Gill epithelial responses of Cyprinus carpio Linnaeus, 1758 as sensitive histological biomarkers of sublethal anthropogenic stress in the Ile River (Kazakhstan)Abstract
The gills of teleost fish are multifunctional organs involved in respiration, osmoregulation, and immune defense, and are highly sensitive to environmental stressors. This study evaluated the histological and ultrastructural condition of the gill epithelium of common carp (Cyprinus carpio Linnaeus, 1758) inhabiting the middle reaches of the Ile River (Kazakhstan) under chronic anthropogenic pressure. Although hydrochemical parameters remained within permissible limits for fishery waters, all examined specimens (n = 10) exhibited pronounced structural alterations. Histological analysis revealed edema, epithelial hyperplasia, lamellar fusion, necrosis, and desquamation, indicating substantial impairment of gill integrity. Ultrastructural examination demonstrated advanced developmental stages of rodlet cells, mast cell degranulation, and increased activity of mucous and chloride cells, accompanied by mitochondrial alterations and autophagosome formation. Alongside destructive changes, moderate compensatory reactions were observed, reflecting tissue-level adaptation to prolonged environmental stress. These findings demonstrate that gill histopathology provides a sensitive tool for detecting sublethal effects of chronic anthropogenic impact, even when conventional hydrochemical indicators suggest acceptable water quality. The results support the use of cellular and tissue-level biomarkers in freshwater environmental monitoring programs.
Keywords:
Cyprinus carpio; gill histopathology; anthropogenic stress; biomarkers; Kazakhstan
Resumo
As brânquias de peixes teleósteos são órgãos multifuncionais envolvidos na respiração, na osmorregulação e na defesa imune, sendo altamente sensíveis a estressores ambientais. Este estudo avaliou a condição histológica e ultraestrutural do epitélio branquial da carpa comum (Cyprinus carpio Linnaeus, 1758) que habita o trecho médio do rio Ile (Cazaquistão), sob pressão antropogênica crônica. Embora os parâmetros hidroquímicos tenham permanecido dentro dos limites permitidos para águas destinadas à pesca, todos os espécimes examinados (n = 10) apresentaram alterações estruturais pronunciadas. A análise histológica revelou edema, hiperplasia epitelial, fusão lamelar, necrose e descamação, indicando comprometimento significativo da integridade branquial. A avaliação ultraestrutural demonstrou estágios avançados de desenvolvimento de células rodlet, desgranulação de mastócitos e aumento da atividade de células mucosas e de cloreto, acompanhados por alterações mitocondriais e formação de autofagossomos. Além dos processos destrutivos, foram observadas reações compensatórias moderadas, refletindo adaptação tecidual ao estresse ambiental prolongado. Os resultados demonstram que a histopatologia branquial constitui uma ferramenta sensível para detectar efeitos subletais do impacto antropogênico crônico, mesmo quando indicadores hidroquímicos convencionais indicam qualidade aceitável da água. Esses achados reforçam a importância do uso de biomarcadores celulares e teciduais em programas de monitoramento ambiental de ecossistemas de água doce.
Palavras-chave:
Cyprinus carpio; histopatologia branquial; estresse antropogênico; biomarcadores; Cazaquistão
1. Introduction
The transboundary Ile River, located in the southeastern part of Kazakhstan and originating in the Tien Shan Mountains (China), is one of the major waterways of Central Asia, supplying up to 80% of the water flow into Lake Balkhash (de Boer et al., 2021). Since the 1970s, following the construction of the Kapchagay Hydroelectric Power Station and increasing water withdrawal for irrigation in both Kazakhstan and China, the basin has experienced persistent alterations in its hydrological regime and progressive water quality degradation (Pueppke et al., 2018). Industrial and agricultural discharges containing heavy metals, pesticides, and other toxic substances are considered major sources of contamination (Sarkar et al., 2022), exerting substantial pressure on aquatic biota, particularly fish communities.
The ichthyofauna of the Ile River includes approximately 30 species (Talipova et al., 2021), among which the common carp (Cyprinus carpio) represents an ecologically and economically important species. Owing to its ecological plasticity, this species is frequently used as a bioindicator of freshwater ecosystem health. Chronic exposure to environmental pollutants may induce morphofunctional alterations in internal organs, especially in tissues directly interacting with the aquatic environment.
The gills are multifunctional organs involved in respiration, osmoregulation, excretion, and immune defense (Koppang et al., 2015; Alsafy et al., 2025). Due to their direct and continuous contact with water, they are among the primary targets of environmental stressors (Evans et al., 2005; Chen et al., 2023). Acting as a semipermeable barrier, the gill epithelium maintains ionic homeostasis and gas exchange while being continuously exposed to chemical pollutants, pathogens, and hydrochemical fluctuations.
In addition to their respiratory role, gills contribute significantly to innate immune responses. Key cellular components include mucous cells, chloride cells, rodlet cells, and mast cells, all of which participate in barrier protection and local immune regulation (Esteban, 2012; Sayyaf Dezfuli et al., 2022; Mokhtar et al., 2023). Structural and ultrastructural alterations in these cells may reflect both adaptive responses and pathological processes associated with chronic environmental stress.
Histopathological assessment of gill tissues is therefore considered a sensitive approach for detecting sublethal effects of anthropogenic impact and for evaluating ecosystem-level disturbances in freshwater systems (Evans and Nunez, 2015; Azadikhah et al., 2023).
The aim of this study was to assess the histological and ultrastructural condition of the gills of Cyprinus carpio inhabiting the middle reaches of the Ile River under chronic anthropogenic pressure and to evaluate their potential as tissue-level biomarkers of freshwater ecosystem health.
2. Materials and Methods
2.1. Field research
Fish and water sampling was conducted during a field expedition in the middle reaches of the Ile River (Southeast Kazakhstan, Zhetysu region, Panfilov district) from September 5 to 8, 2024 (Figure 1). The study area is characterized by ongoing anthropogenic pressure affecting aquatic ecosystems (Thevs et al., 2017).
Expedition route and sampling sites in the middle reaches of the Ile River near the mouth of the Usek River (South-East Kazakhstan).
2.2. Sampling and fish collection
Ten specimens of Cyprinus carpio were collected at the study site concurrently with water sampling. Fish were captured using standard ichthyological nets and transported to the laboratory in aerated containers.
Sampling and handling procedures were conducted in accordance with national regulatory standards (GOST 57133-2016) and were approved by the Local Ethics Committee of al-Farabi Kazakh National University (IRB00010790).
Given the limited sample size, the present study should be regarded as an exploratory assessment of histological, morphometric, and ultrastructural responses in wild Cyprinus carpio exposed to chronic anthropogenic pressure.
2.3. Water sampling
Water samples were collected simultaneously with fish sampling from the surface layer (0–0.5 m) into 1-L polyethylene bottles pre-rinsed with site water. Water temperature, pH, and dissolved oxygen were measured in situ using a portable multiparameter meter. Samples were transported at 4°C for laboratory analysis using standard methods (GOST 17.1.5.05–85; RD 52.24.643–2002; SanPiN 1.2.3685–21).
2.4. Biomorphological and histological processing of the material
Before slaughter and dissection of the fish, morphobiological parameters were measured (Table 1), including total and standard body length, body weight, condition factors (Fulton’s and Clark’s indexes). Mean values of all parameters were characterized by low to moderate biological variability (CV < 15%), indicating relative homogeneity of the sampled fish.
Morphobiological parameters of Cyprinus carpio collected from the middle reaches of the Ile River (n = 10).
Histological examination of the ichthyological material was carried out using standard methods. Organs were fixed in 10% neutral buffered formalin, and three slides per specimen were prepared in the Vertebrate Morphology Laboratory at Al-Farabi Kazakh National University. General staining was performed with Mayer's hematoxylin and alcoholic eosin (Prophet et al., 1992; Kaviani et al., 2013).
Microphotographs of histological and semithin gill sections were obtained using an iScope camera attachment at magnifications of ×100, ×200, ×400, and ×600 at the Vertebrate Morphology Laboratory, Al-Farabi Kazakh National University (Almaty, Kazakhstan).
2.5. Electron microscopy
For transmission electron microscopy, organs were fixed in 2.5% glutaraldehyde. Subsequent sample preparation followed standard protocols and was carried out at Nazarbayev University (Astana, Kazakhstan). Semi-thin sections were stained with methylene blue, Azure II, and basic fuchsin.
Electron micrographs were taken with a JEM 1400Plus transmission electron microscope at Nazarbayev University.
2.6. Morphometric and statistical analysis
Morphometric analysis was performed using ImageFocus Plus V2 software at ×100 magnification. Measurements included the thickness of the primary gill epithelium and the epithelial layer area. For morphometric comparison, the examined gill regions were conditionally subdivided into three areas based on the predominant morphological pattern and their relative representation in the gill epithelium: Area 1 – the most represented regions, showing necrosis and destruction of secondary lamellae; Area 2 – regions characterized mainly by epithelial hyperplasia and fusion of secondary lamellae; Area 3 – the least represented regions, showing moderate changes, including edema and proliferation of cells in the primary gill epithelium. For each specimen, measurements were obtained from seven visual fields.
The epithelial area was estimated using image-based morphometric measurements for comparative assessment of the selected epithelial regions. Differences between the analyzed epithelial areas were assessed using Student’s t-test (p ≤ 0.05). Data are presented as mean ± standard error (M ± m). Standard deviation (SD) and coefficient of variation (CV, %) were calculated to assess intragroup variability. Statistical analysis was performed using Microsoft Excel (Microsoft Corp., USA). Given the exploratory nature of the study, the statistical analysis was intended to identify major trends in morphometric variation among epithelial areas with different predominant histological patterns.
3. Results
3.1. Water analysis
Water analysis revealed a slightly alkaline pH (7.87). Total mineralization was 356 mg/L, dry residue 242 mg/L, and total hardness 4.2 mmol/L, including carbonate hardness of 2.9 mmol/L. Permanganate oxidizability was 0.96 mg O2/L, indicating low organic matter content.
Major cations were Ca2+ (58.1 mg/L) and Mg2+ (15.8 mg/L), while dominant anions included HCO3− (177 mg/L) and SO42− (61.3 mg/L). Concentrations of Na+ (19.5 mg/L), K+ (2.6 mg/L), Cl− (12.4 mg/L), NO3− (4.0 mg/L), and F− (0.8 mg/L) remained below permissible limits. NH4+, NO2−, and Fe3+ were below the detection threshold.
According to the Unified Water Quality Classification System (Republic of Kazakhstan, 2025), the water corresponded to classes I–II (clean to moderately clean), indicating a low level of anthropogenic load.
3.2. Histological analysis
Histological examination of gill tissues from all ten Cyprinus carpio specimens revealed pronounced structural alterations of varying severity.
3.2.1. Destructive alterations
Destructive and necrotic changes occupied approximately 45% of the total gill epithelium area (Table 2, Figures 2AC). Observed lesions included desquamation of respiratory cells, loss of intercellular contacts, detachment of primary and secondary epithelia, and focal epithelial necrosis. In some regions, partial necrosis of gill filaments and lysis of muscle fibers at the filament base were detected (Figure 2B). Complete loss of secondary lamellae due to atrophy and degeneration was also observed (Figure 2C).
Descriptive statistics of epithelial thickness (µm) in gill tissues of ten Cyprinus carpio specimens.
Histological alterations in the gill epithelium of Cyprinus carpio. (A) Detachment of the secondary epithelium due to edema (thin arrows), edema at the base of primary lamellae (thick arrows), destruction of secondary lamellae (arrowheads), and epithelial hyperplasia (asterisk). H&E, ×100, scale bar = 50 μm. (B) Focal necrosis of the gill epithelium (thin arrows) with lysis of muscle fibers (asterisk). H&E, ×600, scale bar = 20 μm. (C) Necrosis of epithelial cells (thin arrows), destruction of secondary lamellae (arrowhead), and blood stasis (thick arrow). H&E, ×100, scale bar = 50 μm. (D) Fusion (thick arrows) and destruction (arrowhead) of secondary lamellae with mast cell hyperplasia (thin arrows). H&E, ×200, scale bar = 50 μm. (E) Semithin section showing proliferation of rodlet cells (arrowheads), mucous cells (thick arrows), and mast cells (thin arrows). ×600, scale bar = 20 μm. (F) Edema of the primary epithelium (thin arrows) with mast cell proliferation (thick arrows). H&E, ×400, scale bar = 50 μm.
Edema of secondary lamellae resulted in separation of epithelial layers from underlying tissue and formation of lacunar spaces. Degeneration of respiratory cells was evident in affected regions.
3.2.2. Proliferative and adaptive responses
Approximately 30% of the gill surface was occupied by zones of epithelial hyperplasia, leading to partial or complete fusion of secondary lamellae (Figures 2D, F). In certain areas, hyperplasia extended through up to 75% of the epithelial thickness.
Moderate edema was also observed in the primary filament epithelium, with dilation of basal intercellular spaces while overall epithelial organization was preserved. Flattened respiratory cells with hyperchromatic nuclei predominated in these areas.
3.2.3. Immune-related cellular elements
Active proliferation of mast cells was observed within the epithelium and in perivascular regions. Some mast cells exhibited partial destruction and extracellular release of granules (Figures 2E, F). Proliferation of fibroblasts and undifferentiated cells forming connective tissue strands was also noted.
Mucous and rodlet cells were detected in both primary and secondary epithelia, with occasional clustering in the interlamellar regions.
3.3. Morphometric analysis
Morphometric evaluation confirmed heterogeneity in epithelial responses. Regions with destructive and necrotic alterations (Area 1) constituted the largest proportion of the respiratory epithelium, whereas regions with moderate changes, including edema and proliferation in the primary epithelium (Area 3), were less represented. Hyperplastic regions with fusion of secondary lamellae (Area 2) occupied an intermediate position. Differences in the average epithelial area among Areas 1–3 are shown in Figure 3 and reflect heterogeneity of morphofunctional responses in gill tissues.
Mean epithelial area in different gill regions (Area 1–Area 3) of Cyprinus carpio. Vertical bars represent standard deviation (SD). Differences were statistically significant at p ≤ 0.05.
A statistically significant 1.22-fold difference in primary epithelial thickness was observed between the most altered and least altered regions (p ≤ 0.05). The coefficient of variation exceeded 34%, indicating marked individual variability.
Extensive proliferative regions showed substantial variation in epithelial thickness (14–138.05 µm). Quantitative analysis demonstrated a statistically significant 1.63-fold reduction (p ≤ 0.05) in the area of normally organized epithelium compared with altered zones. The coefficient of variation ranged from 7.78% to 31.55%.
Differences in the average epithelial area among Areas 1–3 indicated spatial heterogeneity of morphofunctional responses.
3.4. Ultrastructural characteristics of gill immune cells
3.4.1. Mucous cells
Mucous cells were predominantly located in the superficial layers of the interlamellar epithelium. They exhibited basally positioned nuclei and cytoplasm filled with membrane-bound secretory granules of variable size and density. Moderately dilated cisternae of rough endoplasmic reticulum were observed adjacent to secretory granules, consistent with active synthetic processes (Figure 4A).
(A) Ultrastructure of light and dark chloride cells, a rodlet cell at the secretory stage, and a mucous cell with numerous secretory granules. Transmission electron microscopy (TEM; JEM-1400Plus, JEOL), scale bar = 5 μm. (B) Ultrastructure of chloride cells during degradation, showing loss of membrane integrity and partial cytoplasmic disruption. Transmission electron microscopy (TEM; JEM-1400Plus, JEOL), scale bar = 5 μm. (C) Ultrastructure of mast cells. Transmission electron microscopy (TEM; JEM-1400Plus, JEOL), scale bar = 2 μm. (D) Ultrastructure of rodlet cells at stages III and IV of development showing destruction and loss of cellular components. Transmission electron microscopy (TEM; JEM-1400Plus, JEOL), scale bar = 2 μm.
3.4.2. Chloride cells
Chloride cells were localized mainly in interlamellar regions and occurred as light and dark forms. Dark cells contained an electron-dense cytoplasm with numerous polymorphic mitochondria. Light cells were more abundant and exhibited an electron-lucent matrix. Both immature and mature forms were identified.
Mitochondrial swelling and dilation of the tubular reticulum were observed in several cells. Occasional autophagosomes were detected. In mature forms, apical membranes showed shallow invaginations and microvilli (Figures 4A, B).
3.4.3. Mast cells
Mast cells were detected in perivascular and epithelial regions. Ultrastructurally, their cytoplasm was densely filled with electron-dense and vacuolated granules, partially obscuring the nucleus. Only isolated mitochondria and elements of rough endoplasmic reticulum were present (Figure 4C).
3.4.4. Rodlet cells
Rodlet cells were predominantly observed at stages III and IV of development. Mature cells exhibited a characteristic trilaminar envelope and numerous electron-dense granules localized mainly in the apical cytoplasm.
At stage IV, granule extrusion into the extracellular space was evident, accompanied by partial membrane disruption and cytoplasmic depletion. Degenerative changes included thinning of the outer membrane, cytoplasmic disorganization, and loss of mitochondria and Golgi structures (Figures 4A, D).
4. Discussion
The hydrochemical characteristics of the Ile River during the sampling period were used as background parameters for interpreting histological changes in the gills of Cyprinus carpio as indicators of physiological reactivity under environmental stress. Although no toxicants exceeded permissible limits and water quality was classified as “clean” or “moderately clean” according to national standards (Republic of Kazakhstan, 2025), pronounced structural alterations were detected in the gill tissues of all examined specimens. This discrepancy suggests that histological and ultrastructural parameters may represent more sensitive indicators of environmental stress than hydrochemical measurements alone, particularly under chronic, low-intensity anthropogenic exposure. Such tissue-level alterations likely reflect cumulative and sublethal effects that remain undetected by routine chemical analyses.
The gill apparatus, due to its continuous contact with the aquatic environment, represents one of the primary target organs of environmental stressors (Laurent et al., 1995). The predominance of necrotic and destructive changes, including epithelial desquamation, lamellar atrophy, edema, and muscle fiber lysis, indicates marked structural impairment. Similar alterations have been described as responses to sublethal exposure to toxicants in freshwater fish (Alesci et al., 2022; Mendonça et al., 2005; Leino, 1974). The coexistence of compensatory processes, such as epithelial hyperplasia and increased mucous cell activity, alongside pathological alterations suggests a progressive pattern of tissue response to prolonged stress.
Morphometric analysis confirmed substantial heterogeneity in epithelial organization and thickness. High interindividual variability may reflect differences in adaptive capacity among wild fish exposed to fluctuating anthropogenic pressure. The significant reduction in normally organized epithelial areas indicates that the stress response affects the overall functional integrity of the gill apparatus rather than isolated regions.
Ultrastructural observations provided further insight into cellular mechanisms underlying these changes. Alterations in mucous, chloride, mast, and rodlet cells, including mitochondrial swelling, dilation of the tubular reticulum, autophagosome formation, and advanced stages of cellular degeneration, indicate sustained cellular stress. Reduced mitochondrial integrity in chloride cells suggests impaired metabolic activity, while structural modifications in mucous cells are consistent with enhanced barrier protection.
The pronounced presence of rodlet cells at advanced developmental stages (III–IV), particularly in areas adjacent to damaged epithelium, supports their involvement in innate immune responses under chronic stress conditions (Perry, 1997; Manera, 2024; Wendelaar Bonga et al., 1990; Genten et al., 2008; Mautalieva et al., 2023). Similarly, the distribution and ultrastructural characteristics of mast cells correspond to known inflammatory and protective responses in teleost tissues (Reite and Evensen, 2006; Sfacteria et al., 2015), although their precise functional role under sublethal anthropogenic exposure warrants further investigation.
Taken together, the integration of histological, morphometric, and ultrastructural findings indicates that the gill apparatus functions not only as a respiratory and osmoregulatory organ but also as a dynamic immune barrier capable of mounting coordinated tissue-level responses to chronic environmental stress. The presence of significant morphofunctional alterations despite acceptable hydrochemical parameters highlights the limitations of conventional chemical monitoring and supports the inclusion of biological and cellular biomarkers in freshwater ecosystem assessment, particularly in transboundary river systems subjected to diffuse anthropogenic pressures.
Several limitations should be acknowledged. The relatively small sample size and single-season sampling restrict assessment of temporal variability. In addition, the present study was not designed as a comparative analysis between impacted and reference sites. Instead, the interpretation was based on the spatial heterogeneity of histological alterations within the examined gill tissues and on comparison with generally accepted descriptions of normal gill morphology reported in the literature. Early developmental stages of rodlet cells were identified only by light microscopy, and the absence of immunohistochemical markers limited detailed characterization of inflammatory pathways. Future studies incorporating seasonal sampling, expanded datasets, reference sites, and molecular or immunohistochemical approaches would provide deeper insight into adaptive and pathological mechanisms in fish gills under chronic environmental stress.
5. Conclusions
The present study demonstrates that the gills of the common carp Cyprinus carpio are sensitive indicators of environmental conditions and can reflect sublethal anthropogenic stress even when hydrochemical parameters remain within regulatory standards. Pronounced histological and ultrastructural alterations in the gill epithelium, including destructive and necrotic changes, epithelial hyperplasia, edema, and activation of mucous, mast, chloride, and rodlet cells, indicate sustained tissue-level responses to chronic environmental exposure.
Overall, the findings support the use of histological and ultrastructural biomarkers in freshwater bioindication and ecological monitoring programs, particularly for river systems exposed to diffuse anthropogenic pressure.
Acknowledgements
We thank the U.M. Akhmedsafin Institute of Hydrogeology and Geoecology (Almaty, Kazakhstan) for assistance with water analyses and Nazarbayev University (Astana, Kazakhstan) for support in conducting transmission electron microscopy.
This work was supported by the Ministry of Education and Science of the Republic of Kazakhstan under Grant No. AP23486220 (2024–2026), titled “Study of the important organ systems reactivity in the main commercial fish species of the Ile-Balkhash basin under anthropogenic load”.
Data Availability Statement
All data generated or analyzed during this study are included in this published article. Additional data may be requested from the corresponding author.
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Ethics and consent
All procedures involving animals were approved by the Local Ethics Committee of Al-Farabi Kazakh National University (Protocol No. IRB00010790) and conducted in accordance with national and international guidelines for the use of animals in scientific research.
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Editor:
Takako Matsumura Tundisi
