CC BY
12
Journal of Stress Physiology & Biochemistry, Vol. 20, No. 4, 2024, pp. 44-51 ISSN 1997-0838 Original Text Copyright © 2024 by Adesanya, Idowu, Alegbeleye, Adekola, Towolawi and Ibrahim
ORIGINAL ARTICLE
OPEN ACCESS
Water Quality Parameters and Histopathological Changes in Gills and Liver of Clarias gariepinus Juveniles Exposed to Ethanol Leaf Extract of Senna occidental's
Adesanya Oluwatosin E. 1, Idowu Adekunle Adedoyin 1*, Alegbeleye Winifred Olusegun 1, Adekola Mukaila B. 2, Towolawi Adeleke Taofik 3, Ibrahim Farida O.1
1 Department of Aquaculture and Fisheries Management, Federal University of Agriculture, Abeokuta, Ogun State, Nigeria
2 Department of Environmental Toxicology and Toxicology, Federal University of Agriculture, Abeokuta, Ogun state, Nigeria
3 Department of Environmental Health Science, Fountain University Osogbo, Osun State, Nigeria
*E-Mail: [email protected]
Received May 22, 2024
The leaf of coffee senna or septic weed, Senna occidentalis, is among the medicinal and toxic plants whose toxicity on fish has not thoroughly been assessed. The study used 120 Clarias gariepinus juveniles with an average body weight of 16 ± 2 g and length of 8.5 ± 0.5 cm, randomly distributed in 12 plastic tanks of 35 L capacity filled up to 10 L volumes of water, acclimatised for 14-day, and fed twice daily with 1.8 mm skretting feed. Various ethanol leaf extracts of Senna occidentalis (0, 3000, 5000 and 7000 mg L-1) were added with a 5 mL syringe across the 12 plastic tanks, adopting a renewal bioassay, following the range-finding test of 500, 1000, and 1500 mg L-1, which had no visible impacts on the tested fish samples over 96-h. Five in-situ parameters (Dissolved Oxygen, Temperature, Conductivity, and Total Dissolved Solids) were monitored daily for water quality over 96 hours. Analysis of Variance analysed the data with the Duncan Multiple Range Test separating the mean. There were no significant (p > 0.05) differences across the monitored water parameters. The control fish had normal histopathology (gills and liver), while the gill of the exposed fish had severe lamellar hyperplasia with complete occlusion and congestion of pillar capillaries. Moderate hepatic necrosis, mild sinusoidal congestion and atrophy of hepatocytes were observed on the liver of the test C. gariepinus. The study concluded that levels of the Senna occidentalis used in the main experiment exhibited phytotoxicity, thereby necessitating adherence to the levels used in the range-finding test.
Key words: Lamellar hyperplasia, Necrosis, Renewal bioassay, Water quality, SDG 14
According to Oladimeji et al. (2016), Nigeria is classified as a typical coastal nation with an abundance of vegetation and water resources, both quantitatively and qualitatively sufficient to support a large fish population. The country has 87 km3 of groundwater and approximately 214 billion m3 of surface water, both of which are suitable for artisanal fishing and aquaculture.
Plant phytochemical extracts have biological properties that include illness prevention and nutrition production. For this reason, the tradition of utilising plants in the form of crude extracts to treat common infections and long-term conditions in fish species as a means of controlling parasites and pests as well as dietary nutrients has been adopted in Nigeria and other countries worldwide (Meskin et al., 2002).
According to Haruna (2006), fish is a preferred food because it is readily available as a major source of protein for Nigerians and its prices have been fair and quite affordable. Fish has emerged as one of Nigerians' main sources of protein in their diets over the past few decades. Notably, FAO (2014) states that increasing fish production and lowering reliance on fish imports are two of aquaculture's top priorities. Sall et al. (2020) examined global food consumption patterns of fish and its byproducts along with other seafood varieties. Moreover, researchers in fields including microbiology, pathology, toxicology, nutrition, and pharmacology have embraced the use of fish in their fields of study.
Over a billion people worldwide, according to FAO (2014), rely primarily on animal proteins found in foods like fish. Commercial aquaculture also contributes to greater food security by creating jobs and revenue for nearby communities. Fish provides high-quality protein, accounting for up to 16% of all animal protein consumed globally. The production of fish is also advancing globally, outpacing other livestock by roughly 10% annually.
Clarias gariepinus is a popular aquaculture fish species raised for human consumption among Africans; its marketability and acceptability boost its monetary value among Nigerian marketers. Aquaculture production needs to be increased and intensified to
attain maximum or sustainable production and guarantee that fisheries do not decline over time (Delgado et al., 2003).
Senna occidentals, also known as Coffee Senna or Septic Weed, is one of the many important wild plant species that are spreading faster across Nigeria's savanna region (Fig. 1). It was brought to Africa from tropical Asia (Umar and Ahmad, 2014). The plants go by a number of common names, including Mogdad coffee, Negro coffee, Stephanie coffee, Stinking coffee, Styptic weed, Coffee senna, and Coffee weed. Local names for the plant include Sanga-sanga or Rai dore (Hausa), Akidi agbara (Ibo), and Abo rere (Yoruba) in Nigeria (Isah et al., 2018); Bana Chakunda in Odisha, India (Jain and Jain, 2017).
Studies have shown that S. occidentals is toxic to a variety of animal species, like cattle (André et al., 2017), pigs (André et al., 2017), horses (André et al., 2017), rabbits (Tasaka et al., 2000), and poultry (André et al., 2017).
Consumers of fish products and food have become more aware of related health issues and are curious about the safety of the fish they eat (Zhou et al., 2020; Hassan et al., 2021; van Bussel et al., 2022). Thus, it is necessary to investigate fish toxicants found in the environment, such as botanical plants which exhibit piscicidal characteristics (Simeon et al., 2011).
It has also been established that S. occidentalis is both toxic and medicinal (that is, it possesses dual properties). However, Senna occidentalis leaves are among the toxic and medicinal plants whose toxicity has not been thoroughly assessed, particularly on fish. Thus, the current study aims to advance our understanding of water quality parameters and histopathological changes in the exposed C. gariepinus juveniles' gills and liver to ethanolic leaf extract of S. occidentalis. Histopathology of Fish
When evaluating the health of fish, histology and histopathology, which are used interchangeably, are helpful instruments because they provide important information about the extent of injuries, tissue damage, and organ functionality (Raibeemol et al., 2020). The literature had examples of using histology to ascertain
the dietary and medical state of Clarias gariepinus (Temitope et al., 2020), other fish (Harkrishan et al., 2020), and farm animals like chickens (Hussein et al., 2020). The fish gill is the primary organ through which pollutants enter the body and subsequently travel to other organs; this is because of its respiratory system and direct contact with water. According to Erdogan et al. (2022), fish are susceptible to aquatic toxicants because their gills are respiratory organs that often come into contact with the outside world. The delicate gills are in charge of preserving the ideal balance between acid and base in bodily fluids as well as osmoregulation. Because of their vast surface area and contact with external bodies, the gills are the organs that many pollutants in water target. As a result, they react quickly to even minute alterations in the chemical, biological, or physical environment (Sula et al., 2020).
The liver is a crucial organ that participates in the proteins carbohydrates, and fats metabolism. Hepatocyte alterations serve as the primary marker of a toxic environment, according to Hinton and Lauran (1990), who also claim that the liver serves as the body's primary detoxification centre and that this function is carried out by the liver cells (hepatocytes). Furthermore, the liver is the primary metabolic organ where detoxification occurs, making it vulnerable to harm from toxicants (Odigie et al., 2023). Although the liver has an important function in the glucose metabolism to glycogen for storage, lipid regulation, and amino acid deamination (Abubakar et al., 2023), it is impossible to overstate how vulnerable it is to any harm from toxicants. Toxins may also target it as an organ (Velkova-Jordanoska and Trajcevski, 2020).
MATERIALS AND METHODS
Experimental Site
The study was carried out at the Fish Hatchery Complex, Department of Aquaculture and Fisheries Management, Federal University of Agriculture, Abeokuta, Ogun State, Nigeria (FUNAAB). Collection of juveniles of Clarias gariepinus
A total of one hundred and twenty (120) juveniles of Clarias gariepinus with an initial average body weight of 16 ± 2 grams and length of 8.5 ± 0.5 cm were obtained
from Path Farm, Sagamu, Remo, Ogun State, Nigeria, and transported in a 50 L keg to Fish Hatchery, FUNAAB.
Acclimatisation of the C. gariepinus Juveniles
The C. gariepinus juveniles were acclimatised for two weeks; during this period, they were fed 1.8 mm imported Skretting feed, which contained 45% crude protein, two times a day, in the early hours of the morning and the late hours. Feeding was stopped 48-h to the experiment's inception, and wastes and wasted feed were taken out every day along with replenishing water.
Collection of Senna occidentalis leaves
The leaves of Senna occidentalis were obtained at Old Bola Ahmed Tinubu road, off Iju road, Ifako-Ijaiye LGA, Lagos State, Nigeria, and were validated at the Forestry and Wildlife Management Department, FUNAAB.
Experimental Design and Procedure
The experiment had four treatments and three replicates, each with 10 fish per treatment tank. From the acclimatised fish, one hundred and twenty juvenile catfish were randomly distributed into twelve plastic tanks of 35 L capacity volume, filled with 10 L of water for the main experiment.
Determination of Physico-Chemical Parameters
Using the calibrated multi-parameter Hanna Instrument (Model HI 98129) and DO meter (PCE-DOM Series oxygen meter), measurements of temperature, hydrogen ion concentration (pH), total dissolved solids (TDS), electrical conductivity (EC), and dissolved oxygen (DO) concentration were made in each treatment group (Table 1). Statistical Analysis
Analysis of variance was used to assess the data, and the distinction between treatment groups was found using the least significance difference (LSD) at the 0.05 significance level. The toxicity indices were obtained using SPSS (version 20.0), a computer statistical program.
RESULTS
Water quality parameters
The study's analysis of the physical and chemical parameters of water quality is highly pertinent to the level of water quality that C. gariepinus can tolerate. The outcome of the water parameters is shown in the table below.
Histopathology of the gill
Fish that were exposed to varying amounts of S. occidentals showed altered gill structures, which are shown in Fig. 2 A-D. The findings indicated that Fig. 2 A had no visible lesion, Fig. 2 B had no visible lesion, Fig. 2 C had pillar capillary congestion and Fig. 2 D had significant lamellar hyperplasia with total blockage of the inter-lamellar space.
Results of the effect of S. occidentals ethanollc leaf
extract on C. gariepinus' gills are shown in plate 2. A = control (0.00 mg/ 25 cL), B = Treatment B (3000 mg/ 25 cL), C = Treatment C (5000 mg/ 25 cL) and D = Treatment D (7000 mg/ 25 cL). Histopathology of the liver
The observed changes in the liver of C. gariepinus exposed to ethanolic leaf extract of S. occidentalis revealed no observable lesion in Fig. 3 E, Fig. 3 F showed moderate hepatic necrosis, Fig. 3 G displayed mild sinusoidal congestion, and there was atrophy of hepatocytes in Fig. 3 H.
Results of the effect of ethanolic leaf extract of S. occidentalis on the liver of C. gariepinus are shown in Fig. 3. E = control (0.00 mg/ 25 cL), F = Treatment B (3000 mg/ 25 cL), G = Treatment C (5000 mg/ 25 cL) and H = Treatment D (7000 mg/ 25 cL).
Figure 1. Picture of Senna occidentalis
Table 1. Physico-chemical parameters of the test water
Water Parameters Unit Range Mean
Temperature °C 25.37-28.43 26.90 ± 1.53
Dissolved oxygen mg/l 5.34-6.99 6.17 ± 0.83
pH - 6.83-8.40 7.62 ± 0.79
TDS mg/l 0.20-0.40 0.30 ± 0.10
Conductivity |s/cm 0.30-0.40 0.35 ± 0.05
Figure 2. A had no visible lesion; B had no visible lesion; C had pillar capillary congestion;
D had significant lamellar hyperplasia with total blockage of the inter-lamellar space.
»1 v ;) awx y
i k • K * r V V' u i I ^ ikJ^M 1 11/W '^H[niiM If
frjvs h Jfc
r fit
«J \ . k \ li I ~ 1
' IT-LvXiV : \ H | 'I 1*Y
.'« V V. I« 1
k > • T I I' A ,
Figure 3. E there is no observable lesion; F showed moderate hepatic necrosis;
G displayed mild sinusoidal congestion; H showed atrophy of hepatocytes.
DISCUSSION
Gebrelibanos et al. (2014) reported that Senna species have been known to cause a variety of toxicities despite their many potential medicinal benefits; this has been a major concern in aquaculture production (Idowu et al., 2017). Considering the level of water quality that C. gariepinus can tolerate, the physical and chemical water quality parameters examined in this study are of great importance. Table 1 described that there was no significant difference (p > 0.05) in the water parameters; the values recorded were within the optimal range, meaning the observed parameters did not stray from regulatory norms; this is consistent with the findings of Jamabo et al. (2015); it can therefore be said that the water had no negative impact on C. gariepinus juveniles. According to this study, different amounts of S. occidentalis ethanolic leaf extracts caused varying degrees of histopathological alterations in C. gariepinus liver and gills. Tissue histopathological examination provides a reliable means of identifying and observing different kinds of tissue damage (Yang et al., 2014). The healthy gills of fish are essential for breathing, osmoregulation, and the excretion of nitrogenous waste (Jimoh et al., 2023), among other metabolic activities (Herrero et al., 2018). The result of histology of the gills revealed that there was no visible lesion in the control treatment. Congestion in the pillar capillaries affected the juveniles in treatment B, which caused a major blockage or obstruction of oxygen flow. The gill of C. gariepinus juveniles in treatment D was severely affected; this might be a result of its vast surface area and direct contact with external bodies, as reported by Sula et al. (2020); the gills are the organs that many pollutants in water target and it was earlier said that they react quickly to even minute alterations in the chemical, biological, or/and physical environment. According to Foyle et al. (2020), an abrupt change in gill activity may be fatal, which was likely the case in this research work. Moreover, Agbebi et al. (2013) observed hyperplasia in the gills of C. gariepinus fed different dietary treatments; in contrast, the fish in treatment D was typified with severe lamellar hyperplasia with complete occlusion of inter-lamellar distance; meaning, there was an unusual
increase in the size of the organ due to an increase in the number of cells which led to an obstruction in the lamellar of the gills.
As earlier reported, the liver is the primary metabolic organ where detoxification takes place. For this reason, the liver becomes vulnerable to harm from toxicants (Odigie et al., 2023) and is also a target for toxins (Velkova-Jordanoska and Trajcevski, 2020). The result of the liver histology revealed that there was no visible lesion in the control treatment. However, the fish's liver displayed moderate hepatic necrosis in treatment B, which was in line with studies of Jimoh et al. (2015) and Olukunle (2011), who also noted minor hepatocyte alterations; this could lead to cirrhosis in the long run, as the injury or death of hepatic cells in the organ could result in diseases of the liver caused by damage from toxins. Hepatocyte atrophy was seen in treatment D and mild sinusoidal congestion in treatment C, respectively; this could result in a decrease in the liver's functionality because sinusoidal congestion means a block in the channel through which blood flows in the liver and can also result in cirrhosis; this aligned with the findings of Jia et al. (2022), who reported hepatic cell shrinkage, which could cause cirrhosis and impaired portal flow through the liver.
CONCLUSION
Given the values of the water quality parameters recorded, it can be concluded that the water quality did not deviate from optimal value despite the toxins released by S. occidentalis. However, the toxicity of S. occidentalis was capable of causing intensive damage to the internal organs of C. gariepinus, most especially the gills, which have direct contact with external bodies. The study would advise that usage of the test plant should not exceed the concentration of the range-finding test to prevent the phytotoxic effect of the likes of the test fish in this study.
ACKNOWLEDGEMENTS
The authors would like to express their gratitude to the anonymous reviewers in advance for their constructive feedback, which will undoubtedly enhance the quality and clarity of the manuscript.
The authors will also appreciate one another for
working together to ensure the success of this experiment.
CONFLICTS OF INTEREST
The authors declare that they have no potential conflicts of interest.
REFERENCES
Abubakar, M. I., Adeshina, I., Moruf, R. O. and Ayelabowo, A. A. (2023). Gills and liver histopathology of Clarias gariepinus exposed to Aqueous Extract of Carica papaya Seed under Laboratory Condition, J. Mater. Environ. Sci., 14(2), 224-233.
Agbebi, O. T., Ogunmuyiwa, T. G. and Herbert, S. M.
(2013). Effect of dietary garlic source on feed utilisation, growth and histopathology of the African catfish (Clarias gariepinus). Journal of Agricultural Science, 5(5), 26-34.
André, T., Gotardo, M., Haraguchi, Paulo, C. F., Raspantini, Maria, L. Z., D. and Silvana L. G. (2017). Toxicity of Senna occidentalis seeds in laying hens and its effects on egg production, Avian Pathology, 46(3), 332-337. Delgado, C. L., Wada, N., Rosegrant, M. W., Meijer, S. and Ahmed, M. (2003). Fish to 2020. Supply and demand in changing global markets. WorldFish Center Technical Report 62. WorldFish Center. Penang, Malaysia, 226 p. Erdogan, K., Örün, G. N., Korkmaz, N., Erkmen, B., Polat, H., Dogru, A., and Örün, i. (2022). Stress, growth, cytokines and histopathological effects of permethrin in common carp (Cyprinus carpio). Chemistry and Ecology, 38(2), 162-179. FAO, (2014). State of World Fisheries and Aquaculture. Opportunities and challenges. Fisheries and Aquaculture Department of the United Nations, Rome, Italy. 243 p. Foyle, K. L., Hess, S., Powell, M. D., & Herbert, N. A. (2020). What is gill health and what is its role in marine finfish aquaculture in the face of a changing climate?. Frontiers in Marine Science, 7, 400. Gebrelibanos, M., Periyasamy, G. and Sintayehu, B.
(2014). Senna occidentalis seed: is it health risk or potential medicine?" International Journal of
Pharmacognosy, 1(3), 161-167.
Harkrishan, K., Anil, K. T., Bhardwaj, J. K., and Saraf, P. (2020). Effect of Imidacloprid on Histopathological Alterations of Brain, Gills and Eyes in hatchling carp (Cyprinus carpio L.). Toxicology International, 27(1-2), 70-78
Haruna, A. B. (2006). Studies on the aspect of socioeconomic factors influencing fish farming in Adamawa State, Nigeria. J Arid Zone Fish 2(1), 814.
Hassan, F., Ali, H. and Zaidi, S. F. (2021). Consumer perceptions and behaviours towards seafood sustainability: A systematic review. Marine Policy, 122, 103946.
Herrero, A., Thompson, K. D., Ashby, A., Rodger, H. D., and Dagleish, M. P. (2018). Complex gill disease: An emerging syndrome in farmed Atlantic Salmon (Salmor salar L.). Journal of Comparative Pathology, 163, 23-28.
Hinton, D. E., and Lauren, D. J. (1990). Liver structural alterations accompanying chronic toxicity in fishes: potential biomarkers of exposure. In: Biomarkers of Environmental Contaminations (edited by J. F. McCarthy and L. R. Shugart). Lewis Publisher, Boca Raton, Florida. p.17-57.
Hussein, E., Ahmed, S., Abudabos, A. E., and Aljumaah, M. (2020). Effect of antibiotic, phytobiotic and probiotic supplementation on growth, blood indices and intestine health in broiler chicks challenged with Clostridium perfringens. Animals (MDPI), 10(3), 10.3390/ani10030507 Idowu, T. A., Adedeji, H. A. and Sogbesean O. A. (2017). Fish disease and health management in aquaculture production. International Journal of Environment and Agricultural Science, 1(1), 1-6.
Jain, V., and Jain, S. K. (2017). Dictionary of Local Botanical Names in Indian Folk Life. Scientific Publishers.
Jamabo, N. A., Fubara, R. I. and Dienye, H. E., (2015). Feeding frequency on growth and feed conversion of Clarias gariepinus (Burchell, 1822) fingerlings. International Journal of Fisheries and Aquatic Studies, 3(1), 353-356.
Jia, R., Hou, Y., Feng, W., Li, B. and Zhu, J. (2022). Alterations at biochemical, proteomic and
transcriptomic levels in the liver of tilapia (Oreochromis niloticus) under chronic exposure to environmentally relevant levels of glyphosate. Chemosphere, 294, 133818.
Jimoh, J. O., Omobepade, B. P., Akinsorotan, A. M., Olasunkanmi, J. B., Ariyomo, T. O. and Fatoyinbo, V. O., (2023). Histopathological observations on liver and gills of Clarias gariepinus juveniles treated with some prophylactics. Journal of Aquaculture and Fish Health, 12(3), 380-388.
Jimoh, W. A.; Sodamola, M. O.; Adebayo, M. D.; Banjo, O. T.; Ayeloja, A. A. and Adeleke, A. B. (2015). Histological changes in the liver and kidney of Clarias gariepinus fed Chrysophyllum albidum seed meal as maise replacer. International Journal of Zoological Research, 11(1), 29-36.
Meskin, M. S., Davies, A. J., Bidlack, W. R., and Omaye, S. T. (2002). Phytochemicals in nutrition and health. CRC Press, p.123. ISBN 978-1-58716-083-7.
Odigie, E. B., Ugwuanyi, R. N. and Omoregbe, E. O. (2023). Clarias gariepinus (African Catfish) liver and gills susceptible to heavy metal toxicity in fish farms harvested in Benin Metropolis, Nigeria.
Oladimeji, Y. U., Abdulsalam, Z., Muhammed L. A., Adefalu, L. L. and Adepoju, S. A. (2016). Effects of water hyacinth (Eichhomia crassipes) on artisanal fishery of River Niger in North-Central Nigeria. Journal of Animal Production and Research, 28(2), 338-349.
Olukunle, O. (2011). Evaluation of different dietary oil sources on growth performance and nutrient utilisation of Clarias gariepinus juveniles. Nigerian Journal of Fisheries, 8(2), 184-196.
Raibeemol, K. P. and Chitra, K. C. (2020). Fish and shellfish immunology induction of immunological, hormonal and histological alterations after sublethal exposure of chlorpyrifos in the freshwater fish, Pseudetroplus maculatus (Bloch, 1795). Fish Shellfish Immunology, 102, 1-12.
Sall, M. L., Diaw, A. K. D. and Gningue-Sall, D. (2020). Toxic heavy metals: impact on the environment and human health, and treatment with conducting organic polymers, a review. Environmental Science Pollution Research, 24, 29927-29942
Simeon, O. A., Kuton, M. P., Idowu, A. A and Adelekun, A. B. (2011). Acute toxicity of Nile Tilapia (Oreochromis niloticus) juveniles exposed to aqueous and ethanolic extracts of Ipomoea aquatica Leaf. Nature and Science, 9(3), 91-99.
Sula, E., Aliko, V., Mark, E., Nuro, A., and Faggio, C. (2020). Evaluation of kidney histopathological alterations in Crucian Carp, Carassius carassius, from a pesticide and PCB-contaminated freshwater ecosystem, using light microscopy and organ index mathematical model. International Journal of Aquatic Biology, 8(3), 154-165.
Tasaka, A. C., Weg, R., Calore, E. E., Sinhorini, I. L., Dagli, M. L., Haraguchi, M., Gorniak, S. L. (2000). Toxicity testing of Senna occidentalis seed in rabbits. Vet Res Commun, 24(8), 573-582.
Temitope, D. M. (2020). Morphological, haematological and biochemical changes in African catfish Clarias gariepinus (Burchell 1822) juveniles exposed to clotrimazole. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 236, 108815.
Umar, T. and Ahmad, F. A. (2014). Macro and micro minerals composition of Senna obtusifolia and S. occidentalis in Sudano - Sahelian Ecosystem, Nigeria. A paper presented at the National Conference of Forestry Association of Nigeria (FAN) held at Minna, Niger State, Nigeria.
Van-Bussel, L. M., Kuijsten, A., Mars, M. and Van't-Veer, P. (2022). Consumers' perceptions on food-related sustainability: A systematic review. Journal of Cleaner Production, 341, 130904.
Velkova-Jordanoska, L. and Trajcevski, B. 2020. Assessment of ecosystem pressure and impact on fish population in the Channel Studencista (Lake Ohrid) through haematological and histopathological biomarkers. Acta Zoologica bulgarica, Suppl. 15, 181-184.
Yang, X., Schnackenberg, L. K., Shi, Q. and Salminen, W. F. (2014). Hepatic toxicity biomarkers. In: Biomarkers in Toxicology Gupta, R (Ed) p. 241-259.
Zhou, Y., Chan, L. and Gao, D. (2020). Consumer perceptions and preferences for sustainable and safe seafood: A review. Food Control, 113, 107194
