IMPACT OF SEEDLING REMOVAL ON NATURAL REGENERATION IN THE SOUTHERN ATLANTIC FOREST REMNANT

In the present scenario of a high deforestation rate in tropical forests (Hansen et al., 2013), it is critical to develop strategies to conserve or at least minimize the loss of biodiversity (Rodrigues et al., 2011), as well as to protect soil structure (Rodrigues et al., 2011; Rocha Junior et al., 2013).

Forest restoration approaches vary depending on the level of degradation, residual vegetation, and the desired results (Chazdon, 2008). Environmental analysis is required to define the most appropriate reforestation technique (Chazdon, 2008). In highly degraded environments with impoverished soils and with no potential for natural resilience, the planting of highly diverse forest species (Rodrigues et al., 2009) can speed up the restoration process, providing benefits such as soil and water conservation, carbon sequestration, and other ecosystem services (Rodrigues et al., 2009; Gazell et al., 2012; Ferez et al., 2015).

However, there is a low supply of native forest species available for commercialization in nurseries, as can be seen in the low species diversity of restoration plantations (Viani and Rodrigues, 2008). In addition, two-thirds of these species belong to the early stages of secondary succession (Barbosa et al., 2003) and may reduce the ecological viability of forests in the process of restoration, as is the case for areas in fragmented landscapes (Rodrigues et al., 2011).

Under these circumstances, some studies have shown that transplantation of naturally regenerated seedlings could be a strategy for the production of seedlings in nurseries (Calegari et al., 2011; Viani et al., 2012; Turchetto et al., 2016). The main advantage of this technique is the production of seedlings adapted to their bioclimatic regions, mainly of pioneering species that are not available in nurseries.

The formation of a seedling bank is a strategy that can be used for species of plants that germinate under the canopy (Whitmore, 1989). The process of recruitment and establishment in tropical forests depends on a number of factors, including moisture, nutrients, predation of herbivorous seeds and seedlings, and the occurrence of pathogens (Molofsky and Fisher, 1993; Brearley et al., 2003). Therefore, of the total number of germinated seeds that constitute the seedling bank, approximately 10% survive beyond the juvenile phase. Thus, utilization of these seedlings which would normally be eliminated can be greatly beneficial to restoration practices (Carrington, 2014).

However, according to Viani and Rodrigues (2008), any anthropic action, modification, or management practice in natural areas, in this case specifically related to the seedling community, requires previous investigation in order to avoid irreparable damage to the diversity, productivity, and connectivity of the population, the community, and the ecosystem as a whole. This information can be obtained by analyzing the restoration capacity of an individual/species/community after exposure to adverse conditions (Higa et al., 2000); these conditions may be related to environmental restrictions or the intensity of anthropic interference, which define the potential for resilience of the community.

In this context, the present study aimed to characterize the resilience and dynamics of the seedling bank of a forest remnant in the extreme south of the Atlantic Forest biome when subjected to seedling transplantation. We sought to answer the following questions: a) Does seedling transplantation impair the dynamics of the community? b) Is there a limit of acceptable removal? and c) Does the impact vary among species?

Our results show that the regeneration community can tolerate the removal of up to 25% of regenerating seedlings, while removal intensities over 50% interfere with the resilience of the seedling bank, as the vegetal community was not able to reestablish the species and seedlings initially present. Viani and Rodrigues (2008), investigating the impact on a seedling bank caused by different removal intensities in a semideciduous seasonal forest in the state of São Paulo, found that at 18 months, seedlings and species numbers in plots with 50% removal of individuals did not differ significantly from those in the control (0% removal).

This shows the resilience potential of the environment when the remnant vegetation is not considerably affected. Thus, the results indicate that naturally regenerated seedlings can be used to enrich restoration projects in degraded areas without compromising the regenerative potential of forests.

On the other hand, the removal of more than 50% of the seedlings led to a reduction in the number of individuals and species sampled, indicating a limit on the possible removal of regenerating individuals. In this case, a larger number of species ceased to constitute the seedlings bank, probably due to the need to maintain a “stock” with some species with more difficult dispersion and/or regeneration. This scenario demonstrates that the impact of the removal of individuals contained in the seedling bank may be significant for some species, especially those with low regeneration density

Comparisons over the different periods of evaluation demonstrated the influence of the season on recruitment of tree-shrub seedlings. There was a greater density of individuals at 6 and 9 months (autumn and winter), with considerable reductions in the density of individuals from the 12^th month (spring). Other studies of seedling banks in seasonal forests have also found variation over time both in the richness and abundance of regenerating species (Mclaren and Mcdonald, 2003; Ceccon et al., 2004; Venturoli et al., 2011).

The phenology of species in seasonal forests, mechanisms of dormancy (Andeis et al., 2005), germination of many individuals in the seed bank at the end of spring and summer (Viani and Rodrigues, 2008), and seasonality due to supra-annual reproductive characteristics of many tropical tree species, all influence the seedling bank composition over the year.

In this study, increased seedling recruitment at 6 (autumn) and 9 months (winter) may be related to the reproductive characteristics of A. concolor (laranjeira-do-mato). This species presented the greatest density and was the only species with a greater number of individuals at 3 months (February 2014) than at the initial evaluation, for plots with 100% transplantation of regenerating individuals.

The initial evaluation was carried out in the flowering/fruiting period for A. concolor, which is between September and November (Andreis et al., 2005). In the subsequent evaluations, an increase in the number of emergent individuals is expected due to seed dispersion, since it is an understory species (Scipioni et al., 2013), indicating a seedling bank regeneration strategy.

The decreased number of seedlings at 12 months (November 2014) may be related to the increased temperature at this time of year, since seedlings with a height lower than 55 cm are sensitive to temperature variation. (Huxman et al., 2004), evaluating the efficiency of water utilization in different ecosystems, found that temperature and precipitation interfered in seedling survival and growth. According to Metz et al. (2008), seedlings are more susceptible to seasonal water deficit because they do not have deep enough roots to obtain water from deeper in the soil. The effects of the water deficit on the dry period are greater because of the increased temperatures and intensities of solar radiation, which may lead to plant desiccation and death (Lieberman and Mingguang, 1992; Vieira and Scariot, 2006).

When we analyzed the most abundant species in the seedling bank (A. concolor, E. rostrifolia, N. megapotamica, and T. claussenii), different regeneration strategies following seedling bank removal were observed. The variations between treatments and between seasons within each treatment may be related to reproductive and silvicultural characteristics of the species.

According to Janzen (1970), the survival, establishment, and development of seedlings are influenced by several morphological, physiological, and abiotic factors, as well as by biological interactions. The way each species responds to these factors is determined by seedling adaptations, that is, the way each species interacts with the environment and with other organisms (Melo et al., 2004).

E. rostrifolia and A. concolor presented intraspecific thinning. According to Freckleton and Watkinson (2002), survival rates in most plants decrease as density increases. Moreover, higher temperatures and lack of rain can also contribute to seedling mortality in these species. Because most of the individuals presented a height below 10 cm, they did not possess photosynthetic capacity efficient enough for establishment.

T. claussenii and N. megapotamica presented a significant reduction in the number of individuals at removal intensities over 75%. T. claussenii presents a low germination rate (Backes and Irgang, 2002), while N. megapotamica is characterized by abundant regeneration under shade (Backes and Irgang, 2002; Carvalho, 2006). Davide et al. (2003) note that species of the genus Nectandra present seeds with short longevity (recalcitrant). Thus, the existence of a seedling bank for these species may constitute a survival strategy, as these remain in the understory until recruitment by higher classes.

According to Viani and Rodrigues (2008), the use of seedling banks of natural areas for seedling production aimed at forest restoration should focus on species with high regeneration density and evident intraspecific thinning, which was the case for E. rostrifolia and A. concolor in all treatments evaluated.

T. claussenii and N. megapotamica did not present intraspecific thinning. However, for the treatments up to 50% removal, the number of individuals was similar to that found for the control (0% removal) at 12 months. Of the species studies here, these show good potential for use in forest nurseries, considering that their seedlings are difficult to obtain and produce since they are adapted to regional edaphoclimatic conditions.

The remnant studied presented partial capacity for self-regeneration following low-intensity seedling bank removal.

Removal of up to 25% of the seedling bank over a short period of time does not interfere with the dynamics of the most abundant populations in the forest understory and may be a useful strategy to produce seedlings of species presenting difficult propagation.

Seedling removal of up to 25% does not impair the persistence of the communities of the species A. concolor, E. rostrifolia, T. claussenii, and N. megapotamica, which present abundant natural regeneration and/or intraspecific thinning. However, more studies with a longer period of evaluation are necessary to more fully understand the interference of seedling removal on vegetal community resilience.

This research was supported by the Foundation for Research Support of the Rio Grande do Sul State (FAPERGS) and the Environmental Fund of the Caixa Econômica Federal (AC FSA CAIXA, Nº. 015,007 / 2012).