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The Influence of Depth on Mercury Levels in Pelagic Fishes and Their Prey

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The Influence of Depth on Mercury Levels in Pelagic Fishes and Their Prey The influence of depth on mercury levels in pelagic fishes and their prey C. Anela Choya,1, Brian N. Poppb, J. John Kanekoc, and Jeffrey C. Drazena aDepartment of Oceanography, University of Hawaii, 1000 Pope Road, Honolulu, HI 96822; bDepartment of Geology and Geophysics, University of Hawaii, 1680 East-West Road, Honolulu, HI 96822; and cPacMar Inc., 3615 Harding Avenue, Suite 409, Honolulu, HI 96816 Edited by David M. Karl, University of Hawaii, Honolulu, HI, and approved June 23, 2009 (received for review January 21, 2009) Mercury distribution in the oceans is controlled by complex bio- temperature, algal concentrations) (11), and perhaps most com- geochemical cycles, resulting in retention of trace amounts of this monly, size (12). Despite extensive measurements of mercury in metal in plants and animals. Inter- and intra-specific variations in both the environment and biota, it is still not known why, mercury levels of predatory pelagic fish have been previously irrespective of size, some fish species have elevated mercury linked to size, age, trophic position, physical and chemical envi- concentrations and others do not. ronmental parameters, and location of capture; however, consid- Biogeochemical studies detailing the movement of mercury erable variation remains unexplained. In this paper, we focus on between air, land, and ocean reservoirs have offered insight into differences in ecology, depth of occurrence, and total mercury where mercury may be distributed in the marine environment levels in 9 species of commercially important pelagic fish (Thunnus (13). In the Pacific Ocean specifically, vertical profiles show that obesus, T. albacares, Katsuwonus pelamis, Xiphias gladius, Lampris methylated mercury species are usually below limits of detection guttatus, Coryphaena hippurus, Taractichthys steindachneri, Tet- in open ocean surface waters whereas subthermocline, low- rapturus audax, and Lepidocybium flavobrunneum) and in numer- oxygen deeper intermediate waters are sites for enhanced mer- ous representatives (fishes, squids, and crustaceans) of their lower cury methylation (14–17). Monomethylmercury (CH3Hg) is the trophic level prey sampled from the central North Pacific Ocean. organic form of mercury that bioaccumulates in food webs and Results indicate that total mercury levels of predatory pelagic is toxic at elevated levels (1); therefore, if oxygen depletion is fishes and their prey increase with median depth of occurrence in coupled with enhanced methylation rates in open ocean waters ECOLOGY the water column and mimic concentrations of dissolved organic (16), it suggests that via the microbial loop (18), low oxygen mercury in seawater. Stomach content analysis results from this deeper open ocean waters containing higher levels of bioavail- study and others indicate a greater occurrence of higher-mercury able mercury will transfer elevated concentrations to animals containing deeper-water prey organisms in the diets of the deeper- both living at depth and predators foraging at depth. In support ranging predators, X. gladius, T. obesus, and L. guttatus. While of this hypothesis, results of studies examining mercury levels in present in trace amounts, dissolved organic mercury increases with apex predatory seabirds suggest that the presence of mesopelagic depth in the water column suggesting that the mesopelagic hab- prey in their diet may have contributed to elevated mercury itat is a major entry point for mercury into marine food webs. These levels (19, 20). Additionally, Monteiro et al. (21) found a positive data suggest that a major determinant of mercury levels in oceanic mercury gradient with depth of occurrence in small epi- and predators is their depth of forage. mesopelagic fishes from the North Atlantic. However, these studies did not look concurrently at a diversity of predators and depth of forage ͉ marine pelagic predators ͉ North Pacific Ocean ͉ prey. mercury bioaccumulation ͉ mesopelagic zone To better understand the mechanisms governing mercury bioaccumulation in open ocean animals, we examined mercury ercury is a trace element distributed throughout the contents in predators and their lower trophic level prey in an Mearth’s atmosphere, biosphere, and geosphere. With nu- ecological food web context. Using marine animals collected merous redox states, mercury is readily transformed by a suite of from waters surrounding Hawaii in the central North Pacific physical and biologically mediated reactions, which results in Ocean, we examined the hypothesis that animal mercury levels global biogeochemical cycling and trace retention in plants and vary as a function of depth of occurrence in the water column. animals. Mercury enters food webs following abiotic or biotic Ingestion of mercury from food has been confirmed as the (i.e., bacterially mediated) methylation (1); after microbial up- dominant uptake pathway for fish, thus recording the integrated take and subsequent consumer uptake, organic forms of mercury feeding behavior of the consumer (22, 23). Mercury levels were (primarily methylmercury) readily bind to proteins and bioac- examined in 9 predatory pelagic fish species with distinct for- aging behaviors and a representative collection of their prey cumulate in higher trophic level organisms (2). items (fishes, cephalopods, and crustaceans comprising 56 taxa), The presence of organic mercury in commercially important inhabiting a large depth continuum. pelagic fishes (e.g., tunas, billfishes, and sharks) has long cap- Lastly, stomach content analysis of predators was used in the tured the interest of scientists, public health officials, and the present study to corroborate satellite/recapture tagging studies general public (3, 4). Industrial activities have increased mercury that have demonstrated differences in vertical water column emissions over past decades (5, 6), and growing awareness of the utilization among various pelagic fishes (24, 25), and augment negative health impacts of mercury have forced many organi- diet data from published studies. By selecting predators with zations (e.g., United States Environmental Protection Agency, Food and Drug Administration, and United Nations Environ- mental Program) to issue advisories and consider mercury Author contributions: C.A.C., B.N.P., and J.C.D. designed research; C.A.C. and J.J.K. per- emission controls. Thus, a comprehensive understanding of the formed research; B.N.P. and J.C.D. contributed new reagents/analytic tools; C.A.C. and J.J.K. environmental and ecological factors controlling mercury bio- analyzed data; and C.A.C., B.N.P., and J.C.D. wrote the paper. accumulation in pelagic fishes is crucial for medical advisors and The authors declare no conflict of interest. resource managers alike. This article is a PNAS Direct Submission. Variations in fish mercury levels have previously been linked 1To whom correspondence should be addressed. E-mail: [email protected]. to an assortment of synergistic factors such as location of capture This article contains supporting information online at www.pnas.org/cgi/content/full/ (7, 8), trophic level (9, 10), environmental parameters (e.g., pH, 0900711106/DCSupplemental. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0900711106 PNAS Early Edition ͉ 1of5 Downloaded by guest on October 2, 2021 3.5 XIP 3.0 BET POM OPAH WALU 2.5 YFT SKJ log THg (μg/kg) 2.0 MAHI MARL 1.5 3.0 3.5 4.0 4.5 5.0 5.5 log Mass (g) Fig. 1. Comparison of regressions of log-transformed THg concentrations (␮g/kg) as a function of log-transformed body mass (g) for 9 predators. Broadbill Swordfish (Xiphias gladius), XIP (solid circles) (n ϭ 24): THg ϭ 0.22(mass) ϩ 2.11, r2 ϭ 0.18; Bigeye Tuna (Thunnus obesus), BET (solid diamonds) (n ϭ 32): THg ϭ 0.49(mass) ϩ 0.47, r2 ϭ 0.71; Moonfish or Opah (Lampris guttatus), OPAH (X’s) (n ϭ 31): THg ϭ 0.92(mass) Ϫ 1.30, r2 ϭ 0.56; Skipjack Tuna (Katsuwonus pelamis), SKJ (open squares) (n ϭ 29): THg ϭ 0.11(mass) ϩ 2.11, r2 ϭ 0.02; Yellowfin Tuna (T. albacares), YFT (open triangles) (n ϭ 34): THg ϭ 0.25(mass) ϩ 1.30, r2 ϭ 0.22; Common Dolphinfish or Mahi-mahi (Coryphaena hippurus), MAHI (open diamonds) (n ϭ 33): THg ϭ 0.63(mass) Ϫ 0.28, r2 ϭ 0.39; Striped Marlin (Tetrapturus audax), MARL (crosses) (n ϭ 30): THg ϭ 1.85(mass) Ϫ 5.75, r2 ϭ 0.84; Sickle Pomfret (Taractichthys steindachneri), POM (solid triangles) (n ϭ 9): THg ϭ 1.42(mass) Ϫ 3.02, r2 ϭ 0.40; and Escolar (Lepidocybium flavobrunneum), WALU (solid squares) (n ϭ 20): THg ϭ 0.47(mass) ϩ 0.91, r2 ϭ 0.31. known foraging behaviors and prey with distinct vertical distri- trations increase with mass (Fig. 1) but the slopes varied as butions it is likely that trophic transfers of mercury will be more indicated by the significant interaction term between species and clearly observed. The present approach is comprehensive in its size (P Ͻ 0.05). All other interaction terms were not significant. coupling of analyses in predators and prey concurrently and Fish lengths were converted to ages (years) using published von provides information on food web dynamics and the factors Bertalanffy growth curves from the central North Pacific Ocean. governing mercury distributions in oceanic top predators. Linear regressions examining the relationship between age and mercury concentration were significantly positive (P Ͻ 0.05) for Results and Discussion 5 predators (age and growth not available for L. guttatus, T. Predators were designated as being either ‘‘shallow-ranging’’ steindachneri, L. flavobruneum, and T. audax). Age explained (i.e., swimming/foraging generally above the thermocline) more variance in mercury than size. Inter- and intra-specific {Coryphaena hippurus [0–50 m (26)], Thunnus albacares [0–100 mercury variation has been attributed to size or age in numerous m (27)], Tetrapturus audax [0–100 m (28, 29)]; Katsuwonus marine and freshwater studies (7, 10, 38, 39). The present results pelamis [0–300 m (30, 31)]} or ‘‘deep-ranging’’ (i.e., with the confirm these trends.
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