http://myjms.mohe.gov.my/index.php/bsk
Copyright © 2022 Faculty of Health Science UKM. All right reserved Artikel Asli/Original Article
The Use of Eye Diameter Fluctuating Asymmetry to Indicate
Developmental Instability of Channa striata upon Exposure to Various Cadmium Concentrations
Penggunaan Asimetri Turun Naik Diameter Mata untuk Menunjukkan Ketakstabilan Perkembangan Channa striata setelah Didedahkan kepada Pelbagai
Kepekatan Kadmium
SHARIFAH MUSAISHA AINNA SYED MUSTAFA, MOHD RIDUAN ABDULLAH AND MOHD SHAM OTHMAN
ABSTRACT
Fluctuating asymmetry (FA) is a widely used research tool to indicate the effect of pollution on development instability. This study was conducted to observe the effects of different concentrations and durations of cadmium exposure on developmental instability of Channa striata, by assessing FA of the eye diameter. The fishes were exposed to four exposure groups of different cadmium concentrations (0.000 mg/L, 0.005 mg/L, 0.010 mg/L and 0.015 mg/L) for 16 weeks. The FA of eye diameter was first measured on week 4 and every two weeks henceforth for 12 weeks. The results of this study showed that there was a statistically significant increase (p<0.001) in the average FA of the eye diameter of C. striata as the concentration of cadmium exposure increased. Nevertheless, there was no statistically significant increase in average FA of eye diameter as the concentration of cadmium and duration of exposure increased. However, increasing trend of average FA of eye diameter was observed with the increasing concentration of cadmium and duration of exposure. The results concluded that a higher concentration of cadmium exposure caused higher FA of eye diameter of C. striata.
Meanwhile, higher concentration and duration of cadmium exposure may influence higher FA of eye diameter of C. striata. Therefore, in the case that the sentinel species used were chronically exposed to cadmium, the duration of exposure shall be lengthened to observe the significant effects of FA measured in fish.
Keywords: Cadmium, duration, effects, fluctuating asymmetry, eye diameter
ABSTRAK
Asimetri turun naik (FA) adalah satu alat kajian yang sering digunakan bagi mementukan kesan pencemaran terhadap ketidakstabilan perkembangan. Kajian ini dijalankan bagi menentukan kesan dedahan kadmium pada kepekatan dan durasi yang berbeza ke atas ketidakstabilan perkembangan pada Channa striatus. Dengan mengukur FA diameter mata. Ikan-ikan tersebut telah didedahkan kepada empat kumpulan dedahan cadmium (0.000 mg/L, 0.005 mg/L, 0.010 mg/L and 0.015 mg/L) selama 16 minggu. Keputusan kajian menunjukkan terdapat peningkatan signifikan (p<0.001) purata FA diameter mata C. striata dengan peningkatan kepekatan kadmium. Namun tiada peningkatan yang signifikan pada purata FA diameter mata yang dilihat dengan peningkatan kepekatan dan durasi dedahan cadmium. Namun, wujud trend peningkatan purata FA diameter mata dengan peningkatan kepekatan dan durasi dedahan terhadap kadmium. Keputusan menunjukkan bahawa dedahan terhadap kepekatan kadmium yang tinggi menyebabkan peningkatan nilai FA diameter mata C. striata.
Manakala, peningkatan kepekatan dan durasi dedahan mungkin mempengaruhi FA diameter mata C. striata.
Oleh yang demikian, sekiranya spesies sentinel yang digunakan didedahkan secara kronik terhadap cadmium, durasi dedahan perlu ditingkatkan untuk melihat perubahan signifikan FA pada ikan tersebut.
Kata kunci: Kadmium, durasi, kesan, asimetri turun naik, diameter mata
INTRODUCTION
Cadmium is a trace metal with high toxicity and has the tendency to be accumulated in living organisms (Sharma and Sachdeva 2015). Thus, the concentration of trace metals found in living organisms increases with increasing trophic levels (Zhang et al. 2016). The solubility of cadmium in water makes it readily
absorbed by the fish from the water and through food ingestion (Govind and Madhuri 2014). Since cadmium is poorly regulated by an organism, it can induce oxidative stress, causing injuries to the liver and kidney and affecting their developmental and morphological stability (Perera et al. 2015). These effects could impact the fish population negatively as the developmental and morphological instability
affect their survival and growth rate (Hazrat et al.
2019).
The most common method to analyze the impact of developmental instability on a particular morphological feature is fluctuating asymmetry (FA) (Benitez et al. 2018). FA measures the small random deviations occurring between the right and left sides of bilaterally symmetrical traits of an organism (Omar et al. 2015). The symmetrical trait in fish is more sensitive toward induced environmental stressors as compared to other animals, thus, fish serve as a useful bio-indicator to detect the negative impact on the environmental quality of an aquatic ecosystem (Lutterschmidt et al. 2016). For instance, higher FA levels are expected in marine fish under environmental stresses when compared to the control population (Trokovic et al. 2012).
In this study, Channa striata or its common name; Snakehead fish has been chosen as a sentinel species for cadmium contamination study based on criteria such as it is not threatened by extinction, ubiquitous, suitable size, has a large distribution area, and has a stable population (International Union for Conservation of Nature 2019). The aims of this study are to measure and compare the FA for the eye diameter of C. striata treated with different cadmium concentrations as well as treated with various concentrations and durations of cadmium exposure.
While FA for eye diameter traits has been reported in other fish species, the use of the tool in C. striata is novel. C. striata is an aquaculturally important fish species in Malaysia and Southeast Asia. The fish is considered a valuable fish because of its good taste, and nutritional and pharmaceutical values (Muntaziana et al. 2013). The fish is also a carnivorous species, hence it is important in population control of prey species to maintain ecological balance in the freshwater aquatic ecosystem (Talde et al. 2004).
MATERIALS AND METHODS
ETHICS STATEMENT
Ethics approval was not required for this study because the target fish species is a commercially exploited aquaculture fish in Malaysia (Fisheries Development Authority of Malaysia 2018).
SAMPLE COLLECTION
The 500 snakehead fish fingerlings with an average length of 6.5±0.41 cm and average body weight of 2.21±0.027 g were acclimatized to laboratory conditions for three days in dechlorinated tap water prior to any treatment.
EXPOSURE GROUPS
The fingerlings were then divided into four exposure groups of different cadmium concentrations: 0 mgL-1 (control), 0.005 mgL-1 (low exposure), 0.010 mgL-1 (medium exposure) and 0.015 mgL-1 (high exposure) for 16 weeks. Fingerlings were stocked at 5 individuals per L (Kok 1981) into 5 separate 5 L aquariums for each treatment group. The top of the aquariums was closed with a net to prevent the fingerlings from moving outside of the experimental aquariums.
REARING CONDITIONS
The fingerlings were fed chicken liver ad libitum twice a day with the total for each feed did not exceed the recommended feeding rate of 3% of their body weight (Yakupitiyage 2013). Excess leftover feed was removed after feeding and water change was carried out every week to ensure the water is suitable for fish to survive and grow without affecting the intended cadmium exposure conditions. Dechlorinated treated water was used for the purpose of this experiment in all treatment groups. The average laboratory ambient temperature recorded was 26.1±0.3 °C and natural light was utilized during the entire experimental process conducted. The rearing process of fingerlings utilized natural ventilation without aeration installation. Only surviving fingerlings are sampled and the number of dead fingerlings before sampling was not taken into consideration.
FA MEASUREMENT
The eye diameters of the fish were measured using a digital vernier caliper in cm and their FA was first calculated on week 4 and subsequent biweekly measurement for 12 weeks. All FA measurements were made exclusively by one person to avoid possible inter-observer variability (Kozlov et al.
2017). FA is measured as the percentage of measurement deviation of a paired structure from the average values. FA value for the eye diameter of Channa striata was calculated using the formula shown as Eqn. (1) below (Wilkins et al. 1995). Data were analyzed with the SPSS version 25.0 program using one-way analysis of variance (ANOVA) to compare the effects of different concentrations of cadmium exposure on FA for eye diameter of C.
striata while using two-way analysis of variance (ANOVA) to compare the effects of different concentration and duration of cadmium exposure on FA for eye diameter of C. striata.
|Left – Right| × 100
FA = (1)
½|Left - Right|
RESULTS
COMPARISON OF FA ACCORDING TO TREATMENT GROUPS
Fig. 1 shows the comparison of FA for the eye diameter of C. striata exposed to various concentrations of cadmium over 16 weeks period. The results showed that the level of FA significantly (p<0.05) increases as the exposure to cadmium concentration increases. Hence, indicates a higher FA occurred in the cadmium exposed population as the exposure to cadmium concentration increased. It is also noted that the results of FA for the eye diameter of C. striata showed that the increase was statistically significant (p<0.05) when the comparison between control and other three cadmium exposed groups was made. However, the increase of FA for the eye diameter of C. striata was not statistically significant (p>0.05) when compared among the three cadmium exposed groups (0.005 mg/L, 0.010 mg/L, and 0.015 mg/L) was made. Fish exposed to 0.015 mgL-1 Cd group (highest exposure) showed the highest FA while those in the control group showed the lowest FA for eye diameter.
COMPARISON OF FA ACCORDING TO TREATMENT GROUPS AND
DURATION OF EXPOSURE
Fig. 2 shows the FA for eye diameter of C. striata exposed to different concentrations and durations of cadmium exposure over 16 weeks period. The results showed that the increase of FA for the eye diameter of C. striata was not significant (p>0.001) as the concentration and duration of cadmium exposure increased. Additionally, an increasing trend of FA was observed for the parameter assessed as the concentration and duration of cadmium exposure increased. Thus, indicating higher developmental instability of C. striata as the concentration and duration of cadmium exposure increases. It is also noted that the results of FA for the eye diameter of C.
striata showed that the increase was not statistically significant (p>0.001) when the comparison between control and the three cadmium exposed groups (0.005 mg/L, 0.010 mg/L, and 0.015 mg/L) was made. In addition, the increase of FA for the eye diameter of C.
striata was not statistically significant (p>0.001) when compared among the three cadmium exposed groups (0.005 mg/L, 0.010 mg/L, and 0.015 mg/L) was made.
Fish exposed to 0.015 mgL-1 Cd group (highest exposure) at the 16th week (longest duration) showed the highest FA while those in the control group (no exposure) at the 4th week (shortest duration) showed the lowest FA for eye diameter.
FIGURE 1 Overall average FA for eye diameter of Channa striata exposed to different cadmium concentration over 16 weeks
FIGURE 2 Average FA for eye diameter of Channa striata exposed to different concentration and duration of cadmium exposure
DISCUSSION
The increased FA of the paired structures indicates the organism's ability to stabilize homeostasis (stability) during growth under environmental stress has been compromised (Benítez et al. 2018). The result of this study is consistent with previous findings which have detected a significant increase of variations for pectoral fin length and eye diameter of Grass Goby Fish in the highly contaminated site as compared to the low contaminated site along the coastline of Eastern Tunisia (Gharred et al. 2017). Both findings indicate that environmental stress does influence developmental instability in fish (Allenbach 2011).
Thus, increasing values of FA in animals can be an indicator to reflect the increasing degree of ecological stress in the environment (Coda et al. 2017). A continuously elevated level of environmental stress will enhance the morphological variations to be more obvious which could potentially affect the survival of organisms and their population size (Panfili et al.
2005).
The role of cadmium exposure on the increased FA of the paired structures between the control group and the three cadmium exposed groups was supported by a previous study that found cadmium causes developmental instability and phenotypic variation in fish species (Annabi et al. 2013). This study’s finding is consistent with the results from another study that reported significant variations of six bilateral metrics (length of pre-orbital distance, length of sub-orbital distance, orbital diameter of the eyes, pre-pectoral distance from pectoral fin, length of ventral fin, length
of pectoral fin) of Grass Goby Fish inhabiting between the polluted and unpolluted area in Tunisia (Mabrouk et al. 2014). The FA of the six bilateral metrics was significantly higher in the polluted area as compared to the unpolluted area. Cadmium affects developmental stability in fish as cadmium was reported to be the major contaminant found in the polluted area (Mabrouk et al. 2014). Thus, increasing values of FA in animals can be an effective bio- indicator to indicate trace metal contamination in the environment (Authman et al. 2015) and thereby, serve as an early warning sign of ecological stress in the aquatic ecosystem as it is the most straightforward method to study the effects of trace metal contamination in fish as compared to other invasive biomarkers (Beasley et al. 2013).
The increased FA for the eye diameter of C.
striata is not statistically significant (p>0.001) when the comparison between the concentration and duration of cadmium exposure was made because C.
striata have a slow growth rate. Based on several growth studies conducted, C. striata on average weighed 60g by 12 weeks past the fingerling stage (Mehrajuddin et al. 2011; Talpur et al. 2014). This species requires a long raising period of seven to ten months before harvesting depending on the optimum conditions achieved during the breeding season (Kok 1981). This study was conducted only for 16 weeks, therefore, the manifestation of effects of exposure to cadmium at different concentrations and time- examined were subtle due to its slow growth rate.
Perhaps, extending the duration of this study to 10 months may yield a better representation of how
cadmium exposure affects the FA of the eye diameter of C. striata. Additionally, an increasing trend of FA for the paired structures was observed as the concentration and duration of exposure to surrounding ecological stress increased. This signifies the animal grows less symmetrically (De Coster et al. 2013).
The growth rate of fish is reduced as a result of exposure to cadmium (Authman et al. 2015). This is evident in the previous study that reported a significant decrease in the growth rate of Tilapia fish (Oreochromis niloticus) which were exposed to cadmium as compared to the control group (Heydarnejad et al. 2013). When the growth rate of fish is reduced or started to slow down, the animal's ability to cope with environmental stress increases over time (Michaelsen et al. 2015). Thus, explaining the increment of FA for the eye diameter of C. striata observed was not statistically significant (p>0.001) as the concentration and duration of cadmium exposure increased. In addition, the slow growth rate of C.
striata (Mehrajuddin et al. 2011; Talpur et al. 2014) further reduces the manifestation of the effects on developmental instability of C. striata upon environmental stressors including trace metal contamination. Therefore, it further strengthens the increase of FA for the paired structures assessed in this study were subtle as the concentration and duration of exposure to cadmium increased (De Coster et al. 2013).
Besides, a study reported that FA for 11 paired structures in the Australian estuarine smooth toadfish (Tetractenos glaber) showed a significant positive correlation across the total length of fish measured and sampled from September 1997 up to November 2003 in two estuaries of the Sydney region, New South Wales, Australia (Lajus et al. 2015). The results reported in the study were inferred to the increased pollution patterns that occurred in the area under study as there was a clear association between heavy metal (Cd, Cr, Cu, Ni, Pb and Zn) and organic pollution (DDE, DDD, DDT, Dieldrin, Lindane &
Chlordane) across increasing sampling period from
September 1997 up till November 2003. Thus, the study, it showed that the morphological variations of an organism will be more obvious to be observed when the duration of exposure to an environmental stressor is lengthened such as measuring across various seasons throughout the year. Hence, it further strengthens the results obtained in this study.
Therefore, in the case that the sentinel species used were chronically exposed to cadmium, the duration of exposure shall be lengthened in order to observe the significant effects of FA on the assessed parameter measured in fish.
The lowest FA for eye diameter of C. striata was detected in the control group, and these are probably due to minor inconsistencies during development (Manthey & Ousley 2020). Stable development shall result in identical left and right sides (perfect symmetry) of paired traits in an organism in the absence of an environmental stressor (Swaddle 2017).
However, organisms rarely develop with perfect symmetry as developmental disturbances caused by various random perturbations results in low levels of asymmetry (Hingabay et al. 2016).
This study’s findings are consistent with findings from other studies as shown in Table 1 when a comparison of FA value between the different concentrations of cadmium exposure was made. This implies that the presence of heavy metal contamination such as cadmium in the aquatic ecosystem will affect phenotypic variation in fish species (Jawad et al. 2020). However, the findings of this study are not consistent with findings from the previous study as shown in Table 2 when a comparison of FA value between different concentrations and duration of cadmium exposure was made. This may be inferred from the difference in the length of the study (the duration of cadmium exposure) conducted. Therefore, in the case that the sentinel species used were chronically exposed to cadmium, it is important to lengthen the duration of cadmium exposure in order to observe a more obvious effect on FA of paired external structures.
TABLE 1 Comparison of average FA value between the control group and cadmium exposed group in different fish studies
Research Species Results
Average FA value for eye diameter of the fish species under study
Non-polluted Polluted p-value
Gharred et al. 2017 Zosterisessor ophiocephalus
0.030 0.100 <0.001 (Significant) Mabrouk et al. 2014 Zosterisessor
ophiocephalus
0.030 0.150 <0.001 (Significant) Michaelsen et al.
2015
Menidia beryllina 0.022 0.030 <0.001 (Significant)
This study Channa striata 0.002 0.013 <0.001 (Significant) Note: p<0.001 indicate there was a significant increase of average FA value for eye diameter of fish species under study obtained from polluted area (cadmium exposed group) as compared to non-polluted area (control group).
TABLE 2 Comparison of average FA value between different concentration and duration of cadmium exposure in different fish studies
Research Species Sampling period Bilateral traits Results
Average FA value p-value Lajus et al.
2015
Tetractenos glaber
3 times per year
(Autumn, Winter and Spring)
1. Premaxilla bone length
2. Maxilla bone length 3. Angular bone length 4. Dentary bone length 5. Preopercle bone
length
6. Opercle bone length 7. Hyomandibular bone
length
8. Quadrate bone length 9. Articular bone length 10. Epihyal bone length 11. Ceratohyal bone
length
<0.001 (Significant)
This study Channa striata First 4 weeks and every 2 weeks for 12 weeks
Eye diameter >0.001 (Not Significant) Note: p<0.001 indicate there was a significant increase of average FA value obtained as the concentration and duration of exposure to environmental stressor increases.
CONCLUSION
We documented a significantly increased (p<0.05) average FA for the eye diameter of C. striata as the concentration of cadmium exposure increases.
However, the average FA for the eye diameter of C.
striata did not significantly increase (p>0.001) as the concentration and duration of cadmium exposure increased. Additionally, an increasing trend of average FA for the eye diameter of C. striata was observed as the concentration and duration of cadmium exposure increased. It was also noted that the highest average FA values were obtained from the highest cadmium exposure group (0.015 mg/L). This research concluded higher concentration of cadmium exposed to C. striata will result in higher average FA of bilateral metrics such as eye diameter. Hence, signifies the effect of cadmium exposure to cause developmental instability in a sentinel species. Higher concentration and duration of cadmium exposure to C.
striata may influence higher FA of the assessed parameter. The implication of this study showed that eye diameter may be used as an effective parameter in assessing FA to indicate ecological stress in fish.
ACKNOWLEDGEMENT
The author(s) would like to thank Environmental Health and Industrial Safety Programme, Faculty of Health Sciences and The Center for Toxicology &
Health Risk Assessment, Universiti Kebangsaan Malaysia for research support. This research is also partly funded by Geran Galakan Penyelidik Muda (GGPM-2011-092).
REFERENCES
Allenbach, D. M. 2011. Fluctuating asymmetry and exogenous stress in fishes: a review. Rev. Fish Biol. Fish. 21(3): 355–376.
Annabi, A., Said, K. & Messaoudi, I. 2013. Heavy metal levels in gonad and liver tissues-effects on the reproductive parameters of natural populations of Aphanius facsiatus. Environ. Sci.
Pollut. Res. 20(10): 7309–7319.
Authman, M. M., Zaki, M. S., Khallaf, E. A. &
Abbas, H. H. 2015. Use of fish as bio-indicator of
the effects of heavy metals pollution. J. Aquac.
Res. Dev. 06(04): 2–13.
Beasley, D. A. E., Bonisoli-Alquati, A. & Mousseau, T. A. 2013. The use of fluctuating asymmetry as a measure of environmentally induced developmental instability: a meta-analysis. Ecol.
Indic. 30: 218–226.
Benítez, H. A., Lemic, D., Püschel, T., Virić, G. H., Kos, T., Barić, B., Bažok, R. & Pajač Živković, I.
2018. Fluctuating asymmetry indicates levels of disturbance between agricultural productions: an example in Croatian population of Pterostichus melas melas (Coleptera: Carabidae). Zool. Anz.
276: 42–49.
Coda, J. A., Martínez, J. J., Steinmann, A. R., Priotto, J. & Gomez, M. D. 2017. Fluctuating asymmetry as an indicator of environmental stress in small mammals. Mastozool. Neotrop. 24(2): 313–321.
De Coster, G. S., Van Dongen, P., Malaki, M., Muchane, A., Alcántara-Exposito, H., Matheve &
Lens, L. 2013. Fluctuating asymmetry and environmental stress: understanding the role of trait history. PLOS ONE 8(3): 57966.
Lembaga Kemajuan Ikan Malaysia. 2018. Buku Data dan Statistik Lembaga Kemajuan Ikan Malaysia Tahun 2016 - Tahun 2018. Kuala Lumpur:
Lembaga Kemajuan Ikan Malaysia.
Gharred, T., Mabrouk, L. & Hellal, A. N. 2017.
Effect of pollution on the fluctuating asymmetry in the Grass Goby Zosterisessor ophiocephalus (Pallas, 1811) as contamination indicator of Eastern Tunisia. SDRP J. Aquac. Fish. Fish Sci.
1(1): 30–36.
Govind, P. & Madhuri, S. 2014. Heavy metals causing toxicity in animals and fishes. Res. J. Animal Vet.
Fish. Sci. 2(2): 17–23.
Hazrat, A., Khan, E. & Ilahi, I. 2019. Environmental chemistry and ecotoxicology of hazardous heavy metals: environmental persistence, toxicity, and bioaccumulation. J. Chem. 2019: 1–14.
Heydarnejad, M. S., Khosravian-Hemamai, M. &
Nematollahi, A. 2013. Effects of cadmium at sub-lethal concentration on growth and biochemical parameters in rainbow trout (Oncorhynchus mykiss). Irish Vet. J. 66(1): 1–7.
Hingabay, V. S., Kamantu, H. G., Protacio, K. J. T., Requieron, E. A., Lobredo, G. G. & Torres, M.
A. J. 2016. Fluctuating asymmetry as a measure of developmental stability of three-spotted gourami, Trichopodus trichopterus (Pallas, 1770) in Lake Sebu, South Cotabato, Philippines. AACL Bioflux 9(2): 260–269.
IUCN. 2019. International Union for Conservation of Nature Annual Report 2019. Gland, Switzerland:
IUCN.
Jawad, L. A., Ghazwan, M. I. & Rutkayová, J. 2020.
Directional fluctuating asymmetry in certain morphological characters as a pollution indicator:
Tigris catfish (Silurus triostegus) collected from
the Euphrates, Tigris, and Shatt al-Arab Rivers in Iraq. Fish. Aquat. Life 28(1): 18-32.
Kok, L. W. 1981. Snakehead (Channa striatus) Farming in Thailand. In: M. Boonyaratpalin, E.
W. McCoy & T. Chittapalapong (eds.), Network of Aquaculture Centres in Asia, Rome, Italy:
Food and Agriculture Organization (FAO).
Lajus, D., Yurtseva, A., Birch, G. & Booth, D. J.
2015. Fluctuating asymmetry as a pollution monitor: the Australian estuarine smooth toadfish Tetractenos glaber (Teleostei: Tetraodontidae).
Mar. Pollut. Bull. 101(2): 758–767.
Lutterschmidt, W., Martin, S. & Schaefer, J. 2016.
Fluctuating asymmetry in two common freshwater fishes as a biological indicator of urbanization and environmental stress within the middle Chattahoochee watershed. Symmetry 8(11): 124.
Mabrouk, L., Guarred, T., Hamza, A., Messaoudi, I.
& Hellal, N. 2014. Fluctuating asymmetry in grass goby Zosterisessor ophiocephalus Pallas, 1811 inhabiting polluted and unpolluted area in Tunisia. Mar. Pollut. Bull. 85(1): 248-251.
Manthey, L. & Ousley, S. D. 2020. Geometric, Morphometrics, Statistics and Probability. In: Z.
Obertova, A. Stewart, C. Cattaneo (eds.), Forensic Anthropology, London: Academic Press.
Mehrajuddin, W., Kareem, A. & Abdulkhader, H. M.
2011. Biological diversity of the Turkish Black Sea Coast. Turkish J. Fish. Aquat. Sci. 11: 377–
383.
Michaelsen, S., Schaefer, J. & Peterson, M. S. 2015.
Fluctuating asymmetry in Menidia beryllina before and after the 2010 Deepwater Horizon Oil Spill. PLoS One 10(2): 1174–1192.
Muntaziana, A. M. S., Amin, M. N., Aminur Rahman, M. A. & Rahim, A. 2013. Present culture status of the endangered Snakehead, Channa striatus (Bloch, 1793). Asian J. Anim. Vet. Adv. 8(2): 369- 375.
Omar, W. A., Mikhail, W. Z. A., Abdo, H. M., Abou El Defan, T. A. & Poraas, M. M. 2015.
Ecological risk assessment of metal pollution along greater Cairo sector of the Nile River, Egypt, using Nile Tilapia (Oreochromis niloticus) as bioindicator. J. Toxicol. 2015: 1–11.
Panfili, J., Durand, J. D., Diop, K., Gourène, B. &
Simier, M. 2005. Fluctuating asymmetry in fish otoliths and heterozygosity in stressful estuarine environments (West Africa). Mar. Freshw. Res.
56(5): 505 - 516.
Perera, P. A. C. T., Kodithuwakku, S. P., Sundarabarathy, T. V. & Edirisinghe, U. 2015.
Bioaccumulation of cadmium in freshwater fish:
an environmental perspective. Ins. Ecol. 4(1): 1–
12.
Sharma, A. & Sachdeva, S. 2015. Cadmium toxicity and its phytoremediation: a review. Int. J. Sci.
Eng. Res. 6(9): 395–405.
Swaddle, J. P. 2003. Fluctuating Asymmetry, Animal Behavior and Evolution. In: A. Berglund, J. K.
Bester-Meredith, I. D. Couzin, S. D. Healy, G.
Heth, T. A. Hurly, J. Krause, C. A. Marler, G.
Rosenqvist, J. Todrank, B. C. Trainor & K. E.
Wynne-Edwards (eds.), Advances in the study of behavior, Massachusetts, United States:
Academic Press.
Talde, C. M., Augustus, C., Mamaril, R. & Palomares, M. L. D. 2004. The diet composition of some economically important fishes in the three floodplain lakes in Agusan Marsh wildlife sanctuary in the Philippines. Sri Lanka J. Aquat.
Sci. 9(1): 45–56.
Talpur, A. D., Munir, M. B., Mary, A. & Hashim, R.
2014. Dietary probiotics and prebiotics improved food acceptability, growth performance, haematology and immunological parameters and disease resistance against Aeromonas hydrophila in Snakehead (Channa striata) fingerlings.
Aquac. 426(427): 14–20.
Trokovic, N., Herczeg, G., Ghani, N. I. A., Shikano, T. & Merilä, J. 2012. High levels of fluctuating asymmetry in isolated stickleback populations.
BMC Evol. Biol. 12: 115.
Wilkins, N. P., Gosling, E., Curatolo, A., Linnane, A., Jordan, C. & Courtney, H. P. 1995. Fluctuating asymmetry in Atlantic salmon, European trout and their hybrids, including triploids. Aquac. 137:
77–85.
Yakupitiyage, A. 2013. On-farm Feeding and Feed Management Strategies in Tropical Aquaculture.
In: Hasan, M. R. & New, M. B. (eds.), On-farm feeding and feed management in aquaculture, FAO fisheries and aquaculture, Rome, Italy: Food and Agriculture Organization (FAO).
Zhang, Y., Lu, X., Wang, N., Xin, M., Geng, S., Jia, J.
& Meng, Q. 2016. Heavy metals in aquatic organisms of different trophic levels and their potential human health risk in Bohai Bay, China.
Env. Sci. Pollut. Res 23(17): 17801–17810.
Sharifah Musaisha Ainna Syed Mustafa Mohd Riduan Abdullah
Mohd Sham Othman
Center for Toxicology & Health Risk Studies (CORE) Faculty of Health Sciences
Universiti Kebangsaan Malaysia Wilayah Persekutuan Kuala Lumpur Malaysia
Corresponding author: Mohd Sham Othman E-mail: [email protected]
Tel.: +603-92897423 Fax: +603-26987832 Received: 26 January 2022 Revised: 25 April 2022
Accepted for publication: 25 May 2022
