Bluefish diet and stable isotope analysis
Direct visual analysis of stomach contents affirmed that bluefish foraging habits are age specific and consistent with documented ontogenetic shifts in diet 30. In this study, the stomachs of 590 age 0 and 121 age 1 + bluefish were examined, of which 66.1% and 52.0% contained prey (Table 1). For age 0 bluefish, 10 unique prey taxa were identified in stomach contents (six teleost and four invertebrate taxa), and age 1 + bluefish consumed seven different prey taxa (five teleost and two invertebrate). The broader diet of age 0 bluefish, relative to older conspecifics, was reflected in the niche breadth index (B = 2.06 and 1.05; Table 1). Specifically, age 0 bluefish consumed vertebrate and invertebrate prey from both the pelagic and benthic realm, whereas age 1 + bluefish fed almost exclusively on pelagic forage fish.
Table 1. Stomach contents of age 0 and age 1 + bluefisha
|Prey taxon||Age 0||Age 1 +|
|Fish|| ||[79.0]||[87.7]|| ||[97.5]||[99.8]|
| Bay anchovy||0.5||0.2||0.00||3.7||1.0||0.10|
| Winter flounder||2.3||3.2||0.27||0.0||0.0||0.00|
| Unidentified fish||44.4||25.9||42.7||14.8||5.8||2.32|
|Crustaceans|| ||[18.5]||[12.2]|| ||[1.3]||[0.19]|
| Copepods and crab/shrimp zoea||23.6||6.3||5.52||0.0||0.0||0.00|
| Grass shrimp||5.1||1.4||0.27||0.0||0.0||0.00|
| Sand shrimp||18.5||8.9||6.14||5.6||1.3||0.19|
| Unidentified decapods||3.7||1.9||0.26||0.0||0.0||0.00|
|Cephalopods|| ||[2.5]||[0.13]|| ||[1.2]||[0.06]|
|Stomachs examined (n)|| ||590|| || ||121|| |
|Stomach with unidentified contents (%)|| ||29.5|| || ||9.4|| |
|Empty stomachs (%)|| ||33.9|| || ||48.0|| |
|Niche breadth index (B)|| ||2.06|| || ||1.05|| |
|Dietary overlap index (α)||0.26|
The dominant prey of age 0 bluefish, with respect to frequency of occurrence (%F), were silversides, planktonic crustaceans, and sand shrimp (Table 1). Collectively, these prey were observed in 18.5 to 34.7% of the stomachs analyzed. Teleost fish accounted for the largest percentage by weight of age 0 bluefish stomach contents (%W = 79.0%), followed by crustaceans (%W = 18.5%) and squid (%W = 2.5%). The order of importance of identifiable prey to the diet of age 0 bluefish, as expressed by the alimentary index (%IA), were as follows: silversides, sand shrimp, planktonic crustaceans, and herring. The remaining identified prey had %IA less than 1% and included striped killifish, juvenile winter flounder, grass shrimp, squid, and gobies. For age 1+ bluefish, Atlantic menhaden and herring were the most utilized prey resource, collectively accounting for 81.5, 87.4, and 96.9% of the %F, %W, and %IA, respectively (Table 1). The remaining identified prey, silversides, sand shrimp, bay anchovy, squid, and scup, were of secondary importance (%IA < 1%).
Although there was no indication of significant competition for prey resources between age 0 and age 1 + bluefish (α = 0.26) 37, appreciable levels of dietary overlap occurred for herring, and to a lesser extent, silversides, sand shrimp, and squid. Resource partitioning still occurred among communal prey, however, such that age 0 bluefish consumed smaller individuals within a defined prey taxon (fish and squid < ∼5 cm < ∼4 cm length). This prey size selectivity by age 0 bluefish agrees with prior accounts from field research and laboratory experiments 27, 44, 45. Moreover, results from this study are consistent with previous analyses of the foraging habits of bluefish collected from the western North and Mid-Atlantic, including Maine (USA) inshore waters 46, New York–New Jersey (USA) estuaries 47, 48, 49, Chesapeake Bay and coastal Virginia (USA) 50, 51, and the inner continental shelf 30, 34. Geographic and seasonal differences in bluefish diet are also reported in the literature, however, and are likely attributable to ontogenetic shifts in habitat use and spatiotemporal variations in prey availability 30, 52.
The visual analysis of a predator's stomach contents provides valuable information on diet composition but is limited to only recent foraging activity. Therefore, nitrogen stable isotope (δ15N) signatures also were used in this study to assess time-integrated feeding history and trophic positioning of bluefish and prey. Mean δ15N values and trophic levels differed significantly across taxa (Tables 2 and 3). Among prey, mean δ15N values ranged between 11.91‰ and 14.91‰, corresponding to trophic levels between 2.44 and 3.48 (Table 2). Scup, silversides, and anchovy had significant 15N enrichment (δ15N > 14‰), and occupied relatively high trophic positions in the food web (trophic level = 3.30–3.48). Conversely, δ15N values were significantly depleted for killifish, menhaden, and planktonic crustaceans (δ15N < 13‰), with calculated trophic levels between 2.44 and 2.75. Spatiotemporal dynamics in environmental conditions (e.g., nutrient loading and nitrogen biogeochemistry) can affect δ15N signatures of prey, as determined in the Narragansett Bay 53. In the present investigation, however, prey were collected over comparable spatial and temporal scales, and thus relative differences in interspecies δ15N signatures are attributed to trophic processes.
Table 2. Comparison of total length, wet weight, nitrogen and carbon isotope (δ15N and δ13C) signatures, estimated tropic level, and total mercury (Hg, ppm wet wt) in bluefish and preya
|Species||n||Length (cm)||Wet wt (g)||δ15N (‰)b||δ13C (‰)b||Trophic level||Hg (ppm)|
| Age 0||478||13.1 (0.1)||32.4 (7.3)||15.58 (0.22)||−16.52 (0.17)||3.55 (0.07)||0.041 (0.001)|
| Age 1 +||154||51.2 (0.9)||1278 (151)||16.09 (0.22)||−17.33 (0.11)||3.71 (0.07)||0.254 (0.007)|
| Anchovyc||39||7.3 (0.1)||2.72 (0.12)||14.39 (0.13)||−18.34 (0.11)||3.30 (0.05)||0.035 (0.001)|
| Grass shrimp||192||1.0 (0.0)||0.40 (0.02)||13.60 (0.20)||−16.46 (0.34)||3.03 (0.07)||0.030 (0.002)|
| Herringc||200||6.1 (0.1)||2.37 (0.15)||13.42 (0.19)||−19.73 (0.47)||2.97 (0.07)||0.028 (0.001)|
| Killifish||91||4.1 (0.1)||0.85 (0.04)||12.79 (0.38)||−16.45 (0.65)||2.75 (0.13)||0.016 (0.001)|
| Menhadenc||32||4.2 (0.2)||0.72 (0.13)||12.08 (0.13)||−18.77 (0.11)||2.50 (0.04)||0.016 (0.002)|
| Plankton||133||-||-||11.91 (0.19)||−19.28 (0.30)||2.44 (0.06)||0.005 (0.001)|
| Sand shrimpc||297||3.8 (0.1)||0.49 (0.02)||13.70 (0.18)||−16.37 (0.38)||3.06 (0.06)||0.021 (0.001)|
| Scupc||58||10.0 (0.5)||23.0 (2.2)||14.91 (0.22)||−17.09 (0.22)||3.48 (0.08)||0.032 (0.002)|
| Silverside||588||8.2 (0.1)||4.46 (0.14)||14.52 (0.14)||−17.02 (0.27)||3.34 (0.05)||0.054 (0.002)|
| Squidc||62||8.7 (0.4)||29.1 (2.4)||13.44 (0.26)||−17.90 (0.22)||2.97 (0.09)||0.037 (0.004)|
| Winter flounderc||313||5.4 (0.1)||3.11 (0.40)||13.82 (0.17)||−16.32 (0.62)||3.10 (0.06)||0.017 (0.001)|
Table 3. Summary statistics for one-way analysis of variance (ANOVA) models testing for mean differences in nitrogen and carbon stable isotope (δ15N and δ13C) signatures, trophic levels, and total mercury (Hg) concentrations among bluefish and prey. Statistical results are also presented for ANOVA models examining the effects of tissue type (muscle vs whole body; Fig. 2A) and tissue location (multiple muscle biopsies; Fig. 2B) on age 0 and age 1 + bluefish total Hg concentrations, respectively.
|Variable||F||Degrees of freedom||p|
|Response||Explanatory|| || || |
|δ15N||Bluefish and prey||36.49||12, 284||< 0.0001|
|δ13C||Bluefish and prey||12.19||12, 284||< 0.0001|
|Trophic level||Bluefish and prey||30.58||12, 284||< 0.0001|
|Hg||Bluefish tissue type||31.96||1, 516||< 0.0001|
|Hg||Bluefish tissue location||0.76||6, 97||0.605|
|Hg||Bluefish age-class||1662.3||1, 631||< 0.0001|
|Hg||Prey||157.76||14, 1958||< 0.0001|
Total length and date of capture were the most significant factors affecting bluefish δ15N signatures, such that fish length and day of year accounted for a cumulative R2 of 0.285 in the stepwise multiple linear regression model (Table 4). Moreover, estimated coefficients for both variables were positive (Table 4), and are explained by 15N enrichment in age 0 bluefish during early ontogeny (Fig. 3A). Specifically, age 0 bluefish between 8 and 12 cm TL experienced a 2.5‰ increase in δ15N values (∼ 78% of one trophic level). This rapid change in δ15N is attributed to the seasonal recruitment of juvenile bluefish into the estuary and the subsequent diet shift from copepod to piscine prey 27, 28. Indeed, stomach content analysis from this investigation showed that age 0 bluefish smaller than 12 cm TL consumed zooplankton (δ15N = 11.91‰), whereas silversides were the dominant prey of larger age 0 bluefish (δ15N = 14.52‰). This observed ontogenetic diet shift in age 0 bluefish would increase trophic position by approximately 81% of one full level.
Table 4. Parameter estimates (standard error [SE]) and summary statistics for stepwise multiple linear regression models used to analyze bluefish nitrogen (δ15N) and carbon (δ13C) stable isotope signatures and total mercury (Hg) concentrationa
|Relationship||Model parameters||F||Degrees of freedom||R2||p|
| Lengthb||0.545||0.200||8.12||1, 39||0.176||< 0.01|
| Day||0.014||0.006||5.63||1, 39||0.109||< 0.05|
| Day||0.017||0.004||13.37||1, 39||0.260||< 0.001|
| Lengthb||−0.392||0.138||8.08||1, 39||0.133||< 0.01|
| Lengthb||0.151||0.003||1858.02||1, 631||0.747||< 0.0001|
| Day||−0.001||0.000||196.57||1, 631||0.060||< 0.0001|
| Longitude||−0.177||0.037||23.30||1, 631||0.007||< 0.0001|
Figure 3. Nitrogen (δ15N) and carbon (δ13C) stable isotope signatures of bluefish (A and B, respectively; n = 40) as a function of total length. Least-squares logarithmic regression models were fit to the full data sets.
Download figure to PowerPoint
Age 0 and age 1 + bluefish had comparable mean δ15N signatures (δ15N = 15.58 and 16.09‰), and bluefish across multiple life stages occupied similar trophic levels (trophic level = 3.55 and 3.71) (Table 2). The similar trophic status of age 0 and age 1 + bluefish is explained by the trophic positioning of their respective prey. Age 0 and age 1 + bluefish feed on prey with collective mean trophic levels of 2.89 and 3.11, respectively. Reevaluating the data for only preferred prey (%IA > 35%), however, revealed that age 0 bluefish (> 12 cm TL) consumed prey of higher trophic status than the preferred prey of age 1 + bluefish (mean trophic level = 3.22 and 2.73 for small silversides and large herring/menhaden, respectively). The reduced trophic position of age 1 + bluefish is attributed to the dietary contribution of menhaden (52, this study); a phytoplanktivorous forage fish that occupies a low trophic level in the estuary (trophic level = 2.50) 26.
Carbon stable isotope (δ13C) signatures were used to differentiate among sources of carbon to the Narragansett Bay ecosystem. Mean δ13C values of bluefish and prey ranged from −19.73‰ to −16.32‰ and varied significantly among taxa (Tables 2 and 3). Evidence of distinct δ13C isotopic groupings within the data (−18 to −19‰ and −16 to −17‰) indicated two principal sources of primary production to the estuary. Specifically, depleted δ13C values denoted phytoplankton-based primary production, whereas enriched isotope values represented a benthic macroalgal carbon source 39. Assuming an increase of −0.5‰ per trophic level, the depleted δ13C signatures of planktonic crustaceans, planktivorous forage fish, and squid suggested that these prey derived carbon from a phytoplankton (pelagic) source (Table 2). Conversely, decapod crustaceans and demersal/benthic fish had enriched δ13C values consistent with a benthic carbon source.
The mean δ13C signatures of age 0 and age 1 + bluefish (−16.52‰ and −17.33‰) indicated that carbon was derived from different trophic pathways (Table 2). The more depleted mean δ13C signature of age 1 + bluefish implies that older fish have an increased reliance on pelagic prey. This supposition is supported by the stomach content data, whereby planktivorous forage fish (herring, menhaden, and anchovy) and squid accounted for more than 97% of the estimated %IA for age 1 + bluefish (Table 1). Conversely, the more enriched δ13C signature of age 0 bluefish is explained by the relative dietary contribution of shrimp and demersal/benthic fish (predominantly silversides), with a cumulative %IA of 46.5%. Moreover, in the stepwise multiple linear regression model, date of capture and total length explained the most variability in bluefish δ13C signatures (cumulative R2 = 0.393; Table 4; Fig. 3B). These results again indicate a subtle ontogenetic diet shift toward pelagic prey as the bluefish aged.
Mercury contamination in bluefish and prey
The initial statistical analysis of bluefish Hg data examined the effects of tissue type (muscle vs whole body) and location (multiple muscle biopsies) on contaminant concentrations (Fig. 2). For age 0 bluefish, total Hg bioaccumulation rates were significantly faster in muscle filets relative to whole bodies (Table 3; Fig. 2A, 2C), thus precluding direct comparisons across the different tissue types. For age 1 + bluefish, no significant difference was seen in the mean total Hg concentration among muscle biopsies performed along the dorsolateral surface (Table 3; Fig. 2B, 2D); thus, Hg concentrations in the D0 biopsy are consistent with levels measured in other locations of the filet. Based on these results, Hg in age 0 and age 1 + bluefish are hereafter reported for isolated muscle filets and D0 biopsies only.
Total Hg concentrations of bluefish collected from the Narragansett Bay ranged from 0.011 to 0.616 ppm (n = 632), with mean values equal to 0.041 and 0.254 ppm for age 0 and age 1 + bluefish, respectively (Table 2). These observed Hg concentrations differ from values reported for bluefish from other geographic areas. Bluefish from the Long Island Sound and the greater New York Bight (Long Island Sound: mean TL = 40.6 cm; n = 46; New York Bight: mean TL = 53.3 cm; n = 14), for example, had mean MeHg and total Hg concentrations equal to 0.137 ppm (Hg ∼ 0.130 ppm assuming %MeHg = 95%) and 0.102 ppm, respectively 19, 54. These contaminant levels are 62 to 145% lower than the predicted Hg content of bluefish from the Narragansett Bay; bluefish of consistent sizes had projected Hg concentrations of 0.210 to 0.250 ppm (Table 2; Fig. 4). In contrast to these findings, bluefish sampled from coastal New Jersey had increased Hg levels (mean Hg = 0.345 ppm; mean TL = 46.3 cm; n = 206) relative to the same-sized fish from the Narragansett Bay (0.229 ppm; Table 2; Fig. 4) 55.
Figure 4. Total Hg concentrations of bluefish muscle tissue (n = 632) as a function of total length. A least-squares logarithmic regression model was fit to the full data set.
Download figure to PowerPoint
Previous investigations report that bluefish Hg concentrations vary over relatively broad spatial and temporal scales 18, 19, 55, which is attributed to localized differences in Hg loadings to the environment, as well as in situ sediment MeHg production and mobilization 20. Moreover, the extent to which MeHg biomagnifies in estuarine and marine food webs is affected by spatiotemporal dynamics in resident prey populations. This is especially relevant to bluefish because of their expansive coastal migrations and ontogenetic shifts in diet and habitat use. Accordingly, a complete evaluation of Hg contamination in this species would benefit from a synoptic examination over broad spatial scales and protracted temporal periods 55.
Bluefish muscle Hg concentrations were affected by its physical attributes. Foremost, total Hg increased significantly with bluefish length, despite concentrations being highly variable in age 1 + fish (stepwise regression: length; partial R2 = 0.747; Table 4; Fig. 4). Comparable Hg-length (or weight) trends have been reported for bluefish in the Long Island Sound and coastal New Jersey 18, 19, 54, as well as other estuarine and coastal fishes from the northwestern Atlantic 6, 7, 54, 56. The significant positive correlation between bluefish muscle Hg and length affirms that Hg biomagnifies in this tissue, and is likely attributable to the rapid uptake of the contaminant relative to its excretion from the body 21, 57. Alternatively, Hg elimination rates may be negatively correlated with bluefish body size, as demonstrated in several freshwater and marine finfish species 57. Bluefish total Hg concentrations also varied over relatively small spatiotemporal scales in the estuary (longitude and date of capture; Table 4), although these variables accounted for only 6.7% of the observed variation in fish Hg content.
The biomagnification of Hg in bluefish was maximal during early life stages and decelerated over time (Fig. 4). Similarly, Burger 55 observed high rates of Hg bioaccumulation in bluefish between 11 to 25 cm fork length (∼ 17–36 cm TL), after which Hg concentrations remained relatively constant for fish 26 to 50 cm fork length (∼37–68 cm TL). Burger 55 also observed rapid Hg accumulation in bluefish larger than 50 cm fork length, but this larger size class was not examined in the current study. Nevertheless, the pattern of Hg biomagnification for bluefish 6 to 70 cm TL is atypical of estuarine and marine fish, where the standard response is an exponential increase in Hg throughout the entire life history of the fish 6, 7, 42, 54. Consequently, early-stage bluefish have increased Hg concentrations relative to similarly aged estuarine and coastal fishes, with possible deleterious effects to both the individual (e.g., compromised behavior and growth) and population (e.g., reduced survival and recruitment success) 18. The unusually high rate of Hg biomagnification in juvenile bluefish is attributed to its diet and high trophic status in the estuary, as discussed previously.
Results from previous investigations in the Narragansett Bay indicate that dietary preference and trophic processes are key factors affecting Hg bioaccumulation in the estuary 6, 7. Accordingly, Hg is transferred through the estuarine food web via predator–prey interactions, and high trophic level fishes have increased contaminant exposure because they feed on Hg-enriched prey 58. To evaluate the effect of food preference on bluefish Hg concentrations, the main prey of bluefish were collected from the estuary and analyzed for whole-body Hg content. Prey common to the diet of both age 0 and age 1 + bluefish were divided into specific length categories (demarcation length = 5.0 cm for herring, silversides, and squid and 4.0 cm for sand shrimp), such that specimens smaller and larger than the demarcation length were defined as age 0 and age 1 + bluefish prey, respectively. Mean Hg concentrations of bluefish prey varied significantly across species (Tables 2 and 3; Fig. 5). Collectively, age 0 bluefish consumed prey with a lower mean Hg concentration than the prey of age 1 + bluefish (0.021 and 0.035 ppm, respectively). With respect to preferred prey (%IA > 35%; Table 1), however, the Hg concentration of age 0 and age 1 + bluefish prey were equivalent (0.021 ppm for small silversides and large herring/menhaden; Fig. 5). These results strongly suggest that age 0 bluefish are highly responsive to prey Hg contamination 18, 58, which in turn partly explains the rapid accumulation of Hg during the juvenile life stage.
Figure 5. Total Hg concentrations (mean + standard error) of prey whole bodies: Atlantic silverside (n = 471 and 117 for small and large, respectively), long-finned squid (n = 54 and 8 for small and large, respectively), bay anchovy (n = 39), scup (n = 58), sand shrimp (n = 96 and 155 for small and large, respectively), herring (n = 40 and 160 for small and large, respectively), grass shrimp (n = 192), winter flounder (n = 313), killifish (n = 91), Atlantic menhaden (n = 32), and zooplankton (n = 133). Unique letters above histogram bars indicate significant differences in mean prey Hg concentrations (Ryan's Q multiple comparison test).
Download figure to PowerPoint