Environ. Sci. Technol. 1996, 30, 654
Influence of Trophic Position and Feeding Location on Contaminant Levels in the Gulf of the Farallones Food Web Revealed by Stable Isotope Analysis
values in the food web. Lower values of δ15N in egg albumen than in the muscle tissue from common murres reflect a switch in diet to a lower trophic position during the egg formation period. The high contaminant levels in the murre suggest a mobilization of stored lipids into the eggs.
Introduction W A L T E R M . J A R M A N , * ,† KEITH A. HOBSON,‡ WILLIAM J. SYDEMAN,§ CORINNE E. BACON,† AND ELIZABETH B. MCLAREN§ Institute of Marine Sciences, University of California, Earth and Marine Sciences Building, Santa Cruz, California 95064, Prairie and Northern Wildlife Research Centre, Canadian Wildlife Service, 115 Perimeter Road, Saskatoon, Saskatchewan, S7N OX4, Canada, and PRBO International Biological Research, 4990 Shoreline Highway, Stinson Beach, California 94970
In this study, we present the levels of organochlorine (∑DDT, ∑HCH, ∑chlordane, HCB, and ∑PCBs) and metal (Pb, Hg, and Se) contaminants and their relationship to stable carbon and nitrogen isotope values in the Gulf of the Farallones marine food web. This food web consisted of two species of euphausiids (Euphausia pacifica and Thysanoessa spinifera), two fish species [short-bellied rockfish (Sebastes jordani) and anchovy (Engraulis mordax)], four bird species [common murre (Uria aalge), Brandt’s cormorant (Phalacrocorax penicillatus), rhinoceros auklet (Cerorhinca monocerata), and pigeon guillemot (Cepphus columba)], and the northern sea lion (Eumetopias jubatus). We used a novel method of using egg albumen to determine stable isotope values. The values of δ13C ranged from -20.1‰ in the euphausiids to -15.0‰ in the northern sea lion and were consistant with a pelagic/offshore vs benthic/inshore results found in other studies. Values of δ15N in the Gulf of the Farallones food web ranged from 11.2‰ in the euphasiids to 19.8‰ in the northern sea lion and generally demonstrate an equivalence with trophic level. The levels of organochlorine compounds were lowest in the euphausiids [∑DDT 11, and ∑PCB 4.5 µg/kg dry weight geometric mean (GM)] and highest in the northern sea lion blubber (∑DDT 9500 and ∑PCB 3500 µg/kg dry weight GM). The highest levels of organochlorine compounds in the birds were in the common murre (∑DDT 8200 and ∑PCB 5900 µg/kg dry weight GM). Levels of Pb, Hg, and Se ranged from 80 to 1000, from 100 to 19000, and from 1900 to 4100 µg/kg dry weight GM, respectively. All of the organochlorine compounds and Hg were significantly correlated with δ15N
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Essential to understanding contaminant pathways and influences in any ecosystem is a knowledge of trophic relationships within those systems. In most productive marine food webs, trophic relationships are complex, involving numerous species and prey alternatives. Traditional analyses of marine food chains consisted of direct field observations, gut content analysis, or radiotracer methods to elucidate food web interactions. Recently, stable isotopes of C, N, S, and H have been used as tracers in examining the trophic relationships and/or origins of prey in marine food webs (1, 2). The most commonly used stable isotopes in marine food web studies are 13C and 15N (1). In general, 15N abundance increases (enriches) relative to 14N at approximately 3-5‰ per trophic level (1). Trophic enrichment of 13C also occurs but the increase is minor (approximately 1‰), and often there is no net increase (1, 3). Carbon-13 also shows greater enrichment in inshore or benthic food webs relative to offshore or pelagic food webs (ref 4, reviewed by France in refs 5 and 6). Lipophillic persistent organic compounds have been shown to bioconcentrate and biomagnify with increasing trophic levels (7). Broman et al. (8, 9) combined the analysis of stable isotopes and organochlorine contaminants to examine trophic level biomagnification of polychlorinated dibenzo-p-dioxins (PCDDs) and polychlorinated dibenzofurans (PCDFs) in two northern Baltic food webs. They found that the enrichment of 15N was strongly associated with concentrations of PCDD and PCDFs, and the biomagnification factor of three PCDDs and the biodepuration of octachlorodibenzo-p-dioxin (OCDD) and octachlorodibenzofuran (OCDF) in the food chains could be quantified using N isotopes. Kidd et al. (10) also found a strong relationship between total hexachlorocyclohexane (ΣHCH), total DDT (ΣDDT), total chlorinated bornanes (ΣCHB), and trophic position as defined by δ15N in a subarctic freshwater lake. The Farallon Islands supports the largest and most diverse marine bird and mammal colony in the continental United States (11-13). Despite this productivity and biologically diversity, the overall health of this ecosystem is in question. Many bird populations on the Islands have declined (11). Disposal of both radioactive and chemical wastes occurred at two sites southwest of the Farallon Islands from 1946 to 1962 (14), and Melzian et al. (14) found levels of organochlorine compounds in fish collected from * Corresponding author telephone: (408) 459-3769; fax: (408) 4594882; e-mail address:
[email protected]. † University of California. ‡ Canadian Wildlife Service. § PRBO International Biological Research.
0013-936X/96/0930-0654$12.00/0
1996 American Chemical Society
near the Farallon Islands to be higher than fish collected in other highly contaminated southern California waters. Gress et al. (15) found high DDE levels (297 mg/kg lipid weight) and eggshell thinning of 13% in common murre eggs collected on the Farallon Islands in 1968 and 1970. Future plans for ocean dumping near the Farallones and the discharge of agricultural, industrial, and urban chemicals into San Francisco Bay may also introduce contaminants into the Farallon ecosystem (16, 17). In this study, we develop further the application of stable isotope analysis as a means of investigating the influence of trophic position and feeding source of organisms within marine food webs on levels of contaminants. Our investigation consisted of a stable isotopic analysis of components of a food web based in the Gulf of the Farallones central California comprised of euphausiids (Euphausia pacifica and Thysanoessa spinifera), two fish species [shortbellied rockfish (Sebastes jordani) and anchovy (Engraulis mordax)], four bird species [common murre (Uria aalge), Brandt’s cormorant (Phalacrocorax penicillatus), rhinoceros auklet (Cerorhinca monocerata), and pigeon guillemot (Cepphus columba)], and the northern sea lion (Eumetopias jubatus). We present the relationship between selected metal and organochlorine compounds in this food web and the δ13C and δ15N values of consumer tissues. We use the novel isotopic analysis of seabird egg albumen as a means of linking dietary patterns of laying females with contaminant levels in their eggs (18).
Materials and Methods Sample Collection. Euphausiid samples were collected by biologists aboard National Marine Fisheries Service RV David Starr Jordan in February 1994. Age-class short-bellied rockfish and anchovy samples were obtained in June and July 1993 while netting rhinoceros auklets on the Farallon Islands during the chick-rearing period. We collected egg samples from marine birds nesting on the Farallon Islands and An ˜ o Nuevo Island in May, June, and July 1993. Steller sea lion liver, brain, and blubber samples primarily from dead pups were collected on An ˜ o Nuevo Island from June through December 1993. Sample Preparation. All samples were prepared in a clean room using metal and organic contaminant-free dissection tools and homogenized using a precleaned blender equipped with a titanium blade assembly. Organic samples were stored in precleaned glass jars, and samples for metals analysis were stored in precleaned polyethylene jars. The eupausiid and fish samples consisted of homogenized composites. Whole bird eggs were first subsampled for albumin and yolk, then blended individually, and analyzed. Stable Isotope Analysis. Egg albumin, euphausiid composites, whole fish composites, and sea lion muscle were freeze-dried and powdered using an analytical mill. Lipids were removed from all samples using a Soxhlet apparatus for 4-6 h with chloroform as a solvent. Euphausiid samples were also treated with 1 N HCl to remove carbonates before isotopic analysis. Samples for δ13C and δ15N analysis were loaded in Vycor tubes with wire-form CuO, silver foil, and elemental Cu, then sealed under vacuum, and combusted at 800 °C for at least 6 h. Carbon dioxide and nitrogen gas were then separated cryogenically and analyzed using a VG Optima isotope ratio mass spectrometer at the National Hydrology Research Institute,
Saskatoon, Saskatchewan. Stable isotope concentrations are expressed in δ notation as parts per thousand (‰) according to the following:
δX ) [(Rsample/Rstandard) - 1] × 1000 where X is 15N or 13C and R is the corresponding ratio 15N/ or 13C/12C. Rstandard for 15N and 13C are atmospheric N (air) and the PDB standard, respectively. Replicates using glycine (nitrogen) and lentil (carbon) standards indicate analytical error of (0.3 and 0.1‰, respectively. Organochlorine and PCB Determination. The analytical methodology used for organochlorine and PCB determinations is a modification of Jarman et al. (19). A brief description of the methods used in this study are as follows: An accurately weighed subsample of homogenate was spiked with a surrogate standard and ground with anhydrous sodium sulfate to remove excess moisture. The sample was then solvent extracted with 50% hexane/ dichloromethane (DCM) and reduced on a rotary evaporator, and lipid weight was determined. Florisil columns were used to separate each extract into two different fractions. Prior to analysis, each sample was spiked with a gas chromatography internal standard (GCI standard) to account for volume differences among samples. Fractions were analyzed on a Hewlett-Packard (HP) 5890 Series II gas chromatograph (GC) equipped with a 63Ni electron-capture detector and a HP 7673A automatic sampler. Two 60 m, 0.25 mm i.d., 0.25 mm (film thickness), DB-5 and DB-17 columns (J&W Scientific) were used to provide dual-column confirmation. Standard Reference Material, spiked egg matrices, and 10% duplicate samples were analyzed under identical conditions as samples to ensure quality control. Total DDT (ΣDDT) was calculated from the sum p,p′DDE, p,p′-DDT, and p,p′-DDD. ΣPCB (total polychlorinated biphenyl) was calculated from the sum of 45 individual congeners. ΣChlordane (total chlordane) was calculated from the sum of six chlordane compounds (oxychlordane, heptachlor epoxide, cis-chlordane, trans-chlordane, cisnonachlor, and trans-nonachlor. ΣHCH (total hexachlorocyclohexane) is the sum of four HCH compounds (RHCH, β-HCH, λ-HCH, and δ-HCH). Metal Determinations. Samples were prepared for analysis by a nitric acid/hydrogen peroxide digestion. The extracts were diluted using deionized/distilled water and analyzed by the following techniques: Selenium was analyzed using a Perkin Elmer Model 5000 dual-beam atomic absorption spectrophotometer coupled to a PerkinElmer Model MHS-20 automated hydride generation system (U.S. EPA Method 7000). Lead was analyzed using a Varian Model Spectra AA-300 single-beam atomic absorption spectrophotometer equipped with an automatic Zeeman background-corrected electrothermal atomizer (U.S. EPA Method 7000). Mercury was analyzed using a Pharmacia Model UV mercury monitor equipped with a 30-cm absorption cell (U.S. EPA Method 7000). Statistics. Data analysis was performed on an IBMcompatible microcomputer using the software Minitab (release 9 for Windows) (20). All concentrations are reported as milligram per kilogram (mg/kg) of the dry weight.
14N
Results and Discussion Stable Isotopes. The values of δ13C in the Gulf of the Farallones food web ranged from -20.1‰ in the euphausiids to -15.0‰ in the northern sea lion (Table 1).
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TABLE 1
Stable Isotope Composition of Organisms in the Gulf of the Farallones Food Weba nb invertebrates euphausiid fish Sebastes jordani Engraulis morax marine birds Uria aalge egg albumen muscle Phalacrocorax penicillatus egg albumin muscle Cerorhinca monocerata egg albumen muscle Cepphus columba egg albumen muscle marine mammals Eumetopias jubatus (muscle)
δ13C
δ15N
5*
-20.1 ( 0.3
5* 4*
-16.8 ( 0.4 A 13.7 ( 0.4 A -16.8 ( 0.4 A 13.9 ( 0.8 AB
13 3
-16.9 ( 0.5 A 15.0 ( 1.0 B -16.6 ( 0.4 17.3 ( 0.7
7 -15.9 NM
11.2 ( 0.5
17.3 ( 0.2 C
5 2
-17.7 ( 0.8 B 17.1 ( 0.4 C -17.1 ( 0.6 17.8 ( 1.0
12 2
-17.7 ( 0.2 B 16.9 ( 0.6 C -16.2 ( 0.2 15.3 ( 0.6
5
-15.2 ( 0.5
19.8 ( 0.6
Values are given as X ( SD in ‰. Species that share a letter are not significantly different (Tukey’s test of means, p > 0.05). Bird muscle was not used in the statistical analysis. b An asterisk (*) indicates that samples were composite samples (>5 individuals). a
The values of δ13C in the eight species were significantly different (ANOVA, F ) 108, df ) 7 and 54, p < 0.001). A Tukey’s test was used to determine between which species significant differences existed. It was found that the mean of the rockfish, anchovy, and common murre was similar, as was the rhinoceros auklet and pigeon guillemot. The δ13C values of the euphausiids, Brandt’s cormorants, and northern sea lion samples were not statistically similar to any other species in the food web. The values of δ13C in this study are consistent with a pelagic/offshore vs benthic/inshore results found elsewhere in the Pacific (21) and high Arctic (22). The euphausiids are known to be epipelagic offshore feeders (23), and they have the most negative δ13C values in this study (Table 1 and Figure 1). The rockfish and anchovy are both planktophagous; however, adult rockfish feed exclusively on euphausiids, while anchovies will also feed on fish (24, 25). The δ13C values of the rockfish and anchovy (-16.8‰) show some enrichment of 13C over the euphausiids (-20.1‰) (Table 1 and Figure 1). In general, the intermediate δ13C values of the marine bird species in this study are consistant with field observations of diet (26, 27). During breeding, pigeon guillemots feed on small demersal and midwater fishes in the neritic zone. Rhinoceros auklets diet is dominated by midwater and demersal fishes most often found further offshore on the Continental Shelf. Brandt’s cormorants primarily feed on midwater fish, but demersal fish in neritic waters and coastal estuaries also are taken in significant numbers. Northern sea lions feed on fish, cephalopods, and a small percentage of birds (28). As opposed to those of carbon, nitrogen isotope ratios have been reported to show a strong relationship with trophic position, with an increase of approximately 2-3.5‰ per tropic level (1, 3). Values of δ15N in the Gulf of the Farallones food web ranged from 11.2‰ in the euphasiids to 19.8‰ in the northern sea lion and generally demonstrate an equivalence with trophic level (Table 1 and Figure 1).
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The values of δ15N were significantly different between species (ANOVA, F ) 25.40, df ) 7 and 54, p < 0.001). As with δ13C, the δ15N values in euphausiids and northern sea lions were not statistically related to any other species in the Gulf of the Farallones food web (Tukey’s test of means) (Table 1). Groups that were statistically similar using Tukey’s test were rockfish and anchovy; anchovy and the common murre; Brandt’s cormorant, rhinoceros auklet, and pigeon guillemot (Table 1). Stable isotope ratios in consumer tissues provide dietary information that is integrated over various time periods, which is dependent on the metabolic rate of the tissue being examined (1, 29-32). Components of eggs also represent dietary integrations based on different periods of formation during egg production. Hobson (18) determined that isotope ratios in albumen represent the diet of the laying female over a few days before egg laying, and so our isotopic data represents a relatively short dietary period. Common murres are primarily piscivorous except during the breeding season when they switch their diets to a large percentage of euphausiids prior to egg laying (26). This was reflected in the relatively low δ15N value for albumen in this species (Table 1). In contrast, the measurement of muscle tissue salvaged from common murres from this area confirmed that long-term diet was at a higher trophic level and was consistent with an expected piscivorous diet (Table 1). Contaminant Levels. The levels of contaminants in the Gulf of the Farallones food web are presented in Table 2. Melzian et al. (14) reported organochlorine levels in dover sole (Microstomus pacificus) and sablefish (Anoplopoma fimbria) collected from the Farallon Islands in the 1980s that were nearly as high as the same species in heavily contaminated waters off southern California. Although it is difficult to establish trends in contaminant profiles between different age-classes and species, it is interesting to note that the averaged level of ∑DDT was over 500 times lower in rockfish and anchovy from 1994 when compared with dover sole and sablefish from 1985 (51 verses 43 000 mg/kg, assuming 80% water). Investigations of contaminant levels in marine birds from the Farallon Islands from the 1970s documented high levels of DDE and PCB in both the common murre (15) and the ashy petrel (Oceanodroma homochroa) (33); both studies concluded that elevated organochlorine levels may be associated with eggshell thinning in marine birds breeding at the Farallon Islands. Levels of DDE in murres have decreased nearly 15-fold since 1971, from 115 000 (assuming 80% water in the eggs) to 8200 µg/kg, while PCB levels have decreased nearly 20 times, from 110 000 (assuming 80% water in the eggs) to 5900 µg/kg. Organochlorine levels were documented in 1983 for northern sea lions from the Gulf of the Farallones, investigating the possible relationship between contaminants and premature pupping (34). Huber (34) reported DDE and PCB levels for seven premature sea lion fetuses (blubber and brain tissue). DDE and ΣPCB levels in blubber have decreased dramatically over the period 1983-1994 from 133 000 to 9500 µg/kg for DDE levels and from 133 000 to 3500 µg/kg for PCB levels. The PCB trend data for the murre and sea lion data should be evaluated with caution since ∑PCB values in this study were calculated from the sum of 45 congeners (see methods), while data from refs 15 and 34 were calculated from Aroclor mixtures, a technique that may falsely elevate PCB levels by a factor of 2 or more (35).
FIGURE 1. Relationship of δ13C and δ15N values (averages and standard deviations) of marine food web organisms from the Gulf of the Farallones. Abbreviations for the species are as follows: EUPH, Euphausia pacifica and Thysanoessa spinifera; ROCKFISH, Sebastes jordani; ANCH, Engraulis mordax; COMU, Uria aalge; BRCO, Phalacrocorax penicillatus; RHAU, Cerorhinca monocerata; PIGU, Cepphus columba; and EUJU, Eumetopias jubatus.
Tanabe et al. (36) reported that the relative PCB congener composition shifted from a higher percentage of lower chlorinated congeners (i.e., chlorobiphenyls with two to four chlorines) to a higher percentage of heavily chlorinated congeners (i.e., six to nine chlorines) with increasing trophic position in a western North Pacific ecosystem. Patterns of chlorobiphenyls have also been shown to vary with location in marine biota and air, with pelagic locations having a higher percentage of lower chlorinated congeners than inshore areas (37, 38). In general, the data in this study reflect both of these reported trends. The percentage of higher chlorinated congeners increases with trophic position for the euphausiids, fish, and birds; however, the northern sea lion has an intermediate profile (Table 2 and Figure 2). Within the bird species, the most pelagic feeder has the highest percentage of lower chlorinated congeners, and the nearshore feeding Brandt’s cormorant has a greater proportion of the higher chlorinated congeners (Table 2 and Figure 2). The common murre, which has the highest levels of both ΣDDT and ΣPCB of the bird species, also has the highest percentage of higher chlorinated congeners (Table 2 and Figure 2). The levels of mercury (Hg), lead (Pb), and selenium (Se) in the Gulf of the Farallones food web are presented in Table 2. Both Pb and Hg are nonregulated metals and have been reported to bioaccumulate in marine food webs (39). Lead levels showed a significant difference in the food chain (ANOVA, F ) 4.0, df ) 7 and 37, p ) 0.003). Levels of Pb decreased with increasing trophic level, which probably reflects the biodepuration of Pb (accumulation of Pb in hard tissues) in the food chain (39). However, the difference in matrix sampled (e.g., whole body versus egg versus liver) makes interpretation difficult (40). Mercury levels in the food chain were significantly different (ANOVA, F ) 62.53, df ) 7 and 55, p < 0.001); levels increased with increasing trophic levels. As with the Pb data, the egg data must be interpreted with caution. Mercury has been shown to have pronounced age-related
concentration changes and variation between species and is one of the most toxic metals (39). Data from the Gulf of the Farallones food web food chain indicate biomagnification of Hg at each level of the food chain. Selenium levels in the food chain were statistically different (ANOVA, F ) 2.56, df ) 7 and 55, p ) 0.025). However, levels in the bird eggs were not different. Several studies indicated that bioconcentrations of metals can increase with increasing trophic level up to the level of fish; once at this level, however, a decline in concentration was usually noted (41). The concentration of selenium found at different levels in this food web nicely followed this description of metals bioconcentration, e.g., an increase in concentration up to the level of fish with a decrease in the food web above fish. Integrating Stable Isotope and Contaminant Data. Broman et al. (8, 9) found that the fractionation of 15N was strongly associated with the PCDD and PCDFs and that the biomagnification factor of three PCDDs and the biodepuration of octachlorodibenzo-p-dioxin (OCDD) and octachlorodibenzofuran (OCDF) in the food chains could be quantified using δ15N. They developed an equation relating the regression of the δ15N to contaminant concentration of the form e(A+B*δ15N), where A is a constant dependent on background concentration, and B was the change in concentration per unit of δ15N over the entire food chain (8). Positive values of B indicate that a substance is biomagnified in the food web, and negative values indicate biodepuration of the compound. Kidd et al. (10) found a strong relationship between ΣHCH, ΣDDT, total chlorinated bornanes (ΣCHB), and trophic position as defined by δ15N in a subarctic freshwater lake. They also used regression equations of the logarithmic wet and lipid weight concentrations versus the δ15N values to estimate the biomagnification potential of these compounds using the slope (10). The slopes (biomagnification power) of PCBs are the highest in this study with a slope of 0.88 (Figure 3A). ΣDDT
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a
(290-1400) 30-40) (3100-3400)
nb
210 3300 2000
(150-1000) (1100-2000) (1900-2200)
380 1500 2000
2 5 5
900 78 65 28 580
5 5 5 5 5
(1300-2800) (14-25) (60-89) (18-28) (820-1900)
1900 19 73 22 1200
GM
(550-1600) (80-100) (3200-4000)
(38-52) (9.1-13) (3.8-5.4) (2.5-3.5) (14-21)
(1 SD
Sebastes jordani
b
8 10 10
11 11 11 11 11
nb
5 5 5
5 5 5 5 5
nb
NM NM NM
2800 63 82 0.09 1200
84 8
GM
1000 100 1900
56 19 5 2.2 34
(460-1700) (9.2-440) (8.5-790) (0.07-0.13) (230-6400)
(1 SD
brain
(210-5100) (90-110) 1600-2400
(31-99) (12-31) (3.1-8) (1.1-4.3) (16-72)
(1 SD
Engraulis mordax
82 5.1
GM
Number of samples above the detection limit.
(100-430) (2100-5200) (1700-2300)
(670-1200) (60-100) (39-110) (22-35) (420-800)
(1 SD
Cepphus columba
940 90 3600
75 10
(1 SD
5 5 5
70 13
GM
Cororhinca monocerata
630 30 3200
5 5 5 5 5
45 11 4.6 3 17
(9.3-13) (2.8-3.8) (1.7-3) (0.26-0.37) (3.7-5.5)
11 3.3 2.3 0.31 4.5
GM 83 4.3
nb
85 0.7
(1 SD
euphausiid
The levels are presented as µg/kg of the dry weight geometric mean with 1 SD.
av % H2O av % lipid organochlorines ∑DDT ∑HCH ∑chlordane hexachlorobenzene ∑PCBs metals Pb (lead) Hg (mercury) Se (selenium)
av % H2O av % lipid organochlorines ∑DDT ∑HCH ∑chlordane hexachlorobenzene ∑PCBs metals Pb (lead) Hg (mercury) Se (selenium)
GM
Levels of Contaminants in the Gulf of the Farallones Food Weba
TABLE 2
5 5 5 2 5
nb
4 4 4
4 4 4 4 4
nb
NM NM NM
9500 160 310 NM 3500
55 32
GM
80 550 1900
8200 78 85 41 5900
(60-120) (370-810) (1500-2300)
(5400-13000) (45-140) (31-230) (20-87) (3400-10000)
(1 SD
Uria aalge
5 12 12
13 13 13 13 13
nb
7 7 7 7
(1000-12000)
nb
(2100-43000) (38-640) (95-990)
(1 SD
blubber
Eumetopias jubatus
72 13.6
GM
130 19000 4100
NM NM NM NM NM
77 NM
GM
290 1300 2000
5300 140 510 43 5000
85 5
(4800-7300) (1100-16000)
(1 SD
liver
(80-100) (550-3200) (1700-2400)
(2000-14000) (85-220) (270-970) (21-89) (2000-12000)
(1 SD
Phalacrocorax penicillatus GM
1 8 8
nb
7 7 7
7 7 7 7 7
nb
FIGURE 2. Normalized PCB homologue distribution for marine food web organisms from the Gulf of the Farallones. Species abbreviations are the same as in Figure 1.
PCDDs. Hg had a high bioaccumulation power (0.74) and a strong relationship to δ15N (p < 0.001) in this study. Although not statistically significant, Pb appears to be negatively correlated with δ15N in this food web (Figure 3B), which agrees with the conclusion that Pb is sequestered in bone and biodepurates with increasing trophic position (39). A notable outlier in the regression of Figure 3 is the common murre. We interpret the discrepancy between contaminant levels and δ15N in this species to reflect the mobilization of stored lipid reserves into eggs. Lipids stored from periods when murres are feeding on fish (i.e., immediately preceding the egg-laying period) will contain higher levels of bioaccumulating contaminants than lipids obtained directly from lower trophic level euphausiids that comprise diet during egg laying. Contaminant measurements based on murre egg lipids will thus represent a longer-term, higher trophic level average than expected from δ15N measurements of egg albumen which reflect short-term trophic level (18).
FIGURE 3. Average of the natural logarithms of the concentrations of (A) ∑PCB and ∑DDT (dry weight, µg/kg) and (B) lead (Pb) and mercury (Hg) (dry weight, mg/kg) vs the average δ15N values for marine organisms from the Gulf of the Farallones. Data for the northern sea lion is the blubber contaminant levels vs muscle δ15N values. Species abbreviations are the same as in Figure 1.
has a biomagnification power of 0.79 in this study, which is higher than that found by Kidd et al. (10). Broman et al. (8) reported a biomagnification power of 0.21 for three
An important area of avian ecological research is an understanding of how birds allocate nutrients to reproduction, and there is great interest in whether birds use endogenous or exogenous reserves for egg formation (reviewed by Alisauskas and Ankney (42)). The allocation of stored nutrients such as lipids to egg formation also has profound implications to the study of contaminant pathways, particularly in birds that migrate between areas that vary in contaminant level. Our results indicate that the combined use of stable isotope and contaminant analysis may provide a convenient means of investigating nutrient allocation during egg laying for those species that change trophic level during this period.
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Acknowledgments Funding was provided by the Gulf of the Farallones National Marine Sanctuary Contract CX8140-93-008, the Bradford Foundation, and the Homeland Foundation. We thank L. Wassenaar for the use of his stable-isotope facility and R. George for his help in running samples for isotope analysis. J. A. Bott and J. W. Newman assisted with the preparation of samples for contaminants analysis and assisted with data analysis. Laboratory facilities were provided by the Prairie and Northern Wildlife Research Centre of the Canadian Wildlife Service and the Institute of Marine Sciences, UCSC. This is PRBO Contribution No. 699.
Literature Cited (1) Michener, R. H.; Schell, D. M. In Stable isotopes in ecology and environmental sciences; Lajtha, K., Michener, R. H., Eds.; Blackwell Scientific Publications: Oxford, UK, 1994; Chapter 7. (2) Fry, B.; Sherr, E. B. In Stable isotopes in ecological research; Rundel, P. W., Ehleringer, J. R., Nagy, K. A., Eds.; Springer-Verlag: New York, 1988; Chapter 12. (3) Fry, B. Limnol. Oceanogr. 1988, 33, 1182-1190. (4) Hobson, K. A.; Welch, H. E. Mar. Ecol. Prog. Ser. 1992, 84, 1,918. (5) France, R. L. Limnol. Oceanogr., in press. (6) France, R. L. Mar. Ecol. Prog. Ser., in press. (7) Connel, D. W. Bioaccumulaiton of xenobiotic compounds; CRC Press: Boca Raton, FL, 1990; pp 187-205. (8) Broman, D.; Na¨f, C.; Rolff, C.; Zebu ¨ hr, Y.; Fry, B.; Hobbie, J. Environ. Toxicol. Chem. 1992, 11, 331-345. (9) Rolff, C.; Broman, D.; Na¨f, C.; Zebu ¨ hr, Y. Chemosphere 1993, 27, 1-3 and 461-468. (10) Kidd, K. A.; Schindler, D. W.; Hesslein, R. H.; Muir, D. C. G. Sci. Total Environ. 1995, 161, 381-390. (11) Ainley, D. G.; Sydeman, W. J.; Hatch, S. A.; Wilson, U. W. In A Century of avifaunal change in western North America; Jehl, J. R., Johnson, N. K., Eds.; Cooper Ornithological Society: Sacramento, CA, 1994; pp 119-133. (12) Abundance and distribution of seabirds and marine mammals in the Gulf of the Farallones; Ainley, D. G., Allen, S. G., Eds.; Environmental Protection Agency (Region IX), LTMS Study Group: San Franciso, CA, 1992. (13) Ainley, D. G.; Lewis, T. J. Condor 1974, 76, 432-446. (14) Melzian, B. D.; Zoffmann, C.; Spies, R. B. Mar. Pollut. Bull. 1987, 18 (7), 388-393. (15) Gress, F.; Risebrough, R. W.; Sibley, F. C. Condor 1971, 73, 368369. (16) Griggs, G. B.; Hein, J. R. J. Geol. 1980, 88, 541-566. (17) Draft environmental impact statement for proposed new dredging: U.S. Navy military construction projects; P-202 Naval Air Station, Alameda, P-082 Naval Supply Center, Oakland, San Francisco Bay, California; United States Department of the Navy, W.D.N.F.E.C.; PRC Environmental Management; Entrix I; Tetra Tech I; Western Division Naval Facilities Engineering Command: San Bruno, CA, 1990.
660
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 30, NO. 2, 1996
(18) Hobson, K. A. Condor 1995, 97, 752-762. (19) Jarman, W. M.; Norstrom, R. J.; Simon, M.; Burns, S. A.; Bacon, C. A.; Simoneit, B. R. T. Environ. Pollut. 1993, 81, 127-136. (20) Minitab Reference Manual. Release 9 for Windows; Minitab Inc.; Sowers Printing Company: Lebanon, PA, 1993. (21) Spies, R. Mar. Environ. Res. 1984, 13, 195-230. (22) Hobson, K. A. Mar. Ecol. Prog. Ser. 1993, 95, 1-2 and 7-18. (23) Brinton, E. Bull. Scripps Inst. Oceanogr. Univ. Calif. 1962, 8, 51-270. (24) Kucas, S. T. Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (Pacific Southwest): northern anchovy; U.S. Fish and Wildlife Service Biological Report 82 (11.50); Fish and Wildlife Service, U.S. Department of the Interior: Vicksburg, MS, 1986. (25) Phillips, J. B. Calif. Dept. Fish Game Fish Bull. 1964, 126, 5-70. (26) Briggs, K. T. In Seabirds: feeding ecology and role in marine ecosystems; Croxall, J. P., Ed.; Cambridge University Press: Cambridge, U.K., 1987; pp 279-301. (27) Boekelheide, R. J.; Ainley, D. G. Auk 1989, 106, 389-401 (28) Riedman, M. The pinnipeds. Seals, sea lions, and walruses; University of California Press: Berkeley, 1990; Chapter 5. (29) Hobson, K. A.; Clark, R. G. Condor 1992, 94 (1), 181-188. (30) Hobson, K. A.; Clark, R. G. Condor 1992, 94 (1), 189-197. (31) Tieszen, L. L.; Boutton, T. W.; Tesdahl, K. G.; Slade, N. A. Oecologia 1983, 57, 32-37. (32) Mosora, F.; Lacroix, M.; Puchesne, J. C. R. Acad. Sci. Ser. D 1971, 273, 1423-1425. (33) Coulter, M. C.; Risebrough, R. W. Condor 1973, 75 (2), 254-255. (34) Huber, H. Premature pupping in northern sea lions on the Farallon Islands; Point Reyes Bird Observatory: Stinson Beach, CA, 1984. (35) Turle, R.; Norstrom, R. J.; Collins, B. Chemosphere 1991, 22, 201214. (36) Tanabe, S.; Tanaka, H.; Tatsukawa, R. Arch. Environ. Contam. Toxicol. 1984, 13, 731-738. (37) Duinker, J. C.; Hillebrand, M. T. J.; Zeinstra, T.; Boon, J. P. Aquat. Mamm. 1989, 15, 95-124. (38) Schreitmuller, J.; Vigneron, M.; Bacher, R.; Ballschmiter, K. Int. J. Environ. Anal. Chem. 1994, 57, 33-52. (39) Thompson, D. R. In Heavy Metals in the Marine Environment; Furness, R. W., Rainbow, P. S., Eds.; CRC Press: Boca Raton, FL, 1990; pp 143-182. (40) Leonzio, C.; Massi, A. Bull. Environ. Contam. Toxicol. 1989, 43, 402-406. (41) Dallinger, R.; Prosi, F.; Segner, H.; Back, H. Oecologia 1987, 73, 91-98. (42) Alisauskas, R. T.; Ankney, C. D. In Ecology and management of breeding waterfowl; Batt, B. D., Afton, A. D., Anderson, M. G., Ankney, C. D., Johnston, D. H., Kadlec, J. A., Krapu, G. L., Eds.; University of Minesota Press: Minneapolis, MN, 1992; Chapter 2.
Received for review June 7, 1995. Revised manuscript received September 25, 1995. Accepted October 3, 1995.X ES950392N X
Abstract published in Advance ACS Abstracts, December 15, 1995.
