The taxonomic status of Lesser Redpoll Alan G. Knox, Andreas J. Helbig, David T. Parkin and George Sangster' Alan Harris

ABSTRACT Lesser Redpoll Carduelis cabaret has until recently been widely regarded as a subspecies of Common Redpoll C.flammea. In the past, it was geographically isolated from other redpolls during the breeding season, but expansion of its range since the 1950s has brought it closer to nesting Common Redpolls in southern Scandinavia. In 1994, breeding occurred sympatrically without mixed pairs being noted. Lesser Redpoll is diagnosably distinct from all other redpolls, and there are preliminary reports of vo< al molecular and behavioural differences. It is recommended that Lesser Redpoll is best treated as a separate species.

any of the taxa which we currently understanding and application of species regard as subspecies were consid­ concepts, it is now increasingly recognised Mered to be full species in the nine­ that a number of these subspecies would be teenth century, before the concept of more appropriately treated once again as full polytypic species became widespread. The species. Lesser Redpoll Carduelis cabaret (hereafter The breeding range of cabaret encom­ referred to as cabaret), which has until passes Britain & Ireland and countries bor­ recently been widely treated as a race of dering the North Sea from France to Common Redpoll C. flammea, is one such southern Norway, and central Europe (Hage- example. With new data, re-examination of meijer & Blair 1997; fig 1). existing information, and changes in the Populations from these areas winter in

1. On behalf of the Association of European Rarities Committees and the British Ornithologists' Union Records Committee

260 British Birds 94:260-267, June20 2001 Knox et al.: The taxonomic status of Lesser Redpoll

Fig. 1. Breeding ranges in Europe of Lesser Carduelis cabaret. Common C. flammea and Arctic Redpolls C. hornemanni. Modified from Riddington et al. (2000).

Britain and continental Europe, south to the Scandinavia, and commented that, should the Alps. Redpolls were also introduced into two forms come together and fail to New Zealand, and have since colonised hybridise, cabaret would have to be treated nearby islands. The large population there as a separate species. was previously considered, on the basis of appearance, to consist of both cabaret and Differentiation 'Mealy Redpolls' C. f. flammea (hereafter There are clear morphological differences referred to as flammea'), which were said to between cabaret and flammea. With its be interbreeding. Fennell et al. (1985) small size and rich plumage tones, cabaret is showed that, in fact, phenotypic variation dif­ the most distinctive of all the redpoll taxa, fered little from that of British cabaret, apart and the only form that is not liable to be con­ from the frequent occurrence of whiter fused with any other (Knox 1988; Herre- wing-bars.They suggested that this may have mans 1990). In Sweden, the most useful been due to founder effects. characters for distinguishing female and Apart from the enigmatic Icelandic red­ young male cabaret are their smaller size, polls of unknown affinities, cabaret was also, until recently, the only form isolated geo­ the uniform brown colour on the back and graphically from all other redpoll taxa during nape, and the buff flanks and breast-sides the breeding season (Knox 1988). Although which contrast with whitish underparts its allopatric breeding distribution made it (Lindstrom et al. 1984). These morphological difficult to assess the status of the taxon differences are complemented by differ­ under the Biological Species Concept, Knox ences in vocalisations (Herremans 1989) (1988) noted the spread of cabaret towards and, apparently, behaviour (Lifjeld & Bjerke the breeding range of flammea in southern 1996, see page 264). Herremans (1989

British Birds 94:260-267, June20 2001 261 Knox ct al.: The taxonomic status of Lesser Redpoll

148 & 149. Lesser Redpolls Carduelis cabaret, Kent.July 1989.The plumage of both of these birds, prior to the post-breeding moult, is heavily worn, particularly that of the individual below, on which the pale greater-covert wing-bar is almost completely worn away. As a result of feather wear, both look rather pale and bleached, the ground colour of the underparts being almost uniform whitish on the female; the upperparts of both, however, are rather uniform brown.

described the flight-call 'chatter' of cabaret 'dsooee' perching-calls. Glutz von Blotzheim as being higher-pitched and less staccato & Bauer (1997) did not clearly distinguish than that offlammea, and lacking the latter's between flammea and cabaret in their treat­ broad frequency span: 'tji tji tji' in cabaret ment of redpoll vocalisations. Although sono­ and 'che che che' in flammea. There were grams were presented in the account of also subtle, but detectable, differences in the cabaret, some are clearly from vocalisations

262 British Birds 94:260-267, June 2001 Knox et al.: The taxonomic status of Lesser Redpoll David Tipling/'Wmdrush

150 & 151. Common Redpolls Carduelis flammea of mce flammea ('Mealy Redpoll'), northern Finland, March 1999. In fresh plumage, prior to the breeding season, the clean, whitish flanks and generally 'frosty' appearance of Common Redpoll are quite different from those of Lesser Redpoll C. cabaret. David Tipling /Windrush of flammea, and potential differences hornemanni and exilipes), as well as dark and between the taxa were not discussed. pale redpolls from Iceland. This revealed There are also possible molecular differ­ little, if any, differentiation between any of the ences between cabaret and all the other red­ taxa examined, except for cabaret, which dif­ polls. A preliminary molecular study was fered from all other taxa at three apparent made of the feather proteins of flammea, band positions (Knox 1977). In other avian rostrata, cabaret, and the two forms of taxa, such differences occurred only Arctic Redpoll C. hornemanni (nominate between well-marked species (Knox 1980).

British Birds 94:260-267, June20 2001 263 Knox et al.: The taxonomic status of Lesser Redpoll

Geographical distribution for many years in southern Norway (Grimsby In Europe, the distribution of cabaret has & R0er 1992), no sympatry was reported changed dramatically over the last 150 years. until nearly 20 years later. In the mid-1800s, it was confined mainly to northern Britain, Ireland and the Alps, where Sympatric breeding it nested in semi-open woodland, particularly Irruptive breeding finally brought flammea at higher altitudes. By 1910 it had increased into contact with cabaret in southeast in lowland Britain, but its range subsequently Norway in 1994 (Lifjeld & Bjerke 1996). The retracted rapidly, followed by another, more habitat was an area of mixed spruce and determined expansion from the 1950s deciduous woodland on a former clear-fell onwards. From Britain, the distribution of surrounding a farm in 0stfold county, where cabaret soon crossed the North Sea to The redpolls did not normally breed at all. An Netherlands, Germany and Denmark. From abundance of spruce seed early in 1994 the 1970s, cabaret was found in southern attracted large numbers of Common Cross­ Sweden and Belgium, and was first discov­ bills Loxia curvirostra, and led to extensive ered nesting in France in 1983- Concurrently breeding by Siskins C. spinas and redpolls in with this expansion around the North Sea the region. Of 11 redpoll nests found, six coasts, a similar increase was occurring in were of cabaret and five of flammea. Both Central Europe. It first bred in the former members of each pair were seen and posi­ Czechoslovakia in 1952, and now nests in a tively identified, and no mixed pairs were broad belt across the Alps and the Czech detected. With the appropriate permissions, Republic. It has since spread northwards some individuals were collected to confirm through central Germany to meet up with an identification; the specimens have been inland population in the Ardennes, in deposited in the Zoological Museum, Oslo. Belgium (Knox et al. 1997; Ernst 1998). Both redpolls bred throughout the area Although cabaret is still increasing in many studied, with nests of the two forms as little areas, significant reductions have occurred as 50 m apart. There was no apparent spatial recently in Britain, The Netherlands and segregation of the taxa, nor any apparent dif­ Belgium (Knox et al. 1997). ference in the timing of their breeding. All During recent decades, cabaret has con­ the nests were in spruce, apart from one in tinued to increase and spread in southwest Scots Pine Pinus sylvestris. Some differences Sweden (e.g. Gotmark 1978; Lindstrom et al. were noted, although not quantified. The 1984; Ottvall & Raberg 1998) and southern nests of cabaret were mostly well hidden in Norway (e.g. Grimsby & R0er 1992). Gener­ dense conifers, so that twigs had to be ally, flammea breeds a little farther north in moved to see them, while those of flammea Scandinavia, in birch Betula and willow were usually visible from several metres Salix scrub, and open forests of Norway away. Additionally, cabaret also tended to Spruce Picea abies. As such, the breeding nest in denser stands of trees, whereas ranges of the two forms were initially quite several flammea nests were in solitary separate. In years when there is an abundant spruces. There was also a marked difference .seed crop, however, flammea is also an in the behaviour of adults when disturbed at irruptive breeder' (Gotmark 1982), and may the nest: flammea would remain in the nest nest well to the south of its normal breeding tree close to the observer, whereas cabaret range. would fly in circles several metres above the intruder's head. In 1975, confirmed breeding of cabaret in Sweden was recorded for the first time, and Although sympatric breeding by cabaret this coincided with irruptive breeding by and flammea has so far been reported in only flammea. Even so, the two did not quite one season, several pairs of both taxa were come together, since cabaret nested in involved, in close proximity to each other, and coastal pine Pinus plantations and heaths, seemingly without differences in the timing of and flammea bred in inland spruce forests their breeding (Lifjeld & Bjerke 1996).There is (Gotmark 1978). The two forms were effec­ no evidence to suggest that pairing occurred tively isolated by habitat. Although the distri­ before the birds arrived on the breeding butions of cabaret and flammea were close grounds (see Knox & Lowther 2000).

264 British Birds 94:260-267, June 2001 Knox et al Knox.: The c t taxonomical The taxonomic status status of Lesser of Lesser Redpoll Redpoll

The only recorded instance of attempted interbreeding between the two redpoll forms occurred in 1987, onTexel,The Netherlands. Following an invasion of flammea in the previous autumn, a female was found paired with a male cabaret, but the nest was subsequently destroyed (Dijksen 1989). The female was hundreds of kilometres from her normal breeding range. Such circumstances frequently lead to inter­ specific pairings as a result of a lack of con- specific mates, and these events are therefore not particularly significant as indi­ cators of absence of reproductive isolation or specific distinctness. Under Biological, Phylogenetic and Evolu­ tionary Species Concepts, it would therefore seem that the Lesser Redpoll is best treated as a separate species, Carduelis cabaret.

Other redpoll taxa

The affinities of the pale and dark redpolls Roger Riddington which breed in Iceland are uncertain. The (unnamed) pale birds resemble Arctic 152. First-winter Lesser Redpoll Carduelis cabaret, Fair Isle, Shetland, September 1997. Redpoll of the race exilipes, while the dark Compared with the adults in plates 148 & 149, individuals (islandica) are similar to 'Greater this first-winter is much darker and more warmly Redpoll'C.f.rostrata (Knox 1988;Herremans coloured; the nape and mantle are uniformly 1990). Leaving these two forms aside, the dark, rich brown, while the flanks are strongly status of the remaining redpoll taxa is also washed with buff. controversial. Opinion varies between one and four species. The usual treatment (fol­ • 'Greater Redpoll'C.f.rostrata (Arctic: lowing Molau 1985 and Knox 1988) is to Canadian islands & Greenland) recognise two species: Arctic Redpoll C. hornemanni, comprising • 'Coues's Redpoll' C. h. exilipes (circum- Common Redpoll C. flammea, comprising polar in low Arctic) • 'Mealy Redpoll' C.f. flammea (circum- • 'Hornemann's Redpoll' C. h. hornemanni polar in low Arctic) (Arctic: Canadian islands & Greenland) Roger Riddington

153. First-winter Lesser Redpoll Carduelis cabaret (left) and first-winter Common Redpoll Carduelis flammea of race rostrata/islandica ('Greater Redpoll', right), Fair Isle, Shetland, October 1997. The difference in size between these two species is striking when they are photographed side by side.

British Birds 94:260-267, June 2001 265 Knox et al.: The taxonomic status of Lesser Redpoll

The two races of each species are Redpolls looked for genetic variation within allopatric, although each is widely sympatric and between the redpolls by comparing the with one race of the other species. Thus, patterns of mitochondrial DNA (mtDNA) over considerable areas, flammea is sym­ fragments (the Restriction Fragment Length patric with exilipes and rostrata is sympatric Polymorphism haplotypes) that are obtained with hornemanni. The conventional treat­ when DNA from different individuals is cut ment assumes the following relationships: with the same enzymes (Seutin et al. 1995). Seventeen haplotypes were found in 31 indi­ f. flammea and rostrata are each other's viduals examined. One haplotype occurred closest relatives, rostrata being larger, in all the taxa (14 individuals), and the others longer and darker than flammea. (almost all single-site differences) were rep­ 2. exilipes is most closely related to horne­ resented in single individuals in all but one manni, which is larger, longer and paler case (two individuals).The pattern of mtDNA than exilipes. divergence was unrelated to geographical or traditional taxonomic relationships, and the An alternative viewpoint might be that differences were slight compared with those the morphological and plumage similarities between typical sister species (Seutin et al. are due to convergence. Therefore, exilipes 1995). Possible explanations for this lack of might just be a pale relative of flammea, and differentiation between the Common and hornemanni a pale relative of rostrata (Her- Arctic Redpolls include the very large effec­ remans 1990). Could the shared plumage tive population sizes, the nomadic breeding characters of exilipes and hornemanni be systems and the recent divergence of the due simply to their more northerly distribu­ named taxa. Further molecular studies of this tion and more terrestrial behaviour? Such group are required. reasoning would suggest that flammea, In the meantime, it is recommended that exilipes, rostrata and hornemanni would be the redpolls be treated as three species: best treated as four separate species (Herre- Common Redpoll C. flammea (including C.f. mans 1990).There is, however, a general ten­ rostrata and C.f. islandica),kvctic Redpoll C. dency for the closest relatives of any taxon hornemanni (including C. h. exilipes) and to be allopatric. This, and the plumage simi­ Lesser Redpoll C. cabaret (monotypic).These larities, would suggest that the conventional recommendations are made on behalf of the treatment of the various species and races is Association of European Rarities Committees more likely to be correct. and have been adopted by the British A study of Common, Arctic and Lesser Ornithologists' Union Records Committee. Tim Loseby

154. Common Redpoll Carduelis flammea of race rostrata/islanciica ('Greater Redpoll) Fair Isle

Shetland, September 1997. .;...•—••

26 6 British Birds 94:260-267, June 2001 Knox et al.: The taxonomic status of Lesser Redpoll Tim Loseby

155. Arctic Redpoll Carduelis hornemanni, Fair Isle, Shetland, September 1987.

Acknowledgments ecology in the taxonomy of crossbills and redpolls. PhD thesis, University of Aberdeen. We are grateful to members of the BOURC and its — 1980. Feather protein as a source of avian Taxonomic Sub-committee for comments. taxonomic information. Comp. Biochem. Physiol. B. 65:45-54. References — 1988.The taxonomy of redpolls. Ardea 76:1-26. Dijksen, L. J. 1989. Broedpoging van een gemengd paar — & Lowther, R E. 2000. Common Redpoll (Carduelis van Kleine Barmsijs Carduelis flammea cabaret en flammed). In PooIe.A., & Gill, F. (eds.), The Birds of Grote Barmsijs C.f.flammea.Limosa 62:48. North America, No. 543. Philadelphia, PA. Ernst, S. 1998. Die Birkenzeisige. Klingenthal. — Nystrom, B., & Nystrom, H. 1997. Carduelis FennellJ. F. M., Sagar, P. M., & FennellJ. S. 1985 .Variation flammea Redpoll. In Hagemeijer.W J. M., & Blair, M. within the Redpolls of Canterbury. Notornis 32: J. (eds.), The EBCC Atlas of European Breeding 245-253. Birds: their distribution and abundance. London. Glutz von Blotzheim, U. N., & Bauer, K. M. 1997. LifjeldJ.T., & Bjerke, B.A. 1996. Evidence for assortative Handbuch der Vogel Mitteleuropas. Vol. 14: 801- pairing by the cabaret And flammea subspecies of 887. Wiesbaden. the Common Redpoll Carduelis flammea in SE Gotmark, F. 1978. Grasiskan Carduelis flammea - en Norway.Fauna norv.Ser.C, Cinclus 19:1-8. expanderande hackfagel i sydvastra Sverige. Vdr Lindstrom, A., Ottosson, U., & PetterssonJ. 1984. Sydlig Fagelvarld 37:133-135. grasiska Carduelis flammea cabaret i Sverige samt — 1982. Grasiskans Carduelis flammea forekomst i forslag till kriterier for rasbestamning. Vdr sodra Sverige under "sydhackningsaret" 1975. Vdr Fagelvarld 43: 525-530. Fagelvarld 41:315-322. Molau, U. 1985. Grasiskkomplexet i Sverige. Vdr Grimsby, A., & RoerJ. E. 1992. Innvandringen av liten Fagelvarld 44:5-20. grasisken Carduelis flammea cabaret til Norge Ottvall, R., & Raberg, L. 1998. Den sydliga grasiskans 1962-1991. Fauna norv.Ser.C, Cinclus 15:17-24. (Carduelis flammea cabaret) etablering i Skane. Hagemeijer.W J. M„ & Blair, M. J. (eds.) 1997. The EBCC Anser 37: 225-230. Atlas of European Breeding Birds: their Riddington, R.,Votier, S. C, & Steele,J. 2000.The influx distribution and abundance. London. of redpolls into Western Europe, 1995/96. Brit. Birds Herremans, M. 1989. Vocalizations of Common, Lesser 93: 59-67. and Arctic Redpolls. Dutch Birding 11:9-15. Seutin, G, Ratcliffe, L. M., & Boag, P. T. 1995. — 1990. Taxonomy and evolution in Redpolls Mitochondrial DNA homogeneity in the Carduelis flammea-hornemanni; a multivariate phenotypically diverse redpoll finch complex (Aves: study of their biometry. Ardea 78:441-458. Carduelinae: Carduelis flammea-hornemanni). Knox, A. G. 1977. Feather keratins, morphology and Evolution 49:962-973.

DrAlan Knox, Historic Collections, University of Aberdeen, King's College, Aberdeen AB243SW Dr Andreas Helbig, Vogelwarte Hiddensee, Universitdt Greifswald, D-18565 Kloster, Germany Prof. David Parkin, Institute of Genetics, University of Nottingham, Queen's Medical Centre, Nottingham NG7 2UH George Sangster, President Steinstraat 3A, 2312 ZP Leiden, The Netherlands

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