Gannets and toxic chemicals

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.
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[Brit. Birds 70: 372-384 September 1977]