We present the results of the first large-scale study carried out in the Cerrado-Amazon ecotone (CAE) on the woody encroachment process in savanna. We provide robust information on the succession mechanisms that drive changes in tree structure and diversity during the process of woody encroachment of the dominant savanna phytophysiognomy, ‘Cerrado tipico’. We also address the key microenvironmental changes responsible for woody encroachment, and their importance for biodiversity conservation. Finally, we provide insights into which species determine savanna woody encroachment at different development stages.
Effects of woody encroachment on microenvironmental conditions
Overall, the close association between the changed local environment and floristic-structural characteristics in the areas surrounding focal plants supports the inference of a causal relationship that favors grouping of forest species together. This is characteristic of a nucleation process (Yarranton and Morrison 1974) and corroborates our first hypothesis. Microclimate modification under focal plants is a crucial initial factor in facilitating juveniles of forest species, which prefer more shaded places and milder temperatures than savanna species (Aschehoug et al. 2016; Mistry 2000; Morandi et al. 2015; Passos et al. 2014, 2018). The successful development of species from a different vegetation class, forests, even within the typical savanna environment that we observed, is consistent with other work (Passos et al. 2014; Salazar et al., 2012; Veenendaal et al. 2015). It therefore strengthens confidence in the generality and importance of this vegetation succession process of “woody encroachment” in tropical savannas.
As observed in other microenvironmental studies, the greater accumulation of the litter layer, organic matter, and nutrients in areas with focal plants contribute to woody encroachment (Kellman 1979; Passos et al. 2014; Rodrigues-Souza et al. 2015). Remarkably, the quantities of organic matter and nutrients in the soil and the litter layer, we recorded in areas under focal plant canopies are similar to those found in forest areas, such as the dense woodland (Cerradão) in the Cerrado-Amazon ecotone (Oliveira et al. 2016; Peixoto et al. 2018; Valadão et al. 2016). The accumulation of litterfall and the decrease in the soil surface temperature cause a significant physical environmental change, as well as altering the dynamics of organic matter accumulation and the return of nutrients to the soil in savanna environments (Elias et al. 2019; Oliveira et al. 2016; Passos et al. 2014). These changes allow (facilitate) rapid encroachment, with the establishment and development of new forest species adapted to these conditions (Morandi et al. 2015) triggering the woody encroachment process.
The reduction in grass cover that we observed in the areas surrounding focal plants is another microenvironmental change that reflects woody plant encroachment. This may itself be supported by the global increase in atmospheric CO2 concentrations that favors C3 plants (trees) over C4 grasses by permitting increased water use efficiency in the C3 carbon assimilation process (Kerbauy 2012), and the increased resulting competitive exclusion of grasses by trees through light interception (e.g. Khavhagali and Bond 2008, Morandi et al. 2015).
Woody encroachment: the importance of nurse plants for floristics and structure
We found higher density and aboveground biomass values of adult trees in the area under the influence of focal plants than in open areas, which partially corroborated our second hypothesis. Thus, we conclude that focal plants favor the concentrated establishment and development of species, making them ‘nurse plants’. In the savannas of the southern Amazon-Cerrado transition zone, these form islands of diversity and facilitate the establishment of new species, causing plant encroachment. As predicted in the literature, they drive long-term environmental, structural, and floristic changes that turn the savanna environment into a forest environment (Arantes et al. 2014; Connell and Slatyer 1977; Franks 2003; Passos et al. 2014, 2018; Yarranton and Morrison 1974).
Our study concentrated on the very local and initital process of facilitation driven by trees. Over time, the microclimatic and edaphic changes induced by nurse plants are likely to persist and continue to favor the establishment and development of juvenile individuals of a suite of forest species (Gómez-Aparicio et al. 2005; Ren et al. 2008), including some with the potential to form large canopies and dominate the vegetation such as Tachigali vulgaris (Morandi et al. 2018). There are of course also larger scale regional and global contexts to such changes. A potential regional ‘end state’ is reflected in the high aboveground biomass values in areas close to moist forest environments, such as the dense woodlands in the states of Mato Grosso (Passos et al. 2018; Peixoto et al. 2017) and Minas Gerais (Scolforo et al. 2008). More broadly, in the Amazon-Cerrado transition study area, factors such as high rainfall (Morandi et al. 2018) and the increasing concentration of CO2 since the beginning of the industrial revolution (Veenendaal et al. 2015) may be favoring the process of woody encroachment generally. However, long-term studies are essential to corroborate this expectation.
Facilitating species as promoters of ecological succession in the Cerrado-Amazon ecotone
Our data demonstrated that areas influenced by focal plants favor the establishment and development of forest species, with values of aboveground biomass, stem density and species richness up to twice as high as open areas, corroborating our third hypothesis. Forest species, such as Emmotum nitens and Hirtella glandulosa, associated with the large generalist Tachigali vulgaris, are classified as connectors of forest vegetation (Oliveira-Filho and Ratter 1995; Solórzano et al. 2012) and recognized as indicators of change from savanna to forest communities (Marimon et al. 2006; Morandi et al. 2015; Ratter 1992). Other generalist species, such as Roupala montana and Guapira graciliflora, may also favor encroachment, and, according to Morandi et al. (2015) are tending to increase in abundance in both savanna and forest vegetation in the region. Our work shows that these key species for the woody plant encroachment process in the Cerrado-Amazon ecotone create environmental conditions that facilitate the establishment and development of species with characteristics different from those in the original environment.
The establishment and development of forest species, as well as the woody encroachment process as a whole, is likely to be further enhanced by the fast turnover (“hyperdynamism”) of the tree vegetation (Marimon et al. 2014) and the fast cycling (“hypercycling”) of nutrients in the different vegetation types of the CAE (Oliveira et al. 2016). Rapid stem turnover and rapid nutrient cycling are both promoted by nurse plants. For example, while dystrophic soils in savanna environments limit the occurrence of forest species (Oliveira et al. 2016), nurse plants create enriched microenvironments that facilitate tree recruitment and growth (Passos et al. 2018), ensuring increasing biomass and species diversity and the successional replacement of savanna species by forest species (Elias et al. 2019; Morandi et al. 2015).
Step-by-step of the woody encroachment process of savanna areas in CAE
Based on our results, we can define four stages in the woody encroachment process of savanna areas. The first is characterized by microenvironmental changes created by nurse plants under their crowns, such as an increase in shading, litter layer thickness, and SOM content (Fig. 3). Although these effects have already been documented in the central heartland of the Cerrado (Durigan and Ratter. 2016; Geiger et al. 2011; Passos et al. 2014), our results more than 1,000 km distant from these studies in the transition zone, suggest that they can occur more intensely, more rapidly, and broadly at the landscape scale in the CAE. The proximity to Amazonia contributes to the potential for these microenvironmental changes, given the less intense seasonality (Gloor et al. 2013), the more forest-like floristic composition (Passos et al. 2018), and the higher diversity and biomass in CAE savanna physiognomies than in their equivalents in the Cerrado core to the east (Marimon et al. 2014; Morandi et al. 2020). These conditions, combined with stem hyperdynamism and nutrient hypercycling, both characteristic of CAE vegetation (Esquivel-Muelbert et al. 2020; Marimon et al. 2014; Oliveira et al. 2016), prime the region for potential widespread woody encroachment.
The second stage is characterized by changes in species composition after formation of the nuclei (nucleation), which creates natural perches or refuges for the landing and shelter of seed-dispersing animals (Passos et al. 2014; Reis et al. 2014). With the establishment of forest species to the detriment of savanna species (Passos et al. 2018), environmental heterogeneity increases locally as a patchwork of vegetation develops. The third stage is characterized by expansion of the nuclei, enhanced by the arrival of new facilitating species. In this stage, there is an increase in the complexity of interspecific interactions, including increased variety of ecological niches and their dispersion (Oliveira-Filho and Ratter 2002; Reis et al. 2014), which can favor the input of species that feedback onto the process positively.
Finally, in the last stage, plant encroachment occurs through the fusion of previously formed nuclei spatially scattered throughout the area. In this stage, there is a general change in species structure and composition, with dominance of generalist and forest species and a suppression of savanna species (Arantes et al. 2014; Durigan and Ratter 2006; Elias et al. 2013; Franks 2003; Kellman 1979). In the absence of major disturbances, such as fire or extreme drought events (Gloor et al. 2013), the savanna woody encroachment process is completed.