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Oryx - The International Journal of Conservation

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Recent changes in the number of spoon-billed sandpipers Calidris pygmaea wintering on the Upper Gulf of Mottama in Myanmar

Journal: Oryx

Manuscript ID Oryx-18-A-0051.R1

Manuscript Type: Article

Date Submitted by the Author: n/a

Complete List of Authors: AUNG, PYAE-PHYO; BANCA, BANCA Moses, Saw; BANCA, BANCA Clark, Nigel; British Trust for Ornithology, British Trust for Ornithology Anderson, Guy; RSPB, Centre for Conservation Science Hilton, Geoff; WWT, Research Department Buchanan, Graeme; RSPB, none Zöckler, Christoph; ArcCona Consulting, Spoon-billed Sandpiper Task Force Green, Rhys; Cambridge University, Department of Zoology; RSPB, Conservation Science Department

Keywords: shorebird, intertidal, population monitoring

Number of Words (all 5194 inclusive, except tables):

The spoon-billed sandpiper Calidris pygmaea, a migratory arctic-breeding shorebird, is one of the world’s rarest birds and its population has declined in recent decades. We surveyed its most important known wintering area in the Upper Gulf of Mottama in Myanmar to estimate recent (2009 – Abstract: 2016) changes in its numbers there. The total number of small shorebirds present in the Upper Gulf was counted and the proportion of them that were spoon-billed sandpipers was estimated from sample scans. These two quantities were multiplied together to give the estimated number of spoon-billed sandpipers in each of four years. Total numbers of combined

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small shorebird species tripled from 21,000 to 63,000 between 2009 and 2016, coincident with efforts to reduce hunting pressure on waterbirds. However, the proportion of small shorebirds that were spoon- billed sandpipers declined and their estimated absolute numbers fell by about half from 244 to 112 individuals. It is probable that loss of intertidal habitat and shorebird hunting elsewhere on the migration route of the spoon-billed sandpipers wintering at Mottama is causing a continued decline, though this is occurring at a less rapid rate than that recorded from Arctic Russia before 2010. The number of spoon-billed sandpipers wintering on the Upper Gulf of Mottama remains the highest single-site total for this species from any known wintering site. Preventing resurgence of illegal shorebird hunting and ensuring long-term protection of the intertidal feeding habitats and roost sites in the Gulf are high priorities if extinction of this species is to be aver

For Peer Review

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1 Recent changes in the number of spoon-billed sandpipers

2 Calidris pygmaea wintering on the Upper Gulf of Mottama in

3 Myanmar

5 PYAE-PHYO AUNG, SAW MOSES, NIGEL A. CLARK, GUY Q.A. ANDERSON, 6 GEOFF M. HILTON,For GRAEME Peer M. BUCHANAN, Review CHRISTOPH ZÖCKLER and 7 RHYS E. GREEN

9 Abstract

10 The spoon-billed sandpiper Calidris pygmaea, a migratory arctic-breeding shorebird,

11 is one of the world’s rarest birds and its population has declined in recent decades.

12 We surveyed its most important known wintering area in the Upper Gulf of

13 Mottama in Myanmar to estimate recent (2009 – 2016) changes in its numbers there.

14 The total number of small shorebirds present in the Upper Gulf was counted and the

15 proportion of them that were spoon-billed sandpipers was estimated from sample

16 scans. These two quantities were multiplied together to give the estimated number

17 of spoon-billed sandpipers in each of four years. Total numbers of combined small

18 shorebird species tripled from 21,000 to 63,000 between 2009 and 2016, coincident

19 with efforts to reduce hunting pressure on waterbirds. However, the proportion of

20 small shorebirds that were spoon-billed sandpipers declined and their estimated

21 absolute numbers fell by about half from 244 to 112 individuals. It is probable that 1

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22 loss of intertidal habitat and shorebird hunting elsewhere on the migration route of

23 the spoon-billed sandpipers wintering at Mottama is causing a continued decline,

24 though this is occurring at a less rapid rate than that recorded from Arctic Russia

25 before 2010. The number of spoon-billed sandpipers wintering on the Upper Gulf of

26 Mottama remains the highest single-site total for this species from any known

27 wintering site. Preventing resurgence of illegal shorebird hunting and ensuring 28 long-term protectionFor of the intertidal Peer feeding Review habitats and roost sites in the Gulf are 29 high priorities if extinction of this species is to be averted.

31 Introduction

32 The spoon-billed sandpiper Calidris pygmaea is listed as Critically Endangered in the

33 IUCN Red List because of its small global population size and rapid population

34 declines (BirdLife International, 2017; Zöckler et al., 2010a). In late summer, its

35 population migrates from breeding grounds on coastal tundra in the arctic and

36 subarctic zones of the Chukotka Autonomous Okrug and northern Kamchatka Kraj

37 in Russia, through the southern Russian Far East, North Korea, South Korea, China

38 and Japan to wintering areas on intertidal mudflats in southern China, Thailand,

39 Myanmar, Vietnam, Malaysia and Bangladesh (Clark et al., 2014; Zöckler et al.,

40 2016).

41 The largest known wintering population of spoon-billed sandpipers is in the

42 northern part of the Gulf of Mottama (also known as the Bay of Martaban), a large

43 estuary in Myanmar. Studies at this site in 2009 and 2010 estimated the numbers of 2

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44 spoon-billed sandpipers and other shorebirds and also showed that spoon-billed

45 sandpipers were killed frequently by hunters who were netting larger shorebird

46 species for food (Zöckler et al., 2010b). All shorebird species are legally protected

47 under the Wildlife Act of Myanmar, which prohibits their killing or capture, but the

48 law is not fully implemented. Beginning early in January 2010 and continuing since

49 then, efforts have been made to reduce mortality by assisting local authorities to 50 implement bans on Forshorebird Peer hunting and Review helping former bird hunters to switch to 51 alternative livelihoods, especially fishing (Htin Hla & Eberhardt, 2011; Clark et al.,

52 2014).

53 These actions appear to have been largely successful, with recent surveys

54 detecting little evidence of shorebird trapping gear in the Gulf of Mottama and other

55 sites in Myanmar and Bangladesh (Pyae-Phyo Aung et al., 2014, 2015; 2016; 2017).

56 However, there continue to be reports of mortality of spoon-billed sandpipers

57 caused by hunting and entanglement in fishing nets in other parts of the non-

58 breeding range, including China (Pain et al., 2011; Clark et al., 2014; Martinez &

59 Lewthwaite, 2013; Martinez, 2016, Peng et al., 2017). In addition, conversion of

60 intertidal areas for human use, especially in the Yellow Sea region of South Korea

61 and China, is having significant effects on survival and population size of migratory

62 shorebirds along the East Asian–Australasian flyway, where more shorebird species

63 are declining than in any other flyway in the world (Kirby, 2010; Mackinnon et al.,

64 2012; Piersma et al., 2015; Piersma et al., 2017). The spoon-billed sandpiper is thought

65 to be among the species most threatened by these changes. A comparison of a 3

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66 compilation of recent counts of wintering spoon-billed sandpipers (Zöckler et al.,

67 2016) with a mark-resighting estimate of the world population of the species (Clark

68 et al., 2018) suggests that the locations of only about half of the population are

69 known in winter. Based on wintering population estimates from Zöckler et al.

70 (2016), the Upper Gulf of Mottama is the most important known wintering site. It

71 holds about two-thirds of the global total of sandpipers counted in winter (Zöckler et 72 al., 2016) and one quarterFor of Peer the winter Review population estimated by mark-resighting 73 (Clark et al., 2018). Counting spoon-billed sandpipers at any wintering site is

74 challenging because they are rare and usually dispersed within large flocks of other

75 small shorebirds, especially the similarly coloured and sized red-necked stint Calidris

76 ruficollis. In the Upper Gulf of Mottama, complete direct counts of spoon-billed

77 sandpipers are impractical because of the large numbers of other small shorebirds

78 that must be checked, the large size of the intertidal area, day-to-day variation in the

79 extent and location of foraging habitat exposed at low tide and frequent changes in

80 the location of high tide roosts. Roosts are often on very soft substrates, making it

81 impossible to approach them before the birds leave on the falling tide. A highly

82 dynamic tidal flow in the estuary restricts the availability of areas where boats can

83 be beached at low tide so that surveys of foraging birds can be carried out safely on

84 foot. In this paper, we report a recent series of estimates of the numbers of spoon-

85 billed sandpipers in the Upper Gulf of Mottama made using methods comparable to

86 those of Zöckler et al. (2010b). To circumvent the difficulties mentioned above, our

87 surveys determined (i) the total number of small shorebirds present in the Upper 4

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88 Gulf, without counting the different species separately, and (ii) the proportion of

89 small shorebirds that were spoon-billed sandpipers from sample scans. The number

90 of spoon-billed sandpipers was then estimated as the product of these two

91 quantities. Using this method, Zöckler et al. (2010b) estimated that there were 200

92 spoon-billed sandpipers in the Upper Gulf of Mottama in 2010 and considered that

93 there might be about 20 more in other parts of the Gulf, based on sightings in that 94 and other years. For This estimate Peer (220 individuals)Review was used in a later global 95 compilation of recent winter population assessments (Zöckler et al., 2016). However,

96 there has been no assessment of possible changes in the wintering population at the

97 Gulf of Mottama since measures were introduced there to restrict hunting. In this

98 paper, our objective is to assess the recent trend in the spoon-billed sandpiper

99 population wintering in the Upper Gulf of Mottama, and changes in the proportion

100 of small shorebirds that are spoon-billed sandpipers, by combining the data for 2010,

101 previously reported by Zöckler et al. (2010b), with results for 2009 and four more

102 recent years.

103

104 Study area

105 The Gulf of Mottama (or Martaban) is located in Yangon Region, Bago Region and

106 Mon State in Myanmar, at the mouth of the Sittaung River. It is a large funnel-

107 shaped estuary about 100 km wide at the southern end, covering a total area of

108 about 2,500 km2. Its tidal cycle is extremely pronounced in speed and amplitude (6 –

109 7 m tidal range), causing a powerful bore phenomenon which is highly unusual in 5

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110 the region and which makes this one of the most dynamic estuaries in the world,

111 with constant sediment redistribution, channel-shifts, erosion and accretion on a

112 large scale. We surveyed part of the Gulf north of latitude 17°N (Fig. 1). We selected

113 this part because only small numbers of spoon-billed sandpipers have been recorded

114 in the parts further to the south (Zöckler et al. 2010b) and because its large tracts of

115 intertidal mud are accessible by fishing boats from villages on the eastern side of the 116 Gulf. For Peer Review 117 The dynamic nature of the estuary means that the location and extent of intertidal

118 flats changes substantially from month to month. This dynamism is illustrated by

119 the movement of the main channel of the Sittaung from the east to the west side of

120 the estuary following a cyclone in 2008. In order to produce an estimate of the extent

121 of the intertidal zone relevant to our study period, we analysed Landsat 8 satellite

122 images from spring 2016. Visual inspection of Landsat 8 images showed that the

123 mudflats were stable during this time. The area of mud between high tide on 13

124 February 2016 and low tide on 17 April 2016 was estimated from changes in the

125 radiance in atmospherically corrected band 5 between the Landsat 8 images from

126 these dates. This near infra-red band is useful for mapping shorelines (Barsi et al.,

127 2014). The radiance values associated with exposed mud were determined from

128 visual inspection of both images, and comparison of the extent of mud was used to

129 identify the intertidal area. At that time, we estimated that the intertidal zone within

130 our survey area covered 217 km2 (Fig. 1). Part of the Gulf within Mon State,

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131 overlapping our study area and covering 425 km2 was site designated in 2017 under

132 the Ramsar Convention on Wetlands 1971 (Ramsar Site no. 2299).

133

134 Fieldwork methods

135 This paper reports scan surveys to estimate spoon-billed sandpiper numbers in the

136 Upper Gulf of Mottama during January or February, or both, of 2009, 2010, 2011, 137 2012, 2015 and 2016.For Survey Peer visits conducted Review in these months because migratory 138 overwintering shorebirds were likely to have all arrived by then and few birds

139 would be expected to have departed on their return migration. Within this period,

140 visits were timed to cover the highest series of spring tides because the boats we

141 used only had free access over all of the intertidal flats at high spring tides and

142 because shorebirds are likely to be concentrated at high tides and to gather in large

143 flocks which we would be less likely to miss when attempting to count the total

144 numbers of small shorebirds (see below).

145 The survey team was transported to as many parts of the study area as possible in

146 shallow-draft fishing boats, which were grounded on the mud in the intertidal zone

147 at low tide to allow observation of birds from the boat and on foot. In this way, we

148 were able to conduct scan surveys throughout the daylight period of tidal cycles and

149 at a wide range of elevations relative to the high and low water marks. The study

150 area was divided up into sections, which we call blocks, in each of which we spent 1-

151 2 days surveying before moving on to another. Blocks were determined according to

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152 tidal and wind conditions, the number of observers and the locations of high-tide

153 roosts during the visit and therefore differed among years. Groups of 2-4 observers

154 walked the intertidal zone, diverging from the place where the boat was grounded,

155 and also viewed birds from the boats, especially when the tide was high. Each

156 group of observers included individuals experienced in shorebird identification who

157 scanned flocks of resting and foraging small shorebirds using a telescope. The 158 observers were notFor the same Peer individuals Review in all years, but one observer (NAC) 159 participated in all the surveys reported here and several other individuals

160 participated in two or more of the surveys. The small-bodied shorebird species

161 (body weight < 80 g) present, in addition to spoon-billed sandpipers, mostly

162 comprised calidrid sandpipers (curlew sandpiper Calidris ferruginea, broad-billed

163 sandpiper Calidris falcinella and red-necked stint) and plovers (greater sandplover

164 Charadrius leschenaultia, lesser sandplover Charadrius mongolus, Kentish plover

165 Charadrius alexandrinus and little ringed plover Charadrius dubius). These species

166 tended to feed and roost in mixed species flocks and were readily distinguished at a

167 distance on the ground and in flight from the larger-bodied shorebird species (> 120

168 g) present (great knot Calidris tenuirostris, Tringa species, Limosa species and

169 Numenius species). However, separate identification and counting of all spoon-

170 billed sandpipers and other species was not possible.

171 A scan consisted of a search by one observer through a group of small

172 shorebirds, at the end of which the numbers of small shorebirds of each species were

173 recorded, together with the date and time of the record and the GPS location. Often 8

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174 the observer spoke the numbers of birds of each species checked at intervals within

175 the scan, whilst viewing the birds through a telescope, and these were written down

176 by another group member. An individual small shorebird was only included in the

177 scan record if it was seen well enough to be sure whether it was a spoon-billed

178 sandpiper or not and observers were trained to spend enough time observing each

179 bird do this accurately. Training was given by the experienced observers to achieve 180 consistency. Some For scans were Peer conducted Review by inexperienced observers for training 181 purposes and checked by a repeat survey of the same flock by an experienced

182 observer. Results from these duplicated training scans were discarded. Individual

183 scan records covered varying numbers of birds, from a few individuals to over one

184 thousand. Because of this variation, and because it took longer per bird to check

185 species identity at a long distance or under difficult light conditions, the scans were

186 not of fixed duration or of a fixed area. During our scan counts, we almost certainly

187 scanned the same individuals more than once at different stages of the tidal cycle

188 and on different days. However, the sole objective of the scan counts was to

189 estimate the proportion of small shorebirds that were spoon-billed sandpipers, so

190 this only introduces pseudo-replication into our estimates, rather than biasing them.

191 Because our survey period in a given year was short, it is unlikely that much

192 movement of birds occurred among the survey blocks.

193 In addition, we made counts of the total number of small shorebirds in each

194 block in the years 2009, 2010, 2015 and 2016, mostly by estimating the size of large

195 flocks of shorebirds at roosts, when they were flying between feeding areas and high 9

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196 tide roosts or when they were flushed by raptors. In these years, we consider that

197 coverage of the Upper Gulf was sufficient to provide a valid count of the small

198 shorebird total, whereas in 2011 and 2012 coverage for full counting was incomplete

199 for logistical reasons. Estimates were made using standard methods in which counts

200 of individuals in parts of flocks were made and scaled up by eye to give the flock

201 total. These estimates were made by an observer (NAC) with substantial previous 202 experience in using For this method Peer elsewhere. Review It was usually not possible to identify 203 birds to species when making these counts, but it is likely that nearly all the birds

204 counted were of the same set of small shorebird species targeted by the scans

205 because these species are markedly smaller than the smallest of the larger shorebird

206 species. An estimate of the total number of small shorebirds present in each block

207 was obtained by combining results from these counts across groups of observers and

208 at different times and discussing the location and timing of different records to

209 reduce the risk of double counting.

210

211 Analysis methods

212 We followed the approach used by Zöckler et al. (2010b) in calculating the number of

213 spoon-billed sandpipers. The principle of the method is that the estimated number

214 of sandpipers in a survey year is given by the product of the estimate of the

215 proportion of small shorebirds that are spoon-billed sandpipers and the count of

216 small shorebirds. We multiplied the proportion of small shorebirds that were spoon-

217 billed sandpipers, obtained from the scan data pooled across blocks for a given year, 10

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218 by the total number of small shorebirds estimated from the shorebird counts

219 summed across survey blocks for that year. To assess trends in the proportion of

220 small shorebirds that are spoon-billed sandpipers and the estimated number of

221 spoon-billed sandpipers, we performed ordinary least squares regressions of year-

222 specific logit-transformed proportions of small shorebirds that were spoon-billed

223 sandpipers and loge-transformed estimated numbers of sandpipers on the decimal 224 calendar year of theFor midpoint Peer of the survey Review period. We calculated 95% confidence 225 intervals of year-specific estimates of proportion and number by bootstrapping. To

226 do this, we grouped our scans into bootstrap units comprising consecutive scan

227 records by a single group of observers within a single period between two high

228 tides. We combined sets of scans adjacent in time to ensure that each bootstrap unit

229 included at least 50 small shorebirds. We then drew a bootstrap sample of size n

230 bootstrap units at random, with replacement, from the n units available in each year

231 and performed the calculations of the proportion of small shorebirds that were

232 spoon-billed sandpipers in a given year and the estimated number of spoon-billed

233 sandpipers as described above. We repeated this procedure 10,000 times for a given

234 year and took the bounds of the central 9,500 bootstrap values to define the 95%

235 confidence limits of the estimated proportion or population estimate for that year.

236 Having done these calculations separately for all calendar years, we aligned the

237 10,000 bootstrap estimates for each year in random order and fitted the two

238 regression models described above to estimate trends of proportion and number in

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239 relation to calendar year. We took the bounds of the central 9,500 bootstrap values

240 of the bootstrap values of the regression slopes to define their 95% confidence limits.

241

242 Results

243 The 95% confidence interval of the slope of the ordinary least squares regression of

244 logit-transformed proportion of scanned small shorebirds that were spoon-billed 245 sandpipers on decimalFor calendar Peer year did notReview overlap zero (slope = -0.2240; 95% C.L. - 246 0.3001 to -0.1105). The proportion of scanned small shorebirds that were spoon-

247 billed sandpipers thus declined significantly and markedly by about six-fold

248 between 2009 and 2016 (Table 1; Fig. 2). The total count of small shorebirds

249 increased by about three-fold from 21,000 to 63,000 between 2009 and 2016 (Table 1).

250 The correlation between the natural logarithm of the total count of small shorebirds

251 and calendar year was high, indicating a statistically significant increase with little

252 variation in annual counts around the trend (Pearson correlation r = 0.955, t2 = 4.53,

253 two-tailed P = 0.045). The slope of the least squares regression of the natural

254 logarithm of the small shorebird count on year was 0.144, which indicates a mean

255 exponential population multiplication rate of e0.144 = 1.155 (15.5% increase per year).

256 However, the increase in the total count of small shorebirds was not sufficient to

257 fully cancel out the decline in the proportion of small shorebirds that were spoon-

258 billed sandpipers. Hence, the estimated number of spoon-billed sandpipers,

259 calculated as the product of the total small shorebird count and the proportion that

260 were spoon-billed sandpipers, declined by about half from 244 to 112 individuals 12

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261 (Table 1; Fig. 3). The 95% confidence interval of the slope of the ordinary least

262 squares regression of loge-transformed spoon-billed sandpiper population estimate

263 on decimal calendar year overlapped zero marginally (slope = -0.0906; 95% C.L. -

264 0.1710 to +0.0352). This trend estimates the mean annual population growth rate and

265 is suggestive of population decline, being equivalent to a mean annual rate of

266 population decline of 8.7% per year. It is also equivalent to an overall decline 267 between 2009 and For 2016 of 47%,Peer but with Review substantial uncertainty (95% C.L. 70% 268 decline to 28% increase). Despite the wide confidence interval, only 6.6% of

269 bootstrap replicates had a positive population trend, so the results are sufficiently

270 close to demonstrating a population decline using a conventional significance test to

271 be of concern.

272

273 Discussion

274 The observed large increase in numbers of small shorebirds counted between 2009

275 and 2016 coincides with a reduction in hunting pressure on waterbirds in the Gulf of

276 Mottama occasioned by the implementation of bird hunting bans and efforts of

277 conservation agencies and local authorities to assist former bird hunters to switch to

278 alternative livelihoods (Htin Hla & Eberhardt 2011; Pyae-Phyo Aung et al., 2015;

279 2016; 2017). Although we are convinced that this increase has occurred, the nature

280 of the fieldwork used to determine the small shorebird total does not allow us to

281 estimate the precision of each of the counts or to evaluate sources of error. It is

282 certainly possible that some flocks or roosts were missed and that the estimation of 13

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283 the size of large flocks of shorebirds by eye was subject to error. Independent small

284 shorebird counts in the same winter month by separate teams of observers would

285 have been needed to assess these uncertainties, and we did not have the resources

286 for this. Against this caveat about the apparent small shorebird increase, we note

287 that counts for individual years deviated only slightly from the fitted regression of

288 small shorebird count on year, which suggests that possible errors were consistent 289 across survey years,For which Peer would not Review bias the spoon-billed sandpiper trend 290 estimate.

291 We found strong evidence that the proportion of small shorebirds that were spoon-

292 billed sandpipers declined and moderately strong evidence that absolute numbers of

293 spoon-billed sandpipers in the Upper Gulf declined during the same period.

294 Although we could only estimate the absolute population size of the spoon-billed

295 sandpiper in the four years for which we had a count of all small shorebirds, the

296 data on the proportion of small shorebirds that were spoon-billed sandpipers in two

297 additional years were also consistent with a decline. However, the mean annual

298 population growth rate r we estimated for the Upper Gulf of Mottama (-0.0906; 95%

299 C.L. -0.1710 to +0.0352) indicated a considerably less rapid decline than that reported

300 by Zöckler et al., (2010a), based upon counts at four well-monitored sites on the

301 breeding grounds in arctic Russia between 2002 and 2009 (r = -0.3065). This

302 difference corresponds to a mean annual rate of decline of 8.7% per year for

303 Mottama in 2009-2016 compared with 26.4% per year for Russia in 2002-2009. If the

304 rate of decline estimated for Russia had continued and applied to the Upper Gulf of 14

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305 Mottama, the number of spoon-billed sandpipers there would have declined by 88%

306 between 2009 and 2016, instead of the 47% decline over that period estimated from

307 our regression (Fig. 3). Annual counts of breeding pairs at a consistently monitored

308 part of Meinypilgyno, the best-studied of these four breeding sites, during 2003-2009

309 also indicated a statistically significant decline (population growth rate r = -0.2134,

310 95% C.L. from a Poisson regression -0.3267 to -0.1001) at a similar rate to that for the 311 four sites in a similarFor period, Peer but continued Review monitoring of the same part of 312 Meinypilgyno from 2009 up to 2016 showed that the breeding population there then

313 became approximately stable (r = -0.0030, 95% C.L. -0.1114 to +0.1055: Tomkovich et

314 al., 2016). Because of the wide confidence intervals of the estimated mean annual

315 population growth rates for both Myanmar and Russia, the population growth rates

316 at the two sites in 2009-2016 were not significantly different from each other (8.7%

317 decline per year for Mottama cf. 0.3% decline per year for Meinypilgyno).

318 Conservation measures that might account for a recent slowing of the rate of decline

319 include increased efforts to reduce losses to hunting in the non-breeding season at

320 Mottama and elsewhere and a head-starting programme at Meinypilgyno which

321 began in 2012. Spoon-billed sandpiper eggs were removed from nests and artificially

322 incubated (Clark et al. 2014). The chicks were then reared until fully-grown and

323 released near the breeding site. Up to 2017, over 140 young sandpipers have been

324 headstarted and some have returned to the site and bred. Other factors may also

325 have changed between the period of decline and stability, but there are no

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326 comparable measurements of other potential drivers at a population level before and

327 after the change.

328 If the wintering population of spoon-billed sandpipers in the Upper Gulf of

329 Mottama really declined by almost half between 2009 and 2016, this may reflect

330 continuing effects of hunting and habitat loss elsewhere along the migration route of

331 this part of the population. The species migrates through the Yellow Sea (China, 332 North Korea, South ForKorea), wherePeer considerable Review loss of intertidal habitats caused by 333 land claim for human use has occurred and is continuing (Mackinnon et al., 2012;

334 Peng et al., 2017). Hunting of shorebirds using mist-nets, poison baits and other

335 methods also continues in many parts of South China and south-east Asia used as

336 migration staging areas (Martinez & Lewthwaite 2013; Martinez 2016) and

337 shorebirds also become entangled in static fishing nets in these areas. Another

338 possibility is that the spoon-billed sandpiper population of the Gulf of Mottama as a

339 whole has not declined, but that part of the population has moved to areas of the

340 Gulf south of 17°N which were not covered by our surveys, because of changes in

341 the distribution of intertidal mud and sand flats. However, if such a shift has

342 occurred, it is not clear why it has not also had a similar negative effect on the

343 numbers of small shorebirds of other species in the Upper Gulf. At present, we are

344 unable to quantify changes over time in the extent and quality of intertidal spoon-

345 billed sandpiper habitats, using remotely-sensed data, sufficiently accurately to

346 exclude this possibility.

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347 The Upper Gulf of Mottama continues to be a key wintering area for spoon-

348 billed sandpipers, and the number wintering there remains the highest single-site

349 total for this species from any known wintering site (Zöckler et al., 2016). The Gulf

350 as a whole is also an important site for many other species of waterbirds (Zöckler et

351 al., 2014) and our counts of small shorebirds indicate that the importance of the

352 Upper Gulf for these has increased. Future conservation efforts for spoon-billed 353 sandpipers and otherFor waterbirds Peer there should Review focus on preventing any resurgence of 354 illegal shorebird hunting, minimizing accidental captures in fishing gear and

355 ensuring long-term protection of the intertidal feeding habitats and safe roosting

356 areas. Steps towards achieving these objectives have been made recently, with much

357 of the eastern half of the Upper Gulf (within Mon State) being designated as a

358 Ramsar site. It is hoped that Ramsar designation will be extended to the western

359 portion of the Upper Gulf (Bago State) in the near future.

360

361 Acknowledgements

362 RSPB, the Wildfowl & Wetlands Trust and the BBC Wildlife Fund helped to fund the

363 surveys. Leica Camera AG provided optical equipment through the Wildfowl &

364 Wetlands Trust. We are grateful to the boatmen, without whom the surveys would

365 have been impossible, and the many surveyors from Myanmar and elsewhere who

366 assisted us. Two anonymous reviewers made constructive comments on a previous

367 version.

368 17

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369 Author contributions

370 NAC designed the survey method. PPA and SM made practical arrangements for

371 the surveys. All authors conducted the fieldwork. NAC, GQAA and REG designed

372 and conducted the analysis. GMB conducted the analysis of satellite imagery. REG

373 wrote the paper. All authors commented on the paper.

374 375 References For Peer Review 376

377 BARSI, J.A., LEE, K., KVARAN, G., MARKHAM, B.L., & PEDELTY, J.A. (2014) The

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380 BIRDLIFE INTERNATIONAL (2017) Calidris pygmaea (amended version of 2017

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383 3.RLTS.T22693452A117520594.en. Downloaded on 23 January 2018.

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385 update on the conservation programme. British Birds, 107, 467–475.

386 CLARK, N.A., ANDERSON, G.Q.A., LI, J., SYROECHKOVSKIY, E.E.,

387 TOMKOVICH, P.S., ZÖCKLER, C., LEE, R. & GREEN, R.E. (2018) First formal

388 estimate of the world population of the Critically Endangered spoon-billed

389 sandpiper Calidris pygmaea. Oryx, 52, 137-146.

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390 HTIN HLA, T. & EBERHARDT, K. (2011) New Hope from Nan Thar Island and Bay

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392 KIRBY, J. (2010) Review 2: Review of Current Knowledge of Bird Flyways, Principal

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398 Survival Commission No. 47. IUCN, Gland, Switzerland and Cambridge, UK.

399 MARTINEZ, J. & LEWTHWAITE, R. (2013) Rampant shorebird trapping threatens

400 spoon-billed sandpiper Eurynorhynchus pygmeus in south-west Guangdong,

401 China. Birding Asia, 19, 26-30.

402 MARTINEZ, J. (2016) Massive loss of wetland habitat and rampant illegal

403 mistnetting observed near Wenling city, Zhejiang province, China, May 2015.

404 spoon-billed sandpiper Task Force News Bulletin, 16, 19-21.

405 PAIN, D., GREEN, R. & CLARK, N. (2011) On the edge: can the spoon-billed

406 sandpiper be saved? British Birds, 104, 350–363.

407 PENG, H.-B., ANDERSON, G.Q.A., CHANG, Q., CHOI, C.-Y., CHOWDHURY, S.U.,

408 CLARK, N.A., GAN, X., HEARN, R.D., LI, J., LAPPO, E.G., LIU, W. MA, Z.,

409 MELVILLE, D.S., PHILLIPS, J.F., SYROECHKOVSKIY, E.E., TONG, M.,

410 WANG, S., ZHANG, L. & ZÖCKLER, C. (2017) The intertidal wetlands of

411 southern Jiangsu Province, China – globally important for spoon-billed 19

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412 sandpipers and other threatened waterbirds, but facing multiple serious

413 threats. Bird Conservation International, 27, 305-322.

414 PIERSMA, T., LOK, T., CHEN, Y., HASSELL, C.J., YANG, H.-Y., BOYLE, A.,

415 SLAYMAKER, M., CHAN, Y.-C., MELVILLE, D.S., ZHANG, Z.-W. & MA, Z.

416 (2015) Simultaneous declines in summer survival of three shorebird species

417 signals a flyway at risk. Journal of Applied Ecology, 53, 479–490. 418 PIERSMA, T., CHAN,For Y.-C., MU,Peer T., HASSELL, Review C.J., MELVILLE, D.S., PENG, H.-B., 419 MA, Z., ZHANG, Z. & WILCOVE, D.S. (2017) Loss of habitat leads to loss of

420 birds: reflections on the Jiangsu, China, coastal development plans. Wader

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425 wintering grounds in Myanmar 2013-2014. BANCA, Yangon, Myanmar.

426 PYAE-PHYO AUNG, SAW MOSES, MIN THIHA ZAW, HTET PHYO NAUNG,

427 MIN THEIN HTET & AUNG NAING OO (2015) Monitoring Programme for

428 the Critically endangered Spoon-billed sandpiper on its most important

429 wintering grounds in Myanmar. BANCA, Yangon, Myanmar.

430 PYAE-PHYO AUNG, SAW MOSES, MIN THIHA ZAW, HTET PHYO NAUNG,

431 MIN THEIN HTET & AUNG NAING OO (2016) Monitoring Programme for

432 the Critically endangered Spoon-billed sandpiper on its most important

433 wintering grounds in Myanmar. BANCA, Yangon, Myanmar. 20

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434 PYAE-PHYO AUNG, SAW MOSES, MIN THIHA ZAW, HTET PHYO NAUNG,

435 MIN THEIN HTET & AUNG NAING OO (2017) Monitoring of Migratory

436 Shore Birds Survey in the Gulf of Mottama: Community-Led Coastal

437 Management Gulf of Mottama Project. CLCMGOMP, Yangon, Myanmar.

438 TOMKOVICH, P., SYROECHKOVSKIY, E., YAKUSHEV, N., LOKTIONOV, E.,

439 DIGBY, R. & SHEPELEV, I. (2016) Spoon-billed sandpipers in Meinypilgyno: 440 update of theFor 2016 breeding Peer season. Review Spoon-billed Sandpiper Task Force News 441 Bulletin, 16, 13-15.

442 ZÖCKLER, C., SYROECHKOVSKY, E.E. & ATKINSON, P.W. (2010a) Rapid and

443 continued decline in the spoon-billed sandpiper Eurynorhynchus pygmeus

444 indicates imminent extinction unless conservation action is taken. Bird

445 Conservation International, 20, 95–111.

446 ZÖCKLER, C., HTIN HLA, T., CLARK, N., SYROECHKOVSKY, E., YAKUSHEV, N.,

447 DAENGPHAYON, S. & ROBINSON, R. (2010b) Hunting in Myanmar is

448 probably the main cause of the decline of the spoon-billed sandpiper Calidris

449 pygmeus. Wader Study Group Bulletin, 117, 1–8.

450 ZÖCKLER, C., THET ZAW NAING, SAW MOSES, YAN NAUNG SOE & TONY

451 HTIN HLA (2014) The Importance of the Myanmar Coast for Water Birds.

452 Stilt, 66, 37–51.

453 ZÖCKLER, C., BERESFORD, A.E., BUNTING, G., CHOWDHURY, S.U., CLARK,

454 N.A., FU, V.K., HTIN HLA, T., MOROZOV, V.V., SYROECHKOVSKIY, E.E.,

455 KASHIWAGI, M., LAPPO, E.G. TONG, M., LONG, T.L., YU, Y-T., 21

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456 HUETTMANN, F., AKASOFU, H.K., TOMIDA, H. & BUCHANAN, G.M.

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458 Bird Conservation International, 26, 476-489.

459

460 Biographical sketches

461 PYAE-PHYO AUNG and SAW MOSES work on conservation and biodiversity

462 surveys in Myanmar.For NIGEL Peer A. CLARK, Review GUY Q.A. ANDERSON, GEOFF M. 463 HILTON and RHYS E. GREEN research the conservation of threatened birds.

464 GRAEME M. BUCHANAN applies remote sensing methods to conservation.

465 CHRISTOPH ZÖCKLER is Co-ordinator of the EAAFP Spoon-billed Sandpiper Task

466 Force.

467

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nd nd 244 199 156 112 population

Estimated SBS Estimated SBS

determined.

nd nd count 21,325 35,000 64,183 63,260 not

shorebird shorebird Total small Total means

SBS 2016.

0.0114 0.0057 0.0039 0.0063 0.0024 0.0018 –

Proportion Proportion of 2009

Mottama 19 99 51

175 215 280 units of

bootstrap Number of of Number Gulf

Upper

46 33 93 195 202 163 the

http://www.oryxthejournal.org scanned in

Number of NumberSBS of (SBS)

Oryx - The International Journal of Conservation

sandpipers 4,022 8,462

34,250 32,098 67,234 52,754 scanned

shorebirds For Peer Review Number of small Numbersmall of billed -

spoon

surveys

February

11 scan

January January January

February

February 16 21 23

2 13 - - - January

Results - -

13 1 19 24 17 7 Earliest and latest survey dates survey latest Earliest and 1.

TABLE 2009 2010 2011 2012 2015 2016 Year

Page 25 of 27 Oryx - The International Journal of Conservation

LEGENDS TO FIGURES

FIG. 1. The Upper Gulf of Mottama, with its location within Myanmar in the inset. The rectangular box on the main map defines the study area, within which we surveyed spoon- billed sandpipers. The intertidal zone in spring 2016 (the area between high tide on 13 February 2016 and low tide on 17 April 2016 ) is shown by the light grey shading.

FIG. 2. Proportion of spoon-billed sandpipers in scan surveys of small shorebirds in winter in the Upper Gulf of Mottama in relation to the year of the survey. Plotted points are overall proportions for each of six winter surveys. Vertical lines are 95% bootstrap confidence limits. The curve is the back-transformed relationship logit(proportion) = 445.2393-0.22396*calendar year fitted by ordinaryFor least squares Peer to the logit-transformed Review annual values. FIG. 3. Estimated population of spoon-billed sandpipers in winter in the Upper Gulf of Mottama in relation to the year of the survey for the four winters for which both proportions of spoon-billed sandpipers and total counts of small shorebirds were available. Plotted points are population estimates for each winter survey. Vertical lines are 95% bootstrap

confidence limits. The curve is the back-transformed relationship loge(population) =

187.4045 - 0.09056*calendar year fitted by ordinary least squares to the loge -transformed annual values.

http://www.oryxthejournal.org Oryx - The International Journal of Conservation Page 26 of 27

For Peer Review

http://www.oryxthejournal.org Page 27 of 27 Oryx - The International Journal of Conservation

0.025

0.020 For Peer Review

0.015

Proportion 0.010

0.005

0.000 2008 2009 2010 2011 2012 2013 2014 2015 2016 2017 Year

http://www.oryxthejournal.org Oryx - The International Journal of Conservation Page 28 of 27

FIG. 3. Estimated population of spoon-billed sandpipers in winter in the Upper Gulf of Mottama in relation to the year of the survey for the four winters for which both proportions of spoon-billed sandpipers and total counts of small shorebirds were available. Plotted points are population estimates for each winter survey. Vertical lines are 95% bootstrap confidence limits. The curve is the back-transformed relationship loge(population) =

187.4045 - 0.09056*calendar year fitted by ordinary least squares to the loge -transformed annual values.

For Peer Review

http://www.oryxthejournal.org