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Bird Conservation International, page 1 of 19. © BirdLife International, 2011
doi:10.1017/S0959270911000360
Biology, taxonomy and conservation
status of the Short-tailed Green Magpie
Cissa [t.] thalassina from Java
S. (BAS) VAN BALEN, JAMES A. EATON and FRANK E. RHEINDT
Summary
The Short-tailed Green Magpie Cissa thalassina, a member of an Asian lineage of uniquely
coloured corvids, is represented by two subspecies, thalassina and jefferyi, that occur on the
islands of Java and Borneo, respectively. The distinct Javan nominate form is poorly described in
the literature and next to nothing is published on its biology and occurrence in the wild. We here
document the biology and distribution of this taxon based on hitherto unpublished historical data
and on our own fieldwork. We also analyse vocal data of jefferyi, thalassina and two other Cissa
species and show that jefferyi and thalassina are well-differentiated, and that thalassina
is bioacoustically more similar to another Cissa species from the Asian mainland. We also
demonstrate important and significant biometric differences between jefferyi and thalassina that
may reflect divergent adaptations to the environment, as well as plumage differences that may
serve signalling functions. Finally, the application of a novel species delimitation test to our data
suggests that jefferyi and thalassina deserve to be classified as biological species because their
phenotypic divergence exceeds that found in many sympatric species. The revised taxonomic
status of Javan thalassina invites a reconsideration of its threat status. Based on its restricted
range, extreme rarity and threats by bird trapping and habitat destruction, we consider the Javan
Green Magpie as globally Critically Endangered.
Introduction
The Asian genus Cissa Boie, 1826 is a complex of twelve taxa of green magpies. Although
sometimes lumped with the five predominantly blue species of Urocissa into one genus
(dos Anjos 2009), they form a discrete lineage, members of which look uniform with a green
plumage, unique amongst corvids. Their present taxonomic relationships are still insufficiently
studied, and in particular the taxonomic status of both races of Short-tailed Green Magpie Cissa
thalassina needs to be elucidated (Wolters 1977, Dickinson et al. 2004).
To date the following taxa have been described: (1) chinensis – Himalayas and northern
Indochina, (2) minor – Sumatra and Borneo, (3) robinsoni – extreme south-west Thailand and
peninsular Malaysia, (4) klossi – central Annam (Vietnam) and central Laos, (5) margaritae – Mt
Lang Bian (central-southern Vietnam), (6) hypoleuca – south-east Thailand, central and southern
Laos, southern Vietnam (southern Annam and Cochinchina), (7) chauleti – central Annam
(Vietnam), (8) concolor – eastern Tonkin and northern Annam (north Vietnam), (9) jini – south-
central China, (10) katsumatae – Hainan Island, (11) thalassina – west and central Java,
(12) jefferyi – northern Borneo.
Various arrangements have been described on geographical and morphological grounds. The
most speciose was by Delacour (1929) who recognised six species: C. chinensis (taxa 1–
5),
C. hypoleuca (taxa 6–7), C. jefferyi, C. katsumatae, C. concolor (taxa 8–9) and C. thalassina.
Kuroda (1933) and Chasen (1935) lumped all forms into one species. Vaurie (in Peters 1962)
recognised two species: Green C. chinensis (taxa 1–5) and Short-tailed Magpie C. thalassina (taxa
6–12). This system was followed by Sibley and Monroe (1990), who, however, considered the
latter as having three distinct subspecies: Yellow-breasted, Bornean and Short-tailed Magpie.
Goodwin (1976, 1986) grouped the forms into three species: Common C. chinensis (taxa 1–5),
Indochinese C. hypoleuca (taxa 6–10) and Short-tailed C. thalassina (taxa 11–12), and this is
followed by many subsequent standard works, such as Walters (1980) and Howard and Moore
(1980). These three species are considered a superspecies by dos Anjos (2009), an arrangement
that is obviously mistaken in view of the sympatry between Common Green Magpie and both
other species.
The (sub)specific distinctions are based on body size, tail length and shape, colour pattern of
tertials and tail, and yellow wash on body and crown (see Table 1). Both Short-tailed Magpie taxa
(thalassina and jefferyi) are mainly distinguished by their short tails. Not surprisingly,
vocalisation has never been used as a taxonomic character as this aspect of the genus is complex,
and rather intangible as in most corvids, due to intergradation, individual variation, frequent
vocal mimicry, etc. (dos Anjos 2009). Cissa thalassina was first described by Temminck in 1826.
Although being lumped with the other green magpies, the race thalassina is described as a very
distinct form by Kuroda (1933). In this paper we use morphological characters as well as vocal
characters to examine the level of differentiation between jefferyi and thalassina. We also use
a novel phenotypic species delimitation test (Tobias et al. 2010) to evaluate if phenotypic
differences between jefferyi and thalassina are comparable to other pairs of sister taxa that are
ranked at the biological species level.
Very little is published on the natural history of the distinct Javan race of Short-tailed
Green Magpie (Madge and Burn 1994
, dos Anjos 2009), and its specific name thalassina (meaning
sea-green or bluish-green, the general colour of preserved skins or of birds kept in captivity)
given by its describer, C. J. Temminck in 1826, is symptomatic of the status of knowledge of
these birds in their natural environment, described as rugged and inaccessible (de Visard de
Bocarmé 1829).
This paper summarises all that is presently known about the biology and status of the Javan
Short-tailed Green Magpie. Once listed as near-threatened in Collar et al. (1994), Short-tailed
Green Magpie was not considered in BirdLife International (2001). New insight into its taxonomy
necessitates a reassessment of its global status.
Table 1. Measurements and plumage characteristics for three Cissa taxa (from Madge and Burn 1994).
thalassina/jefferyi hypoleuca chinensis
Tail length (mm) 97–110 [114–]157 171–210
Body length (cm) 31–33 34–35 37–39
Tail shape short, bluntly
graduated
intermediate,
central feathers hardly
project beyond next pair
strongly graduated
Tertials no obvious
pattern
Plain, broadly tipped &
fringed green, no spotting
tipped with black-
and-white spots
Underparts green strongly washed lemon-
yellow
pea or leaf green
Crown colour green green yellowish green (most races)
to bright golden yellow
Crown structure shorter feathers intermediate? elongated rear crown &
nape feathers
S. van Balen et al. 2
Material and methods
Data acquisition
We gathered sound recordings for both currently recognised subspecies of C. thalassina as well as
for a number of individuals each of C. chinensis and C. hypoleuca. Recordings of different
subspecies of C. hypoleuca and C. chinensis were each pooled for vocal analysis. We recorded
vocalisations in the field in Indonesia, Cambodia and Vietnam and supplemented our own
recordings with those made by colleagues and deposited in the xeno-canto ornithological sound
collection (www.xeno-canto.org). Details of all 18 recordings, including localities, dates and
names of the sound recordists, can be found in Table S1 in the online Supplementary Materials.
Two major collections, National Museum of Natural History (Nederlands Centrum voor
Biodiversiteit (NCB) Naturalis, Leiden, Netherlands) and the Natural History Museum (Tring,
UK) provided the skins that were examined for a mensural analysis. In the analyses, 21 skins of
Cissa t. thalassina and 10 Cissa t. jefferyi were measured, with near-equal numbers (1:1) for
males and females for each taxon (Table S2).
Field observations were made during general and more specialised forest bird surveys on Java
between 1980 and 1997 (S. v. B), and excursions in 2002–2010 (J. A. E). Data on museum
specimens, publications in often obscure journals, and birding reports provided historical data on
distribution and biological information. Requests for field data yielded a small additional number
of field observations.
Bioacoustic analysis
Both analogue and digital recordings were converted into WAV format if they had not been initially
created in that format. Recordists used different equipment for sound recordings. However, we
consider any bias caused by equipment differences on parameter measurements to be negligible. For
instance, the level of variability in background noise and slight differences in note shape among
recordings from the same recordist are equivalent to the variability among recordings from different
recordists, indicating that differences in recording quality are much more important than equipment
differences. Furthermore, in many cases we analysed multiple recordings from several different
recordists for each taxon, which should remove any such bias. In each case, we made an attempt to
account for levels of sound pollution in our measurements by setting the background level equal.
We prepared and analysed sonograms of vocalisations using the program Syrinx version 2.6hby
John Burt (available at www.syrinxpc.com). Levels of background noise were set to an equal level,
otherwise default settings were employed. Cissa vocalisations are characterised by great variability and
a large individual repertoire of notes and song motifs. In order to carry out meaningful comparisons
among taxa, we classified sounds in each recording into one of twelve different motif types, each
designated by a unique letter ranging from A to L. Each motif type consists of one to several notes.
For each motif type in each recording, we then counted the number of times the motif was uttered, as
well as the number of notes the motif contained. We compared overlap in the presence of motif types
among taxa as well as overlap in the number of notes per motif type in each taxon.
Since many motif types in Cissa, especially the non-melodious ones, are characterised by
harmonics (component frequencies of waves that are an integer multiple of the fundamental
frequency), we also noted their presence or absence in the motifs of each recording and used
a binomial test to compare taxon-specific incidence of harmonics. In poor recordings, harmonics
can be difficult to detect even when present. However, virtually all our recordings were loud
enough for harmonics to show up on the sonogram in the presence of several multiples, and
multiple recordings were sampled for each taxon so we rule out recording quality as
a confounding factor in comparisons of harmonics. We measured three different frequency
parameters (highest frequency, lowest frequency and frequency range) as well as the duration for
each motif and compared them among all taxa.
Biology and conservation of Short-tailed Green Magpie in Java 3
One set of comparisons involved an across-taxon Kruskal-Wallis test and pairwise two-tailed
Mann-Whitney U-tests of the frequency parameters (not the duration) of all motifs measured for
each taxon, regardless of motif type, to test for taxon differences in general vocal pitch. In another
set of inter-taxon comparisons, we contrasted frequency parameters and duration of shared motifs
among taxa to check for overlap in measurements. Since only six motifs were shared amongst 2–3
taxa, and there were only 1–6 sample recordings per taxon per shared motif, sample size for this
second set of comparisons was too low for statistical analysis and overlap was only evaluated in
comparisons involving more than one sample recording in at least one taxon. All statistical
analysis was carried out using the program SPSS (SPSS Institute Inc., Chicago).
Biometric analysis
We measured eight biometric traits for 21 individuals of thalassina and 10 individuals of jefferyi
(each 50%maleand50% female): tail length, wing length, bill height, bill length, total length,
tarsus, tail/wing ratio and tarsus/wing ratio. Table 4 lists all measurements and specimen details
including museum voucher numbers. Female and male specimens were pooled for each species,
because sample sizes for significance testing of sex-specific groups were too low, and because we did
not detect any sexual dimorphism. For each trait, we performed a two-tailed Mann-Whitney U-test
to examine differences between the two taxa. To increase the stringency of this test, we considered
a difference significant at P # 0.01.Oncesignificant differences were detected between the two taxa,
we additionally examined if the measurements for a particular trait passed a second – more stringent –
significance hurdle by assessing if the ranges of measurements for either taxon overlapped.
Phenotypic species delimitation test
We used the species delimitation criteria recently proposed by Tobias et al. ( 2010) to assess the
biological species status of thalassina and jefferyi based on the biometric, ecological, behavioural,
and plumage characters presented in this paper. This species delimitation test assesses phenotypic
differences between two taxa by assigning each character difference a score of 1–4, based on
whether the difference can be considered ‘minor’, ‘medium’, ‘major’ or ‘exceptional’. The final
score of a comparison is then applied against a threshold generated from a large global sample of
sympatric bird species; if it exceeds the threshold, phenotypic evidence can be seen to support
species status. For exact definitions of categories and assignment rules, see Tobias et al. (2010).
Results
Bioacoustics
For the Bornean jefferyi the call is described as “not nearly so clear as that of C. minor, but is still
a feeble attempt at ‘Ton-ka-kis’” (Whitehead 1893: 206). Interestingly, the main calls of the Javan
taxon thalassina appear to show a greater resemblance to the hypoleuca and chinensis complexes,
than to its present congener jefferyi. On Java, the Sundanese names èkèk gêling, kèkèt gêlèng,
dèrètdèt kêlèng , kèrèkèk kêlèng, cucak keling (WJ), and Javanese names dingdingbak (CJ), and
kekek kelang (Yogya) and variations (Bartels 1897-1931, Koningsberger 1907, van Oort 1910,
S. v. B. unpubl. data) closely describe the most stereotypic call of its large repertoire, which also
includes mimicking, and is accurately described as “a nasal chiuu – chiuu – kèkèng ê ngliéng”,
also “uttered in flight” (Bartels 1897-1931, J. H. Becking unpubl. data).
Vocal parameters for each taxon are specified in Table S1 in the online Supplementary
Materials. In our 18 recordings of four taxa, we found 12 different motif types (A-L), six of which
(A-F) were shared amongst more than one taxon. Fig. 1 depicts a typical example of each motif
type, and Fig. 2 shows the overlap in motif types among taxa, indicating that C. t. thalassina and
S. van Balen et al. 4
Figure 1. Twelve motifs found in Cissa vocalisations.
Biology and conservation of Short-tailed Green Magpie in Java 5
C. t. jefferyi only share a single motif type (D) that is also present in C. hypoleuca. On the other
hand, overlap between C. t. thalassina and C. hypoleuca is particularly pronounced, with four
shared motif types, three of which are exclusive to these two taxa.
In our assessment of whether the number of notes given by each taxon for each shared motif type
(i.e. motifs A-F) is approximately equal, we found that there is complete overlap in the number of
notes given by each taxon for motifs A, B, D, E and F. The only shared motif that showed no overlap
is C, which is characterised by 3–4 notes in C. t. thalassina and two notes in C. hypoleuca. However,
an increased sample size could easily establish overlap for the number of notes given for motif C by
these two species. All in all, we interpret the lack of inter-taxon differences in the number of notes
given for each motif type to corroborate that our definition of shared motif types is robust and that
only homologous vocalisations were grouped into common motif types.
Each vocalisation was scored for the presence or absence of harmonics, and a binomial test
showed that there is a significant propensity for C. t. jefferyi to lack harmonics in its vocalisations
(two-tailed P-value , 0.001). No such propensity was found in the other taxa, although
C. hypoleuca exhibited a near-significant propensity for uttering vocalisations containing
harmonics (two-tailed P-value 5 0.09), which – with increased sampling – may well turn out
to be a real vocal characteristic that sets this taxon apart.
We compared three frequency parameters in the overall vocal repertoire amongst each taxon,
regardless of motif type. A Kruskall-Wallis test (P 5 0.418) and pairwise Mann-Whitney U-tests
(results not shown) yielded no significant differences among taxa in the highest vocal frequencies
of motif delivery. Equally, taxa did not differ significantly in terms of the frequency range of
overall motifs uttered (Kruskal- Wallis: P 5 0.314; pairwise Mann-Whitney U-test: not shown).
The only frequency differences detected refer to the lowest frequencies (Kruskal-Wallis:
P 5 0.075) of overall motif delivery in C. t. thalassina, which were significantly lower than in
C. t. jefferyi (two-tailed Mann-Whitney U-test: P 5 0.016), and almost significantly lower than
in C. hypoleuca
(P 5 0.079) and C. chinensis (P 5 0.12). In contrast, no differences in lowest
Figure 2. Motif types unique to each taxon or shared among taxa; letters refer to motif types as
shown in Fig. 1.
S. van Balen et al. 6
frequencies were found in comparisons involving C. t. jefferyi, C. hypoleuca and C. chinensis, but
to the exclusion of C. t. thalassina.
As only six (A–F) out of twelve motif types were shared among a range of 2–3 taxa, and since
motifs were represented only 1–6 times in each taxon (Table 2), sample size for motif-specific vocal
comparisons was too low for statistical analysis. Nonetheless, we performed a crude comparison
among taxa using all three frequency parameters and motif duration to check for general overlap in
these measurements. Wherever a shared motif was represented by more than one measurement in at
least one taxon in our sampling regime (i.e. in motifs A, B, D, E and F; Table 2), we ascertained
whether the value(s) for the other 1–2 taxa overlapped with this range. We found a complete overlap
of measurements for motifs D and E in all three frequency parameters and in motif duration
(Table 2). For motifs A and B, there was measurement overlap between the two taxa involved
(C. t. thalassina and C. hypoleuca) only at the highest frequency, but not in the other three vocal
parameters (Table 2). Similarly, in motif F, there was overlap among C. t. jefferyi, C. hypoleuca and
C. chinensis only at the lowest frequency, but not in the three remaining parameters. It is important
to note that a higher sample size may lead to the detection of fine-scale vocal differences between taxa
in overlapping parameters or – conversely – may show vocal overlap in parameters that seem to differ
among taxa using the current dataset. Overall, we expect many motifs to share the same vocal
properties among taxa, and we interpret this result as confirmation that we have generally classified
homologous vocalisations into equal motif categories. Even in homologous vocalisations that are
appropriate for comparative analysis, taxon-specific differences in some vocal parameters are expected
to involve at least a number of motif types, so differences in motifs A, B and F may well be real
indicators of vocal differentiation between Cissa taxa.
Morphology
Biometrics
Table 3 shows the measurements of eight biometric parameters of 21 specimens of thalassina and
10 jefferyi. Table 4 gives the mean values and P-values using a two-tailed Mann-Whitney U-test.
Bornean jefferyi has a significantly shorter wing length than thalassina (although their
measurements display some overlap), and a comparatively even shorter tarsus length with no
overlap in measurements. Accordingly, the tarsus-wing ratio showed significant differences
although measurements overlapped. In terms of tail length, size dimensions are reversed, as
jefferyi displays significantly longer measurements than thalassina, with no apparent overlap,
and intermediate between thalassina and the other species of green magpie (Tables 1 and 3).
Consequently, tail-wing ratios also differ significantly between both taxa, with no overlap in
measurements. Whilst bill length does not differ significantly between the two taxa, bill heights
are significantly different between the two species with no overlap in measurements, resulting in
Table 2. Biometrics of two taxa of Short-tailed Green Magpie (all measurements in mm, unless indicated
otherwise; from skins stored in the Leiden Museum, mostly thalassina, and Tring, mostly jefferyi).
Mann-Whitney U-test P-values are given.
Wing L Tail L Bill L Bill H Tarsus Total L
(cm)
Tarsus/
wing
Tail/
wing
thalassina
(n 5 21)
mean 137.2 107.235.915.442.326.30.31 0.78
SD 3.04.82.10.81.41.50.01 0.04
range 133-142 101-118 32.5-41.013.9-17.040.1-45.024.5-30 0.29-0.33 0.75-0.87
jefferyi
(
n 5 10)
mean 132.8 124.934.312.739.427.40.30 0.94
SD 2.14.11.60.81.30.50.02 0.02
range 130-136 118-129 32.2-36.711.0-13.637.7-42.327-28 0.29-0.32 0.90-0.97
P 0.0006 ,0.0001 0.0404 ,0.0001 0.0001 0.0193 0.0099 ,0.0001
Biology and conservation of Short-tailed Green Magpie in Java 7
an obviously finer bill in jefferyi (Fig. 3b). This divergence in tail length and bill shape may
indicate slight differences in ecological adaptations. Finally, there is no significant difference in
total length between jefferyi and thalassina. Male and female measurements were always pooled
in each taxon, since limited sexual differences were detected (data not shown).
Table 3. Descriptive notes of the plumage and soft parts of C. t. thalassina and C. t. jefferyi.
Trait thalassina jefferyi Interpretation of
difference (as per
Tobias et al. 2010)
Score
Tertials more extensively
light green (white
in museum specimens);
base of outer webs
reddish brown, outermost
tertiary with the outer web
near tip also reddish brown,
in some cases with only two
pale spots at the tip (Kuroda
1933; pers. obs.)
Inner secondaries
greenish white,
except on outer web,
which is for the most
part claret-red, the
outermost one with a
oblique pale tip (Whitehead
1893; pers. obs.)
Considerable variation
in pattern in both
taxa is not gender-
specific but individual
or age-related. This
difference is ‘medium’,
as it involves a different
tone of a distinctly-
demarcated body part
2
Rectrices uniform bluish green, with
diffusely pale tips only to
the outermost rectrices
rectrices have white tips
and dark subterminal bars.
‘major’, as it involves a
different pattern
(barring versus no
barring) in a tract
of feathering
3
Eyes red (Vorderman 1886a) to
bright coral red
(Kuroda 1933)
white with a faint pink
tinge round the pupil
(Whitehead 1893)
Note that – contra dos
Anjos (2009) – orbital
ring in jefferyi is not
light blue but crimson
red as in thalassina
(see photos www.oriental
birdimages.org. Iris colour
difference is ‘major’ as it
involves a different
bare-parts coloration
3
Table 4. Interpretation of biometric differences according to criteria in Tobias et al. (2010); note that body
ratios are not listed since they co-vary with their constituent parameters.
Biometric difference
between jefferyi and thalassina
Effect size (Cohen’sd)
and interpretation (as per
Tobias et al. 2010)
Score
Tail longer in jefferyi d 5 3.99, i.e. ‘medium’ 2
Tarsus longer in thalassina d 5 2.14, i.e. ‘medium’ 0
Wing longer in thalassina d 5 1.64, i.e. ‘minor’ (score 1),
but cap on # 2 biometric traits
0
Bill higher in thalassina d 5 3.47, i.e. ‘medium’ (score 2),
but cap on # 2 biometric traits
2
Bill longer in thalassina d 5 0.89, i.e. ‘minor’ (score 1),
but co-varies with bill height
0
Body longer in
jefferyi d 5 1.38, i.e. ‘minor’, but co-varies
with tail length
0
S. van Balen et al. 8
Weight of all taxa is about the same, 120–133 g(chinensis), 125 g(hypoleuca), 125 g
(thalassina / jefferyi), although this dataset is far too small for statistical analysis.
Plumage and soft parts
Fig. 3 shows representative adult specimens of both Javan and Bornean Short-tailed Green
Magpie. Table 3 provides descriptions of the body parts that are most strikingly different between
these two taxa.
Figure 3. a-c. Specimens (in NCB Naturalis, Leiden) of Cissa t. thalassina (above) and
C. t. jefferyi (below) showing the differences in tail length and tertial pattern (a, dorsal), bill
shape and size (b, lateral), and pattern of under tail (c, ventral.) (Photos: S. v. B).
Biology and conservation of Short-tailed Green Magpie in Java 9
Phenotypic species delimitation test
We carried out a novel species delimitation test introduced by Tobias et al. (2010) that interprets
phenotypic taxon differences related to biometrics, coloration, bioacoustics, ecology and
behaviour, and assigns scores from zero to four according to strict criteria on the level of
differentiation in those traits. Based on a comparison with a large pool of pairs of known sister
species, Tobias et al. (2010) consider the score of 7 a threshold for recognition as a biological
species. Table 3 lists the differences in coloration between thalassina and jefferyi and indicates
a total score of 8 for colour traits, which already surpasses Tobias et al.’s(2010) species threshold
and indicates that the two taxa merit recognition as species based on coloration alone.
A fourth trait has been given by dos Anjos (2009) as subspecifically diagnostic, i.e. a yellow
wash on crown and underparts of the Javan birds. As there is only a very slight difference in green
between the two taxa, mainly on the head (see Figure 3) we did not consider it in our analysis.
Moreover, Vorderman (1886) who described a freshly killed bird from Mt Salak, west Java, makes
no mention of a yellow wash: “...plumage bright pale blue-green, that has a pronounced green
wash on head, belly and flanks.”
Table 4 lists the interpretation of biometric differences according to the criteria set forth by
Tobias et al. (2010 ) and indicates an additional score of 4, which adds up to a score of 12, well
beyond the species threshold. Ecological or behavioural differences between the two taxa appear
to be insignificant, although there is a difference in altitudinal range (see below), and the Javan
birds seem to venture out of the forest (see below), resembling Cissa chinensis rather than the
Bornean Short-tailed, that never leaves true forest (Whitehead 1893).
As far as vocal differentiation between jefferyi and thalassina is concerned, the extensive
complexity of vocal characters and the abundance of motif types as well as the difficulty in
classifying motif types into ‘songs’ and ‘calls’ make the application of Tobias et al.’s(2010)
criteria to bioacoustic data in the genus Cissa challenging. In our vocal analysis of taxon
differences (see above), we have dealt with these difficulties by showing that thalassina
is vocally
closer to C. chinensis than to jefferyi, and by focusing on a comparison of motif types, but it is
not straightforward to adjust this type of analysis to the methodology put forth by Tobias et al.
(2010). Therefore, we here abstain from applying their phenotypic test to vocal characters in
jefferyi and thalassina, while noting that inclusion of the extensive vocal differences between
homologous vocalisations detected by us (see above) would certainly further increase the test
score. Since the test diagnostic is already at 12 – and well beyond the species threshold at 7 – after
only biometric and colour characters are included, we deem the incorporation of vocal characters
unnecessary for the purposes of this test.
Discussion
Vocal differences
Cissa magpies belong to the oscine songbirds, in which vocalisations are a learned rather than an
inherent trait. In addition, they are great vocal imitators and are characterised by an astounding
vocal repertoire. Consequently, they are a difficult subject for vocal analysis, since bioacoustic
parameters must be compared amongst homologous vocalisations only. With the wide range of
different motifs given by each Cissa taxon, the difficulty lies in the assignment of vocalisations to
correct homologous motif classes. Using a range of 18 recordings from four taxa, but with
a special emphasis on C. t. thalassina, C. t. jefferyi and C. hypoleuca, we have classified Cissa
sounds into 12 motif types (A–L) – depicted in Fig. 1 – six of which (A–F) we believe to be shared
amongst 2–3 Cissa taxa. We believe that our assignment of vocalisations into homologous motif
types has been successful, because we have detected almost no discrepancies in the number of
notes given per motif type amongst different taxa. Equally, when comparing each shared motif
type (A –F) among different taxa in terms of motif durations and three different frequency
parameters, we found substantial overlap in measurements between taxa (Table 1). No such
S. van Balen et al. 10
overlap would be expected in categories that consist of non-homologous vocalisations
inaccurately classified into the same motif types. Even so, vocal differentiation amongst taxa is
expected to produce measurement differences in at least a number of parameters and motif
classes, which conforms to our observation of limited overlap between taxa in some vocal
parameters in motifs A, B and F.
C. t. jefferyi and C. t. thalassina were found to share only one motif type (D), which is
probably ancestral because it is not exclusive to them, having been found also in C. hypoleuca
(Fig. 2). In contrast, sharing of motif types was greatest between C. t. thalassina and C. hypoleuca
(Fig. 2). Further vocal evidence that C. t. jefferyi and C. t. thalassina exhibit substantial vocal
differences is the finding that C. t. jefferyi was the only one of all four taxa that is characterised
by a significant lack of harmonics in its vocal delivery. Harmonics create a particular vocal timbre
that often sounds scratchy or non-melodious to the human ear, and they are regularly employed
by C. t. thalassina as well as the two other Cissa species investigated. Therefore, C. t. jefferyi
sounds considerably more melodious than the other taxa in its overall motif delivery. Last but not
least, we found that the overall lowest frequency in motif delivery – regardless of motif type – is
considerably lower-pitched in C. t. thalassina than in the other species, especially (and
significantly so) in comparison to C. t. jefferyi.
Although the vocal complexity of Cissa vocalisations renders bioacoustic analysis challenging,
it is clear that the vocal repertoire and a number of general vocal qualities of C. t. thalassina differ
greatly from its supposed conspecific C. t. jefferyi, and that C. t. thalassina may in fact be vocally
more similar to C. hypoleuca. This similarity between the Javan and the Indochinese taxa
supports biogeographic findings in other bird species that Javan fauna may be more closely related
to species from the subtropical monsoon forests north of the Sundaic rainforest zone (Medway
and Wells 1976, Wells 1985, Holmes 1985). Whereas these are exclusively lowland species, there
are examples of montane bird species that have also been separated sufficiently long for speciation
and whose distributions show analogies with that of the magpie, i.e. Javan Tesia Tesia
superciliaris, and Spotted Crocias Crocias albonotatus, all restricted to the western half of Java
and with their closest relatives in mainland Asia, not on Sumatra or Borneo. Other west Javan
endemics have allospecies on Sumatra (e.g. Javan Trogon Apalharpactes reinwardti and Javan
Cochoa Cochoa azurea).
Morphological differences
Statistical analysis of biometric differences demonstrates that thalassina is a significantly shorter-
tailed bird than jefferyi, even though its tarsus and wings are significantly longer. In addition, the
two taxa exhibit an important divergence in bill morphology, with thalassina having a slightly
longer and distinctly more massive bill than jefferyi. These biometric differences may reflect
adaptations to slightly different life histories, but more research is needed to confirm this. We also
document important differences in coloration, especially in brightly-coloured parts of the body (iris,
wing panel, tail) that may serve a signalling function. In summary, our morphological data support
our bioacoustic analysis in that jefferyi and thalassina should be afforded biological species rank.
Phenotypic species delimitation test and taxonomic recommendation
Even though our application of Tobias et al.’s(2010) species delimitation test did not include our
bioacoustic dataset (see Results), and despite the fact that its inclusion would have further
increased the test diagnostic, we arrived at a score of 12, well beyond the species threshold of 7.
This high score confirms our conclusion that jefferyi and thalassina are well-differentiated taxa
that deserve to be recognised at the biological species level. Perhaps most importantly, this
conclusion is based on the independent documentation of profound differences in vocalisations,
visual cues as well as structural parameters that may reflect adaptations to the environment.
Biology and conservation of Short-tailed Green Magpie in Java 11
Ecology
Distribution and habitat
The elevational distribution of C. t. thalassina of 1,000 - 1,200 m as reported in the latest standard
works (dos Anjos 2009) does not fully match our findings. Although occasionally encountered in
lowland forest (Koningsberger 1915), the main distribution is in submontane and montane forests
at 500–2,000 m (Sody 1956). Appendix S1 in the online Supplementary Materials lists all records
of Cissa t. thalassina that we could find. Three specimens in RMNH and MZB without dates or
exact localities (Bogor, Sukabumi and Priangan) have been omitted.
Bornean and Javan Green Magpies occupy largely overlapping altitudinal ranges, respectively
305–2,735 and 500–2,000 m. The former seems to occur higher up in the hills, possibly because of
competitive exclusion with its congener C. chinensis in the lowlands, as nowhere do they seem to
co-occur (Whitehead 1893). There is no obvious reason why the apparently more stenotopic
Javan birds do not occur above 2,000 m, where no competitors occur, and theoretically its larger
size should actually be in its favour (James 1970). This anomaly may be partly explained by the
massenerhebung effect of the 4,101 m high Mt Kinabalu, as compared to the smaller mountains
in western Java, the highest of which is the 3,418 m Mt Slamet, but most are c.3,000 m or lower.
Bartels (1931) described its habitat in and around a tea plantation on the south-western slopes of
Mt Patuha, where during their raiding parties the magpies venture out far into the tea gardens;
they prefer the forest fringes along the rivers.
Food
The old names Hunting Crow or Hunting Cissa (Madge and Burn 1994) very aptly describe its
voracious nature. They are found in troops, or seasonally in pairs (Koningsberger 1915), not
uncommonly accompanied by Rufous-fronted Laughingthrush Garrulax rufifrons (Konings-
berger 1907), and often found near mixed bird parties (Delsman 1927).
Table 5 shows the items found in the stomach content of 34 specimens (Vorderman 1886,
Bartels 1897-1931, Sody, in Becking 1989). Throughout the year invertebrates form the most
important element. A variety of prey items has been found in stomachs: snails; crustaceans:
crayfish Astacidae (Decapoda), pill bugs Armadilliidae (Isopoda); insects: cockroaches Blattidae
(Dyctyoptera), grasshoppers (Orthoptera), ‘may-beetles’ Scarabaeidae, weevils Curculionidae,
Chalcothea spp. Cetoniidae, horned beetles Cerambycidae, click beetles Elateridae (Coleoptera),
cicadas (Homoptera), caterpillars (Lepidoptera), large ants Formicidae (Hymenoptera). Larger
vertebrate prey (small birds, lizards, including their eggs, tree frogs, and snakes) constitutes
a large part in first three months of the year only, largely coinciding with the breeding season.
Breeding
Although data are scarce and conclusions cannot be reliably drawn, it appears that breeding takes
place during most of the year with a preponderance for the wettest months, i.e. October –April in
Table 5. Food items in stomach content of Cissa thalassina (from Vorderman 1886; M. Bartels 1897-1931).
I: Jan-Mar, II: Apr-Jun; III: Jul-Sep; IV: Oct-Dec.
I II III IV
n samples 10 11 2 12
Invertebrates 18 24 7 20
Vertebrates 13 1 1 5
Fruits 100 2
S. van Balen et al. 12
west Java (Voous 1950): Jan (3), Feb (1), Mar (1), Apr ( 3), Sep (1), Dec (2) (after data from Bartels
1897-1931, Hoogerwerf 1949, 1950, Hellebrekers and Hoogerwerf 1967, J. H. Becking unpubl.
data). Birds are freshly moulted at the end and beginning of the year (Bartels 1902).
Meyer (1884) reported a “...cup-shaped nest on the thin twigs of a large-leaved tree, consists of
a base of stronger stalks or branches, then tendrils and thin twigs, intertwined with many dry
leaves of bamboo, rice etc; inside lined with black thin roots; 80 mm high, 170-180 mm wide,
inner cup 65 mm deep and 110 mm wide.”. Bartels (1897-1931) “... found its nest twice on thin
trees in a tree fork close to the trunk, of rather solid built, but not very large in relation to bird’s
size ...“. Hoogerwerf (1950):“...usually not high above the ground (3–6 m)...in not thick
branches...base and outside consists of dry leaves, both from trees and rattan etc. Nest cup lined
with plant parts looking like thin, dark rootlets, and petioles, stems, etc...”. Becking (unpubl. data)
reported a nest in a Tarenna incerta tree at 2.5 m above the ground in a Manglietia experimental
plot, another in a small tree in undergrowth at 3 m above the ground in primary forest.
Clutch size is one egg (n 5 1) or two (n 5 7) (Hoogerwerf 1949, Hellebrekers and Hoogerwerf
1967). The egg is described as “oval, coarse-grained, smooth, and moderately glossy, with
yellowish-white ground colour with few grey violet primary stains, and marked on the entire
surface with uniformly distributed smaller reddish-yellow secondary stains; also this egg shows
the close relationship with
Cissa chinensis” (Kuschel 1895). Eggs of C. t. thalassina (n 5 17;
Hoogerwerf 1949, Hellebrekers and Hoogerwerf 1967, Becking unpubl. data) average 32.78 mm
(31.1-34.3 mm) x 22.61 mm (range 22.0–23.30).
It has been frequently reported that incubating birds with young or eggs are very steady,
“... leaving their nest only when the nest tree is climbed... ” (Bartels 1897-1931; J.H. Becking
unpubl. data); this certainly makes them vulnerable to bird trapping.
Conservation
Bird trade
According to Rutgers and Norris (1977), they do not appear often in collections, and in 1861 the
taxon was first imported to London. The magpie is a moderately popular cage bird on Java, despite
the quick loss of its bright green colour in captivity, but possibly compensated by its loud and clear
calls, making it attractive for local bird fanciers. Numbers seen on local bird markets have always
been small and during 1979–1986 they were rather erratically seen for sale on the bird markets in
Bandung and Bogor (S. v. B pers. obs.), i.e. not always present and mostly in singles: (i) Many
(25–125 birds, relatively expensive) in October-May 1978, Bandung (Iskandar 1980). (ii) A
comprehensive survey of the Yogya bird market in February 1979 counted a single bird (van
Balen et al. in prep.). (iii) Regular visits to the bird market in Bogor in 1979-81 yielded only few
records; in Bandung 1981–86, few each time. (iv) None were seen among 150,000 birds on
a Jakarta bird market in December 1987 (Basuni and Setiyani 1989). (v) A study into the bird
trade in Indonesia in 1992–93 found C. t. thalassina in 25 of 39 surveys of mainly Javan bird
markets; it was also reported that 320 were authorised for export between August-December
1992 (Nash 1993). (vi) Often seen on bird markets in the past, but now very rarely, and currently
prices have been sky-rocketing to Rp 1,200,000 per bird (R. Sözer in litt. 2011), which is more
than the local minimum wage per month (Wordpress 2011).
The relative popularity of green magpies in general is indicated by the moderately large
numbers of Cissa chinensis found during a bird market survey in 1997–2001 in Medan: between
121 and 264 (Shepherd et al. 2004) meaning an average of 10–20 birds each survey, suggesting
a certain popularity of green magpies, and in February 1995, three
Cissa chinensis were seen
offered for sale in the west Javan town of Purwakarta (S. v. B. unpubl. data).
For Mt Halimun, Riffel (1991) reports that many are caught, as also communicated in April
1995 by Suandi (Carucub village) to S. v. B. In the Lumping (Dieng Mts) in the mid 1990s bird
catchers were mostly people of the village, but also a trapper from western Java who specialised in
Biology and conservation of Short-tailed Green Magpie in Java 13
green magpies was reportedly active in the area. These trappers were only active in October and
November when the main bait to catch forest birds, winged termites (laron), were available in
abundance.
Habitat fragmentation
Most forest up to 1,000 m and locally up to 1,500 m has disappeared on Java (van Balen 1999), thus
largely affecting the range of the magpie. No magpies are known from montane forest patches that
are small and have been isolated since prehistoric times, such as Mts Karang, Muriah, Ciremai, and
Ungaran, indicating that the species is sedentary. This might also explain why this species never
occurred in the eastern half of Java.
Although classified by Wells (1985) as dependent on montane habitat, they might be better
regarded as one of his ‘lowland slope specialists’. With the near-total deforestation of Java’s
lowlands and ongoing encroachment beyond 1,000 m and even 1,500 m, this taxon faces a real
risk of local or even overall extirpation, as it is being ‘locked up’ in increasingly narrow forest
bands (van Balen 1988). Interestingly, the Bornean jefferyi has a considerably wider range, from
305 to 2,735 m, though rarely below 1,400 m, where it overlaps at lower altitudes, 305-1,530 m,
with the Common Green Magpie Cissa chinensis minor, but both species appear to be mutually
exclusive on Mt Kinabalu (Whitehead 1893) above and below 1,000 m.
Status assessment
The taxon jefferyi appears to be secure in its remote haunts in the interior of Borneo, especially in
well-protected reserves such as Kinabalu National Park. The following discussion on conservation
therefore solely refers to the Javan Green Magpie.
Three parameters for IUCN threatened category thresholds (Collar et al. 1994, IUCN 2001,
BirdLife International 2001) were assessed for the Javan Green Magpie: (i) population decline,
(ii) population size, and (iii) small range size. (i) The observation that few or no green magpies
have been seen in the past 25 years, even in areas where they used to be seen quite regularly (Mts
Halimun-Salak, and Mts Gede-Pangrango), and the nearly total disappearance from local bird
markets where they were seen more or less frequently in the past, suggests a serious decline in
numbers, which certainly exceeds 80% in the past 10 years. As shown, they have probably been
completely extirpated from many of the sites where they were last recorded in the 20
th
century.
(ii) Populations at the 1–4 sites where there is a potential chance of their present survival must
certainly be very small, probably not exceeding one or two dozen individuals. The global wild
population size therefore probably does not exceed 100 and is quite possibly below 50 individuals.
Excessive capture for the bird trade and habitat destruction are the ultimate causes of the extreme
rarity of the magpies. The survival of small remaining populations is now jeopardised by the fact
that catchers specialise in one or more species. This inevitably means that local populations are
specifically targeted, with an increased risk that the last remaining birds in the wild are extirpated
sooner or later. (iii) Their extent of occurrence (global range) is probably c.2,410 km
2
. The
ongoing deterioration of suitable habitat has undoubtedly caused the shrinking of its range from
nine to four, or fewer, localities.
The area of occupancy (actual area inhabited) of 1,680 km
2
is calculated from the total area of
localities where the magpie has been seen since 2000 (Table 6). This figure is more than likely too
optimistic, given the lack of more recent records, and the fact that only part of these areas consists
of suitable habitat. Moreover, only four localities are reserves that are moderately or hardly
fragmented, enjoy sufficient protection against hunting and habitat destruction, and where
observations date from this century.
Based on the above observations, we note that the Javan Green Magpie fulfils four criteria for
‘Critically Endangered’ status:
S. van Balen et al. 14
- Criterion A2a: a projected decline of $ 80% over 10 years based on observation;
- Criterion C1: a global population size of # 250 mature individuals that are
declining at $25%;
- Criterion C2a: a global population size of # 250 mature individuals that are
severely fragmented, with # 50 individuals per sub-population;
- Criterion D: a global population size that may well be # 50 mature individuals.
Measures taken
Cissa thalassina has been observed in only four localities in the last 10 years. These are Mts
Halimun-Salak, Mts Gede-Pangrango, Gunung Simpang and Mt Merapi. The first and second
sites are more or less well-established national parks, where despite the huge importance of the
endemic biodiversity they support, much encroachment (agriculture, logging, mining, bird-
catching) occurs along their borders. Gunung Simpang is a strict nature reserve, whereas Mt
Merapi was given national park status a few years ago, but its efficacy is debatable, as there is
much resistance from local communities, and recent volcanic eruptions have destroyed much of
the natural forest.
Measures proposed
(i) The Javan Green Magpie qualifies for immediate protection because of its precarious current
situation. Any official protection measures however have to be taken with the greatest care, as
drawing too much attention could easily boost its market price as a cage bird, as has happened
previously with endangered species (Nijman et al. 2009). (ii) Law enforcement and awareness
programmes in the last refuges of the magpie, Mts Halimun-Salak, Mts Gede-Pangrango,
Gunung Simpang and Mt Merapi protected areas should be intensified, and focused on proper
protection of the forest at the lower to mid-elevations. (iii) Any Javan Green Magpies that are
encountered in captivity should be immediately rescued for either a captive breeding programme
or release into the wild. Only birds that are unsuitable for release, for instance by having been in
captivity too long (as indicated by fading of the green plumage into blue) should be considered for
a captive breeding programme. Currently a feasibility study for a breeding programme in the
Cikananga wildlife rescue center at Sukabumi, West Java, is supported by Chester Zoo (UK)
(R. Sözer in litt. 2011). Release attempts should be undertaken into their areas of origin, or in
areas where re-stocking is preferable, but only provided that these actions are backed by increased
law enforcement and awareness programmes, as otherwise the released individuals may well be
Table 6. Forest blocks in West and Central Java with recent and historical records of Cissa thalassina.
Abbreviations: NP, National Park; NR, Nature Reserve; PF, Protection Forest. Fragmentation score: 1, one
large compact area; 2, several medium-sized, interconnected forest areas; 3, several small to intermediate
areas, with or without adjacent smaller areas.
Status Area (km
2
) Alt. range (m asl) Fragmen-
tation
Most recent
record
Mts Halimun-Salak NP 500 400 – 2,210 1 2005
Jampang Kulon - 100 0 – 400 3 1906
Mts Gede-Pangrango /
Megamendung
NP 200 500 – 3,019 2 2002
North Parahyangan PF/NR 100 900 – 2,018 3 1941
South Parahyangan PF/NR 900 300 – 2,622 2 2006
Pembarisan Mts PF 130 300 – 1,351 2 1994
Mt Slamat PF 150 700 – 3,418 1 1917
Dieng Mts PF 250 250 – 2,565 2 1995
Mt Merapi NP 80 1,000 – 3,142 2 2005
Biology and conservation of Short-tailed Green Magpie in Java 15
illegally captured again shortly after release. (iv) Surveys should be undertaken in remaining
forest patches with extensive suitable habitat, that have been undersurveyed but where the
presence of green magpies is expected, e.g. Gunung Sawal (5,400 ha, 600–1,764 m) and Gunung
Ciremai (12,000 ha, 1,000–3,078 m). Areas where magpies were historically known to occur
should also be surveyed.
Conclusion
The signifi cant differences in biometrics and coloration as well as strong vocal differences warrant
an upgrading of both the Bornean and Javan subspecies of Short-tailed Green Magpie to species
status. We propose the English names Bornean Green Magpie Cissa jefferyi and Javan Green
Magpie Cissa thalassina.
Only four or fewer localities in western Java appear to harbour Javan Green Magpie. Their
numbers must have seriously declined in the past 25 years; and its present extent of occurrence is
little more than 2,100 km
2
, whereas in its area of occupancy only a fraction of the original
population may remain. Pending specialised surveys in potential areas, we propose the status of
globally ‘Critically Endangered’ for the Javan Green Magpie, based on IUCN criteria.
Supplementary Material
The supplementary materials for this article can be found at journals.cambridge.org/bci
Acknowledgements
Thanks are due to Vincent Nijman, Pupung Nurwatha, Adhy Maruly, Prayudhi, Indra Ferdinand,
Nick Brickle, Pete Wood, David K. Bishop, Frank Lambert and Resit Sözer for sharing their
records of Green Magpie on Java. Thanks also go to Steven van der Mije (NCB Naturalis, Leiden),
Mohammad Irham (Museum Zoologicum Bogoriense at Bogor, Indonesia) and Mark Adams
(British Natural History Museum at Tring, UK) for access to their bird collections. Dave Farrow,
Craig Robson, David Edwards, Brian Cox, Arnold Meijer, Nick Athanas, Rob Hutchinson, Mike
Nelson and Frank Lambert are thanked for providing their sound recordings through the online
database http://www.xeno-canto.org.
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*Author for correspondence; e-mail: bvanbalen001@hotmail.com
Received 17 February 2011; revision accepted 29 July 2011
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