Journal of Applied Ecology 2015, 52, 1483–1491
doi: 10.1111/1365-2664.12508
The ecology and economics of shorebird conservation
in a tropical human-modified landscape
Jonathan M. H. Green1,2*, Siriya Sripanomyom3, Xingli Giam4,5 and David S. Wilcove1,4
1
Woodrow Wilson School, Princeton University, Princeton, NJ 08544, USA; 2Department of Geography, University of
Cambridge, Downing Place, Cambridge CB2 3EN, UK; 35/1 moo 9, Nonnamthang Sub-district, Muang District, Amnat
Charoen Province 37000, Thailand; 4Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544,
USA; and 5School of Aquatic and Fishery Sciences, University of Washington, Box 355020, Seattle, WA 98195, USA
Summary
1. Rapid and extensive land-use change in intertidal foraging habitat and coastal roosting
habitat is thought to be driving major population declines of shorebirds migrating through
the East Asian–Australasian Flyway. Along the Inner Gulf of Thailand, a critical stopover
and wintering ground for these birds, artificial wetlands (salt pans and aquaculture ponds)
have replaced much of the natural coastal ecosystem.
2. We conducted a two-part study to (i) assess the importance of salt pans and semi-traditional aquaculture ponds to shorebirds and (ii) understand the economic forces that drive
land-use change in this region by interviewing salt pan and aquaculture operators.
3. Salt pans provide important roost habitat, particularly for shorter-legged birds, which are
less able to utilize aquaculture ponds due to their greater depth. Moreover, three focal shorebird species foraged extensively in salt pans and semi-traditional aquaculture ponds, even
when intertidal mudflats were exposed, suggesting that artificial wetlands could buffer against
the impacts of degraded intertidal foraging areas for some shorebird species.
4. Economic profits from salt production and semi-traditional aquaculture are similar. Risks
to investment and per capita profitability are key factors in determining whether to convert
land from one use (e.g. salt pan) to the other (aquaculture).
5. Synthesis and applications. Salt pans provide an important resource to migrating shorebirds.
As development pressures increase, operators may need financial incentives if salt pans are to
be maintained over large areas. Although semi-traditional aquaculture is used less by shorebirds, drained ponds provide opportunities to roost and forage. Semi-traditional aquaculture
operators should drain their ponds regularly to provide supplementary habitat for shorebirds.
Use of nets and pond liners should be discouraged in both systems. Optimizing aquaculture
pond and salt pan management for shorebirds could provide a more pragmatic, cost-effective
and geographically extensive solution to conserving these birds than protected areas alone.
Key-words: aquaculture, artificial wetlands, East Asian–Australasian Flyway, migration,
roost site, salt pan, stopover, wintering
Introduction
Migratory species are challenging to conserve because
identifying and addressing the particular environmental
changes causing population declines is difficult when different life stages are completed in geographically disparate
places. Effective conservation requires an understanding
of both the ecological and socio-economic dynamics
underlying the threats. However, even when threats are
well understood for a given migratory species, implement*Correspondence author. E-mail: jmhg2@cam.ac.uk
ing conservation measures in one jurisdiction may be confounded by detrimental policies in another (Webster et al.
2002; Caddell 2005; Wilcove & Wikelski 2008). Migratory
shorebirds undertake some of the longest migrations
known, and many species are experiencing large population declines (IWSG 2003; Milton 2003). Species associated with the East Asian–Australasian Flyway (EAAF),
which includes shorebirds that migrate from Arctic breeding grounds to Australasian and South-East Asian wintering grounds, are of special concern. The flyway hosts the
greatest number of shorebird species of any major flyway
and has the highest proportion of threatened or near-
© 2015 The Authors. Journal of Applied Ecology © 2015 British Ecological Society
1484 J. M. H. Green et al.
threatened species (Kirby 2010; Mackinnon, Verkuil &
Murray 2012). It is also experiencing rapid conversion of
intertidal mudflats (Murray & Fuller 2015).
In addition to seasonal long-distance migration, many
shorebirds must also regularly commute to and from hightide ‘roost sites’ as the tide inundates and exposes intertidal
‘foraging’ grounds. There has been less focus on maintenance of these smaller-scale migrations and, more generally, the importance of roost sites for shorebirds (Burger,
Niles & Clark 1997; Masero & Perez-Hurtado 2001; Dias
et al. 2006; Dias 2009; Zharikov & Milton 2009). However,
both roost and forage sites require attention from conservationists, as conditions in one can affect the use of the
other. Disturbance at a roost site, for example, may lead to
underuse of nearby foraging sites (focal point regulation;
Dias et al. 2006; Rogers, Piersma & Hassell 2006; Zharikov
& Milton 2009). Alternatively, reduced feeding success in
foraging sites due to habitat degradation or density-dependent food availability may cause birds to seek supplementary feeding opportunities where they roost (e.g. Masero &
Perez-Hurtado 2001; Smart & Gill 2003). Spatial coupling
between roost and forage sites may therefore be as vital as
maintaining the network of stopover sites that link the
breeding and wintering grounds (Zharikov & Milton 2009).
The coastal region that sustains migratory shorebirds in
the EAAF has some of the highest human population densities on the planet (Creel 2003). Protecting shorebirds that
use this flyway requires that conservation practitioners reconcile multiple land uses with the multiple needs (resting,
foraging, migrating, breeding) of shorebirds. However, little work has been done to link our increasingly informed
understanding of shorebird ecology to that of the economic decisions taken by land managers. Here, we address
both ecological and economic issues affecting a key wintering site in the EAAF in order to guide policymakers
who must balance biodiversity concerns with human
development needs in this densely populated region.
As part of the EAAF, the Inner Gulf of Thailand provides important stopover and wintering habitat for shorebirds (Round 2006). The area supports internationally
important numbers (>1% of flyway population) of 19
shorebird species, including the near-threatened Asian
dowitcher Limnodromus semipalmatus, the endangered
Nordmann’s greenshank Tringa guttifer and the critically
endangered spoon-billed sandpiper Eurynorhynchus pygmeus (Round & Gardner 2008). One of the most pertinent
threats to shorebirds inhabiting the Inner Gulf of Thailand
is land-use change to roost habitat (Round & Gardner
2008; Mackinnon, Verkuil & Murray 2012). Coastal habitat
within 3 km of the shoreline comprises a mosaic of aquaculture ponds (40%), urban areas (21%), salt pans (17%),
mangroves (9%) and agriculture (6%) (Narungsri 2012; see
Table S1 in Supporting Information). It is here where roost
sites provide refuge for shorebirds during high tide.
Significant habitat alteration began as much as 800 years
ago, when coastal habitat was converted to salt pans for
the production of salt from sea water (Reid 1988; Round
2006). Salt production occurs in many coastal areas of the
world and provides roosting and foraging opportunities
for shorebirds (Warnock & Takekawa 1995; Masero &
Perez-Hurtado 2001; Warnock et al. 2002; Masero 2003;
Yasue & Dearden 2009; Sripanomyom et al. 2011). Salt
pans in the Inner Gulf, however, are now in significant
decline (Sintusaard 2009). In the 1980s, Thailand experienced a boom in intensive aquaculture production, and
rapid coastal development for shrimp ponds ensued. The
Inner Gulf was the first area to be exploited due to its
proximity to the country’s capital, Bangkok, resulting in
85% loss in mangrove area between 1975 and 1993 (Huitric, Folke & Kautsky 2002). Although this rapid change
was driven by the large profits that could be made, there
were concerns that much of the revenue was going to
wealthy external individuals who were investing in the
area, rather than to local farmers or communities (Sathirathai 1998). The increases in shrimp-farming intensity and
extent were eventually curtailed by the crash of the industry following rampant pollution and disease, which left
many ponds abandoned as investment was directed elsewhere along the coast (Sathirathai & Barbier 2001; Huitric,
Folke & Kautsky 2002). Alongside well-documented mangrove declines, many of the region’s salt pans were also
converted into shrimp ponds during the same period and
since (Sripanomyom et al. 2011; Narungsri 2012). Sripanomyom et al. (2011) showed clearly that, at a landscape
scale, shorebird richness and abundance were associated
with the presence of both intertidal mudflats and salt pans.
The authors also show that aquaculture ponds have lower
shorebird richness and abundance and that both salt pans
and, to a lesser extent, aquaculture ponds may be used for
supplementary feeding or roosting (Sripanomyom et al.
2011). Although conversion of salt pans to aquaculture in
Thailand is widely believed to be detrimental to shorebirds,
our knowledge about exactly how artificial wetlands are
used is limited and, crucially, even less is known about the
socio-economic incentives behind the conversions. Aquaculture is increasing globally, particularly in South-East
Asia, yet in these working landscapes, there is little formal
protection (Bostock et al. 2010). The remaining salt pan
operations in the Inner Gulf, and presumably elsewhere in
South-East Asia, could well be threatened again with conversion to aquaculture (Round 2006).
We undertook a two-part study to understand (i) how
shorebirds use the mosaic of anthropogenic and natural
habitats available in the Inner Gulf and (ii) the economic
forces that drive changes in land use, especially from salt
pans to aquaculture. We then linked these data to understand how different management strategies affect shorebirds.
Materials and methods
STUDY SITES
The study was conducted in the Inner Gulf of Thailand along a
50-km stretch of coast between the Mae Klong River (13371°N
© 2015 The Authors. Journal of Applied Ecology © 2015 British Ecological Society, Journal of Applied Ecology, 52, 1483–1491
Ecology and economics of shorebird conservation
100006°E) and the Samut Sakhon/Bangkok Provincial boundary
(13493°N 100394°E). At low tide, intertidal mudflats host thousands of foraging shorebirds. The rising tide displaces these birds
to inland roost sites. Little remains of the natural habitat that
they must once have used, but one semi-natural fragment, maintained as a nature reserve, persists 35 km east of our study region
at Bang Pu, Mueang Samut Prakan District (13518°N
100656°E), within a heavily industrialized area (Parr, Pukotchasarnseen & La-orphanphol 2012). That site is primarily mangrove, interspersed with abandoned, unvegetated shrimp ponds.
Salt pans are the primary roost habitat for shorebirds in most of
the Inner Gulf. During the months of salt production (October
to May), which coincide with the presence of overwintering
shorebirds, salt pan water depths are kept between 0 and 15 cm.
Using pumps and gravity, salt water is drawn from the ocean
and, through solar evaporation, its salinity increased as it passes
through a series of pans to produce an average of 70 tonnes of
hand-harvested salt per ha per year. Shallow pan depths and
sparse vegetation allow shorebirds good all-round visibility for
the detection of predators. Aquaculture ponds (particularly more
intensive ones), however, are deeper (water depths regularly
exceed 1 m), often surrounded by vegetation, and have steeper
banks; even when drained, shorebirds using them are probably
less able to detect terrestrial or airborne predators. Although
some aquaculture ponds have year-round water depths of >1 m,
precluding their use by shorebirds, many are drained periodically
for harvesting, maintenance, disease control or to mimic the natural tidal cycle. This is particularly true for less intensive systems,
as primarily found in our study region. Previous studies frequently classify aquaculture into either intensive or traditional
(e.g. Sathirathai & Barbier 2001). This dichotomy, however, hides
the continuum of intensities that are in operation. We found few
intensive aquaculture farms in our survey (i.e. those that tend to
rely heavily upon chemical and biological inputs, often operate at
an industrial scale and supply directly to an aquaculture products
company). We also found no traditional prawn-capture ponds in
which there are no chemical or biological inputs and which operate for subsistence and local markets. Instead, the majority of
ponds were either semi-traditional, in which biological inputs
(e.g. larvae and feed) remain high but chemical inputs are low, or
extensive traditional, in which ponds are enlarged (depth and
area) and in which some larvae may be used, but there are no
chemical inputs, and farmers still make use of natural tidal cycles
to drain and fill the ponds. Drainage cycles depend upon the
product. Fish and crab ponds, for example, were rarely drained,
unless the entire pond was to be harvested or if the farmer
wanted to dry out the pond bed in the sun, usually only once or
twice per year. Conversely, water depths in shrimp and clam
ponds were often subject to tidal cycles and then fully drained
once or twice a month. During drawdowns, even short-legged
shorebirds, such as small sandpipers, may be able to use them. In
addition, shorebirds may use pond edges (where not too steep),
drainage channels and associated waterworks.
DATA COLLECTION
Using recent coastal land-use data and ArcGIS (ESRI 2010; Narungsri 2012), we randomly selected points within 3 km of the
coast in salt pans (n = 50; median size = 72 ha; range = 26–
504 ha) and aquaculture ponds (n = 50; median size = 66;
range = 03–344; all pans and ponds are from separate farms).
1485
We also visited intertidal mudflats (n = 6, one visit per site) and
made two visits to the semi-natural conservation area at Bang Pu
(hereafter ‘mangrove–mudflat’; Parr, Pukotchasarnseen &
La-orphanphol 2012). These represent natural foraging habitat
and semi-natural roosting habitat, respectively. We did not collect
enough data to accurately estimate species richness or abundance
in intertidal mudflat or mangrove–mudflat habitat, and the sites
were not selected at random (Fig. S1). Instead, these habitats
were surveyed for data on time budgets and foraging success for
comparison with artificial wetlands. Surveys of bird richness and
abundance, behaviour and foraging success were completed over
two field seasons: March–April and October–November 2013.
Socio-economic questionnaire data were collected during the
second field season.
Each salt pan and aquaculture operation (hereafter ‘farm’; one
salt pan farm actually consists of a series of pans) was surveyed
once at high tide (2 hours) and once at low tide (2 hours).
We recorded all birds that alighted within a farm, walking along
its perimeter where necessary. We also recorded farm area,
weather conditions and water depth. For analyses, we split our
observations into shorebirds (Recurvirostridae, Charadriidae and
Scolopacidae) and non-shorebirds (all other species). Shorebirds
were subdivided into short-legged (<30 mm), medium-legged (30–
50 mm) and long-legged (>50 mm) shorebirds on the basis of tarsus length (Wells 1999; see Table S2 for species list and leg-length
classifications). In total, 49 species (15 708 individual birds) were
identified in aquaculture ponds and 54 species (34 594 individual
birds) in salt pans. Bird taxonomy is according to the IOC World
Bird List (Gill & Donsker 2015).
Intertidal mudflats were surveyed once at low tide (2 hours).
We could not survey an entire mudflat, so birds were enumerated
within a 100-m-radius semicircle from the observer standing on the
shore. This was the distance over which red-necked stint, our smallest focal species (see next paragraph), could be reliably observed.
Two high-tide visits were made to the mangrove–mudflat site.
Activity budgets and foraging success were estimated for three
focal shorebird species that represent different leg lengths (see
Table S2): red-necked stint Calidris ruficollis (short-legged), common redshank Tringa totanus (medium-legged) and black-tailed
godwit Limosa limosa (long-legged). Activity budgets were estimated from instantaneous flock scans, in which an entire flock
was scanned and the number of birds feeding (probing or scanning the ground for food), preening, roosting, being vigilant (stationary, not feeding, alert and looking about) or interacting with
other birds (chasing, aggression or mating behaviour) were
counted (Altmann 1974). Flocks were contiguous groups, within
which individuals had a maximum separation distance of <10 m.
Foraging success was estimated by conducting 90-second focal
observations on single birds (to minimize pseudoreplication, the
minimum distance between chosen individuals was 10 m). The
time spent actively foraging, number of pecks and number of successful pecks were recorded. Successes were ascertained from
observing the bird swallowing prey. Owing to their small prey
size and high intake rate, it was not possible to observe successes
for red-necked stints.
We also collected quantitative (e.g. estimates of revenue and
costs of production) and qualitative (e.g. motivations for converting farms) data during socio-economic surveys of salt pan
(n = 33) and aquaculture pond (n = 39) operators. Interviews
were conducted with operators of the same set of 100 salt pans
and aquaculture ponds surveyed for birds. If an operator was
© 2015 The Authors. Journal of Applied Ecology © 2015 British Ecological Society, Journal of Applied Ecology, 52, 1483–1491
1486 J. M. H. Green et al.
unavailable or unwilling to participate, then, where possible, the
operator of the nearest pan or pond using similar management
techniques was interviewed. Results were qualitatively similar
irrespective of whether these data were included or excluded from
analyses. We excluded data from five operators who were unable
to give detailed information due to recent changes in land use.
Values were recorded in Thai Baht (THB) and converted to 2013
$US for analysis and reporting (1THB = $US0.03).
MODELLING ABUNDANCE AND RICHNESS
Geographic data were analysed and processed in ArcGIS 10
(ESRI 2010). All other data manipulation, plotting and statistics
were completed in R using the FSA, mcmcplot, plyr and rjags
packages (Wickham 2011; McKay Curtis 2012; R Core Team
2013; Ogle 2014; Plummer 2014). Generalized linear mixed models (GLMMs) were constructed using the Bayesian framework in
JAGS (Plummer 2014). Abundance was modelled with negative
binomial errors due to the count data being overdispersed. Richness was modelled with Poisson errors. Each model contained
farm area as an offset and the sample site as a random intercept.
Candidate predictor variables, modelled as fixed effects, were
habitat type (aquaculture = 0, salt pan = 1), tide level (low = 0,
high = 1) and water level (in cm). To estimate posterior distributions, we ran Markov chain Monte Carlo (MCMC) simulations
using Gibbs sampling algorithm implemented in the rjags library
in R. Non-informative normal priors with mean 0 and an arbitrarily large variance 1000 were used for GLMM intercepts and
slopes. Non-informative uniform priors bounded between 0 and 5
were used to estimate the standard deviation of GLMM random
intercepts as well as the overdispersion parameter in the negative
binomial GLMM (for abundance). We used 10 000 iterations for
the initiation phase and 100 000 for burn-in. Posterior distributions were then derived by summing 4 MCMC chains, each consisting of 10 000 iterations thinned from 200 000. Models were
assessed visually for convergence. To identify the best-supported
predictors, we used covariate indicators in which the model is
extended to include, for each predictor, an extra Bernoullidistributed parameter (wj). This can vary from 0, no evidence that
the variable explains any of the variation in the response, to 1,
indicating the highest support for the predictor, j, to be retained
in the model (Graves et al. 2012). Initial values were set to
include all potential predictors (wj = 1).
Results
DIVERSITY AND ABUNDANCE
At high and low tides, shorebird richness and abundance
were higher in salt pans than in aquaculture ponds,
particularly for short-legged and medium-legged birds
(Figs 1 and S1). Shorebird abundance and richness were
higher in both salt pans and aquaculture ponds during
high tides vs. low tides, supporting the hypothesis that
shorebirds prefer to use intertidal mudflats when they are
accessible. However, some individuals, particularly longlegged and short-legged shorebirds, remained in salt pans
even during low tide when their natural intertidal foraging
habitat is exposed. Overall, the bird communities in aquaculture were dominated by non-shorebirds (e.g. herons,
egrets, cormorants, terns and gulls; Table S2). Salt pan
bird communities, on the other hand, have much greater
representation of short-legged and medium-legged shorebirds, which make up 74% of all the birds recorded in
this habitat (Fig. S2).
In GLMMs, the best predictors of short-legged and
medium-legged shorebird abundance and richness in
anthropogenic roost sites were habitat type (salt pan preferred over aquaculture; indicator variables = 087–1),
water depth (lower numbers as depth increased; indicator
variables = 061–1; see also Fig. S3) and tide (higher numbers at high tide; indicator variables = 1; Fig. 2). Habitat
type was less important for long-legged shorebirds (indicator variables = 001).
ACTIVITY BUDGETS AND FORAGING SUCCESS
The percentage of birds feeding within a flock was higher in
salt pans (black-tailed godwit: 49% of individuals; common
redshank: 53%; red-necked stint: 87%) than in aquaculture
(black-tailed godwit: 44%; common redshank: 11%; no
observations of red-necked stint due to their scarcity in
aquaculture). During feeding periods, however, foraging
rate and success were similar between salt pans and aquaculture with no significant differences for any of our three
focal species found at the a = 005 threshold for statistical
significance (Mann–Whitney U-tests: P value range:
022–041; see Fig. S4 and Table S3).
Across all three focal shorebird species and all habitats,
the mean proportion of time devoted to vigilance is
between 4% and 10%, but highly variable. Overall, the
mean percentage of vigilant individuals (not feeding or
resting) was slightly higher in aquaculture (7%) than in
salt pans (4%), but not significantly so for common redshank (Mann–Whitney U-tests: mean aquaculture = 11%,
mean salt pan = 2%, P = 0202) or black-tailed godwit
(Mann–Whitney U-tests: mean aquaculture = 2%, mean
salt pan = 2%, P = 1).
COMPARISON WITH NATURAL HABITAT
The most common behaviour in semi-natural mangrove–
mudflat habitat was roosting (39% of black-tailed godwits and 83% of common redshank; Fig. 3). Of our focal
species, only black-tailed godwit was observed foraging
in mangrove–mudflat (2% of individuals). Conversely,
intertidal mudflats were solely utilized for feeding by all
focal species (Fig. 3). We found little evidence that the
rate and success of feeding in anthropogenic landscapes
were significantly lower than those in more natural
habitats. At the a = 005 level, the only significant difference was a lower probe rate (but not a lower success
rate) for common redshank feeding in aquaculture
compared to intertidal mudflats (P = 0045; see Fig. S4
and Table S3).
There were, however, large differences between habitats
in the proportion of the flock displaying vigilance. Across
© 2015 The Authors. Journal of Applied Ecology © 2015 British Ecological Society, Journal of Applied Ecology, 52, 1483–1491
1
Tide
•
0
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–50
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3
0·61
0·5
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1·0
1·5
2·0
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Habitat
•
(e)
0·87
Water
•
0·69
Tide
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0·5
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0·5
–100
1·0
1·5
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3·0
Habitat
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Water
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Tide
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(f)
100
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Tide
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0·01
50
2
Habitat
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Habitat
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Water
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Tide
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(c)
–100
3
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•
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(d)
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Habitat
•
(b)
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Richness ha–1
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4
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long–legged
(f)
Low
1
3
1
Richness ha–1
0
1
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2
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High
1
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High
long–legged
(c)
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medium–legged
(e)
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Log10 abundance ha–1
High
Water
•
0
1487
short–legged
High
medium–legged
(b)
Habitat
•
(a)
(d)
Low
0
Log10 abundance ha–1
High
Fig. 1. Comparison between aquaculture
ponds (grey) and salt pans (white) of
abundance (a–c; log10[bird density+1]) and
richness (d–f) for high and low tides. For
both abundance and richness, differences
between habitat types decrease as shorebird leg length increases from short-legged
(a, d), through medium-legged (b, e) to
long-legged shorebirds (c, f). Solid bars
show median; grey and white boxes show
interquartile range (IQR); whiskers indicate the lowest and highest points within
15 times the IQR of the upper and lower
quartiles; data points beyond 159 IQR
are shown as circles. Non-overlapping
notches around the medians are good evidence for significantly different distributions (Chambers et al. 1983).
3
short–legged
2
3
(a)
0
Log10 abundance ha–1
Ecology and economics of shorebird conservation
–50
0
0·01
1
0·78
50
100
Fig. 2. Summary of parameter coefficients and variable importance. Mean (black circle) and density plot (dark horizontal line) of
parameter coefficients is given for each variable for abundance (a–c) and richness (d–f). Analyses were run for short-legged (top row),
medium-legged (second row) and long-legged (third row) shorebirds. For each, the influence of the fixed effect component of the model
is plotted for habitat type (‘habitat’: either aquaculture = 0 or salt pan = 1), water level in the pond/pan (‘water’: in cm) and tide level
(‘tide’: low = 0 or high = 1). The grey bars to the right of the plots show the proportion of times in which the variable was chosen for
inclusion in the model and, hence, its importance on a scale of 0 to 1 (actual proportion is written by each bar).
focal species, vigilance was highest in mangrove–mudflat
habitat (30%), which was three times greater than in
aquaculture and ten times greater than in salt pans. No
birds were observed being vigilant in intertidal mudflats.
OPERATOR CHARACTERISTICS
There was little difference in the distribution of age (aquaculture: mean = 54 years 13[sd]; salt pans: mean = 57 years
© 2015 The Authors. Journal of Applied Ecology © 2015 British Ecological Society, Journal of Applied Ecology, 52, 1483–1491
20
40
60
80
Other
Preening
Roosting
Feeding
n = 32(1)
n = 2754(42)
n = 0(0)
n = 36(2)
n = 822(8)
n = 249(7)
n = 612(6)
40
60
80
100
0
20
40
60
80
100
n = 0(0)
20
0
Black−tailed godwit (% of flock)
Common redshank (% of flock)
0
Red−necked stint (%of flock)
100
1488 J. M. H. Green et al.
n = 2601(6)
n = 2194(7)
n = 2296(14)
n = 3806(5)
Fig. 3. Activity budgets for focal species: from top, red-necked
stint, common redshank and black-tailed godwit. Budgets (% of
flock undertaking each behaviour) are shown for four sampled
habitat types: mangrove–mudflat, intertidal mudflat, salt pans
and aquaculture ponds (left to right). Total number of birds from
which percentage is taken is given below each bar along with the
number of flocks (i.e. independent samples) in brackets.
12) or land holdings (as a proxy for wealth; aquaculture:
mean = 137 ha 171; salt pans: mean = 162 ha 187)
of salt pan and aquaculture pond operators, suggesting that
they are drawn from a similar demographic. Land tenure is
also similar between the groups. Approximately half of all
interviewees own their farms and the remainder rent it or
manage it for a fee (aquaculture: own = 56%, rent = 38%,
manage = 5%, n = 39; salt pans: own = 44%, rent = 47%,
manage = 9%, n = 32). We found no evidence that aquaculture farmers are richer, younger or live farther away than salt
pan farmers. Moreover, many aquaculture farmers were
previously salt pan farmers.
BENEFITS AND COSTS
Net revenues are similar between salt pans and aquaculture, both generating around $US1000 per ha although
there is greater variation for aquaculture, a more hetero-
Fig. 4. Comparison of profits (left) and costs (right) for aquaculture (grey boxes) and salt pans (white boxes, black border). The
number of hours worked by household members (HH hours) is
plotted against the right-hand axis. Solid bars show median;
boxes show interquartile range; whiskers indicate the lowest and
highest points within 15 times the interquartile range of the
upper and lower quartiles; outliers are not plotted to visualize
differences in medians more clearly.
geneous group of enterprises (Fig. 4). The costs of production are also broadly similar within categories with
two notable exceptions: the greatest aquaculture expenses
are related to chemical and biological inputs to improve
water quality and to stock ponds, whilst this kind of
expenditure is not necessary for harvesting salt, where the
biggest expense was hired labour. Both farm types used
household labour, but salt pan farmers used a greater
amount. Net revenue per ha per hour of household labour
shows aquaculture to be slightly more profitable in terms
of household labour investment, but not significantly so.
FARMER MOTIVATIONS AND RISK
As a proxy for risk, we first looked at the variability in
profits. Although median profits are similar between farm
types, there is greater variability in aquaculture, where
both the rewards and the losses can be greater (Fig. 4).
Secondly, we asked farmers to report changes in farming
productivity that they have experienced over the past
5 years. Aquaculture farmers experienced greater percentage declines (median = 50%; range 0 to 90%) than
salt pan farmers (median = 30%; range 0 to 50%),
which were largely attributed to increased water pollution
(aquaculture) and changing rainfall patterns (salt pans).
Lastly, we asked farmers their reasons for not converting
to the other farm type. Those who chose to operate aquaculture ponds were concerned that salt pans were too
labour intensive both in terms of household labour and
for hired labour, which can be difficult to obtain and is
increasingly expensive. Salt pan operators, on the other
hand, feared the high risks that they associate with aquaculture farming, in particular, the external threat to productivity from water pollution by factories.
© 2015 The Authors. Journal of Applied Ecology © 2015 British Ecological Society, Journal of Applied Ecology, 52, 1483–1491
Ecology and economics of shorebird conservation
HOW DOES PROFITABILITY AFFECT USE BY
SHOREBIRDS?
We tested (separately for aquaculture and salt pans)
whether farm profitability negatively influenced abundance or richness of birds on surveyed farms. When profit
was included as a predictor, covariate indicator values
were always zero, suggesting that, within the range of
farms encompassed by this study, shorebird communities
can be as species rich and abundant in highly profitable
farms as in less profitable ones (see also Fig. S5).
Discussion
Aquaculture ponds and salt pans provide suitable habitat
for shorebirds, with 19 and 28 species recorded in them,
respectively. At high tide, salt pans are preferred, particularly for short- and medium-legged shorebirds. With continuing salt pan declines, these birds (including threatened
great knot, Nordmann’s greenshank and spoon-billed
sandpiper) will suffer disproportionately. Aquaculture
ponds are used less often, especially by shorter-legged
shorebirds, probably because of greater water depths and
steeper banks (the latter heightening predation risk).
Although drained aquaculture ponds are used for roosting
and foraging by these birds (e.g. Bellio, Kingsford &
Kotagama 2009), we caution that this is not necessarily
representative of other areas. There are concerns amongst
bird conservation organizations over the increased numbers of intensive aquaculture ponds in the Inner Gulf of
Thailand, which require large capital investments, often
use large amounts of biological and chemical inputs and
actively exclude birds, and are incompatible with shorebird conservation (P. Round pers. comm.). Understanding
and recognizing the value of different types of aquaculture
to different shorebird species is essential.
Use of artificial wetlands as foraging habitat may become
increasingly important with decreases in quality or extent
of intertidal mudflat. If, as predicted, intertidal mudflats
are lost through increased rates of erosion, whilst being
squeezed between impermeable coastal developments and
rising sea levels (Iwamura et al. 2013), they may no longer
support shorebirds in their current numbers and densities,
thereby increasing the importance of supplementary feeding
opportunities in salt pans and aquaculture ponds to maintain shorebird populations (Round 2006; Ma et al. 2010).
When water levels allow, shorebirds in salt pans and
aquaculture ponds show similar levels of feeding success to
that observed in intertidal mudflats. Many individual
shorebirds, particularly short- and long-legged species,
remain in salt pans at low tide. Salt pans cannot substitute
intertidal mudflats but, although we cannot generalize to all
shorebird species, these individuals are displaying a preference for feeding in roost sites. This suggests that, in some
situations and for some species, salt pans are as good as, or
better than, intertidal mudflats for foraging, once the energetic costs of moving between sites and the difference in
1489
energy intake rates are accounted for (Smart & Gill 2003;
Yasue & Dearden 2009). This corresponds with findings
from southern Europe, where the majority of shorebird
energy needs were met through feeding in salt pans, which
were preferred over intertidal mudflats during the critical
pre-migration period, when birds must deposit large
amounts of fat (Masero & Perez-Hurtado 2001; Masero
2003). Our conclusions, however, are limited by a lack of
data on prey size and type in surveyed habitats. Elsewhere
in Thailand, the main food resources available to shorebirds in roosting habitats are polychaete worms, beetles,
midge and fly larvae, backswimmers and dragonfly larvae
(Yasue & Dearden 2009). Salt pans were found to provide
higher-quality habitat for small shorebirds than natural
supratidal wetlands due to the greater abundance of midge
and fly larvae (Yasue & Dearden 2009). Difficulties accessing privately managed salt pans and aquaculture ponds prevented us from taking benthic samples, which would help
determine differences in prey size, availability and quality
to allow a more complete analysis of any differences in
energy intake rates between all habitat types.
Although intake rates are similar between habitats when
shorebirds were feeding, they spent a greater proportion of
time feeding in intertidal mudflats than in salt pans or
aquaculture ponds. In areas with greater vegetation cover
or predation risk, shorebirds spend more time vigilant and
undertaking predator avoidance strategies (Rogers,
Piersma & Hassell 2006; Zharikov & Milton 2009). Vigilance was indeed lowest in the most open habitat (mudflats)
and increased through salt pans and then aquaculture as
vegetation cover increased. Shorebirds in mangrove–mudflat were most vigilant, possibly because it is the most heavily vegetated. Therefore, the net energetic benefit derived
from feeding on intertidal mudflats could still be greater
than from artificial wetlands. Aquaculture ponds, with
steep sides, surrounding vegetation and positioned below
ground level, may have higher rates of predation or require
greater vigilance, particularly as sediment is dug out and
sold to construction companies, creating ever-deeper
ponds. Although we did not investigate this directly, our
impression is that whilst excavating pond beds was not
cited as a primary incentive to convert from salt pans to
aquaculture, it seems likely that it can help to reduce the
burden of initial capital costs of aquaculture production. In
addition, there remain many aquaculture farmers with
debts from the aquaculture crash of the 1990s for whom
selling sediment provides an important source of capital.
Moreover, the cost of filling in excavated aquaculture
ponds could present a barrier to farmers wishing to reinstate salt pans. Although salt pans are better for shorebirds
than aquaculture, there could nonetheless be a benefit to
maintaining aquaculture ponds to ensure a diversity of
anthropogenic land uses that contribute to shorebird survival. This is because some types of aquaculture pond are
certainly better than other uses (e.g. urban or industrial)
and because providing habitat for longer-legged birds such
as herons and egrets may, if density dependence is impor-
© 2015 The Authors. Journal of Applied Ecology © 2015 British Ecological Society, Journal of Applied Ecology, 52, 1483–1491
1490 J. M. H. Green et al.
tant for foraging or roosting opportunities, be beneficial to
shorter-legged species by reducing crowding on salt pans.
Land-use diversity will also confer economic resilience to
the local community in the face of environmental changes
or fluctuations in salt or aquaculture markets.
Primary considerations for landowners along the Gulf of
Thailand include their expected profit and the security of
their financial or labour investment. Profits for aquaculture
were similar to those for salt pans. Disease and pollution
from nearby industrial and urban centres pose significant
risks for aquaculture farmers (Flaherty, Vandergeest &
Miller 1999). These externalities are largely beyond an individual farmer’s control. The aquaculture industry is also
susceptible to changes in international demand and supply,
given that 90% of production is exported (Huitric, Folke &
Kautsky 2002; Bostock et al. 2010). Vulnerabilities increase
for more intensive aquaculture, which requires larger capital investment, and could explain why there were few such
operations in our study area. Whilst semi-traditional and
extensive-traditional aquaculture farmers satisfy much of
their labour requirements through household efforts, the
dependence of salt harvesting upon hired workers means
that salt farmers are more vulnerable to changes in the
labour market. Labour shortages and increasing wages are
chief concerns. However, expenditure on hired labour is
also a mechanism for distribution of revenue through a
community. Salt pan operators also reported that changes
in rainfall patterns had decreased their annual yields, which
could become an increasing concern if climate change
results in shorter or wetter dry seasons.
Several management recommendations follow from our
study. First, where possible, salt pans should be maintained
extensively across the landscape to provide supplementary
foraging opportunities to species that are not limited to foraging exclusively in the intertidal region. Secondly, semitraditional and extensive-traditional aquaculture ponds
should be managed to enhance their value to shorebirds by,
for example, regular draining of ponds. If draining cycles
are asynchronous between farms and frequent enough
across the farming landscape, it seems possible that aquaculture ponds could contribute significantly to conservation
of shorebirds, although this hypothesis remains to be
tested. Other factors likely to be important are the depth
and steepness of ponds and banks, the use of pond liners
and nets, and the surrounding vegetation cover. Further
work is needed to discern the effects of different aquaculture management actions on the quality of the habitat for
shorebirds. Thirdly, reducing water pollution may have a
twofold effect: improving the quality of foraging and roosting sites for shorebirds, whilst simultaneously reducing
yield losses from aquaculture, making operations more economically viable. Urgent efforts should be made to reduce
the industrial and urban pollution that accumulates in
waterways, as well as the pollution and disease that are particularly associated with more intensive aquaculture.
Finally, we found no evidence that more profitable salt
pans or aquaculture ponds provided poorer habitat for
shorebirds. Therefore, within the range of farming practices
and strategies covered in our surveys, conservation organizations can work with farmers to help them maximize
revenues.
Given increasing pressure on coastal ecosystems, conservation scientists must investigate ways that anthropogenic land uses can be better managed for shorebirds.
Salt pans, in particular, appear to offer similar benefits to
some shorebird species as nearby habitat within a nature
reserve. They are, however, vulnerable to conversion with
changing markets and environmental conditions. With
only one nature reserve existing in the area, maintaining
an extensive network of shorebird roost sites in salt pans
and aquaculture ponds may be an economically efficient
strategy to preserve crucial shorebird habitat in the
region. A major challenge for conservationists will be to
incentivize salt pan maintenance in the face of other, perhaps more lucrative, land-use options. Combining ecological analyses with a deeper understanding of the economic
forces driving change is vital to the work of reconciling
land-use conflicts that is needed to formulate timely and
equitable conservation policies that effectively conserve
shorebirds within the constraints and opportunities associated with maintaining human livelihoods.
Acknowledgements
We thank the farmers who gave their time and expertise during interviews.
We also thank Charlotte Chang, Bert Harris, Morgan Tingley, members
of the Bird Conservation Society of Thailand, particularly Phil Round and
Wicha Narungsri, and three anonymous reviewers and the editors for
insightful comments on this manuscript. The High Meadows Foundation
and the Program in Science, Technology, and Environmental Policy at the
Woodrow Wilson School for Public and International Affairs supported
the work. Approval was obtained from the Institutional Review Board for
Human Subjects, Princeton University (protocol #6157).
Data accessibility
Bird survey data (abundance, foraging rates and activity budgets) and
anonymized socio-economic data: DRYAD entry doi:10.5061/dryad.kc470.
(Green et al. 2015)
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Handling Editor: Richard Fuller
Supporting Information
Additional Supporting Information may be found in the online version
of this article.
Figure S1 Species accumulation curves for surveyed habitat types.
Figure S2 Proportion of shorebirds (by size class) within salt pan
and aquaculture bird communities.
Figure S3 Relationship between water level and bird abundance
and richness.
Figure S4 Focal species’ foraging rate and foraging success by
habitat type.
Figure S5 Relationship between operator profits and shorebird
abundance and richness.
Table S1 Coastal land use in the Inner Gulf of Thailand.
Table S2 Number of individuals and frequency of observations of
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Table S3 Mann-Whitney U test results for Fig. S4.
© 2015 The Authors. Journal of Applied Ecology © 2015 British Ecological Society, Journal of Applied Ecology, 52, 1483–1491