Content of Short-Lived Radionuclides (⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn) in Fish

Abstract

This review summarizes data on the accumulation of three short-lived biogenic radionuclides—⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn—in various fish species in the cooling pond of the Chornobyl Nuclear Power Plant in Ukraine, along with an analysis of the available literature. Significant differences exist in ⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn accumulation levels among the different fish species. Food intake is the primary pathway for these radionuclides to enter the fish organisms. These radionuclides accumulate differently in various organs and tissues. There is no consensus on the specific organ that primarily accumulates each radionuclide. In most studies, the highest concentrations of ⁵⁴Mn have been recorded in internal organs. The kidneys are identified as the main organ accumulating ⁶⁰Co. The highest concentrations of ⁶⁵Zn are typically found in the liver and kidneys; however, significant accumulation is also noted in external organs and tissues (gills, fins). In most cases, the lowest concentrations of ⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn are observed in the muscle tissues of fish.

1. Introduction

Short-lived radionuclides such as ⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn enter the environment through nuclear explosions, accidents, and regulated emissions from nuclear facilities and mining plants [1]. Their accumulation in fish is critical for understanding ecological and human health risks. These radionuclides vary in half-lives, making their study in nature challenging: ⁶⁰Co (5.27 years), ⁵⁴Mn (312 days), and ⁶⁵Zn (245 days) [2].

Metals enter fish via gills, skin, and the gastrointestinal tract, transporting through the bloodstream and binding to proteins. This results in differential accumulation across organs, with external tissues acting as primary entry points, while internal organs like the liver and kidneys show the highest concentrations [3,4].

Manganese plays a role in metabolic functions, influencing respiration, bone formation, and reproduction. It remains relatively stable in fish tissues, irrespective of external concentrations [3,5]. Cobalt, vital for hemoglobin synthesis, aids in iron assimilation and influences calcium and phosphorus metabolism [5]. Zinc is crucial for enzymatic reactions, tissue oxygenation, and redox processes, accumulating predominantly in bones and scales [3,5].

One of the earliest studies on ⁵⁴Mn and ⁶⁵Zn accumulation in marine organisms was conducted in the Atlantic Ocean, near Beaufort, North Carolina, between 1964 and 1966. The research revealed that levels of these radionuclides varied among different aquatic organisms. For example, the highest concentration of ⁶⁵Zn was observed in the mollusk Crassostrea virginica (Gmelin, 1791), while Argopecten irradians (Lamarck, 1819) showed the highest levels of ⁵⁴Mn [6]. Similarly, research on the genus Oncorhynchus fish on the U.S. Pacific coast during the 1960s detected high ⁶⁰Co and ⁶⁵Zn levels in liver and roe, exceeding muscle concentrations [7].

Similar studies were carried out in freshwater ecosystems. For instance, between 1963 and 1967, ⁶⁵Zn was found in the body of Acipenser transmontanus (Richardson, 1836) sampled from the Hanford Reach River and the McNary Pool (USA) [8]. By 1990, this radionuclide was undetectable in the species. Poston T.M. and Klopfer D.C [3] concluded that these isotopes accumulate unevenly in different organs and tissues of fish. The highest concentrations of ⁶⁰Co were found in the kidneys, while the lowest levels of ⁵⁴Mn were observed in muscle tissue, with bone tissue showing the highest levels of this radionuclide. The distribution of ⁶⁵Zn in fish organs and tissues was as follows: kidneys = gonads > liver > gills > muscles = heart.

The radiation risk to humans from consuming fish containing short-lived isotopes (e.g., ⁶⁵Zn) was assessed in the United States in the mid-1960s. During an experiment, volunteers consumed the muscle tissue of Coregonus houi (Linnaeus, 1758) from the Columbia River daily for 11 weeks. The concentration of ⁶⁵Zn in the fish muscle was 5 nCi/200 g (i.e., 185 Bq/200 g) of fresh weight. The researchers concluded that this concentration of ⁶⁵Zn in the fish muscle posed no significant health risk to humans [9]. Although global fallout decreased after atmospheric nuclear test bans, research on ⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn continued, focusing on uptake mechanisms.

Despite the rapid disappearance of manganese, cobalt, and zinc radionuclides from the environment following the ban on atmospheric nuclear tests and the subsequent decline in global fallout, interest in studying the accumulation of ⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn by fish persisted. Throughout the 1970s and 1980s, researchers conducted laboratory studies to investigate the primary pathways through which these radionuclides enter fish and the variations in their accumulation across different organs and tissues.

Laboratory experiments confirmed food as the primary uptake pathway for ⁵⁴Mn and ⁶⁵Zn, while ⁶⁰Co is absorbed from both food and water [10,11,12,13]. Pentreath [14] found that waterborne cobalt contributes minimally to fish uptake. Studies with Seriola quinqueradiata (Temminck and Schlegel, 1845) showed that ⁶⁰Co concentrates in blood-rich organs, while ⁵⁴Mn accumulates in bones, and ⁶⁵Zn distributes evenly across organs and muscles [10].

Research on Phoxinus laevis (Kessler, 1879) found that kidneys retained the highest ⁶⁰Co levels, while ⁵⁴Mn accumulated mostly in external organs [15]. Another study on Pleuronectes platessa (Linnaeus, 1758) confirmed that ⁵⁸Co concentrates in intestines and gills, with minimal muscle accumulation [14]. In experiments conducted by Koyanagi T. et al. [16], radionuclides ⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn were introduced directly into the stomach of Kareius bicoloratus (Basilewsky, 1855) in the form of gelatin capsules filled with moist bottom sediments containing these radionuclides. The distribution of radionuclides across organs and tissues was determined one week after introduction. The highest concentrations of ⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn were detected in the intestines. High levels in internal organs (liver and kidneys) indicated a relatively rapid transfer of radionuclides from the stomach to these organs. Muscles generally contain the lowest levels of radionuclides.

Pentreath [11] found that ⁶⁵Zn in P. platessa distributes evenly across bones, skin, and muscles, with high gonadal levels. Studies on Raja clouata (Linnaeus, 1758) showed ⁶⁵Zn concentration in the liver and spleen, while ⁵⁴Mn accumulated in cartilage and the highest ⁵⁸Co levels were in gills and heart [12].

Different aquatic species accumulate radionuclides at varying rates. Experiments showed that algae rapidly absorb and release ⁶⁰Co, while mollusks and fish retain it longer [13]. These findings underline the need for continued research into radionuclide behavior in aquatic ecosystems and their implications for environmental safety.

The study of short-lived radionuclides is particularly important due to their ecological and human health implications. These radionuclides can enter the environment following nuclear accidents, such as the Chornobyl disaster, leading to contamination of aquatic ecosystems. Understanding the behavior of these radionuclides in fish populations is crucial for assessing their potential risks to ecosystem stability and human consumers.

One of the key challenges in studying short-lived radionuclides is their rapid decay, which makes long-term tracking and analysis difficult. This has resulted in inconsistencies in the literature regarding organ-specific accumulation and uptake pathways. Additionally, differences in experimental conditions, species physiology, and environmental factors further complicate the interpretation of results, leading to a lack of consensus on the distribution of these radionuclides in fish tissues.

The objective of this review is to synthesize the available literature on the accumulation and distribution of ⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn in fish, highlighting key findings and unresolved questions. It aims to discuss pathways of uptake, organ-specific behavior, and potential implications for both ecological stability and human health. By identifying existing knowledge gaps, this review seeks to inform future research directions and enhance risk assessment methodologies. Understanding these processes is essential for developing improved environmental monitoring strategies and ensuring the safety of aquatic food resources.

2. Methodology

To perform this literature review, focusing on the content of short-lived radionuclides in fish, we utilized a variety of databases and search engines. We selected Scopus, PubMed, and Google Scholar as our primary sources for the literature, as well as the institutional library of the Institute for Nuclear Research of the National Academy of Sciences of Ukraine in Kyiv. The keywords included bioaccumulation, fish, content, radioactive element, radionuclides, manganese, cobalt, zinc, Chernobyl, Chornobyl, nuclear testing, global fallout, water contamination, mining, ecological half-life, etc., and the search results were further specified by the employment of a combination of keywords with Boolean operators (AND, OR, NOT). We included peer-reviewed articles published in English, Russian, and Ukrainian. We excluded the studies that were not available in full text and the research that was not directly related to aquatic biota. We included some illustrative experimental data (Tables 1–4) to discuss the literature findings. These data were obtained from controlled studies in the Chornobyl area performed by N. E. Zarubina.

3. Impact of the Chornobyl Nuclear Accident on the Cooling Pond and Its Biota

The unprecedented nuclear disaster at Chornobyl on 26 April 1986 led to extensive radionuclide contamination of vast areas. The levels of these radionuclides in the biological components of the water bodies within the 30 km exclusion zone soared to tens of thousands or even tens of millions of times higher than pre-accident levels. Among the most contaminated sites was the Chornobyl Nuclear Power Plant’s (ChNPP) cooling pond (CP).

During the accident response, including firefighting and cleanup operations, irradiated construction materials, graphite fragments, nuclear fuel, and various kinds of contaminated debris were introduced into the CP. In 1986, decontamination efforts at the plant site resulted in dust, debris, and dirt being washed into the intake and, to some extent, the discharge channels of the pond. Dust generation and waste from constructing the “sarcophagus” also contributed to the additional influx of radioactive materials into the CP [1].

Initial assessments indicate that up to 200,000 Ci (approximately 7.4 × 10¹⁵ Bq) of various fission products were introduced into the CP during the early phases of the disaster [17,18].

Before 2013, when the water level of the CP was reduced by halting water inflow from the Prypiat River, the CP was an artificial pond located southeast of the NPP and created by damming a section of the river’s floodplain. The dam stretches 21.6 km, with a drainage channel running along its downstream slope, divided into northern and southern sections. The CP is roughly oval, encircled by a levee, with a divider dam along its longitudinal axis. A coastal pumping station in the northeast replenished water losses by drawing from the river [1] (Figure 1, Figure 2 and Figure 3).

Before the accident, the CP’s warm waters were used for industrial fish farming [1]. From its establishment as an experimental fish tank farm in 1978–1979, it developed into a powerful industrial fish production facility by 1986. Various fish species, including Hypophthalmichthys molitrix (Valenciennes, 1844), Aristichthys nobilis (Richardson, 1845), Ctenopharyngodon idella (Valenciennes, 1844), Ictalurus punctatus (Rafinesque, 1818), and several breeds of carp and crucian carp were raised in fish tanks. Experiments were also conducted on cultivating sturgeon and salmon species. Moreover, the CP was stocked with valuable fish species such as H. molitrix, A. nobilis, C. idella, and Cyprinus carpio (Linnaeus, 1758) [19].

4. Radionuclide Contamination in Chornobyl NPP Cooling Pond: Effects on Water and Aquatic Biota

The primary source of radionuclide contamination in the CP under normal plant operating conditions was liquid effluents, including imbalanced water and waste from specialized laundries and sanitary checkpoints. The greatest volume of imbalanced water discharge typically occurred during the plant’s initial operating period [20]. Before the 1986 accident, the presence of ⁵⁴Mn and ⁶⁰Co in CP water was regularly detected, although at low concentrations—no more than 0.003 Bq/L in 1980. These radionuclides were quickly removed from the water, predominantly accumulating in the sediment and aquatic vegetation. For example, sediment samples taken in the fall of 1981 showed radionuclide levels of 243 Bq/kg for ⁵⁴Mn and 500 Bq/kg for ⁶⁰Co, while ⁶⁵Zn was not detected in either water or sediment before the accident [21].

Manganese (⁵⁴Mn): Before the accident, ⁵⁴Mn levels in free-living fish species were relatively low, with the highest concentration in muscle tissue at 8.5 Bq/kg. Levels in the head and internal organs did not exceed 23.5 Bq/kg. The peak influx likely occurred in 1980–1981, and by 1985, due to its short half-life, ⁵⁴Mn levels had decreased. It was primarily found in non-predatory planktophages and benthophages, with significantly lower levels observed in fish raised in tanks on clean, artificial feeds. After the accident, ⁵⁴Mn concentrations in all the CP’s components increased significantly but were detected in only 3–4% of approximately 5000 radionuclide measurements. The highest specific activity of ⁵⁴Mn was observed in the water’s vegetation in March 1987, at 2000 Bq/kg dry weight. In fish, ⁵⁴Mn levels were orders of magnitude lower than those of other radionuclides, generally ranging between 10 and 500 Bq/kg fresh weight, with the highest concentration (561 Bq/kg) found in the roe of Perca fluviatilis (Linnaeus, 1758) in March 1988. Post-accident, ⁵⁴Mn was still primarily detected in benthophages and planktophages, but unlike pre-accident data, it was now mainly found in the internal organs, comprising over 50% of the detections. Its distribution across fish tissues was relatively uniform, with no single organ or tissue identified as a specific accumulator of this radionuclide [22].

Cobalt (⁶⁰Co): Pre-accident ⁶⁰Co levels in fish were generally low, peaking at 22.2 Bq/kg in the second half of 1981, with a minimum specific activity of 0.49 Bq/kg in fish tissue. By 1985, ⁶⁰Co levels had decreased several times, not exceeding 4.6 Bq/kg, with an average of 1.5 Bq/kg. After the accident, ⁶⁰Co levels in the biota of the cooling pond increased significantly. ⁶⁰Co was widely detected in high concentrations in filamentous algae (Cladophora spp.) and water plants (Potamogeton spp.) with specific activities of 2300 Bq/kg and 3400 Bq/kg dry weight, respectively. Different fish species showed varied ⁶⁰Co levels, with the highest found in planktophages H. molitrix (Table 1) and A. nobilis. Benthophages such as C. carpio (Table 2), Rutilus rutilus (Linnaeus, 1758), and Abramis brama (Linnaeus, 1758) also had significant levels of ⁶⁰Co. In fish with a mixed type of nutrition (Silurus glanis (Linnaeus, 1758), I. punctatus, and P. fluviatilis), the ⁶⁰Co content is similar in value to the benthophages—R. rutilus and A. brama. The lowest concentrations were found in ichthyophages Sander lucioperca (Linnaeus, 1758) (Table 4) and Aspius aspius (Linnaeus, 1758). Ingestion is proposed as the primary pathway for cobalt uptake in fish. The contribution of the nutrition pathway to the accumulation of ⁶⁰Co by fish of low trophic levels is probably more significant than the accumulation of this radionuclide by ichthyophages. However, studies have suggested that ⁶⁰Co can enter the organisms of the studied fish species both through the trophic chain and directly from the water. ⁶⁰Co distribution within fish bodies was uneven, with the highest levels found in the kidneys, followed by the liver, swim bladder, eggs, spine, fat, and red muscles. Scales and heads in direct contact with water also frequently showed high cobalt levels, while the lowest concentrations were detected in the heart, stomach, ribs, and fat [23].

Zinc (⁶⁵Zn): Unlike manganese and cobalt, zinc was more frequently detected in fish samples before the accident. The range of ⁶⁵Zn concentrations across different organs and tissues varied by more than tenfold, with the lowest levels found in scales, internal organs, and muscles, and the highest (up to 500.8 Bq/kg fresh weight) in the spine and head. ⁶⁵Zn was detected in fish of all studied ecological groups, including obligate phytophages (C. idella), benthophages (Blicca bjoerkna (Linnaeus, 1758), A. brama, R. rutilus, Carassius carassius (Linnaeus, 1758), and C. carpio), planktophages (A. nobilis and H. molitrix), facultative planktophages (Abramis ballerus (Linnaeus, 1758)), and obligate ichthyophages (S. lucioperca and Esox lucius (Linnaeus, 1758)). Post-accident, ⁶⁵Zn was predominantly found in fish, with specific activities reaching 6000 Bq/kg fresh weight. It was detected in only one water sample and one sample of periphyton, represented by filamentous algae (Cladophora spp.). Unlike this radionuclide’s relatively uniform pre-accident distribution among ecological fish groups, it was more frequently detected in peaceful species post-accident. Approximately 85% of fish samples detected ⁶⁵Zn were benthophages (B. bjoerkna (Table 3), A. brama, C. carpio, and R. rutilus) and planktophages (H. molitrix and A. nobilis). Around 15% of all samples that had ⁶⁵Zn were from fish with mixed types of nutrition (S. glanis, I. punctatus, and P. fluviatilis), with only about 8% of all samples in obligate ichthyophages (L. lucioperca and A. aspius). Post-accident, the distribution of ⁶⁵Zn in fish tissues differed significantly from pre-accident patterns, with its presence in muscles and bones becoming rare and in lower concentrations than in other organs and tissues. The highest frequency of ⁶⁵Zn detection occurred in organs and tissues directly exposed to water, such as fins, scales, gills, skin, and head, indicating that these tissues are reliable indicators of ⁶⁵Zn presence in the water [24]. Table 1, Table 2, Table 3 and Table 4 summarize the organ-specific content of the discussed short-lived radionuclides in four selected fish species, providing illustrative examples of their distribution and accumulation patterns.

Table 1. Content of radionuclides (⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn) in H. molitrix (Bq/kg fresh weight) with years before the Chornobyl accident labelled with an asterisk (*).

Organ	Year	54Mn	60Co	65Zn
Head	1981 *	25.3 ± 10.1	51.5 ± 15.7	500.8 ± 101.4
	1985 *	-	1.23 ± 0.26	-
	1987	-	89.6 ± 10.1	204.2 ± 62.2
	1988	-	121.5 ± 10.6	110.9 ± 13.4
	1990	-	18.4 ± 3.4	-
Internal Organs	1985 *	0.8 ± 0.2	2.7 ± 0.4
	1987		568.0 ± 54.9	519.2 ± 80.6
	1988	98.0 ± 17.2	977.2 ± 72.3	94.8 ± 31.2
Caviar	1985 *		1.67 ± 0.4
	1987		167.3 ± 23.6
	1988		152.9 ± 16.6	513.4 ± 74.1
	1990		87.8 ± 13.4
Muscles	1985 *	-	0.93 ± 0.26
	1987		60.2 ± 16.1
	1988	49.1 ± 10.7	54.1 ± 11.7
	1989		42.9 ± 6.4
	1990		15.9 ± 4.1

Table 1. Content of radionuclides (⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn) in H. molitrix (Bq/kg fresh weight) with years before the Chornobyl accident labelled with an asterisk (*).

Organ	Year	54Mn	60Co	65Zn
Head	1981 *	25.3 ± 10.1	51.5 ± 15.7	500.8 ± 101.4
	1985 *	-	1.23 ± 0.26	-
	1987	-	89.6 ± 10.1	204.2 ± 62.2
	1988	-	121.5 ± 10.6	110.9 ± 13.4
	1990	-	18.4 ± 3.4	-
Internal Organs	1985 *	0.8 ± 0.2	2.7 ± 0.4
	1987		568.0 ± 54.9	519.2 ± 80.6
	1988	98.0 ± 17.2	977.2 ± 72.3	94.8 ± 31.2
Caviar	1985 *		1.67 ± 0.4
	1987		167.3 ± 23.6
	1988		152.9 ± 16.6	513.4 ± 74.1
	1990		87.8 ± 13.4
Muscles	1985 *	-	0.93 ± 0.26
	1987		60.2 ± 16.1
	1988	49.1 ± 10.7	54.1 ± 11.7
	1989		42.9 ± 6.4
	1990		15.9 ± 4.1

Table 2. Content of radionuclides (⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn) in C. carpio (Bq/kg fresh weight) after the Chornobyl accident.

Organ	Year	54Mn	60Co	65Zn
Head	1986	-	140.3 ± 30.3	867.8 ± 100.8
	1987	-	44.6 ± 8.9	279.4 ± 38.2
	1988	-	14.9 ± 3.2	270.5 ± 29.7
	1989	-	74.2 ± 10.1	82.8 ± 23.3
	1990	-	10.7 ± 2.8	33.9 ± 5.8
Fins	1986	-	-	754.0 ± 74.8
	1987	-	-	1339.1 ± 124.5
	1988	-	-	259.9 ± 28.1
Scales	1986	-	61.6 ± 28.6	751.44 ± 122.6
	1987	-	191.3 ± 24.7	775.2 ± 78.4
	1988	-	26.2 ± 5.6	70.4 ± 27.7
	1989	-	44.1 ± 9.7	-
	1990	-	79.7 ± 13.3	-
Internal Organs	1986	-	87.1 ± 20.0	626.3 ± 87.2
	1987	-	173.4 ± 20.4	1385.1 ± 114.0
	1989	-	74.2 ± 10.1	82.8 ± 23.3
	1990	-	12.2 ± 3.6	-
Muscles	1986	168.9 ± 55.3	52.2 ± 15.3	283.6 ± 96.0
	1987	-	415.3 ± 46.3	754.2 ± 110.1
	1988	-	17.6 ± 3.5	63.3 ± 14.7
	1989	-	15.8 ± 6.7	-
	1990	-	3.5 ± 1.3	-

Table 2. Content of radionuclides (⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn) in C. carpio (Bq/kg fresh weight) after the Chornobyl accident.

Organ	Year	54Mn	60Co	65Zn
Head	1986	-	140.3 ± 30.3	867.8 ± 100.8
	1987	-	44.6 ± 8.9	279.4 ± 38.2
	1988	-	14.9 ± 3.2	270.5 ± 29.7
	1989	-	74.2 ± 10.1	82.8 ± 23.3
	1990	-	10.7 ± 2.8	33.9 ± 5.8
Fins	1986	-	-	754.0 ± 74.8
	1987	-	-	1339.1 ± 124.5
	1988	-	-	259.9 ± 28.1
Scales	1986	-	61.6 ± 28.6	751.44 ± 122.6
	1987	-	191.3 ± 24.7	775.2 ± 78.4
	1988	-	26.2 ± 5.6	70.4 ± 27.7
	1989	-	44.1 ± 9.7	-
	1990	-	79.7 ± 13.3	-
Internal Organs	1986	-	87.1 ± 20.0	626.3 ± 87.2
	1987	-	173.4 ± 20.4	1385.1 ± 114.0
	1989	-	74.2 ± 10.1	82.8 ± 23.3
	1990	-	12.2 ± 3.6	-
Muscles	1986	168.9 ± 55.3	52.2 ± 15.3	283.6 ± 96.0
	1987	-	415.3 ± 46.3	754.2 ± 110.1
	1988	-	17.6 ± 3.5	63.3 ± 14.7
	1989	-	15.8 ± 6.7	-
	1990	-	3.5 ± 1.3	-

Table 3. Content of radionuclides (⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn) in B. bjoerkna (Bq/kg fresh weight) after the Chornobyl accident.

Organ	Year	54Mn	60Co	65Zn
Head	1987	-	171.9 ± 46.5	765.2 ± 135.5
	1988	-	36.7 ± 5.0	52.9 ± 11.4
	1989	-	14.9 ± 4.2	21.9 ± 10.2
	1990	-	9.8 ± 3.1	-
Fins	1987	-	286.6 ± 73.7	478.4 ± 157.9
	1988	-	47.6 ± 9.1	-
Internal Organs	1987	-	115.2 ± 30.0	-
	1988	-	84.9 ± 10.8	178.9 ± 25.7
	1989	-	66.3 ± 9.2	-
	1990	-	38.4 ± 8.3	-
Muscles	1987	-	64.7 ± 26.2	-
	1988	-	28.7 ± 8.44	-
	1989	-	12.9 ± 4.1	-
	1990	-	4.78 ± 1.2	-

Table 3. Content of radionuclides (⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn) in B. bjoerkna (Bq/kg fresh weight) after the Chornobyl accident.

Organ	Year	54Mn	60Co	65Zn
Head	1987	-	171.9 ± 46.5	765.2 ± 135.5
	1988	-	36.7 ± 5.0	52.9 ± 11.4
	1989	-	14.9 ± 4.2	21.9 ± 10.2
	1990	-	9.8 ± 3.1	-
Fins	1987	-	286.6 ± 73.7	478.4 ± 157.9
	1988	-	47.6 ± 9.1	-
Internal Organs	1987	-	115.2 ± 30.0	-
	1988	-	84.9 ± 10.8	178.9 ± 25.7
	1989	-	66.3 ± 9.2	-
	1990	-	38.4 ± 8.3	-
Muscles	1987	-	64.7 ± 26.2	-
	1988	-	28.7 ± 8.44	-
	1989	-	12.9 ± 4.1	-
	1990	-	4.78 ± 1.2	-

Table 4. Content of radionuclides (⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn) in S. lucioperca (Bq/kg fresh weight) after the Chornobyl accident.

Organ	Year	54Mn	60Co	65Zn
Fins	1987	-	12.9 ± 5.3	73.9 ± 25.2
	1988	-	195.2 ± 22.7	128.5 ± 22.5
	1989	-	17.9 ± 5.4	-
	1990	-	-	26.8 ± 15.3
Scales	1987	-	-	529.6 ± 147.7
	1988	-	-	304.1 ± 65.8
	1990	-	46.3 ± 15.2	-
Internal Organs	1987	-	82.1 ± 2.1	378.8 ± 75.9
	1988	-	48.2 ± 10.8	-
	1989	-	67.2 ± 18.4	-
	1990	-	20.4 ± 4.7	-
Muscles	1987	58.2 ± 19.8	-	390.6 ± 82.9
	1989	-	17.5 ± 8.9	-
	1994	-	15.8 ± 4.5	-

Table 4. Content of radionuclides (⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn) in S. lucioperca (Bq/kg fresh weight) after the Chornobyl accident.

Organ	Year	54Mn	60Co	65Zn
Fins	1987	-	12.9 ± 5.3	73.9 ± 25.2
	1988	-	195.2 ± 22.7	128.5 ± 22.5
	1989	-	17.9 ± 5.4	-
	1990	-	-	26.8 ± 15.3
Scales	1987	-	-	529.6 ± 147.7
	1988	-	-	304.1 ± 65.8
	1990	-	46.3 ± 15.2	-
Internal Organs	1987	-	82.1 ± 2.1	378.8 ± 75.9
	1988	-	48.2 ± 10.8	-
	1989	-	67.2 ± 18.4	-
	1990	-	20.4 ± 4.7	-
Muscles	1987	58.2 ± 19.8	-	390.6 ± 82.9
	1989	-	17.5 ± 8.9	-
	1994	-	15.8 ± 4.5	-

5. Accumulation of ⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn in Fish After the Chornobyl Accident

Investigating the accumulation and redistribution of radioactive isotopes such as manganese, cobalt, and zinc in fish persisted following the Chornobyl nuclear accident. The results of the studies [25,26] asserted that the belonging of fish to a certain trophic level significantly affects the concentration of isotopes ⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn in them. These findings are consistent with experimental results obtained in the Chornobyl exclusion zone (Table 1, Table 2, Table 3 and Table 4), which showed that concentrations of these radionuclides decrease with higher trophic levels (trophic transfer coefficients, TTF < 1). The scheme of ⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn intake is shown in Figure 4.

Radionuclides enter fish organisms through two main pathways: direct uptake from water and indirect intake via food sources (plankton, benthos, plants, and other fish). The efficiency and dominance of these pathways vary depending on the trophic level of the fish.

Radionuclides dissolved in water can be absorbed through the gills, skin, and gastrointestinal tract of fish. This pathway is particularly significant for cobalt (⁶⁰Co), as direct absorption from water is a key source of its accumulation [11]. The gills, which have a large surface area and thin epithelial layers, serve as a primary site for the uptake of dissolved metals, including radionuclides.

Studies indicate that fish in contaminated waters exhibit high radioactivity levels in their gills and intestines, confirming the importance of waterborne radionuclide absorption [16]. However, the extent of waterborne uptake varies among species and environmental conditions.

Food intake is the predominant pathway for the accumulation of ⁵⁴Mn and ⁶⁵Zn, while ⁶⁰Co is absorbed both through food and directly from water [10]. Different fish species, depending on their trophic level, exhibit variations in the efficiency of assimilation and accumulation of these radionuclides.

Fish are classified into different trophic levels based on their diet, which influences the pathways and magnitude of radionuclide accumulation.

Phytophage fish primarily consume aquatic plants, which can accumulate radionuclides from water and sediments. ⁶⁵Zn tends to be more concentrated in plants compared to ⁵⁴Mn and ⁶⁰Co, making it the most prevalent radionuclide in this group [3]. These fish accumulate radionuclides mainly through digestion, with the highest levels found in digestive organs and liver.

Planktophage acquire radionuclides by consuming plankton, which rapidly absorb contaminants from water. ⁵⁴Mn and ⁶⁵Zn are more effectively transferred through this pathway due to their biological functions in metabolic processes [27]. These elements tend to accumulate in the gills and bones, whereas ⁶⁰Co is less prevalent in this group since it does not strongly bind to plankton.

Benthophage fish consume benthic organisms, such as detritus feeders, mollusks, and invertebrates that live in contaminated sediments. This feeding behavior makes them particularly susceptible to ⁶⁰Co and ⁶⁵Zn accumulation, as these radionuclides bind strongly to sediment particles [27]. They accumulate mainly in the liver, kidneys, and bones. ⁵⁴Mn concentrations tend to be lower in benthophages compared to planktophages due to its preferential uptake by plankton [11].

Fish with mixed feeding consume different types of animal food (benthic organisms and fish), allowing them to accumulate radionuclides from multiple sources. The relative levels of ⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn in these fish depend on their predominant food source. Those with a higher intake of benthic organisms show increased ⁶⁰Co accumulation [27].

Ichthyophage fish, which feed on other fish, accumulate radionuclides primarily through trophic transfer. Unlike lower trophic levels, where direct waterborne uptake plays a larger role, predatory fish primarily accumulate ⁶⁰Co, ⁶⁵Zn, and ⁵⁴Mn via their diet. However, trophic transfer coefficients (TTF) for these radionuclides are often <1, meaning that concentrations decrease as they move up the food chain [3]. Consequently, predatory fish exhibit lower overall radionuclide levels than their prey, particularly for ⁵⁴Mn, which is not efficiently biomagnified.

Because ⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn have nearly disappeared from the environment due to their relatively short half-lives, many studies on these radionuclides have been conducted in laboratory settings since 1986. It should be noted that the Fukushima Dai-ichi nuclear accident in Japan in 2011 did not result in the release of these isotopes into the environment. Therefore, studies of the accumulation of radioactive isotopes of manganese, cobalt, and zinc by fish in natural conditions were not possible after this accident.

Recent decades of research largely confirm previously obtained data. Laboratory experiments with Oncorhynchus mykiss (Walbaum, 1792) have demonstrated that different organs accumulate the radionuclide ⁵⁴Mn at varying levels. The skin, gills, kidneys, liver, and intestines are the primary entry sites, while bones, the head, brain, and fins are receptor and storage sites. However, unlike the findings from other studies, this research identifies muscles as a significant tissue for storing radioactive manganese [28].

Other studies have also suggested that muscles are a storage site for ⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn in fish [29]. Experiments on the distribution of these radionuclides, accumulated from seawater by S. canicula, Raja undulata (Lacepède, 1802), Torpedo marmorata (Risso, 1810), Scophthalmus maximus (Linnaeus, 1758), Sparus aurata (Linnaeus, 1758), and Dicentrarchus labrax (Linnaeus, 1758), revealed their heterogeneous distribution within the fish body. The kidneys were a secondary storage site for radionuclides for all these species, while the head, muscles, and skin were identified as the main sites of accumulation.

The accumulation of ⁶⁰Co in different organs of O. mykiss under laboratory conditions was also found to be uneven. The highest concentrations of this radionuclide were found in the gills, internal organs (swim bladder, heart, and spleen), and kidneys. By the end of the experiment, the kidneys had the highest concentrations of radio cobalt, followed by internal organs, the head, gills, and liver. The lowest concentration of ⁶⁰Co was found in the muscles [30], contrasting with previous findings.

Researchers have no consensus regarding the primary organ that stores ⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn in fish. For example, Jeffree R.A. and co-workers [31] suggest that the skin is the main reservoir for these radionuclides based on laboratory studies with Scyliorhinus canicula (Linnaeus, 1758). In a laboratory study on C. carpio, the highest concentrations of ⁶⁵Zn were found in the gills, kidneys, internal organs, and eyes, as noted in [32].

However, Jeng S.-S. and Lian J.-L. [33] report that in laboratory studies on four fish species, neither the kidneys nor gills had as high specific radioactivity for ⁶⁵Zn as the digestive tract, regardless of whether the zinc was ingested through food or water. Different fish species absorbed varying amounts of zinc from their diet, with the order of absorption being C. carpio > Oreochromis niloticus x O. aureus > Ctenopharyngodon idellus (Valenciennes, 1844) > H. molitrix when adequate zinc concentrations were present in the diet and the water was uncontaminated.

The findings in [34] confirm the results obtained in earlier studies of ⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn accumulation by fish. Under laboratory conditions, the primary route of intake of these radionuclides into Psetta maxima (Linnaeus, 1758) and Scyliorhinus canicula (Linnaeus, 1758) was through food. Species differences were observed, particularly in the uptake of Co, which the authors attribute to differences in diet and physiological and ecological conditions.

Previously noted differences in the accumulation of manganese, cobalt, and zinc radioisotopes by different fish species are discussed in [35]. As in the previous research, the studies were conducted with P. maxima and S. canicula. Radionuclides accumulated faster in S. canicula than in P. maxima. In S. canicula, the highest levels of ⁵⁴Mn were found in the kidneys, while the highest levels of ⁶⁵Zn were in the digestive tract, although they also remained high in other organs and tissues. In P. maxima, the highest concentrations of ⁶⁵Zn and the second-highest concentrations of ⁵⁴Mn and ⁵⁷Co were found in the kidneys.

The absorption efficiency in juvenile Menidia menidia (Linnaeus, 1758) fed copepods (Acartia spp.) contaminated with radioactive cobalt and zinc isotopes under laboratory conditions was low, with ⁵⁷Co at just 2% and ⁶⁵Zn slightly higher at 6% [36]. The authors suggest that the behavior of radiopharmaceuticals in fish fed artificial diets may not reflect their behavior in natural systems.

A significant result of studies on manganese, cobalt, and zinc accumulation in fish is that the concentrations of stable and radioactive elements differ within the fish. For example, the study described in [6] indicates that ⁵⁴Mn accumulates selectively compared to stable Mn. Mollusks of the Pectinidae spp. also selectively accumulate ⁵⁴Mn. Laboratory studies confirm field data on the differences in the accumulation of stable and radioactive isotopes of Zn and Mn by fish [11].

Despite the significant differences in the concentrations of stable and radioactive isotopes of the same element in fish, as reported in various studies, the authors decided to present findings on the accumulation of stable manganese, cobalt, and zinc in fish.

Similar to the accumulation of radioactive isotopes of manganese, cobalt, and zinc, variations in the accumulation of their stable isotopes (Mn, Co, and Zn) are often associated with the trophic levels of aquatic organisms [37]. Research presented in [38] discusses the impact of the trophic level of marine animals on the accumulation of various elements. Studies conducted in Baffin Bay (Canada) revealed that Co and Mn do not exhibit biomagnification at each level of the ecological pyramid within the food chain of this ecosystem. However, stable Zn was found to biomagnify, increasing concentration with higher trophic levels.

Investigations carried out in the Olifants River, Mpumalanga (South Africa) with fish species Oreochromis mossambicus (Peters, 1852) and Clarias gariepinus (Burchell, 1822) demonstrated that muscle tissue consistently contained significantly lower levels of stable Zn than other tissues and organs, corroborating findings from studies on the accumulation of radioactive metal isotopes in fish. Gills and liver exhibited relatively high concentrations of Zn, with somewhat lower levels in the skin. The primary reason for species-specific differences in Zn bioaccumulation was attributed to variations in the dietary habits and behavior of the studied fish species [4].

Canli M. and Atli G. [39] reported that the average concentration of stable Zn in the muscles, gills, and liver of six fish species (Sparus auratus (Linnaeus, 1758), Atherina hepsetus (Linnaeus, 1758), Mugil cephalus (Linnaeus, 1758), Trigla cuculus (Linnaeus, 1758), Sardina pilchardus (Walbaum, 1792), and Scomberesox saurus (Walbaum, 1792)) from the northeast Mediterranean Sea, Karatas (Turkey), varied significantly. The authors suggested that these differences are due to ecological needs, swimming behavior, and metabolic activity among the different species. Zinc concentrations were highest in the liver and gills and lowest in the muscles of all studied fish species.

The relationship between the content of stable Zn and Mn isotopes in fish of different species and their diet was investigated by Malik and Maurya [40]. Benthic fish (Heteropneustes fossilis (Bloch, 1794)) in the Kali River (India) exhibited higher levels of concentration of zinc and manganese compared to surface-feeding fish (Pethia ticto (Hamilton, 1822)). Seasonal variations in the accumulation of these metals were also observed, with minimal zinc and manganese accumulation during the rainy season and maximum levels in the summer.

The influence of species, sampling location, and season on the concentration of stable zinc in seven sampling stations distributed along the Ria de Aveiro (Portugal) in fish muscles is highlighted in [41]. However, contrasting results were presented in [42], where zinc levels in the muscles of two catfish species (Channa punctata (Bloch, 1793) and Aorichthys aor (Hamilton, 1822)) from the Ganges River at Allahabad (India) were found to be independent of the season. That study also noted that zinc concentrations in fish muscles were higher than the content of other heavy metals.

In Pterois spp. fish caught in the Atlantic Ocean near the island of Cuba, the highest concentrations of stable Mn and Zn were found in the liver, compared to their levels in the kidneys and muscles. The highest levels of stable Co were measured in the kidneys, which the authors attributed to this organ’s excretory function. Although the level of Co in the kidneys was low, it was an order of magnitude higher than in the liver and muscles [43].

In three fish species (Solea vulgaris (Linnaeus, 1758), Anguilla anguilla (Linnaeus, 1758), and Liza aurata (Risso, 1810)) from water bodies in the Odiel estuary and two in the Bay of Cádiz on the southwestern Atlantic coast of Spain, significant levels of stable zinc were found in the liver. At the same time, manganese concentrations were minimal [44]. The authors noted that Mn concentrations were higher in muscles than in the liver; however, this ratio varied among different fish species. This finding of higher manganese content in fish muscles contradicts numerous reports that this chemical element is minimally present in muscles.

Stable isotopes of Mn and Zn were measured in the fish Dicentrarchus labrax (Linnaeus, 1758), Liza ramada (Risso, 1827), and A. anguilla from Lake Bafa (Turkey). The concentrations of these elements did not exceed 50 mg/kg for zinc [45].

In laboratory studies of Morone saxatilis (Walbaum, 1792), it was found that Zn distribution varied significantly within different organs of the fish. The element was primarily associated with the head (55–63%), with only 4% of Zn detected in the intestines [46].

The ability of fish to regulate the levels of certain essential elements within their organisms is discussed in [47]. Reinfelder et al. suggest that the concentrations of most trace elements in fish tissues are regulated through a feedback mechanism. According to the authors, the mechanism by which fish regulate the accumulation of trace elements likely involves concentration-dependent changes in intestinal absorption or adaptive modifications in excretory pathways. The degree of regulation may also vary across different tissues. This implies that the increase in element content within tissues is not necessarily proportional to its concentration in the diet. Observations on the accumulation of stable zinc in O. mykiss during laboratory studies revealed that Zn levels in the blood plasma of this species were regulated within a narrow range. It was also found that Zn concentrations in muscle tissue remained relatively constant, regardless of its concentration in food and water.

Research on the accumulation of stable zinc in Lutjanus argentimaculatus (Forsskål, 1775) under laboratory conditions indicates the existence of regulation mechanisms for Zn levels within fish [48]. Dietary intake is crucial for maintaining metal levels in various fish tissues, though the authors stress that the absorption of metals from water cannot be ignored.

Experiments on the accumulation of stable zinc in two different fish species (Colossoma macropomum (Cuvier, 1818) and Trichogaster trichopterus var. Marble (Pallas, 1770)) revealed that Zn concentrations in the fish were higher than in the water [49]. This study also emphasized that different marine biota species have varying capacities for Zn accumulation.

6. Summary

The bioaccumulation of manganese (⁵⁴Mn), cobalt (⁶⁰Co), and zinc (⁶⁵Zn) in different fish species and their redistribution within the food chain may contribute to long-term ecological disruptions. Changes in fish physiology, reproductive system, and survival rates could alter population dynamics, potentially affecting entire aquatic ecosystems. Understanding the accumulation of these radionuclides in fish is crucial for assessing their potential risks to aquatic organisms and human consumers.

6.1. Key Findings and Their Implications

Variability in Accumulation Across Organs and Tissues: The accumulation of ⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn varies significantly among different fish organs and tissues. External organs such as gills and skin serve as primary entry points, while internal organs, particularly the kidneys and liver, often exhibit the highest concentrations of radionuclides. These differences are influenced by species-specific physiological and ecological factors.

Pathways of ⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn Entry: Food intake is the primary pathway for radionuclide accumulation in fish, although direct absorption from water is also a contributing factor. This finding underscores the importance of studying trophic transfer processes and biomagnification potential within aquatic food chain.

Influence of Trophic Levels: The concentration of radionuclides generally decreases with increasing trophic levels, suggesting a dilution effect in the food chain. While higher trophic-level fish exhibit lower concentrations, potential risks to human consumers remain, particularly from species that show high bioaccumulation tendencies.

Radionuclide Concentrations in Muscle Tissue: Muscle tissue, the primary component consumed by humans, consistently exhibits the lowest radionuclide concentrations. Nevertheless, continued monitoring is essential to evaluate the long-term health risks associated with consuming fish from contaminated environments.

Potential for Physiological Regulation: Some studies indicate that fish have regulatory mechanisms to control concentrations of essential elements, including both stable and radioactive isotopes of manganese, cobalt, and zinc. Understanding these mechanisms could enhance predictive models for radionuclide distribution in aquatic organisms.

6.2. Limitations and Challenges

While significant progress has been made in understanding radionuclide accumulation in fish, several challenges complicate data interpretation and comparison:

Variability in Experimental Conditions: Differences in water chemistry, temperature, sediment composition, and ecological interactions across studies make direct comparisons challenging. Variations in experimental setups, such as exposure durations, radionuclide concentrations, and species selection, further contribute to inconsistencies in findings.

Challenges in Comparing Historical and Recent Data: Older studies often relied on different detection methods, making it difficult to directly compare historical and contemporary radionuclide concentrations. Advances in analytical techniques have improved sensitivity and accuracy, but discrepancies between past and present data persist.

Potential Biases in Literature: The reviewed studies exhibit variations in sample sizes, species selection, and data reporting methodologies. Additionally, studies where these radionuclides were not detected or detected at low concentrations, especially before the Chornobyl accident, were likely conducted during radioecological monitoring but never publicly reported. This could influence the perceived magnitude of radionuclide accumulation trends.

Knowledge Gaps in Long-Term Ecological Effects: Despite extensive research, the long-term ecological effects of short-lived radionuclides on fish health, reproductive system, and population dynamics remain poorly understood. Further investigation is needed to determine the potential chronic impacts of radionuclide exposure on aquatic ecosystems.

6.3. Future Research Directions

Given the remaining knowledge gaps, future research should focus on:

Trophic Transfer and Biomagnification Studies: Investigating how ⁵⁴Mn, ⁶⁰Co, and ⁶⁵Zn transfer through aquatic food chain and assessing their biomagnification potential.

Long-Term Monitoring Programs: Establishing comprehensive, standardized monitoring programs to track changes in radionuclide concentrations over time and across different environmental conditions. Longitudinal studies assessing radionuclide concentrations in fish tissues and sediments can help determine trends and predict potential long-term consequences. Advanced bioindicators, such as species with higher accumulation tendencies, could be utilized for early detection of contamination events. Additionally, implementing standardized methodologies for sampling and analysis will improve data comparability across different regions and timeframes.

Multi-Stressor Assessments: Evaluating the combined effects of radionuclide exposure alongside other environmental stressors, such as pollution, climate change, and habitat degradation.

Improved Policy and Management Strategies: Strengthening regulations on radioactive discharge into aquatic environments and fostering collaboration between environmental scientists, policymakers, and fishery managers to mitigate contamination risks. The insights gained from this study could inform regulatory policies for environmental and public health protection. Authorities should establish permissible levels of these radionuclides in commercially available fish to mitigate human exposure risks. Strengthening regulations regarding radioactive waste disposal and nuclear facility management is crucial for preventing further contamination. Education and public awareness campaigns can also help communities make informed decisions regarding fish consumption in affected areas.

By expanding discussions on ecological consequences, health risks, and policy interventions, this research can significantly enhance its impact, contributing to more effective environmental protection and public safety measures.

7. Conclusions

The study of manganese (⁵⁴Mn), cobalt (⁶⁰Co), and zinc (⁶⁵Zn) radionuclide accumulation in fish highlights key environmental and public health concerns. Accumulation patterns vary across organs, with external tissues facilitating initial exposure and internal organs exhibiting the highest concentrations, particularly the liver and kidneys. Food intake remains the dominant pathway for radionuclide entry, though waterborne absorption also plays a role.

Radionuclide concentrations tend to decrease at higher trophic levels, suggesting a dilution effect in the food web. However, species prone to bioaccumulation may still pose risks to human consumers. Muscle tissue, the main part consumed by humans, generally contains the lowest concentrations, yet ongoing monitoring is necessary to assess long-term exposure effects.

Some fish species exhibit regulatory mechanisms influencing radionuclide retention, providing insight into species-specific contamination responses.

Future research should prioritize the study of trophic transfer, biomagnification, and the interplay of radionuclides with other environmental stressors. Enhanced regulatory measures and interdisciplinary collaboration among scientists, policymakers, and fishery managers are essential for mitigating contamination risks and ensuring the safety of aquatic ecosystems and food resources.