Advertisement

Aquatic Sciences

, 80:45 | Cite as

Interplay between productivity and regional species pool determines community assembly in aquatic microcosms

  • Cátia Lúcio Pereira
  • Miguel Bastos Araújo
  • Miguel Graça Matias
Research Article

Abstract

The relative importance of deterministic and neutral processes in shaping assembly of communities remains controversial, partly due to inconsistencies between theoretical, empirical, and experimental studies. We investigate the interplay between local (productivity) and regional (size of species pool) assembly mechanisms in communities of phytoplankton and zooplankton in 72 experimental microcosms. Local environmental conditions were manipulated by varying the level of nutrients in the water (ambient, low, high). The size of regional species pool colonizing each microcosm was manipulated by mixing phytoplankton and zooplankton species from different numbers of source ponds (n = 2, 4, 8 and 16). Our results show that local communities assembled differently depending on the numbers of sources available for colonization. Microcosms with larger species pools supported greater numbers of species. In contrast, the effects of productivity led to different results across trophic groups. Phytoplankton communities were, on average, more diverse on more productive treatments, while zooplankton communities were more diverse under less productive treatments. Phytoplankton and zooplankton communities responded to both sources of variation, although the size of species pool was a better predictor of communities’ composition than the local effects of productivity. These results reinforce the view that community assembly is influenced by the interplay of both local and regional drivers but that the relative importance of these factors varies with trophic groups.

Keywords

Deterministic processes Phytoplankton Stochastic processes Trophic group Zooplankton 

Notes

Acknowledgements

Research by CLP, MGM, and MBA was supported through the Integrated Program of IC&DT (1/SAESCTN/ALENT-07-0224-FEDER-001755). MGM acknowledges support by a Marie Curie Intra-European Fellowship within the 7th European Community Framework Programme (FORECOMM) and TrophicResponse-Trophic responses to macroecological gradients funded by FCT (PTDC/BIA-BIC/0352/2014). CLP acknowledges support by the Portuguese Science and Technology Foundation (FCT) through Ph.D. studentship (SFRH/BD/102020/2014). MBA acknowledges support by a Spanish Ministry of Economy and Competitiveness project (CGL2015-68438-P).

Author contributions

MGM designed the experiment; CLP and MGM performed the surveys, collected and processed samples; MGM, CLP and MBA conceived and performed the analysis of data; CLP, MGM and MBA wrote the first draft of the manuscript and contributed revisions to the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics

The surveys performed comply with the current laws of Spain.

References

  1. Altermatt F, Fronhofer EA, Garnier A, Giometto A, Hammes F, Klecka J, Legrand D, Mächler E, Massie TM, Pennekamp F, Plebani M, Pontarp M, Schtickzelle N, Thuillier V, Petchey OL (2015) Big answers from small worlds: a user’s guide for protist microcosms as a model system in ecology and evolution. Methods Ecol Evol 6:218–231.  https://doi.org/10.1111/2041-210X.12312 CrossRefGoogle Scholar
  2. Anderson MJ, Crist TO, Chase JM, Vellend M, Inouye BD, Freestone AL, Sanders NJ, Cornell HV, Comita LS, Davies KF, Harrison SP, Kraft NJB, Stegen JC, Swenson NG (2011) Navigating the multiple meanings of beta diversity: A roadmap for the practicing ecologist. Ecol Lett 14:19–28.  https://doi.org/10.1111/j.1461-0248.2010.01552.x CrossRefGoogle Scholar
  3. Barnett A, Beisner BE (2007) Zooplankton biodiversity and lake trophic state: explanations invoking resource abundance and distribution. Ecology 88:1675–1686.  https://doi.org/10.1890/06-1056.1 CrossRefGoogle Scholar
  4. Bergström A-K, Blomqvist P, Jansson M (2005) Effects of atmospheric nitrogen deposition on nutrient limitation and phytoplankton biomass in unproductive Swedish lakes. Limnol Oceanogr 50:987–994.  https://doi.org/10.4319/lo.2005.50.3.0987 CrossRefGoogle Scholar
  5. Cadotte MW (2006) Metacommunity influences on community richness at multiple spatial scales: a microcosm experiment. Ecology 87:1008–1016.  https://doi.org/10.1890/0012-9658(2006)87%5B1008:MIOCRA%5D2.0.CO;2 CrossRefPubMedGoogle Scholar
  6. Cadotte MW, Drake JA, Fukami T (2005) Constructing nature: laboratory models as necessary tools for investigating complex ecological communities. Adv Ecol Res 37:333–353.  https://doi.org/10.1016/S0065-2504(04)37011-X CrossRefGoogle Scholar
  7. Cañedo-Argüelles M, Boersma KS, Bogan MT, Olden JD, Phillipsen I, Schriever TA, Lytle DA (2015) Dispersal strength determines meta-community structure in a dendritic riverine network. J Biogeogr 42:778–790.  https://doi.org/10.1111/jbi.12457 CrossRefGoogle Scholar
  8. Carpenter SR (1996) Microcosm experiments have limited relevance for community and ecosystem. Ecology 77:677–680.  https://doi.org/10.2307/2265490 CrossRefGoogle Scholar
  9. Chase JM (2003) Community assembly: When should history matter? Oecologia 136:489–498.  https://doi.org/10.1007/s00442-003-1311-7 CrossRefGoogle Scholar
  10. Chase JM (2007) Drought mediates the importance of stochastic community assembly. Proc Natl Acad Sci USA 104:17430–17434.  https://doi.org/10.1073/pnas.0704350104 CrossRefPubMedGoogle Scholar
  11. Chase JM (2010) Stochastic community assembly causes higher biodiversity in more productive environments. Science 328:1388–1391.  https://doi.org/10.1126/science.1187820 CrossRefGoogle Scholar
  12. Chase JM, Leibold M (2002) Spatial scale dictates the productivity-biodiversity relationship. Nature 416:427–430.  https://doi.org/10.1038/416427a CrossRefPubMedGoogle Scholar
  13. Chase JM, Myers JA (2011) Disentangling the importance of ecological niches from stochastic processes across scales. Philos Trans R Soc B Biol Sci 366:2351–2363.  https://doi.org/10.1098/rstb.2011.0063 CrossRefGoogle Scholar
  14. Chase JM, Biro EG, Ryberg WA, Smith KG (2009) Predators temper the relative importance of stochastic processes in the assembly of prey metacommunities. Ecol Lett 12:1210–1218.  https://doi.org/10.1111/j.1461-0248.2009.01362.x CrossRefPubMedGoogle Scholar
  15. Chase JM, Kraft NJB, Smith KG, Vellend M, Inouye BD (2011) Using null models to disentangle variation in community dissimilarity from variation in α-diversity. Ecosphere 2:art24.  https://doi.org/10.1890/ES10-00117.1 CrossRefGoogle Scholar
  16. Cornell HV, Harrison SP (2014) What are species pools and when are they important? Annu Rev Ecol Evol Syst 45:45–67.  https://doi.org/10.1146/annurev-ecolsys-120213-091759 CrossRefGoogle Scholar
  17. Cottenie K (2005) Integrating environmental and spatial processes in ecological community dynamics. Ecol Lett 8:1175–1182.  https://doi.org/10.1111/j.1461-0248.2005.00820.x CrossRefGoogle Scholar
  18. Declerck S, Vanderstukken M, Pals A, Muylaert K, Meester LD (2007) Plankton biodiversity along a gradient of productivity and its mediation by macrophytes. Ecology 88:2199–2210.  https://doi.org/10.1890/07-0048.1 CrossRefPubMedGoogle Scholar
  19. Diamond J, Case TJ (1986) Community ecology. Harper and Row, New YorkGoogle Scholar
  20. Dodson SI, Arnott SE, Cottingham KL (2000) The relationship in lake communities between primary productivity and species richness. Ecology 81:2662–2679.  https://doi.org/10.1890/0012-9658(2000)081%5B2662:TRILCB%5D2.0.CO;2 CrossRefGoogle Scholar
  21. Ejrnæs R, Bruun HH, Graae BJ (2006) Community assembly in experimental grasslands: suitable environment or timely arrival? Ecology 87:1225–1233.  https://doi.org/10.1890/0012-9658(2006)87%5B1225:CAIEGS%5D2.0.CO;2 CrossRefPubMedGoogle Scholar
  22. Forbes AE, Chase JMN (2002) The role of habitat connectivity and landscape geometry in experimental zooplankton metacommunities. Oikos 96:433–440.  https://doi.org/10.1034/j.1600-0706.2002.960305.x CrossRefGoogle Scholar
  23. Fukami T (2004) Community assembly along a species pool gradient: implications for multiple-scale patterns of species diversity. Popul Ecol 46:137–147.  https://doi.org/10.1007/s10144-004-0182-z CrossRefGoogle Scholar
  24. Fukami T, Dickie IA, Paula Wilkie J et al (2010) Assembly history dictates ecosystem functioning: evidence from wood decomposer communities. Ecol Lett 13:675–684.  https://doi.org/10.1111/j.1461-0248.2010.01465.x CrossRefPubMedGoogle Scholar
  25. Gravel D, Canham CD, Beaudet M, Messier C (2006) Reconciling niche and neutrality: the continuum hypothesis. Ecol Lett 9:399–409.  https://doi.org/10.1111/j.1461-0248.2006.00884.x CrossRefPubMedGoogle Scholar
  26. Heino J, Grönroos M, Soininen J, Virtanen R, Muotka T (2012) Context dependency and metacommunity structuring in boreal headwater streams. Oikos 121:537–544.  https://doi.org/10.1111/j.1600-0706.2011.19715.x CrossRefGoogle Scholar
  27. Heino J, Melo AS, Siqueira T, Soininen J, Valanko S (2015a) Metacommunity organisation, spatial extent and dispersal in aquatic systems: patterns, processes and prospects. Freshwater Biol 60:845–869.  https://doi.org/10.1111/fwb.12533 CrossRefGoogle Scholar
  28. Heino J, Melo AS, Bini LM, Altermatt F, Al-Shami SA, Angeler DG, Bonada N, Brand C, Callisto M, Cottenie K, Dangles O, Dudgeon D, Encalada A, Göthe E, Grönroos M, Hamada N, Jacobsen D, Landeiro VL, Ligeiro R, Martins RT, Miserendino ML, Rawi CSM, Rodrigues ME, Roque FO, Sandin L, Schmera D, Sgarbi LF, Simaika JP, Siqueiro T, Thompson RM, Townsend CR (2015b) A comparative analysis reveals weak relationships between ecological factors and beta diversity of stream insect metacommunities at two spatial levels. Ecol Evol 5:1235–1248.  https://doi.org/10.1002/ece3.1439 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Hessen DO, Faafeng BA, Smith VH, Bakkestuen V, Walseng B (2006) Extrinsic and intrinsic controls of zooplankton diversity in lakes. Ecology 81:2662–2679.  https://doi.org/10.1890/05-0352 CrossRefGoogle Scholar
  30. Hill MJ, Heino J, Thornhill I, Ryves DB, Wood PJ (2017) Environmental of dispersal mode on the environmental and spatial correlates of nestedness and species turnover in pond communities. Oikos 126:1575–1585.  https://doi.org/10.1111/oik.04266 CrossRefGoogle Scholar
  31. Hillebrand H, Blenckner T (2002) Regional and local impact on speies diversity—from pattern to processes. Oecologia 132:479–491.  https://doi.org/10.1007/s00442-002-0988-3 CrossRefPubMedGoogle Scholar
  32. Hoffmann MD, Dodson SI (2005) Land use, primary productivity, and lake area as descriptors of zooplankton diversity. Ecology 86:255–261.  https://doi.org/10.1890/03-0833 CrossRefGoogle Scholar
  33. Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University Press, PrincetonGoogle Scholar
  34. Jessup CM, Kassen R, Forde SE, Kerr B, Buckling A, Rainey PB, Bohannan BJM (2004) Big questions, small worlds: Microbial model systems in ecology. Trends Ecol Evol 19:189–197.  https://doi.org/10.1016/j.tree.2004.01.008 CrossRefPubMedGoogle Scholar
  35. Karger DN, Tuomisto H, Amoroso VB, Darnaedi D, Hidayat A, Abrahamczyk S, Kluge J, Lehnert M, Kessler M (2015) The importance of species pool size for community composition. Ecography 38:1243–1253.  https://doi.org/10.1111/ecog.01322 CrossRefGoogle Scholar
  36. Kärnä O-M, Grönroos M, Antikainen H, Hjort J, Ilmonen J, Paasivirta L, Heino J (2015) Inferring the effects of potential dispersal routes on the metacommunity structure of stream insects: as the crow flies, as the fish swims or as the fox runs? J Anim Ecol 84:1342–1353.  https://doi.org/10.1111/1365-2656.12397 CrossRefPubMedGoogle Scholar
  37. Kassen R, Buckling A, Bell G, Rainey PB (2000) Diversity peaks at intermediate productivity in a laboratory microcosm. Nature 406:508–551.  https://doi.org/10.1038/35020060 CrossRefGoogle Scholar
  38. Kneitel JM, Chase JM (2004) Trade-offs in community ecology: linking spatial scales and species coexistence. Ecol Lett 7:69–80.  https://doi.org/10.1046/j.1461-0248.2003.00551.x CrossRefGoogle Scholar
  39. Korhonen JJ, Wang J, Soininen J (2011) Productivity-diversity relationships in lake plankton communities. PLoS One 6:e22041.  https://doi.org/10.1371/journal.pone.0022041 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Kraft NJB, Comita LS, Chase JM, Sanders NJ, Swenson NG, Crist TO, Stegen JC, Vellend M, Boyle B, Anderson MJ, Cornell HV, Davies KF, Freestone AL, Inouye BD, Harrison SP, Myers JA (2011) Disentangling the drivers of beta diversity along latitudinal and elevational gradients. Science 333:1755–1758.  https://doi.org/10.1126/science.1208584 CrossRefPubMedGoogle Scholar
  41. Lawton JH (1999) Are there general laws in ecology? Oikos 84:177–192.  https://doi.org/10.2307/3546712 CrossRefGoogle Scholar
  42. Leibold MA (1999) Biodiversity and nutrient enrichment in pond plankton communities. Evol Ecol Res 1:73–95. doiGoogle Scholar
  43. Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM, Hoopes MF, Holt RD, Shurin JB, Lae R, Tilman D, Loreau M, Gonzalez A (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett 7:601–613.  https://doi.org/10.1111/j.1461-0248.2004.00608.x CrossRefGoogle Scholar
  44. Lessard J-P, Belmaker J, Myers JA, Chase JM, Rahbek C (2012) Inferring local ecological processes amid species pool influences. Trends Ecol Evol 27:600–607.  https://doi.org/10.1016/j.tree.2012.07.006 CrossRefPubMedGoogle Scholar
  45. Lessard J-P, Weinstein BG, Borregaard MK, Marske KA, Martin DR, McGuire JA, Parra JL, Rahbek C, Graham CH (2016) Process-based species pools reveal the hidden signature of biotic interactions amid the anfluence of temperature filtering. Am Nat 187:75–88.  https://doi.org/10.1086/684128 CrossRefPubMedGoogle Scholar
  46. Livingston G, Matias M, Calcagno V, Barbera C, Combe M, Leibold MA, Mouquet N (2012) Competition–colonization dynamics in experimental bacterial metacommunities. Nat Commun 3:1234.  https://doi.org/10.1038/ncomms2239 CrossRefPubMedGoogle Scholar
  47. Márquez JC, Kolasa J (2013) Local and regional processes in community assembly. PLoS One 8:e54580.  https://doi.org/10.1371/journal.pone.0054580 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Matias MG, Combe M, Barbera C, Mouquet N (2013) Ecological strategies shape the insurance potential of biodiversity. Front Microbiol 3:1–9.  https://doi.org/10.3389/fmicb.2012.00432 CrossRefGoogle Scholar
  49. Matias MG, Pereira CL, Raposeiro PM, Gonçalves V, Cruz AM, Costa AC, Araújo MB (2017) Divergent trophic responses to biogeographic and environmental gradients. Oikos 126:101–110.  https://doi.org/10.1111/oik.02604 CrossRefGoogle Scholar
  50. Mitra A, Flynn KJ (2006) Promotion of harmful algal blooms by zooplankton predatory activity. Biol Lett 2:194–197.  https://doi.org/10.1098/rsbl.2006.0447 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 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 HH (2016) Vegan: 2.4-0., community ecology package. R package version. https://CRAN.R-project.org/package=vegan
  52. Olenina I, Hjdu 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. HELCOME Balt Sea Enciron Proc 106:144 ppGoogle Scholar
  53. Östman Ö, Kneitel JM, Chase JM (2006) Disturbance alters habitat isolation’s effect on biodiversity in aquatic microcosms. Oikos 114:360–366.  https://doi.org/10.1111/j.2006.0030-1299.14521.x CrossRefGoogle Scholar
  54. Petchey OL (2000) Prey diversity, prey composition, and predator population dynamics in experimental microcosms. J Anim Ecol 69:874–882.  https://doi.org/10.1046/j.1365-2656.2000.00446.x CrossRefPubMedGoogle Scholar
  55. Ptacnik R, Andersen T, Brettum P, Lepistö L, Willén E (2010) Regional species pools control community saturations in lake phytoplankton. Proc Biol Sci 277:3755–3764.  https://doi.org/10.1098/rspb.2010.1158 CrossRefPubMedPubMedCentralGoogle Scholar
  56. R Core Team (2016) R: a language and environment for statistical computing. Foundation for Statistical Computing, Vienna. https://www.R-project.org/
  57. Ricklefs R (1987) Community Diversity Relative Role of Local and Regional Processes. Science 235:167–171.  https://doi.org/10.1126/science.235.4785.167 CrossRefGoogle Scholar
  58. Ricklefs R (2000) The relationship between local and regional species richness in birds of the Caribbean Basin. J Ecol 69:1111–1116.  https://doi.org/10.1111/j.1365-2656.2000.00456.x CrossRefGoogle Scholar
  59. Ricklefs R (2004) A comprehensive framework for global patterns in biodiversity. Ecol Lett 7:1–15.  https://doi.org/10.1046/j.1461-0248.2003.00554.x CrossRefGoogle Scholar
  60. Smith VH, Tilman GD, Nekola JC (1998) Eutrophication: Impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environ Pollut 100:179–196.  https://doi.org/10.1016/S0269-7491(99)00091-3 CrossRefGoogle Scholar
  61. Srivastava DS, Lawton JH (1998) Why more productive sites have more species: an experimental test of theory using tree-hole communities. Am Nat 152:510–529.  https://doi.org/10.1086/286187 CrossRefPubMedGoogle Scholar
  62. Srivastava DS, Kolasa J, Bengtsson J, Gonzalez A, Lawler SP, Miller TE, Munguia P, Romanuk T, Schneider DC, Trzcinski MK (2004) Are natural microcosms useful model systems for ecology? Trends Ecol Evol 19:379–384.  https://doi.org/10.1016/j.tree.2004.04.010 CrossRefPubMedGoogle Scholar
  63. Stewart RIA, Dossena M, Bohan DA, Jeppesen E, Kordas RL, Ledger MR, Meerhoff M, Moss B, Mulder C, Shurin JB, Suttle B, Thompson R, Trimmer M, Woodward G (2013) Mesocosm experiments as a tool for ecological climate-change research. Adv Ecol Res 48:71–181.  https://doi.org/10.1016/B978-0-12-417199-2.00002-1 CrossRefGoogle Scholar
  64. Strong DR, Simberloff DS, Abele LG, Thistle AB (1984) Ecological communities: conceptual issues and the evidence. Princeton University Press, PrincetonCrossRefGoogle Scholar
  65. Sun J, Liu D (2003) Geometric models for calculating cell biovolume and surface area for phytoplankton. J Plankton Res 25:1331–1346.  https://doi.org/10.1093/plankt/fbg096 CrossRefGoogle Scholar
  66. Tõnno I, Agasild H, Kõiv T, Freiberg R, Nõges P, Nõges T (2016) Algal diet of small-bodied crustacean zooplankton in a cyanobacteria-dominated eutrophic lake. Plos One 11:e0154526.  https://doi.org/10.1371/journal.pone.0154526 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Wang J, Pan F, Soininen J, Heino J, Shen J (2016) Nutrient enrichment modified temperature-biodiversity relationships in large-scale field experiments. Nat Commun 7:13960.  https://doi.org/10.1038/ncomms13960 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Warren PH, Law R, Weatherby AJ (2003) Mapping the assembly of protist communities in microcosms. Ecology 84:1001–1011.  https://doi.org/10.1890/0012-9658(2003)084%5B1001:MTAOPC%5D2.0.CO;2 CrossRefGoogle Scholar
  69. White EP, Hurlbert AH (2010) The combined influence of the local environment and regional enrichment on bird species richness. Am Nat 175:E35–E43.  https://doi.org/10.1086/649578 CrossRefPubMedGoogle Scholar
  70. Woodward G, Perkins DM, Brown LE (2010) Climate change and freshwater ecosystems: impacts across multiple levels of organization. Philos Trans R Soc B Biol Sci 365:2093–2106.  https://doi.org/10.1098/rstb.2010.0055 CrossRefGoogle Scholar
  71. Wright DH (1983) Species-energy theory: an extension of species-area theory. Oikos 41:496–506.  https://doi.org/10.2307/3544109 doiCrossRefGoogle Scholar
  72. Zobel M (1997) The relative role of species pools in determining plant species richness: an alternative explanation of species coexistence? Trends Ecol Evol 12:266–269.  https://doi.org/10.1016/S0169-5347(97)01096-3 CrossRefGoogle Scholar
  73. Zobel M (2016) The species pool concept as a framework for studying patterns of plant diversity. J Veg Sci 27:8–18.  https://doi.org/10.1111/jvs.12333 CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.InBio/CIBIOUniversity of ÉvoraÉvoraPortugal
  2. 2.Center for Macroecology, Evolution and Climate, Natural History Museum of DenmarkUniversity of CopenhagenCopenhagenDenmark
  3. 3.Museo Nacional de Ciencias Naturales, CSICMadridSpain
  4. 4.Imperial College LondonAscotUK

Personalised recommendations