Forest structural complexity could be a good predictor of overall species
diversity. Since tree harvesting has a negative effect on forest structure,
it is important to analyse the effects of this disturbance on sensitive
groups, as forest birds. In this study, we aimed to shed light on this
aspect by analysing a set of univariate metrics in bird communities
breeding in three coppiced forest habitats (coppiced of chestnut, coppiced
of Turkey oak and high forest of beech) along a gradient in age classes. We
hypothesised that, with increasing forest age, (i) breeding bird communities will
progressively increase in diversity and, (ii) due to higher habitat
heterogeneity due to coppicing, a higher species turnover in the first age
classes could appear. In each forest habitat, all the metrics significantly
increased, from recently coppiced to more mature forests, due to
progressively higher availability of resources and niches along the gradient.
When comparing paired forest habitats, abundance and richness were
significantly different only in the two oldest age classes, highlighting that
responses to different tree composition were more marked in the mature
phase. In all forest habitats, species turnover (
Forests are universally recognised as a mosaic of complex and multifunctional ecosystems with intrinsic value. Therefore, forest management cannot be based only on the principles of the market economy but also on those of biodiversity conservation and ecosystem services (Lindenmayer et al., 2000; Siitonen, 2001; Pardini et al., 2005, 2010).
The structural complexity of a forest seems to be a good predictor of overall species diversity (Annand and Thompson, 1997; Dìaz et al., 2005). Accordingly, analysis of forest structures is known as a reliable criterion with which to assess the conservation value of forest stages (Doyon et al., 2005). Moreover, the structural changes of the forests have implications on their ecological functions, by alteration of the microclimate, the production of food resources and the capacity to provide shelter or nesting sites to animals (Wiens, 1989; Chapin III et al., 2000).
Forest birds, for their easy detectability and high sensitivity to human-induced environmental stress, are an important group for analysing the effects of forest ecosystem transformations (Blondel, 1975, 1981a; Wiens, 1989; Noss, 1990; Villard, 1998). Moreover, these animals depend very heavily on vegetation structure and their populations can be deeply affected by forest cutting (Ferry and Frochot, 1974; Canterbury et al., 2000; Jobes et al., 2004), one of the major anthropogenic threats recognised by the IUCN (International Union for Conservation of Nature, code 5.3 “Logging and wood harvesting”; review in Brawn et al., 2001; Battisti et al., 2016).
Tree harvesting has a negative effect on forest bird populations at different levels. Its intensity depends on spatial and soil features, as well as on the forest type (Donovan et al., 1997; Villard et al., 1999; Austen et al., 2001). Therefore, it is important to analyse the ecological effects of forest cuts, especially when these occur with high frequency and intensity as in the case of coppicing. Nevertheless, in southern Europe studies in this direction are few and rarely analyse the structural evolution of the differently characterised coppiced woods along age classes (Ciancio et al., 2006; Gil-Tena et al., 2007; Nascimbene et al., 2007; Torras and Saura, 2008; Spinelli et al., 2010).
The aim of this paper is to compare the structure of the bird communities in
three different types of managed forests (Turkey oak coppicing, chestnut
coppicing and beech high forest) belonging to different age classes in a
regional nature reserve. Since these habitat types increase their structural
complexity, moving from recently coppiced to high forest (and since
structural complexity is a strong driving forces of resource and niche
availability; Wiens, 1989), we hypothesised that breeding bird communities
will progressively increase their univariate metrics of diversity, such as
species abundance, richness and diversity. Moreover, since immediately after
cutting, forest habitats become more heterogeneous, with the presence of open
habitats and shrub vegetation, we hypothesised a higher species turnover
(calculated with a
The study was carried out inside the Bracciano–Martignano Regional Park
(provinces of Rome and Viterbo, central Italy, Lazio; Fig. 1), in the
northern sector of the Sabatini Mountains (size: 3000 ha, geographic
coordinates:
Map of the study area, depicting Italy (top right), the Lazio region and the sampling area on the hills north-west of Lake Bracciano (bottom left, dotted).
We studied three forest habitats: (1) coppiced woodlands of chestnut
(
Forest habitats differ in structural traits due to different practices of coppice management: in particular, in chestnuts and Turkey oak woods traditional practices of coppicing were carried out with a specific time frequency for cutting (about 15–18 years). In contrast, beech forest were managed as high forest and practices are completely different (Ciancio et al., 2006). In southern Europe, high forest is a form of government characterised by a turn of about 90 years, followed by the birth of seedlings (details in Table 1).
Structural traits of forest habitats in the study area (see Methods for details). DBH is diameter at breast height.
For each forest habitat, we selected four age classes following the dynamic steps of their structure and local history of coppicing (Pregitzer and Euskirchen, 2004; Scarfò, 2012): the first three age classes belong to different succeeding steps of cutting, while the fourth step (an unmanaged wood) has been considered a control (i.e. woods with the oldest age when compared to coppicing turn; Scarfò, 2012; Table 1).
Breeding bird communities was studied in the 2014 spring season (from March
to May) with the point count method (Bibby et al., 2000). This method is
particularly suitable for studies in patchy landscapes and in the spring period
when species show territorial behaviour, so they can be easily detected
(Blondel, 1981b; Sutherland, 2006). We used a 4 (age classes)
In each age class of each forest habitats, we located six point counts.
Sampling points were randomly selected using a random number generator:
Within each point count we recorded any individual bird seen and/or heard (song, call, drumming, alarm display), during a standardised fixed time (5 min), within a radius of 50 m. The use of this sampling distance was considered reliable for reducing the bias of detectability between mature and recently cut woodlands, where the probability of contacting birds is much broader and less sound absorbing because of dense vegetation (Sutherland, 2006).
In each point count we carried out two sampling sessions (session I: March, from 7 to 25; II: from 1 to 11 May 2014; total time effort: 720 min). We recorded birds in the morning from dawn to approximately 10:00. The distance among point counts remained at least 250 m to avoid counting the same individuals several times (pseudoreplication bias; see Rossi de Gasperis et al., 2016). For each species, in each point count, the highest value recorded in the two sampling sessions was considered valid (Blondel, 1975; Malavasi et al., 2009).
We used Nikon Monarch binoculars
For each age class of each forest habitat, we obtained the species-specific
abundance (number of individuals,
Analysis has also been carried out at forest guild level (sensu stricto Verner, 1984), i.e. separately considering the species linked even partially with forest habitats (see Moore and Hooper, 1975; Cieslak, 1985; Opdam et al., 1985; Møller, 1987; Hinsley et al., 1995; Bellamy et al., 1996; Ukmar et al., 2007; list in Supplement Sect. S2) and calculating the percentage of their frequency in total for the whole assemblage (% FrFor).
To assess the level of intra-turnover of species inside the bird
communities, we calculated the
To test if there are significant differences among mean values among
multiple paired samples (i.e. samples with the same number of replicates,
In total, we recorded 868 individuals belonging to 30 species of breeding birds (checklist and data on abundances and on their frequencies at species level are reported in the Supplement Sect. S3).
Mean abundance and mean richness resulted in significant differences among the four age classes for all the forest habitats (Friedman test; Table 2), with highest values in class 4 at all sites. Analogously, Shannon–Wiener index also increased progressively from the youngest (1) to oldest (4) age classes.
Structural parameters of the bird community in the different forest
habitats (Ch is chestnut; Oa is Turkey oak; Be is beech woods).
Mean abundance of forest bird species (see Table 2) in the different forest habitats (age class and tree composition). Chestnut in white, Turkey oak in grey and beech in black. Error bars represent the standard deviation.
Bird communities were mainly composed of forest species, both
qualitatively and quantitatively, with their frequency ranging between
87.2 % and 100 % of the total number of communities (Table 2). Considering
only these species, we observed a significant difference among age classes
in each forest habitat, both for mean abundance (chestnut:
Mean richness of forest bird species (see Table 2) in the different forest habitats (age class and tree composition). Chestnut in white, Turkey oak in grey and beech in black. Error bars represent the standard deviation.
Comparing mean abundance and mean richness between paired forest habitats
for each age class, we observed significant differences (
Comparison of mean abundance and mean richness between paired
forest habitats (Ch is chestnut; Oa is Turkey oak; Be is beech woods) for each age
class (from 1 to 4).
*
Comparisons between mean abundance and mean richness between
contiguous age classes (from 1 to 4) for different forest habitats.
*
Regarding intra-habitat
We observed a progressive and significant increase in diversity of breeding birds along an age gradient of different coppiced forest types. These results corroborated the general model that bird diversity metrics increase with the structural diversity of vegetation rather than its floristic composition (Johnston and Odum, 1956; Shugart and James, 1973; Shugart et al., 1975; Fuller and Henderson, 1992; Holmes and Sherry, 2001; Renfrew et al., 2005), following an analogous increase in resources and niches available for different species (see the relationship between abundance resources and richness niches; e.g. Ferry and Frochot, 1974; Blondel, 1981a; Maurer, 1986; Wiens, 1989; Martensen et al., 2008; Moning and Müller, 2009; Martensen et al., 2012; Sánchez et al., 2012; Bergner et al., 2015).
When we compared forest habitats, controlling for age class, we observed that mean abundance and richness significantly differ only in the most mature classes, while no difference occurs between recently cut woods (age classes 1 and 2). In the youngest age classes, forest habitats show a simplified structure which appears suitable only for a restricted number of species, which are more ecologically linked to shrubs, edge and open habitats and not specialised toward different tree species. Quantitative differences between forest habitats become significant only when these habitats markedly change their structure (oldest age classes: 3 and 4); i.e. when the woods grow older, the structural differences increase among different habitats, making new and different resources and niches available and favouring a quantitative differentiation in abundance and richness of bird communities.
Specifically, at species level, some hole-nesting species increases in
abundance as tree size progressively increases, for example tits (Paridae),
woodpeckers (Picidae),
Coppice management practices induce an increase in environmental
heterogeneity at landscape and patch scale (Turner, 1989; McGarigal and
McComb, 1995), affecting forest bird communities (Camprodon and Brotons,
2006; Castro et al., 2009; Dickson et al., 1993; Paillet et al., 2010). In
our study, the younger age classes of coppice (1 and 2) also showed the
highest level of intra-habitat
The bird communities associated with forest habitats are subject to different effects of forestry, depending on their level of specialisation (Dickson et al., 1993). Our communities were mainly composed of forest species. Therefore, patterns observed for overall bird assemblages have also been confirmed for the guild of strictly forest species: their structure significantly changed in all forest types, both in terms of mean abundance and richness along age groups, with a gradually increasing trend toward the older age class.
Forest species responses to structural changes were also evident. Forest
species can be divided into two groups, (i) forest species sensu lato, i.e. generalist
species linked to forest, wooded mosaics and wood-edge habitats, and (ii)
forest interior species, i.e. specialised species that nest only within the
interior of the forest and tend to avoid edge habitats (Whitcomb et al.,
1981; Villard, 1998). The generalist forest species, such as tits (Paridae),
Our study analysed communities almost entirely composed of forest species and found an inverse pattern to that reported by Fuller and Moreton (1987) and Fuller and Henderson (1992), in which total abundance and diversity were highest in the youngest coppiced woods. Independently of tree species composition, older age class forests showed forest bird communities characterised by the highest values of diversity metrics (abundance, richness and Shannon–Wiener diversity), which were highly sensitive and specialised for more complex vegetation structure.
To conclude, our work shows that in forest bird communities when increasing
age of the forests (i) habitat heterogeneity (
However, these patterns could be dependent on forest types, on geographic and climatic conditions and contexts (Mediterranean area), on peculiar species composition (also due to distributional factors of species at regional scale) and on the local history of coppicing. Moreover, although our stratified sampling design allowed consistent data patterns to be obtained on different treatments (multiple age classes for each forest habitat), it is probable that increasing the number of sampling points for each treatment could add information on some rare species not recorded in our analysis. Therefore, long-term studies at wider spatial scales will be desirable to corroborate our patterns, by providing support to select sensitive bird species in managed forest landscapes (see Villard and Jonnson, 2009).
Data available only on personal request to the authors.
The supplement related to this article is available online at:
LM, CB and GMC designed the study, LM carried out the field sampling, and LM and CB performed the analyses. All the authors wrote and revised the manuscript.
The authors declare that they have no conflict of interest.
We thank Andrea Cerulli (Parco Naturale Regionale di Bracciano–Martignano) and Fabio Scarfò (Riserva Naturale Regionale Monterano), for their information on local forest management and for facilitations in the study areas. Two anonymous reviewers and the editor-in-chief (Daniel Montesinos) largely improved the first draft of the manuscript with useful suggestions and comments. Alessandro Zocchi reviewed the English style and language.Edited by: Daniel Montesinos Reviewed by: two anonymous referees