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

Long-term dynamics of the zooplankton community during large salinity fluctuations in a coastal lagoon

Luciana Rabelo Araújo A C , Paloma Marinho Lopes A , Jayme Magalhães Santangelo B , Francisco de Assis Esteves A and Reinaldo Luiz Bozelli A
+ Author Affiliations
- Author Affiliations

A Universidade Federal do Rio de Janeiro (UFRJ), Avenida Carlos Chagas Filho, 373, CEP 21941-902, PO Box 68020, Rio de Janeiro, RJ, Brazil.

B Universidade Federal Rural do Rio de Janeiro (UFRRJ), Departamento de Ciências Ambientais, Rodovia BR 465, Km 07, CEP 23890-000, Seropédica, RJ, Brazil.

C Corresponding author. Email: luciana.rabelo.araujo@gmail.com

Marine and Freshwater Research 66(4) 352-359 https://doi.org/10.1071/MF14083
Submitted: 26 March 2014  Accepted: 15 July 2014   Published: 26 November 2014

Abstract

Aquatic coastal systems are affected by high fluctuations in salinity and the zooplankton may rely on dispersal or dormancy to recolonise these environments. Here, we analysed the long-term dynamics of the zooplankton community over 6 years during large salinity fluctuations in a coastal lagoon (Garças Lagoon, Brazil) and the effect of salinity on the hatching patterns of the resting egg bank. We hypothesised that salinity is the main driving factor of the zooplankton community structure, and that increases in salinity reduce the species richness and the abundance of hatchlings. Multiple regression analysis showed that salinity was associated negatively with species richness in the open water, whereas total phosphorus and chlorophyll-a concentrations were negatively and positively related to abundance respectively. Redundancy analysis demonstrated that temporally structured environmental variables (total phosphorus and salinity) were important for zooplankton composition. Periods of low salinity allowed the presence of freshwater organisms, changing the zooplankton composition over the years. However, our hatchling experiment showed a depauperate resting egg bank. Overall, our results showed a strong influence of salinity on the structure and dynamics of the zooplankton at Garças Lagoon, and that the resting egg bank likely plays a minor role in the zooplankton colonisation during low-salinity periods.

Additional keywords: coastal lake, environmental variables, resting eggs, salinity, shallow lake, temporal variables.


References

Aladin, N. V., and Potts, W. T. W. (1995). Osmoregulatory capacity of the Cladocera. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 164, 671–683.
Osmoregulatory capacity of the Cladocera.Crossref | GoogleScholarGoogle Scholar |

Arnér, M., and Koivisto, S. (1993). Effects of salinity on metabolism and life history characteristics of Daphnia magna. Hydrobiologia 259, 69–77.
Effects of salinity on metabolism and life history characteristics of Daphnia magna.Crossref | GoogleScholarGoogle Scholar |

Attayde, J. L., and Bozelli, R. L. (1998). Assessing the indicator properties of zooplankton assemblages to disturbance gradients by canonical correspondence analysis. Canadian Journal of Fisheries and Aquatic Sciences 55, 1789–1797.
Assessing the indicator properties of zooplankton assemblages to disturbance gradients by canonical correspondence analysis.Crossref | GoogleScholarGoogle Scholar |

Bailey, S. A., Duggan, I. C., Van Overdijk, C. D. A., Johengen, T. H., Reid, D. F., and MacIsaac, H. J. (2004). Salinity tolerance of diapausing eggs of freshwater zooplankton. Freshwater Biology 49, 286–295.
Salinity tolerance of diapausing eggs of freshwater zooplankton.Crossref | GoogleScholarGoogle Scholar |

Blanchet, F. G., Legendre, P., and Borcard, D. (2008). Forward selection of explanatory variables. Ecology 89, 2623–2632.
Forward selection of explanatory variables.Crossref | GoogleScholarGoogle Scholar | 18831183PubMed |

Boeuf, G., and Payan, P. (2001). How should salinity influence fish growth? Comparative Biochemistry and Physiology 130, 411–423.
| 1:STN:280:DC%2BD3MnptFCisA%3D%3D&md5=2b6682bc0672efd8241a67c9f52859cdCAS | 11738629PubMed |

Borcard, D., and Legendre, P. (2002). All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecological Modelling 153, 51–68.
All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices.Crossref | GoogleScholarGoogle Scholar |

Branco, C. W. C., Esteves, F. D., and Kozlowsky-Suzuki, B. (2000). The zooplankton and other limnological features of a humic coastal lagoon (Lagoa Comprida, Mace, RJ) in Brazil. Hydrobiologia 437, 71–81.
The zooplankton and other limnological features of a humic coastal lagoon (Lagoa Comprida, Mace, RJ) in Brazil.Crossref | GoogleScholarGoogle Scholar |

Brucet, S., Boix, D., Gascon, S., Sala, J., and Quintana, X. D. (2009). Species richness of crustacean zooplankton and trophic structure of brackish lagoons in contrasting climate zones: north temperate Denmark and Mediterranean Catalonia (Spain). Ecography 32, 692–702.
Species richness of crustacean zooplankton and trophic structure of brackish lagoons in contrasting climate zones: north temperate Denmark and Mediterranean Catalonia (Spain).Crossref | GoogleScholarGoogle Scholar |

Caliman, A., Carneiro, L. S., Santangelo, J. M., Guariento, R. D., and Pires, A. P. F. (2010). Temporal coherence among tropical coastal lagoons: a search for patterns and mechanisms. Brazilian Journal of Biology 70, 803–814.
Temporal coherence among tropical coastal lagoons: a search for patterns and mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M%2FgtlOhsA%3D%3D&md5=05528d1b37631c444f6dca4e163d96d7CAS |

Cohen, G. M., and Shurin, J. B. (2003). Scale-dependence and mechanisms of dispersal in freshwater zooplankton. Oikos 103, 603–617.
Scale-dependence and mechanisms of dispersal in freshwater zooplankton.Crossref | GoogleScholarGoogle Scholar |

de Macedo-Soares, P. H. M., Petry, A. C., Farjalla, V. F., and Caramaschi, E. P. (2010). Hydrological connectivity in coastal inland systems: lessons from a Neotropical fish metacommunity. Ecology Freshwater Fish 19, 7–18.
Hydrological connectivity in coastal inland systems: lessons from a Neotropical fish metacommunity.Crossref | GoogleScholarGoogle Scholar |

Dray, S., Legendre, P., and Blanchet, F. G. (2011). packfor: forward selection with permutation (Canoco p.46). R package version 0.0-8/r100. Available at http://R-Forge.R-project.org/projects/sedar/ [Verified 8 October 2014].

Duggan, I. C., and White, M. A. (2010). Consequences of human-mediated marine intrusions on the zooplankton community of a temperate coastal lagoon. New Zealand Journal of Marine and Freshwater Research 44, 17–28.
Consequences of human-mediated marine intrusions on the zooplankton community of a temperate coastal lagoon.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXltF2qu70%3D&md5=15ce037125bfdcfe7917a248b13e7a2bCAS |

Dutilleul, P. (1993). Modifying the t test for assessing the correlation between two spatial processes. Biometrics 49, 305–314.
Modifying the t test for assessing the correlation between two spatial processes.Crossref | GoogleScholarGoogle Scholar |

Elmoor-Loureiro, L. M. A. (1997). ‘Manual de Identificação de Cladóceros Límnicos do Brasil.’ (Universa: Taguatinga.)

Enrich-Prast, A., Bozelli, R. L., Esteves, F. A., and Meirelles, F. P. (2004). Lagoas costeiras da restinga de Jurubatiba: descrição de suas variáveis limnológicas. In ‘Pesquisas de Longa Duração na Restinga de Jurubatiba: Ecologia, História Natural e Conservação’. (Eds C. F. D. Rocha, F. A. Esteves and F. R. Scarano.) pp. 374–382. (Rima Editora: Rio de Janeiro, Brazil.)

Esteves, F. A., Caliman, A., Santangelo, J. M., Guariento, R. D., Farjalla, V. F., and Bozelli, R. L. (2008). Neotropical coastal lagoons: an appraisal of their biodiversity, functioning, threats and conservation management. Brazilian Journal of Biology 68, 967–981.
Neotropical coastal lagoons: an appraisal of their biodiversity, functioning, threats and conservation management.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M7ltVSktQ%3D%3D&md5=14de2597d7cdab0ee83e70114c33c08dCAS |

Farjalla, V. F., Laque, T., Suhett, A. L., Amado, A. M., and Esteves, F. A. (2005). Diel variation of bacterial abundance and productivity in tropical coastal lagoons: the importance of bottom-up factors in a short time scale. Acta Limnologica Brasiliensia 17, 373–383.

Fox, J., and Weisberg, S. (2011). An {R} Companion to Applied Regression, 2nd edn. (Sage: Thousand Oaks, CA.) Available at http://socserv.socsci.mcmaster.ca/jfox/Books/Companion [Verified 8 October 2014].

García-Roger, E. M., Armengol, X., Carmona, M. J., and Serra, M. (2008). Assessing rotifer diapausing egg bank diversity and abundance in brackish temporary environments: an ex situ sediment incubation approach. Fundamental and Applied Limnology 173, 79–88.
Assessing rotifer diapausing egg bank diversity and abundance in brackish temporary environments: an ex situ sediment incubation approach.Crossref | GoogleScholarGoogle Scholar |

Gołdyn, R., and Kowalczewska-Madura, K. (2008). Interactions between phytoplankton and zooplankton in the hypertrophic Swarzędzkie Lake in western Poland. Journal of Plankton Research 30, 33–42.
Interactions between phytoplankton and zooplankton in the hypertrophic Swarzędzkie Lake in western Poland.Crossref | GoogleScholarGoogle Scholar |

Golterman, H. L., Climo, R. S., and Ohnstad, M. A. M. (1978). ‘Methods for Physical and Chemical Analysis of Freshwaters.’ IBP Handbook number 8. (Blackwell Scientific Publications: Oxford, UK.)

Graham, M. H. (2003). Confronting multicollinearity in ecological multiple regression. Ecology 84, 2809–2815.
Confronting multicollinearity in ecological multiple regression.Crossref | GoogleScholarGoogle Scholar |

Gyllström, M., and Hansson, L. A. (2004). Dormancy in freshwater zooplankton: induction, termination and the importance of benthic–pelagic coupling. Aquatic Sciences 66, 274–295.
Dormancy in freshwater zooplankton: induction, termination and the importance of benthic–pelagic coupling.Crossref | GoogleScholarGoogle Scholar |

Hairston, N. G., Hansen, A. M., and Schaffner, W. R. (2000). The effect of diapause emergence on the seasonal dynamics of a zooplankton assemblage. Freshwater Biology 45, 133–145.
The effect of diapause emergence on the seasonal dynamics of a zooplankton assemblage.Crossref | GoogleScholarGoogle Scholar |

Hart, C. M., Gonzalez, M. R., Simpson, E. P., and Stuart, H. H. T. (1998). Salinity and fish effects on Salton Sea microecosystems: zooplankton and nekton. Hydrobiologia 381, 129–152.
Salinity and fish effects on Salton Sea microecosystems: zooplankton and nekton.Crossref | GoogleScholarGoogle Scholar |

Havel, J. E., and Shurin, J. B. (2004). Mechanisms, effects, and scales of dispersal in freshwater zooplankton. Limnology and Oceanography 49, 1229–1238.
Mechanisms, effects, and scales of dispersal in freshwater zooplankton.Crossref | GoogleScholarGoogle Scholar |

Heine-Fuster, I., Vega-Retter, C., Sabat, P., and Ramos-Jiliberto, R. (2010). Osmoregulatory and demographic responses to salinity of the exotic cladoceran Daphnia exilis. Journal of Plankton Research 32, 1405–1411.
Osmoregulatory and demographic responses to salinity of the exotic cladoceran Daphnia exilis.Crossref | GoogleScholarGoogle Scholar |

Jeppesen, E., Jensen, J. P., Sondergaard, M., Lauridsen, T., and Landkildehus, F. (2000). Trophic structure, species richness and biodiversity in Danish lakes: changes along a phosphorus gradient. Freshwater Biology 45, 201–218.
Trophic structure, species richness and biodiversity in Danish lakes: changes along a phosphorus gradient.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotlymsrc%3D&md5=ad44857931af1c19af9882908cdb1ab2CAS |

Kefford, B. J., Palmer, C. G., Pakhomova, L., and Nugegoda, D. (2004). Comparing different approaches to measuring the salinity tolerance of freshwater invertebrates. Water S.A. 30, 499–506.
Comparing different approaches to measuring the salinity tolerance of freshwater invertebrates.Crossref | GoogleScholarGoogle Scholar |

Kibirige, I., Perissinoto, R., and Thwala, X. (2006). A comparative study of zooplankton dynamics in two subtropical temporarily open/closed estuaries, South Africa. Marine Biology 148, 1307–1324.
A comparative study of zooplankton dynamics in two subtropical temporarily open/closed estuaries, South Africa.Crossref | GoogleScholarGoogle Scholar |

Koste, W. (1978). ‘Die Radertiere mitteleuropas begrundet von Max Voigt.’ (Gebruder Borntraeger: Stuttgart).

Legendre, P. (1993). Spatial autocorrelation: trouble or new paradigm? Ecology 74, 1659–1673.
Spatial autocorrelation: trouble or new paradigm?Crossref | GoogleScholarGoogle Scholar |

Legendre, P., Borcard, D., Blanchet, F. G., and Dray, S. (2012). PCNM: MEM spatial eigenfunction and principal coordinate analyses. R package ver. 2.1–2/r106. Available at http://R-Forge.R-project.org/projects/sedar/ [Verified 8 October 2014].

Louette, G., and De Meester, L. (2005). High dispersal capacity of cladoceran zooplankton in newly founded communities. Ecology 86, 353–359.
High dispersal capacity of cladoceran zooplankton in newly founded communities.Crossref | GoogleScholarGoogle Scholar |

Mackereth, F. J. H., Heron, J., and Talling, J. F. (1978). ‘Water Analysis: Some revIsed Methods for Limnologists.’ Scientific Publication 36. (Freshwater Biological Association: Ambleside, UK.)

McLusky, D. S., and Elliott, M. (2007). Transitional waters: a new approach, semantics or just muddying the waters? Estuarine, Coastal and Shelf Science 71, 359–363.
Transitional waters: a new approach, semantics or just muddying the waters?Crossref | GoogleScholarGoogle Scholar |

Nicholls, R. J., Wong, P. P., Burkett, V. R., Codignotto, J. O., and Hay, J. E. (2007). Coastal systems and low-lying areas. In ‘Climate Change 2007: Impacts, Adaptation and Vulnerability’. (Eds M. L. Parry, O. F. Canziani, J. P. Palutikof, P. J. van der Linden and C. E. Hanson.) pp. 315–356. (Cambridge University Press: Cambridge, UK.)

Nielsen, D. L., Smith, D., and Petrie, R. (2012). Resting egg banks can facilitate recovery of zooplankton communities after extended exposure to saline conditions. Freshwater Biology 57, 1306–1314.
Resting egg banks can facilitate recovery of zooplankton communities after extended exposure to saline conditions.Crossref | GoogleScholarGoogle Scholar |

Nusch, E. A., and Palme, G. (1975). Biologische Methoden fur die Praxis der Gewasseruntersuchung. GWF – Wasser/Abwasser 116, 562–565.

Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O’Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H., and Wagner, H. (2012). Vegan: community ecology package. R package ver. 2.0-4. Available at http://CRAN.R-project.org/package=vegan [Verified 8 October 2014].

Onbe, T. (1978). Sugar flotation method for sorting the resting eggs of marine cladocerans and copepods from sea-bottom sediment. Bulletin of the Japanese Society of Scientific Fisheries 44, 1411.

Pinder, A. M., Halse, S. A., McRae, J. M., and Shiel, R. J. (2005). Occurrence of aquatic invertebrates of the wheat belt region of Western Australia in relation to salinity. Hydrobiologia 543, 1–24.
Occurrence of aquatic invertebrates of the wheat belt region of Western Australia in relation to salinity.Crossref | GoogleScholarGoogle Scholar |

Pinto-Coelho, R., Pinel-Alloul, B., Methot, G., and Havens, K. E. (2005). Crustacean zooplankton in lakes and reservoirs of temperate and tropical regions: variation with trophic status. Canadian Journal of Fisheries and Aquatic Sciences 62, 348–361.
Crustacean zooplankton in lakes and reservoirs of temperate and tropical regions: variation with trophic status.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkvFCis7Y%3D&md5=997096dc8e9d41247b16df73feabf65fCAS |

R Core Team (2012). R: a language and environment for statistical computing. (R Foundation for Statistical Computing: Vienna, Austria.) Available at http://www.R-project.org/ [Verified 8 October 2014].

Remane, A., and Schlieper, C. (1978). ‘Biology of Brackish Water.’ (Wiley Interscience: Stuttgart.)

Santangelo, J. M., Rocha, A. D. M., Bozelli, R. L., Carneiro, L. S., and Esteves, F. A. (2007). Zooplankton responses to sandbar opening in a tropical eutrophic coastal lagoon. Estuarine, Coastal and Shelf Science 71, 657–668.
Zooplankton responses to sandbar opening in a tropical eutrophic coastal lagoon.Crossref | GoogleScholarGoogle Scholar |

Santangelo, J. M., Bozelli, R. L., Rocha, A. D., and Esteves, F. D. (2008). Effects of slight salinity increases on Moina micrura (Cladocera) populations: field and laboratory observations. Marine and Freshwater Research 59, 808–816.
Effects of slight salinity increases on Moina micrura (Cladocera) populations: field and laboratory observations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1WnsbvL&md5=6de6c3b9fd830dbd6f4e8244854ac184CAS |

Santangelo, J. M., Araújo, L. R., Esteves, F. A., Manca, M., and Bozelli, R. L. (2011a). Method for hatching resting eggs from tropical zooplankton: effects of drying or exposing to low temperatures before incubation. Acta Limnologica Brasiliensia 23, 42–47.
Method for hatching resting eggs from tropical zooplankton: effects of drying or exposing to low temperatures before incubation.Crossref | GoogleScholarGoogle Scholar |

Santangelo, J. M., Esteves, F. A., Manca, M., and Bozelli, R. L. (2011b). Abundance, composition and spatial variation in the egg bank of a tropical zooplankton community. Studies on Neotropical Fauna and Environment 46, 225–232.
Abundance, composition and spatial variation in the egg bank of a tropical zooplankton community.Crossref | GoogleScholarGoogle Scholar |

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

Siqueira, T., Roque, F. O., and Trivinho-Strixino, S. (2008). Phenological patterns of neotropical lotic chironomids: is emergence constrained by environmental factors? Austral Ecology 33, 902–910.
Phenological patterns of neotropical lotic chironomids: is emergence constrained by environmental factors?Crossref | GoogleScholarGoogle Scholar |

ter Braak, C. J. F. (1985). Correspondence analysis of incidence and abundance data: properties in terms of a unimodal response model. Biometrics 41, 859–873.
Correspondence analysis of incidence and abundance data: properties in terms of a unimodal response model.Crossref | GoogleScholarGoogle Scholar |

Tollrian, R. (1993). Neckteeth formation in Daphnia pulex as an example of continuous phenotypic plasticity – morphological effects of Chaoborus kairomone concentration and their quantification. Journal of Plankton Research 15, 1309–1318.
Neckteeth formation in Daphnia pulex as an example of continuous phenotypic plasticity – morphological effects of Chaoborus kairomone concentration and their quantification.Crossref | GoogleScholarGoogle Scholar |

UNESCO (1981). Background papers and supporting data on the practical salinity scale 1978. UNESCO technical papers in marine science 37, Paris. Available at http://unesdoc.unesco.org/images/0004/000479/047932eb.pdf [Verified 8 October 2014].

Vandekerkhove, J., Niessen, B., Declerck, S., Jeppesen, E., Porcuna, J. M. C., Brendonck, L., and De Meester, L. (2004). Hatching rate and hatching success with and without isolation of zooplankton resting stages. Hydrobiologia 526, 235–241.
Hatching rate and hatching success with and without isolation of zooplankton resting stages.Crossref | GoogleScholarGoogle Scholar |

Vandekerkhove, J., Declerck, S., Brendonck, L., Conde-Porcuna, J. M., Jeppesen, E., and De Meester, L. (2005). Hatching of cladoceran resting eggs: temperature and photoperiod. Freshwater Biology 50, 96–104.
Hatching of cladoceran resting eggs: temperature and photoperiod.Crossref | GoogleScholarGoogle Scholar |

Waterkeyn, A., Vanschoenwinkel, B., Vercampt, H., Grillas, P., and Brendonck, L. (2011). Long-term effects of salinity and disturbance regime on active and dormant crustacean communities. Limnology and Oceanography 56, 1008–1022.
Long-term effects of salinity and disturbance regime on active and dormant crustacean communities.Crossref | GoogleScholarGoogle Scholar |