This research manuscript reports the heavy metal accumulation in four marine seaweeds <i> sp. </i> 1) <i> Caulerpa sertlatioides </i> (Cuba); 2) <i> Caulerpa cf. brachypus </i> ; (Bali, Indonesia); 3) <i> Undaria pinnatifida </i> (West-Donegal, Ireland); 4) <i> Ulva lactuca </i> (Easters-Scheldt, the Netherlands). Mechanical pressure at 10 bar of fresh seaweed fronds <i> casu quo </i> biomass in the laboratory delivered seaweed moisture which was analyzed by Inductively Coupled Plasma Spectroscopy (ICP)-techniques for heavy-metals = [HM], (Al, As, Cd, Co, Cr, Cu, Fe, Mo, Ni, Pb & Zn). Three important observations were made: 1) The [HM] in the seaweed moisture is higher than in the surrounding seawater which directs to mechanism(s) of <i> bio-accumulation </i> ; 2) The accumulation factor [AF] is varying per metallic-cation with an overall trend for our four seaweeds and sampling locations for [HM] are: As & Co & Cu: 5000 - 10,000 μg/l; Ni & Zn: 3000 - 5000 μg/l; Cd: 2000 - 3000 μg/l; Cr: 1000 - 2000 μg/l; Al: 200 - 1000 μg/l; Mo & Pb & Fe: 0 - 200 μg/l range. 3) Seaweed moisture detected that [HM]: Pb & Zn & Fe —which all three could not be detected in the seawater—supports the view that seaweeds have a preference in their <i> bio-accumulation </i> mechanism for these three HM. Major conclusion is in general that “overall” for the macro-elements Ca, Fe, K, Mg, Mn, Na, P & S in the moisture of the four seaweed species the concentration is lower in the seaweed species, or equals the concentration, in comparison to the surrounding sea water. For the HM (Al, As, Cd, Co, Cr, Cu, Mo, Ni, Pb & Zn) the opposite is the case species and is the concentration “overall” higher in the seaweed species in comparison to the surrounding sea water. Further topics addressed include strategies of irrigation of the Sahara desert with the moisture out of seaweeds under conditions of low anthropogenic influences.
Heavy Metal (HM), often used in this manuscript is a general collective term which applies to the group of metals and metalloids with an atomic density greater than 4 g/cm3 which have in general a large impact on environment in general and inhabiting organisms (flora and fauna) including at the highest trophic level of the ecosystem, the humans [
The following Heavy Metals (HM) from the Periodic System (
accumulate in living systems with resultant toxicity. The metals included in the “Borderline” category exhibit “Class a” and “Class b” properties. In some cases, a clear distinction between the three different categories cannot be made. Some fall under both categories; like copper may be either “Class b” or “Borderline” depending upon whether it is Cu(I) or Cu(II), respectively; lead may be either “Class b” or “Borderline” depending upon whether it is Pb (II) or Pb (IV), respectively; and iron may be either “Class a” or “Borderline” depending upon it is Fe (III) or Fe (II), respectively (reviewed: [
We hope to address answers to the following questions:
1) What is the impact of these selected intermediate remote oceanic locations on [HM] concentration in seaweed moisture in comparison to FAO defined [
2) Because seaweeds are used in field studies as a bio-monitoring system for HM contamination of the oceanic environment [
3) If such a correlation is confirmed by literature data the mechanism of bio-accumulation of HM in the metabolism of the living seaweed at such high concentrations needs to be understood and described (see discussion);
4) After checking the correlation between oceanic HM contamination and [HM] in seaweed moisture: a) the laboratory experiment described in this manuscript; b) literature studies, finally the most important question can be posed: Are the oceanic waters around the Sahara clean enough to form a sound basis for a seaweed industry which in the end can deliver irrigation water with [HM] far below the FAO-thresholds for irrigation water? Our initial hypothesis is yes they can!
The following materials were used in the experiments.
− Ulva lactuca (Chlorophyta): =>origin: KatseHeule, Easters-Scheldt, The Netherlands; approximate coordinates: 51˚32'30N and 3˚52'E (Figures 2-5).
− Caulerpa sertularioides (Chlorophyta): =>origin: Denpassar, Bali, Indonesia; approximate coordinates: 8˚41'S and 115˚17'E (
− Caulerpa cf. brachypus (Chlorophyta): =>origin: Cuba): approximate coordinates: 23˚50'S and 82˚50'W (
− Undaria pinnatifida, (Wakame) (Phaeophyceae): =>origin, Kilcar, West-Donegal, Ireland, approximate coordinates: 54˚37'N and 8˚37'W (
Ulva lactuca was collected ourselves and brought directly to the laboratory―together with surrounding water―for species determination with a binocular and microscope according to the criteria of [
To be able to press juice out of the seaweed biomass the materials were first pulped using a laboratory homogenizer (manufacturer: Foss Tecator, type: Tecator 1094 homogenizer). For seaweed biomass a smooth knife was used, for others a serrated knife was used. For most materials the lower speed of 1500 rpm was sufficient, for other the higher speed of 3000 rpm was needed. Juice was pressed out of the pulp, approximately 100 grams of pulp was used, using a LLOYD INSTRUMENTS (type: LR30K) testing machine that was fitted with a specially constructed unit for pressing pulps at a maximum pressure of 60 bar (see
1) Al, As, Ca, Cd, Cr, Cu, Fe, K, Mg, Mn, Na, Ni, P, Pb, S & Zn in seaweed moisture and in the sample of the surrounding waters were measured on an ICP-AES (Thermo Iris) according pretreatment SWV E-3404, measurement SWV E-1304 and conservation SWV E-3404 guide lines at the Chemical Biological Laboratory for Soil & Water Research, Wageningen University, Wageningen (The Netherlands).
2) As, B, Ba, Cd, Co, Cr, Cu, La, Li, Mn, Mo, Ni, Pb, Sb, Se, Sn, & V in seaweed moisture and in the sample of the surrounding waters were measured on an HR-ICP-MS (Thermo Element 2) according pretreatment SWV E-3404, measurement SWV E-1325 and conservation SWV E-3404 guide lines at the same laboratory.
Determination of P was performed on an HR-ICP-MS (Thermo Element 2) according pretreatment SWV E-3404, measurement SWV E-1325 and conservation SWV E-3404 guide lines at the same laboratory.
The basic principle of our method is based on the fluid mosaic membrane which surrounds a seaweed cell but also organelles. We call this the “seaweed battery” because by sampling at both sides of the fluid mosaic bilayer we can get an impression of the interior milieu of the seaweed cell. All concentrations of macro- or micro-elements [HM]-indeed at each side of the membrane bilayer-can have distinctive concentration differences dependent on the transport mechanisms (active or passive), and in some way related to their function or seaweed bilayer composition.
Accumulation Factor [ AF ] = HM in the seaweed moisture HM in the oceanic water
The accumulation factor represents the concentration of the heavy metal in the seaweed moisture compared with the concentration in the seawater. Some parameters affecting the performance of this parameter are: 1) the physiological state of the seaweed, 2) the age of the cells, 3) the availability of micronutrients during their growth and finally 4) the environmental conditions during uptake dependent on pH, temperature, light intensity etcetera => see Discussion. To our awareness the “Accumulation factor” based on the described “seaweed battery” principle is new and applied for the first time.
Data processing was performed in Excel and SPSS [
To our awareness the Accumulation Factor [AF] has for the first time been applied in heavy metal [HM] studies with seaweeds.
For the [HM] for all four seaweed-species the following general conclusions can be made based on the Accumulation Factor given in
1) The [HM] in the seaweed moisture is higher than in the surrounding seawater which directs to mechanism (s) of bio-accumulation.
2) Accumulation factor is varying per metallic cation. Overall trend for our four seaweeds and sampling locations for HM are: Cu, Co: (5000 - 10,000 Accumulation Factor [AF] range; Ni & Zn: 3000 - 5000 [AF] range; Cd: 2000 - 3000 [AF] range; Cr: 1000 - 2000 [AF] range; Al: 200 - 1000 [AF] range; Mo, Pb, Mg & Fe: 0 - 200 [AF] range.
3) For the HM Pb, Zn & Fe these micro-elements could not be detected in the seawater, so in order to calculate the accumulation factor we had to use the threshold value of the oceanic water for the ICP technique used. The fact that these HM could not be detected in the oceanic water while their concentration in the seaweed moisture is rather high seems to support the view that seaweeds have a preference in their bio-accumulation mechanism for these three HM (see discussion).
4) In addition to observation 3). Zn falls with [AF] extremely in the extremely high range of 3000 - 5000 for all four seaweed-species. This again partly can be explained because this HM could not be detected in the seawater, and in order to calculate the [AF] we had to use the threshold value of the oceanic water for the ICP technique used.
5) In incidental cases, a certain seaweed has an extremely high AF for a certain specific HM like in case of Ulva lactuca its preference for Ni2+ with an [AF]-factor of ≈5200 (see
From
If we take the “overall” correlation coefficient for macro- and microelements
Fe2+ [mg/l] | Mg2+ [mg/l] | Mn2+ [mg/l] | Cu2+ [µg/l] | Al3+ [µg/l] | Zn2+ [µg/l] | Cd2+ [µg/l] | Co2+ [µg/l] | Cr3+ [µg/l] | Mo4+ [µg/l] | Ni2+ [µg/l] | Pb2+ [µg/l] | ||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
U. lactuca | Mean | 2.74 | 1762.00 | 3.77 | 330.75 | 153.00 | 1232.25 | 2.39 | 13.88 | 18.65 | 14.33 | 157.50 | 1.26 |
(n = 4) | SD | 0.40 | 47.85 | 0.16 | 74.29 | 20.99 | 236.99 | 0.34 | 0.33 | 0.90 | 1.00 | 9.68 | 1.66 |
Oceanic | 0.09 | 1214.00 | 0.01 | 0.13 | 0.30 | 0.30 | 0.01 | 0.01 | 0.01 | 2.07 | 0.03 | 0.04 | |
Ratio | 30.39 | 1.45 | 376.75 | 2544.23 | 510.00 | 4107.50 | 199.17 | 1982.14 | 1865.00 | 6.92 | 5250.00 | 31.38 | |
C. sertlatioides | Mean | 1.08 | 509.25 | 1.18 | 117.85 | 582.75 | 1169.50 | 5.72 | 6.99 | 14.50 | 6.99 | 129.75 | 2.45 |
(n = 4) | SD | 0.04 | 9.03 | 0.03 | 13.23 | 175.55 | 361.52 | 0.47 | 0.21 | 0.39 | 4.61 | 5.32 | 1.53 |
Oceanic | 0.09 | 1206.00 | 0.01 | 0.02 | 0.70 | 0.30 | 0.00 | 0.01 | 0.01 | 1.14 | 0.36 | 0.04 | |
Ratio | 11.94 | 0.42 | 118.25 | 5892.50 | 832.50 | 3898.33 | 2860.00 | 1397.50 | 1611.11 | 6.13 | 360.42 | 61.19 | |
C. brachypus | Mean | 0.90 | 675.50 | 2.05 | 788.25 | 230.00 | 1136.00 | 4.43 | 22.13 | 20.23 | 8.54 | 295.25 | 1.33 |
(n = 4) | SD | 0.14 | 4.12 | 0.07 | 69.21 | 46.45 | 146.50 | 0.22 | 0.22 | 1.25 | 0.35 | 9.36 | 0.95 |
Oceanic | 0.09 | 361.00 | 0.01 | 0.10 | 1.00 | 0.30 | 0.02 | 0.01 | 0.05 | 2.49 | 0.16 | 0.04 | |
Ratio | 9.98 | 1.87 | 204.75 | 7882.50 | 230.00 | 3786.67 | 221.63 | 3687.50 | 396.57 | 3.43 | 1845.31 | 33.19 | |
U. pinnatifida | Mean | 0.25 | 121.25 | 0.02 | 73.90 | 156.00 | 178.75 | 0.81 | 1.04 | 6.16 | 14.80 | 20.08 | 0.09 |
(n = 4) | SD | 0.03 | 5.32 | 0.01 | 12.78 | 9.93 | 18.45 | 0.13 | 0.12 | 0.27 | 3.00 | 3.89 | 0.15 |
Oceanic | 0.09 | 547.00 | 0.01 | 0.01 | 0.30 | 0.30 | 0.00 | 0.01 | 0.00 | 1.11 | 0.03 | 0.04 | |
Ratio | 2.73 | 0.22 | 2.05 | 7390.00 | 520.00 | 595.83 | 201.88 | 207.50 | 1540.63 | 13.33 | 669.17 | 2.31 |
Seaweed type | Macro-elements | Micro-elements | All elements | ||||||
---|---|---|---|---|---|---|---|---|---|
A | R2 | A | R2 | A | R2 | ||||
Ulva lactuca | 0.1677 | −0.3970 | 17.372 | −0.3267 | >sea | 0.1677 | −0.0520 | ||
Caulerpa cf. brachypus | 0.4991 | 0.9756 | 61.65 | −0.5406 | >sea | 0.4991 | 0.9796 | ||
Caulerpa sertlatioides | 0.3209 | 0.9432 | 1401.0 | −0.1158 | >sea | 0.3209 | 0.9531 | ||
Undaria pinnatifida | 0.1726 | 0.9990 | 25.256 | −0.7211 | >sea | 0.1726 | 0.9992 | ||
>Seawater moisture elements content higher than element contents seawater |
together, the bio-accumulation effect of seaweeds for [HM] is dominating and the determines the “all-over” correlation coefficient between the macro- and micro-elements in the moisture of the seaweeds in comparison to the surrounding sea water.
From
Unit | Human Consumption (HC) | Agricultural Irrigation (Ai) | Ulva lactuca (mean ± SD) (N = 4) | HC | Ai | Caulerpa sertlatioides (Mean ± SD) (N = 4) | HC | Ai | Caulerpa cf. brachypus (mean ± SD) (N = 4) | HC | Ai | Undaria pinnatifida (Mean ± SD) (N=4) | HC | Ai | |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Al | ug/l | 200 | 5000 | 122.4 ± 20.99 | 0.61 | 0.02 | 582.8 ± 175.6 | 2.9 | 0.12 | 184 ± 46.45 | 0.92 | 0.04 | 156.0 ± 9.93 | 0.78 | 0.03 |
Ca | mg/l | 100 | 400 | 442.0 ± 20.70 | 4.42 | 1.1 | 530.0 ± 25.5 | 5.3 | 1.32 | 352 ± 3.27 | 3.52 | 0.88 | 110.5 ± 1.00 | 1.11 | 0.28 |
Cu | ug/l | 100 | 200 | 264.6 ± 74.29 | 2.65 | 1.3 | 117.9 ± 13.2 | 1.2 | 0.59 | 630.6 ± 69.21 | 6.30 | 3.15 | 73.9 ± 12.78 | 0.74 | 0.37 |
Fe | mg/l | 0.2 | 5 | 2.188 ± 0.40 | 10.9 | 0.4 | 1.08 ± 0.04 | 5.4 | 0.22 | 0.718 ± 0.14 | 3.6 | 0.14 | 0.2 ± 0.03 | 0.002 | 0.04 |
K | mg/l | 12 | 2 | 964.0 ± 34.29 | 80.3 | 482 | 481.0 ± 5.35 | 40 | 241 | 540.4 ± 4.12 | 45 | 270 | 121.3 ± 5.32 | 10.1 | 60.7 |
Mg | mg/l | 50 | 60 | 1409.6 ± 47.85 | 28.2 | 23.5 | 509.3 ± 9.03 | 10.2 | 0.49 | 620.8 ± 12.25 | 12.4 | 10.3 | 327.5 ± 8.66 | 6.6 | 5.46 |
Mn | mg/l | 0.05 | 0.2 | 3.014 ± 0.16 | 60.3 | 15.1 | 1.2 ± 0.03 | 24 | 6.0 | 1.638 ± 0.07 | 32.8 | 8.19 | 0.02 ± 0.01 | 0.40 | 0.10 |
Na | mg/l | 175 | 920 | 1090.4 ± 26.26 | 6.2 | 1.19 | 6238.8 ± 92.33 | 35.7 | 6.8 | 5342.8 ± 75.1 | 30.5 | 5.81 | 3147.0 ± 32.3 | 18.0 | 3.42 |
S | mg/l | 150 | 320 | 4394.6 ± 87.55 | 29.3 | 13.7 | 581.8 ± 155.56 | 3.9 | 1.8 | 1101.2 ± 79.4 | 7.3 | 3.44 | 345.5 ± 7.19 | 2.30 | 1.08 |
Zn | ug/l | 100 | 2000 | 985.8 ± 236.99 | 9.9 | 0.49 | 1169.5 ± 361.5 | 11.7 | 0.58 | 908.8 ± 146.5 | 9.1 | 0.45 | 178.8 ± 18.45 | 1.79 | 0.09 |
As | ug/l | 50 | 100 | 96.4 ± 4.65 | 1.9 | 0.96 | 474.5 ± 6.35 | 9.5 | 4.8 | 228.4 ± 6.35 | 4.6 | 2.28 | 164.8 ± 10.97 | 3.30 | 1.65 |
Cd | ug/l | 5 | 10 | 1.912 ± 0.34 | 0.4 | 0.19 | 5.7 ± 0.47 | 1.1 | 0.57 | 3.55 ± 0.22 | 0.71 | 0.36 | 0.70 ± 0.06 | 0.14 | 0.07 |
Co | ug/l | 5 | 50 | 11.1 ± 0.33 | 2.2 | 0.22 | 7.0 ± 0.21 | 1.4 | 0.14 | 17.7 ± 0.22 | 3.54 | 0.35 | 1.0 ± 0.12 | 0.20 | 0.02 |
Cr | ug/l | 50 | 100 | 14.92 ± 0.90 | 0.3 | 0.15 | 14.5 ± 0.39 | 0.3 | 0.15 | 16.18 ± 1.25 | 0.32 | 0.16 | 6.2 ± 0.27 | 0.12 | 0.06 |
Mo | ug/l | 5 | 10 | 11.46 ± 1.00 | 2.3 | 1.15 | 7.0 ± 4.61 | 1.4 | 0.70 | 6.832 ± 0.35 | 1.37 | 0.68 | 14.8 ± 3.00 | 2.96 | 1.48 |
Ni | ug/l | 50 | 200 | 126.0 ± 9.68 | 2.5 | 0.63 | 129.8 ± 5.32 | 2.6 | 0.65 | 236.2 ± 9.36 | 4.72 | 1.18 | 20.1 ± 3.89 | 0.40 | 0.10 |
Pb | ug/l | 50 | 5000 | 1.004 ± 1.66 | 0.02 | 0.0002 | 2.4 ± 1.53 | 0.05 | 0.0005 | 1.062 ± 0.95 | 0.02 | 0.0002 | 0.10 ± 0.15 | 0.002 | 0.00002 |
In this study, at first sight a detrimental property of seaweeds that can accumulate HM in their moisture (far above the level of the surrounding seawater) was confirmed by other studies with seaweeds, some of which are mentioned below. But intensifying the reasoning why living seaweeds accumulate HM in their biomass and metabolism the following explanation can be given. In general terms, this specific property of seaweeds to accumulate HM can be ascribed to the effect that HM can be classified as essential mineral nutrients that for both macro- and micro-elements are essential in an aquatic environment were live seaweeds. In general terms, this virginal aquatic not by anthropogenic influences often tropical seas or oceans at great depth with lack of light (in quantity and quality) can be characterized by low levels of macronutrients (N & P) (in mg/l), micronutrients like Fe, Cu, Mg & Zn (also in mg/l; see
1) With respect to a reliable practical bio-monitoring system, recently it has been verified in two recent studies that seaweeds growing at the Antarctic (for which it was assumed it was a virginal nearly unpolluted environment stripped of any anthropogenic contamination with HM) were contaminated with HM like mercury (Hg), lead (Pb) and cadmium (Cd) [
2) The fact that seaweeds can have a function as a bio-monitoring system to estimate the accumulation of HM discharged in the oceanic―and thus can serve as an environmental bio-monitoring system―implies that there is a close relation to the oceanic [HM] and the [HM] in living seaweed-biomass. Because HM are available to seaweeds only from the dissolved phase, concentrations in these organisms may only reflect the bioavailable levels of a HM in the solute aquatic phase [
3) In addition, several studies have indicated that metal concentrations in Enteromorpha sp. directly reflect metal concentration in the surrounding water [
4) The Moroccan phosphate industry releases large amounts of heavy metals in the Atlantic Ocean of which is major waste is called phosphor-gypsum. From the yearly amount of phosphor-gypsum produced by the Moroccan industry and the element concentrations in phosphor-gypsum, it has been possible to estimate a yearly flux of heavy metals introduced in the Atlantic Ocean. Seaweeds were used as bio-accumulator materials of heavy metals in the marine environment, in the region of “Jorf Lasfar”, in order to significantly reveal the signal of the heavy metal pollution. Ulva lactuca (Linnaeus) was selected to assess heavy metal pollution around the waste release point. Accumulation factors were determined for 47 elements in U. lactuca, by comparing mean concentrations obtained in algae collected in non-polluted sites (background sites) and an average sea water concentration given in the literature. The ratio between the concentration in U. lactuca, collected in a polluted site to the background concentration in U. lactuca, was determined, giving an estimate of the pollution factor for the same elements by the phosphate industry. The decrease of the pollution due to the dilution in the sea water was observed as far as 6 km southward of the release point [
“Bio-sorption”―often confused by many authors by the term “Bio-accumulation”―is the removal of HM from an aqueous solution by passive binding to non-living seaweed biomass [
Accumulation of HM by living seaweeds has been shown to occur in two phases. The first is a rapid surface reaction (reviewed in [
It can be considered as an optimistic “signal” from this study that the seaweed Undaria pinnatifida (Wakame), collected at the “to intermediate anthropogenic influences” exposed area West-Donegal, Ireland was according to the FAO standards for irrigation and drainage [
oceanic water in the vicinity of the Sahara. [
van Ginneken, V. and de Vries, E. (2018) Seaweeds as Biomonitoring System for Heavy Metal (HM) Accumulation and Contamination of Our Oceans. American Journal of Plant Sciences, 9, 1514-1530. https://doi.org/10.4236/ajps.2018.97111