Research ArticleEVOLUTIONARY BIOLOGY

Seed predation increases from the Arctic to the Equator and from high to low elevations

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Science Advances  20 Feb 2019:
Vol. 5, no. 2, eaau4403
DOI: 10.1126/sciadv.aau4403
  • Fig. 1 Photos illustrating depot setup at field sites.

    Depots were not overly visible from >1 m away (A; arrow), as care was taken not to disturb litter and vegetation around depots (B). Invertebrate seed predation was assessed by excluding vertebrates from some sunflower seed depots using wire mesh cages (C). Photos are from 49°N in Canada at 880 meters above sea level (masl) (A) and 80 masl (B) and from 5°N in Colombia at 2120 masl (C). Photo credits: (A and B) A. Hargreaves, McGill University, and (C) S. David, University of British Colombia.

  • Fig. 2 Latitudinal and elevational declines in seed predation.

    (A) Sampling transects from the Arctic to the Equator; the Tropic of Cancer (23.5°N) divides the temperate versus tropical zones. Circle area is proportional to the mean times the experiment was run at each site on the transect (1 to 6), and pie slices show the proportion of sites per biome: above upper treeline, forest, and below lower treeline. Seed predation differed among latitudinal zones (B; model 1) and biomes (C; model 4); different letters indicate significant differences; and dots, boxes, and whiskers show the means, 1 SE, and 95% confidence interval (CI), respectively, extracted from generalized linear mixed-effects models (GLMMs). (D to G) Continuous geographic trends in seed predation (±95% CIs) fitted by GLMMs. Elevational trends (D and F) are shown for the median latitude (31°N, black), median tropical latitude (10.5°N, red), and median temperate latitude (47.7°N, blue; models 2 and 3). Dashed trend lines show model extrapolations for temperate sites above 2500 masl. Latitudinal trends (E and G) are shown for the median elevation (1500 m) across biomes (black; models 2 and 3, respectively) and in forests specifically (green; model 5). Points are partial residuals for the all-site model (black) in each panel. (B to E) Total seed predation (56 experimental runs across 79 sites). (F and G) Seed predation by invertebrates only (25 experimental runs across 60 sites). Note that the steeper slopes in (F) and (G) compared to (D) and (E) are due to the different sites and dates included; among sites and dates where vertebrates were experimentally excluded, total and invertebrate predation showed the same geographic patterns (Fig. 3). Results are shown for sunflower seeds: Geographic patterns did not differ for oat seeds (fig. S3). Statistical results are shown in Table 1.

  • Fig. 3 Excluding vertebrate granivores reduced seed predation but did not change geographic patterns.

    The figure compares invertebrate seed predation (light gray) and total seed predation (dark gray) from sites and dates that included the vertebrate exclusion treatment (25 experimental runs across 60 sites). The latitudinal trend in invertebrate seed predation is as strong as the trend in total seed predation (trends shown for the median site elevation ±95% CI; note that invertebrate predation is as shown in Fig. 2G), although vertebrate exclusion reduced seed predation overall (right); different letters indicate significant differences; and center line, boxes, and whiskers show the means, 1 SE, and 95% CI, respectively. Data were extracted from GLMM model 3 (Table 1).

  • Table 1 Results from GLMMs analyzing latitudinal and elevational patterns in seed predation.

    Models are described in the text. Model 4 (effect of biome) and model 5 (forests only) were run twice, first on total predation (uncaged depots only) and then on invertebrate predation (caged depots only). Initial models (gray rows) included all possible interactions (indicated by “×”), but nonsignificant interactions were dropped from final models (white rows), improving model convergence. Significance of factors and interactions was obtained from testing the final model against a model without that factor or interaction. Effect sizes are given for noninteracting effects in the final model; for categorical variables, these are categorical latitude = temperate versus tropical, seed type = sunflower versus oat, cage treatment = uncaged (total predation) versus caged (invertebrate predation), and biome = below trees versus above trees (top) and within forest versus above trees (bottom).

    Model
    no.—predation
    type, biomes
    Fixed effectsχ2(df) statistic from likelihood ratio tests
    Effect size ±SE in the final model (logit scale)
    Model χ2
    deviance
    (residual df)
    R2GLMM
    Latitude
    (decimal
    degrees)
    Elevation
    (km asl)
    Seed
    species,
    df = 1
    Lat × Elev,
    df = 1
    Additional factor
    1—Total, AllInitial:
    categorLat ×
    elev × seed.
    sp
    Final: categorLat
    + elev + seed.
    sp
    20.6(1)***
    −0.48 ± 0.10
    8.0(1)**
    −0.18 ± 0.06
    50.5***
    0.46 ± 0.07
    1.6, P > 0.11500(464)0.053
    2—Total, AllInitial: lat × elev
    × seed.sp
    Final: lat + elev
    + seed.sp
    17.5(1)***
    −0.01 ± 0.003
    7.0(1)**
    −0.17 ± 0.06
    55.2***
    0.48 ± 0.07
    2.6, P > 0.11501(464)0.058
    3—Tot vs. Invert,
    All
    Initial: lat × elev
    × cage.treat
    Cage treat:
    Final: lat × elev
    + cage.treat
    39.0(2)***
    21.8(2)***
    7.5 **
    −0.01 ± 0.004
    13.7(1)***
    0.32 ± 0.09
    704(195)0.083
    4t—Total, AllInitial: lat × elev
    × seed.sp. ×
    biome
    Biome:
    Final: lat + elev
    + seed.sp. +
    biome
    6.4(1)*
    −0.007 ± 0.003
    2.6(1) P > 0.1
    −0.11 ± 0.07
    54.7***
    0.48 ± 0.07
    2.6, P > 0.18.0(2)*
    0.20 ± 0.23
    0.44 ± 0.23
    1493(462)0.057
    4i—Invert, AllInitial: lat × elev
    × biome
    Biome:
    Final: lat + elev
    + biome
    10.0(1)**
    −0.02 ± 0.005
    6.3(1)*
    −0.31 ± 0.13
    2.2, P > 0.18.1(2)*
    0.78 ± 0.39
    0.84 ± 0.30
    350(94)0.123
    5 t—Total, ForestInitial: lat × elev
    × seed.sp
    Final: lat × elev + seed.sp8.6(2)*
    8.0(2)*
    45.6***
    −0.008 ± 0.004
    4.3*
    0.48 ± 0.07
    1177(361)0.039
    5i—Invert, ForestInitial: lat × elev
    Final: lat + elev10.9(1)***
    −0.02 ± 0.005
    5.4(1)*
    −0.28 ± 0.13
    3.7, P = 0.06253(65)0.036

    *P < 0.05.

    **P < 0.01.

    ***P < 0.001.

    †Pseudo conditional R2 (variance explained by both fixed and random effects) for GLMMs with link-specific theoretical variances, calculated via the r.squaredGLMM function in the R MuMIn package (49) according to (50).

    ‡Sunflower seeds only, including only sites and dates that included the vertebrate exclusion treatment.

    • Table 2 Explanatory power of top SEMs.

      Summary of top SEMs explaining predation intensity for each seed × predator type (from table S2). Data were arcsin-transformed and standardized to means = 0 and SD = 1 before analyses; hence, estimates are for relative comparison only. Full ranking of all 15 SEMs is shown in table S2.

      Predator
      type, seed
      type
      SEM: independent
      variables
      Estimate
      (95% CI)
      R2
      Total
      predation,
      sunflower
      13: Annual
      temperature
      range
      Elevation
      −0.63 (−0.81, −0.44)****
      −0.27 (−0.46, −0.09)**
      0.366
      Total
      predation,
      oats
      13: Annual
      temperature
      range
      Elevation
      −0.32 (−0.54, −0.10)**
      −0.14 (−0.36, 0.08)
      0.095
      15: Latitude
      Elevation
      −0.21 (−0.44, 0.02)*
      −0.12 (−0.35, 0.11)
      0.042
      Invert
      predation,
      sunflower
      15: Latitude
      Elevation
      −0.68 (−0.90, −0.46)****
      −0.46 (−0.68, −0.24)****
      0.39

      *P < 0.05.

      **P < 0.01.

      ****P < 0.0001.

      Supplementary Materials

      • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/5/2/eaau4403/DC1

        Supplementary Methods

        Fig. S1. Photos of field sites and seed predator signs.

        Fig. S2. Mean seed predation by site.

        Fig. S3. Geographic trends in total predation on sunflower versus oat seeds.

        Fig. S4. Large-scale patterns emerged despite variation among the 18 transects.

        Fig. S5. Snow cover could steepen latitudinal and elevational interaction gradients.

        Fig. S6. Correlations between continuous environmental variables.

        Fig. S7. Path diagrams of SEM1 to SEM9.

        Table S1. Transect details.

        Table S2. Relative performance of SEMs.

        Table S3. Multispecies surveys of time to germination.

        References (5175)

      • Supplementary Materials

        This PDF file includes:

        • Supplementary Methods
        • Fig. S1. Photos of field sites and seed predator signs.
        • Fig. S2. Mean seed predation by site.
        • Fig. S3. Geographic trends in total predation on sunflower versus oat seeds.
        • Fig. S4. Large-scale patterns emerged despite variation among the 18 transects.
        • Fig. S5. Snow cover could steepen latitudinal and elevational interaction gradients.
        • Fig. S6. Correlations between continuous environmental variables.
        • Fig. S7. Path diagrams of SEM1 to SEM9.
        • Table S1. Transect details.
        • Table S2. Relative performance of SEMs.
        • Table S3. Multispecies surveys of time to germination.
        • References (5175)

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