear whether the migratorypathway we documented through the YaluRiver Estuary is a historical or recently-developed route that arose in response toland use and land cover changes in easternChina. However, Takekawa et al. (2010)report that several different duck species,migrating from Poyang Lake to northeastChina and eastern Russia in the spring, made extensive use of the region as astaging area, as do many shorebirds (van de Kam 2010). Thus, if we wish toconserve stopover sites along routes formigratory bird species in east Asia,obtaining a better understanding of theeffects of urban area expansion anddevelopment at key stopover sites such asthe Yalu River Estuary is crucial. Thoseimpacts may be most visible for species withlarger body size and narrow habitat nichessuch as the Swan Goose.

Acknowledgements

This work was funded by the U.S.Geological Survey (Patuxent WildlifeResearch Center, Western EcologicalResearch Center, Alaska Science Center, andAvian Influenza Program), the UnitedNations Food and Agriculture Organization, Animal Production and Health Division,EMPRES Wildlife Unit. The field work ofMongolian and Korean researchers in 2006was funded by the Cultural HeritageAdministration of Korea through Korean-Mongolia Joint Swan Goose ResearchProject. The data analysis was supported bya grant from the U.S. National ScienceFoundation EPSCoR programme (NSF-0919466). We are grateful to Sabir BinMuzaffar, Eric Palm, David Douglas,



Bill Perry (U.S. Geological Survey), TaejMundkur (Wetlands International), MartinGilbert (Wildlife Conservation Society),Paek Won Kee, Chun Byung Sun (KoreanNational Science Museum), and the staff ofthe Wildlife Science and ConservationCenter of Mongolia for their assistance. The Ministry of Nature and Environmentof Mongolia provided permission tocapture and satellite-tag Swan Geesethrough the Institute of Biology, MongolianAcademy of Sciences. Any use of trade,product, or firm names in this publication is for descriptive purposes only and does not imply endorsement by the U.S.government.

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Photograph: Swan Geese grazing and sleeping. Photograph courtesy of the WSCC of Mongolia.

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Documents

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