Abstract
Sturgeon populations worldwide are threatened with extirpation but little is known about their tendency to bioaccumulate contaminants and their sensitivities to environmental burdens of these contaminants. Shortnose sturgeon and Atlantic sturgeon, two species that are federally endangered in the USA, co-occur in the Hudson River (HR) where high sediment levels of polychlorinated biphenyls (PCBs), polychlorinated dibenzo-p-dioxins (PCDDs) and polychlorinated dibenzo-p-furans (PCDFs) occur. Previous controlled laboratory studies showed that young life-stages of both species are sensitive to toxicities at low levels of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) and PCB126 exposure. The objective here was to measure congener-specific hepatic levels of PCBs and PCDD/Fs in HR specimens in order to determine if in situ bioaccumulation of these compounds is sufficiently high to have caused the early life-stage toxicities previously observed. Estimates of hepatic burdens of PCBs and PCDD/Fs were obtained from a small number of specimens of each species collected between 2014 and 2016 and specimens of shortnose sturgeon collected over 30 years earlier and archived in a museum collection. Several significant patterns emerged. Hepatic levels of legacy PCBs and PCDDs were low in specimens of both species but typically higher in shortnose than Atlantic sturgeon, a pattern consistent with their habitat use in the HR. Hepatic burdens in shortnose sturgeon tended to be higher in archived specimens than in more recently collected ones despite expected reduction in archived specimens due to preservation methods. Several inadvertent PCBs congeners were detected at high levels, including PCB11, but their toxicity to natural populations remains unknown. Levels of select PCDFs congeners, 2,3,7,8-TCDF and 2,3,4,7,8 PeCDF, were elevated in some shortnose sturgeon individuals from the HR. Using Relative Potency (ReP) factors derived from white sturgeon, the observed levels of some hepatic PCDFs in HR shortnose sturgeon may have been sufficiently high to impair recruitment of young life-stages in this ecosystem.
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Altenritter ME, Zydlewski GB, Kinnison MT, Zydlewski JD, Wippelhauser GS (2018) Understanding the basis of shortnose sturgeon (Acipenser brevirostrum) partial migration in the Gulf of Maine. Can J Fish Aquat Sci 75:464–473
Bain MD (1997) Atlantic and shortnose sturgeons of the Hudson River: common and divergent life history attributes. Environ Biol Fishes 48:347–358
Caron F, Tremblay S (1999) Structure and management of an exploited population of Atlantic sturgeon (Acipenser oxyrinchus) in the St. Lawrence estuary, Quebec, Canada. J Appl Ichthyol 15:153–156
Carlson DM, Simpson KW (1987) Gut contents of juvenile shortnose sturgeon in the Upper Hudson Estuary. Copeia 1987:796–802
Chambers RC, Davis DD, Habeck EA, Roy NK, Wirgin I (2012) Early life-stage toxic effects of PCB126 and TCDD on shortnose sturgeon and Atlantic sturgeon. Environ Toxicol Chem 31:2324–2337
Courtenay S, Grunwald C, Kreamer G-L, Fairchild WL, Arsenault JT, Ikonomou M, Wirgin I (1999) A comparison of the dose and time response of CYP1A1 mRNA induction in chemically treated Atlantic tomcod from two populations. Aquat Toxicol 47:43–69
Dadswell MJ (2006) A review of the status of Atlantic sturgeon in Canada, with comparisons to populations in the United States and Europe. Fisheries 31:218–229
Dadswell MJ, Taubert BT, Squiers TS, Marchette D, Buckley J (1984) Synopsis of biological data on shortnose sturgeon, Acipenser brevirostrum LeSueur 1818. NOAA Technical Report NMFS-14, FAO Fisheries Synopsis No. 140
Doering J (2016) Predicting the Relative Sensitivity of Sturgeon to Aryl Hydrocarbon Receptor Agonists. Ph.D. Thesis. Toxicology Graduate Program. University of Saskatchewan
Doering JA, Wiseman S, Beitel SC, Giesy JP, Hecker M (2014) Identification and expression of aryl hydrocarbon receptors (AhR1 and AhR2) provide insight in an evolutionary context regarding sensitivity of white sturgeon (Acipenser transmontanus) to dioxin-like compounds. Aquat Toxicol 150:27–35
Doering JA, Farmahin R, Wiseman S, Beitel SC, Kennedy SW, Giesy JP, Hecker M (2015) Differences in activation of aryl hydrocarbon receptors of white sturgeon relative to lake sturgeon are predicated by identities of key amino acids in the ligand binding domain. Environ Sci Technol 49:4681–4690
Eisner BK, Doering JA, Beitel SC, Wiseman S, Raine JC, Hecker M (2016) Cross-species comparison of relative potencies and relative sensitivities of fishes to dibenzo-p-dioxins, and polychlorinated biphenyls in vitro. Environ Toxicol Chem 35:173–181
Elonen GE, Spehar RL, Holcombe GW, Johnson RD, Fernandez JD, Erickson RJ, Tietge JE, Cook PM (1998) Comparative toxicity of 2,3,7,8 tetra- chlorodibenzo-p-dioxin to seven freshwater fish species during early life-stage development. Environ Toxicol Chem 17:472–483
Erickson DL, Kahnle A, Millard MJ, Mora EA, Bryja M, Higgs A, Mohler J, DuFour M, Kenney G, Sweka J, Pikitch EK (2011) Use of pop-up satellite archival tags to identify oceanic-migratory patterns for adult Atlantic sturgeon, Acipenser oxyrinchus oxyrinchus Mitchell, 1815. J Appl Ichthyol 27:356–365
Everly AW, Boreman J (1999) Habitat use and requirements of important fish species inhabiting the Hudson River Estuary: availability of information. NOAA Technical Memorandum NMFS-NE-121
Farley KJ, Thomann RV (1998) Fate and bioaccumulation of PCBs in aquatic contaminants. In: Rom WN (ed) Environmental occupational medicine. Lippincott-Raven, Philadelphia, pp 1581–1594
Farley KJ, Wands JR, Damiani DR, Cooney TF III (2006) Transport, fate, and bioaccumulation of PCBs in the lower Hudson River. In: Levinton JS, Waldman JR (eds) The Hudson River estuary. Cambridge University Press, pp 368–382
Federal Register (2012a) Endangered and threatened wildlife and plants; threatened and endangered status for distinct population segments of Atlantic sturgeon in the Northeast region. 77:5880–5912
Federal Register (2012b) Endangered and threatened wildlife and plants; threatened and endangered status for two distinct population segments of Atlantic sturgeon Acipenser oxyrinchus oxyrinchus in the southeast. 77:5914–5984
Fernandez MP, Ikonomou MG, Courtenay SC, Wirgin II (2004) Spatial variation in hepatic levels and patterns of PCBs and PCDD/Fs among young-of-the-year and adult Atlantic tomcod (Microgadus tomcod) in the Hudson River Estuary. Environ Sci Technol 38:976–983
Fox AG, Peterson DL (2019) Movement and out-migration of juvenile Atlantic sturgeon in Georgia. Trans Am Fish Soc, USA. https://doi.org/10.1002/tafs.10189
Gilbert CR (1989) Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (Mid‐Atlantic Bight)—Atlantic and shortnose sturgeons. U.S. Fish Wildl Serv Biol Rep 82 (11.122). U.S. Army Corps of Engineers, TR EL82‐4
Grabe SA (1978) Food and feeding habits of juvenile Atlantic tomcod, Microgadus tomcod from Haverstraw Bay, Hudson River. Fish Bull 76:89–94
Grabe SA (1980) Food of age 1 and 2 Atlantic tomcod from Haverstraw Bay, Hudson River. Fish Bull 77:1003–1006
Greeley J.R (1937) XI. Fishes of the area with annotated list. Pages 45-103 in A Biological Survey of the Lower Hudson Watershed. Supplement to 26th Annual Report, 1936. New York State Conservation Department, Albany, New York
Gundersen DT, Zeug SC, Bringolf RB, Merz J, Jackson Z, Webb MAH (2017) Tissue contaminant burdens in San Francisco Estuary white sturgeon (Acipenser transmontanus): implications for population recovery. Arch Environ Contam Toxicol 73:334–347
Haley N (1998) A gastric lavage technique for characterizing diets of sturgeons. N Am J Fish Manage 18:978–981
Hager CH, Watterson JC, Kahn JE (2020) Spawning drivers and frequency of endangered Atlantic sturgeon in the York River system. Trans Am Fish Soc 149:474–485
Hauge PM, Belton TJ, Ruppel BE, Lockwood K, Mueller RT (1994) 2,3,7,8-TCDD and 2,3,7,8-TCDF in blue crabs and American lobsters from the Hudson-Raritan Estuary and the New York Bight. Bull Environ Contam Toxicol 52:734–741
Heine L, Tebilcock C (2018) Inadvertent PCBs in Pigments. Final Report prepared for The Spokane River Regional Toxics Task Force. Submitted by: Submitted by Northwest Green Chemistry, 16 October 2018
Henry TR, Spitsbergen JM, Hornung MW, Abnet CC, Peterson RE (1997) Early life stage toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin in zebrafish (Danio rerio). Toxicol Appl Pharmacol 142:56–68
Jaric I, Riepe C, Gessner J (2018) Sturgeon and paddlefish life history and management: expert’s knowledge and beliefs. J Appl Ichthyol 34:244–257
Kazyak D, Flowers AM, Hostetter NJ, Madsen JA, Breece MW, Higgs A, Brown LM, Royle JA, Fox DA (2020) Integrating side-scan and acoustic telemetry to estimate the annual spawning run of Atlantic sturgeon in the Hudson River. Can J Fish Aquat Sci. https://doi.org/10.1139/cjfas-2019-2039
Litten S (2007) CARP chemicals in New York Harbor. In: CARP conference, museum of the American Indian, Nov. 29, 2007, New York
Matsche MA (2011) Evaluation of tricaine methanesulfonate (MS-222) as a surgical anesthetic for Atlantic sturgeon Acipenser oxyrinchus oxyrinchus. J Appl Ichthyol 27:600–610
Matsche M (2013) Relative physiological effects of laparoscopic surgery and anesthesia with tricaine methanesulfonate (MS-222) in Atlantic sturgeon Acipenser oxyrinchus oxyrinchus. J Appl Ichthyol 29:510–519
McLaren JB, Peck TH, Dey WP, Gardinier M (1988) Biology of Atlantic tomcod in the Hudson River Estuary. Am Fish Soc Monogr 4:102–112
Nacci D, Champlin D, Jayaraman S (2010) Adaptation of the estuarine fish Fundulus heteroclitus (Atlantic killifish) to polychlorinated biphenyls (PCBs). Estuaries Coasts 33:853–864
Nittel M (1976) Food habits of Atlantic tomcod (Microgadus tomcod) in the Hudson River. In: Hudson River ecology. Fourth symposium on Hudson River ecology. Bear Mountain, March 28–30, 1976. Hudson River Environmental Society
O’Keefe P, Hilker D, Meyer C, Aldous K, Shane L (1984) Tetrachlorodibenzo-p-dioxins and tetrachlorodibenzofurns in Atlantic Coast striped bass and in selected Hudson River fish, waterfowl and sediments. Chemosphere 13:849–860
Rodenburg L, Guo J, Christie R (2015) Polychlorinated biphenyls in pigments: inadvertent production and environmental significance. Colora Technol 131:353–369
Rothermel ER, Balazik M, Best JE, Breece MW, Fox DA, Gahagan BI, Haulsee DE, Higgs AL, O’Brien MHP, Oliver MJ, Park IA, Secor DH (2020) Comparative migration ecology of striped bass and Atlantic sturgeon in the US Southern mid-Atlantic bight flyway. PLoS ONE 15(6):e0234442. https://doi.org/10.1371/journal.pone.0234442
Roy NK, Walker N, Chambers RC, Wirgin I (2011) Characterization and expression of cytochrome P4501A in Atlantic sturgeon and shortnose sturgeon experimentally exposed to coplanar PCB 126 and TCDD. Aquat Toxicol 104:23–31
Roy NK, Candelmo A, DellaTorre MS, Chambers RC, Nadas A, Wirgin I (2018a) Characterization of AHR2 and CYP1A expression in Atlantic sturgeon and shortnose sturgeon treated with coplanar PCBs and TCDD. Aquat Toxicol 197:19–31
Roy N, DellaTorre M, Candelmo A, Chambers RC, Habeck E, Wirgin II (2018b) Characterization of AHR1 and its functional activity in Atlantic sturgeon and shortnose sturgeon. Aquat Toxicol 205:25–35
Roy MA, Sant KE, Venezia OL, Shipman AB, McCormick SD, Saktrakulka P, Hornbuckle KC, Timme-Laragay AR (2019) The emerging contaminant 3,3′-dichlorobiphenyl (PCB-11) impedes Ahr activation and CYP1a activity to modify embryotoxicity of Ahr ligands in the zebrafish embryo model (Danio rerio). Environ Pollut 254(Part A):113027
Sethi S, Keil KP, Lein PJ (2018) 3,3′-Dichlorophenyl (PCB11) promotes dendritic arborization in primary rat cortical neurons via a CREB-dependent mechanism. Arch Toxicol 92:3337–3345
Simpson KW, Fagnani JP, DeNicola DM, Bode RW (1985) The freshwater macrobenthos of the main channel, Hudson River. Part A. General study description and results, including a discussion of organism-substrate relationships. Final report to Hudson River Foundation for Grant No. 8/83A/39. Hudson River Foundation, New York
Skinner LC (2011) Distributions of polyhalogenated compounds in Hudson River (New York, USA) fish in relation to human uses along the river. Environ Pollut 159:2565–2574
Sloan RJ, Simpson KW, Schroeder RA, Barnes CR (1983) Temporal trends toward stability of Hudson River PCB contamination. Bull Environ Contamin Toxicol 31:377–385
Umbreit TH, Hess EJ, Gallo MA (1986) Bioavailability of dioxin in soil from a 2,4,5-trichlorophenoxyacetic acid manufacturing site. Science 232:497–499
Van den Berg M et al (1998) Toxic equivalency factors (TEFs) for PCBs, PCDDs, PCDFs for humans and wildlife. Environ Health Perspect 106:775–792
Vorkamp K (2016) An overlooked environmental issue? A review of the inadvertent formation of PCB-11 and other PCB congeners and their occurrence in consumer products and in the environment. Sci Total Environ 541:1463–1476
Waldman J, Alter SE, Peterson D, Maceda L, Roy NK, Wirgin II (2018) Contemporary and historical effective population sizes of Atlantic Sturgeon Acipenser oxyrinchus oxyrinchus. Conserv Genet 20:167–184
Walker MK, Spitsbergen J, Olson JR, Peterson RE (2011) 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) toxicity during early life stage development of lake trout (Salvelinus namaycush). Can J Fish Aquat Sci 48:875–883
Wenning R, Paustenbach D, Johnson G, Erlich R, Harris M, Bedbury H (1993) Chemometric analysis of potential sources of polychlorinated dibenzo-p-dioxins and dibenzofurans in surficial sediments from Newark Bay, New Jersey. Chemosphere 27:55–64
Wilk SJ, McMillan DG, Pikanowski RA, MacHaffie EM, Pacheco AL, Stehlik LL (1997) Fish, mega invertebrates, and associated hydrographic observations collected in Newark Bay, New Jersey during May 1993–April 1994. Northeast Fisheries Science Center Reference Document 97–10, June 1997, National Marine Fisheries Service, Highlands
Wirgin I, Roy NK, Loftus M, Chambers RC, Franks DG, Hahn ME (2011) Mechanistic basis of resistance to PCBs in Atlantic tomcod from the Hudson River, USA. Science 331:1322–1325
Wirgin I, Maceda L, Grunwald C, King T (2015) Population origin of Atlantic sturgeon bycaught in U.S. Atl Coast Fish J Fish Biol 85:1–20
Acknowledgements
This study was supported by a research grant from the Hudson River Foundation and funding from NOAA Protected Species. We also acknowledge support from National Institute of Environmental Health Sciences Center Grant EHS00260 to NYU and the continued support of the NOAA Northeast Fisheries Science Center. We thank Mark Matsche and Kevin Rosemary of the Maryland DNR and Fred Jacobs and Justin Krebs of AKRF, Inc. for their assistance in sample collections.
Funding
This study was funded by a Grant from the Hudson River Foundation and was supplemented with support from NOAA. Support of the Molecular Facilities Core of National Institute of Environmental Health Sciences Center Grant EHS00260 is also acknowledged.
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Drs. IW and RCC contributed equally to study conception and design. Sample acquisition and analyses by AXYS were coordinated by IW. The first draft of the manuscript was written by IW. Both authors read approve of the final manuscript.
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Wirgin, I., Chambers, R.C. Hepatic Burdens of PCB and PCDD/F Congeners in Federally Endangered Shortnose Sturgeon and Atlantic Sturgeon from the Hudson River, New York, USA: Burden Patterns and Potential Consequences in Offspring. Arch Environ Contam Toxicol 83, 21–35 (2022). https://doi.org/10.1007/s00244-022-00935-6
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DOI: https://doi.org/10.1007/s00244-022-00935-6