Black woodpecker Dryocopus martius (L., 1758) distribution, abundance, habitat use and breeding performance in a recently colonized region in SW Europe

Abstract

At the southwestern edge of its global distribution, the Pyrenean population of the black woodpecker Dryocopus martius has increased its range during the last three decades, colonizing new areas where the species was previously unknown. This is the case for Gipuzkoa, where a systematic survey was performed in the breeding season of 2013 aimed at describing the species distribution, abundance, habitat use and reproductive performance. Potential locations were identified using forest inventories and were visited since January until March. Locations were considered occupied when nests or pairs were found, or single individuals were detected during three consecutive visits. Breeding performance in active nests was monitored during May and June. We found 21 breeding home ranges, mainly distributed across the Eastern and Southern fringes of the study area. The environmental variables positively related to the presence of breeding home ranges were higher proportions of canopy cover, mature structure of the stand, cover of beech Fagus sylvatica, mixed deciduous and black pine Pinus nigra stands, and unfragmented forest patches. Monterey pine P. radiata plantations and low tree heights were negatively selected. Preferred foraging areas comprised proportions of American oak Quercus rubra and black pine plantations. Thirteen active nests were found. All nests but two were excavated in beech trees. Breeding success was high (92%) but fledging success (1.8) was below the average reported in Europe, suggesting intrinsic limitations associated to a peripheral population. [Excerpt: Discussion] [::The colonizing process] The absence of paleozoological records for the black woodpecker in Europe west and south of the Alps might suggest that the species is a historic colonizer of the Atlantic section of the continent (Arribas, 2004; Holm & Svenning, 2014). During the 20th century, considerable range expansions have been described in The Netherlands, Belgium, France and Italy, with birds invading lowland, reforested regions (Cuisin, 1985; Mikusinski, 1995; Cuisin, 1998; Ceccarelli et al., 2008). In Northern Iberia, at the south-western edge of the global distribution, the black woodpecker has also increased its breeding range, colonizing formerly vacant areas over the last 30 years (Martínez-Vidal, 2004; Camprodon et al., 2007). In Gipuzkoa, the first report of the black woodpecker dates back to the 1960’s (Noval, 1967), but until the 2000’s the species was extremely rare and irregular (Gainzarain, 1998; Aierbe et al., 2001). In 2011, the first successful reproduction was confirmed (Ruiz de Azua, 2012), though, without doubt, the Black Woodpecker was already breeding a few years before (T. Aierbe, com. pers.). [] This particular colonizing event is part of the wider range expansion across the Basque Mountains, which is currently filling the intermediate gap between the Pyrenean and the Cantabrian populations (Gainzarain & Fernández-García, 2013). The geographic origin of this recent population is unknown so far. There is not genetic or ringing information to support a Cantabrian or Pyrenean origin, which are the closest source areas. However, based on the favourable population trend of the neighbouring Pyrenean population (Martínez-Vidal, 2004), opposite to the Cantabrian one (Simal & Herrero, 2003; García, 2008; Sánchez et al., 2009), it is plausible to speculate about a Pyrenean origin. [] The black woodpecker fulfills several biological features that Mikusinski (2006) related to decline-prone woodpecker species in transformed landscapes, like large body size and extensive home-ranges, therefore needing a network of vast forest tracts to maintain viable populations. But, on the the other hand, this species maintains a huge distribution indicating adaptability (Croci et al., 2007), is relatively tolerant to forestry practices (Cárcamo, 2006) which associates to rapid occupation of vacant habitats (Villard & Taylor, 1994), and has good dispersal abilities, in turn related to the velocity of expansion (Lensink, 1997). Although there are hardly any studies in Europe reporting on emigration and immigration rates (Passinelli, 2006), recoveries of ringed birds show a noticeable proportion of long post-juvenile movements (Gorman, 2011) and high average natal dispersal distance (16.25 km in Denmark; Christensen, 2002). Both this kind of life-history traits and tolerance to disturbance are fair predictors of colonizer birds (Shigesada & Kawasaki, 2002) and may explain the black woodpecker capability to expand its distribution, as shown from our study area. [] At the continental scale, the expansion of the black woodpeckers’ range has been attributed to extensive coniferous reforestation (Mikusinski, 1995), but at the regional scale more emphasis is placed on forest maturation, due to a decline in timber exploitation (Gil- Tena et al., 2010). The occupancy of patches in Gipuzkoa did not seem to be influenced by distance to population sources, which was not unexpected given the comparatively small scale of our study area. In the Eastern Pyrenees, about three times larger, the pattern of colonization by the black woodpecker was mediated by connectivity among forest patches, depending in turn on distance to source and forest structure (i. e. basal area; Gil- Tena et al., 2013). The availability of a network of stepping stones is crucial to explain the progressive spread of the population (Saura et al., 2014). Such spatially explicit models could be improved if indicators of foraging quality, such as availability of dead wood, are taken into account (see below). Foraging quality enhances breeding performance and the production of a surplus of individuals than can disperse to non-occupied patches (Newton, 1998). [::Plantations and the black woodpecker] The black woodpecker inhabits several different types of Palearctic boreal and temperate forests, including coniferous plantations (Mikusinski, 1995; Gorman, 2011). In boreal and hemiboreal forests, the species is tolerant to plantation managing, provided that thick trunks (diameter >40 cm) for excavating nests remain, and decaying trees are also left as foraging substrates (Angelstam & Mikusinski, 1994). In the framework of worldwide afforestation and reforestation activities for commercial purposes, intense debates focus on the effect of plantation forestry on biodiversity (Bremer & Farley, 2010). As for birds, metaanalyses in Europe have shown that landscape history and spatial structure (patch size, matrix pattern) are probably more informative in explaining species richness than management at the stand scale (Paillet et al., 2009). [] Extensive Monterey pine plantations in Northern Spain have contributed to the restoration of forest bird communities (Carrascal & Tellería, 1990), but for the black woodpecker in particular our study has found a number of limitations. Plantations of this pine species in the Basque region are a novel habitat for the black woodpecker across its entire range (Mead, 2013). The species’ selection for nesting habitats is rather demanding, both for cavity- trees and cavity-tree plots (Martínez-Vidal, 2001; Camprodon et al., 2007; Pirovano & Zecca, 2014). Preference for beech as nesting substrate has been demonstrated over much of Western Europe (Gorman, 2011; Zahner et al., 2012), and our own data supports this view. Beech trees provide less accessible nests: high holes and smooth bark are associated to lower predation pressure (Zahner & Bauer, 2014). But pine trees (i.e. black pine, Scots pine) are also used in some mountain regions, like the Pyrenees and the Alps, in similar proportion to their availability on the landscape (Martínez-Vidal, 2001; Bocca et al., 2007). In Gipuzkoa, the avoidance of Monterey pine patches deserves further research, but the reason may lie on the combined absence of suitable (i.e thick, tall and debranched) nesting trees and the scarcity of foraging resources in dense, shaded stands (see below). On the contrary, stands of mixed deciduous trees were favoured because they probably supply hole-trees (beech and American oak, even though these two species do not dominate such stands). Because of the forest history of the study area, mixed deciduous stands appear scattered at lower altitudes, surrounded by the matrix of Monterey pine plantations. Similarly, Bocca et al. (2007) found a negative selection for the mountain pine Pinus uncinata in the Alps -in spite of accounting for half of the surface of their study area- attributed to the unsuitable tree conformation and the dense structure of this kind of forest. [::The role of habitat fragmentation] An interesting outcome was the influence of the spatial structure of the habitat on the presence of black woodpecker BHR. Fragmentation of suitable forest patches embedded in a matrix dominated by intensively managed plantations largely determines the composition of bird assemblages (Estades & Temple, 1999) but in a species-specific-way (Mönkkonen et al., 2014). Woodpeckers are thought to be relatively tolerant to fragmentation because, as primary cavity-nesters, they avoid the increasing effect of predation while decreasing patch size. This seems to be the case for the black woodpecker, whose density and breeding performance was not influenced by fragmentation in Sweden (Tjernber et al. 1993) or landscape structure in Finland (Brotons et al., 2003). [] But more detailed analyses have shown differences referred to patch size and density of edges in another generalist species, the great spotted woodpecker Dendrocopos major (Mazgajski & Rejt, 2006; Barbaro et al., 2007). Reduced clutch size, low number of fledglings and delayed breeding phenology were observed in smaller woodlots. Therefore even generalist woodpeckers can be sensitive to fragmentation processes, and this could also apply to the black woodpecker (Mikusinski, 1995). The preference for larger, less complex forest patches in ou