Abstract
After much discussion about the cosmopolitan nature of microbes, the great issue nowadays is to identify at which spatial extent microorganisms may display biogeographic patterns and if temporal variation is important in altering those patterns. Here, planktonic ciliates were sampled from shallow lakes of four Neotropical floodplains, distributed over a spatial extent of ca. 3000 km, during high and low water periods, along with several abiotic and biotic variables potentially affecting the ciliate community. We found that common ciliate species were more associated with environmental gradients and rare species were more related to spatial variables; however, this pattern seemed to change depending on the temporal and spatial scales considered. Environmental gradients were more important in the high waters for both common and rare species. In low waters, common species continued to be mainly driven by environmental conditions, but rare species were more associated with the spatial component, suggesting dispersal limitation likely due to differences in dispersal ability and ecological tolerance of species. We also found that common and rare species were related to different environmental variables, suggesting different ecological niches. At the largest spatial extents, rare species showed clear biogeographic patterns.
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Hutchinson GE (1957) Concluding remarks. Population studies. Anim Ecol Demogr 22:415–427
Chase JM, Leibold MA (2003) Ecological niches: linking classical and contemporary approaches. University of Chicago Press, Chicago
Kuang JL, Huang LN, Chen LX, Hua ZS, Li SJ, Hu M, et al (2013) Contemporary environmental variation determines microbial diversity patterns in acid mine drainage. ISME J 7:1038–1050
Ortmann AC, Ortell N (2014) Changes in free-living bacterial community diversity reflect the magnitude of environmental variability. FEMS Microbiol Ecol 87:291–301
Pinel-Alloul B, Ghadouani A (2007) Spatial heterogeneity of planktonic microorganisms in aquatic systems. In: Franklin RB, Mills AL (eds) The spatial distribution of microbes in the environment. Springer, New York, pp. 203–310
Souffreau C, Van der Gucht K, Gremberghe I, Kosten S, Lacerot G, Lobão LM, et al (2015) Environmental rather than spatial factors structure bacterioplankton communities in shallow lakes along a> 6000 km latitudinal gradient in South America. Environ Microbiol 17:2336–2351
Baas Becking LGM (1934) Geobiologie of inleiding tot de milieukunde. WP Van Stockum & Zoon, Hague
De Wit R, Bouvier T (2006) ‘Everything is everywhere, but, the environment selects’; what did Baas Becking and Beijerinck really say? Environ Microbiol 8:755–758
Finlay BJ (2002) Global dispersal of free-living microbial eukaryote species. Science 296:1061–1063
Fenchel T, Finlay BJ (2004) The ubiquity of small species: patterns of local and global diversity. Bioscience 54:777–784
Beisner BE, Peres-Neto PR, Lindström 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
De Bie T, Meester L, Brendonck L, Martens K, Goddeeris B, Ercken D, et al (2012) Body size and dispersal mode as key traits determining metacommunity structure of aquatic organisms. Ecol Lett 15:740–747
Whitaker RJ, Grogan DW, Taylor JW (2003) Geographic barriers isolate endemic populations of hyperthermophilic archaea. Science 301:976–978
Lepère C, Domaizon I, Taïb N, Mangot JF, Bronner G, Boucher D, Debroas D (2013) Geographic distance and ecosystem size determine the distribution of smallest protists in lacustrine ecosystems. FEMS Microbiol Ecol 85:85–94
Green JL, Green JL, Holmes AJ, Westoby M, Oliver I, Briscoe D, et al (2004) Spatial scaling of microbial eukaryote diversity. Nature 432:747–750
Green J, Bohannan BJ (2006) Spatial scaling of microbial biodiversity. Trends Ecol Evol 21:501–507
Martiny JBH, Bohannan BJ, Brown JH, Colwell RK, Fuhrman JA, Green JL, et al (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112
Chase JM, Myers JA (2011) Disentangling the importance of ecological niches from stochastic processes across scales. Phil Trans R Soc B 366:2351–2363
Martiny JB, Eisen JA, Penn K, Allison SD, Horner-Devine MC (2011) Drivers of bacterial β-diversity depend on spatial scale. Proc Natl Acad Sci 108:7850–7854
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. Freshw Biol 60:845–869
Langenheder S, Berga M, Östman O, Székely AJ (2012) Temporal variation of b-diversity and assembly mechanisms in a bacterial metacommunity. ISME J 6:1107–1114
Bulit C, Diaz-Avalos C, Montagnes DJS (2009) Scaling patterns of plankton diversity: a study of ciliates in a tropical coastal lagoon. Hydrobiologia 624:29–44
Chase JM (2007) Drought mediates the importance of stochastic community assembly. Proc Natl Acad Sci U S A 104:17430–17434
Thomaz SM, Bini LM, Bozelli RL (2007) Floods increase similarity among aquatic habitats in river-floodplain systems. Hydrobiologia 579:1–13
Lindström ES, Langenheder S (2012) Local and regional factors influencing bacterial community assembly. Environ Microbiol Rep 4:1–9
Pandit SN, Kolasa J, Cottenie K (2009) Contrasts between habitat generalists and specialists: an empirical extension to the basic metacommunity framework. Ecology 90:2253–2262
Algarte VM, Rodrigues L, Landeiro VL, Siqueira T, Bini LM (2014) Variance partitioning of deconstructed periphyton communities: does the use of biological traits matter? Hydrobiologia 722:279–290
Székely AJ, Langenheder S (2014) The importance of species sorting differs between habitat generalists and specialists in bacterial communities. FEMS Microbiol Ecol 87:102–112
Petsch DK, Pinha GD, Dias JD, Takeda AM (2015) Temporal nestedness in Chironomidae and the importance of environmental and spatial factors in species rarity. Hydrobiologia 745:181–193
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
Magurran AE, Henderson PA (2003) Explaining the excess of rare species in natural species abundance distributions. Nature 422:714–716
Dolan JR, Ritchie ME, Tunin-Ley A, Pizay M (2009) Dynamics of core and occasional species in the marine plankton: tintinnid ciliates in the north-west Mediterranean Sea. J Biogeogr 36:887–895
Siqueira T, Bini LM, Roque FO, Marques Couceiro SR, Trivinho-Strixino S, Cottenie K (2012) Common and rare species respond to similar niche processes in macroinvertebrate metacommunities. Ecography 35:183–192
Chase JM, Amarasekare P, Cottenie K, Gonzalez A, Holt RD, Holyoak M, et al (2005) Competing theories for competitive metacommunities. In: Holyoak M et al. (eds) Metacommunities. Spatial dynamics and ecological communities. University of Chicago Press, Chicago, pp. 335–354
Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM, Hoopes MF, et al (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett 7:601–613
Boulangeat I, Gravel D, Thuiller W (2012) Accounting for dispersal and biotic interactions to disentangle the drivers of species distributions and their abundances. Ecol Lett 15:584–593
Soininen J, Korhonen JJ, Luoto M (2013) Stochastic species distributions are driven by organism size. Ecology 94:660–670
Berga M, Östman Ö, Lindström ES, Langenheder S (2015) Combined effects of zooplankton grazing and dispersal on the diversity and assembly mechanisms of bacterial metacommunities. Environ Microbiol 17:2275–2287
Madoni P (1984) Estimation of the size of freshwater ciliate populations by a sub-sampling technique. Hydrobiologia 111:201–206
Foissner W, Berger H, Kohmann F (1992) Taxonomische und ökologische Revision der Ciliaten des Saprobiensystems. Band II: Peritrichia, Heterotrichida, Odontostomatida. Informationsberichte des Bayerischen Landesamtes für Wasserwirtschaft, München
Foissner W, Berger H, Kohmann F (1994) Taxonomische und ökologische Revision der Ciliaten des Saprobiensystems. Band III: Hymenostomata, Prostomatida, Nassulida. Informationsberichte des Bayerischen Landesamtes für Wasserwirtschaf, München
Foissner W, Berger H, Blatterer H, Kohmann F (1995) Taxonomische und ökologische Revision der Ciliaten des Saprobiensystems. Band IV: Gymnostomatea, Loxodes, Suctoria. Informationsberichte des Bayerischen Landesamtes für Wasserwirtschaft, München
Foissner W, Berger H (1996) A user friendly guide to the ciliates (Protozoa, Ciliophora) commonly used by hydrobiologists as bioindicators in rivers, lakes, and waste waters, with notes on their ecology. Freshw Biol 35:375–482
Berger H (1999) Monograph of the Oxytrichidae (Ciliophora, Hypotrichia). Monographiae Biologicae, 78. Kluwer Academic Publishers, Dordrecht
Foissner W, Berger H, Schaumburg J (1999) Identification and ecology of limnetic plankton ciliates. Bavarian State Office for Water Management, Munich
Foissner W, Agatha S, Berger H (2002) Soil ciliates (Protozoa, Ciliophora) from Namibia (Southwest Africa), with emphasis on two contrasting environments, the Etosha Region and the Namib Desert. Denisia 5, Biologiezentrum der Oberösterreichischen, Linz
Sherr EB, Sherr BF (1993) Preservation and storage of samples for enumeration of heterotrophic protists. In: Kemp P, Sherr BF, Sherr EB, Cole J (eds) Current methods in aquatic microbial ecology. Lewis Publishers, Boca Raton, pp. 207–212
Porter KG, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948
Golterman HL, Clymo RS, Ohmstad MAM (1978) Methods for physical and chemical analysis of fresh water. Blackwell Scientific, Oxford
Bottrell HH, Duncan A, Gliwicz ZM, Grygierek E, Herzig A, Hillbricht-Ilkowska A, et al (1976) A review of some problems in zooplankton production studies. Norw J Zool 24:419–456
Mackereth FYH, Heron J, Talling JJ (1978) Water analysis: some revised methods for limnologists. Freshwater Biol Assoc 36:1–120
Giné MF, Zagatto EAG, Reis BF (1980) Simultaneous determination of nitrate and nitrite by flow injection analysis. Anal Chim Acta 114:191–197
Gaston KJ (1994) Rarity. Chapman and Hall, London, London
Magurran AE (2004) Measuring biological diversity. Blackwell Science, Oxford
Legendre P, Legendre L (2012) Numerical Ecology. Elsevier, Amsterdam
Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280
Borcard D, Gillet F, Legendre L (2011) Numerical ecology with R. Springer, New York
Blanchet FG, Legendre P, Borcard D (2008) Forward selection of explanatory variables. Ecology 89:2623–2632
Dray S, Legendre P, Peres-Neto PR (2006) Spatial modelling: a comprehensive framework for principal coordinate analysis of neighbour matrices (PCNM). Ecol Model 196:483–493
Borcard D, Legendre P, Avois-Jacquet C, Tuomisto H (2004) Dissecting the spatial structure of ecological data at multiple scales. Ecology 85:1826–1832
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
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
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB et al. (2015) Vegan: Community Ecology Package. R package version 2.2–1. http://CRAN.R-project.org/package=vegan
Legendre P, Borcard D, Blanchet FG, Dray S (2013) PCNM: MEM spatial eigenfunction and principal coordinate analyses. R package version 2.1–2/r109. http://R-Forge.R-project.org/projects/sedar
R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna URL http://www.R-project.org
Cottenie K, Michels E, Nuytten N, De Meester L (2003) Zooplankton metacommunity structure: regional vs. local processes in highly interconnected ponds. Ecology 84:991–1000
Van der Gucht K, Cottenie K, Muylaert K, Vloemans N, Cousin S, Declerck S, et al (2007) The power of species sorting: local factors drive bacterial community composition over a wide range of spatial scales. Proc Natl Acad Sci U S A 104:20404–20409
Vanormelingen P, Cottenie K, Michels E, Muylaert K, Vyverman WIM, De Meester L (2008) The relative importance of dispersal and local processes in structuring phytoplankton communities in a set of highly interconnected ponds. Freshw Biol 53:2170–2183
Adams HE, Crump BC, Kling GW (2014) Metacommunity dynamics of bacteria in an arctic lake: the impact of species sorting and mass effects on bacterial production and biogeography. Front Microbiol 5:1–10
Nolte V, Pandey RV, Jost S, Medinger R, Ottenwaelder B, Boenigk J, Schloetterer C (2010) Contrasting seasonal niche separation between rare and abundant taxa conceals the extent of protist diversity. Mol Ecol 19:2908–2915
Doherty M, Tamura M, Costas BA, Ritchie ME, McManus GB, Katz LA (2010) Ciliate diversity and distribution across an environmental and depth gradient in Long Island Sound, USA. Environ Microbiol 12:886–898
Declerck SAJ, Winter C, Shurin JB, Suttle CA, Matthews B (2013) Effects of patch connectivity and heterogeneity on metacommunity structure of planktonic bacteria and viruses. ISME J 7:533–542
Galand PE, Casamayor EO, Kirchman DL, Lovejoy C (2009) Ecology of the rare microbial biosphere of the Arctic Ocean. Proc Natl Acad Sci U S A 106:22427–22432
Logares R, Audic S, Bass D, Bittner L, Boutte C, Christen R, et al (2014) Patterns of rare and abundant marine microbial eukaryotes. Curr Biol 24:813–821
Dunthorn M, Stoeck T, Clamp J, Warren A, Mahé F (2014) Ciliates and the rare biosphere: a review. J Eukaryot Microbiol 61:404–409
Pedrós-Alió C (2006) Marine microbial diversity: can it be determined? Trends Microbiol 14:257–263
Gliwicz ZM (2004) Zooplankton. In: O’Sullivan PE, Reynolds CS (eds) The lakes handbook. Limnology and limnetic ecology. Blackwell Science, Oxford, pp. 461–516
Bini LM, Silva LCF, Velho LFM, Bonecker CC, Lansac-Tôha FA (2008) Zooplankton assemblage concordance patterns in Brazilian reservoirs. Hydrobiologia 598:247–255
Müller H, Geller W (1993) Maximum growth rates of aquatic ciliated protozoa: the dependence on body size and temperature reconsidered. Arch Hydrobiol 126:315–315
Boenigk J, Novarino G (2004) Effect of suspended clay on the feeding and growth of bacterivorous flagellates and ciliates. Aquat Microb Ecol 34:181–192
Küppers GC, Claps MC (2012) Spatiotemporal variations in abundance and biomass of planktonic ciliates related to environmental variables in a temporal pond, Argentina. Zool Stud 51:298–313
De Meester L (2011) A metacommunity perspective on the phylo- and biogeography of small organisms. In: Fontaneto D (ed) Biogeography of microscopic organisms: is everything small everywhere. Cambridge University Press, New York, pp. 324–334
Thompson RM, Townsend CR (2006) A truce with neutral theory: local deterministic factors, species traits and dispersal limitation together determine patterns of diversity in stream invertebrates. J Anim Ecol 75:476–484
Astorga A, Oksanen J, Luoto M, Soininen J, Virtanen R, Muotka T (2012) Distance decay of similarity in freshwater communities: do macro- and microorganisms follow the same rules? Glob Ecol Biogeogr 21:365–375
Padial AA, Ceschin F, Declerck SAJ, De Meester L, Bonecker CC, Lansac-Tôha FA, et al (2014) Dispersal ability determines the role of environmental, spatial and temporal drivers of Metacommunity structure. PLoS One 9:1–8
Heino J (2013) Does dispersal ability affect the relative importance of environmental control and spatial structuring of littoral macroinvertebrate communities? Oecologia 171:971–980
Hillebrand H, Watermann F, Karez R, Berninger UG (2001) Differences in species richness patterns between unicellular and multicellular organisms. Oecologia 126:114–124
Bates ST, Clemente JC, Flores GE, Walters WA, Parfrey LW, Knight R, Fierer N (2013) Global biogeography of highly diverse protistan communities in soil. ISME J 7:652–659
Vyverman W, Verleyen E, Sabbe K, Vanhoutte K, Sterken M, Hodgson DA, Flower R (2007) Historical processes constrain patterns in global diatom diversity. Ecology 88:1924–1931
Heino J, Bini LM, Karjalainen SM, Mykrä H, Soininen J, Vieira LCG, Diniz-Filho JAF (2010) Geographical patterns of micro-organismal community structure: are diatoms ubiquitously distributed across boreal streams? Oikos 119:129–137
Foissner W, Strüder-Kypke M, van der Staay GW, Moon-van der Staay SY, Hackstein JH (2003) Endemic ciliates (Protozoa, Ciliophora) from tank bromeliads (Bromeliaceae): a combined morphological, molecular, and ecological study. Eur J Protistol 39:365–372
Foissner W (2006) Biogeography and dispersal of micro-organisms: a review emphasizing protists. Acta Protozool 45:111–136
Wilkinson DM, Koumoutsaris S, Mitchell EAD, Bey I (2012) Modelling the effect of size on the aerial dispersal of microorganisms. J Biogeogr 39:89–97
Pace ML (1982) Planktonic ciliates: their distribution, abundance, and relationship to microbial resources in a monomictic lake. Can J Fish Aquat Sci 39:1106–1116
Weisse T (2008) Distribution and diversity of aquatic protists: an evolutionary and ecological perspective. Biodivers Conserv 17:243–259
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
Pither J (2007) Comment on" dispersal limitations matter for microbial Morphospecies". Science 316:1124–1124
Liu L, Yang J, Yu Z, Wilkinson DM (2015) The biogeography of abundant and rare bacterioplankton in the lakes and reservoirs of China. ISME J 9:2068–2077
Martin GK, Adamowicz SJ, Cottenie K (2016) Taxonomic resolution based on DNA barcoding affects environmental signal in metacommunity structure. Freshw Sci 35:701–711
Verleyen E, Vyverman W, Sterken M, Hodgson DA, De Wever A, Juggins S, et al (2009) The importance of dispersal related and local factors in shaping the taxonomic structure of diatom metacommunities. Oikos 118:1239–1249
Heino J, Soininen J (2007) Are higher taxa adequate surrogates for species-level assemblage patterns and species richness in stream organisms? Biol Conserv 137:78–89
Farjalla VF, Srivastava DS, Marino NAC, Azevedo FD, Dib V, Lopes PM, Rosado AS, Bozelli RL, Esteves FA (2012) Ecological determinism increases with organism size. Ecology 93:1752–1759
Andersson MGI, Berga M, Lindström ES, Langenheder S (2014) The spatial structure of bacterial communities is influenced by historical environmental conditions. Ecology 95:1134–1140
Acknowledgements
BTS is grateful for the funding and doctoral scholarship provided by the Coordination for the Improvement of Higher Education Personnel (CAPES). We would also like to thank the Brazilian National Council of Technological and Scientific Development (CNPq) for providing doctoral (BRM, FMLT) and post-doctoral scholarships (AFC, JDD), and research productivity scholarships and grants (FALT, LMB and LFMV). LFMV work was also supported by the Cesumar Institute of Science, Technology and Innovation (ICETI). We would also like to thank two anonymous reviewers for fruitful comments that helped improve the manuscript.
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Segovia, B.T., Dias, J.D., Cabral, A.F. et al. Common and Rare Taxa of Planktonic Ciliates: Influence of Flood Events and Biogeographic Patterns in Neotropical Floodplains. Microb Ecol 74, 522–533 (2017). https://doi.org/10.1007/s00248-017-0974-2
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DOI: https://doi.org/10.1007/s00248-017-0974-2