Oecologia (2001) 127:435Ð443 DOI 10.1007/s004420000596

Ola Olsson á Ulf Wiktander á Andreas Malmqvist Sven G. Nilsson Variability of patch type preferences in relation to resource availability and breeding success in a bird

Received: 22 February 2000 / Accepted: 13 November 2000 / Published online: 8 February 2001 © Springer-Verlag 2001

Abstract This paper investigates how variability in par- overall food availability. This conclusion is strengthened tial foraging preferences for patch types can be used as a by two additional facts: the preference for lime corre- behavioral indicator of the energetic value of that patch lates positively (1) with the average giving-up density of type, and of overall food availability in the territory. The food, which has previously been shown to estimate over- species studied was the lesser spotted woodpecker all food availability in the territories, and (2) with repro- (Dendrocopos minor) and the patch types it uses are four ductive success, at least during the early stages of repro- groups of tree species (oak Quercus robur, birch Betula duction. pendula, B. pubescens, alder Alnus glutinosa, and lime Tilia cordata), in which it feeds upon wood-living insect Keywords Foraging preferences á Giving-up density á larvae. We partition the variation in foraging preferences Food availability á Reproduction á Dendrocopos minor into three scales. Firstly, within territories, the foraging preference for a tree species group was positively related to the prey density in that species group. That is, the Introduction preferences measure the patch types’ energetic profit- abilities. This result should be general in cases like the It is common to find that animals do not use resources in present, where the costs of using different alternatives do relation to their availability. Some are used more than not differ substantially. It may therefore be the preferred expected by chance, i.e., preferred, whereas others are behavioral indicator in determining the relative benefits used less (e.g., McDonald et al. 1990; Podolsky and associated with different alternatives. Secondly, between Price 1990; Crist and MacMahon 1992; Whitehead et al. the seven years of study, much of the variation in tree 1995). Many of the patterns of resource use can obvious- species group preferences was attributable to measured ly be thought of as species-specific (e.g., McDonald et fluctuations in the density of one important prey species al. 1990; Moser et al. 1990), and some are considered as (Argyresthia goedarthella, Argyresthidae, Lepidoptera), individual-specific characteristics (Sherratt and Mac- which occurred in some years on birch, in others on al- Dougall 1995). However, there is ample evidence that der, and in one year was virtually absent. Thus, in con- foraging preferences are variable within both species and cordance with the previous result, the values of these individuals in both space and time (Schooley 1994; tree species groups fluctuated between years according Arthur et al. 1996). Based on predictions from foraging to prey density. Thirdly, between territories, we found theory (MacArthur and Pianka 1966; Lucas 1983; that the preference for one tree species, lime, was higher Stephens et al. 1986; Mitchell 1989) we should expect in areas where it was more abundant. We attribute this to the extent to which a resource is used to be related to the the fact that the density (per patch) of at least one impor- fitness inputs an animal is expecting from it. If so, ecolo- tant prey species (Stenostola dubia, Cerambycidae, Cole- gists should be able to use foraging preferences as a be- optera) on lime increased with the abundance of its host havioral indicator of how the individual values different tree species in the territory. That is, the overall food alternatives. If both costs and gains may differ between availability was higher in territories where lime was alternatives, foraging preferences are likely to reflect the more common. Hence, the preference for lime estimates trade-off between these (Holbrook and Schmitt 1988) and may yield a complicated picture. In such cases, these O. Olsson (✉) á U. Wiktander á A. Malmqvist á S.G. Nilsson costs may best be evaluated applying patch use theory Department of Ecology, Animal Ecology, Lund University, Ecology Building, 223-62 Lund, Sweden (Brown 1988). However, in cases where costs are instead e-mail: [email protected] likely to be similar among alternatives the preferences Tel.: +46-46-2223817, Fax: +46-46-2224716 should straightforwardly reflect the foragers’ expected 436 energetic gains from using that alternative (Mitchell Olsson 1998; Wiktander et al., in press a). This food, 1989). Thus, foraging preferences could be a powerful however, seems to be relatively plentiful in all territories, and general way to estimate the energetic rewards that and does not seem to constrain food supply or create be- foragers gain from specific foods. So far, they have rare- tween-territory differences in breeding success. ly been used to make such inferences. In this paper, we will show how the patch type (tree In this paper we study the lesser spotted woodpeck- species group) preferences vary in a population of lesser er’s (Dendrocopos minor) preferences among groups of spotted woodpeckers. We will consider how the prefer- tree species (oak Quercus robur, birch Betula pendula, ences (within territories) for four tree species groups are B. pubescens, alder Alnus glutinosa, and lime Tilia cor- related to their respective prey densities, how these pref- data), that are likely to vary in energetic reward, but not erences vary between years with different food availabil- in energetic or predation-related costs associated with ity, and between territories between which reproductive using them. success varies. We will evaluate to what extent the forag- The lesser spotted woodpecker inhabits deciduous ing preferences can be used as a behavioral indicator to and mixed deciduous/coniferous forests in the Palearctic. the energetic value a tree species has to the woodpeck- From early autumn to late spring (August to May), it ers. In addition we will evaluate to what extent they can feeds almost exclusively on wood-living insect larvae in be used to estimate overall food availability in the terri- thin dead tree branches, mostly in living trees (Cramp tories, and how well they indicate territory quality, i.e., 1985; Olsson 1998). Most of the prey are larvae of Cer- reproductive success. ambycid beetles, such as Stenostola dubia (Ceramby- cidae, Coleoptera), and these are to a great extent special- ists on their host tree species (Palm 1959). An exception Methods to this is when it feeds on larvae of the moth Argyresthia goedarthella (Aryresthidae, Lepidoptera). These occur Study area abundantly in the years when either birch or alder bloom (Agassiz 1987). A. goedarthella eggs are laid in the male The study was conducted in a 150-km2 study area in the hemibo- catkins of the trees, but in spring when the flowers de- real vegetation zone in southern Sweden (56¡ 40′N, 14¡10′E) be- tween 1990 and 1997. The landscape is dominated by coniferous velop the larvae move down to the lower regions of the forest, mainly spruce (Picea abies), but with deciduous forests and trees and bore into the trunk bark or into dead branches. agricultural land occurring patchily, particularly on richer soils Here they are accessible to the woodpeckers. and close to lakes. The forested parts of the study area are divided The variable occurrence of A. goedarthella, and per- into homogeneous stands (average size: 3.6 ha, SD 3.3), according to dominating tree species and age of the trees. Most non-conifer- haps also population fluctuations of other prey species, ous stands contain a mix of several tree species. The forests in the inevitably lead to the value of tree species fluctuating be- study area are generally managed for timber production, although tween years. However, prey density within and between many of the deciduous forests are cautiously managed, with some tree species may also vary between territories. consideration of conservation. In a previous study (Olsson et al. 1999), we used a technique based on giving-up densities (GUDs, i.e., the Estimation of foraging preferences number of prey left in exploited patches, cf. Brown 1988) to infer that the most important component of ter- Foraging behavior and breeding success were observed in 12 non- ritory quality of this species is the availability of food overlapping territories (average size 205 ha; Wiktander et al., in press b), in which a total of 68 different color-banded lesser spot- several weeks before egg laying. In depleting patches, ted woodpeckers occurred during the 7 years (1990Ð1996) when GUDs measure the forager’s intake rate when it decides foraging observations were made. Data collection started each to leave the patch. Therefore, GUDs contain information year on 21 March and lasted until the day when oaks burst into about the animal’s foraging costs (e.g., Brown 1988, leaf (3Ð20 May; Wiktander et al., in press a) as at that time the woodpeckers started to glean surface-living insects from the fo- 1999). By combining measures of GUDs with measures liage (Török 1990; Olsson 1998). of patch residence times and fitness it is possible to de- We collected the great majority of data from birds that were lo- termine which is the most important environmental or in- calized by radio tracking. We localized birds that remained with- dividual factor determining the variation in fitness out a radio transmitter by carefully walking through all parts of the territory, and adjacent areas. There we listened for drummings and among individuals (Olsson and Holmgren 1999; Olsson vocalizations, which are performed to the same extent by both et al. 1999). The foraging variables were measured dur- sexes. Once found, the birds can usually be followed for a period ing the pre-breeding period, i.e., when the woodpeckers (several minutes to 1 h), as they are moving through the forest. are specialized on the dead-wood fauna. We found that Therefore, regardless of where the individuals were found, they the average GUDs of a breeding pair correlated positive- were often observed for long enough periods that they moved to entirely different parts of the territory. Thus, all observations are ly both with its average patch residence time, and its re- likely to be representative of the woodpeckers’ actual habitat use. productive success (Olsson et al. 1999). From this, we The tree species in which the woodpeckers foraged were not- concluded that food availability weeks before egg laying ed, and the time spent feeding in each tree was measured. These was essential in determining the success of the breeding data, together with the stand location, were noted in the field. We measured foraging behavior separately within each forest pair. During egg laying and the rest of the breeding peri- stand where observations were made (average 7.3 stands with ob- od, the woodpeckers switch to glean surface-living in- servations per territory and year). We thus minimized the potential sects that become available at leafing (Török 1990; risk that our definition of the territory reflects tree species avail- 437 ability incorrectly. In addition, the stand is a spatial scale within goedarthella larvae were counted. This was done in a number of which the woodpeckers have to select individual trees, of one or randomly selected alders in several territories each year, i.e., inde- another species, rather than the general area for foraging. In order pendently of whether the woodpeckers had been foraging on these to calculate one preference index for each tree species group for trees or not. Alders were sampled in nine different territories. Four each territory, we pooled the observations of the individuals in all of these were sampled in all types of years. Due to the irregular used stands in each territory. Thus, in the analyses, we used one shape of the trunk bark of birches, the corresponding estimate time-weighted average for each territory. could not be made for these species. The tree species composition and total density of trees was es- Secondly, in 1995 three to four branches, from three to four timated in each forest stand using the quarter method (Cottam and randomly selected trees from each of the four tree species groups Curtis 1956). A grid with 50 m mesh size was placed over each (oak, birch, alder, and lime) were cut down in seven of the territo- territory. At each grid point the nearest tree with diameter at breast ries in the study area. A maximum of 90 cm of length was saved height 10 cm or more in each quadrant was identified to species, from each branch. Branches shorter than 90 cm were saved in their and the distances to these trees were measured. These data give entirety. In order to estimate the number of prey of all species in both the proportions of trees of each species group and the total the branches we X-rayed them using a 10-kW mammograph with density of trees in each stand. Thus, the average proportion of Mo anode and 0.6 mm focus size. Exposure times varied accord- trees of all different species was estimated for the 12 breeding ter- ing to branch diameter from 0.04 to 0.4 s at 25 kV. To acquire high ritories. resolution images we used Kodak MIN-R cassettes with a green- Preference indices were calculated for the four most used tree emitting Gd2O2S amplifying screen and single emulsion Fuji species groups (oak Quercus robur, birch Betula pendula, B. pu- MI-NH film. From the radiographs, we could count the number of bescens, alder Alnus glutinosa, and lime Tilia cordata) and for all available prey items. The prey density was then calculated as the other species lumped together. The species in this latter group in- number of prey per 1 dm2 of surface area of branches. cluded spruce (Picea abies), beech (Fagus sylvaticus), aspen Thirdly, using the same X-ray technique, we estimated the av- (Populus tremula), sallow (Salix caprea), pine (Pinus silvestris) erage GUD in a sample of branches on which the woodpeckers and rowan (Sorbus aucuparia), and some other rare and rarely had been observed to forage. That is, the woodpeckers were ob- used species. Birches were used for approximately 36% of the for- served at sufficiently close ranges to identify the individual branch aging time, oak, alder and lime approximately 16% each. All other where they were foraging. When they were foraging on branches species were used for 6% of the time or less. Approximately 37% that could be reached from the ground (c. 12 m above ground) the of the trees in the territories were birches, 17% oaks, 5% alders branch was memorized and subsequently cut down within a few and 2% limes. In addition, 32% of the trees in the territories were hours, before there was any risk of a woodpecker revisiting. Only spruces, 2% aspens, 1% rowans. All other species occurred at less the part of the branch where the woodpecker had been searching than 1%. for prey was collected. This sampling was done in the years To compute preferences we used the maximum likelihood esti- 1993Ð1996. When comparing GUD values with preference values α α mator , which is a vector of i (Chesson 1983): we used data only from the years when we had observations of both variables from the same territory. Both variables were then Ui averaged within territories, and we used these averages for subse- f α = i (1) quent analyses. For further details of the GUD technique, please i l U refer to Olsson et al. (1999). ∑ j = f Finally, during April and early May in 1997 we selected J 1 j 17 forests in which there was a high proportion of lime. These for- where Ui is the use of species i, fi is the (relative or absolute) ests were chosen to get a range of sizes (range 0.2Ð18 ha) and den- availability of the species, and a total of l species are considered in sities of lime trees (range 6Ð65 haÐ1). Three of these areas coincid- the study. That is, the subscript j refers to all tree species, includ- ed with the woodpecker territories. In each area, the density of ing i. The index is hence the utilization of species i standardized limes was estimated by direct counting. We then selected five for its availability, and therefore allows us to compare use when limes randomly, and from each of these, we cut down two dead availability varies. Use in direct relation to availability means that branches of diameter ranging from 1.5 to 3.5 cm. From each, one α i=1/l. Values larger than this indicate preference, and smaller val- 50-cm-long piece was saved. Only clearly dead branches (without ues indicate avoidance of the species. As the indices are based on leaves or buds) and with at least 75% bark cover were sampled. α a total of five species (or species groups) a value of i=0.2 means Thus, we tried to sample the types of branches most used by the that tree species i is used in relation to its abundance in the stand. woodpeckers for foraging (Olsson 1998). These branches were α As is desirable for a measure of preference, i does not vary with then stored in paper tubes (one per tree), and emerging adult bee- fi unless behavior changes with fi. The use (Ui) is measured in time tles were collected as they hatched. The collection proceeded dai- units, and the availability (f ) as the proportion of all stems in a ly, from the sampling of the branches and until 1 week after the i α stand that belongs to species i. i can be considered as multivari- last beetle emerged. Several species of cerambycid beetles were ate normal random variables (Chesson 1983), and the normal para- found, but only S. dubia was found in sufficient numbers to allow metrical statistical procedures apply. If hypotheses about equality useful analysis. α α of all i are tested it is necessary make adjustments to (Chesson 1983). In the present case, however, we are only interested in the four commonest species groups (oak, birch, alder, and lime). The Reproductive success remaining “species”, which is a group of all other species pooled, is obviously not an ecologically homogeneous entity. Therefore, To estimate reproductive success, we measured relative laying we are not interested in making inferences about the contrasts be- date, clutch size and brood size. All three measures are tightly cor- tween this group and the other tree species. Thus, we will base all related with one another, and relative laying date furthermore in- results and analyses on only the preferences for oak, birch, alder, fluences the number of recruits produced and the survival of and lime, and we can use these values without adjustments. young breeding females (Wiktander et al., in press a). In fact, lay- ing date is a better predictor of number of recruits than clutch size or brood size. The laying dates were established by inspecting Estimation of prey density nests daily with a mirror, during the time when laying was expect- ed, until the first egg appeared. Clutch size was then counted by Prey density was measured in four ways. Firstly, the available again inspecting the nests until no more eggs appeared. Brood size density of A. goedarthella larvae in the trunk bark of alder was es- was the number of surviving nestlings leaving the nest. The rela- timated by scaling off the outer bark layer with a knife in a ran- tive laying date is the date of the first egg laid by the breeding pair domly selected 2-dm2 squares 1.5 m above ground. All visible A. minus the date of the median laying date in the population in the 438 year. That means that pairs laying relatively early in the season have a negative value, and those laying late have a positive one. The median laying dates varied between 5 and 23 May over the years (Wiktander et al., in press a).

Statistical analyses

When relating the tree species preferences to reproductive success, only one measure per pair can sensibly be used. Thus, in these cases we averaged the preference indices of the male and the fe- male, weighted by the observation time per individual. We are interested in both within- and between-year differences in tree species preferences. However, we will confine the between- year analysis to the difference between four types of years, rather than the between-year difference in general. The blooming of birches and/or alder, i.e., the potential for A. goedarthella to occur in these species, identifies the four types of years. Only birches bloomed in 1990 and 1996 (1), only alders in 1991 and 1995 (2), both species in 1992 and 1993 (3) and neither in 1994 (4). To test whether the woodpeckers’ preferences for the four tree species groups differed in the different types of years, we per- formed a repeated-measures ANOVA with two trial factors (Wilkinson et al. 1992), tree species group and type of year, and the territories as the subjects. When analyzing between-territory differences in preferences, we first accounted for the between-year differences by producing the residuals from a one-way ANOVA with type of year as a fac- tor, and then averaged these residuals for each territory, to get one single estimate per territory, and hence avoid pseudo-replication (Hurlbert 1984). We then used the averaged residuals (which we call adjusted preferences) for testing various between-territory ef- fects. The other variables, i.e., GUD and reproductive success measures, were simply pooled within territories, without removing Fig. 1 A The average (±SE) of natural logarithms of prey density any between-year-group differences. of the four most used tree species groups in seven territories sam- In all cases when we have used parametric tests we have in- pled in 1995. B The preferences for these tree species in the same spected the residuals using Q-Q plots (Sokal and Rohlf 1995) to territories verify their normality.

four territories (random factor: F3,69=0.94, P=0.4), and Results no significant interaction (F3,69=1.18, P=0.3). Because of this, we wanted to test to what extent the Within territories preferences for the tree species were different, and if the preferences for a tree species varied between years For the data on prey density (available only from (Figs. 1, 2). Using repeated-measures ANOVA, we found 1995), we tested whether, within each territory, there that the differences in preferences for the different tree was a correlation between prey density in a tree species species were indeed significantly different (F3,15=6.03, and its preference index. In all seven territories there P=0.006). As expected, there was no between-year effect was a positive relation between prey density and prefer- on the average preferences (F3,15=2.17, P=0.15), i.e., the ence, i.e., the regression coefficients were in all cases average value of preference for a tree species was close greater than zero (t=4.70, n=7 territories, P=0.003). Av- to 0.2 in all years. Nevertheless, the preferences for a erage preference index for a tree species (Fig. 1A) in- given tree species varied between types of years (interac- creased with increasing prey density in the species tion term; F9,45=4.38, P=0.0005). Most strikingly, the (Fig. 1B). blooming of birch and alder heavily influenced the pref- erences for these tree species(Fig. 2). Considering the preference for alder separately, we Between years found that when averaged over all territories observed in a year, this preference was strongly influenced by the av- In the four territories where we sampled A. goedarthella erage density of A. goedarthella in the same year in years both with and without alder bloom, we found a (r2=0.87, n=7 years, P=0.002, Fig. 3). Therefore, it difference in the densities of these larvae. When alders seems as if the between-year differences in preferences bloomed the density was on average 2.2 larvae dmÐ2 are to a great extent determined by the dynamics of A. whereas during other years it was only 0.2 larvae dmÐ2. goedarthella. The effect of blooming (fixed factor) was clearly signifi- cant in a mixed model ANOVA (F1,3=13.03, P=0.036), whereas there was no significant difference between the 439

Fig. 3 The preference index for alder plotted against the density of Argyresthia goedarthella larvae in the trunk bark of alders. Each point is the average of all the territories in a year, in which we obtained data on both A. goedarthella density and the wood- peckers’ preference

Fig. 2 The average preference indices for different tree species Fig. 4 The adjusted preference for lime plotted against the num- groups by individual lesser spotted woodpeckers observed during ber of limes per hectare in the 12 territories. the four types of years studied. The types of years are defined by which tree species bloomed, and None refers to the years when neither alder nor birch bloomed. The number of territories ob- served in each year (N) is shown under the graph. Error bars indi- stola emerged correlated significantly with lime density cate 95% confidence limits, and the dashed lines indicates use in (r2=0.39, n=17 areas, P=0.007). relation to availability, i.e., α=0.2 In contrast to the result on the between-year scale, we found that within the different types of years, we could Between territories not explain the preference for alder in a territory by the A. goedarthella density alone. That is, the adjusted pref- We found that the infestation rate of S. dubia per lime erences for alder did not correlate with the between-year- tree increased with increasing density of limes in the for- type residuals for the A. goedarthella density (r2=0.20, est area. That is, the number of trees from which Steno- n=9 territories, P=0.23). 440

Fig. 6 Adjusted preference index for lime plotted against average giving-up density (GUD) in the 10 territories where both variables were estimated

spective tree species in the territories (r2=0.16, P=0.3; r2=0.21, P=24; r2=0.03, P=1 respectively, n=12 territo- ries in all cases). These reported P-values are one-tailed, as we would not be able to sensibly interpret negative re- lations, and would hence treat them as non-significant. They are also, however, Dunn-Sidak-corrected for four multiple comparisons (Sokal and Rohlf 1995), as we are giving ourselves four chances of a type-I error. Further- more, the preference for lime was also correlated with the number of lime trees in the 200-ha area around the center of activity of the woodpeckers (r2=0.32, n=12 ter- ritories, P=0.026). Breeding success of the woodpeckers was positively related to the preference for lime (Fig. 5A). We found this by entering the adjusted preferences for the four tree species groups in a stepwise multiple regression against the average relative laying date in each territory. Only lime entered the regression as a significant predictor of laying date (r2=0.38, n=12 territories, P=0.033). The par- tial correlations for the other tree species were not even close to significance (birch: rp=Ð0.16, P=0.6; alder: rp=0.35, P=0.3; oak: rp=Ð0.07, P=0.8; n=12 in all cases). Also the number of eggs produced (Fig. 5B) was strong- ly positively related to the adjusted preferences for lime (r2=0.55, P=0.006, n=12), but not to any other tree spe- cies (birch: rp=Ð0.005, P=1; alder: rp=0.37, P=0.3; oak: Fig. 5 A The average relative laying date in the 12 territories, r =Ð0.48, P=0.13; n=12 in all cases). Finally, the number plotted against the adjusted preference for lime in the same territo- p ries. B The average brood size in the same territories. C The aver- of fledglings were weekly positively related to the ad- age clutch size in the same territories justed references for lime (Fig. 5C; r2=0.27, P=0.084, n=12), but not at all to the other tree species (birch: rp=Ð0.14, P=0.7; alder: rp=0.38, P=0.25; oak: rp=Ð0.15, P=0.7; n=12 in all cases). The woodpeckers’ preference for lime in a territory We found a positive relation between the average was higher the higher the density of limes in the territo- GUD and the adjusted preferences in a territory (Fig. 6, ry. That is, the adjusted preference for lime correlated r2=0.44, n=10 territories, P=0.037). This indicates that significantly positively with the number of limes per the adjusted preferences, like the average GUDs, esti- hectare in the used forests (Fig. 4, r2=0. 46, n=12 territo- mate food availability in the territories. ries, P=0.030. In contrast, the preferences for birch, al- der, and oak did not correlate with the densities of the re- 441 Discussion triguingly however, use of e.g., alders before the occur- rence of A. goedarthella larvae is very rarely observed Within territories (O. Olsson, own observation; Olsson 1998).

Within territories in one year, the woodpeckers consis- tently preferred tree species according to their prey den- Between territories sity. This confirms the value of patch type preferences as a good behavioral indicator of the energetic value of the Between territories, there is a chain of results leading us patch type, i.e., tree species, within a territory. That is, to conclude that the preferences for lime measures over- the preferences are the woodpeckers’ own ranking of the all food availability in the territories. available alternatives. We have shown here that, as ex- Firstly, the amount of lime in an area predicts the den- pected from foraging theory (e.g., Stephens et al. 1986; sity of at least one important species of prey (S. dubia) Mitchell 1989), this ranking corresponds very well with for the woodpeckers. Secondly, the amount of lime in a prey abundance on the tree species in question. The ex- territory also predicts the woodpeckers’ preference for pectations of foraging theory are, however, based on the that species in a territory. We hence conclude that the ab- assumption that costs are not very different between al- solute value of lime in a territory, in terms of prey densi- ternatives (e.g., Holbrook and Schmitt 1988; Lima and ty, determines the absolute preference for lime in that ar- Dill 1990). In this case, where the alternatives are tree ea. Note that this is different from the comparisons of species that are structurally similar, and mostly occur relative values made at the within-territory scale. Third- side by side in mixed species stands, costs should not ly, the preferences for the other tree species seemed to be differ. There are probably numerous other cases where determined by the preference for lime, rather than by the this assumption holds. In such cases, we may regard the availability of these other tree species themselves or, preferences for a foraging alternative as a general, easily e.g., between-territory differences in density of A. goe- obtainable and straightforward indicator of the energetic darthella. This gives lime a seemingly pivotal role, pos- value of that alternative. We propose that, for many spe- sibly because the values of the other tree species do not cies, foraging preferences may be a useful management differ much between territories. tool to find out the values of different foods, without la- We therefore propose that, in our study area, the prefer- borious sampling and analysis of prey density, handling ence for lime is a measure of the total food availability in a times, and attack rates. In cases where costs are likely to territory. This conclusion is further strengthened by the differ between alternatives, GUDs may be a preferred in- positive influence the lime preference had on our fitness dicator, having the advantage of incorporating total fit- measures. That is, the higher the preference for lime (ad- ness inputs (Brown 1988; Olsson and Holmgren 1999; justed for between-year variations), the earlier the wood- Olsson et al. 1999). However, the use of GUDs cannot peckers laid their eggs and the larger clutches they pro- reveal the benefits associated with exploiting different duced. Like in many other bird species in temperate re- alternatives, only their costs. gions (e.g., Källander 1974; Daan et al. 1988; Daan et al. 1990) the lesser spotted woodpeckers’ clutches that are initiated first are those that contribute to the largest num- Between years ber of offspring and most recruits to the breeding popula- tion (Wiktander et al., in press a). However, we found only Between years, most of the variation in preferences is re- a rather weak (not significant) relation between the prefer- lated to the fluctuations of the prey species A. goedarth- ence for lime and the number of fledglings produced. ella, which in turn is dependent on availability of catkins Therefore, we dare not conclude that this preference indi- of birch and alder. Thus, the blooming of these tree spe- cates the prospective fitness of the parents, only their re- cies, which is synchronous (within each species or ge- productive success during the early breeding stages. nus) over large regions, determines much of the wood- Nevertheless, this means that in our system the pref- peckers’ behavior. Such between-year variation deter- erence for lime can be interpreted as a behavioral indica- mined by extrinsic factors has been reported for several tor of food availability in the breeding territory, before species (e.g., Steenhof and Kochert 1988; Miller et al. the onset of breeding. Unlike other behavioral indicators, 1994; Kinnaird et al. 1996) but has probably also often e.g., GUD, vigilance levels and patch-residence times been concealed by pooling data from different years (e.g., Brown 1988; Olsson and Holmgren 1999; Brown (Schooley 1994). 1999) the foraging preference for a particular tree spe- The phenomenon is similar to prey switching (e.g., cies, occurring mixed with other species, should not con- Leckie et al. 1998; Bond and Kamil 1998). Unlike in a tain information about the total fitness value of an envi- standard prey-switching case, however, the encounter ronment. That is, there is no reason to argue that, e.g., rates with different tree species remain constant in an ar- predation costs could be measured by the preference in- ea from year to year; only their profitabilities may vary. dex between territories. This is however an advantage in As the prey are hidden in the wood or bark of the so far as it makes it a pure measure of food availability. trees the woodpeckers cannot estimate their densities Thereby the positive relation between the preference without sampling currently unprofitable tree species. In- for lime and the average GUD in the territories verifies 442 the conclusions from a previous study (Olsson et al. References 1999). Olsson et al. (1999) concluded that food avail- ability was the main difference between territories that Agassiz DJL (1987) The British Argyresthiinae and Yponomeuti- caused variation in reproductive success. This conclu- nae. Proc Trans Br Entomol Nat Hist Soc 20:1Ð26 sion was based on the patterns of how average GUD Arthur SM, Manly BFJ, McDonald LL, Garner GW (1996) As- sessing habitat selection when availability changes. Ecology and average patch-residence times varied with repro- 77:215Ð227 ductive success. However, in that study there was no in- Bond AB, Kamil AC (1998) Apostatic selection by blue jays pro- dependent measure of food availability. This data set duces balanced polymorphism in virtual prey. Nature 395: provides one, and we may be confident of the value of 594Ð596 using GUDs and that the main differences in territory Brown JS (1988) Patch use as an indicator of habitat preference, predation risk, and competition. Behav Ecol Sociobiol 22: quality to the woodpeckers lay in differences in food 37Ð47 availability. Brown JS (1999) Vigilance, patch use and habitat selection: For- We must also emphasize that, unlike GUD and patch- aging under predation risk. Ecol Evol Res 1:49Ð71 residence time, the preference for lime per se (on the be- Chesson J (1983) The estimation and analysis of preference and its relationship to foraging models. Ecology 64:1297Ð1304 tween-territory scale), may not be a very general behav- Cottam G, Curtis JT (1956) The use of distance measures in ioral indicator for lesser spotted woodpeckers in other phytosociological sampling. Ecology 37:451Ð460 areas (e.g., northern Scandinavia or Central Europe, or Cramp S (1985) The birds of the Western Palearctic, vol IV. Ox- even other parts of southern Sweden). One reason is that ford University Press, Oxford Crist TO, MacMahon JA (1992) Harvester ant foraging and shrub- in our study area lime is on the generally commoner steppe seeds: interactions of seed resources and seed use. than in many other areas. We find it reasonable to be- Ecology 73:1768Ð1779 lieve that the dependence of S. dubia on the host tree Daan S, Dijkstra C, Drent RH, Meijer T (1988) Food supply and density is connected to the species’ dispersal and host the annual timing of avian reproduction. Proc Int Ornithol finding. However, in other areas the density of limes Congr 19:392Ð407 Daan S, Dijkstra C, Tinbergen JM (1990) Family planning in the may be too low to host a population of S. dubia at all. kestrel Falco tinnunculus: the ultimate control of covariation Hence, the densities of S. dubia, and perhaps other spe- of laying date and clutch size. Behaviour 114:83Ð116 cies, may not reach levels where they are profitable at Holbrook SJ, Schmitt RJ (1988) The combined effects of preda- all for the woodpeckers. On the other hand, several oth- tion risk and food reward on patch selection. Ecology 69: 125Ð134 er tree species are very rare in our study area, e.g., Hurlbert SH (1984) Pseudoreplication and the design of ecological beech (Fagus sylvatica), ash (Fraxinus excelsior), and field experiments. Ecol Monogr 54:187Ð211 elm (Ulmus glabra). These certainly occur more abun- Källander H (1974) Advancement of laying of great tits by the dantly elsewhere, and the wood-living fauna on them provision of food. Ibis 116:365Ð367 Kinnaird MF, O’Brien TG, Suryadi S (1996) Population fluctua- may show the same host-density dependence as do S. tion in sulawesi red-knobbed hornbills: tracking figs in space dubia in our area. Thus, the pivotal role played by lime and time. Auk 113:431Ð440 in our study may be played by other species in other ar- Leckie FM, Thirgood SJ, Redpath SM (1998) Variation in the diet eas. That, however, will have to be evaluated on a case- of red foxes on Scottish moorland in relation to prey abun- by-case basis. Furthermore, in cases where the main be- dance. Ecography 21:599Ð604 Lima SL, Dill LM (1990) Behavioral decisions made under the tween-territory differences in food availability do not risk of predation: a review and prospectus. Can J Zool 68: depend on differences in the value of a single patch 619Ð640 type, but rather on factors such as overall patch density Lucas JR (1983) The role of foraging time constraints and variable or habitat patch size, the kind of results we got may not prey encounter in optimal diet choice. Am Nat 122:191Ð209 MacArthur RH, Pianka ER (1966) On optimal use of a patchy en- be expected. vironment. Am Nat 100:603Ð609 McDonald LL, Manly BFJ, Raley CM (1990) Analyzing foraging Acknowledgement We are grateful the assistance in the field and habitat through selection functions. Studies Avian Biol from Anders Stagen, Fredrik Östrand, Leif Appelgren, Fredrik 13:325Ð331 Haas, Martin Stjernman, Anna Fohrman, and Simon Schubert, and Miller CK, Knight RL, McEwen LC, George TL (1994) Respons- for help in the laboratory from Shahrzad Bakthiar. We also thank es of nesting savannah sparrows to fluctuations in grasshopper Gudmund Swahn, at the Department of X-ray technology at Lund densities in interior Alaska. Auk 111:962Ð969 University Hospital. The field work was partly financed by WWF Mitchell WA (1989) Informational constraints on optimally forag- Sweden, Swedish Ornithological Society, Stiftelsen Oscar och ing hummingbirds. Oikos 55:145Ð154 Lilli Lamms Minne, and Stiftelsen Lunds Djurskyddsfond. The Moser EB, Barrow WC, Hamilton RB (1990) An exploratory use manuscript has improved by discussions and suggestions from of correspondence analysis to study relationships between avi- Jan-Åke Nilsson. William Block, Gitogo Maina, Jason Moll, an foraging behavior and habitat. Stud Avian Biol 13:309Ð317 Michael Morrison, Scott Robinson, and two anonymous referees Olsson O (1998) Through the eyes of a woodpecker: understand- provided valuable comments on an earlier version of the manu- ing habitat selection, territory quality and reproductive success script. from individual behaviour. PhD dissertation, Lund University Olsson O, Holmgren NMA (1999) Gaining ecological information about Bayesian foragers through their behaviour. I. Models with predictions. Oikos 87:251Ð263 Olsson O, Wiktander U, Holmgren NMA, Nilsson SG (1999) Gaining ecological information about Bayesian foragers through their behaviour. II. A field test with woodpeckers. Oikos 87:264Ð276 443 Palm T (1959) Die Holz- und Rinden-Käfer der Süd- und Mittel- Török J (1990) resource partitioning among three woodpecker schwedischen Laubbäume. Opusc Entomol Suppl 16:1–421 species (Dendrocopos spp.) during the breeding season. Hol- Podolsky RH, Price MV (1990) Patch use by Dipodomys deserti arct Ecol 13:257Ð264 (Rodentia: Heteromyidae): profitability, preference, and deple- Whitehead SC, Wright J, Cotton PA (1995) Winter field use by the tion dynamics. Oecologia 83:83Ð90 European starling Sturnus vulgaris: habitat preferences and the Schooley RL (1994) Annual variation in habitat selection: patterns availability of prey. J Avian Biol 26:193Ð202 concealed by pooled data. J Wildl Manage 58:367Ð374 Wiktander U, Olsson O, Nilsson SG (in press a) Annual and sea- Sherratt TN, MacDougall AD (1995) Some population conse- sonal reproductive trends in the lesser spotted woodpecker quences of variation in preference among individual predators. Dendrocopos minor. Ibis Biol J Linn Soc 55:93Ð107 Wiktander U, Olsson O, Nilsson SG (in press b) Seasonal varia- Sokal RR, Rohlf FJ (1995) Biometry. Freeman, New York tion in home range size, and habitat area requirement of the Steenhof K, Kochert MN (1988) Dietary responses of three raptor lesser spotted woodpecker (Dendrocopos minor) in south Swe- species to changing prey densities in a natural environment. J den. Biol Conserv Anim Ecol 57:37Ð48 Wilkinson L, Hill M, Vang E (1992) SYSTAT for the Macintosh, Stephens DW, Lynch JF, Sorensen AE, Gordon C (1986) Prefer- version 5.2. Systat, Evanston ence and profitability: theory and experiment. Am Nat 127: 533Ð553