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The next common and widespread bunting to go? Global population decline in the
Rustic Bunting Emberiza rustica
LARS EDENIUS, CHANG-YONG CHOI, WIELAND HEIM, TUOMO JAAKKONEN, ADRIAAN DE
JONG, KIYOAKI OZAKI and JEAN-MICHEL ROBERGE
Bird Conservation International / FirstView Article / April 2016, pp 1 - 10
DOI: 10.1017/S0959270916000046, Published online: 18 April 2016
Link to this article: http://journals.cambridge.org/abstract_S0959270916000046
How to cite this article:
LARS EDENIUS, CHANG-YONG CHOI, WIELAND HEIM, TUOMO JAAKKONEN, ADRIAAN DE
JONG, KIYOAKI OZAKI and JEAN-MICHEL ROBERGE The next common and widespread
bunting to go? Global population decline in the Rustic Bunting Emberiza rustica. Bird Conservation
International, Available on CJO 2016 doi:10.1017/S0959270916000046
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Bird Conservation International, page 1 of 10 . © BirdLife International, 2016
doi:10.1017/S0959270916000046
The next common and widespread bunting to go?
Global population decline in the Rustic Bunting
Emberiza rustica
LARS EDENIUS , CHANG-YONG CHOI , WIELAND HEIM ,
TUOMO JAAKKONEN , ADRIAAN DE JONG , KIYOAKI OZAKI and
JEAN-MICHEL ROBERGE
Summary
Populations of several long-distance migratory songbirds in Eurasia are in peril, drastically
illustrated by the recent range-wide population collapse in the Yellow-breasted Bunting
Emberiza aureola . There are signals of a strong decline also in the Rustic Bunting E. rustica , but
no range-wide assessment of population trends in this superabundant and widespread bunting
species has yet been undertaken. The conservation status of Rustic Bunting is ‘Least Concern’
on the global IUCN Red List, but it has recently been upgraded to ‘Vulnerable’ on the European
Red List. To assess the Rustic Bunting’s global conservation status we compiled, for the first
time, population data across its breeding and wintering ranges. The analysis reveals a 75–87%
decline in overall population size over the last 30 years and a 32–91% decline over the last 10
years. The trend estimates indicate that the long-term (30-year) range-wide population decline
in the Rustic Bunting is of similar magnitude to two well-known examples of declining species
within the same genus, the Yellow-breasted Bunting and the Ortolan Bunting E. hortulana . The
magnitude of the range-wide population decline over the last 10 years suggests that the Rustic
Bunting could be upgraded from ‘Least Concern’ to ‘Vulnerable’ or ‘Endangered’ on the IUCN
global Red List. Agricultural intensification in the wintering range and intensified levels of
disturbance, including logging and fire, in the breeding range could be important drivers of the
range-wide population decline, and persecution could also contribute. Untangling threat factors
and their interactions on Rustic Bunting is necessary for conservation, but hampered by our
currently limited understanding of the relationships between population dynamics and different
threats.
Introduction
A large number of long-distance migratory songbirds exhibit decreasing population trends in
Eurasia (Sanderson et al. 2006 , Laaksonen and Lehikoinen 2013 , Vickery et al. 2014 ). Amongst
the 170 long-distance migratory songbird species using the East Asian flyway, for example, one
third show declining trends and 12% are classified as threatened or near-threatened (Yong et al.
2015 ). Whilst the drivers of population declines are comparatively well studied in the Afro-
Palearctic migratory system (Vickery et al. 2014 ), such knowledge is scarce for the East Asian
flyway (Yong et al. 2015 ). Asia has seen a strong intensification in agriculture during recent
decades, and witnessed increasing urbanisation and industrialisation (Alauddin and Quiggin 2008 ).
Anthropogenic and climate-related stressors in the form of logging, draining, and forest fires
have also increased (Goldammer and Furyaev 1996 , Achard et al. 2006 ) as has trapping of songbirds
L. Edenius et al. 2
for consumption and religious merit release (Gilbert et al. 2012 , Townsend 2015 , Yong et al. 2015 ).
Stronger environmental pressures on breeding and wintering habitats and increased levels of
persecution have therefore emerged as serious threats to long-distance migratory songbird popu-
lations in East Asia.
Habitat loss and persecution are considered as threats to rare and range-restricted species,
but the scale of these factors may now have reached levels whereby even superabundant and
wide-ranging species are becoming threatened. For example, data for Yellow-breasted Bunting
Emberiza aureola , compiled across its distribution in Eurasia, showed that the global popula-
tion of this once very abundant species, virtually collapsed over a time period of only 25 years
(Kamp et al. 2015 ). The Rustic Bunting Emberiza rustica shares many ecological traits with
the Yellow-breasted Bunting. For example, both have very large and almost overlapping
breeding ranges, being superabundant long-distance migrants, and use similar migration
routes (Byers et al. 2013 ). There are some signals of a strong population decline also in the
Rustic Bunting (BirdLife International 2015a ), but the details and causes of the decline remain
unclear.
The distribution of the Rustic Bunting spans roughly 170 degrees of longitude, across Eurasia
from Fennoscandia in the west to the Kamchatka peninsula in the east (Cramp and Perrins 1994 ).
The breeding range, which is estimated at 218 Mha (BirdLife International 2015a ), is intimately
linked to the boreal forest, wherein the typical breeding habitat is wet coniferous forest with birch
Betula spp. and willow Salix spp. growth along slow-flowing water (Öhrn 1963 , Pulliainen and
Saari 1989 , Kretchmar 2000 ). Current evidence suggests that the winter range of the Rustic
Bunting is confined to East Asia comprising Japan, the Korean Peninsula, and eastern and central
mainland China north of the tropic of Cancer (Byers et al. 2013 ). For the bulk of the population,
autumn migration follows forested regions eastwards, turning south in Asia east of Mongolia
(Cramp and Perrins 1994 , Byers et al. 2013 ). While just a few birds migrate through or winter in
Kazakhstan (Berezovikov and Levinskiy 2008 ), the Rustic Bunting is one of the most common
species during migration in the Russian Far East (Averin et al. 2012 , Heim et al. 2012 , Heim and
Smirenski 2013 ). Birds from Kamchatka (sometimes regarded as a separate subspecies latifascia )
are believed to migrate south-west across the Sea of Okhotsk or south to Japan across the Sea
of Japan (Valchuk et al. 2005 ). The spring migration in the Rustic Bunting appears to mirror the
autumn migration, but the details of its migratory patterns including stopover sites are inade-
quately known.
During the breeding season, the diet of Rustic Bunting mostly consists of invertebrates,
whereas it shifts to seeds, grasses, and other vegetable food in other seasons (Cramp and Perrins
1994 ). A variety of semi-open habitats are used during stopovers and in the winter range, including
woodlands, willow thickets, clearings, rice stubble, reed beds and riverbanks (Cramp and Perrins
1994 , Fujioka et al. 2010 , Yoo et al. 2011 , Schäfer et al. in prep ). At its winter feeding sites, the
Rustic Bunting prefers wet grassy places with plenty of seeds and presence of dense shrubs or
trees (Iijima 1973 , Maeda 2001 ). Maeda ( 1973 ) observed spatially segregated habitat use in the
Rustic Bunting during winter, with flocks of several hundred birds feeding in rice paddies during
daytime and roosting in loosely dispersed groups in shrubby or grassy patches in woodland areas
up to 1 km from the feeding sites.
The Rustic Bunting is classified as a species of ‘Least Concern’ (LC) on the IUCN Red List,
i.e. it is not considered globally threatened (BirdlLife International 2012 ). However, it has recently
been upgraded to ‘Vulnerable’ (VU) on the European Red List (BirdLife International 2015b ).
Population trends have been estimated for Fennoscandia (Dale and Hansen 2013 ) and Europe
(BirdLife International 2015a ) but not for the whole distribution range. Trend assessments and
expert opinions suggest that the European breeding population of Rustic Bunting has declined by
30–49% over the last 10 years in Europe, but only around one-fifth of the species’ global breeding
range is within Europe (Symes 2015 ). For large parts of the breeding range, population trends
remain unknown. While earlier population assessments have focused on restricted parts of the
distribution range and included a limited amount of time series data, we here present the first
Rustic Bunting population trends 3
range-wide assessment of population trends in the Rustic Bunting based on several short and long
term time series.
We compiled Rustic Bunting data from different countries to determine the range-wide rates
of population change and hence assess the species’s global status. We also present an overview of
possible drivers underlying the decline and propose key research activities to help overcome the
current lack of knowledge about the bunting’s ecology which hampers effective conservation
policies.
Material and methods
Data collection
We collated time series data on the Rustic Bunting from countries in the breeding range (Norway,
Sweden and Finland) and from stop-over sites during migration (Japan and north-eastern China).
Standardised breeding survey data were preferentially used, but since such data are scarce we also
included ringing data. In case of ringing data we only included standardised time series data,
i.e. data controlled for capture effort. We used nationwide breeding survey data from Sweden and
Finland and breeding territory count data for the very small Norwegian population (Green and
Lindström 2015a , Hansen 2015 , Aleksi Lehikoinen pers. comm.). In Sweden, breeding survey
counts have been carried out on fixed routes systematically distributed across Sweden since 1998
(Green and Lindström 2015a ). However, the number of surveyed fixed routes within the Rustic
Bunting’s breeding range in northern Sweden was low during the first years. Therefore, we used
Swedish breeding bird data only from the last 10 years (2005–2014). To increase the length of the
overall time series we complemented the Swedish breeding survey data with Rustic Bunting data
from ringing stations. The Japanese and Chinese data consisted of the number of Rustic Buntings
ringed during autumn migration at ringing stations. In total, we compiled seven time series of
data of up to 30 years in length, see Table 1 and Appendix S1 in the online supplementary materials
for details.
Statistical analysis
For the Swedish and Finnish breeding bird survey data, we used TRIM-estimated (Pannekoek and
van Strien 2013 ) yearly population indices and linear trends provided to us by the national pro-
gramme organisers. To make the ringing data comparable with these breeding survey data, we
also used TRIM (ver. 3.54) to calculate indices and trends. In the case of the Norwegian breeding
survey data we applied TRIM to the numbers of occupied territories 2008–2014 (Hansen 2015 ;
Table 1 , Figure 1b ). The widespread TRIM (TRends and Indices for Monitoring data) software
uses log-linear models with a Poisson error distribution and allows for missing counts. Yearly
population indices were scaled (indexed) to 1 for the starting year. We employed models that
controlled for over-dispersion and serial correlation, and used trend estimates based on the
imputed population indices (to account for missing values) as recommended by Pannekoek
Table 1. TRIM-estimated annual decline rates for national data sets 1985–2014. P -levels denote significance
of deviation of slope values from 1 (= no change).
Country Time period Annual change, % P -level
Norway 2005–2014 -30 < 0.05
Sweden 1985–2014 -6.0< 0.01
Sweden 2005–2014 -5.3< 0.001
Finland 1985–2014 -6.1< 0.001
Japan 1985–2014 -4.5< 0.01
China 2005–2014 -20 < 0.05
L. Edenius et al. 4
and van Strien ( 2013 ). Rangewide trends were estimated by averaging the national time-series
trends. Trends were estimated for 30 years (1985–2014, long-term) and 10 years (2005–2014,
short-term), respectively. Missing values amounted to 2% ( n = 2) and 7% ( n = 5) of the data
points in the long- and short-term datasets, respectively. The small population in Norway, where
the Rustic Bunting is dwindling and is estimated currently at less than 10 pairs (Hansen 2015 ),
may have a disproportionate impact on the range-wide trend estimates. Therefore, we analysed
the time-series data also without the Norwegian data.
Figure 1. TRIM estimated yearly indices of Rustic Bunting numbers in long-term (a) and short-term
(b) data series.
Rustic Bunting population trends 5
Results
The TRIM-estimated yearly indices of the national data series revealed consistent population
declines across the range ( Table 1 , Figure 1 ). For the long-term data (1985–2014), the average
range-wide annual decline rate was estimated at 5.5% (± 1.0% 95% CI), which corresponds to an
82% (75–87%) reduction in population size over 30 years. The short-term (2005–2014) annual
decline rate was 12.4% (± 8.6% 95% CI), corresponding to a 73% (32–91%) reduction over
10 years ( Figure 1b ). When we re-ran the analyses after excluding the Norwegian data, it yielded
a 10-year annual decline rate of 8.9% (± 6.3% 95% CI), i.e. a 60% (23–81%) overall decline.
Discussion
Our analysis provides compelling evidence for a strong range-wide decline in Rustic Bunting
populations in recent times. To put the magnitude of the population decline into perspective,
we can compare it with two better-known examples of dramatic range-wide population declines
within the same genus: the Yellow-breasted Bunting and the Ortolan Bunting E. hortulana . The
decline in the Yellow-breasted Bunting was estimated at 84–95% over 34 years (Kamp et al.
2015 ). An extrapolation of our 82% (75–87%) long-term (30 year) trend in the Rustic Bunting
yields an 85% range-wide decline over 34 years. For the Ortolan Bunting, Vickery et al. ( 2014 )
reported an 84% decline over 30 years (1980–2009), which was the strongest population decline
of all long-distance migratory species in the Afro-Palearctic migratory system they studied. In
the case of the Yellow-breasted Bunting, the population collapse was accompanied by a strong
eastward range contraction. Although such a dramatic global range contraction has not yet been
observed in the Rustic Bunting, the range contraction towards north-east within Fennoscandia
has been dramatic. On the western edge of the global distribution huge areas of habitat on the
former Rustic Bunting distribution are now more or less empty of the species (Valkama et al.
2011 , Dale and Hansen 2013 , Green and Lindström 2015b ).
The decline rate estimates have strong relevance for the ongoing discussion about the conser-
vation status of the Rustic Bunting on the IUCN global Red List where it is currently listed in the
‘Least Concern’ (LC) category. Our range-wide estimate of a 61% (73% with the Norwegian
data) population decline for 2005–2014 (a time span roughly corresponding to three generations
in the Rustic Bunting; Symes 2015 ) indicates a decline well over the 30% threshold required for
classification as ‘Vulnerable’ (VU). Moreover, the observed population reduction exceeds the 50%
threshold for the category ‘Endangered’ (EN) on the global Red List.
Our data samples are biased towards Fennoscandia. This is an unavoidable consequence of the
fact that more data series are available from that part of the distribution range. From Russia,
which holds the bulk of the breeding population, we found only scattered information on breed-
ing densities (e.g. Rogacheva 1992 – Central Siberia, Kretchmar 2000 – noth-east Siberia), but no
standardised data on long-term population development. However, numbers of Rustic Buntings
captured during standardised ringing at Muraviovka Park in the Amur region of Russia show a
decrease of > 90% in recent years (2012–2015) (Wieland Heim pers. obs.). The Gaofeng Bird
Ringing Station located on the Chinese side of the Amur River also reports a strong recent decline
( Table 1 , Figure 1b ). This suggests that the decline in numbers of Rustic Buntings passing through
this part of East Asia during migration has been particularly strong. The negative trend expressed
by the Fukushimagata Ringing Station data in Japan ( Figure 1a ) is also seen in the non-standardised
national ringing sums of Rustic Bunting in that country for the same time period (Kiyoaki Ozaki
pers. obs.). In South Korea no long-term standardised data series exist, but non-standardised
short-term ringing data show that capture rates of Rustic Bunting (measured as the proportion of
total ringing sums) are now about 10 times lower than they were in the mid-1960s (Chang-Yong
Choi pers. obs.). Also in China there is a shortage of standardised ringing data (Bo Pettersson pers.
comm.). We included the most comprehensive data series from China, from the Gaofeng Bird
Ringing Station, Heilongjiang Province (Appendix S1) in our analysis, and it showed a strong
L. Edenius et al. 6
Table 2. Changes in land use practices, natural processes and persecution, and their potential impacts on Rustic
Bunting populations.
Practice/process Effect on Rustic Bunting
habitat or populations
Estimated
strength of
impact
Trend Reference
Breeding range
Draining to
enhance forest
productivity
Habitat loss/degradation.
Decreasing in the western
range but may be increasing
elsewhere
Moderate Increasing? Skogsstyrelsen
( 2014 ), Metla
( 2015 )
Forest logging Habitat loss. Increasing intensity
in parts of the range
Moderate-
strong
Increasing Skogsstyrelsen
( 2014 ), Achard
et al. ( 2006 )
Wild fires Habitat loss. Increasing,
particularly in central and
eastern parts in response to
climate change and increased
anthropogenic disturbance
Strong Increasing Achard et al.
( 2006 ),
Flannigan et al.
( 2009 )
Melting/
retreating
permafrost
Habitat loss/degradation. Drying
up of wet forests related to
climate change. Large areas
in the eastern range potentially
affected
Strong Increasing Soja et al. ( 2007 )
Dam
constructions
Habitat loss. Central and eastern
parts of the range
Moderate Unknown Achard et al.
( 2006 )
Wintering range
Use of pesticides Reduced food resources, potential
poisoning. High application
rates in China, Japan and the
Republic of Korea
Strong Increasing Bright et al.
( 2008 )
Multiple crop
cycles
Habitat loss and/or degradation
due to reduction in winter
stubbles which are important
feeding habitats
Strong Increasing Round and
Gardner ( 2008 )
Reduction
in grassland
area
Habitat loss. Grasslands important
as feeding habitat. Significant
reduction in grassland area in
China 1990-2000
Strong Increasing Maeda ( 2001 ), Shi
et al. ( 2012 )
Changes in area
of fallow land
Habitat loss/degradation when
fallow land becomes actively
managed, vice versa when use
ceases. Variable trends reported
across the range
Strong Diverging Round and
Gardner ( 2008 ),
Amano (
2009 ),
Long et al.
( 2009 )
Transformation of
farmland and
woody areas to
other land uses
Habitat loss in case of urban and
rural settlement expansion,
potential habitat enrichment
after abandonment of
farmland
Strong Diverging Long et al. ( 2009 ),
Wu et al.
( 2009 )
Planting of trees
and other
woody
vegetation
Unknown; improved habitat
conditions due creation of
woody patches in rural
residential areas, but potential
habitat loss when food-rich
farmland is turned into
large-scale tree plantations
Moderate Increasing? Wu et al. ( 2009 )
Rustic Bunting population trends 7
decline in number of Rustic Buntings over the last 10 years ( Table 1 , Figure 1b ). To conclude, both
available standardised data and anecdotal information give unequivocal support for a strong
range-wide population decline in Rustic Bunting over the last decades.
Possible drivers and knowledge gaps
Little is known about the magnitude of the impact of different threat factors and their interactions
with regard to the population decline of long-distance migratory songbirds in the East Asian
Flyway (Yong et al. 2015 ). In Table 2 we have compiled threat factors related to changes in land
use practices, natural processes and persecution that may affect population dynamics in the Rustic
Bunting. To untangle the effects of different threats we need better data on population demo-
graphics. For example, using data modelling Kamp et al. ( 2015 ) concluded that an initial harvest
rate of 2% followed by a 0.2% annual increase was sufficient to produce a population collapse in
the Yellow-breasted Bunting over a time period of 34 years. Currently we do not know to what
extent survival in the Rustic Bunting is affected by habitat change and persecution. Similarly, our
knowledge about the effects of habitat change on Rustic Bunting productivity is limited. Poor
nesting success coupled to habitat loss and degradation could be a population limiting factor, as
has been suggested in case of Jankowski’s Bunting E. jankowskii (Jiang et al. 2008 ) .
Assessment of the impacts of different threat factors is also hampered by our limited under-
standing of the connectivity between breeding and wintering ranges in the Rustic Bunting.
Lightweight, light-level geolocators and stable isotope analysis provide new tools for studying
such questions, but to date they have not been used to any larger degree on migratory songbirds
in Asia (Yong et al. 2015 ). Knowledge about the migration routes and the wintering areas of the
Rustic Bunting will be vital for prioritizing sites for new monitoring schemes in the Far East and
for planning international conservation efforts.
Supplementary Material
The supplementary materials for this article can be found at journals.cambridge.org/bci
Acknowledgements
Jesper Hornskov, Aleksi Lehikoinen, Åke Lindström, Bo Pettersson, Philip Round, Sergei M.
Smirenski, and Terry Townsend kindly responded to personal inquiries and provided population
data. We appreciate the comments from two anonymous reviewers and the associate editor.
Funding was received from Göran Gustafsson Foundation (to LE), the Finnish Cultural Foundation
(to TJ) and the Kempe Foundation (to JMR).
Practice/process Effect on Rustic Bunting
habitat or populations
Estimated
strength of
impact
Trend Reference
Climate change
and unfavorable
weather
conditions
Drought and lowered ground
water table; may change
vegetation structures in
natural grasslands and shrub
habitats
Moderate Increasing Tamada et al.
( 2014 )
Trapping for the
trade market,
private use or
merit release
Communal roosting habits
increase susceptibility to
trapping
Strong
(regionally)
Persisting;
increasing?
Maeda ( 1973 ),
Kamp et al.
( 2015 ), Yong
et al. ( 2015 )
Table 2. Continued.
L. Edenius et al. 8
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LARS EDENIUS * , ADRIAAN DE JONG , JEAN-MICHEL ROBERGE
Department of Wildlife , Fish, and Environmental Studies , Swedish University of Agricultural
Sciences , SE-90183 Umeå , Sweden .
CHANG-YONG CHOI
Department of Forest Sciences , Seoul National University , Seoul 151-921 , Republic of Korea .
WIELAND HEIM
Amur Bird Project , Roseggerstraße 14 , 14471 Potsdam , Germany, and Animal Ecology ,
University of Potsdam , Maulbeerallee 1 , 14469 Potsdam , Germany .
TUOMO JAAKKONEN
University of Oulu , Department of Biology , P O. Box 3000 , FI-90014 Oulu , Finland .
KIYOAKI OZAKI
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Ornithology , 115 Konoyama , Abiko 270-1145 , Japan .
* Author for correspondence: lars.edenius@slu.se
Received 22 September 2015 ; revision accepted 1 February 2016
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