UNIVERSIDADE FEDERAL DE OURO PRETO
Programa de Pós-Graduação em Ecologia de Biomas Tropicais
Ello Brasil Ribeiro da Silva
Samarco dam breach: an environmental disaster on a highly impacted river basin and the use of Leaf Fluctuating Asymmetry for bioindication
Ouro Preto – Minas Gerais 2020
Ello Brasil Ribeiro da Silva
Samarco dam breach: an environmental disaster on a highly impacted river basin and the use of Leaf Fluctuating Asymmetry for bioindication
Orientador: Dr. Sérvio Pontes Ribeiro Co-orientadora: Dra. Tatiana Cornelissen
Dissertação apresentada ao Programa de Pós-graduação em Ecologia de Biomas Tropicais da Universidade Federal de Ouro Preto como requisito para obtenção de título de Mestre em Ecologia.
Ouro Preto – Minas Gerais 2020
Brasil, Ello Ribeiro da Silva.
BraSamarco dam breach [manuscrito]: an environmental disaster on a highly impacted river basin and the use of Leaf Fluctuating Asymmetry for bioindication. / Ello Ribeiro da Silva Brasil. - 2020.
Bra29 f.: il.: color., gráf..
BraOrientador: Prof. Dr. Sérvio Pontes Ribeiro.
BraCoorientadora: Profa. Dra. Tatiana Garabini Cornelissen.
BraDissertação (Mestrado Acadêmico). Universidade Federal de Ouro Preto. Departamento de Biodiversidade, Evolução e Meio Ambiente. Programa de Pós-Graduação em Ecologia de Biomas Tropicais.
BraÁrea de Concentração: Evolução e Funcionamento de Ecossistemas.
Bra1. Doce, Rio, Bacia (MG e ES). 2. Indicadores biológicos. 3. Barragens de rejeitos. I. Cornelissen, Tatiana Garabini. II. Ribeiro, Sérvio Pontes. III. Universidade Federal de Ouro Preto. IV. Título.
Bibliotecário(a) Responsável: Celina Brasil Luiz - CRB6-1589 B823s
https://sei.ufop.br/sei/controlador.php?acao=documento_imprimir_web&acao_origem=arvore_visualizar&id_documento=100129&infra_sistema=1… 1/1 UNIVERSIDADE FEDERAL DE OURO PRETO
REITORIA
INSTITUTO DE CIENCIAS EXATAS E BIOLOGICAS
PROGRAMA DE POS-GRADUACAO EM ECOLOGIA DE BIOMAS TROPICAIS FOLHA DE APROVAÇÃO
ELLO BRASIL RIBEIRO DA SILVA
A Assimetria Flutuante Pode Ser Usada Como um Bioindicador Ambiental Causado por Rejeito de Mineração? Membros da banca
Dra. Yumi Oko - Universidade Federal de Minas Gerais
Dra. Giselle Mar ns Lourenço - Universidade Federal de Minas Gerais Dr. Sérvio Pontes Ribeiro - Universidade Federal de Ouro Preto Versão final
Aprovado em 04 de maio de 2020 De acordo
Professor (a) Orientador (a) Dr. Sérvio Pontes Ribeiro - Universidade Federal de Ouro Preto
Documento assinado eletronicamente por Servio Pontes Ribeiro, PROFESSOR DE MAGISTERIO SUPERIOR, em 25/09/2020, às 15:05, conforme horário oficial de Brasília, com fundamento no art. 6º, § 1º, do Decreto nº 8.539, de 8 de outubro de 2015.
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Agradecimentos
Agradeço imensamente a minha Mãe por me apoiar em todas as minhas escolhas, por ser minha fortaleza, meu alicerce. À minha querida Avó que, mesmo com tanta dificuldade, sempre me incentivou a buscar o meu melhor. Ao Lucas, que tanto me ajuda, me apoia e me incentiva. Obrigado pela
paciência, compreensão e carinho. Aos meus amigos de laboratório, em especialmente à Bárbara, Victor, Fernanda e Glória, que sempre me deram força e sempre me incentivaram. Obrigado por toda ajuda. Aos funcionários, técnicos e professores do DEBIO, sempre prestativos. Ao Secretário do Programa de Pós-Graduação em Ecologia de Biomas
Tropicais, Rubens, por toda atenção. À Vivi, pela atenção e por ter disponibilizado os materiais do herbário para
minhas coletas. À Profa. Dra. Patrícia, por toda paciência e dedicação. Aos meus queridos orientadores, Profa. Dra. Tatiana Cornelissen e ao Prof. Dr. Sérvio Ribeiro, por confiarem em mim, por terem me dado essa
grande oportunidade de transformação profissional e pessoal. Serei eternamente grato a vocês. À CAPES pela concessão de bolsa de mestrado, ao projeto REC - Recuperação dos habitas da mata ciliar e aquático da Bacia do Rio Doce (projeto: 88887,124088/2016-06) pelo apoio financeiro e ao Instituto Federal de Florestas.
SUMMARY HIGHLIGHTS... 1 GRAPHICAL ABSTRACT ... 1 ABSTRACT ... 2 1. Introduction ... 4 2. Methods ... 8 Study area ... 8 Vegetation sampling ... 9
FA, Herbivory and SLA measures ... 10
Data analysis ... 10
4. Discussion ... 15
1 HIGHLIGHTS
We investigated the impact of mining waste discharged on riparian forests
Iron tailings did not represent a source of impact to alter FA levels of plants.
Herbivory is higher in the midbasin, indicating greater nutritional quality. The long history degradation might be a source of stress parallel to the
mud.
2 Samarco dam breach: an environmental disaster on a highly impacted river basin and the use of Leaf Fluctuating Asymmetry for bioindication
Ello Brasil¹, Tatiana Cornelissen², Sérvio Pontes Ribeiro¹
¹Pós-Graduação em Ecologia de Biomas Tropicais (Departamento de Biodiversidade, Evolução e Meio Ambiente/ICEB, Universidade Federal de Ouro
Preto –UFOP, Ouro Preto, Minas Gerais, Brasil; ²Pós-Graduação em Ecologia,
Conservação e Manejo da Vida Silvestre (ECMVS) Universidade Federal de Minas Gerais – UFMG, Belo Horizonte, Minas Gerais, Brasil.
ABSTRACT
In November 2015, the Doce River hydrographic basin, one of the main river basins in Brazil with an European occupation varying from 200-300 years, suffered an environmental disaster, caused by the breach of a mining tailing dam (Fundão dam). We evaluated leaf Fluctuating Asymmetry (FA) as a proxy for environmental stress, along with herbivory levels and specific leaf area (SLA) from plants in a community of riparian vegetation impacted by the iron tailings resulted from this disasters along the Doce River basin. True patterns of FA were detected in the community of riparian plants from the upper Doce River basin. We did not find, however, significant differences in FA levels for the plant community in control and impacted areas, neither for levels of herbivory. However, when comparing the points in upper and mid Doce River, herbivory levels were higher in the mid basin. The same pattern was observed for the SLA levels, indicating that plants from the mid Doce River may have better nutritional quality, being more consumed by herbivores. Although plants in the areas studied are asymmetric, it appears that the mining toxic mud did not represent a source of impact capable to increase further asymmetry to the levels already found in plant communities in places where the tailings did not reach. The long history of
3
degradation of the Doce River basin may be a source of stress in the plant community parallel to that caused by the mud. Thus, other factors associated with land-use intensity and abiotic factors may influence plant stress, levels of asymmetry and herbivory and deserve further investigation.
Key words: Doce River, bioindicator, leaf area, herbivory, mining tailing,
4 1. Introduction
Biomonitoring biodiversity under environmental gradients is a valuable working tool for the identification of anthropic and/or natural changes on biological communities and ecosystems (Gerhardt, 2000). A great challenge, however, is the lack of control of what may be a healthy ecosystems to define what would be the impact scale of a certain event, as human activities over the centuries (Friberg et al., 2011). Still, environmental stress may be revealed by the use of biomonitoring tools, especially for early warning of decline in environmental quality (Depledge and Galloway, 2005). A quickly, simply and cheap way to understand the negative impacts of environmental alteration is through the use of tools that detect possible instabilities in organisms development (Palmer, 1994).
Fluctuating asymmetry (FA) is a widespread tool to detect and measure developmental instability and consists in the analysis of small phenotypic variation in bilateral characters, resulting from the failure to correct genetic noises during orthogenetic development (Beasley et al., 2013). Because the development of both sides of a bilateral organism is expressed by the same genes, FA indicates an inability of genotypes to express phenotypes. Interference during the development process is observed when organisms are, for example, subjected to certain biotic and/or abiotic stressful conditions (Graham et al., 2010).
Significant increases in FA have been studied in plants and animals, in response to several environmental stress, such as climatic conditions (Møller et al., 2018), temperature (Kozlov and Zverev, 2018), urbanization (Frota et al.,
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2019), pollution (Guo et al., 2017), salinity (Cornelissen and Stiling, 2011) and biotic interactions, such as competition (Chirichella et al., 2020), predation and parasitism (Cuevas-Reyes et al., 2011). Previous studies indicate higher levels of FA in individuals that suffered severe negative anthropogenic disturbance (Beasley et al., 2013), which can reduce fertility and cause lowered growth rates (Mal et al., 2002). Additionally, recent studies suggest the use of FA as an efficient tool to monitor population ecological stresses. Most studies addressing variation in FA are conducted for populations of plants (e.g. (Cuevas-Reyes et al., 2018) and animals (Coda et al., 2017; Frota et al., 2019) and only a few have addressed FA variation at the community’s scale, except for birds in fragmented landscapes of Atlantic Forest (Anciães and Marini, 2000) and butterflies along elevation gradients in Brazilian campos rupestres (Henriques and Cornelissen, 2019).
Besides being an intrinsic trait and a predictor of environmental health, FA can also be used as an indicator of plant nutritional quality for herbivores (Cornelissen and Stiling, 2005). Likewise, herbivory levels can be altered due to stress conditions experienced by plants and these may present a lower capacity for chemical protection and production of secondary compounds in the leaves, causing a decrease in chemical defenses. Moreover, stressed plants tend to reduce the protein synthesis, leaving more nitrogen as available amino acids in the leaves, which also favor the attack by herbivorous insects (Cornelissen and Stiling, 2005; Ribeiro et al., 2016). Another trait that has also been used as an indicator of plant quality and globally associated to herbivory is specific leaf area (SLA) (see Ribeiro and Fernandes, 2000; Kozlov et al., 2015). Higher SLA values
6
indicate reduced investments in defense on leaves and plants with high SLA are expected to be more consumed by insects (Cornelissen et al., 2003).
In November 2015, the Doce River hydrographic basin, one of the main river basins in Brazil, between 200 (mid-basin) to 300 years (upper basin) of European occupation, suffered an environmental disaster, caused by the breach of a mining tailing dam (Fundão dam belonging to the Samarco Company), located in the sub-district of Bento Rodrigues, in the Mariana municipality, Minas Gerais State. The tailing was considered the largest environmental disaster of this kind in 100 years in the whole planet (Carmo et al., 2017; Fernandes et al., 2016). The dam rupture dumped approximately 43 million m3 of alkaline mineral
tailings, rich in heavy metals, esters and amines, damaging the regions silting, causing deposition of tailings along the riverbed and adjacent banks, impairing the environment natural regeneration process, especially the riparian vegetation (Fernandes et al., 2016; Santos et al., 2019). This impact summed up to a long-term intense land use, by agriculture and urbanization. Disturbances layers in time scale likely accumulated environmental stress on the riparian vegetation beyond the direct destruction of some habitats. Likewise, the impact may have distinct effects between the upper and the mid-basin. In one hand, vegetation on the montane part of the basin is adapted to coexist with high natural levels of heavy metals (Ribeiro et al. 2017), but were in large scale physically impacted by the strength of the mud flow; in the other hand, the mid-basin riparian forest were not destroyed by the mud flow, but the tailing accumulated along the margins, changing the chemical composition of the soil, in an ecosystem where there is no natural high level of heavy metals.
7
This study aimed to evaluate the negative impact caused in the riparian forest of the Doce River basin as a consequence of iron tailing caused by the Fundão dam rupture. We tested the following predictions: i) plant communities impacted by iron tailing will exhibit higher levels of asymmetry, herbivory and SLA than plant communities not directly impacted; ; ii) the impact of iron tailing on the vegetation will be more severe in the mid-basin than in the upper basin, causing higher levels of asymmetry in the former, due to the fact that high levels of heavy metal is a natural condition in the high altitudes of the Doce River basin; iii) herbivory will be positively related to plant SLA.
8 2. Methods
Study area
The Doce River basin has 83,400 km² of drainage and runs 879 km from its source in the Mantiqueira and Espinhaço mountains in Minas Gerais state, to the Atlantic Ocean, in the state of Espírito Santo (Marcuzzo et al., 2011). The Doce River basin has elevations that vary from zero to 2,627 m a.s.l. and its predominant vegetation is in the Atlantic Forest domain, with semideciduous seasonal forest (Marcuzzo et al., 2011). The climate is predominantly tropical in altitude (Köppen classification: Cwb). The average annual rainfall ranges from 900 mm to 1,500 mm; and the average temperature is 18ºC (Alvares et al., 2013; Cupolillo et al., 2008).
Study system
Plant community sampling was conducted in 2018, three years after dam breach, at nine sample areas in different rivers. Three areas were not directly impacted by mud and were used as control areas. Six of these areas were impacted by the mud, three in upper of the basin and three in the mid basin (Fig.1).
9
Figure 1 - Location map of sampling points in the Doce River basin in Minas Gerais. Green circles indicated control areas in the upper basin, red squares indicate impacted areas in the upper basin, yellow squares indicate impacted areas in the mid Doce River basin and brown triangles indicate the location of the Fundão dam breach (Map: Glória Soares).
Vegetation sampling
Five riparian individual plants were selected in each area in August 2018. Plants of different species were located two or three meters from the river margin where the tailings accumulated, and were 50 meters apart from each other. The selection criteria were shrub or young tree plants with more than 5 mm of DBH, an average height of 1.5 m and sufficiently mature leaves for collections. From each individual plant, we sampled 10 intact leaves around the plant and 20 damaged leaves from a randomly chosen branch at a distance. The damaged leaves were sampled from the basal to the apical portion of a branch chosen at random. When plants did not have enough leaves in a single branch, another branch was chosen with the same criteria. All leaves were pressed, herborized,
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digitalized and analyzed using the ImageJ software, with the measurement adjusted in millimeters (Schneider et al., 2012).
FA, Herbivory and SLA measures
Fluctuating asymmetry was calculated in 10 intact leaves randomly chosen from each individual (n=6), totaling 300 leaves. Three areas were selected at random for equivalence of the sampling effort. We measured the right (RW) and left (LW) widths of the leaves, using the mid vein as a reference in all digital images. Additionally, 20% of the leaves were randomly selected and remeasured, without reference to previous measurements to eliminate the possibility of measurement errors (Kozlov, 2017). FA index from the riparian community was calculated using the average difference between the widths on each side, adjusted by the group variance (Anciães and Marini, 2000).
To evaluate herbivory levels, the remaining 20 damaged leaves from each individual were measured (n=45), totaling 900 leaves. Herbivory levels were determined as the ratio of the leaf area removed by chewing herbivores to the total leaf area (mm²) ²) and expressed as percentage of leaf area removed. To evaluate SLA, leaves were oven dried, weighed with a precision scale and their mass was measured in mg-1. The SLA was calculated by the ratio of the leaf area
(mm²) to the leaf biomass (mg-1) (Cornelissen et al., 2003).
Data analysis
To identify the existence of asymmetry in the riparian community, the RW-LW values were submitted to the Lilliefors normality test (α = 0.05) and to a one-sample t-test (μ = 0). For true patterns of asymmetry to be found, the mean of the difference between the leaf sides must not differ from zero, and the data need
11
to be symmetric and normal distributed. In order to discard measurement errors a mixed ANOVA model was created using the widths twice as dependent variables and both AF measurements as independent factors (Palmer and Strobek, 1986). General linear models (GLM) were constructed to evaluate the impact of iron tailings on FA values, on herbivory levels and on SLA between the impacted areas and control areas, and the upper and mid basin. For FA, we used the points as replicates. For herbivory and SLA, the plants were used as replicates. In GLM models we used impact by iron tailing, upper and mid basin as the predictive variable and FA, herbivory and SLA as response variables. To test the existence of the relationship between herbivory and SLA, the average percentages of leaf area removed were response variable and SLA predict variable, using GLM. Statistical analyses were performed using SYSTAT 12 software (Wilkinson 1992).
12 3. Results
True patterns of FA were found in the riparian community of Doce River basin. The measured values of the right and left sides of the leaf were normally distributed, whose mean of -0.023 mm, did not differ significantly from zero (t = 0.779, p = 0.803), showing no evidence of directional symmetry or antisymmetry. The index of repeatability indicated that FA measurements were accurate (r = 0.823; P < 0.001), discarding the possibility of measurement errors. The absolute leaf width deviations (|RW-LW|) varied from 0 to 7.10 mm. FA index of the riparian communities impacted by iron tailings (1.72 mm ± 0.59; mean ± SE) did not differ from non-impacted areas (1.17 mm ± 0.06) (F1,4 = 0.866,
p = 0.405) (Fig. 2A). When we categorized the areas as belonging to upper and mid basin areas, no significant difference in FA index was also found among communities in the Doce River basin (F2,6 = 0.492, p = 0.634) (Fig. 2B).
Fig. 2. Fluctuating Asymmetry of riparian communities (A) between control, impacted areas (B) between impacted upper and mid basin of Doce River.
13
Herbivory in plants impacted areas by iron tailing was not different than that observed in not impacted pants (F1,43 = 2.43; p = 0.126) (Fig. 3A) Impacted
areas by iron tailings exhibited levels of herbivory with mean (SE) values of almost 10% of leaf area lost to herbivores (9.71±1.16), whereas control areas averaged almost 7% of leaf area damaged (7.02 ± 0.68).
The greatest herbivory levels were observed in impacted areas in the mid basin, where plants loss 12.3% of leaf area and the lowest leaf removal was in the control area with about 7% of leaf area loss to herbivores (F1,43 = 7.795, p =
0.008). When comparing the upper and mid Doce River, the herbivory levels of the mid basin were significantly higher than the other areas (Fig. 3B)
Fig. 3. Herbivory of riparian plants (A) between control and impacted areas (B) between control, impacted upper and mid basinof Doce River.
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SLA in impacted areas was significantly higher in impacted than in not impacted areas by iron waste (F1,43= 5.127, p = 0.028) (Fig. 4A). Areas impacted
by the iron tailing in the mid Doce River exhibit higher SLA values (F1,43= 8.00, p
= 0.001) (Fig. 4B). There was also no significant relationship between SLA and herbivory (p> 0.05).
Figure 6 – Specific Leaf Area (SLA) of riparian plants (A) between control and impacted areas (B) between control, impacted upper and mid basin of Doce River.
15 4. Discussion
This study revealed patterns of fluctuating asymmetry in the riparian plant communities of the Doce River Basin, supporting this parameter as a quick, low-cost, easy-handling and efficient tool to detect abiotic stresses (Anciães and Marini, 2000; Beasley et al., 2013). However, FA did not differ between waste-impacted and control areas, which accumulate other historical disturbances. Hence, we rejected the hypothesis that levels of FA should be higher in areas impacted by the environmental disaster in an already impacted environment. We found true patterns of FA in all areas, however, these values were not related to the mining impact. We here suggest possible mechanisms that interfere with the detection of environmental stress in these areas impacted by the dam rupture.
Although, we did not find an association between FA and the impact caused by iron tailing, several previous studies, as reviewed quantitatively by Beasley et al. (2013), have suggested the use of this tool to evaluate the impact of distinct anthropogenic sources. We propose that time after impact might be an important factor to be accounted when using FA as a measurement of stress. From the studies reviewed in a meta-analysis on the effects of FA as a tool for developmental instability detection, most of them (70%) were conducted right after disturbances occurrence indicating that timing of sampling might be important if this tool is to be used. We suggest that the impact caused by damage may not represent a stress factor during plant development strong enough to cause differences in leaf asymmetry three years after impact of the dam rupture. Besides that, the long history of degradation the land use in the Doce River basin may have level up similar effects as those caused by the tailings on the remaining
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riparian vegetation, therefore causing the absence of difference in plant developmental instability amongst areas.
Although previous studies indicate changes in levels of leaf area removed by chewing herbivores in modified environments (Cornelissen and Stiling, 2005), we did not observe that herbivory pattern changed with impact of the tailing. Leaf area removed by insect herbivores in the impacted areas was around 10%, which is higher than the global average of herbivory, as evaluated by Kozlov et al. (2015). In the control areas, plants experienced around 7.5% of leaf area loss to herbivores, which is closer to the global data on herbivory. Although the control areas were not affected by the mud, the riparian community may be affected by other factors, such as urbanization (along with air pollution), pasture, and agriculture (along with perticide applications). Even under natural conditions, plants are affected by several factors during their growth and development, such as temperature, drought and changes in precipitation regimes (Kozlov and Zverev, 2018, Maldonado-López et al., 2019). The highest level of herbivory in the impacted areas may be in accordance with an assessment of plant stress (PSH) by White (1969) and White (1984) and other studies that have found higher herbivory in plants of lower nutritional quality, as an strategy of insects to compensate for tissue of low quality
After the dam rupture, an avalanche of mining tailings buried the riparian forests as well as conservation areas close to the rupture, causing total vegetation cover removal, making natural regeneration on inert tailings impossible (Fernandes et al., 2016). The tailings were also deposited along the whole river margins and, although they did not destroy the vegetation in the mid-basin, these plants now coexist with a severely contaminated layer of mud, which
17
covered the original soils. We suggest that the stress caused by tailings was homogenized in these areas after 36 months of the disturbance and communities evolved to new steady-states after impact, as shown for other disturbed systems (Lauck, 2006; Michaelsen et al., 2015). The Fundão dam rupture is not the first case of degradation in the Doce River basin. The region has a long history of impact, occupation and exploration that began in the early 18th century, with the gold exploration cycle, intensified by the construction of the Vitória-Minas railway for the disposal of iron and precious stones (Coelho, 2009). The industrialization process strengthened human exploration and currently, activities such as mining, agriculture, swine, and forestry have become scenarios current throughout the hydrographic basin (Coelho, 2009; Santolin et al., 2015).
Our study indicates that FA is a trait present in the riparian Doce River basin community. However, we do not consider FA to be a reliable proxy for stress caused by tailings, in areas that have been historically impacted by others' cumulative stressors that may mask the results. The approach with fluctuating asymmetry at the community level is recent and its application should be developed in search of an additional tool in biomonitoring studies.
18 Conflict of interests
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
We are grateful to Federal University de Ouro Preto (UFOP), State Forestry Institute (IEF) and Parque State of Rio Doce (PERD) staff for logistical provision
Funding
This work was supported by the Fundação Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES 88887.185914/2018-00); RecRioDoce and authors acknowledge funding from CNPq and FAPEMIG.
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