Effect of Metallic Trace Elements on Fish: History
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Contributor:
Saima Naz
,
Ahmad Manan Mustafa Chatha
,
Guillermo Téllez-Isaías
,
Shakeeb Ullah
,
Qudrat Ullah
,
Muhammad Zahoor Khan
,
Muhammad Kamal Shah
,
Ghulam Abbas
,
Azka Kiran
,
Rubina Mushtaq
,
Baseer Ahmad
,
Zulhisyam Abdul Kari

Metallic trace elements toxicity has been associated with a wide range of morphological abnormalities in fish, both in natural aquatic ecosystems and controlled environments. The bioaccumulation of metallic trace elements can have devastating effects on several aspects of fish health, encompassing physiological, reproductive, behavioural, and developmental functions. 

  • metallic trace elements
  • toxicity
  • growth
  • fish
  • ROS
  • contaminated sites
  • nervous system
  • reproductive system
  • embryonic development

1. Introduction

Recent advancements in industrialization and increased human influence on the environment have caused an exponential increment of different pollutants, such as dyes, metallic trace elements, pharmaceuticals, pesticides, fluoride, phenols, insecticides, and detergents which enter into water resources [1]. These toxicants are serious health concerns for humans and water-living organisms [2]. Similarly, surface water contamination by pesticides is also a serious health-related and environmental issue highlighted at different forums [3]. Bioaccumulation of pollutants in an aquatic ecosystem affects humans and marine life directly and indirectly through the food chain [4]. Metallic trace elements like Cd, Co, Ni, and Pb have been found to impact fishes and other aquatic organisms directly [5]. Majority of metallic trace elements also act as environmental toxins. Some of these metallic trace elements, such as Cu, Zn, Cr, Pb, Cd, Hg, and As affect the health of living beings more adversely as these could quickly transfer from one trophic level to another and hence show higher persistence in the food web [6]. Moreover, the ions of trace elements in water bodies have also become a serious concern globally, as these metallic ions have shown adverse effects on the aquatic ecosystem, and human health [7]. Therefore, simple but effective methods are required for their detection and to maintain water quality to solve water scarcity and further its reuse [8][9]. Despite being able to cause serious damage, these metals are not being identified easily due to insufficient methods and limited laboratory facilities. The present detection methods like UV–Visible spectroscopy, atomic emission spectroscopy (AAS), gas chromatography/mass spectrometries (GC/MS) are not economic and user-friendly [10]. For instance, the technological advancements have raised major concern over environmental safety, due to increasing generation of toxicants [11]. To overcome this and provide ease of analysis, with accuracy and cost effectively, “biosensor” came to existence. A biosensor has a readable biological element, responsible for providing and transforming the information that is used to detect the concentration of a particular analyte in environment. The bio-element based sensors are qualitative, quantitative, and semi-quantitative and can be used against conventional methods [12]. Biosensors possess unique features that make them more adept at measuring the level of metallic trace elements concentration on-site and therefore are advantageous in water quality control. For instance, ligand-rich membranes like tannin-reinforced 3-aminopropyltriethoxysilane crosslinked polycaprolactone (PCL) based nanofibrous membrane have shown effective and quick response to trace elements’ toxicity as compared to uncross linked membranes [13].
Figure 1 illustrates the impact of metallic trace elements on fish from different sources. These selected metals belong to the first transition series of the periodic table and are known to trigger the production of reactive oxygen species (ROS) in living systems, which contribute to their toxicity [14][15]. Exposure to sub-lethal or lethal concentrations of metallic trace elements can lead to stress in fish, which eventually accumulates in various tissues and organs such as gills, kidneys, liver, skin, muscles, etc. [16]. Fish have their defence mechanism to cope with the stressful conditions caused by metallic trace elements exposure by utilizing more energy from reserved carbohydrates, proteins, and lipids in their body. Metallic trace elements such as As, Cd, Cr, Cu, Fe, Hg, Ni, Pb, and Zn are active redox components that contribute to the formation of ROS, which play an essential role in certain physiological functions in fish [15].
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Figure 1. Effects of metallic trace elements on the fish physiology and biochemistry.
The excess of ROS Indicates an imbalance in the production of ROS and causes oxidative stress, which eventually interferes with cellular function by damaging lipids, proteins and DNA [17]. Enzymes such as superoxide dismutase (SOD), catalase (CAT), glutathione S transferase (GST), and non-enzymatic compounds such as reduced glutathione (GSH) are essential in maintaining the dynamic balance of ROS through detoxification. SOD converts superoxide free radicals into hydrogen peroxide, which is further broken down into non-toxic oxygen and water by the CAT enzyme [18]. GST aids in detoxification by catalysing the conjugation of electrophiles to GSH. However, electrophilic substances (free radicals and ROS) can also oxidize GSH non-enzymatically to glutathione disulfide. Any hindrance in the enzymatic reaction can generate excess ROS that accumulates in fish tissues, leading to oxidative stress. ROS can degenerate the cell membrane through lipid peroxidation, causing genotoxicity through DNA damage [17]. There is a wealth of information on the effects of metallic trace elements on fish physiology in various fish species.

2. Effect of Metallic Trace Elements on Fish Collected from Contaminated Sites

Estuaries are highly sensitive zones that serve as a natural conduit for transferring agricultural, industrial, and urban pollution to the sea [19]. Rapid industrial growth during the past century has led to an increase in industrial effluents [20] and anthropogenic run-off in coastal and estuarine environments [21]. The fate of metallic trace elements in water is mainly influenced by their initial concentration and several chemical, physical, and biological factors [22]. Table 1 provides details on the effects of metallic trace elements on fish collected from various contaminated sites.
Table 1. Effects of heavy metals on fish collected from different contaminated sites.
Fish Specie Location Metal
Detected		 Organ Affected Effect on Fish References
Channa striata,
Heteropnuestes fossilis		 Yamuna Barrage (India) Cr, Ni, Pb Kidney, gills,
liver, muscle		 Ruptured veins, hemorrhages in the liver, necrotic urinary tubules. [23]
Clarias gariepinus Abuja (Nigeria) Pb, Cd, Cu, Zn, Cr Liver, gill, kidney, spleen Congested central veins in the liver, interstitial hemorrhages in the kidney, congested splenic vein. [24]
Cyprinus carpio Slovak University of Agriculture in Nitra, University Farm Kolíňany Cu, As, Pb, Cr, Cd, Hg Testes Reduced sperm DNA fragmentation, reduced motility of spermatozoa. [25]
Cyprinus carpio and Capoeta Kor River (Fars Province) Hg, Cd, As, Pb Blood cells, liver, kidney Hyperemia, cellular degeneration, and vacuolation. [26]
Oreochromis niloticus Challawa River (Kano, Nigeria) Zn, Cd, Fe, Pb Muscles Higher bioaccumulation in muscles compared to bioaccumulation factor. [27]
Clarias gariepinus Lake Maryout (Egypt) Cd, Pb, Hg, As Gonads The ovary exhibits lytic characteristics with oocytes at various stages, a decreased quantity of germinal cells, and an augmented interstitial space in the testes. [28]
Auchenoglanis occidentalis Tiga Dam (Nigeria) Zn, Cd, Pb, Fe Gills, liver, kidney Lesions in the gills, liver, and kidney. [29]
Hypophthalmichthys molitrix, Ctenopharyngodon idellus, Carassius auratus, Cyprinus carpio, Silurus asotus Yangtze River Cd, Cr, Cu, Hg, Pb, Zn Fish size Positive and negative relationships were observed between fish size and metal concentration. [30]
Channa striatus,
Heteropneustes fossilis		 Kali River (India) Cr, Cd, Pb, Ni Liver, kidney, gill, muscle, brain Decreased level of glutathione (GSH), increased oxidative stress. [31]
Etroplus maculates, Cirrhinus reba, and Ompok bimaculatus Bhadra River
(Karnataka)		 Cu, Zn, Cd, Ni, Fe, Pb Liver, kidney,
muscle, gills		 Degeneration of the hepatocytes in liver, vacuolar degeneration in the tubular epithelium in kidney. [32]
Oreochromis niloticus, Geophagus brasiliensis, Hoplias malabaricus, Astyanax altiparanae, Rhamdia quelen Sao Francisco do Sul River (Brazil) Cr, Mn, Fe, Ni, Cu, Zn, As, Se, Pb Muscle, liver, and gonads Metals accumulated in the gonads, liver, and muscle, with chromium levels in the muscle reaching fifty times the maximum limit set by Brazilian legislation. [33]
Oligosarcus spp., Chyphocharax voga Sinos River (Brazil) Al, As, Cd, Co, Cr, Cu, Fe, Mn, Zn, Pb Liver Detritivores species accumulated more metals than carnivorous species. [34]
Salminus franciscanus Paraopeba River (Brazil) Cu, Pb, Cd, Zn, Cr, Hg, Fe Liver, spleen, and muscle Hepatocytes exhibited fat accumulation along with pigmented macrophages in the liver. Fibrosis was observed in the spleen, and contaminated fish showed decreased oocyte diameter and increased follicular atresia. [35]
Pseudoplatystoma corruscans Paraopeba River (Brazil) Hg, Cd, Zn, Cr, Pb Liver, muscle, and spleen The liver and spleen showed higher concentrations of metals compared to the muscle. Additionally, liver fibrosis was observed. [36]
Bryconamericus iheringii Ilha River
(Brazil)		 Al, Cd, Mn, Ni, Fe, Pb, Cr, Zn Blood—micronucleus analysis, gills, and muscle In rural areas, a higher frequency of micronuclei, nuclear abnormalities, and mucous cells was detected. Conversely, urban areas exhibited a lower condition factor, higher frequencies of lamellar alterations, and higher concentrations of chromium (Cr) and nickel (Ni) in muscle. [37]
Prochilodus magdalenae, Pimelodus blochii Magdalena River (Colombia) Cd, Pb, Ni Gills, liver, and muscle Pimelodus Blochii showed a higher accumulation of metals, particularly an increased concentration of cadmium (Cd) in the liver. [38]
Aequidens metae, Astyanax bimaculatus Ocoa River
(Colombia)		 Hg, Cd Blood and liver There was a decrease in the number of erythrocytes, lymphocytes, and neutrophils, as well as a decrease in hemoglobin concentration and hematocrit percentage. [39]

3. Effect on the Nervous System

Deposition of various metallic trace elements in fish can cause serious damage to the nervous system, affecting behaviour, response to stimuli, and recognition patterns among fish [40]. Mercury is known to cause numerous disorders, primarily on the biochemical level in the central nervous system of fish. For example, exposure to HgCl caused a significant increase in lipid peroxidation and depletion of total lipids in the brain of catfish (Heteropneustes fossilis) [41]. Copper-induced morphological abrasions are evident in the sensory organs of fish [40]. Copper is a vital metal and a fundamental component of many enzymes, but it can be extremely toxic to fish when its concentration exceeds normal levels [42], especially in freshwater due to the high ionic copper content [43]. Increased Cu concentration in cellular membranes reduces the antioxidative capacity of lipids, causing lipid peroxidation and severe damage to cellular membranes [44].
As the formation of free radicals and lipid peroxidation increases, they can cause serious cellular trauma. In Cu-exposed marbled electric ray (Torpedo marmorata), ultrastructural analysis of neurons in the central nervous system showed an increased number of lipofuscin granules erosion of mitochondria [45] and a reduction in Golgi apparatus as well [46]. Long-term exposure to Pb can cause neurochemical changes in the brain of walking catfish (Clarias bathrachus). For instance, Pb increases the histamine and serotonin levels while decreasing the gamma-aminobutyric acid (GABA), monoamine oxidase (MAO), and acetylcholinesterase (AChE) contents. Furthermore, cholesterol, brain lipid, and protein contents are also decreased [47]. The adverse effects of different metals on the nervous system (CNS and peripheral) from various studies are compared (Table 2).
Table 2. Effects of heavy metals on nervous system of different fish species.
Fish Species Metal Concentration (mg L−1) Metal Composition Stage of Exposure Exposure Duration Effect Observed on Fish References
Effect of Cadmium (Cd)  
Danio rerio 0.970 Cd † Juvenile 12 h Elevated immunotoxicology. [48]
Danio rerio 0.040 CdCl2 0–168 hpf 7 days Increased rotational movement, Hyperactivity, and decreased size of otolith. [49]
Pimephales promelas 0.003 Cd(NO3)2 Adult 4 days Elevated auditory threshold. [50]
Pimephales promelas 0.060 CdCl2 Adult 21 days Decreased vitellogenin gene expression and increased estrogen receptor beta. [51]
Danio rerio 0.112 CdCl2 0–96 hpf 4 days Immunotoxicity, behavioural alteration, and oxidative stress. [52]
Effect of Mercury (Hg)  
Diplodus sargus 0.002 HgCl2 Juvenile 7 days Increased anxiety, decreased number of optic tectum cells, and altered swim behaviour. [53]
Pimephales promelas 0.720 MeHg Adult 30 days Decreased levels of dopamine and hyperactivity. [54]
Danio rerio 10 MeHg Adult 56 days Mitochondrial dysfunction, and
oxidative phosphorylation.		 [55]
Danio rerio 0.720 MeHg Adult and embryo 30 days Decreased level of dopamine and hyperactivity. [56]
Danio rerio 0.027 HgCl2 5–72 hpf ~3 days Hyperactivity causing mortality. [57]
Effect of Lead (Pb)          
Danio rerio 0.010 Pb(CH3COO)2 0–72 hpf 3 days 10 Gene expression changes in 89 genes associated with nervous system development. [58]
Danio rerio 0.020 Pb(CH3COO)2 0–144 hpf 6 days Decreased axon length and decreased locomotion (speed). [59]
Danio rerio 0.100 Pb(CH3COO)2 2–120 hpf ~5 days Altered color preference (adults). [60]
Danio rerio 0.207 Pb(CH3COO)2 2–24 hpf ~2 days Decreased learning (adults). [61]
Danio rerio 1.730 Pb(CH3COO)2 0–24 hpf 24 h Decreased Nrxn2a gene expression. [62]
Effect of Copper (Cu)          
Cyprinus carpio 0.60 Cu Juvenile 96 h Increases in brain ROS production, lipid peroxidation, and protein oxidation. [63]
Capoeta umbla 3.0 CuSO4∙5H2O 112 ± 5 g 96 h Induce astroglial response accompanied by modulations of NF-kB and PARP-1 expression. [64]
Danio rerio 0.100 CuSO4∙5H2O Adult 10 days Negatively affect the associative learning capabilities. [65]
Oreochromis niloticus 120 CuSO4∙5H2O Adult 96 h Loss of balance and exhaustion. [66]
Effect of Arsenic (As)          
Danio rerio 15 Na2HAsO4 Adult 96 h Alteration in behaviour and ectonucleotidase activities. [67]
Danio rerio 0.050 As2O3 Juvenile 96 h Antagonistic effects on brain. [68]
Danio rerio 0.500 As+ Larvae, juvenile and adult 96 h Alteration in motor function
(embryo-adult), effects on associative learning.		 [69]
Clarias batrachus 20 As2O3 Adult 96 h Increased body discoloration, excessive mucous secretion, loosening of the skin, and complete loss of skin (head region and fins). [70]
Effect of Zinc (Zn)          
Anguilla anguilla 0.12 Zn Juvenile 28 days Cholinergic neurotoxicity did not occurr, only liver GST increased significantly. [71]
Leporinus obtusidens 4.57 ZnSO4·5H2O Adult 45 days Significantly increased AChE activity. [72]
Danio rerio 1750 ZnCl2 Adult 25 days Significant decrease in acetylcholinesterase activity and abnormal neural signaling. [73]
Note: † Metallic trace elements written without their respective chemical formulas were administered in their metallic forms.

4. Effect on the Reproductive System

The adverse effects of metals on the fish reproductive system are increasing every day, mainly due to increased water pollution and the usage of polluted water for fish culture. Healthy eggs and sperms are essential for the process of successful fertilization. However, the quality of eggs and sperm is affected by induced spawning, gamete storage methods, and more importantly, water pollution. The motility time of spermatozoa is very important for effective fertilization. According to the literature, sperm motility is affected by metallic trace elements. For example, although the sperm morphology of mummichog (Fundulus heteroclitus) was not affected by methylmercury (CH3Hg), it triggered a significant loss in the motility of sperms [74][75]. Lead, Cd, and Cu caused a significant decrease in the motility of European carp (Cyprinus carpio) spermatozoa [76][77][78].
Similarly, Cu toxicity caused adverse effects in the spermatozoa activity in C. carpio [79], while Sionkowski et al. [80] showed that the higher concentration of Cu and Pb caused reduced spermatozoa motility in grass carp (Ctenopharyngodon idella). Likewise, the effects of Zn on the sperm motility of some common carp were also explored. Metallic trace elements are also responsible for several endocrine complications among fish. For example, Cd decreased the thyroid hormone level, inhibited the estrogen receptors, and interrupted the expression of growth hormone [81]. On the other hand, iodine metabolism interruption by Pb was also recorded to inhibit thyroid synthesis [82]. Prooxidative possessions of the metal ions could also cause oxidative harm to the cell membrane. They can also induce oxidative stress in fish. Lead, Pb, and Cu can also trigger the genotoxic effects on the fish [83][84][85]. A tabulated review of different references is provided to show the deteriorating effects of different metals on fish’s reproductive system (Table 3).
Table 3. Effects of heavy metals on reproductive system of different fish species.
Fish Species Metal Concentration (mg L−1) Metal Composition Stage of Exposure Exposure Duration Effect Observed on Fish References
Effect of Cadmium (Cd)          
Heteropneustes fossilis 0.050 CdCl2 Adult 24 h Decreased ovulation. [86]
Pimephales promelas 0.005 CdCl2 12 months 21 days Reduced egg production. [51]
Oryzias melastigma 0.010 CdCl2 5 months 30 days Decreased gonadal development. [87]
Prochilodus magdalenae 24.90 CdCl2 2 years 7 days Reduced fertility rate. [88]
Effect of Mercury (Hg)          
Heteropneustes fossilis 0.050 HgCl2 Adult 24 h Increased germinal vesicle breakdown. [86]
Cyprinus carpio 4.990 HgCl2 3 years 12 h Decreased motility and fertility of sperms, damaged eggs. [89]
Oncorhynchus mykiss 10.00 HgCl2 3 years 4 h Reduced motility of sperm. [90]
Danio rerio 0.015 HgCl2 Adult 5 days Delayed gonadal development,
imbalanced sex hormone.		 [91]
Danio rerio 0.030 HgCl2 Adult 30 days Decreased testosterone level. [92]
Clarias gariepinus 0.119 HgCl2 Adult 30 days Disruptive effect on gamete development. [93]
Effect of Lead (Pb)          
Heteropneustes fossilis 0.050 (Pb(NO3)2 Adult 96 h Increased germinal vesicle breakdown. [86]
Clarias gariepinus 140.0 Pb(C2H3O2)2 Adult 96 days Reduced sperm motility. [94]
Oryzias melastigma 0.050 PbCl2 5 months 30 days Decreased gonadal development. [87]
Effect of Copper (Cu)          
Danio rerio 0.040 CuSO4 Adult 30 days Damaged structure of gonads, altered steroid hormone level. [95]
Pimephales promelas 0.075 CuCl2 12 months 21 days Decreased abundance of post-vitellogenic follicles, increased follicular atresia. [96]
Daphnia magna 1.041 CuCl2 Adult 21 days Reduced rate of reproduction. [97]
Poecilia reticulata 45 CuO Adult
Larvae		 96 h Decreased reproduction success. [98]
Poecilia reticulate 0.026 CuSO4 5H2O 2.5–3 months 56 days Gonadosomatic index, offspring production decreased. [99]
Effect of Arsenic          
Gobiocypris rarus 40.00 NaAsO2 3 months 96 days Accumulation in testis. [100]
Daphnia magna 0.049 NaAsO2 Adult 48 h Stable reproduction rate. [101]
Gambusia affinis 0.075 NaAsO2 Juvenile 30 days Lower gonadal-somatic indices. [102]
Effect of Zinc (Zn)          
Odontesthes bonariensis 0.021 ZnSO4 7H2O Adult 10 days Reduced embryo and larval survivability. [103]
Danio rerio 500 Zn Adult 4 days Majority of eggs were dead, larger hatching time. [104]
Clarias magur 300 Zn(CH3COO)2 Mature 60 days The highest GSI and fecundity. [105]
Oryzias melastigma 0.010 ZnSO4·7H2O Adult 30 Irregular oocytes, partly adhesion, empty follicle, and increased follicular atresia, loose follicular lining. [87]

5. Effect on Embryonic Development

The influence of water-borne metals can disrupt the embryonic development of spawners. [106] found elevated levels of Cd, Zn, and Pb in the female gonads of stone loach when exposed to toxic concentrations of these metals. Ellenberger et al. [107] investigated the levels of Cu in the reproductive organs of European perch (Perca fluviatilis) exposed to Cu-polluted ponds. White suckers in polluted lakes exhibited higher amounts of Cu and Zn in their testicles and female gonads compared to fish in uncontaminated water [108][109]. Common carp exposed to Cu, Cd, and Pb showed decreased egg swellings in a concentration-dependent manner, contrasting with about 40% expansion in egg width observed in the untreated groups [110]. Copper and Cd accumulation in the gonads of Mozambique tilapia (Orechromis mossambicus) was found to be elevated when fish were kept in metal-polluted water, and blue tilapia (Oreochromis aureus) exposed to Cd and Pb for seven days showed metal accumulation in the testicles and female gonads, particularly Cd levels in the ovaries [111]. Metal exposure to spawners can result in the deposition of metallic trace elements accumulated in eggs and sperm, severely affecting the survival of fertilized eggs and the embryonic development of fish [79].
Metals can also influence the physical characteristics of an egg’s outer surface. Benoit and Holcombe [112] observed that eggs of Zn-exposed fathead minnow (Pimephales promelas) became sticky and more prone to breakage soon after egg laying. Fathead minnow embryos rapidly absorb Hg from surrounding water sources, with concentrations in juveniles increasing to 2.80 µg per gram humid mass after four days of exposure to 25 µg per cubic decimeter of methylmercury [113]. Chromium was found to accumulate in the outer protective coatings of Cyprinus carpio eggs at pH 6.3 [114]. Copper can alter selective membrane permeability, disrupting cation trade between the liquid in the yolk membrane and the outside water [115]. During the early development of fish eggs in a toxic (metallic trace elements) environment, the outer protective coating of the egg blocks most of the metal concentration, but a significant toxic amount still enters the fluid inside the egg membranes, while only a small amount infiltrates the embryo [116]. Beattie and Pascoe [117] found that eggs of Atlantic salmon (Salmo salar) exposed to 10 mg per litre of Cd at 22 h old retained 98% of the metal in the outermost membrane. Similarly, the outer membrane of Japanese rice fish (Oryzias latipes) eggs retained 94.4% of Cd [118]. In Zn-treated Atlantic herring (Clupea harengus) eggs, 30% to 50% of Zn accumulated in the outermost membrane, while the rest accumulated primarily in the yolk sac and in lower quantities in the embryos. However, even a small amount of metals penetrating the egg can significantly influence fish embryonic growth [117][119]. Devlin [113] observed significant abnormalities in fathead minnow embryos treated with Hg, including spinal curves, heart damage, and abnormal growth of the heart cavity. Samson and Shenker [120] reported tissue anomalies in zebrafish (Danio rerio), including abnormalities in fin overlaps and caudal parts.
The first 24 h of fish embryonic development are the most vulnerable to metallic trace elements toxicity. A study found that during the first 24 h after insemination in contaminated water, almost 20% of developing embryos died, even in a controlled environment [121]. The blastula stage had the highest mortality rate (15%), and metal exposure during this stage significantly affected the life span of developing embryos. Embryos exposed to 0.1 mg/L of Cu had significantly decreased survival rates compared to the control group, and at 0.3 mg per litre, all embryos died. Copper exposure caused most fish embryo deaths during the blastula stage (25%), followed by the stage of body division (15%). However, embryo mortality decreased significantly at later developmental stages [79]. Slominski et al. [121] also reported that mortality significantly declined during organ formation, the division of the body, and eye coloration phases. Most fetuses (5%) expired during organ formation before the eye coloration phase. Metallic trace elements toxicity also increases the death of fish hatchlings in various species, including rainbow trout (Onchorynchus mykiss), Atlantic salmon, common carp, and grass carp. Freshly inseminated ovum of Oncorhynchus mykiss were more susceptible to Ni than the embryo at the organogenesis stage, while goldfish (Carassius auratus) eggs’ mortality was greater during the blastula stage than at the eyed stage when exposed to Cd or Hg. Rainbow trout (Oncorhynchus mykiss) fetuses were more vulnerable at the eyed stage than newly inseminated eggs when presented with a mixture of metals. The abnormalities caused by different metallic trace elements at the embryonic stages of fish are reviewed in Table 4.
Table 4. Effects of heavy metals on embryonic development fish species.
Fish Species Metal Concentration (mg L−1) Metal Composition Stage of Exposure Exposure Duration Effect Observed on Fish References
Effect of Cadmium (Cd)          
Leuciscus idus 0.1000 CdCl2 Egg, sperm 21 dpf Reduced larval survival, growth, and delayed development. [78]
Oryzias latipes 0.0019 CdCl2 2H2O Embryo, larva 20 dpf Morphological abnormalities were observed. [122]
Cyprinus carpio 0.06 CdCl2 Eggs 60 dpf Retardation in the developmental stages of eye pigmentation and spine curvature, lack of tail formation and head. [123]
Danio rerio 34.8 CdCl2 72 hpf 72 h Neuromast damage, coagulated egg, increased mortality rate. [124]
Danio rerio 0.8018 CdCl2 6 hpf 24 h Increased apoptotic event and induced cell death in brain of embryo. [125]
Leuciscus idus 0.1 CdCl2 Embryonic and larval 21 days Reduced embryonic survival, increased frequency of malformation, and delayed hatching. [78]
Danio rerio 0.8909 CdCl2 Embryonic and larval 96 hpf Increased heartbeat rate of larvae and decreased brain size. [126]
Leuciscus idus L. 0.1 CdCl2 Embryos and newly hatched larvae 2 h Reduced egg swelling, slowed the rate of development (especially body movements), and delayed hatching. [127]
Odontesthes bonariensis 0.00025 CdCl2 Advanced-stage embryos and newly hatched larvae 10 days Decreased hatching rate and survival of embryo and larvae. [103]
Effect of Mercury (Hg)          
Danio rerio 0.016 HgCl2 Adult 2 hpf T3 and T4 content in larvae increased. [128]
Danio rerio 0.016 HgCl2 Adult 168 hpf Decreased hatching rate, increased mortality, increased malformation rate in larvae. [92]
Cyprinus carpio 0.00001 HgCl2 Embryo 96 h SOD and GPx reduced up to 85%. [129]
Effect of Lead (Pb)          
Danio rerio 0.100 Pb (C2H3O2)2 Adult 30 dpf Distance moved by juvenile zebra fish decreased, and swimming activity alterations in larvae and juvenile fish. [130]
Danio rerio 0.005 Pb (CH3COO)2 Adult 144 hpf Delayed hatching, spinal and tail deformity, pericardial edema, and yolk swelling was observed. [131]
Danio rerio 99.885 Pb (C2H3O2)2 Adult 72 hpf Deformed CNS, increased levels of Gamma-aminobutyric acid (primary inhibitory neurotransmitter). [132]
Danio rerio 1.6 Pb (NO₃)₂ Embryo 120 hpf Spinal malformation. [133]
Pterophyllum scalar 20 PbCl2 Embryo 3 days Tilt, loss of vision or the lack of effect on growth delay. [134]
Effect of Copper (Cu)          
Leuciscus idus 0.100 CuSO4·5H2O Egg, sperm 21 dpf Reduced larval survival, growth, and delayed development. [78]
Oryzias latipes 0.0185 CuCl2 H2O Embryo, larva 20 dpf Percentage of deformed larvae significantly increased. [122]
Poecilia reticulata 1.50 CuSO4·5H2O Embryo 15 days Abnormalities in blastodisc to middle-eyed stages of development. [135]
Danio rerio 0.018 CuSO4 72 hpf 72 h Neuromast damage, coagulated egg, increased mortality rate. [124]
Leuciscus idus 0.10 CuSO4·5H2O Embryo and larval 21 days Reduced embryonic survival, increased frequency of malformation. [78]
Leuciscus idus L. 0.10 CuSO4 Embryos and newly hatched larvae 2 h Reduced egg swelling slowed the rate of development (especially body movements) and delayed hatching. [127]
Odontesthes bonariensis 0.00025 CuSO4 Advanced-stage embryos and newly hatched larvae 10 days Decreased hatching rate and survival of embryo and larvae. [103]
Carassius auratus 1 Cu2− Embryo 24 h post-hatching Scoliosis and tail curvatures. [136]
Effect of Arsenic (As)          
Danio rerio 360.32 NaAsO2 Adult 120 h Tail bud deformation in embryo. [137]
Danio rerio 0.5 NaAsO2 Adult 120 hpf No effect on mortality and developmental deformations. [138]
Labeo rohita 198.18 NaAsO2 Adult 120 hpf Reduced survival rate with abnormal development. [139]
Danio rerio 0.5 NaAsO2 Embryo 14 dpf Thinning of the retinal pigmented epithelium (RPE) layer in embryos. [140]
Effect of Zinc (Zn)          
Odontesthes bonariensis 0.021 ZnSO4 7H2O Hatchling 10 days Cumulative embryo survival was significantly reduced. [103]
Pagrus major 2.5 ZnCl2 2 years 10 days Low hatching rate, high mortality, abnormal pigmentation, hooked tail, spinal deformity, pericardial edema, and visceral hemorrhage. [141]
Melanotaenia fluviatilis 33.3 Zn Embryo 2 h Spinal deformities. [142]

This entry is adapted from the peer-reviewed paper 10.3390/w15163017

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