1 Introduction

Failures in tailing dams have occurred in many countries and the frequency of such events has been increasing. The Fundão dam, located in Mariana, Minas Gerais, Brazil, suffered a failure in 2015, causing the largest iron mining tailing disposal ever registered, thereby damaging forests and urban areas along the course of the Doce river (Fernandes et al. 2016). This failure released over 55 million cubic meters of mine tailings into the environment and this large volume of residue covered soils and reached river basins, thus impeding natural recovery (Ibama 2015). The hydrological network affected by the tailings from Fundão dam is linked to the Doce river basin which stretches to 663.2 km. The disaster also impacted 41 cities along this basin by eliminating various ecosystems and natural resources, with the estimated cost for restoration of the forests reaching around 20 billion dollars (Fernandes et al. 2016). The Fundão dam tailings are the waste product of iron mining activities, which are characteristic of the central regions of Minas Gerais state, Brazil, with high Fe concentrations (Pádua et al. 2021).

After the Fundão dam failure, water samples collected from the Doce River showed the presence of potentially toxic elements (PTEs) in concentrations above the permitted limits defined by the Brazilian Environmental Law (Carvalho et al. 2017). High PTE concentrations in the soil can damage the growth and development of plants (Gomes et al. 2011). The tailings from Fundão dam showed the presence of several PTEs including Al, As, Ba, Cr, Cd, Cu, Mn, Ni, Pb, V, and Zn (Guerra et al. 2017; Pádua et al. 2021). According to Guerra et al. (2017), As and Mn were present at anomalous levels, and Pádua et al. (2021) highlighted the presence of high Al concentration in the tailings. Thus, selection of plant species with potential for reforestation is not easy, owing to the challenges imposed on plants by the mining areas (Almeida and Sánchez 2004). These challenges include the presence of PTEs in mining tailings; therefore, potential species for reforestation should have some degree of tolerance to metal(loid)s stress.

Information on the biology and tolerance to mining tailings and secondary limitations imposed by the climate is required for selecting species having reforestation potential. For instance, inadequate information on the species selected for reforestation will lead to difficulties in the successful implementation of such systems (Barbosa 2000). A major issue in mining areas is that unvegetated spots are prone to erosion and further environmental degradation (Moterroso et al. 1998). Mining tailings may be a continuous source of PTEs that may spread by erosion, and reforestation may limit this effect (Vega et al. 2005). Reforestation is essential to promote the phytostabilization of mining tailings to prevent further environmental degradation (Mendez and Maier 2008). According to Vega et al. (2005), selecting species for the reforestation of regions with water limitation, requires native plants, which show multiple tolerances. The region affected by the Fundão dam failure experiences dry weather for a few months (Álvares et al. 2013), which may affect seed germination and seedling growth. Thus, besides selecting tolerant plants for reforestation of the affected areas, it is also important to test their response to water limitation to provide adequate reforestation conditions.

Cenostigma pluviosum var. peltophoroides (Benth.) E. Gagnon & G.P. Lewis, previously known as Caesalpinia peltophoroides Benth. (Gagnon et al. 2016), is a widely distributed tree species belonging to the Fabaceae family. This species is native to the regions of the Espirito Santo state located in the Atlantic rainforests (Gaem 2020), large areas of which were destroyed by the mine tailings from the Fundão dam failure. This species was used for the reforestation of the Atlantic Forest and is also widely used for urban afforestation (Silva et al. 2008). In addition, this tree is a deciduous heliophyte with large seed production and has the potential for timber production (Silva et al. 2008). The possible uses of its wood render it attractive for reforestation in regions with small properties, so that owners may harvest its resources over time. When introduced in areas previously occupied by natural forests, this species reveals itself as a relevant resource because of its high seed set, which is favorable for natural regeneration, and also because of its deciduous phenology, which provides organic matter to the soil. According to Pontes et al. (2006), C. pluviosum grows in several soil types and can facilitate recovery of degraded areas; this is an important trait for trees applied to reforestation systems, because soils show considerable variations during the time required for revegetation. Thus, C. pluviosum shows potential to be used for reforestation systems and may act as a pioneer species in degraded areas. However, further information regarding its tolerance to mining tailings and water limitation is necessary, because this information is not available in the literature.

The hypothesis of this study was that reduced water availability influences the growth, physiology, and anatomy of plants growing in mining tailings. Therefore, the objective of this study was to investigate the growth, gas exchange, and anatomy of C. pluviosum grown in the tailings from Fundão dam failure under two water availabilities.

2 Material and methods

2.1 Study site

The study site is located in the Mariana city, state of Minas Gerais, Brazil, between 20° 22′ 40″ S, 43° 24′ 57″ W and 20° 11′ 58″ S, 43° 29′ 28″ W, and the samples were collected from locations 4 km away from the Fundão dam location. The area affected by the Fundão dam disaster is, however, much larger since it includes 229 municipalities covering an area of 87,711 km2, and 600 km of the course of the Doce river along with most of its basin area (Fernandes et al. 2016). The study site has CWb climate (temperate or subtropical) with dry winters and wet and temperate summers. The precipitation is low during the months of June and July, at approximately 3 mm, and high during the months of November to February, reaching 330 mm (Dutra et al. 2005; Alvares et al. 2013). The annual precipitation is 1800 mm and the mean temperature is 19.7 °C. The affected area comprises two main biomes (the Atlantic forest and Cerrado savannah), with the Atlantic forest being the larger biome (Ibama 2015). The Atlantic forest is mainly comprised of deciduous trees, such as C. pluviosum, as well as non-deciduous trees.

2.2 Materials and experimental design

The experiments were carried out in a growth chamber located at the Universidade Federal de Alfenas (Federal University of Alfenas). Seeds were collected from ten C. pluviosum trees growing in the campus of the University and kept in paper bags until the start of the experiments. The total amount of mining tailings removed from the sampling site was approximately 1.0 m3, which was packaged in 20-L plastic bags and then transported to the Universidade Federal de Lavras and Universidade Federal de Alfenas being stored protected from rainfall and other environmental factors. This large volume was necessary because this work is part of a bigger project, which included other experiments in different fields. Thus, just a part of this volume was used for the experiments in this work.

Mining tailing samples were collected from 4.0 km away from the Fundão dam location (20° 11′ 58″ S and 43°29′ 28″ W). At the site of sampling, the tailings formed a 1.0 m thick layer above the soil. The sampled tailings were transported to the laboratory and sieved using a 2.6 mm mesh sieve. The maximum water holding capacity (HC) of the tailings was estimated according to Souza et al. (2000) and Pádua et al. (2021).

The seeds were kept submerged in distilled water for 8 h, following which the fungicide Captana 500 was applied for disinfestation. Individual seeds were sown in 500 mL plastic pots containing 400 mL of mining tailings, which were kept at maximum water holding capacity for 53 days in a growth chamber at 23 °C, 60% relative humidity, 40 µmol m−2 s−1 radiation intensity, and a 12-h photoperiod. After seedling establishment, the plants were subjected to two water conditions: maximum water holding capacity (HC) and 50% of this capacity (50% HC). Tap water was used for irrigation. The plants were kept under experimental conditions for 40 days in the same growth chamber environment as described for seed germination. The majority of the area affected by the dam failure was completely covered by several meters of mining tailings, such that the soil was unavailable for plant establishment. Reforestation programs in these regions must deal with plants planted directly in the mining tailings and therefore, this experiment did not employ treatments containing a different substrate. The experimental design was completely randomized with two treatments (HC and 50% HC) and 17 replicates. Each replicate comprised one plant from one seed.

2.3 Mining tailings analysis

The levels of macronutrients (P, Ca, K and Mg), micronutrients (Mn, Fe, Zn, Cu and Na), and PTEs (Al, Cr, Cd and Pb) were determined as follows: the tailing samples were oven dried at 40 °C for 72 h and digested with nitric and perchloric acids by transferring 0.5 g of the samples and 6 mL of HNO3 to each digestion tube and kept overnight in this condition. The tubes were then placed in a digestion block and gradually heated to 140 °C, and digestion was continued until the samples reached approximately 1 mL each and acquired a transparent aspect. The tubes were then cooled to room temperature and 2 mL of HClO4 was added and heated again at 190 °C for 2 h (Abbruzzini et al. 2014). The samples were removed from the block, cooled to room temperature, and elements concentration was determined by atomic absorption spectrometry using a Perkin-Elmer Elemental Analyzer 2400 (CHNS/O). The pH was determined using a soil pH meter at water-saturated conditions.

The mining tailing granulometry was determined by measuring its particle diameter. The tailing samples were oven dried at 60 °C for 48 h. The samples were then spread over a microscope slide containing 50% glycerol (V V−1) and covered with coverslips. The slides were photographed using a Zeiss Axio Scope A1 microscope (Zeiss, Oberkochen, Germany). Ten slides and three fields were evaluated and the diameters of ten particles of mining tailings from each field were measured.

2.4 Gas exchange, chlorophyll content, and water potential analyses

Gas exchange analysis was performed using an infrared gas analyzer model LI-6400XT (LI-COR, Lincoln, Nebraska, USA) with a LI-6400-02B chamber and the radiation intensity fixed at 400 µmol m−2 s−1. The radiation intensity was selected in accordance with the light saturation point determined in a previous light response curve test. The net photosynthesis (A), transpiration rate (E), and stomatal conductance (gs) were measured. The water use efficiency (WUE) was calculated as follows: WUE = A/E. The chlorophyll content was estimated using a SPAD-502 chlorophyll meter (Konica Minolta, Osaka, Japan). Analyses were performed on the first fully developed leaf from the shoot apex. The water potential (Ψw) was measured using a pressure chamber (Model 3115, Soilmoisture Equipment Corp., Santa Barbara, USA) at predawn (lights kept off until the end of the analysis), from one leaf per plant.

2.5 Growth analysis

Plant height was measured using a ruler at intervals of 10 days. At 40 days after the start of the experiment, the plants were collected and separated into roots, leaves, and stem. The leaves were counted and photographed and the total leaf area per plant was measured using the ImageJ software. The fresh mass of each organ was measured using the analytical scale AY220 (Shimadzu, Tokyo, Japan). Each plant organ was oven dried at 60 °C until constant mass. The biomass allocation to each organ was calculated as follows: AL% = (ODM/TDM) × 100, where AL is the biomass allocation, ODM is the dry mass of a given organ, and TDM is the dry mass of the whole plant. Plant water content was calculated as follows: WC = [(PFM˗PDM)/PFM] × 100, where WC is the plant water content, PFM is the whole plant fresh mass, and PDM is the whole plant dry mass.

2.6 Anatomical analysis

At the end of the experiment, the first fully developed leaf was sampled for anatomical analysis. The leaves were fixed in FAA 70 (formaldehyde:acetic acid:70% ethanol, in the proportion 0.5:0.5:9.0 V V−1) for 72 h (Johansen 1940) and stored in 70% ethanol. Paradermal imprints were obtained from the abaxial surface at the median region of the leaves for the study of stomatal traits. The abaxial surface of the leaflet was covered with cyanoacrylate resin and after polymerization, the film was removed and mounted on slides. The slides were observed and imaged using an Axio A1 light microscope (Zeiss, Oberkochen, Germany) coupled with a Canon PowerShot G-10 digital camera (Canon, Tokyo, Japan). The ImageJ software was used to measure the stomatal length and width, and the number of stomata was counted. These variables were used to calculate the stomatal length/width ratio and the stomatal density.

Handmade transverse sections were obtained from the median region of the leaflets using steel blades. The sections were clarified with 50% sodium hypochlorite (V V−1) for 10 min and washed twice with distilled water (Johansen 1940). The sections were then stained with a solution of 1% safranine (m V−1) and 0.1% astra blue (m V−1) in a 3:7 ratio (Bukatsch 1972). The slides were observed and imaged using the Axio A1 light microscope coupled with the Canon PowerShot G-10 digital camera. The images were captured at the interveinal region. Anatomical traits were measured using the ImageJ software. The areas of bundle sheath, fibers, and phloem and xylem in the vascular bundles were measured and the proportion of each tissue was calculated using the equation: T% = (TA/VBA) × 100, where T is the proportion of the given tissue, TA is the tissue area, and VBA is the vascular bundle area. The diameter of the xylem vessel in the vascular bundles was also measured. The thicknesses of the whole leaf, adaxial and abaxial epidermis, and spongy and palisade parenchyma were measured. The palisade/spongy parenchyma ratio was then calculated.

2.7 Statistical analysis

Data were averaged to one plant per replicate in cases where multiple sections, fields, and leaves were measured. The data were subjected to one-way ANOVA and the means were compared by F test to p < 0.05 using the Sisvar statistical software (Ferreira 2011).

3 Results

The concentrations of macronutrients (P, K, Mg, and Ca) and micronutrients (Mn, Fe, Zn, Cu, and Na) in the mine tailings from Fundão dam failure are shown in Table 1. Mining tailings showed potentially toxic elements (Al, Cr, Cd, and Pb) but only Cd exceeded the limit for soil quality (Table 1) although Fe and Al concentrations were noticeably higher than other elements. These elements may show reduced availability due to the pH value showed by mining tailings. The pH was slightly acidic and the particle size was very small (Table 1). Although potentially toxic elements were detected in the tailings, there was no evidence of deformation or toxicity, such as chlorosis or necrosis of plant parts, during the growth and development of C. pluviosum.

Table 1 Nutrients and potentially toxic elements found in the mining tailings from Fundão dam failure at Mariana, Brazil. *Highest value considering Conama (2009) and CCME (2007)
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Reduced water availability did not affect the leaf (Fig. 1A, E), stem (Fig. 1B, F), and total (Fig. 1D, H) fresh or dry masses, whereas the fresh and dry masses of root were higher at lower water availability (Fig. 1C, G).

Fig. 1
figure 1

Growth parameters of Cenostigma pluviosum var. peltophoroides under two different water availabilities in mining tailings from the Fundão dam failure at Mariana, Brazil. HC = mining tailings at maximum water holding capacity; 50% HC = mining tailings at 50% of the maximum water holding capacity. * indicates significant differences according to F test for p < 0.05 and ns indicates no significant difference. Bars indicate standard error

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The biomass allocation to roots in C. pluviosum was increased by the reduced water availability (Fig. 2C), but no significant changes were seen in the leaf (Fig. 2A) and stem allometry (Fig. 2B). The 50% HC treatment did not produce any changes in the number of leaves (Fig. 2D), leaf area (Fig. 2E), and root length (Fig. 2F) of C. pluviosum when compared to plants from HC treatment. In addition, neither the leaf water content (Fig. 2G) nor the plant water potential (Fig. 2H) was reduced by the reduced water availability.

Fig. 2
figure 2

Biometry and water status of Cenostigma pluviosum var. peltophoroides under two different water availabilities in mining tailings from the Fundão dam failure at Mariana, Brazil. HC = mining tailings at maximum water holding capacity; 50% HC = mining tailings at 50% of the maximum water holding capacity. * indicates significant differences according to F test for p < 0.05 and ns indicates no significant difference. Bars indicate standard error

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Reduced water availability in mining tailings did not cause any change in the photosynthesis of C. pluviosum (Fig. 3A); however, it reduced the stomatal conductance (Fig. 3B) and transpiration (Fig. 3C) and increased the water use efficiency (Fig. 3D). There were no changes in the stomatal length (SL), width (SW), and SL/SW ratio, whereas the stomatal density was increased by 50% HC (Table 2). The chlorophyll content showed no significant changes (Fig. 3E) between treatments.

Fig. 3
figure 3

Gas exchange and chlorophyll content of Cenostigma pluviosum var. peltophoroides under two different water availabilities in mining tailings from the Fundão dam failure at Mariana, Brazil. HC = mining tailings at maximum water holding capacity; 50% HC = mining tailings at 50% of the maximum water holding capacity. * indicates significant differences according to F test for p < 0.05 and ns indicates no significant difference. Bars indicate standard error

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Table 2 Stomatal traits of Cenostigma pluviosum var. peltophoroides grown under two different water availabilities in mining tailings from the Fundão dam failure at Mariana, Brazil. HC = mining tailings at maximum water holding capacity; 50% HC = mining tailings at 50% of the maximum water holding capacity. Data are shown as mean ± SD. *significant according to F test to p < 0.05, ns = no significant difference
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The leaves of C. pluviosum preserved their anatomical structure during both HC and 50% HC treatments (Fig. 4), but quantitative analysis revealed a few modifications (Fig. 5). Likewise, 50% HC treatment did not cause any change in phloem (Figs. 4 and 5A), xylem (Figs. 4 and 5B), and fiber (Figs. 4 and 5C) proportions, as well as in the xylem vessel diameter (Figs. 4 and 5D). Low water availability reduced the thicknesses of leaf (Figs. 4 and 5E), epidermis (both adaxial and abaxial) (Figs. 4 and 5F, G), and spongy parenchyma in C. pluviosum (Figs. 4 and 5I). However, thickness of the palisade parenchyma was not significantly changed by the reduced water availability (Figs. 4 and 5H) as the palisade/spongy ratio was increased in this treatment (Figs. 4 and 5J).

Fig. 4
figure 4

Transverse sections of leaflets from Cenostigma pluviosum var. peltophoroides grown under two different water availabilities in mining tailings from the Fundão dam failure at Mariana, Brazil. A and C = plants grown under maximum water holding capacity; B and D = plants grown under 50% of the maximum water holding capacity. A and B = interveinal region; C and D = midrib region. ade = adaxial epidermis; abe = abaxial epidermis; pp = palisade parenchyma; sp = spongy parenchyma; fb = fibers; xl = xylem; phl = phloem. Bar = 25 µm

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Fig. 5
figure 5

Leaf anatomical traits of Cenostigma pluviosum var. peltophoroides under two different water availabilities in mining tailings from the Fundão dam failure at Mariana, Brazil. HC = mining tailings at maximum water holding capacity; 50% HC = mining tailings at 50% of the maximum water holding capacity.* indicates significant differences according to F test for p < 0.05 and ns indicates no significant difference. Bars indicate standard error

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4 Discussion

Macro and micronutrients and water limitation in mining tailings from the Fundão dam failure did not promote evident symptoms of nutritional deficiency in C. pluviosum plants. Trees may show lower nutritional dependency compared with other pioneer species (Rincón and Huante 1994). Cenostigma pluviosum var. peltophoroides was, until recently, classified under the Caesalpinia genus (Gagnon et al. 2016) and its basionym was Caesalpinia peltophoroides. This information is important because nutritional knowledge is limited for this species; however, studies on other Caesalpinia trees can be found. For instance, Caesalpinia eriostachys shows low nutritional dependence during its establishment, and this species has a limit for nutrient-driven growth increase (Rincón and Huante 1994). However, Caesalpinia echinata showed limited growth and deficiency symptoms during the absence of several macro and micronutrients (Valeri et al. 2014). In addition, Caesalpinia ebano showed low mycorrhizal dependence and improved growth with organic amendments added to the soil (Gómez et al. 2018). These studies on Caesalpinia species show that, in general, these trees have low nutritional dependence. Thus, iron mining tailings from Fundão dam failure caused not evident nutritional stress to C. pluviosum but further analysis is necessary since our data is limited about the nutritional aspects of the mining tailings. It is also noteworthy that the properties of mining tailings can vary significantly.

The Fe concentration in the tailings, despite being the highest detected in the samples is similar to values found in Brazilian soils (Ker 1997; Oliveira et al. 2001) and this concentration is even lower when compared with soils from iron mining areas (Carvalho Filho et al. 2011). According to Ker (1997), there are different soil types in Brazil and the means for Fe concentration can vary from 8900.0 to 745,000.0 mg kg−1. Iron is an important micronutrient for plants but may cause growth limitation and oxidative stress at high concentrations (Jucoski et al. 2016). However, C. pluviosum plants grown in mining tailings showed no abnormalities and, according to Henrique et al. (2009), plants of this species at the same age had similar biomass. The high Fe concentrations found in the tailings may be related to the mining activity at the region of the Fundão dam (Fernandes et al. 2016) in Mariana, Brazil, but no Fe toxicity was observed in the studied plants.

Aluminum is another element that was found at high concentrations in the tailings from Fundão dam. However, Brazilian soils often show Al concentrations higher than those found in this experiment (Ker 1997; Andrade et al. 2012). According to Ker (1997) Al concentrations can vary in Brazilian soils from 89,300.0 to 319,000.0 mg kg−1. Plants under Al toxicity show root and shoot necrosis, growth limitation, and leaf folding (Tabaldi et al. 2007; Gordin et al. 2013) though Al-driven damage is potentially increased in pH below 5 (Kochian et al. 2005). Because C. pluviosum showed no evidence of Al toxicity, this may also be related to the pH of the mining tailings (Table 1), which is higher than the values at which Al toxicity for plants is generally observed. Potentially toxic elements such as Pb, and Cr were also found in the tailings, but their concentrations did not exceed the limits defined by Brazilian environmental law and the references from the Canadian Council of Ministers of the Environment (Table 1). Cadmium exceeded the limit concentrations for soil quality (Table 1) was found in C. pluviosum plants.

It was expected that the reduced water availability in the tailings would reduce the growth parameters of C. pluviosum. However, both growth and development of C. pluviosum remained unaffected by the 50% HC condition. In fact, growth limitations in plant species under water stress are expected (Costa et al. 2008), and 50% HC is a sufficient privation to cause severe water stress and decreased plant growth (Díaz et al. 2018; Cruz et al. 2019). However, reduction in water availability to 50% HC in the tailings did not cause any stress to C. pluviosum.

One significant response from C. pluviosum plants under 50% HC was the increased investment in the root system. This was evidenced in both fresh and dry root masses, as well as in increased biomass allocation to roots. This response is an important feature for drought tolerance, because higher investment in roots permits plants to obtain water and nutrients under lower water availability conditions, and it is a common response in plants (Jaramillo et al. 2013; Lynch 2015). Reduction in water availability to 50% HC in the tailings did not cause drought stress in C. pluviosum; nevertheless, this treatment was sufficient to stimulate root growth as a compensation mechanism to improve water uptake.

The reduction in transpiration and stomatal conductance of C. pluviosum plants under 50% HC, may be related to enhanced stomatal traits facilitating better control of water loss. The size of stomata was not modified by 50% HC treatment although there was an increase in stomatal density, which may have improved the control of transpiration and water loss. Under water stress, plants develop smaller stomata with increased stomatal density, and these alterations are often interpreted as a response to reduce water loss by transpiration (Bosabalidis and Kofidis 2002; Grisi et al. 2008; Cruz et al. 2019). Species in which stomatal density remains unchanged under drought conditions show growth limitations (Cruz et al. 2019). However, C. pluviosum retained the stomatal dimensions while increasing their density, which were sufficient to reduce stomatal conductance and transpiration. This trait seems to be important to maintain growth under 50% HC conditions.

Cenostigma pluviosum grown under 50% HC maintained its anatomical structure, which shows that there was no water stress. The vascular tissues were also not affected by 50% HC treatment; thus, these tissues remained functional by facilitating water, nutrients, and photoassimilate transportation throughout the plant and supporting growth. Thin leaf tissues develop under water limitation conditions, which is a common effect of drought. Water stress lowers water and biomass transport to leaves, limiting leaf area formation, as well as the thickness of leaf tissues, thereby reducing photosynthesis and growth (Cruz et al. 2019). Nonetheless, no significant effect was detected on the photosynthesis or growth of C. pluviosum under 50% HC. In addition, the increased palisade/spongy parenchyma ratio favored photosynthesis by increasing the proportion of the palisade parenchyma.

A trait of the mining tailings that may have led to the absence of water stress is the small particle diameter (Table 1). This attributes a clay texture to the tailings from Fundão dam (clay < 2 µm). Clay soils are well known for their high water retention capacity (Beutler et al. 2002). This increased water retention capacity enables the preservation of adequate water content in the tailings even under 50% HC, thereby preventing water stress. The region affected by the mining tailings from the Fundão dam failure has a period of dry weather conditions, resulting in reduced water availability. However, reforestation programs may not be harmed by this constraint because of the capacity of the mining tailings to retain water, thereby favoring the growth of tree species such as C. pluviosum throughout the year and contributing to restoration success.

5 Conclusion

Cenostigma pluviosum var. peltophoroides can be grown in the mining tailings from Fundão dam failure at maximum water holding capacity (HC) or 50% HC. Reducing the water availability to 50% HC in the tailings does not cause water stress in the plants. The clay texture of this substrate increases its water retention capacity. Cenostigma species with similar anatomical and physiological traits may behave similarly to C. pluviosum in the mining tailings from iron industries with similar traits. The information obtained in this study may help researchers in selecting appropriate species for the reforestation of regions impacted by iron mine tailings, and also to understand the effects of the tailings on the physiology and anatomy of trees with potential for reforestation. Understanding the effects of water limitation, even under 50% of the maximum water holding capacity in the mining tailings, can be improved by studying their particle size distribution and matric potential. Globally, mining tailings with similar traits may show similar results.