Restoration of areas degraded by alluvial sand mining

Environ Monit Assess (2017) 189:120 DOI 10.1007/s10661-017-5852-3

Restoration of areas degraded by alluvial sand mining: use of soil microbiological activity and plant biomass growth to assess evolution of restored riparian vegetation Graziela R. Venson & Rosemeri C. Marenzi & Tito César M. Almeida & Alexandre Deschamps-Schmidt & Renan C. Testolin & Leonardo R. Rörig & Claudemir M. Radetski

Received: 22 June 2016 / Accepted: 15 February 2017 # Springer International Publishing Switzerland 2017

Abstract River or alluvial sand mining is causing a variety of environmental problems in the Itajaí-açú river basin in Santa Catarina State (south of Brazil). When this type of commercial activity degrades areas around rivers, environmental restoration programs need to be executed. In this context, the aim of this study was to assess the evolution of a restored riparian forest based on data on the soil microbial activity and plant biomass growth. A reference site and three sites with soil degradation were studied over a 3-year period. Five campaigns were performed to determine the hydrolysis of the soil enzyme fluorescein diacetate (FDA), and the biomass productivity was determined at the end of the studied period. The variation in the enzyme activity for the different campaigns at each site was low, but this

parameter did differ significantly according to the site. Well-managed sites showed the highest biomass productivity, and this, in turn, showed a strong positive correlation with soil enzyme activity. In conclusion, soil enzyme activity could form the basis for monitoring and the early prediction of the success of vegetal restoration programs, since responses at the higher level of biological organization take longer, inhibiting the assessment of the project within an acceptable time frame. Keywords Alluvial sand mining . Degraded riverbank . Riparian soil reforestation . Fluorescein diacetate hydrolysis . Plant biomass

Introduction G. R. Venson : R. C. Marenzi : A. Deschamps-Schmidt Laboratório de Conservação, Gestão e Governança Costeira, UNIVALI—Universidade do Vale do Itajaí, Rua Uruguai, 458, Itajaí, SC 88302-202, Brazil T. C. M. Almeida Laboratório de Ecologia de Comunidades, UNIVALI—Universidade do Vale do Itajaí, Rua Uruguai, 458, Itajaí, SC 88302-202, Brazil R. C. Testolin : C. M. Radetski (*) Laboratório de Remediação Ambiental, UNIVALI—Universidade do Vale do Itajaí, Rua Uruguai, 458, Itajaí, SC 88302-202, Brazil e-mail: [email protected] L. R. Rörig Laboratório de Ficologia, Universidade Federal de Santa Catarina, Campus Trindade, Florianópolis, SC 88040-970, Brazil

The coast of Santa Catarina State located in the south of Brazil has experienced a rapid transition from a natural to an urban landscape, in part due to the attraction of the bathing beaches in this region. The development of cities along the coast has had a negative impact on natural terrestrial and marine/estuarine areas, and social, cultural, economic, and political aspects have also been affected (Polette and Vianna 2006). This urban development has led to an increased demand for alluvial sand as a source of construction material. The high demand for sand has allowed small producers to enter this market without proper environmental management of their activities, a fact aggravated by a lack of stringent mining management guidelines, despite the 1988s Brazilian

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Federal Constitution, which establishes that anyone who exploits mineral resources must recover degraded areas. From the ecological point of view, the most important impact is on the functioning of environments with riparian vegetation, which will disturb the physical, chemical, and biological processes. These processes ensure the proper maintenance of the geomorphic and ecological systems in rivers, for example, the protection of riverbanks and bars against erosion, of host (micro)biological organisms in roots and of downed trees that allow nutrient cycling, all of these being necessary for the integrity and functioning of the aquatic ecosystem as a whole (Langer and Kolm 2001). Thus, the uncontrolled exploitation of sand in a river basin gives rise to various environmental problems including deforestation and erosion in the riparian zone, river water quality degradation, river bed degradation, and encroachment into the river buffer zone (Collins and Dunne 1990; Langer 2003). In a general sense, each river or stream has its own unique set of geological, hydrological, climatic, and anthropogenic characteristics with their associated potential environmental impacts (Langer 2003). To address the various environmental problems, state authorities have demanded the implementation of a project for the recovery of areas degraded due to sand mining activities, aimed at ensuring that sand and gravel extraction is carried out in a sustainable way. Basically, the recovery of a degraded riparian area involves soil preparation (i.e., mechanical ploughing and fertilizer application), followed by the cultivation of pioneer species. Secondary and native species can then be cultivated later on. This basic project is in accordance with reports based on bibliographic surveys, where it is suggested that pioneer species are recommended for the initial recovery of degraded areas, while secondary and climactic species play a major role in area enrichment (Gris et al. 2012). In general, the classical biomass plant growth criterion (i.e., productivity) is used to assess the evolution of a restored riparian forest. This criterion reflects the response on the higher biological levels, but it takes a certain time to become measurable. In contrast, soil properties based on biological and biochemical activities have been shown to respond rapidly to small changes in the soil conditions. In this context, soil enzyme activity has been proposed as an appropriate indicator of soil quality due to its close relationship with the soil biology, the ease of measurement, and the rapid response to changes in soil management practices (Lee

Environ Monit Assess (2017) 189:120

1994; Pankhurst et al. 1997; García-Ruiz et al. 2008; Sofi et al. 2016). The hydrolytic enzyme activity measured as fluorescein diacetate (FDA) hydrolysis is representative of a pool of enzymes involved in organic matter decomposition and nutrient cycling, and thus, it reflects the microbial activity of the soil (Schnürer and Rosswall 1982; Adam and Duncan 2001; Schumacher et al. 2015). As a consequence, microbiological enzymatic activity could form the basis of reforestation project monitoring, since it can be used as a sensitive early indicator of changes induced by management practices, which can be correlated with biomass productivity during the early stage of the restoration process (Carlson et al. 2015). In a broader remediation management, others factors, as soil physical characteristics, as well as soil chemical composition, can be used to assess soil quality and remediation evolution, but this more complex approach will be more time-consuming and will increase costs of the remediation project. In this context, the objective of this study was to examine whether the soil microbiology can be used to assess the development of native and non-native plants during the initial restoration period. The relationship between the increase in the plant biomass growth and fluorescein acetate hydrolysis carried out by soil microbes was investigated at three sand mining sites involved in a restoration project and one reference site. All sites are located in the basin of the Itajaí-açú River along the center-north coast of Santa Catarina State. Some basic recommendations in terms of the potential use of the FDA hydrolysis method for the long-term management of sand mining activities are also provided.

Material and methods Site description, soil and plant biomass sampling procedure, and characterization The four experimental riparian sites are all located in the Itajaí-açú river basin in the Santa Catarina State (south region of Brazil). The program for the restoration of the degraded soil area was similar for the three sites, and one apparently undisturbed natural forest site was used as the reference site. The geographical coordinates (Datum horizontal WGS 84) of the sites are as follows: site 1 (PUN): 26°50′11.21″S 49°00′02.02″W; site 2 (FAN): 26°53′29.43″S 49°00′00.46″W; site 3 (HOR): 26°53′35.41″S 49°00′02.05″W; site 4 (BOS): 26°89′


27.04″S 49°00′01.33″W. Site 4 (BOS) is the native riparian forest that was used as the reference site, while the other three sites show signs of past soil degradation due to river sand mining. Ten soil samples of each site (top 10 cm) were collected in each of the five campaigns carried out in October 2013, in April and in October 2014 and in April and October 2015 according to a standardized methodology (EMBRAPA 1999). The ten samples from each site were mixed to compose a single sample. Therefore, five samples were generated for each site in a time series. The samples were kept at 4 °C until physico-chemical analysis. These samples were air-dried, passed through a 2-mm sieve before physicochemical characterization. The pH of a soil suspension in deionized water (1:1 w/v) was determined, as well as the clay, fertilizing elements and organic matter contents and the CEC values, since these are the most important parameters in terms of agronomic productivity. Metal analysis was carried out according to the APHA, AWWA, and WPCF (1995) methodologies, and other physicochemical parameters were measured according to published methodologies (EMBRAPA 1999). For the plant biomass growth measurement, three plots of 1 × 1 m were designated in October 2015, after assessing the topsoil vegetation of each site by analyzing visually the overall species richness and the abundance of three species (Cooke and Zack 2009). All topsoil vegetation present in each plot was harvested, weighed (wet weight), dried in an oven (7 days at 60 ° C), and weighed again (dry weight). Microbiological enzyme activity of the soil Five analytical campaigns to assess the microbiological enzyme activity in the soil at the four sites studied were carried out between October 2013 and October 2015. At each site, 10 soil plots were cleared of the topsoil vegetation, and the soil was sampled (top 10 cm). The soil sample was homogenized, and five sub-samples of 10 g (dry weight) from each site were analyzed to determine the FDA hydrolysis. Total hydrolytic enzyme activity was determined using the hydrolytic FDA method of Schnürer and Rosswall (1982), with slight modifications. Soil sub-samples were placed in 100-mL polycarbonate centrifuge tubes, and 40 mL of 30 mM phosphate buffer (adjusted to pH 7.5) was added. The tubes were shaken gently for 5 min. After which, 50 mL of a 2-mg/ L FDA solution in acetone was added. A further 24-h period of shaking was then applied before terminating

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the reaction through the addition of 20 mL of acetone. The test tubes were then centrifuged at 500 rpm for 15 min followed by filtration of the supernatant (Whatman 0.45 μm). The filtrate absorbance was monitored at 490 nm. The hydrolytic enzyme activity analysis was conducted in triplicate for each sub-sampled soil. Statistical analysis The correlation between the FDA hydrolysis (enzyme activity) and plant biomass productivity was established by the Pearson test. Statistical analysis for enzyme activity was carried out on a microcomputer using TOXSTAT 3.0 software. The data were analyzed by ANOVA applying the Tukey test (P ≤ 0.05) after verifying the normality (Shapiro-Wilk test) and homogeneity of variance (Hartley test) of the data.

Results Agronomic characterization of soil samples collected at the sites The results obtained from the physicochemical analysis of the soils collected at the different sites in all campaigns are summarized in Table 1. According to these results, sandy soils are prevalent in the restored areas. The SMP index was relatively high for all soil samples, while the organic matter content and CEC values were relatively low. From Table 1, there was no significant variation in the quantitative of organic matter (indirect indication of soil fertility), but there was significant variation in the enzymatic activity among sites, like we will see in Figs. 1 and 2. Soil enzyme activity for different campaigns at the same site The evolution of the enzyme activity of the soil samples over time was investigated, and Fig. 1 shows FDA hydrolysis results for the five campaigns carried out at the four sites. Site 1 (PUN) was characterized by insufficient management after implementation of the restoration project, and only grass species were able to colonize through natural regeneration.

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Table 1 Mean physicochemical characteristics of the soil samples collected from the different sites in each campaign (n = 5) Parameter

Site 1 (PUN)

Clay (%)

17.5 ± 1.7

7.8 ± 4.2

18.8 ± 9.3

20.8 ± 7.0

pH (water 1:1)

7.1 ± 0.3

7.3 ± 0.3

4.7 ± 0.1

5.7 ± 0.2

SMP index

7.2 ± 0.2

7.4 ± 0.2

6.6 ± 0.2

6.6 ± 0.1

Pvailable (mg/dm3)

11.5 ± 3.2

18.5 ± 4.8

14.9 ± 2.8

21.9 ± 6.6

Kexchangeable (mg/dm3)

78.0 ± 8.2

152.0 ± 24.7

34.5 ± 8.4

97.3 ± 17.5

Org. matter (%)

2.1 ± 0.3

1.9 ± 0.2

1.8 ± 0.2

1.7 ± 0.2

Al (cmolc dm3)

–

–

0.9 ± 0.2

–

Ca (cmolc dm3)

9.2 ± 0.8

4.9 ± 0.8

3.1 ± 0.3

4.9 ± 0.5

1.2 ± 0.3

0.4 ± 0.2

0.9 ± 0.1

1.8 ± 0.2

Mg (cmolc dm3) 3

Site 2 (FAN)

Site 3 (HOR)

Site 4 (BOS)

CEC (cmolc dm )

11.7 ± 0.8

6.6 ± 0.8

6.5 ± 0.5

9.1 ± 0.8

Exchangeable bases (meq 100 g soil−1)

10.5 ± 0.8

5.7 ± 0.9

6.3 ± 0.6

6.9 ± 0.7

SMP index Shoemaker, MacLean, and Pratt index

At site 2 (FAN), a non-exhaustive management strategy is applied, which allows the growth of grass species and only one native plant species.

In the case of the site 3 (HOR), the presence of several plants species was observed, some pioneers from natural regeneration and others which are planted

Fig. 1 Soil enzyme FDA hydrolysis activity along the 5 campaigns carried out at the four sites. a Site 1 (PUN); b site 2 (FAN); c site 3 (HOR); d site 4 (BOS)


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Fig. 2 Soil enzyme activity for FDA hydrolysis at the different sites

only one native plant species in the case of site 2, while at sites 3 and 4, a wide diversity of plants was present including some pioneering species (e.g., red honeywood (Alchornea triplinervia)), and native species such as the Brazilian pepper tree (Schinus terebinthifolia Raddi), uvaia (Eugenia pyriformis Cambess), race (Psidium cattleianum ), inga (Inga edu lis), ripe fruit (Campomanesia guaviroba), and others. It can be observed in Fig. 3 that both the wet and dry biomass increase under better management practices and the wet to dry biomass ratio is around 58%, with the exception of site 1 (PUN), where this ratio is around 50%. Knowing that FDA hydrolysis activity at the different sites is statistically different from each other (Fig. 2) and that dry biomass productivity was similar between sites 3 (HORT) and 4 (BOS) (Fig. 3), a cross-data can help to better define the relationship between the different measured parameters. Thus, Fig. 4 shows a statistically significant difference between the FDA abs/wet and dry biomass ratios for these two sites.

native species. At the reference, site 4 (BOS), the presence of various native plants species was observed. Soil enzyme activity results for the different sites A comparison of the results for the soil enzyme (FDA hydrolysis) activity at the different sites can be seen in Fig. 2. The Tukey test showed that the values shown in Fig. 2 for the FDA hydrolysis activity at the different sites are statistically different with respect to each other. Site 4 (BOS), which is the control site, showed the highest enzyme activity, while site 1 (PUN) showed the lowest soil microbial activity. Biomass productivity results for the different sites The results for the plant biomass productivity at the different sites can be seen in Fig. 3. As mentioned previously, the plant diversity varied according to the management strategy applied to the degraded areas. Grass species were observed at sites 1 and 2 along with

60

Fig. 3 Plant biomass productivity (kg/m2) at the different sites

g f

Biomass (kg m-2)

50

e

40 d c

30

c

Wet weight

b Dry weight

20

a

10 0 Site 1 (PUN)

Site 2 (FAN)

Site 3 (HOR)

Site 4 (BOS)


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Fig. 4 Ratios (abs units/kg/ m2 × 10−5) between FDA abs and wet and dry biomass at the different sites

20

e

18

Raos (abs units/kg.m-2 X 10-5)

120

d

d

16 14

c

c

12

b

10

FDA/Wet biomass

b

a

FDA/Dry biomass

8 6 4 2 0 Site 1 (PUN)

Discussion Economically, river (or alluvial) sand mining can be divided into two groups: larger companies which can cover the cost of the technological prevention of environmental problems and smaller entities which operate at the limit of the legal requirements, without the resources to pay for environmental impact prevention plans. Following environmental damage, measures for the recuperation of the degraded area are required by the environmental authorities, which are often poorly implemented or poorly managed, due to the lack of strict legal control. An important issue in this regard is the fact that most recuperation programs are costly and another is that the failure of the recovery plan is only perceived in the long term. In this complex socio-environmental context, alternative recovery and monitoring programs need to be encouraged by environmental managers. Considering that, in general, restoration programs basically involve soil preparation for the cultivation of plant species, in the absence of innovative approaches monitoring programs allow the use of simpler and faster techniques. In this regard, the adoption of criteria associated with lower levels of biological organization (e.g., enzyme activity) can improve our understanding of soil quality changes in the short term. Once a restoration program is underway, the relationship (or correlation) between soil enzyme activity and visible damage at higher levels of organization (e.g., changes in biomass growth) could be used to determine the degree of change in the new ecosystem. In relation to the FDA hydrolysis values obtained for the different campaigns carried out at the same site, we observed a slight increasing trend in the soil

Site 2 (FAN)

Site 3 (HORT)

Site 4 (BOS)

microbiological activity, but the campaign with greater activity was not always the most recent. On comparing the FDA hydrolysis values for the different sites, the Tukey test showed a statistical difference in the microbial activities, and an increasing trend in the FDA hydrolysis intensity was established as follows: PUN < FAN < HOR < BOS, which is almost the same order observed for the plant productivity values measured at these sites. A good correlation was observed between the enzyme activity and the wet (r = 0.9971) and dry (r = 0.8593) plant biomass yield. However, it should be noted that this correlation does not imply causation. As mentioned above, at three of the sites studied, several plant species were present, while one site (PUN) contained only exotic grass species. Thus, it appears that an increase in the plant species diversity increases the soil microbial activity, which can help enhance the soil fertility (El-Keblawy and Ksiksi 2005). In this context, Cardinali et al. (2014) recently used FDA hydrolysis to show that the design of riparian buffer strips affects the soil quality parameters, contributing to an improvement in the management of these systems. Our findings with regard to the use of FDA hydrolysis as a soil quality indicator are in agreement with data published in the literature (Adam and Duncan 2001; Silva et al. 2004; Oliveira et al. 2007). This methodology has been used to determine the microbial activity of a soil submitted to four treatments: reforestation with native species of the Atlantic forest, reforestation with exotic species, reforestation with neem, sucupira and stick-pigeon, soil not submitted to reforestation, and the soil of native Atlantic forest, which was used as a reference soil (Silva et al. 2004). The authors observed


that reforestation with native and exotic species presented higher microbial activity, indicating that the FDA hydrolysis results were effective as an indicator of microbial activity in soils submitted to different reforestation strategies. On a regional scale, Oliveira et al. (2007) used the same approach to differentiate microbiologically the soils of five agroecosystems in a semi-arid region of Brazil and found that hydrolysis occurred in all soil types, but at intensities that were dependent on the type of vegetation cultivated. From the ecological point of view, it is clear that certain changes related to the ecological hierarchy occur during the recovery of degraded areas, starting with the physicochemical and microbiological processes in the soil, followed by plant succession to achieve local ecosystem equilibrium. In this regard, Gris et al. (2012) highlighted that pioneer species are very important in the ecological succession process since they are less demanding with regard to the soil quality and have shorter life cycles, requiring high levels of sunlight during the entire cycle. These are fast-growing species that provide soil protection and the microclimate conditions that are required for the establishment of species that belong to the later successional stages. Our results show that FDA hydrolysis represents a tool to indicate soil quality during any of these stages and when this method is used in associated with a restoration management strategy, it allows an easy and rapid response from environmental managers to the conditions associated with plant productivity.

Conclusions This study shows that FDA hydrolysis promoted by the soil microbiota represents a useful single criterion for measuring the status of soil quality at different sites undergoing the restoration process. More specifically, it appears that the FDA hydrolysis assay (or ratios calculated using this parameter and other parameters measured) can provide an integrative measure of soil quality and plant biomass productivity, which are important aspects in the management of restoration programs applied to areas degraded by alluvial sand mining. This easy and rapid microbiological technique could form the basis for monitoring and the early prediction of the success of vegetal restoration programs, since responses at the higher level of biological organization can be assessed only in the long term. The

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following basic recommendations for the management of sand extraction are related to situations where FDA approach can be applied. The degraded area should be limited, i.e., extraction activities should be concentrated in a small area or restricted to a few bars to avoid widespread environmental impact, which can be monitored through measuring the soil enzyme FDA hydrolysis. After the implementation of the restoration program, periodical environmental reports should be presented to local authorities providing data on the evolution of the restoration, which can also be assessed based on the FDA hydrolysis. Special attention must be paid to the recuperation of riparian vegetation buffer at the edge of the water and along riverbanks and of eroded bars. The early generation of data on the progress of the restoration program could help environmental managers to take prompt action for the proper development of the restoration program. Acknowledgements C.M. Radetski gratefully acknowledges the grants awarded by CNPq-Brazilian National. Council for Scientific and Technological Development (Grant No. 302798/ 2013-7).

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