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Trace metals: Cd, Cu, Pb and Zn in gelatinous macroplankton from the Northwestern Mediterranean
War. Res. Vol. 21, No. 10, pp. 1287-1292, 1987 Printed in Great Britain. All rights reserved
0043-1354/87 $3.00+0.00 Copyright © 1987 Pergamon Journals Ltd
TRACE METALS: Cd, Cu, Pb A N D Zn IN GELATINOUS M A C R O P L A N K T O N FROM THE NORTHWESTERN MEDITERRANEAN M. ROMEO~, M. GNASSIA-BARELLI 1 and C. CARRE 2 qNSERM U 303, BP 3 06230, Villefranche-sur-Mer and 2CNRS UA 716, BP 28 06230, Villefranche-sur-Mer, France (Received December 1986) Abstract--Gelatinous macroplankton organisms were collected in May 1984 in Villefranche-sur-Mer Bay and analysed for cadmium, copper, lead and zinc. Analyses were carried out by polarography for Cd, Cu and Pb and by flame atomic absorption for Zn. Phosphorus was also measured in the samples as a biomass parameter due to difficulties inherent in measuring dry weight of gelatinous organisms. The samples belong to the Tunicates, the Cnidarians (Hydromedusae, Siphonophores and Scyphomedusae), the Ctenophores and the Molluscs. Crustaceans living on some Tunicates were also sampled. As regards cadmium, copper and lead, mean concentrations did not show significant differences among the phyla studied: especially for Tunicates with mean values of 0.1 ng Cd #g P-1, 2.0 ng Cu/~g P-t and 0.9 ng Pb #g P- ] and for Cnidarians with mean values of 0.5 ng Cd #g P- t, 2.0 ng Cu/~g P- t and 0.9 ng Pb/zg P-~ and for Cnidarians with mean values of 0.5 ng Cd #g p-t, 2.0ng Cu/~g P-~, 1.0ng Pb #g P-~. On the other hand, mean zinc concentrations were significantly lower in Tunicates (7.9 ng Zn #g p-t) than in Cnidarians (36.8 ng Zn/~g P-~). Zinc seems to be preferentially concentrated in organisms which are rich in collagen, constituting the mesogiea, such as the Cnidarians, the Ctenophore and the gelatinous Mollusc studied, rather than in organisms rich in tunicin such as the Tunicates. Key words--cadmium, copper, lead, zinc, gelatinous macroplankton, Tunicates, Cnidarians, Hydromedusae, Siphonophores, Scyphomedusae, Ctenophore
INTRODUCTION
Gelatinous zooplankton constitute an important part of the plankton in oceanic and coastal waters during various times of the year (Alldredge and Madin, 1982). These organisms in marine food webs may significantly mediate the transport and the cycle of metals and radionuclides in ocean waters (Gorsky et al., 1984; Krishnaswami et al., 1985). Little is known of the content of trace metals in these organisms. This study is concerned with trace metals in gelatinous macroplankton. These organisms (Hydromedusae, Siphonophores, Scyphomedusae, Ctenophores, Thaliceans, Appendicularians and Molluscs) were collected in the Bay of Villefranche-sur-Mer (northwestern Mediterranean Sea) in May 1984. Crustaceans living on some Thaliaceans were also sampled. During spring and summer months, gelatinous organisms often represent a large fraction of the zooplankton biomass in the upper 50 m of the Bay (Braconnot, 1971; T r r g o u b o f f and Rose, 1957; Goy, 1984; M o r a n d et aL, 1987). The samples that we collected included the most abundant and representative species in the ecosystem at this period of the year. Non-gelatinous plankton such as copepods and other crustaceans in the same area have already been considered and their trace metal content analyzed (Hardstedt-Romro, 1982; R o m r o et al., 1985).
Trace metals: cadmium, copper, lead and zinc were determined in all the samples. Cadmium and lead were studied since they are toxic to marine life. Copper and zinc were considered since they are essential to life when present in trace amounts even though they may be harmful at higher quantities. Phosphorus which is an important biological element was also determined in the samples.
MATERIALS AND METHODS
Samples were collected with a plankton net (680#m mesh), 500m from the coast at Station "B" at the entrance of the Bay of Villefranche-sur-Mer, where the hydrological conditions are monitored closely. A sampling depth of 10m was chosen (a) to avoid possible surface contamination, (b) to obtain large numbers of samples and (c) to limit damage to such delicate organisms. After collection, animals were kept in filtered seawater at ambient temperature so that they would empty their guts. The samples, which often contained a relatively large number of individuals of one species (especially for small species) were measured and counted with a stereomicroscope and the species were identified. Samples were stored frozen in plastic vials or bags. Instruments covered with PTFE were used to avoid metallic contamination. Samples were thawed under a laminar flow hood. Each sample was then digested with concentrated nitric acid (65%) (Merck Suprapur). The resulting solution was evaporated to dryness and redissolved in 0.1 N hydrochloric acid to a final volume of 6 ml.
1287
M. ROMEOet al.
1288
Table I. Trace metalconcentrations(ng metal per #g of phosphorus) and phosphorus content(ug per organism)of Tunicates Individuals per sample
Species
Length (mm)
Cd
Stage
Cu Pb (ng metal # g P t)
Blastozooid Oozooid Oozooid Blastozooid Blastozooid Oozooid
12 12 15 4 5 20
DL DL DL DL DL 0.1 DL
0.2 2.0 1. I DL 3.0 2.5 1.8± 1.1
0. I 0.1
3,3 2.0 __+ 1.2
Zn
P (/tg)
0.2 0,9 0.9 DL 0.6 2.1 [).0+0.7
ND 5.3 2.5 18. I 6.8 10.9 8.7 ± 6.0
28 6.4 16 0,7 3.3 56
0.7 0.9 ± 0.6
3.6 7.9 __+5.8
27.2
Thaliaceans
Thalia democratica Thalia democratica Thalia democratica Salpa fusiformis Salpa fusiformis Salpa fusiformis
9 9 10 37 33
I
Mean value for Thaliaceans ± 1 SD Appendicularians: O'fkopleura albicans 10 Total mean value for Tunicates + 1 S D D L = detection limit. N D = not determined.
Cadmium, lead and copper determinations were carried out with a PAR 264A voltammetric analyzer connected to a PAR 303A static mercury drop electrode. 20-200 #1 of the digested solution was added to seawater for the analysis. A simultaneous calibration of Cd, Pb and Cu concentrations was then made using standard additions. The detection limits were as follows: 55 ng 1 i for Cd, 80 ng 1 t for Pb and 70 ng 1- l for Cu. Zinc concentrations were determined directly on the digested solution by flame atomic absorption (Philips Pye Unicam sPg). The analytical procedure was checked regularly using standard reference material (SRM) provided by the U.S. National Bureau of Standard. Results were given in Rom6o and Nicolas (1986). The analyses of total phosphorus were carried out on 20-200 # 1of the digested solution by formation of phosphomolybdic coloured complex (Murphy and Riley, 1962). Trace metal determinations were made in triplicate and phosphorus analyses were carried out 3 or 4 times. In all the cases, appropriate blanks were prepared and their values were subtracted.
RESULTS AND DISCUSSION
The hydrography of the sampling station in May 1984 showed typical spring conditions with increasing temperature and decreasing salinity towards the surface. At 10m the mean temperature was 14.7°C, mean salinity was 37.63%0 and oxygen supersaturation was about l l0%. These were ideal conditions for gelatinous macroplankton development and resulted in the occurrence of many different species for sampling. Gelatinous organisms are very rich (more than 90%) in water. Measuring the dry weight of these organisms has been considered as difficult by some authors (Cecaldi et al., 1978; Shenker, 1985; Larson, 1986). Nevertheless, most authors working on the chemical composition of gelatinous organisms determined the dry weight after a brief rinsing with distilled water. Instead we chose to use phosphorus as a biomass parameter in this study. Beers (1966) reported that the ratio of phosphorus to dry weight varied significantly among major groups of zooplankton (non-gelatinous and gelatinous organisms). Siphonophores, Hydromedusae have nearly the same ratio which is 0.14 and 0.17%, respectively (Beers, 1966). Curl (1962) found ratios of 0.15% for
the Scyphomedusa Pelagia noctiluca, 0.12% for the Ctenophore Beroe and 0.19% for Salps. This ratio is much higher for Crustaceans (in particular Amphipods) reaching 1.23% (Beers, 1966). Trace metal and phosphorus contents were determined per organism. Results, shown in Tables 1, 2(a), (b) and 3 give the concentrations of metals on a phosphorus specific basis (ng metal per #g P) and the size and phosphorus content (#g) of the organisms. The stage of development is also given for the Tunicates in Table 1 and for the Siphonophores in Table 2(b). As regards cadmium, the concentrations in the different organisms were generally low ranging from the detection limit to 4.7 ng Cd #g P-~ found for the smallest organism considered, Podocoryne minima. Copper and lead concentrations were slightly higher and ranged from the detection limit for both metals to 24.0 ng C u / l g P ~ for Podocoryne minima and to 14.5ng Pb #g P t for Beroe ovata. Zinc concentrations presented a wide range of variation from 2.5 ng Zn /~g P-~ for Thalia democratica (oozooid stage) to 136.9 ng Zn /~g P-t for Cymbulia peroni. The Tunicates had generally low concentrations of the four studied metals. For the Cnidarians, the smallest organism Podocoryne minima exhibited the highest trace metal concentrations. The Ctenophore Beroe ovata presented high trace metal concentrations and the mollusc Cymbulia peroni had high lead and zinc concentrations. The Amphipod Crustacean Phronima atlantica that lives on Tunicates had nearly the same metal concentrations relative to phosphorus as these organisms. Nevertheless, mean concentrations calculated for cadmium, copper and lead [Tables 1, 2(a,b) and 3] do not show significant differences between the phyla whereas mean zinc concentrations are significantly lower in Tunicates than in Cnidarians (t-test significant at the 0.0005 level). For the most sampled phylum studied i.e. the Cnidarians, an allometric approach was taken and relationships between trace metal content and phosphorus content per individual were calculated since the body weight in plankton organisms is directly related to phosphorus content (Beers, 1966). Trace metals contents per individual were related to
= diameter of the bell. L ffi length of the nectosome. DL = detection limit.
Mean value for Scyphozoa (Pelagia) + 1 SD Mean value for Cnidarians n = 21 +_ I SD
Pelagia noctiluca Pelagia noctiluca Pelagia noctiluca
4.7* DL DL 0.6 DL DL 0.3 0.4
Cd
24.0* 1.5 0.8 2.0 0.3 2.0 2.7 1.6 _+0.9
13.7* 1.0 0.7 1.1 0.2 0.2 2.5 1.0 _+0.8
Cu Pb (ng metal # g p - l ) 66.7 62.0 29.7 67.6 9.2 20.2 10.8 38.0 _+ 26.5
Zn
0.03 4 53 107 18 4 6
P (#g)
1 1 I
6 2 1 1 2 5 I 3 l
10 10
Individuals per sample
+ Cormidies
Colony with: 3 Gastrozooids 3 Gastrozooids 5 Gastrozooids 8 Gastrozooids
Stage 0.4 0.3 0.4 0.3 1.3 1.3 DL 0,1 DL 0.3 0.3 0.5 __ 0.4 0.2 0.3 0.4 0.3 +_0.1 0.5 + 0.4
= 30 qt = 30 = 50
Cd
60 60 100 100 20 25 25 25 25 25 L = 25
L= L= L= L= L= L= L= L= L= L~
Length or diameter (mm)
1.5 1.0 1.3 1.3 + 0.3 2.0 + 1.3
3.4 2.0 1.9 2.8 5.9 DL 3.4 1.4 DL 0.4 1.5 2.5 + 1.6
0.3 0.2 0.8 0.4 + 0.3 1.0 + 0.6
1.9 1.5 1.3 1.0 1.7 0.6 1.6 1.2 DL 0.3 0.6 1.2 _+0.5
Cu Pb (ng metal #g P-~)
Table 2(b). Trace metal concentrations (ng metal per #g of phosphorus) and phosphorus content (pg per organism) of Cnidarians
Mean value for Siphonophores + 1 SD Scyphozoa: Scyphomedusae
Agalma elegans Agalma elegans Agalma elegans Halistemma rubrum Hippopodius hippopus Chelophyes appendiculata Chelophyes appendiculata Chelophyes appendicuIata Abylopsis tetragona Abylopsis tetragona Abylopsis tetragona
Hydrozoa: Siphonophores:
Species
~= 5 ~= 8 ~ = 14 ~= 10 ~ = 12 ¢)= 12
8 7 25
~ = 0.8
5 I 1
Diameter (mm)
200
Individuals per sample
= diameter of the bell. DL = detection limit. *Values > 3.SD omitted from the calculation of the mean.
Mean value for Hydromedusae _+ 1 SD
Podocoryne minima Zanclea costata Leuckartiara octona Leuckartiara octona Eutima gegenbauri Clytia hemisphaerica Clytia hemisphaerica
Hydrozoa: Hydromedusae:
Species
Table 2(a). Trace metal concentrations (ng metal per # g of phosphorus) and phosphorus content (pg per organism) of Cnidarians
30.4 30.0 30.9 30.4 _+0.5 36.8 +_7.2
28. I 19.4 29.1 48.1 17.5 46.9 49.5 35.5 45.1 48.0 48.9 37.8 _+ 12.4
Zn
P
559 863 2460
33 41 76 118 220 23 20 28 39 39 146
0~g)
~D
oo
e~
1290
M. RoMeo et al.
Table 3. Trace metal concentrations(ng metal per Izg of phosphorus)and phosphoruscontent (izg per organismt of Ctenophores,Molluscs and Crustaceans Individual per sample
Size (mm)
Cd
Beroe ovata
20
2.6
5.9
14.5
81.2
139
Mollusc: Thecosome pteropod: Cymbulia peroni--body without pseudo-shell Arthropod: Crustacean: Amphipod
5(11
O.N
I2
~.5
136.9
942
O.I 0. I
I Xi 3.4
01 0.5
8.6 12.2
378 300
Species
Cu Pb (ng metal ~ug P T)
Zn
P
(#g)
Ctenophore:
Phronima atlantica
Table 4. Log-log relationships between trace metal content per organism and phosphorus content of the Cnidarians Metal
No. of samples
Regression equations
Zn Cd Cu Pb
21 15 19 20
log Zn = 0.971 log P + 1.557 log Cd = 0.799 log P + 0.015 log Cu = 0.816 log P + 0.562 log Pb = 0.780 log P + 0.261
p h o s p h o r u s content as power functions C = a P b. Equations corresponding to the regression lines obtained after logarithmic t r a n s f o r m a t i o n and correlation coefficients are shown in Table 4 for the four metals studied. Similar allometric relationships were found between trace element content and body weight for Molluscs by Boyden (1974, 1977), Cossa e t al. (1980) and A m i a r d e t al. (1986). Boyden (1974, 1977) identified general types o f relationships between trace element and body weight. First, element content was related to b -~ 0.77 power o f body weight; in this case, the slopes may be due to some relationship between uptake and surface area. Second, elemental content was directly related to body weight b ~ 1.00. In this case, tissue element concentrations are independent o f size. The binding by specific chemical constituents whose concentrations are themselves directly related to body size, could account for the size independence o f some element concentrations. The values obtained for bin the case o f Cnidarians were c o m p a r e d for the four
Correlation coefficients and their significance 0.972 0.946 0.924 0.897
P < 0.001 P < 0.001 P < 0.001 P < 0.001
metals studied, to the values given by Boyden (1974, 1977). F o r cadmium, copper and lead these values ranged from 0.78 to 0.82 (Table 4) which are close to the value o f 0.77 mentioned above. According to Boyden's hypothesis o f adsorption for the Molluscs, cadmium, copper and lead may be taken up by the Cnidarians by adsorption. On the contrary, zinc which has a value o f b = 0.97 (close to the value o f 1.00, the later relationship mentioned above) may be linked to the major biochemical constituent o f these organisms which is mesogleal collagen (Madin e t al., 1981). Likewise, the differences found in the concentrations o f zinc between the different phyla (especially between Tunicates and Cnidarians) may be related to the biochemical composition o f the organisms. F o r the Tunicates, with a low zinc content, the main biochemical constituent is tunicin, a form o f cellulose (Hall and Saxl, 1960) whereas the mesoglea in the Cnidarians, which are rich in zinc, contains a high percentage o f the protein collagen (Madin e t al., 1981). The gelatinous Mollusc C y m b u l i a p e r o n i is also
Table 5. Trace metal concentrations(/~g per g of dry weight) in gelatinous macroplankton organisms from different sources. The results in this study were calculated on the P/dry weight ratios given by Curl (1962) and Beers (1966) Location
Species
Cd
Cu
Pb
Zn
Sources
Tunicates: Thaliaceans: N.W, Mediterranean Mediterranean N.W. Mediterranean
Thalia democratica Salpa maxima Salpa maxima Pyrosoma atlanticum T. democratica and S. fusiformis
17.0-22.4 7.3 0.12-0.23 7.6-10.4 0.10--0.21 8.7-13.4 DL 3.4
1.7
93-312 35.6 26-54 64-180 17
Krishnaswamiet al. (1985)
This study Fujita (1972) Fowler et al. (1985) This study Tomicet al. (1983) This study
Fowleret al. (1985)
Cnidarians: Hydromedusae: N. Pacific Mediterranean N.W. Mediterranean
Aglantha digitale Abylopsis tetragona
Adriatic N.W. Mediterranean
Pelagia noctiluca Pelagia noetiluca Ctenophores: Beroe Beroe ovata
N. Atlantic N.W. Mediterranean N. Atlantic DL = detection limit.
Hydromedusae: Cnidarians: Seyphomedusae:
Mixed samples ( > 95% jellyfish)
0.7
2.7
1.7
235 25 65
0.4
5.4 2.0
0.6
29-76 46
0.16 3.1 1.9-2.4
2.0 52 Dube (1982) 7.1 17.4 97 This study 1.6-9.7 11.9-68.1 9.9--355 Greiget al. (1977)
Cd, Cu, Pb and Zn in jellyfish mainly composed of collagen and presents the maximum value for zinc. Zinc may have more affinity for the protein collagen than for the polysaccharide tunicin. Food habits of the different species may also influence their trace metal concentrations. The gelatinous organisms sampled represent phyla that span three trophic levels. The Tunicates (Thalia democratica, Salpa fusiformis and Oikopleura albicans), (Alldredge and Madin, 1982) and the Mollusc C y m bulia peroni are herbivores and showed significant differences in metal concentrations, with C. peroni having high lead and zinc concentrations. The Hydromedusae are carnivores that feed on small herbivorous copepods (Fraser, 1969). The larger Hydromedusae, such as Leuckartiara octona can eat organisms bigger than themselves such as small fish (Fraser, 1969). Siphonophores feed on small crustaceans (Purcell, 1982). Scyphomedusae which are essentially predators eat mostly zooplankton but also salps, pteropods, molluscs and larval fish (Hay, 1984). Both Hydromedusae and Siphonophores had high levels of zinc. The Ctenophore Beroe ovata, which had high concentrations of all four metals studied, is macrophageous, even preying on other Ctenophores (Hoeger, 1983). In fact, both biochemical composition and food habits probably influence the trace metal concentration in organisms. Table 5 summarizes different values published for trace element concentrations in gelatinous organisms. For comparison, our results are expressed here as/~g metal per g of dry weight that were calculated using the ratios of phosphorus to dry weight for the different species given by Curl (1962) and Beers (1966). Very few results concerning the trace metal concentrations of gelatinous macroplankton organisms were found in the literature. Our results are of the same order of magnitude as those found by other authors. Gelatinous organisms have a lower trace metal concentration on a dry weight or phosphorus basis than zooplankton crustaceans collected in the same area (Rom6o et al., 1985; Rom6o and Nicolas, 1986). Nevertheless the gelatinous organisms should not be ignored in the estimation of the transport of trace metals and especially zinc in the oceans since they are capable of frequent proliferation often producing huge swarms that can represent a major part of the zooplankton standing crop. Recent work (Krishnaswami et al., 1985) showed that the Tunicates concentrate trace elements in their fecal pellets and that the ratio of concentration in the feces to concentration in the organisms reaches 2 for zinc and copper and 22 for radioactive lead (2~°pb). Fluxes of trace metal via salp defecation were higher than those measured in crustacean zooplankton species. In conclusion, the importance of gelatinous organisms in the biogeochemical cycling of trace metals in the oceans must be emphasized since these or-
1291
ganisms play an important role in the ecosystem. Further investigations are still needed on the seasonal variation of trace metal in gelatinous macroplankton. REFERENCES Alldredge A. L. and Madin L. P. (1982) Pelagic Tunicates: unique herbivores in the marine plankton. Bioscienee 32, 655-663. Amiard J. C., Amiard-Triquet C., Berthet B. and M6tayer C. (1986) Contribution to the ecotoxicological study of cadmium, lead, copper and zinc in the mussel Mytilus edulis. Mar. Biol. 90, 425-43 I. Beers J. R. (1966) Studies on the chemical composition of the major zooplankton groups in the Sargasso Sea off Bermuda. Limnol. Oceanogr. II, 520-528. Boyden C. R. 0974) Trace element content and body size in molluscs. Nature 251, 311-314. Boyden C. R. (1977) Effect of size upon metal content of shellfish.J. mar. biol. Ass. U.K. 57, 675-714. Braconnot J. C. (1971) Contribution d l'6tude biologique et 6cologique des tuniciers p61agiques Salpides et Doliolides--I. Hydrologic et 6cologie des Salpides. Vie Milieu 22, 257-286. Ceccaldi H. J., Kanazawa A. and Teshima S. I. (1978) Chemical composition of some Mediterranean macroplanktonic organisms--I. Proximate analysis. Tethys 8, 295-298. Cossa D., Bourget E., Pouliot D., Piuze J. and Chanut J. P. (1980) Geographical and seasonal variations in the relationship between trace metal content and body weight in Mytilus edulis. Mar. Biol. 58, 7-14. Curl H. Jr. (1962) Standing crops of carbon, nitrogen and phosphorus and transfer between trophic levels, in continental shelf waters south of New York. Rapp. Cons. int. Explor. Met. 153, 183-189. Dub6 J. (1982) Etude de la distribution de quelques m6taux dans le zooplancton de deux 6cosyst6mes du SaintLaurent. M6moire INRS-Oc6anologie, Universit6 du Qu6bec. Fowler S. W., Papadopoulou C. and Zafiropoulos D. (1985) Trace elements in selected species of zooplankton and nekton from the open Mediterranean Sea. In Heavy Metals in the Environment (Edited by T. D. Lekkas), Vol. I, pp. 670-672. CEP Consultants, Edinburgh. Fraser J. H. (1969) Experimental feeding of some Medusae and Chaetognatha. J. Fish. Res. Bd Can. 26, 1743-1762. Fujita T. (1972) The zinc content in marine plankton. Rec. oceanogr. Wks Japan 11, 73-79. Gorsky G., Fisher N. S. and Fowler S. W. (1984) Biogenic debris from the pelagic tunicate Oikopleura dioica, and its role in the vertical transport of a transuranium element. Est. Coast. Shelf Sci. 18, 13-23. Goy J. (1984) Fluctuations climatiques de la Scypbom6duse Pelagia novtiluca. C.r. Acad. Sci. Paris 299, 507-510. Greig R. A., Adams A. and Wenzloff D. R. (1977) Trace metal content of plankton and zooplankton collected from the New York Bight and Long Island Sound. Bull. envir, contam. Toxic. 18, 3-8. Hall D. A. and Saxl H. (1960) Human and other animal cellulose. Nature 13, 547-550. Hardstedt-Rom6o M. (1982) Some aspects of the chemical composition of plankton from the North-Western Mediterranean Sea. Mar. Biol. 70, 229-236. Hay S. J. (1984) Jellyfish--friend and foe. Scott. Fish. Bull. 48, 55-61. Hoeger U. (1983) Biochemicalcomposition of Ctenophores. J. exp. mar. Biol. Ecol. 72, 251-262. Krishnaswami S., Baskaran M., Fowler S. W. and Heyraud M. (1985) Comparative role of salps and other zooplankton in the cycling and transport of selected dements and natural radionuclides in Mediterranean waters. Biogeochemistry 1, 353-360.
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Larson R. J. (1986) Water content, organic content and carbon and nitrogen composition of medusae for the northeast Pacific. J. exp. mar. Biol. Ecol. 99, 107-120. Madin L. P., Cetta C. M. and McAlister V. L. (1981) Elemental and biochemical composition of salps (Tunicata: Thaliacea). Mar. Biol. 63, 217-226. Morand P., Carr6 C. and Biggs D. C. (1987) Feeding and metabolism of the jellyfish, Pelagia noctiluca (Scyphomedusae semeostomae). J. Plank. Res. In press. Murphy J. and Riley J. P. (1962) A modified single solution method for the determination of phosphate in natural waters. Analytica chim. Acta 27, 31-36. Purcell J. E. (1982) Feeding and growth of the Siphonophore Muggiaea atlantica (Cunningham 1893) J. exp. mar. Biol. EcoL 62, 339-354.
Rom6o M., Gnassia-Barelli M. et Nicolas E. (1985) Concentrations en plomb du plancton de l a m e r Ligure (M&titerran6e Nord-Occidentale). Chemosphere 14, 1423-1431. Rom6o M. and Nicolas E. (1986) Cadmium, copper, lead and zinc in three species of planktonic crustaceans from the east coast of Corsica. Mar. Chem. 18, 359-367. Shenker J. M. (1985) Carbon content of the neritic scyphomedusa Chrysaora fuscescens. J. Plank. Res. 7, 169-173. Tomic S., Makjanic J., Orlic I. and Valkovic V. (1983) Analysis of trace metals in jellyfish by XRF. Workshop on jellyfish blooms in the Mediterranean, U.N.E.P., Athens, 31 October-4 November, 1983. Tr6gouboff G. et Rose M. (1957) Manuel de Planctonologie M~diterran~enne. CNRS, Paris.
0043-1354/87 $3.00+0.00 Copyright © 1987 Pergamon Journals Ltd
TRACE METALS: Cd, Cu, Pb A N D Zn IN GELATINOUS M A C R O P L A N K T O N FROM THE NORTHWESTERN MEDITERRANEAN M. ROMEO~, M. GNASSIA-BARELLI 1 and C. CARRE 2 qNSERM U 303, BP 3 06230, Villefranche-sur-Mer and 2CNRS UA 716, BP 28 06230, Villefranche-sur-Mer, France (Received December 1986) Abstract--Gelatinous macroplankton organisms were collected in May 1984 in Villefranche-sur-Mer Bay and analysed for cadmium, copper, lead and zinc. Analyses were carried out by polarography for Cd, Cu and Pb and by flame atomic absorption for Zn. Phosphorus was also measured in the samples as a biomass parameter due to difficulties inherent in measuring dry weight of gelatinous organisms. The samples belong to the Tunicates, the Cnidarians (Hydromedusae, Siphonophores and Scyphomedusae), the Ctenophores and the Molluscs. Crustaceans living on some Tunicates were also sampled. As regards cadmium, copper and lead, mean concentrations did not show significant differences among the phyla studied: especially for Tunicates with mean values of 0.1 ng Cd #g P-1, 2.0 ng Cu/~g P-t and 0.9 ng Pb #g P- ] and for Cnidarians with mean values of 0.5 ng Cd #g P- t, 2.0 ng Cu/~g P- t and 0.9 ng Pb/zg P-~ and for Cnidarians with mean values of 0.5 ng Cd #g p-t, 2.0ng Cu/~g P-~, 1.0ng Pb #g P-~. On the other hand, mean zinc concentrations were significantly lower in Tunicates (7.9 ng Zn #g p-t) than in Cnidarians (36.8 ng Zn/~g P-~). Zinc seems to be preferentially concentrated in organisms which are rich in collagen, constituting the mesogiea, such as the Cnidarians, the Ctenophore and the gelatinous Mollusc studied, rather than in organisms rich in tunicin such as the Tunicates. Key words--cadmium, copper, lead, zinc, gelatinous macroplankton, Tunicates, Cnidarians, Hydromedusae, Siphonophores, Scyphomedusae, Ctenophore
INTRODUCTION
Gelatinous zooplankton constitute an important part of the plankton in oceanic and coastal waters during various times of the year (Alldredge and Madin, 1982). These organisms in marine food webs may significantly mediate the transport and the cycle of metals and radionuclides in ocean waters (Gorsky et al., 1984; Krishnaswami et al., 1985). Little is known of the content of trace metals in these organisms. This study is concerned with trace metals in gelatinous macroplankton. These organisms (Hydromedusae, Siphonophores, Scyphomedusae, Ctenophores, Thaliceans, Appendicularians and Molluscs) were collected in the Bay of Villefranche-sur-Mer (northwestern Mediterranean Sea) in May 1984. Crustaceans living on some Thaliaceans were also sampled. During spring and summer months, gelatinous organisms often represent a large fraction of the zooplankton biomass in the upper 50 m of the Bay (Braconnot, 1971; T r r g o u b o f f and Rose, 1957; Goy, 1984; M o r a n d et aL, 1987). The samples that we collected included the most abundant and representative species in the ecosystem at this period of the year. Non-gelatinous plankton such as copepods and other crustaceans in the same area have already been considered and their trace metal content analyzed (Hardstedt-Romro, 1982; R o m r o et al., 1985).
Trace metals: cadmium, copper, lead and zinc were determined in all the samples. Cadmium and lead were studied since they are toxic to marine life. Copper and zinc were considered since they are essential to life when present in trace amounts even though they may be harmful at higher quantities. Phosphorus which is an important biological element was also determined in the samples.
MATERIALS AND METHODS
Samples were collected with a plankton net (680#m mesh), 500m from the coast at Station "B" at the entrance of the Bay of Villefranche-sur-Mer, where the hydrological conditions are monitored closely. A sampling depth of 10m was chosen (a) to avoid possible surface contamination, (b) to obtain large numbers of samples and (c) to limit damage to such delicate organisms. After collection, animals were kept in filtered seawater at ambient temperature so that they would empty their guts. The samples, which often contained a relatively large number of individuals of one species (especially for small species) were measured and counted with a stereomicroscope and the species were identified. Samples were stored frozen in plastic vials or bags. Instruments covered with PTFE were used to avoid metallic contamination. Samples were thawed under a laminar flow hood. Each sample was then digested with concentrated nitric acid (65%) (Merck Suprapur). The resulting solution was evaporated to dryness and redissolved in 0.1 N hydrochloric acid to a final volume of 6 ml.
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M. ROMEOet al.
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Table I. Trace metalconcentrations(ng metal per #g of phosphorus) and phosphorus content(ug per organism)of Tunicates Individuals per sample
Species
Length (mm)
Cd
Stage
Cu Pb (ng metal # g P t)
Blastozooid Oozooid Oozooid Blastozooid Blastozooid Oozooid
12 12 15 4 5 20
DL DL DL DL DL 0.1 DL
0.2 2.0 1. I DL 3.0 2.5 1.8± 1.1
0. I 0.1
3,3 2.0 __+ 1.2
Zn
P (/tg)
0.2 0,9 0.9 DL 0.6 2.1 [).0+0.7
ND 5.3 2.5 18. I 6.8 10.9 8.7 ± 6.0
28 6.4 16 0,7 3.3 56
0.7 0.9 ± 0.6
3.6 7.9 __+5.8
27.2
Thaliaceans
Thalia democratica Thalia democratica Thalia democratica Salpa fusiformis Salpa fusiformis Salpa fusiformis
9 9 10 37 33
I
Mean value for Thaliaceans ± 1 SD Appendicularians: O'fkopleura albicans 10 Total mean value for Tunicates + 1 S D D L = detection limit. N D = not determined.
Cadmium, lead and copper determinations were carried out with a PAR 264A voltammetric analyzer connected to a PAR 303A static mercury drop electrode. 20-200 #1 of the digested solution was added to seawater for the analysis. A simultaneous calibration of Cd, Pb and Cu concentrations was then made using standard additions. The detection limits were as follows: 55 ng 1 i for Cd, 80 ng 1 t for Pb and 70 ng 1- l for Cu. Zinc concentrations were determined directly on the digested solution by flame atomic absorption (Philips Pye Unicam sPg). The analytical procedure was checked regularly using standard reference material (SRM) provided by the U.S. National Bureau of Standard. Results were given in Rom6o and Nicolas (1986). The analyses of total phosphorus were carried out on 20-200 # 1of the digested solution by formation of phosphomolybdic coloured complex (Murphy and Riley, 1962). Trace metal determinations were made in triplicate and phosphorus analyses were carried out 3 or 4 times. In all the cases, appropriate blanks were prepared and their values were subtracted.
RESULTS AND DISCUSSION
The hydrography of the sampling station in May 1984 showed typical spring conditions with increasing temperature and decreasing salinity towards the surface. At 10m the mean temperature was 14.7°C, mean salinity was 37.63%0 and oxygen supersaturation was about l l0%. These were ideal conditions for gelatinous macroplankton development and resulted in the occurrence of many different species for sampling. Gelatinous organisms are very rich (more than 90%) in water. Measuring the dry weight of these organisms has been considered as difficult by some authors (Cecaldi et al., 1978; Shenker, 1985; Larson, 1986). Nevertheless, most authors working on the chemical composition of gelatinous organisms determined the dry weight after a brief rinsing with distilled water. Instead we chose to use phosphorus as a biomass parameter in this study. Beers (1966) reported that the ratio of phosphorus to dry weight varied significantly among major groups of zooplankton (non-gelatinous and gelatinous organisms). Siphonophores, Hydromedusae have nearly the same ratio which is 0.14 and 0.17%, respectively (Beers, 1966). Curl (1962) found ratios of 0.15% for
the Scyphomedusa Pelagia noctiluca, 0.12% for the Ctenophore Beroe and 0.19% for Salps. This ratio is much higher for Crustaceans (in particular Amphipods) reaching 1.23% (Beers, 1966). Trace metal and phosphorus contents were determined per organism. Results, shown in Tables 1, 2(a), (b) and 3 give the concentrations of metals on a phosphorus specific basis (ng metal per #g P) and the size and phosphorus content (#g) of the organisms. The stage of development is also given for the Tunicates in Table 1 and for the Siphonophores in Table 2(b). As regards cadmium, the concentrations in the different organisms were generally low ranging from the detection limit to 4.7 ng Cd #g P-~ found for the smallest organism considered, Podocoryne minima. Copper and lead concentrations were slightly higher and ranged from the detection limit for both metals to 24.0 ng C u / l g P ~ for Podocoryne minima and to 14.5ng Pb #g P t for Beroe ovata. Zinc concentrations presented a wide range of variation from 2.5 ng Zn /~g P-~ for Thalia democratica (oozooid stage) to 136.9 ng Zn /~g P-t for Cymbulia peroni. The Tunicates had generally low concentrations of the four studied metals. For the Cnidarians, the smallest organism Podocoryne minima exhibited the highest trace metal concentrations. The Ctenophore Beroe ovata presented high trace metal concentrations and the mollusc Cymbulia peroni had high lead and zinc concentrations. The Amphipod Crustacean Phronima atlantica that lives on Tunicates had nearly the same metal concentrations relative to phosphorus as these organisms. Nevertheless, mean concentrations calculated for cadmium, copper and lead [Tables 1, 2(a,b) and 3] do not show significant differences between the phyla whereas mean zinc concentrations are significantly lower in Tunicates than in Cnidarians (t-test significant at the 0.0005 level). For the most sampled phylum studied i.e. the Cnidarians, an allometric approach was taken and relationships between trace metal content and phosphorus content per individual were calculated since the body weight in plankton organisms is directly related to phosphorus content (Beers, 1966). Trace metals contents per individual were related to
= diameter of the bell. L ffi length of the nectosome. DL = detection limit.
Mean value for Scyphozoa (Pelagia) + 1 SD Mean value for Cnidarians n = 21 +_ I SD
Pelagia noctiluca Pelagia noctiluca Pelagia noctiluca
4.7* DL DL 0.6 DL DL 0.3 0.4
Cd
24.0* 1.5 0.8 2.0 0.3 2.0 2.7 1.6 _+0.9
13.7* 1.0 0.7 1.1 0.2 0.2 2.5 1.0 _+0.8
Cu Pb (ng metal # g p - l ) 66.7 62.0 29.7 67.6 9.2 20.2 10.8 38.0 _+ 26.5
Zn
0.03 4 53 107 18 4 6
P (#g)
1 1 I
6 2 1 1 2 5 I 3 l
10 10
Individuals per sample
+ Cormidies
Colony with: 3 Gastrozooids 3 Gastrozooids 5 Gastrozooids 8 Gastrozooids
Stage 0.4 0.3 0.4 0.3 1.3 1.3 DL 0,1 DL 0.3 0.3 0.5 __ 0.4 0.2 0.3 0.4 0.3 +_0.1 0.5 + 0.4
= 30 qt = 30 = 50
Cd
60 60 100 100 20 25 25 25 25 25 L = 25
L= L= L= L= L= L= L= L= L= L~
Length or diameter (mm)
1.5 1.0 1.3 1.3 + 0.3 2.0 + 1.3
3.4 2.0 1.9 2.8 5.9 DL 3.4 1.4 DL 0.4 1.5 2.5 + 1.6
0.3 0.2 0.8 0.4 + 0.3 1.0 + 0.6
1.9 1.5 1.3 1.0 1.7 0.6 1.6 1.2 DL 0.3 0.6 1.2 _+0.5
Cu Pb (ng metal #g P-~)
Table 2(b). Trace metal concentrations (ng metal per #g of phosphorus) and phosphorus content (pg per organism) of Cnidarians
Mean value for Siphonophores + 1 SD Scyphozoa: Scyphomedusae
Agalma elegans Agalma elegans Agalma elegans Halistemma rubrum Hippopodius hippopus Chelophyes appendiculata Chelophyes appendiculata Chelophyes appendicuIata Abylopsis tetragona Abylopsis tetragona Abylopsis tetragona
Hydrozoa: Siphonophores:
Species
~= 5 ~= 8 ~ = 14 ~= 10 ~ = 12 ¢)= 12
8 7 25
~ = 0.8
5 I 1
Diameter (mm)
200
Individuals per sample
= diameter of the bell. DL = detection limit. *Values > 3.SD omitted from the calculation of the mean.
Mean value for Hydromedusae _+ 1 SD
Podocoryne minima Zanclea costata Leuckartiara octona Leuckartiara octona Eutima gegenbauri Clytia hemisphaerica Clytia hemisphaerica
Hydrozoa: Hydromedusae:
Species
Table 2(a). Trace metal concentrations (ng metal per # g of phosphorus) and phosphorus content (pg per organism) of Cnidarians
30.4 30.0 30.9 30.4 _+0.5 36.8 +_7.2
28. I 19.4 29.1 48.1 17.5 46.9 49.5 35.5 45.1 48.0 48.9 37.8 _+ 12.4
Zn
P
559 863 2460
33 41 76 118 220 23 20 28 39 39 146
0~g)
~D
oo
e~
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M. RoMeo et al.
Table 3. Trace metal concentrations(ng metal per Izg of phosphorus)and phosphoruscontent (izg per organismt of Ctenophores,Molluscs and Crustaceans Individual per sample
Size (mm)
Cd
Beroe ovata
20
2.6
5.9
14.5
81.2
139
Mollusc: Thecosome pteropod: Cymbulia peroni--body without pseudo-shell Arthropod: Crustacean: Amphipod
5(11
O.N
I2
~.5
136.9
942
O.I 0. I
I Xi 3.4
01 0.5
8.6 12.2
378 300
Species
Cu Pb (ng metal ~ug P T)
Zn
P
(#g)
Ctenophore:
Phronima atlantica
Table 4. Log-log relationships between trace metal content per organism and phosphorus content of the Cnidarians Metal
No. of samples
Regression equations
Zn Cd Cu Pb
21 15 19 20
log Zn = 0.971 log P + 1.557 log Cd = 0.799 log P + 0.015 log Cu = 0.816 log P + 0.562 log Pb = 0.780 log P + 0.261
p h o s p h o r u s content as power functions C = a P b. Equations corresponding to the regression lines obtained after logarithmic t r a n s f o r m a t i o n and correlation coefficients are shown in Table 4 for the four metals studied. Similar allometric relationships were found between trace element content and body weight for Molluscs by Boyden (1974, 1977), Cossa e t al. (1980) and A m i a r d e t al. (1986). Boyden (1974, 1977) identified general types o f relationships between trace element and body weight. First, element content was related to b -~ 0.77 power o f body weight; in this case, the slopes may be due to some relationship between uptake and surface area. Second, elemental content was directly related to body weight b ~ 1.00. In this case, tissue element concentrations are independent o f size. The binding by specific chemical constituents whose concentrations are themselves directly related to body size, could account for the size independence o f some element concentrations. The values obtained for bin the case o f Cnidarians were c o m p a r e d for the four
Correlation coefficients and their significance 0.972 0.946 0.924 0.897
P < 0.001 P < 0.001 P < 0.001 P < 0.001
metals studied, to the values given by Boyden (1974, 1977). F o r cadmium, copper and lead these values ranged from 0.78 to 0.82 (Table 4) which are close to the value o f 0.77 mentioned above. According to Boyden's hypothesis o f adsorption for the Molluscs, cadmium, copper and lead may be taken up by the Cnidarians by adsorption. On the contrary, zinc which has a value o f b = 0.97 (close to the value o f 1.00, the later relationship mentioned above) may be linked to the major biochemical constituent o f these organisms which is mesogleal collagen (Madin e t al., 1981). Likewise, the differences found in the concentrations o f zinc between the different phyla (especially between Tunicates and Cnidarians) may be related to the biochemical composition o f the organisms. F o r the Tunicates, with a low zinc content, the main biochemical constituent is tunicin, a form o f cellulose (Hall and Saxl, 1960) whereas the mesoglea in the Cnidarians, which are rich in zinc, contains a high percentage o f the protein collagen (Madin e t al., 1981). The gelatinous Mollusc C y m b u l i a p e r o n i is also
Table 5. Trace metal concentrations(/~g per g of dry weight) in gelatinous macroplankton organisms from different sources. The results in this study were calculated on the P/dry weight ratios given by Curl (1962) and Beers (1966) Location
Species
Cd
Cu
Pb
Zn
Sources
Tunicates: Thaliaceans: N.W, Mediterranean Mediterranean N.W. Mediterranean
Thalia democratica Salpa maxima Salpa maxima Pyrosoma atlanticum T. democratica and S. fusiformis
17.0-22.4 7.3 0.12-0.23 7.6-10.4 0.10--0.21 8.7-13.4 DL 3.4
1.7
93-312 35.6 26-54 64-180 17
Krishnaswamiet al. (1985)
This study Fujita (1972) Fowler et al. (1985) This study Tomicet al. (1983) This study
Fowleret al. (1985)
Cnidarians: Hydromedusae: N. Pacific Mediterranean N.W. Mediterranean
Aglantha digitale Abylopsis tetragona
Adriatic N.W. Mediterranean
Pelagia noctiluca Pelagia noetiluca Ctenophores: Beroe Beroe ovata
N. Atlantic N.W. Mediterranean N. Atlantic DL = detection limit.
Hydromedusae: Cnidarians: Seyphomedusae:
Mixed samples ( > 95% jellyfish)
0.7
2.7
1.7
235 25 65
0.4
5.4 2.0
0.6
29-76 46
0.16 3.1 1.9-2.4
2.0 52 Dube (1982) 7.1 17.4 97 This study 1.6-9.7 11.9-68.1 9.9--355 Greiget al. (1977)
Cd, Cu, Pb and Zn in jellyfish mainly composed of collagen and presents the maximum value for zinc. Zinc may have more affinity for the protein collagen than for the polysaccharide tunicin. Food habits of the different species may also influence their trace metal concentrations. The gelatinous organisms sampled represent phyla that span three trophic levels. The Tunicates (Thalia democratica, Salpa fusiformis and Oikopleura albicans), (Alldredge and Madin, 1982) and the Mollusc C y m bulia peroni are herbivores and showed significant differences in metal concentrations, with C. peroni having high lead and zinc concentrations. The Hydromedusae are carnivores that feed on small herbivorous copepods (Fraser, 1969). The larger Hydromedusae, such as Leuckartiara octona can eat organisms bigger than themselves such as small fish (Fraser, 1969). Siphonophores feed on small crustaceans (Purcell, 1982). Scyphomedusae which are essentially predators eat mostly zooplankton but also salps, pteropods, molluscs and larval fish (Hay, 1984). Both Hydromedusae and Siphonophores had high levels of zinc. The Ctenophore Beroe ovata, which had high concentrations of all four metals studied, is macrophageous, even preying on other Ctenophores (Hoeger, 1983). In fact, both biochemical composition and food habits probably influence the trace metal concentration in organisms. Table 5 summarizes different values published for trace element concentrations in gelatinous organisms. For comparison, our results are expressed here as/~g metal per g of dry weight that were calculated using the ratios of phosphorus to dry weight for the different species given by Curl (1962) and Beers (1966). Very few results concerning the trace metal concentrations of gelatinous macroplankton organisms were found in the literature. Our results are of the same order of magnitude as those found by other authors. Gelatinous organisms have a lower trace metal concentration on a dry weight or phosphorus basis than zooplankton crustaceans collected in the same area (Rom6o et al., 1985; Rom6o and Nicolas, 1986). Nevertheless the gelatinous organisms should not be ignored in the estimation of the transport of trace metals and especially zinc in the oceans since they are capable of frequent proliferation often producing huge swarms that can represent a major part of the zooplankton standing crop. Recent work (Krishnaswami et al., 1985) showed that the Tunicates concentrate trace elements in their fecal pellets and that the ratio of concentration in the feces to concentration in the organisms reaches 2 for zinc and copper and 22 for radioactive lead (2~°pb). Fluxes of trace metal via salp defecation were higher than those measured in crustacean zooplankton species. In conclusion, the importance of gelatinous organisms in the biogeochemical cycling of trace metals in the oceans must be emphasized since these or-
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