Abstract
In Mediterranean temporary ponds, the timing of annual flooding is highly variable and depends on heavy seasonal rains. Ponds can flood in the autumn, winter, or spring, and thus the environmental conditions faced by emerging zooplankton can be very different. We performed an experiment in a climatic chamber where we simulated annual variation in natural temperature and light conditions to study how differences in pond-filling season affected zooplankton assemblage composition. We sampled sediments from a temporary pond and placed them in aquariums that were filled with water during three different seasons: autumn (October), winter (January), and spring (March). Zooplankton abundance, species richness, diversity, and assemblage composition differed significantly among treatments, and post-inundation temperature and pH appeared to be the main drivers of these differences. Diversity was highest in the winter treatment. It was lower in the autumn treatment and the spring treatment, and no indicator species were present in the latter. Our results suggest that interannual variability in initial inundation conditions favours the emergence of different species and thus contributes to high species richness in the egg bank. However, climate change and/or groundwater drawdown could delay pond flooding, impoverishing the zooplankton assemblage in the long term.
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References
Alonso, M., 1996. Crustacea, Branchiopoda. In Ramos, M. A. (ed.), Fauna Ibérica, Vol. 57., Museo Nacional de Ciencias Naturales CSIC, Madrid: 1–486.
Anderson, R. S., 1970. Predator–prey relationships and predation rates for crustacean zooplankters from some lakes in western Canada. Canadian Journal of Zoology 48: 1229–1240.
Anderson, M. J., 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26: 32–46.
Anderson, M. J., R. N. Gorley & K. R. Clarke, 2008. PERMANOVA+ for PRIMER: Guide to software and Statistical Methods. PRIMER-E, Plymouth.
Bottrell, H. H., 1975. Generation time, length of life, instar duration and frequency of moulting and their relationship to temperature in eight species of Cladocera from the River Thames, Reading. Oecologia 19: 129–140.
Brandl, Z., 2005. Freshwater copepods and rotifers: Predators and their prey. Hydrobiologia 546: 475–489.
Brendonck, L. & L. De Meester, 2003. Egg banks in freshwater zooplankton: Evolutionary and ecological archives in the sediment. Hydrobiologia 491: 65–84.
Brendonck, L., B. J. Riddoch, V. Van de Weghe & T. Van Dooren, 1998. The maintenance of egg banks in very short-lived pools – A case study with anostracans (Branchiopoda). Archiv für Hydrobiologie 52: 141–161.
Brendonck, L., T. Pinceel & R. Ortells, 2017. Dormancy and dispersal as mediators of zooplankton population and community dynamics along a hydrological disturbance gradient in inland temporary pools. Hydrobiologia 796: 201–222.
Brock, M. A., D. L. Nielsen, R. J. Shiel, J. D. Green & J. D. Langley, 2003. Drought and aquatic community resilience: The role of eggs and seeds in sediments of temporary wetlands. Freshwater Biology 48: 1207–1218.
Cáceres, C. E., 1997. Temporal variation, dormancy, and coexistence: A field test of the storage effect. Ecology 94: 9171–9175.
Cáceres, C. E. & M. S. Schwalbach, 2001. How well do laboratory experiments explain field patterns of zooplankton emergence? Freshwater Biology 46: 1179–1189.
Chesson, P. & N. Huntly, 1989. Short-term instabilities and long-term community dynamics. Trends in Ecology & Evolution 4: 293–298.
Custodio, E., M. Manzano & C. M. del Olmo, 2009. Las aguas subterráneas en Doñana: Aspectos ecológicos y sociales. Agencia Andaluza del Agua, Consejería de Medio Ambiente, Junta de Andalucía, Seville.
De Cáceres, M., P. Legendre & M. Moretti, 2010. Improving indicator species analysis by combining groups of sites. Oikos 119: 1674–1684.
de Eyto, E. & K. Irvine, 2001. The response of three chydorid species to temperature, pH and food. Hydrobiologia 459: 165–172.
Díaz-Paniagua, C., R. Fernández-Zamudio, M. Florencio, P. García-Murillo, C. Gómez-Rodríguez, A. Portheault, L. Serrano & P. Siljeström, 2010. Temporary ponds from the Doñana National Park: A system of natural habitats for the preservation of aquatic flora and fauna. Limnetica 29: 41–58.
Díaz-Paniagua, C., R. Fernández-Zamudio, L. Serrano, M. Florencio, C. Gómez-Rodríguez, A. Sousa, P. Sánchez Castillo, P. García-Murillo & P. Siljestrom, 2015. El sistema de lagunas temporales de Doñana, una red de hábitats acuáticos singulares. Organismo Autónomo de Parques Nacionales. Miniterio de Agricultura, Alimentación y Medio Ambiente, Madrid.
Dufrêne, M. & P. Legendre, 1997. Species assemblages and indicator species: The need for a flexible asymmetrical approach. Ecological Monographs 67: 345–366.
Dussart, B. H., 1967. Contribution à létude des Copépodes dEspagne. Publicaciones del Instituto de Biologia Aplicada 42: 87–105.
Dussart, B. H., 1969. Les copépodes des eaux continentales d’Europe occidentale. Tome II: Cyclopoïdes et Biologie. N. Boubée et Cie, Paris.
Fahd, K., A. Arechederra, M. Florencio, D. León & L. Serrano, 2009. Copepods and branchiopods of temporary ponds in the Doñana natural area (SW Spain): A four-decade record (1964–2007). Hydrobiologia 634: 219–230.
Florencio, M., C. Díaz-Paniagua, L. Serrano & D. T. Bilton, 2011. Spatio-temporal nested patterns in macroinvertebrate assemblages across a pond network with a wide hydroperiod range. Oecologia 166: 469–483.
Florencio, M., C. Gómez-Rodríguez, L. Serrano & C. Díaz-Paniagua, 2013. Competitive exclusion and habitat segregation in seasonal macroinvertebrate assemblages in temporary ponds. Freshwater Science 32: 650–662.
Florencio, M., C. Díaz-Paniagua & L. Serrano, 2016. Relationships between hydroperiod length, and seasonal and spatial patterns of beta-diversity of the microcrustacean assemblages in Mediterranean ponds. Hydrobiologia 774: 109–121.
Frisch, D., E. Moreno-Ostos & A. J. Green, 2006. Species richness and distribution of copepods and cladocerans and their relation to hydroperiod and other environmental variables in Doñana, south-west Spain. Hydrobiologia 556: 327–340.
Fryer, G., 1968. Evolution and adaptive radiation in the Chydoridae (Crustacea: Cladocera): A study in comparative functional morphology and ecology. Philosophical Transactions of the Royal Society of London B, Biological Sciences 254: 221–385.
Ghazy, M. M. E., M. M. Habashy & E. Y. Mohammady, 2011. Effects of pH on survival, growth and reproduction rates of the Crustacean, Daphnia Magna. Australian Journal of Basic and Applied Sciences 5: 1–10.
Gillooly, F. J., 2000. Effect of body size and temperature on generation time in zooplankton. Journal of Plankton Research 22: 241–251.
Green, A. J., P. Alcorlo, E. T. Peeters, E. P. Morris, J. L. Espinar, M. A. Bravo-Utrera, J. Bustamante, R. Díaz-Delgado, A. Koelmans, R. Mateo, W. M. Mooij, M. Rodríguez-Rodríguez, E. H. van Nes & M. Scheffer, 2017. Creating a safe operating space for wetlands in a changing climate. Frontiers in Ecology and the Environment 15: 99–107.
Hairston Jr., N. G., A.-M. Hansen & W. R. Schaffner, 2000. The effect of diapause emergence on the seasonal dynamics of a zooplankton assemblage. Freshwater Biology 45: 133–145.
Hothorn, T., F. Bretz, P. Westfall & R. M. Heiberger, 2008. multcomp: Simultaneous inference in general parametric models. Biometrical Journal 50: 346–363. http://CRAN.R-project.org. R package version 1.0-0.
Kneitel, J. M., 2014. Inundation timing, more than duration, affects the community structure of California vernal pool mesocosms. Hydrobiologia 732: 71–83.
Koste, W., 1978. Rotatoria. Die Radertiere Mittel-europas, 2nd ed. Gebruder Borntraeger, Berlin and Stuttgart.
Locke, A. & W. G. Sprules, 2000. Effects of acidic pH and phytoplankton on survival and condition of Bosmina longirostris and Daphnia pulex. Hydrobiologia 437: 187–196.
Loreau, M., S. Naeem, P. Inchausti, J. Bengtsson, J. P. Grime, A. Hector, D. U. Hooper, M. A. Huston, D. Raffaelli, B. Schmind, D. Tilman & D. A. Wardle, 2001. Biodiversity and ecosystem functioning: Current knowledge and future challenges. Science 294: 804–808.
Manzano, M. & E. Custodio, 2006. The Doñana aquifer and its relations with the natural environment. In GarcíaNovo, F. & C. Marín (eds), Doñana Water and Biosphere: Confederación Hidrográfica del Guadalquivir. Ministerio de Medio Ambiente, Madrid: 141–150.
Marrone, F. & L. Naselli-Flores, 2004. First record and morphological features of Hemidiaptomus (Occidodiaptomus) ingens (Gurney, 1909) (Copepoda Calanoida) in Italy. Journal of Limnology 63: 250–255.
McArdle, B. H. & M. J. Anderson, 2001. Fitting multivariate models to community data: A comment on distance-based redundancy analysis. Ecology 82: 290–297.
R Development Core Team, 2018. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/.
Pinceel, T., B. Vanschoenwinkel, J. Uten & L. Brendonck, 2013. Mechanistic and evolutionary aspects of light-induced dormancy termination in a temporary pond crustacean. Freshwater Science 32: 517–524.
Pinceel, T., B. Vanschoenwinkel, W. Hawinkel, K. Tuytens & L. Brendonck, 2017. Aridity promotes bet hedging via delayed hatching: A case study with two temporary pond crustaceans along a latitudinal gradient. Oecologia 184: 161–170.
Seminara, M., D. Vagaggini & F. G. Margaritora, 2008. Differential responses of zooplankton assemblages to environmental variation in temporary and permanent ponds. Aquatic ecology 42: 129–140.
Serrano, L. & J. Toja, 1998. Interannual variability in the zooplankton community of a shallow temporary pond. Internationale Vereinigung für Theoretische und Angewandte 26: 1575–1581.
Serrano, L. & K. Fahd, 2005. Zooplankton communities across a hydroperiod gradient of temporary ponds in the Donana National Park (SW Spain). Wetlands 25: 101–111.
Shurin, J. B., M. Winder, R. Adrian, W. Keller, B. Matthews, A. M. Paterson, M. J. Paterson, B. Pinel-Alloul, J. A. Rusak & N. D. Yan, 2010. Environmental stability and lake zooplankton diversity – Contrasting effects of chemical and thermal variability. Ecology Letters 13: 453–463.
Tavernini, S., G. Mura & G. Rossetti, 2005. Factors influencing the seasonal phenology and composition of zooplankton communities in mountain temporary pools. International Review of Hydrobiology 90: 358–375.
Vanderkherkove, J., S. Declerck, L. Brendonck, J. M. Conde-Porcuna, E. Jeppesen & L. De Meester, 2005. Hatching of cladoceran resting eggs: Temperature and photoperiod. Freshwater Biology 50: 96–104.
Verbitsky, V. B. & T. I. Verbitskaya, 2011. Effects of constant and stepwise changes in temperature on the species abundance dynamics of four cladocera species. Knowledge and Management of Aquatic Ecosystems 402(03): 1–19.
Wheeler, B., 2016. lmPerm: Permutation tests for linear models. R package version 2.1.0. https://CRAN.R-project.org/package=lmPerm.
Williams, D. D., 2006. The biology of temporary waters. Oxford University Press, Oxford.
Acknowledgements
MF is grateful for her postdoctoral contracts, which were funded by the University of Alcala and the Universidad Autónoma de Madrid. The field resources, climatic chambers, and laboratory facilities were provided by Doñana ICTS-RBD. We are grateful to Jessica Pearce for her professional language editing services.
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Florencio, M., Fernández-Zamudio, R., Lozano, M. et al. Interannual variation in filling season affects zooplankton diversity in Mediterranean temporary ponds. Hydrobiologia 847, 1195–1205 (2020). https://doi.org/10.1007/s10750-019-04163-3
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DOI: https://doi.org/10.1007/s10750-019-04163-3