Toxic and Trace Elements in Seaweeds from a North Atlantic Ocean Region (Tenerife, Canary Islands)

Abstract

Canary Islands is a North Atlantic Ocean archipelago in the Macaronesian region that stand out for its great algae diversity and its climatic conditions. However, even in this low industrialised area, human activities tend to increase the marine pollution. Asparagopsis spp. and Liagora spp. algae are red algae frequent in the Canary Islands’ coasts. Therefore, they could be used as bio-indicators of marine pollution for trace elements. A total of 30 samples of both algae’s species from Tenerife’s southern coast, specifically in Playa Grande, Porís de Abona, in Arico (Tenerife, Spain) were used to determine trace element content (Mn, B, Ba, Cu, Cd, Co, Fe, Li, Mo, Ni, Pb, Sr, V, Zn, Al, Cr) through inductively coupled plasma atomic emission spectroscopy (ICP—OES). Highest Fe concentrations were found in Liagora spp. concentrations (1190 ± 1545 mg/kg dw) and Al (288 ± 157 mg/kg dw) was more significant in Asparagopsis spp. High concentrations of B were also registered in both species 80.2 ± 34.2 mg/kg dw and 77.9 ± 34.2 mg/kg dw, respectively. The recorded concentrations show a high contamination scenario in the collected area. Porís is known by its marine diversity and by its higher pollution levels, compared with other locations of Tenerife, due to the currents present on the Canary Island and its singular north orientation, actions must be taken to reduce pollution.

1. Introduction

The Canary Islands (Spain) are situated in the eastern sector of the North Atlantic Ocean between 27° and 29° North latitude and 14° and 18° West longitude. The Canary Islands are part of the well-known Macaronesia region, along with other archipelagos, such as the Azores, Cape Verde, Madeira, and the Savage Islands. The Canarian archipelago is made up of seven main islands (El Hierro, La Palma, La Gomera, Tenerife, Gran Canaria, Fuerteventura, Lanzarote) (Figure 1) and four smaller islands (Alegranza, Montaña Clara, La Graciosa, Lobos) [1,2].

The climate of the Canary Islands is marked by factors such as the thermal inversion in altitude, the incidence of the prevailing trade winds, the cold current of the Canary Islands, the Saharan winds that carry the haze, and the Atlantic storms [1,3,4,5].

The origin of the Canary Islands is volcanic and the geographical conditions between the islands vary considerably. Tenerife, with an area of 2034 km², is the largest island, as well as the highest, since Mount Teide, at 3718 m, is the highest mountain in Spain and the third highest volcanic island in the world [1,6].

The climatic variability is what has led to the diversity of species and an exclusive ecosystem. The bottom of sea that surrounds the Canary Islands have a great diversity of macroalgae. Algae can be divided into diatoms (Bacillariophyceae), green algae (Chlorophyta), brown algae (Phycophyta), and red algae (Rhodophyta) [7]. Among the various Rhodophyta species that grow on the coasts of Tenerife, those belonging to the genera Asparagopsis spp. and Liagora spp. are the most common [8,9].

Asparagopsis spp. algae can reach a length of 30 cm, and they are fixed to the substrate by fine rhizoids, although they can also be found floating when this fixation is broken. The characteristic colour of these algae is pale pink [9].

Liagora spp. algae are characterized by their whitish coloration and by their semi-rigid structure, which is due to calcium carbonate (CaCO₃) that is found on the walls of their cells. In addition, this is one of the most abundant species on the coasts of the Canary Islands and can be found in large intertidal pools up to depths of 25 m [9].

However, algae stand out because they are one of the best bioindicators of marine pollution [10] and they could be used as bioremediation treatments in contaminated environments [11,12,13], as support of other non-biological treatment methods like sorption by biochar, activated carbon, nanomaterials, among others [14,15]. Nevertheless, this is not the only application in which algae are used; they are also applied in biofuel production [16], as replacement of the traditional NPK fertilizer [17], and in improvements in aquaculture [18].

Algae can absorb and accumulate several elements [11]. High levels of trace elements may be indicative of anthropogenic pollution, such as wastewater discharges or maritime traffic, or, conversely, due to some climatic factors, such as haze, which can raise the content of elements such as Fe [19]. The wastewater discharges, both domestic and industrial, contain toxic elements to organisms, such as Ni, Pb, Cr, Cd, Zn, and Fe [20]. Likewise, other sources of natural contamination could be erosion, volcanic emissions, or the leaching of minerals [21]. For this reason, determining the content of trace elements in macroalgae is essential to assess marine pollution in a specific place.

Trace elements have a series of harmful effect on microorganisms. Cd, a known marine pollutant, can inhibit cell division and transcription, as well as cause damage to nucleic acids [22,23]. Cr and Zn can impede the plants’ growth and inhibit their metabolism [24,25,26]. Pb and Cu are elements that could hamper the enzymatic activity [23,27,28]. Ni is an element that can hinder enzymatic activity, and, in addition, could cause oxidative stress [23,26,29]. Al is a toxic pollutant to living organisms [30]. In cyanobacteria, high concentrations of elements such as Mn, Co, and Fe are capable of reducing the cell viability and even cause death [31].

Therefore, algae should be studied in order to verify their viability as marine pollution’s bioindicator. This research has an even bigger impact when it is done in areas with a great biodiversity and endemism, such as the Canary Islands, as their ecosystems are more fragile.

The objectives of this study are (i) to determine the content of trace elements (Co, B, Ba, Cd, Cu, Li, Fe, Mn, Mo, Ni, V, Sr, Zn, Pb, Al, Cr) Asparagopsis spp. and Liagora spp. from Tenerife Island, (ii) to evaluate the contamination on the collection site, and (iii) to update the content data on these elements in both genres of red algae.

2. Material and Methods

Chemical reagents of analytical grade and deionized water of high purity obtained from a purification system of the trademark Mili-Q (Milipore, MA, USA) were used in the treatment of the samples and in the analysis.

2.1. Samples and Sampling Zone

A total of 30 samples of algae of the genera Asparagopsis spp. and Liagora spp. collected in Tenerife’s southern coast, Playa Grande, Porís de Abona (Arico, Tenerife, Spain) between April and June 2017 were analysed. This location was selected as previous studies reveal a higher level of contamination there than in the other of Tenerife’s studied areas [32,33,34]. Figure 1 shows the samples collection area. The specimens were collected in hermetic and sterile plastic bags that were closed and labelled (date, collection area, genre). The samples were taken to the laboratory immediately and kept at a freezing temperature of −18 °C until their processing.

2.2. Treatment of the Samples

Three grams of each sample, previously homogenized, were weighed in porcelain capsules (Staatlich, Germany) using an analytical balance (Metler Toledo, OH, USA) and subjected to oven drying (Nabertherm, Germany) at 70–75 °C for 24 h. Subsequently, the hot acid digestion of the samples was processed by adding about 3–6 mL of 65% HNO₃ (Merck, Germany) and, after evaporation of the nitric acid, the samples were subjected to incineration in a muffle furnace (Nabertherm, Germany) with a temperature-time programme of 420 °C for 24 h, with a progressive rise in temperature of 50 °C/h, until obtaining white ashes [35]. The resulting ashes were dissolved in 1.5% nitric acid (HNO₃) to a volume of 25 mL, in a volumetric flask, and transferred to sterile hermetic polyethylene containers with lids, for subsequent analysis [36].

2.3. Analytical Method

The elements were determined by Inductively Coupled Plasma Atomic Emission Spectrometry (ICP-OES) model ICAP 6300 Duo Thermo Scientific (Waltham, MA, USA) with an automatic sampler (CETAX model ASX-520, USA). The instrumental conditions of the spectrometer were as follows: Approximate RF power of 1150 W; gas flow (nebulizer gas flow, auxiliary gas flow) of 0.5 L/min; sample injection to the 50-rpm flow pump; stabilization time of 0 s.

Table 1. Wavelengths, detection, and quantification limits of the analysed trace elements.

Element	Wavelength (nm)	Detection Limit (mg/kg)	Quantification Limit (mg/kg)
Al	167.0	0.033	0.100
B	249.7	0.025	0.100
Ba	455.4	0.008	0.042
Cd	226.5	0.003	0.008
Co	228.6	0.005	0.017
Cr	267.7	0.025	0.067
Cu	327.3	0.033	0.100
Fe	259.9	0.017	0.042
Li	670.8	0.010	0.026
Mn	257.6	0.017	0.067
Mo	202.0	0.006	0.017
Ni	231.6	0.006	0.025
Pb	220.3	0.003	0.008
Sr	407.7	0.006	0.025
V	310.2	0.008	0.042
Zn	206.2	0.017	0.058

shows the wavelengths (nm) of each element analysed, as well as the detection and quantification limits of the method, which were calculated under reproducibility conditions, as three and ten times, respectively, the standard deviation (SD) resulting from the analysis of 15 targets [37].

The quality control of the method, to ensure the accuracy of the analytical procedure, was performed by the study of the recovery percentage obtained with reference materials under reproducible conditions. The reference materials used were SRM 1515 Apple leaves, SRM 1570a Spinach leaves from the “National Institute of Standard and Technology” (NIST), and the BCR 279 Sea lettuce from the “British Certified Reference” (BCR). The recovery percentages (>94%) obtained with the reference materials above-mentioned are shown in

Table 2. Certified concentration (mean ± SD, n = 3) of the reference materials and recovery percentages for the trace elements studied.

Material	Element	C. Certified (mg/kg)	C. Obtained (mg/kg)	Recovery (%)
SRM 1570a Spinach leaves	Sr	55.6 ± 0.8	54.2 ± 0.30	97.5
	V	0.57 ± 0.03	0.55 ± 0.01	96.5
SRM 1515 Apple leaves	B	27 ± 2	26.2 ± 0.03	97
	Ba	49	48.4 ± 0.02	98.8
	Cr	0.3	0.29 ± 0.02	96.7
	Co	0.09	0.09 ± 0.02	100
	Mn	54.0 ± 0.3	53.8 ± 0.30	99.6
	Mo	0.09	0.09 ± 0.01	100
	Fe	80 ± 0.0	79.3 ± 0.02	99.1
	Ni	0.91 ± 0.12	0.89 ± 0.05	97.8
	Al	286	284 ± 0.50	99.3
BCR 279 Sea lettuce	Cu	13.1 ± 0.4	12.7 ± 0.30	96.9
	Zn	51.3 ± 1.2	51.0 ± 0.50	99.4
	Cd	0.27 ± 0.02	0.26 ± 0.01	96.3
	Pb	13.1 ± 0.4	12.8 ± 0.20	97.7
Standard Addition Method	Li	0.2 ± 0.02	0.19 ± 0.03	95.0

. In addition, a statistical analysis was realized, finding no significant differences (p < 0.05) between the certified concentrations and the concentrations obtained.

2.4. Statistical Analysis

Statistical analysis was carried out using IBM Statistics SPSS 24.0 for Windows™ software. First, the normality of the data was checked using the Kolmogorov–Smirnov and Shapiro–Wilk tests, and the Levene Homogeneity of Variances test [38,39,40]. Since the data followed a non-normal distribution, non-parametric tests were applied, in this case, the Kruskal–Wallis test [41].

Statistical analysis was performed to verify the existence or not of significant differences (p < 0.05) between Liagora spp. and Asparagopsis spp.

On the other hand, Spearman’s Rho test was used to study the possible correlations between Cd-Zn, Cd-Al, Cd-Pb, and Al-Pb between the two genres analysed.

3. Results and Discussion

3.1. Trace Element Concentrations in the Genres Analysed

Table 3. Average concentrations, standard deviations (SD), and maximum–minimum of each trace element in the samples of Asparagopsis spp. analysed.

Asparagopsis spp. (n = 20)
Element	Concentration ± SD (mg/kg Dw)	Max–Min
Co	0.37 ± 0.20	0.87–0.10
Cr	1.10 ± 0.41	2.01–0.38
Cu	4.90 ± 1.73	8.36–2.21
Fe	734 ± 521	1630–27.1
Mn	22.4 ± 11.4	48.5–5.96
Mo	0.22 ± 0.19	0.83–0.02
Zn	7.80 ± 4.09	19.2–1.83
B	77.9 ± 39	187–31.8
Ba	7.20 ± 2.8	13.6–2.36
Li	1.28 ± 0.11	6.28–1.11
Ni	1.54 ± 0.40	5.12–0.83
Sr *	<0.003	<0.003
V	5.63 ± 6.48	24.8–0.02
Al	288 ± 157	647–100
Cd	0.13 ± 0.08	0.31–0.02
Pb	4.63 ± 7.28	34.5–0.64

* Under of the quantification limit (0.003 mg/L).

shows the mean concentrations (mg/kg dw) and standard deviations (SD) of the trace elements analysed in Asparagopsis spp. The analysed elements follow the decreasing order of concentration of Fe > Al > B > Mn > Zn > Ba > V > Cu > Pb > Ni > Li > Cr > Co > Mo > Cd.

Table 4. Average concentrations, standard deviations (SD), and maximum–minimum of each trace element in the samples of Liagora spp. analysed.

Liagora spp. (n = 10)
Element	Concentration ± SD (mg/kg Dw)	Max–Min
Co	0.18 ± 0.14	0.43–0.04
Cr	0.70 ± 0.16	0.92–0.43
Cu	6.60 ± 4.71	13.8–1.10
Fe	1190 ± 1545	1093–3.64
Mn	14.9 ± 9.92	29.8–1.35
Mo	0.20 ± 0.07	0.32–0.12
Zn	4.30 ± 3.18	8.48–1.03
B	80.2 ± 34.2	185–23.0
Ba	23.7 ± 12.3	11.5–3.62
Li	4.30 ± 2.67	7.33–0.57
Ni	3.70 ± 3.02	2.10–0.54
Sr *	<0.003	<0.003
V	5.41 ± 5.37	7.83–0.21
Al	256 ± 179	401–38.2
Cd	0.20 ± 0.21	0.20–0.01
Pb	3.92 ± 3.71	4.11–0.14

* Under of the quantification limit (0.003 mg/L).

shows the mean concentrations (mg/kg dw) and standard deviations (SD) of the trace elements analysed in Liagora spp. The order of the elements follows the decreasing sequence of concentration of Fe > Al > B > Ba > Mn > Cu > V > Zn > Li > Pb > Ni > Cr > Mo > Cd > Co.

The Fe content in Liagora spp. (1190 ± 1545 mg/kg dw) is higher than the mean Fe level recorded in Asparagopsis spp. (734 ± 521 mg/kg dw); it is worth mentioning that the high standard deviations registered specially in Fe and Al are due to that they are organic samples where multiple factors can influence the concentrations of their accumulated elements.

It is known that algae are a remarkable Fe source, with high levels found in them. Fe concentrations of 214 mg/kg dw up to 830 mg/kg dw have been recorded in samples of algae such as wakame, nori, and lettuce [42]. Another research in red algae collected from the California coast (USA) detected Fe levels from 229 mg/kg to 846 mg/kg; these were lower than the ones found in Liagora spp. genre [43]. High Fe concentrations (7870 mg/kg dw) were found in algae from Hong Kong (China) in a data collection study, being higher than those found in the present paper [44]. A study conducted in Venezuela showed mean concentrations of Fe of 1569 ± 324 mg/kg dw, 575 ± 311 mg/kg dw, 155 ± 29 mg/kg dw, and 1959 ± 549 mg/kg dw in Sargassum spp., Ulva spp., Porphyra spp., and Gracilariopsis spp., respectively [45], which are similar concentrations to those registered in this research and the same as the samples of sea lettuce collected from the Galician coast, Spain, which have a Fe level of 1868 mg/kg dw [46]. An average Fe concentration of 629 mg/kg dw was detected in brown algae collected in Porís de Abona (Spain); lower than those found in the present study [47].

The Al content found in Asparagopsis spp. is remarkable; an average level of 288 ± 157 mg/kg dw, which is higher than the average Al level (256 ± 179 mg/kg dw) registered in Liagora spp. Previous studies on brown algae collected in Porís de Abona (Spain) recorded mean Al level of 212 mg/kg dw [47]. This level is lower than the one obtained in the present study. The B content (80.2 ± 34.2 mg/kg dw) registered in Liagora spp. stands out as being superior to that found in the Asparagopsis spp. (77.9 ± 39 mg B/kg dw).

The average Pb content (4.63 ± 7.28 mg/kg dw) in Asparagopsis spp. was higher than the average Pb level (3.92 ± 3.71 mg/kg dw) recorded in Liagora spp. However, the Cd level (0.13 ± 0.08 mg/kg dw) in the Asparagopsis spp. algae was lower than the level found in Liagora spp. (0.20 ± 0.21 mg/kg dw). Studies where Rhodophyta algae from Bay Camarones (Argentina) were analysed show higher levels of Cd (1.13 mg/kg dw) and Pb (5.1 mg/kg dw) than those recorded in the present study [48]. Likewise, in other studies where red algae collected from the California coast (USA) were analysed, Pb levels of 16.17–28 mg/kg were found [43], being higher than levels registered in this study.

Statistical analysis confirmed the existence of significant differences (p < 0.05) in the content of B, Co, Cr, Fe, Ni, Cd, and Pb between Asparagopsis spp. and Liagora spp. Considering that the salinity conditions, pH, temperature, element concentration in water, and other external factors are identical in both genres, since they were collected on the same dates and place, the differences found between both genres could be due to intrinsic factors such as the metabolic requirements of each genre [49] or different affinity for each element [50].

The Porís de Abona is a small village that belongs to the municipality of Arico, in the south of the island of Tenerife. It is an area subject to an important indirect anthropogenic activity due to the influence of the ocean currents and the singular orientation of the Playa Grande in the Porís de Abona [32] (Figure 2).

Moreover, there are some direct anthropogenic contaminations by the debris from the construction of the TF-1 motorway, the presence of obsolete marine outfalls, uncontrolled camping areas that are highly occupied in areas near the coast, as well as waste that is thrown to the sea, and accumulation of waste that is carried by marine currents, such as hydrocarbons, plastics and microplastics, and domestic discharges [51,52].

The difference in the concentration of trace elements content in the period time between April and June 2017 was evaluated (Figure 3). The Al, B, Co, Cu, Li, Ni, and Pb concentrations increased from April to June. Meanwhile, the rest of the trace elements contents decreased. The Fe content (849 mg/kg) recorded in the samples collected in April 2017 is noteworthy; this may be related to the episode of haze and high temperatures reported in early March 2017 [52]. It has been proven that the presence of Saharan dust in suspension increases the content of nutrients such as Fe. However, no significant differences (p < 0.05) were detected in the content of trace elements depending on the month of algae collection. The difference in elements’ concentrations, mainly Fe, Mn, and Zn, present in the algae based on the year period agreed with previous studies [53]. In both cases, the concentrations are lower in the warmer seasons.

There has been another already published study in this area [47]; these are very novel studies in this location and currently there are new ones in development. The mean concentration of all elements analysed in both cases (Fe, B, Ba, Li, Ni, V, Al, Cd, Pb) are higher in the present study. In the present study, all algae are part of the Florideophyceae class, which are part of the phylum Rhodophyta (red algae). Meanwhile, in the previous research, all the algae from Porís de Abona analysed were Phaeophyceae (brown algae) [47]. This could be the reason of the different concentrations found [53].

The results of the other locations analysed in the previous study show concentrations 19 times higher in Porís than the other studied areas [47] (

Table 5. Comparison between the current study and a past study in this area and other areas in Tenerife.

	Concentration (mg/kg Dw)
Element	Porís de Abona (Present Study, 2022)	Porís de Abona [47]	La Punta del Hidalgo [47]	El Socorro [47]
Fe	962	629	49.1	59.3
B	79.05	74	103	133
Ba	15.45	13.4	7.04	5.66
Li	2.79	2.54	2.46	4.72
Ni	2.62	2.3	1.2	0.88
V	5.52	3.12	0.36	1.31
Al	272	212	40.2	57.7
Cd	0.165	0.13	0.22	0.16
Pb	4.275	2.7	0.34	0.43

), which confirms that Porís de Abona is a zone with higher levels of pollutants than others in Tenerife, due to the influence of the ocean currents and Playa Grande’s singular orientation, as it has been mentioned previously [32,47] (Figure 2).

3.2. Study of Correlations between Elements

The correlations between Cd-Zn, Cd-Pb, Al-Cd, and Al-Pb were studied in the algae samples analysed (

Table 6. Data from the Spearman’s Rho correlation study between Cd-Zn, Cd-Pb, Al-Pb, Al-Cd.

Spearman’s Rho
		Cd		Zn
Cd	Correlation coefficient	1.000		0.309 **
	Sig. (bilateral)			0.000
	N	158		158
Zn	Correlation coefficient	0.309 **		1.000
	Sig. (bilateral)	0.000
	N	158		158
Spearman’s Rho
		Al	Pb	Cd
Al	Correlation coefficient	1.000	0.863 **	0.310 **
	Sig. (bilateral)	.	0.000	0.000
	N	158	158	158
Pb	Correlation coefficient	0.863 **	1.000	0.303 **
	Sig. (bilateral)	0.000	.	0.000
	N	158	158	158
Cd	Correlation coefficient	0.310 **	0.303 **	1.000
	Sig. (bilateral)	0.000	0.000
	N	158	158	158

** The correlation is significant at the 0.01 level (bilateral).

).

In the case of the Zn-Cd pair, the interest lies in the fact that Zn is an element that, in adequate amounts, is essential for the growth of algae. However, Cd is a toxic element even at low concentrations and one of the most important marine pollutants, due to its long half-life and its biomagnification in marine organisms. Cd can interfere in the organisms with essential elements such as Zn because both elements are divalent. The correlation coefficient between Cd and Zn shows a positive correlation (r = 0.309), although it is low. This very low positive correlation may indicate that Zn and Cd levels increase at the same time.

Regarding the cases of Cd-Pb (r = 0.303), Cd-Al (r = 0.310), and Pb-Al (r = 0.863), it has been shown that there is a positive correlation, which means that, as the concentration of one of these elements increases, so does the other. This fact is interesting, since it means that these three elements do not compete against each other, which would be useful in the case of using the algae for bioremediation treatment of waters, as they are capable of absorbing at the same time these elements that pose serious damage to the environment and that, unfortunately, due to anthropogenic activities, their concentration in the environment is increasing.

Authors recognize as the present study’s limitation the low sample number and the inclusion of only two algae species. This research was planned to be a preliminary study of the area and situation to be follow by more in deep studies.

4. Conclusions

Trace elements concentrations (Ba, B, Co, Cu, Cd, V, Fe, Li, Sr, Mn, Mo, Ni, Pb, Zn, Al, Cr) were determined in two genres of red algae (Asparagopsis spp. and Liagora spp.) from the island of Tenerife, located in the North of the Atlantic Ocean. The algae of the genus Liagora spp. are those that registered the highest mean concentrations of elements such as Fe or B. The Al level stands out in the genus Asparagopsis spp. Significant differences (p < 0.05) in the content of B, Co, Cr, Fe, Ni, Cd, and Pb were found between both genres. Considering that the algae analysed were collected from the same area and on the same dates, the differences found confirm the existence of intrinsic factors specific to the genus.

The correlation study shows the association between Cd and Zn. This fact is necessary to consider, because it means that Zn and Cd levels increase at the same time. It has been shown that Cd, Al, and Pb do not compete, finding a positive correlation between the three elements.

The high concentrations of trace elements found in the algae analysed indicate a high contamination level on the Porís de Abona coast, which coincides with the fact that this area is subject to anthropogenic pollution, due to the presence of obsolete marine outfalls, high occupancy in uncontrolled camping areas, and currents that carry various pollutants towards its coast. Taking into account that the Porís de Abona coast is an area of great diversity of marine species, these data should be considered to take actions in order to decrease this area’s pollution level, which has both touristic and environmental interest.