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Seabirds as biomonitors of mercury inputs to epipelagic and mesopelagic marine food chains
The Science of the Total Environment 213 Ž1998. 299]305
Seabirds as biomonitors of mercury inputs to epipelagic and mesopelagic marine food chains David R. Thompsona,U , Robert W. Furness a , Luis R. Monteiro b a b
Applied Ornithology Unit, Graham Kerr Building, Uni¨ ersity of Glasgow, Glasgow, G12 8QQ UK Department of Oceanography and Fisheries, Uni¨ ersity of the Azores, 9900 Horta, Azores, Portugal
Abstract Mercury concentrations are presented for time-series of feather samples from seabirds feeding near the apex of epipelagic and mesopelagic marine food chains in the south-east and north-east North Atlantic. These quantify historical increases in surface and deep water mercury concentrations due to mercury pollution. Our results highlight the importance of mercury methylation in mesopelagic water as the factor responsible for the greatest increases in seabird mercury concentrations, which occur in seabirds feeding primarily on mesopelagic prey. Seabirds which feed on prey occupying the epipelagic zone exhibited more modest increases in mercury concentration than mesopelagic feeders, but the rates of increase in the epipelagic-feeding birds are in agreement with recent model predictions regarding anthropogenic inputs of mercury to the environment. We investigated the importance of mesopelagic prey in the diet of seabirds, as opposed to trophic status, in determining mercury concentrations. Analysis of stable isotope ratios of nitrogen revealed that trophic status was not the principal factor in determining mercury concentration and that the presence of mesopelagic prey in the diet was likely to contribute more to the patterns of mercury burdens. Q 1998 Elsevier Science B.V. Keywords: Seabirds; Biomonitoring; Mercury; Epipelagic; Mesopelagic; Stable isotopes
1. Introduction Seabirds have featured prominently in monitoring of mercury contamination of the marine
U
Corresponding author. Present address: National Institute of Water and Atmospheric Research, 301 Evans Bay Parade, Greta Point, P.O. Box 14-901, Kilbirnie, Wellington, New Zealand. E-mail: [email protected]
environment ŽWalsh, 1990; Furness, 1993; Monteiro and Furness, 1995; Thompson, 1996.. They tend to accumulate high mercury concentrations compared to other groups within marine food chains since they occupy relatively high trophic positions. Furthermore, mercury binds strongly to feather keratins ŽCrewther et al., 1965. during feather growth and mercury is not lost from feathers, even after various vigorous treatments ŽAppelquist et al., 1984.. The mercury concentra-
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tion in a sample of feathers, therefore provides an easily-obtainable, relatively non-invasive measure of the mercury burden of a given individual. The use of feathers to measure mercury concentrations in seabirds is further enhanced since mercury concentrations of feathers have been shown to correlate positively with those in internal tissues ŽFurness and Hutton, 1979; Thompson et al., 1991., thus avoiding the need to sacrifice large numbers of birds. Mercury concentrations in feathers reflect the uptake and storage of mercury during the period between moults wmost seabirds do not moult feathers over a 5]6-month period ŽGinn and Melville, 1983.x, rather than short-term uptake ŽFurness et al., 1986; Honda et al., 1986; Braune and Gaskin, 1987.. A major advantage afforded by seabirds over other marine groups is their suitability for investigations of temporal patterns of mercury contamination, since many seabirds have been preserved as study skins in museum collections. Feather samples from such collections represent a record of mercury concentrations in different species from many locations dating back to the middle of the 19th century. Problems with sample contamination through the application of inorganic mercury as a preservative can be overcome through an initial organic mercury extraction, since virtually all the biologically incorporated mercury in seabird feathers has been shown to be organic ŽThompson and Furness, 1989.. Time-series of feather samples have been used in this way to investigate long-term patterns of mercury contamination of seabirds from Greenland, the Faeroe Islands, the Baltic Sea and the Kattegat ŽAppelquist et al., 1985., around the British Isles ŽThompson et al., 1992., the German North Sea coast ŽThompson et al., 1993a. and from a range of southern ocean sites ŽThompson et al., 1993b.. Here we present a re-evaluation of the British Isles data ŽThompson et al., 1992., investigating rates of change in mercury concentrations and an initial appraisal of the long-term patterns of mercury contamination in warm-temperate North Atlantic seabirds. For both regions, we examine whether observed patterns of mercury contamination in seabirds Žpatterns of long-term change and inter-specific differences in contemporary
seabirds. are related to differences in diet. We further investigate the importance of diet as a major determinant of mercury concentration in northern fulmars Fulmarus glacialis, incorporating the use of stable isotope analysis to define trophic status. Our results are discussed in relation to model predictions regarding long-term patterns of mercury deposition over the last 100 years. 2. Methods Long-term patterns of mercury concentrations in seabirds were investigated through the analysis of feather samples from study skins held in museum collections, these being compared to mercury concentration in feather samples from contemporary, free-living seabirds of the same species and from the same sites. In all cases, a small number of body feathers Ž6]10. were removed, pooled and stored prior to mercury analysis in polythene bags. Feather samples from historical samples were analysed for organic Žmethyl. mercury only, following a chloroformracetone wash to remove gross surface contamination ŽMuirhead, 1986. and an extraction of organic mercury using toluene. The method used was adapted from that used by Uthe et al. Ž1972. to extract methylmercury from fish tissue and is described more fully by Thompson and Furness Ž1989.. Contemporary samples were analysed for ‘total’ mercury, this being equivalent to the organic Žmethyl. mercury concentration since seabird feather mercury has been shown to be virtually all organic ŽThompson and Furness, 1989., following standard acid digestion. All samples Žextracted methyl mercury from historical samples and total mercury from contemporary samples. were analysed using cold vapour absorption spectrophotometry. For details of species and sites sampled from around the British Isles see Thompson et al. Ž1992.. Seabird species sampled from the warm-temperate North Atlantic Žprimarily the Azores archipelago. were Bulwer’s petrel Bulweria bulwerii, band-rumped storm petrel Oceanodroma castro, Cory’s shearwater Calonectris diomedea, little shearwater Puffinus assimilis and common tern Sterna hirundo. In all cases,
D.R. Thompson et al. r The Science of the Total En¨ ironment 213 (1998) 299]305
comparisons have been made between birds sampled prior to 1931 Žas being indicative of an environment relatively free of anthropogenic mercury; the vast majority of these birds dated from around the turn of this century. and from after 1979 Žas being indicative of an environment relatively contaminated by anthropogenic mercury.. Rates of change in mercury concentrations over this period have been calculated by using the median sampling years from each period as ‘end points’. For all species studied, there was no evidence to indicate any change or shift in diet had occurred over the study period. The relationships between mercury concentration in a seabird and its diet and trophic status were investigated in two geographically distinct populations of northern fulmars known to have markedly different diets. At Foula ŽShetland., northern fulmars are known to feed mainly upon small fish and discarded fish and fish offal from whitefish trawlers, whilst at St Kilda ŽOuter Hebrides., small fish, zooplankton and crustaceans make up the bulk of the fulmar diet ŽFurness and Todd, 1984; Thompson et al., 1995.. Trophic status was defined through the analysis of nitrogen stable isotope ratios Žconventionally expressed as d 15 N s Žw 15 Nr 14 Nsampler 15 Nr 14 Nstandard x y 1. = 10 3 . in homogenised body feather samples. The stable isotope ratio of nitrogen shows a step-wise enrichment up food chains ŽHobson et al., 1994.,
301
such that the higher the value of d 15 N Ženriched in 15 N relative to 14 N., the higher the trophic status of a particular individual or species. Mean d 15 N values from body feather samples for each site were compared with mean mercury concentrations in order to relate any difference in mercury burden between the two sites to trophic status, as defined by the d 15 N signature. 3. Results Historical patterns of mercury in seabirds from the warm-temperate North Atlantic are presented in Table 1. All species exhibited an increase over the study period. However, the increases in mercury concentrations in band-rumped storm petrels Ž397%. and Bulwer’s petrels Ž260%. were considerably greater than those in the other three species from this area Ž65]100%; Table 1.. The corresponding rates of increase in mercury concentration in band-rumped storm petrels Ž4.1% yeary1 . and Bulwer’s petrels Ž2.9% yeary1 . were also far greater than those in the other species Ž0.7]1.4% yeary1 ; Table 1.. Historical patterns of mercury concentrations in seabirds from around the British Isles are presented in Table 2. Again, all species studied exhibited an increase in mercury concentration, but the increase tended to be greatest in Manx shearwaters Puffinus puffinus Ž176% in the
Table 1 Long-term trends in mercury concentrations Ž m g gy1 . in seabird feathers from the warm-temperate North Atlantic Species
Pre-1931a
Post-1979a
Increase Ž%.
Increase Ž% yeary1 .
Band-rumped storm petrel Oceanodroma castro
3.0 Ž16. 0.1
14.9 Ž47. 0.5
394
4.1
Bulwer’s petrel Bulweria bulwerii
6.0 Ž30. 0.7
21.6 Ž55. 0.7
260
2.9
Cory’s shearwater Calonectris diomedea
2.7 Ž48. 0.1
5.4 Ž219. 0.1
100
1.4
Common tern Sterna hirundo
1.1 Ž15. 0.1
2.0 Ž22. 0.1
82
1.3
Little shearwater Puffinus assimilis
1.7 Ž15. 0.2
2.8 Ž34. 0.2
65
0.7
a
Values are mean, sample size Žnumber of birds. in parentheses and S.E.
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D.R. Thompson et al. r The Science of the Total En¨ ironment 213 (1998) 299]305
Table 2 Long-term trends in mercury concentrations Ž m g gy1 . in seabird feathers from the British Isles Species
Pre-1931a
Post-1979a
Increase Ž%.
Increase Ž% yeary1 .
Manx shearwater Puffinus puffinus Žnorth-west British Isles.
1.7 Ž14. 0.2
4.7 Ž78. 0.2
176
2.3
Manx shearwater Žsouth-west British Isles.
1.5 Ž17. 0.2
2.9 Ž22. 0.2
93
1.0
Atlantic puffin Fratercula arctica Žwest Britain.
1.8 Ž49. 0.1
4.4 Ž61. 0.2
144
1.5
Great skua Catharacta skua Žnorth-east Atlantic.
4.2 Ž13. 0.6
7.0 Ž212. 0.3
67
0.4
Gannet Morus bassanus ŽBass Rock, east Britain.
5.9 Ž19. 0.6
7.7 Ž38. 0.5
31
0.3
a
Values are mean, sample size Žnumber of birds. in parentheses and S.E.
north-west and 93% in the south-west, respectively. and Atlantic puffins Fratercula arctica Ž144%., compared to the other species Ž31% in gannets Morus bassanus and 67% in great skuas Catharacta skua; Table 2.. The rates of mercury concentration increase were also greater in shearwaters and puffins Ž1.0]2.3% yeary1 . than those in the other species Ž0.3 and 0.4% yeary1 .. Mercury concentrations and d 15 N values in northern fulmars from Foula and St Kilda are presented in Table 3. The mean mercury concentration in body feather samples in northern fulmars from St Kilda Ž3.3 m g gy1 . was double that in birds from Foula Ž1.6 m g gy1 .. In contrast, the d 15 N value in northern fulmars from Foula Žmean s 14.2. was significantly higher than that in birds from St Kilda Žmean s 13.6: t-test, t s 2.68, d.f.s 58, Ps 0.01.. 4. Discussion In order that seabird feathers can be used reliably to monitor long-term trends in mercury levels in the marine environment, several conditions have to be met. Mercury concentrations in feathers should reflect endogenous incorporation of ingested mercury in a dose-dependent fashion and this is the case ŽLewis and Furness, 1991; Monteiro, 1996.. Mercury in feathers should be chemically and physically stable, which it is
Table 3 Mercury concentrations Ž m g gy1 . and stable nitrogen isotope ratio signatures Ž‰. in northern fulmars Fulmarus glacialis from Foula ŽShetland, UK. and St Kilda ŽOuter Hebrides, UK. Foula
St Kilda
Mercury
1.6" 0.1 Ž0.9]3.9. 3.3" 0.2 Ž1.2]11.5. 32 85 d15 N 14.2" 0.1 Ž12.5]15.4. 13.6" 0.1 Ž12.3]15.2. ŽTrophic status . 30 30 a
Values are mean " 1 S.E., range in parentheses and sample size Žnumber of birds..
ŽCrewther et al., 1965; Appelquist et al., 1984. and should not be affected by atmospheric deposition, which it is not ŽHahn et al., 1993.. Additionally, the diets of study species should not have changed over the course of the study period. There is little, if any, information about seabird diets around the turn of this century. Long-term trends in diet have been assessed in British Manx shearwaters using stable isotope analysis of historical and contemporary feather samples. The stable isotope signatures of nitrogen and carbon reflect those of the diet at the time of feather formation ŽHobson and Clark, 1992., so any change in isotope signature would therefore correspond to a change in diet. No such change was found in Manx shearwaters ŽThompson et al., 1995.. In northern fulmars around the British
D.R. Thompson et al. r The Science of the Total En¨ ironment 213 (1998) 299]305
Isles, however, long-term trends in mercury concentrations have been shown to deviate from the general increases presented in this article ŽThompson et al., 1992.. The patterns of long-term mercury concentration increases in seabirds from the warm-temperate North Atlantic presented in Table 1 can be divided into two broad categories. Firstly, relatively modest absolute increases and rates of increase were detected in Cory’s and little shearwaters and common terns ŽTable 1.. Little shearwaters and common terns are known to feed upon small, epipelagic fish Že.g. Macroramphosus scolapax ., whilst Cory’s shearwaters take mainly epipelagic prey, but with some mesopelagic prey also present in the diet ŽGranadeiro et al., 1995; Granadeiro and Monteiro unpublished data.. Since the diet of these seabirds comprises primarily epipelagic prey, these three species can be thought of as monitors of epipelagic waters. It is noteworthy that the observed rates of increase in mercury concentrations in these species Ž0.7]1.4% yeary1 ; Table 1. are consistent with current estimates of increase rates of mercury in surface ocean waters due to anthropogenic inputs. Mass balance models suggest a three-fold increase in surface ocean mercury concentrations since preindustrial times ŽMason et al., 1994., which translates to an average rate of 1.3% yeary1 over 150 years. In this respect, the use of time-series of feather samples from seabirds to elucidate longterm patterns of mercury contamination is complementary to that of sediment and peat cores and tree-rings ŽMadsen, 1981; Swain et al., 1992; Engstrom et al., 1994.. In contrast to the three species above, bandrumped storm petrels and Bulwer’s petrels exhibited relatively large increases in absolute mercury concentration and high rates of increase in mercury concentration, over the study period ŽTable 1.. Unlike the other species from this region, band-rumped storm petrels and Bulwer’s petrels feed extensively on mesopelagic prey which migrate vertically in the water column to the sea surface at night, notably lanternfish ŽMyctophidae; Granadeiro and Monteiro unpublished data.. The deep-water fish Argyropelecus sp. featured prominently in the diet of Bulwer’s petrel from
303
Madeira ŽZonfrillo, 1986.. Therefore these species represent biomonitors of mesopelagic waters. Increased concentrations of methylated mercury compounds are produced in low-oxygen waters ŽMason and Fitzgerald, 1993.. The enhanced mercury concentrations in seabirds which feed predominantly upon prey from sub-thermocline, low-oxygen water may, therefore indicate an increase in exposure to methylated mercury at depth in the ocean. Mesopelagic fish Žpreyed upon by seabirds. and their prey are known to co-occur over much of the daytime depth range and both migrate into the epipelagic zone at night ŽHopkins and Gartner, 1992; Perissonotto and McQuaid, 1992.. That organisms living at depth in the ocean are exposed to relatively high methylmercury concentrations through their diet is supported further by a relationship between whole-body mercury concentrations and median daytime depth in a range of Azorean fish species ŽMonteiro et al., 1996.. That study showed clearly that fish occupying sub-thermocline, mesopelagic marine zones exhibited relatively high mercury concentrations, in contrast to fish species found in relatively shallow water which had correspondingly lower mercury concentrations ŽMonteiro et al., 1996.. There exists, therefore a clear link between high mercury concentrations in organisms living at depth in the ocean and in seabirds which feed upon such prey. The results for British seabirds presented here also show inter-specific variation in the extent to which mercury concentrations have increased during this century ŽTable 2.. However, whilst feeding on mesopelagic prey has been recorded in Manx shearwaters from the far north-west of Scotland ŽThompson, 1987., the distinction between mesopelagic-feeding species and epipelagic-feeding species is far less well documented for British seabirds than for seabirds from the temperate North Atlantic. The extent to which great skuas and gannets feed on mesopelagic prey is almost certainly minimal, since both species feed during the day when mesopelagic prey would be at depth in the water column and these two species show the most modest absolute increases and rates of increase in mercury concentrations ŽTable 2.. All of the British species and sites
304
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sampled exhibited rates of increase in mercury concentrations which are consistent with estimates of increases in surface water mercury concentrations due to anthropogenic emissions of mercury and can be considered as representative of increases in predominantly epipelagic marine environments. Only Manx shearwaters from north-west Britain Žincluding sampling sites relatively close to the continental shelf edge and deep water. exhibited an increase in mercury concentration Ž176% and 2.3% yeary1 ; Table 2. which would tend to indicate some mesopelagic feeding. The fact that contemporary northern fulmars from St Kilda exhibited higher mercury concentrations than birds from Foula, yet were on average at a lower trophic position, as measured using stable nitrogen isotope analysis ŽTable 3., was perhaps somewhat surprising. Mercury is the only heavy metal for which good evidence exists for biomagnification up food chains ŽBryan, 1979.. Furthermore, dietary information for this species indicated a predominance of small fish, zooplankton and crustaceans at St Kilda, whilst discarded whitefish and fish offal from trawlers, together with sandeels Ammodytes sp., made up the bulk of the diet at Foula ŽFurness and Todd, 1984; Thompson et al., 1995.. However, among prey species taken by northern fulmars at St Kilda two were recorded that can be considered mesopelagic: the oplophorid decapod Acanthephyra pelagica and the melamphid fish Scopelogadus beanii ŽRoe, 1984; Gartner and Musick, 1989.. It would appear that the presence of mesopelagic prey in the diet has at least some influence on mercury concentrations over and above that from trophic status, at least in northern fulmars. Seabirds can effectively track long-term changes in mercury contamination of epipelagic and mesopelagic marine waters, based on inter-specific dietary preferences. Furthermore, measured trends in marine birds are in general agreement with model predictions for the surface waters of the ocean. These findings greatly support the use of seabirds as monitors of mercury within the marine environment. The relatively large increases in mercury concentrations in seabirds which feed on mesopelagic prey have clear implications for future human exploitation of me-
sopelagic marine resources and it would appear that increases in mercury pollution in mesopelagic food webs deserve further research. Acknowledgements This research was supported by The Carnegie Trust, The Nuffield Foundation, NERC and Junta Nacional de Investigac¸˜ ao Cientıfica ´ through grant BDr2289r92-IG to L.R. Monteiro and research contract STRDBrCrMARr228r92. We thank the staff of the museums from which we were allowed to sample seabird feather samples and two anonymous reviewers for their constructive comments of an earlier version of this article. References Appelquist H, Asbirk S, Drabaek I. Mercury monitoring: mercury stability in bird feathers. Mar Pollut Bull 1984;15:22]24. Appelquist H, Drabaek I, Asbirk S. Variation in mercury content of guillemot feathers over 150 years. Mar Pollut Bull 1985;16:244]248. Braune BM, Gaskin DE. Mercury levels in Bonaparte’s gulls Ž Larus philadelphia. during autumn moult in the Quoddy Region, New Brunswick, Canada. Arch Environ Contam Toxicol 1987;16:539]549. Bryan GW. Bioaccumulation of marine pollutants. Philos Trans R Soc London, Ser B 1979;286:483]505. Crewther WG, Fraser RDB, Lennox FG, Lindley H. The chemistry of keratins. Adv Protein Chem 1965;20:191]346. Engstrom DR, Swain EB, Henning TA, Brigham ME, Brezonik PL. Atmospheric mercury deposition to lakes and watersheds } a quantitative reconstruction from multiple sediment cores. Adv Chem Ser 1994;237:33]66. Furness RW. Birds as monitors of pollutants. In: Furness RW, Greenwood JJD, editors. Birds as monitors of environmental change. London: Chapman and Hall 1993:86-143. Furness RW, Hutton M. Pollutant level in the great skua Catharacta skua. Environ Pollut 1979;19:261]268. Furness RW, Todd CM. Diets and feeding of fulmars Fulmarus glacialis during the breeding season: a comparison between St Kilda and Shetland colonies. Ibis 1984;126:379]387. Furness RW, Muirhead SJ, Woodburn M. Using bird feathers to measure mercury in the environment: relationships between mercury content and moult. Mar Pollut Bull 1986;17:27]30. Gartner JV, Musick JA. Feeding habits of the deep-sea fish Scopelogadus beanii ŽPisces: Melamphidae., in the western north Atlantic. Deep Sea Res 1989;36:1457]1469.
D.R. Thompson et al. r The Science of the Total En¨ ironment 213 (1998) 299]305 Ginn HB, Melville DS. Moult in Birds. British Trust for Ornithology, Tring, Hertfordshire, 1983:112. Granadeiro JP, Monteiro LR, Furness RW, Silva MC. The food of common terns Sterna hirundo in the Azores. In: Abstracts of the 5th International Seabird Group Conference. Glasgow, March, 1995:24. Hahn E, Hahn K, Stoeppler M. Bird feathers as bioindicators in areas of the German Environmental Specimen Bank } bioaccumulation of mercury in food chains and exogenous deposition of atmospheric pollution with lead and cadmium. Sci Total Environ 1993;139r140:259]270. Hobson KA, Clark RG. Assessing avian diets using stable isotopes I: turnover of d 13 C in tissues. Condor 1992;94:181]188. Hobson KA, Piatt JF, Pitocchelli J. Using stable isotopes to determine seabird trophic relationships. J Anim Ecol 1994;63:786]798. Honda K, Nasu T, Tatsukawa R. Seasonal changes in mercury accumulation in the black-eared kite, Mil¨ us migrans lineatus. Environ Pollut ŽA. 1986;42:325]334. Hopkins TL, Gartner JV. Resource-partitioning and predation impact of low-latitude myctophid community. Mar Biol 1992;114:185]197. Lewis SA, Furness RW. Mercury accumulation and excretion in laboratory reared black-headed gull Larus ridibundus chicks. Arch Environ Contam Toxicol 1991;21:316]320. Madsen PP. Peat bog records of atmospheric mercury deposition. Nature 1981;293:127]130. Mason RP, Fitzgerald WF. The distribution and biogeochemical cycling of mercury in the equatorial Pacific Ocean. Deep Sea Res 1993;40:1897]1924. Mason RP, Fitzgerald WF, Morel FMM. The biogeochemical cycling of elemental mercury: anthropogenic influences. Geochim Cosmochim Acta 1994;58:3191]3198. Monteiro LR. Seabirds as monitors of mercury contamination in the Portuguese Atlantic. PhD Thesis, University of Glasgow, 1996. Monteiro LR, Furness RW. Seabirds as monitors of mercury in the marine environment. Water Air Soil Pollut 1995;80:851]870. Monteiro LR, Costa V, Furness RW, Santos RS. Mercury concentrations in prey fish indicate enhanced bioaccumulation in mesopelagic environments. Mar Ecol Prog Ser 1996;141:21]25. Muirhead SJ. The accumulation, storage and elimination of metals and organochlorines in the great skua Catharacta skua and metal accumulation in Atlantic Procellariiformes. PhD Thesis, University of Glasgow, 1986. Perissonotto R, McQuaid CD. Land-based predator impact on vertically migrating zooplankton and micronekton advected
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to a southern Ocean archipelago. Mar Ecol Prog Ser 1992;80:15]27. Roe HSJ. The diel migrations and distributions within a mesopelagic community in the north east Atlantic. 2. Vertical migrations and feeding of mysids and decapod Crustacea. Prog Oceanogr 1984;13:269]318. Swain EB, Engstrom DR, Brigham ME, Henning TA, Brezonik PL. Increasing rates of atmospheric mercury deposition in midcontinental North America. Science 1992;257:784]787. Thompson DR. Mercury in birds and terrestrial mammals. In: Beyer WN, Heinz GH, Redmon-Norwood AW, editors. Environmental contaminants in wildlife, SETAC Special Publication Series. Boca Raton, Florida: CRC Lewis Publishers 1996:341-356. Thompson DR, Furness RW. Comparison of the levels of total and organic mercury in seabird feathers. Mar Pollut Bull 1989;20:577]579. Thompson DR, Becker PH, Furness RW. Long-term changes in mercury concentration in herring gulls Larus argentatus and common terns Sterna hirundo from the German North Sea coast. J Appl Ecol 1993a;30:316]320. Thompson DR, Furness RW, Lewis SA. Temporal and spatial variation in mercury concentrations in some albatrosses and petrels from the sub-Antarctic. Polar Biol 1993b;13:239]244. Thompson DR, Furness RW, Lewis SA. Diets and long-term changes in d 15 N and d 13 C values in northern fulmars Fulmarus glacialis from two northeast Atlantic colonies. Mar Ecol Prog Ser 1995;125:3]11. Thompson DR, Furness RW, Walsh PM. Historical changes in mercury concentrations in the marine ecosystem of the north and north-east Atlantic ocean as indicated by seabird feathers. J Appl Ecol 1992;29:79]84. Thompson DR, Hamer KC, Furness RW. Mercury accumulation in great skuas Catharacta skua of known age and sex and its effects upon breeding and survival. J Appl Ecol 1991;28:672]684. Thompson KR. The ecology of the Manx shearwater Puffinus puffinus on Rhum, west Scotland. PhD Thesis, University of Glasgow, 1987. Uthe JF, Solomon J, Grift B. Rapid semimicro method for the determination of methyl mercury in fish tissue. J Assoc Off Anal Chem 1972;55:583]589. Walsh PM. The use of seabirds as monitors of heavy metals in the marine environment. In: Furness RW, Rainbow PS, editors. Heavy Metals in the Marine Environment. Boca Raton, Florida: CRC Press 1990:183-204. Zonfrillo B. Diet of Bulwer’s petrel Bulweria bulwerii in the Madeiran archipelago. Ibis 1986;128:570]572.
Seabirds as biomonitors of mercury inputs to epipelagic and mesopelagic marine food chains David R. Thompsona,U , Robert W. Furness a , Luis R. Monteiro b a b
Applied Ornithology Unit, Graham Kerr Building, Uni¨ ersity of Glasgow, Glasgow, G12 8QQ UK Department of Oceanography and Fisheries, Uni¨ ersity of the Azores, 9900 Horta, Azores, Portugal
Abstract Mercury concentrations are presented for time-series of feather samples from seabirds feeding near the apex of epipelagic and mesopelagic marine food chains in the south-east and north-east North Atlantic. These quantify historical increases in surface and deep water mercury concentrations due to mercury pollution. Our results highlight the importance of mercury methylation in mesopelagic water as the factor responsible for the greatest increases in seabird mercury concentrations, which occur in seabirds feeding primarily on mesopelagic prey. Seabirds which feed on prey occupying the epipelagic zone exhibited more modest increases in mercury concentration than mesopelagic feeders, but the rates of increase in the epipelagic-feeding birds are in agreement with recent model predictions regarding anthropogenic inputs of mercury to the environment. We investigated the importance of mesopelagic prey in the diet of seabirds, as opposed to trophic status, in determining mercury concentrations. Analysis of stable isotope ratios of nitrogen revealed that trophic status was not the principal factor in determining mercury concentration and that the presence of mesopelagic prey in the diet was likely to contribute more to the patterns of mercury burdens. Q 1998 Elsevier Science B.V. Keywords: Seabirds; Biomonitoring; Mercury; Epipelagic; Mesopelagic; Stable isotopes
1. Introduction Seabirds have featured prominently in monitoring of mercury contamination of the marine
U
Corresponding author. Present address: National Institute of Water and Atmospheric Research, 301 Evans Bay Parade, Greta Point, P.O. Box 14-901, Kilbirnie, Wellington, New Zealand. E-mail: [email protected]
environment ŽWalsh, 1990; Furness, 1993; Monteiro and Furness, 1995; Thompson, 1996.. They tend to accumulate high mercury concentrations compared to other groups within marine food chains since they occupy relatively high trophic positions. Furthermore, mercury binds strongly to feather keratins ŽCrewther et al., 1965. during feather growth and mercury is not lost from feathers, even after various vigorous treatments ŽAppelquist et al., 1984.. The mercury concentra-
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tion in a sample of feathers, therefore provides an easily-obtainable, relatively non-invasive measure of the mercury burden of a given individual. The use of feathers to measure mercury concentrations in seabirds is further enhanced since mercury concentrations of feathers have been shown to correlate positively with those in internal tissues ŽFurness and Hutton, 1979; Thompson et al., 1991., thus avoiding the need to sacrifice large numbers of birds. Mercury concentrations in feathers reflect the uptake and storage of mercury during the period between moults wmost seabirds do not moult feathers over a 5]6-month period ŽGinn and Melville, 1983.x, rather than short-term uptake ŽFurness et al., 1986; Honda et al., 1986; Braune and Gaskin, 1987.. A major advantage afforded by seabirds over other marine groups is their suitability for investigations of temporal patterns of mercury contamination, since many seabirds have been preserved as study skins in museum collections. Feather samples from such collections represent a record of mercury concentrations in different species from many locations dating back to the middle of the 19th century. Problems with sample contamination through the application of inorganic mercury as a preservative can be overcome through an initial organic mercury extraction, since virtually all the biologically incorporated mercury in seabird feathers has been shown to be organic ŽThompson and Furness, 1989.. Time-series of feather samples have been used in this way to investigate long-term patterns of mercury contamination of seabirds from Greenland, the Faeroe Islands, the Baltic Sea and the Kattegat ŽAppelquist et al., 1985., around the British Isles ŽThompson et al., 1992., the German North Sea coast ŽThompson et al., 1993a. and from a range of southern ocean sites ŽThompson et al., 1993b.. Here we present a re-evaluation of the British Isles data ŽThompson et al., 1992., investigating rates of change in mercury concentrations and an initial appraisal of the long-term patterns of mercury contamination in warm-temperate North Atlantic seabirds. For both regions, we examine whether observed patterns of mercury contamination in seabirds Žpatterns of long-term change and inter-specific differences in contemporary
seabirds. are related to differences in diet. We further investigate the importance of diet as a major determinant of mercury concentration in northern fulmars Fulmarus glacialis, incorporating the use of stable isotope analysis to define trophic status. Our results are discussed in relation to model predictions regarding long-term patterns of mercury deposition over the last 100 years. 2. Methods Long-term patterns of mercury concentrations in seabirds were investigated through the analysis of feather samples from study skins held in museum collections, these being compared to mercury concentration in feather samples from contemporary, free-living seabirds of the same species and from the same sites. In all cases, a small number of body feathers Ž6]10. were removed, pooled and stored prior to mercury analysis in polythene bags. Feather samples from historical samples were analysed for organic Žmethyl. mercury only, following a chloroformracetone wash to remove gross surface contamination ŽMuirhead, 1986. and an extraction of organic mercury using toluene. The method used was adapted from that used by Uthe et al. Ž1972. to extract methylmercury from fish tissue and is described more fully by Thompson and Furness Ž1989.. Contemporary samples were analysed for ‘total’ mercury, this being equivalent to the organic Žmethyl. mercury concentration since seabird feather mercury has been shown to be virtually all organic ŽThompson and Furness, 1989., following standard acid digestion. All samples Žextracted methyl mercury from historical samples and total mercury from contemporary samples. were analysed using cold vapour absorption spectrophotometry. For details of species and sites sampled from around the British Isles see Thompson et al. Ž1992.. Seabird species sampled from the warm-temperate North Atlantic Žprimarily the Azores archipelago. were Bulwer’s petrel Bulweria bulwerii, band-rumped storm petrel Oceanodroma castro, Cory’s shearwater Calonectris diomedea, little shearwater Puffinus assimilis and common tern Sterna hirundo. In all cases,
D.R. Thompson et al. r The Science of the Total En¨ ironment 213 (1998) 299]305
comparisons have been made between birds sampled prior to 1931 Žas being indicative of an environment relatively free of anthropogenic mercury; the vast majority of these birds dated from around the turn of this century. and from after 1979 Žas being indicative of an environment relatively contaminated by anthropogenic mercury.. Rates of change in mercury concentrations over this period have been calculated by using the median sampling years from each period as ‘end points’. For all species studied, there was no evidence to indicate any change or shift in diet had occurred over the study period. The relationships between mercury concentration in a seabird and its diet and trophic status were investigated in two geographically distinct populations of northern fulmars known to have markedly different diets. At Foula ŽShetland., northern fulmars are known to feed mainly upon small fish and discarded fish and fish offal from whitefish trawlers, whilst at St Kilda ŽOuter Hebrides., small fish, zooplankton and crustaceans make up the bulk of the fulmar diet ŽFurness and Todd, 1984; Thompson et al., 1995.. Trophic status was defined through the analysis of nitrogen stable isotope ratios Žconventionally expressed as d 15 N s Žw 15 Nr 14 Nsampler 15 Nr 14 Nstandard x y 1. = 10 3 . in homogenised body feather samples. The stable isotope ratio of nitrogen shows a step-wise enrichment up food chains ŽHobson et al., 1994.,
301
such that the higher the value of d 15 N Ženriched in 15 N relative to 14 N., the higher the trophic status of a particular individual or species. Mean d 15 N values from body feather samples for each site were compared with mean mercury concentrations in order to relate any difference in mercury burden between the two sites to trophic status, as defined by the d 15 N signature. 3. Results Historical patterns of mercury in seabirds from the warm-temperate North Atlantic are presented in Table 1. All species exhibited an increase over the study period. However, the increases in mercury concentrations in band-rumped storm petrels Ž397%. and Bulwer’s petrels Ž260%. were considerably greater than those in the other three species from this area Ž65]100%; Table 1.. The corresponding rates of increase in mercury concentration in band-rumped storm petrels Ž4.1% yeary1 . and Bulwer’s petrels Ž2.9% yeary1 . were also far greater than those in the other species Ž0.7]1.4% yeary1 ; Table 1.. Historical patterns of mercury concentrations in seabirds from around the British Isles are presented in Table 2. Again, all species studied exhibited an increase in mercury concentration, but the increase tended to be greatest in Manx shearwaters Puffinus puffinus Ž176% in the
Table 1 Long-term trends in mercury concentrations Ž m g gy1 . in seabird feathers from the warm-temperate North Atlantic Species
Pre-1931a
Post-1979a
Increase Ž%.
Increase Ž% yeary1 .
Band-rumped storm petrel Oceanodroma castro
3.0 Ž16. 0.1
14.9 Ž47. 0.5
394
4.1
Bulwer’s petrel Bulweria bulwerii
6.0 Ž30. 0.7
21.6 Ž55. 0.7
260
2.9
Cory’s shearwater Calonectris diomedea
2.7 Ž48. 0.1
5.4 Ž219. 0.1
100
1.4
Common tern Sterna hirundo
1.1 Ž15. 0.1
2.0 Ž22. 0.1
82
1.3
Little shearwater Puffinus assimilis
1.7 Ž15. 0.2
2.8 Ž34. 0.2
65
0.7
a
Values are mean, sample size Žnumber of birds. in parentheses and S.E.
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Table 2 Long-term trends in mercury concentrations Ž m g gy1 . in seabird feathers from the British Isles Species
Pre-1931a
Post-1979a
Increase Ž%.
Increase Ž% yeary1 .
Manx shearwater Puffinus puffinus Žnorth-west British Isles.
1.7 Ž14. 0.2
4.7 Ž78. 0.2
176
2.3
Manx shearwater Žsouth-west British Isles.
1.5 Ž17. 0.2
2.9 Ž22. 0.2
93
1.0
Atlantic puffin Fratercula arctica Žwest Britain.
1.8 Ž49. 0.1
4.4 Ž61. 0.2
144
1.5
Great skua Catharacta skua Žnorth-east Atlantic.
4.2 Ž13. 0.6
7.0 Ž212. 0.3
67
0.4
Gannet Morus bassanus ŽBass Rock, east Britain.
5.9 Ž19. 0.6
7.7 Ž38. 0.5
31
0.3
a
Values are mean, sample size Žnumber of birds. in parentheses and S.E.
north-west and 93% in the south-west, respectively. and Atlantic puffins Fratercula arctica Ž144%., compared to the other species Ž31% in gannets Morus bassanus and 67% in great skuas Catharacta skua; Table 2.. The rates of mercury concentration increase were also greater in shearwaters and puffins Ž1.0]2.3% yeary1 . than those in the other species Ž0.3 and 0.4% yeary1 .. Mercury concentrations and d 15 N values in northern fulmars from Foula and St Kilda are presented in Table 3. The mean mercury concentration in body feather samples in northern fulmars from St Kilda Ž3.3 m g gy1 . was double that in birds from Foula Ž1.6 m g gy1 .. In contrast, the d 15 N value in northern fulmars from Foula Žmean s 14.2. was significantly higher than that in birds from St Kilda Žmean s 13.6: t-test, t s 2.68, d.f.s 58, Ps 0.01.. 4. Discussion In order that seabird feathers can be used reliably to monitor long-term trends in mercury levels in the marine environment, several conditions have to be met. Mercury concentrations in feathers should reflect endogenous incorporation of ingested mercury in a dose-dependent fashion and this is the case ŽLewis and Furness, 1991; Monteiro, 1996.. Mercury in feathers should be chemically and physically stable, which it is
Table 3 Mercury concentrations Ž m g gy1 . and stable nitrogen isotope ratio signatures Ž‰. in northern fulmars Fulmarus glacialis from Foula ŽShetland, UK. and St Kilda ŽOuter Hebrides, UK. Foula
St Kilda
Mercury
1.6" 0.1 Ž0.9]3.9. 3.3" 0.2 Ž1.2]11.5. 32 85 d15 N 14.2" 0.1 Ž12.5]15.4. 13.6" 0.1 Ž12.3]15.2. ŽTrophic status . 30 30 a
Values are mean " 1 S.E., range in parentheses and sample size Žnumber of birds..
ŽCrewther et al., 1965; Appelquist et al., 1984. and should not be affected by atmospheric deposition, which it is not ŽHahn et al., 1993.. Additionally, the diets of study species should not have changed over the course of the study period. There is little, if any, information about seabird diets around the turn of this century. Long-term trends in diet have been assessed in British Manx shearwaters using stable isotope analysis of historical and contemporary feather samples. The stable isotope signatures of nitrogen and carbon reflect those of the diet at the time of feather formation ŽHobson and Clark, 1992., so any change in isotope signature would therefore correspond to a change in diet. No such change was found in Manx shearwaters ŽThompson et al., 1995.. In northern fulmars around the British
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Isles, however, long-term trends in mercury concentrations have been shown to deviate from the general increases presented in this article ŽThompson et al., 1992.. The patterns of long-term mercury concentration increases in seabirds from the warm-temperate North Atlantic presented in Table 1 can be divided into two broad categories. Firstly, relatively modest absolute increases and rates of increase were detected in Cory’s and little shearwaters and common terns ŽTable 1.. Little shearwaters and common terns are known to feed upon small, epipelagic fish Že.g. Macroramphosus scolapax ., whilst Cory’s shearwaters take mainly epipelagic prey, but with some mesopelagic prey also present in the diet ŽGranadeiro et al., 1995; Granadeiro and Monteiro unpublished data.. Since the diet of these seabirds comprises primarily epipelagic prey, these three species can be thought of as monitors of epipelagic waters. It is noteworthy that the observed rates of increase in mercury concentrations in these species Ž0.7]1.4% yeary1 ; Table 1. are consistent with current estimates of increase rates of mercury in surface ocean waters due to anthropogenic inputs. Mass balance models suggest a three-fold increase in surface ocean mercury concentrations since preindustrial times ŽMason et al., 1994., which translates to an average rate of 1.3% yeary1 over 150 years. In this respect, the use of time-series of feather samples from seabirds to elucidate longterm patterns of mercury contamination is complementary to that of sediment and peat cores and tree-rings ŽMadsen, 1981; Swain et al., 1992; Engstrom et al., 1994.. In contrast to the three species above, bandrumped storm petrels and Bulwer’s petrels exhibited relatively large increases in absolute mercury concentration and high rates of increase in mercury concentration, over the study period ŽTable 1.. Unlike the other species from this region, band-rumped storm petrels and Bulwer’s petrels feed extensively on mesopelagic prey which migrate vertically in the water column to the sea surface at night, notably lanternfish ŽMyctophidae; Granadeiro and Monteiro unpublished data.. The deep-water fish Argyropelecus sp. featured prominently in the diet of Bulwer’s petrel from
303
Madeira ŽZonfrillo, 1986.. Therefore these species represent biomonitors of mesopelagic waters. Increased concentrations of methylated mercury compounds are produced in low-oxygen waters ŽMason and Fitzgerald, 1993.. The enhanced mercury concentrations in seabirds which feed predominantly upon prey from sub-thermocline, low-oxygen water may, therefore indicate an increase in exposure to methylated mercury at depth in the ocean. Mesopelagic fish Žpreyed upon by seabirds. and their prey are known to co-occur over much of the daytime depth range and both migrate into the epipelagic zone at night ŽHopkins and Gartner, 1992; Perissonotto and McQuaid, 1992.. That organisms living at depth in the ocean are exposed to relatively high methylmercury concentrations through their diet is supported further by a relationship between whole-body mercury concentrations and median daytime depth in a range of Azorean fish species ŽMonteiro et al., 1996.. That study showed clearly that fish occupying sub-thermocline, mesopelagic marine zones exhibited relatively high mercury concentrations, in contrast to fish species found in relatively shallow water which had correspondingly lower mercury concentrations ŽMonteiro et al., 1996.. There exists, therefore a clear link between high mercury concentrations in organisms living at depth in the ocean and in seabirds which feed upon such prey. The results for British seabirds presented here also show inter-specific variation in the extent to which mercury concentrations have increased during this century ŽTable 2.. However, whilst feeding on mesopelagic prey has been recorded in Manx shearwaters from the far north-west of Scotland ŽThompson, 1987., the distinction between mesopelagic-feeding species and epipelagic-feeding species is far less well documented for British seabirds than for seabirds from the temperate North Atlantic. The extent to which great skuas and gannets feed on mesopelagic prey is almost certainly minimal, since both species feed during the day when mesopelagic prey would be at depth in the water column and these two species show the most modest absolute increases and rates of increase in mercury concentrations ŽTable 2.. All of the British species and sites
304
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sampled exhibited rates of increase in mercury concentrations which are consistent with estimates of increases in surface water mercury concentrations due to anthropogenic emissions of mercury and can be considered as representative of increases in predominantly epipelagic marine environments. Only Manx shearwaters from north-west Britain Žincluding sampling sites relatively close to the continental shelf edge and deep water. exhibited an increase in mercury concentration Ž176% and 2.3% yeary1 ; Table 2. which would tend to indicate some mesopelagic feeding. The fact that contemporary northern fulmars from St Kilda exhibited higher mercury concentrations than birds from Foula, yet were on average at a lower trophic position, as measured using stable nitrogen isotope analysis ŽTable 3., was perhaps somewhat surprising. Mercury is the only heavy metal for which good evidence exists for biomagnification up food chains ŽBryan, 1979.. Furthermore, dietary information for this species indicated a predominance of small fish, zooplankton and crustaceans at St Kilda, whilst discarded whitefish and fish offal from trawlers, together with sandeels Ammodytes sp., made up the bulk of the diet at Foula ŽFurness and Todd, 1984; Thompson et al., 1995.. However, among prey species taken by northern fulmars at St Kilda two were recorded that can be considered mesopelagic: the oplophorid decapod Acanthephyra pelagica and the melamphid fish Scopelogadus beanii ŽRoe, 1984; Gartner and Musick, 1989.. It would appear that the presence of mesopelagic prey in the diet has at least some influence on mercury concentrations over and above that from trophic status, at least in northern fulmars. Seabirds can effectively track long-term changes in mercury contamination of epipelagic and mesopelagic marine waters, based on inter-specific dietary preferences. Furthermore, measured trends in marine birds are in general agreement with model predictions for the surface waters of the ocean. These findings greatly support the use of seabirds as monitors of mercury within the marine environment. The relatively large increases in mercury concentrations in seabirds which feed on mesopelagic prey have clear implications for future human exploitation of me-
sopelagic marine resources and it would appear that increases in mercury pollution in mesopelagic food webs deserve further research. Acknowledgements This research was supported by The Carnegie Trust, The Nuffield Foundation, NERC and Junta Nacional de Investigac¸˜ ao Cientıfica ´ through grant BDr2289r92-IG to L.R. Monteiro and research contract STRDBrCrMARr228r92. We thank the staff of the museums from which we were allowed to sample seabird feather samples and two anonymous reviewers for their constructive comments of an earlier version of this article. References Appelquist H, Asbirk S, Drabaek I. Mercury monitoring: mercury stability in bird feathers. Mar Pollut Bull 1984;15:22]24. Appelquist H, Drabaek I, Asbirk S. Variation in mercury content of guillemot feathers over 150 years. Mar Pollut Bull 1985;16:244]248. Braune BM, Gaskin DE. Mercury levels in Bonaparte’s gulls Ž Larus philadelphia. during autumn moult in the Quoddy Region, New Brunswick, Canada. Arch Environ Contam Toxicol 1987;16:539]549. Bryan GW. Bioaccumulation of marine pollutants. Philos Trans R Soc London, Ser B 1979;286:483]505. Crewther WG, Fraser RDB, Lennox FG, Lindley H. The chemistry of keratins. Adv Protein Chem 1965;20:191]346. Engstrom DR, Swain EB, Henning TA, Brigham ME, Brezonik PL. Atmospheric mercury deposition to lakes and watersheds } a quantitative reconstruction from multiple sediment cores. Adv Chem Ser 1994;237:33]66. Furness RW. Birds as monitors of pollutants. In: Furness RW, Greenwood JJD, editors. Birds as monitors of environmental change. London: Chapman and Hall 1993:86-143. Furness RW, Hutton M. Pollutant level in the great skua Catharacta skua. Environ Pollut 1979;19:261]268. Furness RW, Todd CM. Diets and feeding of fulmars Fulmarus glacialis during the breeding season: a comparison between St Kilda and Shetland colonies. Ibis 1984;126:379]387. Furness RW, Muirhead SJ, Woodburn M. Using bird feathers to measure mercury in the environment: relationships between mercury content and moult. Mar Pollut Bull 1986;17:27]30. Gartner JV, Musick JA. Feeding habits of the deep-sea fish Scopelogadus beanii ŽPisces: Melamphidae., in the western north Atlantic. Deep Sea Res 1989;36:1457]1469.
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