Gannets and toxic chemicals J. L. F. Parslow and D. J. Jefferies Feeding on large fish, Gannets are especially prone t o receive large quantities o f certain toxic c h e m i c a l s . Eggshell thinning h a s b e e n recorded A programme to investigate the occurrence and effects of chemical pollutants in British seabirds has been in progress at Monks Wood Experimental Station, Cambridgeshire, for some years. While the main effort has been concentrated on the auks (Alcidae), some information is also available for other species, including the Gannet Sula bassana. Toxic chemicals in full-grown Gannets Tissues or organs (usually livers) from 19 Gannets (16 adults, two twoyear-olds, one first-autumn) found dead or dying during 1968-74 have been analysed for various toxic chemical residues. Twelve were from the west coast (Cumbria to north Devon), five from the east (Fife to Norfolk), one from the south (south Devon) and one from inland (Northampton). Most had been washed up dead or moribund and were light in weight, having evidently starved before dying; seven were among many Gannets in an incident involving unusually heavy mortality on the Lancashire coast during late May and early June 1972, the cause of which was not fully established (Parslow et al. 1973). Organochlorine insecticides and PCB Measurable residues of polychlorinated biphenyls (PCB) and DDE (the chief breakdown product of DDT found in birds) are present in virtually all British seabirds; many contain residues of other organochlorine materials, such as dieldrin and hexachlorobenzene (HCB), usually in much smaller quantities; PCB and HCB derive chiefly from industrial use, the others mainly from agricultural insecticides. All are fat soluble, and most are highly persistent; they probably enter seabirds mainly in their food. In fish such as the cod Gadus morhua, it has been found that the 366 [Brit. Birds 70: 366-372, September 1977] Gannets and toxic chemicals 367 concentrations of DDT in the liver increase with the animal's weight (Stenersen and Kvalvag 1972): thus, large fish carry actually and relatively greater organochlorine residues than do small fish. This is probably related to the amount of lipid in the bodies of the large fish. Since Gannets feed on large fish (such as pollack Pollachius pollachius, saithe P. virens and haddock Melanogrammus aeglefinus; Wither by et al. 1940) compared with most other British seabirds, they tend to contain larger residues of organochlorines than other species which frequent the offshore marine zone. In healthy birds, organochlorine concentrations in organs such as the liver are low; the greatest are in subcutaneous and other fat, where they are probably inert. They can, however, be mobilised at times of stress, when birds utilise their fat; on release into the circulatory system, they pass to other organs and can affect, for example, the endocrine system (Jefferies and Parslow 1972); if the amounts are high enough, they can cause death (Prestt et al. 1970). The concentrations of organochlorines present in different organ", thus depend in part on the bird's state of health before death: a bird dying after a period of debilitation, without fat deposits, contains higher liver residues than one dying rapidly, due to an accident, for instance (Parslow and Jefferies 1973). Partly because of this, but also because of individual and interspecific differences in sensitivity to diverse materials, interpretation of the biological significance of different liver residues is difficult. A high concentration of, say, PCB may have contributed towards a bird's death, but, at the levels found in British seabirds, is unlikely to have been the initial cause of it. Results of various chemical analyses of British Gannets are set out in table 1. The following main conclusions can be drawn: 1. As in all British seabirds, PCBs are present in higher amounts than is DDE. 2. Mean liver concentrations and amounts in Gannets dying after a period of starvation are higher than in most other seabirds. For example, the mean PCB concentration in the livers of the seven Lancashire Gannets was 200 parts per million (ppm) wet weight, nearly twice as high as in the livers of 57 Guillemots Uria aalge which died in the Irish Sea in autumn 1969 (mean, 116 ppm) (Holdgate 1971, Parslow and Jefferies 1973); and their total body loads were probably five to ten times higher (25-29 mg compared with 3.6-5.5 mg) (Parslow et al. 1973). 3. There is some indication that Gannets dying on the west coast of Britain contain rather more PCB than those dying on the east, and proportionately more PCB than DDE, but the differences are less marked than in some more sedentary seabird species. 4. In five Gannets whose brain tissues were analysed, PCB (also DDE) concentrations in the brain were about three times lower than in the liver: in birds which had died from PCB poisoning, brain residues might be expected to be much closer to liver residues (Prestt et al. 1970). Heavy metals Mercury and cadmium are of particular concern because of their high toxicity. Both occur naturally in seawater, and locally increased levels can arise through natural causes as well as through contamination. Fisheating seabirds contain higher levels of mercury in their livers than most other British birds. Among about 30 marine and estuarine species (about 750 livers analysed), arithmetic mean concentrations of mercury in the * * 1780 1840 1915 Ad Ad Ad Ad Ad Ad Ad Ad Ad Ad 2Y iY Ad 26.3.72 25.4.72 4-'-73 31.8.73 28.4.74 28.8.74 15-9-74 23.10.74 Fife Yorkshire Northampton Pembroke Northumberland Somerset S Devon Norfolk 2Y 1820 1690 3685 2325 2230 2710 2290 2300 2100 2180 1660 3140 1900 * 30-5-72 1.6.72 26.5.72 5.6.72 4.6.72 4.6.72 4.6.72 27.2.72 Ad Ad Ad Ad Ad 8.8.70 12.11.69 12.11.69 N Devon Cumbria Cumbria Lancashire Lancashire Lancashire Lancashire Lancashire Lancashire Lancashire Fife 37-17 27-55 27.23 26.94 24.48 39-37 33-63 58.85 54-3° 34-91 57.88 46.46 96-39 40.02 53-i6 34-74 29-37 37.80 35-12 L L L L L L L L L L L F L F L M L L B L B L B L B L B Body Liver w t ( g ) wt (g) Tissue Date County Age 12 34 2 10 5 5 21 42 3 16 201 13 42 6 3 57 13 5 18 7 < i 8 39 15 5i 13 151 5> 35 21 1.06 4-4» 3-30 7-52 5.80 8.03 4.14 7-56 3-73 6.26 2-34 6.47 62 45 < i 70 321 227 204 11 8 •3 '4 '5 * * * * * * * * * * * * * 2-9 82.16 72.23 7i-3i 80.44 73-65 Si-59 73-73 80.43 75-30 83.28 76.47 4 17 2 6 8 3 6 17 <o.7 <o-5 <o.7 4.6 <o.7 2.8 4.1 <o.8 o-5 <o.7 3 5-5 * 6.3 * * * * * * * * * * * * 9-2 2.4 Cd 12 8 * * * 18 77-99 * 6 * * 3-6 <o.o5 68.54 98 9 20 18 66.81 * 71.16 20 21 16 * 16 * 77-56 75-45 79-43 77-03 74-97 27 53 Hg PPM 13RY WT 0.6 4.0 13 115 226 198 85.68 3-57 2.71 a-53 3-35 3-15 3.16 8.87 66.71 3.11 * * * * * * 10 150 112 3.18 3-39 3-75 , 75-77 73-98 * 0.6 0.8 12 10 * * 120 * 2.52 /a DDE Dieldrin water PPM WET W EIGHT PCB fat % * * * 41 * '45 <4 * 20 * 4 * 40 * 57 * "9 * 135 * 37 47 56 46 * * * * * * * * * * * * 20 128 Cd * 132 * 109 * 254 176 293 "35 279 129 "97 102 * 45° 372 Hg LIVER LC)AD (fJLj * = not measured. Under 'Tissue', L = liver, F = fat, M = muscle, B = brain. ' % fat' column refers to proportion of crude, hexane-extractable fat in sample. Hg = mercury, Cd = cadmium Table i. Chemical analyses of tissues and organs front 19 Gannets Sulci bassana found dead in Britain during 1969-74 Gannets and toxic chemicals 369 19 Gannets listed in table 1 (22 ppm dry weight) were exceeded only by four estuarine or inshore feeders: the Shag Phalacrocorax aristotelis (23 ppm), Cormorant P. carbo (36 ppm), Common Scoter Melanitta nigra (37 ppm) and Red-breasted Merganser Mergus senator (40 ppm). Other species feeding mainly offshore, such as Guillemots and Razorbills Aha tarda, contained, on average, lower concentrations in their livers than did Gannets, while oceanic birds contained much less mercury. This pattern is probably related to differences in exposure to mercury through food: inshore animals are in general more contaminated than those offshore, and larger fish carry actually and relatively higher amounts of mercury than do smaller ones (Johnels et al. 1967, Suzuki et al. 1973). Mercury amounts in the livers of nine west coast adult Gannets (mean 246 jig) were higher than in five east coast adults (mean 157 jig), though the difference is not significant. In the case of cadmium, the picture is different. Gannets, in common with other seabirds which feed mainly in offshore waters, contain less cadmium in their livers (mean 4.7 ppm dry weight, seven adults) than do mainly pelagic feeders (e.g. Fulmar Fulmarus glacialis, mean 37 ppm, 11 individuals) or certain littoral and sublittoral mollusc feeders (e.g. Oystercatcber Haematopus ostralegus, mean 29 ppm, 16 adults; Eider Somateria mollissima, mean 10 ppm, eight adults). The higher concentrations found in oceanic and some littoral species are probably due to certain invertebrates on which they feed being themselves concentrators of cadmium. Toxic chemicals in Gannet eggs During 1971-74, series of Gannet eggs were collected for chemical analysis and investigation of shell thickness from four colonies: Ailsa Craig, Strathclyde (annually), Bass Rock, Lothian (1973-74), Scar Rocks, Strathclyde (1972-73) and Little Skellig, Kerry (1973). Seabird eggs can be of value in monitoring changes in pollutant levels: in many species, residues in eggs lie within comparatively narrow limits at any one locality, this being particularly true for the more sedentary birds which feed on a more limited range of fish species than the Gannet. Nevertheless, it is possible to demonstrate, for example, that, in Gannet eggs collected in 1974 and analysed in a single series, residues of PCB, DDE, dieldrin and mercury averaged significantly higher at the Ailsa Craig colony than at the Bass Rock, and zinc levels averaged significantly lower (table 2). Taking all analyses for mercury, for which there appears to have been little annual variation within each colony, mean concentrations in eggs from the Scar Rocks (10.5 ppm dry weight) were about twice as high as in those from Ailsa Craig, three times higher than Little Skellig and four times higher than the Bass Rock (table 3). A similar pattern of mercury contamination holds true for the eggs of the more sedentary Guillemot (Parslow and Jefferies 1975). Eggshell thinning Since the introduction of DDT in the 1940s, one of the observable effects Gannets and toxic chemicals 370 Table 2. Means and standard errors of concentrations of PCB, DDE and dieldrin (ppm fat weight) and certain heavy metals ( p p m dry weight) in eggs of Gannets Sulci bassana from two Scottish colonies in 1974 Sample sizes: Bass Rock 10 eggs; Ailsa Craig 11 eggs Bass Rock PCB DDE Dieldrin Mercury Copper Zinc Cadmium 169.4 25-6 11.4 2.61 4.72 52.8 max. ± ± ± ± ± ± < Ailsa Craig 412.5 54.2 26.9 4-7 4-53 38.5 max. 29.4 3-7 1.2 0.21 0.13 3.6 0.3 ± ± ± ± ± ± < 64.4 6.6 4-i °-37 °-28 2.4 0.4 Table 3. Means and standard errors of concentrations of mercury (ppm dry weight) in eggs of Gannets Sula bassana from four colonies Colony Years No. of eggs Scar Rocks, Strathclyde Ailsa Craig, Strathclyde Bass Rock, Lothian Little Skellig, Kerry '972-73 I97I-74 1973-74 1973 18 29 18 7 Mean mercury concentration 10.47 4-54 2.62 3.21 ± 0.71 ± 0.36 ±0.17 ± 0.35 Fig. 1. The correlation between the decreasing index of eggshell thickness and the increasing DDE concentration in the lipid of eggs of British Gannets Sula bassana. Also shown is the calculated regression line for this correlation (y = 3.839 — 0.627X, where y = eggshell thickness index and x = log DDE concentration in the egg lipid in parts per million by weight) Gannets and toxic chemicals 37i of DDE contamination has been the phenomenon of eggshell thinning among populations of at least 40 different bird species belonging to 12 or more families (see Ratcliffe 1967, 1970; Cooke 1973). Shell thickness indices (shell weight in mg/length X breadth of egg in mm; Ratcliffe 1967) were calculated for the blown, dried shells of all Gannet eggs that were received intact. Extreme values varied considerably, one egg laid by an inexperienced individual on Ailsa Craig having a shell (index 2.00) 41% thinner than the thickest-shelled egg collected on the Bass Rock (index 3.40). Most indices, however, fell within a much narrower range (2.5-3.1). At least among experienced breeding pairs of Gannets, shell thickness is inversely correlated to a significant degree (r = —0.8074; 26 df; P < 0.001) with the DDE concentration in the egg contents (fig. 1): increasing the DDE concentration tenfold, from 15 to 150 ppm in the lipid, decreased the eggshell index by 20.2%. Four eggs collected on Ailsa Craig late in the season, from isolated n c ts of presumed inexperienced, late-laying, younger individuals, appeared to exhibit extremes of shell thickness, towards high as well as low indices, regardless of DDE content. Apart from the Shag (Ratcliffe 1970), the Gannet is the only British seabird in which eggshell thinning correlated with increased DDE residues is known to occur to any marked extent. Whether it has any effect on reproductive success is not known. Acknowledgements We are grateful to Miss C. Brown, P. Freestone, M. C. French and L. Sheppard for chemical analysis of the specimens; to Miss R. Cox, Mrs H. M. Hanson and Miss J . Ward for assistance in the laboratory; and to P. G. H. Evans, Dr J. B. Nelson, Miss S. Warrless and staff of the Nature Conservancy Council for help in the field. The study was carried out while we were at the Monks Wood Experimental Station of the Institute of Terrestrial Ecology. Summary Gannets Sula bassana found dead or dying on British coasts contained higher concentrations of PCB in the liver than did Guillemots Vria aalge which died in the 1969 Irish Sea 'wreck', and rather more on the west coast than on the east. Their mercury content was surpassed by only four out of 30 other marine and estuarine species analysed. Cadmium levels were relatively low. Residues of PCB, DDE, dieldrin and mercury were significantly higher at Ailsa Craig, Strathclyde, than at the Bass Rock, Lothian, and there was a significant inverse correlation between DDE content and the Ratcliffe (1967) index of eggshell thickness. References COOKE, A. S. 1973. Shell thinning in avian eggs by environmental pollutants. Environ. Pollut. 4: 85-152. HOLDGATE, M. W. (ed.) 1971. The seabird wreck of ig6g in the Irish Sea: analytical and other data. London (Natural Environment Research Council). JEFFERIES, D. J., and PARSLOW, J . L. F. 1972. Effects of one polychlorinated biphenyl on size and activity of the gull thyroid. Bull. Environ. Contant. and Toxicol. 8: 306-310. JOHNELS, A. G., WESTERMARK, T., BERG, W., PERSSON, P. I., and SJOSTRAND, B. 1967. Pike (Esox lucius L.) and some other aquatic organisms in Sweden as indicators of mercury contamination in the environment. Oikos 18: 323-333. PARSLOW, J . L. F., and JEFFERIES, D. J. 1973. Relationship between organochlorine residues in livers and whole bodies of Guillemots. Environ. Pollut. 5: 87-101. 372 Gamuts and toxic chemicals and '975- Geographical variation in pollutants in Guillemot eggs. Ann. Rep. Inst. Terr. Ecol. (1974): 28-31. , and HANSON, H. M. 1973. Gannet mortality incidents in 1972. Marine Pollut. Bull. 4: 41-44. PRESTT, I., JEFFERIES, D. J., and MOORE, N. W. 1970. Polychlorinated biphenyls in wild birds in Britain and their avian toxicity. Environ. Pollut. 1: 3-26. RATCLIFFE, D. A. 1967. Decrease in eggshell weight in certain birds of prey. Nature 215: 208-210. 1970. Changes attributable to pesticides in egg breakage frequency and eggshell thickness in some British birds. J. Appl. Ecol. 7: 67-115. STENERSEN, J., and KVALVAG, J . 1972. Residues of DDT and its degradation products in cod liver from two Norwegian fjords. Bull. Environ. Contam. and Toxicol. 8: 120-121. SUZUKI, T., MIJAMA, T., and TOYAMA, C. 1973. The chemical form and bodily distribution of mercury in marine fish. Bull. Environ. Contam. and Toxicol. 10: 347-355. WITHERBY, H . F., JOURDAIN, F. G. R., TICEHURST, N . F., and TUCKER, B. W. 1940. The Handbook of British Birds, vol. 4. London. J. L. F. Parslow, Royal Society for the Protection of Birds, The Lodge, Sandy, Bedfordshire SG19 2DL Dr D. J. Jefferies, Nature Conservancy Council, George House, Huntingdon, Cambridgeshire [Brit. Birds 70: 372-384 September 1977]
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