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Fish Gill Structural Changes Induced by Toxicants and Other Irritants: A Statistical Review
Abstract
Here I quantitatively review the literature on how fish gill morphology is affected by chemical and physical irritants in the surrounding water (e.g. various toxicants, extremes of temperature or pH). I catalogued histopathological gill lesions that were reported, and used statistics to explore how such lesions relate to the irritant-exposure conditions under which they occurred (specifically, to dose and class of irritant, to temperature, and to salinity of the surrounding water). Frequently recorded histopathologic lesions include changes in gill epithelium (lifting, necrosis, hyperplasia, hypertrophy, rupture), bulbing or fusing of gill lamellae, hypersecretion and proliferation of mucocytes, and changes in chloride cells and gill vasculature. I conclude that these lesions are largely nonspecific in nature, as each was detected under many different exposure conditions. The lesions are not entirely independent of exposure conditions, however, as my statistical analysis discerns these trends: (1) Most gill lesion types have been reported more frequently after lethal than after sublethal exposure to irritants. (2) Some lesions were more frequently detected in studies employing heavy metals than in studies using organic toxicants or other irritants; such lesions include necrosis and hypertrophy of gill epithelial cells, plus mucous hypersecretion. (3) Lifting of the branchial epithelium, the most commonly reported lesion, was reported more often in freshwater than in marine fish, suggesting that osmolarity of the ambient water influences this lesion. Little relation was found between recorded lesion frequencies and temperature. Following my statistical analysis, the etiology of irritant-induced gill lesions is considered. The nonspecificity of branchial alterations suggests that they primarily represent stereotyped physiological reactions of gills to stress, and many of them are logically considered defense responses. Some branchial alterations have been considered inflammatory, but I conclude that the literature cannot support that hypothesis. Ultrastructural studies have detected irritant-induced disruptions of branchial epithelial cells, including cytoplasmic vacuolization, autophagosomes and inclusions, loss of microvilli, and abnormal mitochondria and nuclei.
... Generally, liver and gill histopathological changes are sensitive and responsive but not specific to pollutant exposure. The occurrence of similar lesion types under a wide range of stressors and contaminants (Mallatt 1985) and chemical interactions (e.g., synergism/ antagonism) precludes our ability to directly study the cause-effect relationship between specific pollutants and lesions (Au 2004). Because the liver is the primary location for metabolic and detoxification processes and the gills are one of the first exposure routes for waterborne contaminants, these are the primary tissues used for the assessment of morphological alterations. ...
The Delta Smelt is a largely zooplanktivorous, endangered fish endemic to the San Francisco Estuary (the estuary). High flows increase the availability of fresh and brackish water habitat for Delta Smelt, but also may mobilize contaminants, potentially increasing toxicological stress. Here, we examine the association between contaminants and Delta Smelt health across contrasting water year types and flow-related management actions. Our study spanned the fall season of three years: 1 dry year (2018) bracketed by 2 wet years (2017 and 2019) and coincided with several management actions meant to benefit Delta Smelt. We collected field water from six sites in the estuary that encompass the freshwater and low-salinity habitat of Delta Smelt and analyzed the water for contaminant concentrations. After a 96-hour exposure to the field water, we assessed cultured Delta Smelt survival and the histopathological condition of the gill and liver. Insecticides, particularly fipronil metabolites, were the most prevalent contaminants detected in 2017 and 2018, and a variety of contaminants associated with the rice harvest were detected in 2019. No acute toxicity was observed during any exposure, but we observed negative effects in the livers of Delta Smelt exposed to agricultural water from the Toe Drain and Cache Slough during a 2019 pulse flow action, which coincided with elevated detections and concentrations of organic pesticides. Other noteworthy sub-lethal effects, likely occurring in response to contaminant mixtures, included severe gill lesions in Delta Smelt exposed to Decker Island water in 2019. In the drier year of 2018, lesions were generally mild or absent. Thus, the trade-offs between increased habitat availability and contaminant loading may provide one explanation for why Delta Smelt abundance does not consistently respond positively to outflow.
... The dissected organs for histological microscopy analysis of C. gariepinus fingerlings revealed small alterations upon exposure to Zn-EDTA. Studies that examined the toxic effects of various concentrations of elemental Zn in different salts (ZnSO 4 or ZnCl 2 ) on O. mykiss, Tilapia sparmanii, or C. gariepinus revealed alterations in the epithelium (Lloyd, 1960;Skidmore, 1970;Hogstrand et al., 2002) and in the functionality of the gills (Burton et al., 1972;Mallatt, 1985;Van Rensbrug, 1989;Wood, 2017), as well as accumulations in different organs such as the gill, liver, muscle, and skin (Awoyemi et al., 2014;Duran et al., 2015). Later, using ICP-MS analysis, the combined effects and influence of Zn and Zn-EDTA (in concentrations from 4.0 to 8.0 mg/L) on C. carpio were investigated simultaneously by Karayakar et al. (2021) for more than 7 days of exposure. ...
As nutrient-rich water in aquaponic systems cannot supply growing plants with all the required trace elements, supplementation with specific fertilizers is performed to make up for this deficit. While chelated fertilizers such as ethylenediaminetetraacetic acid–zinc disodium complex (Zn-EDTA) are becoming more popular in this context for improving plant growth in aquaponic systems, little is known about their effects on fish. During two experiments, a total of 576 individuals of catfish fry (0.19 g) and fingerlings (220.01 g) of the African catfish ( Clarias gariepinus ; Burchell, 1822) were kept separately for 32 days under experimental aquarium conditions. The fry was exposed to 0.125 and 0.5 mg/L, while the fingerlings were exposed to 0.5 and 2.0 mg/L Zn-EDTA in a plantless aquaponic system. The third treatment group consisted of a control group without Zn-EDTA. The growth, mortality, and ethological indicators were assessed for all growth stages, while the leukocyte distribution and histopathological changes were additionally determined for the fingerlings. As the feed intake in the experiment was limited, the investigations were focused on the effects of Zn-EDTA and not on the growth process of a respective fish growth stage. While the growth, mortality, and behavior were not significantly different in both growing stages, the number of mature neutrophils changed significantly in all treatments in fingerlings. Zn was not detected in the histologically investigated organs at the tested concentrations using the staining method. However, morphological alterations of the gill epithelium were found on the secondary lamellae. Quantitative multiplex PCR was used to simultaneously evaluate the expression of 17 genes related to Zn metabolism and stress physiology in head kidney samples. The transcripts of several selected genes changed by up to 70-fold. Due to high individual variances, only the copy numbers of the KMT2A (lysine-specific methyltransferase 2a) gene were significantly different across treatment groups and sampling points. However, the present results indicate that the addition of Zn-EDTA at the tested concentrations can be considered relatively benign for the health and welfare of C. gariepinus , as no toxic effects of Zn-EDTA were observed in moderately hard to hard water.
... A variety of gill irritants including parasites, ammonia, metal contaminants, and suspended sediment are known to influence gill morphology and the capacity for structural remodelling, although the mechanism(s) are currently unknown. The many pathological effects of these irritants, while important, fall outside of our definition of gill remodelling and will not be discussed at length here (for reviews, see Mallatt 1985;Feist and Longshaw 2008;Rodger et al. 2011;Salamat and Zarie 2016). However, respiratory irritation can also influence "typical" aspects of gill remodelling. ...
The complex relationships between the structure and function of fish gills have been of interest to comparative physiologists for many years. Morphological plasticity of the gill provides a dynamic mechanism to reversibly alter its structure in response to changes in the conditions experienced by the fish. The best known example of gill remodelling is the growth or retraction of cell masses between the lamellae, a rapid process that alters the lamellar surface area that is exposed to the water (i.e. the functional lamellar surface area). Decreases in environmental O2 availability and/or increases in metabolic O2 demand stimulate uncovering of the lamellae, presumably to increase the capacity for O2 uptake. This review addresses four questions about gill remodelling: (1) what types of reversible morphological changes occur; (2) how do these changes affect physiological function from the gill to the whole animal; (3) what factors regulate reversible gill plasticity; and (4) is remodelling phylogenetically widespread among fishes? We address these questions by surveying the current state of knowledge of gill remodelling in fishes, with a focus on identifying gaps in our understanding that future research should consider.
... Data presented as mean ± standard error. Significant value was p < 0.05 it can impair the efficiency of gas exchange and ion transport (Mallat 1985;Winkaler et al. 2001). Different studies have shown the occurrence of these changes in the gills of fish when exposed to different pollutants and chemical agents (Handy and Penrice 1993;Mazon et al. 2002;Pacheco and Santos 2002;Thophon et al. 2003). ...
The aim of the present study was to evaluate propofol as an anesthetic and its effects on physiology and histology in Ictalurus punctatus. To determine the ideal concentration, juvenile of I. punctatus (96.60 ± 27.70 g) were used, submitted to different concentrations of the anesthetic: 1.5, 2.0, 2.5, 3.0, 4.0, 5.0, and 6.0 mg L⁻¹. The concentration evaluated as ideal was 2.5 mg L⁻¹. To evaluate the physiological and histological effects of propofol exposure, juvenile of I. punctatus (99.71 ± 26.38 g) were sampled immediately (T0) and 30 min after anesthesia (T30) with 2.5 mg L⁻¹, had blood, liver, and gill samples collected. The exposure of the animals to propofol in both treatments (T0 and T30) caused increases in plasma glucose and lactate levels (p < 0.05) but prevented an increase in cortisol (p > 0.05). The histological study showed mild to moderate changes in the gills (congestion in the lamellar vessels and central vein and epithelial elevation) and moderate and severe changes in the liver (congestion and degeneration). This study concludes that the concentration of 2.5 mg L⁻¹ of propofol provides safe anesthesia for I. punctatus and prevents increased plasma cortisol levels.
... Structural alterations in exposed tissues of animals are detected through histological examination (a simple and sensitive tool). In fish, gills are the first organ to which the pollutant primarily contacts and also functions as the site of respiration, osmoregulation and excretion (Mallatt, 1985). Thus, gills are often predisposed to damage. ...
Cosmetics are one of the major pollutants in the aquatic ecosystem due to the quantum of production to meet the astronomical demand of users that eventually becomes harmful to organisms. Changes in physic-chemical parameters such as potential of hydrogen (pH), Electrical conductivity (EC), Temperature (T oC) Dissolved oxygen (DO) were investigated at the beginning and after 96 hours of cosmetic exposure. This study also investigated the effects of four facial cosmetic products (Powder, foundation, concealer, and primer) histopathologically in fingerlings of Clarias gariepinus (gills) exposed to binary, trinary, and quaternary mixtures in o laboratory bioassays for 48 hours and 96 hours. The results of pH, T C, EC and DO ranged from 6.21 - 6.64, o 25.40 - 26.70 oC, 0.04 - 0.14 mS/cm, and 10.00 -12.00 mg/l respectively. The joint action toxicity evaluation of the binary, trinary, and quaternary mixtures of the cosmetics prepared based on an equitoxic ratio against the test organism was in concordance with the model of synergism. Results showed the prevalence of severe lamellar necrosis in the gills of C. gariepinus which was observed across all combinations except in the combinations of Powder + Primer as well as Powder + Foundation + Concealer + Primer. Moderate lamellar necrosis and hypertrophied epithelium were observed in fish exposed to a mixture of Powder + Foundation + Concealer. The results obtained in this study suggested that the presence of facial cosmetics in the aquatic ecosystem could be dangerous to fish and subsequently human health via biomagnification. Therefore, there is an urgent need for environmental regulators to enforce safety standards for the emission of these selected cosmetics wastes into the waterways to prevent damage to aquatic organisms and public health issues.
... The liver is also often chosen because of its role in antioxidant defense and generally strong metabolic index. On the other hand, gills are of interest as they represent a soft tissue which is in direct contact with water, and which has an increased sensitivity to the mixtures of xenobiotics in it due to its unique role in respiration (Mallatt 1985). ...
Lake Ludaš is a protected nature reserve in Serbia that has been the focus of scientific interest, due to perpetual water quality deterioration that has led to consistent cyanobacterial blooms for almost five decades. To describe the possible effects of cyanotoxins on fish (Carrasius gibelio) inhabiting Lake Ludaš, several examinations were performed in November of 2018, including: assessment of water quality (physical and chemical parameters, as well as water microbiology), and assessment of several tissues of C. gibelio (micronucleus test, comet assay, and histopathologi-cal analyses). The water quality of Lake Ludaš has been categorized as class III, indicating moderate pollution. Physical and chemical parameters from November of 2018 seemed to be within acceptable levels. Examined fish tissues showed signs of DNA damage (highest in the blood, followed by the liver and gills), and histological alterations (in the liver and gills). Although other xenobiotics can induce similar changes, cyanotoxins could be the most likely cause of the observed alterations in C. gibelio tissues. The present study demonstrates the need to monitor this important wetland of international significance, since the living organisms in Lake Ludaš are showing signs of environmental stress suggesting that the preservation and natural balance of this ecosystem could be in danger.
... The most common gill changes observed under increased turbidity (epithelial lifting, epithelial thickening, hyperplasia, and mucous production) typically increase lamellar width, increasing the oxygen diffusion distance, which is presumed to protect the gills from abrasion and irritants reaching the bloodstream (Mallatt, 1985). Eastern sand darter may not have been exposed to sufficiently high-turbidity levels at our study sites to have elicited significant changes in lamellar width, gill pathologies, or ionocytes. ...
Anthropogenic stressors such as agriculture and urbanization can increase river turbidity, which can negatively impact fish gill morphology and growth due to reduced oxygen in the benthic environment. We assessed the gill morphology, field metabolic rate (FMR), and two hypoxia tolerance metrics (oxygen partial pressure at loss of equilibrium, PO2 at LOE, and critical oxygen tension, Pcrit) of eastern sand darter (Ammocrypta pellucida), a small benthic fish listed as threatened under the Species at Risk Act in Canada, from rivers in southern Ontario. Field trials were conducted streamside in the Grand River (August 2019; mean NTU 8) and in the comparatively more turbid Thames River (August 2020; mean NTU 94) to test the effect of turbidity on each physiological endpoint. Gills were collected from incidental mortalities and museum specimens, and were assessed using hematoxylin and eosin and immunofluorescent staining. The between‐river comparison indicated that turbidity significantly increased interlamellar space and filament width but had no significant influence on other gill morphometrics or FMR. Turbidity significantly increased PO2 at LOE (i.e., fish had a lower hypoxia tolerance) but did not significantly impact Pcrit. Therefore, although turbidity influences hypoxia tolerance through LOE, turbidity levels were not sufficiently high in the study rivers to contribute to measurable changes in gill morphology or metabolism in the wild. Determining whether changes in gill morphology or metabolism occur under higherturbidity levels would help resolve the ecological importance of turbidity on species physiology in urban and agricultural ecosystems.
The current study investigated the toxicological effects of lead acetate trihydrate on bioaccumulation, hematology and histopathological changes in the gills and muscles of common carp (Cyprinus car-pio). The fishes were divided into seven groups and were treated with different concentrations of lead. Lead bioaccumulation was analyzed in gills and muscles with the help of atomic absorption. Gill tissue absorbed the maximum concentration of lead, followed by muscles. After 24 hours, decrease in the concentration of Hb (65.13±16.81) and RBCs (0.52±0.137) and a maximum increase in the concentration of lymphocytes (91±21.30) with a dose of 30mg /l lead was observed. Results showed that in every experiment, the amount of lead in the gills increased gradually with the increase of the doses, as 259.83±58.4 with a dose of 5mg/I, 276.9±71.1 using dose of 10mg/l, 284.3±70.1 treated with 15mg/l, 299.63± 76.80 deal with 20mg/l , 310.26± 79.61 by 25mg and 331.4± 85.42 with a dose of 30mg. A maximum decrease in the concentration of Hb (65.13±16.81) and RBCs (0.52±0.137) and increase in the concentration of lymphocytes (91±21.30) with a dose of 30mg /l was observed from 24 hours exposure. Our findings suggest that common carp exposed to lead develop. histological alterations such as epithelial lifting, interlamellar spaces, gill bridging, curling filaments, swelling, fusion and cell necrosis, irregular and inflammatory cells were observed in gill tissues, while inflammation ,degenaration and necrosis of muscle fibers, edema of muscle bundles, and lesions were observed in muscle tissues.
Acute heavy metal toxicity to fish has been attributed to the coagulation or precipitation of mucus on the gills and/or to cytological damage to the gills. The physiological mechanism of death by either of the above causes is related to a breakdown in gas exchange at the gills. This study of acute zinc toxicity to rainbow trout (Salmo gairdneri) supports an earlier hypothesis that modification of the gas exchange process at the gills creates hypoxia at the tissue level. Tissue hypoxia appears to be a major physiological change preceding death once the gas exchange process at the gills is no longer sufficient to supply the oxygen requirements of the fish.
Description
The second symposium on Aquatic Toxicology was held in Cleveland, Ohio, on 31 Oct.-1 Nov. 1977. This symposium was sponsored by the American Society for Testing and Materials through its Committee E35 on Pesticides. L. L. Marking, U.S. Fish and Wildlife Service, and R. A. Kimerle, Monsanto Co., presided as chairmen of the symposium and served as editors of this publication.
Effects of sub-acute levels of 3-(3,4-dichlorophenyl)-1,1-dimethylurea (diuron) on bluegill sunfish ( Lepomis macrochirus Rafinesque) were assessed in a pond environment. Eight 0.1-A earthen ponds were each stocked with 300 bluegill fingerlings and treated once with diuron wettable powder at 0, 0.5, 1.5, and 3.0 ppmw, two ponds per treatment level. Dissolved oxygen was reduced severely in some pond waters 2 days following treatment and the low level persisted for 3 to 4 days. Gill lamellae were ruptured and hemorrhagic in 20% of the fish from the 3.0 ppmw ponds at 3 days post-treatment. Fish in a cage succumbed during this period in a 3.0 ppmw pond. No further bluegill mortality was observed in treated ponds 3 days after treatment. Hematocrit measurements of treated and control fish could not be correlated with treatment level. Best growth was exhibited by control fish and their progeny. Diuron residues were not detectable in treated pond waters after 28 days. Residues of diuron in treated-pond vegetation were detectable up to 95 days following treatment, whereas residues in mud were measured by gas chromatography 122 days after treatment. Invertebrate populations increased in all ponds with time, indicating little or no effect of the herbicide on their numbers. Good control of filamentous algae and vascular aquatic vegetation was demonstrated in the treated ponds.
In fish of all groups examined including Teleostei, Chondrostei, Holostei, Chondrichytes, and Dipnoi, the primary epithelium that surrounds the primary lamellae has a close relationship with the venous compartment. Except in Dipnoi that displays a specialized epithelial drainage, the venous compartment consists of a central venous sinus that is connected with the systemic vasculature by noninnervated muscular arteriovenous anastomoses and drains into the branchial veins. Primary epithelium contains the chloride cells, which vary in morphology and number according to the milieu where the fish lives. The presence of an accessory cell beside the chloride cell is characteristic of seawater or seawater-adapted fish. The secondary epithelium that covers the free part of the secondary lamellae has an exclusive relationship with the arterioarterial vasculature, i.e., the pillar capillary compartment. This compartment is actively controlled by innervated sphincters located in the primary lamellae and in lower species by pre- and postlamellar noninnervated sphincters. Contraction of pillar cells may also contribute to this control. The secondary epithelium consists of an outermost layer of pavement cells that exhibited structural characteristics suggestive of cell coat secretion and an innermost layer of less differentiated cells. In contrast to the primary epithelium, the secondary epithelium does not exhibit any obvious differences between freshwater and seawater fish or undergo any obvious change during transfer of fish from fresh- to seawater. However, in conditions which exaggerate the absorptive functions of freshwater chloride cells, the secondary epithelium become modified by an intensive differentiation of freshwater chloride cells from its innermost layer of cells. These observations suggest possible specialized functional relationships between seawater chloride cells and the central venous sinus, and freshwater chloride cells and the arterioarterial compartment.
Short chain hydrocarbons and arene compounds in crude oil have a relatively greater dispersability and solubility in sea water than the longer chained fractions. Short chained fractions are often considered insignificant in environmental pollution as they are rapidly dissipated by volatilization and possibly by microbial degradation. Personal investigations as well as repeated references in the literature indicate the gills of fish to be excellent indices of the effects of external irritants and toxins upon fish populations in the field. The damage to gills reported apears to have resulted from short-term exposure to freshly spilled oil. The data, however, are subject to the following limitations: (1) the actual composition of the oil in question is not known since its origin was not determined; however its odor indicated a short residence time; (2) no data are available at this time concerning such critical subjects as recovery from gill damage; and (3) certain questions arise concerning the migration of the specimens examined. There appears, however, to be an inverse relationship between the amount of gill damage and the speed with which the fish in question usually swims, suggesting a direct relationship between damage and time of exposure (escape time).
In Langzeitversuchen (63 Tage) wurde das Herbizid NaTA (Natriumsalz der Trichloressigsäure) auf Nebenwirkungen an Karpfen untersucht. Dazu wurden insgesamt 32 einsommrige Karpfen gruppenweise in 50 1 Becken ausgesetzt, denen 700 (Gruppe 1), 70 (Gruppe 2) und 7 ppm (Gruppe 3) NaTA zugefügt wurden. Eine Versuchsgruppe ohne Zusatz diente als Kontrolle. Bei der klinischen Überwachung der Versuchs- und Kontrollfische fielen bei ersteren mehr oder weniger starke Veränderungen der Hautfarbe, Gewichtsverlust und insbesondere Atemstorungen auf.