Research Article
Habitat Association and Conservation
Status of the Endangered Giant Nuthatch
(Sitta magna) in Thailand
Tropical Conservation Science
Volume 11: 1–10
! The Author(s) 2018
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DOI: 10.1177/1940082918798332
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Supatchaya Techachoochert1, George A. Gale2,
Jenjit Khudamrongsawat1, and Philip D. Round1
Abstract
The Giant Nuthatch Sitta magna is restricted to southwestern China, eastern Myanmar, and northern Thailand. Although
globally endangered, most aspects of its ecology remain as yet unquantified. To assess its habitat associations and population
size, we conducted point counts with playback at 42 sample points across 12 discrete historical and potential localities within
its Thai range during October to November 2015. Eleven habitat variables were measured, including three site-level vegetation variables and eight landscape variables were assessed, using geographic information system land cover maps. Nmixture models were applied to estimate density and extrapolate the size of the population. The Giant Nuthatch was found
at four localities (12 of the 42 sample points) at elevations between 1,192 m and 1,738 m. It was not detected at four
historical Giant Nuthatch localities in protected areas. Abundance increased with increasing elevation, increasing proportion
of evergreen forest, and greater distance from villages. We estimated that the Thai population of Giant Nuthatch was
approximately 964 individuals based on an average density of 1.96 individuals/km2 in approximately 491.8 km2 of appropriate
forest habitat at 1,192 m to 1,951 m elevation. This may be an overestimate because available forest cover maps and images
do not distinguish between the characteristic, patchily distributed, lower montane open pine–oak forest association used by
Giant Nuthatch and denser, closed-canopy forest. Although Thailand’s Giant Nuthatch population may be better protected
than those in adjoining countries, we suggest that it remains threatened by forest fragmentation and habitat degradation
throughout its range. Further comprehensive research is needed to assess the status of the remaining global population and
the reasons for its scarcity.
Keywords
population estimate, distribution, N-mixture models, habitat degradation, Sitta magna
Introduction
The Giant Nuthatch (Aves: Sittidae: Sitta magna) is a
resident species of mixed coniferous and broad-leaved
forest, in which pines (Pinus spp.), oaks, and chestnuts
(Fagaceae) predominate at montane elevations between
approximately 1,200 and 3,400 m (BirdLife
International, 2016; Round, 1983). Its world range
encompasses southwestern China, eastern Myanmar,
and northern Thailand (BirdLife International, 2016;
Harrap & Quinn, 1996; Matthysen, 1998). The global
threat status of Giant Nuthatch was uplisted from vulnerable to endangered in 2012 (BirdLife International,
2016) due primarily to the loss and degradation of pine
and mixed forest habitats through shifting cultivation,
logging, and frequent fires. The nuthatch has
disappeared from some former localities and has
become rarer in all countries in its range (Bezuijen,
Eaton, Gidean, & Rheindt, 2010; BirdLife
International, 2016; Round, 1984). Its global population
is thought to have declined dramatically and was estimated at approximately 1,000 to 2,499 individuals with
1
Department of Biology, Faculty of Science, Mahidol University,
Bangkok, Thailand
2
Conservation Ecology Program, School of Bioresources & Technology,
King Mongkut’s University of Technology Thonburi, Bangkok, Thailand
Corresponding Author:
Supatchaya Techachoochert, Department of Biology, Faculty of Science,
Mahidol University, Bangkok, Thailand.
Email: t.supatchaya@gmail.com
Creative Commons Non Commercial CC BY-NC: This article is distributed under the terms of the Creative Commons AttributionNonCommercial 4.0 License (http://www.creativecommons.org/licenses/by-nc/4.0/) which permits non-commercial use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages (https://us.
sagepub.com/en-us/nam/open-access-at-sage).
2
only 6 to 50 mature individuals in the largest subpopulation (BirdLife International, 2016). There is great
uncertainty as to its numeric status, however. The population for Yunnan province, China, alone was estimated at 800 to 2,000 mature individuals (BirdLife
International, 2016), but this was based on very limited
data. There are no recent published records whatsoever
from Myanmar. However, even an upper limit of 2,499
individuals across its world range would be indicative of
extreme scarcity for this relatively small bird. Clearly,
there is an urgent need for more information on the
status of this species.
Montane areas in northern Thailand have been subjected to rapid land-use change, especially since the
1960s (Fox, Krummel, Yarnasarn, Ekasingh, &
Podger, 1995). Overall, forest cover in Thailand was
reduced from 53% of the country’s area in 1961 to
approximately 25% in 1998, an average annual loss of
120,000 ha (Charuphat, 2000; Fox & Vogler, 2005).
Moreover, road development and human population
growth expanded greatly during the same period.
During 1976 to 1989, approximately 1.2 million new
agricultural households and 17,000 km of roads were
added in northern and northeastern Thailand
(Cropper, Griffiths, & Mani, 1999). Deforestation not
only causes habitat loss but also increases habitat fragmentation, reducing patch sizes and core areas and isolating
suitable
habitats
(MacDonald,
2003;
Pattanavibool & Dearden, 2002). Activities such as
slashing and burning of natural vegetation, associated
with shifting cultivation, and excessive use of pesticides
are also major factors decreasing the habitat quality
(Fox & Vogler, 2005; Rerkasem, 1998).
Nonetheless, coverage of protected areas in the montane zone of three provinces of northern Thailand in
which Giant Nuthatch occurs (Chiang Rai, Chiang Mai,
and Mae Hong Son) is high: 55% of the montane forest
area above 1,000 m (2,146 km2) is already protected as
either national park or wildlife sanctuary (data retrieved
from Royal Forest Department [RFD] geographic information system shapefiles). Despite this relatively high level
of protection, the Giant Nuthatch population in Thailand
is still thought to be declining.
Our objective was to estimate the likely population
size of Giant Nuthatch in Thailand to assess the country’s contribution to the global population of the species
and contribute toward the formulation of a species conservation plan.
We focused on the historical and potential areas of
occurrence to assess the presence and estimate the abundance of the nuthatch throughout its range in Thailand.
We expected that habitat features such as the proportion
of pine and hill evergreen forest, canopy height, and tree
density would all positively influence the probability
of presence.
Tropical Conservation Science
Methods
Study Area
Northern Thailand has a complex, mainly mountainous,
terrain supporting a mosaic of different forest types
(Smitinand, 1977) that rises to a maximum elevation of
2,565 m. The study was conducted at sites with historical
records of Giant Nuthatch identified from BirdLife
International (2001), Bird Conservation Society of
Thailand (recent unpublished data), and other potential
areas within the historical range of Giant Nuthatch.
Surveys extended as far east as the western flank of the
Khun Tan mountain range which delineates the eastern
border of Chiang Mai Province and west to the border
with Myanmar (18 200 –20 70 N, 97 400 –99 240 E; Table 1,
Figure 1).
The surveys were restricted to forest areas between
1,000 and 1,830 m, as there were no confirmed historical
records below 1,200 m, while there was only one record
above 1,830 m (Deignan, 1946; Lekagul & Round, 1991;
Robson, 2000). Sampling large areas of forest completely randomly was not logistically feasible due to the ruggedness of the terrain. We therefore selected 42
accessible survey points (Figure 1) where native pines
Pinus kesiya Royle ex Gordon were frequent or occasionally dominant at elevations above 1,000 m, and
each point was located at least 1 km apart to avoid
site dependence. We conducted observations on three
occasions at each point from October 6 to November
24, 2015.
Observation Methods
We conducted field studies during the prebreeding
season when bird activity was thought to be high and
individuals frequently responded to each other’s calls
(Charonthong & Sritasuwan, 2009). Because Giant
Nuthatches have loud and distinctive calls, we considered that the probability of missing calling nuthatches
that were present in the area of study was low. We conducted point-count surveys by using playback of vocalizations of Giant Nuthatch to increase the probability of
detection (Bibby, Burgess, & Hill, 1992). Recordings of
calls and songs were obtained from the Xeno-canto
database (www.xeno-canto.org). During the surveys,
the nuthatch contact call was played for 30 s, followed
by 5 min of observation and repeated. If there was no
response in either the first or the second round, a third
round in which the bird’s territorial song was played
instead, for 30 s, followed by observations for a further
5 min, took place. Playback of song was then repeated
once more if there was still no response. Each session
might therefore extend to a maximum of 22 min (30 s of
call or song þ5 min observation, repeated four times).
3
Techachoochert et al.
Table 1. Localities Surveyed for Giant Nuthatch During This Study (2015) Including Known Historical Sites and Potential Sites, Protection
Status of Each Locality, and Detection During This Study.
Survey localities
Doi Langka, Khun Chae National Park
(Chiang Mai and Chiang Rai)
Huai Hin Lad Nai Village, Wiang Pa Pao
District (Chiang Rai)
Mae Ngai Watershed Station
(Chiang Mai)
Baan Mae Kiang, Mueang Na District
(Chiang Mai)
Doi Ang Khang Royal Project Center
(Chiang Mai)
Doi Pha Hom Pok National Park
(Chiang Mai)
Doi Lang, Doi Pha Hom Pok National
Park (Chiang Mai)
Pang Ung Royal Project Center (Mae
Hong Son)
Pha Son Wat Chan Royal Project
Center (Chiang Mai)
Khun Mae Ya Watershed Management
Unit (Mae Jok Luang), Huai Nam
Dang National Park (Chiang Mai and
Mae Hong Son)
Doi Inthanon National Park
(Chiang Mai)
Doi Chiang Dao Wildlife Sanctuary
(Chiang Mai)
Doi Suthep-Pui National Parka
(Chiang Mai)
GPS locations
0
0
Designation
Latest historical record
Riley (1938)
Detection
during this
study
19 00 N, 99 05 E
Protected area
19 170 N, 99 200 E
Nonprotected
19 300 N, 98 480 E
Nonprotected
2009 (sight record)b
Yes
19 420 N, 98 500 E
Nonprotected
2009 (sight record)b
No
19 510 N, 99 020 E
Nonprotected
1983 onward
Yes
20 000 N, 99 090 E
Protected Area
No
20 030 N, 99 050 E
Protected Area
1982 sight record (BirdLife
International, 2001)
2012 onward
19 290 N, 97 540 E
Nonprotected
No records known
No
19 050 N, 98 200 E
Nonprotected
No records known
No
19 140 N, 98 350 E
Nonprotected
1997 sight record (BirdLife
International, 2001)
No
18 300 N, 98 300 E
Protected area
1931 (two specimens)
No
19 220 N, 98 500 E
Protected area
1987 onward
Yes
19 000 N, 99 050 E
Protected area
1967 (a specimen)
No records known
No
No
Yes
Note. Province name is in parentheses.
Doi Suthep-Pui National Park (not surveyed) has had no records of Giant Nuthatch since 1967 despite multiple surveys over the past 50 years.
b
Unattributed sight records are those held on file by Bird Conservation Society of Thailand.
a
We recorded the presence of the species by either sighting (measuring the distance of the bird from the observer
with Bushnell Sport 450 laser range finder) or when
hearing vocalization (the distance was estimated).
Surveys were conducted from sunrise to 10:00 h, only
on days without rain or high winds, by two observers.
Vegetation Sampling
We measured habitat characteristics at each sample
point following Bibby et al. (1992) to assess possible
habitat requirements of the species. We used a fivefactor angle-gauge centered at the sample point (Avery
& Burkhart, 2015), which is held a set distance (60 cm)
from the eye of the observer. All trees that were larger
than the width of the angle gauge, as viewed from the
center of the plot, were counted. Three components: tree
species, height, and diameter at breast height were
recorded (Table 2), and diameter at breast height was
used for calculating the basal area (m2/ha).
We measured landscape composition metrics within a
300 m radius around each sample point (Table 2). This
distance was based on very limited telemetry data indicating that a male Giant Nuthatch territory was approximately 19.7 ha (Techachoochert, 2018). Distance from
the observation point to the nearest village was measured using ArcGIS 10.6 (ESRI, Redlands, USA).
The pine species with which Giant Nuthatches are
associated in northern Thailand, P. kesiya, typically
occurs mixed with broad-leaved trees. Pines do not usually dominate, except in small stands on drier ridges, so
that areas of hill evergreen forest in which pines were
frequent were usually indistinguishable from other hill
evergreen forest associations in available satellite images
4
Tropical Conservation Science
Figure 1. Map showing 42 survey points across 12 localities in northern Thailand. Former known localities but not detected (18 sites);
former known localities where detected (11 sites). Additional sites with apparently suitable habitat (not detected, 12 sites; detected,
one site).
Table 2. Descriptions, Means, and SE of Site and Landscape-Scale Variables in 42 Sample Sites Where Giant Nuthatch Was Detected or
Nondetected, Used in Our N-Mixture Models Analysis.
Detected
Variable
Description
Site covariates
BA
Basal area (m2/ha) at sample point
Height
Average canopy height of counted trees
Oak
Oak ratio (number of oaks and chestnuts or total number
of trees counted with angle gauge)
Landscape covariates
Elev
Elevation (m) above sea level
Slope
Slope (%) from horizontal
Aspect
Aspect (degrees) from the north
Village
Distance (km) to the closest village
Pine
Proportion of pine forest in 300 m radius around survey point
Evg
Proportion of hill evergreen forest in 300 m radius around
survey point
Mix
Proportion of mixed deciduous forest in 300 m radius
around survey point
Agri
Proportion of agricultural land in 300 m radius around survey point
Note. SE ¼ standard error.
Nondetected
Mean
SE
Mean
SE
16.6
16.9
0.21
1.6
1.9
0.06
21.8
18.1
0.14
1.9
0.7
0.04
1,536
12.5
157.5
8.0
0.230
0.650
41
0.8
29.3
1.3
0.121
0.121
1,346
14.6
169.3
6.7
0.450
0.250
39
1.4
19.1
0.6
0.087
0.075
0
0
0.030
0.018
0
0
0.220
0.073
5
Techachoochert et al.
of forest cover. We used accessible maps of forest cover
provided by the Forest Survey and Assessment Division,
RFD, Thailand based on Landsat data from year 2000
and intensive ground surveys. Forest cover was classified
following Smitinand’s (1977) forest classification which
separates pine forest from hill evergreen forest.
However, Maxwell (2004) and other authors (Santisuk,
1988; Werner & Santisuk, 1993) do not use the term
“pine forest” but refer to this as either “primary evergreen forest with pines” or “lower montane pine–
oak forest.”
Following Smitinand (1977), pine forest was defined
as forest about 200 to 1,300 m in elevation with poor
acid soils in which either of the native pines P. kesiya or
P. merkusii Jungh et De Vriese are predominant.
Although pine forest classified by RFD therefore included some areas of P. merkusii—deciduous dipterocarp
association that were not used by Giant Nuthatches, as
most such areas were below 1,000 m they could be
excluded from the areas covered by our assessment.
Hill evergreen forest, also known as lower montane
forest, was defined as forest at or above 1,000 m elevation with annual rainfall 1,500 to 2,000 mm. The dominant trees were oaks and chestnuts (Fam. Fagaceae),
but pines also occur admixed in many areas.
Abundance Model Analysis
We assessed the abundance of Giant Nuthatches in our
study area by using N-mixture models (Royle, 2004). We
assumed population closure as our surveys took place
over relatively few successive days at each survey
point. N-mixture provides an estimate of two parameters: mean abundance per site (n) and detection probability (p). The density can be estimated by dividing
abundance (n) by a fixed-radius area.
For the analysis of habitat associations, continuous
variables were standardized by dividing their value by
twice the standard deviation (Vaughn, 2008). We also
tested correlations among habitat variables to avoid
multicollinearity using Spearman’s correlation coefficients and removed one of each pair where the correlation coefficient was .6. Following this, we eliminated
the proportion of pine forest, proportion of oak and
chestnut trees, and basal area from the same models.
To model abundance, the global model was adjusted
according to three different distributions (i.e., negative
binomial, Poisson, and zero-inflated Poisson) and differing values for the upper limit of integration (K). All
global models were then tested for goodness of fit by
means of a Pearson chi-square test (MacKenzie &
Bailey, 2004) using parametric bootstrap resampling
(1,000 resamplings). Abundance with site covariates
was then modeled using a negative binomial distribution
(c-hat ¼ 1.04) while setting the detection probability
constant over all three-survey periods. The models
were ranked using second-order Akaike’s information
criterion (AICc; Akaike, 1998). We considered models
competitive for inference if model DAICc 2. Model
averaging was employed to obtain averaged estimates
(Burnham & Anderson, 2003). We performed the analysis using R version 3.4.0 (R Development Core Team,
2008) using N-mixture models with the “unmarked”
package (Fiske & Chandler, 2011) and model averaging
with the “MuMIn” package (Barto
n, 2013).
Population Estimates
Based on our surveys, the lowest elevation at which the
nuthatch was detected was 1,192 m above sea level and
the highest 1,738 m (see later): However, the highest
elevation of any historical record in Thailand was
1,951 m (Deignan, 1946). Thus, we constructed two estimates based on the observed and historical data to estimate the upper limit of the population size.
No nuthatches were detected closer than 4 km to any
village, nor closer than 300 m to any agricultural area.
Thus, areas within a 4-km buffer of villages and 300 m
buffer of agriculture areas were removed from the analysis. Forest patches smaller than 19.7 ha were also not
considered as suitable habitat because they were smaller
than the estimated breeding home range of a male Giant
Nuthatch (Techachoochert, 2018).
A final minimum convex polygon (MCP) covering all
historical sites, recently discovered sites and areas considered to comprise suitable habitat was generated, with
the addition of a 300 m buffer around its margin. The
areas of hill evergreen forest and pine forest within our
accepted elevational limits within the buffered MCP
were extracted from the RFD map using ArcGIS. The
estimated population of Giant Nuthatches in Thailand
was then calculated by multiplying the estimated total
suitable habitat area by the average density derived from
the point surveys described previously.
Results
Abundance and Habitat Associations
We detected Giant Nuthatches at 12 of the 42 sample
points (28.6%) during a total of 126-point survey sessions that involved a total of 19 detections, across an
elevation range of 1,192 to 1,738 m above sea level.
The detections at each of the 12 locations were taken
to constitute a presumed territory or pair. These were
clustered within four major localities (Figure 1), namely,
Doi Ang Khang Royal Project Center (two territories),
Doi Chiang Dao Wildlife Sanctuary (three territories),
Doi Lang (an outlier of the present-day Doi Pha Hom
Pok National Park; five territories), and Mae Ngai
6
Tropical Conservation Science
Watershed Station (two territories). All but four sightings were from within protected areas (national parks or
wildlife sanctuaries). In contrast, the nuthatch was not
detected during our survey from four historical localities
where previously detected during 1930 to 1997 (Doi
Inthanon National Park, Doi Langka (on the common
border of Khun Chae National Park and Jae Sorn
National Park), Doi Pha Hom Pok (the core area of
Doi Pha Hom Pok National Park), and Khun Mae Ya
Watershed Management Unit (part of Huai Nam Dang
National Park; Table 1).
We generated a set of 24 regression models to explain
the abundance of Giant Nuthatch (Table 3). Five of the
24 models were competitive for inference (AICc 2).
The most supported five models were averaged to
estimate the coefficients of those variables (Table 4).
The model-averaged coefficients indicated that the abundance of the nuthatch increased with increasing
Table 3. Rankings of N-Mixture Models Using Site and Landscape
Variables to Explain the Abundance of Giant Nuthatch (k) and
Their Probability of Detection (p) at 42 Sample Sites in Northern
Thailand, Surveyed October to November 2015.
Model
K
AICc
DAICc
xi
k (Elev) p (.)
k (Elev þ Evg) p (.)
k (Evg) p (.)
k (Elev þ Evg þ Village) p (.)
Null
k (Village) p (.)
k (Elev þ Evg þ BA) p (.)
k (BA) p (.)
k (Elev þ Evg þ Village þ BA) p (.)
k (Tree) p (.)
k (Pine) p (.)
k (Oak) p (.)
k (Height) p (.)
k (Aspect) p (.)
4
5
4
6
3
4
6
4
7
4
4
4
4
6
110.83
110.86
110.88
110.98
112.74
113.14
113.47
113.51
113.74
113.81
114.28
114.76
115.12
116.64
0
0.03
0.05
0.15
1.91
2.31
2.64
2.69
2.91
2.98
3.45
3.93
4.30
5.81
0.16
0.16
0.16
0.15
0.06
0.05
0.04
0.04
0.04
0.04
0.03
0.02
0.02
0.01
Note. Columns indicate AIC adjusted for small sample size (AICc), delta
AICc (DAICc), AICc weight (xi), and number of parameters (K). Variables
are defined in Table 2. AIC ¼ Akaike’s information criterion.
Table 4 . Model-Averaged Parameter Estimates, SEs, and 95% CIs
for Abundance (k) of Giant Nuthatch in 42 Sample Sites in
Northern Thailand, October to November 2015.
k
k
k
k
(Intercept)
(Elev)
(Evg)
(Village)
Estimate
SE
95% CI
0.864
0.535
0.517
0.453
0.507
0.315
0.291
0.285
[ 1.371, 0.357]
[0.220, 0.850]
[0.226, 0.808]
[0.168, 0.738]
Note. Variables are defined in Table 2. CI ¼ confidence interval;
SE ¼ standard error.
elevation, increasing proportion of hill evergreen
forest, and greater distance from villages.
Population Estimates
We obtained a mean abundance per site of 0.55 Giant
Nuthatches with a detection probability of .287 .145.
Assuming a territory size of 19.7 ha and a detection area
of 0.28 km2 based on a 300-m detection radius (see
“Methods” section), the density of Giant Nuthatch in
suitable habitat was estimated at 1.96 birds/km2.
Within the MCP of the likely historical or present
range (Figure 2), the total forest cover of hill evergreen
and pine forest within the elevational range in which we
detected Giant Nuthatch, 1,192 to 1,738 m, was estimated
at 448.2 km2. Thus, the estimated Giant Nuthatch population in Thailand was 878 individuals. However, if an
upper elevational limit of 1,951 m is assumed, taking
into account three specimens collected at that elevation
from Doi Pha Hom Pok (Deignan, 1946), this would yield
an estimated potential habitat area of 491.8 km2 and a
slightly larger population, 964 individuals.
Discussion
Distribution and Population Estimates
In our study, Giant Nuthatch was found at 12 of the 42
sample points at four different major localities. Our findings indicate that the nuthatch occurred in a relatively
restricted, patchy habitat, and at low density. Due to its
low calling rate and limited response to playback, detection during field surveys was problematic. The estimated
probability of detection was low, .287, even with tape
playback in habitat thought to be favored by
Giant Nuthatch.
Giant Nuthatch was not detected at four known historical locations which are present-day protected areas
(Table 1). We think it likely that the bird was extirpated
from one of these, Doi Inthanon National Park, where
the latest specimen record was in 1931, by habitat loss
and human settlement before the national park was
established in 1972 (Dearden, Chettamart, Emphandu,
& Tanakanjana, 1996). Although there has been some
regeneration of pine and hill evergreen in recent decades,
Giant Nuthatch has not recolonized the site.
The Giant Nuthatch was likely already extirpated
from a fifth site, Doi Suthep-Pui National Park several
decades ago. No fewer than 10 specimens were collected
from Doi Suthep-Pui during 1928 to 1933 (Table 1) and
an 11th specimen, collected in 1967 (THNHM-B-07457,
original number TISTR 53–793) was the last recorded.
We did not resurvey Doi Suthep-Pui as multiple surveys
over the past 50 years, most particularly during 1978 to
Techachoochert et al.
7
Figure 2. Map of northern Thailand showing suitable habitat of Giant Nuthatch (black) within a minimum convex polygon of historical
limits of its range (gray).
1983 (Round, 1984) and subsequently, failed to reveal
any Giant Nuthatches.
The population estimate of Giant Nuthatch in
Thailand was a maximum of 964 individuals based on
an average density of 1.96 individuals/km2 in approximately 491.8 km2 of hill evergreen forest and pine forest
at elevational range between 1,192 m and 1,951 m.
However, even this may overestimate the size of the population in Thailand for reasons that we outline later.
Habitat Associations
The habitat-use model suggested that Giant Nuthatch
abundance increased with increasing proportion of hill
evergreen forest, increasing elevation, and greater distance from villages. The avoidance of villages is no surprise, as areas closer to villages are subject to higher
incidence of fire damage and habitat fragmentation
(Bezuijen et al., 2010; Pattanavibool & Dearden, 2002).
Remaining forest patches in the vicinity of villages may
be too small or too degraded to hold any nuthatches.
Our results only suggest broadscale habitat associations because neither forest cover maps nor available
satellite images were sufficiently accurate to take account
of the microscale variation in the habitat important to
the nuthatch. In Thailand, Giant Nuthatch appears to
be restricted to a drier subtype of more open hill evergreen forest, dominated by oak and chestnuts, in which
P. kesiya is frequent (Matthysen, 1998; Round, 1983)
and is usually absent from denser, closed canopy moist
evergreen forest lacking pines, which constitutes a significant proportion of the total estimated area of hill evergreen forest. The lack of accurate habitat cover maps
that reliably distinguish between drier, more open hill
evergreen forest that contain pines, and moister, more
closed forest, still classified as hill evergreen was a limitation of our study. Without habitat maps of much finer
resolution, we cannot safely say by how much we may
have overestimated the area of potentially suitable habitat and therefore the size of the Giant
Nuthatch population.
The distribution of P. kesiya is clearly associated with
dry ridges and nutrient-poor soils (Kiianmaa, 2005;
Pousujja, Granhof, Willan, & Graudal, 1986; Santisuk,
1997). Such areas are fire prone although under natural
conditions, dry-season fires are of low-to-moderate
8
frequency. Areas closer to villages may burn annually, as
local residents use fires to aid nontimber forest product
collection, and in clearance for agriculture, and hunting
(Phairuang, Hata, & Furuuchi, 2017). Too frequent fires
kill P. kesiya seedlings which do not develop fire resistance until about 5 years of age (Pousujja et al., 1986;
Turakka, Luukkanen, & Bhumibhamon, 1982). In addition, resinous wood is repeatedly hacked from the trunks
of mature pines for kindling either for home use or for
sale. This makes mature pines more vulnerable to fire
and to wind damage: such trees eventually fall (Savage,
1994). Therefore, forest structure in human-used areas is
adversely affected by both low recruitment of young
pines and the destruction of mature pines which leads
to a relatively uniform age structure among remaining
pine stands (Savage, 1994; Turakka et al., 1982).
Although quantitative data are lacking, the possible disappearance of the Giant Nuthatch population at Kalaw,
Shan State, Myanmar, where the pine forests have been
subjected to extensive clearance and burning for many
decades, has been attributed to habitat degradation and,
in particular, the loss of mature pines (Bezuijen et al.,
2010). Thus, the effects of frequent fires on the Giant
Nuthatch and other threatened species that share the
same habitat require urgent further study.
Implications for Conservation
A relatively high proportion (55%) of the montane habitat of Giant Nuthatch in Thailand is already protected
(as national park or wildlife sanctuary) in comparison
with other Giant Nuthatch range countries. This might
suggest that its population in Thailand, though small, is
relatively secure. However, as we have shown Giant
Nuthatch has probably been lost from as many as five
historical sites inside protected areas, almost certainly due
to degradation and fragmentation of its preferred habitat.
Although montane habitats are naturally fragmented
on ridges and mountaintops, expanding cultivation and
upland development increases the level of habitat isolation and reduces patch size (Burgess, Sharpe, & Bruner,
1981). Zeng, Estes, et al. (2018) and Zeng, Gower, et al.,
(2018) have shown that the rate of annual upland forest
loss in northern Thailand has accelerated since year 2000,
notwithstanding the establishment of protected areas, due
mainly to increased market-oriented growing of corn,
especially as animal feed. Clearance took place both
inside and outside national parks and other protected
areas. Zeng, Estes, et al. (2018) rigorous assessment of
forest loss across South East Asian uplands during 2000
to 2014 showed that simulations of forest loss based on
United Nations Food and Agriculture Organization statistics underestimated actual forest loss by 36%.
The relative magnitude of the decline in population
size of birds and mammals due to habitat fragmentation
Tropical Conservation Science
is often greater than expected from habitat loss alone,
with those that are habitat specialists suffering more
than habitat generalists (Andrén, 1994). Menon,
Soberon, and Peterson (2008) suggested that Asian
nuthatches in general showed low proportionate range
filling which they attributed to fragmented montane habitats limiting their ability to disperse. The continued degradation of native forest containing stands of mature
pines both inside and outside protected areas presents
a major threat to the survival of the Giant Nuthatch.
Conservation of the Giant Nuthatch in Thailand will
depend on rigorous protection of native hill evergreen
forest in its favored zone (1,100 to 1,900 m) so as to
restrict upland development and agricultural expansion
and enable presently fragmented habitat patches to
gradually coalesce into larger units. A more rigorous
system of fire suppression that seeks to limit the extent
of burning of both broad-leaved and pine forests, combined with a system of tracking the frequency and intensity of fires, implemented by forest management
authorities, will likewise be essential for the long-term
management of Giant Nuthatch habitat in Thailand.
The existing prohibition on firewood collection in protected areas should be more strictly enforced and extended to a ban on the collection of firewood or kindling
from all native forest patches.
While our upper estimate of 964 Giant Nuthatch individuals in northern Thailand might accord tolerably
with BirdLife International’s (2016) global population
estimate of 1,000 to 2,499 individuals, shared among
three countries, we remain cautious about our baseline
estimate, which may be overly optimistic due to our
inability to distinguish the patchy microhabitat of the
species within areas of hill evergreen forest. More intensive study with higher resolution multispectral imagery
to precisely delineate areas of suitable nuthatch habitat
is also needed.
An occupancy survey of the forest patches that we
identified would be labor-intensive but would further
refine our population estimate. Furthermore, we also
urgently recommend further surveys of potential Giant
Nuthatch sites in China and, especially, Myanmar,
where the areas of suitable montane uplands in the
Shan States are potentially quite large (1,600 km2).
This would enable better assessment of habitat conditions and update knowledge of its distribution and
global population. An assessment of long-term threats
and the likely impact of climate change on montane
biota should be considered for further study.
Acknowledgments
The authors are grateful to Mr. Mongkol Safoowong
Superintendent of Chiang Dao Wildlife Research Station for
accommodation and for assisting our research in Chiang Dao
Wildlife Sanctuary. The authors would like to thank the
Techachoochert et al.
Chiang Dao Research Station team, all rangers, and all others
who helped in fieldwork, especially, Andrew Pierce, Sontaya
Manawatthana, Amphapat Toonin, Perawit Insuan, and
Atiwich Kaewchum. The authors would like to thank Dusit
Ngoprasert,
Wanlop
Chutipong,
and
Naruemon
Tantipisanuh who helped in data analysis. The authors thank
Narong Mahannop, the Director of Forest and Plant
Conservation Research Office, Department of National
Parks, Wildlife, and Plant Conservation for his kind advice
and assistance. The authors also would like to acknowledge
Dr. Stephen Elliott who shared useful information on the ecology of pine. The authors would like to thank two anonymous
reviewers who provided constructive comments on an earlier
version of this manuscript.
Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest with
respect to the research, authorship, and/or publication of
this article.
Funding
The author(s) declared no potential conflicts of interest with
respect to the research, authorship, and/or publication of this
article: This research was funded by The Rufford Small Grants
for Nature Conservation (16834–1) and Development and
Promotion of Science and Technology Talents Project.
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