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Toxic effects of arsenic on growth, hematological parameters, and plasma components of starry flounder, Platichthys stellatus, at two water temperature conditions

Toxic effects of arsenic on growth, hematological parameters, and plasma components of starry... The purpose of this study is to investigate the changes in growth, hematological parameters, and plasma components of juvenile starry flounder, Platichthys stellatus, following exposure to varying arsenic concentrations present at different water temperatures. P. stellatus (total length, 15.9 ± 0.4 cm; body weight, 62.2 ± 4.2 g) were exposed for 4 weeks to waterborne arsenic (sodium arsenite, As) at 0, 150, 300, and 600 μg/L at temperatures of 12 °C and 18 °C. Toxic effects of As exposure on P. stellatus were higher at the higher temperature and the growth and hematological parameters measured decreased with increasing arsenic concentration, while the concentration of plasma components measured increased. This indicates that waterborne As exposure and water temperature can cause toxic effects on growth, hematological parameters, and plasma components in Platichthys stellatus. Keywords: Starry flounder, Arsenic, Growth, Hematological parameters Introduction The extent of arsenic’s ability to produce toxicity in Arsenic (As) is an ubiquitous element, released into the the aquatic environment can vary depending on physio- aquatic environment through anthropogenic activities chemical characteristics such as temperature, pH, salin- such as metal smelting, chemical manufacturing, and ity, and water hardness (Min et al. 2014). Of these agriculture (Schlenk et al. 1997; Singh and Banerjee parameters, water temperature is one of the most crit- 2008). It is considered to be a toxic trace element, and ical factors for fish, because they are poikilothermic an- ecological dangers can arise if large amounts of arsenic imals and their metabolism is affected by water are released into the environment as a result of indus- temperature (Besson et al. 2016). Generally, the higher trial and agricultural activities (Canivet et al. 2001; the (water?) temperature, the faster the growth, but op- Pedlar et al. 2002). Environmental toxins can induce timal temperature for fish growth is often higher than physiological and biochemical changes in fish that lead the species’ normal body temperature.Optimal to growth inhibition (Beyers et al. 1999). Arsenic expos- temperature for growth and survival varies depending ure in the aquatic environment causes bioaccumulation on the fish species, and temperatures outside optimal in aquatic organisms and can lead to physiological and ranges can act as stressors (Handeland et al. 2008; biochemical disorders, such as poisoning, liver lesions, Chang et al. 2001). However, differences in water decreased fertility, cell and tissue damage, and cell temperature even within the optimal range can also death (Bears et al. 2006; Ribeiro et al. 2005). cause differences in metabolism, including the metabol- ism of toxins (Handeland et al. 2008). Hematologic in- * Correspondence: jckang@pknu.ac.kr dices, such as inorganic substances, organic substances, Department of Aquatic Life Medicine, Pukyong National University, Busan, and enzyme activity can be used as indicators of toxic South Korea stress (Kavitha et al. 2010). Normally, when exposed to Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Han et al. Fisheries and Aquatic Sciences (2019) 22:3 Page 2 of 8 toxic substances, hematologic levels increase or de- contamination of food waste, the aquarium completely crease beyond the normal range, enabling them to be changed the test water once every 2 days and maintained used as markers of physiological changes (Manik et al. the same concentration in each aquarium before and after 2013), and are widely used as indicators of fish health the change. The total exposure period was 4 weeks, no (Alwan et al. 2009). mortality occurred, and sampling was performed each 48 Starry flounder, P. stellatus, is commerciallly fished fishes at 2 weeks (total length, 16.56 ± 0.5 cm; body weight, offthe coastofNorth America. It livesinthe East 62.7 ± 5.3 g) and 4 weeks (total length, 17.37 ± 0.5 cm; Sea in Korea and throughout the entire North Pacific body weight, 63.35 ± 6.7 g). Ocean. The optimal temperature of the starry floun- der is 13~18 °C. At water temperatures above 20 °C, Growth performance the flounder does not take in food and its resistance The weight and length of the starry flounder were mea- becomes weak. However, because starry flounder can sured immediately before the start of the experiment and withstand low temperatures, it can feed and grow at at 2 and 4 weeks. Daily length gain, daily weight gain, con- 5 °C. Only since the late1990s have starry flounder dition factor, and feed efficiency were calculated. These been utilized to study water pollution and toxicity, so values were calculated using the following formula. there remains much to learn about their response to Daily length gain = (final length − initial length)/day environmental toxic exposure (Byun et al. 2009). Daily weight gain = (final weight − initial weight)/day According to Byun et al. (2009), it is assumed that Condition factor (%) = [weight(g)/length (cm)]× 100 there will be a physiological difference between them Feed efficiency = live weight gain/dry feed given (?) because the feed efficiency is remarkably different around 15 °C. Therefore, the temperatures studied Hematological parameters here (12 °C, 18 °C) were chosen to encompass the Blood samples were collected from the caudal vein of interval before and after 15 °C and the objective was fish using a heparinized disposable syringe (1 ml) to to evaluate the combined effect of water temperature prevent clotting. The total red blood cell (RBC) count, and arsenic exposure on hematologic health indices. hemoglobin (Hb), and hematocrit (Ht) were analyzed immediately after blood collection. The RBC counts Materials and method were counted using an optical microscope with a Experimental fish and conditions hemo-cytometer (Improved Neubauer, Germany) after Juvenile starry flounder, P. stellatus, were obtained 400 times dilution with PBS (phosphate buffer solu- from a local fish farm in Gijang, Korea. The fish were tion). The Hb concentrations were measured by the acclimated to adapt to the laboratory environment for cyan-methemoglobin technique using a clinical kit 2 weeks. The temperature was set at two sections (12 (Asan Pharm. Co., Ltd., Korea). The Ht values were ob- °C, 18 °C), and the temperature was maintained using tained by collecting blood from microhaematocrit ca- electronic thermostats (MS701-H, Mink, Korea). The pillary tubes and centrifuging at 12,000 rpm for 5 min water temperature control was also used with an elec- at 4 °C in microhematocrit centrifugation (Model; tronic thermostat, and the temperature was raised by 01501, HAWKSLEY AND SONS Ltd., England). Then, 1 °C per day to reach a final temperature of 12 °C and Ht values were measured using a reader (Micro-Haematocrit 18 °C. The amount of feed was set at 3% of the reader, HAWKSLEY AND SONS Ltd., England). weight of the fish with reference to the Byun et al. (2009) and fed once a day. After acclimation, 96 Plasma component fishes (total length, 15.9 ± 0.4 cm; body weight, 62.2 ± The collected blood was centrifuged at 3000g for 5 min 4.2 g) were randomly selected for the experiment. The at 4 °C to separate the plasma. The separated plasma arsenic experiment was performed with waterborne, samples were analyzed for changes in inorganic sub- and the exposure solution was sodium arsenite stances (ASAN Ca-Lq Reagents, Magnesium), organic (Sigma, St. Louis, MO, USA). Waterborne As expos- substances (Total protein, V-Glucose), and enzyme ure took place in 40 L aquaria containing 12 fish per activity (ASAN GOT-Lq Reagents, ASAN GPT-Lq Re- treatment group. The concentrations of arsenic were agents) using clinical kit (Asan Pharm. Co.,Ltd.). The divided into 0, 150, 300, and 600 μgper L(usingso- inorganic substances assay included calcium and magnesium. dium arsenite solution diluted in distilled water). The Calcium was analyzed by the o-cresolphthalein-complexon concentration of each tank was measured using technique, and magnesium was analyzed by the xylidyl ICP-MS, and the actual concentrations were 0.668, blue technique. The organic substances assay included 167, 312, and 626 μg/L. The ICP-MS measurements glucose and total protein. Glucose was analyzed by were performed using an ELAN 6600DRC ICP-MS in- GOD/POD technique and total protein was analyzed by strument with argon gas (Perkin-Elmer). To minimize biuret technique. The enzyme activity assay included Han et al. Fisheries and Aquatic Sciences (2019) 22:3 Page 3 of 8 glutamic oxalate transaminase (GOT) and glutamic Hematological parameters pyruvate transaminase (GPT). GOT and GPT were Change in RBC counts, hematocrit (Ht), and analyzed by Kind-King technique using clinical kit. hemoglobin (Hb) concentrations of P. stellatus are demonstrated in Fig. 2. The RBC counts were signifi- Results cantly decreased at the concentration of 600 μg/L at Growth performance 18 °C after 2 weeks and significantly decreased at the The growth factors of P. stellatus are demonstrated in concentration of 600 μg/L at 12 °C and 18 °C after 4 Fig. 1. The daily length gain was considerably decreased weeks. The Ht was significantly decreased at the con- at the concentration of 600 μg/L at 12 °C after 2 weeks centration of 600 μg/L at 18 °C after both 2 and 4 and at the concentration of 600 μg/L at 12 °C and 18 °C weeks. The Hb was a noticeable decline at the con- after 4 weeks. In daily weight gain, it was observed to centration of 600 μg/L at 18 °C after 2 weeks and was the totally same tendency as the result of the daily a noticeable decline at the concentration of over length gain. A significant decline in condition factor was 300 μg/L at 12 °C and 18 °C after 4 weeks. indicated at the concentration of 600 μg/L of all temperature and all period. The feed efficiency was notably Plasma components declined at the concentration of 600 μg/L at 12 °C after 2 The plasma inorganic substances of P. stellatus are weeks and at the concentration of 600 μg/L at 12 °C and demonstrated in Table 1 and analyzed for calcium 18 °C after 4 weeks. and magnesium. The calcium and magnesium did not 1.0 12¡É 12¡É 18¡É 18¡É 4 weeks 4 weeks 2 weeks 2 weeks 0.8 a a a a 0.6 a a a a a a a ab a ab ab a a ab 4 b ab b b 0.4 0.2 0.0 0 150 300 600 0 150 300 600 0 150 300 600 0 150 300 600 As concentration (§¶/L) As concentration (§¶/L) 3.0 2.0 12¡É 12¡É 18¡É 18¡É 2.5 4 weeks 4 weeks 2 weeks 2 weeks 1.5 2.0 a a ab a a a a a a a a 1.5 a a 1.0 a b a b b b 1.0 0.5 0.5 0.0 0.0 0 150 300 600 0 150 300 600 0 150 300 600 0 150 300 600 As concentration (§¶/L) As concentration (§¶/L) Fig. 1 Daily length gain, daily weight gain, condition factor, and feed efficiency of starry flounder, Platichthys stellatus, exposed to the different arsenic concentrations and water temperature. Values with different superscript are significantly different in 2 and 4 weeks (P < 0.05) as determined by Duncan’s multiple range test Condition factor (%) Daily length gain (mm/day) Feed efficiency Daily weight gain (mg/day) Han et al. Fisheries and Aquatic Sciences (2019) 22:3 Page 4 of 8 The plasma organic substances of P. stellatus are 12¡É demonstrated in Table 2 andanalyzedfor totalpro- 18¡É tein and glucose. Total protein was notably decreased 4 weeks 2 weeks only at the concentration of 600 μg/L at 18 °C. Glu- cose was notably increased at the concentration of ab a a a a 600 μg/L at both 12 °C and 18 °C after 2 weeks. At 4 ab a a a ab 300 ab b weeks, there was a notable increase at the concentra- tion of 600 μg/L at 12 °C and a notable increase at the concentration of over 300 μg/L at 18 °C. The plasma enzyme activity of P. stellatus are demon- strated in Table 3 and analyzed for GOT and GPT. GOT and GPT were not shown any considerable change com- pared with the control group of each temperature range 0 150 300 600 0 150 300 600 after 2 weeks, whereas, after 4 weeks, it seems to in- As concentration (§¶/L) crease overall and a considerable increase was shown at the concentration of 600 μg/L. 12¡É 18¡É 4 weeks 2 weeks Two-way ANOVA analysis Two-way ANOVA was performed to investigate the correlation between growth factor, hematological pa- rameters, and plasma components changes due to a a 30 a ab a ab water temperature and As concentration. The growth b ab factor results of two-way ANOVA are demonstrated in Table 4. The daily length gain showed significant difference only at As concentration, and daily weight gain, condition factor, and feed efficiency showed sig- nificant difference at both water temperature and As 0 150 300 600 0 150 300 600 concentration. But there were no significant interac- As concentration (§¶/L) tions between As concentration and water temperature. The hematological parameter results of the two-way 12¡É ANOVA are demonstrated in Table 5.The RBCcount 18¡É was a notable difference only at As concentration, 4 weeks 2 weeks hematocrit was a notable difference at both water temperature and As concentration, and hemoglobin was a notable difference at only As concentration. In- a a a a a a a a a a ab teractions between As concentration and water 6 b b temperature were also not significantly different in hematological parameter. The plasma component re- sults of two-way ANOVA are demonstrated in Table 6. Calcium and magnesium, the plasma inorganic sub- stances, showed no remarkable difference between water temperature and concentration. As a plasma or- 0 150 300 600 0 150 300 600 ganic substance, total protein was a remarkable differ- As concentration (§¶/L) ence at water temperature and glucose was a Fig. 2 Changes of RBC count, hematocrit, and hemoglobin in starry remarkable difference at As concentration. Among the flounder, Platichthys stellatus, exposed to the different arsenic plasma enzyme, GOT was a noticeable difference at concentrations and water temperature. Values with different water temperature and GPT was a noticeable difference superscript are significantly different in 2 and 4 weeks (P < 0.05) as at both water temperature and As concentration. Like- determined by Duncan’s multiple range test wise, interactions between As concentration and water temperature was not significant. change in all of the sections. After 4 weeks, calcium Discussion and magnesium were slightly reduced with increasing Metallic materials that enter the aquatic environment arsenic concentration, but not remarkable. accumulate in aquatic animal tissue. Aquatic animals 4 3 Hemoglobin (g/dL) Hematocrit (%) RBC count (¡¿10 mm ) Han et al. Fisheries and Aquatic Sciences (2019) 22:3 Page 5 of 8 Table 1 Changes of plasma inorganic substances in starry flounder, Platichthys stellatus exposed to the different sodium arsenate concentration and water temperature Parameters Period Temperature Arsenic concentration (μg/L) (weeks) (°C) 0 150 300 600 a a a a Calcium (mg/dL) 2 12°C 9.97±1.15 10.58±1.06 10.79±0.88 10.16±1.21 a a a a 18°C 10.14±0.72 9.74±0.70 9.92±0.82 9.05±0.64 a a a a 4 12°C 8.96±0.95 9.63±0.92 10.14±0.91 9.40±0.98 a a a a 18°C 9.85±0.70 10.19±0.80 9.58±0.85 9.01±0.75 a a a a Magnesium (mg/dL) 2 12°C 2.38±0.17 2.42±0.15 2.41±0.20 2.33±0.14 a a a a 18°C 2.41±0.24 2.42±0.21 2.38±0.16 2.27±0.20 a a a a 4 12°C 2.37±0.19 2.46±0.18 2.34±0.19 2.35±0.25 a a a a 18°C 2.33±0.17 2.21±0.16 2.25±0.18 2.19±0.19 Values are mean±S.E. Values with different superscript are significantly different at 2 weeks and 4 weeks (P < 0 .05) as determined by Duncan's multiple range test metabolize to release these metal substances, but they daily weight gain, condition factor, and feed efficiency can be toxic if not removed during metabolism (Far- were analyzed. All items showed a decrease at the highest ombi et al. 2007). The accumulation of metals such concentration and showed a larger decrease at lower tem- as arsenic affects a variety of physiological systems, peratures than at higher temperatures. In most cases, including fish growth, reproduction, immune function, there is a negative relationship between heavy metal con- and enzyme activity (Datta et al. 2009). Furthermore, centrations and fish weights, and the chronic and high changes in water temperature are able to affect fish concentrations of heavy metal toxicity are associated with metabolism, and water temperatures outside the a decrease in growth and increase in mortality (Wood- appropriate temperature range have a detrimental ef- ward et al. 1994; Hussain et al. 2010). In general, heavy fect on fish (Bagnyukova et al. 2007). In particular, metal toxicity can delay fish development, but heavy metal rising water temperature accelerates oxygen consump- toxicity such as mercury, zinc, and chromium appears to tion and metabolic rate and can cause stress and be more effective than others (Canli and Atli 2003). In this immunity degradation (Lushchak and Bagnyukova, study, the growth rate was significantly reduced in 600 μg/ 2006). Therefore, growth performance and plasma L of arsenic, all the growth values of the low temperature componentof starryflounderwereanalyzedbyar- were significantly decreased, but some growth values of senic and temperature. high temperature were not significantly decreased. The Growth is an expression of dietary intake, such as en- reason is that moderately high temperatures have in- ergy metabolism, which can determine many physiological creased growth. Universally, the higher the temperature, changes. In general, when fish are exposed to the toxicity the higher the metabolic rate, and therefore, the growth of of metals, feed intake rate and metabolic rate decrease, the feed is increased and the growth is increased (Harris resulting in a decrease in growth rate (Farkas et al. 2002; and Bodaly 1998). As a result, normal growth occurs be- Hayat et al. 2007). As a growth factor, daily length gain, cause the temperature range is within the optimal water Table 2 Changes of plasma organic substances in starry flounder, Platichthys stellatus exposed to the different sodium arsenate concentration and water temperature Parameters Period Temperature Arsenic concentration (μg/L) (weeks) (°C) 0 150 300 600 a a a a Total protein (mg/dL) 2 12°C 2.59±0.16 2.55±0.15 2.52±0.14 2.51±0.17 a a a a 18°C 2.52±0.13 2.47±0.14 2.49±0.16 2.43±0.12 a a a a 4 12°C 2.54±0.18 2.58±0.23 2.54±0.17 2.48±0.12 a ab ab b 18°C 2.55±0.16 2.41±0.15 2.36±0.19 2.14±0.22 a a a b Glucose (mg/dL) 2 12°C 92.71±7.80 95.49±8.60 96.36±7.59 111.31±5.61 a a a b 18°C 90.16±8.57 92.78±10.14 96.66±5.58 113.46±6.52 a a a b 4 12°C 88.58±5.79 92.69±8.46 96.47±8.27 114.11±9.16 a ab b b 18°C 90.63±8.09 102.62±10.14 113.11±9.97 116.14±9.00 Values are mean±S.E. Values with different superscript are significantly different at 2 weeks and 4 weeks (P < 0 .05) as determined by Duncan's multiple range test Han et al. Fisheries and Aquatic Sciences (2019) 22:3 Page 6 of 8 Table 3 Changes of plasma enzyme activity in starry flounder, Platichthys stellatus exposed to the different sodium arsenate concentration and water temperature Parameters Period Temperature Arsenic concentration (μg/L) (weeks) (°C) 0 150 300 600 a a a a GOT (karmen/ml) 2 12°C 23.28±2.59 22.58±1.76 24.27±2.13 25.51±2.69 a a a a 18°C 23.03±2.28 23.66±1.44 25.14±1.79 24.64±1.59 a a a ab 4 12°C 23.28±1.96 23.37±2.12 24.66±1.52 27.04±2.39 a a a b 18°C 23.22±1.53 23.36±1.72 26.96±2.22 28.73±2.26 a a a a GPT (karmen/ml) 2 12°C 12.39±1.35 15.50±1.93 16.65±1.82 15.60±0.94 a a a a 18°C 16.20±1.33 16.00±0.65 16.56±0.87 17.45±1.49 a a ab ab 4 12°C 16.25±1.56 16.94±2.02 19.54±1.81 18.99±1.49 a a ab b 18°C 16.41±1.87 17.15±1.89 19.81±1.90 21.07±2.27 Values are mean ±S.E. Values with different superscript are significantly different at 2 weeks and 4 weeks (P < 0 .05) as determined by Duncan's multiple range test temperature range, and heavy metal exposure tends to de- The plasma inorganic substances, calcium and magne- crease growth. For this reason, the growth values at high sium, were slightly decreased at high concentration after temperature were canceled by increases and decreases, 4 weeks, but there was no significant decrease. Plasma and therefore, no significant changes in some growth were calcium is maintained at a certain level and related to seen. However, it cannot be considered safe that no sig- various enzymatic actions. When exposed to metallic nificant changes in growth have occurred. Failure to grow substances, plasma calcium concentration decreases in a in a growth-enabling environment means that it is not a short period of time, but gradually recover to a certain safe condition (Ogata et al. 1987). level over time (Pratap et al. 1989). Calcium in this ex- The hematological characteristics of fish are used to periment was not significant but decreased overall. monitor environmental pollution in aquatic ecosystems, Therefore, the plasma calcium level is considered to and arsenic can lead to changes in hematologic character- have recovered in the short term and finally recovered, istics (Kavitha et al. 2010). Hematological parameters such and magnesium, a plasma inorganic substance, is pre- as RBC, WBC, Ht, and Hb are often used to assess the sumed to be a mechanism such as calcium. health status of fish (Carvalho and Fernandes 2006). In The plasma organic substance, total protein, was a this study, hematologic parameters such as RBC counts, notabledecreaseonlyathighconcentration after4 hematocrit (Ht), and hemoglobin (Hb) tended to decrease weeks, but glucose increased with rising concentra- overall. The striking decrease in RBC count was observed tions of arsenic in all periods and noticeably in- at the highest of concentration arsenic regardless of creased at higher concentrations. Total protein is a temperature. In the case of Ht, there was change at 12 °C biological parameter important for understanding and 18 °C high concentration section. Hemoglobin was health status and metabolism by toxic stress. De- significantly decreased at the highest concentration of ar- creased plasma protein can be a cause of protein syn- senic and high temperature. Arsenic exposure affects thesis disorder and appears to be the result of arsenic blood cells and lymphocytes because arsenic toxicity is as- accumulation in the liver (Lavanya et al. 2011). In sociated with bone marrow damage (Ferrario et al. 2008). addition, arsenic changes glucose metabolism by Such hematopoietic tissue damage may result in insuffi- changing the cellular metabolism and forming metal cient erythropoiesis and low concentration of hematocrit complexes that affect carbohydrate metabolism such and hemoglobin. In addition, arsenic-induced anemia due as glucose, glycogen, and lactate. Glucose is fre- to hemolysis of intravascular erythrocytes may also occur quently used as an indicator of environmental stress, (Cockell et al. 1991). and elevated blood glucose levels may be due to Table 4 P-values from two-way ANOVA for growth factors of starry flounder, Platichthys stellatus by As concentration and water temperature Two-way ANOVA Daily length Daily weight Condition Factor Feed Efficiency * * * Water Temperature 0.724 0.000 0.047 0.000 * * * * As Concentration 0.000 0.000 0.000 0.000 Interaction 0.799 0.607 0.937 0.604 Values are mean ± S.E. Values with asterisks are significantly different (P < 0.05) as determined by Duncan’s multiple range test Han et al. Fisheries and Aquatic Sciences (2019) 22:3 Page 7 of 8 Table 5 P-values from two-way ANOVA for hematological Abbreviations As: Arsenic; GOT: Glutamate oxalacetate transaminase; GPT: Glutamate parameters of starry flounder, Platichthys stellatus,byAs pyruvate transaminase concentration and water temperature Two-way ANOVA RBC count Hematocrit Hemoglobin Acknowledgements This research was supported by Basic Science Research Program through the Water Temperature 0.609 0.000 0.073 National Research Foundation of Korea (NRF) funded by the Ministry of * * * As Concentration 0.000 0.008 0.000 Education (2017R1D1A3B03030464). Interaction 0.906 0.078 0.291 Funding Values are mean± S.E. Values with asterisks are significantly different (P < 0.05) This study was funded by the National Institute of Fisheries Science under as determined by Duncan’s multiple range test Technology Development Program for Fisheries Research. Availability of data and materials gluconeogenesis to fulfill increased metabolic de- All datasets generated and/or analyzed during the current study are available mands by arsenic (Kavitha et al. 2010). from the corresponding author on reasonable request. Liver function tests have been used as an index of liver Authors’ contributions function changes to arsenic exposure, and plasma enzyme HJ and JH carried out the environmental toxicity studies and manuscript (GOT,GPT) analysisisone of theliver function tests writing. JM participated in the design of the study and data analysis. JC (Abdel-Hameid 2009). In this study, the plasma enzyme ac- participated in its design and coordination and helped to draft the manuscript. All authors read and approved the final manuscript. tivity such as GOT and GPT showed a considerable in- crease at high concentration after 4 weeks irrespective of Ethics approval and consent to participate temperature. Abdel-Hameid (2009) reported substantial in- All experimental animals used in this study were maintained under a protocol approved by the Institutional Animal Care and Use Committee of creases in GOT and GPT of Nile Catfish, Clarias gariepi- the Pukyong National University. nus, exposed to arsenic, and elevated levels of these parameters mayreflect liverdamagedue to arsenictoxicity. Consent for publication Not applicable. This means exposure to metal toxicity, such as arsenic, can lead to elevated plasma enzymes as a whole, and significant Competing interests increases in high concentrations of arsenic suggest that liver The authors declare that they have no competing interests. regeneration may proceed to restore GOT and GPT levels when exposed to low concentrations of arsenic (Roy and Publisher’sNote Springer Nature remains neutral with regard to jurisdictional claims in Bhattacharya, 2006). The temperature on hematological pa- published maps and institutional affiliations. rameters did not have much effect. The reason seems to be that 18 °C was not high enough to rapidly stimulate metab- Author details Department of Aquatic Life Medicine, Pukyong National University, Busan, olism to within a range of optimum water temperatures South Korea. West Sea Fisheries Research Institute, National Institute of and seems to be more influenced by As concentration. 3 Fisheries Science, Incheon, South Korea. Department of Aquaculture, Korea In this study, two-way ANOVA analysis showed no National College of Agriculture and Fisheries, Hwaseong, South Korea. significant interaction between concentration and Received: 16 October 2018 Accepted: 3 January 2019 water temperature in growth factor, hematological pa- rameters, and plasma components. The two-way References ANOVA value in growth factors and hematological Abdel-Hameid NAH. 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Toxic effects of arsenic on growth, hematological parameters, and plasma components of starry flounder, Platichthys stellatus, at two water temperature conditions

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Life Sciences; Fish & Wildlife Biology & Management; Marine & Freshwater Sciences; Zoology; Animal Ecology
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Abstract

The purpose of this study is to investigate the changes in growth, hematological parameters, and plasma components of juvenile starry flounder, Platichthys stellatus, following exposure to varying arsenic concentrations present at different water temperatures. P. stellatus (total length, 15.9 ± 0.4 cm; body weight, 62.2 ± 4.2 g) were exposed for 4 weeks to waterborne arsenic (sodium arsenite, As) at 0, 150, 300, and 600 μg/L at temperatures of 12 °C and 18 °C. Toxic effects of As exposure on P. stellatus were higher at the higher temperature and the growth and hematological parameters measured decreased with increasing arsenic concentration, while the concentration of plasma components measured increased. This indicates that waterborne As exposure and water temperature can cause toxic effects on growth, hematological parameters, and plasma components in Platichthys stellatus. Keywords: Starry flounder, Arsenic, Growth, Hematological parameters Introduction The extent of arsenic’s ability to produce toxicity in Arsenic (As) is an ubiquitous element, released into the the aquatic environment can vary depending on physio- aquatic environment through anthropogenic activities chemical characteristics such as temperature, pH, salin- such as metal smelting, chemical manufacturing, and ity, and water hardness (Min et al. 2014). Of these agriculture (Schlenk et al. 1997; Singh and Banerjee parameters, water temperature is one of the most crit- 2008). It is considered to be a toxic trace element, and ical factors for fish, because they are poikilothermic an- ecological dangers can arise if large amounts of arsenic imals and their metabolism is affected by water are released into the environment as a result of indus- temperature (Besson et al. 2016). Generally, the higher trial and agricultural activities (Canivet et al. 2001; the (water?) temperature, the faster the growth, but op- Pedlar et al. 2002). Environmental toxins can induce timal temperature for fish growth is often higher than physiological and biochemical changes in fish that lead the species’ normal body temperature.Optimal to growth inhibition (Beyers et al. 1999). Arsenic expos- temperature for growth and survival varies depending ure in the aquatic environment causes bioaccumulation on the fish species, and temperatures outside optimal in aquatic organisms and can lead to physiological and ranges can act as stressors (Handeland et al. 2008; biochemical disorders, such as poisoning, liver lesions, Chang et al. 2001). However, differences in water decreased fertility, cell and tissue damage, and cell temperature even within the optimal range can also death (Bears et al. 2006; Ribeiro et al. 2005). cause differences in metabolism, including the metabol- ism of toxins (Handeland et al. 2008). Hematologic in- * Correspondence: jckang@pknu.ac.kr dices, such as inorganic substances, organic substances, Department of Aquatic Life Medicine, Pukyong National University, Busan, and enzyme activity can be used as indicators of toxic South Korea stress (Kavitha et al. 2010). Normally, when exposed to Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Han et al. Fisheries and Aquatic Sciences (2019) 22:3 Page 2 of 8 toxic substances, hematologic levels increase or de- contamination of food waste, the aquarium completely crease beyond the normal range, enabling them to be changed the test water once every 2 days and maintained used as markers of physiological changes (Manik et al. the same concentration in each aquarium before and after 2013), and are widely used as indicators of fish health the change. The total exposure period was 4 weeks, no (Alwan et al. 2009). mortality occurred, and sampling was performed each 48 Starry flounder, P. stellatus, is commerciallly fished fishes at 2 weeks (total length, 16.56 ± 0.5 cm; body weight, offthe coastofNorth America. It livesinthe East 62.7 ± 5.3 g) and 4 weeks (total length, 17.37 ± 0.5 cm; Sea in Korea and throughout the entire North Pacific body weight, 63.35 ± 6.7 g). Ocean. The optimal temperature of the starry floun- der is 13~18 °C. At water temperatures above 20 °C, Growth performance the flounder does not take in food and its resistance The weight and length of the starry flounder were mea- becomes weak. However, because starry flounder can sured immediately before the start of the experiment and withstand low temperatures, it can feed and grow at at 2 and 4 weeks. Daily length gain, daily weight gain, con- 5 °C. Only since the late1990s have starry flounder dition factor, and feed efficiency were calculated. These been utilized to study water pollution and toxicity, so values were calculated using the following formula. there remains much to learn about their response to Daily length gain = (final length − initial length)/day environmental toxic exposure (Byun et al. 2009). Daily weight gain = (final weight − initial weight)/day According to Byun et al. (2009), it is assumed that Condition factor (%) = [weight(g)/length (cm)]× 100 there will be a physiological difference between them Feed efficiency = live weight gain/dry feed given (?) because the feed efficiency is remarkably different around 15 °C. Therefore, the temperatures studied Hematological parameters here (12 °C, 18 °C) were chosen to encompass the Blood samples were collected from the caudal vein of interval before and after 15 °C and the objective was fish using a heparinized disposable syringe (1 ml) to to evaluate the combined effect of water temperature prevent clotting. The total red blood cell (RBC) count, and arsenic exposure on hematologic health indices. hemoglobin (Hb), and hematocrit (Ht) were analyzed immediately after blood collection. The RBC counts Materials and method were counted using an optical microscope with a Experimental fish and conditions hemo-cytometer (Improved Neubauer, Germany) after Juvenile starry flounder, P. stellatus, were obtained 400 times dilution with PBS (phosphate buffer solu- from a local fish farm in Gijang, Korea. The fish were tion). The Hb concentrations were measured by the acclimated to adapt to the laboratory environment for cyan-methemoglobin technique using a clinical kit 2 weeks. The temperature was set at two sections (12 (Asan Pharm. Co., Ltd., Korea). The Ht values were ob- °C, 18 °C), and the temperature was maintained using tained by collecting blood from microhaematocrit ca- electronic thermostats (MS701-H, Mink, Korea). The pillary tubes and centrifuging at 12,000 rpm for 5 min water temperature control was also used with an elec- at 4 °C in microhematocrit centrifugation (Model; tronic thermostat, and the temperature was raised by 01501, HAWKSLEY AND SONS Ltd., England). Then, 1 °C per day to reach a final temperature of 12 °C and Ht values were measured using a reader (Micro-Haematocrit 18 °C. The amount of feed was set at 3% of the reader, HAWKSLEY AND SONS Ltd., England). weight of the fish with reference to the Byun et al. (2009) and fed once a day. After acclimation, 96 Plasma component fishes (total length, 15.9 ± 0.4 cm; body weight, 62.2 ± The collected blood was centrifuged at 3000g for 5 min 4.2 g) were randomly selected for the experiment. The at 4 °C to separate the plasma. The separated plasma arsenic experiment was performed with waterborne, samples were analyzed for changes in inorganic sub- and the exposure solution was sodium arsenite stances (ASAN Ca-Lq Reagents, Magnesium), organic (Sigma, St. Louis, MO, USA). Waterborne As expos- substances (Total protein, V-Glucose), and enzyme ure took place in 40 L aquaria containing 12 fish per activity (ASAN GOT-Lq Reagents, ASAN GPT-Lq Re- treatment group. The concentrations of arsenic were agents) using clinical kit (Asan Pharm. Co.,Ltd.). The divided into 0, 150, 300, and 600 μgper L(usingso- inorganic substances assay included calcium and magnesium. dium arsenite solution diluted in distilled water). The Calcium was analyzed by the o-cresolphthalein-complexon concentration of each tank was measured using technique, and magnesium was analyzed by the xylidyl ICP-MS, and the actual concentrations were 0.668, blue technique. The organic substances assay included 167, 312, and 626 μg/L. The ICP-MS measurements glucose and total protein. Glucose was analyzed by were performed using an ELAN 6600DRC ICP-MS in- GOD/POD technique and total protein was analyzed by strument with argon gas (Perkin-Elmer). To minimize biuret technique. The enzyme activity assay included Han et al. Fisheries and Aquatic Sciences (2019) 22:3 Page 3 of 8 glutamic oxalate transaminase (GOT) and glutamic Hematological parameters pyruvate transaminase (GPT). GOT and GPT were Change in RBC counts, hematocrit (Ht), and analyzed by Kind-King technique using clinical kit. hemoglobin (Hb) concentrations of P. stellatus are demonstrated in Fig. 2. The RBC counts were signifi- Results cantly decreased at the concentration of 600 μg/L at Growth performance 18 °C after 2 weeks and significantly decreased at the The growth factors of P. stellatus are demonstrated in concentration of 600 μg/L at 12 °C and 18 °C after 4 Fig. 1. The daily length gain was considerably decreased weeks. The Ht was significantly decreased at the con- at the concentration of 600 μg/L at 12 °C after 2 weeks centration of 600 μg/L at 18 °C after both 2 and 4 and at the concentration of 600 μg/L at 12 °C and 18 °C weeks. The Hb was a noticeable decline at the con- after 4 weeks. In daily weight gain, it was observed to centration of 600 μg/L at 18 °C after 2 weeks and was the totally same tendency as the result of the daily a noticeable decline at the concentration of over length gain. A significant decline in condition factor was 300 μg/L at 12 °C and 18 °C after 4 weeks. indicated at the concentration of 600 μg/L of all temperature and all period. The feed efficiency was notably Plasma components declined at the concentration of 600 μg/L at 12 °C after 2 The plasma inorganic substances of P. stellatus are weeks and at the concentration of 600 μg/L at 12 °C and demonstrated in Table 1 and analyzed for calcium 18 °C after 4 weeks. and magnesium. The calcium and magnesium did not 1.0 12¡É 12¡É 18¡É 18¡É 4 weeks 4 weeks 2 weeks 2 weeks 0.8 a a a a 0.6 a a a a a a a ab a ab ab a a ab 4 b ab b b 0.4 0.2 0.0 0 150 300 600 0 150 300 600 0 150 300 600 0 150 300 600 As concentration (§¶/L) As concentration (§¶/L) 3.0 2.0 12¡É 12¡É 18¡É 18¡É 2.5 4 weeks 4 weeks 2 weeks 2 weeks 1.5 2.0 a a ab a a a a a a a a 1.5 a a 1.0 a b a b b b 1.0 0.5 0.5 0.0 0.0 0 150 300 600 0 150 300 600 0 150 300 600 0 150 300 600 As concentration (§¶/L) As concentration (§¶/L) Fig. 1 Daily length gain, daily weight gain, condition factor, and feed efficiency of starry flounder, Platichthys stellatus, exposed to the different arsenic concentrations and water temperature. Values with different superscript are significantly different in 2 and 4 weeks (P < 0.05) as determined by Duncan’s multiple range test Condition factor (%) Daily length gain (mm/day) Feed efficiency Daily weight gain (mg/day) Han et al. Fisheries and Aquatic Sciences (2019) 22:3 Page 4 of 8 The plasma organic substances of P. stellatus are 12¡É demonstrated in Table 2 andanalyzedfor totalpro- 18¡É tein and glucose. Total protein was notably decreased 4 weeks 2 weeks only at the concentration of 600 μg/L at 18 °C. Glu- cose was notably increased at the concentration of ab a a a a 600 μg/L at both 12 °C and 18 °C after 2 weeks. At 4 ab a a a ab 300 ab b weeks, there was a notable increase at the concentra- tion of 600 μg/L at 12 °C and a notable increase at the concentration of over 300 μg/L at 18 °C. The plasma enzyme activity of P. stellatus are demon- strated in Table 3 and analyzed for GOT and GPT. GOT and GPT were not shown any considerable change com- pared with the control group of each temperature range 0 150 300 600 0 150 300 600 after 2 weeks, whereas, after 4 weeks, it seems to in- As concentration (§¶/L) crease overall and a considerable increase was shown at the concentration of 600 μg/L. 12¡É 18¡É 4 weeks 2 weeks Two-way ANOVA analysis Two-way ANOVA was performed to investigate the correlation between growth factor, hematological pa- rameters, and plasma components changes due to a a 30 a ab a ab water temperature and As concentration. The growth b ab factor results of two-way ANOVA are demonstrated in Table 4. The daily length gain showed significant difference only at As concentration, and daily weight gain, condition factor, and feed efficiency showed sig- nificant difference at both water temperature and As 0 150 300 600 0 150 300 600 concentration. But there were no significant interac- As concentration (§¶/L) tions between As concentration and water temperature. The hematological parameter results of the two-way 12¡É ANOVA are demonstrated in Table 5.The RBCcount 18¡É was a notable difference only at As concentration, 4 weeks 2 weeks hematocrit was a notable difference at both water temperature and As concentration, and hemoglobin was a notable difference at only As concentration. In- a a a a a a a a a a ab teractions between As concentration and water 6 b b temperature were also not significantly different in hematological parameter. The plasma component re- sults of two-way ANOVA are demonstrated in Table 6. Calcium and magnesium, the plasma inorganic sub- stances, showed no remarkable difference between water temperature and concentration. As a plasma or- 0 150 300 600 0 150 300 600 ganic substance, total protein was a remarkable differ- As concentration (§¶/L) ence at water temperature and glucose was a Fig. 2 Changes of RBC count, hematocrit, and hemoglobin in starry remarkable difference at As concentration. Among the flounder, Platichthys stellatus, exposed to the different arsenic plasma enzyme, GOT was a noticeable difference at concentrations and water temperature. Values with different water temperature and GPT was a noticeable difference superscript are significantly different in 2 and 4 weeks (P < 0.05) as at both water temperature and As concentration. Like- determined by Duncan’s multiple range test wise, interactions between As concentration and water temperature was not significant. change in all of the sections. After 4 weeks, calcium Discussion and magnesium were slightly reduced with increasing Metallic materials that enter the aquatic environment arsenic concentration, but not remarkable. accumulate in aquatic animal tissue. Aquatic animals 4 3 Hemoglobin (g/dL) Hematocrit (%) RBC count (¡¿10 mm ) Han et al. Fisheries and Aquatic Sciences (2019) 22:3 Page 5 of 8 Table 1 Changes of plasma inorganic substances in starry flounder, Platichthys stellatus exposed to the different sodium arsenate concentration and water temperature Parameters Period Temperature Arsenic concentration (μg/L) (weeks) (°C) 0 150 300 600 a a a a Calcium (mg/dL) 2 12°C 9.97±1.15 10.58±1.06 10.79±0.88 10.16±1.21 a a a a 18°C 10.14±0.72 9.74±0.70 9.92±0.82 9.05±0.64 a a a a 4 12°C 8.96±0.95 9.63±0.92 10.14±0.91 9.40±0.98 a a a a 18°C 9.85±0.70 10.19±0.80 9.58±0.85 9.01±0.75 a a a a Magnesium (mg/dL) 2 12°C 2.38±0.17 2.42±0.15 2.41±0.20 2.33±0.14 a a a a 18°C 2.41±0.24 2.42±0.21 2.38±0.16 2.27±0.20 a a a a 4 12°C 2.37±0.19 2.46±0.18 2.34±0.19 2.35±0.25 a a a a 18°C 2.33±0.17 2.21±0.16 2.25±0.18 2.19±0.19 Values are mean±S.E. Values with different superscript are significantly different at 2 weeks and 4 weeks (P < 0 .05) as determined by Duncan's multiple range test metabolize to release these metal substances, but they daily weight gain, condition factor, and feed efficiency can be toxic if not removed during metabolism (Far- were analyzed. All items showed a decrease at the highest ombi et al. 2007). The accumulation of metals such concentration and showed a larger decrease at lower tem- as arsenic affects a variety of physiological systems, peratures than at higher temperatures. In most cases, including fish growth, reproduction, immune function, there is a negative relationship between heavy metal con- and enzyme activity (Datta et al. 2009). Furthermore, centrations and fish weights, and the chronic and high changes in water temperature are able to affect fish concentrations of heavy metal toxicity are associated with metabolism, and water temperatures outside the a decrease in growth and increase in mortality (Wood- appropriate temperature range have a detrimental ef- ward et al. 1994; Hussain et al. 2010). In general, heavy fect on fish (Bagnyukova et al. 2007). In particular, metal toxicity can delay fish development, but heavy metal rising water temperature accelerates oxygen consump- toxicity such as mercury, zinc, and chromium appears to tion and metabolic rate and can cause stress and be more effective than others (Canli and Atli 2003). In this immunity degradation (Lushchak and Bagnyukova, study, the growth rate was significantly reduced in 600 μg/ 2006). Therefore, growth performance and plasma L of arsenic, all the growth values of the low temperature componentof starryflounderwereanalyzedbyar- were significantly decreased, but some growth values of senic and temperature. high temperature were not significantly decreased. The Growth is an expression of dietary intake, such as en- reason is that moderately high temperatures have in- ergy metabolism, which can determine many physiological creased growth. Universally, the higher the temperature, changes. In general, when fish are exposed to the toxicity the higher the metabolic rate, and therefore, the growth of of metals, feed intake rate and metabolic rate decrease, the feed is increased and the growth is increased (Harris resulting in a decrease in growth rate (Farkas et al. 2002; and Bodaly 1998). As a result, normal growth occurs be- Hayat et al. 2007). As a growth factor, daily length gain, cause the temperature range is within the optimal water Table 2 Changes of plasma organic substances in starry flounder, Platichthys stellatus exposed to the different sodium arsenate concentration and water temperature Parameters Period Temperature Arsenic concentration (μg/L) (weeks) (°C) 0 150 300 600 a a a a Total protein (mg/dL) 2 12°C 2.59±0.16 2.55±0.15 2.52±0.14 2.51±0.17 a a a a 18°C 2.52±0.13 2.47±0.14 2.49±0.16 2.43±0.12 a a a a 4 12°C 2.54±0.18 2.58±0.23 2.54±0.17 2.48±0.12 a ab ab b 18°C 2.55±0.16 2.41±0.15 2.36±0.19 2.14±0.22 a a a b Glucose (mg/dL) 2 12°C 92.71±7.80 95.49±8.60 96.36±7.59 111.31±5.61 a a a b 18°C 90.16±8.57 92.78±10.14 96.66±5.58 113.46±6.52 a a a b 4 12°C 88.58±5.79 92.69±8.46 96.47±8.27 114.11±9.16 a ab b b 18°C 90.63±8.09 102.62±10.14 113.11±9.97 116.14±9.00 Values are mean±S.E. Values with different superscript are significantly different at 2 weeks and 4 weeks (P < 0 .05) as determined by Duncan's multiple range test Han et al. Fisheries and Aquatic Sciences (2019) 22:3 Page 6 of 8 Table 3 Changes of plasma enzyme activity in starry flounder, Platichthys stellatus exposed to the different sodium arsenate concentration and water temperature Parameters Period Temperature Arsenic concentration (μg/L) (weeks) (°C) 0 150 300 600 a a a a GOT (karmen/ml) 2 12°C 23.28±2.59 22.58±1.76 24.27±2.13 25.51±2.69 a a a a 18°C 23.03±2.28 23.66±1.44 25.14±1.79 24.64±1.59 a a a ab 4 12°C 23.28±1.96 23.37±2.12 24.66±1.52 27.04±2.39 a a a b 18°C 23.22±1.53 23.36±1.72 26.96±2.22 28.73±2.26 a a a a GPT (karmen/ml) 2 12°C 12.39±1.35 15.50±1.93 16.65±1.82 15.60±0.94 a a a a 18°C 16.20±1.33 16.00±0.65 16.56±0.87 17.45±1.49 a a ab ab 4 12°C 16.25±1.56 16.94±2.02 19.54±1.81 18.99±1.49 a a ab b 18°C 16.41±1.87 17.15±1.89 19.81±1.90 21.07±2.27 Values are mean ±S.E. Values with different superscript are significantly different at 2 weeks and 4 weeks (P < 0 .05) as determined by Duncan's multiple range test temperature range, and heavy metal exposure tends to de- The plasma inorganic substances, calcium and magne- crease growth. For this reason, the growth values at high sium, were slightly decreased at high concentration after temperature were canceled by increases and decreases, 4 weeks, but there was no significant decrease. Plasma and therefore, no significant changes in some growth were calcium is maintained at a certain level and related to seen. However, it cannot be considered safe that no sig- various enzymatic actions. When exposed to metallic nificant changes in growth have occurred. Failure to grow substances, plasma calcium concentration decreases in a in a growth-enabling environment means that it is not a short period of time, but gradually recover to a certain safe condition (Ogata et al. 1987). level over time (Pratap et al. 1989). Calcium in this ex- The hematological characteristics of fish are used to periment was not significant but decreased overall. monitor environmental pollution in aquatic ecosystems, Therefore, the plasma calcium level is considered to and arsenic can lead to changes in hematologic character- have recovered in the short term and finally recovered, istics (Kavitha et al. 2010). Hematological parameters such and magnesium, a plasma inorganic substance, is pre- as RBC, WBC, Ht, and Hb are often used to assess the sumed to be a mechanism such as calcium. health status of fish (Carvalho and Fernandes 2006). In The plasma organic substance, total protein, was a this study, hematologic parameters such as RBC counts, notabledecreaseonlyathighconcentration after4 hematocrit (Ht), and hemoglobin (Hb) tended to decrease weeks, but glucose increased with rising concentra- overall. The striking decrease in RBC count was observed tions of arsenic in all periods and noticeably in- at the highest of concentration arsenic regardless of creased at higher concentrations. Total protein is a temperature. In the case of Ht, there was change at 12 °C biological parameter important for understanding and 18 °C high concentration section. Hemoglobin was health status and metabolism by toxic stress. De- significantly decreased at the highest concentration of ar- creased plasma protein can be a cause of protein syn- senic and high temperature. Arsenic exposure affects thesis disorder and appears to be the result of arsenic blood cells and lymphocytes because arsenic toxicity is as- accumulation in the liver (Lavanya et al. 2011). In sociated with bone marrow damage (Ferrario et al. 2008). addition, arsenic changes glucose metabolism by Such hematopoietic tissue damage may result in insuffi- changing the cellular metabolism and forming metal cient erythropoiesis and low concentration of hematocrit complexes that affect carbohydrate metabolism such and hemoglobin. In addition, arsenic-induced anemia due as glucose, glycogen, and lactate. Glucose is fre- to hemolysis of intravascular erythrocytes may also occur quently used as an indicator of environmental stress, (Cockell et al. 1991). and elevated blood glucose levels may be due to Table 4 P-values from two-way ANOVA for growth factors of starry flounder, Platichthys stellatus by As concentration and water temperature Two-way ANOVA Daily length Daily weight Condition Factor Feed Efficiency * * * Water Temperature 0.724 0.000 0.047 0.000 * * * * As Concentration 0.000 0.000 0.000 0.000 Interaction 0.799 0.607 0.937 0.604 Values are mean ± S.E. Values with asterisks are significantly different (P < 0.05) as determined by Duncan’s multiple range test Han et al. Fisheries and Aquatic Sciences (2019) 22:3 Page 7 of 8 Table 5 P-values from two-way ANOVA for hematological Abbreviations As: Arsenic; GOT: Glutamate oxalacetate transaminase; GPT: Glutamate parameters of starry flounder, Platichthys stellatus,byAs pyruvate transaminase concentration and water temperature Two-way ANOVA RBC count Hematocrit Hemoglobin Acknowledgements This research was supported by Basic Science Research Program through the Water Temperature 0.609 0.000 0.073 National Research Foundation of Korea (NRF) funded by the Ministry of * * * As Concentration 0.000 0.008 0.000 Education (2017R1D1A3B03030464). Interaction 0.906 0.078 0.291 Funding Values are mean± S.E. Values with asterisks are significantly different (P < 0.05) This study was funded by the National Institute of Fisheries Science under as determined by Duncan’s multiple range test Technology Development Program for Fisheries Research. Availability of data and materials gluconeogenesis to fulfill increased metabolic de- All datasets generated and/or analyzed during the current study are available mands by arsenic (Kavitha et al. 2010). from the corresponding author on reasonable request. Liver function tests have been used as an index of liver Authors’ contributions function changes to arsenic exposure, and plasma enzyme HJ and JH carried out the environmental toxicity studies and manuscript (GOT,GPT) analysisisone of theliver function tests writing. JM participated in the design of the study and data analysis. JC (Abdel-Hameid 2009). In this study, the plasma enzyme ac- participated in its design and coordination and helped to draft the manuscript. All authors read and approved the final manuscript. tivity such as GOT and GPT showed a considerable in- crease at high concentration after 4 weeks irrespective of Ethics approval and consent to participate temperature. Abdel-Hameid (2009) reported substantial in- All experimental animals used in this study were maintained under a protocol approved by the Institutional Animal Care and Use Committee of creases in GOT and GPT of Nile Catfish, Clarias gariepi- the Pukyong National University. nus, exposed to arsenic, and elevated levels of these parameters mayreflect liverdamagedue to arsenictoxicity. Consent for publication Not applicable. This means exposure to metal toxicity, such as arsenic, can lead to elevated plasma enzymes as a whole, and significant Competing interests increases in high concentrations of arsenic suggest that liver The authors declare that they have no competing interests. regeneration may proceed to restore GOT and GPT levels when exposed to low concentrations of arsenic (Roy and Publisher’sNote Springer Nature remains neutral with regard to jurisdictional claims in Bhattacharya, 2006). The temperature on hematological pa- published maps and institutional affiliations. rameters did not have much effect. The reason seems to be that 18 °C was not high enough to rapidly stimulate metab- Author details Department of Aquatic Life Medicine, Pukyong National University, Busan, olism to within a range of optimum water temperatures South Korea. West Sea Fisheries Research Institute, National Institute of and seems to be more influenced by As concentration. 3 Fisheries Science, Incheon, South Korea. Department of Aquaculture, Korea In this study, two-way ANOVA analysis showed no National College of Agriculture and Fisheries, Hwaseong, South Korea. significant interaction between concentration and Received: 16 October 2018 Accepted: 3 January 2019 water temperature in growth factor, hematological pa- rameters, and plasma components. The two-way References ANOVA value in growth factors and hematological Abdel-Hameid NAH. 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Fisheries and Aquatic SciencesSpringer Journals

Published: Jan 30, 2019

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