Acta Limnologica Brasiliensia
Acta Limnologica Brasiliensia
Original Article

Zooplankton functional complementarity between temporary and permanent environments

Complementariedade funcional zooplanctônica entre ambientes aquáticos temporários e permanentes

Rayanne Barros Setubal; Reinaldo Luiz Bozelli

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Abstract:: Aims: This study aims to evaluate the functional complementarity of the zooplankton community between temporary ponds and permanent lagoons. We hypothesize that temporary environments will be functionally more diverse than permanent environments and will have different functional composition.

Methods: Five temporary ponds and five permanent lagoons were compared regarding their limnological characteristics, species richness, functional diversity indices and functional trait composition.

Results: No differences between ponds and lagoons were found regarding mean species richness and functional diversity. However, a larger number of species was found in the set of temporary environments i.e., although the mean richness was the same, the species' identity varied from one pond to another. Ponds showed greater variability in functional trait composition, resulting in significant differences in zooplankton functional dispersion. Ponds also presented a greater range of limnological characteristics.

Conclusions: Temporary and permanent environments present high limnological and functional complementarity, which make them important for maintaining biodiversity on a regional scale. Temporary environments seem to be refugees for species that do not settle in more stable environments because these species are more likely to colonize environments that periodically restart their successional trajectory. Therefore, actions that seek to preserve complementary environments are essential and urgent, especially those related to small and temporary environments.


functional dispersion, ponds, lagoons, functional diversity, species richness


Resumo:: Objetivo: Este estudo tem como objetivo avaliar a complementaridade funcional da comunidade zooplanctônica entre poças temporárias e lagoas permanentes. Nossa hipótese é de que ambientes temporários serão funcionalmente mais diversificados que ambientes permanentes e terão composição funcional diferente, sendo complementares entre si.

Métodos: Cinco lagoas e cinco poças foram comparadas quanto às características limnológicas, riqueza de espécies, índices de diversidade funcional e composição de características funcionais.

Resultados: Não foram encontradas diferenças significativas entre lagoas e poças em relação à riqueza e diversidade funcional. Todavia, uma maior variabilidade de espécies foi encontrada no conjunto de ambientes temporários, ou seja, embora a riqueza média tenha sido a mesma, a identidade das espécies variou de uma poça para outra. Poças apresentaram maior variabilidade na composição de traços funcionais, resultando em diferenças significativas nos valores de dispersão funcional. Poças apresentaram também uma maior amplitude de variação das características limnológicas.

Conclusões: Ambientes temporários e permanentes apresentam alta complementaridade limnológica e funcional, o que os torna importantes para a manutenção da biodiversidade em escala regional. Ambientes temporários parecem ser refúgios de espécies que não se estabelecem em ambientes mais estáveis, porque essas espécies têm maior probabilidade de colonizar ambientes que reiniciam periodicamente sua trajetória sucessional. Ações que buscam preservar ambientes complementares são essenciais e urgentes, principalmente aquelas direcionadas a ambientes pequenos e temporários.


dispersão funcional, poças, lagoas, diversidade funcional, riqueza de espécies


AL-THAWADI, S. Microplastics and nanoplastics in aquatic environments: challenges and threats to aquatic organisms. Arabian Journal for Science and Engineering, 2020, 45(6), 4419-4440.

ANTON-PARDO, M., ORTEGA, J.C.G., MELO, A.S. and BINI, L.M. Global meta-analysis reveals that invertebrate diversity is higher in permanent than in temporary lentic water bodies. Freshwater Biology, 2019, 64(12), 2234-2246.

ARAÚJO, L., LOPES, P.M., SANTANGELO, J.M., PETRY, A.C. and BOZELLI, R.L. Zooplankton resting egg banks in permanent and temporary tropical aquatic systems. Acta Limnologica Brasiliensia, 2013, 25(3), 235-245.

ARAÚJO, L.R., LOPES, P.M., SANTANGELO, J.M., ESTEVES, F.A. and BOZELLI, R.L. Long-term dynamics of the zooplankton community during large salinity fluctuations in a coastal lagoon. Marine and Freshwater Research, 2015, 66(4), 352-359.

BARNETT, A.J. and BEISNER, B.E. Zooplankton biodiversity and lake trophic state: explanations invoking resource abundance and distribution. Ecology, 2007, 88(7), 1675-1686. PMid:17645014.

BIGGS, J., VON FUMETTI, S. and KELLY-QUINN, M. The importance of small waterbodies for biodiversity and ecosystem services: implications for policy makers. Hydrobiologia, 2017, 793(1), 3-39.

BOIX, D., SALA, J. and MORENO-AMICH, R. The faunal composition of espolla pond (NE Iberian Peninsula): The neglected biodiversity of temporary waters. Wetlands, 2001, 21(4), 577-592.[0577:TFCOEP]2.0.CO;2.

BOZELLI, R.L., FARIAS, D.S., LIMA, S.K.F., LIRA, R.T.S., NOVA, C.C., SETUBAL, R.B. and SODRÉ, E.O. Pequenas áreas úmidas: importância para conservação e gestão da biodiversidade brasileira. Biodiversidade e Gestão, 2018, 2(2), 122-138.

BRANCO, C.C., KOZLOWSKY-SUZUKI, B., ESTEVES, F.A. and AGUIARO, T. Zooplankton distribution and community structure in a Brazilian coastal lagoon. Vie et Milieu-Life and Environment, 2008, 58(1), 1-9.

BRENDONCK, L., PINCEEL, T. and ORTELLS, R. Dormancy and dispersal as mediators of zooplankton population and community dynamics along a hydrological disturbance gradient in inland temporary Ponds. Hydrobiologia, 2017, 796(1), 201-222.

BURKEPILE, D.E. and HAY, M.E. Feeding complementarity versus redundancy among herbivorous fishes on a Caribbean reef. Coral Reefs, 2011, 30(2), 351-362.

CALHOUN, A.J.K., MUSHET, D.M., BELL, K.P., BOIX, D., FITZSIMONS, J.A. and ISSELIN-NONDEDEU, F. Temporary wetlands: challenges and solutions to conserving a ‘disappearing’ ecosystem. Biological Conservation, 2017, 211, 3-11.

CALIMAN, A., CARNEIRO, L.S., SANTANGELO, J.M., GUARIENTO, R.D., PIRES, A.P.F., SUHETT, A.L., QUESADO, L.B., SCOFIELD, V., FONTE, E.S., LOPES, P.M., SANCHES, L.F., AZEVEDO, F.D., MARINHO, C.C., BOZELLI, R.L., ESTEVES, F.A. and FARJALLA, V.F. Temporal coherence among tropical coastal lagoons: a search for patterns and mechanisms. Brazilian Journal of Biology = Revista Brasileira de Biologia, 2010, 70(3, Suppl.), 803-814. PMid:21085785.

CASTILLO, A.M., SHARPE, D.M.T., GHALAMBOR, C.K. and DE LEÓN, L.F. Exploring the effects of salinization on trophic diversity in freshwater ecosystems: a quantitative review. Hydrobiologia, 2018, 807(1), 1-17.

CONNELL, J.H. Diversity in tropical rain forests and coral reefs. Science, 1978, 199(4335), 1302-1310. PMid:17840770.

DAY, J.W. and RYBCZYK, J.M. Global change impacts on the future of coastal systems: perverse interactions among climate change, ecosystem degradation, energy scarcity, and population. In: E. WOLANSKI, J.W. DAY, M. ELLIOT and R. RAMACHANDRAN, eds. Coasts and estuaries: the future. New York: Elsevier, 2019, pp. 621-639.

DECLERCK, S., CORONEL, J.S., LEGENDRE, P. and BRENDONCK, L. Scale dependency of processes structuring metacommunities of cladocerans in temporary Ponds of High-Andes wetlands. Ecography, 2011, 34(2), 296-305.

DRENNER, S.M., DODSON, S.I., DRENNER, R.W. and PINDER III, J.E. Crustacean zooplankton community structure in temporary and permanent grassland ponds. Hydrobiologia, 2009, 632(1), 225-233.

ELMOOR-LOUREIRO, L.M.A. Manual de identificação de cladóceros Limnicos do Brasil. Brasilia:Editora Universa, 1997.

ELMQVIST, T., FOLKE, C., NYSTRÖM, M., PETERSON, G., BENGTSSON, J., WALKER, B. and NORBERG, J. Response diversity, ecosystem change, and resilience. Frontiers in Ecology and the Environment, 2003, 1(9), 488-494.[0488:RDECAR]2.0.CO;2.

ESTEVES, F.A., CALIMAN, A., SANTANGELO, J.M., GUARIENTO, R.D., FARJALLA, V.F. and BOZELLI, R.L. Neotropical coastal lagoons: an appraisal of their biodiversity, functioning, threats and conservation management. Brazilian Journal of Biology = Revista Brasileira de Biologia, 2008, 68(4, Suppl.), 967-981. PMid:19197469.

FONSECA, B.M., DE MENDONÇA-GALVÃO, L., SOUSA, F.D.R., ELMOOR-LOUREIRO, L.M.A., GOMES-E-SOUZA, M.B., PINTO, R.L., PETRACCO, P., OLIVEIRA, R.C. and JESUS LIMA, E. Biodiversity in pristine wetlands of Central Brazil: a multi-taxonomic approach. Wetlands, 2018, 38(1), 145-156.

FRAINER, A., MCKIE, B.G. and MALMQVIST, B. When does diversity matter? Species functional diversity and ecosystem functioning across habitats and seasons in a field experiment. Journal of Animal Ecology, 2014, 83(2), 460-469. PMid:26046457.

FUKAMI, T., MARTIJN BEZEMER, T., MORTIMER, S.R. and PUTTEN, W.H. Species divergence and trait convergence in experimental plant community assembly. Ecology Letters, 2005, 8(12), 1283-1290.

GESSNER, M.O., INCHAUSTI, P., PERSSON, L., RAFFAELLI, D.G. and GILLER, P.S. Biodiversity effects on ecosystem functioning: insights from aquatic systems. Oikos, 2004, 104, 419-422.

GOLTERMAN, H.L., CLIMO, R.S. and OHNSTAD, M.A.M. Methods for physical and chemical analysis of freshwaters. Oxford: Blackwell Scientific Publications, 1978. I.B.P. Handbook, no. 8.

GOZLAN, R.E., KARIMOV, B.K., ZADEREEV, E., KUZNETSOVA, D. and BRUCET, S. Status, trends, and future dynamics of freshwater ecosystems in Europe and Central Asia. Inland Waters, 2019, 9(1), 78-94.

GRAPHPAD. Graphpad Prism 5 for Windows. Version 5.01. San Diego, 2007.

HUMBERT, J.F. and DORIGO, U. Biodiversity and aquatic ecosystem functioning: a mini-review. Aquatic Ecosystem Health & Management, 2005, 8(4), 367-374.

HUNTER JUNIOR, M.L., ACUÑA, V., BAUER, D.M., BELL, K.P., CALHOUN, A.J.K., FELIPE-LUCIA, M.R., FITZSIMONS, J.A., GONZÁLEZ, E., KINNISON, M., LINDENMAYER, D., LUNDQUIST, C.J., MEDELLIN, R.A., NELSON, E.J. and POSCHLOD, P. Conserving small natural features with large ecological roles: a synthetic overview. Biological Conservation, 2017, 211, 88-95.

JENKINS, D.G. and BUIKEMA JUNIOR, A.L. Do similar communities develop in similar sites? A test with zooplankton structure and function. Ecological Monographs, 1998, 68(3), 421-443.[0421:DSCDIS]2.0.CO;2.

JOCQUE, M., FIELD, R., BRENDONCK, L. and MEESTER, L. Climatic control of dispersal-ecological specialization trade-offs: a metacommunity process at the heart of the latitudinal diversity gradient? Global Ecology and Biogeography, 2010, 19(2), 244-252.

JUNK, W.J., AN, S., FINLAYSON, C.M., GOPAL, B., KVĚT, J., MITCHELL, S.A., MITSCH, W.J. and ROBARTS, R.D. Current state of knowledge regarding the world’s wetlands and their future under global climate change: a synthesis. Aquatic Sciences, 2013, 75(1), 151-167.

KAHMEN, A., RENKER, C., UNSICKER, S.B. and BUCHMANN, N. Niche complementarity for nitrogen: an explanation for the biodiversity and ecosystem functioning relationship? Ecology, 2006, 87(5), 1244-1255.[1244:NCFNAE]2.0.CO;2. PMid:16761603.

KOSTE, W. Rotatoria: Die Rädertiere Mitteleuropas. Berlin: Gebrüder Borntraeger, 1978.

LALIBERTÉ, E. and LEGENDRE, P. A distance-based framework for measuring functional diversity from multiple traits. Ecology, 2010, 91(1), 299-305. PMid:20380219.

LITCHMAN, E., OHMAN, M.D. and KIORBOE, T. Trait-based approaches to zooplankton communities. Journal of Plankton Research, 2013, 35(3), 473-484.

LOPES, P.M., BOZELLI, R.L., BINI, L.M., SANTANGELO, J.M. and DECLERCK, S.A.J. Contributions of airborne dispersal and dormant propagule recruitment to the assembly of rotifer and crustacean zooplankton communities in temporary ponds. Freshwater Biology, 2016, 61(5), 658-669.

LOREAU, M., NAEEM, S., INCHAUSTI, P., BENGTSSON, J., GRIME, J.P., HECTOR, A., HOOPER, D.U., HUSTON, M.A., RAFFAELLI, D., SCHMID, B., TILMAN, D. and WARDLE, D.A. Biodiversity and ecosystem functioning: current knowledge and future challenges. Science, 2001, 294(5543), 804-808. PMid:11679658.

MACEDO-SOARES, P.H.M., PETRY, A.C., FARJALLA, V.F. and CARAMASCHI, E.P. Hydrological connectivity in coastal inland systems: Lessons from a Neotropical fish metacommunity. Ecology Freshwater Fish, 2010, 19(1), 7-18.

MACKERETH, F.J.H., HERON, J. and TALLING, J.F. Water analyses: some revised methods for Limnologists. Michigan: Freswater Ecological Association, 1978.

MARGULES, C.R. and PRESSEY, R.L. Systematic conservation planning. Nature, 2000, 405(6783), 243-253. PMid:10821285.

MASSICOTTE, P., FRENETTE, J.J., PROULX, R., PINEL-ALLOUL, B. and BERTOLO, A. Riverscape heterogeneity explains spatial variation in zooplankton functional evenness and biomass in a large river ecosystem. Landscape Ecology, 2014, 29(1), 67-79.

MEESTER, L., DECLERCK, S., STOKS, R., LOUETTE, G., VAN DE MEUTTER, F., DE BIE, T., MICHELS, E. and BRENDONCK, L. Ponds and Ponds as model systems in conservation biology, ecology and evolutionary biology. Aquatic Conservation, 2005, 15(6), 715-725.

MORI, A.S., FURUKAWA, T. and SASAKI, T. Response diversity determines the resilience of ecosystems to environmental change. Biological Reviews of the Cambridge Philosophical Society, 2013, 88(2), 349-364. PMid:23217173.

MULLINS, M.L. and DOYLE, R.D. Big things come in small packages: why limnologists should care about small ponds. Acta Limnologica Brasiliensia, 2019, 31(105), e105.

NORBERG, J. Resource-niche complementarity and autotrophic compensation determines ecosystem-level responses to increased cladoceran species richness. Oecologia, 2000, 122(2), 264-272. PMid:28308381.

NUSCH, E.A. and PALMER, G. Biologische methoden fur die praxis der gewasseruntersushung. GWF – Wasser/Abwasser, 1975, 116, 562-565. PMid:28308381.

OKSANEN, J., BLANCHET, F.G., FRIENDLY, M., KINDT, R., LEGENDRE, P., MCGLINN, D., MINCHIN, P.R., O’HARA, R.B., SIMPSON, G.L., SOLYMOS, P., STEVENS, M.H.H., SZOECS, E. and WAGNER, H. vegan: Community Ecology Package. R package version 2.5-2. Vienna: R Foundation for Statistical Computing, 2018.

OSKARSSON, A. and WRIGHT, M.C. Ionic liquids: new emerging pollutants, similarities with Perfluorinated Alkyl Substances (PFASs). Environmental Science & Technology, 2019, 53(18), 10539-10541. PMid:31442027.

PAVOINE, S., VALLET, J., DUFOUR, A.-B., GACHET, S. and DANIEL, H. On the challenge of treating various types of variables: application for improving the measurement of functional diversity. Oikos, 2009, 118(3), 391-402.

PETCHEY, O.L. and GASTON, K.J. Functional diversity (FD), species richness and community composition. Ecology Letters, 2002, 5(3), 402-411.

PETCHEY, O.L. Integrating methods that investigate how complementarity influences ecosystem functioning. Oikos, 2003, 101(2), 323-330.

PINCEEL, T., BUSCHKE, F., WECKX, M., BRENDONCK, L. and VANSCHOENWINKEL, B. Climate change jeopardizes the persistence of freshwater zooplankton by reducing both habitat suitability and demographic resilience. BMC Ecology, 2018, 18(1), 2. PMid:29361977.

PINCEEL, T., HAWINKEL, W., WYNANTS, E., BRENDONCK, L. and VANSCHOENWINKEL, B. Habitat uncertainty explains variation in offspring provisioning strategies in a temporary pond crustacean. Hydrobiologia, 2017, 801(1), 141-151.

POWELL, J.S.V. and BABBITT, K.J. Buffer-mediated effects of clearcutting on in-Pond amphibian productivity: Can aquatic processes compensate for terrestrial habitat disturbance? Forests, 2016, 8(1), 10.

PRESSEY, R.L., HUMPHRIES, C.J., MARGULES, C.R., VANE-WRIGHT, R.I. and WILLIAMS, P.H. Beyond opportunism: Key principles for systematic reserve selection. Trends in Ecology & Evolution, 1993, 8(4), 124-128. PMid:21236127.

R CORE TEAM. R: a language and environment for statistical computing [online]. Vienna: R Foundation for Statistical Computing, 2018 [viewed 27 May 2020]. Available from:

RUBBO, M.J., COLE, J.J. and KIESECKER, J.M. Terrestrial subsidies of organic carbon support net ecosystem production in temporary forest ponds: evidence from an ecosystem experiment. Ecosystems, 2006, 9(7), 1170-1176.

RUSSI, D., TEN BRINK, P., FARMER, A., BADURA, T., COATES, D., FORSTER, J., KUMAR, R. and DAVIDSON, N. The economics of ecosystems and biodiversity for water and wetlands. London: Ramsar Secretariat, 2013.

SANTANGELO, J.M., BOZELLI, R.L., ROCHA, A.M. and ESTEVES, F.A. Effects of slight salinity increases on Moina micrura (Cladocera) populations: field and laboratory observations. Marine and Freshwater Research, 2008, 59(9), 808-816.

SANTANGELO, J.M., ESTEVES, F.A., MANCA, M. and BOZELLI, R.L. Disturbances due to increased salinity and the resilience of zooplankton communities: the potential role of the resting egg bank. Hydrobiologia, 2013, 722(1), 103-113.

SANTANGELO, J.M., ROCHA, A.M., BOZELLI, R.L., CARNEIRO, L.S. and ESTEVES, F.A. Zooplankton responses to sandbar opening in a tropical eutrophic coastal lagoon. Estuarine, Coastal and Shelf Science, 2007, 71(3-4), 657-668.

SCARANO, F.R. Biodiversity sector: risks of temperature increase to biodiversity and ecosystems. In: C. NOBRE, J. MARENGO and W. SOARES, eds. Climate change risks in Brazil. Cham: Springer, 2019. p. 131-141.

SCHEFFER, M., VAN GEEST, G.J., ZIMMER, K., JEPPESEN, E., SØNDERGAARD, M., BUTLER, M.G., HANSON, M.A., DECLERCK, S. and DE MEESTER, L. Small habitat size and isolation can promote species richness: Second-order effects on biodiversity in shallow lakes and ponds. Oikos, 2006, 112(1), 227-231.

SCHRIEVER, T.A., CADOTTE, M.W. and WILLIAMS, D.D. How hydroperiod and species richness affect the balance of resource flows across aquatic-terrestrial habitats. Aquatic Sciences, 2014, 76(1), 131-143.

SEMINARA, M., VAGAGGINI, D. and MARGARITORA, F.G. Differential responses of zooplankton assemblages to environmental variation in temporary and permanent ponds. Aquatic Ecology, 2008, 42(1), 129-140.

SERRANO, L. and FAHD, K. Zooplankton communities across a hydroperiod gradient of temporary ponds in the Doñana National Park (SW SPAIN). Wetlands, 2005, 25(1), 101-111.[0101:ZCAAHG]2.0.CO;2.

SETUBAL, R.B., PETRY, A.C., BONECKER, C.C., MARTINS, T., NOVA, C.C., FIGUEIREDO-BARROS, M.P. and BOZELLI, R.L. Biotic factors determine ecosystem processes in environments with different hydrological regimes. Freshwater Biology, 2020, 65(8), 1376.

SETUBAL, R.B., SANTANGELO, J.M., ROCHA, A.M. and BOZELLI, R.L. Effects of sandbar openings on the zooplankton community of coastal lagoons with different conservation status. Acta Limnologica Brasiliensia, 2013, 25(3), 246-256.

SHURIN, J.B. Dispersal limitation, invasion resitance, and the structure of pond zooplankton commnities. Ecology, 2000, 81(11), 3074-3086.[3074:DLIRAT]2.0.CO;2.

SHURIN, J.B., HAVEL, J.E., LEIBOLD, M.A. and PINEL-ALLOUL, B. Local and regional zooplankton species richness: a scale-independent test for saturation. Ecology, 2000, 81(11), 3062-3073.[3062:LARZSR]2.0.CO;2.

TILMAN, D., KNOPS, J., WEDIN, D., REICH, P., RITCHIE, M. and SIEMANN, E. The influence of functional diversity and composition on ecosystem processes. Science, 1997, 277(5330), 1300-1302.

VANE-WRIGHT, R.I., HUMPHRIES, C.J. and WILLIAMS, P.H. What to protect? The agony of choice. Biological Conservation, 1991, 55(3), 235-254.

VANSCHOENWINKEL, B., HULSMANS, A., DE ROECK, E., DE VRIES, C., SEAMAN, M. and BRENDONCK, L. Community structure in temporary freshwater Ponds: disentangling the effects of habitat size and hydroregime. Freshwater Biology, 2009, 54(7), 1487-1500.

VILLÉGER, S., MASON, N.W.H. and MOUILLOT, D. New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology, 2008, 89(8), 2290-2301. PMid:18724739.

WALKER, B., KINZIG, A. and LANGRIDGE, J. Plant attribute diversity, resilience, and ecosystem function: the nature and significance of dominant and minor species. Ecosystems, 1999, 2(2), 95-113.

WILLIAMS, P.H. Complementarity. In: S. A. LEVIN, ed. Encyclopedia of biodiversity. San Diego: Academic Press, 2011, pp. 813-829.

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