Environmental Pollution (Series A) 40 (1986) 17-35
Comparison Between Concentrations of Mercury and Other Contaminants in Eggs and Tissues of Cory's
Shearwater Co[onectris diomedeo Collected on Atlantic and Mediterranean Islands
A. Renzoni, S. Focardi, C. Fossi, C. Leonzio & J. Mayol*
Dipartimento di Biologia Ambientale, via delle Cerchia 3, 53100 Siena, Italy
A B S T R A C T
Trace elements (Hg, Se, Cd, Pb and Zn) and chlorinated hydrocarbons (hexachlorobenzene, pp'DDE and PCBs) were measured in eggs and tissues of a pelagic seabird (Calonectris diomedea) collected in one station of the eastern Atlantic and in three stations of the Mediterranean Sea. Mercury and chlorinated hydrocarbons were much higher in tissues and eggs of the Mediterranean specimens than in those from the Atlantic. Atlantic eggs had thicker shells than Mediterranean ones. In all the specimens selenium levels in the liver were strongly correlated with mercury; cadmium levels were high in the kidney and, to a lesser extent, in the liver. PCB isomers and congeners were studied in detail.
I N T R O D U C T I O N
Repeated observations during the 5-year-long F A O / U N E P project for the monitoring of the Mediterranean have shown that the residues of mercury in various marine organisms living in this basin are high and most of the time well above the so-called background levels (International Register of Potentially Toxic Chemicals, 1978).
In various areas of the Mediterranean, and particularly in the Tyrrhenian Sea, primary-consumer pelagic fish have higher mercury
* Present address: Instituto Nacional para la Conservacion de la Naturaleza, Majorca. 17
18 A. Renzoni, S. Focardi, C. Fossi, C. Leonzio, J. Mayol
residues than in the Atlantic just outside Gibraltar (Baldi et al., 1978). The same is true of a predatory fish, the blue-fin tuna (Renzoni et al., 1978). For this last species, Baldi & Renzoni (1980) and Buffoni et al. (1982) reported that in the western Mediterranean there are two distinct populations of tuna: a 'low-mercury population' and a 'high-mercury population'; the first being of Atlantic origin, entering the Mediterranean only for spawning and leaving shortly after, the second resident in the Mediterranean.
The above-mentioned results on pelagic fish prompted this study of Cory's shearwater Calonectris diomedea, a bird that spends a great deal of time over the open ocean and feeds upon pelagic organisms. The fact that the populations of the Mediterranean area are geographically distinct from those in the Atlantic promised to be useful in the evaluation of possible differences in levels of contamination between the two water bodies.
We analysed mercury and other environmental contaminants (Cd, Pb, polychlorinated biphenyls, hexachlorobenzene, pp'DDE) in eggs and tissues of adults in three Mediterranean populations of Cory's shearwater on three islands (Majorca, Linosa and Crete*), and a population from Selvagen (a small Atlantic island south-west of Gibraltar, about 320 km south of the Island of Madeira, Fig. 1).
Measurements of egg-shell thickness of specimens from each of the four colonies were made in order to establish the possible negative influence of some contaminants on reproductive success and physiology.
MATERIALS AND METHODS
Eggs and tissues were collected in May 1982 (Linosa), in April 1983 (Crete and Selvagen) and in May 1984 (Majorca); the material was freeze-dried and then broken up. The residual water content was evaluated in sub- samples (24h at l l0°C). Before freezing, sub-samples were dried to determine the water content and fresh weight/dry weight ratio.
Accuracy of methodologies was evaluated by the intercalibration exercises conducted by the International Laboratory of Marine Radioactivity of the IAEA (Monaco, Principality of Monaco).
* For the ease of the reader we will speak of Majorca and Crete; but eggs and birds were actually obtained on a small island (Dragonada) several km north-east of Crete, and another small island (Cabrera) several km south-east of Majorca.
Mercury in shearwater eggs and tissues 19
Fig. 1. Location of the sampling stations: 1, Selvagen Island; 2, Majorca Island; 3, Linosa Island; 4, Crete Island.
Trace elements
Freeze-dried material was treated with nitric acid in decomposition vessels of teflon (teflon bomb) under pressure at 120°C for 6-8h (Stoeppler & Backhaus, 1978).
The mineralized solution was analysed by Atomic Absorption Spectrophotometry using a Perkin-Elmer AAS (model 300 S).
Mercury was atomized by the cold vapour stream system; zinc by the air-acetylene flame; cadmium and lead by a graphite furnace (HGA 500); selenium by hydride generation followed by electrothermal atomization (Perkin-Elmer MHS- 1).
Interferences due to sensitivity were eliminated by the method of addition, before pretreatment. Interferences due to nonspecific absorb- ance were eliminated by a deuterium background compensator.
Chlorinated hydrocarbons
A 1-10 g aliquot of the freeze-dried homogeneous material was extracted for 12 h on a Soxhlet apparatus. The extract was subjected to sulphuric acid clean-up (Murphy, 1972), followed by Florisil chromatography. The purified sample was transferred to another glass column filled with silica- gel to separate DDT and analogues from PCB (Snyder & Reinert, 1971).
20 A. Renzoni, S. Focardi, C. Fossi, C. Leonzio, J. Mayol
08L
I
9M
T~L
ILL
IlIL
~ 3 J
__¢
e. ,
z~ G
0
~ . ~
E ~
~ ~
a ~
e4
Mercury in shearwater eggs and tissues 21
Measurements were made using a Perkin-Elmer Sigma 3 Gas Chromatograph, equipped with a Ni63 Electron Capture Detector and a Sigma 10 Data Station. The chromatographic columns used were 2-m- long glass columns (i.d. 3 mm) packed with 4 ~o SE-30 + 6 % SP-2401 on Supelcoport (100-120 mesh) and with 5 ~o OV- 101 on Chromosorb W H P (80-100 mesh). A 50 m fused silica capillary column covered with SE-54 was also used.
Calculations were based on standard reference solutions (Aroclor 1254, Aroclor 1260 and single isomers and congeners for PCB), after the losses had been evaluated.
A typical capillary chromatogram of the eggs of Cory's shearwater is shown in Fig. 2.
Measurements of shell thickness
The eggshell was washed and dried at 40 °C for 3 days, then measured with the shell membrane left intact. Measurements of thickness were taken randomly around the equator (4 measurements) and the two poles (4 measurements per pole) using a Borletti micrometer. Mean shell thickness was calculated for each egg.
RESULTS
All results are expressed as dry weight.
Trace elements (Figs 1 and 3; Tables 1 and 2).
Mercury The levels of this metal in the eggs collected in the Mediterranean were 2.5 to 3.5 times higher than those collected in the Atlantic station. The values in the three Mediterranean stations are quite homogeneous.
In the analysed tissues, mercury increases progressively from the fat to the uropygial gland, brain, muscle, kidney and liver. As in the case of eggs, in all tissues the mercury content was higher in the material collected in the Mediterranean stations than in that from the Atlantic one. In particular, the liver residues of birds from Stations 2, 3 and 4 are four to six times higher than those from Station 1. Mercury concentrations in the liver and kidney are highly correlated statistically (p < 0.001).
I0
4
12i
84)
100
[ ] EGG
[ ] L,vER
~ B 00E ~ B OC)E ~ B ~ E ~ B ~ E
Cd H
H L Ca H
•
e ~
m
Cd ~ L .
1_
CJ
Fig. 3. C on t am i nan t s in eggs and livers in the four stations.
T A B L E 1 Trace Elements in the Eggs (/~g g-1 dry weight)
S t a t i o n 1 S t a t i o n 2 S t a t i o n 3 S t a t i o n 4
Cadmium In the eggs cadmium levels were always below the detection limits of the instrument (0.03 #g g-1). In the kidney, cadmium levels reached their maximum, especially in Stations 1 (214/~g g- 1) and 4 (187 #g g- 1). In the liver cadmium levels are quite high (from 7 to 55 #g g-1). In the fat, uropygial gland, muscle and brain, concentrations vary from 0.21 to 3.93 pg g- i.
24 A. Renzoni, S. Focardi, C. Fossi, C. Leonzio, J. Mayol
L e a d
The eggs from all the stations presented concentrations of lead below the instrumental sensitivity (0.3#gg-1) . In organs and tissues, levels never exceeded 1.1/~g g- 1.
Z i n c
Zinc concentrations varied in eggs from a minimum of 37 #g g-1 in Station 2 to a maximum of 86#g g-1 in Station 1. Zinc increased progressively from the fat to the uropygial gland, muscle, brain, kidney and liver, and differences from station to station were negligible. Cadmium and zinc concentrations in the kidney were positively correlated (p < 0-01).
S e l e n i u m
In eggs selenium levels were quite homogeneous in the various stations. There were low levels in fat, muscle and brain, higher and scattered concentrations in the uropygial gland, kidney and liver; the maximum values were in Station 3. In the liver, selenium levels were positively correlated with the mercury concentrations (p < 0.01).
Chlorinated hydrocarbons (Figs 1 and 3; Tables 3 and 4)
H e xach lo r oben zene
Egg, tissue and organ values were below 0.1 #g g - l , except for the uropygial gland and fat of Station 2 (0.2 and 0.4/tg g-1, respectively).
TABLE3 Organochlorinesin Eggs(pgg-~dryweight) and EggshellThickness
Station 1 Station 2 Station 3 Station 4 n=20 n= 10 n= 11 n =2
£ SD 2 SD 2 SD
Lipids % dry weight 36.8 5.4 39"1 3.2 35"5 6"7 40.2 a 36"9" Hexachlorobenzene 0.045 0.015 0.036 0.016 0.072 0-016 0.035 a 0-048 a pp'DDE 1.49 0.68 18.77 12-46 3.75 2.08 4.79 a 9.99 a PCBs b 4.19 1.70 95.08 56.72 10.59 4-18 7.96" 20.81 ~ PCBs/DDE 2.87 0.62 5.55 2.20 3-00 0.72 1-66 a 2.08 ~ Thickness (pm) 385 18 330 24 308 16 324 a 318 ~
a Single value; b Calculated as Aroclor 1260.
Mercury in shearwater eggs and tissues
TABLE 4 Chlorinated Hydrocarbons in Tissues and Organs (#g g- ~ dry weight)
pp'DDE Atlantic eggs had the lowest concentrations. Within the Mediterranean the residues in Station 2 (18.7 #g g- 1) were much higher (5-6 times) than in Stations 3 and 4. Quite similar results were obtained for the tissues and organs" in Station 2 of the Mediterranean DDE values were particularly high (80.2 pg g-1 in the fat).
26 A. Renzoni, S. Focardi, C. Fossi, C. Leonzio, J. Mayol
,° 1 15
I0
:)
I U pce. Q~DOd P~lt lipid h~,i'* j
M
STATION 1
L K U B
500, 400. 300.
lO0
O, F
STATION 2
M L K U B
Fig. 4.
40
2o
STATION 3
F M L K U B
40
~o
o~
Sr~K~ 4
F M L K U B
PCBs and pp'DDE, expressed as pg g-~ on lipid basis, in tissues and organs: F, fat; M, muscle; L, liver; K, kidney; U, uropygial gland; B, brain.
The trend of distribution in tissues and organs shows the increase of pp 'DDE from the kidney to the brain, liver, muscle, uropygial gland and fat. If we normalize the concentrations on a lipid basis (Fig. 4) the trend does not change except for the uropygial gland and brain: the two last organs become the compartments with the lowest DDE residues.
PCBs In the eggs of the Mediterranean stations PCB values were from 2 to 25 times higher than in the Atlantic. In Station 2 there was an exceptional level of PCB residues (as high as 95 #gg-1) . Tissues and organs also reached remarkable levels in Station 2; the levels were about 20 times higher than those in Station 1. The distribution of PCBs in the organs is like that of DDE.
Mercury in shearwater eggs and tissues 27
TABLE 5 PCB Congeners and Isomers in Eggs; nd = Not Detected
IUPAC Station 1 Station 2 Station 3 Station 4 number % ~ °/o °/o
28 A. Renzoni, S. Focardi, C. Fossi, C. Leonzio, J. Mayol
P C B s / D D E ratio In eggs as well as in tissues and organs the ratio was highest in Station 2, followed by Stations 3, 1 and 4. In all the stations the lowest ratio occurred in the uropygial gland, whereas the highest was found in the brain, except at Station 2.
P C B isomers and congeners The composition of PCBs in eggs and tissues did not vary appreciably from one station to another. The major part of the total residues (from 50.5 to 63"3~o in the eggs) comprised four distinct components (2,2',3,4,4',5'; 2,2',4,4',5,5'; 2,2',3,3',4,4',5 and 2,2',3,4,4',5,5'), according to the IUPAC numbers 138, 153, 170 and 180 (International Oceanographic Commission, 1984). The other PCB congeners and isomers that were detected were mostly penta-, hexa-, hepta- and octachlorobiphenyls (Table 5).
Eggshell thickness (Table 3)
The Atlantic material had thicker eggshells than that of Mediterranean: the difference is statistically significant (p < 0.01).
the
DISCUSSION
The levels of mercury were consistently much higher in the Mediterranean material--whether eggs, organs or tissues--than in that from Atlantic. These findings confirm previous results from pelagic fish, especially blue- fin tuna, collected in the two basins (Baldi et al., 1978; Renzoni et al., 1978; Stoeppler et al., 1979; Buffoni et al., 1982). Within the Mediterranean no statistically significant differences were detected between mercury levels in the three stations.
As for cadmium, high levels were found in tissues and organs, and very low ones in eggs; these results are in general agreement with those for other pelagic bird species (Anderlini et al., 1972; Hutton, 1981). Rather than considering these high levels a consequence of pollution, they should be related to the natural content of cadmium in the organisms upon which the birds feed.
Levels of chlorinated hydrocarbons were also higher in the
Mercury in shearwater eggs and tissues 29
Mediterranean than in the Atlantic material (eggs and tissues or organs). These findings, together with those for trace elements, offer clear evidence of the different level of contamination in the two seas. This fact may be explained by the features of the Mediterranean basin: for mercury, the geochemical anomaly of cinnabar in several inland areas around the basin; for mercury and all other pollutants, the slow turnover of the water, shallowness, small number "of rivers (flowing through highly industrialised areas), agricultural development and human settlements, which lead to a general diffusion and persistence of pollutants.
Within the Mediterranean the material from Linosa and Crete seems to be quite similar; for Crete our data on pp 'DDE are consistent with those obtained by Bourne & Bogan (1976) in eggs of the same species. Much higher levels of pp 'DDE and, particularly, of PCB were found on the island of Majorca; our data are quite similar to those reported for Audouin's gull eggs by Bijleveld et al. (1979) from the same area. (Our previously unpublished data show that levels of chlorinated hy- drocarbons in 6 eggs of herring gulls breeding in the colonies of Majorca are quite heterogeneous, with a range of 15-80/~g g- 1 for pp 'DDE and of 35-210 #g g-1 for PCBs.) In the colony of Majorca, DDE is in the same range as in eggs of the common cormorant (Fossi et al., 1984) from the Danube Delta, whereas PCB attained one of the highest levels described for the Mediterranean in eggs and tissues of all the species so far examined (Viviani et al., 1974; Mendola et al., 1977; Vannucchi et al., 1978; Bourne & Bogan, 1980; Focardi et al., 1980; Renzoni et al., 1982). For the moment there is insufficient information (only Chacartegui (1981) furnishes some data on the levels of PCBs--1.1 ~g g-~ fresh weight--in M u l l u s barba tus caught around the islands) to be sure whether high levels of chlorinated hydrocarbons are to be found throughout the marine fauna of the Majorca area.
Industrial activities in the Balearic Archipelago are very limited, so that it is difficult to understand how such a high level of pollution could occur around these islands. The fact that, in herring gull's eggs of the Rhone Delta, PCB levels as high as 52 #g g-~ wet weight (Mendola et al., 1977) have been found suggests that the Rhone Delta and the Marseille area could be an important source of pollutants in the North West Mediterranean and that coastal pollutants from these areas could reach the Balearics by the counterclockwise stream of the sea-water in the Western Mediterranean. Another possible source of contamination of the Archipelago is the Ebro river, where Alberto & Nadal (1981) and Ruiz et
30 A. Renzoni, S. Focardi, C. Fossi, C. Leonzio, J. Mayol
al. (1983) reported high levels of chlorinated hydrocarbons in the eggs of eleven species of estuarine birds.
The contamination of sea-birds may be linked to the dietary importance of fish in these species: fish-eating sea-birds contain higher levels of pollutants than most other avian species (Fimreite, 1979; Leonzio et al., in press). Such high pollutant levels related to diet may induce the development of a protective mechanism against the toxicity of the contaminants. One of the best studied protection mechanisms is the antagonistic role of selenium against mercury toxicity (Ganther et al., 1972; Frost, 1975). In our material the levels of mercury in liver are significantly correlated with selenium levels, confirming the observations of Koeman et al. (1973) and Cappon & Smith (1981) in the liver of mammals, of Hutton (1981) in the liver and kidney of birds, of Focardi et al. (1980) and Renzoni et al. (1982) in the eggs of birds. A detoxification mechanism based on demethylation of methylmercury and complexation of mercury and selenium in a non-toxic compound in the liver cells is the explanation advocated by Thibaud (in press).
Our findings of high cadmium levels in tissues of Cory's shearwater, particularly in the kidney, are in fair agreement with those reported by Anderlini et al. (1972) and by Cottiglia et al. (1982) for other sea-birds. Most probably, the cadmium is of natural origin and these pelagic birds may have evolved a protective mechanism (involving zinc, Friberg et al., 1976) whereby cadmium is bound to a specific protein and is subsequently retained and excreted by the kidney. Hutton (1981) has demonstrated that most of the cadmium in the kidney cytosol of a pelagic sea-bird is bound to a protein with properties similar to metallothionein. Our data confirm that very little cadmium is transferred from the female to the egg, thus indicating the existence of an efficient binding mechanism.
Chlorinated hydrocarbons have been found in great concentrations in the adipose tissues of these pelagic birds and their lipo-affinity is quite well known. However, the specific affinity for the lipid component of each tissue is quite different. On a lipid basis the maximum uptake of chlorinated hydrocarbons occurs in the adipose tissue, then in the muscle, liver, kidney, uropygial gland and brain. These lipo-affinity discrepancies are probably due to the physical-chemical properties and to the selective ability to link the pollutant molecules (Brown & Lawton, 1984).
The presence of high levels of chlorinated hydrocarbons in the animal body is thought to have several negative metabolic effects; one of them is the reduction of eggshell thickness. Observations in the field, confirmed by laboratory experiments, indicate that eggshell thinning and decreased
Mercury in shearwater eggs and tissues 31
reproductive success observed in certain species of sea-birds have been largely caused by residues of pp 'DDE or other compounds or metabolites of the DDT group and dieldrin and PCB (Peakall & Peakall, 1973; Klaas et al., 1978; Ohlendorf et al., 1978; Fox & Donald, 1980; Blus, 1982).
In our Mediterranean material, the residues of potential thinning inducers (PCB and pp'DDE) are higher than in the Atlantic material and a slight thinning of the Mediterranean eggshell seems to occur. However, even though all the eggs of the Mediterranean colonies are thinner than the Atlantic ones, within the material of the first group the most polluted eggs are not the ones with the thinnest shells. More data are therefore necessary to confirm this finding and to evaluate the reduction on a statistical basis.
Great emphasis has also been recently placed on the modifications undergone by members of the PCB group once in the environment, and especially their metabolism within the animal body. Studies of the last 10 years (De Freitas & Norstrom, 1974; Burse et al., 1976; Baker et al., 1977; Matthews & Tuey, 1980) have demonstrated that many of the lower chlorinated di-, tri- and tetrachloro isomers and congeners, and selected higher chlorinated PCB were preferentially eliminated from body tissues and organs. Data of other authors confirm such findings in mammals and in birds (Safe, 1980), and are the basis for a more general subdivision: persistent and nonpersistent PC B congeners (Bush et aL, 1974; Kuroki & Masuda, 1977; Wolfe et al., 1982).
Most recently Bush et al. (1984) have indicated that 'when chlorine substitution patterns 245, 234, 24, and 34 occur in each ring of the biphenyl moiety, the molecules are persistent; their absence on one ring, however, causes the whole molecule to be rapidly eliminated'. We may deduce that in our material the PCB congeners and isomers that follow the above pattern of persistence represent the majority of the total PCB residue.
ACKNOWLEDGMENTS
The research was supported by the FAO-UNEP (MED-POL Phase II) and by the ECC (ENV 512,I). We are grateful to Bruno Massa (Italy), Alec Zino (Portugal), George Handrinos (Greece) and the 'Unidad de Vida Silvestre' del Servicio de Icona en Baleares (Spain) for their help with the collection of the material. Our best thanks to Ann Henderson, who has pulled our English into intelligible and concise shape.
32 A. Renzoni, S. Focardi, C. Fossi, C. Leonzio, J. Mayol
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