Seed rain
For seed rain, an average of 398 seeds was identified (15 collectors) per year and 25 seeds/m2 for the evaluated periods. A significant number of seeds was observed in November, with 992 seeds in the area (0.36 ha), about 62 seeds/m2 (Table 4). Seed rain contributes to the horizontal component of the area. Thus, the presence of 26 species were observed, with a total of 1,198 propagules collected in August, November, and February (Table 4).
Table 4
Species in the seed rain at Farm, Santana do São Francisco, Sergipe.
Family | Species | Habit | Ecological Group | Number of Seeds |
| Ago | Nov | Fev |
Anacardiaceae | Mangifera indica L. | arboreous | Exotic | - | - | 1 |
Schinus terebinthifolia Raddi. | arboreous | Pioneer | 19 | 23 | - |
Bignoneaceae | Tabebuia aurea (Silva Manso) Benth. & Hook. F. ex S. moore | arboreous | Pioneer | - | 3 | - |
Fabaceae | Anadenanthera colubrina (Vell.) Brenan | arboreous | Initial Secondary | - | - | 41 |
Cassia grandis L. f | arboreous | Initial Secondary | - | - | 9 |
Erythrina velutina Willd. | arboreous | Pioneer | 15 | - | - |
Inga vera Willd. | arboreous | Initial Secondary | 1 | - | - |
Libidibia ferrea var. Leiostachya (Benth.) L. P. Queiroz | arboreous | Climax | 26 | 13 | - |
Lonchocarpus sericeus (Poir.) Kunthex DC | arboreous | Initial Secondary | - | 746 | 24 |
Fabaceae sp.1 | - | - | - | - | 2 |
Fabaceae sp.2 | - | - | - | 3 | - |
Euphorbiaceae | Euphorbiaceae sp. | - | - | - | 2 | - |
Lamiaceae | Vitex rufescens A. Juss | arboreous | Climax | 10 | 4 | - |
Myrtaceae | Psidium guianense SW. | arboreous | Initial secondary | - | 78 | - |
Rhamnaceae | Ziziphus joazeiro Mart. | arboreous | Late secondary | 2 | 1 | - |
Rubiaceae | Genipa americana L. | arboreous | Climax | 45 | - | - |
Not identified | sp. 1 | | | - | 24 | - |
sp. 2 | | | - | 3 | - |
sp. 3 | | | 1 | 1 | - |
sp. 4 | | | 1 | - | - |
sp. 5 | | | - | 90 | - |
sp. 6 | | | - | 1 | - |
sp. 7 | | | 2 | 2 | - |
sp. 8 | | | - | - | 2 |
sp. 9 | | | - | - | 3 |
Total seeds* | | 122 | 992 | 82 |
Estimated seeds per m2 | | 8 | 66 | 5 |
Estimate of seeds in the sample area ** | | 28,467 | 289,333 | 19,333 |
* Sampled area = 15 m2 (collector area 1m2 x 15 collectors); ** planted area: ≅3500 m2 |
Fourteen species were identified (Fig. 2), three at the family level, and the remaining without identification due to the lack of information. The unidentified propagules represent only 11% of individuals.
The density in seed rain was 25 seeds/m2. These values differ from those found in other works in the Atlantic Forest. In a deciduous forest remnant of 560 ha, a density of 1,350 seeds/m2 was reported (Sccoti, 2011).
Eight botanical families were observed in the collected samples, emphasizing the Fabaceae family with remarkable diversity in species (08) and Anacardiaceae (02). The other families presented only one species each (Table 4). The highest number of seeds produced was for Lonchocarpus sericeus (Poir.) Kunthex DC. The occurrence of the Craibeira (Tabebuia aurea (Silva Manso) Benth. & Hook. F. ex S. Moore) in the area was probably due the process of introduction via dispersion since it was not initially used in the area.
There were species of different groups: pioneers, early secondary, late secondary, and climax. The initial and climax secondary species stand out, with 890 and 107 individuals, respectively.
All identified species are arboreal. This attribute, associated with the low presence of pioneers, permits to infer the current situation of the implanted forest. Considering that these species have already fulfilled their ecological role of providing better conditions for secondary species to develop, as shading; the absence of pioneers and the significant presence of secondary and climax species as conclusion the area is in the advanced stages of the succession.
Due to the small number of pioneer species propagules in the seed rain in the project's initial phase, the species probably began a physiological decline due to the shading provided by the climax species. In this course, these species fulfilled their ecological function in the area. Also, pioneer species have restricted seed dispersal when subjected to adversity due to genetic and dispersal factors (Lowe et al., 2018).
During the development of the monitoring, anthropic interferences were observed, such as broken and remotion of collectors.
Seed Bank
Among the three regeneration strategies used, the seed bank had the lowest number of species (Table 5). Cassia grandis L. f., Erythrina velutina Willd., Libidibia ferrea var. leiostachya (Benth.) L. P. Queiroz and Lonchocarpus sericeus (Poir.) Kunthex DC was identified in the Fabaceae family. Three species were not identified (Table 5).
Table 5
Species in seed bank of the rainy and dry seasons in area in Santana do São Francisco, Sergipe.
Family | Species | habit | Ecological Goup | Quantity of seeds per season |
Rainny | Dry |
Fabaceae | Cassia grandis L. f | arboreous | Climax | - | 3 |
| Erythrina velutina Willd. | arboreous | Pioneer | 1 | 1 |
| Libidibia ferrea var. Leiostachya (Benth.) L. P. Queiroz | arboreous | Climax | 15 | - |
| Lonchocarpus sericeus (Poir.) Kunthex DC | arboreous | Initial Secondary | - | 1 |
Indefined | Sp. 1 | | | - | 1 |
| Sp. 2 | | | - | 1 |
| Sp. 3 | | | - | 2 |
16 | 9 | |
21 | 12 | |
74,550 | 42,000 | |
*Sampled area = 0.75 m2 (collector area 0.0625 m2 x 12 plots); **Planted area: ≅ 3,500 m2. |
Differences were observed in the number of individuals (Fig. 3-B) and species. The density in the rainy season was 21 seeds/m2, 64% of total seeds sampled in both periods, and there was a reduction to 12 seeds/m2 in the dry season. Four species are arboreal; among them, two were climaxes, one initial secondary and one pioneer. Leiostachya and Cassia grandis showed higher values r of individuals, density, and frequency (Fig. 3-A).
In this method, the soil seed bank proved self-renewing the area and presents essential species in this process. It is worth mentioning that the recovered area is relatively new, and the species found in the seed bank reflect the presence of adults used during the beginning of the restoration. It is still possible to observe that the composition reflects the fulfillment of the ecological role of the pioneer species, like E. velutina.
Therefore, a lower presence of pioneer species is due the replacement succession by the climax and late secondary species, which have been the majority. The species primarily were on the seedling bank, where they developed under the canopy of the pioneer plants until they reached the highest strata of the forest (Miranda, 2009; Almeida, 2016).
Seedling Bank
In the seedling bank, 170 individuals were identified (106 of rainy seasons and 64 of dry seasons), which correspond to 28 botanical families (Table 6).
Table 6
Species in the seedling bank in restored area in Santana do São Francisco, Sergipe.
Family | Species | Habit | Ecological Goup | Quantity |
Rainny | Dry |
Acanthaceae | Ruellia bahiensis (Nees) Morong. | herb | Pioneer | 12 | 7 |
Anacardiaceae | Mangifera indica L. | arboreous | Exotic | - | 1 |
Apocynaceae | Matelea ganglinosa (Vell.) Rapini | climbing habit | Pioneer | 1 | - |
Asteraceae | Bidens pilosa L. | herb | Pioneer | 1 | - |
Boraginaceae | Varronia curassavica Jacq. | shrub | Initial Secondary | 1 | 3 |
Cannabaceae | Celtis iguanaea (Jacq.) Sarg. | shrub | Pioneer | 3 | 5 |
Capparaceae | Cynophalla flexuosa (L.) J. Presl | shrub | Initial Secondary | 3 | 6 |
Chrysobalanaceae | Licania tomentosa (Benth.) Fritsch | arboreous | Not Classified | - | 3 |
Cyperaceae | Cyperus distans L. | herb | Pioneer | 4 | - |
Cyperus laxus Lam. | herb | Pioneer | 1 | - |
Cyperaceae | Rhynchospora nervosa (Vahl) Boeckeler | herb | Pioneer | 2 | - |
Euphorbiaceae | Caperonia palustris (L.) A.St.-Hil. | herb | Not Classified | 1 | - |
Croton blanchetianus Baill. | arboreous | Pioneer | - | 2 |
Croton heliotropiifolius Kunth | shrub | Pioneer | 2 | - |
Chamaecrista ramosa (Vogel) H.S.Irwin & Barneby | | Pioneer | 1 | - |
Fabaceae | Crotalaria retusa L. | herb | Pioneer | 1 | - |
Crotalaria stipularia Desv. | herb | Pioneer | 2 | - |
Bauhinia cheilantha (Bong.) Steud. | shrub | Pioneer | 1 | - |
Inga vera Willd. | arboreous | Initial Secondary | 3 | 1 |
Machaerium hirtum (Vell.) Stellfeld | arboreous | Initial Secondary | 3 | 2 |
Senegalia tenuifolia (L.) Britton & Rose | shrub | Climax | 5 | - |
Senna splendida (Vogel) H.S.Irwin & Barneby | shrub | Not Classified | 3 | - |
Stylosanthes scabra Vogel | herb | Pioneer | 1 | - |
Lamiaceae | Aegiphila verticillata Vell. | shrub | Not Classified | - | 1 |
Vitex rufescens A. Juss | arboreous | Climax | - | 9 |
Loganiaceae | Spigelia anthelmia L. | herb | Pioneer | 1 | - |
Lygodiaceae | Lygodium venustum Sw. | herb | Not Classified | 3 | - |
Malvaceae | Pavonia communis A.St.-Hil. | herb | Not Classified | 6 | - |
Menispermaceae | Cissampelos glaberrima A.St.-Hil. | climbing habit | Not Classified | 1 | 1 |
Myrtaceae | Campomanesia aromatica (Aubl.) Griseb. | arboreous | Climax | 1 | 1 |
Campomanesia dichotoma (O.Berg) Mattos | arboreous | Not Classified | - | 2 |
Eugenia ligustrina (Sw.) Willd. | arboreous | Not Classified | 1 | - |
Psidium guajava L. | arboreous | Late Secondary | 1 | - |
Psidium guineense Sw. | arboreous | Climax | 1 | - |
Orchidaceae | Oeceoclades maculata (Lindl.) Lindl. | herb | Pioneer | 3 | - |
Poaceae | Leersia hexandra Sw. | herb | Not Classified | 9 | - |
Urochloa fusca (Sw.) B.F.Hansen & Wunderlin | herb | Pioneer | 1 | - |
Polygonaceae | Coccoloba ramosissima Wedd. | shrub | Pioneer | - | 1 |
Rhamnaceae | Ziziphus joazeiro Mart. | arboreous | Late Secondary | 5 | 8 |
Rubiaceae | Borreria verticillata (L.) G.Mey | herb | Pioneer | 5 | - |
Genipa americana L. | arboreous | Climax | 4 | 1 |
Guettarda angelica Mart. ex Müll.Arg. | shrub | Pioneer | 1 | - |
Tocoyena formosa (Cham. & Schltdl.) K.Schum | shrub | Pioneer | - | 3 |
Rutaceae | Ertela trifolia (L.) Kuntz | herb | Initial Secondary | - | 1 |
Salicaceae | Casearia lasiophylla Eichler | shrub | Pioneer | 2 | - |
Sapindaceae | Allophylus quercifolius (Mart.) Radlk. | shrub | Not Classified | - | 1 |
Paullinia pinnata L. | climbing habit | Initial Secondary | 2 | 3 |
Urticaceae | Urtica dioica L. | herb | Not Classified | 1 | - |
Verbenaceae | Lantana camara L. | shrub | Initial Secondary | 5 | 2 |
Violaceae | Pombalia oppositifolia (L.) Paula-Souza | herb | Not Classified | 2 | - |
Total seedlings sampled * | | | 106 | 64 |
Estimate of seeds per m2 Estimation of seeds in the planted area ** | | | 9 | 5 |
| | 30.917 | 18.677 |
*Sampled area = 12m2 (collector area 1m2 x 12 plots); **Planted area: ≅ 3500 m2 |
Euphorbiaceae and Fabaceae stood out with six species each, followed by Myrtaceae (05) and Rubiaceae (04).
These families represented 42% of the specimens in the area. The Fabaceae has been increasingly reported due to the increase in its use in areas of natural regeneration (Fernandes et al., 2018; Silva, 2019). Such species have a high ecological impact and favor the choice of individuals in recovery projects. Its ability to develop root nodules as a symbiosis with atmospheric nitrogen-fixing bacteria and mycorrhizal fungi promotes nitrogen fixation in the soil, accelerating plant establishment and growth (Nogueira, 2012; Rodrigues et al., 2016).
Forest's tree-shrub are represented by 28 families (57%), and many individuals were on the floor. Herbs represented 19 families, and 64 seedlings were identified.
There was a high species diversity during the rainy season; 106 specimens, with an average density of ≅ 9/m2, in contrast to 5 seedlings/m2, during the dry period. These results differ from those reported in other areas in Sergipe, where the regenerants had a lower average density of 1.86 seedlings/m2 and 3.77 seedlings/m2 for the rainy and dry seasons, respectively (Silva, 2019).
For the rainy season, dominance (absolute and relative) and importance (IVI) was seen for Cynophalla flexuosa (L.) J.Presl, Genipa americana L., Inga vera Willd, Senna splendida (Vogel) H.S.Irwin & Barneby, Ziziphus joazeiro Mart., Eugenia ligustrina (Sw.) Willd. (Annex 1). For the same index in the dry period, the species that stood out were Mangifera indica L., Paullinia pinnata L., Z. joazeiro, Vitex rufescens A. Juss, Varronia curassavica Jacq., Ruellia bahiensis (Nees) Morong (Appendix 2).
In the seedling bank, the species G. americana stood out for density and relative frequency with the highest rates in the rainy season.
Shannon's (IDS) and Pielou's (P) diversity index differed between seasons. The IDS and P for the rainy season were 3.34 and 3.25, higher than in the dry season, where IDS = 2.13 and P = 2.04. Thus, the rainy season presents higher diversity of specimens.
Despite the farm limits being protected with a fence to avoid human and animal interference, such actions interfere with the local dynamics. The main human interferences were collection of fruits, woody suppression even of the collectors for domestic purposes, and the occurrence of criminal forest fires. These activities trigger impacts on the farm's forest restoration process. The gain in terms of the horizontal and vertical structure of the area is evident. Recompositing of environments and features of an area of forest inclines us to assess whether the benefits went beyond the visual. For this purpose, a chemical analysis of the soil was conducted to verify if the recovery action changes the soil condition.
Soil Attributes
Soil attributes differed, as seen in Fig. 4. The pH increased (from 5.10 to 5.85), showing a reduction in acidity. In degraded areas, the reduction in soil acidity led to benefits such as a decrease in the mobilization of toxic elements such as aluminum, arsenic (Guimarães et al., 2017) and magnesium (Teran et al., 2020). pH between 5.8 to 6.2 is an optimal range promoting availability of essential nutrients for the plant. In addition, pH above 5.5 indicates that aluminum is in its precipitated form, completely insolubilized, and without damaging the roots (Sobral et al., 2015).
Soil chemical properties differed between 2003 and 2021. There were improvements in soil fertility over time, indicating a positive effect on soil attributes. No adverse effects of regeneration on the chemical and physical attributes of the soil were observed after 18 years of project implementation.
In areas of bauxite soil chemical attributes permitted significant contributions to forest restoration with increased soil quality and decreased elements such as aluminum (Xue, 2019).
The value of organic matter was not measured in the initial phase, but in 2021 its content was classified as medium (1.58%). Organic matter is the primary source of soil nutrients (Liu et al., 2016) and is directly affected by plant species diversity, composition, and distribution (Anwar et al., 2019). Soil chemical characteristics are influenced by the quality of the decomposed material from the litter produced by individuals in each area (Oliveira et al., 2019).
The values of exchangeable bases (sodium, potassium, calcium + magnesium), SB, effective and potential CTC, PST, and V% increased after 19 years. Thus, the area in this study overcomes the changes suffered and is re-established, favoring excellent vegetation development. It can be seen by the increase in exchangeable bases (Sobral et al., 2015). Reducing soil acidification reduces the leaching of exchangeable cations (Lu et al., 2014), and higher values for exchangeable bases such as calcium and magnesium can be identified (Yan et al., 2020). It indicates that the studied area presents higher availability of nutrients for the plants after re-establishing the forest restoration.
The effective CTC went from medium to high levels over the years and the potential CTC, increased, remains in the medium range (Sobral et al., 2015). Evaluations of organic matter, CEC, and pH are essential to understand the availability of storage capacity of cations, the concentration of ions, and the presence of toxic substances in the soil. The CTC in the soil makes it possible to know its capacity to retain cations and facilitate the absorption of nutrients by plants (Coelho et al., 2011). High CTC indicate balanced fertility (Silva et al., 2015), and low values indicate that the soil has little capacity to retain cations in exchangeable form (Ronquim, 2010).
When using soil chemical variables as abiotic indicators in a transition region between the Atlantic Forest and Caatinga, researchers observed that they are efficient in indicating changes in soil attributes over the ecological succession process (Novak et al., 2017).
The potential acidity (Hydrogen + Aluminum) decreased, a fact that should be seen as positive since this parameter is linked to the increase in pH (Sobral et al., 2015), and its reduction over the years indicates that the species present in the area have better growth conditions when compared to the beginning of the implantation (Ferreira et al., 2012). In tropical riparian forests, the soil's chemical attributes and the intensity of the decomposition process of organic matter are correlated with the vegetation's structure, therefore the composition and forest diversity (Soares et al., 2020).
There was a restructuring of the soil physical condition, where the clay and silt increased, and the sand content decreased. Nitrogen-fixing species can increase clay and silt content and reduce sand content (Li et al., 2022) making soil particles more uniform (Zhang et al., 2019a). The results expressed for granulometry prove that the restoration reduced the sand content and increased the acceptable particle content.
The Landscape Scenarios
The results in Fig. 5 demonstrate that the landscape was changed over 18 years. The areas that were altered in 2002 were restored and 100% stabilized.
Within the area, only the classes of dense vegetation and altered areas were identified, with the other classes described in the methodology. The average Kappa index (0.84) indicates the efficiency as excellent.
During the restoration of the first four years (2002–2006), an increase of 97.81% in vegetation was observed. In 2010, the area reached 100% of its coverage with dense vegetation, maintained until 2020 (Fig. 6). In Fig. 6, the area and adjacent were enriched by vegetation. Therefore, the reforestation applied in 2003 favored forest connectivity. The process of artificial or active restoration increases the diversity of forest species dynamically when compared to the natural method, without intervention, granting improvements in structural and ecological terms (Jayawardhane; Gunaratne, 2020). The insertion of forest species from vegetative propagules (seedlings and seeds) can reestablish functions such as gene flow and dispersion over time and favor ecosystem services (Cordeiro et al., 2019).
We evaluated the production of plant biomass and organic carbon (GPP) through estimates of the MODIS (Fig. 7). We observed that the flows of both variables showed a positive linear tendency (Fig. 7-B and C).
A decrease between 2002 and 2006 was observed to produce biomass and GPP. The reduction may be due to the high mortality of the species initially planted at the beginning. The gross primary production of organic carbon (GPP) continued to grow, while for biomass, there was another decrease between 2010 and 2015.
The reduction in biomass reflects the ecological succession process in the area where the pioneer species (short life cycle) begin to die, giving opportunity for secondary and climax species, which present slow growth. In areas under succession, a reduction number of pioneer species and their subsequent decline is expected (Chai; Wang, 2016).
GPP represents the ability to transform carbon dioxide into organic carbon through photosynthesis and depends on factors such as evapotranspiration (Zhao; Running, 2010; Collalti; Prentice, 2019). Biomass was estimated from the relationship of NPP and GPP, where the NPP/GPP ratio should be applied to measure total carbon at the ecosystem scale (Landsberg et al., 2020).
The Farm is in an area of riparian forest, defined as an APP. The APP was categorized in a disturbance stage (Torres et al., 2021). Therefore, interventions are an emergence. The lack of restoration actions in this region has shown severe consequences, where the degradation of forests contributed to the increase of suspended sediments in water bodies and alteration in the process of deposition of river sediments (Dompieri et al., 2020; Torres et al., 2021), as the absence of riparian vegetation that accentuates the marginal erosive processes (Holanda et al., 2021). The geospatial tools, such as satellite images to study the earth's surface, can detect changes in land use and cover over different temporal scales and make it possible to identify exploratory activities (Philogene; Ni-Meister, 2021).
A temporal analysis of land use and cover in Brazilian Biomes was constructed from Landsat archives for the last three decades (1985–2017), and the results showed that the country lost about 71 million hectares of natural vegetation (Souza et al., 2020). These tools are an essential data source for relevant environmental studies (Hansen et al., 2013). In addition, it facilitates the monitoring of the passive conservation and can be applied preventively and proactively to avoid environmental damages.
Monitoring environments in the restoration process should be included as one of the project's stages, as it can prevent situations that jeopardize co-benefits and how ecosystem services return to the local community (Hayward et al., 2021). It is possible to verify the connection among forest fragments and consequently maintenance of diversity. The remote sensing data for environmental monitoring consists of estimated results.
The biomass produced by an area undergoing restoration also influences the improvement of the soil's physical structure since it is the primary source of organic matter that promotes soil stability (Flores et al., 2008). The diversity of species benefits a more outstanding and varied litter and root biomass. It acts indirectly on soil properties, as it generates an increase in carbon inputs and activity of the micro and macro fauna of the soil that, consequently, promotes increased water holding capacity (Zhang et al., 2019b).
Reforestation with native species is one of the efficient ways to restore soil fertility, as this type of vegetation improves the soil's organic matter content, available nutrients, cation exchange capacity, increases biological activities, and improves physical soil conditions (Zhang et al., 2019b; Celentano et al., 2016). In regions with soils compacted, after 25 years of restoration with different forest species, it was observed that the chemical properties of the soil had full recovery (Jourgholami et al., 2019).
In riparian forests, soil fertility is related to the preservation of ecosystems, as its levels are influenced by the condition and composition of the local vegetation. The degradation alters soil fertility and triggers problems in the spontaneous development of plants (Celentano et al., 2016). Consequently, negatively influence the process of ecological succession and the resilience of the habitat. Soil analyses are of paramount importance to indicate the nutritional conditions of plants, allowing intervention through forest management to guarantee the continuity and functionality of ecosystems, especially in riparian forest areas, because of their ecological and social relevance.
Six years after the implementation of the restoration project, it was observed that the survival of the species planted in the initial phase was higher than 54%, and there was no difference (P ≤ 0.05) in growth and survival. At 12 years old, in this same area was an enrichment of 165 species, 134 genera, and 51 botanical families. Herbaceous species were predominant, with 74 species (44.8%), followed by 42 trees (25.5%), 33 shrubs (20%), and 16 vines (9.7%). The species presented a height from 3.26 and 8.05 m.
Active restoration, it is a method used in the project implementation in 2003, is seen as a silvicultural technique capable to improve the ecological succession and granting short and lon-term benefits to degraded environments, mainly concerning soil stability (Chaves, 2007; Ferreira et al., 2011).