Abstract
Disentangling the mechanisms that maintain the stability of communities and ecosystem properties has become a major research focus in ecology in the face of anthropogenic environmental change. Dispersal plays a pivotal role in maintaining diversity in spatially subdivided communities, but only a few experiments have simultaneously investigated how dispersal and environmental fluctuation affect community dynamics and ecosystem stability. We performed an experimental study using marine phytoplankton species as model organisms to test these mechanisms in a metacommunity context. We established three levels of dispersal and exposed the phytoplankton to fluctuating light levels, where fluctuations were either spatially asynchronous or synchronous across patches of the metacommunity. Dispersal had no effect on diversity and ecosystem function (biomass), while light fluctuations affected both evenness and community biomass. The temporal variability of community biomass was reduced by fluctuating light and temporal beta diversity was influenced interactively by dispersal and fluctuation, whereas spatial variability in community biomass and beta diversity were barely affected by treatments. Along the establishing gradient of species richness and dominance, community biomass increased but temporal variability of biomass decreased, thus highest stability was associated with species-rich but highly uneven communities and less influenced by compensatory dynamics. In conclusion, both specific traits (dominance) and diversity (richness) affected the stability of metacommunities under fluctuating conditions.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abrams P (1984) Variability in resource consumption rates and the coexistence of competing species. Theor Popul Biol 25:106–124. doi:10.1016/0040-5809(84)90008
Bai Y, Han X, Wu J, Chen Z, Li L (2004) Ecosystem stability and compensatory effects in the Inner Mongolia grassland. Nature 431:181–184. doi:10.1038/nature02850
Bouvier T, Venail P, Pommier T, Bouvier C, Barbera C, Mouquet N (2012) Contrasted effects of diversity and immigration on ecological insurance in marine bacterioplankton communities. PLoS ONE 7:e37620. doi:10.1371/journal.pone.0037620
Cadotte MW, Dinnage R, Tilman D (2012) Phylogenetic diversity promotes ecosystem stability. Ecology 93:223–233. doi:10.1890/11-0426.1
Chesson P (1994) Multispecies competition in variable environments. Theor Popul Biol 45:227–276. doi:10.1006/tpbi.1994.1013
Chesson P (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31:343–366. doi:10.1146/annurev.ecolsys.31.1.343
Chesson P, Warner R (1981) Environmental variability promotes coexistence in lottery competitive systems. Am Nat 117:923–943. doi:10.1086/283778
Descamps-Julien B, Gonzalez A (2005) Stable coexistence in a fluctuating environment: an experimental demonstration. Ecology 86:2815–2824. doi:10.1890/04-1700
Downing AL, Brown BL, Perrin EM, Keitt TH, Leibold MA (2008) Environmental fluctuations induce scale-dependent compensation and increase stability in plankton ecosystems. Ecology 89:3204–3214. doi:10.1890/07-1652.1
Ebenhöh W (1988) Coexistence of an unlimited number of algal species in a model system. Theor Popul Biol 34:130–144. doi:10.1016/0040-5809(88)90038
Eddison J, Ollason J (1978) Diversity in constant and fluctuating environments. Nature 275:309–310. doi:10.1038/275309a0
Eggers SL, Eriksson BK, Matthiessen B (2012) A heat wave and dispersal cause dominance shift and decrease biomass in experimental metacommunities. Oikos 121:721–733. doi:10.1111/j.1600-0706.2011.19714.x
Fischer J, Frost T, Ives A (2001) Compensatory dynamics in zooplankton community responses to acidification: measurement and mechanisms. Ecol Appl 11:1060–1072. doi:10.1890/1051-0761(2001)011[1060:CDIZCR]2.0.CO;2
Flöder S, Burns CW (2005) The influence of fluctuating light on diversity and species number of nutrient-limited phytoplankton. J Phycol 41:950–956. doi:10.1111/j.1529-8817.2005.00124.x
Flöder S, Hillebrand H (2012) Species traits and species diversity affect community stability in a multiple stressor framework. Aquat Biol 17:197–209. doi:10.3354/ab00479
Flöder S, Urabe J, Kawabata Z (2002) The influence of fluctuating light intensities on species composition and diversity of natural phytoplankton communities. Oecologia 133:395–401. doi:10.1007/s00442-002-1048-8
Gaston KJ, McArdle BH (1994) The temporal variability of animal abundances: measures, methods and patterns. Philos Trans R Soc B Biol Sci 345:335–358. doi:10.1098/rstb.1994.0114
Gervais F (1997) Diel vertical migration of Cryptomonas and Chromatium in the deep chlorophyll maximum of a eutrophic lake. J Plankton Res 19:533–550. doi:10.1093/plankt/19.5.533
Gonzalez A, Descamps-Julien B (2004) Population and community variability in randomly fluctuating environments. Oikos 106:105–116. doi:10.1111/j.0030-1299.2004.12925.x
Gonzalez A, Loreau M (2009) The causes and consequences of compensatory dynamics in ecological communities. Annu Rev Ecol Evol Syst 40:393–414. doi:10.1146/annurev.ecolsys.39.110707.173349
Gouhier TC, Guichard F, Gonzalez A (2010) Synchrony and stability of food webs in metacommunities. Am Nat 175:E16–E34. doi:10.1086/649579
Grover J (1988) Dynamics of competition in a variable environment: experiments with two diatom species. Ecology 69:408–417. doi:10.2307/1940439
Grover JP (1991) Dynamics of competition among microalgae in variable environments: experimental tests of alternative models. Oikos 62:231–243. doi:10.2307/3545269
Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. Can J Microbiol 8:229–239. doi:10.1139/m62-029
Hammer A, Schumann R, Schubert H (2002) Light and temperature acclimation of Rhodomonas salina (Cryptophyceae): photosynthetic performance. Aquat Microb Ecol 29:287–296. doi:10.3354/ame029287
Hardin G (1960) The competitive exclusion principle. Science 131:1292–1297. doi:10.1126/science.131.3409.1292
Hector A, Hautier Y, Saner P, Wacker L, Bagchi R, Joshi J, Scherer-Lorenzen M, Spehn EM, Bazeley-White E, Weilenmann M, Caldeira MC, Dimitrakopoulos PG, Finn JA, Huss-Danell K, Jumpponen A, Mulder CPH, Palmborg C, Pereira JS, Siamantziouras ASD, Terry AC, Troumbis AY, Schmid B, Loreau M (2010) General stabilizing effects of plant diversity on grassland productivity through population asynchrony and overyielding. Ecology 91:2213–2220. doi:10.1890/09-1162
Hillebrand H, Lehmpfuhl V (2011) Resource stoichiometry and consumers control the biodiversity-productivity relationship in pelagic metacommunities. Am Nat 178:171–181. doi:10.1086/660831
Hillebrand H, Dürselen CD, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424. doi:10.1046/j.1529-8817.1999.3520403.x
Hillebrand H, Bennett DM, Cadotte MW (2008) Consequences of dominance: a review of evenness effects on local and regional ecosystem processes. Ecology 89:1510–1520. doi:10.1890/07-1053.1
Hillebrand H, Burgmer T, Biermann E (2012) Running to stand still: temperature effects on species richness, species turnover, and functional community dynamics. Mar Biol 159:2415–2422. doi:10.1007/s00227-011-1827-z
Holyoak M, Lawler SP (1996) Persistence of an extinction-prone predator–prey interaction through metapopulation dynamics. Ecology 77:1867–1879. doi:10.2307/2265790
Holyoak M, Leibold MA, Holt RD (2005) Metacommunities: Spatial dynamics and ecological communities. University of Chicago Press, Chicago
Houlahan JE, Currie DJ, Cottenie K, Cumming GS, Ernest SKM, Findlay CS, Fuhlendorf SD, Gaedke U, Legendre P, Magnuson JJ, McArdle BH, Muldavin EH, Noble D, Russell R, Stevens RD, Willis TJ, Woiwod IP, Wondzell SM (2007) Compensatory dynamics are rare in natural. Proc Natl Acad Sci USA 104:3273–3277. doi:10.1073/pnas.0603798104
Howeth JG, Leibold MA (2010) Species dispersal rates alter diversity and ecosystem stability in pond metacommunities. Ecology 91:2727–2741. doi:10.1890/09-1004.1
Hutchinson GE (1961) The paradox of the plankton. Am Nat 95:137–145. doi:10.1086/282171
Ives AR, Carpenter SR (2007) Stability and diversity of ecosystems. Science 317:58–62. doi:10.1126/Science.1133258
Ives AR, Gross K, Klug J (1999) Stability and variability in competitive communities. Science 286:542–544. doi:10.1126/science.286.5439.542
Kendall BE, Bjørnstad J, Bascompte J, Keitt TH, Fagan WF (2000) Dispersal, environmental correlation, and spatial synchrony in population dynamics. Am Nat 155:628–636. doi:10.1086/303350
Klug J, Fischer J, Ives A, Dennis B (2000) Compensatory dynamics in planktonic community responses to pH perurbations. Ecology 81:387–398. doi:10.2307/177435
Koelle K, Vandermeer J (2005) Dispersal-induced desynchronization: from metapopulations to metacommunities. Ecol Lett 8:167–175. doi:10.1111/J.1461-0248.2004.00703.X
Lehman CL, Tilman D (2000) Biodiversity, stability, and productivity in competitive communities. Am Nat 156:534–552. doi:10.1086/303402
Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM, Hoopes MF, Holt RD, Shurin JB, Law R, Tilman D, Loreau M, Gonzalez A (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett 7:601–613. doi:10.1111/J.1461-0248.2004.00608.X
Levins R (1979) Coexistence in a variable environment. Am Nat 114:765–783. doi:10.1086/283527
Lewontin RC, Cohen D (1969) On population growth in a randomly varying environment. Proc Natl Acad Sci USA 62:1056–1060. doi:10.1073/pnas.62.4.1056
Liebhold A, Koenig W, Bjørnstad O (2004) Spatial synchrony in population dynamics. Annu Rev Ecol Evol Syst 35:467–490. doi:10.1146/annurev.ecolsys.34.011802.132516
Litchman E (1998) Population and community responses of phytoplankton to fluctuating light. Oecologia 117:247–257. doi:10.1007/s004420050655
Litchman E (2000) Growth rates of phytoplankton under fluctuating light. Freshw Biol 44:223–235. doi:10.1046/j.1365-2427.2000.00559.x
Litchman E, Klausmeier CA (2001) Competition of phytoplankton under fluctuating light. Am Nat 157:170–187. doi:10.1086/318628
Logue JB, Mouquet N, Peter H, Hillebrand H (2011) Grp MW (2011) Empirical approaches to metacommunities: a review and comparison with theory. Trends Ecol Evol 26:482–491. doi:10.1016/J.Tree.04.009
Loreau M, de Mazancourt C (2008) Species synchrony and its drivers: neutral and nonneutral community dynamics in fluctuating environments. Am Nat 172:E48–E66. doi:10.1086/589746
Loreau M, Mouquet N (1999) Immigration and the maintenance of local species diversity. Am Nat 154:427–440. doi:10.1086/303252
Loreau M, Mouquet N, Gonzalez A (2003) Biodiversity as spatial insurance in heterogeneous landscapes. Proc Natl Acad Sci USA 100:12765–12770. doi:10.1073/Pnas.2235465100
Matthiessen B, Hillebrand H (2006) Dispersal frequency affects local biomass production by controlling local diversity. Ecol Lett 9:652–662. doi:10.1111/j.1461-0248.2006.00916.x
Matthiessen B, Mielke E, Sommer U (2010) Dispersal decreases diversity in heterogeneous metacommunities by enhancing regional competition. Ecology 91:2022–2033. doi:10.1890/09-1395.1
McArdle B, Gaston K, Lawton J (1990) Variation in the size of animal populations: patterns, problems and artefacts. J Anim Ecol 59:439–454. doi:10.2307/4873
McNaughton SJ (1977) Diversity and stability of ecological communities: a comment on the role of empiricism in ecology. Am Nat 111:515–525. doi:10.1086/283181
Mouquet N, Loreau M (2002) Coexistence in metacommunities: the regional similarity hypothesis. Am Nat 159:420–426. doi:10.1086/338996
Naeem S, Li SB (1997) Biodiversity enhances ecosystem reliability. Nature 390:507–509. doi:10.1038/37348
Norberg J, Swaney DP, Dushoff J, Lin J, Casagrandi R, Levin SA (2001) Phenotypic diversity and ecosystem functioning in changing environments: a theoretical framework. Proc Natl Acad Sci USA 98:11376–11381. doi:10.1073/pnas.171315998
Oksanen J, Guillaume Blanchet F, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2012) vegan: Community Ecology Package
Olenina I, Hajdu S, Edler L, Andersson A, Wasmund N, Busch S, Göbel J, Gromisz S, Huseby S, Huttunen M, Jaanus A, Kokkonen P, Ledaine I, Niemkiewicz E (2006) Biovolumes and size-classes of phytoplankton in the Baltic Sea. Helsinki
Petchey OL, Casey T, Jiang L, McPhearson PT, Price J (2002) Species richness, environmental fluctuations, and temporal change in total community biomass. Oikos 99:231–240. doi:10.1034/j.1600-0706.2002.990203.x
R Development Core Team R (2011) R: language and environment for statistical computing
Ranta E, Kaitala V, Fowler MS, Laakso J, Ruokolainen L, O’Hara R (2008) Detecting compensatory dynamics in competitive communities under environmental forcing. Oikos 117:1907–1911. doi:10.1111/J.1600-0706.2008.16614.X
Robinson DH, Arrigo KR, Iturriaga R, Sullivan CW (1995) Microalgal light-harvesting in extreme low-light environments in McMurdo Sound, Antarctica. J Phycol 31:508–520. doi:10.1111/j.1529-8817.1995.tb02544.x
Romanuk TN, Kolasa J (2002) Environmental variability alters the relationship between richness and variability of community abundances in aquatic rock pool microcosms. Ecoscience 9:55–62
Roscher C, Weigelt A, Proulx R, Marquard E, Schumacher J, Weisser WW, Schmid B (2011) Identifying population- and community-level mechanisms of diversity-stability relationships in experimental grasslands. J Ecol 96:1460–1469. doi:10.1111/j.1365-2745.2011.01875.x
Shurin JB, Winder M, Adrian R, Keller WB, Matthews B, Paterson AM, Paterson MJ, Pinel-Alloul B, Rusak JA, Yan ND (2010) Environmental stability and lake zooplankton diversity - contrasting effects of chemical and thermal variability. Ecol Lett 13:453–463. doi:10.1111/j.1461-0248.2009.01438.x
Sommer U (1984) The paradox of the plankton: fluctuations of phosphorus availability maintain diversity of phytoplankton in flow-through cultures. Limnol Oceanogr 29:633–636. doi:10.4319/lo.1984.29.3.0633
Sommer U (1985) Comparison between steady state and non-steady state competition: experiments with natural phytoplankton. Limnol Oceanogr 30:335–346. doi:10.4319/lo.1985.30.2.0335
Steiner CF, Stockwell RD, Kalaimani V, Aqel Z (2011) Dispersal promotes compensatory dynamics and stability in forced metacommunities. Am Nat 178:159–170. doi:10.1086/660835
Tilman D (1996) Biodiversity: population versus ecosystem stability. Ecology 77:350–363. doi:10.2307/2265614
Tilman D (1999) The ecological consequences of changes in biodiversity: a search for general principles. Ecology 80:1455–1474. doi:10.2307/176540
Tilman D, Naeem S, Knops J, Reich P, Siemann E, Wedin D, Ritchie M, Lawton J (1997) Biodiversity and ecosystem properties. Science 278:1866–1867. doi:10.1126/science.278.5345.1865c
Weissing FJ, Huisman J (1994) Growth and competition in a light gradient. J Theor Biol 168:323–336. doi:10.1006/jtbi.1994.1113
Wickham H (2009) ggplot2: elegant graphics for data analysis In:(R Gentleman, K Hornik, G Parmigiani, eds.). Springer, New York
Yachi S, Loreau M (1999) Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc Natl Acad Sci USA 96:1463–1468. doi:10.1073/pnas.96.4.1463
Acknowledgments
We thank Robert Ptacnik, Stefanie Moorthi, Elena Litchman and two anonymous reviewers for fruitful comments improving the quality of the manuscript as well as Jan Freund for his help in data analysis. Katherina Schoo is heartily thanked for proof reading. We would also like to thank Patrick Neumann and Encarnacion Nunez for their help during the experimental phase. This study was financially supported by the German Research Foundation (DFG, contract Hi 848/8-1).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Elena Litchman.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Guelzow, N., Dirks, M. & Hillebrand, H. Effect of (a)synchronous light fluctuation on diversity, functional and structural stability of a marine phytoplankton metacommunity. Oecologia 176, 497–510 (2014). https://doi.org/10.1007/s00442-014-3015-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-014-3015-6