Abstract
Although some efforts have been made to understand the role of hydrology in structuring aquatic systems, little is known about how rainfall affects the relative roles of local environmental and spatial processes in structuring plankton metacommunities in tropical drylands. We hypothesize that the role played by spatial variables is more important in the dry than in the rainy season, because drought increases lakes isolation in semiarid regions. To test our hypothesis, we compared the variation in plankton structure between seasons attributable to local and spatial predictors by using variation-partitioning techniques. We used data for phytoplankton and zooplankton communities as a whole and separately by their size groups (nanoplankton, microplankton and mesoplankton) from 40 man-made lakes in northeastern Brazil. Our results showed that rainfall homogenized limnological variables and reduced total phytoplankton and nanophytoplankton beta diversity, but no effect of season was observed for microphytoplankton and zooplankton communities. Overall, in the dry season, both environmental and spatial variables were important structuring factors for the total phytoplankton, total zooplankton and microzooplankton communities, concurring with both niche- and neutral-based models. In the rainy season, spatial variables were neither important for shaping the phytoplankton nor the zooplankton metacommunities, confirming our hypothesis. The main ecological implication of our findings is that both niche- and neutral-based processes might play an important role on phytoplankton and zooplankton metacommunities dynamics in a future warmer and drier climate in tropical semiarid regions.
Similar content being viewed by others
References
Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek PC (2013) Köppen’s climate classification map for Brazil. Meteorol Z 22:711–728
Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62:245–253
Angeler DG, Alvarez-Cobelas M, Rojo C, Sánchez-Carrillo S (2010) Phytoplankton community similarity in a semiarid floodplain under contrasting hydrological connectivity regimes. Ecol Res 25:513–520
APHA (1998) Standard methods for the examination of water and wastewater. American Public Health Association, Washington DC
Araújo HPF, Rodrigues RC (2011) Birds from open environments in the caatinga from state of Alagoas, northeastern Brazil. Rev Bras Zool 28:629–640
Attayde JL, Panosso R (2011) Capacidade de suporte de oito açudes do Rio Grande do Norte para a piscicultura intensiva em tanques-rede. In: Anais do XIX Simpósio Brasileiro de Recursos Hídricos pp 1–18
Beisner BE, Peres-Neto PR, Lindstrom ES, Barnett A, Longhi ML (2006) The role of environmental and spatial processes in structuring lake communities from bacteria to fish. Ecology 87:2985–2991
Blanchet F, Legendre GP, Borcard D (2008) Forward selection of explanatory variables. Ecology 89:2623–2632
Borcard D, Legendre P, Avois-Jacquet C, Tuomisto H (2004) Dissecting the spatial structure of ecological data at multiple scales. Ecology 85:1826–1832
Bouvy M, Falcão D, Marinho M, Pagano M, Moura A (2000) Occurrence of Cylindrospermopsis (Cyanobacteria) in 39 Brazilian tropical reservoirs during the 1998 drought. Aquat Microb Ecol 23:13–27
Bouvy M, Nascimento SM, Molica RJR, Ferreira A, Huszar V, Azevedo SMFO (2003) Limnological features in Tapacurá reservoir (northeast Brazil) during a severe drought. Hydrobiologia 493:115–130
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
Brasil J, Attayde JL, Vasconcelos FR, Dantas DDF, Huszar VLM (2016) Drought-induced water-level reduction favors cyanobacteria blooms in tropical shallow lakes. Hydrobiologia 770:145–164
Cabral CR, Guariento RD, Ferreira FC, Amado AM, Nobre RLG, Carneiro LS, Caliman A (2019) Are the patterns of zooplankton community structure different between lakes and reservoirs? A local and regional assessment across tropical ecosystems. Aquat Ecol 53:335–346
Chase JM (2007) Drought mediates the importance of stochastic community assembly. PNAS 104:17430–17434
Chase JM, Leibold MA (2002) Spatial scale dictates the productivity-biodiversity relationship. Nature 416:427–430
Chessel D, Dufour AB, Thioulouse J (2004) The ade4 package—I: One-table methods. R News 4:5–10
Costa MRA, Attayde JL, Becker V (2016) Effects of water level reduction on the dynamics of phytoplankton functional groups in tropical semi-arid shallow lakes. Hydrobiologia 778:75–89
De Bie TD, De Meester L, Brendonck L et al (2012) Body size and dispersal mode as key traits determining metacommunity structure of aquatic organisms. Ecol Lett 15:740–747
Declerck SAJ, Coronel JS, Legendre P, Brendonck L (2011) Scale dependency of processes structuring metacommunities of cladocerans in temporary pools of High-Andes wetlands. Ecography 34:296–305
Dias JD, Simões NR, Meerhoff M, Lansac-Tôha FA, Velho LFM, Bonecker CC (2016) Hydrological dynamics drives zooplankton metacommunity structure in a Neotropical floodplain. Hydrobiologia 781:109–125
Diniz-Filho JAF, Siqueira T, Padial AA, Rangel TF, Landeiro VL, Bini LM (2012) Spatial autocorrelation analysis allows disentangling the balance between neutral and niche processes in metacommunities. Oikos 121:201–210
Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20
Dray S, Dufour AB, Chessel D (2007) The ade4 package-II: two-table and k-table methods. R News 7:47–52
Dray S, Legendre P, Blanchet FG (2007b) Packfor: forward selection with permutation (Canoco p.46), R package version 0.0 - 8. Software retrieved from http://R-Forge.R-project.org/projects/sedar/
Duarte LDS, Prieto PV, Pillar VD (2012) Assessing spatial and environmental drivers of phylogenetic structure in Brazilian Araucaria forests. Ecography 35:952–960
Hansen PJ, Bjørnsen PK, Hansen BW (1997) Zooplankton grazing and growth: scaling within the 2–2000-µm body size range. Limnol Oceanogr 42:687–704
Heino J, Melo AS, Siqueira T, Soininen J, Valanko S, Bini LM (2015) Metacommunity organisation, spatial extent and dispersal in aquatic systems: patterns, processes and prospects. Freshwater Biol 60:845–869
HilleRisLambers J, Adler PB, Harpole WS, Levine JM, Mayfield MM (2012) Rethinking community assembly through the lens of coexistence theory. Annu Rev Ecol Evol Syst 43:227–248
Holyoak M, Leibold MA, Holt RD (2005) Metacommunities: spatial dynamics and ecological communities. University of Chicago Press, Chicago
Huang J, Yu H, Guan X, Wang G, Guo R (2016) Accelerated dryland expansion under climate change. Nature Clim Change 6:166–171
Hubbell SP (2001) A unified neutral theory of biodiversity and biogeography. Princeton University Press, Princeton
Huszar VLM, Silva LHS, Marinho M, Domingos P, Anna CLS (2000) Cyanoprokaryote assemblages in eight productive tropical Brazilian waters. Hydrobiologia 424:67–77
Huszar VLM, Nabout JC, Appel MO, Santos JBO, Abe DS, Silva LHS (2016) Environmental and not spatial processes (directional and non-directional) shape the phytoplankton composition and functional groups in a large subtropical river basin. J Plankton Res 37:1190–1200
Incagnone G, Marrone F, Barone R, Robba L, Naselli-Flores L (2015) How do freshwater organisms cross the “dry ocean”? A review on passive dispersal and colonization processes with a special focus on temporary ponds. Hydrobiologia 750:103–123
Jeppesen E, Brucet S, Naselli-Flores L et al (2015) Ecological impacts of global warming and water abstraction on lakes and reservoirs due to changes in water level and related changes in salinity. Hydrobiologia 750:201–227
Jespersen AM, Christoffersen K (1988) Measurements of chlorophyll-a from phytoplankton using ethanol as extraction solvent. Arch Hydrobiol 109:445–454
Klamt A-M, Hu K, Huang L, Chen X, Liu X, Chen G (2020) An extreme drought event homogenises the diatom composition of two shallow lakes in southwest China. Ecol Indic. https://doi.org/10.1016/j.ecolind.2019.105662
Laliberté E, Paquette A, Legendre P, Bouchard A (2009) Assessing the scale-specific importance of niches and other spatial processes on beta diversity: a case study from a temperate forest. Oecologia 159:377–388
Legendre P, Legendre L (2012) Numerical ecology. Elsevier, Amsterdam
Leibold MA, Holyoak M, Mouquet M, Amarasekare P, Chase JM, Hoopes MF, Holt RD, Gonzalez A (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett 7:601–613
Lins RPM, Ceballos BSO, Lopez LCS, Barbosa LG (2017) Phytoplankton functional groups in a tropical reservoir in the Brazilian semiarid region. Int J Trop Biol 65:1129–1141
Loverde-Oliveira SM, Huszar VLM, Mazzeo N, Scheffer M (2009) Hydrology-driven regime shifts in a shallow tropical lake. Ecosystems 12:807–819
Lund JWG, Kipling C, Lecren ED (1958) The inverted microscope method of estimating algae number and the statistical basis of estimating by counting. Hydrobiologia 11:143–170
Mackereth FJH, Heron J, Talling JF (1978) Water analysis: some revised methods for limnologists. Freshwater Biological Association, Cumbria
Marengo JA, Jones R, Alves LM, Valverde MC (2009) Future change of temperature and precipitation extremes in South America as derived from the PRECIS regional climate modeling system. Int J Climatol 29:2241–2255
Mazaris AD, Moustaka-Gouni M, Michaloudi E, Bobori DC (2010) Biogeographical patterns of freshwater micro- and macroorganisms: a comparison between phytoplankton, zooplankton and fish in the eastern Mediterranean. J Biogeogr 37:1341–1351
Medeiros LCM, Mattos A, Lürling M, Becker V (2015) Is the future blue-green or brown? The effects of extreme events on phytoplankton dynamics in a semi-arid manmade lake. Aquat Ecol 49:293–307
Morais-Junior CS, Melo-Júnior M, Gonçalves-Souza T, Lyra-Neves RM (2019) Zoochory of zooplankton: seasonality and bird morphological diversity can influence metacommunity dynamics of temporary ponds. J Plankton Res 41:465–477
Naselli-Flores L, Termine R, Barone R (2005) Water-level fluctuations in Mediterranean reservoirs: setting a dewatering threshold as a management tool to improve water quality. Hydrobiologia 548:85–99
Naselli-Flores L, Termine R, Barone R (2016) Phytoplankton colonization patterns. Is species richness depending on distance among freshwaters and on their connectivity? Hydrobiologia 764:103–113
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2019) vegan: Community Ecology Package. R package version 2.5-6. https://CRAN.R-project.org/package=vegan
Olmos F, Silva WAG, Albano CG (2005) Aves em oito áreas de caatinga no sul do Ceará e oeste de Pernambuco, nordeste do Brasil: composição, riqueza e similaridade. Pap Avulsos Zool 45:179–199
Padial A, Ceschin F, Declerck SAJ (2014) Dispersal ability determines the role of environmental, spatial and temporal drivers of metacommunity structure. PLoS ONE 9:e111227
Padisák J, Scheffler W, Kasprzak P, Koschel R, Krienitz L (2003) Interannual variability in the phytoplankton composition of Lake Stechlin (1994–2000). Arch Hydrobiol Spec Issues Adv Limnol 58:101–133
Pereira GA (2010) Avifauna associada a três lagoas temporárias no estado do Rio Grande do Norte, Brasil. Atual Ornitol 156:53–60
Peres-Neto PR, Legendre P, Dray S, Borcard D (2006) Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87:2614–2625
R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 2 Nov 2019
Reynolds CS (2006) Ecology of phytoplankton. Cambridge University Press, Cambridge
Rojo C, Álvarez-Cobelas M, Benavent-Corai J, Barón-Rodriguez MM, Rodrigo M (2012) Trade-offs in plankton species richness arising from drought: insights from long-term data of a National Park wetland (central Spain). Biodivers Conserv 21:2453–2476
Rojo C, Mesquita-Joanes F, Monrós JS, Armengol J, Sasa M, Bonilla F et al (2016) Hydrology affects environmental and spatial structuring of microalgal metacommunities in tropical Pacific Coast wetlands. PLoS ONE 11:e0149505. https://doi.org/10.1371/journal.pone.0149505
Santos JBO, Silva LHS, Branco CWC, Huszar VLM (2016) The roles of environmental conditions and geographical distances on the species turnover of the whole phytoplankton and zooplankton communities and their subsets in tropical reservoirs. Hydrobiologia 764:171–186
Shurin JB, Cottenie K, Hillebrand H (2009) Spatial autocorrelation and dispersal limitation in freshwater organisms. Oecologia 159:151–159
Sieburth JMN, Smetacek V, Lenz J (1978) Pelagic ecosystem structure: heterotrophic compartments of the plankton and their relationship to plankton size fractions. Limnol Oceanogr 23:1256–1263
Silva JMC, Leal IR, Tabarelli M (2018) Caatinga: the largest tropical dry forest region in South America. Springer, New York
Simões NR, Lansac-Tôha FA, Bonecker CC (2013) Drought disturbances increase temporal variability of zooplankton community structure in floodplains. Int Rev Hydrobiol 98:24–33
Soininen J, Korhonen JJ, Karhu J, Vetterli A (2011) Disentangling the spatial patterns in community composition of prokaryotic and eukaryotic lake plankton. Limnol Oceanogr 56:508–520
Souffreau C, Van der Gucht K, van Gremberghe I (2015) Environmental rather than spatial factors structure bacterioplankton communities in shallow lakes along a %3e 6000 km latitudinal gradient in South America. Environ Microbiol 17:2336–2351
Sousa AEBA, Lima DM, Lyra-Neves RM (2012) Avifauna of the Catimbau National Park in the brazilian state of Pernambuco, Brazil: species richness and spatio-temporal variation. Rev Bras Ornitol 20:230–245
Thomaz SM, Bini LM, Bozelli RL (2007) Floods increase similarity among aquatic habitats in river-floodplain systems. Hydrobiologia 579:1–13
Uehlinger V (1964) Étude statistique des méthodes de dénobrement planctonique. Arch Sci 77:121–123
Utermöhl H (1958) Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Mitt Int Ver Theor Angew Limnol 9:1–38
Vanschoenwinkel B, Waterkeyn A, Vandecaetsbeek T, Pineau O, Grillas P, Brendonck L (2008) Dispersal of freshwater invertebrates by large terrestrial mammals: a case study with wild boar (Sus scrofa) in Mediterranean wetlands. Freshwater Biol 53:2264–2273
Wetzel RG, Likens GE (2000) Limnological analyses, Book 3. Springer, New York
Wetzel CE, Bicudo DC, Ector L, Lobo EA, Soininen J, Landeiro VL, Bini LM (2012) Distance decay of similarity in neotropical diatom communities. PLoS ONE 7:e45071
Winegardner AK, Jones BK, Ng ISY, Siqueira T, Cottenie K (2012) The terminology of metacommunity ecology. Trends Ecol Evol 27:253–254
Acknowledgements
We want to thank the staff of the Secretaria Estadual do Meio Ambiente e dos Recursos Hídricos do Rio Grande do Norte (SEMARH), especially Celso Veiga, Gláucia Costa, Maria Gorete Pereira, Selma Silva, Antônio Paiva, Josenilton Silva, and Fernando Silva for their logistical assistance during the sampling work and for providing lake data. Special thanks go to Francisco Vasconcelos and Danyhelton Dantas for field and laboratory assistance and to Fábio Roland for his enormous contribution with nutrient analyses. We thank João Nabout and Letícia Quesado for help with R statistics and Dr. Janet W. Reid (JWR Associates) for English editing and helpful comments. JB and RFM were supported by the Coordination for the Improvement of Higher Educational Personnel (CAPES/PNPD; Project No. 2304/2011). VLMH was partially supported by the National Council for Scientific and Technological Development (CNPq; Grant 304284/2017-3). We also acknowledge Dr. Télesphore Sime-Ngando and the two anonymous reviewers for providing valuable comments and suggestions to improve our manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Handling Editor: Télesphore Sime-Ngando.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Brasil, J., Santos, J.B.O., Sousa, W. et al. Rainfall leads to habitat homogenization and facilitates plankton dispersal in tropical semiarid lakes. Aquat Ecol 54, 225–241 (2020). https://doi.org/10.1007/s10452-019-09738-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10452-019-09738-9