Foraging patterns of common crossbills (Loxia curvirostra) on spruces (Picea spp.) in Scotland

Foraging patterns of common crossbills (Loxia curvirostra) on spruces (Picea spp.) in Scotland Abstract Common crossbills forage on Sitka spruce and Norway spruce when the cones reach full size in late summer until the seeds have shed in the following spring. Sitka spruce start shedding seed in autumn, thereby reducing the food supply for crossbills through autumn to spring, whereas Norway spruce retain their seeds until spring. Crossbills forage on cones that are attached to the tree (more so for Norway spruces) or are removed from the tree by the crossbills before feeding. The latter cones are then dropped after seed extraction. The mean length of dropped Sitka spruce cones was 72 mm, close to the average length in a widespread survey. This suggests little size selection. The mean length of dropped Norway spruce cones was 90 mm, which was much smaller than the average length in the survey. Although used, large cones are probably left attached to trees because they are too heavy to handle if cut from the tree. The average percentage of seeds extracted before a cone was dropped was 45% for Sitka spruce and 42% for Norway spruce. There was a trend for fewer Sitka spruce seeds to be taken per cone across the period between autumn and spring. Incomplete extraction of seeds suggests that cones become unprofitable as the seed number is depleted in cones and that the threshold for switching cones changes as the number of seeds per cone declines. Introduction The common crossbill Loxia curvirostra (known as the red crossbill in North America) is a finch that is adapted to extracting seeds from conifers, mainly across the boreal region of the Holarctic (Cramp and Perrins, 1994). Within northern Europe, the common crossbill is regarded as being dependent on the seeds of Norway spruce Picea abies for its food supply, whereas the larger-billed parrot crossbill Loxia pytyopsittacus and Scottish crossbill L. scotica are able to extract seeds from the tougher cones of Scots pine Pinus sylvestris (Lack, 1944; Cramp and Perrins, 1994). Norway spruce has widespread synchronous variations in its cone crop (Hagner, 1965; Broome et al., 2007), resulting in irruptions of crossbills from northern Europe to regions south of the normal range when a large seed crop is followed by a poor one (Svärdson, 1957; Newton, 1972, 2006). Norway spruce is not native to Britain, so invading common crossbills would have had difficulty in extracting seeds from the woody cones of the native Scots pines until Norway spruce (from AD 995) and Sitka spruce Picea sitchensis (from AD 1832) were introduced to gardens in Britain, and latterly at a vastly greater scale to enhance the national timber crop (Anderson, 1967; Preston et al., 2002). These conifers have thinner scales than pines, so the seeds are less well protected than those of Scots pines (Marquiss and Rae, 1994; Summers and Broome, 2012). This would have increased the possibility for irrupting common crossbills becoming established as a breeding species in Britain, from at least the early 1800s (Knox, 1990). In 2008, Sitka spruce comprised approximately half of the woodland area in Scotland, whilst Norway spruce comprised c. 3% (Forestry Commission, 2009). Marquiss and Rae (1994) found common crossbills foraging on Sitka spruce and Norway spruce from December to April in Deeside (northeast Scotland), though crossbills did not breed whilst foraging on those species. In Wales, common crossbills breed mainly in February in mixed conifer plantations, which were predominantly of Sitka spruce (Dixon and Haffield, 2013). The only extensive survey is that by Summers and Broome (2012) who found that common crossbills were closely associated with Sitka spruce across Highland Scotland during January to April 2008, but not with Norway spruce, perhaps due to its scarcity. Apart from these records of foraging, breeding and habitat association, there is little known about the feeding ecology of crossbills in Scotland whilst foraging on spruces, one of which is not native to Europe yet dominates Scottish conifer plantations (Forestry Commission, 2009). The aims of this study were to describe the sizes of spruce cones available to crossbills and the seasonal changes associated with maturation prior to and whilst shedding seed. I also describe the feeding habits of the crossbills in relation to the maturation of the cones and availability of seeds. This will help to assess the value of these non-native conifers to common crossbills and how this may impact the endemic Scottish crossbill through possible hybridization, as both species now associate with non-native conifers (Summers and Broome, 2012). Methods Cone characteristics Conifer plantations tend to be on the poorer upland soils of the UK, and are managed through a rotation of planting, thinning and clear-felling. Trees become suitable for crossbills when coning. Widespread sampling of Sitka spruce and Norway spruce cones took place across the Highlands of northern Scotland (30 plantations for Sitka spruce and 20 for Norway spruce) during 2009–2016 to describe the sizes of cones available to crossbills. Mature plantations of spruces were selected opportunistically, so may not have been fully representative of the Highlands. Five fallen cones were arbitrarily collected under each of five trees along a c. 50 m transect in each plantation and lengths measured with dial callipers to the nearest 1 mm. The diameter at breast height (DBH) was measured for the five trees in each plantation. It was not possible to be sure of the trees from which cones fell. Therefore, to examine relationships between cone length and DBH, mean values were calculated for each site prior to analyses. To describe seasonal changes in the fresh mass and moisture content of cones, a single fully grown cone was collected with a pruning pole from each of 20 Norway spruces and 20 Sitka spruces in mature Forestry Commission conifer plantations: Inshriach, Strathspey, Inverness-shire (UK grid reference NH871608) and Inchindown, East Ross-shire (NH685742), respectively, in the middle of each month during autumn 2014 to spring 2015. Cone lengths were measured with dial callipers to the nearest 1 mm, and they were weighed fresh to 0.1 g with a digital balance within an hour of collection, and again after drying in an oven at 60°C for 2 days to obtain the dry mass and moisture content by subtraction. The data were analysed in a linear regression in which length was accounted for as a covariate before obtaining monthly averages (Supplementary material). A study of seed shedding was carried out during 2009–2011 in plantations at Inchindown for Sitka spruce and Scotsburn, East Ross-shire (NH745794) for Norway spruce. Ten seed bins (with a 36 cm diameter opening; area = 0.102 m2) were set under the canopy at approximately 20-m intervals along a 200-m transect in each of the woods. A muslin liner was tied into the bins to catch falling seeds. The bins were emptied at the end of each month, the sample dried and the seeds counted, but it was not determined if they contained a kernel. To count the number of seeds in spruce cones, one cone from each of 30 Sitka spruces and 30 Norway spruces was collected from Morinish (NJ242296) and Starthdearn (NH758247), respectively, in autumn, prior to shedding of seed. The Sitka spruce cones were taken from freshly felled trees whilst the Norway spruce cones were cut from standing trees using a pruning pole. Cone length was recorded, the cones dried, and seeds removed and counted. Most seeds were of a similar size but cones also contain tiny seeds at the apex of the cone. These seeds were not counted. Foraging by crossbills Initially, records of foraging crossbills were obtained opportunistically in East Ross-shire and Moray. Later, systematic searches were made each month in stands of Sitka spruce and Norway spruce at Inchindown and Scotsburn in East Ross-shire. When a spruce with foraging birds was located, the tree was approached quietly so that cones dropped by the birds could be observed as they fell and then collected. A maximum of 10 dropped cones was collected per tree. Additionally, plots under the crowns of 10 Norway spruces were cleared and searched for cones dropped by crossbills at the end of each month. Lengths of dropped cones were measured to 1 mm with callipers and the cones were dried at 60°C for 2 days to make it easier to extract residual seeds (as above) for counting. The relationship between seed number and cone length (Figure 4) plus the data on the cumulative seasonal shedding of seeds (Figure 3) were used to estimate the number of seeds available to crossbills prior to foraging. Subtraction of the number remaining after crossbills dropped cones provided estimates of the numbers consumed by crossbills. The mass of dropped cones was derived from length plus the measure of moisture content (Supplementary material). Mean cone characteristics (length, mass and percentage of seeds taken) were obtained for each tree before taking the mean for all trees used for foraging. The height (using a clinometer at a measured distance from the trees) and DBH of the trees used by crossbills were measured. Crossbills were identified to species from biometrics (bill depth and wing length) of captured birds within the plantation at Scotsburn (Summers et al., 2002). All measurements were by the author for consistency. Tape recordings were made from captured birds on release and from foraging birds, allowing them to be assigned to species-specific call types from sonograms (Summers et al., 2002). Results Cone characteristics The mean length of Sitka spruce cones was 69 mm (sd = 10.7, n = 750, range 42–99 mm) in the widespread survey. The mean length of Norway spruce cones was 116 mm (sd = 17.1, n = 500, range 63–164 mm) (Figure 1). There was a significant correlation between mean cone length and mean tree DBH for Sitka spruce for the different stands (r = −0.49, n = 30, P < 0.01). Small Sitka spruces produced longer cones than large Sitka spruces. There was no significant correlation between mean cone length and mean tree DBH for Norway spruce (r = 0.25, n = 20, P > 0.1). Figure 1 View largeDownload slide Frequency distributions for cone lengths for Sitka spruce (black bars) and Norway spruce (grey bars) in Highland Scotland. Figure 1 View largeDownload slide Frequency distributions for cone lengths for Sitka spruce (black bars) and Norway spruce (grey bars) in Highland Scotland. Cone development by both spruces took place during summer. By late summer and autumn (July to September), the cones were fully grown but still green/purple and the moisture content was high. Norway spruce cones were heavier than Sitka spruce cones. As the cones matured, the moisture content fell and they turned brown, but the dry mass remained constant (Figure 2). The moisture content of Sitka spruce rose slightly during wet and snowy weather in December before falling again in spring. Figure 2 View largeDownload slide Least squares mean fresh (●) and dry mass (□) of Sitka spruce and Norway spruce cones for different months. The vertical lines show the 95% confidence limits. Cone length was taken into account during the analyses. Figure 2 View largeDownload slide Least squares mean fresh (●) and dry mass (□) of Sitka spruce and Norway spruce cones for different months. The vertical lines show the 95% confidence limits. Cone length was taken into account during the analyses. The timing of seed fall differed for the two spruces (Figure 3). Sitka spruce started to shed seeds in autumn with a peak in October, such that about a third of the seeds was shed before February. There was then a lull in shedding perhaps because cones closed partly during the wet weather in winter. There was then a second peak in shedding during the warming spring weather (March and April), followed closely by the shedding of Norway spruce seed in April and May. Small amounts of seed were shed in the following months. For both spruces, there were more seeds in longer cones (Figure 4). Figure 3 View largeDownload slide The density of spruce seeds per m2 falling on the ground in different months from August 2010 to February 2012. The vertical lines show the 95% confidence limits. Figure 3 View largeDownload slide The density of spruce seeds per m2 falling on the ground in different months from August 2010 to February 2012. The vertical lines show the 95% confidence limits. Figure 4 View largeDownload slide The relationship between the number of seeds and cone length for Sitka spruce and Norway spruce. The regression equations are y = −106.4 + 4.96x for Sitka spruce (r = 0.76, n = 30, P < 0.001), and y = −69.1 + 2.53x for Norway spruce (r = 0.71, n = 30, P < 0.001). Figure 4 View largeDownload slide The relationship between the number of seeds and cone length for Sitka spruce and Norway spruce. The regression equations are y = −106.4 + 4.96x for Sitka spruce (r = 0.76, n = 30, P < 0.001), and y = −69.1 + 2.53x for Norway spruce (r = 0.71, n = 30, P < 0.001). Foraging by crossbills Fifty-three crossbills were captured at Scotsburn, within 500 m of where many of the observations of foraging crossbills were made. The bill depth and wing length measurements fell largely within the 95% range for common crossbills (Figure 5). In addition, calls recorded from the birds on release confirmed most as being common crossbills. Fifteen were assigned to common crossbill call type 4E and 10 to call type 1A. Only one bird was classed as a Scottish crossbill as it gave calls of call type 3C. Further recordings of crossbills in the areas where crossbills were observed foraging were also of common crossbill call types; 4E (on five occasions) and 1A (on eight occasions) in January, February, March, May, July, August and December. Figure 5 View largeDownload slide A plot of bill depth against wing length for male (●) and female (o) crossbills captured at Scotsburn, East Ross-shire, in February, March and September. The ellipse comprises the 95% range for common crossbills, as defined from museum specimens (Summers et al., 2002). Figure 5 View largeDownload slide A plot of bill depth against wing length for male (●) and female (o) crossbills captured at Scotsburn, East Ross-shire, in February, March and September. The ellipse comprises the 95% range for common crossbills, as defined from museum specimens (Summers et al., 2002). Foraging by crossbills was observed each month from August to May on Sitka spruce, and November to May for Norway spruce, but with no observation in January. There were no autumn searches for crossbills in Norway spruce. The mean heights of the trees used for foraging were 21.2 m high for Sitka spruce and 22.5 m for Norway spruce. The respective mean diameters at breast height were 40 cm and 39 cm (Table 1, Figure 6). There was little variation in the sizes of the Norway spruces because most observations were in the same stand of trees, whereas 14 different plantations comprised the data for Sitka spruces. Figure 6 View largeDownload slide The relationship between height (m) and diameter at breast height (DBH) (cm) for spruce trees used by crossbills for foraging. Sitka spruce (●) and Norway spruce (□). Figure 6 View largeDownload slide The relationship between height (m) and diameter at breast height (DBH) (cm) for spruce trees used by crossbills for foraging. Sitka spruce (●) and Norway spruce (□). The mean length of Sitka spruce cones dropped by crossbills was 72 mm, only 3 mm longer than the mean from the widespread survey. The estimated mean mass of the dropped cones varied from 14.1 g in August to 4.4 g in October. The crossbills cut the peduncle of the cone close to the proximal end of the cone, sometimes with needles from the end of the peduncle. The mean number of needles attached was 6.7 (Table 1, Figure 7). The mean length of Norway spruce cones dropped by crossbills was 90 mm (Table 1). This was much shorter than the cone lengths from the widespread survey, with only 6.6% of cones equal to or less than 90 mm (Figure 1). In addition, the coefficient of variation for the lengths of Norway spruce cones (7.7%) was less than that for Sitka spruce (12.4%), indicating how restricted crossbills were to the lower end of the size distribution for Norway spruce. The estimated mean mass of dropped Norway spruce cones varied from 13.0 g in November to 19.4 g in March. The mean number of needles attached round the peduncle was 7.7 for Norway spruce cones (Table 1, Figure 7). Figure 7 View largeDownload slide Sitka spruce (left) and Norway spruce cones (right) from which common crossbills had removed seeds. Note the longitudinal split to some of the scales (indicated by the white lines). © Ron Summers. Figure 7 View largeDownload slide Sitka spruce (left) and Norway spruce cones (right) from which common crossbills had removed seeds. Note the longitudinal split to some of the scales (indicated by the white lines). © Ron Summers. Table 1 Characteristics of Sitka spruce and Norway spruce trees used by common crossbills and the cones dropped from these trees. Sitka spruce Norway spruce Mean (sd) Range Sample size Mean (sd) Range Sample size Tree height (m) 21.2 (5.7) 9–33 39 22.5 (5.9) 18–26 11 Tree DBH (cm) 39.7 (14.0) 14–73 39 38.9 (5.9) 34–51 11 Cone length (mm) 72.4 (9.0) 57–94 37 89.9 (6.9) 74–98 14 Number of needles 6.7 (7.8) 0–25 25 7.7 (4.4) 1–15 11 Number of seeds taken 87 (58) 11–167 20 68 (37) 12–119 12 Percentage of seeds taken 45 (27) 5–84 20 42 (21) 7–67 12 Sitka spruce Norway spruce Mean (sd) Range Sample size Mean (sd) Range Sample size Tree height (m) 21.2 (5.7) 9–33 39 22.5 (5.9) 18–26 11 Tree DBH (cm) 39.7 (14.0) 14–73 39 38.9 (5.9) 34–51 11 Cone length (mm) 72.4 (9.0) 57–94 37 89.9 (6.9) 74–98 14 Number of needles 6.7 (7.8) 0–25 25 7.7 (4.4) 1–15 11 Number of seeds taken 87 (58) 11–167 20 68 (37) 12–119 12 Percentage of seeds taken 45 (27) 5–84 20 42 (21) 7–67 12 Observations were made largely at Inchindown and Scotsburn (East Ross-shire). View Large Table 1 Characteristics of Sitka spruce and Norway spruce trees used by common crossbills and the cones dropped from these trees. Sitka spruce Norway spruce Mean (sd) Range Sample size Mean (sd) Range Sample size Tree height (m) 21.2 (5.7) 9–33 39 22.5 (5.9) 18–26 11 Tree DBH (cm) 39.7 (14.0) 14–73 39 38.9 (5.9) 34–51 11 Cone length (mm) 72.4 (9.0) 57–94 37 89.9 (6.9) 74–98 14 Number of needles 6.7 (7.8) 0–25 25 7.7 (4.4) 1–15 11 Number of seeds taken 87 (58) 11–167 20 68 (37) 12–119 12 Percentage of seeds taken 45 (27) 5–84 20 42 (21) 7–67 12 Sitka spruce Norway spruce Mean (sd) Range Sample size Mean (sd) Range Sample size Tree height (m) 21.2 (5.7) 9–33 39 22.5 (5.9) 18–26 11 Tree DBH (cm) 39.7 (14.0) 14–73 39 38.9 (5.9) 34–51 11 Cone length (mm) 72.4 (9.0) 57–94 37 89.9 (6.9) 74–98 14 Number of needles 6.7 (7.8) 0–25 25 7.7 (4.4) 1–15 11 Number of seeds taken 87 (58) 11–167 20 68 (37) 12–119 12 Percentage of seeds taken 45 (27) 5–84 20 42 (21) 7–67 12 Observations were made largely at Inchindown and Scotsburn (East Ross-shire). View Large Crossbills damaged Sitka spruce scales when prying them apart during August and September. Scales were displaced outwards and some were split down the middle of the scale (Figure 7). Damage to Sitka spruce scales was not as evident from October onward, when the scales were not so tightly closed, making it more difficult to identify cones foraged on by crossbills. The scales of Norway spruce cones remained more tightly closed than the scales of Sitka spruce, so damage (displaced and split scales) to Norway spruce cones was observed from at least November to March (Figure 7). Such longitudinal splitting also occurs on larch cones but not Scots pine cones, which have thicker scales. The number of seeds taken from cones was determined from the estimated number prior to foraging (Figures 3 and 4), minus the number counted in dropped cones. Some of the estimates for the number of seeds present in a cone prior to foraging were less than the number remaining, leading to negative values for the number taken. However, when the mean was taken for all the cones from a given tree, there were no negative means. The mean number of seeds taken from Sitka spruce cones was 87, and 68 from Norway spruces. These were equivalent to 45% and 42% removed, respectively (Table 1). There was a trend for fewer Sitka seeds to be taken across the period between autumn (August) and spring (March) (rs = −0.47, P < 0.05) coincident with fewer seeds per cone being available as the seasons progressed (rs = −0.70, P < 0.001), but there was no seasonal trend in the percentage taken (rs = 0.19, P > 0.2) (Figure 8). Figure 8 View largeDownload slide The relationships between the mean number of seeds available (□) in Sitka spruce cones and numbers consumed (●) by common crossbills during August to March. Figure 8 View largeDownload slide The relationships between the mean number of seeds available (□) in Sitka spruce cones and numbers consumed (●) by common crossbills during August to March. Discussion Sitka spruce provided an almost year-round supply of seeds for common crossbills during 2010–2011. The observations were over a shorter period for Norway spruce (November–May) but it is likely that their availability to crossbills would be across a similar period as found for Sitka spruce. Small (narrow-stemmed) Sitka spruces tended to produce larger (longer) cones than large Sitka spruces. This relationship also occurs for Scots pines (Bergsten, 1985; Summers and Proctor 1999). Narrow-stemmed conifers tend to occur in dense stands so have small crowns and therefore less opportunity to produce many cones. They may therefore invest reproductive resources in forming large cones. The difference between the cone sizes on large and small Sitka spruces does mean that crossbills could select larger cones with more seeds, though the similarity between the mean size taken with the size in the widespread survey does not suggest this. On average, common crossbills extracted only 45% and 42% of the seeds from Sitka spruce and Norway spruce cones, respectively. The partial consumption of available seeds suggests that it is more profitable to switch to another cone to maximize the average intake rate (Krebs, 1978). This concurs with a study in North America that found that as the kernel mass in tamarack Larix laricina cones was depleted, it was more profitable for two-barred crossbills Loxia leucoptera to switch cones to maximize intake (Benkman, 1989). These findings contrast with that of Tombre-Steen (1991), who found that parrot crossbills foraging on the non-native mountain pine Pinus mugo in Norway extracted almost all the seeds from a cone before selecting another. Although optimal foraging may account for some of the variation in the numbers of Sitka spruce seeds taken, some of the low values in Figure 8 may have been due to birds terminating a feeding bout when disturbed or when a flock decided to forage elsewhere. Given that Sitka spruces begin to shed seed in autumn, there is a declining but still abundant food supply of seed for crossbills through to spring (Figure 8). The declining number of seeds in the Sitka spruce cones may account for the trend of fewer seeds being taken across the period from autumn to spring, and suggests that the threshold for giving up on a cone and switching to another cone changes as the number of seeds available declines. Sitka spruce began to shed seeds in autumn, many months before the Norway spruce. The spring shedding of seed in Norway spruce was similar to that of Scots pine (Summers and Proctor, 2005). The early start to seed dispersal by Sitka spruce is a trait of most non-serotinous North American conifers and is believed to be a strategy to reduce seed losses to pine squirrels Tamiasciurus spp., which begin to remove and cache cones as soon as they have developed (Benkman et al., 2010). Seeds dispersed in autumn then lie on the ground all winter and spring before germinating. During this period, they may be lost to other seeds-eaters such as rodents and beetles (Nystrand and Granström, 1997, 2000). In northern Europe, red squirrels Sciurus vulgaris do not have the same caching tendency (Gurnell, 1987), so there has been less selective pressure on Norway spruce or Scots pine to disperse seed early. Norway spruce cones are bigger and heavier than Sitka spruce cones, and the larger cones exceed the mass of common crossbills; c. 40 g (Marquiss, 1980) (Figure 2). This would make it difficult for crossbills to remove and manipulate cones between the bill and feet, a common method when extracting seeds (Newton, 1972; Benkman, 1987). This probably accounts for the relatively small Norway spruce cones that crossbills did remove and drop from trees (Table 1). It would appear that crossbills are limited to removing cones up to about a third of their body mass. When crossbills were observed foraging on cones attached to trees, it is likely that large cones were involved. Sitka spruce cones have thin papery scales that provide little defence against foraging by common crossbills. In North America, the crossbills (also Loxia curvirostra) that are adapted to foraging on Sitka spruce cones are smaller than the common crossbills of Europe and have smaller bills: bill depths of 8.55 mm for males and 8.37 mm for females (Irwin, 2010). This contrasts with bill depths of 10.7 mm for male and 10.5 mm for female European common crossbills (Knox, 1976). Therefore, it is likely that the common crossbills of Europe feed less efficiently than those in North America. By contrast, the scales of Norway spruce are leathery and three times thicker than Sitka spruce cones (Summers and Broome, 2012). Even though common crossbills are adapted to forage on Norway spruce (Lack, 1944), it is presumably more difficult for crossbills to remove seeds from Norway spruce cones than Sitka spruce (Benkman, 1993) and may explain the heavy use of Sitka spruces by common crossbills in Scotland (Summers and Broome, 2012). However, a penalty for this choice of tree is that the seed size is small (Marquiss and Rae, 1994), and this presumably limits the intake rate. Only one Scottish crossbill was captured close to the study sites and no Scottish Crossbills were tape recorded in the stands of spruce. This suggests that it is common crossbills that largely rely on spruces in Scotland and that the two species rarely overlap in their use of spruce (Jardine, 2002; Summers and Broome, 2012). One conservation concern is that hybridization with Scottish crossbills is more likely when both species share other conifers, such as lodgepole pine (Summers and Broome, 2012), particularly in years when there are no Sitka spruce cones (Broome et al., 2007). To date, however, cases of hybridization have only been recorded between parrot and Scottish crossbills in Caledonian pinewoods (Summers et al., 2007), though it would probably be more difficult to detect hybridization between Scottish and common crossbills when nesting in plantations where the tree density is much higher than in Caledonian pinewoods. Supplementary data Supplementary data are available at Forestry online. Acknowledgements Graeme Findlay of the Forestry Commission kindly provided permission to work in the Forestry Commission woods in Ross-shire. Birds were captured jointly with Nigel Richards. Craig Benkman and Jeremy Wilson commented on the draft. Conflict of interest statement None declared. References Anderson , M.L. 1967 A History of Scottish Forestry , Vol. 2. Nelson, p. 654 . Benkman , C.W. 1987 Crossbill foraging behavior, bill structure, and patterns of food profitability . Wilson. Bull. 99 , 351 – 368 . Benkman , C.W. 1989 Intake rate maximization and the foraging behaviour of crossbills . Ornis. Scand. 20 , 65 – 68 . Google Scholar CrossRef Search ADS Benkman , C.W. 1993 Adaptation to single resources and the evolution of crossbill (Loxia) diversity . Ecol. Monog. 63 , 305 – 325 . Google Scholar CrossRef Search ADS Benkman , C.W. , Parchman , T.L. and Mezquida , E.T. 2010 Patterns of coevolution in the adaptive radiation of crossbills . Ann. N. Y. Acad. Sci. 1206 , 1 – 16 . 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Foraging patterns of common crossbills (Loxia curvirostra) on spruces (Picea spp.) in Scotland

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Institute of Chartered Foresters
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0015-752X
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1464-3626
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10.1093/forestry/cpy002
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Abstract

Abstract Common crossbills forage on Sitka spruce and Norway spruce when the cones reach full size in late summer until the seeds have shed in the following spring. Sitka spruce start shedding seed in autumn, thereby reducing the food supply for crossbills through autumn to spring, whereas Norway spruce retain their seeds until spring. Crossbills forage on cones that are attached to the tree (more so for Norway spruces) or are removed from the tree by the crossbills before feeding. The latter cones are then dropped after seed extraction. The mean length of dropped Sitka spruce cones was 72 mm, close to the average length in a widespread survey. This suggests little size selection. The mean length of dropped Norway spruce cones was 90 mm, which was much smaller than the average length in the survey. Although used, large cones are probably left attached to trees because they are too heavy to handle if cut from the tree. The average percentage of seeds extracted before a cone was dropped was 45% for Sitka spruce and 42% for Norway spruce. There was a trend for fewer Sitka spruce seeds to be taken per cone across the period between autumn and spring. Incomplete extraction of seeds suggests that cones become unprofitable as the seed number is depleted in cones and that the threshold for switching cones changes as the number of seeds per cone declines. Introduction The common crossbill Loxia curvirostra (known as the red crossbill in North America) is a finch that is adapted to extracting seeds from conifers, mainly across the boreal region of the Holarctic (Cramp and Perrins, 1994). Within northern Europe, the common crossbill is regarded as being dependent on the seeds of Norway spruce Picea abies for its food supply, whereas the larger-billed parrot crossbill Loxia pytyopsittacus and Scottish crossbill L. scotica are able to extract seeds from the tougher cones of Scots pine Pinus sylvestris (Lack, 1944; Cramp and Perrins, 1994). Norway spruce has widespread synchronous variations in its cone crop (Hagner, 1965; Broome et al., 2007), resulting in irruptions of crossbills from northern Europe to regions south of the normal range when a large seed crop is followed by a poor one (Svärdson, 1957; Newton, 1972, 2006). Norway spruce is not native to Britain, so invading common crossbills would have had difficulty in extracting seeds from the woody cones of the native Scots pines until Norway spruce (from AD 995) and Sitka spruce Picea sitchensis (from AD 1832) were introduced to gardens in Britain, and latterly at a vastly greater scale to enhance the national timber crop (Anderson, 1967; Preston et al., 2002). These conifers have thinner scales than pines, so the seeds are less well protected than those of Scots pines (Marquiss and Rae, 1994; Summers and Broome, 2012). This would have increased the possibility for irrupting common crossbills becoming established as a breeding species in Britain, from at least the early 1800s (Knox, 1990). In 2008, Sitka spruce comprised approximately half of the woodland area in Scotland, whilst Norway spruce comprised c. 3% (Forestry Commission, 2009). Marquiss and Rae (1994) found common crossbills foraging on Sitka spruce and Norway spruce from December to April in Deeside (northeast Scotland), though crossbills did not breed whilst foraging on those species. In Wales, common crossbills breed mainly in February in mixed conifer plantations, which were predominantly of Sitka spruce (Dixon and Haffield, 2013). The only extensive survey is that by Summers and Broome (2012) who found that common crossbills were closely associated with Sitka spruce across Highland Scotland during January to April 2008, but not with Norway spruce, perhaps due to its scarcity. Apart from these records of foraging, breeding and habitat association, there is little known about the feeding ecology of crossbills in Scotland whilst foraging on spruces, one of which is not native to Europe yet dominates Scottish conifer plantations (Forestry Commission, 2009). The aims of this study were to describe the sizes of spruce cones available to crossbills and the seasonal changes associated with maturation prior to and whilst shedding seed. I also describe the feeding habits of the crossbills in relation to the maturation of the cones and availability of seeds. This will help to assess the value of these non-native conifers to common crossbills and how this may impact the endemic Scottish crossbill through possible hybridization, as both species now associate with non-native conifers (Summers and Broome, 2012). Methods Cone characteristics Conifer plantations tend to be on the poorer upland soils of the UK, and are managed through a rotation of planting, thinning and clear-felling. Trees become suitable for crossbills when coning. Widespread sampling of Sitka spruce and Norway spruce cones took place across the Highlands of northern Scotland (30 plantations for Sitka spruce and 20 for Norway spruce) during 2009–2016 to describe the sizes of cones available to crossbills. Mature plantations of spruces were selected opportunistically, so may not have been fully representative of the Highlands. Five fallen cones were arbitrarily collected under each of five trees along a c. 50 m transect in each plantation and lengths measured with dial callipers to the nearest 1 mm. The diameter at breast height (DBH) was measured for the five trees in each plantation. It was not possible to be sure of the trees from which cones fell. Therefore, to examine relationships between cone length and DBH, mean values were calculated for each site prior to analyses. To describe seasonal changes in the fresh mass and moisture content of cones, a single fully grown cone was collected with a pruning pole from each of 20 Norway spruces and 20 Sitka spruces in mature Forestry Commission conifer plantations: Inshriach, Strathspey, Inverness-shire (UK grid reference NH871608) and Inchindown, East Ross-shire (NH685742), respectively, in the middle of each month during autumn 2014 to spring 2015. Cone lengths were measured with dial callipers to the nearest 1 mm, and they were weighed fresh to 0.1 g with a digital balance within an hour of collection, and again after drying in an oven at 60°C for 2 days to obtain the dry mass and moisture content by subtraction. The data were analysed in a linear regression in which length was accounted for as a covariate before obtaining monthly averages (Supplementary material). A study of seed shedding was carried out during 2009–2011 in plantations at Inchindown for Sitka spruce and Scotsburn, East Ross-shire (NH745794) for Norway spruce. Ten seed bins (with a 36 cm diameter opening; area = 0.102 m2) were set under the canopy at approximately 20-m intervals along a 200-m transect in each of the woods. A muslin liner was tied into the bins to catch falling seeds. The bins were emptied at the end of each month, the sample dried and the seeds counted, but it was not determined if they contained a kernel. To count the number of seeds in spruce cones, one cone from each of 30 Sitka spruces and 30 Norway spruces was collected from Morinish (NJ242296) and Starthdearn (NH758247), respectively, in autumn, prior to shedding of seed. The Sitka spruce cones were taken from freshly felled trees whilst the Norway spruce cones were cut from standing trees using a pruning pole. Cone length was recorded, the cones dried, and seeds removed and counted. Most seeds were of a similar size but cones also contain tiny seeds at the apex of the cone. These seeds were not counted. Foraging by crossbills Initially, records of foraging crossbills were obtained opportunistically in East Ross-shire and Moray. Later, systematic searches were made each month in stands of Sitka spruce and Norway spruce at Inchindown and Scotsburn in East Ross-shire. When a spruce with foraging birds was located, the tree was approached quietly so that cones dropped by the birds could be observed as they fell and then collected. A maximum of 10 dropped cones was collected per tree. Additionally, plots under the crowns of 10 Norway spruces were cleared and searched for cones dropped by crossbills at the end of each month. Lengths of dropped cones were measured to 1 mm with callipers and the cones were dried at 60°C for 2 days to make it easier to extract residual seeds (as above) for counting. The relationship between seed number and cone length (Figure 4) plus the data on the cumulative seasonal shedding of seeds (Figure 3) were used to estimate the number of seeds available to crossbills prior to foraging. Subtraction of the number remaining after crossbills dropped cones provided estimates of the numbers consumed by crossbills. The mass of dropped cones was derived from length plus the measure of moisture content (Supplementary material). Mean cone characteristics (length, mass and percentage of seeds taken) were obtained for each tree before taking the mean for all trees used for foraging. The height (using a clinometer at a measured distance from the trees) and DBH of the trees used by crossbills were measured. Crossbills were identified to species from biometrics (bill depth and wing length) of captured birds within the plantation at Scotsburn (Summers et al., 2002). All measurements were by the author for consistency. Tape recordings were made from captured birds on release and from foraging birds, allowing them to be assigned to species-specific call types from sonograms (Summers et al., 2002). Results Cone characteristics The mean length of Sitka spruce cones was 69 mm (sd = 10.7, n = 750, range 42–99 mm) in the widespread survey. The mean length of Norway spruce cones was 116 mm (sd = 17.1, n = 500, range 63–164 mm) (Figure 1). There was a significant correlation between mean cone length and mean tree DBH for Sitka spruce for the different stands (r = −0.49, n = 30, P < 0.01). Small Sitka spruces produced longer cones than large Sitka spruces. There was no significant correlation between mean cone length and mean tree DBH for Norway spruce (r = 0.25, n = 20, P > 0.1). Figure 1 View largeDownload slide Frequency distributions for cone lengths for Sitka spruce (black bars) and Norway spruce (grey bars) in Highland Scotland. Figure 1 View largeDownload slide Frequency distributions for cone lengths for Sitka spruce (black bars) and Norway spruce (grey bars) in Highland Scotland. Cone development by both spruces took place during summer. By late summer and autumn (July to September), the cones were fully grown but still green/purple and the moisture content was high. Norway spruce cones were heavier than Sitka spruce cones. As the cones matured, the moisture content fell and they turned brown, but the dry mass remained constant (Figure 2). The moisture content of Sitka spruce rose slightly during wet and snowy weather in December before falling again in spring. Figure 2 View largeDownload slide Least squares mean fresh (●) and dry mass (□) of Sitka spruce and Norway spruce cones for different months. The vertical lines show the 95% confidence limits. Cone length was taken into account during the analyses. Figure 2 View largeDownload slide Least squares mean fresh (●) and dry mass (□) of Sitka spruce and Norway spruce cones for different months. The vertical lines show the 95% confidence limits. Cone length was taken into account during the analyses. The timing of seed fall differed for the two spruces (Figure 3). Sitka spruce started to shed seeds in autumn with a peak in October, such that about a third of the seeds was shed before February. There was then a lull in shedding perhaps because cones closed partly during the wet weather in winter. There was then a second peak in shedding during the warming spring weather (March and April), followed closely by the shedding of Norway spruce seed in April and May. Small amounts of seed were shed in the following months. For both spruces, there were more seeds in longer cones (Figure 4). Figure 3 View largeDownload slide The density of spruce seeds per m2 falling on the ground in different months from August 2010 to February 2012. The vertical lines show the 95% confidence limits. Figure 3 View largeDownload slide The density of spruce seeds per m2 falling on the ground in different months from August 2010 to February 2012. The vertical lines show the 95% confidence limits. Figure 4 View largeDownload slide The relationship between the number of seeds and cone length for Sitka spruce and Norway spruce. The regression equations are y = −106.4 + 4.96x for Sitka spruce (r = 0.76, n = 30, P < 0.001), and y = −69.1 + 2.53x for Norway spruce (r = 0.71, n = 30, P < 0.001). Figure 4 View largeDownload slide The relationship between the number of seeds and cone length for Sitka spruce and Norway spruce. The regression equations are y = −106.4 + 4.96x for Sitka spruce (r = 0.76, n = 30, P < 0.001), and y = −69.1 + 2.53x for Norway spruce (r = 0.71, n = 30, P < 0.001). Foraging by crossbills Fifty-three crossbills were captured at Scotsburn, within 500 m of where many of the observations of foraging crossbills were made. The bill depth and wing length measurements fell largely within the 95% range for common crossbills (Figure 5). In addition, calls recorded from the birds on release confirmed most as being common crossbills. Fifteen were assigned to common crossbill call type 4E and 10 to call type 1A. Only one bird was classed as a Scottish crossbill as it gave calls of call type 3C. Further recordings of crossbills in the areas where crossbills were observed foraging were also of common crossbill call types; 4E (on five occasions) and 1A (on eight occasions) in January, February, March, May, July, August and December. Figure 5 View largeDownload slide A plot of bill depth against wing length for male (●) and female (o) crossbills captured at Scotsburn, East Ross-shire, in February, March and September. The ellipse comprises the 95% range for common crossbills, as defined from museum specimens (Summers et al., 2002). Figure 5 View largeDownload slide A plot of bill depth against wing length for male (●) and female (o) crossbills captured at Scotsburn, East Ross-shire, in February, March and September. The ellipse comprises the 95% range for common crossbills, as defined from museum specimens (Summers et al., 2002). Foraging by crossbills was observed each month from August to May on Sitka spruce, and November to May for Norway spruce, but with no observation in January. There were no autumn searches for crossbills in Norway spruce. The mean heights of the trees used for foraging were 21.2 m high for Sitka spruce and 22.5 m for Norway spruce. The respective mean diameters at breast height were 40 cm and 39 cm (Table 1, Figure 6). There was little variation in the sizes of the Norway spruces because most observations were in the same stand of trees, whereas 14 different plantations comprised the data for Sitka spruces. Figure 6 View largeDownload slide The relationship between height (m) and diameter at breast height (DBH) (cm) for spruce trees used by crossbills for foraging. Sitka spruce (●) and Norway spruce (□). Figure 6 View largeDownload slide The relationship between height (m) and diameter at breast height (DBH) (cm) for spruce trees used by crossbills for foraging. Sitka spruce (●) and Norway spruce (□). The mean length of Sitka spruce cones dropped by crossbills was 72 mm, only 3 mm longer than the mean from the widespread survey. The estimated mean mass of the dropped cones varied from 14.1 g in August to 4.4 g in October. The crossbills cut the peduncle of the cone close to the proximal end of the cone, sometimes with needles from the end of the peduncle. The mean number of needles attached was 6.7 (Table 1, Figure 7). The mean length of Norway spruce cones dropped by crossbills was 90 mm (Table 1). This was much shorter than the cone lengths from the widespread survey, with only 6.6% of cones equal to or less than 90 mm (Figure 1). In addition, the coefficient of variation for the lengths of Norway spruce cones (7.7%) was less than that for Sitka spruce (12.4%), indicating how restricted crossbills were to the lower end of the size distribution for Norway spruce. The estimated mean mass of dropped Norway spruce cones varied from 13.0 g in November to 19.4 g in March. The mean number of needles attached round the peduncle was 7.7 for Norway spruce cones (Table 1, Figure 7). Figure 7 View largeDownload slide Sitka spruce (left) and Norway spruce cones (right) from which common crossbills had removed seeds. Note the longitudinal split to some of the scales (indicated by the white lines). © Ron Summers. Figure 7 View largeDownload slide Sitka spruce (left) and Norway spruce cones (right) from which common crossbills had removed seeds. Note the longitudinal split to some of the scales (indicated by the white lines). © Ron Summers. Table 1 Characteristics of Sitka spruce and Norway spruce trees used by common crossbills and the cones dropped from these trees. Sitka spruce Norway spruce Mean (sd) Range Sample size Mean (sd) Range Sample size Tree height (m) 21.2 (5.7) 9–33 39 22.5 (5.9) 18–26 11 Tree DBH (cm) 39.7 (14.0) 14–73 39 38.9 (5.9) 34–51 11 Cone length (mm) 72.4 (9.0) 57–94 37 89.9 (6.9) 74–98 14 Number of needles 6.7 (7.8) 0–25 25 7.7 (4.4) 1–15 11 Number of seeds taken 87 (58) 11–167 20 68 (37) 12–119 12 Percentage of seeds taken 45 (27) 5–84 20 42 (21) 7–67 12 Sitka spruce Norway spruce Mean (sd) Range Sample size Mean (sd) Range Sample size Tree height (m) 21.2 (5.7) 9–33 39 22.5 (5.9) 18–26 11 Tree DBH (cm) 39.7 (14.0) 14–73 39 38.9 (5.9) 34–51 11 Cone length (mm) 72.4 (9.0) 57–94 37 89.9 (6.9) 74–98 14 Number of needles 6.7 (7.8) 0–25 25 7.7 (4.4) 1–15 11 Number of seeds taken 87 (58) 11–167 20 68 (37) 12–119 12 Percentage of seeds taken 45 (27) 5–84 20 42 (21) 7–67 12 Observations were made largely at Inchindown and Scotsburn (East Ross-shire). View Large Table 1 Characteristics of Sitka spruce and Norway spruce trees used by common crossbills and the cones dropped from these trees. Sitka spruce Norway spruce Mean (sd) Range Sample size Mean (sd) Range Sample size Tree height (m) 21.2 (5.7) 9–33 39 22.5 (5.9) 18–26 11 Tree DBH (cm) 39.7 (14.0) 14–73 39 38.9 (5.9) 34–51 11 Cone length (mm) 72.4 (9.0) 57–94 37 89.9 (6.9) 74–98 14 Number of needles 6.7 (7.8) 0–25 25 7.7 (4.4) 1–15 11 Number of seeds taken 87 (58) 11–167 20 68 (37) 12–119 12 Percentage of seeds taken 45 (27) 5–84 20 42 (21) 7–67 12 Sitka spruce Norway spruce Mean (sd) Range Sample size Mean (sd) Range Sample size Tree height (m) 21.2 (5.7) 9–33 39 22.5 (5.9) 18–26 11 Tree DBH (cm) 39.7 (14.0) 14–73 39 38.9 (5.9) 34–51 11 Cone length (mm) 72.4 (9.0) 57–94 37 89.9 (6.9) 74–98 14 Number of needles 6.7 (7.8) 0–25 25 7.7 (4.4) 1–15 11 Number of seeds taken 87 (58) 11–167 20 68 (37) 12–119 12 Percentage of seeds taken 45 (27) 5–84 20 42 (21) 7–67 12 Observations were made largely at Inchindown and Scotsburn (East Ross-shire). View Large Crossbills damaged Sitka spruce scales when prying them apart during August and September. Scales were displaced outwards and some were split down the middle of the scale (Figure 7). Damage to Sitka spruce scales was not as evident from October onward, when the scales were not so tightly closed, making it more difficult to identify cones foraged on by crossbills. The scales of Norway spruce cones remained more tightly closed than the scales of Sitka spruce, so damage (displaced and split scales) to Norway spruce cones was observed from at least November to March (Figure 7). Such longitudinal splitting also occurs on larch cones but not Scots pine cones, which have thicker scales. The number of seeds taken from cones was determined from the estimated number prior to foraging (Figures 3 and 4), minus the number counted in dropped cones. Some of the estimates for the number of seeds present in a cone prior to foraging were less than the number remaining, leading to negative values for the number taken. However, when the mean was taken for all the cones from a given tree, there were no negative means. The mean number of seeds taken from Sitka spruce cones was 87, and 68 from Norway spruces. These were equivalent to 45% and 42% removed, respectively (Table 1). There was a trend for fewer Sitka seeds to be taken across the period between autumn (August) and spring (March) (rs = −0.47, P < 0.05) coincident with fewer seeds per cone being available as the seasons progressed (rs = −0.70, P < 0.001), but there was no seasonal trend in the percentage taken (rs = 0.19, P > 0.2) (Figure 8). Figure 8 View largeDownload slide The relationships between the mean number of seeds available (□) in Sitka spruce cones and numbers consumed (●) by common crossbills during August to March. Figure 8 View largeDownload slide The relationships between the mean number of seeds available (□) in Sitka spruce cones and numbers consumed (●) by common crossbills during August to March. Discussion Sitka spruce provided an almost year-round supply of seeds for common crossbills during 2010–2011. The observations were over a shorter period for Norway spruce (November–May) but it is likely that their availability to crossbills would be across a similar period as found for Sitka spruce. Small (narrow-stemmed) Sitka spruces tended to produce larger (longer) cones than large Sitka spruces. This relationship also occurs for Scots pines (Bergsten, 1985; Summers and Proctor 1999). Narrow-stemmed conifers tend to occur in dense stands so have small crowns and therefore less opportunity to produce many cones. They may therefore invest reproductive resources in forming large cones. The difference between the cone sizes on large and small Sitka spruces does mean that crossbills could select larger cones with more seeds, though the similarity between the mean size taken with the size in the widespread survey does not suggest this. On average, common crossbills extracted only 45% and 42% of the seeds from Sitka spruce and Norway spruce cones, respectively. The partial consumption of available seeds suggests that it is more profitable to switch to another cone to maximize the average intake rate (Krebs, 1978). This concurs with a study in North America that found that as the kernel mass in tamarack Larix laricina cones was depleted, it was more profitable for two-barred crossbills Loxia leucoptera to switch cones to maximize intake (Benkman, 1989). These findings contrast with that of Tombre-Steen (1991), who found that parrot crossbills foraging on the non-native mountain pine Pinus mugo in Norway extracted almost all the seeds from a cone before selecting another. Although optimal foraging may account for some of the variation in the numbers of Sitka spruce seeds taken, some of the low values in Figure 8 may have been due to birds terminating a feeding bout when disturbed or when a flock decided to forage elsewhere. Given that Sitka spruces begin to shed seed in autumn, there is a declining but still abundant food supply of seed for crossbills through to spring (Figure 8). The declining number of seeds in the Sitka spruce cones may account for the trend of fewer seeds being taken across the period from autumn to spring, and suggests that the threshold for giving up on a cone and switching to another cone changes as the number of seeds available declines. Sitka spruce began to shed seeds in autumn, many months before the Norway spruce. The spring shedding of seed in Norway spruce was similar to that of Scots pine (Summers and Proctor, 2005). The early start to seed dispersal by Sitka spruce is a trait of most non-serotinous North American conifers and is believed to be a strategy to reduce seed losses to pine squirrels Tamiasciurus spp., which begin to remove and cache cones as soon as they have developed (Benkman et al., 2010). Seeds dispersed in autumn then lie on the ground all winter and spring before germinating. During this period, they may be lost to other seeds-eaters such as rodents and beetles (Nystrand and Granström, 1997, 2000). In northern Europe, red squirrels Sciurus vulgaris do not have the same caching tendency (Gurnell, 1987), so there has been less selective pressure on Norway spruce or Scots pine to disperse seed early. Norway spruce cones are bigger and heavier than Sitka spruce cones, and the larger cones exceed the mass of common crossbills; c. 40 g (Marquiss, 1980) (Figure 2). This would make it difficult for crossbills to remove and manipulate cones between the bill and feet, a common method when extracting seeds (Newton, 1972; Benkman, 1987). This probably accounts for the relatively small Norway spruce cones that crossbills did remove and drop from trees (Table 1). It would appear that crossbills are limited to removing cones up to about a third of their body mass. When crossbills were observed foraging on cones attached to trees, it is likely that large cones were involved. Sitka spruce cones have thin papery scales that provide little defence against foraging by common crossbills. In North America, the crossbills (also Loxia curvirostra) that are adapted to foraging on Sitka spruce cones are smaller than the common crossbills of Europe and have smaller bills: bill depths of 8.55 mm for males and 8.37 mm for females (Irwin, 2010). This contrasts with bill depths of 10.7 mm for male and 10.5 mm for female European common crossbills (Knox, 1976). Therefore, it is likely that the common crossbills of Europe feed less efficiently than those in North America. By contrast, the scales of Norway spruce are leathery and three times thicker than Sitka spruce cones (Summers and Broome, 2012). Even though common crossbills are adapted to forage on Norway spruce (Lack, 1944), it is presumably more difficult for crossbills to remove seeds from Norway spruce cones than Sitka spruce (Benkman, 1993) and may explain the heavy use of Sitka spruces by common crossbills in Scotland (Summers and Broome, 2012). However, a penalty for this choice of tree is that the seed size is small (Marquiss and Rae, 1994), and this presumably limits the intake rate. Only one Scottish crossbill was captured close to the study sites and no Scottish Crossbills were tape recorded in the stands of spruce. This suggests that it is common crossbills that largely rely on spruces in Scotland and that the two species rarely overlap in their use of spruce (Jardine, 2002; Summers and Broome, 2012). One conservation concern is that hybridization with Scottish crossbills is more likely when both species share other conifers, such as lodgepole pine (Summers and Broome, 2012), particularly in years when there are no Sitka spruce cones (Broome et al., 2007). To date, however, cases of hybridization have only been recorded between parrot and Scottish crossbills in Caledonian pinewoods (Summers et al., 2007), though it would probably be more difficult to detect hybridization between Scottish and common crossbills when nesting in plantations where the tree density is much higher than in Caledonian pinewoods. Supplementary data Supplementary data are available at Forestry online. 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Journal

Forestry: An International Journal Of Forest ResearchOxford University Press

Published: Oct 1, 2018

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