OCEANOLOGICA ACTA 1984- VOL 7- N. 1 ~ -----·~-

Sorne relations between the elementary chemical of marine organisms and that of sea water

Elemental composition Element turnover

Oceanic/biological residence time

compusition Mag~s~~~: Composition élémentaire Circulation des éléments

Temps de résidence océanique/biologique Organismes marins

Crustacés

ABSTRACT

RÉSUMÉ

INTRODUCTION

D. H. Spaargaren •, H. J. Ceccaldi b

a Netherlands Institute for Sea Research, P.O. Box 59, 1790 AB Texel, The Netherlands. b École Pratique des Hautes Études, Station Marine d'Endoume, LA CNRS 41, rue de la Batterie des Lions, 13007 Marseille, France.

Received 15/11/82, in revised form 9/6/83, accepted 15/6/83.

Oceanographical data concerning the concentrations and residence times of various elements in seawater appear to be strongly related to biological data concerning the concentration of various elements in living material. A linear relation between oceanic fluxes of various elements, derived from the ratio between their oceanic concentration and their oceanic residence time, and the corresponding concentrations in biological material could be explained from a mathematical model. In this model, the biological residence times are assumed to be approximately the same: heavier elements, present in lower concentrations, are accumulated and excreted at lower rates than lighter elements. It is concluded that the concentrations of various elements in ocean water are given by non-stable flow-through equilibria. Input and output rates may be strongly affected by biological accumulation processes; the physico-chemical processes involved do not neces~arily reach steady state equilibria.

Oceanol. Acta, 1984, 7, 1, 63-76.

Relations entre la composition chimique élémentaire des orgamsmes marins et celle de l'eau de mer

Des données océanographiques concernant les concentrations et les temps de résidence de divers éléments dans l'eau de mer paraissent être fortement corrélées aux données biologiques concernant les concentrations des mêmes éléments dans la matière vivante. Une relation linéaire entre les flux océaniques des divers éléments, calculée à partir du rapport entre leur concentration dans l'eau de mer et leur temps de résidence dans les océans, peut être expliquée à partir d'un modèle mathématique. Dans ce modèle, les temps de résidence biologique sont considérés comme étant approximativement les mêmes : les éléments les plus lourds présents aux plus faibles concentrations sont accumulés et excrétés à taux plus faibles que les éléments plus légers. On peut conclure que les concentrations des divers éléments dans l'eau des océans sont données par des flux non stables jusqu'à équilibre. L'entrée et la sortie des éléments dans le système peuvent être fortement déterminés par les processus biologiques d'accumulation : les processus physico-chimiques mis en jeu, considérés isolément, n'atteignent pas nécessairement un équilibre dynamique.

Oceanol. Acta, 1984, 7, 1, 63-76.

Living organisms accumulate various substances from their environment for growth and maintenance of their bodies and as energy supply for vital activities. This uptake is in great measure balanced by the excretion of

waste products. In the uptake of material, a distinction may be made between so-called essential and non­essential elements. Apart from C, H, 0, N and P, a number of trace elements are recognized as essential

0399-1784/1984/63/S 5.00/ Cl Gauthier-Villars 63

~·.

D. H. SPAARGAREN. H. J. CECCALDI

elements. Liebscher and Smith (1968) and more recently Giesey and Wiener (1977), studying the concentration distribution of various elements in human tissues arrived at the hypothesis that the concentrations of essential elements in living tissues are normally distributed, whereas the concentrations of non-essential elements show asymmetric, positively skewed distribu­tions, better represented by log-normal distributions. This difference would originate in the regulation of the concentration of the elements: for essential elements, internai concentrations are regulated by active transport processes; for non-essential elements, the physiological regulating mechanisms are lacking. In the latter case, the internai concentrations are controlled by more variable external circumstances, which may lead to asymmetrical distributions of the internai concentra­tions.

Apart from above criterion the distinction between ''non-essential" and "essential in very small quantities" is difficult to establish. As analytical techniques improved during the past decades it appeared that many non-essential elements had to be ascribed a metabolic function. In a detailed study on the frequency distribution of (non-essential) Hg and Pb, Pinder and Giesey (1981) found no significant difference with the essential elements Fe, Cu, Cr, Zn and Se. The uncertainties in discriminating essential and non­essential elements, as weil as the increasing number of non-essential elements which in the course of time had to be ascribed a physiological function, suggest that the number of elements participating in metabolic processes in living organisms is considerably larger than was initially expected. lt is even possible that every element of the periodic system pla ys a role in the functioning of living organisms.

It is clear, however, that the optimal internai concentration and the variability of the internai concentration may vary greatly for various elements. Apart from the difference between essential and non­essential elements, a distinction may be made between micro and macro elements, roughly based on the quantities of various elements as they occur in living organisms. This difference, merely intended to indicate the quantity in which an element occurs, may superficially suggest a difference in biological signifi­cance. For the functioning ofliving organisms, however, both categories are equally important. Lack of micro­elements may, as in the case of a Jack of macro elements, be growth-limiting. The significance of ~ surplus of micro elements is to-day, in circumstances ofincreasing environmental pollution, also evident from the toxic effects of various micro elements.

Primary producers extract various substances directly from their abiotic environment; organisms at higher trophic levels accumulate their body constituents more indirectly. In both cases, the various substances eventually retum to the abiotic environment. This exchange between living organisms and their environ­ment has stimulated a great deal of research concerning the extent to which living organisms determine the elementary cycling and the abiotic environment. In

64

1972, Yamamoto pointed to a remarkable correlation between the concentration factor of various elements (as measured in marine algae) and the oceanic residence time of the elements. The concentration factor (Y) is defined as the ratio between the concentration of an element in a living organism (C;) and that in the surrounding seawater (C,). The oceanic residence time (t) gives the average time an element remains-dissolved or suspended-in seawater before it is removed by a biotic or abiotic precipitation process (Barth, 1952), hence t = A/( dA/dt), where A is the total amount of an element present in seawater and dA/dt or <p, the total amount which, per unit of time, is entering or removed from the ocean. Concentration factor and oceanic residence time . appear to be correlated according to: Y= a tb (a and b being constants): in other words, there exists a linear relation between the logarithm of the concentration factor and oceanic residence time according to: log Y= log a +h log t.

The above correlation was observed for various species of marine algae, but also in limnetic weeds, in zooplankton and even in human tissue, in rain- and hot spring water and in chondrite rock (the constants a and b had different values). The presence of this correlation between a biological quantity (concentration factor) and an oceanographical quantity ( oceanic residence time) was in a general sense explained by the close connection between biosphere and ocean water. For 20 different elements, Fowler (1977) studied the concentrations in faecal pellets produced by marine zooplankton which, by sinking to deeper water, could clearly provide a mechanism for the removal of those elements from surface waters and hence influence the residence time. As marine zooplankton partly feeds on marine algae, the connection between the concentration factor for various elements in algae and the oceanic residence times of these elements could be made plausible. The fact that in limnetic weeds, zooplankton and human tissue the same relation was found between concentration factor and oceanic residence time was explained by the similarity in elementary composition of these organisms, reflecting their common, marine origin. It should, however, be pointed out that in the case of human tissue as weil as in rain- and hot-spring water the concentration factor is no longer defined. In these cases it did not seem possible to offer a satisfactory explanation of the observed correlation.

Oceanic residence time is, as pointed out above, defined by the quotient of the total amount of an element present in ocean water and its influx or effiux to or from the ocean. The total amount of an element present in ocean water may also be described by the product of the average concentration ofthat element (C,) multiplied by the volume (V,) of ocean water. The average seawater concentration, C., is present in the values for oceanic residence time as weil as in the values for the concentration factor, C;fC,. Therefore, a (negative) correlation between concentration factor and oceanic residence time could be expected from the strong covariance built into this relationship thus, t = C,V,f<p, and Y = CtfC,. Elimination of C, yields: Y = C;V,f<p,t,

or: log Y = log (C;V,f<p,)-Jog t . ...

If we compare this with the formula of Yamamoto: log Y = log a + b. log t it foliows that a = C;V,jqJ. and b = -1. The empirical values for b are ali very close to -1 (e.g. -0.76 for Eisénia bicyclis; -1.01 for marine zooplankton; -1.19 for marine phytoplankton), hence approaching the expected value. For log a, values were found between 6 and 9.

Although---considering the method of analysis used-a strong negative correlation could be expected in plotting values for log Y against log t, it remains remarkable that the relation showed straight lines for ali data sets used. This implies that the factor log a ( = log c1V,/(fl.) is highly constant for various elements. For the term v., the ocean volume, this is obvious, but it is not clear why the quotient C;/(fl. yields the same value for different elements, whereas qJ. as weil as C; have strongly varying values for different elements.

In this study, data on the elementary composition of various organisms and seawater are reanalysed. On the one hand, it is worth examining which elements are necessary for the functioning of living organisms and in what concentrations. On the other hand, the linear relation between the concentration factors of various elements and their oceanic residence times, which-as shawn above-points to a constant ratio between the concentration of elements in living organisms and their oceanic circulation, demands a satisfactory, causal explanation.

DATA AND DATA ANALYSIS

Data

Recently Sidwell et al. (1977; 1978) compiled data on the internai elementary composition of various species of finfish, molluscs and crustaceans. From 128 publications, they collected values for the internai concentrations of 6 macro elements (Na, K, Ca, P, Cl and Mg) in 161 species which are commonly eaten. Subsequently, the concentration values for 20 micro­elements (Cu, Fe, Zn, I, Mn, Hg, organic Hg, Pb, As, F, Ag, Cd, Co, Cr, V, Al, Sn, Ni, Ba, Mo) in 167 species were compiled from 224 publications. These data, already standardized in units of mg/lOO ml or in ppm, were converted here to the corresponding logarithms of the molar concentrations (Table 1 ).

Mainly to complete data on lacking elements, data were also derived from the classic work of Vinogradov (1953), compiling data on the elementary composition of marine organisms as obtained from nearly 1 200 publications. Here, only the figures given in Chapter XVI, concerning the elementary composition of crustacea, were used.

In the following text, the above data were also compared with data on the elementary compositions of marine algae, as obtained from numerous measurements at the laboratory of Yamamoto and co-workers (e.g. Yama­moto et al., 1980).

65

ELEMENTAL COMPOSITION OF MARINE ORGANISMS

Data on the average composition of seawater (Table 2) were obtained from the table given by Brewer (1975, p. 417-421 ), also including estima tes of oceanic residence times of various elements as derived by Goldberg et al. (1971). The concentrations and t-values were also converted to corresponding log-values with 2 decimal accuracy.

The logarithmic conversion of concentration and residence time values is associated with Joss in accuracy. One digit variation in the last decimal of the log-value used corresponds to a variation in the original concentration or residence time of 2.3 %. However, the intra- and interspecific variation in internai concentra­tion values of animais, local variations in seawater concentrations, measurement inaccuracies and uncer­tainties in the estimates of residence times render unnecessary a higher accuracy than 0.01 in the log­values in this context. On the . other band, the log­conversion is advantageous in that the order of magnitude of various values may easily be compared without confusion by possible differences in the units in which the quantities are expressed. In the text to follow, concentration values are always expressed in mou-• (or the logarithm-base 1 0---ofthe mol ar concentration; residence times are always expressed in years, respecti­vely log~years; volumes are always expressed in litres, for instance the volume of the oceans V.= 1.4 109 km3

(Kossina, 1921) = 1.4 IQ21 litre, hence log V.= 21.1.

Data analysis

In geochemistry, a distinction is generally made between the various reservoirs in which the elements occur, for instance the oceans, fresh water (rivers, lakes, etc., together with seawater usually denoted as the hydro­sphere), the biosphere, the lithosphere. Each reservoir may be divided into subreservoirs, or considered together with others, depending on the phenomena to be described. Mackenzie (1975), for instance, described the biogeochemical turnover of the elements in a turnover madel with 4 different reservoirs, viz. the atmosphere, the biosphere, the sedimentary lithosphere and the oceans. Each reservoir exchanges material with a number of others; the exchange of elements between various reservoirs may be direct or indirect. The transport processes are, irrespective of the number of reservoirs distinguished, controlled by the general network theorems: 1) each reservoir is for each element (n) characterized by the total amount of the element present and the residence time of the element in the reservoir concerned; and 2) in steady state the algebraic sum of ali streams, entering or leaving a reservoir, equals zero.

The total amount of an element in a given reservoir may also be described as the product of its average concentration and the volume of the reservoir. Generally, the net flux (qJ .. ,.) of an element (n) through a reservoir (x) with volume V .. in which it has a residence time t..,,. can be given by: cp .. ,.= C .. ,..V .. /t .. ,.. Figure 1 a illustrates a network of 7 reservoirs between which transport of material takes place, viz. the

~ .

D. H. SPAARGAREN. H.J. CECCALDI.

Table 1 Abundances (log mo/ar concentrations) of chemica/ elements in various organisms.

Atomic ·, Various number Element crustaceans1

1 H 1.81 ± 0.28(80} 2 He 3 Li 4 Be 5 8 6 c 0.89 ± 0.09(13} 7 N - 0.05 ± 2.20(93} 8 0 1.63 ± 0.05(68) 9 F - 1.69 ± 0.19(10)

10 Ne 11 Na - 1.10 ± 0.37( 8) 12 Mg - 1.54 ± 0.41(35) 13 Al - 2.96 ± 1.17( 6) 14 Si - 1.88 ± 0.66(18) 15 p - 1.11 ± 0.22( 5) 16 s - 1.59 ± 0.55(18) 17 a - 1.01 ± 0.47(11} 18 Ar 19 K - 1.12 ± 0.20(19} 20 Ca - 0.96 ± 0.95(53) 21 Sc 22 Ti 23 v - 5.48 ± 0.34( 2) 24 Cr 25 Mn - 3.61 ± 0.87(19) 26 Fe -2.87 ± 0.89(43) 27 Co 28 Ni 29 Cu - 3.42 ± 0.79(67) 30 Zn -3.17 ± 0.41(26} 31 Ga 32 Ge 33 As - 4.54 ± 1.40(18) 34 Se 35 Br - 2.87 ± 0.21( 8} 36 Kr 37 Rb 38 Sr 39 y 41 Nb 42 Mo - 5.85 ± 0.06( 2) 47 Ag 48 Cd 49 ln 50 Sn 51 Sb 53 1 -4.81 ± 0.78(54) 54 Xe 55 Cs 56 Ba 57 La 58 Ce 74 w 79 Au 80 Hg 81 Tl 82 Pb - 5.o7 ± 0.80(10) 83 Bi 86 Rn 88 Ra - 13.58 ± 0.22( 4) 90 Th 91 Pa 92 u

1 Derived from Vinogradov (1953, ch. XVI). 2 Derived from Sidwell et al. (1977; 1978). 3 Derived from Schmidt-Nielsen (1975). 4 Derived from Yamamoto et al. (1980).

Finfish, molluscs and crustaceans2

- 3.99 ± 0.37( 14)

- 1.43 ± 0.21(109) - 1.85 ± 0.27( 79) - 3.05 ± 0.50( 29}

- 1.17 ± 0.24(140)

- 1.31 ± 0.34( 72)

- 1.13 ± 0.11(122) - 1.94 ± 0.35(139)

- 5.05 ± 0.55( 22) - 5.46 ± 0.30( 19) - 4.59 ± 1.08( 69) - 3.41 ± 0.58(133) - 5.04 ± 0.59( 24) - 5.53 ± 0.36( 14) - 4.11 ± 0.57( 84) - 3.45 ± 1.53( 72)

-4.24 ± 1.14( 58) - 5.17 ± 0.18( 15)

- 5.24 ± 0.43( 9)

- 5.62 ± 0.15( 4)

- 4.82 ± 0.40( 23)

- 5.00 ± 1.56( 67)

-5.84 ( 2)

- 5.60 ± 0.56( 87)

- 5.02 ± 0.87( 34}

lndicated are log C; ± standard. deviation. (number of obseryation~).

' ·~' ' Marine Man· algae4

2.00

-2.69 1.18 0.33 1.61

-1.19 -0.83 -1.69 - 1.07

-2.73

-0.49 -2.30 - 1.11 -1.37

- 1.05 -0.79 -0.43 -0.99

-4.50 -5.30 -5.64 -5.44

-3.14 -3.56 -6.80 -6.05 -5.00 -3.72 -6.77

-2.54

-6.20

-5.50

terrestriallithosphere (11), the marine lithosphere (ml), the terrestria1 hydrosphere (1 h), the marine hydrosphere (mh), the atmosphere (at), the terrestrial biosphere (lb) and the marine biosphere (mb). The abbreviations given in parenthesis appear as indices with thP. symbols for

volume, average concentration and residence tiine of elements for the various reservoirs considered. The right direction of the net fluxes cannot always be given as they are not always the same for various elements. For calculations, however, this is not a problem: for each

66

l .1

l

i

flux entering or leaving a reservoir, a certain direction is merely assumed, and the algebraic sum of ali fluxes coming together in a certain reservoir is postulated to be zero. If, from such calculations, a negative value appears for the flux of a certain element, this means that the actual flow direction is opposite to that initially assumed.

Table 2

ELEMENT AL COMPOSITION OF MARINE ORGANISMS

The model represented in Figure 1 a firstly shows the circulation of elements driven by merely physical forces, transporting elements from the lithosphere to the terrestrial hydrosphere (fresh water), to the ocean waters and back to the (marine) lithosphere, with shunt pathways between terrestrial lithosphere, fresh water and seawater by the atmosphere. Also, two biological

Abundances (log mo/ar concentrations),jluxes (log mole per year) and residence times (log number of years) of chemica/ elements in ocean water.

Atomic number

1 2 3 4 5 6 7 8 9

10 Il 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 jJ 34 35 36 37 38 39 41 42 47 48 49 50 51 53 54 55 56 51 58 74 79 80 81 82 83 86 88 90 91 92

Element

H He Li Be B c N 0 F Ne Na Mg Al Si p s a Ar K Ca Sc Ti v Cr Mn Fe Co Ni Cu Zn Ga Ge As Se Br Kr Rb Sr y Nb Mo Ag Cd In Sn Sb 1 Xe Cs Ba La Ce w Au Hg, Tl Pb Bi Rn Ra Th Pa u

•> Derived from Brewer (1975).

1.74 - 8.77 - 4.59 - 9.20 - 3.39 - 2.64 - 1.97

1.74 - 4.17 - 8.16 - 0.33 - 1.27 - 7.13 - 4.15 - 5.70 - 1.55 - 0.26 - 6.96 - 1.99 - 1.99 -10.89 - 7.70 - 7.30 - 8.24 - 8.44 - 7.46 - 9.10 - 1.55 - 8.10 - 7.12 - 9.37 - 9.16 - 7.30 - 8.60 - 3.08 - 8.62 - 5.85 - 4.04 -10.82 -10.00 - 7.00 - 9.40 - 9.00 -12.10 -10.08 - 8.70 - 6.30 - 9.42 - 9.52 - 6.82 -10.70 -10.00 - 9.30 -10.70 - 9.82 -10.30 - 9.70 -10.00 -20.57

. -15.52 -10.40 -15.70 - 7.85

10.15

10.60

11.22

12.94 12.75 11.97 12.70 11.15

12.84

12.26 13.11

5.61 9.29 8.90 9.08 8.66

11.34 7.53 8.59 8.70 9.68 7.73

. 9.10 8.20

10.02

8.64 10.46

8.80 7.10

8.56 9.20

6.80 9.67 7.62

6.72 5.10 6.37

8.80

8.40

6.77

67

Goldberg et al., 1971

6.36

7.11

5.72

7.83 7.08 2.00 4.26 5.26

8.00

6.85 6.00 4.60 4.11 4.90 3.78 4.00 2.30 4.48 4.95 4.30 4.30 4.00

4.70 4.30

6.60 6.60

5.30 4.60

3.85 5.60

5.78 4.60 2.78

5.08 5.30 4.90

2.60

2.30

6.48

'te

Fowler, 1977

1.59 1.43 3.08 3.56 3.61 3.89

3.89

Calculated: see text

11.55 1.10 5.34 9.78 6.65 7.45 8.18

11.94 6.09 2.16

10.04 9.15 3.35 6.39 4.90 9.10

10.44 3.80 8.83 8.88 0.04 3.29 3.74 2.85 2.71 3.75 2.17 3.77 3.28 4.31 2.12 2.38 4.30 3.06 8.64 3.15 5.97 7.84 1.11 2.05 5.10 2.99

·3.44 0.40 2.48 3.91 6.42 3.36 4.31 6.06 2.24 3.00 4.59 3.47 4.40 3.98 4.64 4.40

- 6.00 - 0.85

4.30 -0.86

7.05

l O. H. SPAARGAREN. H. J. CECCALDI 1

@ Flux (mol·yr-1 )

Resodence tome ( yr)

Volume ( 1)

· Concentration (mol ·1-1 )

Figure 1

b

c

Schemes for the circulation of elements through various biogeochemical compartments. For the direction of the net transport between 2 spaces, an arbitrarily chosen direction is indicated which, also dependent on the element concerned, may have a negative value.

compartments are discriminated, viz. tho se of organisms living on the land and in fresh water and those of seawater organisms. The terrestrial (including freshwa­ter) biosphere exchanges material with the terrestrial lithosphere, the terrestrial hydrosphere and the atmos­phere; the marine biosphere is assumed here to exchange only with seawater and the marine lithosphere (marine sediments). Both biospheres impose on the abiotic transport of elements a circulation driven by biological mechanisms. Even in this extremely simplified model, it is for the moment impossible to quantify ali the various fluxes, even for one single element. In this context, we restrict ourselves to the fluxes which pass the oceanic compartment and refer to a slightly" simplified model (Fig. 1 b ), in which the terrestrial a bio tic compartments and the atmosphere are combined. In equilibrium, the influx of a certain element to the ocean equals the outflux ofthat element. We may divide the influx to the ocean (Fig. 1 b) into a part which bas passed terrestrial organisms and a current, cp~, which

68

merely by physical forces enters the ocean. Similarily, we may also di vide the ocean effiux into a current which passed marine organisms and a merely abiotic 1 precipitation, cp2. For each element holds: ~

oceanic flux = (biotic influx + abiotic influx) = biotic effiux + abiotic effiux or:

V,,..C,,. V.,.11 .C.,.z, cp,,. = = + cp2.

-r.,.,. 't,z, (1)

The abiotic effiux from the ocean, cp2, can also be expressed as being a certain fraction (z) of the biotic effiux, or:

V.,.11 .C,11 cpz=Z.

't.,.z, (2)

By combining equations (1) and (2) and taking the logarithm, it follows that:

V.,.z, log cp.,.,.=log C.,.z,+log (1 +z). -.

't,z, (3)

For a still further simplified model (Fig. 1 c), combining both biospheres to one compartment, Vtb, it may similarly be derived that:

log cp,,.= log C,11 +log ( 1 + z'). V,z,, 't,z,

(4)

in which z' represents the ratio between abiotic and biotic oceanic influx. Equations (3) and (4} will be used (section Ille) to relate data on oceanic fluxes (cpmh) of various elements with values for their concentration in biological material (Cm~~, C,h).

RESULTS

Elementary chemical composition of (marine) organisms

The data on the concentrations of various elements in living organisms as considered here refer to whole animal averages. This is, of course, a very erode approach, as large differences in the chemical compo­sition of various body parts are to be expected. Also one may expect large differences in chemical composition within one species, related to numerous internai and extemal circumstances (e.g. age, feeding condition, sexual maturity, season, geographical distribution). Nevertheless, the figures offer a useful possibility of comparing average concentration values for various elements, comprising ali intraspecific variation. By combining data from different species, the interspecific variation is also included. The frequency distributions of the log-concentration values of various elements (Fig. 2) do not support the hypothesis of Liebscher and Smith (1968) and Giesey and Wiener (1977) that only for non-essential elements the log-concentration values are normally distributed. Hence, a distinction into essential and non-essential elements cannot be made on the basis of the frequency distribution of the concentrations of various elements.

No

10 •• H c 42 • •• 4

14

0 0

F Na ·

0 0

Si 24 p

tl

12

0

10 10 K Ca

0 -2 -4 -6 0 -2 -4 -6

Figure 2

40

30

20

10

0

12

• 0

4

0

4

ELEMENT AL COMPOSITION OF MARINE ORGANISMS

N

Mg

s

v

0 -2 -4 -6

48 0

•• 24

12

0

Al

0

Cl

0

Mn

Ra

o~~~~~~~~ -6 -8 -10 -12 -14 -16

lOC) Cj

Frequency histograms of the logarithms of the molar concentrations ofvarious elements in biological material (various crustacean species). Data derived from concentration values compiled by Vinogradov (1953, chapter XVJ). Curves represent the most likely Gauss-distributions.

Apart from the obvious differences in the average concentrations of different elements, it is clear that the bandwidth of the concentration of various elements is widely variable. No general explanation exists for the large differences in variability in the concentrations of various elements. A normal distribution of the log­concentration values indicates that the concentrations of various elements are not symmetrically distributed: the concentrations of various elements are more sharply limited at lower values, whereas high values may frequently occur. The log-concentration values often extend over a range of several decades, which means that a value for the concentration of a certain element may be up to 100 times larger or smaller than the average concentra­tion found for that element. Despite this large variability, it is clear that there exist certain limits to the concentrations in which varions elements may be found in living tissue. The average concentrations in which various elements are found in living organisms decreases more or less exponentially with increasing atomic number (Fig. 3). A less significant biological function tends to be ascribed

69

to heavier elements, which occur in lower quantities. As stated before, there are no reasons to assume that the heavier elements are less important. The low internat concentrations of the heavier elements are without exception associated with still lower concentrations in the environment (Fig. 4). The concentration factors range between values of 0.1 up to 105

• Only a few elements are found to be present in lower concentrations than those in the enviionment, viz. 0, Na, Mg, Cl and S. Three elements are on the average present in concentration almost equal to those in the environment (H, Ca and Br), but ali other elements for which data are available are concentrated at least 10 times. The absence of accumulation in the above-mentioned essential elements clearly indicates that the concentration factor does not yield a good measure for the biological significance of an element. Nor is the presence of accumulation proof that a substance is actively extracted from the environment.

A better explanation for the low internai concentrations generally found in heavier elements may be sought in the fact that the heavy elements are often associated with large organic molecules, which in living tissues are

D. H. SPAARGAREN. H.J. CECCALDI

loo C;

0

-5

-10

.. 15

0 20 40 60 80

Figure 3 Logarithms of the internai (molar) concen­trations of various elements in relation to their atomic number. e, average internai concentrations as found ln varlous crusta­ceans (data from Vinogradov, 1953); A idem in finfish, molluscs and crusta­ceans (derived from data compiled by Sld­well et al., 1977; 1978); •Idem, in human tissue (data derived from values glven by Schmidt-Nie/sen, 1975); x, Idem in a marine algae, Eisenia bicyclis (data from Yamamoto et al., 1980).

atomic number

log C; /C1

6

4 c • F

: 1 2

0 Figure 4 .... Concentration of various elements in rela-tion to concentration in seawater presen-ted as a function of atomic number. e. log CJC. values in mixed crustacean species (data derived from Vinogradov, 1953); A, idem in finfish, mol/uses and crustaceans (data derived from Sidwell, 1977). Ave-rage concentrations of various elements in seawater according to the list glven by Brewer (1975).

0

-2

-4

0

present in relatively small quantities. For instance, relatively light elements like N, P and S are found in small molecules, present in large quantities. Heavier elements like Cr, Mn, Fe, Co, Ni, Cu, Zn are usually associated with larger organic molecules (enzymes, blood pigments) present in smaller amounts, while a very heavy element such as iodine is, in vertebrates, known to be associated with thyroid hormones, transported by the blood in only very small quantities. It is, however, clear that knowledge in this field is very scarce. Also due to the large intra- and interspecific variation, the differences in the internai concentrations of various elements, as found in different groups of organisms, are

p Al & 1

Si •

% .... • No

70

··,t Mn eol !•4

Zn C• • t

Ni • v

"•T Co :-·

I Cl

20

So • t

8• •

t ... •

40

Cd •

Sn •

1 l So •

60

H9 Pb ...

80

.. •

atomic number

not significant. Data on the internai concentrations of various elements in crustaceans (as derived from the data compilation of Vinogradov), in combined data for finfish, molluscs and crustaceans (as derived from the compilation of Sidwell et al., 1977; 1978) and even data on marine algae (as derived from measurements by Yamamoto et al., 1980) are statistically equal. This leads to the conclusion that the elementary chemical composition of living material is for ali organisms essentially the same, in the sense that the concentration of each particular element is "restricted" to about 2 orders of magnitude. It would be interesting to know more about the concentrations of the elements for which data on the

i 1

internai concentration in living tissues are lacking. Table 1 shows that in all cases this concerns elements which are chemically very inert (the noble gases), or which may be expected to be present in very low concentrations (atomic number higher than ca 50) or otherwise escape accurate chemical analysis. The elements for which data are available reasonably fit into the band (Fig. 3, dashed tines) relating the log­concentration to the atomic number. The higher values for the internai concentration of iodine, tin, mercury and lead may be due to the fact that those substances are only determined in organs or whole animais which were suspected to have high concentrations of these substances. The above results show that each element is present in living organisms within restricted boundaries of concentrations. The low concentrations of the heavy elements are easily affected by relatively small amounts of pollution. This explains the toxic effects of heavy metals (in living tissues restricted to very low concentrations), which are today becoming evident in the natural environment. The limited concentration ranges also suggest that so-called "non-essential" elements may also have a function in metabolic processes.

Elementary chemical composition of seawater

As in the case of concentration of various elements in biological material, considered in the previous section, it should be pointed out that in dealing with seawater concentrations in this context, only the order of magnitudes of the concentrations of elements in average seawater will be compared. Although greatly dependent on geographical position, depth, seasonal variation, etc., it is not likely that the concentration of the various elements present in open seawater will vary over much more than one decade of molar concentration. The quantities in which various elements are present in seawater are extremely variable. Only a small number

Figure 5 Concentration ofvarious ele­ments in seawater as a func­tion of their atomic number (a), and more specifically as

-10

a function of their position -15 in the periodic system (b). Data derived from values given by Brewer (1975).

Sc

0 20

y La

a

40 60

ELEMENT AL COMPOSITION OF MARINE ORGANISMS

of elements (Na, Mg, S, Cl, Ca, K) determine the total salinity, whereas most elements are present only in very low concentrations. The modal concentration of the 63 elements given in Table 2 is found at only 81 nmol.l- 1

(log C, = - 7.09). The elements which occur in high concentrations all belong to the first two periods of the periodic system. A simple correlation with atomic weight does not exist (Fig. 5 a). Within one series, one often finds a regular exponential decrease in concentration of the various elements (Fig. Sb), but in severa! series one observes a sudden increase in the seawater concentration with increasing atomic weight. Such irregular increases in the seawater concentrations with increasing atomic weight are found between He(2) and Ne(IO), between Li(3) and Na(11), between Be(4) and Mg(l2), between F(9) and Cl(17), between Ne(10) and Ar(l8), between Sc(21) and Y(39) and between Cr(24) and Mo(42). The concentrations of the various elements in seawater are roughly related to their chemical properties (atomic number), but it is clear that other factors are also involved. Numerous attempts have been made to explain the differences in concentrations of the various elements in seawater. For instance, chemical reactivity and solubility of the least soluble compounds in which the elements mainly occur, were incorporated in the various considerations (e.g. Goldberg, 1963; Brewer, 1975). However, none of the various factors taken into consideration could yield a satisfactory general expia­nation for the differences in concentration of the various elements in seawater. In the context of this work, it was attractive to relate the concentration of the various elements to the influx (or effiux) values as reflected in the oceanic residence times. It appears that there exists a positive relation between the oceanic concentration of an element and its oceanic residence time, but there is still a considerable residual variation which appeared to be related to the atomic number. If the log of the oceanic flux (cp,= CeY./t,) is plotted against the atomic number of the

log Ce 0

Na Co

N s

K Ca é

Br B

Sr

LI Ab

Mo 0 Fe

cè$ v Gr

8 Mn Ni

Sb s.e 0

ow 0 Pb Bi co

Xe

0 Sn Nb Au

-15 ... b 0 Ra Pa Ra

1 6 ~~ ~..,....._..~~...,--.-.-r--7"'.,........~~

atoAAc number o r a :.:: m y: . w :m lZIIJ group

71

D. H. SPAARGAREN, H. J. CECCALDI

:asi~~~~ Mg• e 1(

12 Al o •

9

6

3

Au .

Figure 6 Oceanic input ( =oceanic output) of various elements as a function of their atomic number. On the Y-axis the logari­thm of the fluxes (expressed in molfyear) as derived from the difference between loge. and logt. (C. and t. values as given by Brewer, 1975).

0,_----,-----~----r---~r----,----~----~-----r----,---0 20 40 60

various elements (Fig. 6), an approximately linear relationship becomes evident. The negative slope indicates that lighter elements are transported at a faster rate than the heavier elements, the decrease in flux values being exponentially related to the atomic number of the elements. It may be asked whether the remaining variation in the relation as illustrated in Figure 6 points to other factors involved in the relation between flux and atomic number, or whether this may ascribed to inaccuracies in the estimates for oceanic residence times (or in the measuring procedure for determining the concentrations of the different elements in seawater). Barth (1952) derived values for the oceanic residence times for a limited number (15) of elements, using data on river inftuxes which only took account of dissolved substances.

log (Zé) cale.

12

10

8

6

80 atomic number

Goldberg and Arrhenius (1958) derived independent estimates based on the effiux of elements and the rate at which they were incorporated into marine sediments. Despite the different procedures, the values showed a reasonable similarity. Brewer (1975), however, advocates extreme caution in the use of the value for oceanic residen.ce time, as locally--for instance in a more or less closed estuary--great deviations may be found. If we assume the variability in the relation between flux and atomic number of the various elements to be due to inaccuracies in the estimates for the oceanic residence time, then, by assuming a linear relationship, it is possible to derive alternative values for the oceanic residence times ('tca1c), merely based on the seawater concentration of each element (C.) and its atomic number (N.) according to: log 'tcalc = . log C. +

Cl ... . c: .~ .

.. • .. • .. .

r:': ~ ~~Mo

~ 4 Fe S./ •v.

c>--AI- ~ .~NI Au . ~~ ·~· 'iiMn .. ~ Figure 7

2 7La :. Ca

Oceanic residence times of various ele-• o--o-

ments log ( t.)c.w estimated from their concentration in seawater and their atomic

Sc number (N) according to log ( t.)corc = 0 . 0.056 N.+log C.+9.76, in relation to the values (•) as derived by Goldberg (1972) and (0) Fowler (1977).

2 4 5 6 7 8 9 log('Oollit.

72

log~

14

12

10

8

6

-8 .

0.056Nn + 9.76 (Table 2). Although a digression in the context of this paper (in the text to follow the estimated values are still used instead of the calculated values), this method also offers an interesting possibility of deducing values for the oceanic residence times, even for elements for which up till now no data were available. Generally, there is a reas~able similarity

log~

Figure 8 Oceanic input (e) of a number of elements for which data are available concerning their concentration in biological material (Â, shown in the lower diagram), in rela­tion to their atomic number.

12 r.v:

Figure 9

•• . Ti

1 "'

,, ,, F l>.e •

c'6cr •/ •• Mo •v v • A -: :.\ Mn Cu NIA Ni,P Pb e e

-6

"• .

•• • Co 0

-4

Al Al . "'

9

6

0

~· ... :-~/ SI#M9 Cl~ AMO

• • . "'

p p

p

•

Br A • •

-2 0 log Cj

Oceanic fluxes of various elements in relation to their concent~ation in living organisms: e, crustaceans, finfish and molluscs (data from Sidwell, 1977); ~.a marine algae, Eisenia bicyclis (data from Yama­moto et al., 1978).

20

73

ELEMENT AL COMPOSITION OF MARINE ORGANISMS

between the values for oceanic residence times as given by Goldberg et al. (1971) and those derived here (Fig. 7). In 1977 Fowler independently derived new values for the residence times of six elements. In ali cases, the residence times obtained were shorter than those given by Goldberg; the considerable differences in the various estimates favours the idea that the residual

40 60

Pb

... , 80

log Cfmb

0

-3

-6

atomic number

variation in the relation between fluxes and residence times is due to inaccuracies in the estimates for the 't­

values. Furthermore, it appears that in most cases the values as derived by Fowler approach more closely the values as derived here using seawater concentration, atomic weight and the combined data for oceanic residence times of various elements, as given by Goldberg et al. (1971).

Relations between the elementary chemical composition of seawater and tbat of (marine) organisms

The oceanic fluxes of various elements show a strong similarity with the concentrations of these elements as observed in biological material: Figure 8 shows the oceanic fluxes for those elements for which also data on the internai concentrations in living organisms were available (shown in the lower diagram) as a function of atomic number. It should be noted that the flux data (upper diagram) are derived from oceanographical literature, completely independent of the data on biological concentrations (lower diagram). If plotted against each other (Fig. 9), an almost linear relationship is obtained in which the calculated slope appears to be 100 with a Y-intercept of 13.84. The linearity of the relation between log cpmh and log cmb is in accordance with the moder rèpresented by equation (3), if the term (1 + z)V mb/'tmb remains constant for different elements.

D. H. SPAARGAREN, H. J. CECCALDI

As it was shown above that there are no significant differences in the elementary chemical composition of various living organisms, we can make a further simplification of the model represented by equation (4), or written in a different way:

log cm,= log c,, +log "t"mll -log v mil

+log ( 1 + z') (V ,11/-r,,) (5)

Multiple linear regression analysis of the available values for log Cmh, log C,b and log "t"mh yields: log Cmh = 1.03 log C,b + 0.94 log "t"mh - 6.88 (r = 0.942; N = 25). In agreement with equation (5) the coefficients (1.03 and 0.945) nearly equal 1.0. The high correlation coefficient shows that the seawater concentrations of various elements may to a great extent be ascribed to the biological concentrations (C,b) and the oceanic residence times (-rmh).

The above model {5) implies that the seawater concentration of each element is positively related to log C,b and the total volume of the biosphere (Vrb), hence to total biomass (V,b.C,h). If in the geological past changes have occurred in the total biomass, then this will have been reflected in the concentration of the various elements in the ocean water. An increase in total biomass may very likely be assumed to have taken plate when ocean life evolved to terrestrial forms. The concurrent rise in seawater salinity during the period that land invasion took place was, for different reasons, suspected from previous work (Spaargaren, 1978). On a small time scale and in an enclosed volume of seawater, changes in biomass may affect environmental concentrations in an opposite manner. The data on the elementary chemical composition of living organisms and on that of seawater yields the opportunity to assess tentatively the compositional changes in an enclosed volume of seawater when living organisms develop, as for instance during a period of plankton bloom. If, during a period of plankton development, no elements are added or removed from a certain volume Vo of seawater then for each element holds:

(6)

where c... represents the original concentration of a certain element in seawater, C •. , the same at time t when the amount of that element incorporated in biomass has increased from zero to V,,,c,. Hence,

(7)

or

Co,t .I00%=(1- C, Vi,r ). 100%. C C0 0 • V0 o, 0 •

(8)

From this it is clear that the relative decrease in concentration of certain elements in seawater strongly depends on the concentration factor (CI/Co,o) and the amount ofbiomass (V1•1) formed. Those elements having a high concentration factor will be exhausted from the wate"r at the fastest rates. Table 3 shows the changes in

74

relative composition of various values for V,, varying between zero and 20.10-6.Vo. The rapid decrease in concentration of sorne trace elements may explain the harmful effects of plankton development, as for instance in the phenomenon of the red tides, in a different way. From this it is also clear that growth limitation may not only be due to changes in concentration of common nutrients (C, N, P, Si) but also to a number of other components of seawater (e.g. Al, Ti, Mn, Fe, Ca, Cu, Zn, Hg, Se). Hence, in an enclosed seawater volume, changes in the amount of biomass may be expected to influence the chemical composition of seawater. Furthermore, the observed relation between the total oceanic fluxes ( <i>mh) of various elements and the biological concentrations (Cmh) suggests that the biotic fluxes through the oceans strongly contribute to the total fluxes. There is no proof that for ali elements the abiotic fluxes are only minor fractions of the total fluxes, but the observed relationship (Fig. 8, 9) makes it plausible that the elementary composition of seawater is strongly determined by biological accumulation processes. Many elements which occur in seawater must be assumed to be present in amounts given by non-stable flow-through equilibria in which concurrent physico-chemical processes also play a role but do not necessarily reach steady state equilibria. It is likely that in the process of evolution, living organisms did not merely adapt to various environmental conditions but that conversely, they also created various environmental conditions. Apart from changing to aerobic conditions, also changes in the elementary composition of the hydrospheres must have taken place.

CONCLUDING REMARKS

Although certain correlations between the elementary composition of seawater and living matter have become evident, it is clear that numerous questions remain unsolved and should be the subject of further research. Firstly, the number of elements considered in this study is far from complete. Only for ca 30 elements are data on their internai biological concentrations availab~e. It will be worthwile to perform additional measurements, in order to complete Table 1. The observed correlations show a considerable variation. lt could be that part of the variation must be ascribed ascribed to measurement inaccuracies. With improved analytical techniques, it would be very useful to collect more accurate data and subsequently search for explanations for the residual variance. In the present study it is suggested that the biological residence times for various elements are approximately the same, not dependent on atomic number. Experi­mental data on biological residence times of various elements are available in the literature, but only for a relatively small number of {radioactive) elements and often expressed semi-quantitatively in not comparable units. 1t would be rewarding to obtain more complete

ELEMENT AL COMPOSITION OF MARINE ORGANISMS

Table 3 Effect of the formation of biomass in a c/osed volume of seawater on the seawater elementary composition. For exp/anation of the symbo/s, see text.

(Co,t/Co,o) X 100% Element no. Element Log Co,o Log Ci* V;,t/Vo = uo-6 5.10-6 20.10-6

1 H 1.74 2.00 100 100 100 5 B - 3.59 - 2.69 100 100 100 6 c - 2.64 1.18 99.3 96.7 86.8 7 N - 1.97 0.33 100 99.9 99.6 8 0 1.74 1.63 100 100 100 9 F - 4.17 - 3.99 100 100 100

10 Na - 0.33 - 1.43 100 100 100 12 Mg - 1.27 - 1.85 100 100 100 13 Al - 7.13 - 3.05 98.8 94.0 76.0 14 Si - 4.15 1.88 100 93.9 99.6 15 p - 5.70 1.17 96.2 83.1 32.2 16 s - 1.55 1.11 100 100 100 17 Cl - 0.26 1.31 100 100 100 19 K - 1.99 1.13 100 lOO 100 20 Ca - 1.99 1.94 100 100 100 22 Ti -10.70 - 4.50 99.8 99.2 96.8 23 v - 7.30 - 5.05 100 99.9 99.6 24 Cr - 8.24 - 5.46 99.9 99.7 98.8 25 Mn - 8.44 - 4.59 99.3 96.5 85.8 26 Fe - 7.46 - 3.41 98.9 94.4 77.6 27 Co - 9.10 - 5.04 98.9 94.3 77.0 28 Ni - 7.55 - 5.53 100 99.9 99.8 29 Cu - 8.10 - 4.11 99.0 95.1 80.5 30 Zn - 7.12 - 3.45 99.5 97.7 90.6 31 Ga - 9.37 - 6.77 100 99.8 99.2 33 As - 7.30 - 4.24 99.9 99.4 97.7 34 Se - 8.60 - 5.17 99.7 98.9 94.6 35 Br - 3.08 - 2.87 100 100 100 38 Sr - 4.04 - 2.54 100 100 99.9 42 Mo .- 7.00 - 5.24 100 100 99.9 48 Cd - 9.00 - 5.62 99.8 98.8 95.2 50 Sn -10.08 - 4.82 81.8 90.7 53 1 - 6.30 - 5.00 100 100 lOO 56 Ba - 6.82 - 5.84 100 100 100 80 Mg - 9.82 - 5.60 98.3 91.7 66.8 82 Pb - 9.70 - 5.02 95.2 76.1 4.3 90 Ra -15.52 -13.58 100 lOO 99.8

• Combined data from crustaceans, finfish, molluscs, man and marine algae.

data on the average time that varions elements are incorporated in living tissue. Values for the biological residence times would yield a good measure for their biological reactivity, and might be very useful in explaining the residual variability in the correlations observed. The flow of elements through varions compartments were considered in this study to be in equilibrium. The method of data analysis presented, discriminating varions compartments exchanging chemical elements with other compartments at a certain rate, also offers possibilities to define other compartments with, for instance seasonally, changing volumes. This approach might be useful in studies on the biological productivity in restricted areas by measuring concentrational changes in previously defined compartments affected by the formation of living matter. For the elements studied, those elements should preferably be chosen w~ich are

75

strongly accumulated by living organisms (see Fig. 4), which can easily and accurately be measured and which do not show a strong abiotic turnover. Using a simple 3-compartment system as depicted in Figure 1 c, it might be possible to derive changes in biological standing stock from changes in elementary chemical composition of an aquatic compartment closely associated with the population studied.

The flow of elements through, as well as the storage of elements into varions compartments is closely related to energy conversion. Accumulation and transport proces­ses must both be considered to require energy at the expense of increased entropy. Further studies on the energetic aspects (-storage, -flow, -conversion, -dissipa­tion) of element turnover between varions compartments constitute another domain in which many questions remain to be solved.

D. H. SPAARGAREN. H. J. CECCALDI

Acknowledgements

Part of this study was carried out at the Station Marine d'Endoume, Laboratoire de Biochimie et Écologie des Invertébrés marins, École Pratique des Hautes Études, Marseille, France. The first author wishes to express his gratitude to staff and personnel of this laboratory for their kind hospitality during his stay at the institute. Many thanks are also · due to Dr. R.F. Burton, University of Glasgow, Scotland, Pr. Dr. T. Yamamoto,

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Brewer P. G,. 1975. Minor elements in seawater, in: Chemical oceanography 1, edited by J. P. Riley and G. Skirrow, Academie Press, London, 415-498.

Fowler S. W., 1977. Trace elements in zooplankton 'particulate products, Nature, 269, 51-53.

Giesey J.P. jr, Wiener J.G., 1977. Frequency distribution of trace metal concentrations in live freshwater fishes, Trans. Am. Fish. Soc., 106. 393-403.

Goldberg E. D., 1963. The oceans as a chemical system, in: The Sea, vol. Il, edited by M. H. Hill, Interscience, London, 3-26.

Goldberg E. D., Arrhenius G. O. S., 1958. Chemistry of Pacifie pelagie sediments, Geochim. Cosmochim. Acta, 13, 153-212. Goldberg E.D., Broecker W.S., Gross M.G., Turekian K.K., 1971. Radioactivity in the marine environment, Nat!. Acad. Sciences, Washington.

Kossina E., 1921. Die Tiefen des Weltmeeres, E. S. Mitt1er und Soho, Berlin. ·

Liebscber K., Smith H., 1968. Essential and non-essential trace elements, Arch. Environ. Hea/th, 17, 881-890. MacKenzie F. T., 1975. Sedlmentary cycling and the evolution of seawater, in: Chemical oceanography 1, edited by J. P. Riley and G. Skirrow, Academie Press, London, 309-365.

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Kyoto University of Education, Kyoto, Japan, as weil as to colleagues at the Netherlands Institute of Sea Research, especially to Dr. J. van Bennekom for critically reading the manuscript, to Mrs. L. Everhardus and J. de Ligondes for typing the text, and to Mr. H. Hobbelink and Dr. M. Djabali for preparing the final drawings.

Pinder J.E., Giesey J.P., 1981. Frequency distribution of the concentrations of essential and non-essential elements in largemouth bass, Micropterus sa/moides, Eco/ogy, 62, 2, 456-468. · Scbmidt-Nielsen K., 1975. Animal physiology. Adaptation and environment, Cambridge University Press, 699 p. Sidwell V.D., Buzzel D.H., Foncannon P.R., Smith A.L., 1977. Composition ofthe edible portion of raw (fresh or frozen) crustaceans, finfish and molluscs. Il. Macro elements: sodium, potassium, chlorine, calcium, phosphorus and magnesium, Mar. Fish. Rev., 39, 1, 1-11. Sidwell V. D., Lomis A. L., Lomis K. J., Foncannon P. R., Buzzel D.H., 1978. Composition of the edible portion of raw (fresh or frozen) crustaceans, finfish and molluscs. III. Micro elements, Mar. Fish. Rev., 40, 9, 1-21. Spaargaren D.H., 1978. A comparison of the blood osmotic composition of various marine and brackish water animais, Comp. Biochem. Physio/., 60, 327-333. Vinogradov A. P., 1953. The elementary composition of marine organisms, Yale University, New Havens. Yamamoto T., 1972. The relation between concentration factor in seaweeds and residence time of sorne elements in seawater, Rec. Oceanogr. Works Jpn, 11, 65-72. Yamamoto T., Otsuka Y., Okazaki M., Okamoto K., 1980. A method of data analysis on the distribution of chemical elements in the biosphere, in: Analytica/ techniques in environmental chemistry, edited by J. Albniges, Pergamon Press, London, 401-405.