Abstract
Mining is responsible for drastic ecosystem changes and rehabilitation is used to promote the return of functions after these impacts. In this scenario, we investigated the responses of ant assemblages and diaspore removal by ants to the transformations caused by mining and rehabilitation predicting that (a) the increase in plant density (a proxy for mining intensity) led to an increase in ant richness, percentage of diaspores removed, and changes in species composition that in turn are correlated with changes in environmental variables; (b) the increase in vegetation structure (a proxy for rehabilitation ages) led to an increase in ant richness, percentage of diaspores removed, and changes in species composition that in turn are correlated with changes in environmental variables. Additionally, we also verified which functional groups were primarily responsible for diaspore removal. We sampled arboreal and epigeic ants, diaspore removal by ants, and environmental variables. We found that ant richness and diaspore removal in mining intensity gradient are positively correlated to plant density. Although vegetation structure is positively correlated with ant richness, we found no changes in diaspore removal in rehabilitation gradient. Epigeic omnivore and epigeic generalist predator ants were the most responsible for diaspore removal. Then, we observed that mining decreases ant richness, altering ant assemblages and their functions, and rehabilitation with exotic plants is ineffective to promote the colonization by the main diaspore-removing ants.
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Alvares CA, Stape JL, Sentelhas PC, de Moraes Gonçalves JL, Sparovek G (2013) Köppen’s climate classification map for Brazil. Meteorol Z 22:711–728. https://doi.org/10.1127/0941-2948/2013/0507
Andersen AN (1995) A classification of Australian ant communities, based on functional groups which parallel plant life-forms in relation to stress and disturbance. J Biogeogr 1995:15–29. https://doi.org/10.2307/2846070
Andersen AN, Majer JD (2004) Ants show the way down under: invertebrates as bioindicators in land management. Front Ecol Environ 2:291–298. https://doi.org/10.1890/1540-9295(2004)002[0292:ASTWDU]2.0.CO;2
Andersen AN, Morrison SC (1998) Myrmecochory in Australia’s seasonal tropics: effects of disturbance on distance dispersal. Austral J Ecol 23:483–491. https://doi.org/10.1111/j.1442-9993.1998.tb00756.x
Angotti MA, Rabello A, Santiago G, Ribas CR (2018) Seed removal by ants in Brazilian savanna: optimizing fieldwork. Sociobiology 65:155–161. https://doi.org/10.13102/sociobiology.v65i2.1938
Anjos DV, Leal LC, Jordano P, Del-Claro K (2020) Ants as diaspore removers of non-myrmecochorous plants: a meta-analysis. Oikos. 129:775–786. https://doi.org/10.1111/oik.06940
Aragão GAS, Oliveira-Filho WLD (2011) Mine dump classification in the iron ore mining. Rem Int Eng J 64:193–198. https://doi.org/10.1590/S0370-44672011000200010
Aronson J, Floret C, Le Floc’h E, Ovalle C, Pontanier R (1993) Restoration and rehabilitation of degraded ecosystems in arid and semi-arid lands. I. A view from the south. Restor Ecol 1:8–17. https://doi.org/10.1111/j.1526-100X.1993.tb00004.x
Arruda AJ, Costa FV, Guerra TJ, Junqueira PA, Dayrell RL, Messeder JV et al (2020) Topsoil disturbance reshapes diaspore interactions with ground-foraging animals in a megadiverse grassland. J Veg Sci 31:1039–1052. https://doi.org/10.1111/jvs.12866
Baccaro FB, Feitosa RM, Fernández F et al (2015) Guia para os gêneros de formigas do Brasil. Editora INPA, Brazil
Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. arXiv preprint arXiv:1406.5823
Bestelmeyer BT, Agosti D, Alonso LE et al (2000) Field techniques for the study of ground-dwelling ants: an overview, description and evaluation. Ants: standard methods for measuring and monitoring biodiversity.
Bihn JH, Gebauer G, Brandl R (2010) Loss of functional diversity of ant assemblages in secondary tropical forests. Ecology 91(3):782–792. https://doi.org/10.1890/08-1276.1
Bolton B (1994) Identification guide to the ant genera of the world. Harvard University Press
Brandão CR, Silva RR, Delabie JH (2012) Neotropical ants (Hymenoptera) functional groups: nutritional and applied implications. Insect bioecology and nutrition for integrated pest management, 213-236.
Campos RI, Lopes CT, Magalhães W, Vasconcelos HL (2008) Estratificação vertical de formigas em Cerrado strictu sensu no Parque Estadual da Serra de Caldas Novas, Goiás, Brasil. Iheringia 98(3):311–316. https://doi.org/10.1590/S0073-47212008000300004
Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, Narwani A, Mace GM, Tilman D, Wardle DA, Kinzig AP, Daily GC, Loreau M, Grace JB, Larigauderie A, Srivastava DS, Naeem S (2012) Biodiversity loss and its impact on humanity. Nature 486(7401):59–67. https://doi.org/10.1038/nature11148
Casimiro MS, Sansevero JB, Queiroz JM (2019) What can ants tell us about ecological restoration? A global meta-analysis. Ecol Indic 102:593–598. https://doi.org/10.1016/j.ecolind.2019.03.018
Chazdon RL (2008) Beyond deforestation: restoring forests and ecosystem services on degraded lands. Science 320(5882):1458–1460. https://doi.org/10.1126/science.1155365
Chevan A, Sutherland M (1991) Hierarchical partitioning. Am Stat 45:90–96. https://doi.org/10.1080/00031305.1991.10475776
Christianini AV (2015) Dispersão de sementes por poneromorfas In Delabie JH, Feitosa RM, Serrão JE, Mariano CDSF, Majer JD (eds). As formigas poneromorfas do Brasil. SciELO-Editus-Editora da UESC.
Christianini AV, Oliveira PS (2010) Birds and ants provide complementary seed dispersal in a neotropical savanna. J Ecol 98:573–582. https://doi.org/10.1111/j.1365-2745.2010.01653.x
Christianini AV, Oliveira PS, Bruna EM, Vasconcelos HL (2014) Fauna in decline: meek shall inherit. Science 345(6201):1129–1129. https://doi.org/10.1126/science.345.6201.1129-a
Costa CB, Ribeiro SP, Castro PT (2010) Ants as bioindicators of natural succession in savanna and riparian vegetation impacted by dredging in the Jequitinhonha River Basin, Brazil. Restor Ecol 18:148–157. https://doi.org/10.1111/j.1526-100X.2009.00643.x
Costa FV, Neves FS, Silva JO, Fagundes M (2011) Relationship between plant development, tannin concentration and insects associated with Copaifera langsdorffii (Fabaceae). Arthropod Plant Interact 5:9–18. https://doi.org/10.1007/s11829-010-9111-6
Costa FV, Mello R, Lana TC, Neves FS (2015) Ant fauna in megadiverse mountains: a checklist for the rocky grasslands. Sociobiology 62:228–245. https://doi.org/10.13102/sociobiology.v62i2.228-245
Crawley MJ (2013) The R book Second edition. John Wiley & Sons.
Cross AT, Young R, Nevill P, McDonald T, Prach K, Aronson J, Wardell-Johnson GW, Dixon KW (2018) Appropriate aspirations for effective post-mining restoration and rehabilitation: a response to Kaźmierczak et al. Environ Earth Sci 77:256. https://doi.org/10.1007/s12665-018-7437-z
De la Mora A, García-Ballinas JA, Philpott SM (2015) Local, landscape, and diversity drivers of predation services provided by ants in a coffee landscape in Chiapas, Mexico. Agr Ecosyst Environ 201:83–91. https://doi.org/10.1016/j.agee.2014.11.006
Delabie JH, Agosti D, Nascimento ID (2000) Litter ant communities of the Brazilian Atlantic rain forest region. Sampling Ground-dwelling Ants: case studies from the world’s rain forests. Curtin University of Technology School of Environmental Biology Bulletin, 18.
Dominguez-Haydar Y, Armbrecht I (2011) Response of ants and their seed removal in rehabilitation areas and forests at El Cerrejon coal mine in Colombia. Restor Ecol 19:178–184. https://doi.org/10.1111/j.1526-100X.2010.00735.x
Drummond GM, Martins CS, Machado AM, Sebaio FA, Antonini YO (2005) Biodiversidade em Minas Gerais: um atlas para sua conservação. Fundação Biodiversitas, Belo Horizonte, p 2
Fernandes GW (ed) (2016) Ecology and conservation of mountaintop grasslands in Brazil. Springer International Publishing
Ferreira LV, Parolin P, Matos DC et al (2016) The effect of exotic grass Urochloa decumbens (Stapf) RD Webster (Poaceae) in the reduction of species richness and change of floristic composition of natural regeneration in the Floresta Nacional de Carajás, Brazil. An Acad Bras Ciênc 88:589–597. https://doi.org/10.1590/0001-3765201620150121
Frazer GW, Canham CD, Lertzman KP (1999) Gap Light Analyzer (GLA), Version 2.0: imaging software to extract canopy structure and gap light transmission indices from true-colour fisheye photographs, user’s manual and program documentation. Simon Fraser University, Burnaby, British Columbia, and the Institute of Ecosystem Studies.
Gibb H, Sanders NJ, Dunn RR, Arnan X, Vasconcelos HL, Donoso DA, Andersen AN, Silva RR, Bishop TR, Gomez C, Grossman BF, Yusah KM, Luke SH, Pacheco R, Pearce-Duvet J, Retana J, Tista M, Parr CL (2018) Habitat disturbance selects against both small and large species across varying climates. Ecography 41(7):1184–1193. https://doi.org/10.1111/ecog.03244
Guerra TJ, Pizo MA, Silva WR (2018) Host specificity and aggregation for a widespread mistletoe in Campo Rupestre vegetation. Flora 238:148–154. https://doi.org/10.1016/j.flora.2016.12.011
Henao-Gallego N, Escobar-Ramírez S, Calle Z, Montoya-Lerma J, Armbrecht I (2012) An artificial aril designed to induce seed hauling by ants for ecological rehabilitation purposes. Restor Ecol 20(5):555–560. https://doi.org/10.1111/j.1526-100X.2011.00852.x
Hautier Y, Tilman D, Isbell F, Seabloom EW, Borer ET, Reich PB (2015) Anthropogenic environmental changes affect ecosystem stability via biodiversity. Science 348(6232):336–340. https://doi.org/10.1126/science.aaa1788
Hobbs RJ, Harris JA (2001) Restoration ecology: repairing the earth’s ecosystems in the new millennium. Restor Ecol 9:239–246. https://doi.org/10.1046/j.1526-100x.2001.009002239.x
Hobbs RJ, Norton DA (1996) Towards a conceptual framework for restoration ecology. Restor Ecol 4:93–110. https://doi.org/10.1111/j.1526-100X.1996.tb00112.x
IBRAM (Instituto Brasileiro de Mineração). 2018. (available from http://portaldamineracao.com.br/ibram/wp-content/uploads/2018/07/Diagrama%C3%A7%C3%A3o_Relat%C3%B3rioAnual_vers%C3%A3oweb.pdf)
Jacobi CM, Do Carmo FF, Vincent RC, Stehmann JR (2007) Plant communities on ironstone outcrops: a diverse and endangered Brazilian ecosystem. Biodivers Conserv 16:2185–2200. https://doi.org/10.1007/s10531-007-9156-8
Jamison SL, Robertson M, Engelbrecht I, Hawkes P (2016) An assessment of rehabilitation success in an African grassland using ants as bioindicators. Koedoe 58(1):1–16. https://doi.org/10.4102/koedoe.v58i1.1383
Kaźmierczak U, Lorenc MW, Strzałkowski P (2017) The analysis of the existing terminology related to a post-mining land use: a proposal for new classification. Environ Earth Sci 76(20):693. https://doi.org/10.1007/s12665-017-6997-7
Koch EBDA, Santos JRM, Nascimento IC, Delabie JHC (2019) Comparative evaluation of taxonomic and functional diversities of leaf-litter ants of the Brazilian Atlantic Forest. Turk J Zool 43:437–546. https://doi.org/10.3906/zoo-1811-7
Lasmar CJ, Queiroz ACM, Rabello AM, Feitosa RM, Canedo-Júnior EO, Schmidt FA, Cuissi RG, Ribas CR (2017) Testing the effect of pitfall-trap installation on ant sampling. Insect Soc 64(3):445–451. https://doi.org/10.1007/s00040-017-0558-7
Leal LC, Andersen AN, Leal IR (2014a) Anthropogenic disturbance reduces seed-dispersal services for myrmecochorous plants in the Brazilian Caatinga. Oecologia 174:173–181. https://doi.org/10.1007/s00442-013-2740-6
Leal LC, Neto MCL, de Oliveira AFM, Andersen AN, Leal IR (2014b) Myrmecochores can target high-quality disperser ants: variation in elaiosome traits and ant preferences for myrmecochorous Euphorbiaceae in Brazilian Caatinga. Oecologia 174:493–500. https://doi.org/10.1007/s00442-013-2789-2
Legendre P, Legendre LF (2012) Numerical ecology. Elsevier, Amsterdam
MacNally R (2000) Regression and model-building in conservation biology, biogeography and ecology: the distinction between–and reconciliation of–‘predictive’and ‘explanatory’models. Biodiv Conserv 9:655–671. https://doi.org/10.1023/A:1008985925162
Magalhães VB, Espírito-Santo NB, Salles LF, Soares-Jr H, Oliveira PS (2018) Secondary seed dispersal by ants in Neotropical cerrado savanna: species-specific effects on seeds and seedlings of Siparuna guianensis (Siparunaceae). Ecol Entomol 43(5):665–674. https://doi.org/10.1111/een.12640
Majer JD (1983) Ants: bio-indicators of minesite rehabilitation, land-use, and land conservation. Environ manage 7:375–383. https://doi.org/10.1007/BF01866920
Majer JD (1985) Recolonization by ants of rehabilitated mineral sand mines on North Stradbroke Island, Queensland, with particular reference to seed removal. Austral J Ecol 10:31–48. https://doi.org/10.1111/j.1442-9993.1985.tb00861.x
Majer JD (1996) Ant recolonization of rehabilitated bauxite mines at Trombetas, Pará, Brazil. J Trop Ecol 12:257–273. https://doi.org/10.1017/S0266467400009445
Majer JD, Nichols OG (1998) Long-term recolonization patterns of ants in Western Australian rehabilitated bauxite mines with reference to their use as indicators of restoration success. J Appl Ecol 35:161–182. https://doi.org/10.1046/j.1365-2664.1998.00286.x
Majer JD, Brennan KEC, Moir ML (2007) Invertebrates in ecosystem restoration: Thirty years of research in land rehabilitation following mining. https://doi.org/10.1111/j.1526-100X.2007.00298.x
Marques TG, Espírito-Santo MM, Neves FS, Schoereder JH (2017) Ant assemblage structure in a secondary tropical dry forest: the role of ecological succession and seasonality. Sociobiology 64:261–275. https://doi.org/10.13102/sociobiology.v64i3.1276
Maunder M (1992) Plant reintroduction: an overview. Biodiv Conserv 1:51–61. https://doi.org/10.1007/BF00700250
McGeoch MA (1998) The selection, testing and application of terrestrial insects as bioindicators. Biol Rev 73:181–201. https://doi.org/10.1017/S000632319700515X
Meira RM, Peixoto AL, Coelho MA et al (2016) Brazil’s mining code under attack: giant mining companies impose unprecedented risk to biodiversity. Biodiv Conserv 25:407–409. https://doi.org/10.1007/s10531-016-1050-9
Neves FS, Braga RF, Espírito-Santo MM et al (2010) Diversity of arboreal ants in a Brazilian tropical dry forest: effects of seasonality and successional stage. Sociobiology 56:177–194
Neves FS, Queiroz-Dantas KS, Da Rocha WD, Delabie JHC (2013) Ants of three adjacent habitats of a transition region between the cerrado and caatinga biomes: the effects of heterogeneity and variation in canopy cover. Neotrop Entomol 42:258–268. https://doi.org/10.1007/s13744-013-0123-7
Nobis M (2005) SideLook 1.1-Imaging software for the analysis of vegetation structure with true-colour photographs. http://www.appleco.ch
Nooten, S, Schultheiss, P, Rowe RC, Facey SL, Cook JM (2019) Habitat complexity affects functional traits and diversity of ant assemblages in urban green spaces (Hymenoptera: Formicidae). Myrmecological News, 29: 67-77. https://doi.org/10.25849/myrmecol.news_029:067
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2015) The vegan package. Community ecology package, version 2-3-1. http://vegan.r-forge.r-project.org
Palacio EE, Fernández F (2003) Capítulo 15 Clave para las subfamilias y géneros. Introducción a las Hormigas de la Región Neotropical.
Palmer MA, Ambrose RF, Poff NL (1997) Ecological theory and community restoration ecology. Restor Ecol 5:291–300. https://doi.org/10.1046/j.1526-100X.1997.00543.x
Palmer MA, Zedler JB, Falk DA (2016) Foundations of restoration ecology. Island Press
Philpott SM, Arendt WJ, Armbrecht I et al (2008) Biodiversity loss in Latin American coffee landscapes: review of the evidence on ants, birds, and trees. Conserv Biol 22:1093–1105. https://doi.org/10.1111/j.1523-1739.2008.01029.x
Philpott SM, Perfecto I, Armbrecht I, Parr CL (2010) Ant diversity and function in disturbed and changing habitats. Ant Ecology 1:137–156. https://doi.org/10.1093/acprof:oso/9780199544639.001.0001
Prach K, Durigan G, Fennessy S, Overbeck GE, Torezan JM, Murphy SD (2019) A primer on choosing goals and indicators to evaluate ecological restoration success. Restor Ecol 27(5):917–923. https://doi.org/10.1111/rec.13011
Queiroz ACM, Ribas CR, França FM (2013) Microhabitat characteristics that regulate ant richness patterns: the importance of leaf litter for epigaeic ants. Sociobiology 60:367–373. https://doi.org/10.13102/sociobiology.v60i4.367-373
Queiroz ACM, Rabello AM, Braga DL et al (2020) Cerrado vegetation types determine how land use impacts ant biodiversity. Biodiv Conserv 29:1–18. https://doi.org/10.1007/s10531-017-1379-8
R Development Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna http://www.rproject.org
Rabello AM, Queiroz ACM, Lasmar CJ, Cuissi RG, Canedo-Júnior EO, Schmidt FA, Ribas CR (2015a) When is the best period to sample ants in tropical areas impacted by mining and in rehabilitation process? Insect Soc 62:227–236. https://doi.org/10.1007/s00040-015-0398-2
Rabello AM, Queiroz ACM, Ribas CR (2015b) Poneromorfas como indicadoras de impacto pela mineração e de reabilitação após mineração In Delabie JH, Feitosa RM, Serrão JE, Mariano CDSF, Majer JD (eds). As formigas poneromorfas do Brasil. SciELO-Editus-Editora da UESC.
Rabello AM, Parr CL, Queiroz ACM, Braga DL, Santiago GS, Ribas CR (2018) Habitat attribute similarities reduce impacts of land-use conversion on seed removal. Biotropica 50(1):39–49. https://doi.org/10.1111/btp.12506
Raimundo RL, Guimarães-Jr PR, Almeida-Neto M, Pizo MA (2004) The influence of fruit morphology and habitat structure on ant-seed interactions: a study with artificial fruits. Sociobiology 44:261–270
Reis PC, DaRocha WD, Falcão LA, Guerra TJ, Neves FS (2013) Ant fauna on Cecropia pachystachya Trécul (Urticaceae) trees in an Atlantic Forest area, southeastern Brazil. Sociobiology 60:222-228. https://doi.org/10.13102/sociobiology.v60i3.222-228
Ribas CR, Schoereder JH, Pic M, Soares SM (2003) Tree heterogeneity, resource availability, and larger scale processes regulating arboreal ant species richness. Austral Ecol 28:305–314. https://doi.org/10.1046/j.1442-9993.2003.01290.x
Ribas CR, Campos RB, Schmidt FA, Solar RR (2012a) Ants as indicators in Brazil: a review with suggestions to improve the use of ants in environmental monitoring programs. Psyche: A Journal of Entomology 2012:Article ID 636749. https://doi.org/10.1155/2012/636749
Ribas CR, Schmidt FA, Solar RR et al (2012b) Ants as indicators of the success of rehabilitation efforts in deposits of gold mining tailings. Restor Ecol 20:712–720. https://doi.org/10.1111/j.1526-100X.2011.00831.x
Salles DM, Carmo FF, Jacobi CM (2019) Habitat loss challenges the conservation of endemic plants in mining-targeted Brazilian mountains. Environ Conserv 46:140–146. https://doi.org/10.1017/S0376892918000401
Schmidt FA, Ribas CR, Schoereder JH (2013) How predictable is the response of ant assemblages to natural forest recovery? Implications for their use as bioindicators. Ecol Indic 24:158–166. https://doi.org/10.1016/j.ecolind.2012.05.031
SER (Society for Ecological Restoration) (2004) Society for ecological restoration international’s primer of ecological restoration (available from https://www.ser.org/resource/resmgr/custompages/publications/SER_Primer/ser_primer.pdf)
Torra J, Atanackovic V, Blanco-Moreno JM, Royo-Esnal A, Westerman PR (2016) Effect of patch size on seed removal by harvester ants. Weed Res 56:14–21. https://doi.org/10.1111/wre.12179
Viana-Silva FEC, Jacobi CM (2012) Myrmecofauna of ironstone outcrops: composition and diversity. Neotrop Entomol 41:263–271. https://doi.org/10.1007/s13744-012-0045-9
Walsh C, MacNally R (2013) hier. part: hierarchical partitioning reference manual. R package version 1.0-3.
Wasylycia-Leis J, Fitzpatrick P, Fonseca A (2014) Mining communities from a resilience perspective: managing disturbance and vulnerability in Itabira, Brazil. Environ Manage 53:481–495. https://doi.org/10.1007/s00267-014-0230-1
Acknowledgements
We are thankful to Vale S.A. for allowing us to sample ants in its mining and rehabilitation sites, and to R. Braga, C. Mendanha, and A. Matos for helping us at the mining sites. We thank E. Fontes, H. Vasconcelos, and two anonymous referees by the valuable comments in the manuscript. We thank “Laboratório de Química, Bioquímica e Análises de Alimentos, DEA, UFLA” for helping us with the production of artificial fruits. We are grateful to our colleagues E.A. Silva, T. Moretti, D. Braga, and F. Tanure for help during this work and to C. Bottcher, R. Campos, J. Louzada, and P. Pompeu, for the suggestions in previous versions of this paper. We also thank L. Prado and R. Feitosa (MZUSP) for verifying ant species identification.
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This work resulted from the research project FAPEMIG-CRA-RDP-00123-10—“Biodiversidade e funções ecológicas de formigas — bioindicação de impactos ambientais e de recuperação de áreas degradadas.” The authors received grants from CAPES, CNPq, and FAPEMIG.
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ACMQ, AMR, and CRR conceived and designed the research; all authors performed the field and lab work; ACMQ analyzed the data and wrote the original draft; all authors wrote and edited the manuscript. ACMQ received a postdoctoral fellowship from CEMIG - Companhia Energética de Minas Gerais S.A. (P&D 611).
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Queiroz, A.C.M., Rabello, A.M., Lasmar, C.J. et al. Diaspore Removal by Ants Does Not Reflect the Same Patterns of Ant Assemblages in Mining and Rehabilitation Areas. Neotrop Entomol 50, 335–348 (2021). https://doi.org/10.1007/s13744-021-00861-7
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DOI: https://doi.org/10.1007/s13744-021-00861-7