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Effects of landscape context on bird species abundance of tree fall gaps in a temperate deciduous forest of Northern Iran
Forest Ecology and Management 267 (2012) 182–189
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Effects of landscape context on bird species abundance of tree fall gaps in a temperate deciduous forest of Northern Iran Maryam Gharehaghaji a,⇑, Afshin Alizadeh Shabani a, Jahangir Feghhi b, Afshin Danehkar a, Mohammad Kaboli a, Sohrab Ashrafi a a b
Department of Environment Science, Faculty of Natural Resources, University of Tehran, Karaj, Iran Department of Forestry, Faculty of Natural Resources, University of Tehran, Karaj, Iran
a r t i c l e
i n f o
Article history: Received 29 September 2011 Received in revised form 30 November 2011 Accepted 1 December 2011 Available online 30 December 2011 Keywords: Forest gap Natural disturbance Breeding bird abundance Bird richness Landscape context Hyrcanian forest
a b s t r a c t Tree fall gaps caused by natural disturbances are a major source of heterogeneity in intact forests. Bird species are known as ecological indicators, reflecting landscape level changes. Yet, the role of landscape context in bird species abundance within small gaps is not fully addressed. We examined the difference between avian richness and abundance within tree fall gaps and closed canopy forest areas in Kheyrud forest, located on the east of Noshahr Township, Mazandaran province in Iran as a representation of Hyrcanian forest. Breeding bird census was taken in 20 selected gaps (0.1–0.4 ha) and 250 m from the center of each gap known as controls. Birds were surveyed during breeding season in spring 2010. We also determined whether landscape context affected the abundance, richness and particular species abundance within the gaps. For this, we assessed landscape metrics by the Landscape Context Tool for every gap. Abundance (P = 0.003) and richness (P = 0.014) of birds were significantly higher in the gaps than in closed canopy controls. Gaps were higher in herb cover, coarse woody debris density and volume as well as pit and mound micro topography than controls. Great Tit (Parus major), Coal Tit (Parus ater), Eurasian Nuthatch (Sitta europaea), Common Chaffinch (Fringilla coelebs) and European Goldfinch (Carduelis carduelis) were more abundant in gaps than in controls. Among which, European Goldfinch was the only gap specialist species. Song Thrush (Turdus philomelos) was the only species more abundant in controls than gaps. Mean tree diameter had a significant positive relation with avian richness and abundance in gaps, rather than landscape context rate but forest specialist richness was negatively related to gap size. Abundance of Great Tit was related to landscape context rate. Our study highlights the role of gap quality for breeding birds; therefore improving the quality of gap habitats especially maintaining dead wood should be considered as an important conservation factor. Management practices for providing habitat of gap specialists by taking out the remaining trees and making the gaps larger would increase bird species richness in a landscape scale but the shape and size of the openings should be according to the species requirements. We suggest that maintenance of tree fall gaps as a heterogeneous habitat and dead wood resource is crucial for promoting species richness. Ó 2011 Elsevier B.V. All rights reserved.
1. Introduction Disturbance is a constant feature of forest ecosystems (McCarthy, 2001) often leading to creation of forest openings (Turner, 2005). Depending on the intensity and area of disturbance, gaps of different sizes are formed in forest stands at different points of time, introducing different mosaic patterns in the forest landscape (Busing and White, 1997). The structure of this patch mosaic (e.g. patch density, distance between patches, patch arrangement) is important to many species (Forman and Godron, 1986). ⇑ Corresponding author. Tel.: +98 9124242503; fax: +98 2612229721. E-mail address: [email protected] (M. Gharehaghaji). 0378-1127/$ - see front matter Ó 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2011.12.001
Tree fall gaps affect the vertical and horizontal structure of the forest. This creates a specific microhabitat that differs from the understory of the surrounding forest in vegetation structure, plant species composition, microclimatic condition and resource abundance. Birds may select habitats based on minor differences in vegetation or microclimate (Blake and Hoppes, 1986). Increased primary productivity caused by higher light incidence in gaps creates greater vegetation density, structural heterogeneity and higher density of insects (Noss, 1991). Some birds may prefer early successional gap habitat based on the unique qualities of the vegetation, for instance dense understory, well-developed herb and shrub layer (Bowen et al., 2007). In addition, higher densities of invertebrates have been confirmed at edges between forest and disturbed areas (Helle and Muona, 1985).
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The distribution and abundance of early successional birds are potentially determined not only by vegetation characteristics and the area of forest gaps, but also by the amount and pattern of early successional habitats in the surrounding landscape (Lichstein et al., 2002). Every species perceive habitat patterns in different ways and at different spatial scales (Wiens, 1989). Perforations create a forest edge near the interior of forest patches and thereby they are considered as an ecologically important type of fragmentation because they introduce potential edge effects deeper into intact forests (Riitters and Coulston, 2005). Many studies have shown that particular species reach their highest or lowest abundances at particular habitat edges (Dale et al., 2000). For many species, the requirements for moving between habitat/resources patches and establishing in new habitats are rather broad (e.g. generalist species). These species can occur in forest and open spaces. There are also many species (e.g. specialist species) that require more specific conditions for movement and dispersal within landscapes (Kuuluvainen et al., 2004) like species associated with interior forest which avoid edges. Other species may occur only in canopy gaps assigned as gap specialists. The Hyrcanian (Caspian) forest in Northern Iran, unlike the arid and semiarid landscape throughout most of Central and Southern Iran, is one of the remnants of natural closed-canopy deciduous forests in the world. The Caspian forests, which form a long and narrow vegetation belt on the northward slopes of the Alborz Mountains cover an area of 1.84 million hectare. The Caspian forest is known as the oldest forest in the world and is mother of European forests. This area is characterized by a Euro-Siberian flora unique to Iran (Siadati et al., 2010). The Hyrcanian forest is rich in biological diversity, and includes many endemic and endangered species but is among the highly threatened ecosystems in Iran because of extensive urbanization, timber harvest, overgrazing and tourism (Akhani et al., 2010). Few gap-studies have been conducted in the temperate deciduous forests. Also, many of the temperate-zone studies focus on managed canopy gaps (such as group selection cuts) rather than natural gaps caused by blowdowns and the death of large trees. Bird species abundance and richness are thought to be different in forest gaps and controls owing to microclimate and resource differences. Forest generalists, forest specialists and gap specialists may respond differently to tree fall gaps. Landscape context (e.g. gap size, shape, density, arrangement) may affect the abundance of particular species as well. This study aims firstly to test if there are differences in the abundance and richness of breeding birds between gaps and forest controls in an intact deciduous forest. Secondly we test if landscape context affects the abundance and richness of total birds and ecological groups within gaps. Finally we determine whether landscape context affects particular species abundance within the gaps.
2. Methods 2.1. Study area and tree fall gaps This study was carried out in Gorazbon district; a 1000 ha forest tract and the third district of Kheyrud Forest (36°400 N; 51°430 E) located on the east of Noshahr Township, Mazandaran Province in Iran as a representation of Hyrcanian forest. The climate of this region is sub-Mediterranean. Mean annual temperature is 15.9 °C and mean precipitation reaches to 1380.5 mm per year. Elevation ranges from 1000 to 1300 m. Common tree species include Oriental Beech (Fagus orientalis), Caucasian Alder (Alnus subcordata), European Hornbeam (Carpinus betulus), Scots Elm (Ulmus glabra), Chequers tree (Sorbus torminalis), Persian Iron Wood (Parrotia
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persica), Chestnut-leaved Oak (Quercus castaneifolia) and Smallleaved Linden (Tilia cordata) (Forest Management Plan, 2010). Kheyrud experimental forest has been under the direct supervision and protection by Tehran University Since 1962 for training purposes (Siadati et al., 2010). The Gorazbon district is an intact un-even aged forest in which canopy gap formation occurs naturally. The trees range from 20 to 200 years. Creation of gaps is the result of blowdowns by windstorms and the natural process of trees reaching their longevity. Logging and clearing is prohibited in this area but traditional grazing takes place. The management plan of Gorazbon was assigned in year 2010 which is after the study was conveyed (Forest Management Plan, 2010). In the Gorazbon district 35 tree fall gaps have been identified, which are larger than 0.1 ha in size. Among which, we selected 20 tree fall gaps with at least 250 m from each other (Ralph et al., 1995). Study gaps ranged from 0.1 to 0.4 ha and were less than 50 m in minimum width. The center of each gap was determined using the center of mass extension (Jenness, 2006) in ArcView 3.2 (ESRI Inc., 1999). Closed canopy control sites (n = 20) were determined 250 m from the center of each gap (Fig. 1). It should be noted that some gaps (larger gaps) were more homogenous in that they were dominated by herbs with few/no trees or CWD. 2.2. Bird censuses We used the unlimited radius point-count to survey birds (Robinson and Robinson, 1999). Each site was visited twice between 19 May and 14 June. All counts were conducted between 06:00 and 10:00. Surveys began 2 min after arriving at the site and lasted for 10 min. All point counts were conducted by one observer (first author) to minimize observer bias effects (Ralph et al., 1993). The order in which points were re-surveyed was reversed to compensate for time of day bias associated with singing behavior (Costello et al., 2000). Surveys were not conducted in rainy or windy weather. Gap area was quantified by using a Global Positioning System devise. 2.3. Vegetation sampling We measured vegetation structure and habitat complexity within circular plots of 0.05 ha (12.62 m radius) in extent (Bibby et al., 1992). Vegetation structure variables included tree (>7 m in height) density, dead tree number, snag density and basal area, coarse woody debris (CWD) density and volume, mean tree diameter, mean tree height, shrub number, mean shrub height and pit and mound microtopography. Within each plot we tallied all live trees, snags and CWD. In addition, trees were classified to four categories (5–9 cm, 10–29 cm, 30–59 cm, >60 cm) based on trunk diameter (Diaz, 2006). Habitat complexity variables were visually estimated in the plots (Watson et al., 2004) and included percent cover of litter, herb, low shrub (1–2.5 m in height), tall shrub (2.5–7 m in height) and canopy. Snag basal area (BA) was calculated using, diameter at breast height (DBH) measurements of all trees >12 cm DBH (Greenberg and Lanham, 2001). CWD volume of all trees >12 cm DBH was calculated using the method described by Fridman and Walheim (2000). 2.4. Landscape context assessment For assessing the spatial characteristics of gap patches, we used Landscape Context Tool (LCT). The tool is an extension (landcontrmit.avx) in ArcView 3.2 (Ferwerda, 2003). This geospatial analysis tool calculates a landscape context rating for patches, based on patch size and shape, and landscape connectivity and proximity. Rating ranges from value 0 to 100.
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Fig. 1. Locations of 20 selected gaps and 20 forest controls in Gorazbon division, Mazandaran, Iran.
The analysis process has been based on the general paradigm that large, round patches provide the best opportunity for healthy ecological processes and that remnants that are surrounded by other remnants or connected to larger remnants by corridors, links or stepping stones provide better habitat opportunities than isolated remnants. Landscape context metrics include: patch size, maximum thickness, focal abundance, weighted linear (Ferwerda, 2003). Internal distance to edge (or maximum patch thickness) will be used as a surrogate measure of patch shape. Thickness is half the width of a patch. Focal neighborhood analysis will be used to determine the amount of gap vegetation cover surrounding each cell within a raster landscape. In this case each cell (treed or non-treed) will be assessed for the percentage cover within a series of concentric circular neighborhood. A concentric isolation measure has the advantage that size and distance of potential habitat patches in all directions is assessed and is probably a more realistic description of isolation in relation to actual dispersal processes (Vos and Stumpel, 1995). Weighted distance is a measure of distance from a cell to the nearest patch of a specified size and shape (source patches). The closer or more connected a patch is to one of these patches, the more chance there is of the patch being utilized and colonized by particular species. Landscape Context is the sum of patch (size and maximum thickness) and landscape (focal abundance and weighted linear) rate (Ferwerda, 2003). For the purpose of this study, all of the identified gaps larger than 0.1 ha (n = 35) were converted to grid using cell size 0.5 0.5 m. The grid data set was classified to gap patches valued 1 and forest matrix valued 0. Each landscape context metric was calculated by either the default rating table in the setting of the tool or creating new rating tables that were adjusted to better reflect the real characteristics of the gaps in the study area. Patch size smaller than 0.3 ha in size was rated the value 10 (the minimum rate), whereas patch larger than 0.3 ha was rated 20 as some studies showed, changes in bird abundance began to occur in gaps of 0.3 ha (Moorman and Guynn, 2001). The patch size and thickness ratings were added together resulting in an overall patch rating. Percentage gap vegetation within focal neighbourhoods of 50, 100, 150, 250, 500, 750 and 1000 m were calculated. The resulting
values were then added together to create the overall focal abundance rate. A series of distance analysis from each cell to a patch of a certain size or shape was done by the weighted linear measurement. Distance analysis of each cell to source patches was used (Ferwerda, 2003).
2.5. Statistical analysis Vegetation variables and mean species abundance were compared between gaps and forest controls using non-parametric Mann–Whitney test due to the fact that some of the data were not normal and did not turn into normal using transformation methods. Two-way ANOVA was used to test for differences among site, visit, and site visit interactions on bird abundance and species richness. Effects of visit and site visit were not significant (P > 0.05) therefore mean bird species abundance and the total number of species detected in the two visits was represented as bird abundance and richness in the two visits. Paired t-tests were used to compare mean abundance and total species richness between gaps and controls. These statistical tests were carried out in SPSS 16 (SPSS Inc., 2007). In order to understand the relation between bird abundance, richness and particular bird species abundance in gaps with habitat and landscape variables, we used multivariate linear regression analysis in R 2.8.1 (R Development Core team, 2009). In addition, every species was related to an ecological group (forest generalist, forest specialist and gap specialist) and multivariate linear regression was used to perceive better relationship between mean abundance and total richness of these groups and landscape context rate, gap size and habitat variables as Kurosawa and Askins (2003) suggest that when dealing with the effect of forest area on a bird community, it is essential to analyze separately the distribution of groups of species with different habitat preferences. This may be efficient for forest gaps too. We also used multivariate regression analysis to determine the relation between particular bird species abundance in forest controls and habitat variables. Colinearity between habitat variables was tested using Spearman correlation analysis so that variables with high correlation coefficients (r-values > 0.7) were excluded. Models
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were selected according to the least AIK (Akaike’s Information Criterion). 3. Results 3.1. Bird and habitat variables among gaps and forest controls The abundance of breeding birds was higher in gaps than in controls (t = 3.363, d.f. = 19, P = 0.003). Total species richness was higher in gaps than in controls (t = 2.703, d.f. = 19, P = 0.014) (Fig. 2). Species including Eurasian Nuthatch (Sitta europaea), Coal Tit (Parus ater), Great Tit (Parus major), Common Chaffinch (Fringilla coelebs) and European Goldfinch (Carduelis carduelis) were significantly more abundant in gaps than in controls. Among which, European Goldfinch was the only gap specialist species. Chiffchaff, Scops owl and Eagle owl were only heard in the gaps but they were not significantly more abundant in gaps than forest controls. Song Thrush (Turdus philomelos) was the only species recorded more in controls. The numbers of Eurasian Jay which are nest predators were not significantly different between gaps and controls (Table 1). Herb cover, mean tree DBH, CWD density, CWD volume as well as pit and mound microtopography were higher in gaps than in controls. Tree density, low shrub and canopy cover were lower in gaps than controls (Table 2). 3.2. Bird distribution in relation to habitat and landscape variables Landscape context rate was used as the ultimate landscape value for each patch and entered in multi regression analysis. After applying Spearman correlation analysis, five gap vegetation variables including tree number, mean tree DBH, dead tree number, herb cover and landscape context rate were entered as independent variables in multiple regression analysis of birds abundance, richness and particular bird species abundance in gaps. Mean bird species abundance and total richness in gaps were positively related to mean tree DBH but no relation was found between landscape context rate (e.g. patch size) and the two variables. When mean abundance and total species richness of the different ecological groups (except for gap specialist which included one species) were analyzed, no significant relations between the abundance and richness of each ecological group (forest generalist/specialist) and landscape context rate were found. However, there was a negative relation between forest specialist richness and gap size (Table 3). Also a negative trend between
Fig. 2. Mean (±SE) abundance (P = 0.003) and richness (P = 0.014) of breeding birds in small tree fall gaps and closed canopy forest in Kheyrud Experimental Forest, Mazandaran, Iran.
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forest generalist richness and forest specialist abundance and gap size was shown (Fig. 3). Mean tree DBH was positively related to forest specialist abundance (Table 3). The mean abundance of Great Tit was positively related to landscape context rate (Table 4). European Goldfinch was not related to any of these variables. Also variables, including mean tree DBH, shrub number, tree number >60 cm DBH, dead tree number, litter cover were extracted using spearman correlation analysis and were entered in multiple regression analysis of birds abundance and richness in forest controls. Species that had a significant relationship with forest habitat variables are shown in Appendix A.
4. Discussion 4.1. Role of gaps in providing unique resources The abundance and richness of breeding birds were higher in gaps than in controls. Several other studies indicate higher bird abundance and richness in gaps (Fuller, 2000; Greenberg and Lanham, 2001). It seems that birds are capable of tracking distinct microhabitats of small gaps and utilizing their remarkable resources. Higher bird abundance and richness in gaps than controls seems to be associated with higher coarse woody debris volume and density, greater herb cover as well as pit and mound micro topography. Most habitat characteristics in gaps were in accordance with Greenberg and Lanham (2001) and Doyon et al. (2005). Shrubs were lower in gaps than controls because traditional grazing takes place in the study area so sheep can roam more easily in gaps than forest and remove the lower stratum of vegetation. Also, the gaps that are dominated by herbs are in early successional stages that still do not include shrubs. Birds may be more attracted to gaps due to more food abundance and detectability, nest material, protective cover and accessibility to different habitat types at the same time (Greenberg and Lanham, 2001; Moorman and Guynn, 2001). The pit-and-mound topography created by uprooted trees, lying logs, boulders rapidly covered by a moss litter carpet, brush piles and shrub cover increase the diversity of available insect niches as a main food source for most bird species in the study area. Moreover, in gaps the quantity and diversity of CWD as crucial foraging site are concentrated rather than scattered in the forest (Bouget and Duelli, 2004) hence more easily detectable. The presence of slash may be important to avian habitat selection as it can provide added protective cover to ground nesters (Costello et al., 2000) for instance Winter Wren, Black Bird and Common Chiffchaff or ground foragers like Common Chaffinch and European Goldfinch. Fuller (2000) also found more Winter Wren and Black Birds in small (<50 m minimum dimension) gaps but concluded that Common Chiffchaff selected larger (>90 m minimum dimension) gaps over small ones. This confirms the fact that, Common Chiffchaffs were not significantly more abundant in the studied gaps which were less than 50 m in minimum width. The results indicate that mean DBH may be a deciding factor for predicting bird abundance and species richness in gaps. As trees mature they provide increasingly more suitable substrates for a range of cavity nesters (Blue Tit, Great Tit, Coal Tit, Red breasted Flycatcher, Eurasian Nuthatch and Syrian Woodpecker) and/or bole associated foragers (Eurasian Nuthatch) due to increasing trunk diameter and bark complexity (Holmes et al., 1979). This may be the reason why some forest specialists (Eurasian Nuthatch, Coal Tit) were higher in gaps than in controls. Fuller (2000) also showed that Great Tit and Eurasian Nuthatch were abundant in small natural gaps. We conclude that small natural gaps created in intact forest do not have a negative effect on the abundance of forest specialists; in contrast it will improve some species abundance in breeding season provided that
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Table 1 Abundance (±SE) (mean number of individuals in two visits) of bird species identified in 20 tree fall gaps and 20 closed canopy cover controls in Kheyrud Forest, Mazandaran, Iran. Species
Scientific name
Wood Pigeon Scops Owl Eagle Owl Syrian Woodpecker Green Woodpecker Winter Wren European Robin Common Nightingale Common Blackbird Song Thrush Common Chiffchaff Red-breasted Flycatcher Coal Tit Great Tit Blue Tit Eurasian Nuthatch Common Chaffinch Brambling European Goldfinch Golden Oriole Eurasian Jay a * **
Group a
Columba palumbus Otus scops Bubo bubo Dendrocopos syriacus Picus viridis Troglodytes troglodytes Erithacus rubecula Luscinia luscinia Turdus merula Turdus philomelos Phylloscopus collybita Ficedula parva Pariparus ater Parus major Cyanistes caeruleu Sitta europaea Fringilla coelebs Fringilla montifringilla Carduelis carduelis Oriolus oriolus Garrulus glandarius
G G S G G G G G G G S S S G G S G G GS G S
*
Habitat variable
Control
Gap
P-value
Tree density Mean tree height (m) Mean tree DBH (cm) Shrub height (m) Snag density Snag BA (m2/ha) CWD density CWD volume (m3) % Canopy % Tall shrub % Low shrub % Herb % Tip up mounds % Pits
17.05 17.24 28.01 2 23 1.04 10 0.40 94.04 9.55 5.05 30.40 0.75 0
5.55 16.70 33.48 1.60 12 1.50 22 4.19 13.25 4.7 1.50 78.80 5.5 2.25
0.00** 0.93 0.00** 0.70 0.10 0.51 0.01** 0.00** 0.00** 0.41 0.05* 0.00** 0.04* 0.03*
P < 0.05. P < 0.01.
Table 3 Relationships between habitat and landscape variables and abundance and richness of birds (total/ecological groups) within gaps.
Mean bird abundance Total bird richness Forest specialist abundance Forest specialist richness *
Gap
P-value
0.27 ± 0.07 0.00 ± 0.00 0.00 ± 0.00 0.95 ± 0.13 0.20 ± 0.06 1.37 ± 0.11 1.17 ± 0.11 0.4 ± 0.1 1.60 ± 0.11 1.30 ± 0.125 0.00 ± 0.00 0.22 ± 0.07 1.10 ± 0.10 0.62 ± 0.09 0.85 ± 0.12 0.30 ± 0.07 2.47 ± 0.11 0.22 ± 0.08 0.00 ± 0.00 0.12 ± 0.06 0.17 ± 0.07
0.12 ± 0.05 0.02 ± 0.02 0.02 ± 0.02 1.22 ± 0.15 0.12 ± 0.53 1.67 ± 0.09 0.87 ± 0.10 0.35 ± 0.10 1.82 ± 0.11 0.70 ± 0.11 0.10 ± 0.05 0.40 ± 0.10 1.47 ± 0.13 1.17 ± 0.15 1.22 ± 0.13 0.60 ± 0.11 2.87 ± 0.13 0.07 ± 0.04 0.15 ± 0.05 0.20 ± 0.06 0.22 ± 0.08
n.s n.s n.s n.s n.s n.s n.s n.s n.s 0.00** n.s n.s 0.02* 0.01* n.s 0.05* 0.03* n.s 0.00** n.s n.s
Abbreviations: G, forest generalist; S, forest specialist (BirdLife International, 2010) and GS, gap specialist (interpreted by the study results). P < 0.05. P < 0.01.
Table 2 Mean values of habitat variables for gaps and closed canopy forest (controls) in Kheyrud Forest, Mazandaran, Iran.
**
Control
Model
R2
P
AIC
0.098 (mean tree DBH) + 12.181 0.085 (mean tree DBH) + 9.094 0.056 (mean tree DBH)
0.228
0.033*
84.270
0.308
0.011*
70.687
0.238
0.028
*
61.057
4.863 (gap area) + 3.518
0.233
0.031*
51.433
P < 0.05.
it provides high cover and meets their needs of large trees. As growth of vegetation continues to reduce the abruptness between openings and adjacent forest, gap specialists and some forest interior species may increase their use of gaps as nesting, foraging, or brood rearing habitat (Moorman and Guynn, 2001). These results are in agreement with Fuller (2000) who concluded that there was a considerable overlap in the bird species composition at gaps
and forest controls and Greenberg and Lanham (2001) who deduced that forest interior species were indifferent to small forest gaps that retain a partial canopy. Goldfinch was the only gap specialist found in the studied gaps. Laiolo (2002) also assigned Goldfinch as an edge species and Santos et al. (2002) classified it as a ubiquitous species which can feed and nest on isolated trees or shrubs. Identifying only one gap specialist may be due to the small size of gaps and low shrub cover as Fuller (2000) related few gap specialists in old growth stands of Poland, to larger gaps that had dense understory foliage. A study by Robinson and Robinson (1999) also related the positive effect of gaps on the population of gap dependent species to the dramatic surge in production of shrub and understory plants used for foraging and breeding. There are also some gap species (e.g. Chiffchaff) that benefit from forest management practices and occur in higher densities in managed gaps comparing to natural gaps (Piotrowska and Wesołowski, 1989). Song Thrush was more frequent in forest controls than gaps. A study done by Creegan (2004) also showed that Song Thrushes had an aversion for edge habitat but in fact preferred interior habitat. During the bird survey period, no evidence of Cuckoo as parasite species was observed. The numbers of Eurasian Jay which are nest predators were not significantly different between gaps and controls (Table 1). So edge – associated nest predation and parasitism seem to occur less frequently in the studied gaps hence more species attracted to them. 4.2. Relationship between bird (total/within ecological group) abundance and richness and gap size and landscape context rate The effect of gap size on the abundance and richness of all birds and generalists were not significant. Levey (1988), Fuller (2000) and Bowen et al. (2007) have also concluded no relation between abundance and gap size. However Greenberg and Lanham (2001) and Moorman and Guynn (2001) showed a significant positive relation between gap size and bird abundance in gaps. It seems that larger gaps in our study (0.4 ha) do not provide more favorable habitat than smaller ones. As the results show, bird abundance and richness in gaps were related to mean tree DBH indicating that larger gaps with less mean tree DBH or no trees at all, may lead to less abundance and richness of birds. Forest specialist richness was
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Fig. 3. Relationship between mean abundance and total richness of breeding birds and gap area for ecological groups in Kheyrud forest, Mazandaran, Iran.
Table 4 Relationships between habitat and landscape variables and particular species abundance in gaps.
* **
Species
Model
R2
P
AIC
Eurasian Nuthatch Winter Wren Great Tit European Robin Blue Tit
0.107 (tree number)
0.271
0.018*
29.871
0.026 (mean tree DBH)+0.800 0.090 (landscape context rate) 0.028 (mean tree DBH)
0.267 0.259 0.364
0.019* 0.022* 0.005**
27.309 46.767 21.191
0.229 (dead tree number) + 0.019 (herb)
0.439
0.023*
34.849
P < 0.05. P < 0.01.
negatively related to gap size although some specialist species were higher in smaller gaps. Apparently as gaps became larger (0.2–0.4 ha) species such as Red breasted flycatcher, Chiffchaff and Eurasian jay disappeared. This suggests that larger homogenous gaps did not meet specialist needs for cover and protection as smaller gaps (with higher canopy cover and habitat complexity) did. Consequently, bird species richness in a forest gap is not only related to gap size but also influenced by habitat resources in which result in habitat quality. The natural gaps in our study are
not created at the same time and being so, they reflect different stages of succession and are different according to vegetation structure and complexity. More developed forest stages may benefit forest bird species richness by providing more cavities and a higher amount of dead wood as nesting and feeding substrates (e.g. invertebrates) for many bird species (Camprodon, 2001). The concept of patch as a collective habitat of the species in a guild has great utility as a basis for understanding avian relationships to successional phases (Keller et al., 2003). No study has yet addressed the relationships between breeding bird assemblages and landscape context in gaps of small size as ours. As the results show, the effect of landscape context rate on mean abundance and total richness of total birds and ecological groups was not significant. For many species, it is perhaps not the isolation or size of patches that affects their population sustainability, but the overall area of suitable habitat, which may include matrix and patch habitat (Kupfer et al., 2003). The forest matrix provides a non hostile environment with suitable resources for many forest generalist and specialist species. Many bird species were identified in both gaps and closed canopy forests which shows the similarity between the two communities. It seems that the forest matrix does not impede the movement and occurrence of birds that depend on gaps and edges therefore, the presence of most gap species were not related to landscape variables and distribution of patches.
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4.3. Relationship between Great tit abundance and landscape context rate Great Tit is documented as a forest generalist species which is relatively common in landscapes containing gaps indicating an ability to utilize patchy habitat (Hinsley, 2000). Hunter (1980) deduced that most types of activities by male Great Tit took place in a visually open space as the better view from a perch would facilitate seeing predators and conspecifics. Fuller (2000) showed that Great tits preferred small natural gaps to large ones. Also, a study done by Kacelnik (1979) indicated that light intensity limits foraging efficiency of Great Tits in the early morning. This result implies the importance of light incidence and open space for foraging of the species. Landscape connectivity is a species specific trait (Taylor et al., 2006) thus, Great Tit showed a significant positive relation with landscape context rate. Despite the small size of gaps and high distribution ability of birds, the size and arrangement of patches has shown to be crucial to the abundance and distribution of this species. We suggest that smaller patches with lower landscape context rate may be used as stepping stones for reaching larger patches hence improving landscape connectivity for the species. Moreover, we anticipate that if larger patches had more suitable habitat quality (e.g. large trees, dead wood, shrubs), more species would be related to gap size and hence landscape context rate. In addition the negative effect of gap size on forest specialists would be tempered.
5. Conclusions 5.1. Management and conservation implication Our results highlight the importance of gap quality for total birds and ecological groups. In this light, the first conservation options that should be considered for any habitat patch relate to improving the quality of the existing habitat and the viability of their species’ populations (e.g. maintaining dead tree) (Kettunen et al., 2007). The retention of some canopy trees which provide habitat during forest succession for additional birds associated with mature trees (e.g. Eurasian Nuthatch, Eurasian Jay and Coal Tit) leads to higher species richness. Maintaining large trees with higher bole diameter is fundamental for many particular species (Winter Wren, European Robin) and avian abundance and richness. Grazing should be prohibited in the area to retain the understory needed for gap specialists. This is advocated by the management plan of Gorazbon. A study on the food resources (insects, fruit and seeds) located in gaps and a comparison between their quality and quantity between gaps and controls merits further research. On the other hand, slight management practices could contribute to the presence and abundance of a number of gap specialists. We believe that the conservation value of all the gap remnants were approximately equal and have to be considered for the abundance of gap specialist species (European Goldfinch). The idea of taking out the remaining trees and making the gaps larger to attract gap specialists corresponds to the management plan of the Gorazbon district but research on the habitat requirements of European Goldfinch and other possible gap specialist is essential, prior to any management applications towards them. Cutting plans would need to be designed to create patches of adequate size and shape to meet the requirements of these species (Boutin and Hebert, 2002). The fallen dead wood should remain in the gap to provide a valuable foraging source and increase habitat heterogeneity. This suggests that, Simulation of the local disturbance regime and allowing for the maintenance of physical components of bird habitat is beneficial for bird diversity (Franklin and Armesto, 1996).
Consequently, a combination of both cleared and uncleared treatments may increase species richness in the study area (Bouget and Duelli, 2004). It should be mentioned that these results were concluded for natural gaps in an intact forest. As Robinson and Robinson (1999) and Moorman and Guynn (2001) suggest, landscape context must be considered in assessing the role of gaps (natural or anthropological) and their effect on bird assemblages owing to the fact that the impact differs in a heavily intact forest landscape comparing to a fragmented landscape. Fragmented or heavily managed landscapes (e.g. most of Hyrcanian forests) may have a more detrimental effect (e.g. predation, parasitism, edge effect) and may change bird community. In addition, manmade disturbances cannot replace the role of the natural disturbances in forest ecosystem dynamics. Therefore, integrating natural disturbances into forest management practices (e.g. maintaining or replicating natural disturbances) is critical for securing the movement of disturbance dependent species within landscapes (Kuuluvainen et al., 2004). In conclusion, if maintaining total bird richness is a management goal, a combination of both cleared treatment that is taking out some residual canopy trees according to gap specialist requirements and uncleared treatments which is preserving small gaps containing a partial cover, would be beneficial for all the ecological groups namely generalist, forest specialist and gap specialist species. Acknowledgements This study was funded by the research affairs of University of Tehran. We thank Fattola Ghomi for his valued assistance in the field. We are grateful to Vahid Etemad for his devoted help in providing facilities and useful advice. We also thank Manouchehr Namiranian, the head of Kheyrud experimental forest for providing the facilities needed for this study. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.foreco.2011.12.001. References Akhani, H., Djamali, M., Ghorbanalizadeh, A., Ramezani, E., 2010. Plant biodiversity and endemism of Hyrcanian relict forests, N. Iran: A floristic, palaeoecologic and conservation overview. Pak J. Bot. Special Issue 42, 231–258. Bibby, C.J., Burgess, N.D., Hill, D.A., Mustoe, S., 1992. Bird Census Techniques. Academic Press, London. BirdLife International. 2010. The BirdLife checklist of the birds of the world, with conservation status and taxonomic sources. Version 3. Viewed 28 May 2011,. Blake, J.G., Hoppes, W.G., 1986. Influence of resource abundance on use of treefall gaps by birds in an isolated woodlot. Auk 103, 328–340. Bouget, C., Duelli, P., 2004. The effects of windthrows on forest insect communities: a literature review. Biol. Conserv. 118, 281–299. Boutin, S., Hebert, D., 2002. Landscape ecology and forest management: developing an effective partnership. Ecol. Appl. 12, 390–397. Bowen, L.T., Moorman, C.E., Kilgo, J.C., 2007. Seasonal bird use of canopy gaps in a bottomland forest. Wilson J. Ornithol. 119, 77–88. Busing, R.T., White, P.S., 1997. Species diversity and small-scale disturbance in an old-growth temperate forest: a consideration of gap-partitioning concepts. Oikos 78, 562–568. Camprodon, J., 2001. Tratamientos forestales y conservacio´n de la fauna vertebrada. In: Camprodon, J., Plana, E. (Eds.), Conservacio´n de la Biodiversidad y Gestio´n Forestal. Su Aplicacio´n en la Fauna Vertebrada. Edicions Universitat de Barcelona, Barcelona, pp. 135–179. Costello, C.A., Yamasaki, M., Pekins, P.J., Leak, W.B., Neefus, C.D., 2000. Songbird response to group selection harvests and clearcuts in a New Hampshire northern hardwood forest. For. Ecol. Manage. 127, 41–54. Creegan, H., 2004.Modelling the effects of changing habitat characteristics and spatial pattern on woodland songbird distributions in West and Central Scotland, PhD thesis, University of Stirling, Scotland. Dale, S., Mork, K., Solvang, R., Plumptre, A.J., 2000. Edge effects on the understory bird community in a logged forest in Uganda. Conserv. Biol. 14, 265–276.
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Effects of landscape context on bird species abundance of tree fall gaps in a temperate deciduous forest of Northern Iran Maryam Gharehaghaji a,⇑, Afshin Alizadeh Shabani a, Jahangir Feghhi b, Afshin Danehkar a, Mohammad Kaboli a, Sohrab Ashrafi a a b
Department of Environment Science, Faculty of Natural Resources, University of Tehran, Karaj, Iran Department of Forestry, Faculty of Natural Resources, University of Tehran, Karaj, Iran
a r t i c l e
i n f o
Article history: Received 29 September 2011 Received in revised form 30 November 2011 Accepted 1 December 2011 Available online 30 December 2011 Keywords: Forest gap Natural disturbance Breeding bird abundance Bird richness Landscape context Hyrcanian forest
a b s t r a c t Tree fall gaps caused by natural disturbances are a major source of heterogeneity in intact forests. Bird species are known as ecological indicators, reflecting landscape level changes. Yet, the role of landscape context in bird species abundance within small gaps is not fully addressed. We examined the difference between avian richness and abundance within tree fall gaps and closed canopy forest areas in Kheyrud forest, located on the east of Noshahr Township, Mazandaran province in Iran as a representation of Hyrcanian forest. Breeding bird census was taken in 20 selected gaps (0.1–0.4 ha) and 250 m from the center of each gap known as controls. Birds were surveyed during breeding season in spring 2010. We also determined whether landscape context affected the abundance, richness and particular species abundance within the gaps. For this, we assessed landscape metrics by the Landscape Context Tool for every gap. Abundance (P = 0.003) and richness (P = 0.014) of birds were significantly higher in the gaps than in closed canopy controls. Gaps were higher in herb cover, coarse woody debris density and volume as well as pit and mound micro topography than controls. Great Tit (Parus major), Coal Tit (Parus ater), Eurasian Nuthatch (Sitta europaea), Common Chaffinch (Fringilla coelebs) and European Goldfinch (Carduelis carduelis) were more abundant in gaps than in controls. Among which, European Goldfinch was the only gap specialist species. Song Thrush (Turdus philomelos) was the only species more abundant in controls than gaps. Mean tree diameter had a significant positive relation with avian richness and abundance in gaps, rather than landscape context rate but forest specialist richness was negatively related to gap size. Abundance of Great Tit was related to landscape context rate. Our study highlights the role of gap quality for breeding birds; therefore improving the quality of gap habitats especially maintaining dead wood should be considered as an important conservation factor. Management practices for providing habitat of gap specialists by taking out the remaining trees and making the gaps larger would increase bird species richness in a landscape scale but the shape and size of the openings should be according to the species requirements. We suggest that maintenance of tree fall gaps as a heterogeneous habitat and dead wood resource is crucial for promoting species richness. Ó 2011 Elsevier B.V. All rights reserved.
1. Introduction Disturbance is a constant feature of forest ecosystems (McCarthy, 2001) often leading to creation of forest openings (Turner, 2005). Depending on the intensity and area of disturbance, gaps of different sizes are formed in forest stands at different points of time, introducing different mosaic patterns in the forest landscape (Busing and White, 1997). The structure of this patch mosaic (e.g. patch density, distance between patches, patch arrangement) is important to many species (Forman and Godron, 1986). ⇑ Corresponding author. Tel.: +98 9124242503; fax: +98 2612229721. E-mail address: [email protected] (M. Gharehaghaji). 0378-1127/$ - see front matter Ó 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2011.12.001
Tree fall gaps affect the vertical and horizontal structure of the forest. This creates a specific microhabitat that differs from the understory of the surrounding forest in vegetation structure, plant species composition, microclimatic condition and resource abundance. Birds may select habitats based on minor differences in vegetation or microclimate (Blake and Hoppes, 1986). Increased primary productivity caused by higher light incidence in gaps creates greater vegetation density, structural heterogeneity and higher density of insects (Noss, 1991). Some birds may prefer early successional gap habitat based on the unique qualities of the vegetation, for instance dense understory, well-developed herb and shrub layer (Bowen et al., 2007). In addition, higher densities of invertebrates have been confirmed at edges between forest and disturbed areas (Helle and Muona, 1985).
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The distribution and abundance of early successional birds are potentially determined not only by vegetation characteristics and the area of forest gaps, but also by the amount and pattern of early successional habitats in the surrounding landscape (Lichstein et al., 2002). Every species perceive habitat patterns in different ways and at different spatial scales (Wiens, 1989). Perforations create a forest edge near the interior of forest patches and thereby they are considered as an ecologically important type of fragmentation because they introduce potential edge effects deeper into intact forests (Riitters and Coulston, 2005). Many studies have shown that particular species reach their highest or lowest abundances at particular habitat edges (Dale et al., 2000). For many species, the requirements for moving between habitat/resources patches and establishing in new habitats are rather broad (e.g. generalist species). These species can occur in forest and open spaces. There are also many species (e.g. specialist species) that require more specific conditions for movement and dispersal within landscapes (Kuuluvainen et al., 2004) like species associated with interior forest which avoid edges. Other species may occur only in canopy gaps assigned as gap specialists. The Hyrcanian (Caspian) forest in Northern Iran, unlike the arid and semiarid landscape throughout most of Central and Southern Iran, is one of the remnants of natural closed-canopy deciduous forests in the world. The Caspian forests, which form a long and narrow vegetation belt on the northward slopes of the Alborz Mountains cover an area of 1.84 million hectare. The Caspian forest is known as the oldest forest in the world and is mother of European forests. This area is characterized by a Euro-Siberian flora unique to Iran (Siadati et al., 2010). The Hyrcanian forest is rich in biological diversity, and includes many endemic and endangered species but is among the highly threatened ecosystems in Iran because of extensive urbanization, timber harvest, overgrazing and tourism (Akhani et al., 2010). Few gap-studies have been conducted in the temperate deciduous forests. Also, many of the temperate-zone studies focus on managed canopy gaps (such as group selection cuts) rather than natural gaps caused by blowdowns and the death of large trees. Bird species abundance and richness are thought to be different in forest gaps and controls owing to microclimate and resource differences. Forest generalists, forest specialists and gap specialists may respond differently to tree fall gaps. Landscape context (e.g. gap size, shape, density, arrangement) may affect the abundance of particular species as well. This study aims firstly to test if there are differences in the abundance and richness of breeding birds between gaps and forest controls in an intact deciduous forest. Secondly we test if landscape context affects the abundance and richness of total birds and ecological groups within gaps. Finally we determine whether landscape context affects particular species abundance within the gaps.
2. Methods 2.1. Study area and tree fall gaps This study was carried out in Gorazbon district; a 1000 ha forest tract and the third district of Kheyrud Forest (36°400 N; 51°430 E) located on the east of Noshahr Township, Mazandaran Province in Iran as a representation of Hyrcanian forest. The climate of this region is sub-Mediterranean. Mean annual temperature is 15.9 °C and mean precipitation reaches to 1380.5 mm per year. Elevation ranges from 1000 to 1300 m. Common tree species include Oriental Beech (Fagus orientalis), Caucasian Alder (Alnus subcordata), European Hornbeam (Carpinus betulus), Scots Elm (Ulmus glabra), Chequers tree (Sorbus torminalis), Persian Iron Wood (Parrotia
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persica), Chestnut-leaved Oak (Quercus castaneifolia) and Smallleaved Linden (Tilia cordata) (Forest Management Plan, 2010). Kheyrud experimental forest has been under the direct supervision and protection by Tehran University Since 1962 for training purposes (Siadati et al., 2010). The Gorazbon district is an intact un-even aged forest in which canopy gap formation occurs naturally. The trees range from 20 to 200 years. Creation of gaps is the result of blowdowns by windstorms and the natural process of trees reaching their longevity. Logging and clearing is prohibited in this area but traditional grazing takes place. The management plan of Gorazbon was assigned in year 2010 which is after the study was conveyed (Forest Management Plan, 2010). In the Gorazbon district 35 tree fall gaps have been identified, which are larger than 0.1 ha in size. Among which, we selected 20 tree fall gaps with at least 250 m from each other (Ralph et al., 1995). Study gaps ranged from 0.1 to 0.4 ha and were less than 50 m in minimum width. The center of each gap was determined using the center of mass extension (Jenness, 2006) in ArcView 3.2 (ESRI Inc., 1999). Closed canopy control sites (n = 20) were determined 250 m from the center of each gap (Fig. 1). It should be noted that some gaps (larger gaps) were more homogenous in that they were dominated by herbs with few/no trees or CWD. 2.2. Bird censuses We used the unlimited radius point-count to survey birds (Robinson and Robinson, 1999). Each site was visited twice between 19 May and 14 June. All counts were conducted between 06:00 and 10:00. Surveys began 2 min after arriving at the site and lasted for 10 min. All point counts were conducted by one observer (first author) to minimize observer bias effects (Ralph et al., 1993). The order in which points were re-surveyed was reversed to compensate for time of day bias associated with singing behavior (Costello et al., 2000). Surveys were not conducted in rainy or windy weather. Gap area was quantified by using a Global Positioning System devise. 2.3. Vegetation sampling We measured vegetation structure and habitat complexity within circular plots of 0.05 ha (12.62 m radius) in extent (Bibby et al., 1992). Vegetation structure variables included tree (>7 m in height) density, dead tree number, snag density and basal area, coarse woody debris (CWD) density and volume, mean tree diameter, mean tree height, shrub number, mean shrub height and pit and mound microtopography. Within each plot we tallied all live trees, snags and CWD. In addition, trees were classified to four categories (5–9 cm, 10–29 cm, 30–59 cm, >60 cm) based on trunk diameter (Diaz, 2006). Habitat complexity variables were visually estimated in the plots (Watson et al., 2004) and included percent cover of litter, herb, low shrub (1–2.5 m in height), tall shrub (2.5–7 m in height) and canopy. Snag basal area (BA) was calculated using, diameter at breast height (DBH) measurements of all trees >12 cm DBH (Greenberg and Lanham, 2001). CWD volume of all trees >12 cm DBH was calculated using the method described by Fridman and Walheim (2000). 2.4. Landscape context assessment For assessing the spatial characteristics of gap patches, we used Landscape Context Tool (LCT). The tool is an extension (landcontrmit.avx) in ArcView 3.2 (Ferwerda, 2003). This geospatial analysis tool calculates a landscape context rating for patches, based on patch size and shape, and landscape connectivity and proximity. Rating ranges from value 0 to 100.
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Fig. 1. Locations of 20 selected gaps and 20 forest controls in Gorazbon division, Mazandaran, Iran.
The analysis process has been based on the general paradigm that large, round patches provide the best opportunity for healthy ecological processes and that remnants that are surrounded by other remnants or connected to larger remnants by corridors, links or stepping stones provide better habitat opportunities than isolated remnants. Landscape context metrics include: patch size, maximum thickness, focal abundance, weighted linear (Ferwerda, 2003). Internal distance to edge (or maximum patch thickness) will be used as a surrogate measure of patch shape. Thickness is half the width of a patch. Focal neighborhood analysis will be used to determine the amount of gap vegetation cover surrounding each cell within a raster landscape. In this case each cell (treed or non-treed) will be assessed for the percentage cover within a series of concentric circular neighborhood. A concentric isolation measure has the advantage that size and distance of potential habitat patches in all directions is assessed and is probably a more realistic description of isolation in relation to actual dispersal processes (Vos and Stumpel, 1995). Weighted distance is a measure of distance from a cell to the nearest patch of a specified size and shape (source patches). The closer or more connected a patch is to one of these patches, the more chance there is of the patch being utilized and colonized by particular species. Landscape Context is the sum of patch (size and maximum thickness) and landscape (focal abundance and weighted linear) rate (Ferwerda, 2003). For the purpose of this study, all of the identified gaps larger than 0.1 ha (n = 35) were converted to grid using cell size 0.5 0.5 m. The grid data set was classified to gap patches valued 1 and forest matrix valued 0. Each landscape context metric was calculated by either the default rating table in the setting of the tool or creating new rating tables that were adjusted to better reflect the real characteristics of the gaps in the study area. Patch size smaller than 0.3 ha in size was rated the value 10 (the minimum rate), whereas patch larger than 0.3 ha was rated 20 as some studies showed, changes in bird abundance began to occur in gaps of 0.3 ha (Moorman and Guynn, 2001). The patch size and thickness ratings were added together resulting in an overall patch rating. Percentage gap vegetation within focal neighbourhoods of 50, 100, 150, 250, 500, 750 and 1000 m were calculated. The resulting
values were then added together to create the overall focal abundance rate. A series of distance analysis from each cell to a patch of a certain size or shape was done by the weighted linear measurement. Distance analysis of each cell to source patches was used (Ferwerda, 2003).
2.5. Statistical analysis Vegetation variables and mean species abundance were compared between gaps and forest controls using non-parametric Mann–Whitney test due to the fact that some of the data were not normal and did not turn into normal using transformation methods. Two-way ANOVA was used to test for differences among site, visit, and site visit interactions on bird abundance and species richness. Effects of visit and site visit were not significant (P > 0.05) therefore mean bird species abundance and the total number of species detected in the two visits was represented as bird abundance and richness in the two visits. Paired t-tests were used to compare mean abundance and total species richness between gaps and controls. These statistical tests were carried out in SPSS 16 (SPSS Inc., 2007). In order to understand the relation between bird abundance, richness and particular bird species abundance in gaps with habitat and landscape variables, we used multivariate linear regression analysis in R 2.8.1 (R Development Core team, 2009). In addition, every species was related to an ecological group (forest generalist, forest specialist and gap specialist) and multivariate linear regression was used to perceive better relationship between mean abundance and total richness of these groups and landscape context rate, gap size and habitat variables as Kurosawa and Askins (2003) suggest that when dealing with the effect of forest area on a bird community, it is essential to analyze separately the distribution of groups of species with different habitat preferences. This may be efficient for forest gaps too. We also used multivariate regression analysis to determine the relation between particular bird species abundance in forest controls and habitat variables. Colinearity between habitat variables was tested using Spearman correlation analysis so that variables with high correlation coefficients (r-values > 0.7) were excluded. Models
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were selected according to the least AIK (Akaike’s Information Criterion). 3. Results 3.1. Bird and habitat variables among gaps and forest controls The abundance of breeding birds was higher in gaps than in controls (t = 3.363, d.f. = 19, P = 0.003). Total species richness was higher in gaps than in controls (t = 2.703, d.f. = 19, P = 0.014) (Fig. 2). Species including Eurasian Nuthatch (Sitta europaea), Coal Tit (Parus ater), Great Tit (Parus major), Common Chaffinch (Fringilla coelebs) and European Goldfinch (Carduelis carduelis) were significantly more abundant in gaps than in controls. Among which, European Goldfinch was the only gap specialist species. Chiffchaff, Scops owl and Eagle owl were only heard in the gaps but they were not significantly more abundant in gaps than forest controls. Song Thrush (Turdus philomelos) was the only species recorded more in controls. The numbers of Eurasian Jay which are nest predators were not significantly different between gaps and controls (Table 1). Herb cover, mean tree DBH, CWD density, CWD volume as well as pit and mound microtopography were higher in gaps than in controls. Tree density, low shrub and canopy cover were lower in gaps than controls (Table 2). 3.2. Bird distribution in relation to habitat and landscape variables Landscape context rate was used as the ultimate landscape value for each patch and entered in multi regression analysis. After applying Spearman correlation analysis, five gap vegetation variables including tree number, mean tree DBH, dead tree number, herb cover and landscape context rate were entered as independent variables in multiple regression analysis of birds abundance, richness and particular bird species abundance in gaps. Mean bird species abundance and total richness in gaps were positively related to mean tree DBH but no relation was found between landscape context rate (e.g. patch size) and the two variables. When mean abundance and total species richness of the different ecological groups (except for gap specialist which included one species) were analyzed, no significant relations between the abundance and richness of each ecological group (forest generalist/specialist) and landscape context rate were found. However, there was a negative relation between forest specialist richness and gap size (Table 3). Also a negative trend between
Fig. 2. Mean (±SE) abundance (P = 0.003) and richness (P = 0.014) of breeding birds in small tree fall gaps and closed canopy forest in Kheyrud Experimental Forest, Mazandaran, Iran.
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forest generalist richness and forest specialist abundance and gap size was shown (Fig. 3). Mean tree DBH was positively related to forest specialist abundance (Table 3). The mean abundance of Great Tit was positively related to landscape context rate (Table 4). European Goldfinch was not related to any of these variables. Also variables, including mean tree DBH, shrub number, tree number >60 cm DBH, dead tree number, litter cover were extracted using spearman correlation analysis and were entered in multiple regression analysis of birds abundance and richness in forest controls. Species that had a significant relationship with forest habitat variables are shown in Appendix A.
4. Discussion 4.1. Role of gaps in providing unique resources The abundance and richness of breeding birds were higher in gaps than in controls. Several other studies indicate higher bird abundance and richness in gaps (Fuller, 2000; Greenberg and Lanham, 2001). It seems that birds are capable of tracking distinct microhabitats of small gaps and utilizing their remarkable resources. Higher bird abundance and richness in gaps than controls seems to be associated with higher coarse woody debris volume and density, greater herb cover as well as pit and mound micro topography. Most habitat characteristics in gaps were in accordance with Greenberg and Lanham (2001) and Doyon et al. (2005). Shrubs were lower in gaps than controls because traditional grazing takes place in the study area so sheep can roam more easily in gaps than forest and remove the lower stratum of vegetation. Also, the gaps that are dominated by herbs are in early successional stages that still do not include shrubs. Birds may be more attracted to gaps due to more food abundance and detectability, nest material, protective cover and accessibility to different habitat types at the same time (Greenberg and Lanham, 2001; Moorman and Guynn, 2001). The pit-and-mound topography created by uprooted trees, lying logs, boulders rapidly covered by a moss litter carpet, brush piles and shrub cover increase the diversity of available insect niches as a main food source for most bird species in the study area. Moreover, in gaps the quantity and diversity of CWD as crucial foraging site are concentrated rather than scattered in the forest (Bouget and Duelli, 2004) hence more easily detectable. The presence of slash may be important to avian habitat selection as it can provide added protective cover to ground nesters (Costello et al., 2000) for instance Winter Wren, Black Bird and Common Chiffchaff or ground foragers like Common Chaffinch and European Goldfinch. Fuller (2000) also found more Winter Wren and Black Birds in small (<50 m minimum dimension) gaps but concluded that Common Chiffchaff selected larger (>90 m minimum dimension) gaps over small ones. This confirms the fact that, Common Chiffchaffs were not significantly more abundant in the studied gaps which were less than 50 m in minimum width. The results indicate that mean DBH may be a deciding factor for predicting bird abundance and species richness in gaps. As trees mature they provide increasingly more suitable substrates for a range of cavity nesters (Blue Tit, Great Tit, Coal Tit, Red breasted Flycatcher, Eurasian Nuthatch and Syrian Woodpecker) and/or bole associated foragers (Eurasian Nuthatch) due to increasing trunk diameter and bark complexity (Holmes et al., 1979). This may be the reason why some forest specialists (Eurasian Nuthatch, Coal Tit) were higher in gaps than in controls. Fuller (2000) also showed that Great Tit and Eurasian Nuthatch were abundant in small natural gaps. We conclude that small natural gaps created in intact forest do not have a negative effect on the abundance of forest specialists; in contrast it will improve some species abundance in breeding season provided that
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Table 1 Abundance (±SE) (mean number of individuals in two visits) of bird species identified in 20 tree fall gaps and 20 closed canopy cover controls in Kheyrud Forest, Mazandaran, Iran. Species
Scientific name
Wood Pigeon Scops Owl Eagle Owl Syrian Woodpecker Green Woodpecker Winter Wren European Robin Common Nightingale Common Blackbird Song Thrush Common Chiffchaff Red-breasted Flycatcher Coal Tit Great Tit Blue Tit Eurasian Nuthatch Common Chaffinch Brambling European Goldfinch Golden Oriole Eurasian Jay a * **
Group a
Columba palumbus Otus scops Bubo bubo Dendrocopos syriacus Picus viridis Troglodytes troglodytes Erithacus rubecula Luscinia luscinia Turdus merula Turdus philomelos Phylloscopus collybita Ficedula parva Pariparus ater Parus major Cyanistes caeruleu Sitta europaea Fringilla coelebs Fringilla montifringilla Carduelis carduelis Oriolus oriolus Garrulus glandarius
G G S G G G G G G G S S S G G S G G GS G S
*
Habitat variable
Control
Gap
P-value
Tree density Mean tree height (m) Mean tree DBH (cm) Shrub height (m) Snag density Snag BA (m2/ha) CWD density CWD volume (m3) % Canopy % Tall shrub % Low shrub % Herb % Tip up mounds % Pits
17.05 17.24 28.01 2 23 1.04 10 0.40 94.04 9.55 5.05 30.40 0.75 0
5.55 16.70 33.48 1.60 12 1.50 22 4.19 13.25 4.7 1.50 78.80 5.5 2.25
0.00** 0.93 0.00** 0.70 0.10 0.51 0.01** 0.00** 0.00** 0.41 0.05* 0.00** 0.04* 0.03*
P < 0.05. P < 0.01.
Table 3 Relationships between habitat and landscape variables and abundance and richness of birds (total/ecological groups) within gaps.
Mean bird abundance Total bird richness Forest specialist abundance Forest specialist richness *
Gap
P-value
0.27 ± 0.07 0.00 ± 0.00 0.00 ± 0.00 0.95 ± 0.13 0.20 ± 0.06 1.37 ± 0.11 1.17 ± 0.11 0.4 ± 0.1 1.60 ± 0.11 1.30 ± 0.125 0.00 ± 0.00 0.22 ± 0.07 1.10 ± 0.10 0.62 ± 0.09 0.85 ± 0.12 0.30 ± 0.07 2.47 ± 0.11 0.22 ± 0.08 0.00 ± 0.00 0.12 ± 0.06 0.17 ± 0.07
0.12 ± 0.05 0.02 ± 0.02 0.02 ± 0.02 1.22 ± 0.15 0.12 ± 0.53 1.67 ± 0.09 0.87 ± 0.10 0.35 ± 0.10 1.82 ± 0.11 0.70 ± 0.11 0.10 ± 0.05 0.40 ± 0.10 1.47 ± 0.13 1.17 ± 0.15 1.22 ± 0.13 0.60 ± 0.11 2.87 ± 0.13 0.07 ± 0.04 0.15 ± 0.05 0.20 ± 0.06 0.22 ± 0.08
n.s n.s n.s n.s n.s n.s n.s n.s n.s 0.00** n.s n.s 0.02* 0.01* n.s 0.05* 0.03* n.s 0.00** n.s n.s
Abbreviations: G, forest generalist; S, forest specialist (BirdLife International, 2010) and GS, gap specialist (interpreted by the study results). P < 0.05. P < 0.01.
Table 2 Mean values of habitat variables for gaps and closed canopy forest (controls) in Kheyrud Forest, Mazandaran, Iran.
**
Control
Model
R2
P
AIC
0.098 (mean tree DBH) + 12.181 0.085 (mean tree DBH) + 9.094 0.056 (mean tree DBH)
0.228
0.033*
84.270
0.308
0.011*
70.687
0.238
0.028
*
61.057
4.863 (gap area) + 3.518
0.233
0.031*
51.433
P < 0.05.
it provides high cover and meets their needs of large trees. As growth of vegetation continues to reduce the abruptness between openings and adjacent forest, gap specialists and some forest interior species may increase their use of gaps as nesting, foraging, or brood rearing habitat (Moorman and Guynn, 2001). These results are in agreement with Fuller (2000) who concluded that there was a considerable overlap in the bird species composition at gaps
and forest controls and Greenberg and Lanham (2001) who deduced that forest interior species were indifferent to small forest gaps that retain a partial canopy. Goldfinch was the only gap specialist found in the studied gaps. Laiolo (2002) also assigned Goldfinch as an edge species and Santos et al. (2002) classified it as a ubiquitous species which can feed and nest on isolated trees or shrubs. Identifying only one gap specialist may be due to the small size of gaps and low shrub cover as Fuller (2000) related few gap specialists in old growth stands of Poland, to larger gaps that had dense understory foliage. A study by Robinson and Robinson (1999) also related the positive effect of gaps on the population of gap dependent species to the dramatic surge in production of shrub and understory plants used for foraging and breeding. There are also some gap species (e.g. Chiffchaff) that benefit from forest management practices and occur in higher densities in managed gaps comparing to natural gaps (Piotrowska and Wesołowski, 1989). Song Thrush was more frequent in forest controls than gaps. A study done by Creegan (2004) also showed that Song Thrushes had an aversion for edge habitat but in fact preferred interior habitat. During the bird survey period, no evidence of Cuckoo as parasite species was observed. The numbers of Eurasian Jay which are nest predators were not significantly different between gaps and controls (Table 1). So edge – associated nest predation and parasitism seem to occur less frequently in the studied gaps hence more species attracted to them. 4.2. Relationship between bird (total/within ecological group) abundance and richness and gap size and landscape context rate The effect of gap size on the abundance and richness of all birds and generalists were not significant. Levey (1988), Fuller (2000) and Bowen et al. (2007) have also concluded no relation between abundance and gap size. However Greenberg and Lanham (2001) and Moorman and Guynn (2001) showed a significant positive relation between gap size and bird abundance in gaps. It seems that larger gaps in our study (0.4 ha) do not provide more favorable habitat than smaller ones. As the results show, bird abundance and richness in gaps were related to mean tree DBH indicating that larger gaps with less mean tree DBH or no trees at all, may lead to less abundance and richness of birds. Forest specialist richness was
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Fig. 3. Relationship between mean abundance and total richness of breeding birds and gap area for ecological groups in Kheyrud forest, Mazandaran, Iran.
Table 4 Relationships between habitat and landscape variables and particular species abundance in gaps.
* **
Species
Model
R2
P
AIC
Eurasian Nuthatch Winter Wren Great Tit European Robin Blue Tit
0.107 (tree number)
0.271
0.018*
29.871
0.026 (mean tree DBH)+0.800 0.090 (landscape context rate) 0.028 (mean tree DBH)
0.267 0.259 0.364
0.019* 0.022* 0.005**
27.309 46.767 21.191
0.229 (dead tree number) + 0.019 (herb)
0.439
0.023*
34.849
P < 0.05. P < 0.01.
negatively related to gap size although some specialist species were higher in smaller gaps. Apparently as gaps became larger (0.2–0.4 ha) species such as Red breasted flycatcher, Chiffchaff and Eurasian jay disappeared. This suggests that larger homogenous gaps did not meet specialist needs for cover and protection as smaller gaps (with higher canopy cover and habitat complexity) did. Consequently, bird species richness in a forest gap is not only related to gap size but also influenced by habitat resources in which result in habitat quality. The natural gaps in our study are
not created at the same time and being so, they reflect different stages of succession and are different according to vegetation structure and complexity. More developed forest stages may benefit forest bird species richness by providing more cavities and a higher amount of dead wood as nesting and feeding substrates (e.g. invertebrates) for many bird species (Camprodon, 2001). The concept of patch as a collective habitat of the species in a guild has great utility as a basis for understanding avian relationships to successional phases (Keller et al., 2003). No study has yet addressed the relationships between breeding bird assemblages and landscape context in gaps of small size as ours. As the results show, the effect of landscape context rate on mean abundance and total richness of total birds and ecological groups was not significant. For many species, it is perhaps not the isolation or size of patches that affects their population sustainability, but the overall area of suitable habitat, which may include matrix and patch habitat (Kupfer et al., 2003). The forest matrix provides a non hostile environment with suitable resources for many forest generalist and specialist species. Many bird species were identified in both gaps and closed canopy forests which shows the similarity between the two communities. It seems that the forest matrix does not impede the movement and occurrence of birds that depend on gaps and edges therefore, the presence of most gap species were not related to landscape variables and distribution of patches.
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4.3. Relationship between Great tit abundance and landscape context rate Great Tit is documented as a forest generalist species which is relatively common in landscapes containing gaps indicating an ability to utilize patchy habitat (Hinsley, 2000). Hunter (1980) deduced that most types of activities by male Great Tit took place in a visually open space as the better view from a perch would facilitate seeing predators and conspecifics. Fuller (2000) showed that Great tits preferred small natural gaps to large ones. Also, a study done by Kacelnik (1979) indicated that light intensity limits foraging efficiency of Great Tits in the early morning. This result implies the importance of light incidence and open space for foraging of the species. Landscape connectivity is a species specific trait (Taylor et al., 2006) thus, Great Tit showed a significant positive relation with landscape context rate. Despite the small size of gaps and high distribution ability of birds, the size and arrangement of patches has shown to be crucial to the abundance and distribution of this species. We suggest that smaller patches with lower landscape context rate may be used as stepping stones for reaching larger patches hence improving landscape connectivity for the species. Moreover, we anticipate that if larger patches had more suitable habitat quality (e.g. large trees, dead wood, shrubs), more species would be related to gap size and hence landscape context rate. In addition the negative effect of gap size on forest specialists would be tempered.
5. Conclusions 5.1. Management and conservation implication Our results highlight the importance of gap quality for total birds and ecological groups. In this light, the first conservation options that should be considered for any habitat patch relate to improving the quality of the existing habitat and the viability of their species’ populations (e.g. maintaining dead tree) (Kettunen et al., 2007). The retention of some canopy trees which provide habitat during forest succession for additional birds associated with mature trees (e.g. Eurasian Nuthatch, Eurasian Jay and Coal Tit) leads to higher species richness. Maintaining large trees with higher bole diameter is fundamental for many particular species (Winter Wren, European Robin) and avian abundance and richness. Grazing should be prohibited in the area to retain the understory needed for gap specialists. This is advocated by the management plan of Gorazbon. A study on the food resources (insects, fruit and seeds) located in gaps and a comparison between their quality and quantity between gaps and controls merits further research. On the other hand, slight management practices could contribute to the presence and abundance of a number of gap specialists. We believe that the conservation value of all the gap remnants were approximately equal and have to be considered for the abundance of gap specialist species (European Goldfinch). The idea of taking out the remaining trees and making the gaps larger to attract gap specialists corresponds to the management plan of the Gorazbon district but research on the habitat requirements of European Goldfinch and other possible gap specialist is essential, prior to any management applications towards them. Cutting plans would need to be designed to create patches of adequate size and shape to meet the requirements of these species (Boutin and Hebert, 2002). The fallen dead wood should remain in the gap to provide a valuable foraging source and increase habitat heterogeneity. This suggests that, Simulation of the local disturbance regime and allowing for the maintenance of physical components of bird habitat is beneficial for bird diversity (Franklin and Armesto, 1996).
Consequently, a combination of both cleared and uncleared treatments may increase species richness in the study area (Bouget and Duelli, 2004). It should be mentioned that these results were concluded for natural gaps in an intact forest. As Robinson and Robinson (1999) and Moorman and Guynn (2001) suggest, landscape context must be considered in assessing the role of gaps (natural or anthropological) and their effect on bird assemblages owing to the fact that the impact differs in a heavily intact forest landscape comparing to a fragmented landscape. Fragmented or heavily managed landscapes (e.g. most of Hyrcanian forests) may have a more detrimental effect (e.g. predation, parasitism, edge effect) and may change bird community. In addition, manmade disturbances cannot replace the role of the natural disturbances in forest ecosystem dynamics. Therefore, integrating natural disturbances into forest management practices (e.g. maintaining or replicating natural disturbances) is critical for securing the movement of disturbance dependent species within landscapes (Kuuluvainen et al., 2004). In conclusion, if maintaining total bird richness is a management goal, a combination of both cleared treatment that is taking out some residual canopy trees according to gap specialist requirements and uncleared treatments which is preserving small gaps containing a partial cover, would be beneficial for all the ecological groups namely generalist, forest specialist and gap specialist species. Acknowledgements This study was funded by the research affairs of University of Tehran. We thank Fattola Ghomi for his valued assistance in the field. We are grateful to Vahid Etemad for his devoted help in providing facilities and useful advice. We also thank Manouchehr Namiranian, the head of Kheyrud experimental forest for providing the facilities needed for this study. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.foreco.2011.12.001. References Akhani, H., Djamali, M., Ghorbanalizadeh, A., Ramezani, E., 2010. Plant biodiversity and endemism of Hyrcanian relict forests, N. Iran: A floristic, palaeoecologic and conservation overview. Pak J. Bot. Special Issue 42, 231–258. Bibby, C.J., Burgess, N.D., Hill, D.A., Mustoe, S., 1992. Bird Census Techniques. Academic Press, London. BirdLife International. 2010. The BirdLife checklist of the birds of the world, with conservation status and taxonomic sources. Version 3. Viewed 28 May 2011,
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