Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Microprotozooplankton as eutrophication bioindicator for tropical coastal lagoons

Gustavo Martins Rocha https://orcid.org/0000-0002-8191-866X A * , Jordana de Carvalho e Féres A , Gustavo Meira Kandler A , Renata Caiado Cagnin A , César Alexandro da Silva A , Sarah Karoline Rodrigues https://orcid.org/0000-0001-5838-8923 B , Bethânia Dal’Col Lehrback A , Kamila Cezar Gramlich https://orcid.org/0000-0003-1022-2929 A , Renato Rodrigues Neto A , Fabian Sá A and Luiz Fernando Loureiro Fernandes A
+ Author Affiliations
- Author Affiliations

A Universidade Federal do Espírito Santo (UFES), Vitoria, Brazil. Email: jordanacferes@gmail.com; gustavomkandler@hotmail.com; renatacaiado@hotmail.com; cesaralexandro@gmail.com; bethania.dalcol@gmail.com; kcgramlich@gmail.com; rrneto@gmail.com; fabian.sa@ufes.br; luiz.ufes@gmail.com

B Universidade Federal Fluminense (UFF), Niteroi, Brazil. Email: sarah.skr@gmail.com

* Correspondence to: gusmrocha@uol.com.br

Handling Editor: Fiona Dyer

Marine and Freshwater Research 75, MF23122 https://doi.org/10.1071/MF23122
Submitted: 5 January 2023  Accepted: 17 May 2024  Published: 4 July 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context and aims

A reliable bioindicator index of eutrophication is still lacking for monitoring zooplankton in saline, coastal lagoons. We aimed to establish plankton bioindicators of eutrophication that are not affected by salinity variation, which is essential for environmental monitoring of coastal lagoons.

Methods

Sampling was conducted for microprotozooplankton, chlorophyll-a, nutrients and sterols in eight tropical coastal lagoons with different saline and nutrient concentrations. A testate amoeba and rotifer bioindication index of eutrophication (T&R index) was proposed after establishing a list of indicator species on the basis of five statistical criteria and one bibliographic criterion.

Key results

Selected species, based on the six criteria, were Arcella hemisphaerica, Brachionus plicatilis, Galeripora (Arcella) discoides, Netzelia corona, Lecane closterocerca, Lepadela patella and Testudinela patina. Biodiversity measures, traditionally used in biomonitoring, varied negatively with salinity (r = −0.60 for Margalef richness and −0.59 for Shannon diversity) and were not correlated with nutrient concentrations. Conversely, the T&R index showed no correlation with salinity (r = 0.002) and was positively correlated with the trophic-state index (TSI) (r = 0.62).

Conclusions and implications

Our results showed that specific patterns of indicator microprotozooplankton species can effectively diagnose organic pollution in coastal lagoons and their use is a more suitable approach than is the use of community indicators such as richness, evenness and diversity, traditionally used for that task.

Keywords: anthropic pressure, IndVal, optimal value, rotifer, salinity, sewage, sterols, testate amoeba.

References

Al-Ghanim KA (2012) Spatio-temporal distribution and composition of zooplankton in Wadi Hanifah stream Riyadh (Saudi Arabia) and Abu Zabaal lakes (Egypt). Pakistan Journal of Zoology 44, 727-736.
| Google Scholar |

Almeida R, Formigo NE, Sousa-Pinto I, Antunes SC (2020) Contribution of zooplankton as a biological element in the assessment of reservoir water quality. Limnetica 39, 245-261.
| Crossref | Google Scholar |

Arima K, Nagasawa M, Bae M, Tamura G (1969) Microbial transformation of sterols. Part I. Decomposition of cholesterol by microorganisms. Agricultural and Biological Chemistry 33(11), 1636-1643.
| Crossref | Google Scholar |

Arndt H (1988) Dynamics and production of a natural population of Brachionus plicatilis (Rotatoria, Monogononta) in a eutrophicated inner coastal water of the Baltic. Kieler Meeresforsch Sonderh 6, 147-153.
| Google Scholar |

Arndt H (1993) A critical review of the importance of rhizopods (naked and testate amoebae) and actinopods (Heliozoa) in lake plankton. Marine Microbial Food Webs 7, 3-29.
| Google Scholar |

Arruda GA, Diniz LP, Almeida VLS, Neumann-Leitão S, de Melo Júnior M (2017) Rotifer community structure in fish-farming systems associated with a Neotropical semiarid reservoir in north-eastern Brazil. Aquaculture Research 48, 4910-4922.
| Crossref | Google Scholar |

Barnett A, Beisner BE (2007) Zooplankton biodiversity and lake trophic state: explanations invoking resource abundance and distribution. Ecology 88, 1675-1686.
| Crossref | Google Scholar | PubMed |

Bhagowati B, Talukdar B, Ahamad KU (2020) Lake eutrophication: causes, concerns and remedial measures. In ‘Emerging issues in the water environment during Anthropocene’. (Eds M Kumar, D Snow, R Honda) pp. 211–222. (Springer: Singapore)

Bhandarkar SV (2015) Species diversity of rotifers in lentic ecosystem of Dhukeshwari Temple Pond Deori with reference to cultural eutrophication. International Journal of Current Microbiology and Applied Sciences 4, 736-743.
| Google Scholar |

Bilal A, Uzbilek M (2020) Zooplankton of Sakaryabaşi-west pond, central Anatolia. Communications Faculty of Sciences University of Ankara – C. Biology 29, 365-378.
| Google Scholar |

Blyakharchuk T, Kurina I (2021) Late Holocene environmental and climatic changes in the Western Sayan Mountains based on high-resolution multi-proxy data. Boreas 50, 919-934.
| Crossref | Google Scholar |

Bobrov AA, Siegert C, Andreev AA, Schirrmeister L (2003) Testaceans (Protozoa: Testacea) in quaternary permafrost sediments of Bykovsky Peninsula, arctic Yakutia. Biology Bulletin of the Russian Academy of Sciences 30, 191-206.
| Crossref | Google Scholar |

Bockwoldt KA, Nodine ER, Mihuc TB, Shambaugh AD, Stockwell JD (2017) Reduced phytoplankton and zooplankton diversity associated with increased cyanobacteria in lake Champlain, USA. Journal of Contemporary Water Research & Education 160, 100-118.
| Crossref | Google Scholar |

Bozkurt A, Akin Ş (2012) Zooplankton fauna of Yeşilırmak (between Tokat and Blacksea), Hasan Uğurlu and Suat Uğurlu Dam Lakes. Turkish Journal of Fisheries and Aquatic Sciences 12, 777-786.
| Crossref | Google Scholar |

Brandorff G-O, Pinto-Silva V, Morini AAET (2011) Zooplankton: species diversity, abundance and community development. In ‘The Pantanal: ecology, biodiversity and sustainable management of a large Neotropical seasonal wetland’. pp. 355–391. (Pensoft Publishers)

Brito TT, Oliveira-Júnior JF, Lyra GB, Gois G, Zeri M (2017) Multivariate analysis applied to monthly rainfall over Rio de Janeiro state, Brazil. Meteorology and Atmospheric Physics 129, 469-478.
| Crossref | Google Scholar |

Camara EM, Caramaschi ÉP, Di Dario F, Petry AC (2018) Short-term changes in two tropical coastal lagoons: effects of sandbar openings on fish assemblages. Journal of Coastal Research 34, 90-105.
| Crossref | Google Scholar |

Castellanos Romero K, Pizarro Del Río J, Cuentas Villarreal K, Costa Anillo JC, Pino Zarate Z, Gutierrez LC, Franco OL, Arboleda Valencia JW (2017) Lentic water quality characterization using macroinvertebrates as bioindicators: an adapted BMWP index. Ecological Indicators 72, 53-66.
| Crossref | Google Scholar |

Chan K-H, Lam MHW, Poon K-F, Yeung H-Y, Chiu TKT (1998) Application of sedimentary fecal stanols and sterols in tracing sewage pollution in coastal waters. Water Research 32, 225-235.
| Crossref | Google Scholar |

Chatterjee K, Gopal B (1998) Experimental study of emergence of zooplankton in temporary water-bodies in relation to dry periods. Internationale Vereinigung für Theoretische und Angewandte Limnologie: Verhandlungen 26, 1309-1315.
| Crossref | Google Scholar |

Conde-Porcuna JM, Ramos-Rodríguez E, Pérez-Martínez C (2002) Correlations between nutrient concentrations and zooplankton populations in a mesotrophic reservoir. Freshwater Biology 47, 1463-1473.
| Crossref | Google Scholar |

Costa BNS, Pinheiro SCC, Amado LL, de Oliveira Lima M (2016) Microzooplankton as a bioindicator of environmental degradation in the Amazon. Ecological Indicators 61, 526-545.
| Crossref | Google Scholar |

Coûteaux M-M (1992) Decomposition of cells and empty shells of testate amoebae (Rhizopoda, Testacea) in an organic acid soil sterilized by propylene oxide fumigation, autoclaving, and γ-ray irradiation. Biology and Fertility of Soils 12, 290-294.
| Crossref | Google Scholar |

da Silva LJG, Silva MB, Fraga RE, Anjos MS, Rocha CVS, Santos SP, Rocha MA (2020) Amebas testáceas (Arcellinida e Euglyphida) em dois biótopos de um corpo aquático temporário contaminado por dejetos orgânicos: novas ocorrências para o estado da Bahia. Scientia Plena 16, 1-19 [In Portuguese].
| Crossref | Google Scholar |

Datta T (2011) Zooplankton diversity and physicochemical conditions of two wetlands of Jalpaiguri district, India. International Journal of Applied Biology and Pharmaceutical Technology 2, 576-583.
| Google Scholar |

De Aguiar MM, Da Silva SR, Mendonça ASF (1997) Eficiência na remoção de coliformes fecais em lagoas de estabilização na grande Vitória-ES. In ‘Anais do 19° Congresso Brasileiro de Engenharia Sanitária e Ambiental’, 14–19 September 1997, Foz do Iguaçu, Brazil. pp. 991–999. (ABES, Associação Brasileira de Engenharia Sanitária e Ambiental) [In Portuguese]

de Almeida SZ, de Oliveira Fernandes V (2013) Effects of intensive fish-farming and domestic wastewater on the periphytic algal community in a tropical coastal lagoon (Juara, Brazil). Acta Scientiarum. Biological Sciences 35, 335-342.
| Crossref | Google Scholar |

de Cardoso LS, Marques DdM (2004) Structure of the zooplankton community in a subtropical shallow lake (Itapeva Lake – south of Brazil) and its relationship to hydrodynamic aspects. Hydrobiologia 518, 123-134.
| Crossref | Google Scholar |

De-Carli BP, Bressane A, Longo RM, Manzi-Decarli A, Moschini-Carlos V, Pompêo MLM (2019) Development of a zooplankton biotic index for trophic state prediction in tropical reservoirs. Limnetica 38, 303-316.
| Crossref | Google Scholar |

Dereczynski CP, dos Reis Lopes Í, de Carvalho NO, da Silva MGAJ, Grossmann KS, Martins RP (2019) Climatology of Espírito Santo and the northern Campos Basin, offshore southeast Brazil. Anuário do Instituto de Geociências 42, 386-401 [In English with abstract in Portuguese and English].
| Crossref | Google Scholar |

Devetter M, Sed’a J (2003) Rotifer fecundity in relation to components of microbial food web in a eutrophic reservoir. Hydrobiologia 504, 167-175.
| Crossref | Google Scholar |

Dias JD, Simões NR, Bonecker CC (2012) Zooplankton community resilience and aquatic environmental stability on aquaculture practices: a study using net cages. Brazilian Journal of Biology 72, 1-11.
| Crossref | Google Scholar |

Dufrêne M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Monographs 67, 345-366.
| Crossref | Google Scholar |

Duggan IC, Green JD, Thomasson K (2001) Do rotifers have potential as bioindicators of lake trophic state? Internationale Vereinigung für theoretische und angewandte Limnologie: Verhandlungen 27, 3497-3502.
| Crossref | Google Scholar |

Dumont HJ (1995) ‘Guides to the Identification of the Microinvertebrates of the Continental Waters of the World. Vol. 2. The Lecanidae (Monogononta).’ (SPB Academic Publishing Bv)

Edmondson WT (1959) ‘Fresh-water biology’, 2nd edn. (Wiley)

Ejsmont-Karabin J (2012) The usefulness of zooplankton as lake ecosystem indicators: rotifer trophic state index. Polish Journal of Ecology 60, 339-350.
| Google Scholar |

Ejsmont-Karabin J, Kuczyńska-Kippen N (2001) Urban rotifers: structure and densities of rotifer communities in water bodies of the Poznań agglomeration area (western Poland). In ‘Rotifera IX’. (Eds L Sanoamuang, H Segers, RJ Shiel, RD Gulati) pp. 165–171. (Springer: Dordrecht, Netherlands)

Ellison RL (1995) Paleolimnological analysis of Ullswater using testate amoebae. Journal of Paleolimnology 13, 51-63.
| Crossref | Google Scholar |

Elmoor-Loureiro LMA (1997) ‘Manual de Identificação de Cladoceros Límnicos do Brasil.’ (Universitária: Brasília, Brazil) [In Portuguese]

Fazelipour M, Takdastan A, Borghei SM (2021) Biological removal of nutrients (N & P) from urban wastewater with a modified integrated fixed-film activated sludge-oxic settling anoxic system using an anoxic sludge holding tank. Water and Environment Journal 35, 830-846.
| Crossref | Google Scholar |

Ferdous Z, Muktadir AKM (2009) A review: potentiality of zooplankton as bioindicator. American Journal of Applied Sciences 6, 1815-1819.
| Crossref | Google Scholar |

Frau D, Battauz Y, Alvarenga PF, Scarabotti PA, Mayora G, Sinistro R (2019) Assessing the relevance of top-down and bottom-up effects as phytoplankton structure drivers in a subtropical hypereutrophic shallow lake. Aquatic Ecology 53, 265-280.
| Crossref | Google Scholar |

Freitas YGC, Ramos BRD, Silva YG, Sampaio GS, Nascimento LS, Castelo Branco CW, Miranda VBS (2022) Testate amoebae: a review on their multiple uses as bioindicators. Acta Protozoologica 61, 1-21.
| Crossref | Google Scholar |

Frisch D, Green AJ, Figuerola J (2007) High dispersal capacity of a broad spectrum of aquatic invertebrates via waterbirds. Aquatic Sciences 69, 568-574.
| Crossref | Google Scholar |

Gazonato Neto AJ, Silva LCd, Saggio AA, Rocha O (2014) Zooplankton communities as eutrophication bioindicators in tropical reservoirs. Biota Neotropica 14, e20140018.
| Crossref | Google Scholar |

Ger KA, Urrutia-Cordero P, Frost PC, Hansson L-A, Sarnelle O, Wilson AE, Lürling M (2016) The interaction between cyanobacteria and zooplankton in a more eutrophic world. Harmful Algae 54, 128-144.
| Crossref | Google Scholar | PubMed |

Gilbert JJ (2003a) Environmental and endogenous control of sexuality in a rotifer life cycle: developmental and population biology. Evolution & Development 5, 19-24.
| Crossref | Google Scholar | PubMed |

Gilbert JJ (2003b) Specificity of crowding response that induces sexuality in the rotifer Brachionus. Limnology and Oceanography 48, 1297-1303.
| Crossref | Google Scholar |

Gilbert JJ (2018) Morphological variation and its significance in a polymorphic rotifer: environmental, endogenous, and genetic controls. BioScience 68, 169-181.
| Crossref | Google Scholar |

Gilbert JJ (2020) Variation in the life cycle of monogonont rotifers: commitment to sex and emergence from diapause. Freshwater Biology 65, 786-810.
| Crossref | Google Scholar |

Gilbert JJ (2022) Food niches of planktonic rotifers: diversification and implications. Limnology and Oceanography 67, 2218-2251.
| Crossref | Google Scholar |

Gomes MB (2008) ‘Guia das tecamebas: bacia do rio Peruaçu, Minas Gerais: subsídio para conservação e monitoramento da bacia do Rio São Francisco.’ (Editora UFMG) [In Portuguese]

Gomes EAT, Godinho MJL (2003) Structure of the protozooplankton community in a tropical shallow and eutrophic lake in Brazil. Acta Oecologica 24, S153-S161.
| Crossref | Google Scholar |

Grasshoff K, Kremling K, Ehrhardt M (1999) Determination of nutrients. In ‘Methods of seawater analysis.’ pp. 159–228. (Wiley-VCH: Weinheim, Germany)

Havel JE, Shurin JB (2004) Mechanisms, effects, and scales of dispersal in freshwater zooplankton. Limnology and Oceanography 49, 1229-1238.
| Crossref | Google Scholar |

Hennemann MC, Petrucio MM (2011) Spatial and temporal dynamic of trophic relevant parameters in a subtropical coastal lagoon in Brazil. Environmental Monitoring and Assessment 181, 347-361.
| Crossref | Google Scholar | PubMed |

Holt EA, Miller SW (2011) Bioindicators: using organisms to measure. Nature 3, 8-13.
| Google Scholar |

Imoobe TOT, Adeyinka ML (2009) Zooplankton-based assessment of the trophic state of a tropical forest river in Nigeria. Archives of Biological Sciences 61, 733-740.
| Crossref | Google Scholar |

Ismail AH, Adnan AAM (2016) Zooplankton composition and abundance as indicators of eutrophication in two small man-made lakes. Tropical Life Sciences Research 27, 31-38.
| Crossref | Google Scholar | PubMed |

Karabin A (1986) Pelagic zooplankton (Rotatoria+ Crustacea) variation in the process of lake eutrophication. I: structural and quantitative features. Ekologia Polska 33, 567-616.
| Google Scholar |

Kaya M, Fontaneto D, Segers H, Altindağ A (2010) Temperature and salinity as interacting drivers of species richness of planktonic rotifers in Turkish continental waters. Journal of Limnology 69, 297-304.
| Crossref | Google Scholar |

Keeler AG, McLemore D (1996) The value of incorporating bioindicators in economic approaches to water pollution control. Ecological Economics 19, 237-245.
| Crossref | Google Scholar |

Koste W (1978) ‘Rotatoria Die Rodertiere Mitteleuropas begründet von Max Voigt – Monogononta. 2. Auflage neubearbeitet von Walter Koste.’ (Gebrüder Borntraeger) [In German]

Kostopoulou V, Carmona MJ, Divanach P (2012) The rotifer Brachionus plicatilis: an emerging bio-tool for numerous applications. Journal of Biological Research 17, 97-112.
| Google Scholar |

Kuhlmann ML, Johnscher-Fornasaro G, Ogura LL, Imbimbo HRV (2012) ‘Protocolo para o biomonitoramento com as comunidades bentônicas de rios e reservatórios do estado de São Paulo.’ (CETESB: São Paulo, Brazil)

Kumar P, Wanganeo A, Wanganeo R, Sonaullah F (2011) Seasonal variations in zooplankton diversity of railway pond, Sasaram, Bihar. International Journal of Environmental Sciences 2, 1007-1016.
| Google Scholar |

Lamentowicz M, Mitchell EAD (2005) The ecology of testate amoebae (Protists) in Sphagnum in north-western Poland in relation to peatland ecology. Microbial Ecology 50, 48-63.
| Crossref | Google Scholar | PubMed |

Lamentowicz M, Tobolski K, Mitchell EAD (2007) Palaeoecological evidence for anthropogenic acidification of a kettle-hole peatland in northern Poland. The Holocene 17, 1185-1196.
| Crossref | Google Scholar |

Lamparelli MC (2004) Graus de trofia em corpos d\’água do estado de São Paulo: avaliação dos métodos de monitoramento. PhD thesis, Universidade de São Paulo, São Paulo, Brazil. [In Portuguese]

Lampert W, Sommer U (2007) ‘Limnoecology: the ecology of lakes and streams.’ (Oxford University Press: New York, NY, USA)

Lippert MAM, Lansac-Tôha FM, Meira BR, Velho LFM, Lansac-Toha FA (2020) Structure and dynamics of the protoplankton community in an environmentally protected urban stream. Brazilian Journal of Biology 80, 844-859.
| Crossref | Google Scholar |

Lobo EA, Heinrich CG, Schuch M, Düpont A, da Costa AB, Wetzel CE, Ector L (2016) Índice trófico de qualidade da água: guia ilustrado para sistemas lóticos subtropicais e temperados brasileiros. (Ed. C Agnes, JCS de Mello) (Universidade de Santa Cruz do Sul: Santa Cruz do Sul, Brazil) Available at https://repositorio.unisc.br/jspui/bitstream/11624/1767/1/%C3%8Dndice%20tr%C3%B3fico%20de%20qualidade%20da%20%C3%A1gua.pdf [In Portuguese]

Matsumura-Tundisi T, Rocha O (1983) Occurrence of copepod (Calanoida Cyclopoida and Harpacticoida) from ‘Broa’ reservoir (São Carlos, São Paulo, Brazil). Revista Brasileira de Biologia 43, 1-17.
| Google Scholar |

Medeiros AMA, Sousa CE, Crispim MC, Montenegro AKA (2013) Effects of experimental eutrophization on zooplankton community. Acta Limnologica Brasiliensia 25, 183-191.
| Crossref | Google Scholar |

Mieczan T, Tarkowska-Kukuryk M (2017) Microbial communities as environmental indicators of ecological disturbance in restored carbonate fen – results of 10 years of studies. Microbial Ecology 74, 384-401.
| Crossref | Google Scholar | PubMed |

Mola HR (2011) Seasonal and spatial distribution of Brachionus (Pallas, 1966; Eurotatoria: Monogonanta: Brachionidae), a bioindicator of eutrophication in lake El-Manzalah, Egypt. Biology and Medicine 3, 60-69.
| Google Scholar |

Montagud D, Soria JM, Soria-Perpiñà X, Alfonso T, Vicente E (2019) A comparative study of four indexes based on zooplankton as trophic state indicators in reservoirs. Limnetica 38, 291-302.
| Crossref | Google Scholar |

Nagasawa M, Bae M, Tamura G, Arima K (1969) Microbial transformation of sterols. Part II. Cleavage of sterol side chains by microorganisms. Agricultural and Biological Chemistry 33(11), 1644-1650.
| Google Scholar |

Needham JG, Needham PR (1982) ‘Guía para el estudio de Los Seres Vivos de Las Aguas Dulces.’ (Reverté: Barcelona, Spain) [In Spanish]

Ogden CG, Couteaux M-M (1988) The effect of predation on the morphology of Tracheleuglypha dentata (Protozoa: Rhizopoda). Archiv für Protistenkunde 136, 107-115.
| Crossref | Google Scholar |

Ortega-Mayagoitia E, Armengol X, Rojo C (2000) Structure and dynamics of zooplankton in a semi-arid wetland, the National Park Las Tablas de Daimiel (Spain). Wetlands 20, 629-638.
| Crossref | Google Scholar |

Ovaskainen O, Weigel B, Potyutko O, Buyvolov Y (2019) Long-term shifts in water quality show scale-dependent bioindicator responses across Russia – insights from 40 year-long bioindicator monitoring program. Ecological Indicators 98, 476-482.
| Crossref | Google Scholar |

Pal S, Patra AK, Chakraborty K (2015) Prospect of Brachionus calyciflorus, a holoplankton, for its potential bio-indicator property: a review. International Journal of Recent Scientific Research 6, 7603-7608.
| Google Scholar |

Pappas JL, Stoermer EF (1996) Quantitative method for determining a representative algal sample count1. Journal of Phycology 32, 693-696.
| Crossref | Google Scholar |

Parmar TK, Rawtani D, Agrawal YK (2016) Bioindicators: the natural indicator of environmental pollution. Frontiers in Life Science 9, 110-118.
| Crossref | Google Scholar |

Patra A, Santra KB, Manna CK (2011) Ecology and diversity of zooplankton in relation to physico-chemical characteristics of water of Santragachi Jheel, West Bengal, India. Journal of Wetlands Ecology 5, 20-39.
| Crossref | Google Scholar |

Pennak RW (1953) ‘Fresh-water invertebrates of the United States.’ (Ronald Press Co.: New York, NY, USA)

Porter KG (1996) Integrating the microbial loop and the classic food chain into a realistic planktonic food web. In ‘Food webs: integration of patterns & dynamics’. (Eds GA Polis, KO Winemiller) pp. 51–59. (Springer: Boston, MA, USA)

Ramos VR, de Rezende Araújo TM, de Oliveira MM (2019) Histórico e caracterização das lagoas do Açu, Salgada, Grussaí e Iquipari, São João da Barra/RJ. Boletim do Observatório Ambiental Alberto Ribeiro Lamego 13, 3-23 [In Portuguese].
| Crossref | Google Scholar |

Redjeki S (1999) Budidaya rotifera (Brachionus plicatilis). Oseana 24, 27-33.
| Google Scholar |

Resh VH (2008) Which group is best? Attributes of different biological assemblages used in freshwater biomonitoring programs. Environmental Monitoring and Assessment 138, 131-138.
| Crossref | Google Scholar | PubMed |

Rocha O, Tundisi TM (1976) ‘Copepoda: Atlas do Zooplâncton (Represa do Broa, São Carlos).’ (UFSCar I: São Carlos, Brazil) [In Portuguese]

Santangelo JM, Rocha AM, Bozelli RL, Carneiro LS, Esteves FA (2007) Zooplankton responses to sandbar opening in a tropical eutrophic coastal lagoon. Estuarine, Coastal and Shelf Science 71, 657-668.
| Crossref | Google Scholar |

Schallenberg M, Hall CJ, Burns CW (2003) Consequences of climate-induced salinity increases on zooplankton abundance and diversity in coastal lakes. Marine Ecology Progress Series 251, 181-189.
| Crossref | Google Scholar |

Sendacz S, Kubo E (1982) Copepoda (Calanoida e Cyclopoida) de Reservatórios do Estado de São Paulo. Boletim do Instituto de Pesca 9, 51-89 [In Portuguese].
| Google Scholar |

Sigala Regalado I, Lozano García S, Pérez Alvarado L, Caballero M, Lugo Vázquez A (2018) Ecological drivers of testate amoeba diversity in tropical water bodies of central Mexico. Journal of Limnology 77, 385-399.
| Crossref | Google Scholar |

Silva CE (2012) Foraminíferos, Tecamebas e Bactérias Bentônicos na Praia de Encantadas (Ilha do Mél, Paraná, Brasil) e a possível influência do afluxo turístico sobre esses organismos. PhD thesis, Universidade Federal do Paraná, Curitiba, Brazil. [In Portuguese]

Silva AMA, Barbosa JEL, Medeiros PR, Rocha RM, Lucena-Filho MA, Silva DF (2009) Zooplankton (Cladocera and Rotifera) variations along a horizontal salinity gradient and during two seasons (dry and rainy) in a tropical inverse estuary (northeast Brazil). Pan-American Journal of Aquatic Sciences 4, 226-237.
| Google Scholar |

Sousa WP, Carvalho CEV, Carvalho CCV, Suzuki MS (2004) Mercury and organic carbon distribution in six lakes from the north of Rio de Janeiro State. Brazilian Archives of Biology and Technology 47, 139-145.
| Crossref | Google Scholar |

Starkweather PL, Gilbert JJ, Frost TM (1979) Bacterial feeding by the rotifer Brachionus calyciflorus: clearance and ingestion rates, behavior and population dynamics. Oecologia 44, 26-30.
| Crossref | Google Scholar | PubMed |

Sterza JM, Fernandes LL (2006) Zooplankton community of the Vitória Bay estuarine system (southeastern Brazil): characterization during a three-year study. Brazilian Journal of Oceanography 54, 95-105.
| Crossref | Google Scholar |

Straznickas B, Jaeckle W (2016) Phage for thought: investigating the ingestion and assimilation of viruses into rotifer (Brachionus plicatilis) tissues. In ‘27th Annual John Wesley Powell IWU Student Research Conference’, 16 April 2016, Bloomington, IL, USA. Poster Presentation P34. (Digital Commons, Illinois Wesleyan University) Available at https://digitalcommons.iwu.edu/cgi/viewcontent.cgi?article=3357&context=jwprc

Suzuki MS, Ovalle ARC, Pereira EA (1998) Effects of sand bar openings on some limnological variables in a hypertrophic tropical coastal lagoon of Brazil. Hydrobiologia 368, 111-122.
| Crossref | Google Scholar |

Suzuki MS, Figueiredo RO, Castro SC, Silva CF, Pereira EA, Silva JA, Aragon GT (2002) Sand bar opening in a coastal lagoon (Iquipari) in the northern region of Rio de Janeiro State: hydrological and hydrochemical changes. Brazilian Journal of Biology 62, 51-62.
| Crossref | Google Scholar |

Szelecz I, Fournier B, Seppey C, Amendt J, Mitchell E (2014) Can soil testate amoebae be used for estimating the time since death? A field experiment in a deciduous forest. Forensic Science International 236, 90-98.
| Crossref | Google Scholar | PubMed |

Sá AKDdS, Cutrim MVJ, Costa DS, Cavalcanti LF, Ferreira FS, Oliveira ALL, Serejo JHF (2021) Algal blooms and trophic state in a tropical estuary blocked by a dam (northeastern Brazil). Ocean and Coastal Research 69, 1-16.
| Crossref | Google Scholar |

Tasevska O, Jersabek CD, Kostoski G, Gušeska D (2012) Differences in rotifer communities in two freshwater bodies of different trophic degree (Lake Ohrid and Lake Dojran, Macedonia). Biologia 67, 565-572.
| Crossref | Google Scholar |

Thorp JH, Covich AP (1991) (Eds) ‘Ecology and classification of North American freshwater invertebrates.’ (Academic Press, Inc.: San Diego, CA, USA)

Tolonen K, Warner BG, Vasander H (1992) Ecology of testaceans (Protozoa: Rhizopoda) in mires in southern Finland: I. Autecology. Archiv für Protistenkunde 142, 119-138.
| Crossref | Google Scholar |

Tsyganov AN, Aerts R, Nijs I, Cornelissen JHC, Beyens L (2012) Sphagnum-dwelling testate amoebae in subarctic bogs are more sensitive to soil warming in the growing season than in winter: the results of eight-year field climate manipulations. Protist 163, 400-414.
| Crossref | Google Scholar | PubMed |

US Environmental Protection Agency (1996) Method 3510C: separatory funnel liquid–liquid extraction. Test methods for evaluating solid waste, physical/chemical methods, 1–8 December. US EPA.

US Environmental Protection Agency (2007) Method 8270d: semivolatile organic compounds by gas chromatography/mass spectrometry (GC/MS). US EPA.

Ustaoğlu MR, Balik S, Mis DÖ (2004) The rotifer fauna of Lake Sazlıgöl (Menemen–İzmir). Turkish Journal of Zoology 28, 267-272.
| Google Scholar |

Valderrama JC (1981) The simultaneous analysis of total nitrogen and total phosphorus in natural waters. Marine Chemistry 10, 109-122.
| Crossref | Google Scholar |

Van Hengstum PJ, Reinhardt EG, Beddows PA, Huang RJ, Gabriel JJ (2008) Thecamoebians (testate amoebae) and foraminifera from three anchialine cenotes in Mexico: low salinity (1.5–4.5 PSU) faunal transitions. The Journal of Foraminiferal Research 38, 305-317.
| Crossref | Google Scholar |

Wagaw S, Mengistou S, Getahun A (2023) Zooplankton community structure in relation to environmental variables in a tropical endorheic Soda Lake Shala, Ethiopia. Journal of Freshwater Ecology 38, 2188882.
| Crossref | Google Scholar |

Wejnerowski Ł, Aykut TO, Pełechata A, Rybak M, Dulić T, Meriluoto J, Dziuba MK (2022) Plankton hitch-hikers on naturalists’ instruments as silent intruders of aquatic ecosystems: current risks and possible prevention. NeoBiota 73, 193-219.
| Crossref | Google Scholar |

Yang L-J, Tao Y, Jiang X, Wang Y, Li Y-H, Zhou L, Wang P-Z, Li Y-Y, Zhao X, Wang H-J, Jeppesen E, Xie P (2023) Interactive effects of nutrients and salinity on zooplankton in subtropical plateau lakes with contrasting water depth. Frontiers in Environmental Science 11, 260.
| Crossref | Google Scholar |

Zadereev E, Drobotov A, Anishchenko O, Kolmakova A, Lopatina T, Oskina N, Tolomeev A (2022) The structuring effects of salinity and nutrient status on zooplankton communities and trophic structure in Siberian lakes. Water 14, 1468.
| Crossref | Google Scholar |

Zakaria HY, Hussien Ahmed M, Flower R (2007) Environmental assessment of spatial distribution of zooplankton community in Lake Manzalah, Egypt. Acta Adriatica: International Journal of Marine Sciences 48, 161-172.
| Google Scholar |

Zhang Y, Feng S, Gao F, Wen H, Zhu L, Li M, Xi Y, Xiang X (2022) The relationship between Brachionus calyciflorus-associated bacterial and bacterioplankton communities in a subtropical freshwater lake. Animals 12, 3201.
| Crossref | Google Scholar |

Zholtkevych GN, Bespalov GY, Nosov KV, Abhishek M (2013) Discrete modeling of dynamics of zooplankton community at the different stages of an antropogeneous eutrophication. Acta Biotheoretica 61, 449-465.
| Crossref | Google Scholar | PubMed |