Savanna woody encroachment in the Cerrado-Amazon ecotone

doi:10.21203/rs.3.rs-1654641/v1

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Research Article

Savanna woody encroachment in the Cerrado-Amazon ecotone

https://doi.org/10.21203/rs.3.rs-1654641/v1

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posted 26 May, 2022

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Purpose We investigated if, in transitional region between the South American savanna (Cerrado) and Amazon Biomes, the facilitation process help drive this development of forest trees in open-canopy and small-treed savannas (‘Typical Cerrado’) in Brazil.

Methods In multiple permanent plots, we recorded all trees (focal plants) with a diameter at ground level > 10 cm, and focused on those species with the highest biomass and stem density. We identified and measured the height and diameter of all plants at least 5 cm tall within a 3 m range of these focal plants and derived structural and diversity parameters. We also collected soil samples and measured microenvironmental parameters, including litter layer, grass cover and soil surface temperature. Then we compared all environmental and vegetation variables with equivalent measurements made in open areas away from the focal plant crowns. We classified all species identified according to their preferred environment (forest, generalist and savanna).

Results Focal plants alter the microenvironment under their crowns, reducing soil surface temperature and grass cover and increasing the litter layer, soil organic matter, and soil nutrient content. These conditions facilitate the increase in species richness, density, and aboveground biomass accumulation of juveniles and adults of key forest and generalist tree species.

Conclusion By changing microenvironmental conditions these trees act as nurse plants, promoting the formation of islands of plant diversity. This process favors encroachment by woody plants typical of forests, leading to the woody encroachment of savanna areas.

Typical Cerrado

facilitation

ecological succession

nurse plant

species richness

aboveground biomass

The mechanisms of ecological succession in ecotone ecosystems are not fully understood, especially in the transition areas between large tropical biomes, such as the Amazon and the Cerrado. These tropical transitional systems tend to be highly dynamic, with potential for rapidly changing floristics and vegetation structure (Elias et al. 2019; Marimon et al. 2014; Morandi et al. 2015; Passos et al. 2018). Transformation from open savanna to more tree-dominated systems can occur due to edaphic and microclimate changes resulting from complex interactions (e.g., positive interactions and competition) between plant species, both at the community level and within the biome itself (Butterfield et al. 2010, Callaway and Walker 1997; Morandi et al. 2015; Passos et al. 2018). Among these interactions, competition is defined by the ability of individuals to obtain resources or prevent other individuals from obtaining resources (Aschehoug et al. 2016), while facilitation involves plants modifying key local environmental conditions (Connell and Slatyer 1977; Franks 2003; Yarranton and Morrison 1974), such as microclimate and soil fertility, so that they favor the establishment of other individuals and plant species.

Both competition and facilitation act simultaneously and are important in the formation, evolution, and functionality of plant communities (Aschehoug et al. 2016; Butterfield et al. 2010), such as that occurring in the Cerrado-Amazon ecotone (hereafter CAE). The vegetation of the CAE is both ‘hyperdynamic’, i.e. undergoing a high temporal turnover of species and individuals (Marimon et al. 2006; 2014), and is very heterogeneous floristically, both for forest and savanna (Elias et al. 2019; Morandi et al. 2015; Passos et al. 2018). A number of studies carried out in the CAE have detected clear changes in species composition and vegetation structure, as well as environmental changes caused by rapid forest-vegetation succession in savannas (Morandi et al. 2015; Passos et al. 2018; Ratter 1992), referred to here as woody encroachment. The succession process can promote an increase in the density of individuals, aboveground biomass, and species diversity (Morandi et al. 2015; Passos et al. 2018; Ratter 1992). However, these changes remain poorly explored (e.g. Staver et al. 2011), especially in tropical soil and climatic conditions.

At larger region, continental, and global scales, these structural and environmental changes in arboreal vegetation can be driven by climatic fluctuations, with hot and humid periods favoring the advance of forest vegetation over the savanna (Mayle et al. 2007; Ratter 1992). In South America these processes are largely driven by movements in the Intertropical Convergence Zone that respond to continuous climate change over the millennia driven by long-term orbital drivers (Mayle 2000). Given this, it is expected that the forests in contact with the savannas in southern Amazon will occur in a state of permanent tension with each other. Significant temporal changes (e.g., Marimon et al. 2006; Ratter 1992), such as plant encroachment and forest advance over the savanna during periods of more favorable climate (Morandi et al. 2015; Passos et al. 2018), are likely even in the absence of anthropogenic changes.

On the other hand, at the very local scale, such changes may occur due to alteration in the environment caused by tree individuals (Ratter 1992). In these models, the facilitation process comes into play (Connell and Slatyer 1977), in which tree species can provide significant microenvironmental changes permitting the arrival and rapid establishment of other species (Celentano et al. 2011; Martins and Rodrigues 1999; Oliveira et al. 2016; Yarranton and Morrison 1974; Valadão et al. 2016Zahawi et al. 2013). Thus, these tree species trigger the succession and, consequently, plant encroachment, which can often be remarkably rapid (Marimon et al. 2014; Morandi et al. 2015; Passos et al. 2018).

These ecological successional processes in savanna vegetation, such in the South American Cerrado, can also lead to large spatial variation at any one point in time including gradients (Ribeiro and Walter 2008) from more open to more dense areas (Durigan and Ratter 2006; Marimon et al. 2006;2016; Ratter 1992). In this case, different stages of succession coexist under the same climatic conditions, with disturbances and stochastic events helping to determine locally unstable community patterns over time (Parker 1997). This idea is consistent with the concept of ‘climax-gradient’, where there is a spatial continuity of different types of communities (physiognomic gradient), varying according to the availability of resources and the frequency of disturbances (environmental gradient) (Elias et al. 2019; Henriques 2005).

The availability of resources, such as the incidence of light and the accumulation of organic matter and nutrients in the litter layer, and the occurrence of disturbances, such as fire and the opening of clearings, are key determining factors that shape the physiognomic gradient to become more savanna-like or more forest-like (Ratter 1992; Ribeiro and Walter 2008). On the other hand, in the process of temporal succession, this entire relationship among vegetation, environment, and disturbances can also work to form a “temporal gradient of phytophysiognomies” (Henriques 2005). These mechanisms act simultaneously, determining how the process of ecological plant succession plays out (Aschehoug et al. 2016; Butterfield et al. 2010) and their particular temporal dynamics. For example, in the absence of disturbance, an Open Cerrado (‘Cerrado Ralo’) area can be gradually colonized by new tree individuals and become increasingly thicker, to the point that it turns into the next phytophysiognomy of the gradient, i.e., Typical Cerrado.

Here, we aim to describe and understand at the local scale the natural woody encroachment process of a savanna vegetation, ‘Typical Cerrado’, in the Cerrado-Amazon ecotone, and particularly the role of individual trees in generating a cascade of successional responses. We assessed plant encroachment in areas influenced by tree crowns and analysed their impact on microenvironmental climatic and edaphic conditions compared to areas without such crown influence. Based on published work and our initial observations, we formulated the following hypotheses concerning potential facilitative processes supported by the largest plants in the savanna: 1) Large focal plants decrease soil surface temperature and grass cover, and increase the litter layer and soil organic matter content (SOM) in the area under their crown's influence; 2) Due to these altered microenvironmental conditions, under focal plant canopies there is a higher density of individuals, aboveground biomass, and species richness of different development stages (young and adult) than in open areas; 3) That favor the higher establishment and associations with forest species in density, species richness and aboveground biomass than in open areas.

Study area and data collection

We carried out the present study in Typical Cerrado areas in the municipalities of Canabrava do Norte (-51.6895, -11.2396), Ribeirão Cascalheira (-51.770, -12.819; -51.768, -12.824; -51.766, -12.835), and Nova Xavantina (-52.352, -14.708; -52.350, -14.700), in the eastern region of the state of Mato Grosso, in the transition between the Cerrado and Amazon Biomes (Fig. 1). These sites are in a region with a climatic gradient from 1400 to 1800 mm per year and they are representative in Cerrado-Amazon ecotone (Marimon et al., 2006; 2014). Typical Cerrado is a savanna vegetation characterized by small trees with a canopy cover between 20 and 50% and average height ranging from 3 to 6 m, spaced over an extensive herbaceous cover (sensu Ribeiro and Walter, 2008).

Fig. 1 Geographic location of Typical Cerrado areas assessed in the present study in the municipalities of Canabrava do Norte (●), Ribeirão Cascalheira (▲), and Nova Xavantina (■), in the Cerrado-Amazon ecotone, Mato Grosso State, Brazil

Woody vegetation sampling

We delimited five permanent plots (1 ha; 100 x 100 m) of Typical Cerrado, distributed among the municipalities of Canabrava do Norte (one plot), Ribeirão Cascalheira (two), and Nova Xavantina (two) in the eastern region of Mato Grosso State, Brazil (Fig. 1). In each plot, we selected 12 individuals of most abundant tree species with higher values of density, basal area, and diameter at 30 cm above ground level (DGL_30cm) > 10 cm, which we denominate as potential ‘focal plants’ due to their structural dominance and hypothesized environmental and biological influence. Around the stem of each, we considered the area of influence as a 3 m radius circle (28.3 m²) from the point of stem emergence from the soil (Fig. 2a). We sampled all adult (DGL_30cm> 5 cm) and juvenile woody individuals (height > 10 cm and DGL_30cm <5 cm) around focal plants. We sampled juveniles in 1-m² subplots randomly distributed in the areas under the influence of focal plants. Systematically, in open areas without any environmental influence of focal plants, we established another 12 points in each plot, using as base a plant with DGL_30cm < 10 cm (Fig. 2b) and applied the same protocol as used for focal plants.

We classified all species sampled according to their preferred site (vegetation) of occurrence: forest, savanna, or generalist (when it occurs in both), based on the empirical experience of the authors and the specialized literature (Mendonça et al. 2008). We estimated grass cover using the cover percentage method (Fournier 1974) within 1-m² subplots delimited around focal plants (3 m radius). In October 2014 (end of the dry season), we sampled adult individuals, and in January 2015 (peak of the rainy season), we sampled juvenile individuals and grass cover.

Fig. 2 Schematic diagram of locations with the presence of focal plants and their area of influence (A) and open areas (B), in Typical Cerrado areas in the Cerrado-Amazon ecotone, Mato Grosso State, Brazil. 1. Focal plant; 2. Adult woody individual (DGL_30cm > 5 cm); 3. Juvenile woody individual (height> 10 cm and DGL_30cm <5 cm); and 4. Grass cover

Sampling of microenvironmental parameters

In the areas under the influence of nurse plants and open areas, we measured the soil surface temperature and litter layer. We also collected soil samples for physical (granulometry) and chemical analysis (soil organic matter - SOM and macronutrients). We determined soil surface temperature values at four random points using a digital infrared thermometer, always at times with high solar intensity (between 11:00 and 15:00). We collected and measured litter layer samples at four random points with the Marimon-Hay collector-meter (Marimon Junior and Hay 2008). We deposited the litterfall samples in an oven with forced air circulation at 80 °C until they reached constant weight and then weighed them on a precision scale to obtain the dry weight. We estimated litter layer dry weight per hectare (Mg ha^-1), following Marimon-Junior and Hay (2008) and Honorio-Coronado and Baker (2010). In addition, we collected 0-15-cm deep soil samples for routine physical (granulometry) and chemical analysis (organic matter and macronutrients) (Embrapa 1997).

Data analysis

We estimated the aboveground dry biomass (DB) using the equation proposed for sensu stricto Cerrado areas (DB = 0.49129 + 0.02912 * DGL * height) (Rezende et al. 2006). To compare biotic (aboveground biomass, species richness, density of individuals, and species vegetation preference) and abiotic parameters (litter layer, soil organic matter content, grass cover) between the areas under the influence of focal plants and open areas, we used ANOVA with permutations, available in the lmPerm package (Wheeler and Torchiano 2016), in the R 3.3.1 program (R Core Team 2016). To verify the degree of species association in the areas under the influence of focal plants and open areas, we used the indicator species analysis - IndVal (Dufrêne and Legendre 1997) included in the labdsv package (Roberts 2016).

We used generalized linear models (GLM) (Bolker et al. 2009) to test the effect of predictor variables (temperature, litterfall, grasses, organic matter, macronutrients, pH, Al, and H + Al) on species richness, biomass, and density of individuals. First, we tested a full model with all predictor variables, but due to the high variance inflation factor (VIF) observed for K and Ca, we excluded these two variables from the models. We adopted a VIF below 10 (Quinn and Keough 2002) and automatically selected the variables derived from soil parameters, where only magnesium (Mg) showed VIF above 5. We considered the importance of variables based on the literature to avoid the exclusion of important variables. Therefore, we maintained temperature, litterfall, grasses, and organic matter in all models (Table S4). After GLM, we selected models using the “dredge” function of the MuMIn package (Barton 2009). The best models were those with a ΔAICc value < 2 (Burnham and Anderson 2002). We checked model assumptions using a graphical analysis of the residues. All analysis and graphics were performed in the software R 3.3.1 (R Core Team, 2016) at a 5% significance level.

Areas close to focal plants had a microenvironment more favorable for the establishment of other plants, showing the facilitative potential of the large, focal plants. These conditions differed significantly from those of open areas (Fig. 3, Table S1), corroborating our first hypothesis. The average soil surface temperature was much higher in open areas, with a difference of approximately 20°C (Fig. 3, Table S1). Likewise, grass cover percentage was five times higher in open areas (Fig. 3, Table S1). Litter layer mass (Fig. 3, Table S1), soil organic matter (SOM) content, and cation exchange capacity (CEC) were all also greater near to focal plants than in open areas (Table S2).

Figure 3 (a) Variation in media soil surface temperature (°C), (b) litter layer mass (Mg ha^− 1), and (c) grass cover (%) in the areas under the influence of focal plants (blue) and open areas (white) in Typical Cerrado areas in the Cerrado-Amazon ecotone, Mato Grosso State, Brazil

GLM models showed that temperature and grass cover were negatively correlated with the density of individuals and species richness (Fig. 4, Table S4). The macronutrients Mg and P were positively correlated with the aboveground biomass of the trees (Fig. 4, Table S4). Soil aluminium content and pH were positively associated with the density and aboveground biomass of woody plants, and negatively with species richness (Fig. 4, Table S4).

Figure 4 Correlation of environmental parameters with species richness, density, and aboveground biomass of woody plants in a Typical Cerrado area in the Cerrado-Amazon ecotone, Mato Grosso State, Brazil. Dots represent the coefficients of GLM models presented in Table S4. Blue and red bars indicate the CI (95%). Asterisks represent significant p-values: *p < 0.05, ** p < 0.01, and *** p < 0.001

The density of adult individuals around focal plants showed a higher density of stem (about 35%) in relation to open areas (Table S1). When we compared the density and the richness of juvenile with adult plant species in each environment (around focal plants and in open areas), we found higher values for juvenile individuals in both environments. We also observed a higher density of adult individuals around focal plants than in open areas (Fig. 5a, b). The aboveground biomass values of adult woody plants were twice as great around focal plants than in open areas (Fig. 5c, Table S1).

Figure 5 Variation in woody plant according total species richness, density of individuals, and aboveground biomass (a-c) and each woody species’ preferred environment (forest: green; generalist: brown; or savanna: red) (d-f) in areas bearing focal plants (FP) and open areas (OA) in white. Developmental stage juvenile are in light colors and adult in dark colors in Typical Cerrado areas in the Cerrado-Amazon ecotone, Mato Grosso State, Brazil

In general, forest species had higher density (66.3%), species richness (63.6%), and aboveground biomass (84.7%) within 3 m of focal plants than further away (Table S1). Regarding the stage of development (juvenile and adult), forest species showed twice as high values of density, species richness, and aboveground biomass around focal plants than open areas (Fig. 6, Table S1). We also observed that several species classified as forest or generalist species occurred is quite frequently around focal stem as, for example, Emmotum nitens, Tachigali vulgaris, Roupala montana, Hirtella glandulosa e Matayba guianensis. On the other hand, only Davilla elliptica was most frequently recorded in open areas (Table S3).

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.

We found that focal trees in savanna environments in central South America induce substantial local environmental change including markedly decreased soil surface temperature and grass cover, as well as increased shading, litter layer, soil organic matter content, and cation exchange capacity. These factors contribute to the facilitative formation of islands of diversity by nurse plants, with the establishment of generalist (Tachigali vulgaris) and forest trees (Emmotum nitens and Hirtella glandulosa) within savanna environments. The values of aboveground biomass, litter layer, and soil organic matter content recorded under nurse plants are similar to those reported for forests in the Cerrado-Amazon ecotone, such as the dense woodland (Cerradão). The succession mechanisms described here reveal that areas with typically savanna vegetation are in the process of encroachment, showing a natural ecological succession towards a more forest-like environment, possibly a dense woodland. This process occurs because nurse plants initially create conditions for local densification in the area under their influence, and then promote expanded changes that favor widespread colonization in open vegetation areas.

Funding

The CAPES (Coordination for the Improvement of Higher Education Personnel) and FAPEMAT (Research Support Foundation of the State of Mato Grosso) to grant scholarships. The CNPq (National Council for Scientific and Technological Development), Process 403725/2012-7 and 441244/2016-5, and FAPEMAT - Process 164131/2013, funded the PELD Project: Cerrado-Amazon Forest Ecotone: ecological and socio-environmental bases for conservation (stages II and III).

Competing Interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Author Contributions

FBP, BSM, and PSM conceived the hypotheses and designed the study. FBP, BSM, PSM, JXN, FE, ECN, and BHMJ collected the data. FBP, PSM, CCV, FE, and ECN analyzed the data and wrote the manuscript. FBP, BSM, PSM, CCV, FE, ECN, JFR, and OLP discussed the results and contributed to the writing of the paper.

Data availability statement

We understand and consider important make the data available. But the datasets generated during and analyzed during the current study are not publicly available due there’s other researches being developed with the same datasets. Nevertheless, we made available the table S1 in supporting information with mean and standard deviation of all the values and minimum and maximum values at each sampling point of all variables.

Thank you for your consideration in reviewing and we are available for any explanations.

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Savanna woody encroachment in the Cerrado-Amazon ecotone

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