Chapter Three - Quantifying the Biodiversity Value of Repeatedly Logged Rainforests: Gradient and Comparative Approaches from Borneo

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Abstract

There is substantial variation in the reported effects of logging on tropical forest fauna. In addition to inherent variation in disturbance sensitivity among taxa, another contributing factor is that most studies use comparative analyses of unlogged versus logged forests, which cannot fully account for heterogeneity in disturbance as well as underlying environmental gradients. To better understand how logging affects biodiversity, we examined changes in bat assemblages across a disturbance gradient ranging from old growth to forest logged several times. In one of the first evaluations of repeatedly logged forest, we use both comparative and gradient analyses to reveal substantial signals in assemblage change in response to habitat alteration. Despite multiple rounds of extraction in the most degraded forest, neither approach revealed a definitive effect of logging on site-based richness. However, each approach generated insight into assemblage compositional responses to forest degradation. Structural differences were evident between old-growth and repeatedly logged forest, and depauperate assemblages characterised degraded sites with low, open canopy. Ordinations identified species that best contributed to the signal of assemblage change, and also key associated forest-structure variables. Models of trap-based abundance confirmed not only the importance of forest height in determining assemblage change but also the role of tree-cavity availability in supporting forest specialists, indicating that efforts to supplement this resource could aid restoration. While highlighting the ecological importance of unlogged stands, we show that heavily degraded forests—even those that have been repeatedly logged—still hold some potential value for tropical biota and could have a role in conservation.

Introduction

Unprecedented levels of deforestation and forest degradation have led to major concerns regarding the fate of tropical biodiversity (Bradshaw et al., 2008, Frumhoff, 1995, Gardner et al., 2009). Throughout the tropics, forests continue to be commercially logged, resulting in considerable ecosystem degradation and fragmentation, to the point that logged-over and degraded habitats now comprise more than 50% of the tropical forest estate (Blaser et al., 2011). Nowhere is this crisis more acute than in Southeast Asia, a region where rates of forest loss and exports of tropical timber are among the world’s highest (Asner et al., 2009, Cleary et al., 2007). Large densities of profitable timber species in this region serve as an incentive for logging operations to harvest multiple times, resulting in potentially high levels of disturbance (Whitmore, 1998). The resulting logged forests are often severely depleted of timber, making them vulnerable targets for conversion to other land uses (Edwards et al., 2011, Fitzherbert et al., 2008). This can have considerable implications for conservation and biodiversity management, not least of which is the loss of potential biological corridors and buffer zones around forest reserves (Chazdon et al., 2009). Nevertheless, although there have been numerous logging-impact studies, only recently have researchers begun to evaluate the biological value of forests logged multiple times (Edwards et al., 2011, Woodcock et al., 2011).

The rapidly expanding coverage of degraded forests across the tropics, and the concomitant scarcity of unlogged habitats, in a large part explain why ecologists have changed their views of this modified resource. By presenting an optimistic future for tropical biodiversity, Wright and Muller-Landau (2006) ignited a fierce debate regarding the ecological value of secondary forests (Laurance, 2007). A central part of Wright and Muller-Landau’s argument was the equal value of these regenerating forests and those that are undisturbed (i.e. old growth, sensu Putz and Redford, 2010) for tropical taxa. Counter-arguments caution against this conclusion, given insufficient knowledge of the ways by which biological communities respond to forest disturbance (Gardner et al., 2007). In addition, numerous tropical species are thought to already be committed to extinction following population declines in degraded and fragmented habitat (Brook et al., 2006). While much of this debate focused on the ecological value of secondary forests regenerating from clearance, most arguments are also applicable to forests heavily degraded by commercial logging. Undisturbed old-growth forests are clearly valuable for tropical species (Gibson et al., 2011), but the conservation value of heavily logged and regenerating forests has been called into question (Didham, 2011, Edwards et al., 2011). Nevertheless, despite some discord, there is a growing recognition among ecologists and conservation planners that the future of tropical biodiversity will depend, to a large degree, on how we manage this modified resource (Chazdon et al., 2009, Clark et al., 2009, Gardner et al., 2009).

Over recent years, it has become progressively clear that large tracts of disturbed forest are more valuable to biodiversity than alternative land uses. In the Brazilian Amazon, for example, secondary forests regenerating after burning are more similar in community composition to primary undisturbed forests than they are to Eucalyptus plantations for the majority of taxa (Barlow et al., 2007). Across the tropics, logged forests also support higher numbers of forest specialists than plantations such as rubber (Hevea brasiliensis) or oil palm (Elaeis guineensis) (Fitzherbert et al., 2008, Gibson et al., 2011). In recognition of this, there are mounting pressures on forest managers to minimise the ecological impacts of logging activities and the inclusion in timber certification schemes of criteria aimed to enhance biodiversity is testament to this (e.g. Forest Stewardship Council; www.fsc.org). Biodiversity safeguards may also feature in payments for ecosystem services programmes. For example, the United Nations mechanism for reducing emissions from deforestation and degradation in developing countries (REDD +; www.un-redd.org) now includes provisions for biodiversity conservation as a co-benefit of protecting forests for carbon stocks, and collating data from ground-based biological inventories is proposed as one way of monitoring implementation (Gardner et al., 2012). Substantive evaluations of biological communities in disturbed forests have thus attracted renewed commercial and scientific interest, with the aim of using sound ecological science to inform tropical forest management and the design of managed landscapes (Clark et al., 2009, Gibson et al., 2011, Meijaard and Sheil, 2008).

Tropical biota are thought to be highly sensitive to disturbance (Stork et al., 2009), particularly in Southeast Asia (Brook et al., 2006, Sodhi et al., 2009). Collateral damage associated with logging operations, including felling of non-harvested trees and road construction, can result in significant alterations to forest structure, including up to 80% loss in canopy cover (Fimbel et al., 2001), and a reduction of canopy height that can take substantial time to recover (Okuda et al., 2003). These changes can have considerable implications for forest fauna. For example, Wells et al. (2007) found logging to have profound effects on the prevalence of rare, small-mammal species in Borneo rainforests, a finding they attributed to reduced canopy space and altered tree composition in disturbed forest stands. Population declines of terrestrial birds in logged forests have been attributed to a reduction in leaf-litter microfauna, foraging sites and tree cavities for nesting (Cockle et al., 2010, Johns, 1989, Lambert and Collar, 2002, Lammertink, 2004), while butterfly abundance is thought to be limited by the availability of larval host trees post logging (Cleary et al., 2009).

Nevertheless, there remains huge variation in the reported impacts of tropical forest disturbance (Chazdon et al., 2009, Foody and Cutler, 2003), which makes any synthesis of habitat value difficult and somewhat controversial (Didham, 2011). Selectively logged forest in Uganda, for example, is reported to host a more abundant and diverse small-mammal assemblage than undisturbed forest, in part due to changes to understory vegetation (Isabirye-Basuta and Kasenene, 1987). Similarly, once-logged forest in Malaysian Borneo hosts comparable levels of bird richness to unlogged forest (Edwards et al., 2011). Overall estimates of the proportion of primary forest species remaining in degraded stands range from less than 10% to more than 90% across taxonomic groups (Berry et al., 2010, Chazdon et al., 2009). Although the negative effects of logging are significant in meta-analyses at the pan-tropical level, in comparison to other disturbances faced by forests, the impact of timber extraction is relatively benign (Gibson et al., 2011).

Several reasons are reported to explain discrepancies in the logging literature. Fundamentally, species are known to differ in their sensitivity to environmental change, and so variation in responses to disturbance across taxonomic groups is evident (Meijaard et al., 2005, Meijaard and Sheil, 2008). For example, of the 15 taxonomic groups sampled in the Brazilian Amazon by Barlow et al. (2007), only four taxa (trees/lianas, birds, fruit-feeding butterflies and leaf-litter amphibians) exhibited the reduced species richness expected in Eucalyptus plantation compared to forest, with most groups exhibiting idiosyncratic responses even between undisturbed and regenerating forest treatments. Variation in population responses is also apparent within taxa and is most evident when regional or global datasets are collated. A synthesis of the literature on birds and butterflies in undisturbed and disturbed forests, for example, found increased and decreased diversity in response to disturbance in almost equal measure (Hill and Hamer, 2004). However, when pan-tropical analyses have partitioned bird assemblages consistently into guilds or ensembles, they reveal the abundance of granivores to increase in logged forests, insectivores and frugivores to decline, and the responses of nectarivores and carnivores to vary by tropical region (Gray et al., 2007).

While variation in disturbance sensitivity among taxa is undoubtedly central to the reported variation in logging impacts, the very nature of timber extraction in the tropics also makes robust comparisons of unlogged and logged forests difficult, and sometimes impossible. While these issues have not gone unnoticed in the logging literature (e.g. Frumhoff, 1995), only recently have ecologists voiced significant concern (Chazdon et al., 2009, Dent and Wright, 2009, Gardner et al., 2009, Lindenmayer and Laurance, 2012, Ramage et al., 2013). There is a growing recognition that at least some statistical signals, or lack of signals, in logging-effect datasets may be confounded by experimental design. The heterogeneous nature of logging in the tropics typically results in a spatial mosaic of forest types and disturbance levels, with some parts of concessions being heavily degraded, while other patches escape logging completely, despite extraction data to the contrary (Cannon et al., 1994).

Logging activities also tend to be undertaken on relatively accessible terrain, and so signals in community data can also be confounded by variation in topography, and hence forest productivity, between these sites and unlogged controls (Gardner et al., 2009). Difficulties of access and an increasing paucity of unlogged controls then raise the problem of finding sufficient numbers of replicate experimental units to undertake comparative studies. These units need to be not only appropriate to detect any response by the study organisms under question (Hamer et al., 2003; Hill and Hamer, 2004) but also large enough to encapsulate landscape-level variation in disturbance, while being sufficiently spaced apart to be considered truly statistically independent (Shea et al., 2004). Combined, these limitations have the potential to mask signals in assemblage datasets (Meijaard et al., 2005, Meijaard and Sheil, 2008), leading most researchers to make understandable and often inevitable tradeoffs between adequate scale, replication and sample sizes in study design. In addition to these problems, the most important effects of forest disturbance are likely to be more prevalent in high-intensity silviculture systems and will accumulate over multiple rounds of logging (Edwards et al., 2011, Lindenmayer and Laurance, 2012).

In summary, although taxonomic variation in sensitivity to disturbance is central to understanding the effects of logging on biodiversity, the impacts of timber extraction, as with other disturbances, are likely to vary over space, time and intensity, even within concessions with a similar management history. This makes true replication for comparative studies of disturbance treatments particularly difficult to achieve in tropical forests and has the potential to confound signals from datasets and thus contribute to some of the variation in logging effects reported in the literature.

Despite methodological challenges being long recognised (Frumhoff, 1995), comparative approaches continue in the logging-impact literature and a somewhat artificial dichotomy between unlogged and logged forests prevails. Assessments of species differences solely between discrete forest management treatments risk overlooking potentially large community changes in response to environmental and/or disturbance gradients that are inherent in the study system. The simple premise of gradient analyses (sensu Ter-Braak and Prentice, 2004) is that species are more abundant around their environmental optimum and so successive changes in the abundance and replacement of species occurs as a function of environmental variation. Gradient approaches are well known in landscape ecology and have had a marked influence on studies of urbanisation, fragmentation and land-use change (Cushman et al., 2010, McDonnell and Pickett, 1990); yet the gradient paradigm has received relatively little attention in the logging-impact literature. Most gradient studies in the tropics to date have focused on extreme gradients of land-use change from forest to non-forest habitats (e.g. Kessler et al., 2009), habitat fragmentation (e.g. Ewers and Didham, 2006) and elevation (McCain and Grytnes, 2010) rather than forest disturbance per se (but see Aguilar-Amuchastegui and Henebry, 2007, Hamer et al., 2003, Lammertink, 2004). This is surprising, since viewing forest landscapes as gradients has the potential to account for spatial variation of inherent environmental parameters (Clark and Clark, 2000) as well as disturbances within otherwise preconceived logging treatments. Gradient analyses are also better equipped to detect subtle variation in population sizes and assemblage structure of forest wildlife pertinent to silvicultural management, and can provide deeper insights into biodiversity change beyond simple measures of species richness. Moreover, quantifying responses in this way also facilitates the prediction of species’ responses to restoration efforts and potentially enables the identification of indicator species for biological monitoring.

We report on the first evaluation of tropical biota in heavily degraded logged forests based on both gradient and traditional comparative analyses. Most previous logging-impact studies have focused on the effects of a single rotation of timber extraction, and only recently has attention focused on the effects of a second round of activity (Edwards et al., 2011, Woodcock et al., 2011). One novel aspect of our study is to take these appraisals one step further by examining the biological importance of forests subject to further logging, whereby the vast majority of commercial timber is removed from the forest prior to conversion to other land uses. Our study is a product of a new large-scale experiment examining forest modification on the Southeast Asian island of Borneo, a biodiversity hotspot with some of the highest timber extraction rates in the world (Fisher et al., 2011). Central to the design of this experiment is a forest modification gradient arising from multiple rounds of logging and the eventual clearance of forest to monoculture, a process that mimics the real-world pattern of habitat conversion across much of the tropics today. The study landscape also exemplifies many of the aforementioned difficulties experienced in the design of logging-effect studies concerning replication and the influence of spatial correlation. We use both gradient analyses and comparative approaches, as well as sensitivity analyses where appropriate, to address these difficulties.

We focus on the effects of logging on insectivorous bats, which form a centre of richness in the Indo-Malayan region where they represent up to half of all forest mammal species (Findley, 1993). A number of ecological traits, such as low fecundity, longevity and high survivorship, indicate that bats are a resource-limited group (Findley, 1993), leading to recent studies promoting their utility as bioindicators (Jones et al., 2009). Nevertheless, there remains substantial variation in the reported effects of logging. To date, the majority of disturbance studies for tropical bats have been undertaken in the neotropics, where bat assemblages in forests are dominated by members of the Phyllostomidae. While some of these studies reveal predictable declines in overall bat richness and abundance in logged forest sites (e.g. Medellín et al., 2000, Peters et al., 2006), others highlight inconsistent responses among species, particularly in low-intensity extraction systems (e.g. Presley et al., 2008). In well-managed forest stands, neotropical bat assemblages are known to recover well from disturbance events (e.g. Clarke et al., 2005a, Clarke et al., 2005b, Willig et al., 2007).

Far fewer logging studies have focused on palaeotropical bats, assemblages of which are structured differently to those in the neotropics as they are dominated by insectivorous species not found outside the Old World. Borneo bat communities comprise at least 93 species, of which 76 are insectivorous, and up to 40 of these species can be readily captured in the forest understory (Struebig et al., 2012). Several lines of evidence suggest that a substantial number of these species use landscapes at much smaller spatial scales than is commonly perceived from their ability to fly. A recent compilation of life-history characteristics of Borneo mammals reveals the home ranges of insectivorous bats to be on average ca. 4–15 times smaller than those of larger forest mammals (median range for: 40 understory bat species = 44 ha; 13 primate species = 200 ha; 21 small carnivore species = 700 ha; Wilson et al., 2010). While the ranges of cave-roosting insectivorous bats can be substantial (median range for 14 species = 2200 ha), the ranges of those species roosting in forest trees and vegetation are comparable to those of terrestrial mammals of similar size (ca. 2 ha: 19 species of bat vs. 19 murid rodents and 10 tree shrews).

The ecological flexibility of palaeotropical bats is thought to be constrained by ecomorphological traits, roosting ecology and social organisation, which vary across taxa (reviewed in Kingston et al., 2003, Rossiter et al., 2012, Struebig et al., 2008). Combinations of these factors affect local dispersion and the capacity for movement, as indicated by differential patterns of genetic structure and gene flow across bat taxa in intact forest (Rossiter et al., 2012) and mosaic habitats (Struebig et al., 2011). Bat assemblages in this region are also known to undergo area-dependent declines in diversity following forest fragmentation (Struebig et al., 2008, Struebig et al., 2011), structural changes following forest degradation (Furey et al., 2010) and major declines in diversity following deforestation in line with other animal groups (Fitzherbert et al., 2008). As a number of ecological traits of bats are often shared with birds and/or other mammals (e.g. wing morphology, Norberg, 1998; insectivorous/frugivorous diets and cavity-nesting tendencies, Kunz and Lumsden, 2006), examining the effects of logging on these animals may yield useful insights into the responses of other taxa.

We examine changes in bat assemblages across a habitat-disturbance gradient, ranging from pristine old growth to twice logged to forest logged several times. Our approach considers the utility of both traditional comparative analyses of forest types, as well as gradient analyses of finely resolved assemblage and forest-structure data. First, we examine patterns in species richness and abundance across forest types and sites. We then quantify variation in assemblage structure among sites using unconstrained ordination and related techniques, capable of partitioning species compositional data both as groups and in relation to gradients. Finally, we extend our gradient appraisal to the use of mixed-effects models to tease out species-abundance responses to forest disturbance at the level of sampling points and confirm the most influential forest structural variables involved in this process. By partitioning analyses in this way, and undertaking sensitivity analyses to account for potential effects of spatial pseudoreplication, we illustrate that gradient approaches can provide deeper insights into the subtle responses of biodiversity to forest disturbance than more traditional comparisons of forest treatments. Nevertheless, we conclude that both approaches are complimentary, each revealing its own element of the disturbance process that can be used to inform tropical forest management and conservation.

Section snippets

Study area

Fieldwork was based at the Stability of Altered Forest Ecosystems Project (www.SAFEproject.net), a recently established landscape modification experiment in Sabah, Malaysian Borneo (Fig. 1). The SAFE project area encompasses 7200 ha of lowland dipterocarp rainforest in the Kalabakan Forest Reserve (4°43′N, 117°35′E), the majority of which has been long designated for conversion to plantation by the Malaysian government (Ewers et al., 2011). International sustainability standards (e.g. //www.rspo.org

Forest-structure gradient

Our measures of forest disturbance—canopy height and openness—defined a clear gradient in habitat structure over the 12 sites sampled (Table 1). The canopy of old-growth forest sites was typically taller and more closed than that in logged forest. Tree density varied substantially over the forested landscape, but as expected, was greatest at sites in taller forest (R = 0.771; p = 0.003) with closed canopy (R =  0.825; p < 0.001) (Table 1). Of the 2724 trees counted in our vegetation plots, 221 (8.1%)

Discussion

There remains much variation in the reported effects of logging on tropical biota. While most of this is likely due to inherent differences in the ways by which taxa respond to environmental change, another contributing factor is that many logging-effect studies evaluate impacts solely via comparative analyses of unlogged versus logged forest treatments, which brings with it methodological constraints. In our study of insectivorous bats in the heavily degraded forests of Borneo, we demonstrate

Acknowledgements

We are especially grateful to the Economic Planning Unit of the Malaysian Government and the Sabah Biodiversity Council for granting permission to undertake our field research in Sabah, as well as Yayasan Sabah, Benta Wawasan Sdn. Bhd. and Sabah Softwoods Sdn. Bhd. for allowing us access to research sites. We also thank Glen Reynolds, the Royal Society Southeast Asian Rainforest Research Programme, the Maliau Basin Management Committee, Rob Ewers and the SAFE Science Committee for reviewing

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