Original articleRegeneration patterns of a long-lived dominant conifer and the effects of logging in southern South America
Introduction
In forested ecosystems, large-scale disturbances like landslides, earthquakes and slash-and-burn agriculture give rise to considerable tracts of successional forests. In contrast to the successional communities that develop following small-scale tree-fall gaps, secondary forests forming after large-scale disturbances are frequently dominated by long-lived pioneer tree species. This successional pathway seems to be a feature common to distinct tropical, subtropical and temperate forest types (Hartshorn, 1978, Swaine and Whitmore, 1988, Guariguata and Ostertag, 2001, Kennard, 2002, Kubota et al., 2005). Long-lived pioneers are shade-intolerant and depend upon disturbances for recruitment opportunities. They frequently attain large adult sizes, not rarely being emergents (Hartshorn, 1978), and present lifespans up to many centuries (Enright and Ogden, 1995).
The life-history syndrome commonly associated with long-lived pioneers seems to be related to the occupation of well-lit areas of forested ecosystems in space (as emergents), rather than time (in short-lived tree-fall gaps). This is accomplished through high growth rates associated with high maximum heights and diameters and high longevity, according to the classification of life-history traits by Easdale et al. (2007). These traits are thought to confer competitive advantage in landscapes subjected to intense and relatively large-scale disturbances (e.g., mountainous habitats) (Armesto et al., 1992, Easdale et al., 2007) that allow the establishment of cohorts in high-light microenvironments that later translate in expressive presence in the upper canopy or even as an even-aged emergent layer (Armesto et al., 1992, Enright and Ogden, 1995).
A thorough understanding of the demography of long-lived pioneers has important implications for forest community ecology and management because these species play a key role in regulating the rate of successional change (Grau et al., 1997, Mailly et al., 2000, Kubota et al., 2005). Considerable variation exists in this regard, since long-lived pioneers may retard succession by blocking the regeneration of shade-tolerant species (Kubota et al., 2005), alter the floristic composition of late-successional regenerants (Grau et al., 1997) or just reduce the time necessary for climax species to dominate the forest canopy (Mailly et al., 2000).
In the southern hemisphere conifers form an outstanding group of long-lived pioneers mostly confined to high-rainfall mountainous areas (Hill and Brodribb, 1999). Their abundance and economic value have made them a recent focus of studies on the regeneration mode and succession of the forests in which they occur (Ogden and Stewart, 1995, Enright et al., 1999, Lusk, 1999, Rigg, 2005, Souza, 2007). Although our understanding of the regeneration ecology of southern conifers is far from complete, a number of generalizations on their dispersal, recruitment requirements and microsite occupancy have been advanced in the Lozengue model (Ogden and Stewart, 1995). According to this model, cohorts of large-sized and light-demanding conifers establish following severe disturbances. They are followed by successive cohorts of smaller angiosperm species that dominate the forest understorey and suppress the recruitment of conifer seedlings, which become restricted to multiple tree-fall gaps. Because of the high longevity and large size of adult conifers, their populations remain as dominant components of the forest biomass and architecture for long periods of time (frequently centuries), although demographically functioning as remnant populations, that lack significant constant regeneration. We investigated whether this model corresponds to the regeneration patterns of Araucaria angustifolia, a long-lived conifer that dominates the poorly studied mixed conifer–hardwood forests of the Brazilian Atlantic Forest complex.
At the beginning of the twentieth century, some 20 million hectares of Araucaria angustifolia forest existed (Guerra et al., 2002) but, as occurred in conifer-dominated temperate forests (Mailly et al., 2000), the high timber value of Araucaria angustifolia led to extensive logging of the Brazilian mixed forests in the last century, reducing them to ca. 2–4% of their former extent (Guerra et al., 2002). The selectively logged forest remnants that comprise the majority of Brazilian mixed forests present an opportunity to better assess the expectations generated by the current model of long-lived pioneer regeneration. In addition, the degraded condition of these logged forest remnants makes a deeper understanding of the regeneration ecology of Araucaria angustifolia a conservation necessity in order to achieve proper restoration and management. Despite its ecological and commercial importance, little is known of the dynamics of natural stands of Araucaria angustifolia and of the species’ regeneration strategy (Veblen et al., 1995).
Specifically, we tested the validity of the following expectations:
Expectation 1: In unlogged forests, Araucaria angustifolia populations are characterized by size distributions with many large individuals and a long tail of relatively rare, small individuals. In logged stands the species’ size-distributions should become more symmetric or even right-skewed, if logging activities were recent. This should reflect not only a reduction in the relative abundance of adult trees but also a marked increase of small and medium-sized individuals.
Left-skewed size distribution characterizes gap-dependent species with large fecundity, seed mortality, seedling mortality, high sapling growth and mortality rates and high proportion of recruits located in tree-fall gaps (Lorimer and Krug, 1983, Poorter et al., 1996, Coomes et al., 2003, Wright et al., 2003). A previous meta-analysis of population size-distribution of the species (Souza, 2007) seems to support this prediction, but the analyzed sites had an unknown range of logging histories.
Expectation 2: As a pioneer species, regeneration of Araucaria angustifolia should be restricted to more open-canopy microsites than expected by chance.
Canopy disturbances are known to enhance pioneer regeneration (Lieberman et al., 1995, Mailly et al., 2000). However, as a long-lived pioneer, Araucaria angustifolia probably does not continue to grow or survive long after canopy closure (Ogden and Stewart, 1995, Enright et al., 1999, Mailly et al., 2000). Hence, the species’ advanced regeneration should also be found under more open-canopy conditions than expected by chance.
Expectation 3: Adult trees should be aggregated at relatively large spatial scales, that correspond to past regeneration following canopy disturbance events at scales coarser than single tree-fall gaps. Regenerating individuals should be positively associated with reproductive females due to the low average dispersal distance resulting from the large seed size coupled with the prevalence of generalist seed predators.
This prediction is based on the premise that the scales of patterns might suggest the scales at which the processes responsible for such patterns operate (Chesson and Murdoch, 1986). Theory predicts that when generalist or mobile seed predators (often vertebrates) are attracted by adult trees but also tend to forage farther away, short dispersal distances are selected for and generate high seed densities that satiate seed predators (the McCanny pattern; Nathan and Casagrandi, 2004). Araucaria angustifolia produces supra-annual large crops of large (ca. 5 g) seeds with low viability (Ntima, 1968). Foraging animals, such as jays, rodents, domestic pigs and peccaries, disperse and consume the seeds widely (Vieira and Iob, in press). We thus expect that the spatial distribution of regenerants reflect the McCanny spatial distribution mentioned above.
Section snippets
Study site and species
The study was undertaken within the Brazilian mixed conifer–hardwood forest (Ombrophilous Mixed Forest, in the Brazilian vegetation classification system) (Veloso et al., 1991), a subtropical extension of Brazilian tropical Atlantic forests, in São Francisco de Paula National Forest (FLONA; 29°25S, 50°23W), municipality of São Francisco de Paula, state of Rio Grande do Sul, southern Brazil. The FLONA (Fig. 1) is a 1606 ha forest reserve with mean annual temperature of 14.5 °C, and mean annual
Definition of ontogenetic stages
The qualitative observations on the external macromorphological structures allowed the distinction of three pre-reproductive and one reproductive ontogenetic stages in the populations. These four stages were characterized as follows.
Discussion
In this work, we provided the first comprehensive analysis of the regeneration patterns of the southern dominant conifer Araucaria angustifolia, and evaluated whether it corresponds to the expectations generated by the current paradigm of the dynamics of forests dominated by long-lived pioneers. In general, the observed patterns fit well with the regeneration syndrome outlined by the Lozenge model for the southern hemisphere and the empirical patterns obtained in North America as well.
Acknowledgments
Financial support was provided by the Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS, grant no. 05/2277.7 to A.F.S.), by the British Ecological Society (grant no. 671-779 SEPG to A.F.S.), by the International Foundation for Science (grant AD/16833 to A.F.S.), and by CNPq (Brazilian Research Council, PIBIC grant to C.F.). The work was only possible due to the collaboration with the União Protetora do Ambiente Natural (UPAN), specially the constant support of Rafael José
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