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Copyright © 2022 Faculty of Health Science UKM. All right reserved Artikel Asli/Original Article
Fluctuating Asymmetry of the Paired Barbels and Fins of a Clarias gariepinus Exposed to Different Levels
of Cadmium Concentrations
Asimetri Turun Naik Barbel dan Sirip Berpasangan pada Clarias gariepinus setelah Didedahkan kepada Pelbagai Kepekatan Kadmium
MOHD SHAM OTHMAN, NUR THAHIRAH ZAKARIA, FATIN NOR’SYAHIRA MOHAMMAD ISA KHAN & MOHD RIDUAN ABDULLAH
ABSTRACT
This study was conducted to determine the impact of cadmium exposure on the fluctuating asymmetries of paired barbels and fins of a sentinel species, the African catfish (Clarias gariepinus). Fluctuating asymmetries of the nasal barbel, outer mandibular barbel, maxillary barbel, inner mandibular barbel, pectoral fin, and ventral fin were compared between fishes exposed to different cadmium levels and at different exposure durations. The fishes were exposed to four concentrations of cadmium (control, 0.005 mg/L, 0.010 mg/L, and 0.015 mg/L) for three months. The lengths of the barbels and fins were measured monthly. The result showed significant increases in fluctuating asymmetries of the fins and barbels except for the inner mandibular barbels. This research concluded that exposure to different cadmium concentrations and over different exposure times would increase fluctuating asymmetry, hence signifying the effect of cadmium exposure on developmental instability in a sentinel species. This study implied that paired barbels and fins fluctuating asymmetries can be used as an indicator to monitor the effect of environmental cadmium on C. gariepinus. Further research should be conducted to determine how fluctuating asymmetry would alter the sensory and locomotive behaviors of C.
gariepinus.
Keywords: Sentinel species, Clarias gariepinus, fluctuating asymmetry, barbel, fin, cadmium
ABSTRAK
Kajian ini dijalankan bagi menentukan impak dedahan cadmium terhadap asimetri turun naik barbel dan sirip berpasangan pada spesies sentinel, Keli Afrika (Clarius gariepinus). Asimetri turun naik barbel nasal, barbel mandibel luar, barbel maksilari, barbel mandibel dalam, sirip pektoral, dan sirip ventral telah dibandingkan antara ikan yang terdedah pada kepekatan dan tempoh dedahan cadmium. Ikan-ikan tersebut telah didedahkan kepada emepat kepekatan cadmium (kawalan, 0.005 mg/L, 0.010 mg/L, dan 0.015 mg/L) selama tiga bulan.
Panjang barbel dan sirip diukur setiap bulan. Hasil menunjukkan peningkatan signifikan asimetri turun naik pada sirip dan barbel, kecuali barbel mandibel dalam. Kajian ini merumuskan dedahan kepada pelbagai kepekatan cadmium dan pada tempoh yang berbeza akan meningkatkan asimetri turun naik, lantas mengukuhkan kesan dedahan cadmium terhadap ketidakstabilan perkembangan pada spesies sentinel. Kajian ini memberi gambaran bahawa barbel dan sirip berpasangan boleh digunakan sebagai petunjuk untuk memonitor kesan cadmium persekitaran terhadap C. gariepinus. Kajian lanjutan perlu dijalankan bagi menentukan bagaimana asimetri turun naik boleh mengubah sensori dan tingkahlaku lokomotif pada C. gariepinus.
Kata kunci: Spesies sentinel, Clarias gariepinus, asimetri turun naik, barbel, sirip, kadmium
INTRODUCTION
The presence of heavy metals including cadmium in the environment and their accumulation in fish and other organisms has been reported in many works of literature (Chahid et al. 2014; Olmedo et al. 2013;
Rajeshkumar & Li 2018). Cadmium has the ability to be bioaccumulated in the various organs in an aquatic
animal such as the liver (Othman et al. 2012) and kidney (Othman et al. 2009). Even at low concentrations, heavy metals in the environment may threaten the health of an organism (Olmedo et al.
2013: Ghazali et al. 2019). This is further supported by Pereira et al. (2016) stating that low concentrations of cadmium have the ability to produce alterations in the physiology and
morphology of freshwater fish. This makes heavy metals, including cadmium some of the common stressors that produce fluctuating asymmetry levels (Almeida et al. 2008). In a study on channel catfish, Paul & Small (2019) reported that exposure to cadmium from the early stage of life would negatively affect development and lead to shifts in life-history patterns in exposed populations. In another study, Othman et al. (2017) reported that low-level cadmium exposure is shown to induce developmental instability by increasing pectoral fin fluctuating asymmetry in Oreochromis mossambicus X O. niloticus.
Developmental instability is one of the effects of pollution on an organism. According to Van Dongen & Gangestad (2011), developmental instability reflects the inability of a developing organism to buffer its development against random genetic or environmental perturbations. It is suggested that fluctuating asymmetry (FA) is used as a primary indicator to measure an organism’s developmental instability. Seixas et al. (2016) described fluctuating asymmetry as random morphologic changes on the bilateral symmetry plan of paired morphometric and meristic characters in response to environmental disturbances. The closer the value of FA to zero, the more symmetrical the structure is. This means that the paired morphometric or meristic characters with zero FA may have developed in perfect equilibrium. Since a number of morphological body structures occur in pairs, therefore there are various avenues where fluctuating asymmetry could be measured in an organism.
In order to determine developmental instability, fluctuating asymmetry measures the small random deviation from the perfect symmetry of paired organs (Tomkins & Kotiaho 2002) such as barbels and fins.
Therefore, it is an assessment tool that has the potential to appraise the state of adaptation of an individual or a population before environmental stressors affect the whole community or ecosystem (Seixas et al. 2016). This is further supported by Beasley et al. (2013) who found that fluctuating asymmetry is a sensitive biomarker of environmental stress. This would make it a legitimate tool to verify the biological relevance of stressors for the study organism. Despite that, Vandenbussche et al. (2018) hypothesized that a high environmental disturbance level is needed to induce significant fluctuating asymmetry variations. However, fluctuating asymmetry is still very relevant in assessing the impact of environmental stressors on an organism. In fact, Guo et al. (2017) suggested that fluctuating asymmetry is more suitable and accurate in measuring the impact of environmental stressors as compared to oxidative stress.
Fish has been extensively studied as a sentinel species for cadmium contamination (Rosli et al. 2018;
Bashir et al. 2013; Ahmad et al. 2009; Yasir et al.
2008; Mohamed et al. 2006). In this study, Clarias
gariepinus (African catfish) has been chosen to be a sentinel species for cadmium contamination based on a few criteria, including a) not threatened by extinction b) ubiquitous c) suitable size d) has a large distribution area and e) has a stable population (Froese & Pauly 2019). This study aimed to measure fluctuation asymmetries of paired barbels and fins of C. gariepinus exposed to various cadmium concentrations.
EXPERIMENTAL METHODS
African catfish (C. gariepinus) fingerlings, with an average length of 8 cm were acclimatized to laboratory conditions for three days in dechlorinated tap water before treatment. The fingerlings were then divided into four exposure groups (n=30 for every exposure group) according to four cadmium concentrations; 0 mg/L (control), 0.005 mg/L (low exposure), 0.010 mg/L (medium exposure) and 0.015 mg/L (high exposure) for three months. Low, medium, and high exposure was determined based on the permissible limit of cadmium in natural water which is 0.010 mg/L. Commercial fish food was given ad libitum (Muntaziana et al. 2013) once a day but the total daily feed did not exceed the recommended feeding rate of 3% of the body weight (Hecht 2013). Excess leftover feed was removed after feeding and water change was carried out every two weeks to ensure water quality was suitable for fish without affecting the condition. The fish were sampled and measured monthly. The length of both left and right paired external structures were measured and based on these measurements, their fluctuating asymmetries were determined. The paired structures included nasal barbels, outer mandibular barbels, maxillary barbels, inner mandibular barbels, pectoral fins, and ventral fins. Fluctuating asymmetry is measured as the percentage of measurement deviation of a paired structure from the average values. The Kruskal-Wallis test was performed to determine the significance of the FA differences according to cadmium concentrations and exposure duration.
RESULTS AND DISCUSSION
Fig. 1 showed the change in the trend of fluctuating asymmetries of paired barbels of C.
gariepinus exposed to various levels of cadmium concentrations over three months. Significant differences (P,0.05) in FA over exposure time were found in the nasal barbel (medium exposure group), outer mandible barbel (low and medium exposure group), maxillary barbell (low exposure group), and outer maxillary barbell (medium exposure group).
FIGURE 1 Fluctuating asymmetries of a) Nasal barbel; b) Outer mandibular barbel; c) maxillary barbel and d) Inner mandibular barbel of C. gariepinus exposed to various cadmium concentrations over 3 months of exposure. Significant differences (P <0.05) in FA over exposure time were found in the nasal barbel (0.01 mg/L group), outer mandible barbel (0.005 mg/L and 0.01 mg/L groups), maxillary barbell (0.0005 mg/L group), and outer maxillary barbell (0.001 mg/L group)
The results showed the levels of fluctuating asymmetries increase in all exposure concentration levels. However, control groups showed the lowest increase in all barbels while the high exposure group showed high FA throughout the exposure time. This showed that the longer the fish is exposed to cadmium, the higher the fluctuating asymmetry, hence the higher the developmental instability. It is also noted that higher exposure concentration would result in higher fluctuating asymmetry. This is also illustrated in Fig. 2 where the fluctuating values of nasal, outer mandibular, mandibular and inner mandibular barbels were higher in the high-exposure group compared to the control group.
Fig. 3 showed the fluctuating asymmetries of the paired fins, the pectoral and ventral fins of C.
gariepinus exposed to various cadmium concentration levels for three months. Unlike the trend in paired barbels, both paired pectoral and ventral showed similar patterns. The fins in the high-exposure groups showed a higher degree of fluctuating asymmetry in every sampling month
while those from the control group showed the lowest FA values. This trend is also supported by the higher average fluctuating asymmetries of both fins in the high-exposure group as compared to the other group, as shown in Fig. 4.
In this study, we were trying to find the effect of cadmium exposure on the developmental stability of a sentinel species. The purpose of this is that any changes in developmental stability could reflect the inability of the species to maintain developmental stability (Van Dongen & Gangestad 2011) hence showing how environmental stress could affect morphometric anomaly. This reiterates how C.
gariepinus in this study has a lowered ability to maintain homeostasis when facing stress as suggested by Moller (2006) thus contributing to higher levels of fluctuating asymmetry in the paired barbels and fins. Almeida et al. (2008) stated that the degree of FA reflects the inability of individuals to maintain homeostasis during development when faced with stress, either genetic or environmental.
0 5 10 15 20 25
Month 1 Month 2 Month 3
Fluctuating Asymmetry (%)
Exposure time
Control 0.005
0.01 0.015
0 5 10 15 20 25
Month 1 Month 2 Month 3
Fluctuating Asymmetry (%)
Exposure time
Control 0.005
0.01 0.015
0 5 10 15 20 25
Month 1 Month 2 Month 3
Fluctuating Asymmetry (%)
Exposure time
Control 0.005
0.01 0.015
(
c
)0 5 10 15 20 25
Month 1 Month 2 Month 3
Fluctuatinf Asymmetry (%)
Exposure time
Control 0.005
0.01 0.015
(d)
(a) (b)
FIGURE 2 Average fluctuating asymmetries of a) Nasal barbel; b) Outer mandibular barbel; c) maxillary barbel and d) Inner mandibular barbel of C. gariepinus exposed to various cadmium concentrations.
Significant differences (P,0.05) of FA was observed in nasal barbel, outer mandibular barbel and maxillary barbell.
Increased fluctuating asymmetries were also observed by Monaliza et al. (2014) in Gafrarium tumidun after being exposed to environmental stress.
A few other studies also found exposure to environmental stressors would lead to increased fluctuating asymmetry in fish. Exposure to environmental stressors was found to cause increased fluctuating asymmetry in Poecilla reticulata (Sheridan & Pomiankowski, 1996) Oreochromis niloticus (Peligro & Jumawan, 2006), Orthopristis ruber (Seixas et al. 2016) Oreochromis mossambicus X Orechromis niloticus (Othman et al. 2017), Lepomis sp. (Lutterschmidt et al. 2016), Zosterisessor ophiocephalus (Gharred et al. 2017) and Menidia beryllina (Michaelsen et al. 2015).
Therefore, environmental stress, including exposure to cadmium, does affect the fluctuating asymmetry of an organism. Even though the findings by Lajus et al.
(2015) showed that FA of Tetractenos glaber was not positively correlated with heavy metal levels, including cadmium, our study found the opposite.
0 5 10 15 20 25
Control 0.005 0.01 0.015
Average Fluctuating Asymmetry/%
Exposure group/mgL-1
0 5 10 15 20 25
Control 0.005 0.01 0.015
Average Fluctuating Asymmetry/%
Exposure group/mgL-1 0
5 10 15 20 25
Control 0.005 0.01 0.015
Average Fluctuating Asymmetry/%
Exposure group/mgL-1
0 5 10 15 20 25
Control 0.005 0.01 0.015
Average Fluctuating Asymmetry/%
Exposure group/mgL-1
(a) (b)
(b)
(c) (c)
(d)
FIGURE 3 Fluctuating asymmetries of a) Pectoral fin and b) Ventral fin of C. gariepinus exposed to various cadmium concentrations over 3 months of exposure. No significant difference was found in the FA of pectoral fins. However, there was a significant (p<0.05) difference in the FA of ventral fins at the 0.005 mg/L and 0.01 mg/L exposure groups.
FIGURE 4 Average fluctuating asymmetries of a) Pectoral fin and b) Ventral fin of C. gariepinus exposed to various cadmium concentrations. Significant differences (P,0.05) of FA were observed for both pectoral and ventral fins.
Another issue addressed in this study is how the length of exposure time would affect fluctuating asymmetry. We found that a longer time of exposure would result in higher FA values. The increase was exhibited in all paired barbels and fins. This is in line with a study by Trono et al. (2015) in which they found that the fluctuating asymmetry of Protoreaster nodosus living in an impacted area showed an increasing FA trend over time.
Increased fluctuating asymmetries of the paired structures could lead to various morphological and behavioral impacts on a sentinel species. Peligro
(2006) stated that fluctuating asymmetry of structure in the head region is commonly higher than the other body part of fish. This would impact the fish’s movement because the head is an important part of locomotive behavior. Based on histological evidence in their studies, Ikpegbu & Nlebedum (2015) suggests that the barbels will aid guide the fish in movement especially in avoiding obstacles and predators and help in food search and selection through gustation. Asymmetry of the paired fins would also hamper movement and locomotive behavior. According to Almeida et al. (2007), 0
5 10 15 20 25
Control 0.005 0.01 0.015
Average Fluctuating Asymmetry%
Exposure time/mgL-1
0 5 10 15 20 25
Control 0.005 0.01 0.015
Average Fluctuating Asymmetry%
Exposure group/mgL-1 0
5 10 15 20 25
Month 1 Month 2 Month 3
AvergaeFluctuating Asymmetry/%
Exposure time
Control 0.005
0.01 0.015
0 5 10 15 20 25
Month 1 Month 2 Month 3
Average Fluctuating Asymmetry%
Exposure time
Control 0.005
0.01 0.015
(a) (b)
(a) (b)
asymmetry in functionally important traits for fish such as fins probably makes locomotion less efficient, as has been observed in some animals. Apart from that, they reiterated that environmental stress can give rise to developmental instability of individuals resulting in reduced performance of fitness components. In conclusion, exposure to cadmium affects fluctuating asymmetry of the paired barbels and fins which would result in developmental instability. This in turn will affect movement and locomotive behavior. Therefore, increased fluctuating asymmetry may be used as an indicator of poor body condition as a result of exposure to cadmium.
CONCLUSION
This research found that C. gariepinus exposed to various concentrations of cadmium resulted in the fluctuating asymmetry of various paired external structures. We documented increased fluctuating asymmetries (FA) of the paired barbels (nasal, outer mandibular, maxillary, and inner mandibular barbels) and paired fins (pectoral and ventral fins) in the high exposure group as compared to other exposure groups. We also found that the longer the exposure duration, the higher the FA recorded for all paired barbels and fins. It is imperative that further research be conducted to determine how fluctuating asymmetry would alter the sensory and locomotive behaviors of C. gariepinus.
ACKNOWLEDGEMENT
The author(s) would like to thank Environmental Health and Industrial Safety Program, Faculty of Health Sciences, and The Center for Toxicology &
Health Risk Assessment, Universiti Kebangsaan Malaysia for research support.
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Mohd Sham Othman Nur Thahirah Zakaria
Fatin Nor’Syahira Mohammad Isa Khan Mohd Riduan Abdullah
Center for Toxicology & Health Risk Assessment Faculty of Health Sciences
Universiti Kebangsaan Malaysia Wilayah Persekutuan Kuala Lumpur Malaysia
*Corresponding Author: Mohd Sham Othman E-mail: [email protected]
Tel: +6017-2968561 Fax: +603-26914304 Received: 26 January 2022 Revised: 10 November 2022
Accepted for publication: 12 December 2022