Assessing ant diversity with bioindicators in a deactivated iron mine: implications for environmental monitoring and recovery effortsAbstract
Mining causes serious environmental damage. Monitoring and restoring mined areas mitigate the impacts caused by mining, and ants are organisms that can be used as bioindicators. Their composition is an excellent method for monitoring environmental conditions. The objective of this study was to describe the diversity of ants in an iron mine that was deactivated ten years ago and to verify the ecological variables that explain this diversity. Ants were collected with pitfall epigeic traps with fish and honey in a mining area in the process of environmental recovery after ten years, and three habitats neighbors of the mine: Brazilian Cerrado, Atlantic Forest, and Campo Rupestre. Environmental variables related to vegetation structure were collected to explain the difference in species composition of all habitats. We collected 84 morphospecies of ants belonging to 23 genera and seven subfamilies. Species richness did vary among the area regeneration with grassy and Campo Rupestre. The composition of ants differed between habitats. The mining area regeneration with grassy was characterized by general species and adapted to disturbed environments. We recommend that the recovery plans must focus on reintroducing native plant species, recovering the vertical structure of the vegetation, and on continuous, long-term monitoring to adjust strategies over time.
Keywords:
Atlantic Forest; iron mine; ecological regeneration; biodiversity; ants
Resumo
A mineração causa sérios danos ambientais. O monitoramento e recuperação de áreas mineradas mitigam os impactos causados, sendo que as formigas são organismos que podem ser utilizados como bioindicadores. Sua composição é um ótimo método para monitorar as condições ambientais. O objetivo desse estudo foi descrever a diversidade de formigas na mina de ferro desativada há dez anos e verificar as variáveis ecológicas que explicam a diversidade de formigas. As formigas foram coletadas com armadilhas epigeicas de queda com peixes e mel em uma área de mineração em processo de recuperação ambiental após dez anos e em três habitats vizinhos à mina: Cerrado Brasileiro, Mata Atlântica e Campo Rupestre do Cerrado. Variáveis ambientais relacionadas à estrutura da vegetação foram coletadas para explicar a diferença na composição de espécies de todos os habitats. Coletamos 84 morfoespécies de formigas pertencentes a 23 gêneros e sete subfamílias. A riqueza de espécies variou entre a área de regeneração com gramíneas e Campo Rupestre. A composição de formigas diferiu entre habitats. A regeneração da área mineira com gramíneas foi caracterizada por espécies gerais e adaptadas a ambientes perturbados. Nós remomendamos que os planos de recuperação devem focar na reintrodução de espécies vegetais nativas, na recuperação da estrutura vertical da vegetação e no monitoramento contínuo e de longo prazo para ajustar as estratégias ao longo do tempo.
Palavras-chave:
Mata Atlântica; mina de ferro; restauração ecológica; biodiversidade; formigas
1. Introduction
The Brazilian Cerrado and Atlantic Forest biomes face threats to the preservation of their natural resources from various causes (Ferreira et al., 2021), including mining areas (Rubim et al., 2023). Mining activities are recognized as primary contributors to environmental degradation, exerting profound impacts on local ecosystems (Aska et al., 2024). This activity typically involves the removal of native vegetation, contamination of soil and water, and alteration of topography, which severely compromise biodiversity and ecosystem functions (Jacka, 2018) up to 50 km from the mining areas (Sonter et al., 2020).
Efforts to mitigate mining damage and restore degraded landscapes have been focused on the scientific community and environmental managers (Bowell et al., 2023). Restoration consists of the reintegration of local ecological functionality, in addition to the preservation of biodiversity and the sustainable use of natural resources (Gastineau et al., 2021; Young et al., 2022).
Environmental recovery methodologies and monitoring of impacted areas are mandatory to reduce impacts related to mining activities (Niemi and McDonald, 2004; Ribas et al., 2012a). Bioindicators of environmental impacts are widely used for environmental monitoring in these areas, especially ants (Cuautle et al., 2016; Groc et al., 2017; Ribas et al., 2012a, b). The ant community composition is used as a sensitive parameter of habitat quality, properly reflecting changes in vegetation structure, resource availability, and anthropogenic disturbances (Ribas et al., 2012a, b; Groc et al., 2017; Souza et al., 2020).
While prior research has underscored the efficacy of ants as indicators of ecosystem health and resilience, more investigations into ant diversity dynamics within deactivated mining areas and their post-recovery states are necessary. Additionally, elucidating the environmental drivers that support ant diversity in such contexts is paramount for informing targeted political conservation and restoration efforts.
In this scenario, the objective was to describe the diversity of ants in the area undergoing environmental recovery after ten years of mining activity, and to assess the environmental variables that explain ant diversity in this mining area to understand the impact of landscape changes caused by mining.
2. Material and Methods
2.1. Study area
The study was conducted in the municipality of Nova Lima, Minas Gerais, Brazil, at the Centro de Tecnologia de Ferrosos (Miguelão), and in the municipality of Brumadinho, at the Córrego do Feijão mine of the Vale S.A. Company, located in the Quadrilátero Ferrífero in the Southeast region of Brazil. Ants were collected from four common habitats in the region, with the phytophysiognomies described by Castro et al. (2017): Brazilian Cerrado - savanna countryside phytophysiognomies (83.60 ha), Atlantic Forest (30.87 ha), Campo Rupestre (58.60 ha), and a mining area undergoing environmental recovery with grassy vegetation (11.20 ha). The sampled points were indicated by Oliveira et al., (2019).
The mining area undergoing environmental recovery was impacted by mining activities, which involved removing its native vegetation (Atlantic Forest) to establish an ore deposit area. After mining operations ceased in 2005, a rehabilitation project was initiated, involving the planting of tree species (predominantly Machaerium nyctitans and Peltophorum dubium, which did not survive due to recurrent fires caused by human activities), grasses (Panicum maximum Jacq, Brachiaria decumbens, Melinis minutiflora), and some leguminous plants (Neonotonia wightii, Mimosa sp., Crotalaria juncea). Currently, grasses dominate the area, which has been undergoing environmental recovery for 10 years and are regarded as revegetation species.
2.2. Ant sampling
Two transects were installed in each habitat, with five collection points spaced 50 m apart. The distance between the transects was also 50 m. At each collection point, a pitfall trap was installed. Each pitfall consisted of a 700 ml plastic pot with a 15 cm diameter opening containing sardine and honey baits. Inside each trap, 200 ml of a water solution with salt and detergent was placed. The bait was placed in a plastic container (50ml) at the center of each trap using a wire as a bait holder. The traps remained in the field for 48 hours. The collected ants were identified to the genus level using the identification keys (Bolton et al., 2006; Baccaro et al., 2015; Instituto Humboldt, 2003), separated into species, identified by Daniele L. Braga using the collections belonging to the institution, and included in the collection at the Laboratory of Forest Entomology (Department of Entomology, UFLA).
2.3. Environmental variables
A plot measuring 400 square meters (20×20 m) was established at each collection point, and the following environmental variables were recorded: understory density, litter weight, canopy cover, circumference at breast height (CBH), height, number, and species richness of all plants with a CBH > 5 cm. These data were collected to examine the correlation between environmental variables and ant species diversity.
Shrub and herbaceous vegetation density (sub-forest density) was assessed following the method of Nobis and Hunziker (2005). Samples of litter were collected within a delimited area measuring 30×30 cm, dried for 96 hours, and weighed using a precision scale with a resolution of 0.1 g. The canopy cover was determined by capturing a hemispheric photograph of the canopy with a camera equipped with a 0.20x fish-eye lens (180° aperture), following the method of Engelbrecht and Herz (2001).
2.4. Analyses
Each sampling point represents the presence or absence of species collected at a site through pitfall traps. To assess the relationship between ant species richness and the different collection environments, we used a generalized linear model (GLM). The dependent variable was ant species richness, expressed as the count of species observed in each environment, and the predictor variable was the type of collection environment. Since the species richness data are counts, we initially fitted a GLM using the Poisson distribution family, which is appropriate for count data, with a log-link function. Model adequacy was assessed through diagnostic plots, such as standardized residual plots and scatter plots. Additionally, to bolster our analysis, we subjected the model to a pairwise contrast examination, harnessing the “lsmeans” package (Lenth, 2016). This analysis was performed using the R 4.4.0 software.
Variations in the composition of ants in different habitats were verified through multivariate permutational analysis of variance (PERMANOVA), using Jaccard dissimilarities with 999 permutations. Sequential Bonferroni corrections were applied to adjust p-values as well as pairwise comparisons. Analyses were conducted in PRIMER V.7 with PERMANOVA (Clarke and Gorley, 2015).
Additionally, the non-metric multidimensional scaling (NMDS) analyzed the differences in ant species composition between habitats using the VEGAN package metaMDS function (Oksanen et al., 2018), with the R 4.4.0 software (R Development Core Team, 2024). NMDS was executed for a range of dimensions (k) from one to six, with the optimal number of dimensions determined by evaluating a scree plot of stress versus k dimensions. NMDS utilized the Jaccard distance index on the matrix of species presence/absence. Furthermore, a cluster analysis was performed on the dissimilarity matrix of sampling sites, calculated using the Jaccard distance index, to identify groups of similar environments.
Indicator species for each treatment type were determined using the Indicator Value Method (IndVal) with presence or absence data. The IndVal assesses the extent to which a species meets the criteria of uniqueness (specificity) and fidelity (frequency within a treatment) for each treatment type. Species with higher IndVal values (%) are reliable indicators due to their increased likelihood of being sampled. In this investigation, species with IndVal > 70% were classified as indicator species for the respective habitat.
A distance-based linear models (DistLM) was done to verify the importance of vegetation variables as predictors of ant species composition variation (as shown by our Bray-Curtis matrices) (Legendre and Anderson, 1999). This was done to assess the environmental contributions to the composition of ant communities across the four habitats. DistLM uses a ‘best method’ AIC model selection procedure (Burnham and Anderson, 2004) considering the value of the selection criterion for all possible combinations of predictor variables. Marginal tests were conducted to assess the relationship between species composition and each predictor variable individually. The results were compared with the best solution model derived from the above conditional tests. All p-values were generated by permutation (n= 999). Analyses using DistLM were conducted in PRIMER V.7 with PERMANOVA (Clarke and Gorley 2015).
3. Results
Eighty-four ant morphospecies were collected belonging to 23 genera and seven subfamilies, ninety-four percent of the ants were identified as morphospecies, while six percent were identified at the species level (see Table S1 - Supplementary material). The number of ant species differed significantly among habitats (estimate = 1.987; std error = 0.117; p <2e-16) (see Figure 1). The Atlantic Forest, Brazilian Cerrado, mining area undergoing environmental recovery, and Campo Rupestre presented 33, 34, 34, and 25 ant species, respectively. The Campo Rupestre has different species richness compared to the Brazilian Cerrado area (estimate = -0.556, standard error = 0.182, p = 0.012) and the mining area undergoing environmental recovery (estimate = 0.544, standard error = 0.183, p = 0.015). More than half of the ant species were exclusive to one habitat (65.7%) and only three species (3.6%) were common to the four habitats: Camponotus rufipes sub1 Fabricius, 1775; Brachymyrmex sp5 and Pheidole sp16 (see Table S1 - Supplementary material).
Logarithmic scale confidence intervals for multiple comparisons of epigeic ants richness collected in a pitfall trap pitched with sardines and honey in different habitats: mining area undergoing environmental recovery with grassy (MR), Brazilian Cerrado (BC), Atlantic Forest (AF) and Campo Rupestre (BR), in Nova Lima, MG, Brazil.
The composition of the species was different among the studied habitats, as demonstrated in PERMANOVA (see Table 1). Atlantic Forest and Brazilian Cerrado fragments formed two distinct clusters, mining area regeneration with grassy and Campo Rupestre presented relative overlap (see Figure 2).
PERMANOVA paired test values to evaluate the difference in ant species composition and multivariate dispersion of points in different habitats: (MR) mining area under recovery with grass, (BC) Brazilian Cerrado, (AF) Atlantic Forest, and (BR) Campo Rupestre, in Nova Lima, MG, Brazil.
Non-metric multidimensional scaling (NMDS), according to the species composition, with presence and absence data for the epigeic ant community, collected in a pitfall trap, in different habitats: mining area under recovery with grass (square), Brazilian Cerrado (triangle), Atlantic Forest (diamond), and Campo Rupestre (cross), in Nova Lima, MG, Brazil.
The mining area under recovery with Brachiaria sp. shared four, eight, and 12 species of ants with the Atlantic Forest, Brazilian Cerrado, and Campo Rupestre, respectively. The mainly species shared were Camponotus rufipes sub1, Camponotus crassus Mayr, 1862, and Pheidole diligens Smith, 1858 (see Table S1 - Supplementary material).
Some species contributed to the differences in the composition between the areas and providing perspectives on the conditions of these environments: Ectatomma suzanae Almeida, 1986; Acromyrmex sp1, and Neoponera striatinodis Emery, 1890 were indicators of the Campo Rupestre, Atlantic Forest, and Brazilian Cerrado, respectively.
The relationship between composition and environmental variables demonstrates that the litter weight (mg), canopy cover (%), average plant height (m), and average CBH (cm) most explained the composition of the species and, together, explained 70.8% of the diversity of ants collected in all habitats (see Table 2).
Effect of structural variables of vegetation according to the DISTLM analysis on the composition of ant species found in different habitats: mining area under recovery with grass, Brazilian Cerrado, Atlantic Forest and Campo Rupestre, in Nova Lima, MG, Brazil.
4. Discussion
This work shows that the ant community reflects the changes caused by mining in the Brazilian Cerrado, Atlantic Forest, and Campo Rupestre. The number of ant species differed significantly among habitats, with the Campo Rupestre presenting lower species richness compared to the Brazilian Cerrado and the mining area under recovery. This indicates that the Campo Rupestre, a more specialized and less diverse environment, supports fewer species of ants than the more open and regenerating habitats. The similarity in species richness between the mining area and the Brazilian Cerrado suggests that ten years of environmental recovery in the mining area may be promoting a fauna similar to that found in natural open habitats. However, the species composition differed between habitats, with greater similarity between the mined area under recovery with grasses and the Campo Rupestre. This demonstrates that environmental factors such as canopy opening and circumference at breast height are important for the restructuring of the ant community. The recovery of the mining area with grasses was characterized by generalist ant species and those adapted to disturbed environments. We indicate that recovery plans should focus on reintroducing of native vegetation and continuous, long-term monitoring to adjust strategies, in addition to recovering the vertical structure of the vegetation.
The 33 species of ants collected in the fragment of Atlantic Forest and 34 in the Brazilian Cerrado were similar to other studies in mining areas close to this study (Ribas et al., 2012a). The equality of richness between the Brazilian Cerrado and mining area under recovery with grassy may be due to the similarity of resources found in these habitats (Gomes et al., 2014).
Two species were common across all four habitats: Camponotus rufipes sub1, and the morphospecie Brachymyrmex sp5, which are omnivorous and generalist species known for their high tolerance to human-disturbed environments (Lanhoso et al., 2024; Baccaro et al., 2015; Silvestre and Silva, 2001). The genera Camponotus, Brachymyrmex, and Solenopsis, found in both the recovering mining area and the Atlantic Forest, are similarly classified as omnivorous and generalist. These ants nest in soil, tree trunks, low vegetation, and rocks, demonstrating strong adaptation to disturbed environments (Instituto Humboldt 2003; Costa-Milanez et al., 2014). Additionally, the genera Crematogaster and Pheidole, observed in both the Brazilian Cerrado fragment and the recovering mining area, are generalists. Species from these genera are opportunistic and effective predators, playing crucial roles in ecological processes such as seed dispersal (Rocha et al., 2018; Tanaka and Tokuda, 2016; Baccaro et al., 2015). The presence of generalist and omnivorous ants in areas undergoing environmental recovery indicates an initial stage of recovery, owing to their adaptation to diverse conditions. This dominance suggests low habitat specialization and resilience to disturbances. Continuous monitoring and adjustment of restoration strategies like the introduction of native tree vegetation and enhancing habitat complexity are necessary, as well as the use of seed dispersing species (Penido et al., 2015). Despite their ecological importance, the absence of specialized plant species may hinder the full recovery of the ecosystem.
The species of the genus Wasmannia and Dorymyrmex collected in the mining area under recovery and Campo Rupestre are aggressive competitors and adapted to anthropized environments (Lanhoso et al., 2024; Golias et al., 2018). Species of the genus Dorymyrmex can forage during the hottest hours of the day and are adapted to environments with a high solar incidence (Baccaro et al., 2015). The presence of ant species classified as aggressive competitors and adapted to environmental disturbances in areas under recovery can compete directly with native species for resources such as food and space, potentially affecting local biodiversity. Furthermore, ants adapted to environmental disturbances are often more resilient to changes in the environment, suggesting that the area may not have yet reached an ideal state of ecological stability for more sensitive species. These disturbances can also simplify ecological relationships, such as mutualism (Barbosa et al., 2015).
Ectatomma Suzanne, the indicator species of the Campo Rupestre area, is a predator of insects in general (Delabie et al., 2015), habitat generalist, collected in native vegetation (Vanolli et al., 2021). This suggests a certain ecological flexibility that may contribute to its persistence and distribution in different environmental conditions in the Campo Rupestre.
The indicator species of the genus Acromyrmex in the Atlantic Forest can be associated with disturbed areas. However, the species Acromyrmex subterraneus Forel, 1893 has already been considered an indicator in fragments of the Atlantic Forest (Lapola and Fowler, 2008) and in primary semi-deciduous forest (Nickele et al., 2023), corroborating our results. The presence of species adapted to anthropic environments can alter natural ecological interactions, competing for resources with native species and potentially affecting the structure and function of the local ecosystem. Furthermore, the occurrence of these ants can serve as an indicator of past or current disturbances in the natural habitat, reflecting nearby human activities that have modified environmental conditions. The ability of these ants to persist in natural environments also suggests their adaptation to changing conditions.
The indicator species Neoponera striatinodis of the Brazilian Cerrado was collected in native environments (Amaral et al., 2021). However, it can be found both in natural environments and urban areas, presenting aggressive behavior (Lanhoso et al., 2024), which can facilitate its occurrence and dominance.
The characteristics of the different habitats explain the variation of ant species composition in the studied sites. Atlantic Forest fragments have greater structural diversification of vegetation, greater canopy cover, and litter diversity. The Brazilian Cerrado has smaller trees and open areas, increasing the susceptibility of ants to adverse humidity and temperature conditions. The Campo Rupestre field has predominantly low vegetation, with shallow soils and occurrences of rocky outcrops at high altitudes. The grass-revegetated area is an area with no diversity of microhabitats and resources due to the removal of the original vegetation cover even after ten years of succession. The loss of ant fauna diversity in the tropics is one of the main consequences of simplifying landscape structure, as most of their taxa occupy specific niches (Lopes et al., 2010; Cardinale et al., 2012). Only the grass revegetation area did not present a representative indicator species. This may indicate a lack of reestablishment of this area for soil organisms.
The mining area under recovery with grassy shared more species with the Campo Rupestre field fragment, possibly due to the greater similarity in vegetation structure between these two habitats. Grassy revegetation is a limiting factor to resource availability, as the absence or low frequency of tree species, also characteristic of the rupestrian field, can reduce the diversity of ants in an area (Gámez-Virués et al., 2015; Prach and Walker, 2011).
The analysis of ant composition across different habitats reveals important patterns regarding the recovery of mining areas and their similarities to natural habitats. The occurrence of generalist species in all habitats, including the regenerating mining area, suggests that, after ten years of recovery, the ant fauna and its ecosystem functions are in the process of reestablishment. The presence of species shared between the mining area and other habitats, particularly Camponotus rufipes sub1, Camponotus crassus, and Pheidole diligens, reinforces this observation, indicating that recovery is promoting suitable conditions for the return of species typical of various environments. However, the overlap between the mining area and the Cerrado and Campo Rupestre, in contrast to its greater dissimilarity with the Atlantic Forest, suggests that, even after a decade of regeneration, the mining area is ecologically closer to open and less complex environments, such as the Cerrado, than to dense forested areas like the Atlantic Forest. This may indicate that regeneration in mining areas initially favors species adapted to less structured environments, possibly due to the more open vegetation and lower soil complexity. The indicator species also reinforce these differences: Ectatomma suzanae and Acromyrmex sp1 are indicator species of the rocky montane savanna and the Atlantic Forest, respectively, while Neoponera striatinodis is associated with the Cerrado, highlighting that these species play different ecological roles in these habitats. Therefore, the results indicate that, although the mining area is recovering and supports an active and fauna, it still differs significantly in species composition compared to the Atlantic Forest, showing greater similarity to environments such as the Cerrado and Campo Rupestre, which may have implications for the full recovery of the original ecosystem functions.
The DISTLM analysis confirms that landscape simplification, smaller vertical vegetation structures, and changing environmental conditions have a strong impact on ant diversity. The environmental variables most correlated with ant diversity were related to forest formations. Revegetation with grass was not able to maintain the ant diversity similar to the Atlantic Forest area after ten years of succession, even though the revegetated area was adjacent to the preserved Atlantic Forest fragment. The process of restoring an area involves succession steps that can be optimized by man (Arroyo-Rodríguez et al., 2017). The recolonization of areas undergoing recovery depends on nearby preserved areas, where the first plants capable of establishing themselves will emerge (Altieri, 1999).
The establishment of the first plants precedes the arrival of arthropods in plant succession (Luz et al., 2013; Jamison et al., 2016), and grass revegetation optimizes this process. However, only covering the soil with grasses in highly degraded areas does not allow the restoration of the vertical structure of the vegetation and an increase in the diversity of plants and arthropods (Altieri, 1999). Most Brazilian mining companies use short-term recovery practices such as simply returning the soil layer and covering it with grass in the process after mining (Trindade et al., 2000). One of the most recommended strategies in recovery plans is to reproduce the natural pattern of plant communities, which increases the likelihood of success in environmental recovery, as well as reducing the costs of these projects (Araújo et al., 2006). This simplification of vegetation can affect the amount of light in these microclimates, influencing the ant community (Queiroz and Ribas, 2016).
Our study showed that the composition and richness of ants in mining area under recovery with grassy after ten years of succession was characterized by generalist species and adapted to disturbed environments. Removal of the vertical structure of the vegetation due to mining activity had a major impact on ant diversity. Recovery techniques need to be improved, even in extremely impacted areas, as simple grass revegetation does not promote structural diversification of vegetation, microhabitat diversification, and increased connectivity to recolonized sources. Our findings provided critical information to refine restoration strategies aimed at enhancing biodiversity conservation and promoting sustainability by shedding light on the ecological succession processes unfolding in post-mining landscapes.
Supplementary Material
Supplementary material accompanies this paper.
Table S1
This material is available as part of the online article from https://doi.org/10.1590/1519-6984.288720
Acknowledgments
The authors would like to thank Vale S.A. for the financial support provided to carry out this study, especially the company's technical team for accompanying the field teams and providing support during the activities. We also thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (INCT Biodiversidade do Solo - CNPq Processo: 406658/2022-6) and Fundação de Amparo à Pesquisa do Estado de Minas Gerais (Fapemig - Processo: APQ-04011-24 and CRA-RDP-00136-10). Additionally, we are grateful to the Departments of Soil Science and Applied Ecology of the Federal University of Lavras (UFLA) for their technical support and collaboration in the field collections. We would like to express our sincere gratitude to Professor Fátima Moreira for the scientific coordination of the project, whose guidance was fundamental to its development. Finally, we extend our appreciation to Daniele de Lima Braga for her valuable contribution to the identification of the ant morphospecies.
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