Polar Biol (1999) 22: 102±108
Ó Springer-Verlag 1999
ORIGINAL PAPER
Mark A. Hindell á Nigel Brothers á Rosemary Gales
Mercury and cadmium concentrations in the tissues of three species of southern albatrosses
Accepted: 15 February 1999
Abstract Cadmium and mercury concentrations were measured in the tissues of 64 individual albatrosses [23 wandering albatrosses (Diomedea exulans), 9 royal albatrosses (Diomedea epomophora) and 32 shy albatrosses (Thalassarche cauta)] which were killed as by-catch in longline ®shing activities between 1991 and 1994. Mercury concentrations were also determined for 33 shy albatross eggs (excluding shells). The birds were all sexed and assigned to one of two age classes (immature and adult). The three species exhibited dierences both in overall concentrations of cadmium and mercury, and also in the pattern of accumulation of metals with age and sex. Wandering albatrosses exhibited the highest mercury concentrations with a mean concentration in adult liver samples of 920.0 794.1 lg g)1 dry weight. Shy albatrosses had the lowest mercury concentrations with mean concentrations in adult livers of 36.3 21.4 mg g)1 dry weight. The highest mercury concentration was 1800 lg g)1 for an adult female wandering albatross. Cadmium concentrations were less variable, with adult royal albatrosses having the highest average concentrations (180.0 165.0 in adult kidneys) and adult shy albatrosses the lowest (40.1 20.0 in adult kidney). The highest individual cadmium concentration was 287 lg g)1 for a juvenile wandering albatross. There was no evidence of increased accumulation of cadmium with age in any of the species, but wandering albatrosses showed higher mercury concentrations in adults than juveniles. Female wandering albatrosses also had signi®cantly higher mercury conM.A. Hindell (&) Antarctic Wildlife Research Unit, Department of Zoology, University of Tasmania, PO Box 252C, Hobart, Tasmania, 7001, Australia e-mail:
[email protected] N. Brothers á R. Gales Parks and Wildlife Service, Department of Environment and Land Management, PO Box 44A, Hobart, Tasmania, 7001, Australia
centrations than males. The mercury contents of the shy albatross eggs were very low, with a maximum concentration of 5.4 lg g)1. The results of this study are consistent with the ®ndings of previous work on albatrosses and support the notion that the life-history strategy of these species (i.e. long-lived with low reproductive output) may be an important determinant in the concentrations of some metals found in their tissues.
Introduction The activities of humans aect albatrosses, and other marine organisms, in a variety of ways. Some anthropogenic impacts, such as mortalities associated with ®sheries by-catch, are obvious and quanti®able (Brothers 1991; Prince et al. 1994; Cherel et al. 1996). Some impacts, however, are less direct and more dicult to measure. Of these, anthropogenic marine pollutants are a source of particular concern due to their ability to exert lethal and sub-lethal in¯uences on a wide range of marine organisms (Bryan 1984). Given that some pollutants can accumulate with increasing trophic level, marine predators, such as albatrosses, may be particularly vulnerable as they are at the top of the marine food web (Walsh 1990). Of the two major groups of marine pollutants, organochlorines and heavy metals, the biological signi®cance of the organochlorines is best understood because they are entirely anthropogenic. The signi®cance of heavy metal concentrations is less well understood because they occur naturally in marine systems, and so will always be present in the tissues of marine organisms (Thompson et al. 1990). To show an anthropogenic in¯uence from heavy metal concentrations, it must be demonstrated that the amounts measured in animal tissues are elevated above these normal background concentrations, which is often dicult in the absence of historical data (Walsh 1990; Ludwig et al. 1998).
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Previous studies of heavy metals in a number of albatross species have indicated that albatrosses have unusually high concentrations of two heavy metals, cadmium and mercury (Muirhead and Furness 1988; Thompson et al. 1990; Lock et al. 1992; Thompson et al. 1993). The mercury concentrations reported for a wandering albatross (Diomedea exulans) of 270 lg g)1 (wet weight) in liver are the highest concentrations reported for any vertebrate (Muirhead and Furness 1988). Sooty albatrosses (Phoebetria fusca) had similarly high concentrations, although yellow-nosed albatrosses (Diomedea chlororhynchus) were within the range of other seabirds. Cadmium concentrations were also highest in wandering albatrosses and sooty albatrosses (137 lg g)1). However, comparisons of this nature are dicult, because a number of potentially confounding factors exist (Thompson 1990): 1. Gender eects. Females often have lower concentrations than do males because they are able to eliminate some metals during egg laying (e.g. Stock et al. 1989), or there may be sexual dierences in foraging behaviours (e.g. Stock et al. 1989). 2. Age eects. Metal concentrations may accumulate over time, particularly in species with limited abilities to regulate metal concentrations in their tissues (e.g. Honda et al. 1986). 3. Seasonal eects. The concentrations of some metals, such as mercury, may be lowest just after the moult, because they are bound into the feathers (Braune and Gaskin 1987; Stewart et al. 1994), or there could be seasonal dierences in diet (Braune 1987). 4. Physiological eects. Some species may have physiological mechanisms that enable metals to be stored in the tissues in a non-toxic chemical form (Monteiro and Furness 1995).
Materials and methods All of the birds sampled in this study were killed as by-catch in the longline ®shery operating in the southern Paci®c and Indian Oceans. Whole carcasses were frozen at sea, within 24 h of being hauled aboard. In all, 64 individual albatrosses [23 wandering albatrosses, 9 royal albatrosses (Diomedea epomophora) and 32 shy albatrosses (Thalassarche cauta)] were sampled between 1990 and 1994. Each bird was assigned to one of two age classes (juvenile or adult) on the basis of plumage and sex was determined on dissection. Liver samples were collected for mercury content and kidney samples were collected for cadmium content. Thirty-three shy albatross eggs were also collected on Albatross Island, in Bass Strait, Australia (40.375°S, 144.565°E). In 1989, eggs were taken from 14 known-age individuals, with ages ranging from 4 to 7 years. Eggs from nine of these individuals were collected again in 1990 and in 1994. Mercury concentrations were determined by drying a sample of liver or egg, before digesting the sample in 3:2 nitric/sulphuric acid solution at 100°C for 4 h. Samples were then oxidised with potassium permanganate and analysed by mercury vapour generation cold vapour atomic absorption. Cadmium concentrations were determined by drying a sample of kidney before digestion in nitric acid solution at 100°C for 2 h. The solution was diluted in de-ionised water and analysed by ¯ame atomic absorption. All data are expressed as lg g)1 dry weight, to eliminate potential problems associated with dierential moisture content between tissues and species. The average water content of kidney tissue was 71.9 1.8%, and the average water content of liver tissue was 66.1 3.3%. Statistical comparisons were made using three-way analysis of variance, using species, sex and age as treatments, and were restricted to the wandering and shy albatrosses, as there were insucient data from the royal albatrosses. Data from royal albatrosses are, however, included in the ®gures and table for comparative purposes. Normality of the data was determined by inspection of normal probability plots. All data were log transformed prior to analysis, and relationships within each treatment were tested using Tukey HSD post-hoc tests. Frequency distributions were tested for normality using SYSTAT V5. The egg data were analysed using repeated-measures analysis of variance.
Results
Our study aimed to further investigate the concentrations of cadmium and mercury in albatrosses, in order to: (1) compare metal concentrations between several albatross species with dierent moult and reproductive cycles, (2) test whether these metal concentrations vary with age and sex, and (3) draw some preliminary conclusions regarding toxic metal concentrations in albatrosses and assessing the role of anthropogenic metals in these burdens.
There were signi®cant dierences in mercury content between wandering and shy albatrosses (F1,45 = 93.282, P < 0.001). Wandering albatrosses had the highest mean mercury values with 482.3 120.7 lg g)1 dry weight, more than 10 times that of shy albatrosses
Table 1 Mean (SD) values of mercury and cadmium in wandering, royal and shy albatross. All values are expressed in lg g)1 dry weight. The mean water content of kidneys (cadmium) in the
sample was 71.9 1.8% and for liver 66.1 3.3%. The sex and age of the samples are also shown. Also indicated are the mercury concentrations for 33 eggs from shy albatrosses
Mean mercury Maximum mercury Mean cadmium Maximum cadmium Total sample (n) Number of males/females Number of adults/juveniles
Mercury concentrations
Eggs (shy albatross)
Shy
Royal
Wandering
2.1 0.8 5.3 ± ± 33 ± ±
39.6 4.6 93.0 53.8 4.9 117.0 29 10/19 4/5
108.6 35.8 350.0 171.2 23.9 265.0 9 3/6 14/15
482.3 120.7 1800.0 136.4 12.5 287.0 22 15/7 6/16
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(Table 1). The maximum value of 1800 lg g)1 (or 680 lg g)1 wet weight) for a wandering albatross is almost 3 times higher than the previously recorded mercury level of any vertebrate. The mean mercury level of royal albatrosses (108.6 35.8) was midway between these two species. The frequency distribution of mercury values was not normally distributed for either wandering (Fig. 1) or shy albatrosses (Fig. 2). There were too few samples for royal albatrosses to make a comparable analysis. Gender eects There were signi®cant dierences in mercury concentrations between the sexes (F1,45 = 5.596, P = 0.022). A post-hoc Tukey test indicated that these dierences were only found in the wandering albatrosses, where the females had signi®cantly higher mercury concentrations than did males (Fig. 2). The highest recorded mercury level was from an adult female. Age eects Overall, there was no relationship between age and mercury concentrations (F1,45 = 3.331, P = 0.075), but a Tukey test indicated that wandering albatross adults
Fig. 2 Mercury and cadmium concentrations in male and female albatross from three species. The boxes indicate the interquartile range, the horizontal line the median, and the vertical lines the range; n.s. indicates no signi®cant dierence between the sexes within a species; * indicates a signi®cant dierence. All concentrations are in lg g)1
had signi®cantly higher concentrations than did juveniles (Fig. 4). The royal albatross data showed a similar trend, although the values were much lower overall. Eggs The eggs from the shy albatrosses had uniformly low values with an overall mean of 2.1 0.8 lg g)1 (Table 1). Repeated measures ANOVA indicated that there were no trends in the amount of mercury deposited in an egg by an individual bird over time (Table 2, F2,16 = 0.694, P = 0.514). Similarly, the youngest birds (4 and 5 years) did not have signi®cantly dierent concentrations to the oldest birds (6 and 7 years) in the 1st year of the study (t7 = 0.056, P = 0.957). Cadmium concentrations
Fig. 1 Frequency distributions of mercury concentrations in the livers of wandering and shy albatross. All concentrations are in lg g)1
There were also signi®cant dierences between the species with respect to their tissue cadmium concentrations (F1,42 = 44.941, P < 0.001). The mean concentrations of cadmium in wandering albatrosses (136.4 12.5) were almost 3 times those of shy albatrosses (53.8 4.9, Table 1). The cadmium concentrations obtained here were normally distributed both in wandering and shy albatrosses (Fig. 2).
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Fig. 3 Frequency distributions of cadmium concentrations in the kidneys of wandering and shy albatross. In both species the distributions were normally distributed, as indicated by the ®tted curve. All concentrations are in lg g)1
Gender eects There were no signi®cant dierences between the sex and species groups (F1,42 = 0.036, P = 0.850), but the wandering albatrosses had higher concentrations overall than the shy albatrosses (F1,42 = 44.941, P < 0.001) (Fig. 2). Age eects Cadmium concentrations were signi®cantly dierent between the species and age groups (F1,45 = 4.719, P = 0.036). A Tukey test revealed that this dierence was con®ned to the shy albatrosses, where the adults had higher concentrations than the juveniles (Fig. 4).
Discussion The three species of albatross in this study have dierent life-history cycles, which make them appropriate subjects for examining the in¯uence of age and gender on heavy metal concentrations in seabirds. Wandering albatrosses have a circumpolar distribution, and breed on subantarctic islands in the southern Indian, Atlantic and
Fig. 4 Cadmium concentrations in juvenile and adult albatross from three species. The boxes indicate the interquartile range, the horizontal line the median and the vertical lines the range; n.s. indicates no signi®cant dierence between the ages within a species; * indicates a signi®cant dierence. All concentrations are in lg g)1
Paci®c Oceans. Royal albatrosses are restricted to breeding on New Zealand and its sub-Antarctic islands. Both species are biennial breeders, commencing breeding at approximately 8 years of age, and living to more than 50 years (Marchant and Higgins 1990). Shy albatrosses breed solely on islands o southern Australia. They are annual breeders, commencing breeding at 4± 5 years of age and living for approximately 30 years (Marchant and Higgins 1990). However, other members of the closely related ``cauta'' complex (Thalassarche steadii, T. salvini and T. eremita) breed in New Zealand and, as our collections were made prior to the recent taxonomic revision, it is possible that some of our specimens are from this group. The species also have dierent foraging patterns, with wandering albatrosses having predominantly oceanic movement patterns, largely con®ned to the Southern Ocean (Prince et al. 1992). Some wandering albatrosses from the Iles Crozet in the southern Indian Ocean regularly forage in shallow coastal waters o the southeast coast of Australia (Nichols et al. 1995). There is also a pronounced gender- and age-related separation of foraging zones in this species, with females utilising more northerly waters than males (Weimerskirch et al. 1993). Less is known about the movements of royal albatrosses, but their distribution appears to be similar to that of the wandering albatross (Woehler et al. 1990). Adult shy albatross are predominantly found over the shelf waters of southeastern Australia (Brothers et al.
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1997), although juveniles and non-breeding birds have been seen south of 60°S (Woehler et al. 1990). In this species, the foraging ranges of adults are restricted to within 200 km of their breeding sites, which engenders marked inter-population dierences in foraging zones (Brothers et al. 1998). This study has con®rmed the ®ndings of earlier studies which indicated that albatrosses in general tend to have high concentrations of some heavy metals in their tissues compared to other seabirds (Muirhead and Furness 1988; Lock et al. 1992; Thompson et al. 1993). This is particularly so for wandering albatrosses, which have the highest mercury concentrations reported for any vertebrate species. Attributing these concentrations to either natural or anthropogenic sources of metals is dicult, however, as the natural concentrations of metals can vary considerably due to a wide range of oceanographic and geological factors (Bryan 1976; Bull et al. 1977; Muirhead and Furness 1988). Interpretation is made more complicated if the study animals have a range of physiological adaptations for dealing with metals incorporated into their tissues, as appears to be the case in some albatrosses (Lock et al. 1992). Mercury The frequency distributions of tissue metal concentrations within a species can provide some indication of how well the species is able to biochemically regulate those metals. If the concentrations follow a normal distribution, there is some evidence that the species has the ability to regulate metal concentrations (Norheim 1987; Muirhead and Furness 1988). This was the case for cadmium concentrations both in wandering and shy albatrosses, but not for mercury concentrations, which ranged between 5 and 100 lg g)1 for shy albatrosses and between 20 and 1800 lg g)1 for wandering albatrosses. The observation that females of neither species had lower mercury concentrations than the males indicates that, unlike some other bird species (Fimreite et al. 1980; Stewart et al. 1994), eggs are not an important source of mercury elimination in these two species of albatross. This is supported by the ®nding that, in shy albatrosses, the eggs had very low concentrations of mercury. Further, there was no evidence that the amount of mercury deposited in eggs changed throughout an individual's life (Table 2). If eggs were an important route of metal excretion, the concentrations might be expected to increase as the birds get older and accumulate more mercury. Conversely, the ®rst eggs laid may have higher metal concentrations as the birds eliminated metals that accumulated before their ®rst breeding attempt. The failure to utilise eggs as a major avenue of mercury elimination may be due to the fact that they lay only a single egg annually or, in wandering and royal albatrosses, biennially.
Table 2 Mercury concentrations in the eggs of nine individual shy albatrosses of known age. Eggs were collected from each individual in 1989 (the year in which they ®rst bred), 1990 and 1994 Bird
280±01316 280±01424 280±02121 280±02139 140±47376 280±01581 280±02893 280±02860 280±05229
Age in 1989
6 6 5 5 7 6 5 5 4
Mercury concentrations (lg g)1) dry weight 1989
1990
1994
Mean
2.4 1.8 2.6 2.5 1.7 1.7 1.1 1.2 2 1.9 0.5
2.1 1.5 5.3 1.8 1.1 1.8 0.9 2.8 3.3 2.3 0.4
1.5 2.3 2.8 2.6 2.5 2.2 1.7 1.8 2.2 2.2 0.4
2.0 1.9 3.6 2.3 1.8 1.9 1.2 1.9 2.5
0.5 0.4 1.5 0.4 0.7 0.3 0.4 0.8 0.7
The higher mercury concentrations in female wandering albatrosses than in males may also be a re¯ection of the dierent foraging strategies between the genders. Satellite-tracking studies have shown that male and female wandering albatrosses utilise dierent parts of the Southern Ocean, with females utilising more northerly waters, at least during the breeding season (Prince et al. 1992; Weimerskirch et al. 1993). The females therefore have the potential to encounter more contaminated areas (i.e. closer to human activity). The dierence could, however, be equally attributable to dierent diets between the genders, so few conclusions can be drawn without further studies. Other studies have presented evidence for accumulation of mercury in wandering albatross as they become older (Muirhead and Furness 1988). Some seabirds may be able to convert toxic methylmercury to more stable, and less toxic inorganic mercury (Lock et al. 1992; Thompson et al. 1993). This would be advantageous in a long-lived animal with low reproductive (i.e. egg production) rates and long moult cycles, such as the wandering albatross, and would give limited opportunity for mercury elimination. It is also unlikely that chicks could acquire mercury from their mothers, because there is no evidence of unloading via eggs. Juvenile wandering albatrosses had higher mercury concentrations than did adult shy albatrosses (Fig. 4), suggesting that there may be species-speci®c metabolic mechanisims for dealing with mercury. It is also possible that juvenile wandering albatrosses are exposed to higher concentrations of environmental mercury than are shy albatrosses. Cadmium The frequency distribution of tissue cadmium concentrations in the samples provides evidence that this metal is regulated to some degree in both shy and wandering albatrosses. This is further supported by the observation that cadmium concentrations do not accumulate with
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age in either species as does mercury (Fig. 4). There was also no evidence of dierential accumulation between males and females (Fig. 2), suggesting that eggs are not an important avenue of elimination. This may indicate that both sexes utilise similar foraging strategies. Interestingly, juvenile shy albatross had higher concentrations than adults. This may re¯ect dierent foraging patterns in these animals, or re¯ect inter- or intra-population dierences. The juveniles in this study may be of dierent origins to the adults, due to our being unable to distinguish between New Zealand and Australian birds, or from dierent populations for the same species using dierent foraging areas. More importantly, however, this indicates that the birds may be able to reduce their cadmium load as they get older. Despite the possible ability to regulate cadmium concentrations, wandering albatrosses in this study have concentrations 2±3 higher than shy albatrosses. The reasons for this are unclear. The more pelagic lifestyle of the wandering albatrosses may expose them to higher environmental concentrations of cadmium than the shy albatrosses. Alternatively, they may have dierent diets, which have dierent concentrations of cadmium (Lock et al. 1992). Neither of these are known for the individuals in this study, although both are ®sh and squid eaters, and both have overlapping foraging grounds to some degree (Marchant and Higgins 1990). Conclusions High concentrations of metals in the tissues of some seabirds may be due to, or at least exacerbated by, the life-history characteristics of the birds rather than by anthropogenic in¯uences (Muirhead and Furness 1988; Thompson et al. 1993; Stewart et al. 1994). Wandering albatrosses are very long-lived, and due to their low reproductive rate (one egg every 2 years) and slow moult they have very few ways of eliminating mercury. Wandering albatrosses may have the ability to demethylate mercury and store it as inorganic molecules in the liver. The logical extension of this, that mercury concentrations should increase in this species with age, was demonstrated empirically. The high cadmium concentrations in this species are more dicult to explain, but may have been due to dietary eects. The natural occurrence of metals in the marine environment, detoxi®cation mechanisms, and the subsequent accumulation of high concentrations of metals all make the detection of anthropogenic metal pollution in seabirds dicult (Stewart et al. 1994). This is particularly so for mercury, but it is probably also true for cadmium, as unusually high concentrations occur in highly oceanic species which would usually not be in contact with high concentrations of pollutants. The approach most likely to yield interpretable results is to look for changes in metal concentrations over time (e.g. Monteiro and Furness 1995) as this will control for many of the confounding eects of short time-frame
studies. Further, studies should also examine the form of metals in the tissues, as this will reveal if the birds are sequestering mercury in a harmless inorganic form. Acknowledgements This work was funded by a grant from the Antarctic Scienti®c Advisory Committee. The samples were analysed in the Tasmanian Department of Environment Analytical laboratories. The birds were collected by Australian Fisheries Management Authority observers on Australian ®shing boats. Tim Reid helped with the dissections.
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