INTRODUCTION

For woodpeckers, which are typically forest birds, the most crucial sites where they collect food are trees. Some woodpecker species are strictly connected with specific tree species or trees with specific characteristics, used as foraging sites. For example, the Middle Spotted Woodpecker Dendrocoptes medius prefers foraging on large oaks with cracked bark (Pasinelli & Hegelbach 1997), the White-backed Woodpecker Dendrocopos leucotos forages chiefly on dead trees or on dead or dying parts of living trees (Czeszczewik 2009), whereas the Three-toed Woodpecker Picoides tridactylus collects food mainly on dead Norway Spruces Picea abies (Pechacek 2006). In opposite to above mentioned specialized species, the Great Spotted Woodpecker Dendrocopos major is an omnivorous bird and the spectrum of its foraging techniques and sites utilized to collect food is very wide (Michalek & Miettinen 2003). In the breeding season and in the summer a significant part of its food are invertebrates collected from the surface of trunks, branches and leaves, which in winter are replaced by invertebrates living in wood (Pavlík 1997, Jiao et al. 2008). An important component of the diet of this woodpecker is plant food, which mainly consists of seeds of coniferous tree species (e.g. Scots Pine Pinus silvestris, Norway Spruce). It may be the main source of food for the Great Spotted Woodpecker, especially in winter and for northern populations (Hogstad 1971a, Alatalo 1978, Osiejuk 1994). However, in spite of its broad food niche, the Great Spotted Woodpecker may also favour some tree species or specific parts of trees as foraging sites. For example, Smith (2007) revealed that this woodpecker very often foraged on dead branches of living trees whereas Kruszyk (2003) showed its strong preference for oaks and hornbeams.

Differential foraging behaviours of particular woodpecker species leading to resource partitioning may reduce competition for food what allow them to coexist in the same habitat (Alatalo 1978, Vanicsek 1988, Török 1990). Resource partitioning is also common between males and females, what is especially important when food resources are limited (Osiejuk 1998, Pechacek 2006). To minimize intersexual competition for food, each sex can: 1) forage on different parts of the trees, 2) use different foraging techniques, or 3) collect food of varying sizes (Selander 1966, Hogstad 1991, Stenberg & Hogstad 2004, Pechacek 2006). Intersexual niche partitioning of woodpeckers may be connected with sexual dimorphism, which is among others, manifested in differences in bill and body size (Hogstad 1978). Size dimorphism allows males and females utilize different feeding niches. For example, males of Hispaniolan Woodpecker Centurus striatus, possessing a larger bill than females, are better adapted to excavating in the harder wood or thicker bark (Selander 1966). In the case of woodpeckers where sexual dimorphism is not distinct, competition for food between the sexes may be reduced by utilizing separate feeding territories (Hogstad 1978). Moreover, niche segregation may be associated with dominance of males over females, being expressed by aggressive behaviour (Osiejuk 1998, Pasinelli 2000). However, differences in foraging patterns between the sexes of the Great Spotted Woodpecker were studied relatively rarely and none of these studies was conducted under primeval conditions (Hogstad 1978, Osiejuk 1994, 1998).

The main goal of our study was to identify the parameters of the trees and their parts most commonly used by the Great Spotted Woodpecker during foraging, in relation to the sex. We assumed, that some trees or sites on them can provide more food than others and therefore foraging sessions should be the longest in such places. Our assumption was based on foraging theory, which suggests that generally, animals choose for foraging habitats or patches with the greatest density of prey (Stephens & Krebs 1986). In patchy environments, which is the forest for woodpeckers, the foragers continually assess the quality of a patch (in our case the site on the tree) and make decisions as to when to leave a patch, based on their energy intake (Cowie & Krebs 1979). Moreover, apart prey availability in habitat, prey accessibility is essential for animals, that can be affected by e.g. weather conditions, temperature, time of day (Rolstad & Rolstad 2000, Czeszczewik 2009, Wiebe & Gow 2013). The decision to choose a feeding place is also influenced by predation risk, therefore, the places with high prey density but with high predator pressure can be avoided (Cresswell 1994, Heithaus 2005). Taking into consideration availability and accessibility of food we hypothesized that dead substrates would be preferred over living substrates and trees with large dimensions (expressed as a trunk diameter at breast height) would be preferred over trees with small dimensions.

Our second objective was to check whether the same parameters of foraging places influence the duration of the foraging sessions for both males and females. We predicted that there are no differences in this respect and both sexes foraged the longest on sites with similar characteristics. Our assumption was based on fact that the Great Spotted Woodpecker is not a strongly dimorphic species (however males have longer bill than females) and therefore it is more likely that in order to minimize the possible intersexual competition, male and female use separate feeding territories, while their foraging behavior remains the same (Hogstad 1978).

STUDY AREA

The study was conducted in the Białowieża National Park (BNP), located in Polish part of Białowieża Forest — a large forest complex (c. 1500 km²) on the border between Poland and Belarus. The BNP is protected since 1921 and after its enlargement in 1996 its area is 105 km² at present. Many tree stands of BNP may be classified as primeval forests, which have never been cut. These forests are characterize by a multistorey profile with great vertical and horizontal diversity, high amount of dead wood and trees which reach large dimensions (Tomiałojć 1991). The study was carried out in the primeval oak-hornbeam-lime stands, Tilio-Carpinetum, located in the strictly protected part of the BNP. This dominant forest type, covering c. 45% of the total area of BNP, is the most structurally diversified with a variety of tree species and three canopy layers. Small-leaved Lime Tilia cordata, Hornbeam Carpinus betulus, Norway Spruce, Pedunculate Oak Quercus robur, Ash Fraxinus excelsior are the most numerous tree species but many other like Norway Maple Acer platanoides, Aspen Populus tremula, elms Ulmus spp. and Great Sallow Salix caprea are in admixture.

MATERIALS AND METHODS

RESULTS

GLMM analysis performed for Great Spotted Woodpecker females revealed that the duration of the foraging session was associated with tree species, dbh and the diameter, height and condition of foraging site. Moreover, the interaction between tree species and condition of foraging place was statistically significant (Table 1, 2). GLMM for males showed that all above mentioned variables were significant except tree dbh (Table 3, 4).

Table 1.

Results of generalised linear mixed model explaining the duration of the foraging sessions of females of the Great Spotted Woodpecker in primeval oak-hornbeam-lime forest.

Table 2.

Estimates of variables from the model presented in Table 1. Asterisk means the reference category.

Table 3.

Results of generalised linear mixed model explaining the duration of the foraging sessions of males of the Great Spotted Woodpecker in primeval oak-hornbeam-lime forest.

Table 4.

Estimates of variables from the model presented in Table 3. Asterisk means the reference category.

Fig. 1.

Mean duration of the foraging session (with 95% confidence limits) of Great Spotted Woodpecker males and females on dead and alive foraging sites. Asterisk indicate significant differences between dead and alive substrates. Numbers indicate sample size.

Generally, the longest foraging sessions were found on Norway Spruce for both sexes whereas the shortest ones on hornbeam in the case of males and maple and aspen in the case of females. Foraging session was longer on dead tree parts than on alive ones which was especially noticeable in the case of females (Fig. 1). This phenomenon was found for all tree species except hornbeam and lime in the case of males (Fig. 2) and maple in the case of females (Fig. 3). The longest foraging was revealed on dead parts of Norway Spruces for both sexes (Fig. 2, 3). Males foraged the longest on sites located above 20 m (Fig. 4) and having a diameter 5–10 cm (Fig. 5) whereas females on sites above 15 m (Fig. 6) and having a diameter 10–20 cm (Fig. 7). The duration of the foraging session of females increased with increasing of tree dbh which was not observed in the case of males (Fig. 8).

Fig. 2.

Mean duration of the foraging session (with 95% confidence limits) of Great Spotted Woodpecker males on particular tree species in relation to substrate condition. Asterisk indicate significant differences between dead and alive substrates. Other: Alder Alnus glutinosa, Ash, birches Betula spp., elms.

Fig. 3.

Mean duration of the foraging session (with 95% confidence limits) of Great Spotted Woodpecker females on particular tree species in relation to substrate condition. Asterisk indicate significant differences between dead and alive substrates. Other: Alder, Ash, birches, Scots Pine, elms.

The random effect “year” was significant in both analysed models (Table 1, 3).

DISCUSSION

Our study revealed that foraging sessions of the Great Spotted Woodpecker were the longest in places having a moderate diameter, located higher up in trees, and being dead what was especially noticeable in the case of females. Thus our assumption that dead substrates would be preferred over living substrates was confirmed.

Fig. 4.

Mean duration of the foraging session (with 95% confidence limits) of Great Spotted Woodpecker males at different heights. Different letters indicate significant differences between particular categories of foraging height. Numbers in brackets indicate sample size.

Fig. 5.

Mean duration of the foraging session (with 95% confidence limits) of Great Spotted Woodpecker males in sites of different diameter. Different letters indicate significant differences between particular categories of foraging places. Numbers in brackets indicate sample size.

The longest foraging sessions of both sexes were revealed on dead parts of Norway Spruce what suggests that this tree species is an important site of foraging for the Great Spotted Woodpecker, where it collects food not only in the form of seeds but also invertebrates.

Spruces, especially dead ones, are inhabited by many organisms, mainly insects (e.g. beetles), which also overwinter inside the wood (Hilszczański 2008, Lõhmus et al. 2010). The study by Hogstad (1970), who observed foraging of the Three-toed Woodpeckers on only one dead spruce for a few days, confirms that this tree species can be excellent storage of food. Dead spruce can also be a frequent place of foraging for the White-backed and Middle Spotted Woodpeckers, which was observed in BPN (Czeszczewik 2009, Stański 2014). However, foraging of the Great Spotted Woodpecker on spruces apart from picking out cones, which are then hammered in the anvils, is uncommonly reported, and if such behaviour is observed this is only a small percentage of observations (Alatalo 1978).

Fig. 6.

Mean duration of the foraging session (with 95% confidence limits) of Great Spotted Woodpecker females at different heights. Different letters indicate significant differences between particular categories of foraging height. Numbers in brackets indicate sample size.

Fig. 7.

Mean duration of the foraging session (with 95% confidence limits) of Great Spotted Woodpecker females in sites of different diameter. Different letters indicate significant differences between particular categories of foraging places. Numbers in brackets indicate sample size.

Fig. 8.

Relationship between tree trunk diameter at breast height and the duration of the foraging session of Great Spotted Woodpecker males and females.

Our second hypothesis assumed that trees with large dimensions should be preferred over trees with small dimensions. It was based on the fact that trees with large dbh are characterized by a higher number of invertebrates compare to trees with smaller dbh, as demonstrated by studies of two species of butterfly caterpillars (Sukovata & Jaworski 2010). The abundance of insects e.g. beetles living in or below the bark also increased significantly with tree diameter (Lõhmus et al. 2010). However, we revealed that duration of foraging session increased with increasing tree dbh only in the case of females. It was not observed in the case of males. Both this phenomenon, as well as much longer foraging on dead tree fragments compare to alive ones in females than in the case of males, may be due to the fact that the former are based more on animal food. Similar results to ours were obtained by Osiejuk (1998), who found that females foraged much more often on dead parts of trees and on thicker trees (taking into account only animal food). However, he stated this only during winter with poor availability of Scots Pine cones, which is when the competition for food was strong. Another study of Osiejuk (1994) showed, that males due to social dominance, expressed by aggressive behaviour, influenced females to feed more often on animal food than on seeds excavated from cones.

Our study showed that woodpeckers foraged longer in places having a moderate diameter and located higher up in trees. This phenomenon may be explain by the fact that the number of potential places rich in food and suitable for foraging is likely to increase with height, which could have been influenced, among others, by their better sun exposure compared to lower situated sites. More insolated trees or their fragments have richer invertebrate fauna, thus may cause the woodpeckers forage there longer (Nicolai 1986). Such places are attractive for woodpecker species that collect food from the surface like the Middle Spotted Woodpecker (Pasinelli & Hegelbach 1997).

Selection of specific foraging places by the Great Spotted Woodpecker could also result from the competition and thus, resource partitioning between different woodpecker species. In order to minimize competition, individual species of woodpeckers inhabiting the same habitat firstly use different feeding techniques, which allows them to obtain different types of food, and secondly, they use places on trees of different diameter or located on different heights (Hogstad 1971b, Alatalo 1978, Török 1988, 1990, Kruszyk 2003). For example, Hogstad (1971b) showed that the Great Spotted Woodpecker preferred to feed on thinner parts of trees and at higher heights than the Three-toed Woodpecker. Such resource partitioning is also apparently present in BPN, where all species of woodpeckers breed, with the exception of the Syrian Woodpecker Dendrocopos syriacus, which means that competition for food could be potentially strong here. For example, spruces, being a great storage of food in BPN, are used not only by the Three-toed Woodpecker, but also by the Great Spotted, the Middle Spotted and the White-backed Woodpeckers (Czeszczewik 2009, Stański 2014). However, particular woodpecker species collect food in different way or in different sites to minimize competition. For example, the Great Spotted Woodpeckers foraged high and on moderate parts of trees, as was shown in this work, while the White-backed woodpecker low and on substrates above 20 cm of diameter (Czeszczewik 2009). On the other hand, Wesołowski (2003) suggests that competition for food does not seem to play an important role in the BNP. His statement was based on data from breeding season, when food resources are usually superabundant here. However, in the non-breeding season, when food resources are less, competition for food may play a greater role (Czeszczewik 2010).

The length of the foraging session was also influenced by the year which may be related to the change of foraging behaviour resulting mainly from the change in the composition of available food. In the BPN, the availability of animal food as well as the degree of fruiting of spruce and hornbeam, which are an important food resource for the Great Spotted Woodpeckers in the non-breeding period, were subject to considerable fluctuations in individual years (Wesołowski & Rowiński 2006, Stański 2014, Wesołowski et al. 2015).

In conclusion, foraging sessions of the Great Spotted Woodpecker were longer in sites located higher, having a moderate diameter, and being dead what was especially noticeable in the case of females. It may suggest that these are attractive places for collecting food. Norway Spruces, in particular, their dead parts, are an important source of food for studied woodpecker species not only in the form of cones but also as invertebrates collected there.