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Black-headed Penduline tits Remiz macronyx in Kazakhstan

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The Black-headed Penduline Tit Remiz macronyx is a poorly known species that breeds in reedbeds Phragmites australis and bulrush Typha latifolia, mainly in Iran, Turkmenistan and Kazakhstan (Harrap & Quinn 1996, Wassink & Oreel 2007, Madge 2008). Kazakhstan is perhaps the most accessible place to see the species, yet there is only one site where it is regularly reported by birdwatchers: the Topar lakes along the Ili river delta near lake Balkhash, Almaty province (Figure 1). Four subspecies have been recognised of which R. m. ssaposhnikowi occurs at the Topar lakes. The Eurasian Penduline Tit Remiz pendulinus does not occur in this area. As part of a research project investigating the evolution of breeding systems in penduline tits (see van Dijk et al 2007a) we studied populations of penduline tits in Kazakhstan. During the period 12–26 June 2008 we visited the Topar lakes in search of Black-headed Penduline Tits. Although we found Black-headed Penduline Tits, the population near the Topar lakes appeared to be of low density. In this paper we describe our findings and speculate about the taxonomy of penduline tits in the genus Remiz.
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171Sandgrouse 31 (2009)
Black-headed Penduline Tits Remiz macronyx
in Kazakhstan
SANDER BOT & RENÉ E VAN DIJK
The Black-headed Penduline Tit Remiz macronyx is a poorly known species that breeds
in reedbeds Phragmites australis and bulrush Typha latifolia, mainly in Iran, Turkmenistan
and Kazakhstan (Harrap & Quinn 1996, Wassink & Oreel 2007, Madge 2008). Kazakhstan
is perhaps the most accessible place to see the species, yet there is only one site where it
is regularly reported by birdwatchers: the Topar lakes along the Ili river delta near lake
Balkhash, Almaty province (Figure 1). Four subspecies have been recognised of which R.
m. ssaposhnikowi occurs at the Topar lakes. The Eurasian Penduline Tit Remiz pendulinus
does not occur in this area. As part of a research project investigating the evolution of
breeding systems in penduline tits (see van Dijk et al 2007a) we studied populations of pen-
duline tits in Kazakhstan. During the period 12–26 June 2008 we visited the Topar lakes
in search of Black-headed Penduline Tits. Although we found Black-headed Penduline
Tits, the population near the Topar lakes appeared to be of low density. In this paper we
describe our findings and speculate about the taxonomy of penduline tits in the genus
Remiz.
WHERE TO FIND A BLACK-HEADED PENDULINE TIT
Black-headed Penduline Tits are scarce in the Topar lakes area. Not every bird watching
tour visiting the Topar lakes finds the species and in the period of research we managed
to see only 14 birds: nine males and five females. We arrived late in the season during
which many birds may be either incubating or feeding offspring. In that period, penduline
tits are generally more quiet and elusive. So we might have been more successful find-
ing Black-headed Penduline Tits if we had visited the area earlier in the breeding season.
Nevertheless, the population near the Topar lakes appears to be small.
Figure 1. Distribution of Black-headed Penduline Tit Remiz macronyx and Eurasian Penduline Tit Remiz pendulinus in
Kazakhstan, following Harrap & Quinn (1996) and Wassink & Oreel (2007). Red: R. macronyx ssaposhnikowi, Yellow:
R. m. macronyx, Pink: R. pendulinus jaxarticus, Green: R.p. caspius.
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172 Sandgrouse 31 (2009)
The area consists of semi-desert inter-
spersed with small lakes and marshes.
The many relatively small lakes in the
sand dunes seem suitable for Black-headed
Penduline Tits, but we failed to find any
there. Although hard to quantify in the
field, we suggest that the apparently limited
abundance of food or nest material might be
the reason they avoid this habitat. We did
find Black-headed Penduline Tits in more
extensive reed beds close to the river Topar
(Plate 1). These reedbeds, however, are scarce and despite extensive searches in the region
we only found them in a lake system some 3 km northeast of Topar village (45° 3’ 31” N,
75° 2’ 50” E). The road from Topar village to Zhelturanga crosses this area. Walking beside
these lakes whilst listening for their call is the way to find your penduline tit (van Dijk et
al 20 07b).
MORPHOLOGY AND BEHAVIOUR
Harrap & Quinn (1996) described subspecies ssaposhnikowi as “rather variable in colour:
head pattern mainly as R. pendulinus caspius (a race of European Penduline Tit)”. Out of the
nine males we observed, four had an all black head, four other males indeed resembled
R. p. caspius, albeit variable in the extent to which the chestnut-brown was present on the
crown and nape. One male exhibited an intermediate head pattern. The four males which
had a completely black head also had a very dark reddish breast and red brown mantle
and scapulars. The tertials, secondaries and primaries had white fringes, creating a white
wing panel. These birds had a tricoloured appearance: black-red-white. In all respects
these birds looked like the nominate subspecies of Black-headed Penduline Tit except for
the broad pale fringes to the flight feathers, which are cinnamon-brown in the nominate
subspecies. The four males that resembled R. pendulinus caspius in their head colouration,
had a black mask, a chestnut brown crown and nape, and a white throat. The rest of their
plumage did not differ from the birds with a completely black head, so that the mantle
and scapulars were a deeply coloured dark red-brown with a lot of red colouration on the
breast and flight feathers with broad white fringes (Plate 2). One male showed an inter-
mediate head pattern: a black head intermixed with some chestnut coloured feathers and
a white throat (Plate 3). All five observed females were very similar to males of Eurasian
Plate 1. Typical habitat of Black-headed Penduline
Tit Remiz macronyx ssaposhnikowi: lakes surrounded by
extensive reedbeds, Topar lakes, Kazakhstan, June 2008.
© René van Dijk
Plate 2. Male Remiz macronyx ssaposhnikowi with black
mask, a chestnut brown crown and nape, and white
throat, thus resembling male R. pendulinus caspius. Topar
lakes, Kazakhstan, June 2008. © René van Dijk
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173Sandgrouse 31 (2009)
Penduline Tit Remiz p. pendulinus, yet with
typical female characteristics: they had a
wide mask, but squared rather than coni-
cally shaped and interspersed with some
grey feathers, especially at the base of the
bill and a grey ring around the eye. In addi-
tion these females had a clear red fringe on
the head above the forehead patch extend-
ing to both sides of the crown and had lots
of red feathers on the breast. A variable
amount of black feathers on the neck was
present and the back was paler than that of
the males (Plate 4). This description fits well
with the description given for female caspius
in Harrap & Quinn (1996). Curiously, we did
not observe any macronyx-type females. Bird
watchers mostly report caspius-like males
Plate 3. (above) Male Remiz macronyx ssaposhnikowi.
The only observed male with intermediate head pattern
characteristics. The black head resembles a nominate
macronyx, but the intermixing chestnut coloured feathers
and white throat resembles a caspius type bird. Topar
lakes, Kazakhstan, June 2008. © René van Dijk
Plate 4. (right) Female Remiz macronyx ssaposhnikowi’.
Topar lakes, Kazakhstan, June 2008. © René van Dijk
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174 Sandgrouse 31 (2009)
and only a very few report black-headed males in their trip reports (see eg www.travel-
lingbirder.com).
Song and call of both male types of ssaposhnikowi differ from those of European R.
p. pendulinus. Different syllables are used in the song repertoire of ssaposhnikowi Black-
headed Penduline Tits and their call is longer and more monotonous compared to the
slightly decreasing and shorter call of the nominate R. pendulinus (Figure 2). Nest building
behaviour may differ between the two types of male. We twice observed a black-headed
male building a nest between two reed stems at about 1.5 m height in a reedbed, while a
pair of the caspius-type had a nest in a tree. Of course, we cannot be certain that this is a
species specific difference in behaviour or a habitat driven behaviour. Either species may
build its nest in trees or reeds dependent on what is available. Incidentally, Black-headed
Penduline Tits Remiz m. macronyx in Turkmenistan build their nests in either trees or reed
(Y Belousov pers comm). A few records exist of nominate Eurasian Penduline Tits building
their nest in reeds.
DOES REMIZ MACRONYX SSAPOSHNIKOWI EXIST?
According to published information on the species’ distribution, all penduline tits in
the Topar lakes area are supposed to be R. m. ssaposhnikowi and Vaurie (1957) treats ssa-
poshnikowi as a hybrid swarm R. pendulinus jaxarticus x R. m. macronyx (jaxarticus is the
subspecies of R. pendulinus occurring north of lake Balkhash, Figure 1). We now doubt
whether we should treat all the Topar lakes birds as ssaposhnikowi and believe Vaurie
(1957) might have been incorrect in suspecting a hybrid swarm. Subspecies R. p. jaxar-
ticus approaches nominate pendulinus in morphology (Harrap & Quinn 1996) and thus
lacks the extent of chestnut colouration found in ssaposhnikowi. Our observations do not
provide support for R. m. ssaposhnikowi being a valid subspecies. Rather, we suspect that
Figure 2. Sonograms of typical calls of Eurasian Penduline Tit Remiz pendulinus pendulinus (top), recorded in Hungary
(46º 19’ N, 20º 5’ E) May 2006, and R. macronyx ssaposhnikowi (bottom) recorded at the Topar lakes, Kazakhstan,
June 2008. Note the difference in call length.
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175Sandgrouse 31 (2009)
Remiz m. macronyx and Remiz pendulinus caspius may well be coexisting in the area, ie R. m.
ssaposhnikowi may in fact be identical to R. p. caspius. Descriptions from published sources
(Harrap & Quinn 1996, Madge 2008) suggest there are no diagnostic plumage character-
istics to distinguish between R. p. caspius and R. m. ssaposhnikowi. The observed possible
variation in nest site selection might promote the coexistence of two distinct populations
(note that the White-crowned Penduline Tit R. coronatus coronatus also occurs in the Topar
lakes area). Out of nine observed males, one showed intermediate features, suggesting that
hybridization may occur to a limited extent.
If our supposition proves correct, this would mean a relatively minor range extension
for nominate R. m. macronyx. However, the known distribution of R. pendulinus caspius
would need considerable revision as R. p. caspius is described to occur only near and
around the Caspian sea, over 1000 km to the west (Figure 1).
TAXONOMY OF PENDULINE TITS OF GENUS REMIZ
Taxonomy of penduline tits in the genus Remiz is complex and confused. Until recently
they were most often treated as one wide-ranging species, Remiz pendulinus, the Penduline
Tit (Snow 1967). However, Harrap & Quinn (1996) and Madge (2008) recognised four
species: Eurasian Penduline Tit R. pendulinus, Black-headed Penduline Tit R. macronyx,
White-crowned Penduline Tit R. coronatus and Chinese Penduline Tit R. consobrinus. Eck
& Martens (2006) lumped Black-headed Penduline Tit with Eurasian Penduline Tit and
White-crowned Penduline Tit with Chinese Penduline Tit. They also stated that “besides
the morphological and biological information already available, acoustic and molecular
data are needed for sound decisions.” Our research reported here has provided a new
hypothesis concerning the ‘ssaposhnikowi’ taxon.
From the data we collected, we cannot conclude with certainty whether to split or lump
Black-headed Penduline Tit and Eurasian Penduline Tit. Nevertheless, the possible coexist-
ence of members of both taxa without evidence for extensive hybridization suggests they
are best treated as different species. Clearly, more data are needed from this and other
populations in Central Asia, to verify this proposition.
We can be more confident about the relationship between the White-crowned
Penduline Tit and the R. m. ssaposhnikowipopulation at the Topar lakes: we argue that
they should be treated as different species. The White-crowned Penduline Tits in the
Topar area did not show any characteristics that suggested hybridisation with the R. m.
ssaposhnikowi’ population. Biometric measurements, song and plumage traits for R. corona-
tus were markedly different from R. m. ssaposhnikowi’: individuals of R. m. ssaposhnikowi
are heavier (mean ± SD: 10.75 ± 0.64 versus 7.55 ± 0.65 g), and have longer tarsi (18.00 ± 0.28
versus 15.20 ± 0.39 mm). The larger feet of R. m. ssaposhnikowi are possibly an adaptation
to living in reedbeds. R. m. ssaposhnikowi used different syllables in its song repertoire
compared to White-crowned Penduline Tits.
Most populations of White-crowned Penduline Tit occur in a different habitat. The
small river along which the White-crowned Penduline Tits occurred in the Topar area
lacked the extensive reedbeds that seem to be preferred by Black-headed Penduline Tits.
White-crowned Penduline Tits that occur in, for instance, the South Kazakhstan province,
breed along small streams, without extensive reedbeds, that come down the western
Tien Shan mountains (van Dijk & Bot unpubl data). Near Topar, they build their nests in
Russian Olives Eleagnus angustifolius, and we never observed a White-crowned Penduline
Tit in a reedbed where ‘ssaposhnikowi’ occurred and vice versa.
Finally, in a collaborative project with the Swedish Museum of Natural History, we are
currently constructing a phylogenetic tree of penduline tits based on molecular genetics.
Provisional results support our proposition that ssaposhnikowiand the White-crowned
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176 Sandgrouse 31 (2009)
Penduline Tit are different species (RE van Dijk, T Székely, M Irestedt & PGP Ericson
unpubl data).
The Chinese Penduline Tit is also included in the phylogenetic analysis and preliminary
results suggest that the Chinese Penduline Tit is distinct from White-crowned Penduline
Tit, and deserves species status. These provisional molecular systematics results are sup-
ported by observations in the field: we found that Chinese and White-crowned Penduline
Tits clearly differ in song, plumage and breeding system (RE van Dijk, Á Pogány, S Bot, J
Komdeur & T Székely unpubl data).
For sound conclusions about the relationship between the Black-headed Penduline Tit
and Eurasian Penduline Tit we need much more field data as well as high resolution phy-
logenetic information. In the present study we only found a limited number of birds and
very little is known from the areas around the Caspian sea where both taxa meet. By pub-
lishing our findings we hope to encourage people to collect and report more information
about behaviour, biometrics, morphology, hybridisation and genetic divergence to reveal
the taxonomy of this morphologically and behaviourally diverse group.
ACKNOWLEDGEMENTS
The research leading to these results has received funding from the European Community’s Sixth Framework
Programme (FP6/2002–2006) under contract n 28696. We thank Vera Voronova for her indispensable help in
the field and Sergey Sklyarenko, Arend Wassink, Lammert Bies and Machiel Valkenburg for their essential
support in arranging practicalities.
REFERENCES
van Dijk, RE, I Szentirmai, J Komdeur & T Székely. 2007a. Sexual conflict over parental care in Penduline
Tits Remiz pendulinus: the process of clutch desertion. Ibis 149: 530–534.
van Dijk, RE, I Szentirmai & T Székely. 2007b. Practical field guide for investigating breeding ecology of penduline
tits Remiz pendulinus. Field Protocol. University of Bath, www.bath.ac.uk/bio-sci/biodiversity-lab/pdfs/
PT_%20Field%20Guide_1_2.pdf.
Eck, S & J Martens. 2006. Systematic notes on Asian Birds. 49. A preliminary review of the Aegithalidae,
Remizidae and Paridae. Zoologische Mededelingen Leiden 80–5 (1): 1–63.
Harrap, S & D Quinn. 1996. Tits, Nuthatches & Treecreepers. Christopher Helm, London.
Madge, S. 2008. In: del Hoyo, J, A Elliott & DA Christie (eds). Handbook of the Birds of the World. Penduline-tits
to Shrikes. Lynx Edicions, Barcelona.
Snow, DW. 1967. The families Aegithalidae, Remizidae and Paridae. In: RA Paynter (ed). Check-list of Birds
of the World. Vol 12. Cambridge, Massachusetts, pp52–124.
Vaurie C, 1957. Systematic Notes on Palearctic Birds. No 28. The families Remizidae and Aegithalidae.
American Museum Novitates 1853: 1–21.
Wassink A & GJ Oreel. 2007. The Birds of Kazakhstan. Arend Wassink, De Cocksdorp, Texel, Netherlands.
Sander Bot, Animal Ecology Group, Centre for Ecological and Evolutionary Studies, University of Groningen, 9750 AA
Haren, Netherlands. sanderbot@yahoo.co.uk
René E van Dijk, Animal Ecology Group, Centre for Ecological and Evolutionary Studies, University of Groningen, 9750 AA
Haren, Netherlands & Department of Biology and Biochemistry, University of Bath, Claverton Down, Bath BA2 7AY, UK.
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... Chinese Penduline Tits at our study site (Table 3) breed in similar habitats to those of the Eurasian Penduline Tit populations in Hungary, Germany, Austria and the Netherlands (Franz 1991;Van Dijk et al. 2010a), and the population of Black-headed Penduline Tits near the Topar River in Kazakhstan (Bot and Van Dijk 2009), containing extensive water bodies and reed beds. The breeding density of Fig. 4 Relationship between date of egg-laying and clutch size of Chinese Penduline Tits (2017 season, n = 61 nests). ...
... Locust trees, moreover, with their thorns and branches at close intervals, provide high security for breeding nests and have the highest nest success rate. However, in the other three species, poplars and willows are common tree species selected by males, as sufficient material can be collected efficiently during the boll-opening stage (Bot and van Dijk 2009;Mei et al. 2009;Persson and Öhrström 1989), which is distinctive of the Chinese Penduline Tits who seek nest materials directly from reeds and cattails. ...
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The Chinese Penduline Tit (Remiz consobrinus) is a small passerine that breeds in Northeast Asia. Despite its common appearance and its high encounter rate, the breeding biology of this species has remained largely unknown. In this paper, we describe for the first time the breeding biology and parental care system of the Chinese Penduline Tit in the coastal area of Northeast China. As a migratory species of birds, it arrives at the Liaohe Delta in late April, the males establish territories in early May, and breeding pairs build their nests from May to July. Most nest building occurs from mid-May to early June. The females produce small white eggs (egg mass, 1.0 ± 0.1 g) and a clutch size of 6.8 ± 0.6 eggs. The parental care system is complicated in Chinese Penduline Tits: uniparental care is dominant (80%) in this population, with a majority (71%) of female-only care and 9% male care for all brooding nests, together with 4% biparental care and 16% biparental desertion. Chicks hatch after 13.9 ± 1.0 days of incubation and fledge after 22.1 ± 1.0 days. The hatching success and nestling survival are 86.7 and 80.6%, respectively. Furthermore, breeding failure is 23.4%, which is commonly caused by predation and nests blown away by strong winds. Compared to other species of the Remiz genus, the Chinese Penduline Tit shows much similarity to the Eurasian Penduline Tit (Remiz pendulinus) but large differences compared to the White-crowned Penduline Tit (Remiz coronatus) with respect to breeding habitat, breeding density, nest site selection and parental care system. Moreover, the good nest attributes, relatively high nestling survival and low risk of nest failure may contribute to the prevalence of the uniparental care system in this Chinese Penduline Tit population.
... The mitochondrial data strongly support the proposition that R. coronatus, R. consobrinus, and R. pendulinus/macronyx form three independent evolutionary lineages, while microsatellite genotyping supported the notion that R. pendulinus and R. macronyx are also differentiated, albeit marginally. The three main linages (R. coronatus, R. consobrinus, and R. pendulinus/macronyx) can not only be genetically differentiated, but also based on morphology, behaviour and the type of habitat they inhabit (Harrap and Quinn 1996, Madge 2008, Bot and van Dijk 2009, Bot et al. 2011). Ivanov (1940 pointed out and R. macronyx, respectively (Fig. 4C). ...
... They preferred to treat coronatus and consobrinus under the species Remiz consobrinus until more data would become available. Bot and van Dijk (2009) showed significant differences between R. coronatus and R. macronyx in biometry, vocalization and plumage traits. Their field observations are in agreement with our results based on the molecular genetics of the two species. ...
... The mitochondrial data strongly support the proposition that R. coronatus, R. consobrinus, and R. pendulinus/macronyx form three independent evolutionary lineages, while microsatellite genotyping supported the notion that R. pendulinus and R. macronyx are also differentiated, albeit marginally. The three main linages (R. coronatus, R. consobrinus, and R. pendulinus/macronyx) can not only be genetically differentiated, but also based on morphology, behaviour and the type of habitat they inhabit (Harrap and Quinn 1996, Madge 2008, Bot and van Dijk 2009, Bot et al. 2011). Ivanov (1940 pointed out that breeding ranges of R. coronatus meet with R. pendulinus and R. macronyx in western Tajikistan. ...
... They preferred to treat coronatus and consobrinus under the species Remiz consobrinus until more data would become available. Bot and van Dijk (2009) showed significant differences between R. coronatus and R. macronyx in biometry, vocalization and plumage traits. Their field observations are in agreement with our results based on the molecular genetics of the two species. ...
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Penduline tits (Remizspp.) are renowned for their diverse mating and parenting strategies, and are a well-studied system by behavioural ecologists. However, the phylogenetic relationships and species delimitations within this genus are poorly understood. Here, we investigate phylogenetic relationships within the genus Remizby examining the genetic variation in the mitochondrial cytochrome-bgene of 64 individuals and in ten autosomal microsatellite markers from 44 individuals. The taxon sampling includes individuals from all currently recognized species (R. pendulinus, R. macronyx, R. coronatus, and R. consobrinus) and most subspecies in the Palearctic region. We showed that R. coronatusand R. consobrinusare genetically well differentiated and constitute independent evolutionary lineages, separated from each other and from R. pendulinus/macronyx. However, we found no evidence for significant differentiation among R. pendulinus/macronyx individuals in mtDNA haplotypes and only marginal differences between R. pendulinusand R. macronyxin microsatellite markers. Hence, based on present data our recommendation is to treat R. pendulinusand R. macronyxas conspecific and R. coronatusand R. consobrinusas separate species.
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Do the two parents at a nest make simultaneous decisions whether to care for their offspring or to desert? If a single parent is sufficient for rearing young, one parent (typically, the male) may desert and reproduce with a new mate within the same breeding season, leaving the other parent with the brunt of care. As each parent is expected to maximize its own reproductive success, the interests of the two parents do not necessarily coincide, and a sexual conflict over care may emerge. Here we investigate the process of clutch desertion in a small passerine bird, the Penduline Tit Remiz pendulinus. Among birds, this species has a remarkably variable breeding system, because a single parent (either the male or the female) may provide the full care of the young, whereas about 30% of clutches are abandoned by both parents. First, we show that biparental desertion occurs within a single day in 73.7% of the clutches (n=14), whereas desertion decisions are sequential in 26.3% of the clutches (n = 5) (male first: 10.5% (n = 2); female first: 15.8% (n = 3); n = 19 clutches in total). Secondly, we observed the behaviour of both parents before desertion, and investigated whether desertion can be predicted from their behaviour. However, neither singing nor nest-building behaviour predicted whether the male or the female would desert. We therefore suggest that biparental desertion may be simultaneous by male and female in our population of Penduline Tits. Furthermore, the parents do not appear to signal their intention to desert their mate. We argue that the parents’ interest may be actually to disguise their intention to desert.