Advertisement

Oecologia

, Volume 186, Issue 1, pp 217–233 | Cite as

Scale-specific drivers of kelp forest communities

  • Thomas Lamy
  • Daniel C. Reed
  • Andrew Rassweiler
  • David A. Siegel
  • Li Kui
  • Tom W. Bell
  • Rachel D. Simons
  • Robert J. Miller
Community ecology – original research

Abstract

Identifying spatial scales of variation in natural communities and the processes driving them is critical for obtaining a predictive understanding of biodiversity. In this study, we focused on diverse communities inhabiting productive kelp forests on shallow subtidal rocky reefs in southern California, USA. We combined long-term community surveys from 86 sites with detailed environmental data to determine what structures assemblages of fishes, invertebrates and algae at multiple spatial scales. We identified the spatial scales of variation in species composition using a hierarchical analysis based on eigenfunctions, and assessed how sea surface temperature (SST), water column chlorophyll, giant kelp biomass, wave exposure and potential propagule delivery strength contributed to community variation at each scale. Spatial effects occurring at multiple scales explained 60% of the variation in fish assemblages and 52% of the variation in the assemblages of invertebrates and algae. Most variation occurred over broad spatial scales (> 200 km) consistent with spatial heterogeneity in SST and potential propagule delivery strength, while the latter also explained community variation at medium scales (65–200 km). Small scale (1–65 km) community variation was substantial but not linked to any of the measured drivers. Conclusions were consistent for both reef fishes and benthic invertebrates and algae, despite sharp differences in their adult mobility. Our results demonstrate the scale dependence of environmental drivers on kelp forest communities, showing that most species were strongly sorted along oceanographic conditions over various spatial scales. Such spatial effects must be integrated into models assessing the response of marine ecosystems to climate change.

Keywords

Multi-scale patterns Spatial ecology Scale dependence Connectivity Kelp forests 

Notes

Acknowledgements

The authors are thankful to Daniel Borcard for stimulating discussions on multiscale analyses and for providing useful comments on an early version of this manuscript. This research was supported by the National Aeronautics and Space Administration Biodiversity and Ecological Forecasting program (NASA Grant NNX14AR62A), the Bureau of Ocean and Energy Management Ecosystem Studies program (BOEM award MC15AC00006) and NOAA in support of the Santa Barbara Channel Biodiversity Observation Network and the US National Science Foundation in support of the Santa Barbara Coastal Long Term Ecological Research program.

Author contribution statement

TL, DR, AR and RM designed the study, TL, AR, DS, LK, TB and RS processed the data and TL performed statistical analyses. TL wrote the first draft of the manuscript, and all authors contributed substantially to revisions.

Supplementary material

442_2017_3994_MOESM1_ESM.docx (776 kb)
Supplementary material 1 (DOCX 775 kb)

References

  1. Airoldi L (2003) The effects of sedimentation on rocky coast assemblages. Oceanogr Mar Biol 41:161–236Google Scholar
  2. Anderson MJ, Crist TO, Chase JM et al (2011) Navigating the multiple meanings of β diversity: a roadmap for the practicing ecologist. Ecol Lett 14:19–28CrossRefPubMedGoogle Scholar
  3. Bell TW, Cavanaugh KC, Reed DC, Siegel DA (2015) Geographical variability in the controls of giant kelp biomass dynamics. J Biogeogr 42:2010–2021CrossRefGoogle Scholar
  4. Bell TW, Cavanaugh KC, Siegel DA (2017) SBC LTER: time series of quarterly NetCDF files of kelp biomass in the canopy from Landsat 5, 7 and 8, 1984 - 2016 (ongoing). St. Barbar. Coast. LTERGoogle Scholar
  5. Bjørnstad ON, Falck W (2001) Nonparametric spatial covariance functions: estimation and testing. Environ Ecol Stat 8:53–70CrossRefGoogle Scholar
  6. Blanchet FG, Legendre P, Borcard D (2008) Forward selection of explanatory variables. Ecology 89:2623–2632CrossRefPubMedGoogle Scholar
  7. Blanchette CA, Helmuth B, Gaines SD (2007) Spatial patterns of growth in the mussel, Mytilus californianus, across a major oceanographic and biogeographic boundary at Point Conception, California, USA. J Exp Mar Biol Ecol 340:126–148CrossRefGoogle Scholar
  8. Blanchette CA, Raimondi PT, Broitman BR (2009) Spatial patterns of intertidal community structure across the California Channel Islands and link to ocean temperature. In: Proceedings of the 7th California Islands Symposium. Institute for Wildlife Studies, Arcata, CA, pp 161–173Google Scholar
  9. 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
  10. Borcard D, Legendre P, Drapeau P (1992) Partialling out the spatial component of ecological variation. Ecology 73:1045–1055CrossRefGoogle Scholar
  11. Borcard D, Legendre P, Avois-Jacquet C, Tuomisto H (2004) Dissecting the spatial structure of ecological data at multiple scales. Ecology 85:1826–1832CrossRefGoogle Scholar
  12. Broitman BR, Kinlan BP (2006) Spatial scales of benthic and pelagic producer biomass in a coastal upwelling ecosystem. Mar Ecol Prog Ser 327:15–25CrossRefGoogle Scholar
  13. Byrnes JEK, Reed DC, Cardinale BJ et al (2011) Climate-driven increases in storm frequency simplify kelp forest food webs. Glob Chang Biol 17:2513–2524CrossRefGoogle Scholar
  14. Caselle JE, Rassweiler A, Hamilton SL, Warner RR (2015) Recovery trajectories of kelp forest animals are rapid yet spatially variable across a network of temperate marine protected areas. Sci Rep 5:14102CrossRefPubMedPubMedCentralGoogle Scholar
  15. Castorani MCN, Reed DC, Alberto F et al (2015) Connectivity structures local population dynamics: a long-term empirical test in a large metapopulation system. Ecology 96:3141–3152CrossRefPubMedGoogle Scholar
  16. Cavanaugh KC, Siegel DA, Reed DC, Dennison PE (2011) Environmental controls of giant-kelp biomass in the Santa Barbara Channel, California. Mar Ecol Prog Ser 429:1–17CrossRefGoogle Scholar
  17. Cavanaugh KC, Kendall BE, Siegel DA et al (2013) Synchrony in dynamics of giant kelp forests is driven by both local recruitment and regional environmental controls. Ecology 94:499–509CrossRefPubMedGoogle Scholar
  18. Chase JM (2010) Stochastic community assembly causes higher biodiversity in more productive environments. Science 328(80):1388–1391CrossRefPubMedGoogle Scholar
  19. Chase JM, Myers JA (2011) Disentangling the importance of ecological niches from stochastic processes across scales. Philos Trans R Soc B Biol Sci 366:2351–2363CrossRefGoogle Scholar
  20. Chase JM, Kraft NJB, Smith KG et al (2011) Using null models to disentangle variation in community dissimilarity from variation in α-diversity. Ecosphere 2:art24CrossRefGoogle Scholar
  21. Coleman MA, Cetina-Heredia P, Roughan M et al (2017) Anticipating changes to future connectivity within a network of marine protected areas. Glob Chang Biol 23:3533–3542CrossRefPubMedGoogle Scholar
  22. Connell JH (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. In: Den Boer PJ, Gradwell GR (eds) Dynamics of populations. PUDOC, pp 298–312Google Scholar
  23. Dayton PK (1971) Competition, disturbance, and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecol Monogr:351–389Google Scholar
  24. Dayton PK, Currie V, Gerrodette T et al (1984) Patch dynamics and stability of some california kelp communities. Ecol Monogr 54:254–289CrossRefGoogle Scholar
  25. 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 34:296–305CrossRefGoogle Scholar
  26. Dong CM, Idica EY, McWilliams JC (2009) Circulation and multiple-scale variability in the Southern California Bight. Prog Oceanogr 82:168–190CrossRefGoogle Scholar
  27. Dornelas M, Gotelli NJ, McGill B et al (2014) Assemblage time series reveal biodiversity change but not systematic loss. Science 344(80):296–299CrossRefPubMedGoogle Scholar
  28. Dray S, Legendre P, Peres-Neto PR (2006) Spatial modelling: a comprehensive framework for principal coordinate analysis of neighbour matrices (PCNM). Ecol Model 196:483–493CrossRefGoogle Scholar
  29. Dray S, Pélissier R, Couteron P et al (2012) Community ecology in the age of multivariate multiscale spatial analysis. Ecol Monogr 82:257–275CrossRefGoogle Scholar
  30. Dungan JL, Perry JN, Dale MRT et al (2002) A balanced view of scale in spatial statistical analysis. Ecography (Cop) 25:626–640CrossRefGoogle Scholar
  31. Ebeling AW, Larson TJ, Alevizon WS (1980) Habitat groups and island-mainland distribution of kelp-bed fishes off Santa Barbara, California. In: Power DM (ed) Multidisciplinary symposium on the California Islands. Santa Barbara Museum of Natural History, Santa BarbaraGoogle Scholar
  32. Edwards MS (2004) Estimating scale-dependency in disturbance impacts: El Niños and giant kelp forests in the northeast Pacific. Oecologia 138:436–447CrossRefPubMedGoogle Scholar
  33. Flinn KM, Gouhier TC, Lechowicz MJ, Waterway MJ (2010) The role of dispersal in shaping plant community composition of wetlands within an old-growth forest. J Ecol 98:1292–1299CrossRefGoogle Scholar
  34. Fraschetti S, Terlizzi A, Benedetti-Cecchi L (2005) Patterns of distribution of marine assemblages from rocky shores: evidence of relevant scales of variation. Mar Ecol Prog Ser 296:13–29CrossRefGoogle Scholar
  35. García Molinos J, Halpern BS, Schoeman DS et al (2016) Climate velocity and the future global redistribution of marine biodiversity. Nat Clim Chang 6:83–88CrossRefGoogle Scholar
  36. Graham HM (2004) Effects of local deforestation on the diversity and structure of Southern California giant kelp forest food webs. Ecosystems 7:341–357CrossRefGoogle Scholar
  37. Grober-Dunsmore R, Pittman SJ, Caldow C et al (2009) A landscape ecology approach for the study of ecological connectivity across tropical marine seascapes. In: Nagelkerken I (ed) Ecological connectivity among tropical coastal ecosystems. Springer, Dordrecht, pp 493–530CrossRefGoogle Scholar
  38. Harms S, Winant CD (1998) Characteristic patterns of the circulation in the Santa Barbara Channel. J Geophys Res 103:3041–3065CrossRefGoogle Scholar
  39. Henderikx Freitas F, Siegel DA, Maritorena S, Fields E (2017) Satellite assessment of particulate matter and phytoplankton variations in the Santa Barbara Channel and its surrounding waters: role of surface waves. J Geophys Res Ocean 122:355–371CrossRefGoogle Scholar
  40. Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University Press, PrincetonGoogle Scholar
  41. Hughes TP, Baird AH, Dinsdale EA et al (1999) Patterns of recruitment and abundance of corals along the Great Barrier Reef. Nature 397:59–63CrossRefGoogle Scholar
  42. Hughes BB, Beas-Luna R, Barner AK et al (2017) Long-term studies contribute disproportionately to ecology and policy. Bioscience 67:271–281CrossRefGoogle Scholar
  43. Jones MM, Tuomisto H, Clark DB, Olivas P (2006) Effects of mesoscale environmental heterogeneity and dispersal limitation on floristic variation in rain forest ferns. J Ecol 94:181–195CrossRefGoogle Scholar
  44. Kenner MC, Estes JA, Tinker MT et al (2013) A multi-decade time series of kelp forest community structure at San Nicolas Island, California (USA). Ecology 94:2654CrossRefGoogle Scholar
  45. Kinlan BP, Gaines SD (2003) Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84:2007–2020CrossRefGoogle Scholar
  46. Koenigs C, Miller RJ, Page HM (2015) Top predators rely on carbon derived from giant kelp (Macrocystis pyrifera). Mar Ecol Prog Ser 537:1–8CrossRefGoogle Scholar
  47. Krumhansl KA, Okamoto DK, Rassweiler A et al (2016) Global patterns of kelp forest change over the past half-century. Proc Natl Acad Sci 113:13785–13790CrossRefPubMedPubMedCentralGoogle Scholar
  48. Kushner DJ, Rassweiler A, McLaughlin JP, Lafferty KD (2013) A multi-decade time series of kelp forest community structure at the California Channel Islands. Ecology 94:2655CrossRefGoogle Scholar
  49. 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 159:377–388CrossRefPubMedGoogle Scholar
  50. Legendre P (1993) Spatial autocorrelation: trouble or new paradigm? Ecology 74:1659–1673CrossRefGoogle Scholar
  51. Legendre P, Anderson MJ (1999) Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monogr 69:1–24CrossRefGoogle Scholar
  52. Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280CrossRefPubMedGoogle Scholar
  53. Legendre P, Legendre L (2012) Numerical ecology. Elsevier, Third EditGoogle Scholar
  54. Legendre P, De Cáceres M, Borcard D (2010) Community surveys through space and time: testing the space–time interaction in the absence of replication. Ecology 91:262–272CrossRefPubMedGoogle Scholar
  55. Legendre P, Oksanen J, ter Braak CJF (2011) Testing the significance of canonical axes in redundancy analysis. Methods Ecol Evol 2:269–277CrossRefGoogle Scholar
  56. Leibold MA, McPeek MA (2006) Coexistence of the niche and neutral perspectives in community ecology. Ecology 87:1399–1410CrossRefPubMedGoogle Scholar
  57. Leibold MA, Holyoak M, Mouquet N et al (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett 7:601–613CrossRefGoogle Scholar
  58. Lester SE, Gaines SD, Kinlan BP (2007) Reproduction on the edge: large-scale patterns of individual performance in a marine invertebrate. Ecology 88:2229–2239CrossRefPubMedGoogle Scholar
  59. Levin SA (1992) The problem of pattern and scale in ecology: the Robert H. MacArthur award lecture. Ecology 73:1943–1967CrossRefGoogle Scholar
  60. MacNeil MA, Graham NAJ, Polunin NVC et al (2009) Hierarchical drivers of reef-fish metacommunity structure. Ecology 90:252–264CrossRefPubMedGoogle Scholar
  61. Magris RA, Treml EA, Pressey RL, Weeks R (2016) Integrating multiple species connectivity and habitat quality into conservation planning for coral reefs. Ecography 39:649–664CrossRefGoogle Scholar
  62. Magurran AE, Dornelas M, Moyes F et al (2015) Rapid biotic homogenization of marine fish assemblages. Nature Com 6:8405CrossRefGoogle Scholar
  63. McGill BJ, Dornelas M, Gotelli NJ, Magurran AE (2015) Fifteen forms of biodiversity trend in the Anthropocene. Trends Ecol Evol 30:104–113CrossRefPubMedGoogle Scholar
  64. Melià P, Schiavina M, Rossetto M et al (2016) Looking for hotspots of marine metacommunity connectivity: a methodological framework. Sci Rep 6:23705CrossRefPubMedPubMedCentralGoogle Scholar
  65. Menge BA, Olson AM (1990) Role of scale and environmental factors in regulation of community structure. Trends Ecol Evol 5:52–57CrossRefPubMedGoogle Scholar
  66. Menge BA, Gouhier TC, Hacker SD et al (2015) Are meta-ecosystems organized hierarchically? A model and test in rocky intertidal habitats. Ecol Monogr 85:213–233CrossRefGoogle Scholar
  67. Meynard CN, Lavergne S, Boulangeat I et al (2013) Disentangling the drivers of metacommunity structure across spatial scales. J Biogeogr 40:1560–1571CrossRefPubMedPubMedCentralGoogle Scholar
  68. Miller RJ, Page HM, Reed DC (2015) Trophic versus structural effects of a marine foundation species, giant kelp (Macrocystis pyrifera). Oecologia 179:1199–1209CrossRefPubMedGoogle Scholar
  69. Mitarai S, Siegel DA, Watson JR et al (2009) Quantifying connectivity in the coastal ocean with application to the Southern California Bight. J Geophys Res Ocean 114:C10026CrossRefGoogle Scholar
  70. Newbold T, Hudson LN, Hill SLL et al (2015) Global effects of land use on local terrestrial biodiversity. Nature 520:45–50CrossRefPubMedGoogle Scholar
  71. Olds AD, Connolly RM, Pitt KA et al (2016) Quantifying the conservation value of seascape connectivity: a global synthesis. Glob Ecol Biogeogr 25:3–15CrossRefGoogle Scholar
  72. Paine RT (1974) Intertidal community structure. Oecologia 15:93–120CrossRefPubMedGoogle Scholar
  73. 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
  74. R Core Team (2014) R: a language and environment for statistical computingGoogle Scholar
  75. Reed DC (2016) SBC LTER: reef: kelp forest community dynamics: fish abundance. Santa Barbara Coastal LTERGoogle Scholar
  76. Reed DC, Raimondi PT, Carr MH, Goldwasser L (2000) The role of dispersal and disturbance in determining spatial heterogeneity in sedentary organisms. Ecology 81:2011–2026CrossRefGoogle Scholar
  77. Reed DC, Rassweiler A, Arkema KK (2008) Biomass rather than growth rate determines variation in net primary production by giant kelp. Ecology 89:2493–2505CrossRefPubMedGoogle Scholar
  78. Ryberg WA, Fitzgerald LA (2015) Landscape composition, not connectivity, determines metacommunity structure across multiple scales. Ecography 39:932–941CrossRefGoogle Scholar
  79. Saarman ET, Carr MH (2013) The california marine life protection act: a balance of top down and bottom up governance in MPA planning. Mar Policy 41:41–49CrossRefGoogle Scholar
  80. Sax DF, Gaines SD, Brown JH (2002) Species invasions exceed extinctions on islands worldwide: a comparative study of plants and birds. Am Nat 160:766–783CrossRefPubMedGoogle Scholar
  81. Schiel DR, Foster MS (2015) The biology and ecology of giant kelp forests, 1st edn. University of California Press, CaliforniaCrossRefGoogle Scholar
  82. Schneider DC (2001) The rise of the concept of scale in ecology. Bioscience 51:545–553CrossRefGoogle Scholar
  83. Schroeter SC, Reed DC, Raimondi PT (2015) Effects of reef physical structure on development of benthic reef community: a large-scale artificial reef experiment. Mar Ecol Prog Ser 540:43–55CrossRefGoogle Scholar
  84. Shanks AL, Grantham BA, Carr MH (2003) Propagule dispersal distance and the size and spacing of marine reserves. Ecol Appl 13:S159–S169CrossRefGoogle Scholar
  85. Siegel DA, Watson JR, Simons RD et al. Characterizing particle transit time metrics in a coastal ocean network. J Geophys Res (unpublished data) Google Scholar
  86. Simons RD, Siegel DA, Brown KS (2013) Model sensitivity and robustness in the estimation of larval transport: a study of particle tracking parameters. J Mar Syst 119–120:19–29CrossRefGoogle Scholar
  87. Simons RD, Page HM, Zaleski S et al (2016) The effects of anthropogenic structures on habitat connectivity and the potential spread of non-native invertebrate species in the offshore environment. PLoS One 11:e0152261CrossRefPubMedPubMedCentralGoogle Scholar
  88. Socolar JB, Gilroy JJ, Kunin WE, Edwards DP (2016) How should beta-diversity inform biodiversity conservation? Trends Ecol Evol 31:67–80CrossRefPubMedGoogle Scholar
  89. Terlizzi A, Anderson MJ, Fraschetti S, Benedetti-Cecchi L (2007) Scales of spatial variation in Mediterranean subtidal sessile assemblages at different depths. Mar Ecol Prog Ser 332:25–39CrossRefGoogle Scholar
  90. Tittensor DP, Mora C, Jetz W et al (2010) Global patterns and predictors of marine biodiversity across taxa. Nature 466:1098–1101CrossRefPubMedGoogle Scholar
  91. Tzanopoulos J, Mouttet R, Letourneau A et al (2013) Scale sensitivity of drivers of environmental change across Europe. Glob Environ Change 23:167–178CrossRefGoogle Scholar
  92. Underwood AJ, Chapman MG (1996) Scales of spatial patterns of distribution of intertidal invertebrates. Oecologia 107:212–224CrossRefPubMedGoogle Scholar
  93. Vellend M, Srivastava DS, Anderson KM et al (2014) Assessing the relative importance of neutral stochasticity in ecological communities. Oikos 123:1420–1430CrossRefGoogle Scholar
  94. Vergés A, Doropoulos C, Malcolm HA et al (2016) Long-term empirical evidence of ocean warming leading to tropicalization of fish communities, increased herbivory, and loss of kelp. Proc Natl Acad Sci 113:13791–13796CrossRefPubMedPubMedCentralGoogle Scholar
  95. Vilà M, Espinar JL, Hejda M et al (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14:702–708CrossRefPubMedGoogle Scholar
  96. Wang D, Gouhier TC, Menge BA, Ganguly AR (2015) Intensification and spatial homogenization of coastal upwelling under climate change. Nature 518:390–394CrossRefPubMedGoogle Scholar
  97. Watson JR, Hays CG, Raimondi PT et al (2011a) Currents connecting communities: nearshore community similarity and ocean circulation. Ecology 92:1193–1200CrossRefPubMedGoogle Scholar
  98. Watson JR, Siegel DA, Kendall BE et al (2011b) Identifying critical regions in small-world marine metapopulations. Proc Natl Acad Sci 108:E907–E913CrossRefPubMedPubMedCentralGoogle Scholar
  99. Wernberg T, Bennett S, Babcock RC et al (2016) Climate-driven regime shift of a temperate marine ecosystem. Science 353(80):169 LP–172Google Scholar
  100. Yeager LA, Layman CA, Allgeier JE (2011) Effects of habitat heterogeneity at multiple spatial scales on fish community assembly. Oecologia 167:157–168CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Marine Science InstituteUniversity of CaliforniaSanta BarbaraUSA
  2. 2.Department of Biological ScienceFlorida State UniversityTallahasseeUSA
  3. 3.Earth Research InstituteUniversity of CaliforniaSanta BarbaraUSA
  4. 4.Department of GeographyUniversity of CaliforniaSanta BarbaraUSA

Personalised recommendations