PHYTOPLANKTON BIOMASS INCREASES IN A SILT-IMPACTED AREA IN AN AMAZONIAN FLOOD-PLAIN LAKE OVER 15 YEARS

Autores

  • Vera Lúcia de Moraes Huszar Universidade Federal do Rio de Janeiro, Museu Nacional-UFRJ.
  • Caio Graco-Roza University of Helsinki, Department of Geosciences and Geography, FI-00014, Helsinki
  • João Carlos Nabout Universidade Estadual de Goiás, Campus Central, CEP 75132-903, Anápolis, GO
  • Patrícia Nunes Federal University of Juiz de Fora, Department of Biology, Juiz de Fora, CEP 36036-900, MG
  • Enoque G. Ribeiro Federal University of Rio de Janeiro, Institute of Biodiversity and Sustainability (NUPEM), Integrated Aquatic Ecology Laboratory, CEP 27965-045, Macaé, RJ
  • Sergio Melo Federal University of Western Pará, Institute of Water Science and Technology, CEP 68040-255, Santarém, PA
  • Simone J. Cardoso Federal University of Juiz de Fora, Department of Zoology, Juiz de Fora, CEP 36036-900, MG
  • Uanderson J. Pereira Federal University of Rio de Janeiro, Museu Nacional, Laboratory of Phycology, CEP 20940-040, Rio de Janeiro, RJ
  • Marcos Paulo Figueiredo-de-Barros Federal University of Rio de Janeiro, Institute of Biodiversity and Sustainability (NUPEM), Integrated Aquatic Ecology Laboratory, CEP 27965-045, Macaé, RJ
  • Reinaldo L Bozelli Universidade Federal do Rio de Janeiro, Departamento de Ecologia, Laboratório de Limnologia, CEP 21941-540, Rio de Janeiro, RJ
  • Fabio Roland Federal University of Juiz de Fora, Department of Biology, Juiz de Fora, CEP 36036-900, MG
  • Lucia Helena Sampaio da Silva Federal University of Rio de Janeiro, Museu Nacional, Laboratory of Phycology, CEP 20940-040, Rio de Janeiro, RJ
  • Francisco A Esteves Universidade Federal do Rio de Janeiro, Departamento de Ecologia, Laboratório de Limnologia, CEP 21941-540, Rio de Janeiro, RJ

Palavras-chave:

Clear water lake, inorganic turbidity, restoration, linear mixed-effect regressions

Resumo

Tailings from bauxite mining in Porto Trombetas (Pará state, Central Amazonia, Brazil) was discharged (1979–1989) into Batata Lake affecting about 30% of its area. The lake belongs to a clear-water flood-plain system along the Trombetas River, a tributary of the Amazon River. Siltation is the main perceived factor impacting aquatic and flooded communities. Besides natural regeneration, a program to restore a section of igapó forest in the impacted area (IA) has been conducted since 1991. Decreased light is the main factor reducing total phytoplankton biomass (PhyBM) in IA. We hypothesized that PhyBM in IA increases over time because of the improvement of the underwater light conditions due to the natural regeneration and restoration. We sampled quarterly PhyBM and limnological variables (depth, transparency, temperature, pH, conductivity, dissolved oxygen, turbidity, suspended solids, total Kjeldahl nitrogen, and total phosphorus), over 15 years (2005–2019) at eight sampling sites in the two areas (N = 349). We also obtained daily climatic and hydrologic data. PhyBM was higher in NIA than in IA. The temporal trend in the annual mean of PhyBM increased significantly over time only in the IA, approximating the NIA values, confirming our general hypothesis. The increase of PhyBM in the IA was negatively related to the residual light attenuation caused by non-phytoplankton turbidity and to total phosphorus, and positively to air temperature and site depth (p < 0.05; Marginal r2 = 0.18; Conditional r2 = 0.29). Instead, in NIA, PhyBM was explained only by the increase in air temperature (p < 0.05; Marginal r2 = 0.15; Conditional r2 = 0.34). We concluded that the PhyBM in the IA positively responds to the synergy between increasing light availability, air temperature, and site depth, and decreasing total phosphorus concentrations, regardless of hydrologic phase.

Biografia do Autor

Vera Lúcia de Moraes Huszar, Universidade Federal do Rio de Janeiro, Museu Nacional-UFRJ.

Tem doutorado em Ecologia e Recursos Naturais pela Universidade Federal de São Carlos (1994). Atualmente é Prof. Titular da Universidade Federal do Rio de Janeiro e Pesquisador 1C do CNPq. Realizou Pós-doutorado no Institute of Ecosystem Studies, NY, USA (1996-1997 e 2004). Coordena e mantém projetos em colaboração com instituições na Holanda, Uruguay, Argentina e Estados Unidos, incluindo o Programa Ciências Sem Fronteiras. É revisora de periódicos internacionais e nacionais e participa de comitês de agências de fomento. Tem experiência na área de Ecologia, com ênfase em ecologia aquática, atuando principalmente em ecologia do fitoplâncton, macroecologia, diversidade, balanço de carbono, abrangendo lagoas costeiras, lagos de inundação, estuários, reservatórios, sistemas de criação de peixes e rios. Atua no Programa de Pós-graduação em Ciências Biológicas (Botânica), tendo orientado ou co-orientado 10 estudantes de doutorado e 16 de mestrado, 12 dos quais são docentes em universidade públicas ou atuam em empresas públicas. Publicou 114 artigos em periódicos nacionais e internacionais (Fator H ISI=31; Scopus=34), 03 trabalhos completos em anais de congresso, 13 capítulos de livro e participou na organização de um livro

Referências

Alvares, C. A., Stape, J. L., Sentelhas, P. C., Gonçalves, J. M., & Sparovek, G. 2014. Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift, 22(6), 711–728. DOI: 10.1127/0941-2948/2013/0507

Anesio, A. M., Abreu, P. C., & Esteves, F. A. 1997. Influence of the hydrological cycle on the bacterioplankton of an impacted clear water Amazonian Lake. Microbial Ecology, 34(1), 66–73.

Barros, N., Farjalla, V. F., Soares, M. C., Melo, R. C., & Roland, F. 2010. Virus-bacterium coupling driven by both turbidity and hydrodynamics in an Amazonian flood-plain lake. Applied and Environmental Microbiology, 76(21), 7194–7201. DOI: 10.1128/AEM.01161-10

Bates, D., Maechler, M., Bolker, B., & Walker, S. 2015. Fitting Linear Mixed-Effects Models Using lme4. Journal of Statistical Software, 67(1), 1–48. DOI: 10.18637/jss.v067.i01

Benincà, E., Huisman, J., Heerkloss, R., Jöhnk, K. D., Branco, P., Van Nes, E. H., Scheffer, M., & Ellner, S. P. 2008. Chaos in a long-term experiment with a plankton community. Nature, 451, 822–825. DOI: 10.1038/nature06512

Bolker, B. M., Brooks, M. E., Clark, C. J., Geange, S. W., Poulsen, J. R., Stevens, M. H. H., & White, J. S. S. 2009. Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology & Evolution, 24(3), 127–135. DOI: 10.1016/j.tree.2008.10.008

Borics, G., Abonyi, A., Salmaso, N., & Ptacnik, R. 2021. Freshwater phytoplankton diversity: models, drivers, and implications for ecosystem properties. Hydrobiologia, 848, 53–75. DOI: 10.1007/s10750-020-04332-9

Bozelli, R. L. 1994. Zooplankton community density in relation to water level fluctuations and inorganic turbidity in an Amazonian lake, Lago Batata, state of Para, Brazil. Amazoniana, 13(1/2), 17–32.

Bozelli, R. L., Esteves, F. A., & Roland, F. 2000. Mitigação do impacto: passado, presente e futuro. In: R. L. Bozelli, F. A. Esteves & F. Roland (Eds.), Lago Batata: impacto e recuperação de um ecossistema amazônico. pp. 297–333. Rio de Janeiro: IB-UFRJ/SBL.

Bozelli, R. L., Caliman, A., Guariento, R. D., Carneiro, L. S., Santangelo, J. M., Figueiredo-Barros, M. P., Leal, J. J. F., Rocha, M., Quesado, L., Lopes, P. M., Farjalla, V. F., Marinho, C. C., Roland, F., & Esteves, F. A. 2009. Interactive effects of environmental variability and human impacts on the long-term dynamics of an Amazonian flood-plain lake and a South Atlantic coastal lagoon. Limnologica, 39(4), 306–313. DOI: 10.1016/j.limno.2009.06.004

Bukaveckas, P. A. 2021. Changes in acidity, DOC, and water clarity of Adirondack lakes over a 30‑year span. Aquatic Sciences, 83, 50. DOI: 10.1007/s00027-021-00807-6

Bürgi, H., & Stadelmann, P. 2002. Change of phytoplankton composition and biodiversity in Lake Sempach before and during restoration. Hydrobiologia, 469(1), 33–48. DOI: 10.1023/A:1015575527280

Callisto, M., & Esteves, F. A. 1995. Distribuição da comunidade de macroinvertebrados bentônicos em um ecossistema amazônico impactado por rejeito de bauxita–Lago Batata (Pará, Brasil). Oecologia Brasiliensis, 1(1), 335–348.

Caramaschi, E. P., Halboth, D. A., & Mannheimer, S. 2000. Ictiofauna. In: R. L. Bozelli, F. A. Esteves, & F. Roland (Eds.), Lago Batata: impacto e recuperação de um ecossistema amazônico. pp. 153–178. Rio de Janeiro: IB-UFRJ/SBL.

Cardoso, S. J., Nabout, J. C., Farjalla, V. F., Lopes, P., Bozelli, R. L., Huszar, V. L. M., & Roland, F. 2017. Environmental factors driving phytoplankton taxonomic and functional diversity in Amazonian flood-plain lakes. Hydrobiologia, 802(1), 115–130. DOI: 10.1007/s10750-017-3244-x

Carneiro, L. S., Bozelli, R. L., & Esteves, F. A. 2002. Long-term changes in the density of the copepod community in an Amazonian Lake impacted by bauxite tailings. Amazoniana, 17(3/4), 553–566.

Cole, G. A., & Weihe, P. E. 2016. Textbook of limnology. 5th ed. Long Grove, IL: Waveland Press Inc.: p. 440.

Cunha, A. P., Zeri, M., Leal, K. D., Costa, L., Cuartas, L. A., Marengo, J. A., Tomasella, J., Vieira, R. M., Barbosa, A. A., Cunningham, C., Garcia, J. V. C., Broedel, E., Alvalá, R., & Ribeiro-Neto, G. 2019. Extreme drought events over Brazil from 2011 to 2019. Atmosphere, 10, 642. DOI: 10.3390/atmos10110642

Dias, A. T. C., Bozelli, R. L., Darigo, R. M., Esteves, F. A., Santos, H. F., Figueiredo-Barros, M. P., Nunes, M. F. Q. S., Roland, F., Zamith, L. R., & Scarano, F. R. 2012. Rehabilitation of a bauxite tailing substrate in Central Amazonia: the effect of litter and seed addition on flood-prone forest restoration. Restoration Ecology, 20(4), 483–489. DOI: 10.1111/j.1526-100X.2011.00811.x

Dowd, M., Martin, J. L., LeGresley, M. M., Hanke, A., & Page, F. H. 2003. Interannual variability in a plankton time series. Environmetrics, 14, 73–86. DOI: 10.1002/env.566

Enrich-Prast, A., & Esteves F. A. 2005. Flood pulse influence and anthropic impact on the chemical composition and energy content of Oryza glumaepatula in an Amazonian Lake. Brazilian Journal of Biology, 65(3), 451–458. DOI: 10.1590/S1519-69842005000300010

Everett, J. D., Baird, M. E., Buchanan, P., Bulman, C., Davies, C., Downie, R., Griffiths, C., Heneghan, R., Kloser, R. J., Laiolo, L., Lara-Lopez, L., Lozano-Montes, H., Matear, R. J., McEnnult, F., Robson, B., Rochester, W., Skerratt, J., Smith, J. A., Strzelecki, J., & Suthers, I. M. 2017. Modelling what we sample and sampling what we model: challenges for zooplankton model assessment. Frontiers in Marine Science, 4(77), 1–19. DOI: 10.3389/fmars.2017.00077

Fonseca, J. J. L., & Esteves, F. A. 1999. Influence of bauxite tailings on the structure of the benthic macroinvertebrate community in an Amazonian Lake (Lago Batata, Pará-Brazil). Revista Brasileira de Biologia, 59(3), 397–405. DOI: 10.1590/S0034-71081999000300004

Garrido, A. V., Bozelli, L. R., Esteves, F. A., & Alves, L. S. 2003. Long-term patterns of the planktonic cladoceran community of Batata Lake, Amazonia, Brazil. Acta Limnologica Brasiliensia, 15, 41–53.

Giani, A., Taranu, Z. E., von Rückert, G., & Gregory-Eaves, I. 2020. Comparing key drivers of 525 cyanobacteria biomass in temperate and tropical systems. Harmful Algae, 97, 1–12. DOI: 10.1016/j.hal.2020.101859

Golterman, H. L., Clymo, R. S., & Ohnstad, M. A. M. 1978. Methods for physical and chemical analysis of freshwater. 2nd ed. Oxford: Blackwell Scientific Publications: p. 213.

Guenther, M., & Bozelli, R. L. 2004a. Effects of inorganic turbidity on the phytoplankton of an Amazonian Lake impacted by bauxite tailings. Hydrobiologia, 511(1), 151–159. DOI: 10.1023/B:HYDR.0000014095.47409.39

Guenther, M., & Bozelli, R. L. 2004b. Factors influencing algae–clay aggregation. Hydrobiologia, 523(1), 217–223. DOI: 10.1023/B:HYDR.0000033127.05034.32

Havens, K. E., Ji, G., Beaver, J. R., Fulton III, R. S., & Teacher, C. E. 2019. Dynamics of cyanobacteria blooms are linked to the hydrology of shallow Florida lakes and provide insight into possible impacts of climate change. Hydrobiologia, 829, 43–59. DOI: 10.1007/s10750-017-3425-7

Hillebrand, H., Dürselen, C. D., Kirschtel, D., Pollingher, U., & Zohary, T. 1999. Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology, 35(2), 403–424. DOI: 10.1046/j.1529-8817.1999.3520403.x

Huszar, V. L. M. 2000. Fitoplâncton. In: R. L. Bozelli, F. A. Esteves & F. Roland (Eds.), Lago Batata: impacto e recuperação de um ecossistema amazônico. pp. 91–104. Rio de Janeiro: IB-UFRJ/SBL.

Huszar, V. L. M., & Reynolds, C. S. 1997. Phytoplankton periodicity and sequences of dominance in an Amazonian flood-plain lake (Lago Batata, Pará, Brazil): Responses to gradual environmental change. Hydrobiologia, 346 (1/3), 169–181. DOI: 10.1023/A:1002926318409

Huszar, V. L. M., Caraco, N. F., Roland, F., & Cole, J. J. 2006. Nutrient–chlorophyll relationships in tropical–subtropical lakes: do temperate models fit? Biogeochemistry, 79, 239–250. DOI: 10.1007/s10533-006-9007-9

Jeppesen, E., Meerhoff, M., Davidson, T. A., Søndergaard, M., Lauridsen, T. L., Beklioglu, M., Brucet, S., Volta, P., González-Bergonzoni, I., Nielsen, A., & Trolle, D. 2014. Climate change impacts on lakes: an integrated ecological perspective based on a multi-faceted approach, with special focus on shallow lakes. Journal of Limnology 73: 88–111. DOI: 10.4081/jlimnol.2014.844

Josué, I. I. P., Sodré, E. O., Setúbal, R. B., Cardoso, S. J., Roland, F., Figueiredo-Barros, M. P., & Bozelli, R. L. 2021. Zooplankton functional diversity as an indicator of a long‐term aquatic restoration in an Amazonian lake. Restoration Ecology, 29(5), 1–10. DOI: 10.1111/rec.13365

Junk, W. J., Piedade, M. T. F., Schöngart, J., Cohn-Haft, M., Adeney, J. M., & Wittmann, F. 2011. A classification of major naturally-occurring Amazonian lowland wetlands. Wetlands, 31, 623–640. DOI: 10.1007/s13157-011-0190-7

Kendall, M. G. 1975. Rank correlation methods. 4th ed. London, UK: Charles Griffin: p. 272.

Kosten, S., Huszar, V. L., Bécares, E., Costa, L. S., van Donk, E., Hansson, L. A., & Scheffer, M. 2012. Warmer climates boost cyanobacterial dominance in shallow lakes. Global Change Biology, 18(1), 118–126. DOI: 10.1111/j.1365-2486.2011.02488.x

Kuznetsova, A., Brockhoff, P. B., & Christensen, R. H. B. 2017. lmerTest Package: Tests in Linear Mixed Effects Models. Journal of Statistical Software, 82(13): 1–26.

Lapa, R. P. 2000. A bauxita e o rejeito de bauxita. In: R. L. Bozelli, F. A. Esteves, & F. Roland (Eds.), Lago Batata: impacto e recuperação de um ecossistema amazônico. pp. 25–36. Rio de Janeiro: IB-UFRJ/SBL.

Lapa, R.P., & Cardoso, W. 1988. Tailings disposal at the Trombetas bauxite mine. Light Metals, 1988, 65–76.

Leal, J. J. F., Enrich-Prast, A., Esteves, A., Bozelli, R., & Farjalla, V. F. 2005. Influence of Campsurus notatus bioturbation on oxygen profile and uptake in sediments of an Amazonian lake impacted by bauxite tailings. Archiv für Hydrobiologie, 162, 557-574. DOI: 10.1127/0003-9136/2005/0162-0557

Lin, D. S. C., & Caramaschi, E. P. 2005. Responses of the fish community to the flood pulse and siltation in a floodplain lake of the Trombetas River, Brazil. Hydrobiologia, 545, 75-91. DOI: 10.1007/s10750-005-2186-x

Lund, J., Kipling, C., & LeCren, E. 1958. The inverted microscope method of estimating algal number and the statistical basis of estimation by count. Hydrobiologia, 11, 143–170.

Mackereth, F. I. F., Heron, J., & Talling, J. F. 1978. Water analysis: some revised methods for limnologists. London: Freshwater Biological Association: p. 121.

Mann, H. B. 1945. Nonparametric tests against trend. Econometrica: Journal of the Econometric Society, 1945, 245–259.

Marengo, J. A., & Espinoza, J. C. 2016. Extreme seasonal droughts and floods in Amazonia: causes, trends, and impacts. International Journal of Climatology, 36, 1033–1050. DOI: 10.1002/joc.4420

Marengo, J. A., Souza Jr, S. M., Thonicke, K., Burton, C., Halladay, K., Betts, R. A., Alves, L. M., & Soares, W. R. 2018. Changes in climate and land use over the Amazon region: current and future variability and trends. Frontiers in Earth Science, 6, 1–21. DOI: 10.3389/feart.2018.00228

Melo, S., & Huszar, V. L. M. 2000. Phytoplankton in an Amazonian flood-plain lake (Lago Batata, Brasil): diel variation and species strategies. Journal of Plankton Research, 22(1), 63–76. DOI: 10.1093/plankt/22.1.63

Nakagawa, S., & Schielzeth, H. 2013. A general and simple method for obtaining R2 from generalized linear mixed‐effects models. Methods in Ecology and Evolution, 4(2), 133–142. DOI: 10.1111/j.2041-210x.2012.00261.x

Nusch, E. A., & Palme, G. 1975. Biologische Methoden für die Praxis der Gewässeruntersuchung. Bestimmung des Chlorophyll-a und Phaeopigmentgehaltes in Oberflächenwasser. GWF-Wasser/Abwasser, 116(12), 562–565.

Padisák, J. 1998. Sudden and gradual responses of phytoplankton to global climate change: case studies from two large shallow lakes (Balaton, Hungary, and the Neusiedlersee Austria/Hungary). In: D. G. George, J. G. Jones, P. Puncochar, C. S. Reynolds, & D. W. Sutcliffe (Eds.), Management of lakes and reservoirs during global change. pp. 111–125. Dordrecht: Kluwer Academic Publishers.

Paerl, H. W., & Huisman, J. 2008. Blooms like it hot. Science, 320, 57–58. DOI: 10.1126/science.1155398

Panosso, R. F., Muehe, D., & Esteves, F. A. 1995. Morphological characteristics of an Amazon flood-plain lake (Lake Batata, Pará State, Brazil). Amazoniana, 13(3/4), 245–258.

Patakamuri, S. K., & O'Brien, N. 2021. modifiedmk: modified versions of Mann Kendall and Spearman's Rho trend tests. R package version 1.6. https://CRAN.R-project.org/package=modifiedmk

Reynolds, C. S. 2006. Ecology of phytoplankton. Cambridge, UK: Cambridge University Press: p. 535.

Reynolds, C. S., Maberly, S. C., Parker, J. E., & De-Ville, M. M. 2012. Forty years of monitoring water quality in Grasmere (English Lake District): separating the effects of enrichment by treated sewage and hydraulic flushing on phytoplankton ecology. Freshwater Biology, 57, 384–399. DOI: 10.1111/j.1365-2427.2011.02687.x

Roland, F., Esteves, F. A., & Barbosa, F. A. R. 2002. Relationship between anthropogenically caused turbidity and phytoplankton production in a clear Amazonian floodplain lake. Amazoniana: Limnologia et Oecologia Regionalis Systematis Fluminis Amazonas, 17(1/2), 65-77.

Roland, F., & Esteves, F. A. 1993. Dynamics of phosphorus, carbon and nitrogen in an Amazonian lake impacted by bauxite tailings (Batata Lake, Pará, Brazil). Internationale Vereinigung für theoretische und angewandte Limnologie: Verhandlungen, 25(2), 925–930. DOI: 10.1080/03680770.1992.11900283

Roland, F., Esteves, F. A., & Barbosa, F. A. R. 1997. The influence of bauxite tailings on the light regime and its consequence on the phytoplankton primary production in an Amazonian floodplain lake. Internationale Vereinigung für theoretische und angewandte Limnologie: Verhandlungen, 26, 765–767. DOI: 10.1080/03680770.1995.11900819

Sas, H., 1989. Lake restoration by reduction of nutrient loading: expectation, experiences, extrapolation. St. Augustin: Academia Verlag Richardz: p. 497.

Satterthwaite, F. E. 1946. An approximate distribution of estimates of variance components. Biometrics Bulletin, 2(6), 110–114.

Scarano, F. R., Bozelli, R. L., Dias, A. T. C., Assireu, A., Capossoli, D. J., Esteves, F. A., Figueiredo-Barros, M. P., Nunes, M. F. Q. S., Roland, F., Sansevero, J. B. B., Rajão, P. H. M., Reis, A., & Zamith, L. R. 2018. Twenty-five years of restoration of an Igapó Forest in Central Amazonia, Brazil. In: R. W. Myster (Ed.), Igapó (black-water flooded forests) of the Amazon basin. pp. 279–294. Switzerland: Springer Nature.

Sen, P. K. 1966. On a distribution-free method of estimating asymptotic efficiency of a class of non-parametric tests. The Annals of Mathematical Statistics, 37(6), 1759–1770. DOI: 10.1214/aoms/1177699164

Soares, B. E., Cabral, G. L., Estrella, F., & Caramaschi, E. P. 2017. Two-decade remaining effects of bauxite tailings on the fish taxonomic structure of a clear-water flood-plain lake in Central Amazon (Batata Lake, Pará State, Brazil). Oecologia Australis, 21(3), 311–322. DOI: 10.4257/oeco.2017.2103.08

Sodré, E. O., Figueiredo-Barros, M. P., Roland, F., Esteves, F. A., & Bozelli, R. L. 2017. Complimentary biodiversity measures applied to zooplankton in a recovering flood-plain lake. Fundamental and Applied Limnology, 190(4), 279–298. DOI: 10.1127/fal/2017/1064

Straile, D. 2000. Meteorological forcing of plankton dynamics in a large and deep continental European lake. Oecologia, 122(1), 44–50. DOI: 10.1007/PL00008834

USGS. 2021. Bauxite and alumina. U.S. Geological Survey, Mineral Commodity Summaries, January 2021. Prepared by E. Lee Bray

Utermöhl, H. 1958. Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Internationale Vereinigung für theoretische und angewandte Limnologie: Mitteilungen, 9, 1–38.

Wickham, H., Averick, M., Bryan, J., Chang, W., McGowan, L. D., François, R., Grolemund, G., Hayes, A., Henry, L., Hester, J., Kuhn, M., Pedersen, T. L., Miller, E., Bache, S. M., Müller, K., Ooms, J., Robinson, D., Seidel, D. P., Spinu, V., Takahashi, K., Vaughan, D., Wilke, C., Woo, K., Yutani, H., 2019. Welcome to the tidyverse. Journal of Open Source Software, 4(43), 1686. DOI: 10.21105/joss.01686

Publicado

2022-07-08