Microclimate and mining stresses the diversity of earthworms and further impact the regeneration of forests along the Rio Doce

Microclimate and mining stresses the diversity of earthworms and further impact the regeneration of forests along the Rio Doce | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article Microclimate and mining stresses the diversity of earthworms and further impact the regeneration of forests along the Rio Doce Walisson Kenedy-Siqueira, Yumi Oki, Marcos Paulo Santos, João Carlos Gomes Figueiredo, and 5 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-5544777/v1 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 14 Nov, 2025 Read the published version in Biological Invasions → Version 1 posted 5 You are reading this latest preprint version Abstract Soil structure, along with the fauna and plant biodiversity it sustains, can be affected by various factors, including both natural and human-induced disturbances such as climate fluctuations and mining activities. Earthworms are ecosystem engineers highly affected by these changes in soil conditions. In the present study, we evaluated earthworm community in different climatic periods and their impact on plant diversity in a region affected by mining tailings. Earthworm diversity was significantly higher during the period of higher precipitation, both in areas affected by mining tailings and in reference sites. Additionally, the composition of earthworm species was impacted, showing predominantly gains despite the influence of mining waste. The total and invasive abundance of earthworms was linked to greater plant diversity in the regenerating stratum of reference sites but not in areas impacted by mining waste. These findings highlight the potential consequences of climate change and mining disasters on earthworm communities, as well as on ecosystem structure and dynamics. Moreover, they underscore the environmental impacts of the world's largest mining disaster on earthworm diversity within one of the planet's key biodiversity hotspots, emphasizing the urgent need for improved recovery strategies. Ecosystem engineers Habitat disturbances Invasive earthworms Mining tailings impact Samarco mining disaster Figures Figure 1 Figure 2 Figure 3 Figure 4 Introduction The diversity and dynamics of species below and above ground are influenced by the frequency and intensity of disturbances in an ecosystem (Walsh and Johnson-Maynard 2016 , Yuan et al. 2021 , Laigle et al. 2021 , Li et al. 2024 ). The disturbance hypothesis suggests that diversity is higher under intermediate levels of disturbance (Huston 1979 ). Low diversity can occur in the absence of disturbance, due to the persistence of superior competitors or under very intense disturbance regimes, due to the persistence of native or exotic colonizers that can become invaders (Huston 1979 , Eisenhauer et al. 2014 ). Climatic variations are natural disturbances that primarily affect precipitation levels and temperature in specific regions (Legg 2021 ), impacting species and populations below ground, impairing development, reproductive rates, immunity to disease, and mortality rates (Beier et al. 2012 , Thakur et al. 2018 ). They can also affect species composition, accelerating extinction rates and migration, thus reducing the diversity of terrestrial species responsible for important ecosystem functions (Singh et al. 2019 ). For example, extended periods of drought and intensified short-term rainfall patterns have a direct impact on resource availability, soil conditions, and the diversity of soil-dwelling invertebrates (Yadav and Mullah 2017 , Phillips et al. 2019 , Singh et al. 2019 ). Furthermore, anthropogenic changes that directly modify the soil (Barros et al. 2004 ), such as deforestation, agricultural practices, and mining are among the factors that can deeply affect soil physical and chemical conditions and the populations and diversity of soil organisms (Nearing et al. 2004 ). These anthropogenic changes have resulted in the loss and degradation of habitats, often leading to soil pollution, which represents a strong stressor for native edaphic species to persist or recolonize. Among the soil organisms, earthworms are true ecosystem engineers that facilitate nutrient cycling by processing organic matter (Frouz 2018 , Barthod et al. 2020 ). During their feeding activities, earthworms construct burrows that facilitate soil aeration and rainwater infiltration (Singh et al. 2016 , Brown et al. 2018 ). The ingestion of organic matter and its subsequent excretion in castings increases plant nutrient availability to roots (Guhra et al. 2020 ). Hence, earthworms facilitate nutrient cycling and plant growth promotion. On the other hand, some invasive earthworm species have a detrimental role on plant survival (Hale et al. 2006 , Larson et al. 2010 ). Experimental studies in closed and open systems have demonstrated that in circumstances where organic matter is scarce, some earthworm species at high abundance can compete with plants for nutrients, or even damage their growth by attacking plants in the early stages of their life cycle (Hale et al. 2008 , Larson et al. 2010 , Sackett et al. 2013 ). For instance, the tropical species Pontoscolex corethrurus has been shown to negatively affect soil structure and hydraulic processes (Hallaire et al. 2000 , Barros et al. 2004 ). This species has been reported as an invader in the Brazilian Amazonia and Mata Atlantica forests and pastures, possibly negatively affecting soil processes (Demetrio et al. 2022 ). Furthermore, it has high reproduction rates and resistance to disturbances (Lavelle et al. 2016 , Taheri et al. 2018 ). Other earthworms can also be considered invasive, such as Amynthas gracilis , a highly competitive species of Asian origin (Brown and Fragoso 2007 , Zhang et al. 2010 ), known to affect soil structure and nutrient cycling as well as plant growth, though generally in a positive manner (Brown et al 1999 , Peixoto & Marochi 1996 ). Several other studies have indicated that the presence of some earthworm species may have detrimental impacts on soil parameters associated with plant diversity (Gibson et al. 2013 , Drouin et al. 2016 , Hale et al. 2016, Craven et al. 2017 , Thouvenot et al. 2024 ). However, these studies were predominantly conducted in temperate regions, and there is a paucity of knowledge regarding the influence of earthworms on plant community structure and diversity in tropical regions (Craven et al. 2017 ), where these ecosystem engineers still need to be fully studied. The invasive potential of native and alien species is both linked to a set of traits that the species possesses and to anthropogenic disturbances (Pop and Pop 2006 , Mathieu et al. 2024 ). The invasion of altered environments complicates efforts to restore the essential functions performed by native species, crucial for maintaining ecosystems (Frelich et al. 2019 ). For instance, the collapse of the Samarco mining tailings dam in Mariana, Brazil, resulted in the burial and destruction of the native fauna, fungi, and flora of a significant portion of the riparian forest of the Rio Doce Basin (Fernandes et al. 2016 , Carmo et al. 2017 ). The catastrophic event occurred nine years ago, yet its residual effects can still be observed in the physical alterations of the soil and the decline in the biomass of native earthworms in the region (Nadolny et al. 2024 ). These modifications may compromise the ecological functions of earthworms, which could impact the recovery of native plant species in the affected sites (see Craven et al. 2017 , Ferlian et al. 2017 , Frelich et al. 2019 ). The return of native vegetation represents a crucial initial phase of environmental resilience, occurring primarily through the spontaneous regeneration of vegetation in areas affected by some forms of disturbance (e.g., Chazdon 2013 , Chazdon and Guariguata 2016 , Crouzeilles et al. 2017 ). Against the backdrop of climate disruptions and soil alterations in the Rio Doce riparian forest, this study aimed to (a) assess the diversity of earthworms in two distinct climatic periods (high and low precipitation), and (b) verify the relationships between native and invasive earthworm abundance on plant diversity in the regenerating stratum. Concerning the diversity of earthworms, climate disturbances, and the impacts of soil contaminated with mining tailings, the following hypotheses were proposed: (H1) in sites with soil not impacted by mining tailings (from here on, referred to as reference sites: Ramos et al. 2024 ), earthworm diversity is greater in periods of high precipitation than in periods of low precipitation; (H2) conversely, in sites with soil impacted by mining tailings (from here on, referred to as impacted sites: Fernandes et al. 2025 under review), earthworm diversity is smaller in periods of low precipitation than in periods of high precipitation; (H3) due to changes in precipitation, earthworm species composition is mediated by the species gains in reference sites and losses in impacted sites. Concerning the abundance of earthworms and the regenerating vegetation of the riparian forest, we hypothesized that: (H4) invasive earthworm abundance is negatively correlated to juvenile plant species diversity in reference and impacted sites, and (H5) native earthworm species abundance is positively correlated to juvenile plant species diversity in reference and impacted sites. Material and Methods Sampling design Sampling was conducted on earthworms and regenerating vegetation (juvenile plants) in five regions of riparian forest along the Rio Doce in Minas Gerais, Brazil (Fig. 1 A). In each region, three areas that had been impacted by mining tailings (Impacted Sites) and three areas that had not been impacted by tailings were sampled (Reference sites). To sample regenerating vegetation, in each area, 15 plots measuring 5 x 5 m were constructed, resulting in a total of 450 plots (Menino et al. 2012 , Neves et al. 2024 , Fernandes et al. 2025 in review). The earthworms were sampled in two consecutive years, May 2023 and May 2024, at the end of the rainy season and the beginning of the dry season. Following a modification of the Tropical Soil Biology and Fertility (TSBF) Programme method (Anderson and Ingram 1993 ), earthworms were sampled a 0.25 x 0.25 x 0.2 m soil monoliths in each plot, resulting in a total of 900 monoliths. Each monolith was manually sorted in the field, and the earthworms were collected and placed in plastic vials containing 80% alcohol. The vials were labeled and sent to the Laboratory of Reproduction and Fish Communities, Federal University of Paraná (LRFC - UFP) for sorting, quantification, and preliminary identification. The sorted material was subsequently sent to the Laboratory of Soil Biology, State University of Maranhão (LSB - UEMA) for identification at the lowest possible taxonomic level by co-author LMHG. The taxonomic identification of the earthworms was based on the keys of Righi ( 1995 ), Blakemore ( 2002 ), dos Santos et al. (2017), and Hernández-García et al. ( 2018 ). After taxonomic identification, the species were classified as native and non-native (invasive) for the ecosystem studied (Atlantic Rainforest) according to Demetrio et al. (2023). The samples were deposited in the earthworm collection of the Department of Genetic, Ecology and Evolution of the Federal University of Minas Gerais (UFMG). The plant saplings were sampled by quantifying and collecting all the plant species in the regenerating stratum with a diameter at breast height < 5 cm (1.30 m from the ground) and diameter at soil height ≥ 1 cm taken from each plot (N total =450) in May 2023. The sampled plants were pressed in the field, labeled, and sent to the Laboratory of Phytogeography and Evolutionary Ecology, Federal University of Lavras (LPEE - UFLA) for identification at the lowest possible taxonomic level by RMS. The plant material was deposited in the Herbarium of Norte Mineiro (ICA-UFMG) and the Herbarium of Montes Claros, Minas Gerais (Unimontes). The Angiosperm Phylogeny Group IV system was used to classify the species into families (APG IV 2016). Averages of precipitation and temperature were collected, 15 days before each earthworm sampling, from the precipitation data of the closest weather station to each area (N = 30) to characterize the climatic period of the samplings. The mean precipitation of the second year of sampling was approximately five times higher than that of the first sampling (Fig. 1 B). Due to the disparate precipitation patterns observed in the samples, we designated sampling 1 as "Low precipitation" and sampling 2 as "High precipitation". Statistical analysis Statistical analyses were conducted using R software (R Core Team 2024 ). The regional diversity of earthworms and plants was calculated by Shannon indices using the "Vegan package" (Oksanen et al. 2022 ). We performed generalized linear mixed models (GLMM) to test the variation in the effects of climatic variation (high vs. low precipitation) on earthworm diversity and the relation between earthworm abundance and juvenile plant diversity. Site location and region were considered random effects. The models had Gaussian distribution and were tested using analysis of variance (ANOVA). When the objective was to analyze the effects of climatic disturbances on sites, the diversity calculations were carried out separately for each condition of the sites (Reference and Impacted). When the aim was to test the relation between earthworm abundance and juvenile plant diversity, the tests were carried out separately for native and invasive earthworms using data only from 2023, when both plants and earthworms were sampled. The models were considered significant when the P value was less than 0.05. In parallel, species composition was calculated using the temporal beta-diversity index (TBI), which employs the pairwise Sorensen dissimilarity index (Year 1: low precipitation and Year2: high precipitation) with the "adespatial package" (Dray et al. 2022 ). The TBI value can be decomposed into two components: species losses (B) and species gains (C). A positive value of [C – B] indicates that the site was dominated by gains, whereas a negative value denotes overall losses of species (Legendre 2019 ). The [C – B] difference across all plots was tested for statistical differences using the parametric P value and permutational paired t-test (N = 999 permutations) computed for the C and B statistics from all plots. The B and C statistics were then used to produce B-C plots, with B (losses per plot) in the abscissa and C (gains per plot) in the ordinate (Legendre 2019 ). Furthermore, the B and C per plot were compared between reference and impacted sites, through generalized linear models (GLM) with Binomial error distribution and tested using ANOVA (P values less than 0.05 were considered significant). Results Trends in abundance and richness of earthworms A total of 2158 individual earthworms were collected, belonging to 19 species during the two consecutive sampling years (Table 1 ). Of this total, 616 individuals were collected in the first year (native: 31, invasive: 585 individuals) and 1542 individuals in the second year (native: 218, invasive: 1324 individuals). Of this total, 1130 individuals were found in the impacted sites (native: 138, invasive: 992 individuals) and 1028 individuals in the reference sites (native: 111, invasive: 917 individuals). During the first sampling (2023), seven species belonging to four families were found: P. corethrurus , Rhinodrilus sp.1 and sp.2 (Rhinodrilidae), Righiodrilus sp.2 and sp.3 (Glossoscolecidae), A. gracilis (Megascolecidae), and some individuals of the family Ocnerodrilidae spp. The native Ocnerodrilidae were found exclusively in the impacted site, while the native R. motucu , Righiodrilus sp.1 and sp.2, as well as the non-native A. gracilis and P. corethrurus were found in both impacted and reference sites (Table 1 ). In the second year of sampling (2024) more and different species were recorded, with the native R. motucu , three species of Ocnerodrilidae, and one of Glossodrilus occurring in the reference sites. Rhinodrilus sp.3 and Ocnerodrilidae spp. were only recorded in impacted sites while the other native species Ocnerodrilidae sp.1, Righiodrilus sp.1, and Rhinodrilus sp.1 were sampled in both reference and impacted sites (Table 1 ). The invasive species A. corticis was sampled only in the reference area, while juvenile Megascolecidae spp. and P. elongata were sampled only in the impacted site. The other invasive species A. gracilis , D. bolaui and P. corethrurus were sampled in both reference and impacted sites (Table 1 ). Rainfall impact on earthworms Precipitation resulted in major changes in earthworm diversity (F (1, 869) = 63.804, P = 4.349e-15), with approximately 10 times higher diversity in the period with more rainfall (0.107 ± 0.012) than in the drier period (0.012 ± 0.004) (Fig. 2 A). Species richness was also higher, with nearly twice the number of species recovered in the wet (17 spp.) than dry year (8 spp.) samples. Earthworm diversity also varied according to the precipitation period in reference (F (1, 434) = 25.42, P = 6.787e-07) and impacted sites (F (1, 434) = 38.504, P = 1.277e-09). In reference sites, diversity was approximately 6 times greater in the period higher (0.090 ± 0.015) than lower precipitation (0.015 ± 0.006) (Fig. 2 B). In impacted sites, diversity was approximately 13 times greater in the period with higher (0.123 ± 0.018) than lower precipitation (0.009 ± 0.005) (Fig. 2 C). Species composition also responded to precipitation (Stat = 5.764, P = 2.22298e-08, P permutation = 0.001). The variation in species composition was mediated by species gain (TBI = 0.658), with more than twice as many species gained (0.455) as lost (0.203) in the period with higher precipitation (Fig. 3 A). Species composition also varied with precipitation within each site: reference (Stat 3.608, P = 0.0004, P permutation = 0.001) and impacted (Stat = 4.520, P = 1.316722e-05, P permutation = 0.001). In reference sites, approximately twice as many species were gained (0.673) than lost (0.326) with higher precipitation (TBI = 0.641, Fig. 3 B). In impacted sites, the variation was also mediated by species gain (TBI = 0.675), with more than twice as many species gained (0.708) than lost (0.291) in 2024 (Fig. 3 C). Species composition did not vary between sites with similar values of TBI for impacted and reference treatments (Fig. 3 D). Abundance of earthworms and the regenerating vegetation Total earthworm abundance was significantly related to plant diversity (F (1, 449) = 5.798, P = 0.01645) and interaction with sites (F (1, 447) = 18.527, P = 2.063e-05). For reference sites, there was a positive relationship between total earthworm abundance and plant diversity (y = 0.85114 + 0.00267x, F (1, 224) = 5.4939, P = 0.0199). However, in impacted sites, this relationship was not significant (y = 0.85114 -0.0006x, F (1, 224) = 0.1106, P = 0.7398) (Fig. 4 A). Native earthworm abundance was not related to plant diversity (F (1, 449) = 3.5439, P = 0.0604) or the interaction with sites (F (1, 447) = 0.8713, P = 0.3511), but the abundance of invasive earthworms was significantly correlated with the diversity of regenerating plants (F (1, 449) = 7.1411, P = 0.0078) and the interaction with sites (F (1, 447) = 19.950, P = 1.01e-05). In reference sites, invasive earthworm abundance was positively related to plant diversity (y = 0.85034 + 0.00285x, F (1, 224) = 6.0578, P = 0.0146) (Fig. 4 B). Conversely, in impacted sites, there was a trend for opposite relationships, though the regression was not significant (y = 0.85034 -0.0006x, F (1, 224) = 0.1540, P = 0.6951). Discussion A total of 19 earthworm species were recorded in the riparian forests of along the Doce River Basin during a two year study. This represents around 4% of the species richness for Brazil (336 species, Brown et al. 2013) and 15% of the species known from the Atlantic Forest (99 species, Demetrio et al. 2023). On the other hand, several of the species were not identified to species level, and many represent new species that must still be described. This highlights the unknown and yet-undiscovered richness of earthworms in the Rio Doce watershed. Therefore, further attention is needed to understand this important guild of ecosystem engineers, particularly considering their on soil processes and plant growth. Additional relevance is observed when we consider that this basin was the theater of the largest impact of a mining dam breach in the world so far (Fernandes et al. 2016 ). This study presents for the first time the temporal nature of earthworm diversity in riparian forest areas impacted by the mining tailings along the Doce River basin. It highlights climate as a key modulator of earthworm diversity, a vector of change shown to be important also at global level (Phillips et al. 2021 ). The gain in species observed between sampling years confirms the need for monitoring and inventories performed in periods of higher rainfall. The trend found in the impacted sites indicates it is a phenomenon independent of land cover. Rainfall maintains soil moisture which is directly related to earthworm abundance, biomass and activity (Yadav and Mullah 2017 ; Singh et al. 2019 ). Earthworms breathe through their skin and must keep it moist at all times (Sharma and Poonam 2014 ). Drier soil can also induce earthworm aestivation or diapause (Maleri et al. 2008). Considering that earthworms are the main soil-engineering macroinvertebrates, climate change can compromise the functioning of ecosystems and the network of ecological interactions (Singh et al. 2019 ). Our results clearly show that the magnitude of the effect of climate on these organisms is dependent on the climatic condition, over and above the condition of the soil itself. Of the earthworm species recorded, one-third were invasive (six species) in the sampled areas of the Atlantic Forest. These results confirm observations of Demetrio et al. (2023), who reported that 39% of the species redorded in the Atlantic Forest are invasives. This scenario reinforces a warning about the silent invasion of exotic earthworms in one of the world's diversity hotspots (Myers et al. 2000 ). Although apparently silent, some of these invasive species, including A. gracilis reported here, possess high physiological and reproductive plasticity, which has been associated with their ability to outcompete native species (Novo et al. 2015 ). Furthermore, we noted in this study that the most abundant species (86% of the individuals sampled) was the invasive and peregrine species P. corethrurus , a highly plastic r-strategist with flexible diet (Taheri et al. 2018 ). This species, along with Eisenia fetida , is considered a bioindicator of soils contaminated by heavy metals due to their high tolerance to such conditions (Sá et al. 2024 ). Although P. corethrurus is also found in undisturbed environments, land use change has been identified as one of the main factors explaining its abundance in various parts of the world (Marichal et al. 2010 ). However, P. corethrurus is also known to alter soil structure depending on soil properties (Taheri et al 2018 ), and cause soil compaction in clayey soils, especially with low concentrations of organic matter and in the absence of species that do not promote decompaction (Hallaire et al. 2000 ). According to Hallaire et al. ( 2000 ), it can increase macroaggregation and reduce water infiltration and soil moisture. On the other hand, it can favor the bioavailability of nitrogen and phosphorus in the soil and consequently be beneficial for the establishment and development of plant species (Teng et al. 2016 ; Trap et al. 2021 ). In our study, we observed that the abundance of earthworms, even predominantly invasive species, was positively correlated with an increase in plant diversity in the regenerating stratum of reference riparian forest sites. Conversely, in riparian forests with soils impacted by mining waste from the Fundão dam, higher earthworm abundance was associated with lower plant diversity. In the reference areas, the forests support a variety of earthworm species and other soil macrofauna that may help mitigate the negative effects of invasive species, such as soil compaction and population imbalances (Barros et al. 2004 ). In areas impacted by mining, earthworms can alter the mobility of heavy metals in the soil through their feeding, digging, and/or casting (Duarte et al. 2012 ; Boukirat and Maatoug 2021 ). The way in which heavy metals are mobilized varies according to the species of earthworm and the type of metal (Boukirat and Maatoug 2021 ). In this sense, several studies have evaluated vermicomposting, i.e. the removal or degradation of contaminants from the soil by earthworms, as an alternative for rehabilitating areas contaminated by heavy metals (Ge et al. 2023 ), consequently increasing the chances of greater re-establishment and plant development. However, this does not seem to be the case for the earthworm species found in the impacted areas. It is known that some earthworm species such as E. fetida can further increase the bioavailability of heavy metals in the soil and interfere with plant development (Ruiz et al. 2009 ). This may be the case with P. corethrurus , suggesting that experimental studies are needed to better elucidate the relationship between these earthworms and tailings-impacted soils with high pH, and high silt and iron concentrations. Our previous studies also indicate that in sites with deposition of mining tailings, some ecological processes have been altered (Nadolny et al. 2024 ). Regarding our original hypotheses, we were able to confirm H1 and H2, with higher earthworm diversity being found in both reference and impacted sites in the year with higher precipitation (2024). Furthermore, we found that earthworm species composition was affected by climate and revealed mostly species gains, though these occurred in both reference and impacted sites, so H3 was not totally confirmed. Finally, regarding the regenerating vegetation of the riparian forest, we found that both total and invasive earthworm species abundance were positively correlated with the diversity of juvenile plant species in reference sites, but not in impacted sites, thus not supporting H4. In contrast, the abundance of native earthworm species was not associated with plant species diversity in either reference or impacted sites, thereby refuting H5. In conclusion, our results highlight the importance of climate variation and mining tailings on earthworm communities and the consequent impacts on vegetation structure and dynamics. In addition, this study contributes to a better understanding of the environmental impacts of the largest mining disaster on one of the world's diversity hotspots and of possible mitigating measures to facilitate its recovery. While soil biodiversity has been neglected in the assessments of environmental impacts in the regions impacted by the disaster, this study clearly shows that soil animals must be considered bioindicators and that their interactions with vegetation are important integral parts of ecosystem functioning and recovery. Furthermore, it also reveals that invasive species, such as the dominant P. corethrurus , do not appear to have negative impacts on vegetation dynamics in reference sites, but that this species and the remaining earthworm community are not assisting vegetation recovery in impacted areas. This is an important finding as increasing soil functionality is needed to accelerate ecosystem development and augment its resilience. Further investigation into the potential positive synergies between earthworm communities and key ecosystem processes — such as soil aggregation, water infiltration and retention, plant growth, and the restoration of native vegetation in impacted areas compared to reference sites — is urgently needed. Additionally, strategies to enhance revegetation and facilitate the recolonization of these impacted areas are essential, in order to attract native soil species and foster biodiversity recovery. Declarations Acknowledgements We are grateful to the anonymous reviewers for their suggestions and contributions to the work. The authors thank Daniel Negreiros for his efforts in organizing the data from the initial plant and earthworm sampling, as well as Rubens M Santos for plant taxonomic identification. This research was supported by Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG: APQ-03622-17, APQ-00031-19) and Brazilian Council for Scientific and Technological Development (CNPq, grant no. 316258/2021-0, 312824/2022-0, and 441930/2020-4 to GWF and GGB) as well as the Fundação Araucária (TAX2021231000002). Conflict of interest The authors have no relevant financial or non-financial interests to disclose. Author Contributions All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Walisson Kenedy-Siqueira, Yumi Oki, Marcos Paulo Santos, João Carlos Gomes Figueiredo, Francisco Alves de Amorim Soares and Herlon Nadolny. The identification of the specimens (earthworms) was done by Luis Manuel Hernández-García. The first draft of the manuscript was written by Walisson Kenedy-Siqueira and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript. References Anderson JM, Ingram JSI (1993) Tropical soil biology and fertility. Soil Sci 157: 265. Barros E, Grimaldi M, Sarrazin M, Chauvel A, Mitja D, Desjardins T, Lavelle P (2004) Soil physical degradation and changes in macrofaunal communities in Central Amazon. Appl Soil Ecol 26:157-168. Barthod J, Dignac MF, Le Mer G, Bottinelli N, Watteau F, Kögel-Knabner I, Rumpel C (2020) How do earthworms affect organic matter decomposition in the presence of clay-sized minerals? Soil Biol Biochem 143:107730. Beier C, Beierkuhnlein C, Wohlgemuth T, Penuelas J, Emmett B, Körner C, Boeck H, Christensen JH, Leuzinger S, Janssens IA, Hansen K (2012). Precipitation manipulation experiments–challenges and recommendations for the future. Ecol Lett 15:899-911. Blakemore RJ (2002) Cosmopolitan earthworms: an eco-taxonomic guide to the peregrine species of the world. Canberra: VermEcology. 506 p. Boukirat D, Maatoug M (2021) Bioremediation of lead contaminated soils for sustainable agriculture. Ecol Intensif Nat Resour Sustain Agric 341-380. Brown GG, da Silva E, Thomazini MJ, Niva CC, Decaëns T, Cunha N, Nadolny HS, Demetrio WC, Santos A, Ferreira T, Maia LS, Conrado AC, Segalla RF, Ferreira AC, Pasini A, Bartz MLC, Sautter KD, James SW, Baretta D, Antoniolli ZI (2018) The role of soil fauna in soil health and delivery of ecosystem services. In: D. Reicosky (Eds.): Managing soil health for sustainable agriculture. 1 ed. Cambridge: Burleigh Dodds Science Publishing Limited. P. 197-242. Brown GG, Fragoso C (2007) Minhocas na América Latina: Biodiversidade e ecologia. 1 ed. Londrina (PR): Embrapa Soja. 547 p. Brown GG, Pashanasi B, Villenave C, Patron JC, Senapati BK, Giri S, Barois I, Lavelle P, Blancharf E, Blakemore RJ, Spain AL, Boyer J (1999). Effects of earthworms on plant production in the tropics. In: P. Lavelle, L. Brussaard, P. Hendrix (Eds.) Earthworm management in tropical agroecosystems. 1 ed. New York: CABI Publishing. P. 87-147. Carmo FF, Kamino LHY, Tobias Junior R, de Campos IC, Carmo FF, Silvino G, de Castro KJSX, Mauro ML, Rodrigues NUA, Miranda MPS, Pinto CEF (2017) Fundão tailings dam failures: the environment tragedy of the largest technological disaster of Brazilian mining in global context. PECON 15:145-151. Chazdon RL (2013) Tropical forest regeneration. In S. A. Levin (Ed.). Encylopedia of biodiversity, (2nd edn), pp. 277–286. Academic Press, Waltham, MA. Chazdon RL, Guariguata MR (2016). Natural regeneration as a tool for large‐scale forest restoration in the tropics: prospects and challenges. Biotropica 48:716-730. Craven D, Thakur MP, Cameron EK, Frelich LE, Beauséjour R, Blair RB, Blossey B, Burtis J, Choi A, Dávalos A, Fahey TJ, Fisichelli NA, Gibson K, Handa IT, Hopfensperger K, Loss SR, Nuzzo V, Maerz JC, Sackett T, Scharenbroch BC, Smith SM, Vellend M, Umek LG, Eisenhauer N (2017) The unseen invaders: introduced earthworms as drivers of change in plant communities in North American forests (a meta‐analysis). Glob Chang Biol 23:1065-1074. Crouzeilles R, Ferreira, MS, Chazdon RL, Lindenmayer DB, Sansevero JB, Monteiro L, Iribarrem A, Latawiec AE, Strassburg BB (2017) Ecological restoration success is higher for natural regeneration than for active restoration in tropical forests. Sci Adv 3:e1701345. Demétrio W, Brown G, Pupin B, Novo R, Dudas R, Baretta D, Römbke J, Bartz M, Borma L (2023) Are exotic earthworms threatening soil biodiversity in the Brazilian Atlantic Forest?. Appl Soil Ecol 182:104693. DOI: 10.1016/j.apsoil.2022.104693 Demetrio W, Cavalieri-Polizeli KMV, Guimarães RML, de Almeida-Ferreira S, Parron LM, Brown GG (2022) Macrofauna communities and their relationship with soil structural quality in different land use systems. Soil Res 60:648-660. DOI:10.1071/SR21157 Dray S, Bauman D, Blanchet G, Borcard D, Clappe S, Guénard G, Jombart T, Larocque G, Legendre P, Madi N, Wagner HH (2022) Adespatial: Multivariate Multiscale Spatial Analysis. R package version 0.3-23 [online]. Retrieved in 2023, November 23, from https://CRAN.R-project.org/package=adespatial Drouin M, Bradley R, Lapointe L (2016) Linkage between exotic earthworms, understory vegetation and soil properties in sugar maple forests. For Ecol Manag 364:113-121. Duarte AP, Brown, GG, Pauletti V (2012) Changes in the forms of lead and manganese in soils by passage through the gut of the tropical endogeic earthworm ( Pontoscolex corethrurus ). Eur J Soil Biol 53:32-39. Eisenhauer N, Stefanski A, Fisichelli NA, Rice K, Rich R, Reich PB (2014) Warming shifts ‘worming’: effects of experimental warming on invasive earthworms in northern North America. Sci Rep 4:6890. Ferlian O, Wirth C, Eisenhauer N (2017) Leaf and root C-to-N ratios are poor predictors of soil microbial biomass C and respiration across 32 tree species. Pedobiologia 65:16-23. Fernandes GW, Ramos L, Goulart FF, Figueiredo JCG, Kenedy-Siqueira W, Toma TSP, ... & Negreiros D (2025) Mining scars may lead riparian ecosystem to multiple tipping points in a biodiversity hotspot. Anthropocene (under review). Fernandes GW, Goulart FF, Ranieri BD, Coelho MS, Dales K, Boesche N, Bustamante M, Carvalho FA, Carvalho DC, Dirzo R, Fernandes S, Galetti PM, Millan VEG, Mielke C, Ramirez JL, Neves A, Rogass C, Ribeiro SP, Scariot A, Soares-Filho B (2016). Deep into the mud: ecological and socio-economic himpacts of the dam breach in Mariana, Brazil. Nat Cons 14:35-45. DOI: 10.1016/j.ncon.2016.10.003 Frelich LE, Blossey B, Cameron EK, Dávalos A, Eisenhauer N, Fahey T, ... & Reich PB (2019) Side‐swiped: ecological cascades emanating from earthworm invasions. Front Ecol Environ 17:502-510. Frouz J (2018) Effects of soil macro-and mesofauna on litter decomposition and soil organic matter stabilization. Geoderma 332:161-172. Ge Y, Huang C, Zhou W, Shen Z, Qiao Y (2023) Eisenia fetida impact on cadmium availability and distribution in specific components of the earthworm drilosphere. Environ Sci Pollut Res 30:112222-112235. Gibson KD, Quackenbush PM, Emery NC, Jenkins MA, Kladivko EJ (2013) Invasive earthworms and plants in Indiana old-and second-growth forests. IPSM 6:161-174. Guhra T, Stolze K, Schweizer S, Totsche KU (2020) Earthworm mucus contributes to the formation of organo-mineral associations in soil. Soil Biol Biochem 145:107785. Hale CM, Frelich LE, Reich PB, Pastor J (2008) Exotic earthworm effects on hardwood forest floor, nutrient availability and native plants: a mesocosm study. Oecologia 155:509-518. DOI: https://doi.org/10.1007/s00442-007-0925-6 Hale CM, Lee EF, Peter BR (2006) "Changes in hardwood forest understory plant communities in response to European earthworm invasions. Ecology 87:1637-1649. DOI: 10.1890/0012-9658(2006)87[1637:cihfup]2.0.co;2 Hale AN, Lapointe L, Kalisz S. Invader disruption of belowground plant mutualisms reduces carbon acquisition and alters allocation patterns in a native forest herb. New Phytol 209:542-549. https://doi.org/10.1111/nph.13709 Hallaire V, Curmi P, Duboisset A, Lavelle P, Pashanasi B (2000) Soil structure changes induced by the tropical earthworm Pontoscolex corethrurus and organic inputs in a peruvian ultisol. Eur J Soil Biol 36:35-44. DOI: 10.1016/S1164-5563(00)01048-7 Hernández-García LM, Burgos-Guerrero JE, Tamires B, Rousseau GX, James SW (2018) Three new species of Holoscolex (Clitellata, Glossoscolecidae) from the Gurupi Biological Reserve, last forest remnant of the Belém endemism area, eastern Amazon. Zootaxa 4496:459-471. DOI: 10.11646/zootaxa.4496.1.35 Huston M (1979) A general hypothesis of species diversity. Am Nat 113:81-101. Laigle I, Moretti M, Rousseau L, Gravel D, Venier L, Handa IT, Messier C, Morris D, Hazlett P, Fleming R, Webster K, Shipley B, Aubin I (2021) Direct and indirect effects of forest anthropogenic disturbance on above and below ground communities and litter decomposition. Ecosystems 24:1-22. Larson ER, Kipfmueller KF, Hale CM, Frelich LE, Reich PB (2010) Tree rings detect earthworm invasions and their effects in northern Hardwood forests. Biol Invasions 12:1053-1066. Lavelle P, Spain A, Blouin M, Brown G, Decaëns T, Grimaldi M, Jiménez JJ, McKey D, Mathieu J, Velasquez E, Zangerlé A (2016) Ecosystem engineers in a self-organized soil. Soil Sci 181:91-109. DOI: 10.1097/SS.0000000000000155 Legendre P (2019) A temporal beta‐diversity index to identify sites that have changed in exceptional ways in space–time surveys. Ecol Evol 9:3500-3514. Legg S (2021) IPCC 2021: climate change 2021-the physical science basis. Interaction 49:44-45. Li X, Zuo X, Qiao J, Hu Y, Wang S, Yue P, Cheng H, Song Z, Chen M, Hautier Y (2024) Context‐dependent impact of changes in precipitation on the stability of grassland biomass. Funct Ecol 38:1185-1198. Marichal R, Martinez A F, Praxedes C, Ruiz D, Carvajal AF, Oszwald J, Hurtado MDelP, Brown GG, Grimaldi M, Desjardins t, Sarrazin M, Decaëns T, Velasquez E, Lavelle P (2010) Invasion of Pontoscolex corethrurus (Glossoscolecidae, Oligochaeta) in landscapes of the Amazonian deforestation arc. Appl Soil Ecol 46:443-449. Mathieu J, Reynolds JW, Fragoso C, Hadly E (2024) Multiple invasion routes have led to the pervasive introduction of earthworms in North America. Nat Ecol Evol 8:489-499. DOI: 10.1038/s41559-023-02310-7 Menino GCO, Nunes YRF, Santos RM, Fernandes GW, Fernandes LA (2012) Environmental heterogeneity and natural regeneration in riparian vegetation of the Brazilian semi-arid region. Edinb. J. Bot 69:29–51. DOI: 10.1017/S0960428611000400. Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GA, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853-858. Nadolny H, Oki Y, Kenedy-Siqueira W, Brown GG, Santos MP, Hernández-García LM, Negreiros D, Figueiredo JC, Goulart FF, Fernandes GW. (2024). Devastating Rio Doce mining disaster sends shockwaves through earthworm populations. Journal of Environmental Quality under review. Nearing MA, Pruski FF, O'neal MR (2004). Expected climate change impacts on soil erosion rates: a review. JSWC 59:43-50. Neves et al. 2024 Flora and Structure of the Naturally Regenerating Riparian Vegetation of the Rio Doce River: Basis for Environmental Restoration Actions Novo M, Cunha L, Maceda-Veiga A, Talavera JA, Hodson ME, Spurgeon D, Bruford MW, Morgan AJ, Kille P (2015) Multiple introductions and environmental factors affecting the establishment of invasive species on a volcanic island. Soil Biol Biochem 85:89-100. Oksanen J, Simpson G, Blanchet F, Kindt R, Legendre P, Minchin P, O'Hara R, Solymos P, Stevens M, Szoecs E, Wagner H, Barbour M, Bedward M, Bolker B, Borcard D, Carvalho G, Chirico M, De Caceres M, Durand S, Evangelista H, Fitzjohn R, Friendly M, Furneaux B, Hannigan G, Hill M, Lahti L, McGlinn D, Ouellette M, Ribeiro, Cunha E, Smith T, Stier A, Ter Braak C, Weedon J (2022) Vegan: Community Ecology Package. R package version 2.6-4. Retrieved from https://CRAN.R-project.org/package=vegan Peixoto RT, Marochi AI (1996) A influência da minhoca Pheretima sp. nas propriedades de um latossolo vermelho escuro álico e no desenvolvimento de culturas em sistema de plantio direto, em Arapoti-PR. Revista Plantio Direto, 35:23-35. Phillips HR, Bach EM, Bartz ML, Bennett JM, Beugnon R, Briones MJ, ... Webster ER (2021) Global data on earthworm abundance, biomass, diversity and corresponding environmental properties. Sci Data 8, 136. DOI:10.1038/s41597-021-00912-z Phillips, HRP et al., Global distribution of earthworm diversity. Science 366,480-485 (2019). DOI:10.1126/science.aax4851 Pop VV, Pop AA (2006) Lumbricid earthworm invasion in the carpathian mountains and some other sites in Romania. In: P.F. Hendrit (Eds) Biological Invasions Belowground: Earthworms as Invasive Species. Dordrecht: Springer. P. 19-22. DOI: 10.1007/978-1-4020-5429-7_3 R Core Team (2024) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available in: https://www.R-project.org/ Ramos L, Negreiros D, Goulart FF, Figueiredo JCG, Kenedy-Siqueira W, Toma TSP, ... & Fernandes GW (2024). Dissimilar forests along the Rio Doce watershed call for multiple restoration references to avoid biotic homogenization. Sci Total Environ 930, 172720. DOI: 10.1016/j.scitotenv.2024.172720 Righi G (1995) Colombian earthworms. In: T. Van der Hammen, A.G. dos Santos, (Eds.): La Cordillera Central Colombiana Transecto Parque Los Nevados. 3 ed. Berlin-Stuttgart. P. 485-607 Ruiz E, Rodríguez L, Alonso-Azcárate J (2009) Effects of earthworms on metal uptake of heavy metals from polluted mine soils by different crop plants. Chemosphere 75:1035-1041. Sá ACN, Souza GF, de Freitas GP, Alves NBP, Silva RMG, Santos LAP, de Lima RM (2024) Eisenia fetida e Pontoscolex corethrurus como bioindicadoras de ambientes contaminados por metais pesados. Contrib Las Cienc Soc 17:e5249-e5249. Sackett TE, Smith SM, Basiliko N (2013) Efeitos indiretos e diretos de minhocas exóticas em nutrientes do solo e depósitos de carbono em florestas temperadas norte-americanas. Soil Biol Biochem 57:459-467. Sharma RK, Poonam B (2014) Earthworm diversity in trans-gangetic habitats of Haryana, India. Res J Agric For Sci 2:1-7. Singh J, Schädler M, Demetrio W, Brown GG, Eisenhauer N (2019) Climate change effects on earthworms - a review. Soil Org 91:114-138. DOI: 10.25674%2Fso91iss3pp114 Singh S, Singh J, Vig AP (2016) Earthworm as ecological engineers to change the physico-chemical properties of soil: Soil vs vermicast. Ecol Eng 90:1-5. DOI: 10.1016/j.ecoleng.2016.01.072 Taheri S, Pelosi C, Dupont L (2018) Harmful or useful? A case study of the exotic peregrine earthworm morphospecies Pontoscolex corethrurus . Soil Biol Biochem 116:277-289. DOI: 10.1016/j.soilbio.2017.10.030 Teng SK, Aziz NAA, Mustafa M, Laboh R, Ismail IS, Devi S (2016) Potential role of endogeic earthworm Pontoscolex corethrurus in remediating banana blood disease: a preliminary observation. Eur J Plant Pathol 145:321-330. Thakur MP, Reich PB, Hobbie SE, Stefanski A, Rich R, Rice KE, Eddy WC Eisenhauer N (2018) Reduced feeding activity of soil detritivores under warmer and drier conditions. Nat Clim Change 8:75-78. The Angiosperm Phylogeny Group, M. W. Chase, M. J. M. Christenhusz, M. F. Fay, J. W. Byng, W. S. Judd, D. E. Soltis, D. J. Mabberley, A. N. Sennikov, P. S. Soltis, P. F. Stevens, An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV, Botanical Journal of the Linnean Society , Volume 181, Issue 1, May (2016), Pages 1–20, https://doi.org/10.1111/boj.12385 Thouvenot L, Ferlian O, Horn L, Jochum M, Eisenhauer N (2024) Effects of earthworm invasion on soil properties and plant diversity after two years of field experiment. NeoBiota 94:31-56. Trap J, Blanchart E, Ratsiatosika O, Razafindrakoto M, Becquer T, Andriamananjara A, Morel C (2021) Effects of the earthworm Pontoscolex corethrurus on rice P nutrition and plant-available soil P in a tropical Ferralsol. Appl Soil Ecol 160:103867. Walsh CL, Johnson-Maynard JL (2016) Earthworm distribution and density across a climatic gradient within the Inland Pacific Northwest cereal production region. Appl Soil Ecol 104:104-110. Yadav S, Mullah M (2017) A review on molecular markers as tools to study earthworm diversity. IJPAZ 5:62-69. Yuan Z, Ali A, Loreau M, Ding F, Liu S, Sanaei A, Zhou W, Ye J, Lin F, Fang S, Hao Z, Wang X, Le Bagousse-Pinguet Y. Divergent above- and below-ground biodiversity pathways mediate disturbance impacts on temperate forest multifunctionality. Glob Chang Biol. (2021) Jun;27(12):2883-2894. doi: 10.1111/gcb.15606. Epub 2021 Mar 30. PMID: 33742479. Zhang M, Zou X, Schaefer DA (2010) Alteration of soil labile organic carbon by invasive earthworms ( Pontoscolex corethrurus ) in tropical rubber plantations. Eur J Soil Biol 46:74-79. DOI: 10.1016/j.ejsobi.2009.11.004 Table 1 Table 1 is available in the Supplementary Files section. Supplementary Files Table1.docx Cite Share Download PDF Status: Published Journal Publication published 14 Nov, 2025 Read the published version in Biological Invasions → Version 1 posted Reviewers agreed at journal 30 Dec, 2024 Reviewers invited by journal 30 Dec, 2024 Editor invited by journal 29 Nov, 2024 Editor assigned by journal 29 Nov, 2024 First submitted to journal 28 Nov, 2024 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-5544777","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":395895416,"identity":"9a0f8f18-e8c0-4240-b695-23970d72d569","order_by":0,"name":"Walisson Kenedy-Siqueira","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAABEElEQVRIiWNgGAWjYBACCRDBA8RsIEYCA4MciD7wgBQtxmAtCcRogYHEBqhenECyvffgg7dtDPZ87DmGDx7usUufH3b4IdAWOzndBuxapHnOJRvObWNIbON5Y2yQ8Cw5d+PtNAOglmRjswPYtchJ5JhJ87YxJLABGRIJB5hzN85OAGk5kLgNlxb5N+a/gVrsgVrMfyQcqE83nJ3+Aa8WaQkeM2agFsY2oC0MCQcOJ8hL5+C3RbInx1hyzjkJoF+eFQMddtxwg3ROwYEEA9x+kTh+xvDDmzIbe/n25I0ffxyolpefnb75w4cKOzlcWsCAkQ0UPQkQjgFYpQEe5WDwhwGhRb6BkOpRMApGwSgYaQAAeWBc0ovcNRQAAAAASUVORK5CYII=","orcid":"https://orcid.org/0000-0001-7766-9077","institution":"Federal University of Minas Gerais: Universidade Federal de Minas Gerais","correspondingAuthor":true,"prefix":"","firstName":"Walisson","middleName":"","lastName":"Kenedy-Siqueira","suffix":""},{"id":395895417,"identity":"c5172a32-ab3b-435a-ad8b-4b5050743305","order_by":1,"name":"Yumi Oki","email":"","orcid":"","institution":"Universidade Federal de Minas Gerais","correspondingAuthor":false,"prefix":"","firstName":"Yumi","middleName":"","lastName":"Oki","suffix":""},{"id":395895418,"identity":"e86fa6f2-9682-470b-8448-d27adb2b6d55","order_by":2,"name":"Marcos Paulo Santos","email":"","orcid":"","institution":"Universidade Estadual de Montes Claros","correspondingAuthor":false,"prefix":"","firstName":"Marcos","middleName":"Paulo","lastName":"Santos","suffix":""},{"id":395895419,"identity":"1e3e80fb-eff3-47cb-80c9-f3fc041d193f","order_by":3,"name":"João Carlos Gomes Figueiredo","email":"","orcid":"","institution":"Universidade Federal de Minas Gerais","correspondingAuthor":false,"prefix":"","firstName":"João","middleName":"Carlos Gomes","lastName":"Figueiredo","suffix":""},{"id":395895420,"identity":"0b917c72-91d7-4253-afd9-d2b61f147278","order_by":4,"name":"Luis Manuel Hernández-García","email":"","orcid":"","institution":"Universidade Estadual do Maranhao","correspondingAuthor":false,"prefix":"","firstName":"Luis","middleName":"Manuel","lastName":"Hernández-García","suffix":""},{"id":395895421,"identity":"6e9589ce-301f-4c80-b9b9-987a441ac361","order_by":5,"name":"Francisco Alves de Amorim Soares","email":"","orcid":"","institution":"Universidade Federal de Minas Gerais","correspondingAuthor":false,"prefix":"","firstName":"Francisco","middleName":"Alves de Amorim","lastName":"Soares","suffix":""},{"id":395895422,"identity":"142df13b-1fac-44fe-bd43-1860d0827908","order_by":6,"name":"Herlon Nadolny","email":"","orcid":"","institution":"Universidade Federal de Minas Gerais","correspondingAuthor":false,"prefix":"","firstName":"Herlon","middleName":"","lastName":"Nadolny","suffix":""},{"id":395895423,"identity":"d98411ea-58bc-409f-8149-37ad844937d4","order_by":7,"name":"George G. Brown","email":"","orcid":"","institution":"Embrapa Florestas","correspondingAuthor":false,"prefix":"","firstName":"George","middleName":"G.","lastName":"Brown","suffix":""},{"id":395895424,"identity":"b6994568-ff23-49e1-9eae-f0ea27907fed","order_by":8,"name":"Geraldo Wilson Fernandes","email":"","orcid":"","institution":"Universidade Federal de Minas Gerais","correspondingAuthor":false,"prefix":"","firstName":"Geraldo","middleName":"Wilson","lastName":"Fernandes","suffix":""}],"badges":[],"createdAt":"2024-11-28 19:43:30","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-5544777/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-5544777/v1","draftVersion":[],"editorialEvents":[{"content":"https://doi.org/10.1007/s10530-025-03694-2","type":"published","date":"2025-11-14T15:58:23+00:00"}],"editorialNote":"","failedWorkflow":false,"files":[{"id":72732296,"identity":"8b57b8e9-8374-4beb-b350-590af8a1468f","added_by":"auto","created_at":"2025-01-01 07:02:14","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":342178,"visible":true,"origin":"","legend":"\u003cp\u003eA. Map showing the location of the 15 areas in the 5 sampling regions (green squares = Reference Sites; brown squares = Impacted Sites) along the Rio Doce in southeastern Brazil (Red circle: site of the collapse of the Fundão mining tailings dam in Mariana, Brazil). B. Mean daily precipitation (lines) and temperature (columns) over the 15 days preceding each sampling period. Standard errors are represented as ranges for lines (precipitation) and as bars for columns (temperature).\u003c/p\u003e","description":"","filename":"Figure1.png","url":"https://assets-eu.researchsquare.com/files/rs-5544777/v1/a9c44f750dbde29224d0340b.png"},{"id":72732299,"identity":"44fc44ed-5a34-472f-bf7e-a49c41cbb6e6","added_by":"auto","created_at":"2025-01-01 07:02:14","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":327087,"visible":true,"origin":"","legend":"\u003cp\u003eEarthworm diversity as a function of a period with low and high precipitation (A) in reference areas (B) and areas impacted by mining tailings in the Rio Doce, Brazil (C).\u003c/p\u003e","description":"","filename":"2.png","url":"https://assets-eu.researchsquare.com/files/rs-5544777/v1/b9152413d7fe865eab5679e9.png"},{"id":72732298,"identity":"4d0e4c19-6409-48f2-a7d1-ded15ecd29e5","added_by":"auto","created_at":"2025-01-01 07:02:14","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":276568,"visible":true,"origin":"","legend":"\u003cp\u003eComposition of earthworm species in two years of sampling (2023 and 2024) with varying precipitation (A), within reference sites (B), within sites with soil impacted by mining tailings (C), and between sites in the Rio Doce, Brazil (D). Square and circle sizes are scaled to their values. The red line indicates the trend of the effect observed and the dashed line indicates the absence of effect.\u003c/p\u003e","description":"","filename":"Figure3.png","url":"https://assets-eu.researchsquare.com/files/rs-5544777/v1/09df641055fe8bcaa826a0a7.png"},{"id":72732562,"identity":"a82f6d67-0788-427f-b1ef-08c810490b47","added_by":"auto","created_at":"2025-01-01 07:10:15","extension":"png","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":552913,"visible":true,"origin":"","legend":"\u003cp\u003eCorrelation between the total abundance (A) and that of invasive earthworms (B) and the diversity of juvenile regenerating plants in reference areas and areas impacted by mining tailings in the Rio Doce, Brazil. An asterisk (*) designates non-significative values.\u003c/p\u003e","description":"","filename":"Figure4.png","url":"https://assets-eu.researchsquare.com/files/rs-5544777/v1/5d91654bc9a6edcd1388f964.png"},{"id":96105112,"identity":"0c6c3779-bfeb-4c19-92a0-f26a9328d349","added_by":"auto","created_at":"2025-11-17 16:08:48","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":2113405,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-5544777/v1/f1a9035b-e1b7-4f2c-9d1b-b74fee8575e1.pdf"},{"id":72732295,"identity":"1a8ca395-ce5e-4779-b2c7-d7ac60fd1eae","added_by":"auto","created_at":"2025-01-01 07:02:14","extension":"docx","order_by":1,"title":"","display":"","copyAsset":false,"role":"supplement","size":29533,"visible":true,"origin":"","legend":"","description":"","filename":"Table1.docx","url":"https://assets-eu.researchsquare.com/files/rs-5544777/v1/baa1cf22bb5609a3631edaf2.docx"}],"financialInterests":"","formattedTitle":"Microclimate and mining stresses the diversity of earthworms and further impact the regeneration of forests along the Rio Doce","fulltext":[{"header":"Introduction","content":"\u003cp\u003eThe diversity and dynamics of species below and above ground are influenced by the frequency and intensity of disturbances in an ecosystem (Walsh and Johnson-Maynard \u003cspan citationid=\"CR69\" class=\"CitationRef\"\u003e2016\u003c/span\u003e, Yuan et al. \u003cspan citationid=\"CR71\" class=\"CitationRef\"\u003e2021\u003c/span\u003e, Laigle et al. \u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e2021\u003c/span\u003e, Li et al. \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2024\u003c/span\u003e). The disturbance hypothesis suggests that diversity is higher under intermediate levels of disturbance (Huston \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e1979\u003c/span\u003e). Low diversity can occur in the absence of disturbance, due to the persistence of superior competitors or under very intense disturbance regimes, due to the persistence of native or exotic colonizers that can become invaders (Huston \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e1979\u003c/span\u003e, Eisenhauer et al. \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e2014\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eClimatic variations are natural disturbances that primarily affect precipitation levels and temperature in specific regions (Legg \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2021\u003c/span\u003e), impacting species and populations below ground, impairing development, reproductive rates, immunity to disease, and mortality rates (Beier et al. \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e2012\u003c/span\u003e, Thakur et al. \u003cspan citationid=\"CR65\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). They can also affect species composition, accelerating extinction rates and migration, thus reducing the diversity of terrestrial species responsible for important ecosystem functions (Singh et al. \u003cspan citationid=\"CR61\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). For example, extended periods of drought and intensified short-term rainfall patterns have a direct impact on resource availability, soil conditions, and the diversity of soil-dwelling invertebrates (Yadav and Mullah \u003cspan citationid=\"CR70\" class=\"CitationRef\"\u003e2017\u003c/span\u003e, Phillips et al. \u003cspan citationid=\"CR52\" class=\"CitationRef\"\u003e2019\u003c/span\u003e, Singh et al. \u003cspan citationid=\"CR61\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). Furthermore, anthropogenic changes that directly modify the soil (Barros et al. \u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2004\u003c/span\u003e), such as deforestation, agricultural practices, and mining are among the factors that can deeply affect soil physical and chemical conditions and the populations and diversity of soil organisms (Nearing et al. \u003cspan citationid=\"CR46\" class=\"CitationRef\"\u003e2004\u003c/span\u003e). These anthropogenic changes have resulted in the loss and degradation of habitats, often leading to soil pollution, which represents a strong stressor for native edaphic species to persist or recolonize.\u003c/p\u003e \u003cp\u003eAmong the soil organisms, earthworms are true ecosystem engineers that facilitate nutrient cycling by processing organic matter (Frouz \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2018\u003c/span\u003e, Barthod et al. \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). During their feeding activities, earthworms construct burrows that facilitate soil aeration and rainwater infiltration (Singh et al. \u003cspan citationid=\"CR62\" class=\"CitationRef\"\u003e2016\u003c/span\u003e, Brown et al. \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). The ingestion of organic matter and its subsequent excretion in castings increases plant nutrient availability to roots (Guhra et al. \u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). Hence, earthworms facilitate nutrient cycling and plant growth promotion.\u003c/p\u003e \u003cp\u003eOn the other hand, some invasive earthworm species have a detrimental role on plant survival (Hale et al. \u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e2006\u003c/span\u003e, Larson et al. \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e2010\u003c/span\u003e). Experimental studies in closed and open systems have demonstrated that in circumstances where organic matter is scarce, some earthworm species at high abundance can compete with plants for nutrients, or even damage their growth by attacking plants in the early stages of their life cycle (Hale et al. \u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e2008\u003c/span\u003e, Larson et al. \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e2010\u003c/span\u003e, Sackett et al. \u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e2013\u003c/span\u003e). For instance, the tropical species \u003cem\u003ePontoscolex corethrurus\u003c/em\u003e has been shown to negatively affect soil structure and hydraulic processes (Hallaire et al. \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2000\u003c/span\u003e, Barros et al. \u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2004\u003c/span\u003e). This species has been reported as an invader in the Brazilian Amazonia and Mata Atlantica forests and pastures, possibly negatively affecting soil processes (Demetrio et al. \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). Furthermore, it has high reproduction rates and resistance to disturbances (Lavelle et al. \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2016\u003c/span\u003e, Taheri et al. \u003cspan citationid=\"CR63\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). Other earthworms can also be considered invasive, such as \u003cem\u003eAmynthas gracilis\u003c/em\u003e, a highly competitive species of Asian origin (Brown and Fragoso \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2007\u003c/span\u003e, Zhang et al. \u003cspan citationid=\"CR72\" class=\"CitationRef\"\u003e2010\u003c/span\u003e), known to affect soil structure and nutrient cycling as well as plant growth, though generally in a positive manner (Brown et al \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e1999\u003c/span\u003e, Peixoto \u0026amp; Marochi \u003cspan citationid=\"CR50\" class=\"CitationRef\"\u003e1996\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eSeveral other studies have indicated that the presence of some earthworm species may have detrimental impacts on soil parameters associated with plant diversity (Gibson et al. \u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e2013\u003c/span\u003e, Drouin et al. \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e2016\u003c/span\u003e, Hale et al. 2016, Craven et al. \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e2017\u003c/span\u003e, Thouvenot et al. \u003cspan citationid=\"CR67\" class=\"CitationRef\"\u003e2024\u003c/span\u003e). However, these studies were predominantly conducted in temperate regions, and there is a paucity of knowledge regarding the influence of earthworms on plant community structure and diversity in tropical regions (Craven et al. \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e2017\u003c/span\u003e), where these ecosystem engineers still need to be fully studied.\u003c/p\u003e \u003cp\u003eThe invasive potential of native and alien species is both linked to a set of traits that the species possesses and to anthropogenic disturbances (Pop and Pop \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e2006\u003c/span\u003e, Mathieu et al. \u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e2024\u003c/span\u003e). The invasion of altered environments complicates efforts to restore the essential functions performed by native species, crucial for maintaining ecosystems (Frelich et al. \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). For instance, the collapse of the Samarco mining tailings dam in Mariana, Brazil, resulted in the burial and destruction of the native fauna, fungi, and flora of a significant portion of the riparian forest of the Rio Doce Basin (Fernandes et al. \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2016\u003c/span\u003e, Carmo et al. \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). The catastrophic event occurred nine years ago, yet its residual effects can still be observed in the physical alterations of the soil and the decline in the biomass of native earthworms in the region (Nadolny et al. \u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e2024\u003c/span\u003e). These modifications may compromise the ecological functions of earthworms, which could impact the recovery of native plant species in the affected sites (see Craven et al. \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e2017\u003c/span\u003e, Ferlian et al. \u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e2017\u003c/span\u003e, Frelich et al. \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). The return of native vegetation represents a crucial initial phase of environmental resilience, occurring primarily through the spontaneous regeneration of vegetation in areas affected by some forms of disturbance (e.g., Chazdon \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2013\u003c/span\u003e, Chazdon and Guariguata \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2016\u003c/span\u003e, Crouzeilles et al. \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e2017\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eAgainst the backdrop of climate disruptions and soil alterations in the Rio Doce riparian forest, this study aimed to (a) assess the diversity of earthworms in two distinct climatic periods (high and low precipitation), and (b) verify the relationships between native and invasive earthworm abundance on plant diversity in the regenerating stratum. Concerning the diversity of earthworms, climate disturbances, and the impacts of soil contaminated with mining tailings, the following hypotheses were proposed: (H1) in sites with soil not impacted by mining tailings (from here on, referred to as reference sites: Ramos et al. \u003cspan citationid=\"CR55\" class=\"CitationRef\"\u003e2024\u003c/span\u003e), earthworm diversity is greater in periods of high precipitation than in periods of low precipitation; (H2) conversely, in sites with soil impacted by mining tailings (from here on, referred to as impacted sites: Fernandes et al. \u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e2025\u003c/span\u003e under review), earthworm diversity is smaller in periods of low precipitation than in periods of high precipitation; (H3) due to changes in precipitation, earthworm species composition is mediated by the species gains in reference sites and losses in impacted sites. Concerning the abundance of earthworms and the regenerating vegetation of the riparian forest, we hypothesized that: (H4) invasive earthworm abundance is negatively correlated to juvenile plant species diversity in reference and impacted sites, and (H5) native earthworm species abundance is positively correlated to juvenile plant species diversity in reference and impacted sites.\u003c/p\u003e"},{"header":"Material and Methods","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eSampling design\u003c/h2\u003e \u003cp\u003eSampling was conducted on earthworms and regenerating vegetation (juvenile plants) in five regions of riparian forest along the Rio Doce in Minas Gerais, Brazil (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003eA). In each region, three areas that had been impacted by mining tailings (Impacted Sites) and three areas that had not been impacted by tailings were sampled (Reference sites). To sample regenerating vegetation, in each area, 15 plots measuring 5 x 5 m were constructed, resulting in a total of 450 plots (Menino et al. \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e2012\u003c/span\u003e, Neves et al. \u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e2024\u003c/span\u003e, Fernandes et al. \u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e2025\u003c/span\u003e in review).\u003c/p\u003e \u003cp\u003eThe earthworms were sampled in two consecutive years, May 2023 and May 2024, at the end of the rainy season and the beginning of the dry season. Following a modification of the Tropical Soil Biology and Fertility (TSBF) Programme method (Anderson and Ingram \u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1993\u003c/span\u003e), earthworms were sampled a 0.25 x 0.25 x 0.2 m soil monoliths in each plot, resulting in a total of 900 monoliths. Each monolith was manually sorted in the field, and the earthworms were collected and placed in plastic vials containing 80% alcohol. The vials were labeled and sent to the Laboratory of Reproduction and Fish Communities, Federal University of Paran\u0026aacute; (LRFC - UFP) for sorting, quantification, and preliminary identification. The sorted material was subsequently sent to the Laboratory of Soil Biology, State University of Maranh\u0026atilde;o (LSB - UEMA) for identification at the lowest possible taxonomic level by co-author LMHG. The taxonomic identification of the earthworms was based on the keys of Righi (\u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e1995\u003c/span\u003e), Blakemore (\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2002\u003c/span\u003e), dos Santos et al. (2017), and Hern\u0026aacute;ndez-Garc\u0026iacute;a et al. (\u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). After taxonomic identification, the species were classified as native and non-native (invasive) for the ecosystem studied (Atlantic Rainforest) according to Demetrio et al. (2023). The samples were deposited in the earthworm collection of the Department of Genetic, Ecology and Evolution of the Federal University of Minas Gerais (UFMG).\u003c/p\u003e \u003cp\u003eThe plant saplings were sampled by quantifying and collecting all the plant species in the regenerating stratum with a diameter at breast height\u0026thinsp;\u0026lt;\u0026thinsp;5 cm (1.30 m from the ground) and diameter at soil height\u0026thinsp;\u0026ge;\u0026thinsp;1 cm taken from each plot (N\u003csub\u003etotal\u003c/sub\u003e=450) in May 2023. The sampled plants were pressed in the field, labeled, and sent to the Laboratory of Phytogeography and Evolutionary Ecology, Federal University of Lavras (LPEE - UFLA) for identification at the lowest possible taxonomic level by RMS. The plant material was deposited in the Herbarium of Norte Mineiro (ICA-UFMG) and the Herbarium of Montes Claros, Minas Gerais (Unimontes). The Angiosperm Phylogeny Group IV system was used to classify the species into families (APG IV 2016).\u003c/p\u003e \u003cp\u003eAverages of precipitation and temperature were collected, 15 days before each earthworm sampling, from the precipitation data of the closest weather station to each area (N\u0026thinsp;=\u0026thinsp;30) to characterize the climatic period of the samplings. The mean precipitation of the second year of sampling was approximately five times higher than that of the first sampling (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003eB). Due to the disparate precipitation patterns observed in the samples, we designated sampling 1 as \"Low precipitation\" and sampling 2 as \"High precipitation\".\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec4\" class=\"Section2\"\u003e \u003ch2\u003eStatistical analysis\u003c/h2\u003e \u003cp\u003eStatistical analyses were conducted using R software (R Core Team \u003cspan citationid=\"CR54\" class=\"CitationRef\"\u003e2024\u003c/span\u003e). The regional diversity of earthworms and plants was calculated by Shannon indices using the \"Vegan package\" (Oksanen et al. \u003cspan citationid=\"CR49\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). We performed generalized linear mixed models (GLMM) to test the variation in the effects of climatic variation (high vs. low precipitation) on earthworm diversity and the relation between earthworm abundance and juvenile plant diversity. Site location and region were considered random effects. The models had Gaussian distribution and were tested using analysis of variance (ANOVA). When the objective was to analyze the effects of climatic disturbances on sites, the diversity calculations were carried out separately for each condition of the sites (Reference and Impacted). When the aim was to test the relation between earthworm abundance and juvenile plant diversity, the tests were carried out separately for native and invasive earthworms using data only from 2023, when both plants and earthworms were sampled. The models were considered significant when the P value was less than 0.05.\u003c/p\u003e \u003cp\u003eIn parallel, species composition was calculated using the temporal beta-diversity index (TBI), which employs the pairwise Sorensen dissimilarity index (Year 1: low precipitation and Year2: high precipitation) with the \"adespatial package\" (Dray et al. \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). The TBI value can be decomposed into two components: species losses (B) and species gains (C). A positive value of [C \u0026ndash; B] indicates that the site was dominated by gains, whereas a negative value denotes overall losses of species (Legendre \u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). The [C \u0026ndash; B] difference across all plots was tested for statistical differences using the parametric P value and permutational paired t-test (N\u0026thinsp;=\u0026thinsp;999 permutations) computed for the C and B statistics from all plots. The B and C statistics were then used to produce B-C plots, with B (losses per plot) in the abscissa and C (gains per plot) in the ordinate (Legendre \u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). Furthermore, the B and C per plot were compared between reference and impacted sites, through generalized linear models (GLM) with Binomial error distribution and tested using ANOVA (P values less than 0.05 were considered significant).\u003c/p\u003e \u003c/div\u003e"},{"header":"Results","content":"\u003cdiv id=\"Sec6\" class=\"Section2\"\u003e\n \u003ch2\u003eTrends in abundance and richness of earthworms\u003c/h2\u003e\n \u003cp\u003eA total of 2158 individual earthworms were collected, belonging to 19 species during the two consecutive sampling years (Table \u003cspan class=\"InternalRef\"\u003e1\u003c/span\u003e). Of this total, 616 individuals were collected in the first year (native: 31, invasive: 585 individuals) and 1542 individuals in the second year (native: 218, invasive: 1324 individuals). Of this total, 1130 individuals were found in the impacted sites (native: 138, invasive: 992 individuals) and 1028 individuals in the reference sites (native: 111, invasive: 917 individuals).\u003c/p\u003e\n \u003cp\u003eDuring the first sampling (2023), seven species belonging to four families were found: \u003cem\u003eP. corethrurus\u003c/em\u003e, \u003cem\u003eRhinodrilus\u003c/em\u003e sp.1 and sp.2 (Rhinodrilidae), \u003cem\u003eRighiodrilus\u003c/em\u003e sp.2 and sp.3 (Glossoscolecidae), \u003cem\u003eA. gracilis\u003c/em\u003e (Megascolecidae), and some individuals of the family Ocnerodrilidae spp. The native Ocnerodrilidae were found exclusively in the impacted site, while the native \u003cem\u003eR. motucu\u003c/em\u003e, \u003cem\u003eRighiodrilus\u003c/em\u003e sp.1 and sp.2, as well as the non-native \u003cem\u003eA. gracilis\u003c/em\u003e and \u003cem\u003eP. corethrurus\u003c/em\u003e were found in both impacted and reference sites (Table \u003cspan class=\"InternalRef\"\u003e1\u003c/span\u003e).\u003c/p\u003e\n \u003cp\u003eIn the second year of sampling (2024) more and different species were recorded, with the native \u003cem\u003eR. motucu\u003c/em\u003e, three species of Ocnerodrilidae, and one of \u003cem\u003eGlossodrilus\u003c/em\u003e occurring in the reference sites. \u003cem\u003eRhinodrilus\u003c/em\u003e sp.3 and Ocnerodrilidae spp. were only recorded in impacted sites while the other native species Ocnerodrilidae sp.1, \u003cem\u003eRighiodrilus\u003c/em\u003e sp.1, and \u003cem\u003eRhinodrilus\u003c/em\u003e sp.1 were sampled in both reference and impacted sites (Table\u0026nbsp;\u003cspan class=\"InternalRef\"\u003e1\u003c/span\u003e). The invasive species \u003cem\u003eA. corticis\u003c/em\u003e was sampled only in the reference area, while juvenile Megascolecidae spp. and \u003cem\u003eP. elongata\u003c/em\u003e were sampled only in the impacted site. The other invasive species \u003cem\u003eA. gracilis\u003c/em\u003e, \u003cem\u003eD. bolaui\u003c/em\u003e and \u003cem\u003eP. corethrurus\u003c/em\u003e were sampled in both reference and impacted sites (Table\u0026nbsp;\u003cspan class=\"InternalRef\"\u003e1\u003c/span\u003e).\u003c/p\u003e\n\u003c/div\u003e\n\u003ch3\u003eRainfall impact on earthworms\u003c/h3\u003e\n\u003cp\u003ePrecipitation resulted in major changes in earthworm diversity (F \u003csub\u003e(1, 869)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;63.804, P\u0026thinsp;=\u0026thinsp;4.349e-15), with approximately 10 times higher diversity in the period with more rainfall (0.107\u0026thinsp;\u0026plusmn;\u0026thinsp;0.012) than in the drier period (0.012\u0026thinsp;\u0026plusmn;\u0026thinsp;0.004) (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003eA). Species richness was also higher, with nearly twice the number of species recovered in the wet (17 spp.) than dry year (8 spp.) samples.\u003c/p\u003e \u003cp\u003eEarthworm diversity also varied according to the precipitation period in reference (F \u003csub\u003e(1, 434)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;25.42, P\u0026thinsp;=\u0026thinsp;6.787e-07) and impacted sites (F \u003csub\u003e(1, 434)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;38.504, P\u0026thinsp;=\u0026thinsp;1.277e-09). In reference sites, diversity was approximately 6 times greater in the period higher (0.090\u0026thinsp;\u0026plusmn;\u0026thinsp;0.015) than lower precipitation (0.015\u0026thinsp;\u0026plusmn;\u0026thinsp;0.006) (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003eB). In impacted sites, diversity was approximately 13 times greater in the period with higher (0.123\u0026thinsp;\u0026plusmn;\u0026thinsp;0.018) than lower precipitation (0.009\u0026thinsp;\u0026plusmn;\u0026thinsp;0.005) (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003eC).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eSpecies composition also responded to precipitation (Stat\u0026thinsp;=\u0026thinsp;5.764, P\u0026thinsp;=\u0026thinsp;2.22298e-08, P\u003csub\u003epermutation\u003c/sub\u003e = 0.001). The variation in species composition was mediated by species gain (TBI\u0026thinsp;=\u0026thinsp;0.658), with more than twice as many species gained (0.455) as lost (0.203) in the period with higher precipitation (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003eA).\u003c/p\u003e \u003cp\u003eSpecies composition also varied with precipitation within each site: reference (Stat 3.608, P\u0026thinsp;=\u0026thinsp;0.0004, P\u003csub\u003epermutation\u003c/sub\u003e = 0.001) and impacted (Stat\u0026thinsp;=\u0026thinsp;4.520, P\u0026thinsp;=\u0026thinsp;1.316722e-05, P\u003csub\u003epermutation\u003c/sub\u003e = 0.001). In reference sites, approximately twice as many species were gained (0.673) than lost (0.326) with higher precipitation (TBI\u0026thinsp;=\u0026thinsp;0.641, Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003eB). In impacted sites, the variation was also mediated by species gain (TBI\u0026thinsp;=\u0026thinsp;0.675), with more than twice as many species gained (0.708) than lost (0.291) in 2024 (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003eC).\u003c/p\u003e \u003cp\u003eSpecies composition did not vary between sites with similar values of TBI for impacted and reference treatments (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003eD).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cdiv id=\"Sec8\" class=\"Section2\"\u003e \u003ch2\u003eAbundance of earthworms and the regenerating vegetation\u003c/h2\u003e \u003cp\u003eTotal earthworm abundance was significantly related to plant diversity (F \u003csub\u003e(1, 449)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;5.798, P\u0026thinsp;=\u0026thinsp;0.01645) and interaction with sites (F \u003csub\u003e(1, 447)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;18.527, P\u0026thinsp;=\u0026thinsp;2.063e-05). For reference sites, there was a positive relationship between total earthworm abundance and plant diversity (y\u0026thinsp;=\u0026thinsp;0.85114\u0026thinsp;+\u0026thinsp;0.00267x, F \u003csub\u003e(1, 224)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;5.4939, P\u0026thinsp;=\u0026thinsp;0.0199). However, in impacted sites, this relationship was not significant (y\u0026thinsp;=\u0026thinsp;0.85114 -0.0006x, F \u003csub\u003e(1, 224)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;0.1106, P\u0026thinsp;=\u0026thinsp;0.7398) (Fig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e4\u003c/span\u003eA).\u003c/p\u003e \u003cp\u003eNative earthworm abundance was not related to plant diversity (F \u003csub\u003e(1, 449)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;3.5439, P\u0026thinsp;=\u0026thinsp;0.0604) or the interaction with sites (F \u003csub\u003e(1, 447)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;0.8713, P\u0026thinsp;=\u0026thinsp;0.3511), but the abundance of invasive earthworms was significantly correlated with the diversity of regenerating plants (F \u003csub\u003e(1, 449)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;7.1411, P\u0026thinsp;=\u0026thinsp;0.0078) and the interaction with sites (F \u003csub\u003e(1, 447)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;19.950, P\u0026thinsp;=\u0026thinsp;1.01e-05). In reference sites, invasive earthworm abundance was positively related to plant diversity (y\u0026thinsp;=\u0026thinsp;0.85034\u0026thinsp;+\u0026thinsp;0.00285x, F \u003csub\u003e(1, 224)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;6.0578, P\u0026thinsp;=\u0026thinsp;0.0146) (Fig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e4\u003c/span\u003eB). Conversely, in impacted sites, there was a trend for opposite relationships, though the regression was not significant (y\u0026thinsp;=\u0026thinsp;0.85034 -0.0006x, F \u003csub\u003e(1, 224)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;0.1540, P\u0026thinsp;=\u0026thinsp;0.6951).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e"},{"header":"Discussion","content":"\u003cp\u003eA total of 19 earthworm species were recorded in the riparian forests of along the Doce River Basin during a two year study. This represents around 4% of the species richness for Brazil (336 species, Brown et al. 2013) and 15% of the species known from the Atlantic Forest (99 species, Demetrio et al. 2023). On the other hand, several of the species were not identified to species level, and many represent new species that must still be described. This highlights the unknown and yet-undiscovered richness of earthworms in the Rio Doce watershed. Therefore, further attention is needed to understand this important guild of ecosystem engineers, particularly considering their on soil processes and plant growth. Additional relevance is observed when we consider that this basin was the theater of the largest impact of a mining dam breach in the world so far (Fernandes et al. \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2016\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eThis study presents for the first time the temporal nature of earthworm diversity in riparian forest areas impacted by the mining tailings along the Doce River basin. It highlights climate as a key modulator of earthworm diversity, a vector of change shown to be important also at global level (Phillips et al. \u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). The gain in species observed between sampling years confirms the need for monitoring and inventories performed in periods of higher rainfall. The trend found in the impacted sites indicates it is a phenomenon independent of land cover. Rainfall maintains soil moisture which is directly related to earthworm abundance, biomass and activity (Yadav and Mullah \u003cspan citationid=\"CR70\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Singh et al. \u003cspan citationid=\"CR61\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). Earthworms breathe through their skin and must keep it moist at all times (Sharma and Poonam \u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e2014\u003c/span\u003e). Drier soil can also induce earthworm aestivation or diapause (Maleri et al. 2008). Considering that earthworms are the main soil-engineering macroinvertebrates, climate change can compromise the functioning of ecosystems and the network of ecological interactions (Singh et al. \u003cspan citationid=\"CR61\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). Our results clearly show that the magnitude of the effect of climate on these organisms is dependent on the climatic condition, over and above the condition of the soil itself.\u003c/p\u003e \u003cp\u003eOf the earthworm species recorded, one-third were invasive (six species) in the sampled areas of the Atlantic Forest. These results confirm observations of Demetrio et al. (2023), who reported that 39% of the species redorded in the Atlantic Forest are invasives. This scenario reinforces a warning about the silent invasion of exotic earthworms in one of the world's diversity hotspots (Myers et al. \u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e2000\u003c/span\u003e). Although apparently silent, some of these invasive species, including \u003cem\u003eA. gracilis\u003c/em\u003e reported here, possess high physiological and reproductive plasticity, which has been associated with their ability to outcompete native species (Novo et al. \u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e2015\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eFurthermore, we noted in this study that the most abundant species (86% of the individuals sampled) was the invasive and peregrine species \u003cem\u003eP. corethrurus\u003c/em\u003e, a highly plastic r-strategist with flexible diet (Taheri et al. \u003cspan citationid=\"CR63\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). This species, along with \u003cem\u003eEisenia fetida\u003c/em\u003e, is considered a bioindicator of soils contaminated by heavy metals due to their high tolerance to such conditions (S\u0026aacute; et al. \u003cspan citationid=\"CR58\" class=\"CitationRef\"\u003e2024\u003c/span\u003e). Although \u003cem\u003eP. corethrurus\u003c/em\u003e is also found in undisturbed environments, land use change has been identified as one of the main factors explaining its abundance in various parts of the world (Marichal et al. \u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e2010\u003c/span\u003e). However, \u003cem\u003eP. corethrurus\u003c/em\u003e is also known to alter soil structure depending on soil properties (Taheri et al \u003cspan citationid=\"CR63\" class=\"CitationRef\"\u003e2018\u003c/span\u003e), and cause soil compaction in clayey soils, especially with low concentrations of organic matter and in the absence of species that do not promote decompaction (Hallaire et al. \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2000\u003c/span\u003e). According to Hallaire et al. (\u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2000\u003c/span\u003e), it can increase macroaggregation and reduce water infiltration and soil moisture. On the other hand, it can favor the bioavailability of nitrogen and phosphorus in the soil and consequently be beneficial for the establishment and development of plant species (Teng et al. \u003cspan citationid=\"CR64\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; Trap et al. \u003cspan citationid=\"CR68\" class=\"CitationRef\"\u003e2021\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eIn our study, we observed that the abundance of earthworms, even predominantly invasive species, was positively correlated with an increase in plant diversity in the regenerating stratum of reference riparian forest sites. Conversely, in riparian forests with soils impacted by mining waste from the Fund\u0026atilde;o dam, higher earthworm abundance was associated with lower plant diversity. In the reference areas, the forests support a variety of earthworm species and other soil macrofauna that may help mitigate the negative effects of invasive species, such as soil compaction and population imbalances (Barros et al. \u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2004\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eIn areas impacted by mining, earthworms can alter the mobility of heavy metals in the soil through their feeding, digging, and/or casting (Duarte et al. \u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; Boukirat and Maatoug \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). The way in which heavy metals are mobilized varies according to the species of earthworm and the type of metal (Boukirat and Maatoug \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). In this sense, several studies have evaluated vermicomposting, i.e. the removal or degradation of contaminants from the soil by earthworms, as an alternative for rehabilitating areas contaminated by heavy metals (Ge et al. \u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e2023\u003c/span\u003e), consequently increasing the chances of greater re-establishment and plant development. However, this does not seem to be the case for the earthworm species found in the impacted areas. It is known that some earthworm species such as \u003cem\u003eE. fetida\u003c/em\u003e can further increase the bioavailability of heavy metals in the soil and interfere with plant development (Ruiz et al. \u003cspan citationid=\"CR57\" class=\"CitationRef\"\u003e2009\u003c/span\u003e). This may be the case with \u003cem\u003eP. corethrurus\u003c/em\u003e, suggesting that experimental studies are needed to better elucidate the relationship between these earthworms and tailings-impacted soils with high pH, and high silt and iron concentrations. Our previous studies also indicate that in sites with deposition of mining tailings, some ecological processes have been altered (Nadolny et al. \u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e2024\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eRegarding our original hypotheses, we were able to confirm H1 and H2, with higher earthworm diversity being found in both reference and impacted sites in the year with higher precipitation (2024). Furthermore, we found that earthworm species composition was affected by climate and revealed mostly species gains, though these occurred in both reference and impacted sites, so H3 was not totally confirmed. Finally, regarding the regenerating vegetation of the riparian forest, we found that both total and invasive earthworm species abundance were positively correlated with the diversity of juvenile plant species in reference sites, but not in impacted sites, thus not supporting H4. In contrast, the abundance of native earthworm species was not associated with plant species diversity in either reference or impacted sites, thereby refuting H5.\u003c/p\u003e \u003cp\u003eIn conclusion, our results highlight the importance of climate variation and mining tailings on earthworm communities and the consequent impacts on vegetation structure and dynamics. In addition, this study contributes to a better understanding of the environmental impacts of the largest mining disaster on one of the world's diversity hotspots and of possible mitigating measures to facilitate its recovery. While soil biodiversity has been neglected in the assessments of environmental impacts in the regions impacted by the disaster, this study clearly shows that soil animals must be considered bioindicators and that their interactions with vegetation are important integral parts of ecosystem functioning and recovery. Furthermore, it also reveals that invasive species, such as the dominant \u003cem\u003eP. corethrurus\u003c/em\u003e, do not appear to have negative impacts on vegetation dynamics in reference sites, but that this species and the remaining earthworm community are not assisting vegetation recovery in impacted areas. This is an important finding as increasing soil functionality is needed to accelerate ecosystem development and augment its resilience. Further investigation into the potential positive synergies between earthworm communities and key ecosystem processes \u0026mdash; such as soil aggregation, water infiltration and retention, plant growth, and the restoration of native vegetation in impacted areas compared to reference sites \u0026mdash; is urgently needed. Additionally, strategies to enhance revegetation and facilitate the recolonization of these impacted areas are essential, in order to attract native soil species and foster biodiversity recovery.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eAcknowledgements\u003c/strong\u003e\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eWe are grateful to the anonymous reviewers for their suggestions and contributions to the work. The authors thank Daniel Negreiros for his efforts in organizing the data from the initial plant and earthworm sampling, as well as Rubens M Santos for plant taxonomic identification. This research was supported by Funda\u0026ccedil;\u0026atilde;o de Amparo \u0026agrave; Pesquisa do Estado de Minas Gerais (FAPEMIG: APQ-03622-17, APQ-00031-19) and Brazilian Council for Scientific and Technological Development (CNPq, grant no. 316258/2021-0, 312824/2022-0, and 441930/2020-4 to GWF and GGB) as well as the Funda\u0026ccedil;\u0026atilde;o Arauc\u0026aacute;ria (TAX2021231000002).\u003c/p\u003e\u003cp\u003e\u003cstrong\u003eConflict of interest\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003e\u0026nbsp;\u003c/strong\u003eThe authors have no relevant financial or non-financial interests to disclose.\u003c/p\u003e\n\u003cp\u003e\u0026nbsp;\u003cstrong\u003eAuthor Contributions\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u0026nbsp;All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Walisson Kenedy-Siqueira, Yumi Oki, Marcos Paulo Santos, Jo\u0026atilde;o Carlos Gomes Figueiredo, Francisco Alves de Amorim Soares and Herlon Nadolny. The identification of the specimens (earthworms) was done by Luis Manuel Hern\u0026aacute;ndez-Garc\u0026iacute;a. The first draft of the manuscript was written by Walisson Kenedy-Siqueira and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.\u003c/p\u003e\n"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003eAnderson JM, Ingram JSI (1993) Tropical soil biology and fertility. Soil Sci 157: 265.\u003c/li\u003e\n\u003cli\u003eBarros E, Grimaldi M, Sarrazin M, Chauvel A, Mitja D, Desjardins T, Lavelle P (2004) Soil physical degradation and changes in macrofaunal communities in Central Amazon. Appl Soil Ecol 26:157-168.\u003c/li\u003e\n\u003cli\u003eBarthod J, Dignac MF, Le Mer G, Bottinelli N, Watteau F, K\u0026ouml;gel-Knabner I, Rumpel C (2020) How do earthworms affect organic matter decomposition in the presence of clay-sized minerals? Soil Biol Biochem 143:107730.\u003c/li\u003e\n\u003cli\u003eBeier C, Beierkuhnlein C, Wohlgemuth T, Penuelas J, Emmett B, K\u0026ouml;rner C, Boeck H, Christensen JH, Leuzinger S, Janssens IA, Hansen K (2012). Precipitation manipulation experiments\u0026ndash;challenges and recommendations for the future. Ecol Lett 15:899-911.\u003c/li\u003e\n\u003cli\u003eBlakemore RJ (2002) Cosmopolitan earthworms: an eco-taxonomic guide to the peregrine species of the world. Canberra: VermEcology. 506 p.\u003c/li\u003e\n\u003cli\u003eBoukirat D, Maatoug M (2021) Bioremediation of lead contaminated soils for sustainable agriculture. Ecol Intensif Nat Resour Sustain Agric 341-380.\u003c/li\u003e\n\u003cli\u003eBrown GG, da Silva E, Thomazini MJ, Niva CC, Deca\u0026euml;ns T, Cunha N, Nadolny HS, Demetrio WC, Santos A, Ferreira T, Maia LS, Conrado AC, Segalla RF, Ferreira AC, Pasini A, Bartz MLC, Sautter KD, James SW, Baretta D, Antoniolli ZI (2018) The role of soil fauna in soil health and delivery of ecosystem services. In: D. Reicosky (Eds.): Managing soil health for sustainable agriculture. 1 ed. Cambridge: Burleigh Dodds Science Publishing Limited. P. 197-242.\u003c/li\u003e\n\u003cli\u003eBrown GG, Fragoso C (2007) Minhocas na Am\u0026eacute;rica Latina: Biodiversidade e ecologia. 1 ed. Londrina (PR): Embrapa Soja. 547 p.\u003c/li\u003e\n\u003cli\u003eBrown GG, Pashanasi B, Villenave C, Patron JC, Senapati BK, Giri S, Barois I, Lavelle P, Blancharf E, Blakemore RJ, Spain AL, Boyer J (1999). Effects of earthworms on plant production in the tropics. In: P. Lavelle, L. Brussaard, P. Hendrix (Eds.) Earthworm management in tropical agroecosystems. 1 ed. New York: CABI Publishing. P. 87-147.\u003c/li\u003e\n\u003cli\u003eCarmo FF, Kamino LHY, Tobias Junior R, de Campos IC, Carmo FF, Silvino G, de Castro KJSX, Mauro ML, Rodrigues NUA, Miranda MPS, Pinto CEF (2017) Fund\u0026atilde;o tailings dam failures: the environment tragedy of the largest technological disaster of Brazilian mining in global context. PECON 15:145-151.\u003c/li\u003e\n\u003cli\u003eChazdon RL (2013) Tropical forest regeneration. In S. A. Levin (Ed.). Encylopedia of biodiversity, (2nd edn), pp. 277\u0026ndash;286. Academic Press, Waltham, MA.\u003c/li\u003e\n\u003cli\u003eChazdon RL, Guariguata MR (2016). Natural regeneration as a tool for large‐scale forest restoration in the tropics: prospects and challenges. Biotropica 48:716-730.\u003c/li\u003e\n\u003cli\u003eCraven D, Thakur MP, Cameron EK, Frelich LE, Beaus\u0026eacute;jour R, Blair RB, Blossey B, Burtis J, Choi A, D\u0026aacute;valos A, Fahey TJ, Fisichelli NA, Gibson K, Handa IT, Hopfensperger K, Loss SR, Nuzzo V, Maerz JC, Sackett T, Scharenbroch BC, Smith SM, Vellend M, Umek LG, Eisenhauer N (2017) The unseen invaders: introduced earthworms as drivers of change in plant communities in North American forests (a meta‐analysis). Glob Chang Biol 23:1065-1074.\u003c/li\u003e\n\u003cli\u003eCrouzeilles R, Ferreira, MS, Chazdon RL, Lindenmayer DB, Sansevero JB, Monteiro L, Iribarrem A, Latawiec AE, Strassburg BB (2017) Ecological restoration success is higher for natural regeneration than for active restoration in tropical forests. Sci Adv 3:e1701345.\u003c/li\u003e\n\u003cli\u003eDem\u0026eacute;trio W, Brown G, Pupin B, Novo R, Dudas R, Baretta D, R\u0026ouml;mbke J, Bartz M, Borma L (2023) Are exotic earthworms threatening soil biodiversity in the Brazilian Atlantic Forest?. Appl Soil Ecol 182:104693. DOI: 10.1016/j.apsoil.2022.104693\u003c/li\u003e\n\u003cli\u003eDemetrio W, Cavalieri-Polizeli KMV, Guimar\u0026atilde;es RML, de Almeida-Ferreira S, Parron LM, Brown GG (2022) Macrofauna communities and their relationship with soil structural quality in different land use systems. Soil Res 60:648-660. DOI:10.1071/SR21157\u003c/li\u003e\n\u003cli\u003eDray S, Bauman D, Blanchet G, Borcard D, Clappe S, Gu\u0026eacute;nard G, Jombart T, Larocque G, Legendre P, Madi N, Wagner HH (2022) Adespatial: Multivariate Multiscale Spatial Analysis. R package version 0.3-23 [online]. Retrieved in 2023, November 23, from https://CRAN.R-project.org/package=adespatial\u003c/li\u003e\n\u003cli\u003eDrouin M, Bradley R, Lapointe L (2016) Linkage between exotic earthworms, understory vegetation and soil properties in sugar maple forests. For Ecol Manag 364:113-121.\u003c/li\u003e\n\u003cli\u003eDuarte AP, Brown, GG, Pauletti V (2012) Changes in the forms of lead and manganese in soils by passage through the gut of the tropical endogeic earthworm (\u003cem\u003ePontoscolex corethrurus\u003c/em\u003e). Eur J Soil Biol 53:32-39.\u003c/li\u003e\n\u003cli\u003eEisenhauer N, Stefanski A, Fisichelli NA, Rice K, Rich R, Reich PB (2014) Warming shifts \u0026lsquo;worming\u0026rsquo;: effects of experimental warming on invasive earthworms in northern North America. Sci Rep 4:6890.\u003c/li\u003e\n\u003cli\u003eFerlian O, Wirth C, Eisenhauer N (2017) Leaf and root C-to-N ratios are poor predictors of soil microbial biomass C and respiration across 32 tree species. Pedobiologia 65:16-23.\u003c/li\u003e\n\u003cli\u003eFernandes GW, Ramos L, Goulart FF, Figueiredo JCG, Kenedy-Siqueira W, Toma TSP, ... \u0026amp; Negreiros D (2025) Mining scars may lead riparian ecosystem to multiple tipping points in a biodiversity hotspot. Anthropocene (under review).\u003c/li\u003e\n\u003cli\u003eFernandes GW, Goulart FF, Ranieri BD, Coelho MS, Dales K, Boesche N, Bustamante M, Carvalho FA, Carvalho DC, Dirzo R, Fernandes S, Galetti PM, Millan VEG, Mielke C, Ramirez JL, Neves A, Rogass C, Ribeiro SP, Scariot A, Soares-Filho B (2016). Deep into the mud: ecological and socio-economic himpacts of the dam breach in Mariana, Brazil. Nat Cons 14:35-45. DOI: 10.1016/j.ncon.2016.10.003\u003c/li\u003e\n\u003cli\u003eFrelich LE, Blossey B, Cameron EK, D\u0026aacute;valos A, Eisenhauer N, Fahey T, ... \u0026amp; Reich PB (2019) Side‐swiped: ecological cascades emanating from earthworm invasions. Front Ecol Environ 17:502-510.\u003c/li\u003e\n\u003cli\u003eFrouz J (2018) Effects of soil macro-and mesofauna on litter decomposition and soil organic matter stabilization. Geoderma 332:161-172.\u003c/li\u003e\n\u003cli\u003eGe Y, Huang C, Zhou W, Shen Z, Qiao Y (2023) \u003cem\u003eEisenia fetida\u003c/em\u003e impact on cadmium availability and distribution in specific components of the earthworm drilosphere. Environ Sci Pollut Res 30:112222-112235.\u003c/li\u003e\n\u003cli\u003eGibson KD, Quackenbush PM, Emery NC, Jenkins MA, Kladivko EJ (2013) Invasive earthworms and plants in Indiana old-and second-growth forests. IPSM 6:161-174.\u003c/li\u003e\n\u003cli\u003eGuhra T, Stolze K, Schweizer S, Totsche KU (2020) Earthworm mucus contributes to the formation of organo-mineral associations in soil. Soil Biol Biochem 145:107785.\u003c/li\u003e\n\u003cli\u003eHale CM, Frelich LE, Reich PB, Pastor J (2008) Exotic earthworm effects on hardwood forest floor, nutrient availability and native plants: a mesocosm study. Oecologia 155:509-518. DOI: https://doi.org/10.1007/s00442-007-0925-6\u003c/li\u003e\n\u003cli\u003eHale CM, Lee EF, Peter BR (2006) \u0026quot;Changes in hardwood forest understory plant communities in response to European earthworm invasions. Ecology 87:1637-1649. DOI: 10.1890/0012-9658(2006)87[1637:cihfup]2.0.co;2\u003c/li\u003e\n\u003cli\u003eHale AN, Lapointe L, Kalisz S. Invader disruption of belowground plant mutualisms reduces carbon acquisition and alters allocation patterns in a native forest herb. New Phytol 209:542-549. https://doi.org/10.1111/nph.13709\u003c/li\u003e\n\u003cli\u003eHallaire V, Curmi P, Duboisset A, Lavelle P, Pashanasi B (2000) Soil structure changes induced by the tropical earthworm Pontoscolex corethrurus and organic inputs in a peruvian ultisol. Eur J Soil Biol 36:35-44. DOI: 10.1016/S1164-5563(00)01048-7\u003c/li\u003e\n\u003cli\u003eHern\u0026aacute;ndez-Garc\u0026iacute;a LM, Burgos-Guerrero JE, Tamires B, Rousseau GX, James SW (2018) Three new species of \u003cem\u003eHoloscolex\u003c/em\u003e (Clitellata, Glossoscolecidae) from the Gurupi Biological Reserve, last forest remnant of the Bel\u0026eacute;m endemism area, eastern Amazon. Zootaxa 4496:459-471. DOI: 10.11646/zootaxa.4496.1.35\u003c/li\u003e\n\u003cli\u003eHuston M (1979) A general hypothesis of species diversity. Am Nat 113:81-101.\u003c/li\u003e\n\u003cli\u003eLaigle I, Moretti M, Rousseau L, Gravel D, Venier L, Handa IT, Messier C, Morris D, Hazlett P, Fleming R, Webster K, Shipley B, Aubin I (2021) Direct and indirect effects of forest anthropogenic disturbance on above and below ground communities and litter decomposition. Ecosystems 24:1-22.\u003c/li\u003e\n\u003cli\u003eLarson ER, Kipfmueller KF, Hale CM, Frelich LE, Reich PB (2010) Tree rings detect earthworm invasions and their effects in northern Hardwood forests. Biol Invasions 12:1053-1066.\u003c/li\u003e\n\u003cli\u003eLavelle P, Spain A, Blouin M, Brown G, Deca\u0026euml;ns T, Grimaldi M, Jim\u0026eacute;nez JJ, McKey D, Mathieu J, Velasquez E, Zangerl\u0026eacute; A (2016) Ecosystem engineers in a self-organized soil. Soil Sci 181:91-109. DOI: 10.1097/SS.0000000000000155\u003c/li\u003e\n\u003cli\u003eLegendre P (2019) A temporal beta‐diversity index to identify sites that have changed in exceptional ways in space\u0026ndash;time surveys. Ecol Evol 9:3500-3514.\u003c/li\u003e\n\u003cli\u003eLegg S (2021) IPCC 2021: climate change 2021-the physical science basis. Interaction 49:44-45.\u003c/li\u003e\n\u003cli\u003eLi X, Zuo X, Qiao J, Hu Y, Wang S, Yue P, Cheng H, Song Z, Chen M, Hautier Y (2024) Context‐dependent impact of changes in precipitation on the stability of grassland biomass. Funct Ecol 38:1185-1198.\u003c/li\u003e\n\u003cli\u003eMarichal R, Martinez A F, Praxedes C, Ruiz D, Carvajal AF, Oszwald J, Hurtado MDelP, Brown GG, Grimaldi M, Desjardins t, Sarrazin M, Deca\u0026euml;ns T, Velasquez E, Lavelle P (2010) Invasion of \u003cem\u003ePontoscolex corethrurus\u003c/em\u003e (Glossoscolecidae, Oligochaeta) in landscapes of the Amazonian deforestation arc. Appl Soil Ecol 46:443-449.\u003c/li\u003e\n\u003cli\u003eMathieu J, Reynolds JW, Fragoso C, Hadly E (2024) Multiple invasion routes have led to the pervasive introduction of earthworms in North America. Nat Ecol Evol 8:489-499. DOI: 10.1038/s41559-023-02310-7\u003c/li\u003e\n\u003cli\u003eMenino GCO, Nunes YRF, Santos RM, Fernandes GW, Fernandes LA (2012) Environmental heterogeneity and natural regeneration in riparian vegetation of the Brazilian semi-arid region. Edinb. J. Bot 69:29\u0026ndash;51. DOI: 10.1017/S0960428611000400.\u003c/li\u003e\n\u003cli\u003eMyers N, Mittermeier RA, Mittermeier CG, Da Fonseca GA, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853-858.\u003c/li\u003e\n\u003cli\u003eNadolny H, Oki Y, Kenedy-Siqueira W, Brown GG, Santos MP, Hern\u0026aacute;ndez-Garc\u0026iacute;a LM, Negreiros D, Figueiredo JC, Goulart FF, Fernandes GW. (2024). Devastating Rio Doce mining disaster sends shockwaves through earthworm populations. Journal of Environmental Quality under review. \u003c/li\u003e\n\u003cli\u003eNearing MA, Pruski FF, O\u0026apos;neal MR (2004). Expected climate change impacts on soil erosion rates: a review. JSWC 59:43-50.\u003c/li\u003e\n\u003cli\u003eNeves et al. 2024 Flora and Structure of the Naturally Regenerating Riparian Vegetation of the Rio Doce River: Basis for Environmental Restoration Actions \u003c/li\u003e\n\u003cli\u003eNovo M, Cunha L, Maceda-Veiga A, Talavera JA, Hodson ME, Spurgeon D, Bruford MW, Morgan AJ, Kille P (2015) Multiple introductions and environmental factors affecting the establishment of invasive species on a volcanic island. Soil Biol Biochem 85:89-100.\u003c/li\u003e\n\u003cli\u003eOksanen J, Simpson G, Blanchet F, Kindt R, Legendre P, Minchin P, O\u0026apos;Hara R, Solymos P, Stevens M, Szoecs E, Wagner H, Barbour M, Bedward M, Bolker B, Borcard D, Carvalho G, Chirico M, De Caceres M, Durand S, Evangelista H, Fitzjohn R, Friendly M, Furneaux B, Hannigan G, Hill M, Lahti L, McGlinn D, Ouellette M, Ribeiro, Cunha E, Smith T, Stier A, Ter Braak C, Weedon J (2022) Vegan: Community Ecology Package. R package version 2.6-4. Retrieved from https://CRAN.R-project.org/package=vegan\u003c/li\u003e\n\u003cli\u003ePeixoto RT, Marochi AI (1996) A influ\u0026ecirc;ncia da minhoca \u003cem\u003ePheretima\u003c/em\u003e sp. nas propriedades de um latossolo vermelho escuro \u0026aacute;lico e no desenvolvimento de culturas em sistema de plantio direto, em Arapoti-PR. Revista Plantio Direto, 35:23-35.\u003c/li\u003e\n\u003cli\u003ePhillips HR, Bach EM, Bartz ML, Bennett JM, Beugnon R, Briones MJ, ... Webster ER (2021) Global data on earthworm abundance, biomass, diversity and corresponding environmental properties. Sci Data 8, 136. DOI:10.1038/s41597-021-00912-z\u003c/li\u003e\n\u003cli\u003ePhillips, HRP \u003cem\u003eet al., \u003c/em\u003eGlobal distribution of earthworm diversity. \u003cem\u003eScience \u003c/em\u003e366,480-485 (2019). DOI:10.1126/science.aax4851\u003c/li\u003e\n\u003cli\u003ePop VV, Pop AA (2006) Lumbricid earthworm invasion in the carpathian mountains and some other sites in Romania. In: P.F. Hendrit (Eds) Biological Invasions Belowground: Earthworms as Invasive Species. Dordrecht: Springer. P. 19-22. DOI: 10.1007/978-1-4020-5429-7_3\u003c/li\u003e\n\u003cli\u003eR Core Team (2024) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available in: https://www.R-project.org/\u003c/li\u003e\n\u003cli\u003eRamos L, Negreiros D, Goulart FF, Figueiredo JCG, Kenedy-Siqueira W, Toma TSP, ... \u0026amp; Fernandes GW (2024). Dissimilar forests along the Rio Doce watershed call for multiple restoration references to avoid biotic homogenization. Sci Total Environ 930, 172720. DOI: 10.1016/j.scitotenv.2024.172720\u003c/li\u003e\n\u003cli\u003eRighi G (1995) Colombian earthworms. In: T. Van der Hammen, A.G. dos Santos, (Eds.): La Cordillera Central Colombiana Transecto Parque Los Nevados. 3 ed. Berlin-Stuttgart. P. 485-607\u003c/li\u003e\n\u003cli\u003eRuiz E, Rodr\u0026iacute;guez L, Alonso-Azc\u0026aacute;rate J (2009) Effects of earthworms on metal uptake of heavy metals from polluted mine soils by different crop plants. Chemosphere 75:1035-1041.\u003c/li\u003e\n\u003cli\u003eS\u0026aacute; ACN, Souza GF, de Freitas GP, Alves NBP, Silva RMG, Santos LAP, de Lima RM (2024) \u003cem\u003eEisenia fetida\u003c/em\u003e e \u003cem\u003ePontoscolex corethrurus\u003c/em\u003e como bioindicadoras de ambientes contaminados por metais pesados. Contrib Las Cienc Soc 17:e5249-e5249.\u003c/li\u003e\n\u003cli\u003eSackett TE, Smith SM, Basiliko N (2013) Efeitos indiretos e diretos de minhocas ex\u0026oacute;ticas em nutrientes do solo e dep\u0026oacute;sitos de carbono em florestas temperadas norte-americanas. Soil Biol Biochem 57:459-467.\u003c/li\u003e\n\u003cli\u003eSharma RK, Poonam B (2014) Earthworm diversity in trans-gangetic habitats of Haryana, India. Res J Agric For Sci 2:1-7.\u003c/li\u003e\n\u003cli\u003eSingh J, Sch\u0026auml;dler M, Demetrio W, Brown GG, Eisenhauer N (2019) Climate change effects on earthworms - a review. Soil Org 91:114-138. DOI: 10.25674%2Fso91iss3pp114\u003c/li\u003e\n\u003cli\u003eSingh S, Singh J, Vig AP (2016) Earthworm as ecological engineers to change the physico-chemical properties of soil: Soil vs vermicast. Ecol Eng 90:1-5. DOI: 10.1016/j.ecoleng.2016.01.072\u003c/li\u003e\n\u003cli\u003eTaheri S, Pelosi C, Dupont L (2018) Harmful or useful? A case study of the exotic peregrine earthworm morphospecies \u003cem\u003ePontoscolex corethrurus\u003c/em\u003e. Soil Biol Biochem 116:277-289. DOI: 10.1016/j.soilbio.2017.10.030\u003c/li\u003e\n\u003cli\u003eTeng SK, Aziz NAA, Mustafa M, Laboh R, Ismail IS, Devi S (2016) Potential role of endogeic earthworm \u003cem\u003ePontoscolex corethrurus\u003c/em\u003e in remediating banana blood disease: a preliminary observation. Eur J Plant Pathol 145:321-330.\u003c/li\u003e\n\u003cli\u003eThakur MP, Reich PB, Hobbie SE, Stefanski A, Rich R, Rice KE, Eddy WC Eisenhauer N (2018) Reduced feeding activity of soil detritivores under warmer and drier conditions. Nat Clim Change 8:75-78.\u003c/li\u003e\n\u003cli\u003eThe Angiosperm Phylogeny Group, M. W. Chase, M. J. M. Christenhusz, M. F. Fay, J. W. Byng, W. S. Judd, D. E. Soltis, D. J. Mabberley, A. N. Sennikov, P. S. Soltis, P. F. Stevens, An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV, \u003cem\u003eBotanical Journal of the Linnean Society\u003c/em\u003e, Volume 181, Issue 1, May (2016), Pages 1\u0026ndash;20, https://doi.org/10.1111/boj.12385\u003c/li\u003e\n\u003cli\u003eThouvenot L, Ferlian O, Horn L, Jochum M, Eisenhauer N (2024) Effects of earthworm invasion on soil properties and plant diversity after two years of field experiment. NeoBiota 94:31-56.\u003c/li\u003e\n\u003cli\u003eTrap J, Blanchart E, Ratsiatosika O, Razafindrakoto M, Becquer T, Andriamananjara A, Morel C (2021) Effects of the earthworm \u003cem\u003ePontoscolex corethrurus\u003c/em\u003e on rice P nutrition and plant-available soil P in a tropical Ferralsol. Appl Soil Ecol 160:103867.\u003c/li\u003e\n\u003cli\u003eWalsh CL, Johnson-Maynard JL (2016) Earthworm distribution and density across a climatic gradient within the Inland Pacific Northwest cereal production region. Appl Soil Ecol 104:104-110.\u003c/li\u003e\n\u003cli\u003eYadav S, Mullah M (2017) A review on molecular markers as tools to study earthworm diversity. IJPAZ 5:62-69.\u003c/li\u003e\n\u003cli\u003eYuan Z, Ali A, Loreau M, Ding F, Liu S, Sanaei A, Zhou W, Ye J, Lin F, Fang S, Hao Z, Wang X, Le Bagousse-Pinguet Y. Divergent above- and below-ground biodiversity pathways mediate disturbance impacts on temperate forest multifunctionality. Glob Chang Biol. (2021) Jun;27(12):2883-2894. doi: 10.1111/gcb.15606. Epub 2021 Mar 30. PMID: 33742479.\u003c/li\u003e\n\u003cli\u003eZhang M, Zou X, Schaefer DA (2010) Alteration of soil labile organic carbon by invasive earthworms (\u003cem\u003ePontoscolex corethrurus\u003c/em\u003e) in tropical rubber plantations. Eur J Soil Biol 46:74-79. DOI: 10.1016/j.ejsobi.2009.11.004\u003c/li\u003e\n\u003c/ol\u003e"},{"header":"Table 1","content":"\u003cp\u003eTable 1 is available in the Supplementary Files section.\u003c/p\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"biological-invasions","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"binv","sideBox":"Learn more about [Biological Invasions](https://www.springer.com/journal/10530)","snPcode":"10530","submissionUrl":"https://submission.nature.com/new-submission/10530/3","title":"Biological Invasions","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"Springer Hybrid","inReviewEnabled":true,"inReviewRevisionsEnabled":false},"keywords":"Ecosystem engineers, Habitat disturbances, Invasive earthworms, Mining tailings impact, Samarco mining disaster","lastPublishedDoi":"10.21203/rs.3.rs-5544777/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-5544777/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eSoil structure, along with the fauna and plant biodiversity it sustains, can be affected by various factors, including both natural and human-induced disturbances such as climate fluctuations and mining activities. Earthworms are ecosystem engineers highly affected by these changes in soil conditions. In the present study, we evaluated earthworm community in different climatic periods and their impact on plant diversity in a region affected by mining tailings. Earthworm diversity was significantly higher during the period of higher precipitation, both in areas affected by mining tailings and in reference sites. Additionally, the composition of earthworm species was impacted, showing predominantly gains despite the influence of mining waste. The total and invasive abundance of earthworms was linked to greater plant diversity in the regenerating stratum of reference sites but not in areas impacted by mining waste. These findings highlight the potential consequences of climate change and mining disasters on earthworm communities, as well as on ecosystem structure and dynamics. Moreover, they underscore the environmental impacts of the world's largest mining disaster on earthworm diversity within one of the planet's key biodiversity hotspots, emphasizing the urgent need for improved recovery strategies.\u003c/p\u003e","manuscriptTitle":"Microclimate and mining stresses the diversity of earthworms and further impact the regeneration of forests along the Rio Doce","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2025-01-01 07:02:09","doi":"10.21203/rs.3.rs-5544777/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"reviewerAgreed","content":"","date":"2024-12-30T21:14:32+00:00","index":0,"fulltext":""},{"type":"reviewersInvited","content":"","date":"2024-12-30T15:56:26+00:00","index":"","fulltext":""},{"type":"editorInvited","content":"Biological Invasions","date":"2024-11-29T19:59:57+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2024-11-29T06:44:16+00:00","index":"","fulltext":""},{"type":"submitted","content":"Biological Invasions","date":"2024-11-28T14:42:29+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"biological-invasions","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"binv","sideBox":"Learn more about [Biological Invasions](https://www.springer.com/journal/10530)","snPcode":"10530","submissionUrl":"https://submission.nature.com/new-submission/10530/3","title":"Biological Invasions","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"Springer Hybrid","inReviewEnabled":true,"inReviewRevisionsEnabled":false}}],"origin":"","ownerIdentity":"a86ff1fb-bc45-4b46-bbd9-f5496854db38","owner":[],"postedDate":"January 1st, 2025","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[],"tags":[],"updatedAt":"2025-11-17T16:03:18+00:00","versionOfRecord":{"articleIdentity":"rs-5544777","link":"https://doi.org/10.1007/s10530-025-03694-2","journal":{"identity":"biological-invasions","isVorOnly":false,"title":"Biological Invasions"},"publishedOn":"2025-11-14 15:58:23","publishedOnDateReadable":"November 14th, 2025"},"versionCreatedAt":"2025-01-01 07:02:09","video":"","vorDoi":"10.1007/s10530-025-03694-2","vorDoiUrl":"https://doi.org/10.1007/s10530-025-03694-2","workflowStages":[]},"version":"v1","identity":"rs-5544777","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-5544777","identity":"rs-5544777","version":["v1"]},"buildId":"8U1c8b4HqxoKbykW_rLl7","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}