Within the strongly polytypic Red Crossbill L. curvirostra there are many ... 1959, Phillips 1974, Monson & Phillips 1981, Groth 1984 (quoted by Payne 1987), ... bill. The taxonomic status of this bird has been uncertain from the time it was.
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The sympatric breeding of Common and Scottish Crossbills Loxia curvirostra and L. scotica and the evolution of crossbills ALAN G . KNOX Technical Centre, Buckinghamshire County Museum, Tring R o a d , Halton, Buckinghamshire HP22 5PJ Submitted 15 December 1988; accepted 23 February 1989
Within the strongly polytypic Red Crossbill L. curvirostra there are many reports of two or more ‘subspecies’nesting sympatrically, without interbreeding. This 13-year study examines one such case, in Scotland, where an endemic form is resident and another was thought to occur after irruptions from its main range in continental Europe. Both forms were present in the study area every year; sympatric breeding was proved in 9 years and probably occurred in the other four. There was no suggestion of interbreeding and the Scottish form should be treated as a separate species, L . scotica, the Scottish Crossbill. This is the only endemic species of bird in Britain and one of very few European endemics. The evolution of crossbills in Europe is discussed in the light of recent palynological evidence and the taxonomic status of the Parrot Crossbill L. pytyopsittacus is re-examined.
T h e Red Crossbill Loxia curvirostra is widely distributed throughout the holarctic coniferous forests. T h e species is strongly polytypic, although many of the subspecies have only poorly defined breeding ranges. T h e main intraspecific variation is associated with bill-size and shape. Crossbills eat the seeds of coniferous trees and very little else, and the shape of their bills is correlated with the hardness of the cones of the main tree species on which they feed (Lack 1944a, 1944b, Benkman 1987, Massa 1987). T h e cone crops of many conifers vary considerably from year to year and, in seasons when the developing crop is poor, many or all the crossbills in a particular area erupt, sometimes travelling several thousand kilometres before settling (Newton 1970). T h e birds may then breed in their new area for one or more seasons before moving again. This irruptive behaviour has given rise to a widespread belief that the birds are nomadic and that the population is panmictic (Buckley 1987). I would, however, suggest that some erupting crossbills, or their offspring, may subsequently return to the original ‘core’ breeding areas from which the birds erupted, thus permitting the development of local adaptation and geographic variation. There have been many reports of two or more ‘subspecies’ of crossbills breeding alongside one another, apparently without hybridizing (e.g. Griscom 1937, Kemper 1959, Phillips 1974, Monson & Phillips 1981, Groth 1984 (quoted by Payne 1987), Peterson 1985, Groth 1988). Such evidence would often be taken to indicate that separate species were involved. This was never considered satisfactory with the crossbills (e.g. Griscom 1937, Groth 1988), for the differences between the ‘subspecies’ were slight and the birds were thought to be only temporarily sympatric following irruptions. Particularly interesting circumstances surround the case of the Scottish Crossbill. The taxonomic status of this bird has been uncertain from the time it was originally described as L. curvirostra scotica in 1904 (Hartert 1904, Knox 1975). Since it was believed to be intermediate between the smaller Common Crossbill L . c.
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curvirostra and the larger Parrot Crossbill L . pytyopsittacus, the Scottish Crossbill was in turn placed as a subspecies of one or the other as opinion changed, often for no obvious reason (Knox 1975). A study of museum specimens suggested that scotica’s affinities probably lay with curvirostra but was unable to suggest how closely the taxa were related (Knox 1975, 1976). Common Crossbills were known to irrupt into the range of scotica and probably to remain there for one or more seasons. This was similar to the reports of the sympatric occurrence (and breeding-but not interbreeding) of ‘subspecies’ in other parts of the crossbill’s range. As such behaviour is apparently contradictory to usual patterns of bird population structure, some aspects of the breeding distribution and ecology of crossbills were studied in the field in Scotland during the 1974 to 1986 breeding seasons. Throughout, unqualified reference to curvirostra is intended to mean the nominate subspecies (also known as the Common Crossbill). Binomials are used where the species is being discussed.
Study area and methods T h e core study area (Fig. 1) comprised the valley of the River Dee and its tributaries in northeast Scotland, Less frequent visits were made to the woods in or near lowland Aberdeenshire and the upper stretches of the River Don. Casual data from adjoining regions are included. T h e coniferous forests of middle and upper Deeside can be grouped into six major blocks: Glen Dye, Finzean (including Birse), Glen Tanar, Glen Muick, Ballochbuie-Invercauld and Mar. Scots pine Pinus sylvestris dominates in the large areas of native Caledonian pine forest (Steven & Carlisle 1959) which still exist at Glen T a n a r , Ballochbuie and Mar. These woods contain many trees over 200 years old although, in Mar especially, there has been little regeneration since the early years of the last century. Elsewhere in the northeast, the woods are generally of more recent origin, most of them planted. There are large areas of Scots pine, larch Larix spp., Norway spruce Picea abies, Sitka spruce Picea sitchensis, Douglas fir Pseudotsuga menzzesii and other introduced species, in stands of varying age and extent. Some of the older stands, especially of Scots pine and larch, were planted more than 100 years ago. I n each of the years 1974-1986 an attempt was made to determine the identity (Knox 1990) and approximate distribution of crossbills within the study area. Visits were made to coniferous forests in Deeside and other parts of the northeast between January and June each year. T h e number of visits and their timing varied from year to year. T h e primary objectives were to locate crossbills, identify them and determine whether or not they were breeding. From previous records and experience it was known that most of the local crossbills were in the large, mature forests in Deeside, and these were visited in most years. Other coniferous woods were searched as well. These were identified from the 1 :63,360 Ordnance Survey maps and, in the years of this study, most were covered several times. Many were unsuitable for crossbills, being too small in area or too young to produce a good cone crop, and only rarely were birds found in them. Reports of crossbills which were sometimes received from birdwatchers were investigated where possible. Some records by other observers are included in the results that follow. Apart from my own data, the only records used here are those where t h e birds were considered to have been reliably identified, or where breeding was unequivocally determined as having occurred locally. None of these records by other observers is critical to the discussion. Apparent slight differences between the results presented here and those in Knox (1987) are due to minor changes to the way the sites were grouped. I n the present paper, proof of breeding is also more strictly defined. Breeding crossbills can be difficult birds to work with in the field. Although sometimes readily located, they are frequently few in number, widely dispersed and hard to find (see Nethersole-Thompson 1975). N o British passerine spends more of its time in the high forest canopy, and crossbills rarely descend to sites convenient for trapping. Their presence in a wood was established by searching for cones from which seeds had been extracted, and by listening for calls or the sounds of feeding birds. Crossbills in Scots pine were only occasionally found by sight alone, although on calm days cast-off seed-wings might be seen fluttering down in the sunlight. Crossbills feeding in larch could sometimes be located visually during winter, when the branches were bare of leaves.
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Figure 1. (a) Location of the main study area (box) in northeast Scotland. The rivers shown are (clockwise): the Spey, Deveron, Ythan, Don and Dee; the broken line is the Aberdeenshire county boundary. Land over 150m a.s.1. is shaded. The inner box is 100 km by 50 km. (b) The core study area (the valley of the River Dee) and the valley of the River Don, showing the main areas in which crossbills were found. Only forests where birds occurred on four or more years between 1974 and 1986 are shown.
Early in the breeding season, feeding crossbills remove cones to extract their seeds (Knox 1987). When the forest is quiet, the sound of cone scales being split by the birds can be heard from some distance, although it must be distinguished from a similar noise made b y red squirrels Sciurus vulgaris gnawing cones. When crossbills have finished with their cones (see Benkman 1989), they are dropped. A single bird may handle more than a hundred in a day, so signs of their activity quickly accumulate. Cones which have been extensively worked on by crossbills are unmistakable (Campbell 1973; see Robertson 1954, for differences between ‘woodpeckered’ and ‘crossbilled’ cones).
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Towards the end of winter and the start of spring, the scales on mature pine cones begin to separate, allowing the seeds to fall out. Crossbills still take cones to perches to feed on them b u t they damage the cone scales less than when they were tightly closed. When the cones open more, the birds may not split any of the scales at all. Such cones are then recognizable by the small indentations made by the tip of the lower mandible on the outer side of some of the scales, and the condition of the torn stump (Knox 1987). Ultimately, the birds extract the seeds from between the open scales as the cones hang on the trees. Careful searching at this time often reveals occasional, new, worked cones on the ground. When fewer cones were being dropped, it u’as more important to try to find the birds by listening for calls. Crossbills can be very quiet for long periods, particularly if feeding or resting. ‘Crossbilled’ cones dropped on the forest floor could be dated by their state of weathering and the freshness of the torn stumps. It was usually possible to estimate the period during which crossbills had been present, in classes representing hours (bright, unweathered cones, and fresh stumps with green cambium), days (stump surface shrivelling, but still showing some green), weeks (no green on the stump; fresh cones only starting to weather), months (well weathered cones) or even years in the past. T h i s information, together with visual estimates of the numbers of worked cones at each stage of weathering, permitted the recent history of crossbills in each wood (approximate numbers and period of occupation) to be ascertained. T h e presence of only a few birds and/or a brief stay by the birds could have been overlooked during a short search When recently ‘crossbilled’ cones were found, an effort was made to locate the birds. T h i s was usually done by listening for calls, or waiting at a tree where birds had been feeding in the previous few hours. Once found, the birds were identified where possible by call, or by sight, using a telescope. In recent years, tape recordings were often made for later analysis to confirm identification. When birds were located, after a short period of observation it was usually possible to tell from their behaviour whether they were likely to be going to breed, or were already breeding, even if no nest was found (Table 1). Only recently fledged young (Table 1 (7)) with uncrossed bills and short tails could be taken as confirmation that the birds had bred nearby, as crossbills may erupt while still in juvenile plumage (e.g. Davis 1963). Likewise, adults with well-fledged young which they are still feeding do not constitute proof of local breeding, as the young continue to be fed for several weeks after leaving the nest. Nevertheless, over the period of the study, no juveniles were ever found between January and June in a forest where breeding was not known to have taken place. During this study breeding was considered proved if an occupied nest was found, copulation between members of an established pair was seen, or following observations 5-7 in Table 1. Nearly all cases of proved breeding were based on nests or recently fledged young
Results T h e rate of contact with crossbills during this study was often very low. Many days could pass with only fleeting glimpses of birds or distant calls being heard. Whole days were spent without hearing a single bird, even in forests where crossbills were known to be present. For these reasons, and considering the size of the area being covered, the data are less complete than was desired. Scottish Crossbills were proved to breed in Deeside in each of the 13 years of this study (Table 2). Common Crossbills were also present every year, sometimes in the same woods. Breeding of Common Crossbills took place in Deeside within the known range of the Scottish Crossbill in 9 of the 1 3 years. There were no reasons to believe that Common Crossbills had not nested in the 4 remaining years of the study (1980,1982,1985,1986).These were years during which only a short time was spent in the field at the appropriate stage of the breeding season. In 2 of these 4 years (1985, 1986), Common Crossbills were proved to breed in woods nearby. Between 1974 and 1985, Scottish Crossbills were confined to the valley of the River Dee and its tributaries between Glen Dye and Glen Derry (Mar). In 1986, a few Scottish Crossbills were also found early in the season in company with some Common Crossbills in a mixed flock in a wood outside Deeside, in Strathdon. T h e birds showed no signs of breeding activity.
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Table 1. Partial sequence of the behaviour of crossbills in Scotland, awayfrom the nest, before, during and after breeding
Observation
Interpretation
Adult birds, most or all in flocks.
Breeding not yet started.
Most or all birds in flocks, but some obviously Birds starting to form pairs. paired. Pairs occasionally leave flock, but return later, Pairs possibly looking for place to nest, or probably from roughly the same direction. starting nest building. Pairs settled, scattered through forest. (There may Pairs on ‘territories’. also be one or more flocks in the forest, if it is large enough.) Single males seen scattered through forest; few or Females on nests, males feeding them at the no females found. T h e males may gather in groups nest. to feed together. Whether alone or in a flock, many or all males depart (singly, if feeding in a group) every hour or so, returning about 1-5 mins later from the same direction. Males and females feeding together, nearly all the Young in the nest. time spent feeding. Both depart regularly and return a few minutes later from the same direction. a. Males, females and recently fledged young seen Birds bred nearby.
together, or b. males and recently fledged young seen together, Birds bred nearby, females probably on no sign of females. second brood. Flocks of all ages and both sexes seen.
If the young are long fledged, they may not have bred locally.
Between 1974 and 1986, Common Crossbills were regularly found in some of the middle Deeside forests, where their range overlapped that of the Scottish Crossbill. In 7 years, both Common and Scottish Crossbills occurred in Glen Dye. Common Crossbills also occurred in the woods of lowland Aberdeenshire, where the Scottish Crossbill was never found. Throughout the northeast of Scotland the numbers of Common and Scottish Crossbill varied from year to year. In particular, Common Crossbills were very common just after large irruptions, becoming generally less so over the following seasons, until the population was again supplemented by immigrants. Neither species was ever rare.
Discussion Crossbills, sometimes reported as Common or Scottish but usually unidentified, have been recorded in northeast Scotland for at least two hundred years (Knox in press). Until the start of this study in 1974 no breeding birds had been identified, although it was suspected that those in upper Deeside were scotica (Watson 1955, Darling & Boyd 1969) and that curvirostra was also present in many years (V. C. Wynne-Edwards pers. comm.). Prior to 1974, there were no satisfactorily documented records of Common Crossbills breeding anywhere within the range of the
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SYMPATRIC BREEDING AND EVOLUTION OF CROSSBILLS
Table 2.Distribution of crossbills in northeast Scotland between January and June, 197g-1986. Only sites where birds were present in four or more years are listed. The localities are shown in Fzg. l a t 3b. Sjs, Scottish Crossbill L o x i a scotica; Cjc, Common Crossbill L. c u r v i r o s t r a ; Xjx, unidentified crossbills; upper case, breeding proven; lower case, breeding not proven. Further details and notes are given below
Forest or locality (a) A w a y f r o m Deeside Deer (north) Deer (south) Kirkhill Monymusk west Midmar Candacraig (b) DPeride Brathens (Banchory) Blackhall lower Glen Dye upper Glen Dye Finzean Birse northeast Glen Tanar Glen Tanar (main) Dinnet Davan Logie-Coldstone lower Glen Muick upper Glen Muick Abergeldie Ballochbuie east lnrercauld west lnrercauld Mar (north and east) Mar (south) Mar (west)
1974
3975
1976
X
x
1977
1978
C C
C C C C c
C
x
1979 1980 1981
x X x
C
SC x x X S
x x S
X
sc C SCX
C
c
x
x sc
c x
x
x
x
x
x s
X
S
S
x
x
s
X
S
SX
X
X
S
x
X
S
S 9
S
s x
s
s
S
c
X
C
x
x
C
x S
s S x x s
X
x s
SCX c C x
s S S
x
C C
C
x s S x
c
x x C x
c
Sc
s c C
s
X x x x
S x
s
s
x
x
sc
X
x
S
S x
S x x x
sc
S
S
x
x c x
s S s
x
7 .
S
X S
x
s
S
S
x
x
S x
x S
s
s
s
S
5
s
x X
X
X x x
c
sc
S
X
x
X
c C
X
X
X
X
x C
x
C X
19x6
C
C
X
SC
x
x
x
C
1982 1983 1984 1985
x
s
1971: Identification of Scottish Crossbills in Glen Tanar and Common Crossbills in Glen Dye confirmed hy birds in the hand. 1975: In lower Glen Dye scotica and curvirostva drank together at a barn gutter during February and March. 'l'he two bred within 1 km of each other, and several (both species) trapped and ringed. In late May, many pairs of Common Crossbills in upper Glen Dye. Scottish Crossbill nest found there in early June, within 150 m of a recently fledged brood of curvirostra. 1976. Identification of Scottish Crossbills in Glen Tanar confirmed in the hand. O n 8 July at least one Common Crossbill heard in Glen Tanar, and one handled later that day. 1977: Scottish Crossbills hred in a number of woods in Glen T a n a r (identification confirmed in the hand). Common Crossbills bred at several sites in Glen Dye. About thirty birds reported from the Forest of Deer (not searched in previous years) in August 1976. These later determined to be curzrirostra. 1978: Following irruption in late 1977, crossbills present at a number of sites out of Deeside in 1978; identified birds all curoirostra. 1979: A dead, full-grown juvenile Scottish Crossbill found in Glen Muick in August. 7Y8I: Scottish Crossbills alsobredat Potarch, near Finzean. Several Scottish and Common Crossbills trapped in lower Glen Dye. 1982: Common Crossbills found in lower Glen Muick, near a pair of nesting srotica. A pair of Scottish Crossbills seen courtship feeding in Glen Dye, near an apparently established pair of Common Crossbills. 198.3: Scottish Crossbills also bred in Glen Cat (between Finzean and Glen Tanar). 1984: Common Crossbills also hred at Durris. Dead Common Crossbill found at Banchorl- (April). Common Crossbills bred near the Forest of Deer, and at Clashindarroch (near Huntly). 1985: Finzean not searched (important part recently clear-felled). Dead Common Crossbill received from Ranchory (Januar)). 1986: A late season. Mixed flock of Common and Scottish Crossbills present in Forest of Birse. Irruption noted at Loch of Strathbeg in June.
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Scottish Crossbill. This study has established that Common and Scottish Crossbills both nest regularly in the forests of northeast Scotland.
The past distribution of the Common Crossbill in northeast Scotland T h e slender bill of the Common Crossbill is said to be particularly well adapted for feeding on the weak cones of spruces rather than the hard cones of pine (Lack 1944a, 1944b). Since the only conifers native to Britain are the Scots pine and the juniper Juniperus communis, the nesting of Common Crossbills might not have occurred until introduced trees started to bear cones, but this seems unlikely. Common Crossbills frequently breed in pine woods in England (Witherby et al. 1938, Lack 1944a), where the birds are even capable of feeding on the unripe, hard, green cones of the Scots pine (Southern 1945). In Fenno-Scandia, Common Crossbills feed (Haapanen 1966, Pulliainen 1974) and nest (von Haartman 1969) in pines, although breeding in spruce is more common. In the Netherlands, breeding has taken place for several years in woods dominated by Scots pine (Bijlsma 1982), a species also used widely in the Pyrenees ( G h a r d & Lescourret 1987, and refs therein). Recently, Common Crossbills have nested for a number of seasons in Scots pine forests in northeast Scotland. Although these have always been plantations, many originated from native seed. The planting of woods and smaller stands of trees in the policies of Scottish country houses has been taking place for at least five hundred years. Larch was first planted in Scotland in the 1600s, and was used on a large scale from the middle of the following century. Norway spruce was first planted over large areas a little earlier than this (Anderson 1967, Davies 1979). As the areas of plantation increased and as these trees matured, it seems likely that the nesting of the Common Crossbill in Britain became more common. T h e first recorded irruption of Common Crossbills into Britain was in 1251 (Paris, quoted by A. Newton 1896) and, since 1800, there have been frequent irruptions into southwestern Europe. In the 1830s alone there were seven irruptions in as many years. Rarely did more than three or four years elapse between consecutive invasions (I. Newton 1972). Not all of these movements necessarily reached northeast Scotland, although other irruptions which were not recorded probably took place. T h e invasion of the northeast by Common Crossbills undoubtedly was, and still is, a common event. Common Crossbills have been found throughout Great Britain (Sharrock 1976, Knox 1986). Although the Scottish Crossbill was not described until the start of the present century, records of crossbills breeding in England and southern Scotland since at least the early 1800s (Witherby et al. 1938) may safely be assigned to the Common Crossbill. No specimens of scotica are known to have been collected outside the Scottish Highlands (Knox 1975), and the Parrot Crossbill was not known to breed in Britain until the 1980s (Knox 1986). T h e identity of some of the old records of Common Crossbill has been confirmed by birds that were shot and are still available in museums. There are also a number of 19th century museum specimens of curvirostra taken in the Highlands between January and May, although all the skins examined lack conclusive breeding data. From the late eighteenth century, birds believed to be Common Crossbills have occurred in lowland northeast Scotland where they were often proved to nest (Knox in press). Common Crossbills now breed widely in Scotland (Sharrock 1976, Knox 1986), and it seems that it was only the difficulty of separating Common and Scottish Crossbills in the field that prevented the earlier realisation that they nested alongside one another.
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The past distribution of the Scottish Crossbill Over the past two centuries for which there are records of crossbills, the ancient Caledonian pinewoods in northeast Scotland never extended beyond middle and upper Deeside. T h e main clearances of the native woods came to an end by the early nineteenth century (Steven & Carlisle 1959) although, even then, broad tracts of large pines still remained (Robson 1819). An increase in the numbers of red deer Cervus elaphus in the late eighteenth century led to heavy browsing on young trees and, in some woods, there has been little natural regeneration since about 1820 (Watson 1983). There are individual trees in some of the pinewoods dating back to the middle seventeenth century (Steven & Carlisle 1959), but the large pines which Robson (1819) described in upper Deeside are now gone, their place having been taken by trees which germinated mainly between 1760 and 1820 (Steven & Carlisle 1959). Despite the forest clearances, continuous, mature pine forest has therefore existed in several areas of Deeside for a considerable period. It seems reasonable to assume that the habitat requirements of the Scottish Crossbill have not altered to any great extent in the last two hundred years, and that scotica has been present more or less continuously in the old pinewoods of middle and upper Deeside over this period (Knox in press). They were probably not found in the lowland woods of the northeast: Scottish Crossbills did not occur there during the present study, even in years with good cone crops when Common Crossbills were scarce or absent. Recent competition with the Common Crossbill is therefore unlikely to be the sole factor keeping Scottish Crossbills from these woods.
Sympatric breeding Rather than being an infrequent and biologically unimportant event, Common Crossbills are now known to breed regularly within the range of the Scottish Crossbill in some numbers. They have shown themselves able to breed in pine woods in Scotland and elsewhere. Common Crossbills have been invading the British Isles for at least 700 years, and have been nesting in other parts of England and Scotland since at least the early 1800s. There is no reason to believe that sympatric breeding has occurred only recently. If Common Crossbills had not bred widely in the Highlands prior to the introduction of exotic conifers, the most likely reasons would have been because they had been prevented from doing so by scotica, or because the old Scottish pine woods were largely unsuitable. In either case, the two forms of crossbill would have been behaving as good species (Mayr 1963). If any exclusion only started to break down following the widespread planting of coniferous woods by man, then the Common Crossbill could still have been breeding throughout the range of the Scottish Crossbill for hundreds of years. Despite their sympatry, there is no evidence that Common and Scottish Crossbills interbreed. There have been no reported cases of mixed breeding pairs, although they would be difficult to detect anyway, because mated birds often differ noticeably in bill structure (wide variation is found within both species (Knox 1990)). Nevertheless, careful examination of many breeding birds during this study revealed no mixed pairings. There is a further, indirect reason to believe that hybridization does not occur to any significant degree. T h e total population of the Scottish Crossbill has been estimated at only 1500 adults at the start of a good year (Nethersole-Thompson 1975). Fewer than 100 pairs may have nested during a population crash in the 1960s (Nethersole-Thompson 1975). As has been shown, the opportunity for hybridiza-
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tion has been present for some time. Often, the numbers of nesting Common Crossbills must have greatly exceeded those of the resident form. Unless interbreeding is absent or rare, or selection is strong, the characters of the Scottish Crossbill would rapidly have been swamped by gene flow from the immigrants (WynneEdwards 1948).
The taxonomic status and relationships of the Scottish Crossbill With Common and Scottish Crossbills breeding sympatrically, apparently without hybridization, it seems inappropriate to regard scotica as a subspecies of L . curvirostra. Since the time of Hartert there have been suggestions that scotica should be treated as a subspecies of the Parrot Crossbill (Hartert & Steinbacher 1932, Meinertzhagen 1934, B.O.U. 1956). However, scotica appears to be closer in morphology to curvirostra than to pytyopsittaczrs (Knox 1975,1976), although there are vocal similarities between scotica and the latter (Knox unpubl.). As scotica and curvirostra seem to be reproductively isolated, the morphological differences between scotica and pytyopsittacus would suggest that they, too, would not interbreed, and that they should be regarded as separate species. It seems that, in this case, the apparent problem with sympatrically breeding subspecies may be resolved, in as much as the Common, Scottish and Parrot Crossbills comprise one of the more poorly differentiated groups of sibling species of birds. T h e Scottish Crossbill is the only species of bird endemic to Britain.
The Western Palearctic crossbills The ability to exploit hard pine cones efficiently has evolved a number of times in crossbills, leading to several named taxa characterized by heavy bills, including L . pytyopsittacus and L . scotica in northern Europe, L . c . corsicana, L. c . poliogyna and L . c. guillemardi in the Mediterranean (Massa 1987), L . c . mesamericana in central America (Howell 1972) and even L . leucoptera megaplaga in Hispaniola (Wetmore & Swales 1931). Feeding on pine, which cones more reliably than spruce (e.g. Reinikainen 1937, Hagner 1965), would have allowed the persistence of small, sedentary populations where differentiation would have been more likely to occur. The large-billed forms in the western palearctic are distributed in a discontinuous arc around the northern, western and southern edges of the region. T h e relationships of these birds to one another are not understood. NethersoleThompson (1975) and Murray (1978) have proposed that Scottish and Parrot Crossbills evolved from a common ancestor that became isolated in pines in western Europe during the last glaciation. At that time, Norway spruce, the preferred habitat of the Common Crossbill, did not occur in significant quantities in the boreal forest west of the Urals (Peterson 1983, Huntley 1988). As the ice retreated, NethersoleThompson and Murray believe that a population of large-billed crossbills followed the pine forests northwards into Britain and Fenno-Scandia, whereupon they became isolated from one another and evolved their present characters. T h e large size of the Parrot Crossbill may have come about through character displacement following sympatry with curvirostra, when the latter moved into northern Europe with the advancing spruce. A portion of the original large-billed population may have remained in the Mediterranean and from it the present-day large-billed Mediterranean forms may have evolved (Murray 1978). T h e suggestion is, therefore, that the large-billed European and North African crossbills are all more closely related to each other than any one of them is to the Common Crossbill. This hypothesis seems unlikely for the following reasons:
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(1) Massa (1987) has demonstrated a cline of plumage characters between curvirostra in northern Europe and some of the named Mediterranean taxa. Males, in particular, are less intensely coloured in the south. However, the trend conforms with Gloger’s Rule, from which we might expect paler plumages in crossbills from more arid climates. Although this may be partly genetic, it is known that diet (and possibly hormonal condition at the time of the moult) has a profound influence on pigmentation in these birds (pers. obs.). T h e cline in colour saturation may have an environmental component, as might the similarity in the plumages of some of the Mediterranean populations. (2) As heavier bills have evolved several times throughout the world in pine-feeding crossbills, it seems more likely that the western palearctic large-billed populations each arose separately. Differentiation following independent colonization by irrupting Common Crossbills could have led to the populations now found on some of the Mediterranean islands and in North Africa. (3) T h e pollen record does not lend strong support to Nethersole-Thompson’s and Murray’s proposals, either. Contrary to earlier belief, there is now evidence that pine forest remained through the Holocene in parts of the area currently occupied by I,. pytyopsittacus (Huntley & Birks 1983, Peterson 1983, Huntley 1988). T h e Parrot Crossbill may have evolved not far from where it is now found. Its range broadly coincides with the main areas of boreal forest dominated by Scots pine and Norway spruce. Further south and west, mixed deciduous forest becomes commoner. T o the east, beyond the Urals, Siberian stone pine Pinus sibirica and other conifers dominate (Peterson 1983, Knystautas 1987, Huntley 1988). Thus, although the Scots pine has the widest geographic range of any plant in Eurasia, the restricted distribution of the Parrot Crossbill may, perhaps, be explained. No other bird has a present distribution pattern similar to that of the Parrot Crossbill (Voous 1960). (4) Evidence is growing that pines survived the last glaciation in southwest Ireland and off northwestern Scotland (Huntley & Birks 1983, Kinloch et al. 1986, Huntley 1988). Palynological data have shown that the Forest of Caledon was developing strongly long before pines crossed the English Channel into southern England in any numbers (Huntley & Birks 1983). T h e northwards migration of Scots pine from southern Europe after the last glaciation was interrupted and reversed before it reached the Highlands, although trees from the south may have reached within 150 km of the native pines (Huntley & Birks 1983, Kinloch et al. 1986).
It is possible that the Scottish Crossbill evolved within, or not far from, the species’ present range. T h e Scottish refuge may not have contained many trees (Kinloch et al. 1986), and the small area(s) of habitat would have supported only a limited population of birds. This would have increased the likelihood of rapid speciation. T h e persistence of the population during the time required for speciation would only have been possible if the food (pine) was relatively reliable (see above). A recent electrophoretic study of North American cardueline finches (including Loxia) suggested that most speciation events in this group took place between 4 million and 500,000years ago (Marten & Johnson 1986; but see also Knox 1988). If these timings are correct, the speciation of scotica since the late Pleistocene or early Holocene would seem exceptional. Although the time of divergence is not known precisely and there are often doubts about the calibration of molecular clocks, the Scottish Crossbill may be an unusually young species. For reasons largely associated with the glacial history of the continent, less than a dozen species of birds are currently recognized as being endemic to Europe: Red-
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legged Partridge Alectoris rufa, Broad-billed Sandpiper Lirnicola fakinellus, Rock Pipit Anthus petrosus, Aquatic Warbler Acrocephaluspaludicola, Marmora’s Warbler Sylvia sarda, Cyprus Warbler Sylvia melanothorax, Crested T i t Parus cristatus, Corsican Nuthatch Sitta whiteheadi, Citril Finch Serinus citrinella, Scottish Crossbill and Parrot Crossbill. That two of these species are crossbills suggests either rapid speciation or an evolutionary history qualitatively different from most of the remaining avifauna of northern Europe.
The Parrot Crossbill No other pine-feeding form has a bill, or body, as large as that of the Parrot Crossbill. Some size and/or structural differences would be expected in the beaks of birds that feed on different species of pines. However, Scottish and Parrot Crossbills feed on the same species, the Scots pine, although on different varieties or subspecies. T h e dimensions of scotica’s bill are more like those of the Mediterranean birds than pytyopsittacus. While Bergmann’s Rule might account for the larger body size in the Parrot Crossbill, and character displacement is a possible explanation for the very heavy bill, the latter may also have evolved in response to the extreme cold that is found throughout the bird’s range during winter. For several months, night-time temperatures drop to - 20°C or less over much of the area. Pine cones which were hard anyway would partially or completely freeze, making them even more difficult to open. T h e strong beak of the Parrot Crossbill may allow this species to forage more efficiently on the tough cones. With its geographic range lying within that of the Common Crossbill, there remains the possibility that the Parrot Crossbill is merely a morph of that species (Meinertzhagen 1934, Dement’ev et al. 1965). If this were so the situation would be similar in many respects to that found in Hook-billed Kites Chondrohierax uncinatus (Smith & Temple 1982)) African seed-crackers Pyrenestes spp. (Smith 1987) and, to a lesser extent, some of the Darwin’s finches (Grant 1986). In all these groups, bills of different morphs have become adapted for different sized foods. Under such circumstances, and providing other conditions are met, it has been predicted that sympatric speciation could take place (Maynard Smith 1966). However, strict trophic isolation does not occur between the Parrot and Common Crossbill; there are subtle (but not diagnostic) plumage differences as well as those of size and proportion, and some vocalizations are quite different (Knox unpubl.). Unlike the other examples referred to, the measurements of the two crossbills are quite distinctive. Complete positive assortative mating occurs, although there are rare claims of interbreeding. I have seen a few skins said to be hybrids, but they were unconvincing. There seems little doubt that Parrot and Common Crossbills are different species. Many land-owners, factors, tenants, foresters and estate workers have shown much tolerance to my curious activities in the northeast over the last fifteen years. I am grateful for permission to work on their land, to catch birds, for accommodation, information and assistance in ways too numerous to mention. I spent much time on two particular estates: Glen Tanar and Glen Dye, for which I would especially like to thank the Hon. Jean Bruceand Sir William Gladstone, Bt., respectively. At Glen Tanar, Jimmy Oswald was most helpful. The hospitality, in many ways, of the staff of the Institute of Terrestrial Ecology at the Hill of Brathens, Banchory, was greatly appreciated. Part of this work started while I was at the Department of Zoology, University of Aberdeen, where I was in receipt of a post-graduate studentship from the Northern Ireland Department of Education. I have benefited from practical help from, discussion or correspondence with a number of people, including Professors A. J. Cain, F. W. Robertson and V. C. Wynne-Edwards, Curt Adkisson, Sam Alexander, Jeff Groth, Jon Hardey, Pekka Helle, Marc Herremans, Brian Huntley, Roxie Laybourne, Bruno Massa, the late Desmond Nethersole-Thompson,
I
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Ian Newton, T i m Parmenter, Nick Picozzi, Robert Rae, Lars Svensson and Adam Watson. P. H . Greenwood, J . J. D. Greenwood, A. M . Reynolds, N. Picozzi and D. W. Snow read and commented on the manuscript. I am grateful to all these people, and the many others who have helped over the years.
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