Edge-effects Drive Tropical Forest Fragments Towards an Early-Successional System
1 Corresponding author; e-mail: email@example.com
O futuro da biodiversidade das florestas tropicais e dos serviços ambientais prestados por este ecossistema está intrinsecamente ligado a nossa habilidade de entender as mudanças deflagradas pela fragmentação de habitats e por outras forças que dirigem a dinâmica biológica em paisagens antrópicas. Neste artigo nós reunimos evidências empíricas e teóricas para argumentar que os efeitos de borda deflagram um processo sucessional rápido e inevitável, o qual conduz a maioria dos fragmentos de florestas neotropicais em direção a um sistema sucessional inicial. Este tipo de sistema emerge e persiste uma vez que os efeitos de borda favorecem, de forma permanente, um pequeno grupo de espécies pioneiras redundantes em detrimento de um grupo muito diverso de espécies que compõe as florestas maduras. Esta mudança na direção de um sistema inicial representa um conjunto de processes inter-relacionados, a qual define a assinatura dos ambientes expostos aos efeitos de borda em termos de estrutura de comunidades e do funcionamento do ecossistema. Nossa intenção é que este ensaio estimule a investigação e, também, uma melhor compreensão das forças que determinam a natureza dos ecossistemas em paisagens alteradas pela ação antrópica. Esta compreensão é um passo fundamental para a definição de normas do uso da terra que sejam capazes de ampliar o papel das paisagens antrópicas em termos de retenção de biodiversidade e prestação de serviços ambientais.
Habitat fragmentation has become the most pervasive and conspicuous anthropogenic form of disturbance in tropical forest landscapes following unprecedented rates of tropical deforestation (Laurance & Peres 2006). In the next decades, the relentless growth and spatial dispersion of the human population of several large tropical countries will continue to alter tropical landscapes in such a way that even vast remote tracts of old-growth forests are likely to be converted into archipelagos of small fragments and regenerating forest patches (Aide & Grau 2004, Wright 2005). With the expansion and consolidation of agricultural frontiers, many small primary forest fragments remaining within private landholdings—that are often scattered around public protected areas—are likely to remain confined to economically marginal lands and become gradually embedded in a human-managed, harsh matrix, dominated by pastures, croplands, and urban areas (Tabarelli et al. 2004). This sort of anthropogenic and highly fragmented agro-mosaic is already the predominant landscape across many previously forested tropical lands (Corlett 2000, Sodhi et al. 2004, Harvey et al. 2008). In fact, most aging deforestation frontiers are currently vastly dominated by very small fragments, which remain embedded within open-habitat matrices (Turner & Corlett 1996, Ranta et al. 1998, Gascon et al. 2000, Mendoza et al. 2005).
The future of tropical forest biodiversity and the invariably undercompensated environmental services provided by this ecosystem, such as carbon storage, are therefore inextricably tied to our ability to understand persistent, ecosystem-level changes triggered by habitat fragmentation and other forces driving the biological dynamic of anthropogenic landscapes (see Bawa et al. 2004). Fortunately, the topic of habitat fragmentation has acquired an increasing importance in the last three decades in the context of tropical forests (e.g., Schellas & Greenberg 1996, Laurance & Bierregaard 1997, Bierregaard et al. 2001; Laurance et al. 2007). Initially inspired by the equilibrium theory of island biogeography and the SLOSS debate (see Simberloff & Abele 1982), a number of studies examining the general question of ‘minimum critical size’ of protected areas have revealed an extensive suite of fragmentation-related effects and greatly extended the applied dimension of fragmentation ecology (Pimm 1998, Jules & Shahani 2003).
Briefly, we highlight only four overall key findings. First, tropical forest fragmentation facilitates and usually operates simultaneously with other human-induced disturbances such as logging, fire, and hunting (Laurance & Cochrane 2001, Peres 2001). Secondly, fragmentation promotes rapid and predictable shifts in the population to ecosystem level patterns of biological organization due to a myriad of processes including habitat loss, sample effect, creation of forest edges, rupture of biological connectivity, subdivision/isolation of populations, and post-isolation proliferation of invasive species (Laurance et al. 2002, 2006a; Fahrig 2003). Thirdly, most shifts lead to pronounced detrimental consequences for ecosystem functioning (i.e., energy flux, nutrient cycling, hydrological budgets), and for the long-term persistence of particular species groups in anthropogenic landscapes (Laurance & Bierregaard 1997, Bierregaard et al. 2001, Wirth et al. 2008). Finally, the intensity and magnitude of fragmentation-induced changes are greatly modulated by the spatial arrangement of forest fragments (landscape configuration) and the matrix harshness (Laurance et al. 2002, Tabarelli & Gascon 2005, Ferraz et al. 2007).
Despite these landmark findings, the overall time trajectory coursed by tropical forest ecosystems in response to the twin processes of habitat fragmentation and human encroachment of tropical landscapes has not been fully assimilated. A more holistic and unifying picture has therefore yet to emerge in order to improve our ability to preempt biodiversity loss in anthropogenic landscapes, and we view this as a cutting-edge, high-priority dimension of applied fragmentation research. Here we assemble empirical and theoretical evidence to argue that edge effects trigger a rapid and inevitable successional process that effectively drive most remaining Neotropical forest fragments towards a persistent, early-successional system. This postdisturbance retrogressive succession (sensuSantos et al. 2008) represents a major force driving the nature of Neotropical forest biotas in anthropogenic landscapes that consist primarily of edge-affected habitats, regardless of whether they are newly configured as a variegated, a truly fragmented or a relictual stage (sensuMcIntyre & Hobbs 1999). This working hypothesis has clear implications for the future agenda of fragmentation research and the imperative debate about the substitution value of conservation services provided by human-impacted habitats (see Bawa et al. 2004, Wright & Muller-Landau 2006).
SUCCESSIONAL TRAJECTORIES IN TROPICAL FOREST FRAGMENTS
Undisturbed primary tropical forests can be described as a self-perpetuating successional mosaic ranging from newly created canopy gaps to old-growth patches. A myriad of shade-tolerant tree and high-climbing liana species comprise the predominant regeneration guild for woody plants in tropical forests (Whitmore 1991, Richards 1996). Collectively, these woody species provide the predominant habitat structure and resources for countless other plant, invertebrate and vertebrate species in this ecosystem. In Neotropical forests, however, this scenario appears to be rapidly altered by habitat fragmentation as briefly synthesized here. As soon as forest edges are created, fragments experience a rapid, hyper-proliferation of short-lived pioneer trees, particularly along their edges (Laurance et al. 2006a). Concomitantly, several groups of shade-tolerant/old-growth tree species (e.g., large-seeded, long-lived emergent, hardwood tree species) are disfavored and these species gradually become rare and eventually may be driven to extinction at the landscape scale (Laurance et al. 2000, Cramer et al. 2007, Michalski et al. 2007).
Collectively, pioneer proliferation and reorganization of the old-growth flora result in a detectable floristic convergence across the landscape (Oliveira et al. 2004, Michalski et al. 2007). This is likely to reduce both alpha (within fragment) and beta (among fragments) diversity, and render tree assemblages more impoverished in terms of species composition, life-history traits and functional diversity (Laurance 2001, 2006b; Girão et al. 2007). As most short-lived pioneers consist of soft-wooded, canopy species (Swaine & Whitmore 1988, Nascimento et al. 2005), their relentless proliferation at the expenses of the old-growth flora inevitably aggravates the forest biomass collapse caused by increased mortality of large trees near forest edges, and contributes to the simplification of forest vertical stratification (Laurance et al. 1997, Nascimento & Laurance 2004). Examples of the highly degraded structure of vertical forest profiles are ubiquitous along the edges of most small fragments and forest corridors, which can be quantified using a mix of field and remote sensing approaches (Lees & Peres 2008). Pioneer proliferation is initially triggered by elevated light availability, which results from higher rates of treefall gaps due to the collapse of the emergent stratum along forest edges (Laurance et al. 1998, 2006a; D'Angelo et al. 2004). As pioneer trees reach maturity and form a more even canopy layer (postclosure forest edges), copious seed rain, increased light availability, and other edge-induced microclimatic changes can maintain suitable conditions for pioneer recruitment and cycles of pioneer self-replacement (i.e., multi- rather than single-generation pioneer assemblages). Meanwhile, edge-affected habitats remain environmentally adverse for many shade-tolerant tree species (Benítez-Malvido 1998, Tabarelli et al. 2004, Laurance et al. 2006b, Wirth et al. 2008). Pioneers should otherwise be largely replaced by shade-tolerant trees in increasingly older fragments, but this has yet to be documented.
In fact, the continued recruitment of pioneers along edge-affected habitats of both recently created (Nascimento et al. 2006) and much older hyper-fragmented landscapes (Tabarelli et al. 1999, Oliveira et al. 2004) supports the hypothesis that pioneer-dominated assemblages may be approaching near-equilibrium conditions, thereby representing a quasi-final, more stagnant rather than a transient successional stage. This rationale is entirely consistent with recent findings from an aging, hyper-fragmented landscape in the northeastern Atlantic forest of Brazil: over time, tree assemblages in either small forest fragments or forest edges converged floristically and became almost indistinguishable from patches of early- to mid-successional secondary forests (< 45-yr old) in terms of tree species richness and species/functional composition, but remained very distinct from those in old-growth, core forest interior areas (Santos et al. 2008). The pervasive simplification and striking convergence of tree assemblages inhabiting edge-affected habitats and regenerating secondary forests resulted from a combination of landscape-scale diffusion of some pioneer species and the patch-scale elimination of a large set of large-seeded, old-growth tree species (Santos et al. 2008).
The findings synthesized here have emerged from one of the most conspicuous patterns of tree assemblage structure that have been documented across a variety of Neotropical forest landscapes. They also underscore our precarious knowledge about the ultimate drivers of tree species recruitment in fragmented landscapes and edge-affected habitats. However, these findings offer clear empirical evidence that habitat fragmentation beyond a habitat loss threshold can trigger a rapid retrogressive successional process in remaining forest areas, with decisive consequences to the maintenance of functional diversity in tropical forests. In other words, habitat fragmentation can effectively drive edge-affected portions of forest fragments towards an early-successional system; i.e., a system dominated by both short- and long-lived pioneers (r-strategists, light-demanding plant species), which in this context largely structure plant assemblages, primary productivity and nutrient cycling. This altered ecosystem emerges and then persists as edge effects and associated shifts in the light regime consistently favor a small set of functionally redundant light-demanding plant species to the detriment of a highly diverse pool of species comprising the old-growth flora. This latter set of species spans the lion's share of the morphological and life-history diversity of tropical forest trees, lianas and epiphytes, including the root system, adult stature, woody density, crown architecture, phenological patterns, pollination and seed-dispersal systems (including fruit and seed morphology and nutritional content), life span, physiological requirements, and antiherbivore defense systems (see Swaine & Whitmore 1988, Whitmore 1991, Richards 1996, Turner 2001, Kang & Bawa 2003, Girão et al. 2007).
The hypothesis that habitat fragmentation can effectively drive Neotropical, edge-dominated forest fragments towards an early-successional system because edge effects consistently favor a small set of pioneers has four important corollaries. First, as successional trajectories towards an early-successional system are essentially an edge-induced phenomenon, they are likely to occur regardless of the effects of other fragmentation-related processes, such as habitat loss and isolation. Secondly, the extent to which forest fragments approach early-successional systems depends primarily on the magnitude and the distance of edge-effects. Thirdly, other forms of disturbance that often co-occur in fragmented landscapes (e.g., selective logging, fire, defaunation driven by overhunting) are likely to influence the pace and extent (but not the successional direction) of the successional changes by additive or aggravating differential effects on either pioneer or shade-tolerant species. In heavily defaunated landscapes, for instance, seed dispersal limitation aggravated by low densities or absence of seed dispersal agents may severely reduce recruitment away from parents and the recolonization rate of edge-affected habitats by gut-dispersed, shade-tolerant trees (Melo et al. 2006, 2007; Nuñez-Iturri & Howe 2007; Peres & Palacios 2007), while favoring small-seeded, abiotically dispersed species (Wright et al. 2007). Finally, the transition towards an early-successional system represents a set of interrelated processes that ultimately shapes the signature of edge-dominated habitats in terms of community structure and ecosystem functioning.
THE WAY FORWARD
Tropical forests are changing rapidly through a myriad of complex phenomena that pose great challenges for the research agenda in tropical conservation ecology (Wright 2005). The notion that severe anthropogenic disturbances invariably alter the rhythm and the successional trajectory of terrestrial ecosystems is not novel (see Bazzaz 2000), but this seminal hypothesis has not been investigated in the context of habitat fragmentation. By assuming that forest fragmentation triggers, deflects or reverses the successional process (from mature to early systems) researchers can heed lessons from succession theory to predict (and eventually verify) the major fragmentation-induced ecosystem changes, their underlying mechanisms, and the potential of anthropogenic landscapes for environmental services and long-term biodiversity retention.
In sum, we suspect that habitat fragmentation and the ensuing creation of artificial forest edges profoundly depress the ability of Neotropical forests to retain forest biodiversity, biomass, and nutrients wherever the matrix remains deforested or as open habitats. As increasingly older forest fragments approach relaxation conditions, ecosystem performance is likely to attain the same patterns observed in patches of early- to middle-aged secondary forests (< 40- to 50-yr old) following prolonged cultivation or pastures, such as low nutrient stocks that cycle via eroded and more simplified foodwebs sustained by pioneers (see Brown & Lugo 1990, Turner et al. 1997, Guarigata & Ostertag 2001, Davidson et al. 2007; for information on secondary succession). To understand this form of ecosystem decay, special attention must be given to population-level mechanisms driving the recruitment of pioneer and shade-tolerant species, since most community/ecosystem-level properties are profoundly influenced by the relative importance that these two broad functional groups achieve along successional trajectories (Richards 1996, Bazzaz 2000, Chazdon 2008). Namely, the way pioneer/shade-tolerant species respond to resource availability (e.g., light, nutrients and seed dispersal vectors), and to selective pressures exerted by herbivores and pathogens must be further investigated. These factors have been consistently identified as the main drivers of both plant recruitment and the successional trajectory of regenerating forest patches across tropical forests (Bazzaz & Pickett 1980, Hooper et al. 2005, Chazdon et al. 2007).
Recent global assessments have shown the limited coverage of protected areas in tropical biotas, which has fuelled a growing interest in the possible conservation services provided by anthropogenic landscapes (Brooks 2004, Harvey & Saénz 2008). By edging towards early-successional systems, significant portions of Neotropical, hyper-fragmented landscapes will likely fulfill a limited value in terms of biodiversity conservation and provision of environmental services. This poses serious questions over the efficiency of any conservation strategy that fails to safeguard the persistence of large blocks of core primary forests, which have been shown to provide an irreplaceable conservation role (Gascon et al. 2000, Barlow et al. 2007). We hope that this essay can instigate a more comprehensive assessment of the forces driving the nature of human-modified tropical ecosystems in both the New and Old World tropics. This is a timely crucial step towards the consolidation of land-use regulations designed to guarantee the full potential of anthropogenic landscapes in terms of their biodiversity conservation and environmental services.
We thank the Brazilian Science Council (CNPq) and Conservation International do Brasil for funding MT and AVL's research program in the Atlantic forest of northeastern Brazil. CAP's work in Neotropical forests was funded by the Center for Applied Biodiversity Science of Conservation International and NERC–UK. We also thank R. Wirth for the invitation to contribute to this section of Biotropica. J. Ghazoul, W. F. Laurance, B. Williamson, and R. Wirth offered constructive criticisms on the manuscript.