Does forest fragmentation affect the same way all growth-forms?

1 Does forest fragmentation affect the same way all growth-forms? Gloria RODRÍGUEZ-LOINAZ1*, Ibone AMEZAGA1,2, Miren ONAINDIA1,3. 1Department of Plant Biology and Ecology. University of the Basque Country, P.O. Box 644. 48080 Bilbao, Spain; 2 E-mail: [email protected]; 3 E-mail: [email protected]; * Corresponding author; Fax: 34-94-6013500; Phone: 34 94 601 2559; E-mail: [email protected]s This document is the Accepted Manuscript version of a Published Work that appeared in final form in Journal of Environmental Management 94 :125-131 (2012). https://doi.org/10.1016/j.jenvman.2011.06.024 © 2012. This manuscript version is made available under the CC-BY-NC-ND 4.0 license https://creativecommons.org/licenses/by-nc-nd/4.0/ 2 Does forest fragmentation affect the same way all growth-forms? 1 2 Fragmentation of natural habitats is one of the main causes of the loss of 3 biodiversity. However, not all plant species show a uniform response to habitat 4 fragmentation due to differences in species traits. We studied the effect of patch size 5 and isolation on the biodiversity of vegetation in the mixed-oak forests in the north of 6 the Iberian Peninsula. The aim was to evaluate whether all the growth-forms of 7 vegetation are equally affected by forest fragmentation in order to improve the 8 management strategies to restore this type of vegetation. 9 This study has shown that the effect of the area and spatial isolation of the 10 patches was not the same for the different growth-forms. Fragmentation had a mainly 11 negative effect on the richness and diversity of forest specialist species, especially ferns 12 and herbaceous growth-forms. Moreover, the presence and/or cover of woodland 13 herbaceous species (such as Lamiastrum galeobdolon and Helleborus viridis) and of 14 woodland ferns (namely Asplenium adiantum-nigrum, Asplenium trichomanes, 15 Polystichum setiferum, Dryopteris affinis) were negatively affected by patch size, 16 possibly due to the reduction of habitat quality. This species have been replaced by 17 more generalist species (such as Cardamine pratensis, Cirsium sp., Pulmonaria 18 longifolia or Rumex acetosella) in small patches. Patch isolation had a negative effect 19 on the presence of forest specialist species (namely, L. galeobdolon, Frangula alnus, 20 Hypericum androsaemum, A. adiantum-nigrum and Athyrium filix-femina) and favored 21 the colonization of more generalist species such as Cirsium sp., Calluna vulgaris, Erica 22 arborea or Ulex sp. Hence, in this region a special attention should be given for the 23 conservation of forest specialist species, especially ferns and herbs. In a conservation 24 3 policy focused on this forest specialist species, which are the most valuable species in 25 forested ecosystems, large forests should be promoted. 26 27 Keywords: Patch size / degree of isolation / species trails / forest specialist species 28 4 1. Introduction 29 The excessive destruction and fragmentation of natural and semi-natural habitats 30 on the Earth’s surface is recognized as one of the principal causes of the loss of wild 31 biodiversity (D’eon and Glenn, 2005; Fischer and Lindenmayer, 2007; Haines-Young, 32 2009; Harrison and Bruna, 1999; Hobbs, 2000; Meffe and Carroll, 1997; Wilcox and 33 Murphy, 1985; Wood et al., 2000). The effects of habitat fragmentation on biodiversity 34 have been studied for several decades, resulting in a vast literature on this topic, and, 35 despite continued debate about the relative importance of habitat fragmentation and 36 habitat loss (Fahrig, 2003; Hanski & Gaggiotti, 2004), it is mostly clear that the size and 37 spatial distribution of habitat remnants alters the patterns of species distribution and 38 abundance within a landscape (Ewers and Didham, 2006). 39 The processes of reduction, spatial division and increased isolation of habitats 40 caused by fragmentation are associated with a reduction in the abundance, distribution 41 and viability of species closely linked to these habitats (Bender et al., 2005; Fahrig and 42 Merriam, 1994; Kleyer et al., 1996; Kupfer et al., 2006). However, not all plant species 43 show a uniform response to habitat fragmentation. For instance, a number of studies 44 have shown that the nature of the species-area relationship describing species loss from 45 habitat fragments is confounded by differences in species traits (Cagnolo et al., 2006; 46 Ewers and Didham, 2006; Godefroid and Koedan, 2003; Kolb and Diekmann, 2005). 47 Some studies show that habitat fragmentation affected plants with specific dispersal 48 modes (Kolb and Diekmann, 2005; Tabarelli et al., 1999), low frequency of occurrence 49 and high habitat specificity (Hill and Curran, 2001; Iida and Nakashizuka, 1995). Plant 50 species with different growth-forms (woody vs. herbaceous; short-lived vs. long-lived) 51 can present different responses to fragmentation. Woody plants grow more slowly and 52 devote the larger part of their photosynthesis to the production of structural materials for 53 5 long-term survival (Chapin, 1991). Meanwhile, the herbaceous plants grow and die 54 more rapidly and devote the larger part of their photosynthesis to reproduction and rapid 55 turn over. These characteristics can make the species respond differently to 56 fragmentation and, if they are affected, have different response times (Ewers and 57 Didham, 2006). In fact, it has been postulated that short-lived species like herbs should 58 be more sensitive to edge effects which would favour colonisation by ruderal species 59 (Cagnolo et al., 2006). Influence from surrounding vegetation may actually increase the 60 total species richness of fragmented woodlots, but reduce the fraction of habitat 61 specialists (Harrison, 1999).Thus, an assessment of the effect of fragmentation on plant 62 communities should be based not only on species richness but also on species type, 63 which can be defined in terms of conservation value or ecological traits (Honnay et al., 64 1999a; Hill and Curran, 2001). 65 In the north of the Iberian Peninsula the potential vegetation is mixed-oak 66 forests, dominated by Quercus robur L. with Fraxinus excelsior L. and Castanea sativa 67 Miller (Onaindia et al., 2004). However, since the beginning of the 20th century most of 68 the potential area has been reforested by fast growing exotic species, namely Pinus 69 radiata and Eucalyptus globulus, that have mainly affected forest specialist species 70 (Amezaga and Onaindia, 1997). The aim of this research was to test whether the spatial 71 configuration of those forests, namely size, form and degree of isolation of the patches, 72 affects in the same way the vegetation as a whole or varies for different growth-forms 73 (herbaceous, ferns, climbers, shrubs and trees) and forest specialist species (Aseginolaza 74 et al., 1988). 75 76 6 2. Methods 77 2.1. Study Area 78 This study was carried out in the Urdaibai Biosphere Reserve (UBR) (area 220 79 km2) located in the north of the Iberian Peninsula (43º19´N, 02º40´W) (Figure 1). The 80 UBR is one of the most important natural areas of the Basque Country (Northern Spain) 81 due to, among other features, its unique and diverse landscape which includes a craggy 82 countryside occupied by meadow land, oak groves, deciduous woods and, especially, 83 pine plantations. 84 The potential vegetation of the 80% of the UBR is mixed-oak forests, dominated 85 by Quercus robur L. with Fraxinus excelsior L. and Castanea sativa Miller (Onaindia 86 et al., 2004). Throughout the 20th century, these native mixed-oak forests were heavily 87 fragmented and, as a result, today they cover only about 6% of the total area of the 88 Urdaibai Reserve (Rodríguez-Loinaz et al., 2011) as has happened with other natural 89 forests in other parts of the word (Schessl et al., 2008). Afterwards, the traditional use of 90 timber and coal production was abandoned and the remaining forest patches started a 91 process of regeneration (Michel, 2006). 92 93 2.2. Patch selection and vegetation sampling 94 A total of 33 patches of mixed-oak forest situated in the UBR were selected by 95 means of the land use map at a 1:10 000 scale (Figure 2). The selection was made as a 96 function of size, since a principal objective was to establish if the diversity of the 97 vascular plant species was affected by the size of the patch. Therefore, 18 patches of a 98 size between two and three hectares and 15 patches of a size between ten and thirty 99 hectares were selected. There was no difference on altitude, slope, soil type or 100 geographical location between small and large patches (small patches: mean altitude: 101 7 133±18.89 m, slope: 25±2.10 %, pH: 4.65±0.10, UTM_X: 525762±687, UTM_Y: 102 4.7984 106±1534 and large: mean altitude: 174±17.36 m, slope: 30±2.61 %, pH: 103 4.76±0.11, UTM_X: 526363±962, UTM_Y: 4.7965 106±1693). This selection was 104 determined after analysis of the distribution of patch sizes given that these were the only 105 sizes that occurred in significant numbers. The following indices were determined for 106 each patch: area, distance to the nearest patch of mixed-oak forests (edge to edge) 107 (NND, measure of the degree of isolation) and the fractal dimension (FD, measure of 108 the form) (Mc Garigal et al., 2002), for which the v-LATE software was used (Lang and 109 Tiede, 2003). 110 Since sampling effort and number of species recorded are usually related 111 (Magurran, 1988; Hill et al., 1994; Lomolino, 2001), the area sampled was kept 112 constant in all sites in order to avoid sampling artefacts on the effects of habitat 113 fragmentation (Hill et al., 1994). In each of the patches (large and small) one plot of 114 25m x 25m was determined approximately in the centre of each patch in order to 115 minimise possible edge effects. Within each plot, five sub-plots of 2x1m were 116 delineated. One was in the centre and the other four separated by 12m, making a cross 117 with an arm running with the slope and the other perpendicular to it. The number of 118 sub-plots was determined according to the method of the species/area curve (Kent and 119 Coker, 1992). In these sub-plots the pattern of vegetation during June and July 2005 120 was studied. In each sub-plot, plant species were identified and the percentage cover for 121 each plant species, calculated through visual estimation, was determined. In order to 122 determine percentage cover, five different strata (levels) were considered, i.e. 0-0.20, 123 0.20-1, 1-3, 3-7, >7 m, following Brower and Zar (1977) and Onaindia et al. (2004). 124 Thus, the first stratum corresponded to herbaceous plants, the second to lower shrub-125 like plants, the third to higher shrub-like plants, the forth to the lower tree canopy and, 126 8 finally, the fifth to the higher tree canopy. The total percentage cover for each plant 127 species was obtained by adding up its percentage cover in each of the five different 128 strata. In addition, the cover of trees as an indirect measure of quantity of light was 129 measured, as light condition is one of the main factors in forest habitats (Sarlöv-Herlin 130 and Fry, 2000) and it is known to affect vegetation (Amezaga et al., 2006; Borchsenius 131 et al., 2004). 132 Summing the cover in the five sub-plots, the total cover of each species in the 133 sampled area was obtained. Using these data the indices of richness (S) and Shannon 134 (H´) and Simpson (1-D) diversity were calculated. These indices were obtained for the 135 overall vegetation, the different growth-forms present (herbaceous, ferns, climbers, 136 shrubs and trees), the overall forest specialist species and finally for the different 137 growth-forms within the forest specialist species. To classify a species as forest 138 specialist the “Illustrated keys of the flora of the Basque Country and bordering 139 territories” (Aseginolaza et al., 1988) was used. In this book the natural habitat for every 140 species is described. All those species whose natural habitat was described as nemoral 141 forest, beech forest, oak forest or humid and shaded sites in forest, were classified as 142 forest specialist species. 143 Besides, the overall vegetation similarity in relation to patch size and distance to 144 the nearest missed-oak forest patch was calculated using the Sorensen´s community 145 similarity index. As the distance to the nearest patch was a continuous variable, the 146 comparison was performed among the five patches with the smallest (<50 m) NND and 147 the five patches with the largest (> 200 m) NND. 148 149 9 2.3. Statistical analysis 150 As patch indices (patch size, patch isolation, fractal dimension) were not 151 correlated (Spearman rank correlation, P>0.05), a General Linear Model (GLM) was 152 performed to analyze the effects of fragmentation on the richness and diversity of the 153 vegetation. In this model the size (large or small) was introduced as a factor and the 154 fractal dimension (FD), degree of isolation (NND) and cover of trees were introduced as 155 co-variants. 156 Having analyzed the effects of fragmentation on richness and diversity, the 157 effect of size and isolation (distance to the nearest patch of mixed-oak forest) on overall 158 species composition was tested by means of the semi-parametric permutational 159 multivariate analyses of variance (hereafter PERMANOVA) developed by Anderson 160 (2001). Indicator Species Analysis (ISA; Dufrene and Legendre, 1997) was used to 161 determine the characteristic species within patch size. Only species with P<0.05 were 162 considered (assessed using Monte Carlo randomizations with 999 permutations and 163 INDVAL> 25). 164 165 3. Results 166 3.1. Vegetation structure 167 A total of 110 plant species of which 53 (27 forest specialist) were herbaceous, 5 168 (4 forest specialist) climbers, 18 (6 forest specialist) trees, 23 (7 forest specialist) shrubs 169 and 11 (7 forest specialist) ferns were found in this study (Table 1). Of these 110 170 species, 84 were found in the large patches and 90 in the small ones. 171 The vegetation similarity results showed that 78% of the species were the same 172 for the large and small patches and 50% for the patches with the smallest and largest 173 NND. Those species only present in the large patches were usually (80 %) forest 174 16 6. Acknowledgments 316 We gratefully acknowledge financial support from the Spanish Ministry of 317 Education and Science (CGL2005-08046-C03 01 and CGL2008-05579-C02-01), the 318 Department of Universities, Research and Education of the Basque Government 319 (Groups bursar), UNESCO Chair of the University of the Basque Country and Basque 320 Government (Industry Department-Etortek Project). We would also like to thank Sir 321 Marrack Goulding for his contribution to the editing of this document.322 17 7. References 323 The effect of evergreen and deciduous coniferous plantations on the field layer and seed 324 bank of native woodlands. Ecography 20, 308-318. 325 Amezaga, I., Albizu, I., Gonzalez, A., Mendarte, S., Onaindia M., 2006. In: Areces R. 326 (Eds), Diversidad biológica y biodiversidad, Madrid, pp. 109-114. 327 Anderson, M.J., 2001. A new method for non-parametric multivariate analysis of 328 variance. 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