Research ArticleECOLOGY

Direct quantification of energy intake in an apex marine predator suggests physiology is a key driver of migrations

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Science Advances  25 Sep 2015:
Vol. 1, no. 8, e1400270
DOI: 10.1126/sciadv.1400270
  • Fig. 1 Extracts of raw data collected by an archival tag implanted into the peritoneal cavity of a wild juvenile Pacific bluefin tuna in 2003.

    (A to C) One month of data (A); 1 week of data (B); one HIF event (over 16 to 17 October) (C). In (A) to (C), the red line shows visceral temperature, the blue line shows ambient temperature, and the green line shows the predicted resting visceral temperature [obtained using a statistical model (22)]. (D) Monthly mean HIF from the raw data for archival tagged Pacific bluefin tuna in the California Current between 2002 and 2009. Vertical bars extend to 1.96 SE below and above the mean.

  • Fig. 2 Tracks with estimated HIF (kcal day−1) for two archival tagged bluefin tuna.

    Tracks are broken into yearly sections, and the first point in each panel is marked with a white triangle. (A to C) HIF track for archival tag 1002020, deployed in August 2002. White triangles correspond to 28 August 2002 (A), 1 January 2003 (B), and 1 January 2004 (C). (D to F) HIF track for archival tag 1003088, deployed in July 2003. White triangles correspond to 7 August 2003 (D), 1 January 2004 (E), and 1 January 2005 (F).

  • Fig. 3 HIF in relation to SST, latitude, and chl-a.

    (A) Three-dimensional contour plot for observed daily energy intake in 2003 (interpolated and smoothed for visualization) against mean daily SST and latitude. (B) Latitudinal distribution of 144 tagged bluefin tuna in the California Current, 2002 to 2007. (Top) Date versus latitude with remotely sensed mean daily SST (°C) indicated by the color scale. (Center) Date versus latitude with median daily energy intake (kcal) indicated by the color scale. (Bottom) Date versus latitude with the logarithm of median daily chlorophyll-a concentration (mg m−3) indicated by the color scale. The solid black line in each panel denotes the median latitude of archival tagged tuna, whereas the dashed lines show the 2.5th and 97.5th percentiles for the latitudinal distribution.

  • Fig. 4 Predicted values for average daily energy intake (kcal) by month from the final GAMM fitted to HIF data between 2002 and 2009 (data from 144 archival tagged Pacific bluefin tuna with 5961 weekly values of HIF).

    Predicted values are plotted within the 90% utilization density (UD) contour; the 50% (solid line) and 75% (dashed) line UD contours are indicated.

  • Fig. 5 Correlates of average daily energy intake (kcal) in tagged Pacific bluefin tuna.

    Estimated response curves (smooth terms) and year effects from the final GAMM. (A to D) SST (A), length of the tagged tuna (B), chlorophyll-a concentration (C), and isothermal layer depth (D). Dashed lines represent 95% confidence limits. Vertical axes are partial responses (estimated, centered smooth functions) on the scale of the linear predictor.

  • Fig. 6 Patterns of habitat use and energy intake by length for archival tagged Pacific bluefin tuna between 2002 and 2009.

    (A) Utilization densities for archival tagged Pacific bluefin tuna in the California Current in October solid line, 50% density contour; dashed lines, 10 and 90% density contours left 95 cm and smaller; center 95 to 119 cm; right larger than 119 cm. (B) Mean HIF by month and age class (age 2.5 and younger, red; age 2.5-3.5, black; age 3.5 and older, blue). Error bars indicate ±1 SE. (C) Boxplots showing the monthly latitudinal distributions of Pacific bluefin tuna of different ages in the California Current (age 2.5 and younger, red; age 2.5-3.5, white; older than 3.5 years, blue). Horizontal lines through the center of each box denote the median, whereas the ends of the box denote the upper and lower quartiles. Whiskers denote the range containing 95% of observations.

  • Table 1 Correlates of the magnitude of weekly average energy intake.

    Entries are approximate percentage deviance explained by term (of the total deviance explained by the model) for the final GAMM for daily energy intake (kcal), adjusted R2 = 34%.

    GAMM termApproximate deviance explained (%)Estimated degrees of freedomApproximate significance level
    Year (factor)3NASee fig. S5
    s(Latitude, longitude)2726.7P < 0.001
    s(Sea surface temperature, °C)266.7P < 0.001
    s(Isothermal layer depth, m)36.8P < 0.001
    s[Log(chlorophyll-a, mg m−3)]103.3P < 0.001
    s(Eddy kinetic energy, cm2 s−2)41.0P < 0.001
    s(Relative light level)97.9P < 0.001
    s(Length, cm)81.3P < 0.001
    s(Day of the year)1212.9P < 0.001

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/1/8/e1400270/DC1

    Fig. S1. Spatial plot of the data set analyzed in this paper by month.

    Fig. S2. Raw data (visceral temperature, red line; ambient temperature, blue line) trace from an archival tagged Pacific bluefin tuna.

    Fig. S3. Raw data (visceral temperature, red line; ambient temperature, blue line) trace from a second archival tagged Pacific bluefin tuna.

    Fig. S4. Tracks with estimated median HIF (kcal day−1) for two archival tagged Pacific bluefin tuna.

    Fig. S5. Correlates of average daily energy intake (kcal) in tagged Pacific bluefin tuna.

    Fig. S6. HIF in relation to SST, latitude, and chl-a.

    Fig. S7. Predicted values for weekly mean thermal excess (°C) plotted by quarter from the final GAMM fitted to thermal excess data between 2002 and 2009 (data from 144 archival tagged Pacific bluefin tuna with 5961 weekly values of thermal excess).

    Fig. S8. Patterns of habitat use and energy intake by length for archival tagged Pacific bluefin tuna between 2002 and 2009.

    Fig. S9. Physiological responses to ambient temperature with mean energy intake.

    Fig. S10. Boxplot of posterior predictive probability distributions for estimated energy intake (kcal) for three archival tagged Pacific bluefin tuna in the feeding experiment (22).

    Fig. S11. Histograms of HIF magnitude observations.

    Fig. S12. Estimated smooth terms from the GAMM for feeding success in archival tagged Pacific bluefin tuna.

    Fig. S13. Predicted feeding success between September 2002 and August 2003 from the binomial GAMM for a subset of archival tagged Pacific bluefin tuna (23 tagged individuals, 6705 observations) released in August 2002.

    Fig. S14. Predicted HIF magnitude (conditional on feeding on a given day) between September 2002 and August 2003 from the Gamma GAMM for a subset of archival tagged Pacific bluefin tuna (23 tagged individuals, 6212 observations) released in August 2002.

    Fig. S15. GAMM-predicted values from the delta-gamma model for HIF magnitude (combining predictions of feeding success and HIF magnitude) between September 2002 and August 2003 for a subset of archival tagged Pacific bluefin tuna (23 tagged individuals, 6212 observations) released in August 2002.

    Table S1. Proximate analysis of sardine and anchovy used as feeds for captive tuna, reproduced from Farwell (43).

    Table S2. Priors in the hierarchical Bayesian regression model.

    Table S3. Wilcoxon rank sums (from two-sided tests) for size-based differences in latitude, SST, and HIF.

    Table S4. Correlates of thermal excess.

    References (3643)

  • Supplementary Materials

    This PDF file includes:

    • Fig. S1. Spatial plot of the data set analyzed in this paper by month.
    • Fig. S2. Raw data (visceral temperature, red line; ambient temperature, blue line) trace from an archival tagged Pacific bluefin tuna.
    • Fig. S3. Raw data (visceral temperature, red line; ambient temperature, blue line) trace from a second archival tagged Pacific bluefin tuna.
    • Fig. S4. Tracks with estimated median HIF (kcal day−1) for two archival tagged Pacific bluefin tuna.
    • Fig. S5. Correlates of average daily energy intake (kcal) in tagged Pacific bluefin tuna.
    • Fig. S6. HIF in relation to SST, latitude, and chl-a.
    • Fig. S7. Predicted values for weekly mean thermal excess (°C) plotted by quarter from the final GAMM fitted to thermal excess data between 2002 and 2009 (data from 144 archival tagged Pacific bluefin tuna with 5961 weekly values of thermal excess).
    • Fig. S8. Patterns of habitat use and energy intake by length for archival tagged Pacific bluefin tuna between 2002 and 2009.
    • Fig. S9. Physiological responses to ambient temperature with mean energy intake.
    • Fig. S10. Boxplot of posterior predictive probability distributions for estimated energy intake (kcal) for three archival tagged Pacific bluefin tuna in the feeding experiment (22).
    • Fig. S11. Histograms of HIF magnitude observations.
    • Fig. S12. Estimated smooth terms from the GAMM for feeding success in archival tagged Pacific bluefin tuna.
    • Fig. S13. Predicted feeding success between September 2002 and August 2003 from the binomial GAMM for a subset of archival tagged Pacific bluefin tuna (23 tagged individuals, 6705 observations) released in August 2002.
    • Fig. S14. Predicted HIF magnitude (conditional on feeding on a given day) between September 2002 and August 2003 from the Gamma GAMM for a subset of archival tagged Pacific bluefin tuna (23 tagged individuals, 6212 observations) released in August 2002.
    • Fig. S15. GAMM-predicted values from the delta-gamma model for HIF magnitude (combining predictions of feeding success and HIF magnitude) between September 2002 and August 2003 for a subset of archival tagged Pacific bluefin tuna (23 tagged individuals, 6212 observations) released in August 2002.
    • Table S1. Proximate analysis of sardine and anchovy used as feeds for captive tuna, reproduced from Farwell (43).
    • Table S2. Priors in the hierarchical Bayesian regression model.
    • Table S3. Wilcoxon rank sums (from two-sided tests) for size-based differences in latitude, SST, and HIF.
    • Table S4. Correlates of thermal excess.
    • References (36–43)

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