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Responses of Takifugu obscurus fertilized eggs and larvae to increased ammonia exposure

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Abstract

Ammonia is a common toxicant in aquatic systems; this substance has become a critical threat to fish, especially in early life stages. This study aimed to evaluate the effects of unionized ammonia (NH3-N: 0, 0.068, 0.138, 0.206, 0.275, 0.343, 0.412, and 0.481 mg L−1) on fertilized eggs and larvae of obscure puffer Takifugu obscurus, a fish species with potential economic value. Results showed that hatch time was significantly retarded and hatch rate was significantly decreased as NH3-N concentrations increased; newly hatched larvae exhibited high rate of abnormalities and low viability. The survival rate of larvae also decreased significantly as NH3-N concentrations increased; larvae could tolerate NH3-N to a less extent than embryos. NH3-N also caused a significant decrease in superoxide dismutase (SOD) and Na+/K+ ATPase activities but not in malondialdehyde (MDA) levels of larvae. Two-way ANOVA indicated that there was a statistically significant interaction between NH3-N concentrations and exposure times on SOD activity but not on Na+/K+ ATPase activity. Such responses indicated that an increase in ammonia concentration in surface water may negatively affect the early development of T. obscurus and thus likely impair population recruitment and persistence of this fish species.

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References

  • Amado LL, Monserrat JM (2010) Oxidative stress generation by microcystins in aquatic animals: why and how. Environ Int 36:226–235

    Article  CAS  Google Scholar 

  • Arillo A, Margiocco C, Melodia F, Mensi P, Schenone G (1981) Ammonia toxicity mechanism in fish: studies on rainbow trout (Salmo gairdneri Rich.). Ecotoxicol Environ Saf 5:316–328

    Article  CAS  Google Scholar 

  • Barimo JF, Walsh PJ (2005) The effects of acute and chronic ammonia exposure during early life stages of the gulf toadfish, Opsanus beta. Aquat Toxicol 75:225–237

    Article  CAS  Google Scholar 

  • Benli AÇK, Köksal G, Özkul A (2008) Sublethal ammonia exposure of Nile tilapia (Oreochromis niloticus L.): effects on gill, liver and kidney histology. Chemosphere 72:1355–1358

    Article  CAS  Google Scholar 

  • Boardman GD, Starbuck SM, Hudgins DB, Li X, Kuhn DD (2004) Toxicity of ammonia to three marine fish and three marine invertebrates. Environ Toxicol 19:134–142

    Article  CAS  Google Scholar 

  • Broderius S, Drummond R, Fiandt J, Russom C (1985) Toxicity of ammonia to early life stages of the smallmouth bass at four pH values. Environ Toxicol Chem 4:87–96

    Article  CAS  Google Scholar 

  • Burkhalter DE, Kaya CM (1977) Effects of prolonged exposure to ammonia on fertilized eggs and sac fry of rainbow trout (Salmo gairdneri). Trans Am Fish Soc 106:470–475

    Article  CAS  Google Scholar 

  • Camargo JA, Alonso Á (2006) Ecological and toxicological effects of inorganic nitrogen pollution in aquatic ecosystems: a global assessment. Environ Int 32:831–849

    Article  CAS  Google Scholar 

  • Chen J, Kou Y (1993) Accumulation of ammonia in the haemolymph of Penaeus monodon exposed to ambient ammonia. Aquaculture 109:177–185

    Article  CAS  Google Scholar 

  • Chen YF, Sun HJ, Yang W, Yang Z (2011) Oxidative stress responses of grass carp Ctenopharyngodon idella larvae exposed to purified microcystin under different ammonia concentrations. Fresenius Environ Bull 20:2869–2874

    CAS  Google Scholar 

  • Chen YF, Sun HJ, Yang W, Yang Z (2012) Incubation and oxidative stress of grass carp (Ctenopharyngodon idella) embryos exposed to different un-ionized ammonia levels. J Freshw Ecol 27:143–150

    Article  CAS  Google Scholar 

  • Chen YF, Li JJ, Sun HJ, Yang Z (2013) Dose-dependent effect of un-ionized ammonia on hatching success of fertilized eggs of silver carp Hypophthalmichthys molitrix and bighead carp Hypophthalmichthys nobilis. J Freshw Ecol 28:39–46

    Article  CAS  Google Scholar 

  • Chew S, Jin Y, Ip Y (2001) The loach Misgurnus anguillicaudatus reduces amino acid catabolism and accumulates alanine and glutamine during aerial exposure. Physiol Biochem Zool 74:226–237

    Article  CAS  Google Scholar 

  • Ching B, Chew S, Wong W, Ip Y (2009) Environmental ammonia exposure induces oxidative stress in gills and brain of Boleophthalmus boddarti (mudskipper). Aquat Toxicol 95:203–212

    Article  CAS  Google Scholar 

  • de la Torre F, Salibián A, Ferrari L (2007) Assessment of the pollution impact on biomarkers of effect of a freshwater fish. Chemosphere 68:1582–1590

    Article  Google Scholar 

  • Doyotte A, Cossu C, Jacquin M-C, Babut M, Vasseur P (1997) Antioxidant enzymes, glutathione and lipid peroxidation as relevant biomarkers of experimental or field exposure in the gills and the digestive gland of the freshwater bivalve Unio tumidus. Aquat Toxicol 39:93–110

    Article  CAS  Google Scholar 

  • Eddy F (2005) Ammonia in estuaries and effects on fish. J Fish Biol 67:1495–1513

    Article  CAS  Google Scholar 

  • Emerson K, Russo RC, Lund RE, Thurston RV (1975) Aqueous ammonia equilibrium calculations: effect of pH and temperature. J Fish Res Board Can 32:2379–2383

    Article  CAS  Google Scholar 

  • Hung CC, Nawata CM, Wood CM, Wright PA (2008) Rhesus glycoprotein and urea transporter genes are expressed in early stages of development of rainbow trout (Oncorhynchus mykiss). J Exp Zool A 309:262–268

    Article  Google Scholar 

  • Ip YK, Chew SF (2010) Ammonia production, excretion, toxicity, and defense in fish: a review. Front Physiol 1:134

    Article  CAS  Google Scholar 

  • Ip YK, Chew SF, Randall DJ (2001) Ammonia toxicity, tolerance, and excretion. In: Wright P, Anderson P (eds) Fish physiol. Academic Press, New York, pp 109–148

    Google Scholar 

  • Ip YK, Chew SF, Randall DJ (2004a) Five tropical air‐breathing fishes, six different strategies to defend against ammonia toxicity on land. Physiol Biochem Zool 77:768–782

    Article  CAS  Google Scholar 

  • Ip YK, Tay AS, Lee KH, Chew SF (2004b) Strategies for surviving high concentrations of environmental ammonia in the swamp eel Monopterus albus. Physiol Biochem Zool 77:390–405

    Article  CAS  Google Scholar 

  • Ip YK, Leong MW, Sim M, Goh GS, Wong WP, Chew SF (2005) Chronic and acute ammonia toxicity in mudskippers, Periophthalmodon schlosseri and Boleophthalmus boddaerti: brain ammonia and glutamine contents, and effects of methionine sulfoximine and MK801. J Exp Biol 208:1993–2004

    Article  CAS  Google Scholar 

  • Kamler E (2002) Ontogeny of yolk-feeding fish: an ecological perspective. Rev Fish Biol Fish 12:79–103

    Article  Google Scholar 

  • Kato A, Doi H, Nakada T, Sakai H, Hirose S (2005) Takifugu obscurus is a euryhaline fugu species very close to Takifugu rubripes and suitable for studying osmoregulation. BMC Physiol 5:18

    Article  Google Scholar 

  • Le Ruyet JP, Boeuf G, Infante JZ, Helgason S, Le Roux A (1998) Short-term physiological changes in turbot and seabream juveniles exposed to exogenous ammonia. Comp Biochem Physiol A 119:511–518

    Article  Google Scholar 

  • Lease HM, Hansen JA, Bergman HL, Meyer JS (2003) Structural changes in gills of lost river suckers exposed to elevated pH and ammonia concentrations. Comp Biochem Physiol C 134:491–500

    Google Scholar 

  • Lee C-H, Sung C-G, Moon S-D, Lee J-H (2013) Effects of ammonia on fertilization, development, and larval survival in the northern pacific asteroid, Asterias amurensis. Bull Environ Contam Toxicol 91:102–106

    Article  CAS  Google Scholar 

  • Leibovitz BE, Siegel BV (1980) Aspects of free radical reactions in biological systems: aging. J Gerontol 35:45–56

    Article  CAS  Google Scholar 

  • Lim CB, Chew SF, Anderson PM, Ip YK (2001) Mudskippers reduce the rate of protein and amino acid catabolism in response to terrestrial exposure. J Exp Biol 204:1605–1614

    CAS  Google Scholar 

  • Livingstone D, Martinez PG, Michel X, Narbonne J, O’hara S, Ribera D, Winston G (1990) Oxyradical production as a pollution-mediated mechanism of toxicity in the common mussel, Mytilus edulis L., and other molluscs. Funct Ecol: 415–424

  • Mobasheri A, Avila J, Cózar-Castellano I, Brownleader M, Trevan M, Francis M, Lamb J, Martín-Vasallo P (2000) Na+/K+-ATPase isozyme diversity; comparative biochemistry and physiological implications of novel functional interactions. Biosci Rep 20:51–91

    Article  CAS  Google Scholar 

  • Randall DJ, Tsui TK (2002) Ammonia toxicity in fish. Mar Pollut Bull 45:17–23

    Article  CAS  Google Scholar 

  • Randall DJ, Wright PA (1987) Ammonia distribution and excretion in fish. Fish Physiol Biochem 3:107–120

    Article  CAS  Google Scholar 

  • Rudneva I (1997) Blood antioxidant system of Black Sea elasmobranch and teleosts. Comp Biochem Physiol C 118:255–260

    Google Scholar 

  • Sancho E, Fernandez-Vega C, Ferrando M, Andreu-Moliner E (2003) Eel ATPase activity as biomarker of thiobencarb exposure. Ecotox Environ Safe 56:434–441

    Article  CAS  Google Scholar 

  • Sies H (1994) Strategies of antioxidant defense, Eur J Biochem Reviews 1993. Springer, Berlin, pp 101–107

    Google Scholar 

  • Sinha AK, AbdElgawad H, Giblen T, Zinta G, De Rop M, Asard H, Blust R, De Boeck G (2014) Anti-oxidative defences are modulated differentially in three freshwater teleosts in response to ammonia-induced oxidative stress. PLoS ONE 9:e95319

    Article  Google Scholar 

  • Smart GR (1978) Investigations of the toxic mechanisms of ammonia to fish–gas exchange in rainbow trout (Salmo gairdneri) exposed to acutely lethal concentrations. J Fish Biol 12:93–104

    Article  CAS  Google Scholar 

  • Stebbing A (1982) Hormesis—the stimulation of growth by low levels of inhibitors. Sci Total Environ 22:213–234

    Article  CAS  Google Scholar 

  • Steele SL, Chadwick TD, Wright PA (2001) Ammonia detoxification and localization of urea cycle enzyme activity in embryos of the rainbow trout (Oncorhynchus mykiss) in relation to early tolerance to high environmental ammonia levels. J Exp Biol 204:2145–2154

    CAS  Google Scholar 

  • Sun HJ, Lü K, Minter EJ, Chen YF, Yang Z, Montagnes DJ (2012) Combined effects of ammonia and microcystin on survival, growth, antioxidant responses, and lipid peroxidation of bighead carp Hypophthalmythys nobilis larvae. J Hazard Mater 221:213–219

    Article  Google Scholar 

  • Tomasso JR (1994) Toxicity of nitrogenous wastes to aquaculture animals. Rev Fish Sci 2:291–314

    Article  Google Scholar 

  • Wilson JM, Randall DJ, Donowitz MW, Vogl A, Ip AK (2000) Immunolocalization of ion-transport proteins to branchial epithelium mitochondria-rich cells in the mudskipper (Periophthalmodon schlosseri). J Exp Biol 203:2297–2310

    CAS  Google Scholar 

  • Wright PA, Wood CM (2009) A new paradigm for ammonia excretion in aquatic animals: role of Rhesus (Rh) glycoproteins. J Exp Biol 212:2303–2312

    Article  CAS  Google Scholar 

  • Wright PA, Wood CM (2012) Seven things fish know about ammonia and we don’t. Respir Physiol Neurobiol 184:231–240

    Article  CAS  Google Scholar 

  • Yadwad VB, Kallapur VL, Basalingappa S (1990) Inhibition of gill Na+ K+-ATPase activity in dragonfly larva, Pantala flavesens, by endosulfan. Bull Environ Contam Toxicol 44:585–589

    Article  CAS  Google Scholar 

  • Yang Z, Chen YF (2004) Induced ovulation in obscure puffer Takifugu obscurus by injections of LHRH-a. Aquac Int 12:215–223

    Article  CAS  Google Scholar 

  • Yang Z, Chen YF (2005) Effect of temperature on incubation period and hatching success of obscure puffer Takifugu obscurus (Abe) eggs. Aquaculture 246:173–179

    Article  Google Scholar 

  • Yang Z, Chen YF (2006) Salinity tolerance of embryos of obscure puffer Takifugu obscurus. Aquaculture 253:393–397

    Article  CAS  Google Scholar 

  • Yang W, Xiang FH, Liang L, Yang Z (2010) Toxicity of ammonia and its effects on oxidative stress mechanisms of juvenile crucian carp (Carassius auratus). J Freshw Ecol 25:297–302

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank three anonymous reviewers for their constructive comments that substantially improved the manuscript. This investigation was funded by the National Natural Science Foundation of China (31370429).

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Authors and Affiliations

  1. Jiangsu Province Key Laboratory for Biodiversity and Biotechnology, College of Life Sciences, Nanjing Normal University, 1 Wenyuan Road, Nanjing, 210023, China

    Jun Wang, Nuo Xu, Jing Li, Ziheng Li & Zhou Yang

  2. Jiangsu Institute of Freshwater Fisheries, 79 East Chating Street, Nanjing, 210017, China

    Jiajia Li

  3. State Key Laboratory of Lake and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, 73 East Beijing Road, Nanjing, 210008, China

    Yafen Chen

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  1. Jun Wang
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  2. Jiajia Li
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  3. Nuo Xu
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  4. Jing Li
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  5. Ziheng Li
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  6. Yafen Chen
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  7. Zhou Yang
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Correspondence to Yafen Chen.

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Responsible editor: Cinta Porte

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Wang, J., Li, J., Xu, N. et al. Responses of Takifugu obscurus fertilized eggs and larvae to increased ammonia exposure. Environ Sci Pollut Res 22, 15976–15984 (2015). https://doi.org/10.1007/s11356-015-4815-x

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  • DOI: https://doi.org/10.1007/s11356-015-4815-x

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