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A pilot study of heavy metal accumulations in a barnacle from the Salton Sea, Southern California
AhttTIw I~olhttiol~ Bulh'tiH. Vol. 36, No. 2, pp. 138 143. 19t,~8
Pergamon PII: S0025-326X(97)00100-8
~) 1998 Elsevier Science l.td All rights reserved. Printed in Greal Britain 0025-326X/98 $19.[)1)+0.00
A Pilot Study of Heavy Metal Accumulations in a Barnacle from the Salton Sea, Southern California* WOJCIECH F I A L K O W S K I t and W.ILLIAM A. NEWMAN~
tJagiellonian University, Department of Hydrobiology, ul. Oleandry 2a, 30-063 Krakow, Poland ~University of California at San Diego, Scripps Institution of Oceanography, La Jolla, CA 92093-0202, USA
Accumulations of Fe, Cu, Zn, Cd, Sn, Hg and Pb in body tissues and egg masses of Balanus amphitrite were measured with an inductively coupled plasma source mass spectrometer (ICP-MS). Barnacles proved to be a good choice as a sentinel species for monitoring of heavy metals. A comparison of their levels in the animals inhabiting the Salton Sea with those from coastal waters of the Pacific Ocean showed that the sea, contrary to expectations, has not been severely contaminated by heavy metals. The accumulations of the metals in barnacle bodies and eggs varied markedly between the stations but appeared least where organic pollution was highest. © 1998 Elsevier Science Ltd. All rights reserved. Keywords: Balanus amphitrite; bioaccumulation; biomonitoring; Pacific Ocean; Salton Sea; trace metals.
The Salton Sea in Southern California, whose surface is over 70_m below sea level, is the most recent body of water in this basin. The present 'sea' came into being in 1907 when a man-made irrigation canal from the Colorado River broke and flooded the depression that extends 82 m below sea level. Nearly all the water entering the sea originates in the Colorado River (Setmire et al., 1993), so the ionic composition of the two bodies is very similar. Measurements made shortly after the sea was formed indicated that its salinity (3.6 ppt) was greater than in the Colorado River (0.7 ppt) due to the dissolution of salts from deposits left over from earlier instances of flooding (Young, 1970). In 1954-1965 the salinity of the Salton Sea was about 33 ppt. Predictions made at that time estimated that it would increase at a rate of approximately 0.4 ppt per year if the level of the Sea remained constant (Carpelan, 1961). Recent surveys report the salinity at about 40 ppt (Schroeder et al., 1993). Most of the salts dissolved in the Salton Sea are of riverine origin and therefore ionic ratios differ some*Contribution of the Scripps Institution of Oceanography, new series. 138
what from those in the ocean. Sea water is proportionately less in magnesium, potassium and chloride, more in calcium, bicarbonate, carbonate and sulphate, and roughly equal in sodium. Salinity is relatively uniform throughout the Salton Sea, the clearest exception being its southeastern part, close to the inputs from the New and Alamo Rivers, where in 1961 salinity varied between 3.5 and 32.1 ppt (Carpelan, 1961). Surface water temperatures in the Salton Sea vary between about 10°C and 36°C. At a depth of approximately 11 m, near the bottom, the temperature is only about 1 to 4 degrees lower, and no permanent thermocline was recorded (Carpelan, 1961), so the sea may be considered polymictic. Due to the abundant phytoplankton and frequent wind mixing, the upper part of the water column is often supersaturated with oxygen. However, this is not the case in deeper parts of the sea, particularly below 9 m where, especially during calm periods, large areas may become nearly or completely anoxic (Carpelan, 1961). The continued existence of the Salton Sea at its current level depends upon water input from the New River and the Alamo River, and upon irrigation runoff from the Coachella and Imperial Valleys. Water of the rivers, particularly of the former, carries huge amounts of industrial, agricultural and municipal waste from as far off as Mexico. The extent of this pollution is a major issue involving the governments of the United States and Mexico (Lindquist and La Rue, 1997). The local runoff also contains wastewater discharge from neighbouring settlements. As the ultimate sink for all inputs, the sea is vulnerable to the accumulation of contaminants. Since it is a wildlife refuge as well as a source of recreational fishing, the quality of its waters and biota should be regularly monitored, and it would be useful to find resident organisms that could be used for this purpose. Filter-feeding macrobenthic invertebrates can be conveniently used to monitor the paths and fates of pollutants entering various bodies of water. The most widely employed are bivalve molluscs, upon which the Mussel Watch Program has been based (Goldberg et al.,
Volume 36/Number 2/February 1998 1978). Other organisms are less frequently studied, although sometimes they are a better choice than mussels or oysters. Barnacles are smaller and more difficult to dissect than bivalves. Nonetheless, they have been employed in several monitoring programmes (Rainbow, 1995). In the mid-1960s, in a survey of backgroimd concentrations of 65Zn along the west coast of North America, it was noted that the sessile barnacle, Balanus amphitrite saltonensis Rogers, 1949 (= Balanus amphitrite Darwin, 1854) from the Salton Sea, contained an order of magnitude less 65Zn than a pedunculate barnacle, Pollicipes polymerus Sowerby, 1833 from La Jolla (0.86 mg 1-1 vs 6.4 mg 1-1, Alexander and Rowland, 1966). These are very different barnacles, and therefore it would be impossible to judge the significance of this isolated finding, but barnacles have since been found to be very good biomonitors of zinc, which accumulates in inorganic granules found in tissues of the alimentary canal (Walker et al., 1975; Walker and Foster, 1979). Recent papers suggest that the usefulness of barnacles as sentinels is not limited to zinc alone (Phillips and Rainbow, 1988; Powell and White, 1990; AI-Thaqafi and White, 1991; Rainbow et al., 1993)i The barnacle Balanus amphitrite Darwin, 1854 was introduced into the Salton Sea, apparently by US Navy seaplanes and equipment moved there from San Diego Bay early in the 1940s (Linsley and Carpelan, 1961). Since then the population has been isolated, and morphological differences found between it and coastal forms recognized by Rogers (1949) were corroborated by Henry and McLaughlin (1975) who also considered it a distinct subspecies. However, a recent study involving transplants has shown that the morphological characteristics separating the Salton Sea from the coastal form are ecophenotypic (Van Syoc, 1992). Therefore it is reasonable to assume that the differences in the heavy metal concentrations between the Salton Sea and coastal populations reflect environmental factors rather than genetic differences. The present paper presents preliminary results on the levels of several heavy metals in tissues of the B. amphitrite collected in central and southern parts of the Salton Sea. The species occurs gregariously on almost all hard substrata throughout the sea, including the shells of their dead, and specimens are easy to collect. Populations of the same species also inhabit bays and estuaries along the Pacific coast as well as in other temperate and tropical regions of the world. Such widespread occurrence facilitates access to reference material in monitoring programmes based on B. amphitrite. It seems an obvious choice as a biomonitor.
Materials and Methods The collections were made in June and July 1991, and at both times the barnacles were brooding well-
I UnitedStatesofAmerica
[ Fig. 1 Sampling stations in the Salton Sea and the coastal Pacific. MB, MissionBay; RH, Red Hill Marina; SC, Salton City.
developed egg masses. Two sites were chosen in the Salton Sea (Fig. 1). One was Martin Flora Park in Salton City, located almost in the middle of the western shore of the sea, far from the major agricultural and domestic water inputs. The barnacles were collected from submerged boulders at the tip of Martin Flora Park jetty, at a depth of about 10 cm. The other site was the Red Hill Marina on the southern shore, not far from the mouth of the Alamo River and channels discharging water with heavy organic loads. Specimens of the barnacle were collected at a depth of 10 to 15 cm from boulders and concrete blocks at the tip of the eastern breakwater sheltering the entry of a boat launching ramp. For comparison with a coastal population of the same species, a site was chosen at Carmel Point, Mission Bay, where barnacles were collected from concrete pilings at mean higher low water (Fig. 1). The animals were transported in a water-filled container chilled with ice to the laboratory, where they were frozen and kept at about - 6 ° C for a period no longer than 2 weeks. Immediately before analyses, five animals from each sample were thawed and their bodies (thorax+prosoma) removed with glass needles and pooled for further investigation. Egg masses were obtained in the same way. Each sample was placed in a Teflon vial, dried for 48 h at 80°C, and weighed. Each was then wet-ashed in distilled concentrated nitric acid. After completely dissolved, each was evaporated to dryness and the residue redissolved in 3% distilled nitric acid. The amount of acid was calculated to dilute each sample 10 000 times by weight. All the samples were spiked with 115In at a concentration of 100 ppb as an internal standard. 139
Marine Pollution Bulletin The following elements were chosen for analyses: iron, copper, zinc, cadmium, tin, mercury and lead. Except for iron, these metals are considered to pose a threat to marine life in California's coastal waters, and they are not only being monitored but their sources are being curtailed. Compounds containing copper and mercury are found in some pesticides used in agricultural and water-management practices. Use of tributyltin (TBT) as well as copper as antifouling agents has raised deep environmental concerns. Thus monitoring o f trace elements in aquatic environments is advocated (Goldberg et al., 1978; Rainbow, 1987; Powell and White, 1990), although their mere presence there is o f less concern than it was several years ago (GESAMP, 1990). While significant influxes of any of these metals into the Salton Sea have yet to be detected, a base line against which future trends in abundances can be judged, is needed. Semi-quantitative analyses were performed at the SIO Analytical Facility on a VG Elemental PlasmaQuad inductively coupled plasma source mass spectrometer (ICP-MS) working in peak count mode. The bodies and the egg masses were analysed separately. Such an approach is widely employed (Walker et al., 1975; Walker and Foster, 1979; Powell and White, 1990). The body of a barnacle accumulates heavy metals throughout its entire life span, while its egg mass does so for only a few weeks between the outset of oogenesis and brooding (see Walker and Foster, 1979 for details). Thus the former serves as a monitor of long-term and the latter as a monitor of short-term accumulations.
Results At Mission Bay the barnacles were less numerous and relatively more difficult to locate than in the Salton Sea. The dry weights of the bodies and egg masses of individuals collected there were approximately four times those o f specimens from the other sites (Table I). Apparently, while recruitment was low, the conditions for growth and longevity for this species were best in the bay. For this reason, the Mission Bay station was chosen as the reference point. For every investigated element, a relative accumulation coefficient was calcu-
TABLE 1
Average dry weight in milligrams (+SD) of the bodies and egg masses of Balanus amphitrite from the Salton Sea and the coastal Pacific. Coasthl Pacific Mission Bay Bodies Egg masses
8.4 (2.4) 5.1 (2.6)
Salton Sea SaltonCity Red Hill 2.7 (1.4) 1.2 (0.5)
lated by dividing the element level in body tissues and egg masses at a given station in the Salton Sea by the corresponding level in the material collected from Mission Bay. The highest concentrations of iron were recorded from the Red Hill Marina. They were up to twice those from the other stations (Table 2, Figs 2 and 3). The differences between Mission Bay and Salton City were less marked, but all of them were significant at F2,t8 =42.2, p < 0.01 (bodies), and F2,t8 =44.3, p < 0.0! (egg masses). The bodies of the barnacles inhabiting Mission Bay accumulated up to two orders of magnitude more copper than those from the Salton Sea (Table 2, Figs 2 and 3). These differences were significant at F2,t8 = 55.1, p<0.01 for bodies and F2,t8=6.2, p < 0 . 0 1 for egg masses. No significant difference was found between the Salton City and Red Hill Marina stations. Zinc, like copper, also reached its highest concentrations in the Mission Bay specimens. In the bodies they were about 30 times higher than those in the Salton City barnacles and over 60 times higher than those in the Red Hill Marina sample. The differences between the concentrations in egg masses were smaller (Table 2, Figs 2 and 3). All of them were significant at F2,t8=36.7, p<0.01 (bodies) and F2,18=4.6, p<0.01 (egg masses). Again, no significant differences were found between the two Salton Sea stations. The levels of cadmium from Mission Bay specimens were, as with copper and zinc, significantly higher than those from the Salton Sea animals (Table 2, Figs 2 and 3). The differences between the body concentrations were significant at F2,~8 = 84.7, p < 0.01, and between the egg masses at F2,~8 = 6.2, p < 0.01). Again, no significant difference showed up within the Saiton Sea.
TABLE 2
Concentration in parts per million (+SD) of heavy metals in the bodies and egg masses of Balanus amphitrite. Mission Bay Bodies Egg masses Fe Cu Zn Cd Sn Hg Pb 140
720 (140) 3750 (1560) 37900 (19400) 58 (16) 67 (52) 11 (5) 14 (4)
1150 (220) 140 (60) 1400 (1300) 21 (14) 21 (17) 7 (3) 5 (2)
Salton City Bodies Egg masses 450 (90) 140 (60) 1200 (1200) 14 (4) 49 (48) 13 (9) 15 (4)
2.9 (1.6) 0.8 (0.5)
1490 (180) 80 (40) 280 (240) 7 (4) 214 (119) 9 (6) II (3)
Red Hill Marina Bodies Egg masses 1150 (240) 40 (20) 620 (500) 6 (3) 27 (21) ll (2) 5 (1)
2270 (420) 90 (40) 510 (500) 9 (6) 60 (54) 9 (4) 21 (5)
Volume 36/Number 2/FebruaU 1998
I-Z c,,)
The concentrations of mercury were fairly uniform in the investigated animals (Table 2, Figs 2 and 3). The differences between the sampling stations were not significant in the egg masses or in the bodies. The population at the Red Hill Marina had the highest levels of lead in the egg masses and the lowest in the bodies (Table 2, Fig. 3). The concentrations of this metal in the bodies from the Mission Bay population were not significantly different from those recorded from Salton City. All the other differences were significant at Fa,18= 19.2, p < 0.01 (bodies) and F2,18=43.9, p<0.01 (egg masses).
Body lc
i.i. u.i 0
Egg Mass Mission Bay level
z
.J Z ¢J (J
0.1
UJ
:i ~
0.01
W.I
Discussion
0.001 ,
Fe
Cu
Zn
Cd
Sn
Hg
Pb
ELEMENT
Fig. 2 Red Hill Marina sampling station. Relative accumulation coefficientof heavy metals in Balanus amphitrite. See text for further explanation.
Tin reached the highest concentration in the egg masses of barnacles from the Salton City population, with those from Mission Bay being more than 10 times lower and those from the Red Hill Marina more than three times lower (Table 2, Figs 2 and 3). The Salton City station was the only one differing significantly from the others (F2,1s=16.7, p<0.01). There were no significant differences between tin concentrations in the bodies. The barnacles from the Salton Sea accumulated more tin in their egg masses than in the bodies. In the specimens from the coastal Pacific this relationship was the reverse, with a much higher level of tin in the bodies (Table 2, Figs 2 and 3).
100: I-Z
Body m
U. U. UJ 0
Egg Mass 1G
Z
2p= 1
< W
0.1
.J W.I IIC 0.01 - -
Fe
Cu
Zn
Cd
Sn
Hg
Pb
ELEMENT
Fig. 3 SaltonCitysamplingstation. Relativeaccumulationcoefficient of heavy metals in Balanus amphitrite. See text for further explanation.
Most water entering the Salton Sea is polluted. Evaporation exceeds runoff, and since there is no flushing the salinity has been increasing. Therefore one might expect the heavy load of entering contaminants to accumulate in the water, sediments and organisms. Thus high levels of trace elements, heavy metals among them, would be expected. Our null hypothesis was that B. amphitrite from the Salton Sea would contain relatively large amounts of heavy metals, compared with the same species from the coastal Pacific. Mission Bay is at least partially flushed by tides twice a day, a phenomenon that should dilute contaminants available to the organisms. The data presented here challenge this assumption. While the differences in metal levels between the coastal ocean and the Salton Sea were smaller than expected, in most cases the levels at Mission Bay were higher than at the Salton Sea. This was especially noticeable in the case of lighter metals: copper, zinc and cadmium (Figs 2 and
3). Such results suggest either that so far the Salton Sea has not been significantly polluted with material containing heavy metals or that if it has, they are being transferred from the water column to the sediments. The substantial load of organic matter that the sea receives may not only be involved in this transfer, but it also could influence heavy metal accumulations in the barnacles. For example, intensive decomposition of organic matter periodically causes anaerobic conditions to develop over large areas of the Salton Sea (Whitney, 1961). Hydrogen sulphide originating in such an environment reacts with heavy metals dissolved in water and precipitates them in the form of sulphides before they can be sequestered by filter-feeders (G. Arrhenius, pers. comm.). It would be instructive to analyse sediments cored from the Salton Sea floor. Bodies generally accumulated greater amounts of heavy metals than the egg masses did (Table 2). However, there were some exceptions. The greater amounts of iron in the eggs than in the bodies could be explained by the high demand for this element in the rapidly developing embryos. More interesting, but more 141
Marine Pollution Bulletin difficult to explain, were the exceptions in other metals. Both B. amphitrite populations in the Salton Sea had much more tin in the egg masses than in their bodies. This was independent of the absolute concentration values, which at the Salton City station were considerably higher than at the Red Hill Marina. At the Red Hill Marina the egg masses also accumulated more copper and lead than the bodies did (Table 2). It is difficult to suggest a cause for such a reversal of metal concentrations. In our opinion, it is probably linked with the nature of Salton Sea pollution. The whole sea, and especially its southern part, receives highly polluted waters. Organic matter may react with metals, forming organometallic compounds which, sequestered by the barnacles, are partitioned into the lipid-rich egg masses (P. Rainbow, pers. comm.). Further studies are needed to test this explanation. The ratio of body-to-egg-mass metal concentrations was always higher in the barnacles living in Mission Bay. The difference may simply be due to the age of the tissues involved; the older the tissue the greater the accumulate of heavy metals. The difference between the ages of bodies and egg masses was greater in animals from Mission Bay than in those from other study sites, and this may also account for the difference in accumulation levels. But, as Walker and Foster (1979) observed, metal concentrations in the body level off as growth slows down. Since the specimens collected from Mission Bay were approaching maximum size, their ability to protect ovaries and eggs by sequestering metals in the body may have been diminished. On the other hand, there are periods in which Mission Bay is well flushed, such as during high runoff and spring tides. The effects of such flushing have been described by Walker and Foster (1979). If the eggs were developing at such times, they would be expected to have lower heavy metal accumulations. Further field and laboratory studies should elucidate this problem. Balanus amphitrite has played an important role in projects involving biomonitoring of trace metals in the coastal waters of Hong Kong, South China Sea (Phillips and Rainbow, 1988; Chan et al., 1990; Rainbow et al., 1993). Compared with the individuals analysed during these projects, those from the Mission Bay attained greater weight, while those from the Salton Sea were smaller (Table 1, Phillips and Rainbow, 1988; Rainbow et al., 1993). Of the elements considered in this paper, copper, zinc, cadmium and lead were also studied on the other side of the Pacific. Although the projects mentioned did not take egg masses into consideration and analytical methods were different, some comparisons can still be made. The barnacles from Mission Bay have apparently accumulated comparatively large amounts of the trace metals in question. Zinc and cadmium were much higher than in the most metal-rich parts of Hong Kong. Copper was recorded at levels similar to those of the 142
most heavily polluted areas there. The amounts of lead in the bay were similar to those found in Hong Kong at sites with moderate bioavailability (Phillips and Rainbow, 1988) (compare also Table 2 in this paper with Table 10 in Rainbow et al., 1993). The bioavailabilities of the trace metals in the Salton Sea were considerably lower than those in the western Pacific. Their levels measured in the barnacles from the sea were close to the lowest values found in specimens from the coastal waters of Hong Kong and mainland China (compare Table 2 in this paper with Table 10 in Rainbow et al., 1993). Notwithstanding the important research just mentioned and other work on B. amphitrite (see Rainbow, 1987 for literature review), the most extensive studies on heavy metal accumulation in barnacles have been done on Semibalanus balanoides (L.) from the Irish Sea (Ireland, 1974; Walker et al., 1975; Walker and Foster, 1979; Rainbow, 1987; A1-Thaqafi and White, 1991). There are no studies comparing the two species, though there are areas where they co-occur. Iron, copper and zinc were studied in the Irish Sea. As in our research, the bodies and egg masses were analysed separately. Bodies of S. balanoides from the Menai Strait, regarded as slightly polluted by heavy metals, showed levels similar to those found in B. amphitrite in Mission Bay. Only in the case of copper, levels in the latter were higher (cf. Rainbow, 1987). Barnacles from the Salton Sea showed generally lower levels of the investigated elements. Salton Sea barnacle egg masses accumulated smaller amounts of zinc, and amounts of copper and iron approximately equal to those from the Irish Sea specimens. The egg masses from Mission Bay had an iron level similar to that found in the Irish Sea egg masses; the other metals were far less abundant than in those from the Irish Sea (Walker and Foster, 1979). The results of this preliminary study confirm that barnacles are an excellent tool for monitoring heavy metals in aquatic biota. Their gregarious occurrence makes it easy to collect enough material. This is especially important in the Salton Sea, where other macrobenthic filter-feeders are either very small or scarce. The findings of this research project suggest that the Salton Sea is not yet heavily polluted by heavy metals derived from industrial, agricultural or domestic wastewater. However, it is presently receiving a big load of organic matter, including raw sewage. The influence of this factor upon the heavy metal concentrations in the water column, and much less accumulation in barnacles, has not been well studied, and it therefore needs fuller understanding. The authorsthank RonaldLaBordeof the SIO AnalyticalFacilityfor his help with the ICP-MS analyses,and an anonymousreviewerfor valuable comments. The research was done during Wojciech Fialkowski's visit to the SIO on a Fulbright Fellowship.
Volume 36/Number 2/Februa~ 1998 Alexander, G. V. and Rowland, R. H. (1966) Estimation of Zinc-65 background levels for marine coastal waters. Nature 210, 155157. Al-Thaqafi, K. and White, K. N. (1991) Effect of shore position and environmental metal levels on body metal burdens in the barnacle Elminius modestus. Environmental Pollution 69, 89-104. Carpelan, L. H. (1961) Physical and chemical characteristics. In The Ecology of the Salton Sea, California, in Relation to the Sportfishery, ed. B. W. Walker, pp. 17-32. State of California Department of Fish and Game, Fish Bulletin, no. 113. Chan, H. M., Rainbow, P. S. and Phillips, D. J. H. (1990) Barnacles and mussels as monitors of trace metal bio-availability in Hong Kong waters. In Proceedings of the Second International Marine Biological Workshop: The Marine Flora and Fauna of Hong Kong and Southern China, Hong Kong, 1986, ed. B. Morton, pp. 12391268. Hong Kong University Press, Hong Kong. GESAMP (1990) The state of marine environment. UNEP Regional Seas Reports and Studies 115: i-vii, 1-111. Goldberg, E. D., Bowen, V. T., Farrington, J. W., Harvey, G., Martin, J. H., Parker, P. L., Risenbrough, R. W., Robertson, W., Schneider, E. and Gamble, E. (1978) The mussel watch. Environmental Conservation 5, 101-125. Henry, D. P. and McLaughlin, P. A. (1975) The barnacles of the Balanus amphitrite complex (Cirripedia Thoracica). Zoological Verhandelingen 141, 203-212. Ireland, M. P. (1974) Variations in the zinc, copper, manganese and lead content of Balanus balanoides in Cardigan Bay, Wales. Environmental Pollution 7, 65-75. Lindquist, D. and La Rue, S. (1997) New River, new hope. The San Diego Union-Tribune 6, I, 14. Linsley, R. H. and Carpelan, L. H. (1961) Invertebrate fauna. In The Ecology of the Salton Sea, California, in Relation to the Sport.fishery, ed. B. W. Walker, pp. 105-151. State of California Department of Fish and Game, Fish Bulletin no. 113. Phillips, D. J. H. and Rainbow, P. S. (1988) Barnacles and mussels as biomonitors of trace elements: a comparative study. Marine Ecology Progress Series 49, 83-93. Powell, M. I. and White, K. N. (1990) Hea~,y metal accumulation by barnacles and its implications for their use as biological monitors. Marine Environmental Research 30, 91-118.
Rainbow, P. S. (1987) Heavy metals in barnacles. In Barnacle Biology, ed. A. J. Southward, pp. 405417. A. A. Balkema, Rotterdam. Rainbow, P. S. (1995) Biornonitoring of heavy metal availability in the marine environment. Marine Pollution Bulletin 31, 183192. Rainbow, P. S., Huang, Z. G., Yan, S. K. and Smith, B. D. (1993) Barnacles as biomonitors of trace metals in the coastal waters near Xiamen, China. Asian Marine Biology 10, 109-121. Rogers, F. L. (1949) Three new subspecies of Balanus amphitrite from California. Journal of Entomology and Zoology, Claremont 41, 3-12. Schroeder, R. A., Rivera, M., Redfield, J. B., Densmore, J. N., Michel, R. L., Norton, D. R., Audet, D. J., Setmire, J. G. and Goodbred, S. L. (1993) Physical, chemical and biological data for detailed study of irrigation drainage in the Salton Sea area, California 1988-90. US Geological Survey open-file report 93-83. US Geological Survey Books and Open-File Reports Section, Denver. Setmire, J. G., Schroeder, R. A., Densmore, J. N., Goodbred, S. L., Audet, D. J. and Radke W. R. (1993) Detailed study of water quality, bottom sediment, and biota associated with irrigation drainage in the Salton Sea area, California, 1988-90. Water Resources Investigations Report 93~4014. US Geological Survey Earth Science Information Center, Denver. Van Syoc, R. J. (1992) Living and fossil populations of a western Atlantic barnacle, Balanus subalbidus Henry, 1974, in the Gulf of California region. Proceedings of the San Diego Society of Natural History 12, 1-7. Walker, G. and Foster, P. (1979) Seasonal variation of zinc in the barnacle, Balanus balanoides (L.) maintained on a raft in the Menai Strait. Marine Environmental Research 2, 209-222. Walker, G., Rainbow, P. S., Foster, P. and Crisp, D. J. (1975) Barnacles: possible indicators of zinc pollution? Marine Biology 30, 57-65. Whitney, R. R. (1961) The Bairdiella icistius (Jordan et Gilbert). In The Ecology of the Salton Sea, California, in Relation to the Sportfishery, ed. B. W. Walker, pp. 105-151. State of California Department of Fish and Game, Fish Bulletin no. 113. Young, D. R. (1970) The distribution of cesium, rubidium and potassium in the quasi marine ecosystem of the Salton Sea. SIO Dissertation. University of California at San Diego, San Diego.
143
Pergamon PII: S0025-326X(97)00100-8
~) 1998 Elsevier Science l.td All rights reserved. Printed in Greal Britain 0025-326X/98 $19.[)1)+0.00
A Pilot Study of Heavy Metal Accumulations in a Barnacle from the Salton Sea, Southern California* WOJCIECH F I A L K O W S K I t and W.ILLIAM A. NEWMAN~
tJagiellonian University, Department of Hydrobiology, ul. Oleandry 2a, 30-063 Krakow, Poland ~University of California at San Diego, Scripps Institution of Oceanography, La Jolla, CA 92093-0202, USA
Accumulations of Fe, Cu, Zn, Cd, Sn, Hg and Pb in body tissues and egg masses of Balanus amphitrite were measured with an inductively coupled plasma source mass spectrometer (ICP-MS). Barnacles proved to be a good choice as a sentinel species for monitoring of heavy metals. A comparison of their levels in the animals inhabiting the Salton Sea with those from coastal waters of the Pacific Ocean showed that the sea, contrary to expectations, has not been severely contaminated by heavy metals. The accumulations of the metals in barnacle bodies and eggs varied markedly between the stations but appeared least where organic pollution was highest. © 1998 Elsevier Science Ltd. All rights reserved. Keywords: Balanus amphitrite; bioaccumulation; biomonitoring; Pacific Ocean; Salton Sea; trace metals.
The Salton Sea in Southern California, whose surface is over 70_m below sea level, is the most recent body of water in this basin. The present 'sea' came into being in 1907 when a man-made irrigation canal from the Colorado River broke and flooded the depression that extends 82 m below sea level. Nearly all the water entering the sea originates in the Colorado River (Setmire et al., 1993), so the ionic composition of the two bodies is very similar. Measurements made shortly after the sea was formed indicated that its salinity (3.6 ppt) was greater than in the Colorado River (0.7 ppt) due to the dissolution of salts from deposits left over from earlier instances of flooding (Young, 1970). In 1954-1965 the salinity of the Salton Sea was about 33 ppt. Predictions made at that time estimated that it would increase at a rate of approximately 0.4 ppt per year if the level of the Sea remained constant (Carpelan, 1961). Recent surveys report the salinity at about 40 ppt (Schroeder et al., 1993). Most of the salts dissolved in the Salton Sea are of riverine origin and therefore ionic ratios differ some*Contribution of the Scripps Institution of Oceanography, new series. 138
what from those in the ocean. Sea water is proportionately less in magnesium, potassium and chloride, more in calcium, bicarbonate, carbonate and sulphate, and roughly equal in sodium. Salinity is relatively uniform throughout the Salton Sea, the clearest exception being its southeastern part, close to the inputs from the New and Alamo Rivers, where in 1961 salinity varied between 3.5 and 32.1 ppt (Carpelan, 1961). Surface water temperatures in the Salton Sea vary between about 10°C and 36°C. At a depth of approximately 11 m, near the bottom, the temperature is only about 1 to 4 degrees lower, and no permanent thermocline was recorded (Carpelan, 1961), so the sea may be considered polymictic. Due to the abundant phytoplankton and frequent wind mixing, the upper part of the water column is often supersaturated with oxygen. However, this is not the case in deeper parts of the sea, particularly below 9 m where, especially during calm periods, large areas may become nearly or completely anoxic (Carpelan, 1961). The continued existence of the Salton Sea at its current level depends upon water input from the New River and the Alamo River, and upon irrigation runoff from the Coachella and Imperial Valleys. Water of the rivers, particularly of the former, carries huge amounts of industrial, agricultural and municipal waste from as far off as Mexico. The extent of this pollution is a major issue involving the governments of the United States and Mexico (Lindquist and La Rue, 1997). The local runoff also contains wastewater discharge from neighbouring settlements. As the ultimate sink for all inputs, the sea is vulnerable to the accumulation of contaminants. Since it is a wildlife refuge as well as a source of recreational fishing, the quality of its waters and biota should be regularly monitored, and it would be useful to find resident organisms that could be used for this purpose. Filter-feeding macrobenthic invertebrates can be conveniently used to monitor the paths and fates of pollutants entering various bodies of water. The most widely employed are bivalve molluscs, upon which the Mussel Watch Program has been based (Goldberg et al.,
Volume 36/Number 2/February 1998 1978). Other organisms are less frequently studied, although sometimes they are a better choice than mussels or oysters. Barnacles are smaller and more difficult to dissect than bivalves. Nonetheless, they have been employed in several monitoring programmes (Rainbow, 1995). In the mid-1960s, in a survey of backgroimd concentrations of 65Zn along the west coast of North America, it was noted that the sessile barnacle, Balanus amphitrite saltonensis Rogers, 1949 (= Balanus amphitrite Darwin, 1854) from the Salton Sea, contained an order of magnitude less 65Zn than a pedunculate barnacle, Pollicipes polymerus Sowerby, 1833 from La Jolla (0.86 mg 1-1 vs 6.4 mg 1-1, Alexander and Rowland, 1966). These are very different barnacles, and therefore it would be impossible to judge the significance of this isolated finding, but barnacles have since been found to be very good biomonitors of zinc, which accumulates in inorganic granules found in tissues of the alimentary canal (Walker et al., 1975; Walker and Foster, 1979). Recent papers suggest that the usefulness of barnacles as sentinels is not limited to zinc alone (Phillips and Rainbow, 1988; Powell and White, 1990; AI-Thaqafi and White, 1991; Rainbow et al., 1993)i The barnacle Balanus amphitrite Darwin, 1854 was introduced into the Salton Sea, apparently by US Navy seaplanes and equipment moved there from San Diego Bay early in the 1940s (Linsley and Carpelan, 1961). Since then the population has been isolated, and morphological differences found between it and coastal forms recognized by Rogers (1949) were corroborated by Henry and McLaughlin (1975) who also considered it a distinct subspecies. However, a recent study involving transplants has shown that the morphological characteristics separating the Salton Sea from the coastal form are ecophenotypic (Van Syoc, 1992). Therefore it is reasonable to assume that the differences in the heavy metal concentrations between the Salton Sea and coastal populations reflect environmental factors rather than genetic differences. The present paper presents preliminary results on the levels of several heavy metals in tissues of the B. amphitrite collected in central and southern parts of the Salton Sea. The species occurs gregariously on almost all hard substrata throughout the sea, including the shells of their dead, and specimens are easy to collect. Populations of the same species also inhabit bays and estuaries along the Pacific coast as well as in other temperate and tropical regions of the world. Such widespread occurrence facilitates access to reference material in monitoring programmes based on B. amphitrite. It seems an obvious choice as a biomonitor.
Materials and Methods The collections were made in June and July 1991, and at both times the barnacles were brooding well-
I UnitedStatesofAmerica
[ Fig. 1 Sampling stations in the Salton Sea and the coastal Pacific. MB, MissionBay; RH, Red Hill Marina; SC, Salton City.
developed egg masses. Two sites were chosen in the Salton Sea (Fig. 1). One was Martin Flora Park in Salton City, located almost in the middle of the western shore of the sea, far from the major agricultural and domestic water inputs. The barnacles were collected from submerged boulders at the tip of Martin Flora Park jetty, at a depth of about 10 cm. The other site was the Red Hill Marina on the southern shore, not far from the mouth of the Alamo River and channels discharging water with heavy organic loads. Specimens of the barnacle were collected at a depth of 10 to 15 cm from boulders and concrete blocks at the tip of the eastern breakwater sheltering the entry of a boat launching ramp. For comparison with a coastal population of the same species, a site was chosen at Carmel Point, Mission Bay, where barnacles were collected from concrete pilings at mean higher low water (Fig. 1). The animals were transported in a water-filled container chilled with ice to the laboratory, where they were frozen and kept at about - 6 ° C for a period no longer than 2 weeks. Immediately before analyses, five animals from each sample were thawed and their bodies (thorax+prosoma) removed with glass needles and pooled for further investigation. Egg masses were obtained in the same way. Each sample was placed in a Teflon vial, dried for 48 h at 80°C, and weighed. Each was then wet-ashed in distilled concentrated nitric acid. After completely dissolved, each was evaporated to dryness and the residue redissolved in 3% distilled nitric acid. The amount of acid was calculated to dilute each sample 10 000 times by weight. All the samples were spiked with 115In at a concentration of 100 ppb as an internal standard. 139
Marine Pollution Bulletin The following elements were chosen for analyses: iron, copper, zinc, cadmium, tin, mercury and lead. Except for iron, these metals are considered to pose a threat to marine life in California's coastal waters, and they are not only being monitored but their sources are being curtailed. Compounds containing copper and mercury are found in some pesticides used in agricultural and water-management practices. Use of tributyltin (TBT) as well as copper as antifouling agents has raised deep environmental concerns. Thus monitoring o f trace elements in aquatic environments is advocated (Goldberg et al., 1978; Rainbow, 1987; Powell and White, 1990), although their mere presence there is o f less concern than it was several years ago (GESAMP, 1990). While significant influxes of any of these metals into the Salton Sea have yet to be detected, a base line against which future trends in abundances can be judged, is needed. Semi-quantitative analyses were performed at the SIO Analytical Facility on a VG Elemental PlasmaQuad inductively coupled plasma source mass spectrometer (ICP-MS) working in peak count mode. The bodies and the egg masses were analysed separately. Such an approach is widely employed (Walker et al., 1975; Walker and Foster, 1979; Powell and White, 1990). The body of a barnacle accumulates heavy metals throughout its entire life span, while its egg mass does so for only a few weeks between the outset of oogenesis and brooding (see Walker and Foster, 1979 for details). Thus the former serves as a monitor of long-term and the latter as a monitor of short-term accumulations.
Results At Mission Bay the barnacles were less numerous and relatively more difficult to locate than in the Salton Sea. The dry weights of the bodies and egg masses of individuals collected there were approximately four times those o f specimens from the other sites (Table I). Apparently, while recruitment was low, the conditions for growth and longevity for this species were best in the bay. For this reason, the Mission Bay station was chosen as the reference point. For every investigated element, a relative accumulation coefficient was calcu-
TABLE 1
Average dry weight in milligrams (+SD) of the bodies and egg masses of Balanus amphitrite from the Salton Sea and the coastal Pacific. Coasthl Pacific Mission Bay Bodies Egg masses
8.4 (2.4) 5.1 (2.6)
Salton Sea SaltonCity Red Hill 2.7 (1.4) 1.2 (0.5)
lated by dividing the element level in body tissues and egg masses at a given station in the Salton Sea by the corresponding level in the material collected from Mission Bay. The highest concentrations of iron were recorded from the Red Hill Marina. They were up to twice those from the other stations (Table 2, Figs 2 and 3). The differences between Mission Bay and Salton City were less marked, but all of them were significant at F2,t8 =42.2, p < 0.01 (bodies), and F2,t8 =44.3, p < 0.0! (egg masses). The bodies of the barnacles inhabiting Mission Bay accumulated up to two orders of magnitude more copper than those from the Salton Sea (Table 2, Figs 2 and 3). These differences were significant at F2,t8 = 55.1, p<0.01 for bodies and F2,t8=6.2, p < 0 . 0 1 for egg masses. No significant difference was found between the Salton City and Red Hill Marina stations. Zinc, like copper, also reached its highest concentrations in the Mission Bay specimens. In the bodies they were about 30 times higher than those in the Salton City barnacles and over 60 times higher than those in the Red Hill Marina sample. The differences between the concentrations in egg masses were smaller (Table 2, Figs 2 and 3). All of them were significant at F2,t8=36.7, p<0.01 (bodies) and F2,18=4.6, p<0.01 (egg masses). Again, no significant differences were found between the two Salton Sea stations. The levels of cadmium from Mission Bay specimens were, as with copper and zinc, significantly higher than those from the Salton Sea animals (Table 2, Figs 2 and 3). The differences between the body concentrations were significant at F2,~8 = 84.7, p < 0.01, and between the egg masses at F2,~8 = 6.2, p < 0.01). Again, no significant difference showed up within the Saiton Sea.
TABLE 2
Concentration in parts per million (+SD) of heavy metals in the bodies and egg masses of Balanus amphitrite. Mission Bay Bodies Egg masses Fe Cu Zn Cd Sn Hg Pb 140
720 (140) 3750 (1560) 37900 (19400) 58 (16) 67 (52) 11 (5) 14 (4)
1150 (220) 140 (60) 1400 (1300) 21 (14) 21 (17) 7 (3) 5 (2)
Salton City Bodies Egg masses 450 (90) 140 (60) 1200 (1200) 14 (4) 49 (48) 13 (9) 15 (4)
2.9 (1.6) 0.8 (0.5)
1490 (180) 80 (40) 280 (240) 7 (4) 214 (119) 9 (6) II (3)
Red Hill Marina Bodies Egg masses 1150 (240) 40 (20) 620 (500) 6 (3) 27 (21) ll (2) 5 (1)
2270 (420) 90 (40) 510 (500) 9 (6) 60 (54) 9 (4) 21 (5)
Volume 36/Number 2/FebruaU 1998
I-Z c,,)
The concentrations of mercury were fairly uniform in the investigated animals (Table 2, Figs 2 and 3). The differences between the sampling stations were not significant in the egg masses or in the bodies. The population at the Red Hill Marina had the highest levels of lead in the egg masses and the lowest in the bodies (Table 2, Fig. 3). The concentrations of this metal in the bodies from the Mission Bay population were not significantly different from those recorded from Salton City. All the other differences were significant at Fa,18= 19.2, p < 0.01 (bodies) and F2,18=43.9, p<0.01 (egg masses).
Body lc
i.i. u.i 0
Egg Mass Mission Bay level
z
.J Z ¢J (J
0.1
UJ
:i ~
0.01
W.I
Discussion
0.001 ,
Fe
Cu
Zn
Cd
Sn
Hg
Pb
ELEMENT
Fig. 2 Red Hill Marina sampling station. Relative accumulation coefficientof heavy metals in Balanus amphitrite. See text for further explanation.
Tin reached the highest concentration in the egg masses of barnacles from the Salton City population, with those from Mission Bay being more than 10 times lower and those from the Red Hill Marina more than three times lower (Table 2, Figs 2 and 3). The Salton City station was the only one differing significantly from the others (F2,1s=16.7, p<0.01). There were no significant differences between tin concentrations in the bodies. The barnacles from the Salton Sea accumulated more tin in their egg masses than in the bodies. In the specimens from the coastal Pacific this relationship was the reverse, with a much higher level of tin in the bodies (Table 2, Figs 2 and 3).
100: I-Z
Body m
U. U. UJ 0
Egg Mass 1G
Z
2p= 1
< W
0.1
.J W.I IIC 0.01 - -
Fe
Cu
Zn
Cd
Sn
Hg
Pb
ELEMENT
Fig. 3 SaltonCitysamplingstation. Relativeaccumulationcoefficient of heavy metals in Balanus amphitrite. See text for further explanation.
Most water entering the Salton Sea is polluted. Evaporation exceeds runoff, and since there is no flushing the salinity has been increasing. Therefore one might expect the heavy load of entering contaminants to accumulate in the water, sediments and organisms. Thus high levels of trace elements, heavy metals among them, would be expected. Our null hypothesis was that B. amphitrite from the Salton Sea would contain relatively large amounts of heavy metals, compared with the same species from the coastal Pacific. Mission Bay is at least partially flushed by tides twice a day, a phenomenon that should dilute contaminants available to the organisms. The data presented here challenge this assumption. While the differences in metal levels between the coastal ocean and the Salton Sea were smaller than expected, in most cases the levels at Mission Bay were higher than at the Salton Sea. This was especially noticeable in the case of lighter metals: copper, zinc and cadmium (Figs 2 and
3). Such results suggest either that so far the Salton Sea has not been significantly polluted with material containing heavy metals or that if it has, they are being transferred from the water column to the sediments. The substantial load of organic matter that the sea receives may not only be involved in this transfer, but it also could influence heavy metal accumulations in the barnacles. For example, intensive decomposition of organic matter periodically causes anaerobic conditions to develop over large areas of the Salton Sea (Whitney, 1961). Hydrogen sulphide originating in such an environment reacts with heavy metals dissolved in water and precipitates them in the form of sulphides before they can be sequestered by filter-feeders (G. Arrhenius, pers. comm.). It would be instructive to analyse sediments cored from the Salton Sea floor. Bodies generally accumulated greater amounts of heavy metals than the egg masses did (Table 2). However, there were some exceptions. The greater amounts of iron in the eggs than in the bodies could be explained by the high demand for this element in the rapidly developing embryos. More interesting, but more 141
Marine Pollution Bulletin difficult to explain, were the exceptions in other metals. Both B. amphitrite populations in the Salton Sea had much more tin in the egg masses than in their bodies. This was independent of the absolute concentration values, which at the Salton City station were considerably higher than at the Red Hill Marina. At the Red Hill Marina the egg masses also accumulated more copper and lead than the bodies did (Table 2). It is difficult to suggest a cause for such a reversal of metal concentrations. In our opinion, it is probably linked with the nature of Salton Sea pollution. The whole sea, and especially its southern part, receives highly polluted waters. Organic matter may react with metals, forming organometallic compounds which, sequestered by the barnacles, are partitioned into the lipid-rich egg masses (P. Rainbow, pers. comm.). Further studies are needed to test this explanation. The ratio of body-to-egg-mass metal concentrations was always higher in the barnacles living in Mission Bay. The difference may simply be due to the age of the tissues involved; the older the tissue the greater the accumulate of heavy metals. The difference between the ages of bodies and egg masses was greater in animals from Mission Bay than in those from other study sites, and this may also account for the difference in accumulation levels. But, as Walker and Foster (1979) observed, metal concentrations in the body level off as growth slows down. Since the specimens collected from Mission Bay were approaching maximum size, their ability to protect ovaries and eggs by sequestering metals in the body may have been diminished. On the other hand, there are periods in which Mission Bay is well flushed, such as during high runoff and spring tides. The effects of such flushing have been described by Walker and Foster (1979). If the eggs were developing at such times, they would be expected to have lower heavy metal accumulations. Further field and laboratory studies should elucidate this problem. Balanus amphitrite has played an important role in projects involving biomonitoring of trace metals in the coastal waters of Hong Kong, South China Sea (Phillips and Rainbow, 1988; Chan et al., 1990; Rainbow et al., 1993). Compared with the individuals analysed during these projects, those from the Mission Bay attained greater weight, while those from the Salton Sea were smaller (Table 1, Phillips and Rainbow, 1988; Rainbow et al., 1993). Of the elements considered in this paper, copper, zinc, cadmium and lead were also studied on the other side of the Pacific. Although the projects mentioned did not take egg masses into consideration and analytical methods were different, some comparisons can still be made. The barnacles from Mission Bay have apparently accumulated comparatively large amounts of the trace metals in question. Zinc and cadmium were much higher than in the most metal-rich parts of Hong Kong. Copper was recorded at levels similar to those of the 142
most heavily polluted areas there. The amounts of lead in the bay were similar to those found in Hong Kong at sites with moderate bioavailability (Phillips and Rainbow, 1988) (compare also Table 2 in this paper with Table 10 in Rainbow et al., 1993). The bioavailabilities of the trace metals in the Salton Sea were considerably lower than those in the western Pacific. Their levels measured in the barnacles from the sea were close to the lowest values found in specimens from the coastal waters of Hong Kong and mainland China (compare Table 2 in this paper with Table 10 in Rainbow et al., 1993). Notwithstanding the important research just mentioned and other work on B. amphitrite (see Rainbow, 1987 for literature review), the most extensive studies on heavy metal accumulation in barnacles have been done on Semibalanus balanoides (L.) from the Irish Sea (Ireland, 1974; Walker et al., 1975; Walker and Foster, 1979; Rainbow, 1987; A1-Thaqafi and White, 1991). There are no studies comparing the two species, though there are areas where they co-occur. Iron, copper and zinc were studied in the Irish Sea. As in our research, the bodies and egg masses were analysed separately. Bodies of S. balanoides from the Menai Strait, regarded as slightly polluted by heavy metals, showed levels similar to those found in B. amphitrite in Mission Bay. Only in the case of copper, levels in the latter were higher (cf. Rainbow, 1987). Barnacles from the Salton Sea showed generally lower levels of the investigated elements. Salton Sea barnacle egg masses accumulated smaller amounts of zinc, and amounts of copper and iron approximately equal to those from the Irish Sea specimens. The egg masses from Mission Bay had an iron level similar to that found in the Irish Sea egg masses; the other metals were far less abundant than in those from the Irish Sea (Walker and Foster, 1979). The results of this preliminary study confirm that barnacles are an excellent tool for monitoring heavy metals in aquatic biota. Their gregarious occurrence makes it easy to collect enough material. This is especially important in the Salton Sea, where other macrobenthic filter-feeders are either very small or scarce. The findings of this research project suggest that the Salton Sea is not yet heavily polluted by heavy metals derived from industrial, agricultural or domestic wastewater. However, it is presently receiving a big load of organic matter, including raw sewage. The influence of this factor upon the heavy metal concentrations in the water column, and much less accumulation in barnacles, has not been well studied, and it therefore needs fuller understanding. The authorsthank RonaldLaBordeof the SIO AnalyticalFacilityfor his help with the ICP-MS analyses,and an anonymousreviewerfor valuable comments. The research was done during Wojciech Fialkowski's visit to the SIO on a Fulbright Fellowship.
Volume 36/Number 2/Februa~ 1998 Alexander, G. V. and Rowland, R. H. (1966) Estimation of Zinc-65 background levels for marine coastal waters. Nature 210, 155157. Al-Thaqafi, K. and White, K. N. (1991) Effect of shore position and environmental metal levels on body metal burdens in the barnacle Elminius modestus. Environmental Pollution 69, 89-104. Carpelan, L. H. (1961) Physical and chemical characteristics. In The Ecology of the Salton Sea, California, in Relation to the Sportfishery, ed. B. W. Walker, pp. 17-32. State of California Department of Fish and Game, Fish Bulletin, no. 113. Chan, H. M., Rainbow, P. S. and Phillips, D. J. H. (1990) Barnacles and mussels as monitors of trace metal bio-availability in Hong Kong waters. In Proceedings of the Second International Marine Biological Workshop: The Marine Flora and Fauna of Hong Kong and Southern China, Hong Kong, 1986, ed. B. Morton, pp. 12391268. Hong Kong University Press, Hong Kong. GESAMP (1990) The state of marine environment. UNEP Regional Seas Reports and Studies 115: i-vii, 1-111. Goldberg, E. D., Bowen, V. T., Farrington, J. W., Harvey, G., Martin, J. H., Parker, P. L., Risenbrough, R. W., Robertson, W., Schneider, E. and Gamble, E. (1978) The mussel watch. Environmental Conservation 5, 101-125. Henry, D. P. and McLaughlin, P. A. (1975) The barnacles of the Balanus amphitrite complex (Cirripedia Thoracica). Zoological Verhandelingen 141, 203-212. Ireland, M. P. (1974) Variations in the zinc, copper, manganese and lead content of Balanus balanoides in Cardigan Bay, Wales. Environmental Pollution 7, 65-75. Lindquist, D. and La Rue, S. (1997) New River, new hope. The San Diego Union-Tribune 6, I, 14. Linsley, R. H. and Carpelan, L. H. (1961) Invertebrate fauna. In The Ecology of the Salton Sea, California, in Relation to the Sport.fishery, ed. B. W. Walker, pp. 105-151. State of California Department of Fish and Game, Fish Bulletin no. 113. Phillips, D. J. H. and Rainbow, P. S. (1988) Barnacles and mussels as biomonitors of trace elements: a comparative study. Marine Ecology Progress Series 49, 83-93. Powell, M. I. and White, K. N. (1990) Hea~,y metal accumulation by barnacles and its implications for their use as biological monitors. Marine Environmental Research 30, 91-118.
Rainbow, P. S. (1987) Heavy metals in barnacles. In Barnacle Biology, ed. A. J. Southward, pp. 405417. A. A. Balkema, Rotterdam. Rainbow, P. S. (1995) Biornonitoring of heavy metal availability in the marine environment. Marine Pollution Bulletin 31, 183192. Rainbow, P. S., Huang, Z. G., Yan, S. K. and Smith, B. D. (1993) Barnacles as biomonitors of trace metals in the coastal waters near Xiamen, China. Asian Marine Biology 10, 109-121. Rogers, F. L. (1949) Three new subspecies of Balanus amphitrite from California. Journal of Entomology and Zoology, Claremont 41, 3-12. Schroeder, R. A., Rivera, M., Redfield, J. B., Densmore, J. N., Michel, R. L., Norton, D. R., Audet, D. J., Setmire, J. G. and Goodbred, S. L. (1993) Physical, chemical and biological data for detailed study of irrigation drainage in the Salton Sea area, California 1988-90. US Geological Survey open-file report 93-83. US Geological Survey Books and Open-File Reports Section, Denver. Setmire, J. G., Schroeder, R. A., Densmore, J. N., Goodbred, S. L., Audet, D. J. and Radke W. R. (1993) Detailed study of water quality, bottom sediment, and biota associated with irrigation drainage in the Salton Sea area, California, 1988-90. Water Resources Investigations Report 93~4014. US Geological Survey Earth Science Information Center, Denver. Van Syoc, R. J. (1992) Living and fossil populations of a western Atlantic barnacle, Balanus subalbidus Henry, 1974, in the Gulf of California region. Proceedings of the San Diego Society of Natural History 12, 1-7. Walker, G. and Foster, P. (1979) Seasonal variation of zinc in the barnacle, Balanus balanoides (L.) maintained on a raft in the Menai Strait. Marine Environmental Research 2, 209-222. Walker, G., Rainbow, P. S., Foster, P. and Crisp, D. J. (1975) Barnacles: possible indicators of zinc pollution? Marine Biology 30, 57-65. Whitney, R. R. (1961) The Bairdiella icistius (Jordan et Gilbert). In The Ecology of the Salton Sea, California, in Relation to the Sportfishery, ed. B. W. Walker, pp. 105-151. State of California Department of Fish and Game, Fish Bulletin no. 113. Young, D. R. (1970) The distribution of cesium, rubidium and potassium in the quasi marine ecosystem of the Salton Sea. SIO Dissertation. University of California at San Diego, San Diego.
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