Research ArticleECOLOGY

Habitat diversity and ecosystem multifunctionality—The importance of direct and indirect effects

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Science Advances  08 Feb 2017:
Vol. 3, no. 2, e1601475
DOI: 10.1126/sciadv.1601475
  • Fig. 1 Conceptual diagram of our framework.

    Ecosystem homogenization (caused by, for example, human disturbance) results in a change in habitat diversity (A). Because habitats have different physical and chemical characteristics, they are likely associated with different sets of species. Loss of habitat diversity thus potentially leads to loss in species diversity (the union of the species in all habitats, indicated by different symbols) (B). Changes in habitat diversity can affect ecosystem functioning not only directly through changes in structural complexity and the cross-habitat exchange of nutrients and other resources (C) but also indirectly via changes in species diversity.

  • Fig. 2 Principal components analysis and nonmetric multidimensional scaling plots on habitat descriptors and OTUs.

    The intra- and interhabitat variability and variability of bacterial community structure during spring, summer, and autumn are shown. (A) Ordination of habitat samples based on habitat descriptors displayed in a principal components analysis (PCA) plot with Euclidean distances; n = 48. (B) Bacterial community structure (OTU-based) displayed in a nonmetric multidimensional scaling (NMDS) plot based on weighted UniFrac distances; n = 48. Color codes indicate the habitat types Sandy beach (light brown), Silty mud (dark brown), Cyanobacterial mats (blue), and Ruppia maritima meadows (green).

  • Fig. 3 Linear functions of relationships between habitat diversity, microbial diversity, and multifunctionality across seasons.

    (A) Relationship between habitat diversity and bacterial diversity, (B) habitat diversity and index of multifunctionality (weighted average value of standardized functions), (C) bacterial diversity and index of multifunctionality, and (D) benthic microalgal diversity (effective number of species) and index of multifunctionality. Shaded areas indicate ±95% confidence interval; ntot = 84, nlevel 1 = 16, nlevel 2,3,4 = 4 per season.

  • Fig. 4 Structural equation models.

    Path diagrams based on SEM showing how habitat and bacterial diversity affect ecosystem multifunctionality during (A) spring, (B) summer, and (C) autumn. Solid paths (blue) are statistically significant (P < 0.05) with standardized path coefficients indicated, whereas the dashed gray lines are not. Percentages indicate the variance explained by the model; ntot = 84, nlevel 1 = 16, nlevel 2,3,4 = 4 per season.

  • Fig. 5 Linear models of individual functions.

    Linear models of individual functions used to calculate multifunctionality against habitat diversity during spring, summer, and autumn are shown. (A) GPP (mmol O2 m−2 day−1), (B) nitrogen fixation (mmol N2 m−2 day−1), (C) uptake of DIN (ammonium and nitrate + nitrite) (mmol DIN m−2 day−1), and (D) denitrification (nmol N g wet sediment−1 hour−1). Shaded areas indicate ±95% confidence interval; ntot = 84, nlevel 1 = 16, nlevel 2,3,4 = 4 per season.

  • Fig. 6 The net habitat diversity effect on individual ecosystem functions and multifunctionality.

    “Expected” is the expected functionality in the treatment based on each of the single habitats, and “observed” is the observed functionality. (A) Denitrification (nmol N g wet sediment−1 hour−1). (B) Nitrogen fixation (mmol N2 m−2 day−1). (C) Uptake of DIN (ammonium and nitrate + nitrite) (mmol DIN m−2 day−1). (D) GPP (mmol O2 m−2 day−1). (E) Index of multifunctionality (weighted average value of standardized functions). The points are slightly spread along the x axis (grouped by season) and jittered (within season) for clarity. The triangles represent group means.

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/3/2/e1601475/DC1

    fig. S1. Phylogenetic bacterial diversity.

    fig. S2. Benthic microalgal diversity.

    fig. S3. Linear model of benthic microalgal diversity and habitat diversity.

    fig. S4. Multifunctionality and multiple thresholds.

    fig. S5. Ecosystem functions and multifunctionality for individual habitats and habitat diversity.

    fig. S6. Temperature and light.

    fig. S7. Concentrations of inorganic nutrients.

    fig. S8. Total nitrogen and organic content.

    fig. S9. Schematic figure illustrating the experimental design.

    fig. S10. Ecosystem functions that were used to calculate the multifunctionality index plotted against each other during spring.

    fig. S11. Ecosystem functions that were used to calculate the multifunctionality index plotted against each other during summer.

    fig. S12. Ecosystem functions that were used to calculate the multifunctionality index plotted against each other during autumn.

    table S1. Linear model of bacterial diversity − habitat diversity × season.

    table S2. Linear model of microalgal diversity − habitat diversity × season.

    table S3. Linear model of multifunctionality − habitat diversity × season.

    table S4. Linear model of multifunctionality − bacterial diversity × season.

    table S5. Linear model of multifunctionality − algal diversity × season.

    table S6. Standardized total, direct, and indirect effects for the group spring.

    table S7. Standardized total, direct, and indirect effects for the group summer.

    table S8. Standardized total, direct, and indirect effects for the group autumn.

    table S9. Linear model of GPP − habitat diversity × season.

    table S10. Linear model of N2 fixation − habitat diversity × season.

    table S11. Linear model of DIN uptake − habitat diversity × season.

    table S12. Linear model of denitrification − habitat diversity × season.

    table S13. Environmental data for each habitat during spring.

    table S14. Environmental data for each habitat during summer.

    table S15. Environmental data for each habitat during autumn.

    table S16. Correlation coefficients for the individual ecosystem functions used to calculate multifunctionality during spring.

    table S17. Correlation coefficients for the individual ecosystem functions used to calculate multifunctionality during summer.

    table S18. Correlation coefficients for the individual ecosystem functions used to calculate multifunctionality during autumn.

  • Supplementary Materials

    This PDF file includes:

    • fig. S1. Phylogenetic bacterial diversity.
    • fig. S2. Benthic microalgal diversity.
    • fig. S3. Linear model of benthic microalgal diversity and habitat diversity.
    • fig. S4. Multifunctionality and multiple thresholds.
    • fig. S5. Ecosystem functions and multifunctionality for individual habitats and habitat diversity.
    • fig. S6. Temperature and light.
    • fig. S7. Concentrations of inorganic nutrients.
    • fig. S8. Total nitrogen and organic content.
    • fig. S9. Schematic figure illustrating the experimental design.
    • fig. S10. Ecosystem functions that were used to calculate the multifunctionality index plotted against each other during spring.
    • fig. S11. Ecosystem functions that were used to calculate the multifunctionality index plotted against each other during summer.
    • fig. S12. Ecosystem functions that were used to calculate the multifunctionality index plotted against each other during autumn.
    • table S1. Linear model of bacterial diversity − habitat diversity × season.
    • table S2. Linear model of microalgal diversity − habitat diversity × season.
    • table S3. Linear model of multifunctionality − habitat diversity × season.
    • table S4. Linear model of multifunctionality − bacterial diversity × season.
    • table S5. Linear model of multifunctionality − algal diversity × season.
    • table S6. Standardized total, direct, and indirect effects for the group spring.
    • table S7. Standardized total, direct, and indirect effects for the group summer.
    • table S8. Standardized total, direct, and indirect effects for the group autumn.
    • table S9. Linear model of GPP − habitat diversity × season.
    • table S10. Linear model of N2 fixation − habitat diversity × season.
    • table S11. Linear model of DIN uptake − habitat diversity × season.
    • table S12. Linear model of denitrification − habitat diversity × season.
    • table S13. Environmental data for each habitat during spring.
    • table S14. Environmental data for each habitat during summer.
    • table S15. Environmental data for each habitat during autumn.
    • table S16. Correlation coefficients for the individual ecosystem functions used to calculate multifunctionality during spring.
    • table S17. Correlation coefficients for the individual ecosystem functions used to calculate multifunctionality during summer.
    • table S18. Correlation coefficients for the individual ecosystem functions used to calculate multifunctionality during autumn.

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