Ecological management of a Mediterranean mountainous reserve (Pindos National Park, Greece) using the bird community as an indicator

ARTICLE IN PRESS Journal for Nature Conservation 17 (2009) 47—59

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Ecological management of a Mediterranean mountainous reserve (Pindos National Park, Greece) using the bird community as an indicator Vassiliki Katia,, Panayotis Dimopoulosa, Haritakis Papaioannoua,b, Kostas Poirazidisc a

Department of Environmental and Natural Resources Management, University of Ioannina, Seferi 2, 30100 Agrinio, Greece b Center of Biological and Cultural Diversity, 44004 Papingo, Greece c Department of Forestry, Environment and Natural Resources, Democritus University of Thrace, 68200 Orestiada, Greece Received 23 April 2008; accepted 5 December 2008

KEYWORDS Ecological structure; Forest management; Indicators; NATURA 2000; Passerines; Protected area

Summary We used the community of passerines and woodpeckers as a target group for the conservation management of Pindos National Park (NW Greece). We conducted bird point counts twice during springtime in 72 plots that represented the main vegetation types (16 sites). We recorded 56 species (14 of conservation concern-SPEC). The montane grasslands were the most important habitats in terms of species of conservation concern, whereas the agricultural mosaics were the most species-rich habitats. The mixed pine-beech woods were significantly richer than the pinewoods, whereas pinewoods and broad-leaved woods did not differ significantly between them. The bird diversity was significantly correlated with the number of tree layers, the vertical structural complexity and the maximum height of trees. The presence of grassland, forest and agricultural habitat type, as well as the altitude and the vegetation structural complexity were the main environmental parameters determining species composition (Canonical Correspondence Analysis). We identified a set of 17 typical species (IndVal analysis) to be used in the monitoring scheme of the Park, which were characteristic of the main bird habitat types distinguished by Ward’s hierarchical clustering. Conservation measures should involve maintenance of the traditional agricultural practices, montane

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E-mail addresses: [email protected], [email protected] (V. Kati). 1617-1381/$ - see front matter & 2008 Elsevier GmbH. All rights reserved. doi:10.1016/j.jnc.2008.12.002

ARTICLE IN PRESS 48

V. Kati et al. grasslands, old growth woods, as well as the vertical vegetation complexity and high trees in forest stands. & 2008 Elsevier GmbH. All rights reserved.

Introduction Birds exhibit a diverse range of ecological functions, and benefit humans by providing a wide range of ecosystem services (Sekercioglu, 2006). However, birds also constitute one of the most vulnerable groups of organisms, with many species currently undergoing significant global population declines, leading to detrimental consequences for total biodiversity and ecosystem function (Sekercioglu et al., 2004). Because birds are, especially in Europe, among the best-studied organisms, they are often used to evaluate the impact of human activities (BirdLife International, 2004; Heath et al., 2000). On account of their ubiquitousness, terrestrial passerine communities in particular have been used as indicators of environmental change (Bani et al., 2005; Gregory et al., 2004), or as ecological substitutes for other, more difficult to quantify groups of organisms (Howard et al., 1998; Kati et al., 2004a; Lombard, 1995; Prendergast et al., 1993). Although their use as indicator taxa has been sometimes criticised for its potentially low extrapolative value to other groups of organisms (Lindenmayer et al., 2006; Simberloff, 1998), small terrestrial birds are considered as an important component of biodiversity and have been integrated into studies evaluating its conservation (Dobson et al., 1997; Kati et al., 2004b; Lawton et al., 1998; Thiollay, 2002; Vessby et al., 2002). Thus, small terrestrial birds have often been used to assess and guide ongoing forest management practices (e.g. Donald et al., 1998; Gil-Tena et al., 2007; Johnson & Freedman, 2002; King & DeGraaf, 2000; Laiolo et al., 2003; Lance & Phinney, 2001; Muller et al., 2007; Sekercioglu, 2002) or current agricultural practices (e.g. Chamberlain et al., 2000; Donald et al., 2001; Pain & Pienkowski, 1997). In this applied context, the European Union has recently adopted, for the first time, an ecological index that considers the conservation status of common farmland birds (Farmland Bird Index) as a formal indicator of sustainable development in Europe (structural-sustainable development indicator). A prerequisite step before using small terrestrial birds as an indicator group is to obtain a deeper understanding of the underlying patterns in diversity and the ecological structure of this community.

In the present study we conducted an ecological study, considering the land bird community (passerine and woodpecker species) as a target group, in order to provide a guideline for the ecological management of a remote area, surrounding the mountainous Pindos (or Valia Calda) National Park in NW Greece. The Park was created in 1966 and is considered to be one of the most important protected areas for the maintenance of mountainous biodiversity and ecosystem integrity at national scale. However, existing knowledge on the biological diversity of the area remains fragmentary (Mertzanis, 1999; Tsounis et al., 1985). The Park is under the administrative authority of a recently created (2003) Management Body, which is responsible for the ecological management of a much larger region that includes eight protected areas of the NATURA 2000 network. This authority together with the local Forest Service is responsible for regulating human activities and maintaining the ecological value of Pindos National Park (NP). However, this target remains elusive, due to a lack of expertise and of a science-based management plan for the NP. Thus a great need exists to conduct conservation-oriented research that can be translated directly into practical management proposals. The present research attempts to fill this gap in relation to the bird community. Specifically, our objectives are: (a) to assess the relative importance of different habitat types for avian conservation; (b) to test whether tree composition, vertical structural complexity and tree height affect bird community in forest stands; (c) to analyse the ecological structure of bird communities and to detect the main environmental factors regulating species diversity and distribution; and, (d) to identify species that are characteristic for the main bird habitat types distinguished. On the applied level, we attempt to translate these findings into practical monitoring and management schemes for the NP. Our findings could provide a management guideline for other national parks throughout the Greek mountains and in the Mediterranean area.

Methods Study area and site selection The study area is located in north-western Greece (391540 N, 211070 E) and covers a surface of

ARTICLE IN PRESS Bird communities and reserve management 16,000 ha. The National Park covers 6868 ha and consists of two sites of the European NATURA 2000 network. The strictly protected core area (GR1310002) covers 3294 ha, and has been declared a ‘‘biogenetic reserve’’ by the European Council; human activities such as woodcutting, grazing, hunting, and access by car are not allowed. The buffer zone (GR1310003) covers 3574 ha and human activities are controlled (Figure 1). The region is extremely mountainous with elevations ranging from 900 to 2177 m asl. The climate is montane and varies depending on elevation and aspect; annual rainfall ranges between 1000 and 1800 mm whereas mean monthly temperatures vary between 0.9 and 21.4 1C (Trakolis et al., 1996). The

49 dominant vegetation type is black pine forest (Pinus nigra) reaching up to 1700 m, whereas common beech forest (Fagus sylvatica) covers the northern slopes up to 1800 m. Sub-alpine grasslands extend above 1800 m to peaks often dotted with Balkan pines (Pinus leucodermis). The region is sparsely populated and human activities mainly include logging and livestock breeding, both regulated by the local Forest Service, as well as agriculture of very limited scope. We selected 16 sites representative of the main habitat types of the study area on the basis of the standard European habitat typology (European Commission, 2003) (Table 1). Sampling covered ten forest sites containing pinewoods (P), beech

Figure. 1. Habitat types and sampling sites in the broader area of Pindos National Park, Greece.

50

Table 1.

Description of the sites sampled and bird diversity. Habitat codes refer to the Appendix I of the Directive 92/43/EEC (European Commission 2003).

Site code Habitat type

P1

B1 B2 PB1 PB2 R G1 G2 G3 G4 A1 A2

Mediterranean pine forests with endemic Mesogean pines (Pinus leucodermis) Asperulo-Fagetum beech forest (Fagus sylvatica) Mixed pine-beech woods Constantly flowing Mediterranean rivers with Salix and Populus alba Semi-natural dry grasslands and scrubland facies on calcareous substrates Endemic oro-Mediterranean heaths with gorse

Rural mosaics

Bird diversity of sites

Habitat code Area (ha)

ALT (m)

NL

1/D

MH (m)

Land use

Zone

S

H

9530

20

1519

2.00

0.39

12–20 w

9530 9530 9530 9540

20 20 20 15

1442 1130 1452 1572

2.67 4.00 2.20 3.00

0.40 0.39 0.39 0.38

20–35 20–25 16–24 18–22

9130 9130 9530  9130 3280

20 20 20 20 20

1419 1558 1356 1479 964

2.86 2.29 3.50 3.20 2.80

0.26 0.31 0.39 0.38 0.39

16–25 12–17 20–35 20–35 15–22

6210

20

1714

2.17

4090 4090 4090 1020 1020

20 10 10 20 20

1733 1412 1461 986 1221

2.17 2.00 2.00 2.20 2.80

Mean S

Mean WS

Points

1, 2

11

3.17

4.83

– – – –

1 3 1 1

20 20 16 7

3.18 3.15 3.19 3.16

9.50 12.00 5 9.60 11.80 5 8.80 11.20 5 7.00 7.00 3

– w w w w

1 2 – – –

17 15 20 19 20

2.93 2.85 3.2 3.21 3.2

6.14 6.71 5 6.14 9.00 5 9.00 13.50 5 8.60 10.80 5 7.20 8.40 5

0.35

g

2

18

3.1

8.33 13.17 5

0.36 0.38 0.39 0.28 0.29

w, g g g g g, a

– 2 1 – –

18 7 15 19 23

3.18 3.18 3.18 2.57 2.89

5.33 9.33 5 5.00 11.00 2 9.00 17.50 2 7.80 9.20 5 10.00 14.40 5

6.33 5

ARTICLE IN PRESS

P2 P3 P4 P5

Sub-Mediterranean pine forests with endemic black pines (Pinus nigra)

Site description

ALT: altitude, NL: mean number of vegetation layers, 1/D: mean Simpson reciprocal index of vertical structure, MH: maximum height of upper tree layer, S: species richness, H: Shannon diversity index, MeanWS: mean weighted species richness, 1: NP core area, 2: NP buffer zone, 3: sacred grove a: agricultural use, g: grazing, w: woodcutting.

V. Kati et al.

ARTICLE IN PRESS Bird communities and reserve management woods (B), mixed woods (PB) and riverine vegetation (R), as well as four grassland sites (G) and two agricultural ones (A) (Table 1). Most of the sites sampled were located inside areas protected by the NATURA 2000 network, and one site (P3) was strictly protected as a sacred grove.

Bird sampling We surveyed the bird communities at 72 point locations, recording all passerine and woodpecker species seen or heard within a circle of a 100 m radius of each point. Points were located at a distance of 200 m between them and at least 100 m from site edge, in order to avoid double counting and edge effects. All sites (20 ha) were represented by five points with the exception of three smaller sites (10–15 ha) that were covered with 2–3 points. To cover both sedentary species and late-arriving migrants, we sampled every site twice, once in late spring (30 April–30 May 2003) and once in early summer (5 June–5 July 2003). In our bird count methodology (see Bibby et al., 1992; Blondel et al., 1970), a singing, territorial male represented a breeding pair and was therefore counted as two individuals. Every call different from the male breeding song was counted as one individual. Each count lasted for 10 min and took place between 30 min before and four hours after sunrise.

Measurement of environmental variables We located a smaller quadrate (50 m  50 m) at the centre of the each one of the 72 bird survey points where we sampled the four main vegetation layers: (1) upper tree layer (47 m); (2) lower tree layer (4.1–7 m); (3) upper shrub layer (2.1–4 m); (4) lower shrub layer (0.5–2 m) (Kent & Coker, 1994). We visually determined the percentage cover (relative area occupied by the vertical projection of all aerial parts of woody plants as a percentage of the surface area of the sample plot) for the separate layers (van der Maarel, 2005), using the following vegetation cover classes (Ku ¨chler, 1988) 1 ¼ 1–5%, 2 ¼ 6–25%, 3 ¼ 26–50%, 4 ¼ 51–75%, 5 ¼ 76–100%. For each quadrate we recorded the altitude (ALT), the overall vegetation cover (COV), the maximum height of the upper tree layer (MH) in forest habitats, the number of vegetation layers (NL) and the reciprocal of Simpson’s diversity index (1/D) as a measure of vertical vegetation complexity (Magurran, 2004). We also noted the general habitat category the station referred to (agriculture, forest, and grassland).

51

Data analysis We estimated the overall number of species of the study area using the software EstimateS (Colwell 2006) with the option of 1000 randomisations. We opted for non-parametric species estimators, which consider mainly the presence of rare species, recorded by one or two individuals (Chao 1), or present in one or two point counts (Chao 2) (Magurran, 2004). Species diversity was estimated in terms of species richness (S), weighted species richness (WS), and Shannon–Weiner index (H) (Magurran, 2004), using the maximum abundance recorded over the two seasons. We also calculated their mean values per sampling point (MeanS, Mean WS) and we compared them for the pine, broad-leaved and mixed woods using the Kruskal–Wallis non-parametric test and then the Mann–Whitney tests with Bonferroni correction, with the help of SPSS software (Field, 2005). Weighted species richness is the species richness of the site, with each species having a different weight based on its conservation status (SPEC category) (BirdLife International, 2004). We assigned a standard weight (w ¼ 1) to the species of favourable conservation status (SPEC 4 category or non-SPEC category). We assigned double weight (w ¼ 2) to the species of SPEC 3 category, which are not concentrated in Europe but have an unfavourable conservation status. Finally we assigned a quadruple weight (w ¼ 4) to the species in the SPEC 2 category, which are concentrated in Europe and have an unfavourable conservation status and to the species listed in Annex I of the European Directive 79/409 EU, which includes all bird species subject to special conservation measures in Europe. We also calculated the bird diversity indices (S, WS, H) for each point count and tested their correlation with the five quantitative environmental variables sampled using Spearman correlation coefficients (SPSS, vers 15.). To assess which environmental factors shape bird community composition, we used the Canonical Correspondence Analysis (CCA) option from the ordination program CANOCO (ter Braak & Smilauer, 2002), because the length of the gradients of Detrended Correspondence Analysis (DCA) indicated a heterogeneous dataset (Leps & Smilauer, 2005). This method extracts the major gradients in the data that are accounted for by the measured variables. The position of a species in the resulting plot indicates the characteristics of the ecological optimum for this taxon; its abundance will decrease with increasing distance from this point. Species encountered only once were not included in the analysis and species abundances were log

ARTICLE IN PRESS 52 transformed. A forward selection procedure using a Monte-Carlo permutation test with 1000 iterations was used to select and present in the CCA diagram only the significant (po0.05) environmental variables that explained variation in community structure. The multi-collinearity of environmental variables was tested using the inflation factor. We used Ward’s clustering method to group hierarchically the point counts into clusters, expressing the different habitat types of bird community. We also used the indicator value procedure (IndVal) (Dufre ˆne & Legendre, 1997) to identify the typical species characterising each of the clusters. IndVal is a percentage that ranges between 0 and 100 and takes its maximum value when the species is present exclusively in all sites of a single cluster. All calculations were carried out using IndVal software (Dufre ˆne, 1999). A species is considered to be a ‘‘symmetrical indicator’’ (IndVal4 50%) for one cluster, when it is present in 470% of the sites of the cluster and when 470% of its individuals occur in the cluster. A random reallocation procedure (1000 iterations) of sites among site groups was used to test IndVal significance (alpha ¼ 0.05).

Results Point count sampling resulted in 56 species (14 of conservation concern), whereas the overall bird species number recorded inside and outside point counts was 62 species, including six woodpeckers (Piciformes) and 56 passerine species (Passeriformes) (Appendix I). The ornithological importance of the study area is high, given that we recorded six and ten species of unfavourable conservation status concentrated in Europe (SPEC 2) or not (SPEC 3), respectively (Appendix I). The overall estimated species richness using non-parametric estimators was between 56 (Chao 1 estimator) and 66 species (Chao 2 estimator). We have therefore sampled exhaustively the bird community of the area.

V. Kati et al. saxatilis, Oenanthe oenanthe). The second most important site, which was also the richest in species number was a traditionally cultivated site (A2), including six out of the 16 species of conservation concern (C. cannabina, E. hortulana, L. collurio, Milaria calandra, Muscicapa striata, Passer domesticus). The next sites in rank was a mixed pine-beech forest (PB1), a montane grassland (G1), a black pine forest located in the core area of the NP that has not been harvested for at least two centuries and is accessible exclusively on foot (P2), and a sacred grove of black pines that has also not been harvested for at least two centuries (P3) (Table 1). The species richness and the weighted species richness were significantly higher in the mixed pine-beech woods than in the pinewoods (Kruskall Wallis test p ¼ o0.05, Mann–Whitney post-hoc tests po0.0160), whereas pinewoods and broad-leaved woods did not differ significantly between them.

Community structure and typical species Bird species richness in each point count (S) decreased significantly (po0.01) with increasing altitude (Table 2). Bird species richness together with the weighted species richness in each point count (WS) increased significantly (po0.01) with the number of vegetation layers (NL) and with the maximum height of upper tree layer (MH) in the forested sites. Finally, the Shannon diversity index for birds in each point count (H) was significantly (po0.01) correlated with the vertical structural complexity as expressed by the Simpson reciprocal index 1/D (Table 2). The CCA model was significant (po0.001) and revealed clearly that the presence of grassland, forest or agricultural habitat type, as well as altitude and vegetation structural complexity Table 2. Spearman correlation coefficients between bird diversity indices of point counts and environmental parameters. Diversity indices

NL

Bird diversity The most important site for bird conservation, on the basis of the criterion of mean weighted species richness (MeanWS) was the montane grassland G4 (Table 1). Although not very species-rich (15 species), it held seven out of the 16 species of conservation concern (SPEC 2: Carduelis cannabina, Emberiza hortulana, Lullula arborea; SPEC 3: Anthus campestris, Lanius collurio, Monticola

Environmental parameters

S WS H

0.385 0.219 –

1/D

MH

ALT

– – 0.637

0.541 0.790

–0.305 –

–

ALT: altitude, NL: number of vegetation layers, 1/D: Simpson reciprocal index of vertical structure, MH: maximum height of upper tree layer, S: species richness, WS: weighted species richness, H: Shannon diversity index.  Po0.01.  Po0.05.

ARTICLE IN PRESS Bird communities and reserve management 1.0

53

Agriculture Mcal Ecirl Ccoc

Tirogl Acaud

Ehort Cchl Mstr

Lcol Ccard

Pmaj Tmer

Grassland Ecitr Lularb

Sattr Erub

Prmod

Cbra Rign Sser Forest

Phochr Ooen

Arriv

Parer

Altitude

1/D

-1.0 -0.6

1.0

Figure 2. Triplot of bird species, significant environmental variables and sampling sites after Canonical Correspondence Analysis. Only species with a fit greater than 30% are shown.

(1/D) affected significantly bird species assemblages (Figure 2). The first CCA axis (11.4% of data variability and 49% of species-environment relation) also explained the first hierarchical division in Ward’s dendrogram; the latter reflected a gradient from forested sites at lower altitudes towards grasslands at higher altitudes (Figure 3). The first ordination axis of species dataset predicts the bird community in the right part of the CCA diagram (montane grassland community) and is calculated as: [0.89 Grassland +0.61 Altitude +0.14 1/D0.29 Agriculture], if we consider the statistically significant environmental variables without multicollinearity in the CCA model (Figure 2). Three species (Emberiza citrinella, L. arborea, O. oenanthe) were typical species of the above community (Figure 3). The second CCA axis (5.6% of species data variability and 24% of species-environment relation) explained the second division in Ward’s dendrogram; the latter reflected a gradient from tall forests towards sites of lower trees and agricultural character (Figure 3). The respective equation of the second axis of species dataset that predicts the bird community in the upper part of the CCA diagram (agriculture and low trees) is the following: [0.68 Agriculture +0.18 Grassland 0.55 1/D0.4 Altitude]. A group of eight species was

Figure 3. Hierarchical clustering of sites produced by Ward’s method and typical species with significant indicator values (in parenthesis) that are greater than 50% for each cluster.

ARTICLE IN PRESS 54 identified as typical for the above community, increasing in abundance along the second axis (Aegithaulus caudatus, Troglodytes troglodytes, Parus major, Parus caerulaeus, M. striata, Turdus merula, Coccothraustes coccothraustes, Emberiza cirlus) (Figure 3). On the other hand, the relative abundance of two typical forest species (Parus ater, Regulus ignicapilla), decreased along this axis. Furthermore, two typical species for pinewoods were identified (Dendrocopos major, Parus cristatus)¸ whereas no typical species existed for beech woods. Finally, we found that some species were generalists, being common throughout the study area and presenting their highest indicator value for all the sites sampled (i.e. Fringilla coelebs, Phylloscopus collybita, Erithacus rubecula), whereas two forest species were general indicators for all sites of forest character (Sylvia atricapilla, Certhia brachydactyla) (Figure 3).

Discussion Community structure The presence of agricultural land, grasslands or forests, as well as altitude and vegetation vertical complexity were the main statistically significant environmental gradients that influence the distribution of bird community in the broader area of Pindos National Park. The bird community was distributed along a gradient from forested habitats at lower altitudes towards montane grasslands at higher altitudes and along a gradient from forest stands with high trees and greater vertical structural complexity towards lower trees and cultivated land. These results are in agreement with other studies in the Mediterranean area (e.g. Dı´az, 2006; Kati & Sekercioglu, 2006; Prodon & Lebreton, 1981). Birds distinguish three general bird habitat types in the study area: grasslands; shrubby habitats of agricultural land or riverine vegetation; and forest habitats of pinewoods or beech woods, thus perceiving the environment at a relatively coarse scale.

Typical species Our study offers a valuable conservation tool for the management and monitoring plan of the study area, as it reveals a set of 17 typical species of the different habitat types, occurring almost exclusively in the relevant habitats and with great abundances. Some of the species recorded were generalists having a broad ecological niche and

V. Kati et al. distribution range in the study area with no indicator value. Several species were encountered with increased abundances in the montane grasslands and three of them were revealed as grassland indicators (Figures 2 and 3). In the same context, eight bird species were typical of the agricultural sites and the bushy habitats of riverine vegetation, whereas another six bird species were typical for the forest conditions (Figures. 2 and 3). If we compare our results with the typical species found in a Mediterranean reserve at low altitude (Dadia NP, less than 600 m), we find some similarities, concerning the generalist species (e.g. F. coelebs, E. rubecula) and the indicator species of forest conditions (e.g. S. atricapilla, C. brachydactyla, typical for broad-leaved woods). However, we found that L. arborea is typical of montane grasslands in Pindos NP but it is also typical for lowland heaths in Dadia NP in eastern Greece (Kati & Sekercioglu 2006). Special attention should be paid to the typical species that have an unfavourable conservation status in Europe at this time (SPEC 2, 3). For our study area, these were: L. arborea and O. oenanthe (typical for montane grasslands); M. striata (typical farmland species); and P. cristatus (typical pine forest species). All indicator species as well as the species with unfavourable conservation status should be integrated into the future monitoring program of the NP, in order to evaluate their own conservation status as well as their habitat condition, on a longterm basis.

Bird diversity Bird species richness was inversely correlated with altitude in our study area, but the weighted species richness, which also considers the conservation status of the species, was not. This well known pattern of decreased species richness with increasing altitude is explained by the theory of island biogeography and has been shown for bird communities in a variety of climatic zones (Kattan & Franco, 2004; Prodon et al., 2002). However, we found that the bird community of montane grasslands, which is a quite widespread habitat type in the Mediterranean mountains, comprises fewer but important species with unfavourable conservation status in Europe (SPEC 2, 3) and therefore should be considered as a primary habitat for conservation in the NP. Another important site for bird diversity conservation in the study area was the agricultural site A2. It was a rural mosaic, situated in the forested zone, alternating small cultivated plots

ARTICLE IN PRESS Bird communities and reserve management with pastures and orchards, separated by natural vegetation of hedges and tree lines. Site A1 was less species-rich, where former agricultural plots were not cultivated any more but were periodically grazed by livestock (Table 1). These rural mosaics were the rarest habitat in our study area, because small-scale farming using traditional agricultural practices has become financially unprofitable over the last decades and has therefore led to land abandonment in the broader area of Pindos NP, as in other mountainous areas in Europe (Gellrich & Zimmermann, 2007; MacDonald et al., 2000). Farmland bird diversity is subject to two major threats in Europe: agricultural intensification mostly in the northern lowlands (Chamberlain et al., 2000; Donald et al., 2001; Kati & Sekercioglu, 2006; Pain & Pienkowski, 1997); and agro-pastoral land abandonment mostly in the Mediterranean mountains. The latter results in forest encroachment, landscape heterogeneity decline, and agricultural habitat loss negatively affecting farmland bird diversity (Farina, 1997; Laiolo et al., 2004; Preiss et al., 1997; Suarez-Seoane et al., 2002). Our results provide additional evidence supporting the need to enhance the agri-environmental measures of the European Common Agricultural Policy (CAP) against land abandonment in less favoured mountainous areas, so as to maintain the traditional agricultural practices and the associated, biologically rich agricultural mosaics. We found that the mixed pine-beech woods were richer and more important for bird conservation rather than the pinewoods. However, the mixed woods did not form a separate cluster in hierarchical clustering analysis and did not hold a specialised avifauna (no indicator species for mixed woods). Mixed stands can be either more speciesrich or not of unmixed stands, but they are known to hold an intermediate bird species community between those of broadleaved and coniferous stands (Archaux & Bakkaus, 2007; Dı´az, 2006; Donald et al., 1998; Willson & Comet, 1996). Besides, we found no statistically significant difference when comparing the species richness (and the weighted species richness) of the unmixed natural pine and broad-leaved woods. We question therefore the general admission that broad-leaved stands hold richer bird communities than pure coniferous stands, when natural native stands are compared. This relationship could be attributed to the reduced ecological value of introduced conifer plantations compared to the natural native character of broad-leaved woods (Archaux & Bakkaus, 2007). These results may have a good extrapolative value to other Mediterranean natural forest ecosystems, since the forest habitat types

55 sampled in Pindos NP, such as the pinewoods (P. nigra) and the beech woods (F. sylvatica) are encountered in other mountains in the Mediterranean (Italy, Corsica, Spain, Portugal, France) with the exception of the Balkan pinewoods, encountered only in Greece and southern Italy. Bird diversity was strongly correlated with vertical structural vegetation complexity (NL, 1/D). Vertical stratification in forest vegetation has a positive influence over forest avifauna, as the presence of shrub layers offers more ecological niches, foraging opportunities and breeding resources especially for undergrowth-dependent bird species (e.g. Camprodon & Brotons, 2006; Dı´az, 2006; James & Wamer, 1982; Prodon & Lebreton, 1981; Wesolowski, 2007). This relationship was detected for the first time in Greek island ecosystems (Watson, 1964), but no other study has been conducted to quantify it in different Greek forest ecosystems since then. Although tree height was not a statistically significant environmental parameter to predict bird species in our CCA model, we found that the presence of high trees was positively correlated with the number of species (S) and also with the number of important bird species (WS) in forest habitats. We also found that two tall old growth pinewoods that have not been harvested for centuries (P2, P3) were richer than those lower pinewoods (P1, P4, P5). Forest bird species richness increases with tree height (Donald et al., 1998; Helle & Monkkonen, 1990). If we assume that high tree stands are also more mature, we could attribute this positive relationship to the fact that older forest stands provide more tree holes, as well as a higher amount of dead wood as breeding and feeding habitat for a variety of specialist taxa (e.g. Dı´az, 2006; Gil-Tena et al., 2007; Hobson & Bayne, 2000; Keller et al., 2003; Laiolo et al., 2003; Sekercioglu, 2002; Wesolowski, 2007).

Conservation management In the applied context, our study proves the importance and the need for maintenance of the montane grasslands in their present status. Secondly, it suggests that the enhancement of traditional agricultural practices in the broader area surrounding the Pindos NP could have beneficial effects on local bird communities. Thirdly, we emphasise the need for protection of the natural remaining old growth forests in the core area. Although timber extraction is not allowed in the core area since the creation of the NP (1966),

ARTICLE IN PRESS 56

V. Kati et al.

logging of old growth pine trees for commercial reasons seems to have occurred in 80s, facilitated by the existing road network. Fourthly, our results indicate that sustainable forestry practices need to maintain the mixed character of forest stands where they occur, the vertical structural complexity as well as a number of high and mature trees in managed forest stands. Finally, we argue that the 14 species of unfavourable conservation status (SPEC 2 and 3) together with the typical species found per bird habitat type should be integrated into the future monitoring scheme of Pindos National Park, as a tool for forest management (Kati & Sekercioglu 2006; Mu ¨ller 2005). The above proposals can have an extrapolative value in other mountainous reserves across the country and in the Mediterranean mountains.

Acknowledgements This research was partially funded by the Hellenic Ministry of Environment and Public Works in the frame of the Sustainable Development Project (ETERPS funds) and from Pindos Perivallontiki NGO. We are grateful to I. Leonardos from the University of Ioannina for support, to J. Foufopoulos and to S. Sfenthourakis for helpful comments on the manuscript.

Appendix I Inventory of all 62 bird species recorded in the study area and weighted index (w) according to their conservation status (SPEC category 2004).

Table A1 Code Pvir Dmart Dmaj Dsyr Dmed Dmin — Larb — — Durb Acamp Atriv Mflav — Malb Ccincl Ttrogl Pmod Erub Lmeg Phocrh Ooen Montsax Tmer Tphil Tvisc — — Satr

Species Piciformes Picus viridis Dryocopus martius Dendrocopos major Dendrocopos syriacus Dendrocopos medius Dendrocopos minor Passeriformes Galerida cristata Lullula arborea Alauda arvensis Hirundo daurica Delichon urbica Anthus campestris Anthus trivialis Motacilla flava Motacilla cinerea Motacilla alba Cinclus cinclus Troglodytes troglodytes Prunella modularis Erithacus rubecula Luscinia megarhynchos Phoenicurus ochrurus Oenanthe oenanthe Monticola saxatilis Turdus merula Turdus philomelos Turdus viscivorus Sylvia melanocephala Sylvia curruca Sylvia atricapilla

w

SPEC 2004

4 4a 1 4a 4a 1

2

2 4a 2 1 2 4a 1 1 1 1 1 1 1 1 1 1 2 2 1 1 1 1 1 1

3 2 3

4 4

3 3

4 4 4 3 3 4 4 4 4 4

Code

Species

w

Phcol Rreg Rign Mstr Ppal Plug Pmont Pcrist Pater Pcaer Pmaj Acaud Seur Cfam Cbra Lcol Ggland Ccor Ccorax Pdom Fcoel Sser Cchl Ccard Ccan Lcurv Pyrpyr Ccoc Ecitr Ecirl Ehort Mcal

Phylloscopus collybita Regulus regulus Regulus ignicapilla Muscicapa striata Parus palustris Parus lugubris Parus montanus Parus cristatus Parus ater Parus caeruleus Parus major Aegithalos caudatus Sitta europaea Certhia familiaris Certhia brachydactyla Lanius collurio Garrulus glandarius Corvus corone Corvus corax Passer domesticus Fringilla coelebs Serinus serinus Chloris chloris Carduelis carduelis Carduelis cannabina Loxia curvirostra Pyrrhula pyrrhyla Coccothraustes coccothraustes Emberiza citrinella Emberiza cirlus Emberiza hortulana Milaria calandra

1 1 1 2 2 1 1 4 1 1 1 1 1 1 1 4a 1 1 1 2 1 1 1 1 4 1 1 1 1 1 4 4

SPEC 2004 4 4 3 3 4 2 4

4 3

3 4 4 4 2

4 4 2 2

a Species of Annex I of 79/409EU. SPEC 2: concentrated in Europe and with unfavourable conservation status, SPEC 3: not concentrated in Europe but with unfavourable conservation status, SPEC 4: concentrated in Europe and with favourable conservation status.

ARTICLE IN PRESS Bird communities and reserve management Species codes are given only for the species recorded during the point counts. See Table A1

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