Article 2024
Article 2024
Article 2024
Environmental Pollution
journal homepage: www.elsevier.com/locate/envpol
Review
A R T I C L E I N F O A B S T R A C T
Handling Editor: Philip N. Smith Physical, chemical weathering and volcanic eruptions release heavy metals into soils and surface waters natu
rally. Contaminants from anthropogenic sources originated from industrial and municipality waste substantially
Keywords: modify and increase their contributions. They are then absorbed by fish gills, amphipod cuticles, and other
Aquatic ecosystem sensitive organs of aquatic creatures. This article discusses the essences on the determination, potential and
Biomagnification
plausible factors of trophic transfer and biomagnification of environmental contaminants particularly heavy
Heavy metals
metals across aquatic ecosystem. In general, arsenic is found to be bio-diminished across food webs in freshwater
Stable isotopes
Trophic transfer ecosystem while it biomagnified in marine ecosystem of higher trophic level (tertiary consumer of predatory fish)
and dilute its concentration from lower trophic level (from producer to bottom level of consumer, secondary and
lastly to tertiary consumer (forage fish)). Early study for Cadmium shown that it has no potential for bio
magnification while later studies prove that cadmium does magnify for gastropod and epiphyte-based food webs.
Mercury shown obvious biomagnification potential where it can bio-magnify from trophic level as low as par
ticulate organic matter (POM) to higher trophic of fish. These findings proved that aquatic ecosystems must be
preserved from contamination not just for human benefit, but also to prevent environmental degradation and
biodiversity loss.
☆
This paper has been recommended for acceptance by Philip N. Smith.
* Corresponding author.
E-mail address: budai.peter@uni-mate.hu (P. Budai).
https://doi.org/10.1016/j.envpol.2023.122815
Received 23 April 2023; Received in revised form 24 October 2023; Accepted 25 October 2023
Available online 27 October 2023
0269-7491/© 2023 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-
nc-nd/4.0/).
N.B. Saidon et al. Environmental Pollution 340 (2024) 122815
shown to be higher than inorganic Se in aquatic animals, most likely due toxic effects (Hare, 2013).
to the greater bioavailability in organic forms (Martens and Suarez, Although numerous reports have been published on some metals and
1997). metalloids biomagnification potential, there are some gaps and limited
Metals dissolved in the environment are then absorbed by fish gills, knowledge to understand the mechanisms due to the debate on the
amphipod cuticles, and other sensitive organs of aquatic creatures environmental scale in order to find the specific factors that could
(Dehghani et al., 2022). Furthermore, it is actively accumulate in the contribute to the trophodynamics as the ecosystems involved are much
bodies of microscopic organisms (phytoplankton and zooplankton), more complex and not yet fully understood (Córdoba-Tovar et al.,
which have a large surface area (surface/volume ratio) (El-Metwally 2022).
et al., 2022). In fish species, heavy metals are potent neuro-toxicants This article aims to provide an overview on the determination, po
that have been linked to malformations in both natural (Abbas et al., tential and possible factors of trophic transfer and biomagnification of
2021; Morales, 2022) and laboratory populations (Pilehvar et al., 2020). contaminants particularly heavy metals across aquatic ecosystem. A
It also alter the biochemical and haematological of fish which resulted in systematic literature review were conducted and results from research
nuclear and cellular anomaly (Shahjahan et al., 2022). The deformities articles were selected based on inclusion and exclusion criteria,
manifested in fish not only affect their survival, but also the complexity including research conducted in an aquatic ecosystems and aquatic or
of their overall health, thus were often used as indicator to evaluate the ganisms, while dismissing any article on land biota. Recent articles from
burdens of heavy metals in the environment (Ali et al., 2019). Corre the last ten years were prioritized to ensure that updated data on metals
spondingly, the transfer of heavy metals to lower trophic level(s) is detection in a particular locations were used.
assessed on the condition where the fish nutrition is investigated from
the contribution of different feeds (Liu et al., 2002). 2. Determination of trophic transfer and biomagnification
The dynamics of potentially toxic elements (PTE) is affected by their
mobility in water column and absorption to suspended materials Fig. 1 illustrates the idea of biomagnification where a chemical is
resulting in gradual increase of accumulation across, and to higher transferred up the food chain to higher trophic levels, and the concen
trophic level (Signa et al., 2013). In general, aquatic organisms are tration in predators surpasses the concentration expected when an or
typically assigned to four trophic levels where example given are among ganism and its environment are in balance (Alexander, 1999). There are
the organisms but not all or limited to; level 0 (producer) consist of different terminologies to better understand the determination of bio
vascular and non-vascular aquatic plants; level 1 (primary consumer) concentration, trophic transfer and biomagnification of an organism in
consist of zooplankton; level 2 (secondary consumer) consist of forages an ecosystem which lead from one process to another.
fish; level 3 where predatory or carnivorous fish were commonly found The biomagnification and trophic transfer determination involve
(Suedel et al., 1994). The concept behind biomagnification, also known several steps. First is the identification of trophic level of each organisms
as secondary poisoning, is that the mass of a pollutant is mostly where mass sampling of organism in an ecosystem were made. This is
conserved along this food chain but the biomass through which it is often determined by studying the gut content or by stable isotopes
transported decreases, resulting in higher concentrations (Janssen et al., analysis. Then, the biomagnification potential of organisms from lower
1993). trophic to higher level could be determined by the calculation of its
The dynamics of heavy metal accumulations are also dependable on trophic transfer factor (TTF) or trophic transfer coefficient (TTC), taking
the rate of accumulation and removal from body, creating a variations of its contaminant’s concentration in each organism into consideration.
its half-lives depending on the species metabolism. Due to its persistency
in the environment, these metals then enter and transferred across the
2.1. Elemental analysis
food chain when it directly enters the body of organisms through abiotic
environment (water, sediments, soil), or indirectly from prey/food. (Ali
The concentration of contaminants in the samples are usually
and Khan, 2018). If these contaminants are not broken down in organ
measured by analytical instruments: inductively coupled plasma - op
isms, their concentrations tend to rise as they move up the aquatic food
tical emission spectroscopy (ICP-OES) or inductively coupled plasma –
chain (biomagnification), making top predators the most vulnerable to
mass spectrometry (ICP-MS) in many studies involving samples of
Fig. 1. The trophic transfer from organism at lowest trophic level to highest trophic in an aquatic ecosystem.
2
N.B. Saidon et al. Environmental Pollution 340 (2024) 122815
aquatic ecosystems (sediments, fish, and arthropods) (Reshqueih et al., TTF is a broad word that encompasses biomagnification, which occurs
2014; Fu et al., 2014; Grotto et al., 2012). According to the manufac when an organism’s substance concentration exceeds that of its diet, and
turer’s instruments, ThermoFisher, ICP-OES is used to measure pollut bio-dilution, which occurs when an organism’s substance concentration
ants and elements with higher regulatory limits for environmental safety falls below that of its food (DeForest et al., 2007).
evaluation. Contrarily, ICP-MS is very helpful for assessing substances Whereas, TTC is also a plausible parameter to determine either the
with low regulatory limitations. Hence, element such as Aluminium is metals is biomagnified or biodiluted. Similar to TTF, TTC value is an
recommended to be determined by ICP-OES because it is usually found estimation of a contaminant’s ability to biomagnified, calculated by
in higher concentrations than the other metals (Pb, Cd and As), which dividing the contaminant’s concentration in consumer tissue (organisms
are preferably to be analysed using ICP-MS (Habte et al., 2015). Both of higher trophic level) by the contaminant’s concentration in food(s)
methods require validation with consideration of validation parameters (organisms of lower trophic level) (Suedel et al., 1994; Kim, 2020).
(calibration range, limit of detection (LOD), limit of quantification
CConsumer
(LOQ) and sample recovery) for quality reassurance (Alkas et al., 2017; TTC =
Cfood
Habte et al., 2015).
LOD can be determined by a few methods: 1) standard “n samples” in When there is a transfer of contaminants (metals or elements) be
many samples, at almost zero concentrations; 2) Thermo Scientific for tween trophic levels, a coefficient with a value greater than 1 is an
mula (Al-Hakkani, 2019). The standard deviations of the 10 separately obvious indication of biomagnification, whereas value less than 1 shows
generated blank solutions were used to calculate the LOD and LOQ the contaminants are not biomagnified across the organism (Chen et al.,
where the degree of results’ variation validated that the routine analysis 2021). In some studies, similar approach were used but with different
methods are deem feasible, regardless of the influence of the samples terminology which is trophic magnification factor (TMF) (Cui et al.,
(Khan et al., 2013). Validation parameters can be determined according 2011; Hu et al., 2021). In addition, TMFs is an important and reliable
to guidelines (Commission Regulation No 333/2007) where LOQ and tools, verifiable by observation in determining and understanding the
LOD were defined as three and ten times the standard deviation of the exact chemicals properties whether it is biomagnify (TMF > or < 1)
signals of blank samples (European Commission, 2007). Spike recovery based on quantitative measurement (Borgå et al., 2012).
are also determine by using spike sample or certified reference material Other than TTF, TTC and TMF, trophic magnification slopes (TMS)
(CRM) where a known quantity of an element or analyte are added to a are often used in trophodynamics determination of metals in a food
sample and comparing the results of the analytical process with the chain. Fig. 2 illustrates the trophic magnification slope (TMS) which can
known quantity and spike recoveries rate of ~85–115% are considered be determined by plotting a single linear regression slope between tro
acceptable (Parikh et al., 2015). Validation method by using CRM phic level and heavy metal concentration (Cui et al., 2011). There are
TORT-2 of lobster hepatopancreas (Cordeiro et al., 2014), standard two important elements to construct the slopes; the log-transformed
mussel (ERM-CE278k) and tuna tissue (ERM-CE464), obtained from the concentration of heavy metal in a test species (Log10 [HM] concentra
Joint Research Centre (B-2440 Geel, Belgium) can also be considered tion), and the trophic level or ration of stables isotopes analysis (δ15N ‰)
(Plachy et al., 2022). In terms of precision, relative standard deviation, from all organisms in the food chain. The slope shows simple linear
and recoveries for metals assessed at an interest concentration range, the relationship between the two factors, hence, quantifying the degree of
data from both instruments were generally comparable (Poirier et al., biomagnification to understand the extend of average change of metals
2016). Whereas Atomic Fluorescence Spectrometry is a feasible instru concentration within trophic position (Lavoie et al., 2013). The stable
ment to evaluate the concentration of Hg and As (Cui et al., 2011). nitrogen isotope ratios were used to produce continuous integrative
measurements of trophic status to determine the trophic level.
2.2. Determination of trophic positions Increasing value of δ15N ‰ shows increasing trophic position of an or
ganism in a food web. This is due to the consistent excretion and
Stable isotope analysis, which reflects a species’ entire feeding his retention of lighter and heavier nitrogen isotopes consecutively (Lavoie
tory, is a frequent method used for determining relative trophic posi et al., 2013). There are obvious indications for biomagnification or
tions (Croteau et al., 2005; Cui et al., 2011). Lipids are extracted from biodilution where a positive slope shows the accumulation in food
the grounded dried samples of an organism and then analysed by stable chains. Contrarily, a negative slope indicates the opposite (bio-dilution),
isotopes ratio mass spectrometer (Du et al., 2020). The ratio of stable suggesting the removal of said elements from food web, or due to the
isotope carbon (13C) and nitrogen (15N) served as a tracers and have interruption of its transfer across the trophic level (Griboff et al., 2018).
recently been proposed for investigating trophic linkages and contami
nant biomagnification. Because the enrichment of nitrogen isotope
happens sequentially across trophic levels at a constant pace, 15N is
helpful in assessing trophic position. The enrichment of carbon isotope
13
C among different trophic levels is not clear. As a result, it is regarded
as a useful biomarker for distinguishing various primary production
sources. In ecotoxicological research, stable isotope analyses are
commonly employed to elucidate contaminant behaviour (e.g., bio
concentration and biomagnifications) over the entire trophic chain (Cui
et al., 2011; Signa et al., 2013).
2.3. Trophic transfer factor (TTF), trophic transfer coefficient (TTC) and
trophic magnification slope (TMS)
3
N.B. Saidon et al. Environmental Pollution 340 (2024) 122815
Tables 1 and 2 provide some data extracted from several single webs in lagoon in China. Moreover, Cr also has decreasing concentration
studies of heavy metals in different water ecosystem (marine water and in organisms’ tissues for samples from two distinct ocean; Indian (Swan
fresh water). The trophodynamics were determine by constructing a Lagoon, China) and Pacific Ocean (Tanzanian coastal area). The varia
slope between log10 [HM] concentration versus the value of δ15N. A tions of trophodynamic were suggested by several factors.
positive slope indicates that there is biomagnification of the said metal
across the food webs, while a negative slope shown biodilution occurred
between the organisms. The conclusions drawn from the slopes can be 3.1. External factors
validated by comparing to the calculated TMF values. It is worth
addressing the different in trophodynamics of certain metal, for 3.1.1. Geographical locations
example, Pb. A study in China shown that Pb biodiluted, while in Tan Since there is no universal rule to draw a conclusion about bio
zanian coastal area, it was biomagnified. This result could be due to the magnification potential of a particular elements, it is crucial to address a
length of food chain studied. The study in China comprises shorter food few external factors that may affect its concentration in different aquatic
chain compared to the study in Tanzania. It’s important not to disregard ecosystems. There are some factors to be considered related to
several factors when determining the biomagnification potential of geographical location when comparing different aquatic ecosystems.
metals. Further explanation on the factors that contribute to different One of the factor is salinity, which explains the different trophody
trophodynamic of metals are discussed in the next section. namics of the same elements between two different aquatic ecosystems.
Arsenic for example, tends to present in higher concentration in fresh
3. Factors affecting bioconcentration, trophic transfer and waters compared to marine waters (Azizur Rahman et al., 2012). Even in
biomagnification the same marine ecosystem, it varies depending on the habit of organ
isms where benthic organisms accumulate As more than pelagic or
There were many studies that had determined the biomagnification ganisms (Du et al., 2021). Furthermore, bioaccumulation of Hg also vary
potential of metals in marine and fresh water ecosystems (Fig. 3). In in epipelagic and mesopelagic (Chouvelon et al., 2018).
marine waters, mercury typically biomagnifies along the food chain, The hydrochemical characteristics and trophicity of reservoirs must
except for benthic food webs. It also shown similar trend in fresh water be considered when studying metal accumulation across the food chains
ecosystems in China, Canada and Argentina. Pb were biomagnified in which consists different trophic (Chernova and Lysenko, 2019). Tro
Tanzanian coastal area, but the concentration decrease along the food phicity in related to total phosphorus content in a studied water bodies
such as mesotrophic or oligotrophic lakes play a vital role in
Table 1
Determination of biomagnification of heavy metals in particular locations (marine waters) by constructing the linear regression slope.
Location Heavy Trophic level Mean HM Trophic Magnification Trophic Magnification Slope Trophodynamic References
metals Concentration Factor (TMF) or Linear regression of log10
(HM) μg/g [HM] versus δ15N
R2 p- Slope
value
Swan Lagoon, China Cd Seagrass 2.46 0.11 0.321 <0.01 Negative Biodiluted Hu et al.
ecosystem (2021)
Molluscs
Fish 0.23
Cr Aquatic plants 7.20 0.94 0.089 <0.01 Negative Biodiluted
Crustaceans 3.51
Cu Molluscs 37.43 0.91 0.055 <0.05 Negative Biodiluted
Fish 7.41
Pb Molluscs 4.50 0.96 0.027 <0.05 Negative Biodiluted
Crustaceans 2.46
Zn Molluscs 79.09 1.03 0.013 >0.05 No trend Neither
Aquatic plants 30.44
Jiaozhou Bay, China THg Urbanized 0.0868 ± 1.29 0.230 <0.01 Positive Biomagnified Mao et al.
coastal 0.06027 (2021)
ecosystem
Crustaceans
Molluscs 0.07197 ±
0.05060
Fish 0.09510 ±
0.08063
Northern Coastal Pb Microalgae 2.75 ± 0.52 0.246 <0.05 Positive Biomagnified Bungala et al.
Marine Area, Bivalves 2.05 ± 0.93 (2017)
Tanzania Crustaceans 1.03 ± 0.46
Fish 2.29 ± 1.05
Zn Microalgae 111.50 ± 5.17 <0.05 No trend Neither
Bivalves 116.10 ± 18.22
Crustaceans 165.90 ± 33.39
Fish 84.00 ± 15.03
As Microalgae 4.10 ± 1.51 0.068 <0.05 Negative Biodiluted
Bivalves 1.87 ± 0.14
Crustaceans 2.25 ± 0.18
Fish 0.62 ± 0.14
Hg Microalgae 0.03 ± 0.01 0.368 <0.05 Positive Biomagnified
Bivalves 0.04 ± 0.01
Crustaceans 0.04 ± 0.02
Fish 0.04 ± 0.01
4
N.B. Saidon et al. Environmental Pollution 340 (2024) 122815
Table 2
Determination of biomagnification of heavy metals in particular locations (fresh waters) by constructing the linear regression slope.
Location Heavy Trophic level Mean HM Trophic Trophic Magnification Slope or Trophodynamic References
metals Concentration Magnification Factor Linear regression of log10 [HM]
(HM) μg/g (TMF) versus δ15N
R2 p-value Slope
Fig. 3. Example of sampling locations of metals and its trophodynamics representing different locations and continents.
1 Jiazhou Bay, China: THg – biomagnified (Mao et al., 2021); Swan Lagoon, China: Cd, Cr, Cu, Pb – biodiluted (Hu et al., 2021). 2 Tanzanian Coastal area: Pb, Hg –
biomagnified; As, Cr – biodiluted. (Bungala et al., 2017). 3 Islands of South Georgia: Hg – biomagnified. (Seco et al., 2021). 4 Frobisher Bay, Canada: MeHg –
biomagnified (benthopelagic & pelagic food webs), not biomagnified (benthic food webs). (Hilgendag et al., 2022). 5Northeastern Chukchi Sea: MMHg – not
biomagnified (benthic food webs). (Fox et al., 2014)
aChaohu lake, China: Hg – biomagnified. (Fang et al., 2019). b Nova Scoatia, Canada: MeHg – biomagnified. (Clayden et al., 2013). c Córdoba, Argentina: As, Se –
biodiluted; Hg – biomagnified. (Griboff et al., 2018)
bioaccumulation of metals in an organism. The metals existed in dis slightly higher in freshwater compared to in brackish water (Chernova
solved form in brackish or freshwater have different concentration. For and Lysenko, 2019).
example, lead concentration is much higher in freshwater than in
brackish water. This is the same for zinc, where the concentration is
5
N.B. Saidon et al. Environmental Pollution 340 (2024) 122815
3.1.2. Complexity of food webs and aquatic plants that are found in environments with the lowest metal
Trophic factor which describe the chain length of food webs, bio concentrations. The likely reason for lower accumulation rate is that
logical productivity (oligotrophic or mesotrophic) and planktonic organisms under these conditions need to actively gather metals from
characteristics at bottom of food webs are also influence the variation of their surroundings and diet in order to achieve the desired physiological
bioaccumulation of metals (Chouvelon et al., 2018). The complexity and levels. One possible explanation for this accumulation rate is the inverse
structure of food webs greatly influenced the efficiency and bio relationship between the mollusc’s rate of filtration and the concentra
concentration of elements from lower to higher trophic level (Boldrocchi tions of suspended particles in water (Chernova and Lysenko, 2019).
et al., 2021). Ni and Cd biomagnified when studied in shorter food chain Meanwhile, for aquatic organisms of higher trophic such as fishes,
where gastropod often have the highest concentration. Conversely, the reasons for wide ranges of concentration are due to their dependency
when the entire food web is studied, it shows diminishing trend where it on various internal and external factors affecting the accumulation in
is biodiluted towards the end of food web due to the ability of organisms tissues. Among the internal factors are the taxonomic group, de
of higher trophic to efficiently regulate their metabolism (Boldrocchi mographic, feeding habits and detoxification/regulatory mechanisms,
et al., 2021). In fresh water ecosystems, there is also relation between whereas physicochemical and climatic condition in the aquatic envi
the complexity of food webs with the latitude where the water bodies is ronment influence the accumulation externally (Ali and Khan, 2018).
located (Lavoie et al., 2013). Hg is biomagnified across a simpler food Demography such as growth stages, age, sex, bodily conditions and
webs in water bodies at higher latitude meanwhile, it biodiluted at lower metallothionein of the organisms influence metal deposition in tissues.
altitude with more complex food webs (Kidd et al., 2012). Moreover, the For instance, even at the same trophic level, animals with rapid growth
concentration of Hg is higher in organisms in water bodies of polar and and shorter life histories may experience less Hg biomagnification (Cui
temperate climate while lower in tropical climate (Lavoie et al., 2013). et al., 2011).
3.2.2. Position in trophic level The following section describes the biomagnification potential based
Metal uptake of aquatic organisms at lower trophic level are proved on the single study of a particular ecosystem.
by its bioaccumulation potential (Zhou et al., 2008). There are essen
tially two ways for any aquatic animal to be exposed to metals: trophic 4.1. Biomagnification on different aquatic food webs
transmission through feeding (diet) and dissolved exposure. In marine
food chain, plankton (organism at lower trophic level) serve as a point of Some studies include the species at top of food webs such as aquatic
entry for metals to the animals feeding on them. The behaviour and birds. The aquatic birds, which the PTE is often associated with species-
ecophysiological characteristics of plankton such as its ingestion, defe specific and are related to its moulting, migration history and trophic
cation rates, gut transit, passage time of the metals, sex and life stages status. In a study area such as Yellow River Delta, China, bird (spot-
are to be considered when assessing the bioaccumulation on metals billed ducks) who resides in the location the entire year, is the best
within the organism. Since other organisms at higher trophic level are species to reflect the heavy metal burden in the area. Migratory birds
feeding on plankton, the metal contamination in the biota can vary (Saunders’s gull, purple heron and little egret) however, moves to the
significantly depending on the behaviour and ecophysiology of the southern part in winter, thus best reflect the variety of bioaccumulation
plankton species, coupled with other external factors such as the metal’s with different habitat show the distinction between local and distant
properties, environment and different coastal locations (Chevrollier feeding preferences. In the study, Spot-billed ducks as the resident bird
et al., 2022). Environmental factors includes pH variation, salinity, have highest Mn concentration than the migratory birds, which in
sunlight, dissolved organic carbon (DOC), nutrients and amount of dicates high level of Mn in the environment (Cui et al., 2011).
sunlight received (Chevrollier et al., 2022). In the coastal area such as the series of ponds (Marinello ponds) of
For instance, a study conducted on the zooplankton samples from Tyrrhenian Sea, Italy, it is influenced by a colony of yellow-legged gulls
Baltic Sea shown variation of recorded metals concentration (Zn and Pb) Larus michahellis. It was suggested that trace metals have been trans
that could be due to the – 1) Effective metals scavenging and absorption ported to the biota in the ponds via bio-transport mediated by these
mechanisms result in a significant drop in the amounts of dissolved seabirds. However, only total mercury (THg) was shown to biomagnify
metals; 2) The bioavailability of dissolved metals is decreased by high in the sample (guano, silt, organic matter, macrophytes, shrimps, and
organic matter concentrations; 3) Large-scale primary production causes fish), while As, Cd, and Pb showed considerable biodilution. Further
dissolved metals to be sequestered and metal concentrations in partic more, the comparatively high amounts of these trace metals in POM and
ulate organic matter to decline; 4) Although they accumulate in algal macrophytes indicate that these metal ions are readily available and
organic matter, heavy metals are not biomagnified as they move up the have high absorption rates in primary producers (Signa et al., 2013).
food chain (Pempkowiak et al., 2006). These factors suggest that the Lakes with brackish water shown similar accumulation properties.
concentration of metals are also heavily influenced by the environ For example, in the food chain from the lakes on the coast of the Sea of
mental properties of a location. Japan consisting suspended matter (SM)-phytoplankton-molluscs, the
Invertebrates, which are the organisms at higher trophic level than concentration of Pb decreases. The levels of these elements in phyto
plankton have the highest bioaccumulation factor compared to shellfish plankton and SM are compatible with the concentrations of Cu, Cd and
6
N.B. Saidon et al. Environmental Pollution 340 (2024) 122815
Zn in molluscs. On average condition, the food chain studied (SM- creatures (Schaeffer et al., 2005). AsB concentrations increased (or
phytoplankton-molluscs) shown no biomagnification trend. However, accounted for a larger percentage of total arsenic) as trophic levels
under certain circumstances (e.g. low suspended, concentration of metal climbed, implying that it biomagnifies through the marine food chain
in the environment and organic matter), the concentration of metal in (Rahman et al., 2012). However, it’s bioaccumulation diminished from
organisms at lower and upper trophic level shown comparable differ small plankton to macrozooplankton to fish (Chen et al., 2000).
ence. Molluscs evidently have equal rate of intake and removal of these Across the food chain, arsenic does not bio-magnify in producers,
elements (Chernova and Lysenko, 2019). primary, secondary, or tertiary consumers (forage fish), however, it can
Another study consisting plankton in the food chain of fresh water bio-magnify in tertiary consumers (predatory fish). In lower-trophic-
ecosystems such as in the watersheds in the north-eastern United States level species, the ability to convert and then excrete arsenic may be
shown that from small plankton to macrozooplankton, there were improved. Some of the arsenic in tertiary consumers may be converted
considerable changes in the degree of metal enrichment. The enrich into forms that are not easily eliminated and hence maintained by the
ment of Hg, Zn, and Cd (Biomagnification factor, BMF>1.0) increase organism, which could explain why some level 3 consumers, such as
from small plankton to macrozooplankton. On the contrary, As and Pb sharks, have been reported to retain arsenic (Suedel et al., 1994).
(BMF<1.0) decreased in concentration. Moving up to higher trophic
level, (zooplankton to fish), Zn and Hg appear to enhance the most, 4.3. Cadmium (Cd)
whereas Pb, Cd, and As appear to diminish (BMF<1.0) (Chen et al.,
2000). There is lack of evidence on the oxidation behaviour of cadmium
Moreover, other study in a food web of newly formed fresh water (Cd) in natural waters. The low availability of Cd in water contributed to
ecosystem, Yellow River Delta, China shown biomagnification of some difficulty in determining its affinity towards ligands to produce different
metals. The trophic level were classified into three (TL: 1.50–2.08 of chemical forms (Crea et al., 2013). Many literatures were addressing
water milfoil, Chinese shrimp, and Chinese mitten crab; TL: 2.85–3.28 of cadmium effects in general, regardless of the cadmium speciation and
Spot-billed Duck and Purple Heron; TL: 2.00–3.80 of fiddler crab, Chi behaviour in water bodies.
nese shrimp, catfish, common carp, javelin goby, redeye mullet, silver While there are clear evidence on cadmium bioconcentration, there
carp, weever, Saunders’s Gull, and Little Egret) and it has been found is scant evidence to elucidate cadmium biomagnification in aquatic
that Cd, Zn, and Hg rise as the TL increases, but Ni, Pb, Cr, Mn, Cu, and ecosystems. Older studies suggested that Cd does not biomagnify in
As have the opposite pattern. Concentration of metals (Pb, Hg and Cu) aquatic ecosystems, except for gastropods (Taylor, 1983). This is due to
were increased considerably. However, from clam ranging to Saunders’s the ability of gastropod species to sequester cadmium in their tissues
gull, the biomagnification (Zn, Ni, Mn, Cr, Cd, As) were not significant. (Suedel et al., 1994). Cadmium concentrations rose with trophic levels
In detailed analysis, Pb, Cu and As were not transferred to Purple Heron, in epiphyte-based food webs containing macrophyte-dwelling in
from the Chinese Shrimp, whereas, it’s amplified across the same species vertebrates (for which the first link is epiphytic algae or fishes). Within
for Cr, Mn, Ni, Zn and Hg (Cui et al., 2011). the scope of two trophic connections in both food webs, Cd concentra
In seagrass ecosystem in China which represent the tropical marine tions were biomagnified by around 16-times. Meanwhile, invertebrates
ecosystem, molluscs has a significantly higher concentration of Pb, Zn, had higher Cd trophic enrichment than fish. Cadmium concentrations in
Cu, and Cd than in fish and crustaceans. Besides, aquatic plants also has fish (e.g., largemouth bass) were substantially lower than in their
a remarkably higher concentration of Cr as compared to fish, crusta possible invertebrate prey (e.g., amphipods, snails, and insect larvae)
ceans and molluscs (Hu et al., 2021). Nonetheless, in freshwater (Croteau et al., 2005). This is due to the presence of gills, which is an
ecosystem there’s favourable connection between prey body (amphipod excellent organs to detoxify the metal (Annabi et al., 2013).
crustaceans) and predator’s muscle (zander fish). The examined heavy
metals (As, Cd, Pb, Cu) were substantially higher in zander than the 4.4. Mercury (Hg)
amphipod, validating its biomagnification ability. Furthermore, zander
is proven prone to lead accumulation when the metal analysis shown Mercury in natural waters existed in the oxidation state of Hg(II)
highest concentration of lead in the tissue from among other studied complexes and variety of ligands. One of them is a highly toxic form of
metals (Dehghani et al., 2022). mercury known as methylmercury (MeHg), which poses risks to human
through consumption of fish. This is due to the redox reaction of Hg in
4.2. Arsenic (As) water bodies which affects the amount of Hg(II) for methylation to
MeHg and its subsequent availability for accumulation in fish (Si et al.,
In aquatic settings, the prevailing types of inorganic arsenic (iAs) are 2022). There is lack of research done on the oxidation state and redox
represented by AsV and AsIII. In contrast, elemental arsenic is infrequent, reaction of mercury specifically from the organisms at the lowest to
and arsine (As− III) is observed solely in severely reduced environments highest trophic level in aquatic ecosystems.
characterized by a low redox potential. iAs are more readily soluble in Hg and Zn both biomagnified from small plankton to macro
organisms’s tissues. They are biotransformed for detoxification when zooplankton, and from macrozooplankton to fish (Chen et al., 2000).
they are reduced and methylated for excretion to arsenocholine (AsC) Total mercury (THg) specifically were biomagnified when the positive
and arsenobetaine (AsB), which are less or non-toxic form of arsenic slope of the linear regressions and the significant connection between
(Byeon et al., 2021). This could explain the dynamics of arsenic δ15N and log THg concentration demonstrated that THg biomagnified.
bioavailability to different trophic levels. The reduced THg concentration in pond sediment compared to guano
A number of studies shown vague trend for arsenic trophodynamic and biota (microphyte, shrimp, and fish) could be explained by the
pattern along trophic levels. Some studies had observed bio-diminish of sedimentary Hg pool’s extensive methylation process, which results in
As in freshwater food webs. However, it shown the opposite trend in higher bioavailability for the biota (Signa et al., 2013). In Mekong Delta
estuarine food webs where it biomagnified (Signa et al., 2013). This is biota (POM, phytoplankton, snail, crustaceans, fish), the result of stable
linear with a finding on a freshwater ecosystem (POM, phytoplankton, Nitrogen isotope analysis (δ15N) value associated with Hg levels shown a
fish, crustacean, and gastropod) in Mekong Delta (Ikemoto et al., 2008). substantial positive linear association, indicating that Hg had been
The trophodynamics of arsenic in water depends on its species. In biomagnified (Ikemoto et al., 2008).
freshwater ecosystem, it is common to detect the concentration of Trophic Transfer Factor (TTF) for rainbow trout (Oncorhynchus
arsenosugars in freshwater organism (Schaeffer et al., 2006; Soeroes mykiss), finescale dace (Phoxinus neogaeus) and fathead minnows
et al., 2005), which is in contrast with marine ecosystem, where (P. promelas) methylmercury were discovered. TTFs for methylmercury
arsenobetaine (AsB) is the most abundant arsenic species in marine were shown to be negatively proportionate to dietary exposure levels.
7
N.B. Saidon et al. Environmental Pollution 340 (2024) 122815
For the finescale dace and fathead minnow, the adverse connection was reports on cases of selenium biomagnification on organisms of higher
most prominent at low concentrations diet and became less prominent in trophic level in an aquatic food chain (Córdoba-Tovar et al., 2022). The
rainbow trout as dietary concentrations increased. This demonstrated lack of evidence on selenium biomagnification potential will contribute
that methylmercury biomagnify or increases its concentration in aquatic to the knowledge gap to better understand antagonistic mechanism of
food webs, with TTFs greater than one for all dietary doses tested selenium.
(DeForest et al., 2007).
4.7. Lead (Pb)
4.5. Chromium (Cr)
Lead present in fresh water in its primary form of Pb2+, and the
Chromium is one of the notorious elements in the aquatic ecosys uncommon species in inorganic forms; Pb(HCO)3, Pb(SO4)2− 2 , PbCl,
tems. Chromium existed in the oxidation state of Cr+3 and Cr+6 are PbCO3 and Pb2(OH)2CO3. Meanwhile, in sea water, common lead spe
known to be highly toxic to living organisms and human health cies are PbCl3− > PbCO3 > PbCl2 > PbCl+ > Pb(OH)+ (United Nations
(Kolarova and Napiórkowski, 2021). There is a contrast between Environment Programme, 2010). They are typically bind to sediment
trophodynamic of chromium in marine and fresh water. In marine and SOM. Changes in water environment such as elevated pH or ionic
water, chromium shown biodilution trend across food webs comprising composition can cause the sediment-bounded lead to remobilize and
of crustaceans, gastropods, bivalves and fishes (Gao et al., 2021). This is becomes available for aquatic organisms uptake (United Nations Envi
slightly contradict to a meta-analysis study that concluded chromium as ronment Programme, 2010). Despite lead ability to induced toxicity to
neither biodiluted nor biomagnified (Sun et al., 2020). In fresh water, various living organisms, we found out that the literature discussing its
consistent results were drawn on the tendency of chromium to biodilute biomagnification potential within aquatic ecosystems is still very
in the food chain consisting shrimps and fishes (Zheng et al., 2023; limited. There are plenty of literature discussing the bioaccumulation of
Griboff et al., 2018). It is worth addressing that the conclusion were lead in single species studies, without addressing the trophic transfer
made on two different characteristics of water; brackish and man-made and biomagnification of lead across a food chain in marine or fresh
reservoir. Although there are many studies on the toxicity and water ecosystem. However, some research did elucidate the bio
bioavailability of Cr specifically in aquatic biota, information on its magnification potential of lead, proving that lead shown some differ
transfer across food chain and biomagnification potential are scarce. ences on its enrichment in a food chain. Majority of the result concluded
Besides, most of the available research were conducted in the area of that lead does not biomagnified in a food chain of marine and fresh
tropical and sub-tropical climate. water ecosystems (Cardwell et al., 2013; Kim and Kim, 2016; Orata and
Sifuna, 2023). The concentration of lead remain constant in a food web
4.6. Selenium (Se) consisting of phytoplankton and fish (Cardwell et al., 2013) and low
potential to biomagnify even in a food chain of terrestrial arthropods –
Selenite was identified as the most bioaccumulated form of selenium aquatic plants – fish in fresh water ecosystem (Kim and Kim, 2016). In
species in an organism (Ouédraogo et al., 2015). Selenium in the aquatic sub-tropical region, lead in lake ecosystems shown biomagnification
ecosystems are often studied for its antagonistic effect with mercury potential in the food chain when the tissue of fish is observed for this
upon consumption by the living organisms. In ocean of temperate metal concentration (Chan et al., 2021). The examined location is
climate, high concentration of Se were recorded in marine apex predator heavily mined, thus influencing the high lead bioavailability and influ
(Atlantic blue marlin) from dataset of 1975–2021, where the concen encing the biomagnification of lead from lower trophic to higher trophic
tration of mercury is decreasing, due to the antagonistic effect of sele level.
nium on mercury (Rudershausen et al., 2023). Moreover, selenium also Lead is poorly soluble and naturally existed in very low concentra
shown increasing concentration (biomagnified) in organisms from lower tion in water, and forms complexes with other elements which made
trophic level to higher trophic levels in marine food webs in marine them not bioavailable for intake by the organisms, other than worms and
ecosystem of tropical climate. The concentration, however, decreased mussels intake from the sediment (Orata and Sifuna, 2023). Bio
for the fish species from pelagic – benthopelagic – benthic environment accumulation and consequently biomagnification of lead are dependent
(Zou et al., 2022). Elevated concentration of Se were also recorded in on the bioavailability of lead in an ecosystem.
mesoplankton and crustacean samples from south Atlantic coastal food
webs (Kehrig et al., 2013). In addition to Se magnification, there is a 5. Health risks from consumption of contaminated marine
literature reporting on diminishing concentration of Se when the TMS products
linearity were not significant, suggesting that Se does not biomagnify
from zooplankton to predatory finfish and to bottlenose dolphins (Hong Metals that are bioaccumulated in the consumable marine animals
et al., 2013). Since the species of Se available for organism’s uptake is an could cause detrimental impacts to the consumer due to their high
important factor that affects the trophodynamic of Se, the contrast of Se toxicity and ability to amplify in the food chains. Human in particular
biomagnification could be due to the availability of other oxidative state are exposed to heavy metals by ingesting marine animals that carry
of Se (i.e. selenate) which is more dominant than selenite in the food these persistent elements in their tissues. Carcinogenic effects of heavy
webs (Ouédraogo et al., 2015). metal on human includes skin, lung and urinary bladder tumour. (Lehel
The variation of Selenium biomagnification potential also applies in et al., 2021). Hence, it is extremely important to estimate the risk of
fresh water ecosystem. River or reservoir in a sub-tropical climate did consuming marine products based on the published guidelines.
not induced Se to biomagnify across the food chain of fish – zooplankton The estimation of its potential to cause harm to human by ingestion
– gastropods – bivalves (Ouédraogo et al., 2015). Meanwhile, evidence can be determined by estimated daily intakes (EDI). EDI can be deter
shown that Se did biomagnified from zooplankton to perch in a lake of mined by multiplication of concentration of metal by the average con
temperate climate (Økelsrud et al., 2016). Ideally, in freshwater sumption of fish in a given locality. Given in the formula, EDI = DFC x
ecosystem of a river, Se concentration were increased and varied MC, where; DFC: daily food consumption; MC: mean metal concentra
depending on the trophic level consisting of invertebrates, plankton and tion in food sample (Ahmed et al., 2015). Meanwhile, regulatory
fish. It is also typical for carnivorous fish in an estuary to have higher agencies such as Food and Agriculture Organization (FAO) and World
concentration due to its feeding habits (Córdoba-Tovar et al., 2022). Health Organization (WHO) had established the tolerance limit for
Although selenium is deemed beneficiary to combat the toxic effect accidental intake of metals for human. The intake limits are; Al (2 mg/kg
of mercury, excessive level of this metalloid could induced deformities bw), As (0.1–3 μg/kg bw/d), Cd (2.5 μg/kg bw/month), Cu (0.5 mg/kg
in fish, mammals and birds. However, there were limited number of bw), Pb (0.02–3 μg/kg bw/d (adult), 0.03–9 μg/kg bw/d (children
8
N.B. Saidon et al. Environmental Pollution 340 (2024) 122815
below 4), Hg (4 μg/kg bw); where: bw = body weight, d = day (de loss.
Almeida Rodrigues et al., 2022). A report in 2013 stated that the WHO’s
recommended limit is exceeded by the bivalve Ruditapes decussatus’ Author statement
estimated weekly lead intake near the Mediterranean Sea coast of
Alexandria (Botté et al., 2022). On the other circumstances, cadmium Nadhirah B. Saidon: Conceptualization and writing—original draft
has a 10–30 year elimination half-life and is highly bio-accumulative in preparation; Rita Szabó;: Conceptualization and writing—original draft
mussels, which can accumulates in human body, especially in the kidney preparation; Péter Budai: Writing—review and editing, supervision;
(Stankovic and Jovic, 2012). József Lehel: Writing—review and editing, supervision.
Metal pollutants can be found in foods and the concentration may No conflict of interest exists.
exceeds regulatory limits. Among them, Cd, Hg, As and Pb predomi We wish to confirm that there are no known conflicts of interest
nantly are found at the highest level in marine fish (Bosch et al., 2016). associated with this publication and there has been no significant
Consumption of marine organism such as shrimps, and bottom-dwellers financial support for this work that could have influenced its outcome.
omnivore fish might put consumer health at risk since they tend to
accumulate higher level of metals (Hossain et al., 2022). Residents of the Funding
arsenic-contaminated area are chronically exposed to arsenic pollution
with carcinogenic and non-carcinogenic risks when they ingest Funding was received for this work.
arsenic-contaminated water with fish (particularly for O. mossambicus) All of the sources of funding for the work described in this publica
(Ahmed et al., 2015). However, organic arsenic compounds are less tion are acknowledged below:
poisonous and quickly removed from the human body, there is far less Project no. RRF-2.3.1-21-2022-00001 with the support provided by
reason to worry about food safety in relation to them (Molin et al., the Recovery and Resilience Facility (RRF), financed under the National
2015). Recovery Fund budget estimate, RRF-2.3.1–21 funding scheme.
These instances highlight the significance of monitoring metals
levels in the environment and in edible seafood in order to reduce Intellectual property
chronic metal exposure in human populations. Therefore, it is critical to
monitor metal pollution of coastal waterways globally from an economic We confirm that we have given due consideration to the protection of
and resource sustainability perspective. intellectual property associated with this work and that there are no
impediments to publication, including the timing of publication, with
6. Conclusion respect to intellectual property. In so doing we confirm that we have
followed the regulations of our institutions concerning intellectual
Bioaccumulation and, eventually, trophic transfer were thought to be property.
dependent on assimilation efficiencies, feeding rates, feeding behav
iours, and other parameters influencing contaminant absorption. It’s Authorship
controversial when addressing about biomagnification of heavy metal in
metal ecotoxicology although numerous studies had been conducted We attest that all authors contributed significantly to the creation of
associating biomagnification potential in discrete aquatic ecosystems. this manuscript, each having fulfilled criteria.
In general, arsenic is found to be bio-diminished across food webs in We confirm that the manuscript has been read and approved by all
freshwater ecosystem while it biomagnified in marine. However, it was named authors.
only biomagnified in higher trophic level (tertiary consumer of preda We confirm that the order of authors listed in the manuscript has
tory fish i.e., shark) and dilute its concentration from lower trophic level been approved by all named authors.
(producer, primary consumer, secondary consumer, and tertiary con
sumer (forage fish)). Cadmium also has similar situation where its Contact with the editorial office
magnification behaviour is different. Early study shown that it has no
potential for biomagnification, while later studies prove that cadmium The Corresponding Author declared on the title page of the manu
does magnify for gastropod and epiphyte-based food webs. In addition, script is: Péter Budai.
mercury shown obvious biomagnification potential where studies has This author submitted this manuscript using his/her account.
shown that it can bio-magnify from trophic level as low as particulate We understand that this Corresponding Author is the sole contact for
organic matter (POM) to higher trophic of fish. the Editorial process (including direct communications with the office).
The contradiction of some conclusions drew from researched that has He is responsible for communicating with the other authors about
been conducted shown that the concentration of metals, leading to its progress, submissions of revisions and final approval of proofs.
biomagnification potential across aquatic food chains are heavily We confirm that the email address shown below is accessible by the
influenced by the environmental characteristics of a sampling location. Corresponding Author, is the address to which Corresponding Author’s
The literature analysis conducted for this review proved that there are account is linked, and has been configured to accept email from the
more evidence needed especially in relation to metal speciation avail editorial office. budai.peter@uni-mate.hu.
able for each individual in a food chain. Hence, biomonitoring efforts
should be conducted in different aquatic ecosystems to collect as many Declaration of competing interest
data as possible, narrowing to better conclusions on biomagnification
potential, based on the ecosystem and species-specific interaction. This The authors declare that they have no known competing financial
is crucial to safeguard human health from the detrimental impacts of interests or personal relationships that could have appeared to influence
toxic heavy metals as well as the safety of an aquatic environment. To the work reported in this paper.
avoid biota loss owing to analysis, non-destructive sample procedures
and the utilization of environmental biomarkers could be implemented. Data availability
Furthermore, untreated urban and industrial wastewaters should not be
drained into natural ecosystems such as rivers and farmlands to avoid No data was used for the research described in the article.
heavy metal pollution of food chains. Freshwater sources, such as rivers
and streams, must be preserved from contamination not just for human
benefit, but also to prevent environmental degradation and biodiversity
9
N.B. Saidon et al. Environmental Pollution 340 (2024) 122815
10
N.B. Saidon et al. Environmental Pollution 340 (2024) 122815
Kehrig, H.A., Seixas, T.G., Malm, O., Di Beneditto, A.P.M., Rezende, C.E., 2013. Mercury Plachy, M., Bartha, A., Budai, P., Palotás, P., Lehel, J., 2022. Toxic elements in Sardina
and selenium biomagnification in a Brazilian coastal food web using nitrogen stable pilchardus and food toxicological significance. Food Addit. Contam. B 15, 212–220.
isotope analysis: a case study in an area under the influence of the Paraiba do Sul Poirier, L., Nelson, J., Leong, D., Berhane, L., Hajdu, P., Lopez-Linares, F., 2016.
River plume. Mar. Pollut. Bull. 75, 283–290. Application of ICP-MS and ICP-OES on the determination of nickel, Vanadium, Iron,
Khan, N., Jeong, I.S., Hwang, I.M., Kim, J.S., Choi, S.H., Nho, E.Y., Choi, J.Y., Kwak, B.- and calcium in petroleum crude oils via direct dilution. Energy Fuel. 30, 3783–3790.
M., Ahn, J.-H., Yoon, T., Kim, K.S., 2013. Method validation for simultaneous Rahman, M.A., Hasegawa, H., Lim, R.P., 2012. Bioaccumulation, biotransformation and
determination of chromium, molybdenum and selenium in infant formulas by ICP- trophic transfer of arsenic in the aquatic food chain. Environ. Res. 116, 118–135.
OES and ICP-MS. Food Chem. 141, 3566–3570. Reshqueih, M., Hamidian, A.H., Poorbagher, H., Ashrafi, S., 2014. Investigation of heavy
Kidd, K.A., Muir, D.C., Evans, M.S., Wang, X., Whittle, M., Swanson, H.K., Johnston, T., metal concentrations in sediment, fish and common reed in Sattarkhan dam,
Guildford, S., 2012. Biomagnification of mercury through lake trout (Salvelinus Azarbayjan-Sharghi, Iran. J. Nat. Environ. 67.
namaycush) food webs of lakes with different physical, chemical and biological Rudershausen, P.J., Cross, F.A., Runde, B.J., Evans, D.W., Cope, W.G., Buckel, J.A., 2023.
characteristics. Sci. Total Environ. 438, 135–143. Total mercury, methylmercury, and selenium concentrations in blue marlin Makaira
Kim, H.-T., Kim, J.G., 2016. Uptake of cadmium, copper, lead, and zinc from sediments nigricans from a long-term dataset in the western north Atlantic. Sci. Total Environ.
by an aquatic macrophyte and by terrestrial arthropods in a freshwater wetland 858, 159947.
ecosystem. Arch. Environ. Contam. Toxicol. 71, 198–209. Schaeffer, R., Francesconi, K.A., Kienzl, N., Soeroes, C., Fodor, P., Váradi, L., Raml, R.,
Kim, S.-K., 2020. Trophic transfer of organochlorine pesticides through food-chain in Goessler, W., Kuehnelt, D., 2006. Arsenic speciation in freshwater organisms from
coastal marine ecosystem. Environ. Eng. Res. 25, 43–51. the river Danube in Hungary. Talanta 69, 856–865.
Kolarova, N., Napiórkowski, P., 2021. Trace elements in aquatic environment. Origin, Schaeffer, R., Soeroes, C., Ipolyi, I., Fodor, P., Thomaidis, N.S., 2005. Determination of
distribution, assessment and toxicity effect for the aquatic biota. Ecohydrol. arsenic species in seafood samples from the Aegean Sea by liquid chromatography–
Hydrobiol. 21, 655–668. (photo-oxidation)–hydride generation–atomic fluorescence spectrometry. Anal.
Lavoie, R.A., Jardine, T.D., Chumchal, M.M., Kidd, K.A., Campbell, L.M., 2013. Chim. Acta 547, 109–118.
Biomagnification of mercury in aquatic food webs: a worldwide meta-analysis. Seco, J., Aparício, S., Brierley, A.S., Bustamante, P., Ceia, F.R., Coelho, J.P., Philips, R.A.,
Environ. Sci. Technol. 47, 13385–13394. Saunders, R.A., Fielding, S., Gregory, S., Matias, R., Pardal, M.A., Pereira, E.,
Lee, S., Lingamdinne, L.P., Yang, J.-K., Koduru, J.R., Chang, Y.-Y., Naushad, M., 2022. Stowasser, G., Tarling, G.A., Xavier, J.C., 2021. Mercury biomagnification in a
Biopolymer mixture-entrapped modified graphene oxide for sustainable treatment of Southern Ocean food web. Environ. Pollut. 275, 116620.
heavy metal contaminated real surface water. J. Water Process Eng. 46, 102631. Shahjahan, M., Taslima, K., Rahman, M.S., Al-Emran, M., Alam, S.I., Faggio, C., 2022.
Lehel, J., Yaucat-Guendi, R., Darnay, L., Palotás, P., Laczay, P., 2021. Possible food safety Effects of heavy metals on fish physiology – a review. Chemosphere 300, 134519.
hazards of ready-to-eat raw fish containing product (sushi, sashimi). Crit. Rev. Food Si, L., Branfireun, B.A., Fierro, J., 2022. Chemical oxidation and reduction pathways of
Sci. Nutr. 61, 867–888. mercury relevant to natural waters: a review. Water 14, 1891.
Liu, X.-J., Ni, I.-H., Wang, W.-X., 2002. Trophic transfer of heavy metals from freshwater Signa, G., Tramati, C.D., Vizzini, S., 2013. Contamination by trace metals and their
zooplankton Daphnia magna to zebrafish Danio reiro. Water Res. 36, 4563–4569. trophic transfer to the biota in a Mediterranean coastal system affected by gull
Mao, L., Liu, X., Wang, Z., Wang, B., Lin, C., Xin, M., Zhang, B.T., Wu, T., He, M., guano. Mar. Ecol. Prog. Ser. 479, 13–24.
Ouyang, W., 2021. Trophic transfer and dietary exposure risk of mercury in aquatic Soeroes, C., Goessler, W., Francesconi, K.A., Schmeisser, E., Raml, R., Kienzl, N.,
organisms from urbanized coastal ecosystems. Chemosphere 281, 130836. Kahn, M., Fodor, P., Kuehnelt, D., 2005. Thio arsenosugars in freshwater mussels
Martens, D.A., Suarez, D.L., 1997. Selenium Speciation of Soil/Sediment Determined from the Danube in Hungary. J. Environ. Monit. 7, 688–692.
with Sequential Extractions and Hydride Generation Atomic Absorption Stankovic, S., Jovic, M., 2012. Health risks of heavy metals in the mediterranean mussels
Spectrophotometry. Environ. Sci. Technol. 31, 133–139. https://digitalcommons. as seafood. Environ. Chem. Lett. 10, 119–130.
unl.edu/usdaarsfacpub/502. Suedel, B., Boraczek, J., Peddicord, R., Clifford, P., Dillon, T., 1994. Trophic transfer and
Molin, M., Ulven, S.M., Meltzer, H.M., Alexander, J., 2015. Arsenic in the human food biomagnification potential of contaminants in aquatic ecosystems. Rev. Environ.
chain, biotransformation and toxicology–Review focusing on seafood arsenic. Contam. Toxicol. 136, 21–89.
J. Trace Elem. Med. Biol. 31, 249–259. Sun, T., Wu, H., Wang, X., Ji, C., Shan, X., Li, F., 2020. Evaluation on the
Morales, D.V., 2022. Behavioral and Physiological Effects of Heavy Metals on Fish: A biomagnification or biodilution of trace metals in global marine food webs by meta-
Review and Preliminary Results. Master’s Thesis. City University of, New York. analysis. Environ. Pollut. 264, 113856.
Økelsrud, A., Lydersen, E., Fjeld, E., 2016. Biomagnification of mercury and selenium in Taylor, D., 1983. The significance of the accumulation of cadmium by aquatic organisms.
two lakes in southern Norway. Sci. Total Environ. 566, 596–607. Ecotoxicol. Environ. Saf. 7, 33–42.
Orata, F., Sifuna, F., 2023. Uptake, bioaccumulation, partitioning of lead (Pb) and United Nations Environment Programme, 2010. Final Review of Scientific Information
cadmium (Cd) in aquatic organisms in contaminated environments. Lead, Mercury on Lead - Version of December 2010 [Online]. United Nations Geneva, Switzerland.
and Cadmium in the Aquatic Environment: Worldwide Occurrence, Fate and Available: https://wedocs.unep.org/20.500.11822/27635. (Accessed 20 September
Toxicity 166. 2023).
Ouédraogo, O., Chételat, J., Amyot, M., 2015. Bioaccumulation and trophic transfer of Yousuf, S., Donald, A., Hassan, A., 2022. A review on particulate matter and heavy metal
mercury and selenium in African sub-tropical fluvial reservoirs food webs (Burkina emissions; impacts on the environment, detection techniques and control strategies.
Faso). PLoS One 10, e0123048. MOJ Eco. Environ. Sci. 7, 1–5.
Pachana, K., Wattanakornsiri, A., Nanuam, J., 2010. Heavy metal transport and fate in Zheng, R., Liu, Y., Zhang, Z., 2023. Trophic transfer of heavy metals through aquatic food
the environmental compartments. NU. Int. J. Sci. 7, 1–11. web in the largest mangrove reserve of China. Sci. Total Environ. 899, 165655.
Parikh, Y., Lang, H., Mahmoud, S., Lallo, J., 2015. Sample preparation method for Zhou, Q., Zhang, J., Fu, J., Shi, J., Jiang, G., 2008. Biomonitoring: an appealing tool for
mercury analysis in reagent chemicals by ICP-OES. Spectroscopy 30, 8–17. assessment of metal pollution in the aquatic ecosystem. Anal. Chim. Acta 606,
Pempkowiak, J., Walkusz-Miotk, J., Bełdowski, J., Walkusz, W., 2006. Heavy metals in 135–150.
zooplankton from the southern Baltic. Chemosphere 62, 1697–1708. Znad, H., Awual, M., Martini, S., 2022. The utilization of algae and seaweed biomass for
Pilehvar, A., Town, R.M., Blust, R., 2020. The effect of copper on behaviour, memory, bioremediation of heavy metal-contaminated wastewater. Molecules 27, 1275.
and associative learning ability of zebrafish (Danio rerio). Ecotoxicol. Environ. Saf. Zou, C., Yin, D., Wang, R., 2022. Mercury and selenium bioaccumulation in wild
188, 109900. commercial fish in the coastal East China Sea: selenium benefits versus mercury
risks. Mar. Pollut. Bull. 180, 113754.
11