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Low PCB Concentrations Observed in American Eel (Anguilla rostrata) in Six Hudson River Tributaries
Karin E. Limburg, Leonard S. Machut, Peter Jeffers, and Robert E. Schmidt

Northeastern Naturalist, Volume 15, Issue 2 (2008): 215–226

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2008 NORTHEASTERN NATURALIST 15(2):215–226 Low PCB Concentrations Observed in American Eel (Anguilla rostrata) in Six Hudson River Tributaries Karin E. Limburg1,*, Leonard S. Machut1,2, Peter Jeffers3, and Robert E. Schmidt4 Abstract - We analyzed 73 eels, collected in 2004 and 2005 above the head of tide in six Hudson River tributaries, for total PCBs, length, weight, age, and nitrogen stable isotope ratios (δ15N). Mean total PCB concentration (wet weight basis) was 0.23 ppm ± 0.08 (standard error), with a range of 0.008 to 5.4 ppm. A majority of eels (84%) had concentrations below 0.25 ppm, and only seven eels (10%) had concentrations exceeding 0.5 ppm. Those eels with higher PCB concentrations were ≥12 yr; there was a weak correlation of PCB concentration with δ15N and also with weight. Compared to recent (2003) data from the mainstem of the Hudson River estuary, these results indicate that tributaries are generally much less contaminated with PCBs. We hypothesize that those tributary eels with high PCB concentrations were relatively recent immigrants from the mainstem. Given concern over the possible adverse effects of PCBs on eel reproduction, these tributaries may serve as refugia. Therefore, providing improved access to upland tributaries may be critically important to this species. Introduction Worldwide, anguillid eels are in decline, with particular concern over Anguilla anguilla Linnaeus (European Eel), A. rostrata Lesueur (American Eel), and A. japonica Temminck and Schlegel (Japanese Eel) (Dekker 2004, Haro et al. 2000, ICES 2004, Katoh and Kobayashi 2003). A number of causes have been suggested, including overharvesting (e.g., Dekker 2003, Robitaille et al. 2003), habitat loss (Feunteun 2002, ICES 2002), parasites such as Anguillicola crassus Kuwahara, Niimi & Itagaki (Sures and Knopf 2004), toxic substances (Lehmann et al. 2005), oceanic conditions (Castonguay et al. 1994, Knights 2003), or combinations thereof. Although none of these potential causes has been identified as having singly affected populations, there is growing concern that PCBs and other dioxin-like compounds may compromise the reproductive system, leading to non-viable offspring (ICES 2006, Palstra et al. 2006) and consequent recruitment failure. There is also growing evidence that toxic substances such as organohalines and heavy metals may lead to reduced resistance to parasites and disease (ICES 2006, Lehmann et al. 2005, Sures et al. 2006). The Hudson River in New York State is a tidal estuary for 252 km, up to the Green Island Dam at Troy, NY (Limburg et al. 1986). American 1SUNY College of Environmental Science and Forestry, One Forestry Way, Syracuse, NY 13210. 2Current address - US Geological Survey, Tunison Laboratory, 3075 Gracie Road, Cortland, NY 13045. 3Department of Chemistry, State University of New York at Cortland, Cortland, NY 13045. 4Bard College at Simon’s Rock, Great Barrington, MA 01230. *Corresponding author - KLimburg@esf.edu. 216 Northeastern Naturalist Vol. 15, No. 2 Eels in the estuary (mainstem) have been exposed to PCBs from point sources above the dam from General Electric manufacturing plants since the 1940s (Limburg et al. 1986). Although discharges ceased in 1977, PCBs have persisted in the system, dispersing downstream and accumulating in the sediments (Baker et al. 2001). Regular monitoring of fishes in the Hudson River mainstem has been ongoing since 1975 (Sloan et al. 2005, Spagnoli and Skinner 1977), with concentrations generally declining from the tens and hundreds of ppm in the 1970s to a level that is, throughout most of the estuary, still above the Food and Drug Administration’s tolerance of 2 ppm total PCB for human consumption. We recently studied American Eel use of small Hudson River tributaries (Machut 2006, Machut and Limburg 2008, Machut et al. 2007). We found some of the highest eel densities ever reported in the lower reaches of these systems, indicating their importance as key habitat (Schmidt et al. 2006). There is also great interest in improving eel access to upper parts of tributary watersheds, most of which contain dams that greatly retard upstream movement (Machut et al. 2007). One of us (R.E. Schmidt) experimented throughout the summer of 2006 with installing an eel ladder in one Hudson River tributary, the Saw Kill, in the central region of the estuary. The ladder, located above a substantial waterfall which in itself represents a barrier, nevertheless passed 132 eels—a remarkably substantial number given the conditions—ranging in size from 70 to 550 mm. Eels thus appear to have potential to recolonize upland parts of tributary watersheds if access is provided. Given the general worldwide decline in eel populations, and given the potential to open up new habitat in tributaries, we conducted a survey of total PCB concentrations in a subset of the eels collected for other analyses (for a complete list, see Machut 2006). We hypothesized that tributaries, because they contain no known point sources of PCBs, would provide relatively clean habitat in this regard. We present these results, and relate them to eel age, size, and point of capture. In addition, we examine trends of PCBs and stable isotope ratios of nitrogen in eel muscle tissue. Now widely studied in ecology, N stable isotopic ratios of organisms tend to be related to trophic position in food webs (Peterson and Fry 1987) and have also been demonstrated to be related to PCB biomagnification (e.g., Paterson et al. 2006). Methods Study area We selected six wadable tributaries that ranged along the north–south axis of the Hudson River mainstem (Fig. 1), These are, from south to north: Minisceongo Creek (length = 18.9 km, drainage area = 47.9 km2); Peekskill Hollow Brook (28.1 km, 135.5 km2); Black Creek (29.6 km, 87.8 km2); Saw Kill (22.6 km, 66.3 km2); Hannacrois Creek (37.8 km, 166.2 km2); and Wynants Kill (26 km, 85.5 km2). Although the Hudson River estuary is brackish in its lower 60 km (with salinity varying as a 2008 K.E. Limburg, L.S. Machut, P. Jeffers, and R.E. Schmidt 217 function of freshwater inputs), all tributary sampling was above the head of tide, and thus all in fresh water. Sample collection and processing Tributaries were sampled in the summers of 2004 and 2005 by electrofishing at six to seven sites more or less evenly spaced from the confluence with the Hudson up to a point at which no eels were found. Sampling details may be found in Machut (2006). All eels were narcotized in the field and total length measured (TL, mm). A length-stratified subsample of eels was taken from each site back to the lab, frozen in water, and processed later. Wet weights (W, g) were recorded, and Fulton condition factor (K) computed from lengths and weights: K = W/(TL3) x 105. Otoliths were removed for aging, and samples (ca. 1 g) of muscle tissue were collected for PCB analysis. Another sample (1 g) of muscle tissue was freeze-dried, pulverized, and 0.8–1.2-mg aliquots of powdered tissue were sent to the University of California-Davis Stable Isotope Facility for stable isotope analysis. These samples were analyzed on a Europa Hydra 20/20, a continuous-flow Isotope Ratio Mass Spectrometer (IRMS). Two samples were analyzed for each eel and averaged to reduce error (coefficient of variation approximately 2%). Nitrogen stable isotopic ratios are expressed in the “del” notation: δ15N = [(15N/14N)sample ÷ (15N/14N)standard] - 1 * 1000, with units of per mil (‰). Figure 1. Map of the Hudson River watershed, showing locations of tributaries along the mainstem axis of the Hudson River estuary. 218 Northeastern Naturalist Vol. 15, No. 2 Eel PCB content analysis A total of 73 eels were haphazardly selected and analyzed for PCBs. Most of the samples were analyzed on eels from Minisceongo Creek (Table 1). Because of a freezer accident, a number of frozen samples were lost. However, freeze-dried tissue from the same eels could be used; these were corrected to wet-weight equivalent values by dividing by 4 (based on percent moisture data from L. Skinner, New York State Department of Environmental Conservation, unpubl. database). All glassware, mortars and pestles, and sample vials were washed, rinsed, and heated to 450 ºC for 6 hr before use. About 1 g of eel skinless muscle tissue, taken dorsally from behind the head, was weighed (to 1 mg) and transferred to a ceramic mortar containing about 5 g anhydrous Na2SO4 and 2 mL of a 1:1 acetone to hexane mix. The tissue sample was ground carefully with a ceramic pestle, so no liquid was splashed out. The liquid was transferred to a 20-mL glass vial using a 14.7-cm (5.75-inch) disposable glass Pasteur pipette. Fresh acetone-hexane solution was added, and the extraction process repeated a total of five times. The 20-mL vial was placed in a hood, and the solvent allowed to evaporate to dryness. Florisil clean-up columns were prepared from a 0.3-m length of 10-mm o.d. Pyrex tubing. A small fiberglass plug was pushed into the drawn end of the tube, and 5 g of Florisil and 2 g of anhydrous Na2SO4 were added, leaving about a 7.6-cm (3-inch) void at the top of the column. (The 60–100 mesh Florisil was pre-treated by adding 20 mL deionized water to 500 g Florisil and rolling the bottle for a day.) The columns were not reused. About 2 mL hexane was added to the “dried” extract. The column was moistened with 2 mL hexane, followed by the 2-mL extract solution as soon as the initial hexane was completely on the column packing. A 1-mL rinse of the extract vial followed, followed by successive 2-mL hexane additions Table 1. Characteristics of Hudson River tributary eels sampled for PCBs. Abbreviation: s.e. = standard error. W = wet weight. TL = total length. Total No. Mean TL, mm Mean W, g Mean age, yr PCBs, ppm δ15N ‰ Tributary eels (range) (range) (range) (± s.e.) (± s.e.) Minisceongo 27 375.3 152.6 11.7 0.36 11.7 (145–692) (4.4–964.8) (3–24) (0.19) (0.22) Peekskill Hollow 15 384.5 175.5 10.1 0.13 11.2 (149–710) (4.7–779.5) (3–21)A (0.04)B (0.30) Black 7 402.9 171.2 12.4 0.12 12.9 (197–653) (12.3–560) (7–23) (0.04) (0.46) Saw Kill 5 438.8 205.1 14.4 0.18 14.2 (252–622) (27.3–435.6) (8–22) (0.06) (0.56) Hannacrois 15 355.9 128.4 10.3 0.15 12.0 (169–596) (7.1–467.3) (4–17) (0.05) (0.32) Wynants Kill 3 516.0 377.6 11.0 0.49 12.3 (294–699) (44.2–820.3) (3–18) (0.38) (0.47) AN = 14. BN = 16. 2008 K.E. Limburg, L.S. Machut, P. Jeffers, and R.E. Schmidt 219 until about 10 mL of eluent was collected in a clean 20-mL glass vial. The eluent vial was placed in a hood till the solvent evaporated to dryness. If a significant amount of oil remained, the column clean-up was repeated. A carefully measured amount of hexane, 0.5 to 5.0 mL, depending on PCB content, was added to the vial as final preparation for GC analysis. PCB identification and analysis utilized a Hewlett-Packard 5890 GC with electron capture detector, Restek RTX 1701 column, 15-m x 0.053-mm, 0.25-micron film thickness. A temperature program of 120 ºC for 3 min followed by a 3.5 deg/min ramp to 200 ºC produced PCB congener peak elution from 2 to 24 min. The chromatogram of a given eel sample extract was matched by pattern to authentic Aroclor 1248, 1254, or 1260 samples and was quantitated by measuring the three corresponding most-abundant peaks of sample and standard. Most samples with measurable PCB content were a close match to the Aroclor 1260 pattern (see Fig. 2). Recovery checks for Aroclor 1260 spikes carried through the entire extraction, clean-up, and sample-preparation process yielded recoveries of 95% to 106% for the eight most-abundant peaks. Method blanks, recovery, and calibration samples were routinely performed as part of each set of analyses. The method was quantitatively effective for determining PCB levels up to 15 ppm in eels from the St. Lawrence River, and up to 300 ppm in fatty tissues from laboratory rats (P. Jeffers, unpubl. data). Results All eels contained measurable amounts of PCBs. Mean total PCB concentration (wet weight basis) was 0.23 ppm ± 0.08 ppm (standard error), with a range of 0.008 to 5.4 ppm. Sixty-one eels (83.6%) had concentrations below 0.25 ppm, and only seven eels (10%) had concentrations exceeding 0.5 ppm. Only two individuals had PCB concentrations above 1 ppm: a 24-year-old eel with the highest condition factor (K = 0.291) had a PCB concentration of 5.4 ppm. This fish, by its size, age, and condition likely to be a maturing female, was caught in Minisceongo Creek at the site closest to the creek mouth (0.7 km). The only other eel with PCB concentration above 1 was a 12-year-old individual in Wynants Kill (1.23 ppm); this fish was collected only 1.2 km from the tributary mouth, but was caught upstream of two dams and four waterfalls, with a cumulative height of 22 m. The relationship between PCB concentrations and δ15N was nonlinear; therefore both logarithmic and square-root data transformations were tested. The best transformation to relate PCB concentration to N stable isotopic ratios was square-root (√[PCB] = - 1.6282 + 0.58667 √(δ15N), R2 = 0.11, p < 0.05). Note that eels from Saw Kill were not included in that analysis, because the δ15N in that tributary is elevated by sewage plant effluent (Machut 2006). Other independent variables were related to greater or lesser degree to PCB concentrations. Age was a significant predictor, on the square-root 220 Northeastern Naturalist Vol. 15, No. 2 transformed PCB data (√ [PCB] = -0.2097 + 0.0402 (Age), R2 = 0.10, p less than 0.05). The best overall regression relationship found was between squareroot transformed PCB concentrations and the Fulton condition index (√ ([PCB] = -0.7136 + 6.859 (K), R2 = 0.19, p < 0.00001). All of these relationships were driven to large extent by the single extreme value (old female from Minisceongo); removal of this extreme value rendered all of the regressions non-significant. Combinations of these independent variables did not improve the fit. Figure 2. a (above). Chromatogram of PCB congeners extracted from a 1.055-g tissue sample from Eel #7 taken at Minisceongo Creek site #3. The PCB concentration is calculated to be 0.28 ppm. Labels on the peaks indicate elution time/peak area/ peak height. The large peak at 20.5 min is due to oil that passed through the clean-up column. b (opposite page). Chromatogram of an authentic sample of Aroclor 1260. Note the close correlation of peaks with Figure 2a. 2008 K.E. Limburg, L.S. Machut, P. Jeffers, and R.E. Schmidt 221 Comparison to mainstem Hudson River eels Sloan et al. (2005) summarize Hudson River fish PCB concentration data from 1977 to 2003. All the fish were collected in the mainstem. Eels were only collected in the mid- and lower parts of the estuary, in the Tappan Zee Bridge vicinity (rkm 43) and in Newburgh Bay (rkm 97). In 2003, eels at Tappan Zee averaged 1.21 ppm total PCB (n = 11, range = 0.31–2.54 ppm); at Newburgh, eels averaged 1.46 ppm (n = 12, range = 0.55–3.05). The closest tributary to these is Minisceongo Creek, which drains into upper Haverstraw Bay at rkm 58. Mean total PCB concentrations in this tributary (n = 27, Table 1) were less than a third of the Tappan Zee concentrations, despite the high value described above. Overall, tributary PCB concentrations were significantly lower than mainstem concentrations (F1,94 = 48.05, p < 10-6; Fig. 3). Post-hoc analysis by site (six tributaries and two Hudson sites) showed that tributaries did not 222 Northeastern Naturalist Vol. 15, No. 2 differ among each other with respect to PCB concentrations, but all were significantly lower than the mainstem sites. (Newman-Keuls test; p < 0.05). There was no relationship between river kilometer location of tributarycaught eels and PCB concentrations (R2 = 0.001, p < 0.76). Discussion With a few exceptions, the eels we assayed from Hudson River tributaries had lower concentrations of PCBs than those reported from mainstem sampling (Sloan et al. 2005). The exceptions were found in lower parts of tributaries, although the fish with second highest PCB levels (1.23 ppm) was caught upstream of 6 barriers in the Wynants Kill in Troy, NY. The Wynants Kill is the closest tributary to the upstream contaminated areas above the Green Island Dam at Troy. It is possible that this fish could have picked up its contaminant burden in the mainstem of the estuary before moving into the Wynants Kill. Alternatively, there may be a point source within the Wynants Kill, although none was listed in the statewide 2004 water quality report (NYSDEC 2004). Similarly, no point sources of PCB contamination are reported in the Minisceongo Creek. However, we note that Minisceongo Creek and Wynants Kill are the most urbanized systems Figure 3. Box plots of PCB concentrations for different collections of eels, shown as a function of position along the Hudson River estuary (river km). The two shaded box plots are of eels collected at mainstem sites (Piermont, river km 40, and Newburgh Bay, river km 93). The other sites are (from downstream going upstream): Minisceongo, Peekskill Hollow, Black, Saw Kill, Hannacrois, and Wynants Kill. 2008 K.E. Limburg, L.S. Machut, P. Jeffers, and R.E. Schmidt 223 in our study, and eels in these systems had higher instances of parasite infections (Machut and Limburg 2008). Riva-Murray et al. (2003) found elevated PCB concentrations in fish from highly urbanized reaches of the Delaware River; urbanized watersheds may be more likely than rural ones to have elevated levels of PCBs. Anguillid eels are facultatively catadromous, and display a wide repertoire of habitat-use and movement patterns (Daverat et al. 2006). Eel residence can be on the order of years (e.g., Limburg et al. 2003, Morrison and Secor 2003); hence, it is entirely plausible that the eels resided for some years in the mainstem, absorbing PCBs, but eventually moved into these tributaries. The largest eel, with highest PCB concentration and highest Fulton condition index, was likely a maturing silver female. Because she was located in a free-running stretch of Minisceongo Creek, it is plausible that she had moved into the creek, or alternatively made feeding forays from the creek into the estuary. Nevertheless, low levels (<0.25 ppm) of PCBs were detected in 82% of the eels we sampled. It is unclear whether there are small or diffuse sources of PCBs within the tributary watersheds, or whether these eels had picked up their PCBs in the Hudson mainstem. Regressions of transformed PCB concentrations on age and δ15N were significant, but driven by the data from the old female from Minisceongo Creek, clearly an extreme value. We propose that the variability and lack of strong correlation between age and stable isotopic ratios (found by McIntyre and Beauchamp [2007] in Lake Washington top predators) is because of eels switching amongst food webs as they move about. To understand the relationships would likely require detailed information on individual diets, habitat use, and growth rates, in order to model uptake and turnover of stable isotopes and PCBs (Paterson et al. 2006). Fulton condition factor (K) proved to be the most robust independent predictor of PCB concentrations. Condition factors such as this, based on weight-to-length ratio expectations, are proxies for fatness. Thus, a fish with high K is fatter than expected for a given length. Given that PCBs are lipophilic, it is reasonable to expect that fatter fish with some likelihood of exposure would accumulate more PCB. Steinbacher and Baker (2002) found a very strong relationship of PCBs to lipid content in Hudson River eels. Biologically, the anomalous eel from Minisceongo is worrisome. In controlled experiments with eels taken from European rivers, Palstra et al. (2006) showed that as eels mature, lipids are translocated into the gonads— and organohaline compounds with the lipid, if the fish was exposed to them. Palstra et al. (2006)’s results suggested an inverse relationship between embryonic eel survival and TEQ (dioxin equivalents), with edemic swelling and head deformities. Thus, some speculate that the dramatic decline in European and American Eel is related in part to reproductive failure due to high levels of dioxin-like compounds being shunted into the developing ovaries (e.g., ICES 2006, Palstra et al. 2006, Robinet and Feunteun 2004). 224 Northeastern Naturalist Vol. 15, No. 2 In terms of management, it is encouraging to see that the PCB levels in most of the eels in our survey were well below those observed in the Hudson mainstem eels. This result suggests that tributaries may have another benefit to eels in this polluted system, namely as refugia from PCB contamination. Although levels are also declining in the Hudson estuary (cf. Ashley et al. 2003, Sloan et al. 2005), it will be years before the upper Hudson River PCB remediation is completed (US EPA 2007), so other measures to improve habitat for eel are warranted. One such measure would be increasing habitat availability in clean tributary streams through removal of non-natural barriers or installation of eel ladders. Acknowledgments We thank J. Anderson, E. Leibu, A. Lang, N. Akpan, P. Simonin, J. Sopacua, and N. Karraker for field and laboratory assistance, L. Skinner and M. Kane of New York State Department of Environmental Conservation for discussion and access to their data, and two anonymous reviewers for their constructive comments. The project was supported by the Hudson River Foundation and NSF DEB-0238121. Literature Cited Ashley, J.T.F., R. Horwitz, J.C. Steinbacher, and B. Ruppel. 2003. A comparison of congeneric PCB patterns in American Eel and Striped Bass from the Hudson and Delaware River estuaries. Marine Pollution Bulletin 46:1294–1308. 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