Assessment of the occurrence and abundance of an exotic zooplankton species (Kellicottia bostiniensis) across a neotropical wetland over 12 years

Limnology - Tập 24 - Trang 137-149 - 2023
Fabiana Palazzo1, Dieison André Moi1, Tatiane Mantovano1, Fábio Amodêo Lansac-Tôha1, Claudia Costa Bonecker1
1Programa de Pós-Graduação em Ecologia de Ambientes Aquáticos Continentais (PEA), Núcleo de Pesquisas em Limnologia Ictiologia e Aquicultura (Nupélia), Universidade Estadual de Maringá (UEM), Maringá, Brazil

Tóm tắt

Understanding how the occurrence and abundance of invasive species vary over time and the environmental factors that cause such variation is important for managing and controlling invasive species. To date, studies with this perspective remain scarce in the Neotropics. We used a database describing 12 years of the occurrence of an invasive rotifer (Kellicottia bostoniensis) in a large neotropical wetland (230 km2) (upper Paraná River) since 2000. We investigated how multiple local abiotic and biotic environmental variables jointly affect occurrence and abundance of an invasive zooplankton species (K. bostoniensis). The abundance and occurrence of K. bostoniensis varied significantly over time, with a marked increase after 2009. Furthermore, biotic (native zooplankton abundance, chlorophyll-a) and abiotic (turbidity, and water level) variables were important drivers of K. bostoniensis. Whereas native zooplankton and turbidity were negatively associated with the occurrence and abundance of K. bostoniensis, chlorophyll-a and water level were positively related. Furthermore, as biotic and abiotic variables naturally fluctuate to extremes, the occurrence and abundance of K. bostoniensis were reduced. Collectively, our findings underline the important role of local variables, particularly, native zooplankton and turbidity to control the abundance and occurrence of K. bostoniensis. Our results also suggest that maintaining natural extreme oscillations of the local variables can be effective in the management of invasive species.

Tài liệu tham khảo

Agostinho AA, Thomaz SM, Gomes LC (2004) Threats for biodiversity in the floodplain of the upper paraná river: effects of hydrological regulation by dams. Ecohydrol Hydrobiol 4:255–268 Amo VE, Ernandes-Silva J, Moi DA (2021) Hydrological connectivity drives the propagule pressure of Limnoperna fortunei (Dunker, 1857) in a tropical river–floodplain system. Hydrobiologia 848:2043–2053 Bajer PG, Beck MW, Hundt PJ (2018) Effect of non-native versus native invaders on macrophyte richness: are carp and bullheads ecological proxies? Hydrobiologia 817:379–391 Bastidas Navarro M, Modenutti B (2007) Effect of macrophytes and food resources on the horizontal distribution of testate amoebae and rotifers in an Andean-Patagonian lake. Rev Chil Hist Nat 80:345–362 Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48 Bayanov NG (2014) Occurrence and abundance level of Kellicotia bostoniensis (Rousselet, 1908) in Lakes of the Nizhny Novgorod region. Russ J Biol Invasions 1:83–87 Blackburn TM, Duncan RP (2001) Determinants of establishment success in introduced birds. Nature 414:195–197 Blackburn TM, Pyšrk P, Bacher S, Carlton JT, Duncan RP, Jarošik V, Wilson JRU, Richardson DM (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339 Bomfim FF, Mantovano T, Schwind LTF, Palazzo F, Bonecker CC, Lansac-Tôha FA (2016) Geographical spread of the invasive species Kellicottia longispina (Kellicott, 1879) and K. bostoniensis (Rousselet 1908): A scientometric approach. Acta Sci Biol Sci 38:29–36 Bonecker CC, Lansac-Tôha FA, Velho LFM, Rossa DC (2001) The temporal distribution pattern of copepods in Corumbá Reservoir, State of Goiás, Brazil. Hydrobiologia 453:375–384 Bonecker CC, Diniz LP, Braghin LSM, Mantovano T, da Silva JVF, Bomfim FF, Moi DA, Deosti S, Santos GNT, Candeias DA, Motta AJMM, Velho LFMV, Lansac-Tôha FA (2020) Synergistic effects of natural and anthropogenic impacts on zooplankton diversity in a subtropical floodplain: a long-term study. Oecol Aust 24:524–537 Bozelli RL, Thomaz SM, Padial AA, Lopes PM, Bini LM (2015) Floods decrease zooplankton beta diversity and environmental heterogeneity in an Amazonian floodplain system. Hydrobiologia 753:233–241 Braghin LSM, Almeida BA, Amaral DC, Canella TS, Gimenez BCG, Bonecker CC (2018) Effects of dams decrease zooplankton functional B-diversity in river-associated lakes. Fresh Biol 63:721–730 Burns CW (2013) Predictors of invasion success by Daphnia species: influence of food, temperature and species identity. Biol Invasions 15:859–869 Byrnes JEK, Gamfeldt L, Isbell F, Lefcheck JS, Griffin JN, Hector A, Cardinale BJ, Hooper DU, Dee LE, Duffy JE (2014) Investigating the relationship between biodiversity and ecosystem multifunctionality: challenges and solutions. Methods Ecol Evol 5:111–124 Byun C, Lee EJ (2017) Ecological application of biotic resistance to control the invasion of an invasive plant, Ageratina altissima. Ecol Evol 7:2181–2192 Byun C, de Blois S, Brisson J (2015) Interactions between abiotic constraint, propagule pressure, and biotic resistance regulate plant invasion. Oecologia 178:285–296 Candeias DA, Moi DA, Simões NR, Azevedo F, Meerhoff M, Bonecker CC (2022) High temperature, predation, nutrient, and food quality drive dominance of small-sized zooplankton in neotropical lakes. Aquat Sci 84:49 Conceição EDO, Higuti J, de Campos R, Martens K (2018) Effects of flood pulses on persistence and variability of pleuston communities in a tropical floodplain lake. Hydrobiologia 807:175–188 Cuthbert RN, Callaghan A, Dick JT (2019) A novel metric reveals biotic resistance potential and informs predictions of invasion success. Sci Rep 9:1–11 Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invisibility. J Ecology 88:528–534 Duncan RP, Cassey P, Pigot AL, Blackburn TM (2019) A general model for alien species richness. Biol Invasions 21:2665–2677 Elton CS (1958) The Ecology of invasions by animals and plants. methuem, London. Reprinted 2000 by The University of Chicago Press, Chicago. Ernandes-Silva J, Ragonha FH, Rodrigues LC, Mormul RP (2016) Freshwater invasibility level depends on the population age structure of the invading mussel species. Biol Invasions 18:1421–1430 Ernandes-Silva J, Moi DA, Amo VE, Silveira MJ, Zango BF, Mormul RP (2022) Factors associated with the population structure of an invasive mollusk in a neotropical floodplain. Aquat Sci 84:11 Fridley JD, Stachowicz JJ, Naeem S, Sax DF, Seabloom EW, Smith MD, Stohlgren TJ, Tilman D, Holle BV (2007) The invasion paradox: reconciling pattern and process in species invasions. Ecology 88:3–17 Gamfeldt L, Roger F (2017) Revisiting the biodiversity–ecosystem multifunctionality relationship. Nat Ecol Evol 1:0168 Giné MF, Bergamin FH, Zagatto EAG, Reis BF (1980) Simultaneous determination of nitrate and nitrite by flow injection analysis. Anal Chim Acta 114:191–197 Golterman HL, Clyno RS, Ohnstad MAM (1978) Methods for physical and chemical analysis of freshwaters, 2nd edn. Blackwell, Oxford Gomes ACAM, Macêdo RL, Gomes LF, Velho LFM, Rocha O, Vieira LDG (2022) Range expansion of Kellicottia bostoniensis (Rousselet 1908) (Rotifera) throughout a biogeographic boundary between the Brazilian savanna and the Amazon. Aquatic Sci 84:28 Goździejewska AM, Kruk M (2022) Zooplankton network conditioned by turbidity gradient in small anthropogenic reservoirs. Sci Rep 12:1–12 Grace JB, Anderson TM, Olff H, Scheiner SM (2010) On the specification of structural equation models for ecological systems. Ecol Monogr 80:67–87 Henriksson A, Wardle DA, Trygg J, Diehl S, Englund G (2016) Strong invaders are strong defenders–implications for the resistance of invaded communities. Ecol Lett 19:487–494 Julio HF Jr, Tós CD, Agostinho AA, Pavanelli CS (2009) A massive invasion of fish species after eliminating a natural barrier in the upper rio Paraná basin. Neotrop Ichthyol 7:709–718 Junk W, Bayley P, Sparks R (1989) The flood pulse concept in river-floodplain systems. Can J Fish Aquat Sci 106:110–127 Koste W (1978) Rotatoria. Die Rädertiere Mitteleuropas. Ein Bestimmungswerk, begründet von Max. Voight Überordnung Monogononta II. Tafelband, Gebüder Borntraeger, Berlin, Stuttgart 1:22–34 ((in German)) Lansac-Tôha FA, Bonecker CC, Velho LFM, Simões NR, Dias JD, Alves GM, Takahashi EM (2009) Biodiversity of zooplankton communities in the upper paraná river floodplain: interannual variation from long-term studies. Braz J Biol 69:539–549 Lázaro-Lobo A, Ervin GN (2020) Native and exotic plant species respond differently to ecosystem characteristics at both local and landscape scales. Biol Invasions 23:1–14 Leentvaar P (1961) Quelques rotateurs rares observés em Hollande. Hydrobiologia 18:245–251 Lefcheck JS (2016) piecewiseSEM: piecewise structural equation modelling in r for ecology, evolution, and systematics. Methods Ecol Evol 7:573–579 Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989 Lewis JS, Farnsworht ML, Burdett CL, Theobald DM, Gray M, Miller RS (2017) Biotic and abiotic factors predicting the global distribution and population density of an invasive large mammal. Sci Rep 7:44152 Lind OT, Doyle R, Vodopich DS, Trotter BG, Limón JG, Dcivalos-Lind L (1992) Clay turbidity: regulation of phytoplankton production in a large, nutrient-rich tropical lake. Limnol Oceanogr 3:549–565 Liu Y, Van Kleunen M (2017) Responses of common and rare aliens and natives to nutrient availability and fluctuations. J Ecol 105:1111–1122 Lowry EE, Rollinson J, Laybourn AJ, Scott TE, Aiello-Lammens ME, Gray SM, Mickley J, Gurevitch J (2013) Biological invasions: a field synopsis, systematic review, and database of the literature. Ecol Evol 37:182–196 MacDougall AS, Gilbert B, Levine LM (2009) Plant invasions and the niche. J Ecol 97:609–615 Mackereth FYH, Heron JR, Tailing JF (1978) Water analysis: some revised methods for limnologists. Amblesie: association; titus wilson e sons Ltda. Freshw Biol 36:121 Mantovano TL, Schwind TF, Braghin LSM, Arrieira RL, Tiburcio VG, Nascimento KC, Bonecker CC, Lansac-Tôha FA (2018) An analysis of publications on Daphnia lumholtzi in freshwater ecosystems. Limnetica 37:199–208 Mantovano T, Diniz LP, Conceição E, Rosa J, Bonecker CC, Bailly C, Ferreira JHD, Rangel TF, Lansac-Tôha FA (2020) Ecological niche models predict the potential distribution of the exotic rotifer Kellicottia bostoniensis (Rousselet 1908) across the globe. Hydrobiologia 848:299–309 McMahon RF (2002) Evolutionary and physiological adaptations of aquatic invasive animals: r selection versus resistance. Can J Fish Aquat Sci 59:1235–1244 Moi DA, Ernandes-Silva J, Baumgartner MT, Mormul RP (2020) The effects of river-level oscillations on the macroinvertebrate community in a river–floodplain system. Limnology 21:219–232 Moi DA, Alves DC, Figueiredo BRS, Antiqueira PAP, Teixeira de Mello F, Jeppesen E, Romero GQ, Mormul RP, Bonecker CC (2021) Non-native fishes homogenize native fish communities and reduce ecosystem multifunctionality in tropical lakes over 16 years. Sci Total Environ 769:144524 Moreira FWA, Leite MGP, Fujaco MAG, Mendonça FPC, Campos LP, Eskinazi-Sant’Anna E M, (2016) Assessing the impacts of mining activities on zooplankton functional diversity. Acta Limn Bras 28: e7. Mormul RP, Thomaz SM, Agostinho AA, Bonecker CC, Mazzeo N (2012) Migratory benthic fishes may induce regime shifts in a tropical floodplain pond. Freshwater Biol 57:1592–1602 Oliveira F, Lansac-Tôha RFM, Meira BR, Segovia BT, Cochak C, Velho LFM (2019) Effects of the exotic rotifer Kellicottia bostoniensis (Rousselet 1908) on the microbial food web components. Aquatic Ecol 53:581–594 Peng S, Kinlock NL, Gurevitch J, Peng S (2019) Correlation of native and exotic species richness: a global meta-analysis finds no invasion paradox across scales. Ecology 100:e02552 Picapedra PHS, Fernandes C, Baumgartner G, Sanches PV (2021) Zooplankton communities and their relationship with water quality in eight reservoirs from the midwestern and southeastern regions of Brazil. Braz J Biol 81:701–713 Pulzatto MM, Cunha ER, Dainez-Filho MS, Thomaz SM (2019) Association between the success of and Invasive macrophyte, environmental variables and abundance of a competing native macrophyte. Front Plant Sci 10:1–11 R Core Team (2018) R: a language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria Reid JW (1985) Chave de identificação e lista de referências bibliográficas para as espécies continentais sulamericanas de vida livre da ordem Cyclopoida (Crustacea, Copepoda). Boletim De Zoologia Universidade De São Paulo Sistema Integrado De Bibliotecas - SIBiUSP 9:17 ((in Portuguese)) Richardson DM, Pyšek P, Rejmánek M, Barbour MG, Panetta FD, West CJ (2000) Naturalization and invasion of alien plants: concepts and definitions. Divers Distrib 6:93–107 Roberto MC, Santana NF, Thomaz SM (2009) Limnology in the upper paraná river floodplain: large-scale spatial and temporal patterns, and the influence of reservoirs. Braz J Biol 69:717–725 Serafim M Jr, Bonecker CC, Rossa DC, Lansac-Tôha FA, Costa CL (2003) Rotifers of the upper paraná river floodplain: additions to the checklist. Brazi J Biol 63:207–212 Serra H, Costa MIS, Godoy W (2011) Allee effect in exotic and introduced blowflies. Neotrop Entomol 40:519–528 Shea K, Chesson P (2002) Community ecology as framework for biological invasions. Trends in Ecol Evol 17:170–176 Simberloff D, Martin JL, Genovesi P, Maris V, Wardle DA, Aronson J, Courchamp F, Galil B, García-Berthou E, Pascal M, Pyšek P (2013) Impacts of biological invasions: what’s what and the way forward. Trends in Ecol Evol 28:58–66 Simões NR, Robertson BA, Lansac-Tôha FA, Takahashi EM, Velho LMF, Joko CY (2009) Exotic species of zooplankton in the upper paraná river floodplain, Daphnia lumholtzi Sars, 1885 (Crustacea: Branchiopoda). Braz J Biol 69:551–558 Sousa WTZ, Thomaz SM, Murphy KJ, Silveira MJ, Mormul RP (2009) Environmental predictors of the occurrence of exotic Hydrilla verticillata (Lf) Royle and native Egeria najas Planch. in a sub-tropical river floodplain: the upper river paraná. Brazil Hydrobiologia 632:65–78 Stokes K, Ward K, Colloff M (2010) Alterations in flood frequency increase exotic and native species richness of understory vegetation in a temperate floodplain eucalypt forest. Plant Ecol 211:219–233 Takeda A, Fujita MDS, Komatsu EH, Pavan CB, Oliveira DP, Rosin GC, Ibarra JJA, Silva CP, Anselmo SF (2004). In: Agostinho AA, Rodrigues L, Gomes LC, Thomaz SM, Miranda LE (eds) Structure and functioning of the Paraná River and its floodplain. Maringá, EDUEM, pp 91–95 Tamburi NE, Martín PR (2011) Effects of food availability on reproductive output, offspring quality and reproductive efficiency in the apple snail Pomacea canaliculata. Biol Invasions 13:2351 Teixeira C, Tundisi JG, Kutner MB (1965) Plankton studies in a mangrove: the standing-stock and some ecological factors. Bol Inst Oceanogr 24:23–41 Thomaz SM, Pagioro TA, Bini LM, Murphy KJ (2006) Effect of reservoir drawdown on biomass of three species of aquatic macrophytes in a large sub-tropical reservoir (Itaipu, Brazil). Hydrobiologia 570:53–59 Thomaz SM, Bini LM, Bozelli RL (2007) Floods increase similarity among aquatic habitats in river-floodplain systems. Hydrobiologia 579:1–13 Thomaz SM, Mormul RP, Michelan TS (2015) Propagule pressure, invasibility of freshwater ecosystems by macrophytes and their ecological impacts: a review of tropical freshwater ecosystems. Hydrobiologia 746:39–59 Vezhnavets VV, Litvinova AG (2015) First record of the North American Rotifer Kellicottia bostoniensis (Rousselet 1908 from the Sozh River, Belarus. Rus J Biol Invasions 6:135–213 Von Holle B, Simberloff D (2005) Ecological resistance to biological invasion overwhelmed by propagule pressure. Ecology 86:3212–3218 Wood S, Scheipl F (2022) Package ‘gamm4’. Retrieved from https://cran.r-project.org/web/packages/gamm4/index.html. Accessed 17 December Zenni RD, Nuñez MA (2013) The elephant in the room: the role of failed invasions in understanding invasion biology. Oikos 122:801–815 Zhang Z, Mammola S, McLay CL, Capinha C, Yokota M (2020) To invaded or not to invaded? exploring the niche-based processes underlying the failure of a biological invasion using the invasive Chinese mitten crab. Sci Total Environ 728:138815 Zhdanova SM, Dobrynin AE (2011) Kellicotia bostoniensis (Rousselet 1908) (Rotifera: Brachionidae) in waterbodies of European Russia. Inland Water Biol 4:39–46