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Environmental contamination and marine mammals in coastal waters from Argentina: an overview
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The Science of the Total Environment 154 (1994) 141-151
Environmental contamination and marine mammals in coastal waters from Argentina: an overview Jorge E. M a r c o v e c c h i o * a, M a r c e l a S. G e r p e a, R i c a r d o O. Bastida b, Diego H. R o d r l g u e z b, S.G. Mor6n b alnstituto Nacional de In testigaci6n y Desarrollo Pesquero (INIDEP), Playa Grande s /n, Casilla de Correo 175, 7600 Mar del Plata, Argentina bDepartimento de Ciencias Marinas, Unioersidad Nacional de Mar del Plata, Fundaci6n Mundo Marino, Mar del Plata, Argentina
Abstract Environmental contamination become an increasing global problem. Different scientific strategies have been developed in order to assess the impact of pollutants on marine ecosystems. The distribution of toxic contaminants in tissues of different marine mammal species - - both cetaceans and pinnipeds - - has been studied in many ecosystems, as well as several related ecological processes, like pollutant accumulation or transfer through the food web. A research program directed towards evaluating the occurrence of pollutants in marine mammals from the coastal waters of Argentina (southwestern Atlantic Ocean) has been developed since 1985, and includes the study of heavy metal contents in stranded or incidentally caught animals. The marine mammal species studied during this period were: the seals Otaria flaoescens and Arctocephalus australis, and small cetaceans Tursiops gephyreus, Pontoporia blain~illei, Kogia bre~ceps and Ziphius cavirostris. In most of the cases, high contents of heavy metals (total mercury, cadmium, zinc, and copper) have been recorded. Moreover, liver showed the maximum capability for accumulation of heavy metals in all studied species. The biological and ecological characteristics of each species of the above-mentioned marine mammals (feeding habits, age, migratory pathways, or sex) contributed to the understanding of the metal sources. Considering the results as obtained during the study period it can be assumed that: (1) The global distribution of toxic contaminants also affects the southwestern Atlantic Ocean ecosystems, and (2) Marine mammals could be appropriate bioindicator species in order to assess this kind of environmental problem.
Keywords: Marine mammals; Heavy metals pollution; Bioindicator species; Bioaccumulation and biomagnification processes; Target tissues
1. Introduction Environmental contamination is a global problem which affects most ecosystems through both direct (by industrial wastes, oil spills, etc.) and indirect (atmospheric or oceanic distribution and
* Corresponding author.
circulation, etc) mechanisms. During the last few years, the number of studies dealing with the occurrence of pollutants in marine mammals has significantly increased, mainly due to: (1) The fact that an increase in pollutant concentrations has been recognized in many areas of the world (Salomons and Forstner, 1984; G.E.S.A.M.P., 1990); (2) Several populations of marine mammals have recently suffered major mortalities
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J.E. Marcovecchio et al. / Sci. Total Environ. 154 (1994)141-151
which have still not been explained (Lavigne and Schmitz, 1990; Harwood and Grenfell, 1990). A large number of papers with different approaches have been written on heavy metal pollutants in marine mammals. There are several papers correlating heavy metals concentration and tissue distribution in different species of pinnipeds and cetaceans (Anas (1974) on Callorhinus ursinus and Phoca ~tulina richardii; Denton et al. (1980) on Dugong dugong and Wagemann (1989) on Phoca hispida). Also, several papers on heavy metals accumulation in marine mammals have been published. Among them, those from Hamanaka et al. (1982) on Eumetopias jubata, Bacher (1985) on Arctocephalus pusillus and Honda et al. (1987) on Balaenoptera acutorostrata. All this information is extremely useful in assessing and characterising different environments from the pollution viewpoint. A research program has been developed in Argentina since 1985, directed at evaluating the occurrence and tissue distribution of heavy metals in marine mammal species from the southwestern Atlantic Ocean, as well as the corresponding accumulation processes and transfer through their trophic webs It has been carried out by researchers from the National Council for Scientific and Technological Research (CONICET), the National Institute for Fisheries Research and Development (INIDEP), Mar del Plata National University (UNMdP), and Fundaci6n Mundo Marino. This paper presents an overview of the results obtained from this program in the framework of the oceanographic conditions of the areas studied, and also considering the biological, ecological and behavioural characteristics of the species studied.
2. Oceanographical description of the Argentine Sea The general superficial circulation in the Southwestern Atlantic Ocean is characterized by the Brazil current - - which flows down to the pole along the continental margin of South America - - and the Malvinas-Falkland current, which
flows to the north parallel to the continental slope of the Argentine shelf (Garzoli and Bianchi, 1987). Both currents are restricted to depths lower than 1500 m. (Reid et al., 1977). Brazil (warm and high salinity) and Malvinas-Falkland (cold and low salinity) currents meet one another in the Argentine basin, at around 38°S. This creates a strong frontal zone (Gordon, 1981; Legeckis and Gordon, 1982), with a horizontal temperature gradient up to 1°C/250 m. This frontal area marks the division between subtropical and subantarctic waters. Three typical water masses occur within the Argentine continental shelf: Malvinas waters, shelf waters, and coastal waters (Lusquifios and Vald6z, 1971; Lusquifios and Schrott, 1983). Martos and Piccolo (1988), who have studied the physical characteristics between 38°S and 42°S, divided the continental shelf in two regions: coastal (depth < 40 m), where the mixture generated by wind and tides produces vertically homogeneous waters during the whole year, and the external shelf (40 m < depth < 90 m) with a warmer superficial layer (thickness about 30 m) from spring to autumn, and strong stratification at the bottom. The horizontal salinity distribution presents minimum values east of the Magallanes Strait (52°30'S, 68°W), increasing to the north up to 33.5% near 38°S. (Piola and Scasso, 1988). The Patagonian shelf is characterized by a strong mixture produced by tides (Glorioso, 1987) and these conditions produce many shelf frontal systems (Bowman, 1977; Lutz and Carreto, 1991), which are extremely important not only as productive systems (Carreto et al., 1985) but as spawning and nursery areas for many fish and shellfish species (i.e. hake, shrimps, anchovies, etc.) (IOC, 1989). Finally, it is important to note that the mean circulation in most of the Argentinean continental shelf is in the north-northeastern direction, with current speeds between 2 and 20 cm/sec (Forbes and Garrafo, 1988). A knowledge of these oceanographical conditions as a whole is extremely important in understanding the possible global distribution and circulation of pollutants in the Argentine Sea, and
J.E. Marcooecchio et al. / Sci. Total Environ. 154 (1994) 141-151
their potential effects on marine organisms living in the study areas. 3. Potential sources of pollutants in the coastal ecosystems of Argentina
The occurrence of potential sources of pollutants in the littoral ecosystems of the Argentine Sea is strongly related to the corresponding location of the most important cities as well as the largest industrial centers (Fig. 1). Area 1. The first potentially critical area is that associated with La Plata River. Buenos Aires, the capital city of Argentina, is located upstream and consequently the largest concentration of population in the country. A great industrial nucleus exists around this city, comprising amongst others metallurgical, petrochemical, textile, and pharmacological industries. Moreover, the wastes from these industrial centers are disposed - - directly or indirectly - - into the La Plata River, as are the domestic wastewaters from the city. La Plata city is located nearly 50 km southeast of Buenos Aires, and has the largest petrochemical refinery in Argentina. Both Buenos Aires and La Plata have large harbours with intense yearround activities. Area 2. Along the coastal area of Buenos Aires Province, there are several cities a n d / o r urban centers: San Clemente del Tuyfi, Pinamar, Villa Gessell, Mar del Plata, and Necochea, with various industries, populations, harbours, etc. Area 3. The Bahia Blanca estuary is situated in the southern Buenos Aires Province and is one of the most impacted coastal environments of Argentina. This semi-enclosed system includes an important industrial center (comprising smelters, petrochemical refineries and reservoirs, pesticide factories and large harbours), as well as several cities which dump their urban wastes into the estuary waters. Area 4. In the coastal system of San Matfas Gulf there are several mining centers, and only a few cities, which suggests this is not a polluted environment. Area 5. The area of Peninsula Vald6s in Chubut Province is a very important region, because of its biological diversity and ecological characteristics.
143
Several cities have been established in this area (e.g. Puerto Madryn), and several industries are developed including the most important aluminium factory in the country. Area 6. The largest development for exploitation, storage and transport of petroleum in Argentina is established in the San Jorge Gulf. Moreover, there are important cities in this area, like Comodoro Rivadavia. Studies related to marine pollution in Argentina are relatively recent, and have been developed in different areas mainly attending to particular environmental problems. Up to this point, there have been no national research programs which integrate current knowledge on this topic. 4. Materials and methods
A research program directed at assessing the occurrence, distribution, and accumulation of several heavy metals (total mercury, cadmium, zinc, copper) in marine mammals from the Southwestern Atlantic Ocean has been ongoing since 1985. During this time, many specimens of different species have been analyzed in order to determine heavy metal levels in tissue. The analyzed animals were stranded on the beaches of the study area, or incidentally caught during fishing operations. Only in the case of the South American fur seal, Arctocephalus australis, were several of the studied specimens obtained through commercial hunting, which has occurred annually in Uruguay for many years. The studied species are as follows: bottlenose dolphin (Tursiops gephyreus), La Plata dolphin or franciscana (Pontoporia blainvillei), pigmy sperm whale (Kogia breviceps), Cuvier's beaked whale (Ziphius cavirostris), South American fur seal (Arctocephalus australis) and the South American sea lion ( Otaria flavescens). In all cases, and after the corresponding dissection, samples of the most important tissue (muscle, liver, kidney and fat among others) were removed and stored in freezer at -20°C until laboratory analysis. For the analysis of total mercury, the samples were mineralized with a wet acid digestion (Uthe
144
J.E. Marcovecchio et aL / Sci. Total Environ. 154 (1994) 141-151
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Location o f the potential sources o f po]]utants in the coastal ecosystems o f Argentina.
57
J.E. Marcovecchio et al. /Sci. Total Environ. 154 (1994) 141-151
et al., 1970; Armstrong and Uthe, 1971), and measuring Hg concentrations by flameless atomic absorption spectrophotometry (AAS). For the determination of cadmium, zinc and copper, the method described by Marcovecchio et al. (1988) was followed, using AAS with an air-acetylene flame and deuterium background correction. A Shimadzu AA-640-13 was utilized for the corresponding analysis. Analytical reagents were used for the blanks and calibration curves, and the analytical quality control was carried out using reference materials provided by the N.I.E.S. (National Institute for Environmental Studies, Tsukuba, Japan), which certified the accuracy and precision of the developed methodology. Comparisons of metal concentrations were performed by one-way analysis of variance (ANOVA). 5. Results and discussion
Six species of marine mammals from the Southwestern Atlantic Ocean have been studied in order to determine heavy metal levels in their tissue. The results obtained from these analyses were very variable and strongly dependent on the corresponding species (Tables 1-4). The occurrence of heavy metals, both essential and non-essential, in the tissue of marine mammals is closely related to their biological characteristics and ecological habits.
145
5.1. Total mercury The distribution of total mercury in tissue showed a clear trend in the studied marine mammal species (Table 1). The liver was the most important organ for the accumulation of mercury, and this fact was verified in all the analyzed species. The mean values determined in liver of the studied marine mammals varied between 0.10 ppm (Ziphius cavirostris) and 86.0 + 7.3 ppm (Tursiops gephyreus) (Marcovecchio et al., 1990). Kidney also showed a significant ability to accumulate mercury, and the values obtained in the corresponding analysis varied between 0.17 ppm (Z. cavirostris) and 13.4 + 2.5 ppm (T. gephyreus), while the concentrations in muscle varied between 0.23 ppm and 5.5 + 0.8 ppm in the same two species. The fact that the minimum concentrations were recorded for Ziphius cavirostris and the maximum for Tursiops gephyreus was related with the corresponding ages of the studied animals. Thus, while the analyzed specimen of Cuvier's beaked whale was a pup (and consequently it would not have been strongly exposed to pollutants - - Marcovecchio et al., 1992a), those of bottlenose dolphin were up 10 years old with a significantly higher time of exposure to pollutants (Marcovecchio et al., 1990). In addition, a strong relationship between mercury concentration and the age of the analyzed organisms was reported by several
Table 1 Total mercury distribution in tissues of the studied marine mammal species from the Argentine Sea Species
N
Analyzed tissue Muscle
Liver
Kidney
Blubber
Reference Marcovecchio et al. (1990) Marcovecchio et al. (1990) Marcovecchio et al. (1990) Marcovecchio et al. (1992a) Pefia et al. (1988) Gerpe et al. (1990)
Tursiops gephyreus
2
5.5 (0.8)
86.0 (7.3)
13.4 (2.5)
ND
Pontoporia blainvillei
7
3.0 (1.2)
3.8 (1.6)
1.9 (0.7)
ND
Kogia breviceps
1
4.2
Ziphius ca virostris
1
0.23
Otariaflavescens
7
1.4 (0.6)
Arctocephalus australis
8
0.8 (0.3)
11.7 0.10
10.5
ND
0.17
ND
46.5 (13.3)
2.1 (0.8)
ND
33.7 (11.7)
0.9 (0.2)
ND
Mean value, in /~g/g wet wt.; S.D. in parenthesis; N, number of specimens analyzed; ND, non-detectable value.
146
J.E. Marcovecchio et al. / Sci. Total Environ. 154 (1994) 1 4 1 - 1 5 1
authors working with different species (Bacher (1985) for Arctocephaluspusillus Yamamoto et al. (1987) for Leptonychotes wedeUi, Honda et al. (1987) for Balaenoptera acutorostrata, Pefia et al (1988) for Otaria flavescens, and Gerpe et al. (1990) for Arctocephalus australis). On the other hand, the mercury concentrations determined in the studied marine mammal species were significantly higher than those corresponding to the organisms they feed on. In this respect, statistical analysis has showed significant differences (P < 0.01) between mercury contents in the marine mammal species (Table 1) and those of their food (Table 5). These results have been interpreted as supporting the occurrence of a mercury biomagnification process through the corresponding food web of each marine mammal species. The occurrence of this ecological process has been reported by several authors, like Drescher et al. (1977) for Phoca vitulina from the North Sea, Wagemann et al. (1988) for Phoca groenlandica, and Muir et al. (1988) for Lagenorhynchus albirostris and Globicephala melaena from Newfoundland (Canada). The trend observed in the distribution of total mercury in the tissue of the studied marine mammal species from the Southwestern Atlantic Ocean (Hg liver > Hg kidney > Hg muscle) clearly agreed with the previous reports of other authors, like Gaskin et al. (1974) for Stenella
longirostris from Lesser Antillas, and Harms et al. (1978) for Phocoena phocoena from the Baltic Sea.
5.2. Zinc and copper The results of the analysis of zinc and copper in the tissue of the studied marine mammal species showed a clear trend, which fully correlates with that reported for total mercury in previous paragraphs. Thus, the liver has the highest concentrations of both metals in all of the analyzed animals, with ranges between 56.5 + 11.0 ppm Zn (Arctocephalus australis) and 196.2 + 34.1 ppm Zn (Tursiops gephyreus) (Table 2), and between 10.3 ppm Cu (Kogia breviceps) and 77.7 + 3.8 ppm Cu (Tursiops gephyreus) (Table 4). Moreover, kidney of the studied specimens has levels varying between 44.2 + 8.2 ppm Zn (Arctocephalus australis) and 169.7 ppm Zn (/~ breviceps) (Table 2), and between 3.9 + 0.9 ppm Cu (A. australis) and 29.5 + 3.9 ppm Cu (T. gephyreus) (Table 4). Finally, muscle showed values ranging between 28.2 + 15.4 ppm Zn (A. australis) and 93.3 + 13.1 ppm Zn (T. gephyreus) (Table 2), and between 1.7 + 0.1 ppm Cu and 6.3 + 1.1 ppm Cu in the same species, respectively (Table 4). In the case of zinc and copper, a good relationship between the concentration of the metal and age (or age classes) of the studied animals has been recorded, which would demonstrate that
Table 2 Zinc distribution in tissue of the studied marine mammal species from the Argentine Sea Species
N
Analyzed tissue Muscle
Liver
Kidney
Blubber
Reference
93.6 (5.9)
4.7 (0.8)
Marcovecchio et al. (1990) Marcovecchio et al. (1990) Marcovecchio et al. (1990) Marcovecchio et al. (1992a) Pefia et al. (1988) Gerpe et al. (1990)
Tursiops gephyreus
2
93.3 (13.1)
196.2 (34.1)
Pontoporia blainvillei
7
49.3 (4.8)
83.4 (40.0)
Kogia breviceps
1
57.5
163.2
169.7
Ziphius cavirostris
1
--
--
--
Otaria fla oescens
7
--
--
--
Arctocephalus australis
8
28.2 (15.4)
56.5 (11.0)
79.4 (21.4)
44.2 (8.2)
Mean value, in /~g/g wet wt.; S.D. in parenthesis; N, number of specimens analyzed.
6.6 (0.6) 0.2
J.E. Marcovecchioet al. /Sci. TotalEnviron. 154 (1994)141-151 bioaccumulation of both metals occurs. These conclusions agree with several reports from other authors, e.g. those by H a m a n a k a at al. (1982) for Eumetopiasjubata, or by H o n d a (1985) and H o n d a et al. (1986) for Stenella coeruleoalba. Unlike total mercury, there was no clear trend on the biomagnification of zinc and copper through the corresponding food web. Thus, when the concentrations of both metals in the marine m a m m a l species (Tables 2,4) were compared with those of their prey (Table 5) it was not possible to establish a clear trend or relationship. It seems that m o r e samples must be reviewed in order to clarify this point. Up until now, the international literature has not reported enough documentation to support the occurrence of the biomagnification process of metals, except for mercury (Waldichuk, 1985) and cadmium (Wagemann, 1989). The trends observed for the distribution of Zn and Cu in the tissues of the study marine m a m mal species (Zn liver > Z n kidney > Zn muscle; Cu liver > Cu kidney >> Cu muscle) fully coincide with those reported by several authors for other marine m a m m a l species, e.g. Falconer et al. (1983) for the harbour porpoise Phocoena phocoena from the Baltic Sea, and Fujise et al. (1988) for the Dali's porpoise Phocoenoides dalli from the Northwestern Pacific.
147
5.3. Cadmium The results as obtained from the analysis of cadmium in the tissue of the studied marine m a m m a l species allow us to observe a particular trend for cadmium distribution. Kidney was the most important organ for the accumulation of cadmium in these species, with values varying between 5.6 + 2.4 p p m Cd (Otariaflavescens) and 412.6 p p m Cd (Kogia breviceps) (Table 3). Liver followed kidney in the ability to accumulate cadmium, and the hepatic levels of this metal ranged between non-detectable values (Ziphius cavirostris) and 34.5 + 17.1 p p m Cd (Arctocephalus australis) (Table 3). Finally, the levels of cadmium in muscle of the studied species were extremely low, and in fact most of the concentrations were below the detection limit of the method. For example, the highest cadmium concentration as determined in muscle was recorded in Arctocephalus australis: 0.4 + 0.1 p p m Cd (Table 3). Cadmium concentrations in tissues of the analyzed species seemed to have a strong relationship with age (or age classes). The results reported in the papers of G e r p e (1990), G e r p e et al. (1990), and Marcovecchio et al. (1991), all for Arctocephalus australis, support this point. Several reports from other authors also agreed with this, i.e. Heppleston & French (1973) for Phoca vitulina,
Table 3 Cadmium distribution in tissues of the studied marine mammal species from the Argentine Sea Species
N
Analyzedtissue Muscle
Liver
Kidney
Blubber
Reference Marcovecchio et al. (1990) Marcovecchio et al. (1990) Marcovecchio et al. (1990) Marcovecchio et al. (1992a) Pefia et al. (1988) Gerpe et al. (1990)
Tursiopsgephyreus
2
ND
0.8 (0.2)
28.4 (4.3)
ND
Pontoporiablainvillei
7
0.1 (0.1)
3.3 (1.4)
9.9 (3.9)
ND
Kogia breviceps
1
0.2
7.6
Ziphius cavirostris
1
ND
ND
Otariaflauescens
7
ND
Arctocephalusaustralis
8
0.4 (0.1)
412.6
ND
ND
ND
1.1 (0.7)
5.6 (2.4)
ND
34.5 (17.1)
48.15 (24.1)
--
Mean value, in tzg/g wet wt.; S.D. in parenthesis; N, number of specimens analyzed; ND, non-detectable value.
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J.E. Marcovecchio et a t / S c i . Total Environ. 154 (1994)141-151
Table 4 Copper distribution in tissues of the studied marine mammal species from the Argentine Sea Species
N
Analyzed tissue Muscle
Liver
Kidney
Blubber
Reference Marcovecchio et al. (1990) Marcovecchio et al. (1990) Marcovecchio et al. (1990) Marcovecchio et al. (1992a) Pefia et al. (1988) Gerpe et al. (1990)
Tursiops gephyreus
2
6.3 (1.1)
77.7 (3.8)
29.5 (3.9)
4.0 (0.6)
Pontoporia blainvillei
7
2.5 (1.5)
16.0 (3.3)
14.0 (4.9)
2.8 (0.3)
Kogia breviceps
1
2.0
10.3
Ziphius cavirostris
1
.
.
.
.
Otaria fla vescens
7
.
.
.
.
Arctocephalus australis
8
1.7 (0.1)
12.2 (2.0)
7.4
ND
3.9 (0.9)
--
Mean value, in /zg/g wet wt.; S.D. in parenthesis; N, number of specimens analyzed; ND, non-detectable value.
Hamanaka et al. (1982) for Eumetopias jubata, and Honda (1985) for Stenella coeruleoalba. As in the case of total mercury, there was enough evidence to support the occurrence of cadmium biomagnification through the corresponding food webs of the studied marine mammal species. Furthermore, the importance of diet as a source of cadmium for the marine mammals must be emphasized, as can be appreciated in Table 5. The trend observed for the distribution of cadmium in the tissues of the studied marine mammal species (Cd kidney >> Cd liver >> Cd muscle) coincided with previous reports from other authors for different species, e.g. Harms et al. (1978) for Phocoena phocoena, or Honda et al. (1983) for Stenella coeruleoalba. 6. Concluding comment
Considering the results presented here, it is necessary to put forward several central ideas which could contribute to a better understanding of this topic. First of all, it is important to emphasise that all of the analyzed marine mammal species have heavy metals in their tissue, not only essentials (as zinc or copper) but also non-essentials (as cadmium or mercury). This point, which is supported by various papers previously published (Marcovecchio et al., 1990, 1991, 1992a; Gerpe et al., 1990) is very important, because it
shows that the Southwestern Atlantic Ocean is not excluded from the global pollution which affects our planet. In this respect, several authors have emphazised the importance of atmospheric (Nurnberg et al., 1983; Jickells et al., 1984; Valenta and Nguyen, 1986), and oceanic transport and circulation (Gardner, 1975; Mart and Nurnberg, 1984). Furthermore, the importance of the relationship between the pollutant content of marine mammal tissue and the characteristics of the species, both biological (age, sex, size) and ecological (feeding habits, migratory pathways) has been strongly underlined. The results showed significant correlations between mercury content and the age of several marine mammal species (Marcovecchio et al., 1990), and gave good explanations for the differences observed in the levels of heavy metals between sexes in the South American fur seal, Arctocephalus australis (Gerpe et al., 1990). The international literature strongly supports these concepts (Hamanaka et al., 1982; Honda, 1985; Muir et al., 1988; Wagemann et al., 1988). The feeding habits as well as the ecological niche were the most important factors in heavy metal accumulation for the studied marine mammal species. This point was clearly confirmed by several of the results obtained. Thus, the highest values of mercury have been recorded in the mammal species with typically icthyophagus
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J.E. Marcovecchio et al. / Sci. Total Entiron. 154 (1994) 141-151
Table 5 Heavy metal concentrations in several food items from the diet of the studied marine mammal species Species
Corvina (fish)
Analyzed metals (/z/g) Hg
Cd
Zn
0.13
3.03
44.30
0.16
3.69
11.75
0.09
0.61
3.97
0.48
0.15
25.08
0.11
0.05
9.28
0.17
0.03
9.16
0.06
0.10
12.60
Micropogonias fumieri a
Pescadilla (fish) Cynoscion striatus a
Anchoita (fish) Engraulis anchoita b
Pez angel (fish) Squatina argentina a
Camar6n (shrimp) Artemesia longinaris a
Langostino (shrimp) Pleoticus muelleri a
Calamar (squid) lllex argentinus c
aAfter Marcovecchio et al. (1988, 1989). bArter A.O. Barral (INIDEP), pers. commun. cArter Marcovecchio et al. (1992b).
trophic habits, like Tursiops gephyreus (it must be emphasised that fish are known to be the single largest source of mercury in the aquatic environment - - Chvojka and Williams, 1980). On the other hand, highest cadmium concentrations have been determined-in the oceanic species Kogia breviceps, which is a squid-eater (squids have been noted as large accumulators of cadmium in the marine environment (Martin and Flegal, 1975). Coincidentally, marine mammal species with different percentages-of fish and squid in their diets
Acknowledgements
(Pontoporia blainvillei, Otaria flatescens, Arctocephalus australis) were shown to have mercury
References
and cadmium concentrations lower than
T.
gephyreus and K breviceps, respectively. Finally, it is interesting to consider the ability of marine mammal species to be used as bioindicators of heavy metal pollution. From the results as reviewed in the present paper, it can be seen that all of the analyzed species have heavy metals present in their tissues. Information on oceanographical conditions of the coastal waters of the Argentine Sea (which contribute to the circulation and dispersion of pollutants) is available, and the potential sources of pollutants to coastal ecosystems are known. Thus, the use of these animals as indicators of the status of their envi-
ronments seems to be adequate, but it would be laudable to complete this viewpoint with others, like concentrations of pollutants in abiotic compartments or diet of the selected indicators.
This paper was partially financed by The National Council for Scientific and Technological Research (CONICET) from Argentina, and by Fundaci6n Mundo Marino.
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Chvojka, R. and R.J. Williams, 1980. Mercury levels in six species of Australian commercial fish. Aust. J. Mar. Freshwater Res., 31: 469-473. Denton, G.R.W., H. Harsh, G.E. Heinsohn and C. BurdonJones, 1980. The unusual metal status of the dugong, Dugong dugong. Mar. Biol., 57: 201-219. Drescher, H.E., U. Harms and E. Huschenbeth, 1977. Organochlorines and heavy metals in the harbour seal Phoca t~tulina from the German North Sea Coast. Mar. Biol., 41 (1977) 99-106. Falconer, C.R., I.M. Davies and G. Topping, 1983. Trace metals in the common porpoise, Phocoena phocoena. Mar. Environ. Res., 8: 119-127. Forbes, D.A. and J.A. Garrafo, 1988. A note on the mean seasonal transport on the Argentinian Shelf. J. Geophys. Res., 93: 2311-2319. Fujise, Y., K. Honda, R. Tatsukawa and S. Mishima, 1988. Tissue distribution of heavy metals in Dali's porpoise in north-western Pacific. Mar. Pollut. Bull., 19: 226-230. Gardner, D., 1975. Observations on the distribution of dissolved mercury in the ocean. Mar. Pollut. Bull., 6: 43-46. Garzoli, S. and A. Bianchi, 1987. Time-space variability of the local dynamics of the Malvinas-Brasil Confluence as revealed by inverted echo sounders. J. Geophys. Res., 92: 1914-1922. Gaskin, D.E., G.J.D. Smith, P.W. Arnold, M.V. Lousy, R. Frank, M. Holdrinet and J.W. McWade, 1974. Mercury, DDT dieldrin, and PCB in the two species of Odontoceti (Cetacea) from St. Lucia, Lesser Antillas. J. Fish. Res. Board Can., 31: 1235-1239. Gerpe, M.S., 1990. Distribuci6n de metales traza, mercurio total, cadmio, cobre y zinc, en el Iobo marino de dos pelos sudamericano Arctocephalus australis (Zimmerman, 1783). Degree Thesis, Mar del Plata University, 71 pp. (in Spanish). Gerpe, M., V. Moreno, A. Prrez, R. Bastida, D. Rodr~guez and J. Marcovecchio, 1990. Trace metals in the South American fur seal, Arctocephalus australis (Zimmerman, 1783). In: J. Barcel6 (Ed.), Environmental Contamination, CEP Consultants Ltd., Edinburgh, UK, pp. 591-594. G.E.S.A.M.P. (Group of Experts on Scientific Aspects of Marine Pollution), 1990. The State of the Marine Environment, IMO / F A O /UNESCO / W M O / W H O / I A E A / U N / UNEP, Rep. Stud. GESAMP No. 39, 111 pp. Glorioso, P.D., 1987. Temperature distribution related to shelf-sea fronts on the Patagonian Shelf. Continental Shelf Res., 7: 27-34. Gordon, A.L., 1981. South Atlantic thermocline ventilation. Deep-Sea Res., 28A: 1238-1264. Hamanaka, T., T. Itoo and S. Mishima, 1982. Age-related change and distribution of cadmium and zinc concentrations in the Steller sea lion, Eumetopias jubata from the coast of Hokkaido, Japan. Mar. Poilut. Bull., 13: 57-61. Harms, U., H.E. Drescher and E. Huschenbeth, 1978. Further data on the heavy metals and organochlorines in marine mammals from German coastal waters. Meeresforschung, 26: 153-161.
Harwood, J. and B. Grenfell, 1990. Long-term risks of recurrent seal plagues. Mar. Pollut. Bull., 21: 284-287. Heppleston, P.B. and M.C. French, 1973. Mercury and other metals in British seals. Nature, 243: 302-304. Honda, K., 1985. Studies on Bioaccumulation of Heavy Metals in Marine Mammals. Ph.D. Thesis, Tokyo Univ., 101 pp. (in Japanese). Honda, K., R. Tatsukawa, K. Itano, N. Miyazaki and T. Fujiyama, 1983. Heavy metal concentrations in muscle, liver, and kidney tissues of the striped dolphin, Stenella coeruleoalba, and their variations with body length, weight, age and sex. Agric. Biol. Chem., 47: 1219-1228. Honda, K., Y. Fujise and R. Tatsukawa, 1986. Age-related accumulation of heavy metals in bone of the striped dolphin, Stenella coeruleoalba. Mar. Environ. Res., 20: 143-160. Honda, K., Y. Yamamoto, H. Kato and R. Tatsukawa, 1987. Heavy metals accumulation and their recent changes in southern minke whales Balaenoptera acutorostrata. Arch. Environ. Contam. Toxicol., 16: 209-216. I.O.C. (Intergovernmental Oceanographic Commission), 1989. Second IOC Workshop on Sardine/Anchovy Recruitment Project (SARP) in the Southwest Atlantic. IOC Workshop Rep. No. 65, 1989, 50 pp. Jickells, T.D., A.H. Knap and T.M. Church, 1984. Trace metals in Bermuda rainwater. J. Geophys. Res., 89: 1423-1428. Lavigne, D.N. and O.J. Schmitz, 1990. Global warming and increasing population densities: a prescription for seal plagues. Mar. Pollut. Bull., 21: 280-284. Legeckis, R. and A.L. Gordon, 1982. Satellite observation of the Brazil-Falkland currents, 1975 to 1976. Deep-Sea Res., 29: 375-401. Lusquifios, A. and A.J. Valdrz, 1971. Aportes al conocimiento de las masas de agua del Atlantico Sud Occidental. Serv. Hidrogr. Nay., Buenos Aires, H-650.38, 42 pp. Lusquifios, A. and A.G. Schrott, 1983. Corrientes en el Mar Epicontinental Argentino en invierno. SECYT, Progr. Nae. Recurs. Renovabl., Argentina, pp. 1-74. Lutz, V.A. and J.I. Carreto, 1991. A new spectrofluorometric method for the determination of chlorophylls and degradation products and its application in two frontal areas of the Argentine Sea. Continental Shelf Res., 11: 433-451. Marcovecchio, J.E., V.J. Moreno and A. Prrez, 1988. Determination of heavy metal concentrations in the biota of Bahia Blanca, Argentina. Sci. Total Environ., 75: 181-190. Marcovecchio, J.E., V.J. Moreno and A. Prrez, 1989. Cadmium, zinc and total mercury distribution in organisms from Samboromb6n Bay (La Plata River estuary), in Argentina. In: J.P. Vernet (Ed.), Heavy Metals in the Environment, CEP Consultants Ltd., Edinburgh, UK, Vol. 1, pp. 366-369. Marcoveochio, J.E., V.J. Moreno, R.O. Bastida, M.S. Gerpe and D.H. Rodriguez, 1990. Tissue distribution of heavy metals in small cetaceans from the Southwestern Atlantic Ocean. Mar. Pollut. Bull., 21: 299-304. Marcovecchio, J.E., M.S. Gerpe, V.J. Moreno, R.O. Bastida and D.H. Rodr[guez, 1991. Organ and tissue distribution of total mercury in the South American fur seal, Arcto-
J.E. Marcovecchio et al. / Sci. TotaI Environ. 154 (1994)141-151 cephalus australis. In: J.G. Farmer (Ed.), Heavy Metals in the Environment, CEP Consultants Ltd., Edinburgh, UK, pp. 378-381. Marcovecchio, J.E., M.S. Gerpe, V.J. Moreno, R.O. Bastida, D.H. Rodnguez and S. Mor6n, 1992a. Trace metals distribution in a Cuvier's beaked whale, Ziphius cauirostris, In: J.P. Vernet (Ed.), Environmental Contamination, CEP Consultants Ltd., Edinburgh, UK, pp. 241-244. Marcovecchio, J.E., A.O. Barral, M.S. Gerpe and W.H. Jeckel, 1992b. El monitoreo de metales pesados como hcrramienta de caracterizaci6n del ambiente marino. In: VIII Congr. Arg. de Toxicol., 22-25/Sept/1992, Buenos Aires, Argentina, pp. 112 (in Spanish). Mart, L. and H.W. Nurnberg, 1984. Trace metals levels in eastern Arctic ocean. Sci. Total Environ., 39: 1-14. Martin, J.H. and A.R. Flegal, 1975. High copper concentrations in squid liver in association with elevated levels of silver, cadmium and zinc. Mar. Biol., 30: 51-55. Martos, P. and M.C. Piccolo, 1988. Hydrography of the Argentine continental shelf between 38° and 42°S. Continental Shelf Res., 8: 1043-1056. Muir, D.C.G., R. Wagemann, N.P. Grift, R.J. Norstrom, M. Simon and J. Lien, 1988. Organochiorine chemical and heavy metal contaminants in white-beaked dolphins ( Lagenorhynchus albirostris) and pilot whales ( Globicephala melaena) from the coast of Newfoundland, Canada. Arch. Environ. Contam. Toxicol., 17: 613-629. Nurnberg, H.W., P. Valenta and V.D. Nguyen, 1983. The wet deposition of heavy metals from the atmosphere in the Federal Republic of Germany. In: Heavy Metals in the Environment, Heidelberg, Vol.1, pp. 115-123. Pefia, N.I., V.J. Moreno, J.E. Marcovecchio and A. P4rez, 1988. Total mercury, cadmium and lead distribution in
151
tissues of the southern sea lion (Otaria flavescens) in the ecosystem of Mar del Plata, Argentina. In: U. Seelinger, L.D. de Lacerda and S.R. Patchineelam (Eds.), Metals in Coastal Environments of Latin America, Springer, Berlin, pp. 140-146. Piola, A.R. and L.M. Scasso, 1988. Circulaci6n en el Golfo San Matias. Geoacta, 15: 33-51. Reid, J.L., W.D. Nowlin and W.C. Patzert, 1977. On the characteristics and circulation of the southwestern Atlantic Ocean. J. Phys. Oceanogr., 7: 62-91. Salomons, W. and U. Forstner, 1984. Metals in the Hydrocycle. Springer, Berlin, 349 pp. Uthe, J.F., F.A.J. Armstrong and M.P. Stainton, 1970. Mercury determination in fish samples by wet digestion and flameless atomic absorption spectrophotometry. J. Fish. Res. Board Can., 27: 805-811. Valenta, P. and V.D. Nguyen, 1986. Trends on heavy metals pollution by wet deposition in the Federal Republic of Germany during 1980-1984. In: H.W. Georgii (Ed.), Atmospheric Pollutants in Forest Areas, Reidel, Dordrecht, pp. 69-78. Wagemann, R., 1989. Comparison of heavy metals in two groups of ringed seals (Phoca hispida) from the Canadian Arctic. Can. J. Fish. Aquat. Sci., 46: 1558-1563. Wagemann, R., R.E.A. Stewart, W.L. Lockhart, E. Stewart and M. Povoledo, 1988. Trace metals and methylmercury: associations and transfer in harp seal (Phoca hispida) mothers and their pups. Mar. Mamm. Sci., 4: 339-355. Waldichuk, M., 1985. Biological availability of metals to marine organisms. Mar. Pollut. Bull., 16: 7-11. Yamamoto, Y., K. Honda, H. Hidaka and R. Tatsukawa, 1987. Tissue distribution of heavy metals in Weddell seals (Leptonychotes weddelli). Mar. Pollut. Bull., 18: 164-169.
ELSEVIER
,,1~ ~
The Science of the Total Environment 154 (1994) 141-151
Environmental contamination and marine mammals in coastal waters from Argentina: an overview Jorge E. M a r c o v e c c h i o * a, M a r c e l a S. G e r p e a, R i c a r d o O. Bastida b, Diego H. R o d r l g u e z b, S.G. Mor6n b alnstituto Nacional de In testigaci6n y Desarrollo Pesquero (INIDEP), Playa Grande s /n, Casilla de Correo 175, 7600 Mar del Plata, Argentina bDepartimento de Ciencias Marinas, Unioersidad Nacional de Mar del Plata, Fundaci6n Mundo Marino, Mar del Plata, Argentina
Abstract Environmental contamination become an increasing global problem. Different scientific strategies have been developed in order to assess the impact of pollutants on marine ecosystems. The distribution of toxic contaminants in tissues of different marine mammal species - - both cetaceans and pinnipeds - - has been studied in many ecosystems, as well as several related ecological processes, like pollutant accumulation or transfer through the food web. A research program directed towards evaluating the occurrence of pollutants in marine mammals from the coastal waters of Argentina (southwestern Atlantic Ocean) has been developed since 1985, and includes the study of heavy metal contents in stranded or incidentally caught animals. The marine mammal species studied during this period were: the seals Otaria flaoescens and Arctocephalus australis, and small cetaceans Tursiops gephyreus, Pontoporia blain~illei, Kogia bre~ceps and Ziphius cavirostris. In most of the cases, high contents of heavy metals (total mercury, cadmium, zinc, and copper) have been recorded. Moreover, liver showed the maximum capability for accumulation of heavy metals in all studied species. The biological and ecological characteristics of each species of the above-mentioned marine mammals (feeding habits, age, migratory pathways, or sex) contributed to the understanding of the metal sources. Considering the results as obtained during the study period it can be assumed that: (1) The global distribution of toxic contaminants also affects the southwestern Atlantic Ocean ecosystems, and (2) Marine mammals could be appropriate bioindicator species in order to assess this kind of environmental problem.
Keywords: Marine mammals; Heavy metals pollution; Bioindicator species; Bioaccumulation and biomagnification processes; Target tissues
1. Introduction Environmental contamination is a global problem which affects most ecosystems through both direct (by industrial wastes, oil spills, etc.) and indirect (atmospheric or oceanic distribution and
* Corresponding author.
circulation, etc) mechanisms. During the last few years, the number of studies dealing with the occurrence of pollutants in marine mammals has significantly increased, mainly due to: (1) The fact that an increase in pollutant concentrations has been recognized in many areas of the world (Salomons and Forstner, 1984; G.E.S.A.M.P., 1990); (2) Several populations of marine mammals have recently suffered major mortalities
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which have still not been explained (Lavigne and Schmitz, 1990; Harwood and Grenfell, 1990). A large number of papers with different approaches have been written on heavy metal pollutants in marine mammals. There are several papers correlating heavy metals concentration and tissue distribution in different species of pinnipeds and cetaceans (Anas (1974) on Callorhinus ursinus and Phoca ~tulina richardii; Denton et al. (1980) on Dugong dugong and Wagemann (1989) on Phoca hispida). Also, several papers on heavy metals accumulation in marine mammals have been published. Among them, those from Hamanaka et al. (1982) on Eumetopias jubata, Bacher (1985) on Arctocephalus pusillus and Honda et al. (1987) on Balaenoptera acutorostrata. All this information is extremely useful in assessing and characterising different environments from the pollution viewpoint. A research program has been developed in Argentina since 1985, directed at evaluating the occurrence and tissue distribution of heavy metals in marine mammal species from the southwestern Atlantic Ocean, as well as the corresponding accumulation processes and transfer through their trophic webs It has been carried out by researchers from the National Council for Scientific and Technological Research (CONICET), the National Institute for Fisheries Research and Development (INIDEP), Mar del Plata National University (UNMdP), and Fundaci6n Mundo Marino. This paper presents an overview of the results obtained from this program in the framework of the oceanographic conditions of the areas studied, and also considering the biological, ecological and behavioural characteristics of the species studied.
2. Oceanographical description of the Argentine Sea The general superficial circulation in the Southwestern Atlantic Ocean is characterized by the Brazil current - - which flows down to the pole along the continental margin of South America - - and the Malvinas-Falkland current, which
flows to the north parallel to the continental slope of the Argentine shelf (Garzoli and Bianchi, 1987). Both currents are restricted to depths lower than 1500 m. (Reid et al., 1977). Brazil (warm and high salinity) and Malvinas-Falkland (cold and low salinity) currents meet one another in the Argentine basin, at around 38°S. This creates a strong frontal zone (Gordon, 1981; Legeckis and Gordon, 1982), with a horizontal temperature gradient up to 1°C/250 m. This frontal area marks the division between subtropical and subantarctic waters. Three typical water masses occur within the Argentine continental shelf: Malvinas waters, shelf waters, and coastal waters (Lusquifios and Vald6z, 1971; Lusquifios and Schrott, 1983). Martos and Piccolo (1988), who have studied the physical characteristics between 38°S and 42°S, divided the continental shelf in two regions: coastal (depth < 40 m), where the mixture generated by wind and tides produces vertically homogeneous waters during the whole year, and the external shelf (40 m < depth < 90 m) with a warmer superficial layer (thickness about 30 m) from spring to autumn, and strong stratification at the bottom. The horizontal salinity distribution presents minimum values east of the Magallanes Strait (52°30'S, 68°W), increasing to the north up to 33.5% near 38°S. (Piola and Scasso, 1988). The Patagonian shelf is characterized by a strong mixture produced by tides (Glorioso, 1987) and these conditions produce many shelf frontal systems (Bowman, 1977; Lutz and Carreto, 1991), which are extremely important not only as productive systems (Carreto et al., 1985) but as spawning and nursery areas for many fish and shellfish species (i.e. hake, shrimps, anchovies, etc.) (IOC, 1989). Finally, it is important to note that the mean circulation in most of the Argentinean continental shelf is in the north-northeastern direction, with current speeds between 2 and 20 cm/sec (Forbes and Garrafo, 1988). A knowledge of these oceanographical conditions as a whole is extremely important in understanding the possible global distribution and circulation of pollutants in the Argentine Sea, and
J.E. Marcooecchio et al. / Sci. Total Environ. 154 (1994) 141-151
their potential effects on marine organisms living in the study areas. 3. Potential sources of pollutants in the coastal ecosystems of Argentina
The occurrence of potential sources of pollutants in the littoral ecosystems of the Argentine Sea is strongly related to the corresponding location of the most important cities as well as the largest industrial centers (Fig. 1). Area 1. The first potentially critical area is that associated with La Plata River. Buenos Aires, the capital city of Argentina, is located upstream and consequently the largest concentration of population in the country. A great industrial nucleus exists around this city, comprising amongst others metallurgical, petrochemical, textile, and pharmacological industries. Moreover, the wastes from these industrial centers are disposed - - directly or indirectly - - into the La Plata River, as are the domestic wastewaters from the city. La Plata city is located nearly 50 km southeast of Buenos Aires, and has the largest petrochemical refinery in Argentina. Both Buenos Aires and La Plata have large harbours with intense yearround activities. Area 2. Along the coastal area of Buenos Aires Province, there are several cities a n d / o r urban centers: San Clemente del Tuyfi, Pinamar, Villa Gessell, Mar del Plata, and Necochea, with various industries, populations, harbours, etc. Area 3. The Bahia Blanca estuary is situated in the southern Buenos Aires Province and is one of the most impacted coastal environments of Argentina. This semi-enclosed system includes an important industrial center (comprising smelters, petrochemical refineries and reservoirs, pesticide factories and large harbours), as well as several cities which dump their urban wastes into the estuary waters. Area 4. In the coastal system of San Matfas Gulf there are several mining centers, and only a few cities, which suggests this is not a polluted environment. Area 5. The area of Peninsula Vald6s in Chubut Province is a very important region, because of its biological diversity and ecological characteristics.
143
Several cities have been established in this area (e.g. Puerto Madryn), and several industries are developed including the most important aluminium factory in the country. Area 6. The largest development for exploitation, storage and transport of petroleum in Argentina is established in the San Jorge Gulf. Moreover, there are important cities in this area, like Comodoro Rivadavia. Studies related to marine pollution in Argentina are relatively recent, and have been developed in different areas mainly attending to particular environmental problems. Up to this point, there have been no national research programs which integrate current knowledge on this topic. 4. Materials and methods
A research program directed at assessing the occurrence, distribution, and accumulation of several heavy metals (total mercury, cadmium, zinc, copper) in marine mammals from the Southwestern Atlantic Ocean has been ongoing since 1985. During this time, many specimens of different species have been analyzed in order to determine heavy metal levels in tissue. The analyzed animals were stranded on the beaches of the study area, or incidentally caught during fishing operations. Only in the case of the South American fur seal, Arctocephalus australis, were several of the studied specimens obtained through commercial hunting, which has occurred annually in Uruguay for many years. The studied species are as follows: bottlenose dolphin (Tursiops gephyreus), La Plata dolphin or franciscana (Pontoporia blainvillei), pigmy sperm whale (Kogia breviceps), Cuvier's beaked whale (Ziphius cavirostris), South American fur seal (Arctocephalus australis) and the South American sea lion ( Otaria flavescens). In all cases, and after the corresponding dissection, samples of the most important tissue (muscle, liver, kidney and fat among others) were removed and stored in freezer at -20°C until laboratory analysis. For the analysis of total mercury, the samples were mineralized with a wet acid digestion (Uthe
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J.E. Marcovecchio et aL / Sci. Total Environ. 154 (1994) 141-151
/
Area
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Area 2 (Mar de1 Plata)
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Location o f the potential sources o f po]]utants in the coastal ecosystems o f Argentina.
57
J.E. Marcovecchio et al. /Sci. Total Environ. 154 (1994) 141-151
et al., 1970; Armstrong and Uthe, 1971), and measuring Hg concentrations by flameless atomic absorption spectrophotometry (AAS). For the determination of cadmium, zinc and copper, the method described by Marcovecchio et al. (1988) was followed, using AAS with an air-acetylene flame and deuterium background correction. A Shimadzu AA-640-13 was utilized for the corresponding analysis. Analytical reagents were used for the blanks and calibration curves, and the analytical quality control was carried out using reference materials provided by the N.I.E.S. (National Institute for Environmental Studies, Tsukuba, Japan), which certified the accuracy and precision of the developed methodology. Comparisons of metal concentrations were performed by one-way analysis of variance (ANOVA). 5. Results and discussion
Six species of marine mammals from the Southwestern Atlantic Ocean have been studied in order to determine heavy metal levels in their tissue. The results obtained from these analyses were very variable and strongly dependent on the corresponding species (Tables 1-4). The occurrence of heavy metals, both essential and non-essential, in the tissue of marine mammals is closely related to their biological characteristics and ecological habits.
145
5.1. Total mercury The distribution of total mercury in tissue showed a clear trend in the studied marine mammal species (Table 1). The liver was the most important organ for the accumulation of mercury, and this fact was verified in all the analyzed species. The mean values determined in liver of the studied marine mammals varied between 0.10 ppm (Ziphius cavirostris) and 86.0 + 7.3 ppm (Tursiops gephyreus) (Marcovecchio et al., 1990). Kidney also showed a significant ability to accumulate mercury, and the values obtained in the corresponding analysis varied between 0.17 ppm (Z. cavirostris) and 13.4 + 2.5 ppm (T. gephyreus), while the concentrations in muscle varied between 0.23 ppm and 5.5 + 0.8 ppm in the same two species. The fact that the minimum concentrations were recorded for Ziphius cavirostris and the maximum for Tursiops gephyreus was related with the corresponding ages of the studied animals. Thus, while the analyzed specimen of Cuvier's beaked whale was a pup (and consequently it would not have been strongly exposed to pollutants - - Marcovecchio et al., 1992a), those of bottlenose dolphin were up 10 years old with a significantly higher time of exposure to pollutants (Marcovecchio et al., 1990). In addition, a strong relationship between mercury concentration and the age of the analyzed organisms was reported by several
Table 1 Total mercury distribution in tissues of the studied marine mammal species from the Argentine Sea Species
N
Analyzed tissue Muscle
Liver
Kidney
Blubber
Reference Marcovecchio et al. (1990) Marcovecchio et al. (1990) Marcovecchio et al. (1990) Marcovecchio et al. (1992a) Pefia et al. (1988) Gerpe et al. (1990)
Tursiops gephyreus
2
5.5 (0.8)
86.0 (7.3)
13.4 (2.5)
ND
Pontoporia blainvillei
7
3.0 (1.2)
3.8 (1.6)
1.9 (0.7)
ND
Kogia breviceps
1
4.2
Ziphius ca virostris
1
0.23
Otariaflavescens
7
1.4 (0.6)
Arctocephalus australis
8
0.8 (0.3)
11.7 0.10
10.5
ND
0.17
ND
46.5 (13.3)
2.1 (0.8)
ND
33.7 (11.7)
0.9 (0.2)
ND
Mean value, in /~g/g wet wt.; S.D. in parenthesis; N, number of specimens analyzed; ND, non-detectable value.
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J.E. Marcovecchio et al. / Sci. Total Environ. 154 (1994) 1 4 1 - 1 5 1
authors working with different species (Bacher (1985) for Arctocephaluspusillus Yamamoto et al. (1987) for Leptonychotes wedeUi, Honda et al. (1987) for Balaenoptera acutorostrata, Pefia et al (1988) for Otaria flavescens, and Gerpe et al. (1990) for Arctocephalus australis). On the other hand, the mercury concentrations determined in the studied marine mammal species were significantly higher than those corresponding to the organisms they feed on. In this respect, statistical analysis has showed significant differences (P < 0.01) between mercury contents in the marine mammal species (Table 1) and those of their food (Table 5). These results have been interpreted as supporting the occurrence of a mercury biomagnification process through the corresponding food web of each marine mammal species. The occurrence of this ecological process has been reported by several authors, like Drescher et al. (1977) for Phoca vitulina from the North Sea, Wagemann et al. (1988) for Phoca groenlandica, and Muir et al. (1988) for Lagenorhynchus albirostris and Globicephala melaena from Newfoundland (Canada). The trend observed in the distribution of total mercury in the tissue of the studied marine mammal species from the Southwestern Atlantic Ocean (Hg liver > Hg kidney > Hg muscle) clearly agreed with the previous reports of other authors, like Gaskin et al. (1974) for Stenella
longirostris from Lesser Antillas, and Harms et al. (1978) for Phocoena phocoena from the Baltic Sea.
5.2. Zinc and copper The results of the analysis of zinc and copper in the tissue of the studied marine mammal species showed a clear trend, which fully correlates with that reported for total mercury in previous paragraphs. Thus, the liver has the highest concentrations of both metals in all of the analyzed animals, with ranges between 56.5 + 11.0 ppm Zn (Arctocephalus australis) and 196.2 + 34.1 ppm Zn (Tursiops gephyreus) (Table 2), and between 10.3 ppm Cu (Kogia breviceps) and 77.7 + 3.8 ppm Cu (Tursiops gephyreus) (Table 4). Moreover, kidney of the studied specimens has levels varying between 44.2 + 8.2 ppm Zn (Arctocephalus australis) and 169.7 ppm Zn (/~ breviceps) (Table 2), and between 3.9 + 0.9 ppm Cu (A. australis) and 29.5 + 3.9 ppm Cu (T. gephyreus) (Table 4). Finally, muscle showed values ranging between 28.2 + 15.4 ppm Zn (A. australis) and 93.3 + 13.1 ppm Zn (T. gephyreus) (Table 2), and between 1.7 + 0.1 ppm Cu and 6.3 + 1.1 ppm Cu in the same species, respectively (Table 4). In the case of zinc and copper, a good relationship between the concentration of the metal and age (or age classes) of the studied animals has been recorded, which would demonstrate that
Table 2 Zinc distribution in tissue of the studied marine mammal species from the Argentine Sea Species
N
Analyzed tissue Muscle
Liver
Kidney
Blubber
Reference
93.6 (5.9)
4.7 (0.8)
Marcovecchio et al. (1990) Marcovecchio et al. (1990) Marcovecchio et al. (1990) Marcovecchio et al. (1992a) Pefia et al. (1988) Gerpe et al. (1990)
Tursiops gephyreus
2
93.3 (13.1)
196.2 (34.1)
Pontoporia blainvillei
7
49.3 (4.8)
83.4 (40.0)
Kogia breviceps
1
57.5
163.2
169.7
Ziphius cavirostris
1
--
--
--
Otaria fla oescens
7
--
--
--
Arctocephalus australis
8
28.2 (15.4)
56.5 (11.0)
79.4 (21.4)
44.2 (8.2)
Mean value, in /~g/g wet wt.; S.D. in parenthesis; N, number of specimens analyzed.
6.6 (0.6) 0.2
J.E. Marcovecchioet al. /Sci. TotalEnviron. 154 (1994)141-151 bioaccumulation of both metals occurs. These conclusions agree with several reports from other authors, e.g. those by H a m a n a k a at al. (1982) for Eumetopiasjubata, or by H o n d a (1985) and H o n d a et al. (1986) for Stenella coeruleoalba. Unlike total mercury, there was no clear trend on the biomagnification of zinc and copper through the corresponding food web. Thus, when the concentrations of both metals in the marine m a m m a l species (Tables 2,4) were compared with those of their prey (Table 5) it was not possible to establish a clear trend or relationship. It seems that m o r e samples must be reviewed in order to clarify this point. Up until now, the international literature has not reported enough documentation to support the occurrence of the biomagnification process of metals, except for mercury (Waldichuk, 1985) and cadmium (Wagemann, 1989). The trends observed for the distribution of Zn and Cu in the tissues of the study marine m a m mal species (Zn liver > Z n kidney > Zn muscle; Cu liver > Cu kidney >> Cu muscle) fully coincide with those reported by several authors for other marine m a m m a l species, e.g. Falconer et al. (1983) for the harbour porpoise Phocoena phocoena from the Baltic Sea, and Fujise et al. (1988) for the Dali's porpoise Phocoenoides dalli from the Northwestern Pacific.
147
5.3. Cadmium The results as obtained from the analysis of cadmium in the tissue of the studied marine m a m m a l species allow us to observe a particular trend for cadmium distribution. Kidney was the most important organ for the accumulation of cadmium in these species, with values varying between 5.6 + 2.4 p p m Cd (Otariaflavescens) and 412.6 p p m Cd (Kogia breviceps) (Table 3). Liver followed kidney in the ability to accumulate cadmium, and the hepatic levels of this metal ranged between non-detectable values (Ziphius cavirostris) and 34.5 + 17.1 p p m Cd (Arctocephalus australis) (Table 3). Finally, the levels of cadmium in muscle of the studied species were extremely low, and in fact most of the concentrations were below the detection limit of the method. For example, the highest cadmium concentration as determined in muscle was recorded in Arctocephalus australis: 0.4 + 0.1 p p m Cd (Table 3). Cadmium concentrations in tissues of the analyzed species seemed to have a strong relationship with age (or age classes). The results reported in the papers of G e r p e (1990), G e r p e et al. (1990), and Marcovecchio et al. (1991), all for Arctocephalus australis, support this point. Several reports from other authors also agreed with this, i.e. Heppleston & French (1973) for Phoca vitulina,
Table 3 Cadmium distribution in tissues of the studied marine mammal species from the Argentine Sea Species
N
Analyzedtissue Muscle
Liver
Kidney
Blubber
Reference Marcovecchio et al. (1990) Marcovecchio et al. (1990) Marcovecchio et al. (1990) Marcovecchio et al. (1992a) Pefia et al. (1988) Gerpe et al. (1990)
Tursiopsgephyreus
2
ND
0.8 (0.2)
28.4 (4.3)
ND
Pontoporiablainvillei
7
0.1 (0.1)
3.3 (1.4)
9.9 (3.9)
ND
Kogia breviceps
1
0.2
7.6
Ziphius cavirostris
1
ND
ND
Otariaflauescens
7
ND
Arctocephalusaustralis
8
0.4 (0.1)
412.6
ND
ND
ND
1.1 (0.7)
5.6 (2.4)
ND
34.5 (17.1)
48.15 (24.1)
--
Mean value, in tzg/g wet wt.; S.D. in parenthesis; N, number of specimens analyzed; ND, non-detectable value.
148
J.E. Marcovecchio et a t / S c i . Total Environ. 154 (1994)141-151
Table 4 Copper distribution in tissues of the studied marine mammal species from the Argentine Sea Species
N
Analyzed tissue Muscle
Liver
Kidney
Blubber
Reference Marcovecchio et al. (1990) Marcovecchio et al. (1990) Marcovecchio et al. (1990) Marcovecchio et al. (1992a) Pefia et al. (1988) Gerpe et al. (1990)
Tursiops gephyreus
2
6.3 (1.1)
77.7 (3.8)
29.5 (3.9)
4.0 (0.6)
Pontoporia blainvillei
7
2.5 (1.5)
16.0 (3.3)
14.0 (4.9)
2.8 (0.3)
Kogia breviceps
1
2.0
10.3
Ziphius cavirostris
1
.
.
.
.
Otaria fla vescens
7
.
.
.
.
Arctocephalus australis
8
1.7 (0.1)
12.2 (2.0)
7.4
ND
3.9 (0.9)
--
Mean value, in /zg/g wet wt.; S.D. in parenthesis; N, number of specimens analyzed; ND, non-detectable value.
Hamanaka et al. (1982) for Eumetopias jubata, and Honda (1985) for Stenella coeruleoalba. As in the case of total mercury, there was enough evidence to support the occurrence of cadmium biomagnification through the corresponding food webs of the studied marine mammal species. Furthermore, the importance of diet as a source of cadmium for the marine mammals must be emphasized, as can be appreciated in Table 5. The trend observed for the distribution of cadmium in the tissues of the studied marine mammal species (Cd kidney >> Cd liver >> Cd muscle) coincided with previous reports from other authors for different species, e.g. Harms et al. (1978) for Phocoena phocoena, or Honda et al. (1983) for Stenella coeruleoalba. 6. Concluding comment
Considering the results presented here, it is necessary to put forward several central ideas which could contribute to a better understanding of this topic. First of all, it is important to emphasise that all of the analyzed marine mammal species have heavy metals in their tissue, not only essentials (as zinc or copper) but also non-essentials (as cadmium or mercury). This point, which is supported by various papers previously published (Marcovecchio et al., 1990, 1991, 1992a; Gerpe et al., 1990) is very important, because it
shows that the Southwestern Atlantic Ocean is not excluded from the global pollution which affects our planet. In this respect, several authors have emphazised the importance of atmospheric (Nurnberg et al., 1983; Jickells et al., 1984; Valenta and Nguyen, 1986), and oceanic transport and circulation (Gardner, 1975; Mart and Nurnberg, 1984). Furthermore, the importance of the relationship between the pollutant content of marine mammal tissue and the characteristics of the species, both biological (age, sex, size) and ecological (feeding habits, migratory pathways) has been strongly underlined. The results showed significant correlations between mercury content and the age of several marine mammal species (Marcovecchio et al., 1990), and gave good explanations for the differences observed in the levels of heavy metals between sexes in the South American fur seal, Arctocephalus australis (Gerpe et al., 1990). The international literature strongly supports these concepts (Hamanaka et al., 1982; Honda, 1985; Muir et al., 1988; Wagemann et al., 1988). The feeding habits as well as the ecological niche were the most important factors in heavy metal accumulation for the studied marine mammal species. This point was clearly confirmed by several of the results obtained. Thus, the highest values of mercury have been recorded in the mammal species with typically icthyophagus
149
J.E. Marcovecchio et al. / Sci. Total Entiron. 154 (1994) 141-151
Table 5 Heavy metal concentrations in several food items from the diet of the studied marine mammal species Species
Corvina (fish)
Analyzed metals (/z/g) Hg
Cd
Zn
0.13
3.03
44.30
0.16
3.69
11.75
0.09
0.61
3.97
0.48
0.15
25.08
0.11
0.05
9.28
0.17
0.03
9.16
0.06
0.10
12.60
Micropogonias fumieri a
Pescadilla (fish) Cynoscion striatus a
Anchoita (fish) Engraulis anchoita b
Pez angel (fish) Squatina argentina a
Camar6n (shrimp) Artemesia longinaris a
Langostino (shrimp) Pleoticus muelleri a
Calamar (squid) lllex argentinus c
aAfter Marcovecchio et al. (1988, 1989). bArter A.O. Barral (INIDEP), pers. commun. cArter Marcovecchio et al. (1992b).
trophic habits, like Tursiops gephyreus (it must be emphasised that fish are known to be the single largest source of mercury in the aquatic environment - - Chvojka and Williams, 1980). On the other hand, highest cadmium concentrations have been determined-in the oceanic species Kogia breviceps, which is a squid-eater (squids have been noted as large accumulators of cadmium in the marine environment (Martin and Flegal, 1975). Coincidentally, marine mammal species with different percentages-of fish and squid in their diets
Acknowledgements
(Pontoporia blainvillei, Otaria flatescens, Arctocephalus australis) were shown to have mercury
References
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T.
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ronments seems to be adequate, but it would be laudable to complete this viewpoint with others, like concentrations of pollutants in abiotic compartments or diet of the selected indicators.
This paper was partially financed by The National Council for Scientific and Technological Research (CONICET) from Argentina, and by Fundaci6n Mundo Marino.
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