Advertisement

Oecologia

, Volume 183, Issue 3, pp 643–652 | Cite as

Making sense of metacommunities: dispelling the mythology of a metacommunity typology

  • Bryan L. BrownEmail author
  • Eric R. Sokol
  • James Skelton
  • Brett Tornwall
Concepts, Reviews and Syntheses

Abstract

Metacommunity ecology has rapidly become a dominant framework through which ecologists understand the natural world. Unfortunately, persistent misunderstandings regarding metacommunity theory and the methods for evaluating hypotheses based on the theory are common in the ecological literature. Since its beginnings, four major paradigms—species sorting, mass effects, neutrality, and patch dynamics—have been associated with metacommunity ecology. The Big 4 have been misconstrued to represent the complete set of metacommunity dynamics. As a result, many investigators attempt to evaluate community assembly processes as strictly belonging to one of the Big 4 types, rather than embracing the full scope of metacommunity theory. The Big 4 were never intended to represent the entire spectrum of metacommunity dynamics and were rather examples of historical paradigms that fit within the new framework. We argue that perpetuation of the Big 4 typology hurts community ecology and we encourage researchers to embrace the full inference space of metacommunity theory. A related, but distinct issue is that the technique of variation partitioning is often used to evaluate the dynamics of metacommunities. This methodology has produced its own set of misunderstandings, some of which are directly a product of the Big 4 typology and others which are simply the product of poor study design or statistical artefacts. However, variation partitioning is a potentially powerful technique when used appropriately and we identify several strategies for successful utilization of variation partitioning.

Keywords

Metacommunity Species sorting Mass effects Neutral theory Patch dynamics Variation partitioning 

Notes

Acknowledgements

Many thanks to my postdoc mentor Mathew Leibold and fellow postdoc Nicolas Loeuille for planting the metacommunity bug in my ear, even though I was supposed to be working on compensatory dynamics at the time. We are also grateful to Mathew Leibold and Pedro Peres-Neto who commented on earlier versions of this manuscript. We acknowledge support from the National Science Foundation Grants DEB-1202932 to BLB and DEB-1406770 to BLB and JS.

Author contribution statement

This manuscript emerged from discussions conducted during meetings of the Brown Lab in the Department of Biological Sciences at Virginia Tech during which all authors were present. All authors contributed significantly to the concept, development and writing of the present manuscript. BLB and ERS were responsible for final construction and editing of the present manuscript.

References

  1. Becking B (1934) Geobiologie of inleiding tot de milieukunde. W.P. Van Stockum & Zoon (in Dutch), The HagueGoogle Scholar
  2. Bell G (2001) Neutral macroecology. Science 293:2413–2418CrossRefPubMedGoogle Scholar
  3. Biswas SR, Mallik AU, Braithwaite NT, Wagner HH (2016) A conceptual framework for the 480 spatial analysis of functional trait diversity. Oikos 125:192–200. doi: 10.1111/oik.02277 CrossRefGoogle Scholar
  4. Blanchet FG, Legendre P, Borcard D (2008) Forward selection of explanatory variables. Ecology 89:2623–2632. doi: 10.1890/07-0986.1 CrossRefPubMedGoogle Scholar
  5. Borcard D, Legendre P (2002) All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecol Model 153:51–68CrossRefGoogle Scholar
  6. Borcard D, Legendre P, Drapeau P (1992) Partialling out the spatial component of ecological 484 variation. Ecology 73:1045–1055CrossRefGoogle Scholar
  7. Brown JH, Kodric-Brown A (1977) Turnover rates in insular biogeography: effect of 488 immigration on extinction. Ecology 58:445–449CrossRefGoogle Scholar
  8. Brown JH et al (2011) Energetic limits to economic growth. Bioscience 61:19–26. doi: 10.1525/bio.2011.61.1.7 CrossRefGoogle Scholar
  9. Canedo-Arguelles M et al (2015) Dispersal strength determines meta-community structure in a dendritic riverine network. J Biogeogr 42:778–790CrossRefGoogle Scholar
  10. Chase JM (2005) Towards a really unified theory for metacommunities. Funct Ecol 19:182–186CrossRefGoogle Scholar
  11. Chase JM, Myers JA (2011) Disentangling the importance of ecological niches from stochastic processes across scales. Philosophical transactions of the Royal Soc of London B: Biological Sci 366:2351–2363. doi: 10.1098/rstb.2011.0063 CrossRefGoogle Scholar
  12. Chase JM et al (2005) Competing theories for competitive metacommunities. In: Holyoak M, Leibold MA, Holt RD (eds) Metacommunities: spatial dynamics and ecological communities, 1st edn. University of Chicago Press, Chicago, pp 335–354Google Scholar
  13. Cottenie K (2005) Integrating environmental and spatial processes in ecological community dynamics. Ecol Lett 8:1175–1182. doi: 10.1111/j.1461-0248.2005.00820.x CrossRefPubMedGoogle Scholar
  14. Datry T, Bonada N, Heino J (2016) Towards understanding the organisation of metacommunities in highly dynamic ecological systems. Oikos 125:149–159. doi: 10.1111/oik.02922 CrossRefGoogle Scholar
  15. De Bie T et al (2012) Body size and dispersal mode as key traits determining metacommunity structure of aquatic organisms. Ecol Lett 15:740–747. doi: 10.1111/j.1461-0248.2012.01794.x CrossRefPubMedGoogle Scholar
  16. 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. doi: 10.1111/j.1600-0706.2011.19563.x CrossRefGoogle Scholar
  17. Dray S et al (2012) Community ecology in the age of multivariate multiscale spatial analysis. Ecol Monogr 82:257–275. doi: 10.1890/11-1183.1 CrossRefGoogle Scholar
  18. Duivenvoorden JF, Svenning JC, Wright SJ (2002) Beta Diversity in Tropical Forests. Science 295:636–637. doi: 10.1126/science.295.5555.636 CrossRefPubMedGoogle Scholar
  19. Fernandes IM, Henriques-Silva R, Penha J, Zuanon J, Peres-Neto PR (2014) Spatiotemporal dynamics in a seasonal metacommunity structure is predictable: the case of floodplain-fish communities. Ecography 37:464–475. doi: 10.1111/j.1600-0587.2013.00527.x Google Scholar
  20. Gilbert B, Bennett JR (2010) Partitioning variation in ecological communities: do the numbers add up? J Appl Ecol 47:1071–1082. doi: 10.1111/j.1365-2664.2010.01861.x CrossRefGoogle Scholar
  21. Gil-Tena A, Lecerf R, Ernoult A (2013) Disentangling community assemblages to depict an indicator of biological connectivity: A regional study of fragmented semi-natural grasslands. Ecol Ind 24:48–55. doi: 10.1016/j.ecolind.2012.05.022 CrossRefGoogle Scholar
  22. Grime JP (2006) Trait convergence and trait divergence in herbaceous plant communities: Mechanisms and consequences. J Veg Sci 17:255–260. doi: 10.1111/j.1654-1103.2006.tb02444.x CrossRefGoogle Scholar
  23. Holyoak M, Leibold MA, Holt RD (eds) (2005) Metacommunities: spatial dynamics and ecological communities, 1st edn. University of Chicago Press, ChicagoGoogle Scholar
  24. Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University Press, PrincetonGoogle Scholar
  25. Hubert N, Calcagno V, Etienne RS, Mouquet N (2015) Metacommunity speciation models and their implications for diversification theory. Ecol Lett 18:864–881. doi: 10.1111/ele.12458 CrossRefPubMedGoogle Scholar
  26. Hutchinson GE (1959) Homage to Santa Rosalia or Why are there so many kinds of animals? Am Nat 63:145–159CrossRefGoogle Scholar
  27. Jabot F, Lohier T (2016) Non-random correlation of species dynamics in tropical tree communities. Oikos. doi: 10.1111/oik.03103 Google Scholar
  28. Lawton JH (1999) Are there general laws in ecology? Oikos 84:177–192. doi: 10.2307/3546712 CrossRefGoogle Scholar
  29. Legendre P, Gauthier O (2014) Statistical methods for temporal and space–time analysis of community composition data. Proc R Soc B Biol Sci 281. doi: 10.1098/rspb.2013.2728
  30. Legendre P et al (2009) Partitioning beta diversity in a subtropical broad-leaved forest of China. Ecology 90:663–674CrossRefPubMedGoogle Scholar
  31. Legendre P, Legendre L (1998) Numerical ecology. ElsevierGoogle Scholar
  32. Legendre P, Borcard D, Peres-Neto PR (2005) Analyzing beta diversity: partitioning the spatial variation of community composition data. Ecol Monogr 75:435–450CrossRefGoogle Scholar
  33. Legendre P, Borcard D, Peres-Neto PR (2008) Analyzing or explaining beta diversity? comment. Ecology 89:3238–3244CrossRefGoogle Scholar
  34. Legendre P, Borcard D, Roberts DW (2012) Variation partitioning involving orthogonal spatial eigenfunction submodels. Ecology 93:1234–1240. doi: 10.1890/11-2028.1 CrossRefPubMedGoogle Scholar
  35. Legendre P, Fortin M-J (2010) Comparison of the Mantel test and alternative approaches for detecting complex multivariate relationships in the spatial analysis of genetic data. Mol Ecol Res 10:831–844. doi: 10.1111/j.1755-0998.2010.02866.x CrossRefGoogle Scholar
  36. Leibold MA et al (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett 7:601–613CrossRefGoogle Scholar
  37. Levin SA (1974) Dispersion and population interactions. Am Nat 108:207–228CrossRefGoogle Scholar
  38. Levins R, Culver D (1971) Regional coexistence of species and competition between rare species. Proc Natl Acad Sci 68:1246–1248CrossRefPubMedPubMedCentralGoogle Scholar
  39. Logue JB, Mouquet N, Peter H, Hillebrand H (2011) Empirical approaches to metacommunities: a review and comparison with theory. Trends Ecol Evol 26:482–491. doi: 10.1016/j.tree.2011.04.009 CrossRefPubMedGoogle Scholar
  40. Meier S, Soininen J (2014) Phytoplankton metacommunity structure in subarctic rock pools. Aquat Microb Ecol 73:81–91. doi: 10.3354/ame01711 CrossRefGoogle Scholar
  41. Meynard CN et al (2013) Disentangling the drivers of metacommunity structure across spatial scales. J Biogeogr 40:1560–1571. doi: 10.1111/jbi.12116 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Mouquet N, Loreau M (2003) Community Patterns in Source-Sink Metacommunities. Am Natur 162:544–557. doi: 10.1086/378857 CrossRefPubMedGoogle Scholar
  43. Moritz C et al (2013) Disentangling the role of connectivity, environmental filtering, and spatial structure on metacommunity dynamics. Oikos 122:1401–1410. doi: 10.1111/j.1600-0706.2013.00377.x Google Scholar
  44. Münkemüller T et al (2012) From diversity indices to community assembly processes: a test with simulated data. Ecography 35:468–480. doi: 10.1111/j.1600-0587.2011.07259.x CrossRefGoogle Scholar
  45. Nekola JC, White PS (1999) The distance decay of similarity in biogeography and ecology. J Biogeogr 26:867–878CrossRefGoogle Scholar
  46. O’Donohue W, Buchanan JA (2001) The weakness of strong inference. Behav Philos 29:1–20Google Scholar
  47. Padial AA et al (2014) Dispersal ability determines the role of environmental, spatial and temporal drivers of metacommunity structure. PLoS One 9:e111227. doi: 10.1371/journal.pone.0111227 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Peres-Neto PR, Legendre P (2010) Estimating and controlling for spatial structure in the study of ecological communities. Glob Ecol Biogeogr 19:174–184. doi: 10.1111/j.1466-8238.2009.00506.x CrossRefGoogle Scholar
  49. Peres-Neto PR, Legendre P, Dray S, Borcard D (2006) Variation partitioning of species data matrices-estimation and comparison of fractions. Ecology 87:2614–2625CrossRefPubMedGoogle Scholar
  50. Platt JR (1964) Strong Inference Certain systematic methods of scientific thinking may produce much more rapid progress than others. Science 146:347–353. doi: 10.1126/science.146.3642.347 CrossRefPubMedGoogle Scholar
  51. Rádková V, Bojková J, Křoupalová V, Schenková J, Syrovátka V, Horsák M (2014) The role of dispersal mode and habitat specialisation in metacommunity structuring of aquatic macroinvertebrates in isolated spring fens. Freshw Biol 59:2256–2267. doi: 10.1111/fwb.12428 CrossRefGoogle Scholar
  52. Ricotta C, Moretti M (2010) Assessing the functional turnover of species assemblages with tailored dissimilarity matrices. Oikos 119:1089–1098CrossRefGoogle Scholar
  53. Seymour M, Fronhofer EA, Altermatt F (2015) Dendritic network structure and dispersal affect temporal dynamics of diversity and species persistence. Oikos 124:908–916. doi: 10.1111/oik.02354 CrossRefGoogle Scholar
  54. Shipley B (2002) Cause and correlation in biology: a user’s guide to path analysis, structural equations and causal inference. Cambridge University Press, CambridgeGoogle Scholar
  55. Shmida A, Wilson MV (1985) Biological determinants of species diversity. J Biogeogr 12:1–20. doi: 10.2307/2845026 CrossRefGoogle Scholar
  56. Simberloff DS, Boecklen WJ (1981) Santa Rosalia reconsidered: Size ratios and competition. Evolution 35:1206–1228CrossRefGoogle Scholar
  57. Skellam JG (1951) Random dispersal in theoretical populations. Biometrika 38:196–218. doi: 10.1007/BF02464427 CrossRefPubMedGoogle Scholar
  58. Smith TW, Lundholm JT (2010) Variation partitioning as a tool to distinguish between niche and neutral processes. Ecography 33:648–655. doi: 10.1111/j.1600-0587.2009.06105.x CrossRefGoogle Scholar
  59. Smouse PE, Long JC, Sokal RR (1986) Multiple regression and correlation extensions of the mantel test of matrix correspondence. Syst Zool 35:627–632. doi: 10.2307/2413122 CrossRefGoogle Scholar
  60. Soininen J (2012) Macroecology of unicellular organisms–patterns and processes. Environmental Microbiology Reports 4:10–22. doi: 10.1111/j.1758-2229.2011.00308.x CrossRefPubMedGoogle Scholar
  61. Soininen J (2016) Spatial structure in ecological communities–a quantitative analysis. Oikos 125:160–166. doi: 10.1111/oik.02241 CrossRefGoogle Scholar
  62. Sokol ER, Benfield EF, Belden LK, Valett HM (2011) The assembly of ecological communities inferred from taxonomic and functional composition. Am Nat 177:630–644CrossRefPubMedGoogle Scholar
  63. Sokol ER, Herbold CW, Lee CK et al (2013) Local and regional influences over soil microbial metacommunities in the Transantarctic Mountains. Ecosphere 4:art136. doi: 10.1890/ES13-00136.1
  64. Sokol ER, Hoch JM, Gaiser E, Trexler JC (2014) Metacommunity structure along resource and disturbance gradients in Everglades wetlands. Wetlands 34:135–146CrossRefGoogle Scholar
  65. Sokol ER, Brown BL, Carey CC, Tornwall B, Swan CM, Barrett JE (2015) Linking management to biodiversity in built ponds using metacommunity simulations. Ecol Model 296:36–45CrossRefGoogle Scholar
  66. Sokol ER, Brown BL, Barrett JE (2016) A simulation-based approach to understand how metacommunity characteristics influence emergent biodiversity patterns. Oikos . doi: 10.1111/oik.03690 Google Scholar
  67. Sokol ER, Brown BL, Barrett JE (In Review) A simulation-based approach to understand how metacommunity characteristics influence emergent biodiversity patterns. Methods Ecol EvolGoogle Scholar
  68. Stegen JC, Hurlbert AH (2011) Inferring ecological processes from taxonomic, phylogenetic and functional trait beta-diversity. PLoS One 6:13. doi: 10.1371/journal.pone.0020906 CrossRefGoogle Scholar
  69. Steinbauer MJ, Dolos K, Reineking B, Beierkuhnlein C (2012) Current measures for distance decay in similarity of species composition are influenced by study extent and grain size. Glob Ecol Biogeogr 21:1203–1212. doi: 10.1111/j.1466-8238.2012.00772.x CrossRefGoogle Scholar
  70. Szekely AJ, Langenheder S (2014) The importance of species sorting differs between habitat generalists and specialists in bacterial communities. FEMS Microbiol Ecol 87:102–112. doi: 10.1111/1574-6941.12195 CrossRefPubMedGoogle Scholar
  71. Thompson RM, Townsend CR (2006) A truce with neutral theory: Local deterministic factors, species traits and dispersal limitation determine patterns of diversity in stream invertebrates. J Anim Ecol 75:476–484CrossRefPubMedGoogle Scholar
  72. Tuomisto H (2012) An updated consumer’s guide to evenness and related indices. Oikos 121:1203–1218. doi: 10.1111/j.1600-0706.2011.19897.x CrossRefGoogle Scholar
  73. Tuomisto H, Ruokolainen K (2006) Analyzing or explaining beta diversity? Understanding the targets of different methods of analysis. Ecology 87:2697–2708CrossRefPubMedGoogle Scholar
  74. Tuomisto H, Ruokolainen K, Yli-Halla M (2003) Dispersal, environment, and floristic variation of western amazonian forests. Science 299:241–244CrossRefPubMedGoogle Scholar
  75. Tuomisto H, Ruokolainen K (2008) Analyzing or Explaining Beta Diversity? Reply. Ecology 89:3244–3256. doi: 10.1890/08-1247.1 CrossRefGoogle Scholar
  76. Tuomisto H, Ruokolainen L, Ruokolainen K (2012) Modelling niche and neutral dynamics: on the ecological interpretation of variation partitioning results. Ecography 35:961–971. doi: 10.1111/j.1600-0587.2012.07339.x CrossRefGoogle Scholar
  77. Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505CrossRefGoogle Scholar
  78. Whittaker RH (1962) Classification of natural communities. Bot Rev 28:1–239. doi: 10.2307/4353649 CrossRefGoogle Scholar
  79. Winegardner AK, Jones BK, Ng ISY, Siqueira T, Cottenie K (2012) The terminology of metacommunity ecology. Trends Ecol Evol 27:253–254. doi: 10.1016/j.tree.2012.01.007 CrossRefPubMedGoogle Scholar
  80. Zhang Y, Zhang J, Wang L, Lu D, Cai D, Wang B (2014) Influences of dispersal and local environmental factors on stream macroinvertebrate communities in Qinjiang River, Guangxi, China. Aquatic Biol 20:185–194. doi: 10.3354/ab00560 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of Biological SciencesVirginia TechBlacksburgUSA
  2. 2.Institute of Arctic and Alpine ResearchUniversity of ColoradoBoulderUSA
  3. 3.School of Forest Resources and ConservationUniversity of FloridaGainesvilleUSA

Personalised recommendations