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Habitat fragmentation due to the conversion of natural habitats into agricultural, industrial or urbanized land has received much attention from conservation biologists (Saunders, Hobbs & Margules 1991; Haila, Saunders & Hobbs 1993; Fahrig & Merriam 1994; Murcia 1995; White et al. 1997). These studies have extended the view of habitat area loss per se to postulate that two more components might be important: (i) reductions in average habitat patch size and (ii) the increase in patch isolation, which turns habitat patches into islands (Andren 1994). Studies of habitat fragmentation generally emphasize the response of biological populations to changes in patch size, shape or configuration at various scales (Picket & Cadenasso 1995; Wiens 1995). In fragmented landscapes, reduction in patch size and increasing isolation enhance the negative effect of the reduction in total habitat area on population size (Andren 1994). Habitat fragmentation often reduces connectivity, which breaks continuous populations into metapopulations (Hanski & Gilpin 1991) or source–sink populations (Pulliam 1988). It may also increase negative edge effects from stochastic processes (reviewed by Simberloff 1994) or from predators or parasites that enter small patches from the core environment (Ambuel & Temple 1983; Wilcove 1985; Blake & Karr 1987; Robinson et al. 1995). The extirpation of a particular species from isolated fragments may be followed by recolonization by individuals of the same or different species according to the concept of dynamic equilibrium (MacArthur & Wilson 1967). Whether a species is re-established and remains in sink populations (Pulliam 1988), or fails to recolonize a patch, may, in turn, influence species diversity.
A major process that both alters and fragments natural habitats is the creation of pine plantations. Exotic pine forests have become increasingly popular in afforestation programmes in mediterranean zones world-wide (Gordo & Gil 1990; Cal 1994; Barbero 1995). For example, pines have been planted in Spain in large areas where oak woodlands were initially cleared to create arable land (Gordo & Gil 1990; Diaz et al. 1998). Studies on bird communities suggested that the reforestation of these former arable lands with pines might not increase forest bird species diversity because suitable microhabitats for specialists are absent, especially in the understorey (Lopez & Moro 1997; Diaz et al. 1998).
In the Northern Negev, Israel, thousands of hectares of scrubland have been afforested with exotic conifers (mostly Pinus halepensis Mill, Pinus pinea L., Pinus canariensis Smith and Cupressus sempervirens L.) since 1956. The mediterranean and semi-arid scrubs of Israel are characterized by low and thick perennials that are unique habitat for specialists such as the long-billed pipit Anthus similis (Shirihai 1995). While many studies on birds in fragmented habitats have involved natural forests fragmented by commercial clear-cutting (Ambuel & Temple 1983; Blake & Karr 1987; Moller 1987; Lynch & Saunders 1991; Robinson et al. 1995; Telleria & Santos 1997), the Negev provides an opportunity to assess effects where forest is the new habitat fragmenting open habitats. Over the past four decades, these forest islands have grown both in size and age, while the once continuous scrub area has become a patchy habitat. These changes in landscape structure have been followed by dramatic changes in the local bird community composition. One conspicuous phenomenon was the immigration of several mediterranean bird species from northern and central Israel to the Negev and their establishment in the plantations (Shirihai 1996).
We investigated whether bird abundance and distribution correlated with area or habitat structure in planted forest and scrubland patches in the Northern Negev. We assumed that two different processes shape bird assemblages in each habitat. In the fragmented scrub we assumed that the reduction in patch size leads to extinction of specialist species, whereas in the planted forests the observed bird assemblage would be the product of colonization. Because the spatial scale in our study was relatively small, we did not consider distance from source populations as an important factor affecting forest bird species diversity. Five of the species studied were long-distance migrants, and the spatial scale of our study is negligible compared with the distance to their wintering grounds. Rather, we assumed that bird species colonize forest patches according to the presence of their preferred habitat subtypes (in terms of tree types or age). We hypothesized that assemblages in both habitats are non-random sets of a regional species pool, and are not the result of an increase in species richness due to increasing area and sample size (Connor & McCoy 1979; Haila 1983) but rather are affected by habitat structure or edge effects (hereafter biological effects). We predicted that (i) in each habitat there will be an increase in both species richness and species diversity with an increase in patch size; (ii) in the fragmented scrub, where specialist species exist, area will be a major correlate with species diversity and population density; and (iii) in the forest, habitat structure will be the primary correlate with species diversity and population density, whereas area would be of minor importance.
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- Study area and methods
The theory of island biogeography (MacArthur & Wilson 1967) initially favoured area over habitat diversity as the primary factor affecting species diversity. Subsequently, however, the relative importance of these two factors has been extensively debated, but their resolution is difficult because the two are often highly correlated (Rosenzweig 1995). Other problems in macroecological studies emerge from dealing with uncontrolled variables that hardly provide evidence for processes or mechanisms involved (Manel, Buckton & Ormerod 2000). To overcome these problems we (i) used multivariate statistical techniques that control for autocorrelations; and (ii) determined whether several complementary hypotheses concurred with one another.
We found that bird distribution in the Northern Negev is not random: ordination analysis separated the whole-landscape bird community into two assemblages representing scrubland and forest (Fig. 2). Area was a good estimator of species richness in both habitats (Figs 2b, 3a), and species diversity increased with area, indicating that species accumulation was faster than expected from random sampling (Fisher, Corbet & Williams 1943; Connor & McCoy 1979; Rosenzweig 1995). In other words, species in both habitats appear to respond to biological factors. The question is whether these factors are associated with area (e.g. edge effects) or with habitat structure (e.g. vegetation profile).
The third-order polynomial pattern of forest species diversity vs. area (Fig. 3a) concurs with forest habitat structure, where patches can be classified into three spatial scale classes. The first class includes small homogeneous patches (5–10 ha). Here, patches consisted of one coniferous plot, planted during one year. These patches are occupied by habitat generalist species only (species that breed in various habitats throughout the Northern Negev), such as olivaceous warbler, greenfinch, goldfinch and other, non-passerine, species (collared dove and turtle dove). At this scale Fisher's alpha decreases, indicating a random sampling. At the second class, 15–1500 ha, patches become heterogeneous. Patches larger than 15 ha include several plantations of either different aged conifers or mixed coniferous and deciduous trees. The addition of new habitat subtypes was succeeded by a substantial increase in species diversity. This increase continued as long as more habitat subtypes were added. The third class included patches larger than 1500 ha. Here, no new habitat subtypes were included, and the few new species were added, again, due to a random sampling process. The idea that habitat diversity is the main factor influencing forest bird species diversity is strongly supported by the direct correlation between these two variables. When Fisher's alpha is plotted vs. BA (Fig. 4a), a linear correlation is sufficient to explain species diversity. This suggests that forest patches in the Negev ‘sample’ bird species according to their habitat composition, as described for true archipelagos in a much larger scale (Haila, Jarvinen & Kuusela 1983).
Other results indicated that habitat structure is the main determinant of forest bird species abundance and distribution. First, area per se did not affect forest species densities (Table 3). In contrast, forest stand age, an estimator of habitat diversity, had a significant effect on overall bird densities in all 3 years (Table 3). Secondly, multivariate habitat models further supported the idea of the importance of forest habitat structure upon area. Area was significantly and positively correlated with the overall population densities of new immigrants (Table 4), but only after accounting for habitat structure. This result tentatively suggests that, as in other case studies (reviewed by Rosenzweig 1995), forest bird diversity in the Negev is influenced by habitat diversity that, in turn, increases with area (BA CV was positively correlated with patch size, Spearman correlation coefficient = 0·78, P = 0·001). We believe that the presence of a suitable habitat subtype per se determines whether breeding birds become established in the planted forests. New immigrants (e.g. Eurasian jay, great tit, spotted flycatcher and blackbird) were more abundant in larger patches, simply because old stands are more common in these patches. We found no indication that this was due to negative edge effects. While different geographical or habitat structure variables frequently entered multivariate habitat models, area was included in relatively few cases (Table 5). In bird populations a decrease in density as patch size decreases may indicate edge effects. However, in our study such a positive correlation between patch size and density exists for Eurasian jay only.
A species-level nested-subset analysis suggested that three forest-dwelling species diverged from nestedness because they were associated with a unique habitat subtype rather than with patch size. Yellow-vented bulbuls breed only in broadleaf trees, and woodchat shrikes rarely breed in pines. These two species were found in small patches with broadleaf groves, but not in larger ones that consisted of mainly coniferous forest. Desert finch distribution had, as far as we can tell, a nested pattern. Yet even here the distribution was probably not random, but a result of habitat preference. Desert finches breed almost exclusively in young pines in small patches. Moreover, as the only forest species that is not originally a mediterranean species (Shirihai 1996), it was restricted to the southern part of the study area (as indicated by its multivariate habitat model; Table 5).
In contrast to the forest species, the abundance and distribution of scrubland birds appeared to be affected by area. This result agrees with findings from other studies where habitat patchiness was the result of fragmentation (Ambuel & Temple 1983; Blake & Karr 1987). The increase of diversity with scrubland area (Fig. 3b) suggests that biological factors are responsible for the observed species–area relationship. The effect of area on the density of scrub specialists (Table 3) suggests that disturbances reduce population density in small scrub patches. Furthermore, area was the only variable that entered the multivariate habitat model of scrub specialist species (Table 4), indicating that it is the most important factor affecting their abundance.
Implications for conservation and management
Habitat fragmentation is generally viewed as a unidirectional process that breaks continuous natural habitat into small and isolated patches (Ambuel & Temple 1983; Wilcove 1985; Blake & Karr 1987; Robinson et al. 1995). However, habitat fragmentation also involves a reverse process in which islands of the new habitat grow to form a continuous habitat. In cases where the new habitat is not completely hostile to the focal organisms, the landscape can be viewed as an undivided mosaic (sensuAddicott et al. 1994) where fitness differs in different patch types but is always greater than zero.
Studies using the mosaic approach (Enoksson, Angelstam & Larsson 1995; McGarigal & McComb 1995; Estades & Temple 1999) suggest that the effect of landscape on bird abundance is species specific. Enoksson, Angelstam & Larsson (1995) in Sweden, and Estades & Temple (1999) in Chile, studied bird communities in landscapes where natural forests have been fragmented by exotic pine plantations. Their results suggest that such landscapes are settled by several bird species as undivided landscapes. The mosaic approach may seem highly relevant to the Negev afforestation programme. On one hand, pines were planted within a scrubland habitat, creating a divided landscape for most scrubland species. Ecologically, this process is similar to forest fragmentation by farmlands. On the other hand, the new human-made habitat in the Negev is relatively diverse in vegetation structure, and is inhabited by more bird species than the scrub it is replacing.
Altogether, afforestation in the Negev increased bird species diversity in the whole landscape. However, the new immigrant mediterranean species are originally habitat generalists that appear to have become habitat specialists in the Negev. These species extended their distribution at the expense of scrub specialists. Thus, conservation efforts should be aimed at scrub species, not at the forest species. Any further decrease in scrub area will reduce scrub species densities, such as long-billed pipit and spectacled warbler, as shown in Tables 2, 3 and 4. These species are sensitive not only to habitat loss, but to any subtle change in their habitat structure where scrublands are prepared for planting. To conserve populations of these threatened species, further scrub fragmentation must be minimized.
In order to increase species diversity in the Northern Negev, the best approach is not to increase forest area, because there was only a slight increase in species richness between 200-ha and 3000-ha forests, but to increase forest habitat diversity. This can be done at two different levels: the habitat subtype level (forest subunit composition) and the microhabitat level (foliage layers).
At the habitat subtype level species diversity may be increased by increasing the proportion of broadleaf trees. Studies in Wales (Bibby, Phillips & Seddon 1985; Bibby, Aston & Bellamy 1989) and Arizona (Rosenstock 1998) showed that mixed oak–conifer stands support higher bird species diversity than exclusive conifer plantations. Easton & Martin (1998) showed that the reduction in deciduous vegetation due to herbicide treatment in managed conifer forests in British Columbia reduced bird species richness and abundance. In the Negev, deciduous forest species attempt to breed in broadleaf plantations, but the total area and average size of broadleaf stands are too small (Shochat 1999). Increasing broadleaf plantation area may increase the abundance of scarce or sporadic breeding species in the forest. Another important habitat variable was coniferous stand age; forest species composition changes as pine trees mature. Continuous replacement of old-growth plantations with young ones would help to maintain a large variety of subunits of different ages with their unique foliage structure.
At the microhabitat level, foliage profile enrichment is required. The forest bird community in pine plantations in the Negev is much poorer than the mediterranean broadleaf woodland bird community in central and northern Israel. The reason may be that the structure of the plantations is comparatively simple and lacks one essential vegetation layer for forest specialists: the understorey. Bibby, Aston & Bellamy (1989) demonstrated how the presence of understorey in old-growth spruce plantations in Wales increased species richness. Because understorey is almost absent in the Negev, it is hard to evaluate its importance to bush-nesting species. Yet, the low density of several understorey-breeding species, and the absence of others, suggests that future management strategy should involve the creation of understorey as the most important step. This may increase densities of Sardinian warbler and rufous bush-robin. It may also facilitate the establishment of species that have started to spread southwards in Israel in recent years (Shochat 1999).
A global perspective
Exotic conifers are now central in afforestation programmes across countries with mediterranean climates, such as Spain, Italy, Australia, South Africa and Chile (reviewed by Izhaki 1999). Cody (1975) showed how planted pine forests in Chile are as rich in bird species as native pine forests in California, whereas similar forests in South Africa are ornithological deserts. He gave two explanations for these findings. First, African bird species are mostly specialists, whereas in Chile there are many more generalists. Secondly, natural bushes and shrubs in Chile, unlike in South Africa, invade pine plantations and form an understorey level. Disney & Stokes (1976) showed that both bird species diversity and density were higher in sclerophyl forests (especially wet ones) than in planted pine forests in Australia. In Spain, Lopez & Moro (1997) showed the importance of the understorey in Aleppo pine forests in south-eastern Spain for several bird species. Diaz et al. (1998) claimed that artificial pine forests, planted on former arable lands in Spain, were too small, and that increasing forest area would not increase species richness of the forest bird community because these forests do not provide high quality habitats. They drew conclusions similar to ours, even though their study was done on a much larger spatial scale, in a more productive area, with a richer and more complex bird community. Our results therefore support the idea that pine forests in mediterranean zones are generally too simplistic in structure to maintain rich bird communities. Because mediterranean bird species co-evolved with low and thick vegetation, managed pine forests appear to be a challenge for new colonizers from native woodlands. Therefore, the management strategies we suggest may be useful across a much larger spatial scale then the Negev, and may serve as the future challenge in modern afforestation programmes.